The Capsids of HIV-1 and HIV-2 Determine Immune Detection of the Viral cDNA by the Innate Sensor cGAS in Dendritic Cells

HIV-2 is less pathogenic for humans than HIV-1 and might provide partial cross-protection from HIV-1-induced pathology. Although both viruses replicate in the T cells of infected patients, only HIV-2 replicates efficiently in dendritic cells (DCs) and activates innate immune pathways. How HIV is sen...

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Published in	Immunity (Cambridge, Mass.) Vol. 39; no. 6; pp. 1132 - 1142
Main Authors	Lahaye, Xavier, Satoh, Takeshi, Gentili, Matteo, Cerboni, Silvia, Conrad, Cécile, Hurbain, Ilse, El Marjou, Ahmed, Lacabaratz, Christine, Lelièvre, Jean-Daniel, Manel, Nicolas
Format	Journal Article
Language	English
Published	United States Elsevier Inc 12.12.2013 Elsevier Limited Elsevier
Subjects	Biochemistry, Molecular Biology Capsid Capsid - immunology Cells, Cultured Dendritic Cells Dendritic Cells - immunology Dendritic Cells - virology DNA, Complementary DNA, Complementary - metabolism DNA, Viral DNA, Viral - metabolism Experiments HIV Infections HIV Infections - immunology HIV Infections - virology HIV-1 HIV-1 - genetics HIV-1 - immunology HIV-1 - metabolism HIV-2 HIV-2 - genetics HIV-2 - immunology HIV-2 - metabolism Human immunodeficiency virus 1 Human immunodeficiency virus 2 Humans Immune system Immunity, Innate Immunity, Innate - physiology Infections Life Sciences Lymphocytes Microscopy Models, Biological Nucleotidyltransferases Nucleotidyltransferases - metabolism Proteins
Online Access	Get full text
ISSN	1074-7613 1097-4180 1097-4180
DOI	10.1016/j.immuni.2013.11.002

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Abstract	HIV-2 is less pathogenic for humans than HIV-1 and might provide partial cross-protection from HIV-1-induced pathology. Although both viruses replicate in the T cells of infected patients, only HIV-2 replicates efficiently in dendritic cells (DCs) and activates innate immune pathways. How HIV is sensed in DC is unknown. Capsid-mutated HIV-2 revealed that sensing by the host requires viral cDNA synthesis, but not nuclear entry or genome integration. The HIV-1 capsid prevented viral cDNA sensing up to integration, allowing the virus to escape innate recognition. In contrast, DCs sensed capsid-mutated HIV-1 and enhanced stimulation of T cells in the absence of productive infection. Finally, we found that DC sensing of HIV-1 and HIV-2 required the DNA sensor cGAS. Thus, the HIV capsid is a determinant of innate sensing of the viral cDNA by cGAS in dendritic cells. This pathway might potentially be harnessed to develop effective vaccines against HIV-1. [Display omitted] •Human dendritic cells sense the cDNA of HIV-2 before integration•The HIV-1 capsid allows the virus to escape sensing of its cDNA by dendritic cells•Dendritic cells sense capsid-mutated HIV-1 without replication and stimulate T cells•The DNA sensor cGAS is essential in human dendritic cells for sensing HIV-1 and HIV-2
AbstractList	HIV-2 is less pathogenic for humans than HIV-1 and might provide partial cross-protection from HIV-1-induced pathology. Although both viruses replicate in the T cells of infected patients, only HIV-2 replicates efficiently in dendritic cells (DCs) and activates innate immune pathways. How HIV is sensed in DC is unknown. Capsid-mutated HIV-2 revealed that sensing by the host requires viral cDNA synthesis, but not nuclear entry or genome integration. The HIV-1 capsid prevented viral cDNA sensing up to integration, allowing the virus to escape innate recognition. In contrast, DCs sensed capsid-mutated HIV-1 and enhanced stimulation of T cells in the absence of productive infection. Finally, we found that DC sensing of HIV-1 and HIV-2 required the DNA sensor cGAS. Thus, the HIV capsid is a determinant of innate sensing of the viral cDNA by cGAS in dendritic cells. This pathway might potentially be harnessed to develop effective vaccines against HIV-1. HIV-2 is less pathogenic for humans than HIV-1 and might provide partial cross-protection from HIV-1-induced pathology. Although both viruses replicate in the T cells of infected patients, only HIV-2 replicates efficiently in dendritic cells (DCs) and activates innate immune pathways. How HIV is sensed in DC is unknown. Capsid-mutated HIV-2 revealed that sensing by the host requires viral cDNA synthesis, but not nuclear entry or genome integration. The HIV-1 capsid prevented viral cDNA sensing up to integration, allowing the virus to escape innate recognition. In contrast, DCs sensed capsid-mutated HIV-1 and enhanced stimulation of T cells in the absence of productive infection. Finally, we found that DC sensing of HIV-1 and HIV-2 required the DNA sensor cGAS. Thus, the HIV capsid is a determinant of innate sensing of the viral cDNA by cGAS in dendritic cells. This pathway might potentially be harnessed to develop effective vaccines against HIV-1. [Display omitted] •Human dendritic cells sense the cDNA of HIV-2 before integration•The HIV-1 capsid allows the virus to escape sensing of its cDNA by dendritic cells•Dendritic cells sense capsid-mutated HIV-1 without replication and stimulate T cells•The DNA sensor cGAS is essential in human dendritic cells for sensing HIV-1 and HIV-2 HIV-2 is less pathogenic for humans than HIV-1 and might provide partial cross-protection from HIV-1-induced pathology. Although both viruses replicate in the T cells of infected patients, only HIV-2 replicates efficiently in dendritic cells (DCs) and activates innate immune pathways. How HIV is sensed in DC is unknown. Capsid-mutated HIV-2 revealed that sensing by the host requires viral cDNA synthesis, but not nuclear entry or genome integration. The HIV-1 capsid prevented viral cDNA sensing up to integration, allowing the virus to escape innate recognition. In contrast, DCs sensed capsid-mutated HIV-1 and enhanced stimulation of T cells in the absence of productive infection. Finally, we found that DC sensing of HIV-1 and HIV-2 required the DNA sensor cGAS. Thus, the HIV capsid is a determinant of innate sensing of the viral cDNA by cGAS in dendritic cells. This pathway might potentially be harnessed to develop effective vaccines against HIV-1.HIV-2 is less pathogenic for humans than HIV-1 and might provide partial cross-protection from HIV-1-induced pathology. Although both viruses replicate in the T cells of infected patients, only HIV-2 replicates efficiently in dendritic cells (DCs) and activates innate immune pathways. How HIV is sensed in DC is unknown. Capsid-mutated HIV-2 revealed that sensing by the host requires viral cDNA synthesis, but not nuclear entry or genome integration. The HIV-1 capsid prevented viral cDNA sensing up to integration, allowing the virus to escape innate recognition. In contrast, DCs sensed capsid-mutated HIV-1 and enhanced stimulation of T cells in the absence of productive infection. Finally, we found that DC sensing of HIV-1 and HIV-2 required the DNA sensor cGAS. Thus, the HIV capsid is a determinant of innate sensing of the viral cDNA by cGAS in dendritic cells. This pathway might potentially be harnessed to develop effective vaccines against HIV-1.
Author	Satoh, Takeshi Hurbain, Ilse Conrad, Cécile El Marjou, Ahmed Gentili, Matteo Manel, Nicolas Lahaye, Xavier Cerboni, Silvia Lacabaratz, Christine Lelièvre, Jean-Daniel
Author_xml	– sequence: 1 givenname: Xavier surname: Lahaye fullname: Lahaye, Xavier organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 2 givenname: Takeshi surname: Satoh fullname: Satoh, Takeshi organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 3 givenname: Matteo surname: Gentili fullname: Gentili, Matteo organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 4 givenname: Silvia surname: Cerboni fullname: Cerboni, Silvia organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 5 givenname: Cécile surname: Conrad fullname: Conrad, Cécile organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 6 givenname: Ilse surname: Hurbain fullname: Hurbain, Ilse organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 7 givenname: Ahmed surname: El Marjou fullname: El Marjou, Ahmed organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France – sequence: 8 givenname: Christine surname: Lacabaratz fullname: Lacabaratz, Christine organization: INSERM U955, Vaccine Research Institute, Université Paris Est Créteil, Faculté de Médecine, 94010 Créteil, France – sequence: 9 givenname: Jean-Daniel surname: Lelièvre fullname: Lelièvre, Jean-Daniel organization: INSERM U955, Vaccine Research Institute, Université Paris Est Créteil, Faculté de Médecine, 94010 Créteil, France – sequence: 10 givenname: Nicolas surname: Manel fullname: Manel, Nicolas email: nicolas.manel@curie.fr organization: Institut Curie, 12 rue Lhomond, 75005 Paris, France
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24269171$$D View this record in MEDLINE/PubMed https://inserm.hal.science/inserm-00959028$$DView record in HAL
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SubjectTerms	Biochemistry, Molecular Biology Capsid Capsid - immunology Cells, Cultured Dendritic Cells Dendritic Cells - immunology Dendritic Cells - virology DNA, Complementary DNA, Complementary - metabolism DNA, Viral DNA, Viral - metabolism Experiments HIV Infections HIV Infections - immunology HIV Infections - virology HIV-1 HIV-1 - genetics HIV-1 - immunology HIV-1 - metabolism HIV-2 HIV-2 - genetics HIV-2 - immunology HIV-2 - metabolism Human immunodeficiency virus 1 Human immunodeficiency virus 2 Humans Immune system Immunity, Innate Immunity, Innate - physiology Infections Life Sciences Lymphocytes Microscopy Models, Biological Nucleotidyltransferases Nucleotidyltransferases - metabolism Proteins
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Title	The Capsids of HIV-1 and HIV-2 Determine Immune Detection of the Viral cDNA by the Innate Sensor cGAS in Dendritic Cells
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