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Article ; Online: Overview of Nonhuman Primate Models of SARS-CoV-2 Infection.

Trichel, Anita M

2021 Volume 71, Issue 5, Page(s) 411–432

Abstract: COVID-19, the disease caused by the SARS-CoV-2 betacoronavirus, was declared a pandemic by the World Health Organization on March 11, 2020. Since then, SARS-CoV-2 has triggered a devastating global health and economic emergency. In response, a broad ... ...

Abstract	COVID-19, the disease caused by the SARS-CoV-2 betacoronavirus, was declared a pandemic by the World Health Organization on March 11, 2020. Since then, SARS-CoV-2 has triggered a devastating global health and economic emergency. In response, a broad range of preclinical animal models have been used to identify effective therapies and vaccines. Current animal models do not express the full spectrum of human COVID-19 disease and pathology, with most exhibiting mild to moderate disease without mortality. NHPs are physiologically, genetically, and immunologically more closely related to humans than other animal species; thus, they provide a relevant model for SARS-CoV-2 investigations. This overview summarizes NHP models of SARS-CoV-2 and their role in vaccine and therapeutic development.
MeSH term(s)	Animals ; COVID-19 ; COVID-19 Vaccines ; Humans ; Pandemics ; Primates ; SARS-CoV-2
Chemical Substances	COVID-19 Vaccines
Language	English
Publishing date	2021-09-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	2006425-1
ISSN	2769-819X ; 0023-6764 ; 1532-0820
ISSN (online)	2769-819X
ISSN	0023-6764 ; 1532-0820
DOI	10.30802/AALAS-CM-20-000119
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Article ; Online: Applications of minimally invasive multimodal telemetry for continuous monitoring of brain function and intracranial pressure in macaques with acute viral encephalitis.

Ma, Henry / Lundy, Jeneveve D / Cottle, Emily L / O'Malley, Katherine J / Trichel, Anita M / Klimstra, William B / Hartman, Amy L / Reed, Douglas S / Teichert, Tobias

PloS one

2020 Volume 15, Issue 6, Page(s) e0232381

Abstract: Alphaviruses such as Venezuelan equine encephalitis virus (VEEV) and Eastern equine encephalitis virus (EEEV) are arboviruses that can cause severe zoonotic disease in humans. Both VEEV and EEEV are highly infectious when aerosolized and can be used as ... ...

Abstract	Alphaviruses such as Venezuelan equine encephalitis virus (VEEV) and Eastern equine encephalitis virus (EEEV) are arboviruses that can cause severe zoonotic disease in humans. Both VEEV and EEEV are highly infectious when aerosolized and can be used as biological weapons. Vaccines and therapeutics are urgently needed, but efficacy determination requires animal models. The cynomolgus macaque (Macaca fascicularis) provides a relevant model of human disease, but questions remain whether vaccines or therapeutics can mitigate CNS infection or disease in this model. The documentation of alphavirus encephalitis in animals relies on traditional physiological biomarkers and behavioral/neurological observations by veterinary staff; quantitative measurements such as electroencephalography (EEG) and intracranial pressure (ICP) can recapitulate underlying encephalitic processes. We detail a telemetry implantation method suitable for continuous monitoring of both EEG and ICP in awake macaques, as well as methods for collection and analysis of such data. We sought to evaluate whether changes in EEG/ICP suggestive of CNS penetration by virus would be seen after aerosol exposure of naïve macaques to VEEV IC INH9813 or EEEV V105 strains compared to mock-infection in a cohort of twelve adult cynomolgus macaques. Data collection ran continuously from at least four days preceding aerosol exposure and up to 50 days thereafter. EEG signals were processed into frequency spectrum bands (delta: [0.4 - 4Hz); theta: [4 - 8Hz); alpha: [8-12Hz); beta: [12-30] Hz) and assessed for viral encephalitis-associated changes against robust background circadian variation while ICP data was assessed for signal fidelity, circadian variability, and for meaningful differences during encephalitis. Results indicated differences in delta, alpha, and beta band magnitude in infected macaques, disrupted circadian rhythm, and proportional increases in ICP in response to alphavirus infection. This novel enhancement of the cynomolgus macaque model offers utility for timely determination of onset, severity, and resolution of encephalitic disease and for the evaluation of vaccine and therapeutic candidates.
MeSH term(s)	Alphavirus/isolation & purification ; Alphavirus/pathogenicity ; Alphavirus Infections/metabolism ; Alphavirus Infections/pathology ; Animals ; Biomarkers/metabolism ; Brain/physiology ; Circadian Rhythm ; Disease Models, Animal ; Electroencephalography/methods ; Encephalitis, Viral/metabolism ; Encephalitis, Viral/pathology ; Female ; Intracranial Pressure/physiology ; Macaca ; Male ; Severity of Illness Index ; Telemetry
Chemical Substances	Biomarkers
Language	English
Publishing date	2020-06-25
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0232381
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Article ; Online: Applications of minimally invasive multimodal telemetry for continuous monitoring of brain function and intracranial pressure in macaques with acute viral encephalitis.

Henry Ma / Jeneveve D Lundy / Emily L Cottle / Katherine J O'Malley / Anita M Trichel / William B Klimstra / Amy L Hartman / Douglas S Reed / Tobias Teichert

PLoS ONE, Vol 15, Iss 6, p e

2020 Volume 0232381

Abstract	Alphaviruses such as Venezuelan equine encephalitis virus (VEEV) and Eastern equine encephalitis virus (EEEV) are arboviruses that can cause severe zoonotic disease in humans. Both VEEV and EEEV are highly infectious when aerosolized and can be used as biological weapons. Vaccines and therapeutics are urgently needed, but efficacy determination requires animal models. The cynomolgus macaque (Macaca fascicularis) provides a relevant model of human disease, but questions remain whether vaccines or therapeutics can mitigate CNS infection or disease in this model. The documentation of alphavirus encephalitis in animals relies on traditional physiological biomarkers and behavioral/neurological observations by veterinary staff; quantitative measurements such as electroencephalography (EEG) and intracranial pressure (ICP) can recapitulate underlying encephalitic processes. We detail a telemetry implantation method suitable for continuous monitoring of both EEG and ICP in awake macaques, as well as methods for collection and analysis of such data. We sought to evaluate whether changes in EEG/ICP suggestive of CNS penetration by virus would be seen after aerosol exposure of naïve macaques to VEEV IC INH9813 or EEEV V105 strains compared to mock-infection in a cohort of twelve adult cynomolgus macaques. Data collection ran continuously from at least four days preceding aerosol exposure and up to 50 days thereafter. EEG signals were processed into frequency spectrum bands (delta: [0.4 - 4Hz); theta: [4 - 8Hz); alpha: [8-12Hz); beta: [12-30] Hz) and assessed for viral encephalitis-associated changes against robust background circadian variation while ICP data was assessed for signal fidelity, circadian variability, and for meaningful differences during encephalitis. Results indicated differences in delta, alpha, and beta band magnitude in infected macaques, disrupted circadian rhythm, and proportional increases in ICP in response to alphavirus infection. This novel enhancement of the cynomolgus macaque model offers utility ...
Keywords	Medicine ; R ; Science ; Q
Subject code	630
Language	English
Publishing date	2020-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: Parallel loss of myeloid and plasmacytoid dendritic cells from blood and lymphoid tissue in simian AIDS.

Brown, Kevin N / Trichel, Anita / Barratt-Boyes, Simon M

Journal of immunology (Baltimore, Md. : 1950)

2007 Volume 178, Issue 11, Page(s) 6958–6967

Abstract: The loss of myeloid (mDC) and plasmacytoid dendritic cells (pDC) from the blood of HIV-infected individuals is associated with progressive disease. It has been proposed that DC loss is due to increased recruitment to lymph nodes, although this has not ... ...

Abstract	The loss of myeloid (mDC) and plasmacytoid dendritic cells (pDC) from the blood of HIV-infected individuals is associated with progressive disease. It has been proposed that DC loss is due to increased recruitment to lymph nodes, although this has not been directly tested. Similarly as in HIV-infected humans, we found that lineage-negative (Lin(-)) HLA-DR(+)CD11c(+)CD123(-) mDC and Lin(-)HLA-DR(+)CD11c(-)CD123(+) pDC were lost from the blood of SIV-infected rhesus macaques with AIDS. In the peripheral lymph nodes of SIV-naive monkeys the majority of mDC were mature cells derived from skin that expressed high levels of HLA-DR, CD83, costimulatory molecules, and the Langerhans cell marker CD1a, whereas pDC expressed low levels of HLA-DR and CD40 and lacked costimulatory molecules, similar to pDC in blood. Surprisingly, both DC subsets were depleted from peripheral and mesenteric lymph nodes and spleens in monkeys with AIDS, although the activation status of the remaining DC subsets was similar to that of DC in health. In peripheral and mesenteric lymph nodes from animals with AIDS there was an accumulation of Lin(-)HLA-DR(moderate)CD11c(-)CD123(-) cells that resembled monocytoid cells but failed to acquire a DC phenotype upon culture, suggesting they were not DC precursors. mDC and pDC from the lymphoid tissues of monkeys with AIDS were prone to spontaneous death in culture, indicating that apoptosis may be a mechanism for their loss in disease. These findings demonstrate that DC are lost from rather than recruited to lymphoid tissue in advanced SIV infection, suggesting that systemic DC depletion plays a direct role in the pathophysiology of AIDS.
MeSH term(s)	Animals ; Cell Death/immunology ; Cells, Cultured ; Dendritic Cells/immunology ; Dendritic Cells/metabolism ; Dendritic Cells/pathology ; Female ; Immunologic Deficiency Syndromes/blood ; Immunologic Deficiency Syndromes/immunology ; Immunologic Deficiency Syndromes/pathology ; Immunophenotyping ; Lymphoid Tissue/immunology ; Lymphoid Tissue/metabolism ; Lymphoid Tissue/pathology ; Macaca mulatta ; Male ; Myeloid Cells/immunology ; Myeloid Cells/metabolism ; Myeloid Cells/pathology ; Simian Acquired Immunodeficiency Syndrome/blood ; Simian Acquired Immunodeficiency Syndrome/immunology ; Simian Acquired Immunodeficiency Syndrome/pathology ; Simian Immunodeficiency Virus
Language	English
Publishing date	2007-04-27
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.178.11.6958
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Article ; Online: Author Correction: Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control.

Nature communications

2019 Volume 10, Issue 1, Page(s) 5768

Abstract: An amendment to this paper has been published and can be accessed via a link at the top of the paper. ...

Abstract	An amendment to this paper has been published and can be accessed via a link at the top of the paper.
Language	English
Publishing date	2019-12-13
Publishing country	England
Document type	Published Erratum
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-019-13816-9
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Article ; Online: Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control.

Nature communications

2019 Volume 10, Issue 1, Page(s) 5101

Abstract: Natural hosts of simian immunodeficiency virus (SIV) avoid AIDS despite lifelong infection. Here, we examined how this outcome is achieved by comparing a natural SIV host, African green monkey (AGM) to an AIDS susceptible species, rhesus macaque (RM). To ...

Abstract	Natural hosts of simian immunodeficiency virus (SIV) avoid AIDS despite lifelong infection. Here, we examined how this outcome is achieved by comparing a natural SIV host, African green monkey (AGM) to an AIDS susceptible species, rhesus macaque (RM). To asses gene expression profiles from acutely SIV infected AGMs and RMs, we developed a systems biology approach termed Conserved Gene Signature Analysis (CGSA), which compared RNA sequencing data from rectal AGM and RM tissues to various other species. We found that AGMs rapidly activate, and then maintain, evolutionarily conserved regenerative wound healing mechanisms in mucosal tissue. The wound healing protein fibronectin shows distinct tissue distribution and abundance kinetics in AGMs. Furthermore, AGM monocytes exhibit an embryonic development and repair/regeneration signature featuring TGF-β and concomitant reduced expression of inflammatory genes compared to RMs. This regenerative wound healing process likely preserves mucosal integrity and prevents inflammatory insults that underlie immune exhaustion in RMs.
MeSH term(s)	Animals ; Chlorocebus aethiops/genetics ; Chlorocebus aethiops/immunology ; Disease Progression ; Fibronectins/immunology ; Fibronectins/metabolism ; Intestinal Mucosa/immunology ; Intestinal Mucosa/metabolism ; Macaca mulatta/genetics ; Macaca mulatta/immunology ; Macrophages/immunology ; Macrophages/metabolism ; Rectum/immunology ; Rectum/metabolism ; Simian Acquired Immunodeficiency Syndrome/immunology ; Simian Immunodeficiency Virus ; Systems Biology ; Transcriptome ; Transforming Growth Factor beta/genetics ; Transforming Growth Factor beta/immunology ; Wound Healing/genetics ; Wound Healing/immunology
Chemical Substances	Fibronectins ; Transforming Growth Factor beta
Language	English
Publishing date	2019-11-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-019-12987-9
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Article ; Online: African green monkeys avoid SIV disease progression by preventing intestinal dysfunction and maintaining mucosal barrier integrity.

Raehtz, Kevin D / Barrenäs, Fredrik / Xu, Cuiling / Busman-Sahay, Kathleen / Valentine, Audrey / Law, Lynn / Ma, Dongzhu / Policicchio, Benjamin B / Wijewardana, Viskam / Brocca-Cofano, Egidio / Trichel, Anita / Gale, Michael / Keele, Brandon F / Estes, Jacob D / Apetrei, Cristian / Pandrea, Ivona

PLoS pathogens

2020 Volume 16, Issue 3, Page(s) e1008333

Abstract: Unlike HIV infection, SIV infection is generally nonpathogenic in natural hosts, such as African green monkeys (AGMs), despite life-long high viral replication. Lack of disease progression was reportedly based on the ability of SIV-infected AGMs to ... ...

Abstract	Unlike HIV infection, SIV infection is generally nonpathogenic in natural hosts, such as African green monkeys (AGMs), despite life-long high viral replication. Lack of disease progression was reportedly based on the ability of SIV-infected AGMs to prevent gut dysfunction, avoiding microbial translocation and the associated systemic immune activation and chronic inflammation. Yet, the maintenance of gut integrity has never been documented, and the mechanism(s) by which gut integrity is preserved are unknown. We sought to investigate the early events of SIV infection in AGMs, specifically examining the impact of SIVsab infection on the gut mucosa. Twenty-nine adult male AGMs were intrarectally infected with SIVsab92018 and serially sacrificed at well-defined stages of SIV infection, preramp-up (1-3 days post-infection (dpi)), ramp-up (4-6 dpi), peak viremia (9-12 dpi), and early chronic SIV infection (46-55 dpi), to assess the levels of immune activation, apoptosis, epithelial damage and microbial translocation in the GI tract and peripheral lymph nodes. Tissue viral loads, plasma cytokines and plasma markers of gut dysfunction were also measured throughout the course of early infection. While a strong, but transient, interferon-based inflammatory response was observed, the levels of plasma markers linked to enteropathy did not increase. Accordingly, no significant increases in apoptosis of either mucosal enterocytes or lymphocytes, and no damage to the mucosal epithelium were documented during early SIVsab infection of AGMs. These findings were supported by RNAseq of the gut tissue, which found no significant alterations in gene expression that would indicate microbial translocation. Thus, for the first time, we confirmed that gut epithelial integrity is preserved, with no evidence of microbial translocation, in AGMs throughout early SIVsab infection. This might protect AGMs from developing intestinal dysfunction and the subsequent chronic inflammation that drives both HIV disease progression and HIV-associated comorbidities.
MeSH term(s)	Animals ; Bacterial Translocation ; Chlorocebus aethiops ; Disease Progression ; Gastrointestinal Microbiome ; HIV Infections/immunology ; HIV Infections/microbiology ; HIV Infections/pathology ; HIV Infections/virology ; HIV-1/physiology ; Humans ; Intestinal Mucosa/immunology ; Intestinal Mucosa/microbiology ; Male ; Simian Acquired Immunodeficiency Syndrome/immunology ; Simian Acquired Immunodeficiency Syndrome/microbiology ; Simian Acquired Immunodeficiency Syndrome/pathology ; Simian Acquired Immunodeficiency Syndrome/virology ; Simian Immunodeficiency Virus/physiology
Language	English
Publishing date	2020-03-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1008333
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Article ; Online: Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control

Nature Communications, Vol 10, Iss 1, Pp 1-

2019 Volume 15

Abstract: Here, the authors compare gene expression signatures in rectal tissues of African green monkeys (AGMs) and rhesus macaques (RMs) acutely infected with simian immunodeficiency virus and find that AGMs rapidly activate and maintain evolutionarily conserved ...

Abstract	Here, the authors compare gene expression signatures in rectal tissues of African green monkeys (AGMs) and rhesus macaques (RMs) acutely infected with simian immunodeficiency virus and find that AGMs rapidly activate and maintain evolutionarily conserved regenerative wound healing mechanisms.
Keywords	Science ; Q
Language	English
Publishing date	2019-11-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control

Nature Communications, Vol 10, Iss 1, Pp 1-

2019 Volume 15

Abstract	Here, the authors compare gene expression signatures in rectal tissues of African green monkeys (AGMs) and rhesus macaques (RMs) acutely infected with simian immunodeficiency virus and find that AGMs rapidly activate and maintain evolutionarily conserved regenerative wound healing mechanisms.
Keywords	Science ; Q
Language	English
Publishing date	2019-11-01T00:00:00Z
Publisher	Nature Publishing Group
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Author Correction

Nature Communications, Vol 10, Iss 1, Pp 1-

Macrophage-associated wound healing contributes to African green monkey SIV pathogenesis control

2019 Volume 1

Abstract: An amendment to this paper has been published and can be accessed via a link at the top of the paper. ...

Abstract	An amendment to this paper has been published and can be accessed via a link at the top of the paper.
Keywords	Science ; Q
Language	English
Publishing date	2019-12-01T00:00:00Z
Publisher	Nature Publishing Group
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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