EcoHIV infection of mice establishes latent viral reservoirs in T cells and active viral reservoirs in macrophages that are sufficient for induction of neurocognitive impairment

Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD...

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Published inPLoS pathogens Vol. 14; no. 6; p. e1007061
Main Authors Gu, Chao-Jiang, Borjabad, Alejandra, Hadas, Eran, Kelschenbach, Jennifer, Kim, Boe-Hyun, Chao, Wei, Arancio, Ottavio, Suh, Jin, Polsky, Bruce, McMillan, JoEllyn, Edagwa, Benson, Gendelman, Howard E., Potash, Mary Jane, Volsky, David J.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.06.2018
Public Library of Science (PLoS)
Subjects
Acquired immune deficiency syndrome
Adoptive Transfer
Aged
AIDS
Animal cognition
Animal tissues
Animals
Anti-Retroviral Agents - therapeutic use
Antigens
Antiretroviral agents
Antiretroviral drugs
Antiretroviral therapy
Biology and Life Sciences
Brain
Brain - virology
CD4 antigen
CD4-Positive T-Lymphocytes - virology
Chronic illnesses
Cognition
Cognitive ability
Dementia
Deoxyribonucleic acid
Disease Reservoirs
DNA
Dosage and administration
Drug therapy
Epigenetics
Female
Health aspects
HIV
HIV - genetics
HIV - immunology
HIV - pathogenicity
HIV - physiology
HIV infections
HIV Infections - complications
HIV Infections - drug therapy
Human immunodeficiency virus
Humans
Immunity
Immunization
Immunocompetence
Immunomodulation
Impairment
In vivo methods and tests
Infections
Learning
Leukemia
Lymphocytes
Lymphocytes T
Macrophages
Macrophages, Peritoneal - virology
Male
Medicine
Medicine and Health Sciences
Memory
Memory cells
Mice
Mice, Inbred C57BL
Mice, Nude
Middle Aged
Modulators
Monocytes
Nervous system
Neurocognitive Disorders - virology
Neuromodulation
Neuropathogenesis
Neurosciences
Pathogenesis
Pharmacology
Physiological aspects
Plasmids
Potash
Prophylaxis
Replication
Research and Analysis Methods
Spleen - cytology
Spleen - immunology
Systematic review
T cells
Therapy
Transgenic animals
Virus replication
Viruses
New York
United States > US
Nebraska
Online AccessGet full text
ISSN1553-7374
1553-7366
1553-7374
DOI10.1371/journal.ppat.1007061

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Abstract Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD4+ T cells. Macrophages are persistently infected with HIV but their role as HIV reservoirs in vivo has not been fully explored. Here we show that infection of conventional mice with chimeric HIV, EcoHIV, reproduces physiological conditions for development of disease in people on ART including immunocompetence, stable suppression of HIV replication, persistence of integrated, replication-competent HIV in T cells and macrophages, and manifestation of learning and memory deficits in behavioral tests, termed here murine HIV-NCI. EcoHIV established latent reservoirs in CD4+ T lymphocytes in chronically-infected mice but could be induced by epigenetic modulators ex vivo and in mice. In contrast, macrophages expressed EcoHIV constitutively in mice for up to 16 months; murine leukemia virus (MLV), the donor of gp80 envelope in EcoHIV, did not infect macrophages. Both EcoHIV and MLV were found in brain tissue of infected mice but only EcoHIV induced NCI. Murine HIV-NCI was prevented by antiretroviral prophylaxis but once established neither persistent EcoHIV infection in mice nor NCI could be reversed by long-acting antiretroviral therapy. EcoHIV-infected, athymic mice were more permissive to virus replication in macrophages than were wild-type mice, suffered cognitive dysfunction, as well as increased numbers of monocytes and macrophages infiltrating the brain. Our results suggest an important role of HIV expressing macrophages in HIV neuropathogenesis in hosts with suppressed HIV replication.
AbstractList Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD4+ T cells. Macrophages are persistently infected with HIV but their role as HIV reservoirs in vivo has not been fully explored. Here we show that infection of conventional mice with chimeric HIV, EcoHIV, reproduces physiological conditions for development of disease in people on ART including immunocompetence, stable suppression of HIV replication, persistence of integrated, replication-competent HIV in T cells and macrophages, and manifestation of learning and memory deficits in behavioral tests, termed here murine HIV-NCI. EcoHIV established latent reservoirs in CD4+ T lymphocytes in chronically-infected mice but could be induced by epigenetic modulators ex vivo and in mice. In contrast, macrophages expressed EcoHIV constitutively in mice for up to 16 months; murine leukemia virus (MLV), the donor of gp80 envelope in EcoHIV, did not infect macrophages. Both EcoHIV and MLV were found in brain tissue of infected mice but only EcoHIV induced NCI. Murine HIV-NCI was prevented by antiretroviral prophylaxis but once established neither persistent EcoHIV infection in mice nor NCI could be reversed by long-acting antiretroviral therapy. EcoHIV-infected, athymic mice were more permissive to virus replication in macrophages than were wild-type mice, suffered cognitive dysfunction, as well as increased numbers of monocytes and macrophages infiltrating the brain. Our results suggest an important role of HIV expressing macrophages in HIV neuropathogenesis in hosts with suppressed HIV replication.
Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD4+ T cells. Macrophages are persistently infected with HIV but their role as HIV reservoirs in vivo has not been fully explored. Here we show that infection of conventional mice with chimeric HIV, EcoHIV, reproduces physiological conditions for development of disease in people on ART including immunocompetence, stable suppression of HIV replication, persistence of integrated, replication-competent HIV in T cells and macrophages, and manifestation of learning and memory deficits in behavioral tests, termed here murine HIV-NCI. EcoHIV established latent reservoirs in CD4+ T lymphocytes in chronically-infected mice but could be induced by epigenetic modulators ex vivo and in mice. In contrast, macrophages expressed EcoHIV constitutively in mice for up to 16 months; murine leukemia virus (MLV), the donor of gp80 envelope in EcoHIV, did not infect macrophages. Both EcoHIV and MLV were found in brain tissue of infected mice but only EcoHIV induced NCI. Murine HIV-NCI was prevented by antiretroviral prophylaxis but once established neither persistent EcoHIV infection in mice nor NCI could be reversed by long-acting antiretroviral therapy. EcoHIV-infected, athymic mice were more permissive to virus replication in macrophages than were wild-type mice, suffered cognitive dysfunction, as well as increased numbers of monocytes and macrophages infiltrating the brain. Our results suggest an important role of HIV expressing macrophages in HIV neuropathogenesis in hosts with suppressed HIV replication.Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD4+ T cells. Macrophages are persistently infected with HIV but their role as HIV reservoirs in vivo has not been fully explored. Here we show that infection of conventional mice with chimeric HIV, EcoHIV, reproduces physiological conditions for development of disease in people on ART including immunocompetence, stable suppression of HIV replication, persistence of integrated, replication-competent HIV in T cells and macrophages, and manifestation of learning and memory deficits in behavioral tests, termed here murine HIV-NCI. EcoHIV established latent reservoirs in CD4+ T lymphocytes in chronically-infected mice but could be induced by epigenetic modulators ex vivo and in mice. In contrast, macrophages expressed EcoHIV constitutively in mice for up to 16 months; murine leukemia virus (MLV), the donor of gp80 envelope in EcoHIV, did not infect macrophages. Both EcoHIV and MLV were found in brain tissue of infected mice but only EcoHIV induced NCI. Murine HIV-NCI was prevented by antiretroviral prophylaxis but once established neither persistent EcoHIV infection in mice nor NCI could be reversed by long-acting antiretroviral therapy. EcoHIV-infected, athymic mice were more permissive to virus replication in macrophages than were wild-type mice, suffered cognitive dysfunction, as well as increased numbers of monocytes and macrophages infiltrating the brain. Our results suggest an important role of HIV expressing macrophages in HIV neuropathogenesis in hosts with suppressed HIV replication.
Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD4+ T cells. Macrophages are persistently infected with HIV but their role as HIV reservoirs in vivo has not been fully explored. Here we show that infection of conventional mice with chimeric HIV, EcoHIV, reproduces physiological conditions for development of disease in people on ART including immunocompetence, stable suppression of HIV replication, persistence of integrated, replication-competent HIV in T cells and macrophages, and manifestation of learning and memory deficits in behavioral tests, termed here murine HIV-NCI. EcoHIV established latent reservoirs in CD4+ T lymphocytes in chronically-infected mice but could be induced by epigenetic modulators ex vivo and in mice. In contrast, macrophages expressed EcoHIV constitutively in mice for up to 16 months; murine leukemia virus (MLV), the donor of gp80 envelope in EcoHIV, did not infect macrophages. Both EcoHIV and MLV were found in brain tissue of infected mice but only EcoHIV induced NCI. Murine HIV-NCI was prevented by antiretroviral prophylaxis but once established neither persistent EcoHIV infection in mice nor NCI could be reversed by long-acting antiretroviral therapy. EcoHIV-infected, athymic mice were more permissive to virus replication in macrophages than were wild-type mice, suffered cognitive dysfunction, as well as increased numbers of monocytes and macrophages infiltrating the brain. Our results suggest an important role of HIV expressing macrophages in HIV neuropathogenesis in hosts with suppressed HIV replication. Antiretroviral therapy (ART) transformed HIV infection from a death sentence to a chronic, largely manageable condition, with near preservation of immune systems and extended life expectancies in infected people. Despite effective ART, roughly half of HIV-infected people suffer problems in learning and memory that can impair day to day activities. In addition, HIV persists in largely silent states during ART, but it can be reactivated and produce infectious, possibly pathogenic virus. We addressed these two issues by infecting mice with a genetically engineered HIV that infects rodents instead of human beings. Unlike infected people we find that infected mice maintain good immune responses to HIV that appear to act like ART to keep virus levels low and allow mice to resist other complications. Like infected people, HIV-infected mice are subject to learning and memory problems; they carry silenced HIV long-term in T lymphocytes but we found that macrophages, infected in both humans and mice, continue to produce HIV in mice indicating that additional means may be needed to control HIV-infected macrophages. Moreover, in mice lacking T lymphocytes HIV infection of macrophages is sufficient to drive dysfunction in learning and memory. Like in people living with HIV, antiretroviral therapy in chronically-infected mice is ineffective against existing HIV infection and cognitive disease. Controlling this infection and brain disease may require tools tailored to actively expressed virus.
Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including neurocognitive impairment (HIV-NCI). Pathogenesis in HIV-suppressed individuals has been attributed to reservoirs of latent-inducible virus in resting CD4.sup.+ T cells. Macrophages are persistently infected with HIV but their role as HIV reservoirs in vivo has not been fully explored. Here we show that infection of conventional mice with chimeric HIV, EcoHIV, reproduces physiological conditions for development of disease in people on ART including immunocompetence, stable suppression of HIV replication, persistence of integrated, replication-competent HIV in T cells and macrophages, and manifestation of learning and memory deficits in behavioral tests, termed here murine HIV-NCI. EcoHIV established latent reservoirs in CD4.sup.+ T lymphocytes in chronically-infected mice but could be induced by epigenetic modulators ex vivo and in mice. In contrast, macrophages expressed EcoHIV constitutively in mice for up to 16 months; murine leukemia virus (MLV), the donor of gp80 envelope in EcoHIV, did not infect macrophages. Both EcoHIV and MLV were found in brain tissue of infected mice but only EcoHIV induced NCI. Murine HIV-NCI was prevented by antiretroviral prophylaxis but once established neither persistent EcoHIV infection in mice nor NCI could be reversed by long-acting antiretroviral therapy. EcoHIV-infected, athymic mice were more permissive to virus replication in macrophages than were wild-type mice, suffered cognitive dysfunction, as well as increased numbers of monocytes and macrophages infiltrating the brain. Our results suggest an important role of HIV expressing macrophages in HIV neuropathogenesis in hosts with suppressed HIV replication.
Audience Academic
Author Polsky, Bruce
Kelschenbach, Jennifer
Potash, Mary Jane
Kim, Boe-Hyun
McMillan, JoEllyn
Volsky, David J.
Arancio, Ottavio
Chao, Wei
Hadas, Eran
Borjabad, Alejandra
Edagwa, Benson
Gendelman, Howard E.
Suh, Jin
Gu, Chao-Jiang
AuthorAffiliation 2 Department of Pathology and Cell Biology, Columbia University Medical Center, New York, New York, United States of America
4 Department of Medicine, NYU Winthrop Hospital, Mineola, New York, United States of America
1 Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America
University of North Carolina at Chapel Hill, UNITED STATES
5 Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska, United States of America
3 Department of Medicine, St. Joseph’s Regional Medical Center, Paterson, New Jersey, United States of America
AuthorAffiliation_xml – name: 5 Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska, United States of America
– name: 4 Department of Medicine, NYU Winthrop Hospital, Mineola, New York, United States of America
– name: University of North Carolina at Chapel Hill, UNITED STATES
– name: 2 Department of Pathology and Cell Biology, Columbia University Medical Center, New York, New York, United States of America
– name: 1 Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America
– name: 3 Department of Medicine, St. Joseph’s Regional Medical Center, Paterson, New Jersey, United States of America
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29879225$$D View this record in MEDLINE/PubMed
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2018 Gu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2018 Gu et al 2018 Gu et al
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– notice: 2018 Gu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Current address: College of Life Science and Health, Wuhan University of Science and Technology, Wuhan, Hubei, P.R. China
The authors have declared that no competing interests exist.
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Snippet Suppression of HIV replication by antiretroviral therapy (ART) or host immunity can prevent AIDS but not other HIV-associated conditions including...
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SubjectTerms Acquired immune deficiency syndrome
Adoptive Transfer
Aged
AIDS
Animal cognition
Animal tissues
Animals
Anti-Retroviral Agents - therapeutic use
Antigens
Antiretroviral agents
Antiretroviral drugs
Antiretroviral therapy
Biology and Life Sciences
Brain
Brain - virology
CD4 antigen
CD4-Positive T-Lymphocytes - virology
Chronic illnesses
Cognition
Cognitive ability
Dementia
Deoxyribonucleic acid
Disease Reservoirs
DNA
Dosage and administration
Drug therapy
Epigenetics
Female
Health aspects
HIV
HIV - genetics
HIV - immunology
HIV - pathogenicity
HIV - physiology
HIV infections
HIV Infections - complications
HIV Infections - drug therapy
Human immunodeficiency virus
Humans
Immunity
Immunization
Immunocompetence
Immunomodulation
Impairment
In vivo methods and tests
Infections
Learning
Leukemia
Lymphocytes
Lymphocytes T
Macrophages
Macrophages, Peritoneal - virology
Male
Medicine
Medicine and Health Sciences
Memory
Memory cells
Mice
Mice, Inbred C57BL
Mice, Nude
Middle Aged
Modulators
Monocytes
Nervous system
Neurocognitive Disorders - virology
Neuromodulation
Neuropathogenesis
Neurosciences
Pathogenesis
Pharmacology
Physiological aspects
Plasmids
Potash
Prophylaxis
Replication
Research and Analysis Methods
Spleen - cytology
Spleen - immunology
Systematic review
T cells
Therapy
Transgenic animals
Virus replication
Viruses
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Title EcoHIV infection of mice establishes latent viral reservoirs in T cells and active viral reservoirs in macrophages that are sufficient for induction of neurocognitive impairment
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