Peter D Kwong

National Institutes of Health, Maryland, United States

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Publications (184)2033.12 Total impact

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    ABSTRACT: The human immunodeficiency virus type 1 (HIV-1) envelope (Env) spike, comprising three gp120 and three gp41 subunits, is a conformational machine that facilitates HIV-1 entry by rearranging from a mature unliganded state, through receptor-bound intermediates, to a post-fusion state. As the sole viral antigen on the HIV-1 virion surface, Env is both the target of neutralizing antibodies and a focus of vaccine efforts. Here we report the structure at 3.5 A resolution for an HIV-1 Env trimer captured in a mature closed state by antibodies PGT122 and 35O22. This structure reveals the pre-fusion conformation of gp41, indicates rearrangements needed for fusion activation, and defines parameters of immune evasion and immune recognition. Pre-fusion gp41 encircles amino- and carboxy-terminal strands of gp120 with four helices that form a membrane-proximal collar, fastened by insertion of a fusion peptide-proximal methionine into a gp41-tryptophan clasp. Spike rearrangements required for entry involve opening th
    Nature 10/2014; advance online publication. · 38.60 Impact Factor
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    ABSTRACT: The HIV-1 envelope (Env) mediates viral entry into host cells. To enable the direct imaging of conformational dynamics within Env we introduced fluorophores into variable regions of the gp120 subunit and measured single-molecule fluorescence resonance energy transfer (smFRET) within the context of native trimers on the surface of HIV-1 virions. Our observations revealed unliganded HIV-1 Env to be intrinsically dynamic, transitioning between three distinct pre-fusion conformations, whose relative occupancies were remodeled by receptor CD4 and antibody binding. The distinct properties of neutralization-sensitive and neutralization-resistant HIV-1 isolates support a dynamics-based mechanism of immune evasion and ligand recognition.
    Science (New York, N.Y.). 10/2014;
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    ABSTRACT: The HIV-1 surface envelope glycoprotein (Env) trimer mediates entry into CD4+/CCR5+ host cells. Env possesses conserved antigenic determinants, such as the gp120 primary receptor CD4 binding site (CD4bs), a known neutralization target. Env also contains variable regions and protein surfaces occluded within the trimer that elicit non-neutralizing antibodies. Here, we engineered additional N-linked glycans onto a cysteine-stabilized gp120 core (0G) deleted of its major variable regions to preferentially expose the conformationally fixed CD4bs. Three, 6, 7 and 10 new NXT/S glycan (G) motifs were engineered into 0G to encode 3G, 6G, 7G and 10G cores. Following purification, most glycoproteins were recognized by broadly neutralizing CD4bs-directed antibodies except for 10G. Gel and glycan mass-spectrometry confirmed that additional N-glycans were post-translationally added to the redesigned cores. Binding kinetics revealed high-affinity recognition by seven broadly neutralizing CD4bs-directed antibodies and low-to-no binding by non-broadly-neutralizing CD4bs-directed antibodies. Rabbits inoculated with the hyperglycosylated cores elicited IgM and IgG responses to each given protein that were similar to those elicited by parental 0G. Site-specific glycan masking effects were detected in the elicited sera and the anti-sera competed with b12 for CD4bs-directed binding specificity. However, the core-elicited sera showed very limited neutralization activity. Trimer priming or boosting of the core immunogens elicited tier 1-level neutralization that mapped to both the CD4bs and V3 and appeared solely trimer-dependent. Fine-mapping at the CD4bs indicated that conformational stabilization of the cores and addition of N-glycans altered the molecular surface, suggesting why the elicited neutralization was not improved by this rational-design strategy.
    Journal of virology. 09/2014;
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    ABSTRACT: Extending our previous analyses to the most recently described broadly neutralizing monoclonal antibodies (bNAbs) we confirm a drift of HIV-1 clade B variants over two decades toward higher resistance to bNAbs targeting almost all the identified gp120 neutralizing epitopes. In contrast, the sensitivity to bNAbs targeting the gp41 MPER remained stable, suggesting a selective pressure on gp120 preferentially. Despite this evolution, selected combinations of bNAbs remain capable to neutralize efficiently most of the circulating variants.
    Journal of virology. 09/2014;
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    ABSTRACT: Induction of HIV-1 broad neutralizing antibodies (bnAbs) is a goal of HIV-1 vaccine development but has remained challenging partially due to unusual traits of bnAbs, including high somatic hypermutation (SHM) frequencies and in-frame insertions and deletions (indels). Here we examined the propensity and functional requirement for indels within HIV-1 bnAbs. High-throughput sequencing of the immunoglobulin (Ig) VHDJH genes in HIV-1 infected and uninfected individuals revealed that the indel frequency was elevated among HIV-1-infected subjects, with no unique properties attributable to bnAb-producing individuals. This increased indel occurrence depended only on the frequency of SHM point mutations. Indel-encoded regions were generally proximal to antigen binding sites. Additionally, reconstruction of a HIV-1 CD4-binding site bnAb clonal lineage revealed that a large compound VHDJH indel was required for bnAb activity. Thus, vaccine development should focus on designing regimens targeted at sustained activation of bnAb lineages to achieve the required SHM and indel events.
    Cell Host & Microbe 09/2014; 16(3):304-313. · 12.61 Impact Factor
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    ABSTRACT: The isolation of human monoclonal antibodies is providing important insights into the specificities that underlie broad neutralization of HIV-1 (reviewed in ref. 1). Here we report a broad and extremely potent HIV-specific monoclonal antibody, termed 35O22, which binds a novel HIV-1 envelope glycoprotein (Env) epitope. 35O22 neutralized 62% of 181 pseudoviruses with a half-maximum inhibitory concentration (IC50) <50 μg ml(-1). The median IC50 of neutralized viruses was 0.033 μg ml(-1), among the most potent thus far described. 35O22 did not bind monomeric forms of Env tested, but did bind the trimeric BG505 SOSIP.664. Mutagenesis and a reconstruction by negative-stain electron microscopy of the Fab in complex with trimer revealed that it bound to a conserved epitope, which stretched across gp120 and gp41. The specificity of 35O22 represents a novel site of vulnerability on HIV Env, which serum analysis indicates to be commonly elicited by natural infection. Binding to this new site of vulnerability may thus be an important complement to current monoclonal-antibody-based approaches to immunotherapies, prophylaxis and vaccine design.
    Nature 09/2014; · 38.60 Impact Factor
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    ABSTRACT: The RV144 vaccine trial implicated epitopes in the C1 region of gp120 (A32-like epitopes) as targets of potentially protective antibody-dependent cellular cytotoxicity (ADCC) responses. A32-like epitopes are highly immunogenic as infected or vaccinated individuals frequently elicit antibodies specific for these determinants. Antibody-binding titers as measured by ELISA against these epitopes, however, do not consistently correlate with protection. Here, we report crystal structures of CD4-stabilized gp120 cores complexed with the Fab fragments of two non-neutralizing, A32-like monoclonal antibodies (mAbs), named N5-i5 and 2.2c, that compete for antigen binding and exhibit similar binding affinities, yet mediate a 75-fold difference in ADCC potency. We find that these mAbs recognize overlapping epitopes formed by mobile layers 1 and 2 of the gp120 inner domain including the C1-C2 regions, but bind gp120 at different angles via juxtaposed VH and VL contact surfaces. A comparison of structural and immunological data further showed that antibody orientation on bound antigen and the capacity to form multivalent antigen-antibody complexes on target cells were key determinants for ADCC potency, with the latter process having the greater impact. These studies provide atomic level definition of A32-like epitopes implicated as targets of protective antibodies in RV144. Moreover, these studies establish that epitope structure and mode of antibody binding can dramatically affect the potency of Fc-mediated effector function against HIV-1. These results provide key insights for understanding, refining, and improving the outcome of HIV-vaccine trials, in which relevant immune responses are facilitated by A32-like elicited responses.
    Journal of virology. 08/2014;
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    ABSTRACT: Development of strategies for induction of HIV-1 broadly neutralizing antibodies (bnAbs) by vaccines is a priority. Determining the steps of bnAb induction in HIV-1-infected individuals who make bnAbs is a key strategy for immunogen design. Here, we study the B cell response in a bnAb-producing individual and report cooperation between two B cell lineages to drive bnAb development. We isolated a virus-neutralizing antibody lineage that targeted an envelope region (loop D) and selected virus escape mutants that resulted in both enhanced bnAb lineage envelope binding and escape mutant neutralization-traits associated with increased B cell antigen drive. Thus, in this individual, two B cell lineages cooperated to induce the development of bnAbs. Design of vaccine immunogens that simultaneously drive both helper and broadly neutralizing B cell lineages may be important for vaccine-induced recapitulation of events that transpire during the maturation of neutralizing antibodies in HIV-1-infected individuals.
    Cell 07/2014; 158(3):481-91. · 31.96 Impact Factor
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    ABSTRACT: We previously identified two small molecule CD4 mimetics-NBD-556 and NBD-557-and synthesized a series of NBD compounds, resulting in improved neutralization activity in a single-cycle HIV-1-infectivity assay. For this investigation, we selected several of the most active compounds and assessed their antiviral activity on a panel of 53 reference HIV-1 ENV pseudoviruses, representing diverse clades of clinical isolates. The selected compounds inhibited tested clades with low micromolar potency. Mechanism studies indicate that they act as CD4-agonists, a potentially unfavorable therapeutic trait, in that they can bind to the gp120 envelope glycoprotein and initiate a similar physiological response as CD4. However, one of the compounds, NBD-09027, exhibited reduced agonist properties, in both functional and biophysical studies. To understand the binding mode of these inhibitors, we first generated HIV-1-resistant mutants and assessed their behavior with NBD compounds and determined the X-ray structures of two inhibitors, NBD-09027 and NBD-10007, in complex with the HIV-1 gp120 core at ∼2-Å resolution. Both studies confirmed that the NBD compounds bind similar to NBD-556 and NBD-557-by inserting their hydrophobic groups into the Phe43-cavity of gp120. The basic nitrogen of the piperidine ring is located in close proximity to D368 of gp120 but does not form any H-bond or salt-bridge-a likely explanation for their nonoptimal antagonist properties. The results reveal the structural and biological character of the NBD series of CD4 mimetics and identify ways to reduce their agonist properties and convert them to antagonists.
    Antimicrobial Agents and Chemotherapy 07/2014; · 4.57 Impact Factor
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    ABSTRACT: HIV-1 infection depends on effective viral entry mediated by the interaction of its envelope (Env) glycoprotein with specific cell surface receptors. Protective antiviral antibodies generated by passive or active immunization must prevent these interactions. Because the HIV-1 Env is highly variable, attention has also focused on blocking the HIV-1 primary cell receptor CD4. We therefore analyzed the in vivo protective efficacy of three potent neutralizing monoclonal antibodies (mAbs) to HIV-1 Env compared to an antibody against the CD4 receptor. Protection was assessed after mucosal challenge of rhesus macaques with simian/HIV (SHIV). Despite its comparable or greater neutralization potency in vitro, the anti-CD4 antibody did not provide effective protection in vivo, whereas the HIV-1-specific mAbs VRC01, 10E8, and PG9, targeting the CD4 binding site, membrane-proximal, and V1V2 glycan Env regions, respectively, conferred complete protection, albeit at different relative potencies. These findings demonstrate the protective efficacy of broadly neutralizing antibodies directed to the HIV-1 Env and suggest that targeting the HIV-1 Env is preferable to the cell surface receptor CD4 for the prevention of HIV-1 transmission.
    Science translational medicine 07/2014; 6(243):243ra88. · 10.76 Impact Factor
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    ABSTRACT: Delineation of the antigenic site, or epitope, recognized by an antibody can provide clues about functional vulnerabilities and resistance mechanisms, and can therefore guide antibody optimization and epitope-based vaccine design. Previously, we developed an algorithm for antibody-epitope prediction based on antibody neutralization of viral strains with diverse sequences and validated the algorithm on a set of broadly neutralizing HIV-1 antibodies. Here we describe the implementation of this algorithm, NEP (Neutralization-based Epitope Prediction), as a web-based server. The users must supply as input: (i) an alignment of antigen sequences of diverse viral strains; (ii) neutralization data for the antibody of interest against the same set of antigen sequences; and (iii) (optional) a structure of the unbound antigen, for enhanced prediction accuracy. The prediction results can be downloaded or viewed interactively on the antigen structure (if supplied) from the web browser using a JSmol applet. Since neutralization experiments are typically performed as one of the first steps in the characterization of an antibody to determine its breadth and potency, the NEP server can be used to predict antibody-epitope information at no additional experimental costs. NEP can be accessed on the internet at
    Nucleic Acids Research 04/2014; · 8.81 Impact Factor
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    ABSTRACT: Antibodies capable of neutralizing HIV-1 often target variable regions 1 and 2 (V1V2) of the HIV-1 envelope, but the mechanism of their elicitation has been unclear. Here we define the developmental pathway by which such antibodies are generated and acquire the requisite molecular characteristics for neutralization. Twelve somatically related neutralizing antibodies (CAP256-VRC26.01-12) were isolated from donor CAP256 (from the Centre for the AIDS Programme of Research in South Africa (CAPRISA)); each antibody contained the protruding tyrosine-sulphated, anionic antigen-binding loop (complementarity-determining region (CDR) H3) characteristic of this category of antibodies. Their unmutated ancestor emerged between weeks 30-38 post-infection with a 35-residue CDR H3, and neutralized the virus that superinfected this individual 15 weeks after initial infection. Improved neutralization breadth and potency occurred by week 59 with modest affinity maturation, and was preceded by extensive diversification of the virus population. HIV-1 V1V2-directed neutralizing antibodies can thus develop relatively rapidly through initial selection of B cells with a long CDR H3, and limited subsequent somatic hypermutation. These data provide important insights relevant to HIV-1 vaccine development.
    Nature 03/2014; · 38.60 Impact Factor
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    ABSTRACT: Conspectus This Account provides an overview of a multidisciplinary consortium focused on structure-based strategies to devise small molecule antagonists of HIV-1 entry into human T-cells, which if successful would hold considerable promise for the development of prophylactic modalities to prevent HIV transmission and thereby alter the course of the AIDS pandemic. Entry of the human immunodeficiency virus (HIV) into target T-cells entails an interaction between CD4 on the host T-cell and gp120, a component of the trimeric envelope glycoprotein spike on the virion surface. The resultant interaction initiates a series of conformational changes within the envelope spike that permits binding to a chemokine receptor, formation of the gp41 fusion complex, and cell entry. A hydrophobic cavity at the CD4-gp120 interface, defined by X-ray crystallography, provided an initial site for small molecule antagonist design. This site however has evolved to facilitate viral entry. As such, the binding of prospective small molecule inhibitors within this gp120 cavity can inadvertently trigger an allosteric entry signal. Structural characterization of the CD4-gp120 interface, which provided the foundation for small molecule structure-based inhibitor design, will be presented first. An integrated approach combining biochemical, virological, structural, computational, and synthetic studies, along with a detailed analysis of ligand binding energetics, revealed that modestly active small molecule inhibitors of HIV entry can also promote viral entry into cells lacking the CD4 receptor protein; these competitive inhibitors were termed small molecule CD4 mimetics. Related congeners were subsequently identified with both improved binding affinity and more potent viral entry inhibition. Further assessment of the affinity-enhanced small molecule CD4 mimetics demonstrated that premature initiation of conformational change within the viral envelope spike, prior to cell encounter, can lead to irreversible deactivation of viral entry machinery. Related congeners, which bind the same gp120 site, possess different propensities to elicit the allosteric response that underlies the undesired enhancement of CD4-independent viral entry. Subsequently, key hotspots in the CD4-gp120 interface were categorized using mutagenesis and isothermal titration calorimetry according to the capacity to increase binding affinity without triggering the allosteric signal. This analysis, combined with cocrystal structures of small molecule viral entry agonists with gp120, led to the development of fully functional antagonists of HIV-1 entry. Additional structure-based design exploiting two hotspots followed by synthesis has now yielded low micromolar inhibitors of viral entry.
    Accounts of Chemical Research 02/2014; · 20.83 Impact Factor
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    ABSTRACT: Abs capable of effectively neutralizing HIV-1 generally exhibit very high levels of somatic hypermutation, both in their CDR and framework-variable regions. In many cases, full reversion of the Ab-framework mutations back to germline results in substantial to complete loss of HIV-1-neutralizing activity. However, it has been unclear whether all or most of the observed framework mutations would be necessary or whether a small subset of these mutations might be sufficient for broad and potent neutralization. To address this issue and to explore the dependence of neutralization activity on the level of somatic hypermutation in the Ab framework, we applied a computationally guided framework-reversion procedure to two broadly neutralizing anti-HIV-1 Abs, VRC01 and 10E8, which target two different HIV-1 sites of vulnerability. Ab variants in which up to 78% (38 of 49 for VRC01) and 89% (31 of 35 for 10E8) of framework mutations were reverted to germline retained breadth and potency within 3-fold of the mature Abs when evaluated on a panel of 21 diverse viral strains. Further, a VRC01 variant with an ∼50% framework-reverted L chain showed a 2-fold improvement in potency over the mature Ab. Our results indicate that only a small number of Ab-framework mutations may be sufficient for high breadth and potency of HIV-1 neutralization by Abs VRC01 and 10E8. Partial framework revertants of HIV-1 broadly neutralizing Abs may present advantages over their highly mutated counterparts as Ab therapeutics and as targets for immunogen design.
    The Journal of Immunology 01/2014; · 5.52 Impact Factor
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    ABSTRACT: Efforts to develop therapeutic agents that inhibit HIV-1 entry have led to the identification of several small molecule leads. One of the most promising is the NBD series, which binds within a conserved gp120 cavity and possesses para-halogen substituted aromatic rings, a central oxalamide linker, and a tetramethylpiperidine moiety. In this study, we characterized structurally the interactions of four NBD analogues containing meta-fluoro substitution on the aromatic ring and various heterocyclic ring replacements of the tetramethylpiperidine group. The addition of a meta-fluorine to the aromatic ring improved surface complementarity and did not alter the position of the analogue relative to gp120. By contrast, heterocyclic ring replacements of the tetramethylpiperidine moiety exhibited diverse positioning and interactions with the vestibule of the gp120 cavity. Overall, the biological profile of NBD-congeners was modulated by ligand interactions with the gp120-cavity vestibule. Herein, six co-crystal structures of NBD-analogues with gp120 provide a structural framework for continued small molecule-entry inhibitor optimization.
    PLoS ONE 01/2014; 9(1):e85940. · 3.53 Impact Factor
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    ABSTRACT: Over the past five years, a new generation of highly potent and broadly neutralizing HIV-1 antibodies has been identified. These antibodies can protect against lentiviral infection in non-human primates, suggesting that passive antibody transfer would prevent HIV-1 transmission in humans. To increase the protective efficacy of such monoclonal antibodies, we employed next-generation sequencing, computational bioinformatics, and structure-guided design to enhance the neutralization potency and breadth of VRC01, an antibody that targets the CD4 binding site of the HIV-1 envelope. One variant, VRC07-523, was 5- to 8-fold more potent than VRC01, neutralized 96% of viruses tested, and displayed minimal autoreactivity. To compare its protective efficacy to VRC01 in vivo, we performed a series of simian-HIV (SHIV) challenge experiments in non-human primates and calculated the doses of VRC07-523 and VRC01 that provide 50% protection (EC50). VRC07-523 prevented infection in NHPs at a 5-fold lower concentration than VRC01. These results suggest that increased neutralization potency in vitro correlates with improved protection against infection in vivo, documenting the improved functional efficacy of VRC07-523 and its potential clinical relevance for protecting against HIV-1 infection in humans.IMPORTANCE In the absence of an effective HIV-1 vaccine, alternative strategies are needed to block HIV-1 transmission. Direct administration of HIV-1-neutralizing antibodies may be able to prevent HIV-1 infections in humans. This approach could be especially useful in individuals at high risk for contracting HIV-1 and could be used together with antiretroviral drugs to prevent infection. To optimize the chance of success, such antibodies can be modified to improve their potency, breadth, and in vivo half-life. Here, knowledge of the structure of a potent neutralizing antibody VRC01, that targets the CD4-binding site of the HIV-1 envelope protein, was used to engineer a next-generation antibody with 5-8 fold increased potency in vitro. When administered to non-human primates, this antibody conferred protection at a five-fold lower concentration than the original antibody. Our studies demonstrate an important correlation between in vitro assays used to evaluate therapeutic potential of antibodies and their in vivo effectiveness.
    Journal of Virology. 01/2014;
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    ABSTRACT: Antibodies m66.6 and 2F5 are the only effective human HIV-1-neutralizing antibodies identified thus far that recognize the N-terminal region of the membrane-proximal external region (MPER) of the gp41 subunit of the HIV-1 viral spike. Although 2F5 has been extensively characterized, much less is known about antibody m66.6 or antibody m66, a closely related light-chain variant. Here, we report the crystal structure of m66 in complex with its gp41 epitope, along with unbound structures of m66 and m66.6. We employed mutational and binding analyses to decipher antibody elements critical for recognition of their gp41 epitopes, and determined the molecular basis that underlies their neutralization of HIV-1. When bound by m66, the N-terminal region of the gp41 MPER adopts a conformation comprising a helix followed by an extended loop. Comparison of gp41-bound m66 with unbound m66.6 identified three light chain residues of m66.6 that were confirmed through mutagenesis to underlie the superior breadth and potency of m66.6-mediated virus neutralization. Recognition of gp41 by m66 also revealed similarities to antibody 2F5 both in the conformation of crucial epitope residues as well as in the angles of antibody approach. Aromatic residues at the tip of the m66.6-heavy chain third complementarity-determining region, as in the case of 2F5, were determined to be critical for virus neutralization in a manner that correlated with antibody recognition of the MPER in a lipid context. Antibodies m66, m66.6, and 2F5 thus utilize similar mechanistic elements to recognize a common gp41-MPER epitope and neutralize HIV-1.
    Journal of Virology 12/2013; · 5.08 Impact Factor
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    ABSTRACT: Respiratory syncytial virus (RSV) is the leading cause of hospitalization for children under 5 years of age. We sought to engineer a viral antigen that provides greater protection than currently available vaccines and focused on antigenic site Ø, a metastable site specific to the prefusion state of the RSV fusion (F) glycoprotein, as this site is targeted by extremely potent RSV-neutralizing antibodies. Structure-based design yielded stabilized versions of RSV F that maintained antigenic site Ø when exposed to extremes of pH, osmolality, and temperature. Six RSV F crystal structures provided atomic-level data on how introduced cysteine residues and filled hydrophobic cavities improved stability. Immunization with site Ø-stabilized variants of RSV F in mice and macaques elicited levels of RSV-specific neutralizing activity many times the protective threshold.
    Science 11/2013; 342(6158):592-8. · 31.20 Impact Factor

Publication Stats

15k Citations
2,033.12 Total Impact Points

Top Journals


  • 2003–2014
    • National Institutes of Health
      Maryland, United States
    • National Institute of Allergy and Infectious Diseases
      • Laboratory of Immunoregulation
      Maryland, United States
  • 2013
    • National Human Genome Research Institute
      Maryland, United States
  • 2011–2013
    • Duke University Medical Center
      • • Duke Human Vaccine Institute
      • • Department of Medicine
      Durham, NC, United States
    • CUNY Graduate Center
      New York City, New York, United States
    • Simon Fraser University
      • Department of Molecular Biology and Biochemistry
      Burnaby, British Columbia, Canada
  • 2012
    • Oxford University Hospitals NHS Trust
      Oxford, England, United Kingdom
    • University of Pennsylvania
      • Perelman School of Medicine
      Philadelphia, PA, United States
    • National Institute of Allergy and Infectious Disease
      Maryland, United States
    • National Institute of Infectious Diseases, Tokyo
      Edo, Tōkyō, Japan
    • Massachusetts Institute of Technology
      Cambridge, Massachusetts, United States
    • Duke University
      Durham, North Carolina, United States
    • Tulane University
      • Department of Pediatrics
      New Orleans, Louisiana, United States
    • Yale-New Haven Hospital
      New Haven, Connecticut, United States
  • 2011–2012
    • Bryn Mawr College
      • Department of Chemistry
      Bryn Mawr, PA, United States
  • 2010–2012
    • Harvard Medical School
      Boston, Massachusetts, United States
    • International AIDS Vaccine Initiative
      New York City, New York, United States
  • 2003–2012
    • University of Alabama at Birmingham
      • • Department of Medicine
      • • Department of Microbiology
      Birmingham, Alabama, United States
  • 2000–2012
    • Dana-Farber Cancer Institute
      • Department of Cancer Immunology and AIDS
      Boston, MA, United States
  • 2004–2009
    • The Scripps Research Institute
      • Department of Immunology and Microbial Science
      La Jolla, California, United States
    • Fachhochschule des bfi Wien
      Wien, Vienna, Austria
  • 1989–2007
    • Columbia University
      • Department of Biochemistry and Molecular Biophysics
      New York City, NY, United States
  • 2000–2002
    • Howard Hughes Medical Institute
      Ashburn, Virginia, United States