Arturo Casadevall

Albert Einstein College of Medicine, New York City, New York, United States

Are you Arturo Casadevall?

Claim your profile

Publications (634)3321.15 Total impact

  • Jacqueline M Achkar, John Chan, Arturo Casadevall
    [Show abstract] [Hide abstract]
    ABSTRACT: Accumulating evidence has documented a role for B cells and antibodies (Abs) in the immunity against Mycobacterium tuberculosis (Mtb). Passive transfer studies with monoclonal antibodies (mAbs) against mycobacterial antigens have shown protection against the tubercle bacillus. B cells and Abs are believed to contribute to an enhanced immune response against Mtb by modulating various immunological components in the infected host including the T-cell compartment. Nevertheless, the extent and contribution of B cells and Abs to protection against Mtb remains uncertain. In this article we summarize the most relevant findings supporting the role of B cells and Abs in the defense against Mtb and discuss the potential mechanisms of protection.
    Cold Spring Harbor perspectives in medicine. 10/2014;
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The release of extracellular vesicles (EV) by fungal organisms is considered an alternative transport mechanism to trans-cell wall passage of macromolecules. Previous studies have revealed the presence of EV in culture supernatants from fungal pathogens, such as Cryptococcus neoformans, Histoplasma capsulatum, Paracoccidioides brasiliensis, Sporothrix schenckii, Malassezia sympodialis and Candida albicans. Here we investigated the size, composition, kinetics of internalization by bone-marrow derived murine macrophages (MO) and dendritic cells (DC), and the immunomodulatory activity of C. albicans EV. We also evaluated the impact of EVs on fungal virulence using the Galleria mellonella larvae model. By transmission electron microscopy and dynamic light scattering we identified two populations ranging from 50-100 and 350-850 nm. Two predominant seroreactive proteins (27 and 37 kDa) and a group of polydispersed mannoproteins were observed in EV by immunoblotting analysis. Proteomic analysis of C. albicans EV revealed proteins related to pathogenesis, cell organization, carbohydrate and lipid metabolism, response to stress and several other functions. The major lipids detected by thin layer chromatography were ergosterol, lanosterol and glucosylceramide. Short exposure of MO to EV resulted in internalization of these vesicles and production of nitric oxide, IL-12, TGF-β and IL-10. Similarly, EV-treated DC produced IL- 12p40, IL-10 and TNF-α. In addition, EV treatment induced the upregulation of CD86 and MHC-II. Inoculation of G. mellonella larvae with EV followed by challenge with C. albicans reduced the number of recovered viable yeasts in comparison to infected larvae control. Taking together, our results demonstrate that C. albicans EV were immunologically active and could potentially interfere with the host responses in the setting of invasive candidiasis.
    Cellular Microbiology 10/2014; · 4.81 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Despite the essential functions of melanin pigments in diverse organisms and their roles in inspiring designed nanomaterials for electron transport and drug delivery, the structural frameworks of the natural materials and their biomimetic analogs remain poorly understood. To overcome the investigative challenges posed by these insoluble heterogeneous pigments, we have used l-tyrosine or dopamine enriched with stable (13)C and (15)N isotopes to label eumelanins metabolically in cell-free and Cryptococcus neoformans cell systems and to define their molecular structures and supramolecular architectures. Using high-field two-dimensional solid-state nuclear magnetic resonance (NMR), our study directly evaluates the assumption of structural commonality between synthetic melanin models and the corresponding natural pigments, demonstrating a common indole-based aromatic core in the products from contrasting synthetic protocols for the first time.
    Organic & Biomolecular Chemistry 07/2014; · 3.57 Impact Factor
  • Arturo Casadevall, R Grant Steen, Ferric C Fang
    [Show abstract] [Hide abstract]
    ABSTRACT: Retraction of flawed articles is an important mechanism for correction of the scientific literature. We recently reported that the majority of retractions are associated with scientific misconduct. In the current study, we focused on the subset of retractions for which no misconduct was identified, in order to identify the major causes of error. Analysis of the retraction notices for 423 articles indexed in PubMed revealed that the most common causes of error-related retraction are laboratory errors, analytical errors, and irreproducible results. The most common laboratory errors are contamination and problems relating to molecular biology procedures (e.g., sequencing, cloning). Retractions due to contamination were more common in the past, whereas analytical errors are now increasing in frequency. A number of publications that have not been retracted despite being shown to contain significant errors suggest that barriers to retraction may impede correction of the literature. In particular, few cases of retraction due to cell line contamination were found despite recognition that this problem has affected numerous publications. An understanding of the errors leading to retraction can guide practices to improve laboratory research and the integrity of the scientific literature. Perhaps most important, our analysis has identified major problems in the mechanisms used to rectify the scientific literature and suggests a need for action by the scientific community to adopt protocols that ensure the integrity of the publication process.-Casadevall, A., Steen, R. G., Fang, F. C. Sources of error in the retracted scientific literature.
    FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 06/2014;
  • [Show abstract] [Hide abstract]
    ABSTRACT: Cryptococcus neoformans produces extracellular vesicles containing a variety of cargo, including virulence factors. To become extracellular, these vesicles must not only be released from the plasma membrane, but also pass through the dense matrix of the cell wall. The greatest unknown in the area of fungal vesicles is the mechanism by which these vesicles are released to the extracellular space given the presence of the fungal cell wall. Here we used electron microscopy techniques to image the interactions of vesicles with the cell wall. Our goal was to define the ultrastructural morphology of the process to gain insights into the mechanisms involved. We describe single and multiple vesicle leaving events, which we hypothesized were due to plasma membrane and multivesicular body vesicle origins, respectively. We further utilized melanized cells to "trap" vesicles and visualize those passing through the cell wall. Vesicle size differed depending on whether vesicles left the cytoplasm in single versus multiple release events. Furthermore, we analyzed different vesicle populations for vesicle dimensions and protein composition. Proteomic analysis tripled the number of proteins known to be associated with vesicles. Despite separation of vesicles into batches differing in size, we did not identify major differences in protein composition. In summary, our results indicate that vesicles are generated by more than one mechanism, that vesicles exit the cell by traversing the cell wall, and that vesicle populations exist as a continuum with regards to size and protein composition.
    Eukaryotic Cell 06/2014; · 3.59 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Polysaccharide capsules are important virulence factors for many microbial pathogens including the opportunistic fungus Cryptococcus neoformans. In the present study, we demonstrate an unusual role for a secreted lactonohydrolase of C. neoformans, LHC1 in capsular higher order structure. Analysis of extracted capsular polysaccharide from wild-type and lhc1Δ strains by dynamic and static light scattering suggested a role for the LHC1 locus in altering the capsular polysaccharide, both reducing dimensions and altering its branching, density and solvation. These changes in the capsular structure resulted in LHC1-dependent alterations of antibody binding patterns, reductions in human and mouse complement binding and phagocytosis by the macrophage-like cell line J774, as well as increased virulence in mice. These findings identify a unique molecular mechanism for tertiary structural changes in a microbial capsule, facilitating immune evasion and virulence of a fungal pathogen.
    PLoS Pathogens 05/2014; 10(5):e1004037. · 8.14 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: /AbstractPreviously, extracellular vesicle production in Gram-positive bacteria was dismissed due to the absence of an outer membrane, where Gram-negative vesicles originate, and the difficulty in envisioning how such a process could occur through the cell wall. However, recent work has shown that Gram-positive bacteria produce extracellular vesicles and that the vesicles are biologically active. In this study, we show that Bacillus subtilis produces extracellular vesicles similar in size and morphology to other bacteria, characterized vesicles using a variety of techniques, provide evidence that these vesicles are actively produced by cells, show differences in vesicle production between strains, and identified a mechanism for such differences based on vesicle disruption. We found that in wild strains of B. subtilis, surfactin disrupted vesicles while in laboratory strains harboring a mutation in the gene sfp, vesicles accumulated in the culture supernatant. Surfactin not only lysed B. subtilis vesicles, but also vesicles from Bacillus anthracis, indicating a mechanism that crossed species boundaries. To our knowledge, this is the first time a gene and a mechanism has been identified in the active disruption of extracellular vesicles and subsequent release of vesicular cargo in Gram-positive bacteria. We also identify a new mechanism of action for surfactin.
    Molecular Microbiology 05/2014; · 5.03 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Extracellular vesicles are produced by many pathogenic microorganisms and have varied functions that include secretion and release of microbial factors, which contribute to virulence. Very little is known about vesicle production by Gram-positive bacteria, as well as their biogenesis and release mechanisms. In this work, we demonstrate the active production of vesicles by Streptococcus pneumoniae from the plasma membrane, rather than being a product from cell lysis. We biochemically characterized them by proteomics and fatty acid analysis, showing that these vesicles and the plasma membrane resemble in essential aspects, but have some differences: vesicles are more enriched in lipoproteins and short-chain fatty acids. We also demonstrate that these vesicles act as carriers of surface proteins and virulence factors. They are also highly immunoreactive against human sera and induce immune responses that protect against infection. Overall, this work provides insights into the biology of this important Gram-positive human pathogen and the role of extracellular vesicles in clinical applications. Pneumococcus is one of the leading causes of bacterial pneumonia worldwide in children and the elderly, being responsible for high morbidity and mortality rates in developing countries. The augment of pneumococcal disease in developed countries has raised major public health concern, since the difficulties to treat these infections due to increasing antibiotic resistance. Vaccination is still the best way to combat pneumococcal infections. One of the mechanisms that bacterial pathogens use to combat the defense responses of invaded hosts is the production and release of extracellular vesicles derived from the outer surface. Little is known about this phenomenon in Gram-positives. We show that pneumococcus produces membrane-derived vesicles particularly enriched in lipoproteins. We also show the utility of pneumococcal vesicles as a new type of vaccine, as they induce protection in immunized mice against infection with a virulent strain. This work will contribute to understand the role of these structures in important biological processes such as host-pathogen interactions and prevention of human disease.
    Journal of proteomics 04/2014; · 5.07 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: After dispersal of anthrax spores through the U.S. mail in 2001, there was heightened awareness of the potential of biological knowledge to be used for nefarious purposes.…
    Journal of Virology 04/2014; · 5.08 Impact Factor
  • Sabriya Stukes, Hillel W Cohen, Arturo Casadevall
    [Show abstract] [Hide abstract]
    ABSTRACT: Cryptococcus neoformans is a facultative intracellular pathogen and the causative agent of cryptococcosis, a disease that is often fatal to those with compromised immune systems. C. neoformans has the capacity to escape phagocytic cells through a process known as non-lytic exocytosis whereby the cryptococcal cell is released from the macrophage into the extracellular environment leaving both the host and pathogen alive. Little is known about the mechanism behind non-lytic exocytosis but there is evidence that both the fungal and host cells contribute to the process. In this study we used time-lapsed movies of C. neoformans-infected macrophages to delineate the kinetics and quantitative aspects of non-lytic exocytosis. We analyzed approximately 800 macrophages containing intracellular C. neoformans and identified 163 non-lytic exocytosis events that were further characterized into three subcategories: Type I (complete emptying of macrophage), Type II (partial emptying of macrophage), and Type III (cell-to-cell transfer). The majority of Type I and II events occurred after several hours of intracellular residence while Type III events occurred significantly earlier in the course of macrophage infection (p < 0.001). Our results show that non-lytic exocytosis is a morphologically and temporally diverse process that occurs relatively rapidly in the course of macrophage infection.
    Infection and immunity 03/2014; · 4.21 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: We previously demonstrated that the purified microbial polysaccharide Galactoxylomannan (GalXM) from the opportunistic fungus Cryptococcus neoformans is able to impair T-cell proliferation and to induce T lymphocyte apoptosis following the interaction with CD45 in normal subjects. Since T lymphocytes are crucially involved in the pathogenesis of rheumatoid arthritis (RA), aim of the present study was to investigate the effects of GalXM on circulatingT-cell subsets in RA and provide the rationale for potential therapeutic application of this compound. Sixty RA patients and 40 healthy donors (HD) were included in the study. RA and HD magnetic sorted-CD3(+), CD4(+) or CD4(+)CD25(high) T cells were cultured in presence or absence of GalXM (10 ng/ml), Dex (10nM), MTX (10ng/ml) or FLLL31 (5µM). Lymphocyte apoptosis was performed at different time-points evaluating propidium iodide staining and in selected experiments cleaved caspase 3 staining by flow cytometry. Flow cytometry was also employed for phenotypic analysis of T cell subsets (CD4, CD25, CD127, FoxP3, IL-17, IL-10, IL-17, TGF-β1) and for the analysis of cell proliferation evaluating CFSE dilution. Western blot was employed to assess phospho-STAT3, STAT3, FoxP3 and T-bet expression in cell lysates. Cytokine concentration in culture supernatants (IL-21, IL-22, IL-23, IL-6, IL-17A, IFN-γ, IL-12p70, IL-8, TGF-β1 and IL-10) was assessed with commercial ELISA kits. GalXM selectively reduced proliferation and increased apoptosis rate in RA Th1 and Th17 cells. GalXM was also able to reduce STAT3 phosphorilation eventually leading to decreased IL-17 production in surviving Th17 cells. To note, GalXM strongly up-regulated FoxP3 expression in CD4(+)T cells, increased the percentage of non-conventional CD4(+)CD25(-)FOXP3(+) Treg cells and enhanced suppressive activity of both CD4(+)CD25(high)FOXP3(+)and CD4(+)CD25(-)FOXP3(+)Treg cells. All these findings were further supported by a rebalance of effector/regulatory cytokines in culture supernatants. Our results suggest that GalXM represents a powerful compound able to rebalance Treg/T-effector ratio in RA and therefore it is worth to be employed for therapeutic purposes in this disease.
    Annals of the rheumatic diseases 03/2014; 73 Suppl 1:A71. · 8.11 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Aims: Glucuronoxylomannan (GXM) is the major polysaccharide component of Cryptococcus neoformans. We evaluated in this study whether GXM fractions of different molecular masses were functionally distinct. Materials & methods: GXM samples isolated from C. neoformans cultures were fractionated to generate polysaccharide preparations differing in molecular mass. These fractions were used in experiments focused on the association of GXM with cell wall components of C. neoformans, as well as on the interaction of the polysaccharide with host cells. Results & conclusion: GXM fractions of variable molecular masses bound to the surface of a C. neoformans acapsular mutant in a punctate pattern that is in contrast to the usual annular pattern of surface coating observed when GXM samples containing the full molecular mass range were used. The polysaccharide samples were also significantly different in their ability to stimulate cytokine production by host cells. Our findings indicate that GXM fractions are functionally distinct depending on their mass.
    Future Microbiology 02/2014; 9:147-61. · 4.02 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: The lethal toxin (LeTx) of B. anthracis plays a central role in the pathogenesis of anthrax-associated shock. Platelet activating factor (PAF) is a potent lipid mediator that has been implicated in endotoxin-associated shock. In this study, we examined the contribution of PAF to the manifestations of lethal toxin challenge in WT mice. LeTx challenge resulted in transient increase in serum PAF levels and a concurrent decrease in PAF acetylhydrolase activity. Inhibition of PAF activity using PAF antagonists or toxin challenge of PAF receptor negative mice reversed or ameliorated many of the pathologic features of LeTx-induced damage, including changes in vascular permeability, hepatic necrosis and cellular apoptosis. In contrast, PAF inhibition had minimal effects on cytokine levels. Findings from these studies support the continued study of PAF-antagonists as potential adjunctive agents in the treatment of anthrax-associated shock.
    Journal of Biological Chemistry 01/2014; · 4.65 Impact Factor
  • Arturo Casadevall, Ferric C Fang
    [Show abstract] [Hide abstract]
    ABSTRACT: As the body of scientific knowledge in a discipline increases, there is pressure for specialization. Fields spawn subfields that then become entities in themselves that promote further specialization. The process by which scientists join specialized groups has remarkable similarities to the guild system of the middle ages. The advantages of specialization of science include efficiency, the establishment of normative standards and the potential for greater rigor in experimental research. However, specialization also carries risks of monopoly, monotony and isolation. The current tendency to judge scientific work by the impact factor of the journal in which it is published may have roots in over-specialization, as scientists are less able to critically evaluate work outside their field than before. Scientists in particular define themselves through group identity and adopt practices that conform to the expectations and dynamics of such of groups. As part of our continuing analysis of issues confronting contemporary science we analyze the emergence and consequences of specialization in science with a particular emphasis on microbiology, a field highly vulnerable to balkanization along microbial phylogenetic boundaries, and suggest that specialization carries significant costs. We propose measures to mitigate the detrimental effects of scientific specialism.
    Infection and immunity 01/2014; · 4.21 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Mycobacterium tuberculosis releases membrane vesicles packed with molecules that can modulate the immune response. Because environmental conditions often influence the production and content of bacterial vesicles, this study examined M. tuberculosis microvesicles released under iron limitation, a common condition faced by pathogens inside the host. The findings indicate that M. tuberculosis increases microvesicle production in response to iron restriction and these microvesicles contain mycobactin which can serve as an iron donor and supports replication of iron-starved mycobacteria. Consequently, the results revealed a role of microvesicles in iron acquisition in M. tuberculosis, which can be critical for survival in the host.
    Journal of bacteriology 01/2014; · 3.94 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: The effector activity of antibodies is dependent on engagement with Fcγ receptors (FcγRs) and activation of the associated intracellular signaling pathways. Preclinical evaluation of therapeutic humanized or chimeric mAbs to study the interactions of their Fc regions with FcγRs is hampered by substantial structural and functional FcγR diversity among species. In this report, we used mice expressing only human FcγRs to evaluate the contribution of FcγR-mediated pathways to the neutralizing activity of an anti-anthrax toxin chimeric mAb. We observed that the protective activity of this mAb was highly dependent upon FcγR engagement, with minimal protection against anthrax toxin observed in FcγR-deficient mice following mAb administration. We generated anti-anthrax toxin mAbs with specific Fc domain variants with selectively enhanced affinity for particular human FcγRs and assessed their activity in FcγR-humanized mice. We determined that Fc domain variants that were capable of selectively engaging activating FcγRs substantially enhanced the in vitro and in vivo activity of anthrax toxin-neutralizing antibodies. These findings indicate that the application of Fc domain engineering is a feasible strategy to enhance toxin-neutralizing activity and suggest that engineered antitoxin antibodies will have improved therapeutic efficacy.
    The Journal of clinical investigation 01/2014; · 15.39 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Cryptococcus neoformans is a fungal pathogen that causes almost half a million deaths each year. It is believed that most humans are infected with C. neoformans, possibly in a form that survives through latency in the lung and can reactivate to cause disease if the host becomes immunosuppressed. C. neoformans has a remarkably sophisticated intracellular survival capacities yet it is a free-living fungus with no requirement for mammalian virulence whatsoever. In this review, we discuss the tools that C. neoformans possesses to achieve survival, latency and virulence within its host. Some of these tools are mechanisms to withstand starvation and others aim to protect against microbicidal molecules produced by the immune system. Furthermore, we discuss how these tools were acquired through evolutionary pressures and perhaps accidental stochastic events, all of which combined to produce an organism with an unusual and unique intracellular pathogenic strategy.
    Advances in applied microbiology 01/2014; 87:1-41. · 4.97 Impact Factor
  • Source
    Arturo Casadevall, Michael J Imperiale
    mBio 01/2014; 5(4). · 6.88 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The number of retracted scientific articles has been increasing. Most retractions are associated with research misconduct, entailing financial costs to funding sources and damage to the careers of those committing misconduct. We sought to calculate the magnitude of these effects. Data relating to retracted manuscripts and authors found by the Office of Research Integrity (ORI) to have committed misconduct were reviewed from public databases. Attributable costs of retracted manuscripts, and publication output and funding of researchers found to have committed misconduct were determined. We found that papers retracted due to misconduct accounted for approximately $58 million in direct funding by the NIH between 1992 and 2012, less than 1% of the NIH budget over this period. Each of these articles accounted for a mean of $392,582 in direct costs (SD $423,256). Researchers experienced a median 91.8% decrease in publication output and large declines in funding after censure by the ORI.DOI: http://dx.doi.org/10.7554/eLife.02956.001.
    eLife. 01/2014; 3:e02956.
  • Source
    MethodsX. 01/2014;

Publication Stats

19k Citations
3,321.15 Total Impact Points

Institutions

  • 1990–2014
    • Albert Einstein College of Medicine
      • • Department of Pediatrics
      • • Department of Microbiology & Immunology
      • • Nuclear Medicine
      • • Department of Medicine
      • • Infectious Diseases
      • • Department of Cell Biology
      New York City, New York, United States
  • 2013
    • University of Wisconsin–Madison
      Madison, Wisconsin, United States
    • University of Brasília
      • Department of Cell Biology
      Brasília, Federal District, Brazil
    • University of North Carolina at Chapel Hill
      North Carolina, United States
  • 2008–2013
    • University of Washington Seattle
      • Department of Medicine
      Seattle, WA, United States
    • Montefiore Medical Center
      • Department of Pediatrics
      New York City, NY, United States
    • Instituto Evandro Chagas
      Ananindeua, Pará, Brazil
    • Institute for Transuranium Elements
      Carlsruhe, Baden-Württemberg, Germany
    • University of Pittsburgh
      Pittsburgh, Pennsylvania, United States
    • City University of New York - Bronx Community College
      New York City, New York, United States
    • Farmingdale State College
      East Farmingdale, New York, United States
  • 2007–2013
    • Federal University of Rio de Janeiro
      • • Instituto de Microbiologia Professor Paulo de Góes (IMPPG)
      • • Instituto de Biologia (IB)
      Rio de Janeiro, Rio de Janeiro, Brazil
    • Trinity University
      • Department of Mathematics
      San Antonio, TX, United States
    • Trinity University of Asia
      Alfonso XIII, Mimaropa, Philippines
  • 2006–2013
    • Yeshiva University
      • • Department of Microbiology & Immunology
      • • Division of Infectious Diseases
      • • Division of Nuclear Medicine
      New York City, New York, United States
  • 1998–2013
    • Università degli Studi di Perugia
      • Department of Clinical and Experimental Medicine
      Terni, Umbria, Italy
    • University of Nevada School of Medicine
      Reno, Nevada, United States
  • 2012
    • University of Coimbra
      • Faculty of Medicine
      Coímbra, Coimbra, Portugal
    • Istituto Superiore di Sanità
      Roma, Latium, Italy
    • AECOM
      Sandy City, Utah, United States
  • 2011–2012
    • CUNY Graduate Center
      New York City, New York, United States
    • City University of New York - Brooklyn College
      Brooklyn, New York, United States
    • City University of New York - Bernard M. Baruch College
      • Department of Natural Sciences
      New York City, NY, United States
    • Universidade Federal do Rio Grande do Sul
      Pôrto de São Francisco dos Casaes, Rio Grande do Sul, Brazil
    • Savannah River National Laboratory
      Aiken, South Carolina, United States
    • Medical University of South Carolina
      • Department of Biochemistry and Molecular Biology (College of Medicine)
      Charleston, SC, United States
  • 2010–2012
    • The Commonwealth Medical College
      • Department of Basic Sciences
      Scranton, PA, United States
  • 2008–2011
    • Instituto de Salud Carlos III
      • Center National of Microbiology (CNM)
      Madrid, Madrid, Spain
  • 2009
    • Centraalbureau voor Schimmelcultures
      Utrecht, Utrecht, Netherlands
  • 2006–2009
    • Department of Nuclear Medicine
      Nyitra, Nitriansky, Slovakia
  • 1993–2009
    • Stony Brook University
      • Department of Medicine
      Stony Brook, NY, United States
  • 2003–2008
    • City University of New York - College of Staten Island
      • Chemistry
      New York City, NY, United States
  • 1999–2008
    • Cornell University
      • • Department of Biological and Environmental Engineering
      • • Department of Pharmacology
      Ithaca, NY, United States
    • New York State
      New York City, New York, United States
    • Howard Hughes Medical Institute
      Ashburn, Virginia, United States
  • 2005
    • University of British Columbia - Vancouver
      • Biomedical Research Centre (BRC)
      Vancouver, British Columbia, Canada
    • Massachusetts General Hospital
      • Division of Infectious Diseases
      Boston, Massachusetts, United States
    • Stockholm University
      • Department of Organic Chemistry
      Stockholm, Stockholm, Sweden
  • 2004
    • All India Institute of Medical Sciences
      • Department of Microbiology
      New Delhi, NCT, India
  • 2000–2003
    • Duke University Medical Center
      • • Division of Infectious Diseases
      • • Department of Medicine
      Durham, NC, United States
  • 2002
    • University of Massachusetts Medical School
      Worcester, Massachusetts, United States
  • 2001
    • The University of Manchester
      Manchester, England, United Kingdom
    • Long Island University
      • Department of Biology
      New York City, NY, United States
  • 1995–1998
    • Georgia State University
      • Department of Chemistry
      Atlanta, Georgia, United States
  • 1997
    • University of Oklahoma Health Sciences Center
      • Department of Microbiology and Immunology
      Oklahoma City, OK, United States