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Article ; Online: Using the nonhuman primate model of HCMV to guide vaccine development.

Deere, Jesse D / Barry, Peter A

2014 Volume 6, Issue 4, Page(s) 1483–1501

Abstract: The natural history of human cytomegalovirus (HCMV) is inextricably associated with mucosal surfaces. The vast preponderance of primary infections occur following mucosal exposure to infectious virions, and the high seroprevalence of HCMV throughout the ... ...

Abstract	The natural history of human cytomegalovirus (HCMV) is inextricably associated with mucosal surfaces. The vast preponderance of primary infections occur following mucosal exposure to infectious virions, and the high seroprevalence of HCMV throughout the world is due to long-term excretion of HCMV in bodily fluids from multiple mucosal sites. Accumulating evidence presents a model where the earliest virus-host interactions following infection dictate the long-term pattern of infection, alter innate immune responses that skew adaptive responses to enable persistence within an immune host, and are essential for reinfection of a host with prior immunity. HCMV has evolved a complex repertoire of viral functions fine-tuned to manipulate the immune environment both locally at the sites of infection and systemically within an infected host. Collectively, viral immune modulation represents a significant impediment for an HCMV vaccine. As HCMV can disseminate beyond mucosal surfaces to reinfect immune hosts, it may not matter whether prior immunity results from prior infection or immunization. A better understanding of the earliest virus-hosts interactions at mucosal surfaces may identify elements of the viral proteome that are especially susceptible to vaccine-mediated disruption and prevent challenge virus from disseminating to distal sites, particularly the maternal-fetal interface.
MeSH term(s)	Animals ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/prevention & control ; Cytomegalovirus Vaccines/immunology ; Cytomegalovirus Vaccines/isolation & purification ; Disease Models, Animal ; Drug Discovery/methods ; Host-Pathogen Interactions ; Humans ; Primates
Chemical Substances	Cytomegalovirus Vaccines
Language	English
Publishing date	2014-03-27
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v6041483
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Article ; Online: FcRγ- NK Cell Induction by Specific Cytomegalovirus and Expansion by Subclinical Viral Infections in Rhesus Macaques.

Lee, Jaewon / Chang, W L William / Scott, Jeannine M / Hong, Suyeon / Lee, Taehyung / Deere, Jesse D / Park, Peter H / Sparger, Ellen E / Dandekar, Satya / Hartigan-O'Connor, Dennis J / Barry, Peter A / Kim, Sungjin

Journal of immunology (Baltimore, Md. : 1950)

2023 Volume 211, Issue 3, Page(s) 443–452

Abstract: Adaptive" NK cells, characterized by FcRγ deficiency and enhanced responsiveness to Ab-bound, virus-infected cells, have been found in certain hCMV-seropositive individuals. Because humans are exposed to numerous microbes and environmental agents, ... ...

Abstract	"Adaptive" NK cells, characterized by FcRγ deficiency and enhanced responsiveness to Ab-bound, virus-infected cells, have been found in certain hCMV-seropositive individuals. Because humans are exposed to numerous microbes and environmental agents, specific relationships between hCMV and FcRγ-deficient NK cells (also known as g-NK cells) have been challenging to define. Here, we show that a subgroup of rhesus CMV (RhCMV)-seropositive macaques possesses FcRγ-deficient NK cells that stably persist and display a phenotype resembling human FcRγ-deficient NK cells. Moreover, these macaque NK cells resembled human FcRγ-deficient NK cells with respect to functional characteristics, including enhanced responsiveness to RhCMV-infected target in an Ab-dependent manner and hyporesponsiveness to tumor and cytokine stimulation. These cells were not detected in specific pathogen-free (SPF) macaques free of RhCMV and six other viruses; however, experimental infection of SPF animals with RhCMV strain UCD59, but not RhCMV strain 68-1 or SIV, led to induction of FcRγ-deficient NK cells. In non-SPF macaques, coinfection by RhCMV with other common viruses was associated with higher frequencies of FcRγ-deficient NK cells. These results support a causal role for specific CMV strain(s) in the induction of FcRγ-deficient NK cells and suggest that coinfection by other viruses further expands this memory-like NK cell pool.
MeSH term(s)	Animals ; Humans ; Cytomegalovirus/genetics ; Cytomegalovirus Infections ; Macaca mulatta ; Coinfection ; Virus Diseases ; Killer Cells, Natural
Language	English
Publishing date	2023-06-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2200380
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Article: SIV clearance from neonatal macaques following transient CCR5 depletion.

bioRxiv : the preprint server for biology

2023

Abstract: Treatment of people with HIV (PWH) with antiretroviral therapy (ART) results in sustained suppression of viremia, but HIV persists indefinitely as integrated provirus in CD4-expressing cells. Intact persistent provirus, the "rebound competent viral ... ...

Abstract	Treatment of people with HIV (PWH) with antiretroviral therapy (ART) results in sustained suppression of viremia, but HIV persists indefinitely as integrated provirus in CD4-expressing cells. Intact persistent provirus, the "rebound competent viral reservoir" (RCVR), is the primary obstacle to achieving a cure. Most variants of HIV enter CD4
Language	English
Publishing date	2023-05-01
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.05.01.533682
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Article ; Online: Rhesus monkeys for a nonhuman primate model of cytomegalovirus infections.

Itell, Hannah L / Kaur, Amitinder / Deere, Jesse D / Barry, Peter A / Permar, Sallie R

Current opinion in virology

2017 Volume 25, Page(s) 126–133

Abstract: Human cytomegalovirus (HCMV) is the leading opportunistic viral infection in solid organ transplant patients and is the most common congenitally transmitted pathogen worldwide. Despite the significant burden of disease HCMV causes in immunosuppressed ... ...

Abstract	Human cytomegalovirus (HCMV) is the leading opportunistic viral infection in solid organ transplant patients and is the most common congenitally transmitted pathogen worldwide. Despite the significant burden of disease HCMV causes in immunosuppressed patients and infected newborns, there are no licensed preventative vaccines or effective immunotherapeutic treatments for HCMV, largely due to our incomplete understanding of the immune correlates of protection against HCMV infection and disease. Though CMV species-specificity imposes an additional challenge in defining a suitable animal model for HCMV, nonhuman primate (NHP) CMVs are the most genetically related to HCMV. In this review, we discuss the advantages and applicability of rhesus monkey models for studying HCMV infections and pathogenesis and ultimately informing vaccine development.
MeSH term(s)	Animals ; Coinfection/virology ; Cytomegalovirus/genetics ; Cytomegalovirus/immunology ; Cytomegalovirus Infections/congenital ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/virology ; Disease Models, Animal ; Humans ; Macaca mulatta
Language	English
Publishing date	2017-09-06
Publishing country	Netherlands
Document type	Journal Article ; Review
ZDB-ID	2611378-8
ISSN	1879-6265 ; 1879-6257
ISSN (online)	1879-6265
ISSN	1879-6257
DOI	10.1016/j.coviro.2017.08.005
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Article ; Online: Cytomegalovirus infection disrupts the influence of short-chain fatty acid producers on Treg/Th17 balance.

Chin, Ning / Narayan, Nicole R / Méndez-Lagares, Gema / Ardeshir, Amir / Chang, W L William / Deere, Jesse D / Fontaine, Justin H / Chen, Connie / Kieu, Hung T / Lu, Wenze / Barry, Peter A / Sparger, Ellen E / Hartigan-O'Connor, Dennis J

Microbiome

2022 Volume 10, Issue 1, Page(s) 168

Abstract: Background: Both the gut microbiota and chronic viral infections have profound effects on host immunity, but interactions between these influences have been only superficially explored. Cytomegalovirus (CMV), for example, infects approximately 80% of ... ...

Abstract	Background: Both the gut microbiota and chronic viral infections have profound effects on host immunity, but interactions between these influences have been only superficially explored. Cytomegalovirus (CMV), for example, infects approximately 80% of people globally and drives significant changes in immune cells. Similarly, certain gut-resident bacteria affect T-cell development in mice and nonhuman primates. It is unknown if changes imposed by CMV on the intestinal microbiome contribute to immunologic effects of the infection. Results: We show that rhesus cytomegalovirus (RhCMV) infection is associated with specific differences in gut microbiota composition, including decreased abundance of Firmicutes, and that the extent of microbial change was associated with immunologic changes including the proliferation, differentiation, and cytokine production of CD8 Conclusions: Gut microbes have an important influence on health and disease. Diet is known to shape the microbiota, but the influence of concomitant chronic viral infections is unclear. We found that CMV influences gut microbiota composition to an extent that is correlated with immunologic changes in the host. Additionally, pre-existing correlations between immunophenotypes and gut microbes can be subverted by CMV infection. Immunologic effects of CMV infection on the host may therefore be mediated by two different mechanisms involving gut microbiota. Video Abstract.
MeSH term(s)	Animals ; CD8-Positive T-Lymphocytes ; Cytokines ; Cytomegalovirus/genetics ; Cytomegalovirus Infections ; Fatty Acids, Volatile ; Macaca mulatta ; Mice ; T-Lymphocytes, Regulatory
Chemical Substances	Cytokines ; Fatty Acids, Volatile
Language	English
Publishing date	2022-10-10
Publishing country	England
Document type	Journal Article ; Video-Audio Media ; Research Support, N.I.H., Extramural
ZDB-ID	2697425-3
ISSN	2049-2618 ; 2049-2618
ISSN (online)	2049-2618
ISSN	2049-2618
DOI	10.1186/s40168-022-01355-3
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Article ; Online: RhCMV serostatus and vaccine adjuvant impact immunogenicity of RhCMV/SIV vaccines.

Chang, W L William / Deere, Jesse D / Kieu, Hung T / Castillo, Luis D / Machmach, Kawthar / Shen, Xiaoying / Tomaras, Georgia D / Shacklett, Barbara L / Barry, Peter A / Hartigan-O'Connor, Dennis J / Sparger, Ellen E

Scientific reports

2020 Volume 10, Issue 1, Page(s) 14056

Abstract: Rhesus cytomegalovirus (RhCMV) strain 68-1-vectored simian immunodeficiency virus (RhCMV/SIV) vaccines are associated with complete clearance of pathogenic SIV challenge virus, non-canonical major histocompatibility complex restriction, and absent ... ...

Abstract	Rhesus cytomegalovirus (RhCMV) strain 68-1-vectored simian immunodeficiency virus (RhCMV/SIV) vaccines are associated with complete clearance of pathogenic SIV challenge virus, non-canonical major histocompatibility complex restriction, and absent antibody responses in recipients previously infected with wild-type RhCMV. This report presents the first investigation of RhCMV/SIV vaccines in RhCMV-seronegative macaques lacking anti-vector immunity. Fifty percent of rhesus macaques (RM) vaccinated with a combined RhCMV-Gag, -Env, and -Retanef (RTN) vaccine controlled pathogenic SIV challenge despite high peak viremia. However, kinetics of viral load control by vaccinated RM were considerably delayed compared to previous reports. Impact of a TLR5 agonist (flagellin; FliC) on vaccine efficacy and immunogenicity was also examined. An altered vaccine regimen containing an SIV Gag-FliC fusion antigen instead of Gag was significantly less immunogenic and resulted in reduced protection. Notably, RhCMV-Gag and RhCMV-Env vaccines elicited anti-Gag and anti-Env antibodies in RhCMV-seronegative RM, an unexpected contrast to vaccination of RhCMV-seropositive RM. These findings confirm that RhCMV-vectored SIV vaccines significantly protect against SIV pathogenesis. However, pre-existing vector immunity and a pro-inflammatory vaccine adjuvant may influence RhCMV/SIV vaccine immunogenicity and efficacy. Future investigation of the impact of pre-existing anti-vector immune responses on protective immunity conferred by this vaccine platform is warranted.
MeSH term(s)	Adjuvants, Immunologic/pharmacology ; Animals ; Antibodies, Viral/biosynthesis ; CD4-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/immunology ; Cytomegalovirus/immunology ; Cytomegalovirus/isolation & purification ; Gene Products, gag/immunology ; Humans ; Immunity, Innate ; Interferon-gamma/metabolism ; Macaca mulatta ; Simian Immunodeficiency Virus/immunology ; Simian Immunodeficiency Virus/isolation & purification ; Viral Load ; Viral Vaccines/immunology
Chemical Substances	Adjuvants, Immunologic ; Antibodies, Viral ; Gene Products, gag ; Viral Vaccines ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2020-08-20
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-020-71075-x
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Article ; Online: Simian immunodeficiency virus macaque models of HIV latency.

Deere, Jesse D / Schinazi, Raymond F / North, Thomas W

Current opinion in HIV and AIDS

2011 Volume 6, Issue 1, Page(s) 57–61

Abstract: Purpose of review: This review will focus on recent developments in several nonhuman primate models of AIDS. These models are being used to address viral latency and persistence during antiretroviral therapy in studies that are not feasible in humans.!## ...

Abstract	Purpose of review: This review will focus on recent developments in several nonhuman primate models of AIDS. These models are being used to address viral latency and persistence during antiretroviral therapy in studies that are not feasible in humans. Recent findings: Further characterization of the various macaque models of AIDS has demonstrated that several aspects of viral persistence during antiretroviral therapy model HIV-1 infection in humans, including viral decay kinetics. Widespread distribution of viral RNA and viral DNA has been detected in many tissue organs. In addition, the brain has been identified as a site of persistent viral DNA. Summary: The macaque models of AIDS are well suited for addressing viral persistence during antiretroviral therapy, including viral latency, residual replication, and tissue organ distribution.
MeSH term(s)	Animals ; Disease Models, Animal ; HIV Infections/virology ; Humans ; Macaca/virology ; Simian Acquired Immunodeficiency Syndrome/virology ; Simian Immunodeficiency Virus/pathogenicity ; Virus Latency
Language	English
Publishing date	2011-01-01
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	2502511-9
ISSN	1746-6318 ; 1746-630X
ISSN (online)	1746-6318
ISSN	1746-630X
DOI	10.1097/COH.0b013e32834086ce
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Article ; Online: Neutralization of rhesus cytomegalovirus IL-10 reduces horizontal transmission and alters long-term immunity.

Deere, Jesse D / Chang, W L William / Villalobos, Andradi / Schmidt, Kimberli A / Deshpande, Ashlesha / Castillo, Luis D / Fike, Joseph / Walter, Mark R / Barry, Peter A / Hartigan-O'Connor, Dennis J

Proceedings of the National Academy of Sciences of the United States of America

2019 Volume 116, Issue 26, Page(s) 13036–13041

Abstract: Human cytomegalovirus (HCMV) causes severe disease in infants and immunocompromised people. There is no approved HCMV vaccine, and vaccine development strategies are complicated by evidence of both persistent infection and reinfection of people with ... ...

Abstract	Human cytomegalovirus (HCMV) causes severe disease in infants and immunocompromised people. There is no approved HCMV vaccine, and vaccine development strategies are complicated by evidence of both persistent infection and reinfection of people with prior immunity. The greatest emphasis has been placed on reducing transmission to seronegative pregnant women to prevent vertical transmission and its potentially severe sequelae. Increasing evidence suggests that the earliest host-HCMV interactions establish conditions for viral persistence, including evasion of host immune responses to the virus. Using a nonhuman primate model of HCMV infection, we show that rhesus macaques immunized against viral interleukin-10 (IL-10) manifest delayed rhesus cytomegalovirus (RhCMV) acquisition and altered immune responses to the infection when it does occur. Among animals with the greatest antiviral IL-10-neutralizing activity, the timing of RhCMV seroconversion was delayed by an average of 12 weeks. After acquisition, such animals displayed an antibody response to the new infection, which peaked as expected after 2 weeks but then declined rapidly. In contrast, surprisingly, vaccination with glycoprotein B (gB) protein had no discernible impact on these outcomes. Our results demonstrate that viral IL-10 is a key regulator of successful host immune responses to RhCMV. Viral IL-10 is, therefore, an important target for vaccine strategies against cytomegalovirus (CMV). Furthermore, given the immunoregulatory function of viral IL-10, targeting this protein may prove synergistic with other vaccine therapies and targets. Our study also provides additional evidence that the earliest host-CMV interactions can have a significant impact on the nature of persistent infection.
MeSH term(s)	Animals ; Antibodies, Neutralizing/blood ; Antibodies, Neutralizing/immunology ; Antibodies, Viral/blood ; Antibodies, Viral/immunology ; Antigens, Viral/administration & dosage ; Antigens, Viral/immunology ; Cytomegalovirus/immunology ; Cytomegalovirus Infections/blood ; Cytomegalovirus Infections/prevention & control ; Cytomegalovirus Infections/transmission ; Cytomegalovirus Infections/virology ; Cytomegalovirus Vaccines/immunology ; Cytomegalovirus Vaccines/pharmacology ; Cytomegalovirus Vaccines/therapeutic use ; Disease Models, Animal ; Female ; Host-Pathogen Interactions/immunology ; Humans ; Immunity, Mucosal ; Immunogenicity, Vaccine ; Infectious Disease Transmission, Vertical/prevention & control ; Interleukin-10/administration & dosage ; Interleukin-10/immunology ; Macaca mulatta ; Pregnancy ; Recombinant Proteins/administration & dosage ; Recombinant Proteins/immunology ; Viral Envelope Proteins/administration & dosage ; Viral Envelope Proteins/immunology ; Virus Shedding/immunology
Chemical Substances	Antibodies, Neutralizing ; Antibodies, Viral ; Antigens, Viral ; Cytomegalovirus Vaccines ; Recombinant Proteins ; Viral Envelope Proteins ; glycoprotein B, Simplexvirus ; Interleukin-10 (130068-27-8)
Language	English
Publishing date	2019-06-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1903317116
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Article ; Online: Cytomegalovirus-vectored vaccines for HIV and other pathogens.

Barry, Peter A / Deere, Jesse D / Yue, Yujuan / Chang, William W L / Schmidt, Kimberli A / Wussow, Felix / Chiuppesi, Flavia / Diamond, Don J / Sparger, Ellen E / Walter, Mark R / Hartigan-O'Connor, Dennis J

AIDS (London, England)

2019 Volume 34, Issue 3, Page(s) 335–349

Abstract: The use of cytomegalovirus (CMV) as a vaccine vector to express antigens against multiple infectious diseases, including simian immunodeficiency virus, Ebola virus, plasmodium, and mycobacterium tuberculosis, in rhesus macaques has generated ... ...

Abstract	: The use of cytomegalovirus (CMV) as a vaccine vector to express antigens against multiple infectious diseases, including simian immunodeficiency virus, Ebola virus, plasmodium, and mycobacterium tuberculosis, in rhesus macaques has generated extraordinary levels of protective immunity against subsequent pathogenic challenge. Moreover, the mechanisms of immune protection have altered paradigms about viral vector-mediated immunity against ectopically expressed vaccine antigens. Further optimization of CMV-vectored vaccines, particularly as this approach moves to human clinical trials will be augmented by a more complete understanding of how CMV engenders mechanisms of immune protection. This review summarizes the particulars of the specific CMV vaccine vector that has been used to date (rhesus CMV strain 68-1) in relation to CMV natural history.
MeSH term(s)	Animals ; Antibodies, Viral ; Cytomegalovirus/immunology ; Cytomegalovirus Vaccines ; Genetic Vectors ; HIV Infections/prevention & control ; Humans ; Macaca mulatta ; Simian Acquired Immunodeficiency Syndrome ; Simian Immunodeficiency Virus/immunology
Chemical Substances	Antibodies, Viral ; Cytomegalovirus Vaccines
Language	English
Publishing date	2019-10-22
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	639076-6
ISSN	1473-5571 ; 0269-9370 ; 1350-2840
ISSN (online)	1473-5571
ISSN	0269-9370 ; 1350-2840
DOI	10.1097/QAD.0000000000002396
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Article ; Online: Subclinical Cytomegalovirus Infection Is Associated with Altered Host Immunity, Gut Microbiota, and Vaccine Responses.

Santos Rocha, Clarissa / Hirao, Lauren A / Weber, Mariana G / Méndez-Lagares, Gema / Chang, W L William / Jiang, Guochun / Deere, Jesse D / Sparger, Ellen E / Roberts, Jeffrey / Barry, Peter A / Hartigan-O'Connor, Dennis J / Dandekar, Satya

Journal of virology

2018 Volume 92, Issue 13

Abstract: Subclinical viral infections (SVI), including cytomegalovirus (CMV), are highly prevalent in humans, resulting in lifelong persistence. However, the impact of SVI on the interplay between the host immunity and gut microbiota in the context of ... ...

Abstract	Subclinical viral infections (SVI), including cytomegalovirus (CMV), are highly prevalent in humans, resulting in lifelong persistence. However, the impact of SVI on the interplay between the host immunity and gut microbiota in the context of environmental exposures is not well defined. We utilized the preclinical nonhuman primate (NHP) model consisting of SVI-free (specific-pathogen-free [SPF]) rhesus macaques and compared them to the animals with SVI (non-SPF) acquired through natural exposure and investigated the impact of SVI on immune cell distribution and function, as well as on gut microbiota. These changes were examined in animals housed in the outdoor environment compared to the controlled indoor environment. We report that SVI are associated with altered immune cell subsets and gut microbiota composition in animals housed in the outdoor environment. Non-SPF animals harbored a higher proportion of potential butyrate-producing
MeSH term(s)	Animals ; Bacteria/classification ; Bacteria/isolation & purification ; Cytokines/metabolism ; Cytomegalovirus/pathogenicity ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/veterinary ; Disease Models, Animal ; Gastrointestinal Microbiome ; Housing, Animal ; Lymphocytes/metabolism ; Macaca mulatta ; Monkey Diseases/immunology ; Monkey Diseases/microbiology ; Phylogeny ; Specific Pathogen-Free Organisms ; T-Lymphocytes/immunology
Chemical Substances	Cytokines
Language	English
Publishing date	2018-06-13
Publishing country	United States
Document type	Comparative Study ; Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.00167-18
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