Douglas F Nixon

George Washington University, Washington, Washington, D.C., United States

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Publications (229)1367.36 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: HTLV-1, the first human retrovirus described, is the causative agent of a neglected disease affecting 5 - 10 million people worldwide. While often considered a lifelong asymptomatic disease, neurological complications including progressive neurodegeneration and an aggressive adult T-cell leukemia (ATL), which can arise in up to 10% of HTLV-1-infected individuals. The mode of transmission for this retrovirus is through blood or sexual contact, and mother-to-child-transmission (MTCT) occurs in approximately 20% of infants breastfed for 6 months or more. However, the advantages of breastfeeding over formula feeding to prevent overall child morbidity and mortality have been well established, especially in developing countries. This creates a paradox, whereby refrainment of breastfeeding to prevent HTLV-1 transmission has been effective in a developed country such as Japan, but is inappropriate for developing countries with higher infant morbidity and mortality. In HIV-1 infection, maternal and infant antiretroviral therapy (ART) is one of the most important measures to prevent HIV-1 MTCT. If ART was used to prevent post partum HTLV-1 infection of neonates through breast milk feeding, HTLV-1 transmission could be halted. However, prevention of vertical HTLV-1 infection is not part of routine health care practice. Interestingly, studies demonstrate the capacity of AZT to significantly inhibit HTLV-1 infection of lymphocytes in vitro. We suggest that in areas of high prevalence of HTLV-1 infection, formal guidelines be adopted to screen pregnant women for HTLV-1 and a trial performed to assess the therapeutic benefit of ART for women during delivery, and for the infant for the duration of breastfeeding, to prevent HTLV-1 transmission. A way to stop HTLV-1 vertical transmission should be pursued and offered to mothers and children in areas of high HTLV-1 prevalence around the globe.
    AIDS research and human retroviruses. 10/2014;
  • JAIDS Journal of Acquired Immune Deficiency Syndromes 10/2014; · 4.39 Impact Factor
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    ABSTRACT: Memory stem T cells (TSCM) constitute a long-lived, self-renewing lymphocyte population essential for the maintenance functional immunity. The hallmarks of HIV-1 pathogenesis are CD4(+) T cell depletion and abnormal cellular activation. We investigated the impact of HIV-1 infection on the TSCM compartment, as well as any protective role these cells may have in disease progression, by characterizing this subset in a cohort of 113 subjects with variable degrees of viral control on and off highly active antiretroviral therapy (HAART). We observed that the frequency of CD8(+) TSCM is decreased in all individuals with chronic, untreated HIV-1 infection, and that HAART has a restorative effect on this subset. In contrast, natural controllers of HIV-1 had the highest absolute number of CD4(+) TSCM cells among all of the infected groups. The frequency of CD4(+) TSCM predicted higher CD8(+) TSCM frequencies, consistent with a role for the CD4(+) subset in helping to maintain CD8(+) memory T cells. In addition, TSCM appeared to be progenitors for effector T cells (TEM), as these two compartments were inversely correlated. Increased frequencies of CD8(+) TSCM predicted lower viral loads, higher CD4(+) counts and less CD8(+) T cell activation. Finally, we found that TSCM express the mucosal homing integrin α4β7 and can be identified in the gastrointestinal-associated lymphoid tissue (GALT). The frequency of mucosal CD4(+) TSCM was inversely correlated with that in the blood, potentially reflecting the ability of these self-renewing cells to migrate to a crucial site of ongoing viral replication and CD4(+) T cell depletion.
    Journal of Virology 09/2014; · 4.65 Impact Factor
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    ABSTRACT: Background Psoriasis is a multifactorial, chronic disease of skin affecting 2-3 % of the world¿s population. Genetic studies of psoriasis have identified a number of susceptibility genes that are involved in anti-viral immunity. Furthermore, physiological studies have also found an increase in anti-viral proteins in psoriatic skin. These findings suggest the presence of an anti-viral state in psoriatic skin. However, the triggers for this anti-viral cascade and its consequences for host immunity are not known. Endogenous retroviruses have previously been described in many autoimmune diseases including psoriasis.Methods In the present study we examined the humoral immune response against human endogenous retrovirus-K (HERV-K) proteins and the cutaneous expression levels of multiple HERV-K genes in psoriasis patients and healthy controls.ResultsIn psoriatic sera we observed a significant decrease in IgM response against three HERV-K proteins: Env surface unit (SU), Env transmembrane protein (TM), and Gag capsid (CA) in comparison to sera obtained from blood bank healthy controls. A decrease in IgG response was also observed against CA. Furthermore, using quantitative RT-PCR we observed a decrease in the expression of HERV-K Env, Gag, Pol and Rec as well as ERV-9 genes in lesional psoriatic skin as compared to healthy skin.Conclusions Together, our results suggest that the pro-inflammatory, anti-viral state in psoriasis is associated with diminished expression of HERV-K gene transcripts and a concomitant decrease in humoral responses to HERV-K. Our results indicate that a simple model where continuous, minimally changing HERV-K expression serves as an antigenic trigger in psoriasis might not be correct and further studies are needed to decipher the possible relationship between psoriasis and HERVs.
    Journal of Translational Medicine 09/2014; 12(1):256. · 3.99 Impact Factor
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    ABSTRACT: In this study, we investigated the expression levels of host restriction factors in six untreated HIV-1-positive patients over the course of infection. We found that the host restriction factor gene expression profile consistently increased over time and significantly associated with CD4(+) T cell activation and viral load. Our data are among the first to demonstrate the dynamic nature of host restriction factors in vivo over time.
    Journal of Virology 07/2014; · 4.65 Impact Factor
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    ABSTRACT: The failure of antiviral vaccines is often associated with rapid viral escape from specific immune responses. In the past, conserved epitope or algorithmic epitope selections, such as mosaic vaccines, have been designed to diversify immunity and to circumvent potential viral escape. An alternative approach is to identify conserved stable non-HIV-1 self-epitopes present exclusively in HIV-1-infected cells. We showed previously that human endogenous retroviral (HERV) mRNA transcripts and protein are found in cells of HIV-1-infected patients and that HERV-K (HML-2)-specific T cells can eliminate HIV-1-infected cells in vitro. In this article, we demonstrate that a human anti-HERV-K (HML-2) transmembrane protein Ab binds specifically to HIV-1-infected cells and eliminates them through an Ab-dependent cellular cytotoxicity mechanism in vitro. Thus, Abs directed against epitopes other than HIV-1 proteins may have a role in eliminating HIV-1-infected cells and could be targeted in novel vaccine approaches or immunotherapeutic modalities.
    The Journal of Immunology 07/2014; · 5.36 Impact Factor
  • Journal of alternative and complementary medicine (New York, N.Y.); 05/2014
  • Journal of alternative and complementary medicine (New York, N.Y.) 05/2014; 20(5):A15. · 1.69 Impact Factor
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    ABSTRACT: Chronic stress has deleterious effects on immune function, which can lead to adverse health outcomes. However, studies investigating the impact of stress reduction interventions on immunity in clinical research have yielded divergent results, potentially stemming from differences in study design and genetic heterogeneity, among other clinical research challenges. To test the hypothesis that reducing glucocorticoid levels enhances certain immune functions, we administered influenza vaccine once (prime) or twice (boost) to mice housed in either standard control caging or environmental enrichment (EE) caging, an approach we have shown reduces mouse corticosterone production. Compared with controls, EE mice had significantly lower levels of fecal corticosterone metabolites (FCM) and increased splenic B and T lymphocyte numbers. Corticosterone levels were negatively associated with the numbers of CD19(+) (r(2)=0.43, p=0.0017), CD4(+), (r(2)=0.28, p=0.0154) and CD8(+) cells (r(2)=0.20, p=0.0503). Vaccinated mice showed non-significant differences in IgG titer between caging groups, although EE mice tended to exhibit larger increases in titer from prime to boost than controls; the interaction between caging group (control vs. EE) and vaccine group (prime vs. boost) showed a strong statistical trend (Cage-Group*Vaccine-Group, F=4.27, p=0.0555), suggesting that there may be distinct effects of EE caging on primary versus secondary IgG vaccine responses. Vaccine-stimulated splenocytes from boosted EE mice had a significantly greater frequency of IL-5 secreting cells than boosted controls (Meandiff 67.7 IL-5 SFU/10(6) splenocytes, CI95 0.24 to 135.1, p=0.0493), and showed a greater increase in the frequency of IL-5 secreting cells from prime to boost. Our results suggest that corticosterone reduction via EE caging was associated with enhanced secondary vaccine responses, but had little effect on primary responses in mice. These findings help identify differences in primary and secondary vaccine responses in relationship to stress mediators that may be relevant in clinical studies.
    Molecular Medicine 03/2014; 20:179-190. · 4.82 Impact Factor
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    ABSTRACT: The enormous sequence diversity of HIV remains a major roadblock to the development of a prophylactic vaccine and new approaches to induce protective immunity are needed. Endogenous retrotransposable elements (ERE) such as endogenous retrovirus K (ERV)-K and long interspersed nuclear element-1 (LINE-1) are activated during HIV-1-infection and could represent stable, surrogate targets to eliminate HIV-1-infected cells. Here, we explored the hypothesis that vaccination against ERE would protect macaques from acquisition and replication of simian immunodeficiency virus (SIV). Following vaccination with antigens derived from LINE-1 and ERV-K consensus sequences, animals mounted immune responses that failed to delay acquisition of SIVsmE660. We observed no differences in acute or set point viral loads between ERE-vaccinated and control animals suggesting that ERE-specific responses were not protective. Indeed, ERE-specific T cells failed to expand anamnestically in vivo following infection with SIVsmE660 and did not recognize SIV-infected targets in vitro, in agreement with no significant induction of targeted ERE mRNA by SIV in macaque CD4+ T cells. Instead, lower infection rates and viral loads correlated significantly to protective TRIM5α alleles. Cumulatively, these data demonstrate that vaccination against the selected ERE consensus sequences in macaques did not lead to immune-mediated recognition and killing of SIV-infected cells, as has been shown for HIV-infected human cells using patient-derived HERV-K-specific T cells. Thus, further research is required to identify the specific nonhuman primate EREs and retroviruses that recapitulate the activity of HIV-1 in human cells. These results also highlight the complexity in translating observations of the interplay between HIV-1 and human EREs to animal models.
    PLoS ONE 03/2014; 9(3):e92012. · 3.53 Impact Factor
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    ABSTRACT: Invariant natural killer T (iNKT) cells are CD1d-restricted immunoregulatory lymphocytes that share characteristics of both the innate and adaptive immune systems. Although it has been reported that iNKT cells are present in the human fetal thymus, it is currently unknown how they distribute, differentiate, and function in fetal peripheral lymphoid and non-lymphoid organs. Here, we show that functional human fetal iNKT cells develop and differentiate in a tissue-specific manner during the second trimester. Fetal iNKT cells accumulated in the small intestine, where they gained a mature phenotype and mounted robust interferon (IFN)-γ responses. In contrast, iNKT cells in the spleen and mesenteric lymph nodes were less frequently detected, less differentiated, mounted poor IFN-γ responses, but proliferated vigorously upon stimulation with α-galactosylceramide. These data demonstrate that fetal iNKT cells can differentiate and acquire potent effector functions in utero before the establishment of the commensal microflora.Mucosal Immunology advance online publication, 19 March 2014; doi:10.1038/mi.2014.13.
    Mucosal Immunology 03/2014; · 7.54 Impact Factor
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    ABSTRACT: Human Endogenous Retroviruses (HERVs) comprise about 8% of the human genome and have lost their ability to replicate or to produce infectious particles after having accumulated mutations over time. We assessed the kinetics of expression of HERV-K (HML-2) Envelope mRNA transcript and surface unit (SU) and transmembrane (TM) subunit proteins during HIV-1 infection. We also mapped the specificity of the humoral response to HERV-K (HML-2) Envelope protein in HIV-1 infected subjects at different stages of disease, and correlated the response with plasma viral load. We found that HIV-1 modified HERV-K (HML-2) Env mRNA expression, resulting in the expression of a fully N-glycosylated HERV-K (HML-2) envelope protein on the cell surface. Serological mapping of HERV-K (HML-2) envelope protein linear epitopes revealed two major immunogenic domains, one on SU and another on the ectodomain of TM. The titers of HERV-K (HML-2) TM antibodies were dramatically increased in HIV-1 infected subjects (p < 0.0001). HIV-1 infected adults who control HIV-1 in the absence of therapy ("elite" controllers) had a higher titer response against TM compared to antiretroviral-treated adults (p < 0.0001) and uninfected adults (p < 0.0001). These data collectively suggest that HIV-1 infection induces fully glycosylated HERV-K (HML-2) envelope TM protein to which antibodies are induced. These anti-HERV-K (HML-2) TM antibodies are a potential marker of HIV-1 infection, and are at higher titer in elite controllers. HERV-K (HML-2) envelope TM protein may be a new therapeutic target in HIV-1 infection.
    Retrovirology 01/2014; 11(1):10. · 4.77 Impact Factor
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    ABSTRACT: Innate-like, evolutionarily conserved MR1-restricted mucosa-associated invariant T (MAIT) cells represent a large antimicrobial T-cell subset in humans. Here, we investigate the development of these cells in second trimester human fetal tissues. MAIT cells are rare and immature in the fetal thymus, spleen and mesenteric lymph nodes. In contrast, mature IL-18Rα(+) CD8αα MAIT cells are enriched in the fetal small intestine, liver and lung. Independently of localization, MAIT cells express CD127 and Ki67 in vivo and readily proliferate in response to Escherichia coli in vitro. Maturation is accompanied by the gradual post-thymic acquisition of the PLZF transcription factor and the ability to produce IFNγ and IL-22 in response to bacteria in mucosa. Thus, MAIT cells acquire innate-like antimicrobial responsiveness in mucosa before exposure to environmental microbes and the commensal microflora. Establishment of this arm of immunity before birth may help protect the newborn from a range of pathogenic microbes.
    Nature Communications 01/2014; 5:3143. · 10.74 Impact Factor
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    ABSTRACT: The ability to reconstitute a normal immune system with antiretroviral therapy in the setting of HIV infection remains uncertain. This study aimed to characterize quantitative and qualitative aspects of various T cell subpopulations that do not improve despite effective ART. CD4∶CD8 ratio was evaluated in HIV-infected subjects with viral loads >10,000 copies/µl ("non-controllers", n = 42), those with undetectable viral loads on ART ("ART-suppressed", n = 53), and HIV-uninfected subjects (n = 22). In addition, T cell phenotype and function were examined in 25 non-controllers, 18 ART-suppressed, and 7 HIV-uninfected subjects. CD4∶CD8 ratio in non-controllers, ART-suppressed, and HIV-uninfected subjects was 0.25, 0.48, and 1.95 respectively (P<0.0001 for all comparisons). The increased ratio in ART-suppressed compared to non-controllers was driven by an increase of CD4+ T cells, with no change in the expanded CD8+ T cell population. Expansion of differentiated (CD28-CD27-CD45RA+/-CCR7-) T cell subpopulations persisted despite ART and minimal changes were noted in naïve T cell frequencies over time. Increased number of CD8+CD28- T cells and increased CD8+ CMV-specific T cell responses were associated with a decreased CD4∶CD8 ratio. Measures of T cell function demonstrated persistence of high frequencies of CD8+ T cells producing IFN-γ. Lastly, though all CD8+ subpopulations demonstrated significantly lower Ki67 expression in ART-suppressed subjects, CD4+ T cell subpopulations did not consistently show this decrease, thus demonstrating different proliferative responses in the setting of T cell depletion. In summary, this study demonstrated that CD4∶CD8 ratios remained significantly decreased and naïve T cell numbers were slow to increase despite long-term viral suppression on ART. In addition, there is a evidence of differential regulation of the CD4+ and CD8+ T cell subpopulations, suggesting independent homeostatic regulation of the two compartments.
    PLoS ONE 01/2014; 9(1):e85613. · 3.53 Impact Factor
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    ABSTRACT: A subset of CD3negCD56negCD16+ Natural Killer (NK) cells is highly expanded during chronic HIV-1 infection. The role of this subset in HIV-1 pathogenesis remains unclear. The lack of NK cell lineage-specific markers has complicated the study of minor NK cell subpopulations. Using CD7 as an additional NK cell marker, we found that CD3negCD56negCD16+ cells are a heterogeneous population comprised of CD7+ NK cells and CD7neg non-classical myeloid cells. CD7+CD56negCD16+ NK cells are significantly expanded in HIV-1 infection. CD7+CD56negCD16+ NK cells are mature and express KIRs, the C-type lectin-like receptors NKG2A and NKG2C, and natural cytotoxicity receptors similar to CD7+CD56+CD16+ NK cells. CD7+CD56neg NK cells in healthy donors produced minimal IFNgamma following K562 target cell or IL-12 plus IL-18 stimulation; however, they degranulated in response to K562 stimulation similar to CD7+CD56+ NK cells. HIV-1 infection resulted in reduced IFNgamma secretion following K562 or cytokine stimulation by both NK cell subsets compared to healthy donors. Decreased granzyme B and perforin expression and increased expression of CD107a in the absence of stimulation, particularly in HIV-1-infected subjects, suggest that CD7+CD56negCD16+ NK cells may have recently engaged target cells. Furthermore, CD7+CD56negCD16+ NK cells have significantly increased expression of CD95, a marker of NK cell activation. Taken together, CD7+CD56negCD16+ NK cells are activated, mature NK cells that may have recently engaged target cells.
    Retrovirology 12/2013; 10(1):158. · 4.77 Impact Factor
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    ABSTRACT: Several host-encoded antiviral factors suppress HIV-1 replication in a cell-autonomous fashion in vitro. The relevance of these defenses to the control of HIV-1 in vivo remains to be elucidated. We hypothesized that cellular restriction of HIV-1 replication plays a significant role in the observed suppression of HIV-1 in "elite controllers", individuals who maintain undetectable levels of viremia in the absence of antiretroviral therapy (ART). We comprehensively compared the expression levels of 34 host restriction factors and cellular activation levels in CD4+ T cells and sorted T cell subsets between elite controllers, HIV-1-infected (untreated) non-controllers, ART-suppressed, and uninfected individuals. Expression of schlafen 11, a codon usage-based inhibitor of HIV-1 protein synthesis, was significantly elevated in CD4+ T cells from elite controllers as compared to both non-controllers (p=0.048) and ART-suppressed individuals (p=0.024), with this effect most apparent in central memory CD4+ T cells. Schlafen 11 expression levels were comparable between controllers and uninfected individuals. Cumulative restriction factor expression was positively correlated with CD4+ T cell activation (r2=0.597, p<0.0001), viral load (r2=0.34, p=0.015), and expression of ISG15 (r2=0.73, p<0.0001), a marker of interferon exposure. APOBEC3C, APOBEC3D, CTR9, TRIM26, and TRIM32 were elevated in controllers with respect to ART-suppressed individuals, while levels were comparable to uninfected individuals and non-controllers. Host restriction factor expression typically scales with cellular activation levels. However, the elevated mRNA and protein expression of schlafen 11, despite low activation and viral load, violates the global pattern and may be a signature characteristic of HIV-1 elite control.
    Retrovirology 10/2013; 10(1):106. · 4.77 Impact Factor
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    ABSTRACT: Type 1 long-interspersed nuclear elements (L1s) are autonomous retrotransposable elements that retain the potential for activity in the human genome, but are suppressed by host-factors. Retrotransposition of L1s into chromosomal DNA can lead to genomic instability, while reverse transcription of L1 in the cytosol has the potential to activate innate immune sensors. We hypothesized that HIV-1 infection would compromise cellular control of L1 elements, resulting in the induction of retrotransposition events. Here, we show that HIV-1 infection enhances L1 retrotransposition in Jurkat cells in a Vif- and Vpr-dependent manner. In primary CD4(+) cells, HIV-1 infection results in the accumulation of L1 DNA, at least the majority of which is extra-chromosomal. These data expose an unrecognized interaction between HIV-1 and endogenous retrotransposable elements, which may have implications for the innate immune response to HIV-1 infection, as well as for HIV-1-induced genomic instability and cytopathicity.
    Journal of Virology 10/2013; · 4.65 Impact Factor
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    ABSTRACT: Expression of cell-intrinsic antiviral factors suppresses HIV-1 replication. We hypothesized that cellular activation modulates host restriction and susceptibility to HIV-1 infection. We measured the gene expression of 34 antiviral factors in healthy PBMC. Cellular activation induced expression of ISG15, TRIM5α, BST-2/tetherin and certain APOBEC3-family members. Expression of RTF1, PAF1, TRIM11, TRIM26 and BST-2/tetherin correlated with decreased HIV-1 infectivity. This study demonstrates synchronous effects of activation-induced antiviral genes on HIV-1 infectivity, providing candidates for pharmacological manipulation.
    Journal of Virology 08/2013; · 4.65 Impact Factor
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    ABSTRACT: The human fetal immune system is naturally exposed to maternal allogeneic cells, maternal antibodies, and pathogens. As such, it is faced with a considerable challenge with respect to the balance between immune reactivity and tolerance. Here, we show that fetal natural killer (NK) cells differentiate early in utero and are highly responsive to cytokines and antibody-mediated stimulation but respond poorly to HLA class I-negative target cells. Strikingly, expression of killer-cell immunoglobulin-like receptors (KIRs) did not educate fetal NK cells but rendered them hyporesponsive to target cells lacking HLA class I. In addition, fetal NK cells were highly susceptible to TGF-β-mediated suppression, and blocking of TGF-β signaling enhanced fetal NK cell responses to target cells. Our data demonstrate that KIR-mediated hyporesponsiveness and TGF-β-mediated suppression are major factors determining human fetal NK cell hyporesponsiveness to HLA class I-negative target cells and provide a potential mechanism for fetal-maternal tolerance in utero. Finally, our results provide a basis for understanding the role of fetal NK cells in pregnancy complications in which NK cells could be involved, for example, during in utero infections and anti-RhD-induced fetal anemia.
    The Journal of clinical investigation 08/2013; · 15.39 Impact Factor
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    ABSTRACT: The genetic background of HIV-1-infected subjects, particularly the HLA class I haplotype, appears to be critical in determining disease progression rates, thought to be a result of the role of HIV-1-specific CD8(+) T cell responses. The HLA-B*57 allele is strongly associated with viremic suppression and slower disease progression. However, there is considerable heterogeneity in HIV-1 disease progression rates among HLA-B*57-positive subjects, suggesting that additional factors may help to contain viral replication. In this report, we investigated the association between host restriction factors, other established immunological parameters, and HLA type in HIV-1-seronegative individuals. Our results demonstrate that healthy, uninfected HLA-B*57-positive individuals exhibit significantly higher gene-expression levels of host restriction factors, such as APOBEC3A, APOBEC3B, BST-2/tetherin, and ISG15. Interestingly, HLA-B*57 individuals have significantly lower CD4(+) T cell frequencies but harbor slightly more activated CD4(+) T cells compared with their HLA-B*35 counterparts. We detected significant correlations between CD4(+) T cell activation and expression of several APOBEC3 family members, BST-2/tetherin, SAMHD1, and TRIM5α in HLA-B*57-positive individuals. To our knowledge, this is the first report showing distinct associations between host restriction factors and HLA class I genotype. Our results provide insights into natural protection mechanisms and immunity against HIV-1 that fall outside of classical HLA-mediated effects.
    Journal of leukocyte biology 08/2013; · 4.99 Impact Factor

Publication Stats

11k Citations
1,367.36 Total Impact Points


  • 2014
    • George Washington University
      Washington, Washington, D.C., United States
  • 2001–2014
    • University of California, San Francisco
      • • Division of Experimental Medicine
      • • Department of Epidemiology and Biostatistics
      • • Gladstone Institute
      San Francisco, California, United States
  • 2013
    • Pierre and Marie Curie University - Paris 6
      Lutetia Parisorum, Île-de-France, France
  • 2008–2013
    • University of Toronto
      • Department of Immunology
      Toronto, Ontario, Canada
    • Swedish Institute for Communicable Disease Control
      Tukholma, Stockholm, Sweden
  • 2012
    • University of Hawaiʻi at Mānoa
      • Department of Tropical Medicine, Medical Microbiology and Pharmacology
      Honolulu, HI, United States
    • University of Hawaiʻi at Hilo
      Hilo, Hawaii, United States
    • San Francisco VA Medical Center
      San Francisco, California, United States
    • National Institute of Allergy and Infectious Diseases
      Maryland, United States
  • 2001–2012
    • Karolinska Institutet
      • • Department of Microbiology, Tumor and Cell Biology (MTC)
      • • Institutionen för medicin, Huddinge
      Stockholm, Stockholm, Sweden
  • 2011
    • University of Chicago
      Chicago, Illinois, United States
  • 2010
    • University of São Paulo
      San Paulo, São Paulo, Brazil
    • Ragon Institute of MGH, MIT and Harvard
      Charlestown, Maryland, United States
  • 2009
    • Monogram Biosciences
      San Francisco, California, United States
  • 2007
    • University of Oxford
      • Nuffield Department of Clinical Medicine
      Oxford, ENG, United Kingdom
  • 2006
    • J. David Gladstone Institutes
      San Francisco, California, United States
  • 2000–2006
    • The Rockefeller University
      • Laboratory of Cellular Physiology and Immunology
      New York City, New York, United States
    • Friedrich Miescher Institute for Biomedical Research
      Bâle, Basel-City, Switzerland
  • 2005
    • University of Oslo
      Kristiania (historical), Oslo County, Norway
  • 1996–1997
    • United Biomedical, Inc.
      Hauppauge, New York, United States
  • 1989–1990
    • Oxford University Hospitals NHS Trust
      • Nuffield Department of Medicine
      Oxford, England, United Kingdom
    • National Institute for Biological Standards and Control
      Potters Bar, England, United Kingdom