Antiretroviral Discovery, Evaluation and Application Research (ADEAR) Training Program

Applications are due July 31 and should be submitted electronically through the REDCap link:

Compile the following materials into a single PDF:

1. Letter of interest from candidate, including statement of interest in academic career and commitment to pursuing a career in HIV-related research. Please specify which pathway the research (basic science, clinical studies/trials, health services, implementation science) will focus upon. Limit 2 pages.
2. Project description from candidate (font Arial 11, 6" margins). Limit 3 pages.
   1. Specific aims/hypotheses
   2. Background
   3. Brief experimental approach
   4. Timeline for research activity and expected products of your research (spanning 2 possible years of funding)
3. Mentored Career Development plan for the proposed 2-year funding period (coursework, conference/workshop attendance, frequency and details of mentor meetings, advisory panel, plan for future grants). Limit 1 page.
4. CV, resume, or NIH biosketch of the applicant.
5. NIH biosketch of the mentors, including current funding.
6. Letters of recommendation (4 total) including at least 1 from proposed postdoctoral mentors for the proposed training project. 
7. References. Limit 1 page, not inclusive of project description.

Please contact PI: Kristine Erlandson (kristine.erlandson@cuanschutz.edu) or Project Coordinator: Chelsee McFarland (chelsee.mcfarland@cuanschutz.edu) with any questions.

Program Leadership: 

Kristine Erlandson, MD, MS, Professor of Medicine and Epidemiology. Dr. Erlandson’s research focuses on promoting successful aging and improving quality of life among people with HIV on long-term ART. Research from her team spans the translational spectrum through exploring mechanisms underlying weight gain associated with antiretrovirals, understanding differences in aging among people with HIV, small and large interventional trials, and understanding ideal models of care delivery. She works collaboratively across multiple disciplines and other institutions. Dr. Erlandson is also passionate about mentoring the next generation of clinical researchers, as evidenced by her mentoring record, her current K24 Mentoring Award, and serving as Associate Program Director on ADEAR since 2020. Email: kristine.erlandson@cuanschutz.edu

Joshua Barocas, MD, Professor of Medicine. Dr. Barocas leads an interdisciplinary research program that is specifically aimed at the goal of improving health outcomes for marginalized populations who are at high risk for HIV including people who use or inject drugs, those with a history of incarceration, and those experiencing homelessness. He is a health services researcher who uses a combination of clinical epidemiology, health economics, simulation modeling, and cost-effectiveness methods. His work has been used to inform clinical and policy decisions at nearly every level. Dr. Barocas is nationally and internationally recognized for his expertise in the syndemic of substance use disorders and HIV. Like Dr.  Erlandson, he is also passionate about mentoring junior investigators across disciplines the next generation of clinical researchers, as is evidenced by his mentoring record. Email: joshua.barocas@cuanschutz.edu

Mamuka Kvaratskhelia, Ph.D., Professor of Medicine. Dr. Kvaratskhelia is a biochemist, pharmacologist, and molecular virologist who has developed an interactive research program with both basic science and translational components. He has been at the forefront of elucidating antiviral mechanisms of action of and drug-resistance to a completely novel class of investigational antiretrovirals termed allosteric HIV-1 integrase inhibitors (ALLINIs) as well as highly potent and long-acting HIV capsid inhibitor lenacapavir. Dr. Kvaratskhelia is robustly funded by the NIH and his findings are published in top tier journals including Cell, Science, Nature Microbiology, PNAS and others. Dr. Kvaratskhelia joined the Division of Infectious Diseases in August 2017 and has served as Co-Director of ADEAR since 2020 to strengthen basic and translational components of the T32 training program. Dr. Kvaratskhelia rapidly integrated into UCD establishing numerous collaborations within Schools of Medicine and Pharmacy. Dr. Kvaratskhelia’s research brings breadth of complementary experience to the ADEAR and trainees benefit from his expertise spanning from basic research components of researching new antiretroviral compounds to bench-to-bedside translational aspects. Email: mamuka.kvaratskhelia@cuanschutz.edu

Faculty Mentors: 

Lisa Abuogi, PhD. Dr. Abuogi is an Associate Professor of Pediatrics in the Section of Infectious Diseases at the University of Colorado. Her research focuses on implementation science to improve HIV prevention and treatment in resource limited settings. She has conducted research on the incidence and prevalence of TB co-infection among HIV infected children in Kenya. She is currently PI for a large multi-site community randomized study to maximize retention and adherence amongst women and infants in the context of Option B+ in Kenya. This includes the evaluation of a large-scale multi-component intervention to rapidly improve PMTCT services in western Kenya, assessment of family testing to identify children with HIV, and assessment of delays in treatment initiation for children with HIV.  She is currently supported by a Mid-Career Mentoring Award (K24), attesting to both her dedication to mentoring and the dedicated time she can contribute to Pathway Leadership.  Her current and prior research also highlight her commitment to collaborative implementation science research in resource limited settings. Dr. Abuogi is currently PI of NIH R01and R34 awards. Email: lisa.abuogi@childrenscolorado.org

Ramesh Akkina, Ph.D., Professor of Microbiology, Immunology and Pathology (CSU). Dr. Akkina’s research focus is on humanized mouse models for evaluation of new approaches to HIV treatment and prevention. He was instrumental in refining several gene transfer protocols and chiefly responsible for developing the SCID-hu mouse model with transplanted human tissue for stem cell reconstitution and gene therapy. His team was among the first to pseudotype an HIV-based lentiviral vector with the VSV-G envelop and achieve high efficiency gene transduction into CD34 hematopoietic progenitor cells. Dr. Akkina served as on numerous NIH study sections and recently was the chair of an NIH study section. In postgraduate training efforts, he trained three PhD and seven master’s students and served as a mentor for 18 postdoctoral trainees. His current trainees include one pre-doctoral students and three postdoctoral fellows. Dr. Akkina will mentor trainees in the use of animal models in HIV treatment and prevention research, the design and utilization of siRNAs/RNAi for gene knock-down, use of retro-and lentiviral vectors for gene transfer and therapy, derivation of hematopoietic cells from human embryonic stem cells and techniques for gene transfer into hematopoietic stem cells. Email: ramesh.akkina@colostate.edu

Peter Anderson, Pharm.D., Professor of Pharmaceutical Sciences (UC-AMC). Dr. Anderson’s research interest is clinical pharmacology of antiretroviral agents. His laboratory has expertise in measuring, interpreting, and analyzing extracellular and intracellular antiretroviral drug concentrations in vivo. He investigates pharmacokinetic considerations for antiretroviral therapy including biological factors that alter pharmacokinetics and the implications of altered pharmacokinetics on drug efficacy and toxicity. He co-directs the Colorado Antiviral Pharmacology Laboratory, which is CLIA-certified and has a long history of innovative and lasting contributions to antiviral clinical-translational research including development and validation of methodologies including intracellular tenofovir-diphosphate and emtricitabine-triphosphate (and other phosphorylated nucleotide analogs) in various cell types from human subjects and animal models. Data from this assay was used to support the pharmacology measurements for the iPrEx study that led to the FDA-indication of daily Truvada for HIV pre-exposure prophylaxis (PrEP), as well as Descovy for PrEP, and Truvada for PrEP in adolescents. Email: peter.anderson@cuanschutz.edu

Kristina Brooks, Pharm.D., MSCS, Assistant Professor of Pharmaceutical Sciences (UC-AMC). Dr. Brooks is Co-Director of the Colorado Antiviral Pharmacology Laboratory (CAVP) alongside Dr. Peter Anderson. Her research is focused on clinical pharmacology, biomarkers of treatment response, and translational approaches to bring therapies and understanding of disease pathology from the bench to the bedside. Her primary focus in  in the treatment and prevention of HIV and related coinfections, notably hepatitis B/C and tuberculosis. She has expertise in understudied populations such as pregnant people, infants, children and persons with alcohol and substance use disorders and serves as a Scientific Member of the US DHHS Perinatal and Pediatric HIV Guidelines Panels. Her lab is a leader in the antiviral pharmacology field and are members of the Pharmacology Support Laboratory for the International Maternal Pediatric Adolescent AIDS Clinical Trials (IMPAACT) Network, AIDS Clinical Trials Group (ACTG), and the HIV Prevention Trials Network (HPTN). Email: kristina.brooks@cuanschutz.edu

Thomas Campbell, M.D., Professor of Medicine and Microbiology (UC-AMC). Dr. Campbell served as ADEAR Program Director from 2020-2025. Dr. Campbell’s research focuses on clinical investigations of antiretrovirals for treating HIV/AIDS and he has worked collaboratively with multi-disciplinary investigators and across institutions. He has served as Site Leader of the University of Colorado Hospital Clinical Research Site (UCH-CRS; 2004-2025) in the international ACTG network. Dr. Campbell has held leadership positions in the ACTG (Scientific Committee Chair/Vice Chair; Protocol Chair/Vice Chair, Executive Committee, Antiretroviral Therapy Strategies Transformative Science Group. As Medical Director for the Adult Clinical Translational Research Center (2008-present), Dr. Campbell is responsible for medical oversight of this NIH-funded clinical research facility which currently supports the conduct of 388 active clinical research studies with 8,500 outpatient and 120 inpatient research visits per year. Dr. Campbell’s mentees have included both laboratory and clinical scientists. Email: thomas.campbell@cuanschutz.edu

Chaoping Chen, Ph.D., Associate Professor of Biochemistry and Molecular Biology (CSU). Dr. Chen’s laboratory uses a cell-based assay to study autoprocessing of HIV protease precursors as a rapid tool for phenotype assessment to evaluate the effects of mutations outside of the protease coding region on protease phenotype. Potential projects for ADEAR trainees include laboratory-based investigations to characterize protease autoprocessing phenotypes from clinical specimens obtained from patients on protease inhibitor-based therapies and correlations between autoprocessing phenotype and virologic response to protease inhibitors. Email: chaoping.chen@colostate.edu

Karen Hampanda, Ph.D., Associate Professor of Obstetrics and Gynecology (UC-AMC). Dr. Hampanda is a mixed-methods global health researcher whose work focuses on behavioral determinants of maternal and child health, sexual and reproductive health, and HIV, with a particular emphasis on perinatal and postpartum women living with HIV, intimate partner violence and male partner involvement in low-resource settings. Her funded research includes an NIMH R00 award (“Promoting HIV Health Behaviors Among Pregnant Couples in Zambia Using an Adaptive Relationship Strengthening Intervention”) and a subsequent R00/R transition award as PI. Dr. Hampanda mentors junior faculty, fellows and MPH/MPH-capstone trainees in global HIV and maternal health research, mixed-methods design, and intervention development among HIV-affected couples. She will serve as a mentor in the T32, providing expertise in behavioral intervention science across the HIV lifespan through the reproductive and maternal health lens. Email: karen.hampanda@cuanschutz.edu

Edward Janoff, M.D., Professor of Medicine, Immunology, and Microbiology (UC-AMC). Dr. Janoff’s laboratory focuses on the development of systemic and mucosal immune responses, particularly antibodies, to provide primary protection against infection and mucosal disease. He studies the natural history of bacterial and viral (HIV) infections in affected persons. He characterizes the humoral immune host factors that are essential in eliciting, or failing to elicit, both natural defense and protection by infections and vaccines. He has carried out this work over a 30 year period, focusing on mucosal and host defense against HIV-1 and against pneumococcus in people with HIV. He has an extensive history of mentorship, developing early-stage investigators on their technical, conceptual and presentation skills. Email: edward.janoff@cuanschutz.edu

Gina Kruse, M.D., Associate Professor of Medicine (UC-AMC). Dr. Kruse’s research focuses on cancer prevention, tobacco use and cessation in global and US community settings with particular experience studying global HIV care settings. She is the PI of a U01 to study tobacco cessation treatment in HIV care in Chennai, India (1U01CA261614-01 and 1U01CA261614-04S1) and has also studied tobacco use patterns among adults initiating HIV care in Uganda and Chennai. She has methodologic expertise in implementation science, mixed methods research, and clinical trials serving previously as the Implementation Laboratory Director for the Implementation Science Center for Cancer Control Research based in Massachusetts. In terms of mixed methods and served as core faculty for the NIH sponsored Mixed Methods Research Training Program (MMRTP) from 2017-2022. She has an extensive mentorship background serving as a mentor on 2 K awards co-mentor and the mixed methods lead on two funded K awards. Email: gina.kruse@cuanschutz.edu

Laurel Lenz, Ph.D., Professor of Immunology and Microbiology (UC-AMC). Dr. Lenz’s research focuses on better-understanding how innate immune responses are regulated and dysregulated in the context of health and disease.  A recent collaboration between Drs. Lenz and Weinberg found that HIV-uninfected infants born to HIV infected mothers, and exposed to antiretroviral drugs in utero, had altered NK cell proportion, phenotype, and function with dysregulation of NK cell cytotoxicity at birth including reduced IFNγ and perforin production. These findings provide an immunologic mechanism to explain why HIV-exposed infants have increased susceptibility to infection. She has mentored 25 students and fellows, with additional undergraduate and rotating graduate students and has served as member or chair of thesis committees for >40 Ph.D. students Dr. Lenz will serve as a mentor for ADEAR trainees who are interested in investigating the effects of antiretrovirals used for HIV treatment or prevention on innate immune responses. Email: laurel.lenz@cuanschutz.edu

Catherine Lozupone, Ph.D., Assistant Professor of Medicine, Division of Bioinformatics and Personalized Medicine (UC-AMC). Dr. Lozupone’s studies the factors that shape human microbiome composition in health and disease and investigates the functional consequences of compositional differences, both in terms of the biological/metabolic properties of individual bacteria and host interactions. She was the primary developer of the UniFrac algorithm for comparing microbial communities among many samples using phylogenetic information, and a contributor to the QIIME software package. Her publication record in human microbiome research includes studies of the relationships between lung and gut microbiome composition and HIV infection. In recent and ongoing R01 funded research she investigated whether gut microbiota composition of individuals with HIV on antiretroviral therapy is linked with metabolic disease; the extent to which microbiome compositional differences are driven by a loss of bacteria that induce CD4+ T regulatory cells; and the interaction between diet and disease in HIV infected subjects in the US and in Zimbabwe. Under her mentorship, trainees can use 16S rRNA analysis, comparative genomics, and meta-analysis to study microbiome changes with HIV-infection, and the relationships between the gut microbiome, chronic inflammation and susceptibility to HIV infection. Email: catherine.lozupone@cuanschutz.edu

Elizabeth McFarland, M.D., Professor of Pediatrics, Head, Section of Infectious Diseases (UC-AMC). Dr. McFarland is the Director of the Children’s Hospital HIV Program which serves HIV-affected infants, children, youth, pregnant women, and families. Dr. McFarland studies the maturation of cell-mediated immune responses in both HIV-exposed and infants with HIV, immune responses to HIV vaccines in HIV-exposed newborns, the role of cytotoxic T-lymphocytes in the pathogenesis of congenitally acquired HIV infection, pediatric HIV clinical trials of antiretroviral therapy and vaccines.  She has co-authored manuscripts and/or has ongoing research collaborations with Drs. Abuogi, Janoff, and Weinberg. Potential research training projects for ADEAR mentees include evaluation of cellular immune response in HIV-uninfected infants and children born to mothers with HIV and exposed to antiretrovirals in utero.  She is Co-PI of the IMPAACT network Clinical Research Site at Children’s Hospital Colorado. Email: betsy.mcfarland@cuanschutz.edu

Charles Neff, Ph.D., Assistant Professor of Medicine, Division of Allergy and Clinical Immunology (UC-AMC). Dr. Neff’s research is focused on studying the effect of the microbiome and HIV on the immune system. He has pursued work in the deep characterization of immune cells using CyTOF in human lungs of HIV-infected subjects and found that HIV infection is associated with a loss of anti-inflammatory alveolar macrophages. He has also worked on several studies detailing the interactions of the microbiome with immune cells and comprehensively analyzed human samples to evaluate the microbiome and its complex interactions with the immune system and epithelial cells. This work is the basis for his most research work on ILC3s depletion with HIV infection. He uses this to determine the mechanisms that drive aberrant immune activation to develop therapeutic targets that alleviate chronic immune cell activation that leads to co-morbidities in treated PWH. Email: charles.neff@cuanschutz.edu

Brent Palmer, Ph.D., Associate Professor of Medicine, Division of Allergy and Clinical Immunology (UC-AMC). Dr. Palmer studies the effects of HIV infection on systemic and mucosal immunity and interactions between commensal microbiota in the gut and lung and the immune system during antiretroviral therapy. His work has demonstrated that HIV-1 replication impacts T cell function by triggering the overexpression of inhibitory receptors, such as PD-1, that induce T cell exhaustion and that that exhaustion can be reversed, and HIV-1 replication reduced, by PD-1 pathway blockade using HIV-infected humanized mouse models.  He serves as the Director of the ACI/ID Flow Cytometry facility and the ClinImmune Clinical Immunology lab also brings with access to state-of-the-art flow cytometric instrumentation. ADEAR trainees will have opportunities for mentored research in the microbiome and mucosal immunity in the gut and the interaction between these mucosal compartments and how they influence one another during HIV treatment and in high-risk men who have sex with men. Email: brent.palmer@cuanschutz.edu

Eric Poeschla, M.D., Professor of Medicine, Division of Infectious Diseases (UC-AMC). Dr. Poeschla was recruited to the University of Colorado in 2014 as the Tim Gill Professor of Medicine. His laboratory investigates basic aspects of retroviral replication, host innate immunity to retroviruses, and retroviral disease pathogenesis including host cell dependency factors, cell-intrinsic innate immunity/restriction factors, integration, and accessory protein function. He contributed foundational work on the role of LEDGF as both HIV integration cofactor and an HIV-1 host dependency factor. The Poeschla lab has graduated ten Ph.D.s in virology and currently supports two graduate students. Dr. Poeschla will provide ADEAR trainees with outstanding mentorship in the molecular mechanisms of HIV related the development of new strategies to treat HIV. Email: eric.poeschla@cuanschutz.edu

Christine Rael, Ph.D., Assistant Professor, College of Nursing (UC-AMC). Dr. Rael’s has an extensive track record of extramurally funded research on HIV. She uses rigorous mixed-methods research designs to understand how the perspectives of gay and bisexual men [GBM] influence their willingness and ability to use HIV prevention and treatment interventions. She tailors tools and interventions to the needs of the end-users in these key populations. She is the PI or MPI of multiple NIH-funded research projects that facilitate dual HIV/syphilis self-testing and linkage-to-PrEP and/or HIV/syphilis treatment using the INSTI Multiplex among TW in South Africa, the development and testing of a digital communication tool to facilitate recruitment and enrollment of TW in Phase 1 HIV vaccine trials, and the development of a shared decision-making tool to help TW and their healthcare providers select their ideal PrEP method. Email: christine.rael@cuanschutz.edu

Mario Santiago, Ph.D., Professor of Medicine, Division of Infectious Diseases (UC-AMC). Dr. Santiago’s laboratory focuses on defining innate antiretroviral mechanisms and their impact on humoral and cell-mediated immune responses in vivo, using three complementary biological systems. First, using genetic tools, he investigates basic innate mechanisms that influence the outcome of pathogenic Friend retrovirus infection in mice. Second, using engineered molecular clones of simian immunodeficiency virus, he investigates the immunological impact of attenuating encoded viral immune antagonists. Finally, using biological samples from human populations resistant or susceptible to HIV, he studies immunogenetic properties that regulate innate HIV resistance. Dr. Santiago will serve as a mentor for ADEAR trainees who seek laboratory-based studies of innate resistance to HIV infection and its role in HIV prevention and treatment. Email: mario.santiago@cuanschutz.edu

Sarah Sawyer, Ph.D., Professor of Molecular, Cellular and Developmental Biology (UC-Boulder).  Dr. Sawyer was recruited to the Department of Molecular, Cellular and Developmental Biology in 2015.  She studies viral restriction factors and viral entry receptors by combining laboratory research in virology with tools from molecular evolution, population genetics, bioinformatics, and genomics. For her work on host-virus interactions, Dr. Sawyer was the recipient of a 2011 PECASE award, conveyed by President Obama at the White House. Her work on HIV-1 spans more than a decade and has focused on cellular-level evolutionary and functional interactions between virus and host. Dr. Sawyer has well-established relationships with primate research centers. Dr. Sawyer will provide mentored research opportunities for ADEAR trainees who wish to study the evolution of HIV-1 in the context of HIV treatment and prevention. Email: ssawyer@colorado.edu

Christiana Smith-Anderson, D.Sc., Associate Professor of Pediatrics, Section of Infectious Diseases and Epidemiology (UC-AMC). Dr. Smith-Anderson has a strong clinical and research interest in infants and children who are living with or exposed to HIV, and specifically in the immunologic consequences of perinatal HIV exposure. She leads a translational research program focused on innate and adaptive immune function in HIV-exposed uninfected (HEU) infants, immune responses to respiratory viral infections such as influenza and respiratory syncytial virus, vaccine responses, and the contribution of co-infections such as cytomegalovirus to immune function. She has identified a pro-inflammatory profile of biomarkers in the peripheral blood of mothers with HIV that correlate inversely with their infants’ RSV responses, suggesting that maternal inflammation is the likely driver of immune dysregulation in HIV-exposed infants. She is leading a separate project evaluating the transcriptomic and epigenomic phenotype of peripheral blood immune cells from HIV-exposed compared to unexposed infants using single cell RNA sequencing and ATAC sequencing. Email: christiana.smith@childrenscolorado.org

Kayla Sprenger, Ph.D., Assistant Professor, Department of Chemical and Biological Engineering (UC-Boulder). Dr. Sprenger leads the Rationally Designed Immunotherapeutics and Interfaces Laboratory, which tackles problems at the intersection of physics, engineering, and immunology. Her work revolves around using computational tools and approaches to study interfacial phenomena, specifically the interface between antibodies and highly mutable pathogens like HIV to enable the design of universal vaccines. She employs tools spanning the atomistic to population level, including mathematical evolutionary modeling, physics-based simulations, bioinformatics, and machine learning, and work in close collaboration with experimentalists to inform, validate, and test our computational predictions. She is currently developing a new animal model for HIV informed by molecular dynamics simulations of HIV-host receptor interactions. She is also developing a to model and predict the transport of anti-HIV antiretroviral drugs across the blood brain barrier, as well as to identify key interactions differentiating the interactions of anti-HIV antiretrovirals with viral proteins and host cell proteins. She is committed to fostering an inclusive and welcoming research environment. Email: kayla.sprenger@colorado.edu

Samantha Stonbraker, Ph.D., Associate Professor, University of Colorado College of Nursing (UC-AMC). Dr. Stonbraker’s research aims to develop and evaluate evidence-based informatics interventions to improve health among various populations. She has formal training in nursing, international public health, research methods, and informatics, which allows her to develop and execute comprehensive, rigorous, and culturally appropriate studies using mixed methods approaches. She is MPI on both an R21 and R34, the former of which is designing a digital tool to enhance recruitment and enrollment of women in Phase I HIV vaccine trials—an ideal project for a mentee from the T32. Her R34 aims to design a digital shared decision-making tool to facilitate conversations to help patients and their healthcare providers select the appropriate PrEP modality (oral or injectable), another ideal project for a T32 trainee. She will facilitate linking trainees from the College of Nursing. Email: samantha.stonbraker@cuanschutz.edu

Linda van Dyk, Ph.D., Professor Immunology and Microbiology (UC-AMC). Dr. van Dyk’s research focus is characterization of host-pathogen interactions in gammaherpesvirus infection, with primary emphasis on latency and reactivation.  Dr. van Dyk received the 2001 American Herpes Foundation Gertrude Elion Research Award. She is the recipient of the Burroughs Wellcome Fund Investigator Award in Pathogenesis of Infectious Disease.  Her laboratory studies the effects of tumor suppressors on chronic viral infection, and the effects of chronic infection on tumor suppressor function. Dr. van Dyk has served as a mentor for seven predoctoral and three postdoctoral past or current trainees. She will serve as a mentor for ADEAR trainees who wish to study the virological mechanisms by which herpesvirus contribution to chronic inflammation during antiretroviral treatment of HIV infection.  Email: linda.vandyk@cuanschutz.edu

Schuyler Van Engelenburg, Ph.D., Assistant Professor of Biological Sciences (DU). Dr. Van Engelenburg completed his postdoctoral training at NIH where he investigated how a single HIV-1 particle is formed in an infected cell using single molecule imaging approaches. His current research uses advanced superresolution microscopy techniques, protein chemistry and probe development, and computational image analysis to quantitatively understand the cellular, biochemical, and genetic drivers of HIV-1 assembly and to construct molecularly accurate spatial and temporal models for HIV biogenesis for the purpose of developing new antiviral therapies targeting the assembly stage of the HIV infection cycle. Dr. Van Engelenburg will serve as mentor for ADEAR trainees interested in laboratory-based training to discover or evaluate inhibitors of HIV assembly. Email: schuyler.vanengelenburg@du.edu

Adriana Weinberg, M.D., Professor of Pediatrics and Medicine, Section of Infectious Diseases (UC-AMC).  Dr. Weinberg’s research evaluates immune restoration in antiretroviral therapy.  She has established virologic correlates of immune reconstitution in children and adults, and identified immune correlates of protection against cytomegalovirus (CMV) infection in patients with HIV. She has developed several lines of investigation of CMV-specific immunity in transplant patients, including the following: impact of CMV infection on graft rejection-immune restoration in bone marrow transplant recipients and immune correlates of protection against CMV infections; use of dendritic cells for establishment of CMV-specific immunity in stem cell and cord blood transplant recipients.  Dr. Weinberg recently described persistent inhibition of cellular immunity to CMV in people with HIV, but not in healthy individuals.  She has co-authored manuscripts with Drs. Campbell, Erlandson, Janoff, McFarland and Levin.  A potential research training project for ADEAR trainees is laboratory studies of the molecular mechanisms of inhibition of cellular immunity in infants exposed to antiretrovirals in utero. Email: adriana.weinberg@cuanschutz.edu

Cara Wilson, M.D., Professor of Medicine, Division of Infectious Diseases.  Dr. Wilson is an experienced cellular immunologist who investigates the role of dendritic cells and HIV-specific T cells in the control of HIV replication. She is Associate Program Director for the Medical Scientist Training Program at the University of Colorado.  Dr. Wilson is an expert in dendritic cell biology and the role of dendritic cells in HIV pathogenesis.  ADEAR trainees can engage in cutting-edge laboratory-based studies of both helper and cytotoxic T-cell responses to HIV, mechanisms of HIV-associated dendritic cell-dependent immunodeficiency, and studies of the mechanisms of induction of HIV specific immune responses with therapeutic HIV vaccines. Dr. Wilson is a former recipient of a K24 award to facilitate patient oriented research in innate and adaptive immunity and to provide mentorship to trainees in clinical research. Email: cara.wilson@cuanschutz.edu

Trainee Highlights

Trainee: Stephanie Bester

PhD Mentor: Mamuka Kvaratskhelia, PhD

Training pathway: HIV Basic/Translational Science

Period of support: 09/01/2020-10/29/21

Research goals:

• Aim 1. Determine the structural basis for capsid inhibitor drug-resistance.
• Aim 2. Elucidate the underlying mechanisms for capsid inhibitor drug-resistance.
• Aim 3. Develop and test candidate second-generation capsid inhibitors.
  

Accomplishments: Dr. Bester’s research investigated structural basis of viral resistance to HIV capsid inhibitors. Dr. Bester solved the structure of the M66I capsid mutant hexamer, which confers substantial resistance to lenacapavir. She then evaluated the hypothesis that the β-branched side chain of isoleucine is responsible for introducing steric conflict with the inhibitor. Dr. Bester conducted structural and mechanistic studies to characterize drug resistant CA mutants and used these results to develop candidate second-generation capsid inhibitors. During year 02 of support, Dr. Bester was awarded the Ward Smith Award for Excellence in Macromolecular Crystallographic Research in recognition of the impact of her work. Dr. Bester completed the training program in Y2, accepting a research scientist position at Pfizer initially and is now a Principal Scientist at Think Bioscience (as of July 2024).

Career development activities: The NIH Review process, Mentorship I: Building Successful Mentor-Mentee Relationships, Surface Plasmon Resonance: Technology for Biosensor Applications, Effective Resumes & Cover Letters

Conference presentations:

• Bester, SM; Adu-Ampratwum, D.; Annamalai, A. S.; Haney, R.; Fuchs, J. R.; Kvaratskhelia, M., “Structural Basis for Viral Resistance of M66I to GS-6207” HIV Interaction and Viral Evolution (HIVE) Meeting, Virtual, Sep 18, 2020, Oral.
• Bester SM., Haney R., Adu-Ampratwum D., Fuchs J.R., Kvaratskhelia M. Structural basis for the evolution of viral resistance to long-acting HIV-1 capsid inhibitor GS-6207. Poster presentation at virtual Conference on Retroviruses and Opportunistic Infections (CROI). March, 2021.
• Bester SM., Haney R., Adu-Ampratwum D., Fuchs J.R., Kvaratskhelia M. Structural basis for the evolution of viral resistance to long-acting HIV-1 capsid inhibitor GS-6207. Poster presentation at virtual Retroviruses meeting. Cold Spring Harbor Laboratory, May 2021.
  

Publications/manuscripts:

• Briganti L…Bester SM… Kvaratskhelia M. Structural and mechanistic bases for resistance of the M66I capsid variant to lenacapavir. mBio. 2025 May 14; 16(5):e03613-24. DOI: 10.1128/mbio.03613-24
• Bester SM, Abrahamsen R, Rodrigues Samora L, Wu W, Mou T. Crystal structure of the GDP-bound human M-RAS protein in two crystal forms. Acta Cryst. F. 2024 Sep 01; 80(9): 220-227. DOI: 10.1107/S2053230X24007969
• Bester SM, Linwood R, Kataoka R, Wu W, Mou T. Enhancing the apo protein tyrosine phosphatase non-receptor type 2 crystal soaking strategy through inhibitor-accessible binding sites. Acta Cryst. F. 2024 Sep 01; 80(9): 210-219. DOI: 10.1107/S2053230X24007866
• Bester SM…Asturias FJ, Kvaratskhelia M. Structural and mechanistic bases for a potent HIV-1 capsid inhibitor. Science. 2020 Oct 16;370(6514):360-364. doi: 10.1126/science.abb4808. PMID: 33060363; PMCID: PMC7831379.
• Bester SM…Fuchs JR, Kvaratskhelia M. Structural and Mechanistic Bases of Viral Resistance to HIV-1 Capsid Inhibitor Lenacapavir. mBio. 2022 Oct 26;13(5):e0180422. doi: 10.1128/mbio.01804-22. Epub 2022 Oct 3. PMID: 36190128; PMCID: PMC9600929.
• Wei G…Bester SM, et al. Prion-like low complexity regions enable avid virus-host interactions during HIV-1 infection. Nature Communications. 2022-10-06 DOI: 10.1038/s41467-022-33662-6
• McGuire JR, Bester SM…Height JJ. Structural and Biochemical Insights into the Inhibition of Human Acetylcholinesterase by G-Series Nerve Agents and Subsequent Reactivation by HI-6. Chemical Research in Toxicology. 2021-02-04 DOI: 10.1021/acs.chemrestox.0c00406
• Bester SM…Kvaratskhelia M. Structural and Mechanistic Bases for a Potent HIV-1 Capsid Inhibitor. Science. 2020 370: 360-4. PMID: 33060363.

Honors, fellowships or other: The Ward Smith Award for Excellence in Macromolecular Crystallographic Research from Rigaku Americas Corporation – 2021

--

Trainee: James Curlin

PhD Mentor: Ramesh Akkina, DVM, PhD

Training pathway: HIV Basic/Translational Science

Period of support: 04/01/2021-03/31/2023

Research goals:

• Aim 1. Evaluate the humanized mouse model for productive infection with SIVmac virus.
• Aim 2. Validate the utility of the hu-mouse model for efficacy testing of ARV effective against SIV and SHIV viruses.
  

Accomplishments: The overall goal of Dr. Curlin’s research training in ADEAR was to validate a hu-mouse model for simultaneous testing of anti-HIV and anti-SIV drugs. His research evaluated the hypothesis that hu-mice that permit productive SIV infections will allow for testing of various ART effective against SIV and HIV.

Career development activities:

•  “Biomedical responsible conduct of research”, CITI online course
• Responsible Conduct of Research Monthly Seminar Series, monthly, CU Anschutz
• “15th Annual NIH Career Symposium” online workshop, 5/11/22-5/13/22
• “Career Experiences and Advice: Federal Agency”, workshop 3/29/22
• “CDO Career Skills Workshop: LinkedIn for Scientists Workshop” 4/12/22
• Bio-Rad Gene Expression Workshop, University RT-qPCR series, 4/4/22-4/8/22
• “CDO Career Skills: CV/Résumé Workshop” 5/10/22
  

Select Conference presentations:

• Curlin, J; et al. Human adaptive changes in SIVsm-derived viruses towards HIV-2 during serial passaging in a humanized mouse model. ePoster. Presented at HIV Pathogenesis and Cure Keystone eSymposia, June 1-4, 2021.
  
• Curlin, J; et al. Deciphering the Evolutionary Mystery of Three SIVsm-Derivatives in Humanized Mice. ePoster. Presented at 38th Symposium on NHP Models for AIDS, September 21-24, 2021.
• Curlin, J.; et al. Characterizing the phenotypic and genetic changes of pre-epidemic HIV-2 Group F virus following serial passage in humanized mice. Poster. Presented at the 39th Symposium on NHP Models for AIDS, Portland, OR, September 13-16, 2022.
• Curlin, J.; et al. Concurrent testing of anti-retrovirals for both SIV and HIV in a dual-purpose hu-mouse model. Oral Presentation. Presented at the 32nd International Workshop on Retroviral Pathogenesis, Vail, CO, October 12-16, 2022.
  

Publications/manuscripts:

• Schmitt, K; Curlin, J; Aboellail, T; Akkina, R. (2023) "Zika virus induced microcephaly and aberrant hematopoietic cell differentiation modeled in neonatal humanized mouse." Frontiers in Immunology 14: 505. doi:10.3389/fimmu.2023.1060959
• Curlin JZ, et al. Evolution of SIVmac239 following serial passaging in humanized mice. J Med Primatol. 2022 Oct;51(5):284-287. doi: 10.1111/jmp.12614. Epub 2022 Aug 28. PMID: 36030392; PMCID: PMC9536747.
• Schmitt K, Curlin J, et al. Long-term evolutionary adaptation of SIVcpz toward HIV-1 using a humanized mouse model. J Med Primatol. 2022 Oct;51(5):288-291. doi: 10.1111/jmp.12616. PMID: 36030391; PMCID: PMC9536748.
• Curlin, J. Z., et al. "In vivo Infection Dynamics and Human Adaptive Changes of SIVsm-Derived Viral Siblings SIVmac239, SIVB670, and SIVhu in Humanized Mice as a Paralog of HIV-2 Genesis." Frontiers in Virology 1; 2021. DOI:10.3389/fviro.2021.813606
• Curlin JZ, et al. Viral evolution of SIV chimpanzee toward HIV-1 using humanized mice. J Med Primatol. 2023 Oct;52(5):294-297. doi: 10.1111/jmp.12675. PMID: 37658595; PMCID: PMC10635509.
• Curlin JZ, et al. Characterizing the phenotypic and genetic changes of pre-epidemic HIV-2 group F virus following serial passage in humanized mice. J Med Primatol. 2023 Oct;52(5):290-293. doi: 10.1111/jmp.12674. PMID: 37658590; PMCID: PMC10635500.
• Schmitt K, Curlin J, et al. Long-term evolutionary adaptation of SIVcpz toward HIV-1 using a humanized mouse model. J Med Primatol. 2022 Oct;51(5):288-291. doi: 10.1111/jmp.12616. PMID: 36030391; PMCID: PMC9536748
• Curlin, JZ; et al. (2021). “In vivo Infection Dynamics and Human Adaptive Changes of SIVsm-Derived Viral Siblings SIVmac239, SIVB670, and SIVhu in Humanized Mice as a Paralog of HIV-2 Genesis." Frontiers in Virology 1. doi:10.3389/fviro.2021.813606

--

Trainee: Brendan Freitas

PhD Mentor: Francisco Asturias, PhD

Training pathway: HIV Basic/Translational Science

Period of support: 06/01/2021-5/31/2023

Research goals:

• Aim 1. Use cryo-EM to examine the interaction of LEN with HIV-1 CA tubes bearing mutations conferring drug resistance and the interaction of 2nd generation CA inhibitor candidates with CA tubes formed by wild-type (wt) and LEN-resistant CA mutants.
• Aim 2. Use cryo-EM to obtain high-resolution (<3.5 Å) maps of LEN-bound HIV-1 CA tubes in the presence of inositol hexakisphosphate (IP6), an abundant cellular cofactor essential for effective assembly of cone-shaped HIV cores.
• Aim 3. Use cryo-EM to obtain high-resolution (<3.5 Å) maps of HIV-1 CA tubes bound to cleavage and polyadenylation specificity factor 6 (CPSF6), a cellular factor essential for nuclear import of HIV cores and integration of viral genomic material into active host chromatin.
  

Accomplishments: Dr. Freitas used X-ray crystallography and enzymatic assays to design and evaluate small molecule inhibitors for SARS family coronavirus papain-like proteases and studied host-pathogen interactions at the protein-protein level, with a focus on ubiquitin-like proteins and deubiquitinases. He used cryogenic electron microscopy (cryo-EM) to study the structural basis for lenacapaivr resistance in HIV-1 that has capsid point mutations and to characterize 2nd generation capsid inhibitor candidates that are not affected by lenacapivr mutations. Through a combination of single particle and helical reconstruction cryo-EM techniques, a helical map of CA hexamers with IP6 was resolved to a resolution of ~6.3Å and a map of a single hexamer with IP6 to ~4.2Å. The helical map of CA-IP6-Lenacapavir® was resolved to a resolution of ~7.4Å. From the CA-IP6-Lenacapivir® helical map, it was discerned that all CA hexamer tubes formed in the presence of Lenacapavir® adopt the same helical symmetry, whereas tubes formed in the absence of Lenacapavir® adopt many symmetry patterns, even if Lenacapavir is then added after tube formation.

Career development activities:

• Responsible Conduct of Research/Ethics in Research course
• Single-particle cryo-EM workshop, America Crystallographic Association's annual conference
• "What's in a name? Understanding Faculty Roles and Ranks" seminar
  

Conference presentations:

• Freitas BT. “Cryo-EM Studies of Small Molecule CA Inhibitors with Capsid and Cellular Co-Factors”. Presented at the 2022 Tim Gill Lecture and T32 Research Symposium, Aurora, CO, October 27, 2022.
  

Publications/manuscripts:

• Freitas BT, Ahiadorme DA, Bagul RS, Durie IA, Ghosh S, Hill J, Kramer NE, Murray J, O'Boyle BM, Onobun E, Pirrone MG, Shepard JD, Enos S, Subedi YP, Upadhyaya K, Tripp RA, Cummings BS, Crich D, Pegan SD. Exploring Noncovalent Protease Inhibitors for the Treatment of Severe Acute Respiratory Syndrome and Severe Acute Respiratory Syndrome-Like Coronaviruses. ACS Infect Dis. 2022 Mar 11;8(3):596-611. doi: 10.1021/acsinfecdis.1c00631. Epub 2022 Feb 24. PMID: 35199517; PMCID: PMC8887654.
• Shepard JD, Freitas BT, Rodriguez SE, Scholte FEM, Baker K, Hutchison MR, Longo JE, Miller HC, O'Boyle BM, Tandon A, Zhao P, Grimsey NJ, Wells L, Bergeron É, Pegan SD. The Structure and Immune Regulatory Implications of the Ubiquitin-Like Tandem Domain Within an Avian 2'-5' Oligoadenylate Synthetase-Like Protein. Front Immunol. 2022 Jan 4;12:794664. doi: 10.3389/fimmu.2021.794664. PMID: 35058932; PMCID: PMC8764230.
• Freitas BT, Ahiadorme DA, Bagul RS, Durie IA, Ghosh S, Hill J, Kramer NE, Murray J, O’Boyle BM, Onobun E, Pirrone MG, Shepard JD, Enos S, Subedi YP, Upadhyaya K, Tripp RA, Cummings BS, Crich D, Pegan
• SD., Exploring Noncovalent Protease Inhibitors for the Treatment of Severe Acute Respiratory Syndrome and Severe Acute Respiratory Syndrome-Like Coronaviruses, ACS Infect Dis. 2022. PMID: 35199517
  

Honors, fellowships, or other: Annual Research Publications Awards, U.S. Naval Research Laboratory, 2021

--

Trainee: Vincent Mainella

PharmD Mentors: Peter Anderson, PharmD, Kristina Brooks, PharmD

Training pathway: Clinical Investigation in HIV/AIDS

Period of support: 06/01/2022-05/31/2024

Research goals:

• Aim 1. To characterize the influence of pregnancy on plasma and intracellular tenofovir moieties in people receiving TAF.
• Aim 2. Identify metabolomic and immunologic pathways that are altered in pregnant and postpartum women receiving TDF-based PrEP.
  

Accomplishments: Dr. Mainella’s research evaluated the hypothesis is that pregnancy alters the PK disposition of TAF/tenofovir in plasma and thus TFV-DP within cells and that TDF differentially alters metabolic and immunologic pathways in pregnant and postpartum women. He received a Junior Investigator Futures Foundation grant from the American College of Clinical Pharmacy for work on “Digital Tool for the Assessment of Adherence in HIV PrEP and Treatment”.

Career development activities:

• PSHC 7326 “PK/PD Journal Club”, fall 2022; BIOS 6601 “Applied Biostatistics I”, fall 2022
• BIOS 6629 “Applied Survival and Longitudinal Analysis”, fall 2023
• CLSC 6270 “Critical Appraisal Seminars”, fall 2023; CLSC 6210 “Research Seminars”, fall 2023
• CLSC 7150 “Responsible Conduct of Research, fall 2023; BIOS 6644 “Practical Data Wrangling’, spring 2024
• BIOS 6648 “Designing Clinical Research”, spring 2024; CLSC 7101 “Grant Writing I’, spring 2024
  

Conference presentations:

• Maniella V, et al. Dried blood spots as a convenient alternative to PBMCs in Intracellular Islatravirtriphosphate assessment in pig-tailed macaques, International Workshop on Clinical Pharmacology of HIV Therapy in September 2022, poster.
  
• Mainella V, Coyle R, Morrow M, Williams M, Brooks K, MaWhinney S, Bushman L, Anderson P. “Development of a universal taggant for adherence to any medication or placebo” International Workshop on Clinical Pharmacology of HIV, Hepatitis, and Other Antiviral Drugs 2023; Rome, Italy.
• Mainella V, Castillo-Mancilla J, Branchford B, Hosford S, Johnson B, Choi Y, Xiong P, Williams M, Zheng J, Bushman L, Kiser J, Anderson P, Brooks K. “TFV-DP & FTC-TP in Blood Cells Subsets of Persons with HIV” Conference on Retroviruses and Opportunistic Infections 2023; Seattle, WA.
• Mainella V, Coyle R, Morrow M, Williams M, Brooks K, MaWhinney S, Bushman L, Anderson P. “Development of a universal taggant for adherence to any medication or placebo” International Workshop on Clinical Pharmacology of HIV, Hepatitis, and Other Antiviral Drugs 2023; Rome, Italy.
• Mainella V, Castillo-Mancilla J, Branchford B, Hosford S, Johnson B, Choi Y, Xiong P, Williams M, Zheng J, Bushman L, Kiser J, Anderson P, Brooks K. “TFV-DP & FTC-TP in Blood Cells Subsets of Persons with HIV” Conference on Retroviruses and Opportunistic Infections 2023; Seattle, WA.
  

Publications/manuscripts:

• Mainella V, Morrow M, Brooks K, Bushman L, Patton D, Cosgrove Sweeney Y, Patel S, Rohan L, Anderson P. Dried Blood Spots (DBS) as a Convenient Alternative to PBMCs for Intracellular Islatravir-Triphosphate Assessment in Pig-tailed Macaques. AIDS Research and Human Retroviruses. 2023 Jun 29. doi:10.1089/AID.2023.0059 PMID: 10.1089/AID.2023.0059
• Mainella V, Castillo-Mancilla J, Branchford B, Hosford S, Johnson B, Choi Y, Xiong P, Williams M, Zheng J, Bushman L, Kiser J, Anderson P, Brooks K. Differential accumulation of intracellular nucleoside analogs by serostatus and cell type. (Accepted by Journal of Antimicrobial Chemotherapy; available upon request)
• Coyle R, Morrow M, Mann S, Mainella V, Ellis S… Kiser J, MaWhinney S, Brooks K, Anderson P, Castillo-Mancilla J. Tenofovir-Diphosphate and Emtricitabine-Triphosphate Adherence Benchmarks in Dried Blood Spots for Persons With Human Immunodeficiency Virus Receiving Tenofovir Alafenamide and Emtricitabine–Based Antiretroviral Therapy (QUANTI-TAF). Clinical Infectious Diseases. 2024 Apr 18. doi:10.1093/cid/ciae212 PMID: 38636950
  

Honors, fellowship, or other: CROI New Investigator Scholarship. Future Foundation Grant

--

Trainee: Szu-Wei Huang

PhD Mentor: Mamuka Kvaratskhelia, PhD

Training pathway: HIV Basic/Translational Science

Period of support: 07/01/2023-08/30/2024

Research goals:

• Aim 1. Determine the underlying mechanism for ultra-potent antiviral activity of lenacapavir (LEN) during the early steps of HIV-1 replication using innovative biochemistry and virology approaches to measure LEN:CA stoichiometries in virions and investigate how LEN impairs the early steps of HIV-1 infection.
• Aim 2. Elucidate the mode of action of LEN during HIV-1 virion maturation using cutting-edge biochemistry and virology assays to understand how LEN binding to CA monomers affects the formation of key assembly intermediates pentamers and hexamers.
  

Accomplishments: Dr. Huang developed an LC-MS/MS-based method to determine the dissociation rate constant of LEN from virions. His results show that a sub-stoichiometric amount of LEN has a slow dissociated rate in the virion, consistent with previous findings with a cross-lined CA hexamer using SPR. He also established an in vitro combination assay to examine the role of IP6 in the formation of LEN-treated Capsid-like particles (CLPs). His results shows that LEN can impair the correct formation of CA regardless of presenting IP6.

Dr. Huang has a faculty position in the Division of Infectious Diseases. Furthermore, Dr. Huang has obtained an R21 award (PI: Huang; Title: HIV-1 Integrase Interactions with Viral RNA; Award number: R21 AI191966; Period: 07/22/2025 – 06/30/2027) from NIAID, and a competitive Department of Medicine faculty development grant.

Career development activities:

• B-HIVE Winter Training Retreat by B-HIVE Winter Behavior of HIV In Viral Environments Center, 2024
• Responsible Conduct of Research (RCR) classes February 2024 to May 2024 hosted by The Office of Regulatory Compliance, University of Colorado.
• New Investigator Workshop. Conference on Retroviruses and Opportunistic Infections 2024 (CROI 2024)
• Current Technical Workshops, Conference on Retroviruses and Opportunistic Infections 2024 (CROI 2024)
  

Conference presentations:

• Huang SW. Sub-Stoichiometric Drug to HIV-1 Capsid Ratio Enables Ultra-Potent Antiviral Activity of Lenacapavir, 7th International Conference on Retroviral Integration, Oral Presentation
  
• Huang SW. Sub-Stoichiometric Drug to HIV-1 Capsid Ratio Enables Ultra-Potent Antiviral Activity of Lenacapavir. 2023 Tim Gill Lecture and T32 Research Symposium, Aurora, CO, November 8, 2023.
• Huang SW. DDX3X interacts with HIV-1 and CPSF6 in early infection. Retroviruses meeting at Cold Spring Harbor Laboratory 2024 (Virtually)
  

Publications/manuscripts:

• Briganti L, Annamalai A, Bester S, Wei G, Andino-Moncada J, Singh S, Kleinpeter A, Tripathi M, Nguyen B, Radhakrishnan R, Singh P, Greenwood J, Schope L, Haney R, Huang S-W, Freed E, Engelman A, Francis A, Kvaratskhelia K. (2025) Structural and Mechanistic Bases for Resistance of the M66I Capsid Variant to Lenacapavir. mBio 13(5):e0180422. https://doi:10.1128/mbio.01804-22
• Huang S-W, Briganti L, Annamalai A, Greenwood J, Shkriabai N, Haney R, Armstrong M, Wempe M, Singh S, Francis A, Engelman A, Kvaratskhelia M. (2025) The mechanism for highly potent inhibition of HIV-1 maturation by lenacapavir. PLoS Pathogens 21(1):e1012862. https://doi:10.1371/journal.ppat.1012862
• Flick H, Venbakkam A, Singh P, Layish B, Huang S-W, Radhakrishnan R, Kvaratskhelia M, Engelman A, Kane M. (2025) Interplay between the cyclophilin homology domain of RANBP2 and MX2 regulates HIV-1 capsid dependencies on nucleoporins. mBio 16(3):e0264624. https://doi:10.1128/mbio.02646-24
• Layish B, Goli R, Flick H, Huang S-W, Zhang RZ, Kvaratskhelia M, Kane M. (2024) Virus specificity and nucleoporin requirements for MX2 activity are affected by GTPase function and capsid-CypA interactions. PLoS Pathogens 20(3): e1011830. https://doi.org/10.1371/journal.ppat.1011830
• Xue G, Yu H, Buffone C, Huang S-W, Lee K, Goh S, Gres A, Guney M, Sarafianos S, Luban J, Diaz-Griffero F. KewalRamani V. (2023) The HIV-1 capsid core is an opportunistic nuclear import receptor. Nature Communications 14(1):3782. https://doi.org/10.1038/s41467-023-39146-5

--

Trainee: Grace Kulik (née Ditzenberger)

DPT Mentors: Kristine Erlandson, MD; Catherine Jankowski, PhD

Training pathway: Clinical Investigation in HIV/AIDS

Period of support: 07/01/2023-12/31/2024

Research goals:

• Aim 1. Determine factors that predict magnitude and type of response to exercise interventions in sedentary older adults with HIV on ART.
• Aim 2. Examine the impact of muscle quality on baseline physical function and response to interventions in older adults with HIV on ART.
• Aim 3. Examine the association between mitochondrial markers with baseline physical function and response to an exercise intervention in older adults with HIV on ART.
  

Accomplishments: Dr. Kulik’s research is elucidating biological mechanisms behind the heterogeneity in response to exercise in people with HIV on ART and to develop interventions to maximize the benefits of exercise in older people with HIV. She is pursuing additional training in rehabilitation sciences (with Dr. Erlandson) and continuing her work above, funded through an R01.

Career development activities:

• RHSC 7002 “Rehabilitation Sciences Seminar”; EPID 6646 “Methods Systematic Reviews and Meta-Analyses”; CLSC 7101 “Grant Writing I”; BIOS 6644, “Practical Data Wrangling’; AAHIVM HIV Core Courses Modules; Responsible conduct of research: weekly HEALTH meetings to discuss study management, AE reporting; Early Investigator Working Group, CNICS investigators/cohort
  

Select Conference presentations:

• Ditzenberger GL, et al. Cardiovascular Responses to Exercise in Aging Adults with HIV: Oral Abstract: International Workshop on Long-term Complications of HIV and SARS-CoV-2. Washington DC. 12/2023.
• Ditzenberger GL, et al. Strength and Lean Mass Responses to Exercise in Aging Adults with HIV.Oral Abstract: International Workshop on HIV & Aging. Washington DC. 10/2023.
• Kulik G.L., et al. Prognostic Factors of Physical Function Decline in the PREPARE Study [Oral presentation]. International Workshop on Aging & HIV 2024. Washington D.C.
• Ditzenberger GL, et al. Effects of Semaglutide on Muscle Structure and Function in the SLIM Liver Study. Conference on Retroviruses and Opportunistic Infections. Denver, CO. March 2024.
  

Selected Publications/manuscripts:

• Ditzenberger GL, et al. The use of non-invasive imaging modalities for the assessment of skeletal muscle quantity and quality in people with HIV: a narrative review. HIV Med. 2023:1176-1189. PMID: 37651982
• Wilson MP… Kulik GL … Erlandson KM. Effect of a Supervised Exercise Program on Exercise Self-Efficacy in Aging Adults With and Without HIV: A Secondary Analysis of the Exercise for Healthy Aging Study. AIDS Behav 2024.
• Sun J, Ditzenberger GL…Erlandson KM. Muscle Quality and Physical Function in Men With and Without HIV. J Gerontol A Biol Sci Med Sci. 2024 Nov 1;79(11):glae229. PMID: 39288937.
• Ditzenberger GL…Erlandson KM. Effects of Semaglutide on Muscle Structure and Function in the SLIM LIVER Study. Clin Infect Dis. 2025. PMID: 39046173.
• Durstenfeld MS…Ditzenberger GL…Erlandson KM. Chronotropic Incompetence among People with HIV Improves with Exercise Training in the Exercise for Healthy Aging Study. J Infect Dis 2024.
• Ditzenberger GL, Oliveira VHF, Jankowski CM, Erlandson KM. The use of non-invasive imaging modalities for the assessment of skeletal muscle quantity and quality in people with HIV: a narrative review. HIV Medicine 2023.
• Kulik GL…Erlandson KM. Prognostic Factors of Physical Function Decline Among Middle-Aged Adults With HIV. Open Forum Infect Dis. 2025;12(6):ofaf311. PMID: 40519631; PMCID: PMC12163370.
• Kulik GL, Wilson MP, Jankowski CM, Fourman LT, Erlandson KM. Examining the Heterogeneity of Exercise Response Among Sedentary Older Adults: A Descriptive Analysis. J Aging Res. 2025: PMID: 40134456.
• Kulik GL… Erlandson KM; RECOVER Adult Cohort Consortium. Physical Function Differences by COVID-19 Status: A Cross-sectional Analysis From the RECOVER Adult Cohort. Phys Ther. 2025 PMID: 40302048.
• Jones R… Kulik GL, et al. Examining High-Intensity Exercise on Cognitive and Vascular Outcomes in Older Adults Living With HIV-A Research Protocol: Design and Rationale From Two Harmonized Clinical Studies in the Deep South. J Assoc Nurses AIDS Care. 2025 PMID: 41026763.

--

Trainee: Stefanie Schwab

PharmD Mentor: Kristina Brooks, PharmD

Training pathway: Clinical Investigation in HIV/AIDS

Period of support: 07/01/2024-6/30/2025

Research goals:

• Aim 1. Identify the clinically relevant TFV-DP concentration threshold in DBS associated with a higher risk of future virologic breakthrough in Step 2 of the ACTG LATTITUDE clinical trial.
• Aim 2: Determine the association between having at least two psychosocial factors (e.g., depression, anxiety, substance use, suicidal ideation) and the odds of low TFV-DP in DBS in PWH who received TAF-containing regimens in Step 2 of LATITUDE.
  

Accomplishments: Dr. Schwab has initiated a research training program in the clinical pharmacology of antiretroviral medications in understudied populations with unique physiologic characteristics, such as pregnant people and children. Her research increases understanding of how the relationships between virologic suppression, psychosocial factors, and objective measures of ART adherence. The T32 support ended early pending T32 renewal (resubmission 1/2026).

Career development activities: Dr Schwab is meeting weekly with Dr. Brooks to ensure that Dr. Schwab hits key milestones during the award period. In addition to these regular meetings, Dr. Schwab will have the opportunity to present research ideas and receive feedback from Dr. Brooks, other faculty and lab members through weekly lab meetings, bi-weekly meetings with statistics mentors (Dr. Samantha MaWhinney, Ms. Mary Morrow) in the Colorado School of Public Health. Dr. Schwab is pursuing a Master’s of Science in Clinical Science (MSCS) degree (see table) and she will also undertake additional training in population pharmacokinetic modeling through courses at the University of Colorado Anschutz campus and workshops offered at the local, national, and international levels as those opportunities arise.

Conference presentations:

• Schwab SK. Intracellular carbovir‐ and lamivudine‐triphosphate concentrations in PBMC and DBS among children with HIV‐1 receiving ABC/DTG/3TC: Results from IMPAACT 2019. International Workshop on Clinical Pharmacology of HIV, Hepatitis, and Other Antiviral Drugs, Amsterdam, NE. September 4, 2025.
  
• Schwab SK, Morrow M, MaWhinney S, et al. TFV-DP is Associated with Baseline Virologic Suppression in PWH on TAF: Results from ACTG A5359 [Abstract 653]. In Special Issue: Abstracts from the 2025 Conference on Retroviruses and Opportunistic Infections. Top Antivir Med. 2025;33(1):3-454.
• Schwab SK, Nemkov T, Nerguizian D, et al. Cellular pharmacology of NRTI anabolites in PBMCs and platelets among persons with HIV receiving ABC/3TC- or TAF/FTC-based ART [Abstract #7]. Br J Clin Pharmacol. 2024;90(S1):3–25.Additional Presentations:
• Schwab SK, Morrow M, Coppinger C, et al. Factors Affecting TFV-DP Concentrations in PBMC and Relationships with DBS in PWH on TAF-Based ART [Encore Presentation]. Skaggs School of Pharmacy and Pharmaceutical Sciences Annual Research Retreat. August 2, 2024.
• A Snapshot of the Colorado Antiviral Pharmacology Laboratory's ACTG Projects and Expertise. AIDS Clinical Trials Group (ACTG) Community Advisory Board Meeting, Aurora, CO. August 30, 2024.
• The Role of Psychotropic Medications in Youth with Autism Spectrum Disorders. American Association of Psychiatric Pharmacists Communities Week, Child and Adolescent Psychiatry Community [Virtual]. October 21, 2024.
  

Publications/manuscripts: Several in progress

Honors, fellowship, or other: Young Investigator Scholarship, 25th International Workshop on Clinical Pharmacology of Antiviral Therapy, September 2024

--

Trainee: Priya Vyas, MD

Mentor: Lisa Abuogi, MD

Training pathway: Clinical Investigation in HIV/AIDS

Period of support: 09/01/2024-7/31/2025

Research goals:

• Aim 1. Conduct a systematic literature review to identify evidence-based models of AYA PrEP delivery and best practices.
• Aim 2. Determine barriers to accessing PrEP and preferences regarding PrEP models of care among AYA at risk for HIV in Colorado.
• Aim 3. Develop an evidence-based, youth informed PrEP model of care for an HIV clinic in Colorado and assess the feasibility, acceptability, and appropriateness of the proposed model among providers and patients.
  

Accomplishments: Dr. Vyas implemented a research training program to obtain expertise in the fundamentals of developing and conducting dissemination and implementation sciences with a plan to transition to an independent investigator over the next two years. T32 support ended early pending T32 renewal (1/2026).

Career development activities: Dr. Vyas will complete advanced training in health services, outcomes, and implementation research through the University of Colorado Adult & Child Center for Outcomes Research & Delivery Science (ACCORDS) program. She will complete ACCORDS workshops focused on theories, models, and frameworks as well as study designs. Specific course will include CLSC 6560 Designs and Mixed Methods in Implementation Research. She will develop a K application to support her training as a mentored clinician scientist and pilot test a youth PrEP model developed based on the results of her research conducted with ADEAR support.

Conference presentations:

• Vyas P. Empowering Youth Health: Optimizing HIV Pre-exposure Prophylaxis (PrEP) Delivery Models in Colorado. 2024 Tim Gill Lecture and T32 Research Symposium, Aurora, CO, November 6, 2024.
• Recruitment Challenges for Youth HIV Pre-exposure Prophylaxis (PrEP) Research. Lisa L. Abuogi, MD, MSc, Alexander Limas, Jennifer Moor, AJ De La Garza, Katherine Leonard, Kimberly Pierce, Sam Gallegos, Priya Vyas, MD, Elizabeth J McFarland, MD, Diane Straub, MD. (ID Week 2024)
  

Publications/manuscripts:

• Abuogi, L.L., Imran, R., Limas, A., Moor, J., Leonard, K., Pierce, K., De La Garza, A.J., Gallegos, S., Duenas, J., Littrell, Z., Vyas, P., Richards, M., Straube, D., McFarland, E.J. Feasibility and effectiveness of a telehealth model for youth PrEP (TelePrEP) among youth at risk for HIV in Colorado (Accepted to JIAS)
• Vyas P., McFarland, E.J., Smith, C. “Diagnosis and Clinical Manifestations of HIV Infection” in Principles and Practices of Pediatric Infectious Diseases, 7th Edition.

--

Trainee: Jacob Flynn

Mentor: Catherine Lozupone

Training pathway: Basic/Translational

Period of support: 01/01/2025 – Present

Research goals:

• Characterize the association between gut microbiome composition and functionality and the elevated risk of metabolic syndrome (MetS) in people living with HIV (PLWH), then apply this knowledge to the development of adjunct therapies. The first part of my research project is focused on expanding on those findings with a larger cohort of PLWH, as well as recruitment of uninfected controls to better parse out specific gut microbiome features associated with MetS. The second part of my project is centered on validating the findings in human samples in a murine model of low-grade intestinal insult, meant to recreate the development of MetS in PLWH after transplanting the gut microbiome of our human volunteers into mice. Once validated, I will test adjunct therapies aimed to ameliorate the development of MetS, including administration of butyrate-producing bacterial species and direct supplementation of butyrate to restore this essential metabolite to levels that can support intestinal health.
  

Accomplishments:

• Recruitment of more than half of PLWH needed to complete the human based work involved in my project, thanks to the cooperative effort of our clinical recruitment team. Currently at 11 out of 20 PLWH/MetS+ volunteers and 13 out of 20 PLWH/MetS- volunteers.
• Completion of four pilot experiments to develop appropriate mouse model for verification of human findings. These have included testing varying doses and combinations of dextran sulfate sodium (DSS) and anti-CD4 antibody administration to humanized (gut microbiome) gnotobiotic mice, meant to recapitulate HIV disease pathogenesis through depletion of CD4 T-cells and impairment of the gastrointestinal epithelial barrier. The most recent pilot has tested the effects of a longer colonization period, as recent studies have shown it may take up to five weeks for a transplanted microbiome to efficiently colonize and appropriate host responses to develop. A longer treatment period was also used, as previous pilot studies have not resulted in the development of phenotypes associated with MetS to a significant degree; phenotypes have trended in the right direction, so the hypothesis is that longer treatment will drive MetS-associated phenotypes to a significant degree.
  

Career development activities:

• Organizer for the CU Anschutz Microbiome Research in Progress Seminar Series for the Spring and Fall 2025 semesters (continuing to organize for the Spring 2026 semester)
• Participated in the NIH Fellowship and Career Development Award Workshop Series put on by the Department of Biomedical Informatics to prepare for submitting an F32 Individual Fellowship application (planned submission May 2026)
  

Publications/manuscripts:

• In Submission: Dietary fiber reduces mortality from secondary blood infections in a murine model of antibiotic-induced Clostridioides difficile infection