Robert B Tesh

University of Texas Medical Branch at Galveston, Galveston, Texas, United States

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Publications (354)1489.9 Total impact

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    ABSTRACT: We conducted phylogeographic modeling to determine the introduction and spread of Guaroa virus in South America. The results suggest a recent introduction of this virus into regions of Peru and Bolivia over the past 60-70 years and emphasize the need for increased surveillance in surrounding areas.
    Emerging infectious diseases. 03/2015; 21(3):460-3.
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    ABSTRACT: RNA viruses exhibit substantial structural, ecological and genomic diversity. However, genome size in RNA viruses is likely limited by a high mutation rate, resulting in the evolution of various mechanisms to increase complexity while minimising genome expansion. Here we conduct a large-scale analysis of the genome sequences of 99 animal rhabdoviruses, including 45 genomes which we determined de novo, to identify patterns of genome expansion and the evolution of genome complexity. All but seven of the rhabdoviruses clustered into 17 well-supported monophyletic groups, of which eight corresponded to established genera, seven were assigned as new genera, and two were taxonomically ambiguous. We show that the acquisition and loss of new genes appears to have been a central theme of rhabdovirus evolution, and has been associated with the appearance of alternative, overlapping and consecutive ORFs within the major structural protein genes, and the insertion and loss of additional ORFs in each gene junction in a clade-specific manner. Changes in the lengths of gene junctions accounted for as much as 48.5% of the variation in genome size from the smallest to the largest genome, and the frequency with which new ORFs were observed increased in the 3' to 5' direction along the genome. We also identify several new families of accessory genes encoded in these regions, and show that non-canonical expression strategies involving TURBS-like termination-reinitiation, ribosomal frame-shifts and leaky ribosomal scanning appear to be common. We conclude that rhabdoviruses have an unusual capacity for genomic plasticity that may be linked to their discontinuous transcription strategy from the negative-sense single-stranded RNA genome, and propose a model that accounts for the regular occurrence of genome expansion and contraction throughout the evolution of the Rhabdoviridae.
    PLoS Pathogens 02/2015; 11(2):e1004664. · 8.06 Impact Factor
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    ABSTRACT: Previous studies have shown that an attenuated West Nile virus (WNV) nonstructural (NS) 4B-P38G mutant induces stronger innate and adaptive immune responses than wild-type WNV in mice, which has important applications to vaccine development. To investigate the mechanism of immunogenicity, we characterized WNV NS4B-P38G mutant infection in two human cell lines-THP-1 cells and THP-1 macrophages. Although the NS4B-P38G mutant produced more viral RNA than the parental WNV NY99 in both cell types, there was no detectable infectious virus in the supernatant of either cell type. Nonetheless, the attenuated mutant boosted higher innate cytokine responses than virulent parental WNV NY99 in these cells. The NS4B-P38G mutant infection of THP-1 cells led to more diverse and robust innate cytokine responses than that seen in THP-1 macrophages, which were mediated by toll-like receptor (TLR)7 and retinoic acid-inducible gene 1(RIG-I) signaling pathways. Overall, these results suggest that a defective viral life cycle during NS4B-P38G mutant infection in human monocytic and macrophage cells leads to more potent cell intrinsic innate cytokine responses. Copyright © 2014. Published by Elsevier Ltd.
    Vaccine 01/2015; · 3.49 Impact Factor
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    ABSTRACT: Background Most alphaviruses are arthropod-borne and utilize mosquitoes as vectors for transmission to susceptible vertebrate hosts. This ability to infect both mosquitoes and vertebrates is essential for maintenance of most alphaviruses in nature. A recently characterized alphavirus, Eilat virus (EILV), isolated from a pool of Anopheles coustani s.I. is unable to replicate in vertebrate cell lines. The EILV host range restriction occurs at both attachment/entry as well as genomic RNA replication levels. Here we investigated the mosquito vector range of EILV in species encompassing three genera that are responsible for maintenance of other alphaviruses in nature.Materials and methodsSusceptibility studies were performed in four mosquito species: Aedes albopictus, A. aegypti, Anopheles gambiae, and Culex quinquefasciatus via intrathoracic and oral routes utilizing EILV and EILV expressing red fluorescent protein (¿eRFP) clones. EILV-eRFP was injected at 107 PFU/mL to visualize replication in various mosquito organs at 7 days post-infection. Mosquitoes were also injected with EILV at 104-101 PFU/mosquito and virus replication was measured via plaque assays at day 7 post-infection. Lastly, mosquitoes were provided bloodmeals containing EILV-eRFP at doses of 109, 107, 105 PFU/mL, and infection and dissemination rates were determined at 14 days post-infection.ResultsAll four species were susceptible via the intrathoracic route; however, replication was 10¿100 fold less than typical for most alphaviruses, and infection was limited to midgut-associated muscle tissue and salivary glands. A. albopictus was refractory to oral infection, while A. gambiae and C. quinquefasciatus were susceptible only at 109 PFU/mL dose. In contrast, A. aegypti was susceptible at both 109 and 107 PFU/mL doses, with body infection rates of 78% and 63%, and dissemination rates of 26% and 8%, respectively.Conclusions The exclusion of vertebrates in its maintenance cycle may have facilitated the adaptation of EILV to a single mosquito host. As a consequence, EILV displays a narrow vector range in mosquito species responsible for the maintenance of other alphaviruses in nature.
    Parasites & Vectors 12/2014; 7(1):595. · 3.25 Impact Factor
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    ABSTRACT: Recently, there has been a dramatic increase in the detection and characterization of insect-specific viruses in field-collected mosquitoes. Evidence suggests that these viruses are ubiquitous in nature and that many are maintained by vertical transmission in mosquito populations. Some studies suggest that the presence of insect-specific viruses may inhibit replication of a super-infecting arbovirus, thus altering vector competence of the mosquito host. Accordingly, we screened our laboratory mosquito colonies for insect-specific viruses. Pools of colony mosquitoes were homogenized and inoculated into cultures of Aedes albopictus (C6/36) cells. The infected cells were examined by electron microscopy and deep sequencing was performed on RNA extracts. Electron micrograph images indicated the presence of three different viruses in three of our laboratory mosquito colonies. Potential implications of these findings for vector competence studies are discussed. © The American Society of Tropical Medicine and Hygiene.
    The American journal of tropical medicine and hygiene 12/2014; 92(2). · 2.74 Impact Factor
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    ABSTRACT: The Le Dantec serogroup of rhabdoviruses comprises Le Dantec virus from a human with encephalitis and Keuriliba virus from rodents, each isolated in Senegal. The Kern Canyon serogroup comprises a loosely connected set of rhabdoviruses many of which have been isolated from bats, including Kern Canyon virus from California, Nkolbisson virus from Cameroon, Central African Republic, and Cote d'Ivoire, Kolente virus from Guinea, Mount Elgon bat and Fikirini viruses from Kenya, and Oita virus from Japan. Fukuoka virus isolated from mosquitoes, midges, and cattle in Japan, Barur virus from a rodent in India and Nishimuro virus from pigs in Japan have also been linked genetically or serologically to this group. Here, we analyze the genome sequences and phylogenetic relationships of this set of viruses. We show that they form three sub-groups within a monophyletic group, which we propose should constitute the new genus Ledantevirus. © The American Society of Tropical Medicine and Hygiene.
    The American journal of tropical medicine and hygiene 12/2014; 92(2). · 2.74 Impact Factor
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    ABSTRACT: Most alphaviruses are mosquito-borne and exhibit a broad host range, infecting many different vertebrates including birds, rodents, equids, humans, and nonhuman primates. This ability of most alphaviruses to infect arthropods and vertebrates is essential for their maintenance in nature. Recently, a new alphavirus, Eilat virus (EILV), was described and in contrast to all other mosquito-borne viruses is unable to replicate in vertebrate cell lines. Investigations into the nature of its host range restriction showed the inability of genomic EILV RNA to replicate in vertebrate cells. Here, we investigated whether the EILV host range restriction is present at the entry level and further explored the viral factors responsible for the lack of genomic RNA replication. Utilizing Sindbis (SINV) and EILV chimeras, we show that the EILV vertebrate host range restriction is also manifested at the entry level. Furthermore, the EILV RNA replication restriction is independent of the 3' untranslated genome region (UTR). Complementation experiments with SINV suggested that RNA replication is restricted by the inability of the EILV non-structural proteins to form functional replicative complexes. These data demonstrate that the EILV host range restriction is multigenic, involving at least one gene from both non-structural (nsP) and structural protein (sP) open reading frames (ORFs). As EILV groups phylogenetically within the mosquito-borne virus clade of pathogenic alphaviruses, our findings have important evolutionary implications for arboviruses.
    Journal of Virology 11/2014; · 4.65 Impact Factor
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    ABSTRACT: Since 1998, cyclic mortality events in common eiders (Somateria mollissima), numbering in the hundreds to thousands of dead birds, have been documented along the coast of Cape Cod, Massachusetts, USA. Although longitudinal disease investigations have uncovered potential contributing factors responsible for these outbreaks, detecting a primary etiological agent has proven enigmatic. Here we identify a novel orthomyxovirus, tentatively named Wellfleet Bay virus (WFBV), as a potential causative agent of these outbreaks. Genomic analysis of WFBV revealed that it is most closely related to members of the Quaranjavirus genus within the family Orthomyxoviridae. Similar to other members of the genus, WFBV contains an alphabaculovirus gp64-like glycoprotein, which was demonstrated to have fusion activity, and also tentatively suggests that ticks (and/or insects) may vector the virus in nature. However, in addition to the six RNA segments encoding the prototypical structural proteins identified in other quaranjaviruses, a previously unknown RNA segment (segment 7) encoding a novel protein designated as VP7 was discovered in WFBV. Although WFBV shows low to moderate levels of sequence similarity to Quaranfil virus and Johnston Atoll virus, the original members of the Quaranjavirus genus, additional antigenic and genetic analyses demonstrated that it is closely related to the recently identified Cygnet River virus (CyRV) from South Australia, suggesting that WFBV and CyRV may be geographic variants of the same virus. Although the identification of WFBV in part may resolve the enigma of these mass mortality events, the details of the ecology and epidemiology of the virus remain to be determined.
    Journal of virology. 11/2014;
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    ABSTRACT: A total of 2,691 mosquitoes representing 17 species was collected from eight locations in southwest Cameroon and screened for pathogenic viruses. Ten isolates of a novel reovirus (genus Dinovernavirus) were detected by culturing mosquito pools on Aedes albopictus (C6/36) cell cultures. A virus that caused overt cytopathic effects was isolated, but it did not infect vertebrate cells or produce detectable disease in infant mice after intracerebral inoculation. The virus, tentatively designated Fako virus (FAKV), represents the first 9-segmented, dsRNA virus to be isolated in nature. FAKV appears to have a broad mosquito host range, and its detection in male specimens suggests mosquito-to-mosquito transmission in nature. The structure of the T=1 FAKV virion, determined to subnanometer resolution by cryoelectron microscopy (cryoEM), showed only four proteins per icosahedral asymmetric unit: a dimer of the major capsid protein, one turret protein, and one clamp protein. While all other turreted reoviruses of known structures have at least two copies of the clamp protein per asymmetric unit, FAKV's clamp protein bound at only one conformer of the major capsid protein. The FAKV capsid architecture and genome organization represent the most simplified reovirus described to date, and phylogenetic analysis suggests that it arose from a more complex ancestor by serial loss-of-function events.
    Journal of Virology 10/2014; · 4.65 Impact Factor
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    ABSTRACT: Until the recent emergence of two human pathogenic tick-borne phleboviruses (TBPVs) (Severe Fever with Thrombocytopenia Syndrome virus (SFTSV), and Heartland virus), TBPVs have been neglected as causative agents of human disease. In particular, no studies have addressed the global distribution of TBPVs and consequently, our understanding of the mechanism(s) underlying their evolution and emergence remains poor. In order to provide a useful tool for the ecological and epidemiological study of TBPVs, we have established a simple system that can detect all known TBPVs, based on conventional RT-PCR with degenerate primer sets targeting conserved regions of the viral L genome segment. Using this system, we have determined that several viruses that had been isolated from ticks decades ago but had not been taxonomically identified, are novel TBPVs. Full-genome sequencing of these viruses revealed a novel fourth TBPV cluster distinct from the three known TBPV clusters (i.e. the SFTS, Bhanja, and Uukuniemi groups) and from the mosquito/sandfly-borne phleboviruses. Furthermore, by using tick samples collected in Zambia, we confirmed that our system had enough sensitivity to detect a new TBPV in a single tick homogenate. This virus, tentatively designated as Shibuyunji virus after the region of tick collection, grouped into a novel fourth TBPV cluster. These results indicate that our system can be used as a first-line screening approach for TBPVs and that this kind of work will undoubtedly lead to the discovery of additional novel tick viruses and will expand our knowledge of the evolution and epidemiology of TBPVs.
    Journal of Virology 10/2014; · 4.65 Impact Factor
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    ABSTRACT: Koolpinyah virus (KOOLV) isolated from healthy Australian cattle and Yata virus (YATV) isolated from a pool of Mansonia uniformis mosquitoes in the Central African Republic have been tentatively identified as rhabdoviruses. KOOLV was shown previously to be related antigenically to kotonkon virus, an ephemerovirus that has caused an ephemeral fever-like illness in cattle in Nigeria, but YATV failed to react antigenically with any other virus tested. Here we report the complete genome sequences of KOOLV (16133 nt) and YATV (14479 nt). Each has a complex genome organisation, with multiple genes, including a second non-structural glycoprotein (GNS) gene and a viroporin (α1) gene, between the G and L genes as is characteristic of ephemeroviruses. Based on an analysis of genome organisation, sequence identity and cross-neutralisation, we demonstrate that both KOOLV and YATV should be classified as two new species in the genus Ephemerovirus.
    Veterinary Microbiology 10/2014; · 2.73 Impact Factor
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    ABSTRACT: Human infection with Bwamba virus (BWAV) and the closely related Pongola virus (PGAV), as well as Nyando virus (NDV), are important causes of febrile illness in Africa. However, despite seroprevalence studies that indicate high rates of infection in many countries, these viruses remain relatively unknown and unstudied. In addition, a number of unclassified bunyaviruses have been isolated over the years often with uncertain relationships to human disease.
    PLoS Neglected Tropical Diseases 09/2014; 8(9):e3147. · 4.49 Impact Factor
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    ABSTRACT: The Orbivirus genus of the family Reoviridae is comprised of 22 virus species including the Changuinola virus (CGLV) serogroup. The complete genome sequences of 13 CGLV serotypes isolated between 1961 and 1988 from distinct geographic areas of the Brazilian Amazon region were obtained. All viral sequences were obtained from single-passaged CGLV strains grown in Vero cells. CGLVs are the only orbiviruses known to be transmitted by phlebotomine sandflies. Ultrastructure and molecular analyses by electron microscopy and gel electrophoresis, respectively revealed viral particles with typical orbivirus size and morphology, as well as the presence of a segmented genome with 10 segments. Full-length nucleotide sequencing of each of the ten RNA segments of the 13 CGLV serotypes provided basic information regarding the genome organization, encoded proteins and genetic traits. Segment 2 (encoding VP2) of the CGLV is uncommonly larger in comparison to those found in other orbiviruses and shows varying sizes even among different CGLV serotypes. Phylogenetic analyses support previous serologic findings, which indicated that CGLV constitutes a separate serogroup within the genus Orbivirus. In addition, 6 out of 13 analyzed CGLV serotypes show reassortment of their genome segments.
    Journal of General Virology 07/2014; · 3.53 Impact Factor
  • Xue-Jie Yu, Robert B Tesh
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    ABSTRACT: This review examines the evidence indicating a role for parasitic mites in the transmission and maintenance of Hantaan virus in nature. The available data, much of it from recent studies in China, indicate that both trombiculid and gamasid mites are naturally infected with Hantaan virus and that infected mites can transmit the virus by bite to laboratory mice and transovarially (vertically) through eggs to their offspring. Collectively, these findings challenge the current paradigm of hantavirus transmission, namely that rodents serve as the reservoir of human pathogenic hantaviruses in nature and that humans are infected with these viruses by inhalation of aerosols of infectious rodent excreta. Further research is needed to confirm the mite-hantavirus association and to determine if parasitic mites are in fact the major source and principal vectors of human pathogenic hantaviruses, such as Hantaan. If the mite hypothesis is correct, then it will significantly alter current concepts about the epidemiology, prevention and control of human hantavirus infection.
    The Journal of Infectious Diseases 06/2014; · 5.78 Impact Factor
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    ABSTRACT: The genus Negevirus consists of insect-only viruses isolated from mosquitoes and sandflies. Here, we report the successful construction of a full-length infectious cDNA clone of Negev virus strain M30957. Viral RNA was transcribed in vitro and virus was readily rescued with or without the use of a cap analog. These results strongly suggest that Negev virus, and likely other members within the genus, is a non-segmented, single stranded, positive sense RNA virus.
    Journal of General Virology 05/2014; · 3.53 Impact Factor
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    ABSTRACT: BACKGROUND: The family Mesoniviridae (order Nidovirales) comprises of a group of positive-sense, single-stranded RNA ([+]ssRNA) viruses isolated from mosquitoes. FINDINGS: Thirteen novel insect-specific virus isolates were obtained from mosquitoes collected in Indonesia, Thailand and the USA. By electron microscopy, the virions appeared as spherical particles with a diameter of ~50 nm. Their 20,129 nt to 20,777 nt genomes consist of positive-sense, single-stranded RNA with a poly-A tail. Four isolates from Houston, Texas, and one isolate from Java, Indonesia, were identified as variants of the species Alphamesonivirus-1 which also includes Nam Dinh virus (NDiV) from Vietnam and Cavally virus (CavV) from Cote d'Ivoire. The eight other isolates were identified as variants of three new mesoniviruses, based on genome organization and pairwise evolutionary distances: Karang Sari virus (KSaV) from Java, Bontag Baru virus (BBaV) from Java and Kalimantan, and Kamphaeng Phet virus (KPhV) from Thailand. In comparison with NDiV, the three new mesoniviruses each contained a long insertion (180 - 588 nt) of unknown function in the 5' region of ORF1a, which accounted for much of the difference in genome size. The insertions contained various short imperfect repeats and may have arisen by recombination or sequence duplication. CONCLUSIONS: In summary, based on their genome organizations and phylogenetic relationships, thirteen new viruses were identified as members of the family Mesoniviridae, order Nidovirales. Species demarcation criteria employed previously for mesoniviruses would place five of these isolates in the same species as NDiV and CavV (Alphamesonivirus-1) and the other eight isolates would represent three new mesonivirus species (Alphamesonivirus-5, Alphamesonivirus-6 and Alphamesonivirus-7). The observed spatiotemporal distribution over widespread geographic regions and broad species host range in mosquitoes suggests that mesoniviruses may be common in mosquito populations worldwide.
    Virology Journal 05/2014; 11(1):97. · 2.09 Impact Factor
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    ABSTRACT: A novel mononegavirus was isolated in 1975 from ticks (Ornithodoros coriaceus) collected during investigation of an outbreak of epizootic bovine abortion (EBA) in northern California. It was originally designated "bovine abortion-tick virus" (BA-T virus). The EBA is now known to be associated with a deltaproteobacterium infection, and not a virus. The BA-T virus had remained uncharacterized until now. We have determined by electron microscopy, serology, and genome sequencing that the BA-T virus is a fourth member of the newly proposed family Nyamiviridae, and we have renamed it Sierra Nevada virus (SNVV). Although antigenically distinct, phylogenetically SNVV is basal to Nyamanini virus (NYMV) and Midway virus (MIDWV), two other tick-borne agents. Although NYMV was found to infect land birds, and MIDWV seabirds, it is presently unknown whether SNVV naturally infects birds or mammals.
    The American journal of tropical medicine and hygiene 04/2014; · 2.53 Impact Factor
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    ABSTRACT: A novel mononegavirus was isolated in 1975 from ticks (Ornithodoros coriaceus) collected during investigation of an outbreak of epizootic bovine abortion (EBA) in northern California. It was originally designated "bovine abortion-tick virus" (BA-T virus). The EBA is now known to be associated with a deltaproteobacterium infection, and not a virus. The BA-T virus had remained uncharacterized until now. We have determined by electron microscopy, serology, and genome sequencing that the BA-T virus is a fourth member of the newly proposed family Nyamiviridae, and we have renamed it Sierra Nevada virus (SNVV). Although antigenically distinct, phylogenetically SNVV is basal to Nyamanini virus (NYMV) and Midway virus (MIDWV), two other tick-borne agents. Although NYMV was found to infect land birds, and MIDWV seabirds, it is presently unknown whether SNVV naturally infects birds or mammals.
    The American journal of tropical medicine and hygiene 04/2014; · 2.74 Impact Factor
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    ABSTRACT: A serosurvey of antibodies against selected flaviviruses and alphaviruses in 384 bats (representing 10 genera and 14 species) was conducted in the Caribbean island of Trinidad. Sera were analysed using epitope-blocking enzyme-linked immunosorbent assays (ELISAs) specific for antibodies against West Nile virus (WNV), Venezuelan equine encephalitis virus (VEEV) and eastern equine encephalitis virus (EEEV), all of which are zoonotic viruses of public health significance in the region. Overall, the ELISAs resulted in the detection of VEEV-specific antibodies in 11 (2.9%) of 384 bats. Antibodies to WNV and EEEV were not detected in any sera. Of the 384 sera, 308 were also screened using hemagglutination inhibition assay (HIA) for antibodies to the aforementioned viruses as well as St. Louis encephalitis virus (SLEV; which also causes epidemic disease in humans), Rio Bravo virus (RBV), Tamana bat virus (TABV) and western equine encephalitis virus (WEEV). Using this approach, antibodies to TABV and RBV were detected in 47 (15.3%) and 3 (1.0%) bats, respectively. HIA results also suggest the presence of antibodies to an undetermined flavivirus(es) in 8 (2.6%) bats. Seropositivity for TABV was significantly (P < 0.05; χ(2) ) associated with bat species, location and feeding preference, and for VEEV with roost type and location. Differences in prevalence rates between urban and rural locations were statistically significant (P < 0.05; χ(2) ) for TABV only. None of the aforementioned factors was significantly associated with RBV seropositivity rates.
    Zoonoses and Public Health 04/2014; · 2.09 Impact Factor
  • Journal of Virology 03/2014; 88(5):3054. · 4.65 Impact Factor

Publication Stats

8k Citations
1,489.90 Total Impact Points

Institutions

  • 1996–2014
    • University of Texas Medical Branch at Galveston
      • Department of Pathology
      Galveston, Texas, United States
  • 2013
    • The Pirbright Institute
      • Vector-borne Viral Diseases (VVD) Programme
      Woking, ENG, United Kingdom
    • University of Pittsburgh
      • Department of Computational & Systems Biology
      Pittsburgh, Pennsylvania, United States
    • Johns Hopkins Bloomberg School of Public Health
      • Department of International Health
      Baltimore, MD, United States
  • 2011–2013
    • Columbia University
      • Center for Infection and Immunity
      New York City, New York, United States
    • University of Victoria
      • Department of Biochemistry and Microbiology
      Victoria, British Columbia, Canada
  • 2012
    • University of Florida
      • Department of Small Animal Clinical Sciences
      Gainesville, FL, United States
  • 2009–2012
    • Washington University in St. Louis
      • Department of Molecular Microbiology
      San Luis, Missouri, United States
    • Biotechnology and Biological Sciences Research Council
      Swindon, England, United Kingdom
    • Institute of Research for Development
      • 190 - Emerging Viral Diseases (EPV)
      Marseille, Provence-Alpes-Cote d'Azur, France
    • University of Washington Seattle
      • Department of Medicine
      Seattle, WA, United States
  • 2009–2011
    • University of South Florida
      • Department of Global Health
      Tampa, FL, United States
  • 1993–2011
    • Colorado State University
      • • Department of Microbiology, Immunology & Pathology
      • • College of Agricultural Sciences
      Fort Collins, Colorado, United States
    • Fundação Oswaldo Cruz
      • Departamento de Imunologia
      Rio de Janeiro, Rio de Janeiro, Brazil
  • 2010
    • University of Buea
      • Department of Plant and Animal Science
      Buea, South-West Region, Cameroon
    • University of Strasbourg
      Strasburg, Alsace, France
  • 2008
    • New York City Department of Health and Mental Hygiene
      New York, United States
  • 1995–2007
    • Connecticut Agricultural Experiment Station
      New Haven, Connecticut, United States
  • 2006
    • University of Houston
      Houston, Texas, United States
    • Centers for Disease Control and Prevention
      • Division of Vector-Borne Diseases
      Druid Hills, GA, United States
  • 2004–2006
    • Instituto Evandro Chagas
      Ananindeua, Pará, Brazil
    • Tulane University
      New Orleans, Louisiana, United States
    • University of Texas Health Science Center at Houston
      • Center for Infectious Diseases
      Houston, TX, United States
  • 2005
    • University of Queensland
      Brisbane, Queensland, Australia
    • U.S. Army Medical Research Institute of Infectious Diseases
      Maryland, United States
    • Autonomous University of Nuevo León
      San Nicolás de los Garza, Nuevo León, Mexico
  • 2003
    • University of Rhode Island
      Kingston, Rhode Island, United States
    • Wisconsin National Primate Research Center
      Madison, Wisconsin, United States
  • 1998
    • Instituto Nacional de Higiene "Rafael Rangel"
      Caracas, Distrito Federal, Venezuela
  • 1988–1997
    • Yale-New Haven Hospital
      New Haven, Connecticut, United States
  • 1989–1995
    • University of Alaska Fairbanks
      • Institute of Arctic Biology
      Fairbanks, AK, United States
    • Harvard Medical School
      Boston, Massachusetts, United States
    • Yale University
      • School of Medicine
      New Haven, CT, United States
  • 1994
    • Instituto Adolfo Lutz
      San Paulo, São Paulo, Brazil
  • 1992
    • University of Georgia
      • Southeastern Cooperative Wildlife Disease Study
      Athens, GA, United States
    • University of Maryland, College Park
      • Department of Entomology
      College Park, MD, United States
  • 1991
    • Youngstown State University
      Youngstown, Ohio, United States