Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory
HIV emerged following cross-species transmissions of simian immunodeficiency viruses (SIVs) that naturally infect non-human primates (NHPs) from Africa. While HIV replication and CD4+ T-cell depletion lead to increased gut permeability, microbial translocation, chronic immune activation, and systemi...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1060985/full |
| _version_ | 1797955271998308352 |
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| author | Anna J. Jasinska Cristian Apetrei Cristian Apetrei Ivona Pandrea Ivona Pandrea |
| author_facet | Anna J. Jasinska Cristian Apetrei Cristian Apetrei Ivona Pandrea Ivona Pandrea |
| author_sort | Anna J. Jasinska |
| collection | DOAJ |
| description | HIV emerged following cross-species transmissions of simian immunodeficiency viruses (SIVs) that naturally infect non-human primates (NHPs) from Africa. While HIV replication and CD4+ T-cell depletion lead to increased gut permeability, microbial translocation, chronic immune activation, and systemic inflammation, the natural hosts of SIVs generally avoid these deleterious consequences when infected with their species-specific SIVs and do not progress to AIDS despite persistent lifelong high viremia due to long-term coevolution with their SIV pathogens. The benign course of natural SIV infection in the natural hosts is in stark contrast to the experimental SIV infection of Asian macaques, which progresses to simian AIDS. The mechanisms of non-pathogenic SIV infections are studied mainly in African green monkeys, sooty mangabeys, and mandrills, while progressing SIV infection is experimentally modeled in macaques: rhesus macaques, pigtailed macaques, and cynomolgus macaques. Here, we focus on the distinctive features of SIV infection in natural hosts, particularly (1): the superior healing properties of the intestinal mucosa, which enable them to maintain the integrity of the gut barrier and prevent microbial translocation, thus avoiding excessive/pathologic immune activation and inflammation usually perpetrated by the leaking of the microbial products into the circulation; (2) the gut microbiome, the disruption of which is an important factor in some inflammatory diseases, yet not completely understood in the course of lentiviral infection; (3) cell population shifts resulting in target cell restriction (downregulation of CD4 or CCR5 surface molecules that bind to SIV), control of viral replication in the lymph nodes (expansion of natural killer cells), and anti-inflammatory effects in the gut (NKG2a/c+ CD8+ T cells); and (4) the genes and biological pathways that can shape genetic adaptations to viral pathogens and are associated with the non-pathogenic outcome of the natural SIV infection. Deciphering the protective mechanisms against SIV disease progression to immunodeficiency, which have been established through long-term coevolution between the natural hosts and their species-specific SIVs, may prompt the development of novel therapeutic interventions, such as drugs that can control gut inflammation, enhance gut healing capacities, or modulate the gut microbiome. These developments can go beyond HIV infection and open up large avenues for correcting gut damage, which is common in many diseases. |
| first_indexed | 2024-04-10T23:31:31Z |
| format | Article |
| id | doaj.art-34308034eb9346b1acc7526616a6af2d |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-10T23:31:31Z |
| publishDate | 2023-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-34308034eb9346b1acc7526616a6af2d2023-01-12T06:11:21ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-01-011310.3389/fimmu.2022.10609851060985Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratoryAnna J. Jasinska0Cristian Apetrei1Cristian Apetrei2Ivona Pandrea3Ivona Pandrea4Division of Infectious Diseases, Department of Medicine (DOM), School of Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesDivision of Infectious Diseases, Department of Medicine (DOM), School of Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Infectious Diseases and Immunology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Infectious Diseases and Immunology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Pathology, School of Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesHIV emerged following cross-species transmissions of simian immunodeficiency viruses (SIVs) that naturally infect non-human primates (NHPs) from Africa. While HIV replication and CD4+ T-cell depletion lead to increased gut permeability, microbial translocation, chronic immune activation, and systemic inflammation, the natural hosts of SIVs generally avoid these deleterious consequences when infected with their species-specific SIVs and do not progress to AIDS despite persistent lifelong high viremia due to long-term coevolution with their SIV pathogens. The benign course of natural SIV infection in the natural hosts is in stark contrast to the experimental SIV infection of Asian macaques, which progresses to simian AIDS. The mechanisms of non-pathogenic SIV infections are studied mainly in African green monkeys, sooty mangabeys, and mandrills, while progressing SIV infection is experimentally modeled in macaques: rhesus macaques, pigtailed macaques, and cynomolgus macaques. Here, we focus on the distinctive features of SIV infection in natural hosts, particularly (1): the superior healing properties of the intestinal mucosa, which enable them to maintain the integrity of the gut barrier and prevent microbial translocation, thus avoiding excessive/pathologic immune activation and inflammation usually perpetrated by the leaking of the microbial products into the circulation; (2) the gut microbiome, the disruption of which is an important factor in some inflammatory diseases, yet not completely understood in the course of lentiviral infection; (3) cell population shifts resulting in target cell restriction (downregulation of CD4 or CCR5 surface molecules that bind to SIV), control of viral replication in the lymph nodes (expansion of natural killer cells), and anti-inflammatory effects in the gut (NKG2a/c+ CD8+ T cells); and (4) the genes and biological pathways that can shape genetic adaptations to viral pathogens and are associated with the non-pathogenic outcome of the natural SIV infection. Deciphering the protective mechanisms against SIV disease progression to immunodeficiency, which have been established through long-term coevolution between the natural hosts and their species-specific SIVs, may prompt the development of novel therapeutic interventions, such as drugs that can control gut inflammation, enhance gut healing capacities, or modulate the gut microbiome. These developments can go beyond HIV infection and open up large avenues for correcting gut damage, which is common in many diseases.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1060985/fullAIDS - acquired immunodeficiency syndromeHIV - human immunodeficiency virusnonhuman primate (NHP)African green monkey (AGM) (Chlorocebus aethiops)mucosal immune barrierinflammation |
| spellingShingle | Anna J. Jasinska Cristian Apetrei Cristian Apetrei Ivona Pandrea Ivona Pandrea Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory Frontiers in Immunology AIDS - acquired immunodeficiency syndrome HIV - human immunodeficiency virus nonhuman primate (NHP) African green monkey (AGM) (Chlorocebus aethiops) mucosal immune barrier inflammation |
| title | Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory |
| title_full | Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory |
| title_fullStr | Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory |
| title_full_unstemmed | Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory |
| title_short | Walk on the wild side: SIV infection in African non-human primate hosts—from the field to the laboratory |
| title_sort | walk on the wild side siv infection in african non human primate hosts from the field to the laboratory |
| topic | AIDS - acquired immunodeficiency syndrome HIV - human immunodeficiency virus nonhuman primate (NHP) African green monkey (AGM) (Chlorocebus aethiops) mucosal immune barrier inflammation |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1060985/full |
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