Biology of Zika Virus Infection in Human Skin Cells
Zika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that causes a mosquito-borne disease transmitted by the Aedes genus, with recent outbreaks in the South Pacific. Here we examine the importance of...
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| Published in | Journal of virology Vol. 89; no. 17; pp. 8880 - 8896 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Society for Microbiology
01.09.2015
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Zika virus (ZIKV) is an emerging arbovirus of the
Flaviviridae
family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that causes a mosquito-borne disease transmitted by the
Aedes
genus, with recent outbreaks in the South Pacific. Here we examine the importance of human skin in the entry of ZIKV and its contribution to the induction of antiviral immune responses. We show that human dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells are permissive to the most recent ZIKV isolate, responsible for the epidemic in French Polynesia. Several entry and/or adhesion factors, including DC-SIGN, AXL, Tyro3, and, to a lesser extent, TIM-1, permitted ZIKV entry, with a major role for the TAM receptor AXL. The ZIKV permissiveness of human skin fibroblasts was confirmed by the use of a neutralizing antibody and specific RNA silencing. ZIKV induced the transcription of Toll-like receptor 3 (TLR3), RIG-I, and MDA5, as well as several interferon-stimulated genes, including OAS2, ISG15, and MX1, characterized by strongly enhanced beta interferon gene expression. ZIKV was found to be sensitive to the antiviral effects of both type I and type II interferons. Finally, infection of skin fibroblasts resulted in the formation of autophagosomes, whose presence was associated with enhanced viral replication, as shown by the use of Torin 1, a chemical inducer of autophagy, and the specific autophagy inhibitor 3-methyladenine. The results presented herein permit us to gain further insight into the biology of ZIKV and to devise strategies aiming to interfere with the pathology caused by this emerging flavivirus.
IMPORTANCE
Zika virus (ZIKV) is an arbovirus belonging to the
Flaviviridae
family. Vector-mediated transmission of ZIKV is initiated when a blood-feeding female
Aedes
mosquito injects the virus into the skin of its mammalian host, followed by infection of permissive cells via specific receptors. Indeed, skin immune cells, including dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells, were all found to be permissive to ZIKV infection. The results also show a major role for the phosphatidylserine receptor AXL as a ZIKV entry receptor and for cellular autophagy in enhancing ZIKV replication in permissive cells. ZIKV replication leads to activation of an antiviral innate immune response and the production of type I interferons in infected cells. Taken together, these results provide the first general insights into the interaction between ZIKV and its mammalian host. |
|---|---|
| AbstractList | UNLABELLEDZika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that causes a mosquito-borne disease transmitted by the Aedes genus, with recent outbreaks in the South Pacific. Here we examine the importance of human skin in the entry of ZIKV and its contribution to the induction of antiviral immune responses. We show that human dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells are permissive to the most recent ZIKV isolate, responsible for the epidemic in French Polynesia. Several entry and/or adhesion factors, including DC-SIGN, AXL, Tyro3, and, to a lesser extent, TIM-1, permitted ZIKV entry, with a major role for the TAM receptor AXL. The ZIKV permissiveness of human skin fibroblasts was confirmed by the use of a neutralizing antibody and specific RNA silencing. ZIKV induced the transcription of Toll-like receptor 3 (TLR3), RIG-I, and MDA5, as well as several interferon-stimulated genes, including OAS2, ISG15, and MX1, characterized by strongly enhanced beta interferon gene expression. ZIKV was found to be sensitive to the antiviral effects of both type I and type II interferons. Finally, infection of skin fibroblasts resulted in the formation of autophagosomes, whose presence was associated with enhanced viral replication, as shown by the use of Torin 1, a chemical inducer of autophagy, and the specific autophagy inhibitor 3-methyladenine. The results presented herein permit us to gain further insight into the biology of ZIKV and to devise strategies aiming to interfere with the pathology caused by this emerging flavivirus.IMPORTANCEZika virus (ZIKV) is an arbovirus belonging to the Flaviviridae family. Vector-mediated transmission of ZIKV is initiated when a blood-feeding female Aedes mosquito injects the virus into the skin of its mammalian host, followed by infection of permissive cells via specific receptors. Indeed, skin immune cells, including dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells, were all found to be permissive to ZIKV infection. The results also show a major role for the phosphatidylserine receptor AXL as a ZIKV entry receptor and for cellular autophagy in enhancing ZIKV replication in permissive cells. ZIKV replication leads to activation of an antiviral innate immune response and the production of type I interferons in infected cells. Taken together, these results provide the first general insights into the interaction between ZIKV and its mammalian host. Zika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that causes a mosquito-borne disease transmitted by the Aedes genus, with recent outbreaks in the South Pacific. Here we examine the importance of human skin in the entry of ZIKV and its contribution to the induction of antiviral immune responses. We show that human dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells are permissive to the most recent ZIKV isolate, responsible for the epidemic in French Polynesia. Several entry and/or adhesion factors, including DC-SIGN, AXL, Tyro3, and, to a lesser extent, TIM-1, permitted ZIKV entry, with a major role for the TAM receptor AXL. The ZIKV permissiveness of human skin fibroblasts was confirmed by the use of a neutralizing antibody and specific RNA silencing. ZIKV induced the transcription of Toll-like receptor 3 (TLR3), RIG-I, and MDA5, as well as several interferon-stimulated genes, including OAS2, ISG15, and MX1, characterized by strongly enhanced beta interferon gene expression. ZIKV was found to be sensitive to the antiviral effects of both type I and type II interferons. Finally, infection of skin fibroblasts resulted in the formation of autophagosomes, whose presence was associated with enhanced viral replication, as shown by the use of Torin 1, a chemical inducer of autophagy, and the specific autophagy inhibitor 3-methyladenine. The results presented herein permit us to gain further insight into the biology of ZIKV and to devise strategies aiming to interfere with the pathology caused by this emerging flavivirus. Zika virus (ZIKV) is an arbovirus belonging to the Flaviviridae family. Vector-mediated transmission of ZIKV is initiated when a blood-feeding female Aedes mosquito injects the virus into the skin of its mammalian host, followed by infection of permissive cells via specific receptors. Indeed, skin immune cells, including dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells, were all found to be permissive to ZIKV infection. The results also show a major role for the phosphatidylserine receptor AXL as a ZIKV entry receptor and for cellular autophagy in enhancing ZIKV replication in permissive cells. ZIKV replication leads to activation of an antiviral innate immune response and the production of type I interferons in infected cells. Taken together, these results provide the first general insights into the interaction between ZIKV and its mammalian host. Zika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that causes a mosquito-borne disease transmitted by the Aedes genus, with recent outbreaks in the South Pacific. Here we examine the importance of human skin in the entry of ZIKV and its contribution to the induction of antiviral immune responses. We show that human dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells are permissive to the most recent ZIKV isolate, responsible for the epidemic in French Polynesia. Several entry and/or adhesion factors, including DC-SIGN, AXL, Tyro3, and, to a lesser extent, TIM-1, permitted ZIKV entry, with a major role for the TAM receptor AXL. The ZIKV permissiveness of human skin fibroblasts was confirmed by the use of a neutralizing antibody and specific RNA silencing. ZIKV induced the transcription of Toll-like receptor 3 (TLR3), RIG-I, and MDA5, as well as several interferon-stimulated genes, including OAS2, ISG15, and MX1, characterized by strongly enhanced beta interferon gene expression. ZIKV was found to be sensitive to the antiviral effects of both type I and type II interferons. Finally, infection of skin fibroblasts resulted in the formation of autophagosomes, whose presence was associated with enhanced viral replication, as shown by the use of Torin 1, a chemical inducer of autophagy, and the specific autophagy inhibitor 3-methyladenine. The results presented herein permit us to gain further insight into the biology of ZIKV and to devise strategies aiming to interfere with the pathology caused by this emerging flavivirus. IMPORTANCE Zika virus (ZIKV) is an arbovirus belonging to the Flaviviridae family. Vector-mediated transmission of ZIKV is initiated when a blood-feeding female Aedes mosquito injects the virus into the skin of its mammalian host, followed by infection of permissive cells via specific receptors. Indeed, skin immune cells, including dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells, were all found to be permissive to ZIKV infection. The results also show a major role for the phosphatidylserine receptor AXL as a ZIKV entry receptor and for cellular autophagy in enhancing ZIKV replication in permissive cells. ZIKV replication leads to activation of an antiviral innate immune response and the production of type I interferons in infected cells. Taken together, these results provide the first general insights into the interaction between ZIKV and its mammalian host. Zika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that causes a mosquito-borne disease transmitted by the Aedes genus, with recent outbreaks in the South Pacific. Here we examine the importance of human skin in the entry of ZIKV and its contribution to the induction of antiviral immune responses. We show that human dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells are permissive to the most recent ZIKV isolate, responsible for the epidemic in French Polynesia. Several entry and/or adhesion factors, including DC-SIGN, AXL, Tyro3, and, to a lesser extent, TIM-1, permitted ZIKV entry, with a major role for the TAM receptor AXL. The ZIKV permissiveness of human skin fibroblasts was confirmed by the use of a neutralizing antibody and specific RNA silencing. ZIKV induced the transcription of Toll-like receptor 3 (TLR3), RIG-I, and MDA5, as well as several interferon-stimulated genes, including OAS2, ISG15, and MX1, characterized by strongly enhanced beta interferon gene expression. ZIKV was found to be sensitive to the antiviral effects of both type I and type II interferons. Finally, infection of skin fibroblasts resulted in the formation of autophagosomes, whose presence was associated with enhanced viral replication, as shown by the use of Torin 1, a chemical inducer of autophagy, and the specific autophagy inhibitor 3-methyladenine. The results presented herein permit us to gain further insight into the biology of ZIKV and to devise strategies aiming to interfere with the pathology caused by this emerging flavivirus. Zika virus (ZIKV) is an arbovirus belonging to the Flaviviridae family. Vector-mediated transmission of ZIKV is initiated when a blood-feeding female Aedes mosquito injects the virus into the skin of its mammalian host, followed by infection of permissive cells via specific receptors. Indeed, skin immune cells, including dermal fibroblasts, epidermal keratinocytes, and immature dendritic cells, were all found to be permissive to ZIKV infection. The results also show a major role for the phosphatidylserine receptor AXL as a ZIKV entry receptor and for cellular autophagy in enhancing ZIKV replication in permissive cells. ZIKV replication leads to activation of an antiviral innate immune response and the production of type I interferons in infected cells. Taken together, these results provide the first general insights into the interaction between ZIKV and its mammalian host. |
| Author | Luplertlop, Natthanej Surasombatpattana, Pornapat Amara, Ali Cao-Lormeau, Van-Mai Neyret, Aymeric Choumet, Valérie Missé, Dorothée Talignani, Loïc Thomas, Frédéric Perera-Lecoin, Manuel Desprès, Philippe Ekchariyawat, Peeraya Hamel, Rodolphe Dejarnac, Ophélie Wichit, Sineewanlaya Briant, Laurence Yssel, Hans |
| Author_xml | – sequence: 1 givenname: Rodolphe surname: Hamel fullname: Hamel, Rodolphe organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France – sequence: 2 givenname: Ophélie surname: Dejarnac fullname: Dejarnac, Ophélie organization: INSERM, U944, Laboratoire de Pathologie et Virologie Moléculaire, Paris, France – sequence: 3 givenname: Sineewanlaya surname: Wichit fullname: Wichit, Sineewanlaya organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France – sequence: 4 givenname: Peeraya surname: Ekchariyawat fullname: Ekchariyawat, Peeraya organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France – sequence: 5 givenname: Aymeric surname: Neyret fullname: Neyret, Aymeric organization: Centre d'Étude d'Agents Pathogènes et Biotechnologies pour la Santé, CNRS-UMR 5236/UM, Montpellier, France – sequence: 6 givenname: Natthanej surname: Luplertlop fullname: Luplertlop, Natthanej organization: Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand – sequence: 7 givenname: Manuel surname: Perera-Lecoin fullname: Perera-Lecoin, Manuel organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France – sequence: 8 givenname: Pornapat surname: Surasombatpattana fullname: Surasombatpattana, Pornapat organization: Pathology Department, Prince of Songkla University, Songkla, Thailand – sequence: 9 givenname: Loïc surname: Talignani fullname: Talignani, Loïc organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France – sequence: 10 givenname: Frédéric surname: Thomas fullname: Thomas, Frédéric organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France – sequence: 11 givenname: Van-Mai surname: Cao-Lormeau fullname: Cao-Lormeau, Van-Mai organization: Institut Louis Malardé, Papeete, Tahiti, French Polynesia – sequence: 12 givenname: Valérie surname: Choumet fullname: Choumet, Valérie organization: Environment and Infectious Risks Unit, Institut Pasteur, Paris, France – sequence: 13 givenname: Laurence surname: Briant fullname: Briant, Laurence organization: Centre d'Étude d'Agents Pathogènes et Biotechnologies pour la Santé, CNRS-UMR 5236/UM, Montpellier, France – sequence: 14 givenname: Philippe surname: Desprès fullname: Desprès, Philippe organization: Département Infections et Epidémiologie, Institut Pasteur, Paris, France, and UMR PIMIT (I2T Team), Université de La Réunion, INSERM U1187, CNRS 9192, IRD 249, GIP-CYROI, Saint Clotilde, La Réunion, France – sequence: 15 givenname: Ali surname: Amara fullname: Amara, Ali organization: INSERM, U944, Laboratoire de Pathologie et Virologie Moléculaire, Paris, France – sequence: 16 givenname: Hans surname: Yssel fullname: Yssel, Hans organization: Centre d'Immunologie et des Maladies Infectieuses, INSERM, U1135, Sorbonne Universités, UPMC, APHP Hôpital Pitié-Salpêtrière, Paris, France – sequence: 17 givenname: Dorothée surname: Missé fullname: Missé, Dorothée organization: Laboratoire MIVEGEC, UMR 224 IRD/CNRS/UM, Montpellier, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26085147$$D View this record in MEDLINE/PubMed https://hal.science/hal-01228435$$DView record in HAL |
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| Snippet | Zika virus (ZIKV) is an emerging arbovirus of the
Flaviviridae
family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that... Zika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis viruses, that... UNLABELLEDZika virus (ZIKV) is an emerging arbovirus of the Flaviviridae family, which includes dengue, West Nile, yellow fever, and Japanese encephalitis... |
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| SubjectTerms | Aedes Aedes - virology Animals Autophagy Autophagy - immunology Axl Receptor Tyrosine Kinase Biochemistry, Molecular Biology Cell Adhesion Molecules Cell Adhesion Molecules - genetics Cell Adhesion Molecules - metabolism Cells, Cultured Cellular Biology Chlorocebus aethiops Cytokines Cytokines - biosynthesis DEAD Box Protein 58 DEAD-Box RNA Helicases DEAD-box RNA Helicases - genetics DEAD-box RNA Helicases - metabolism Dendritic Cells Dendritic Cells - immunology Dendritic Cells - virology Fibroblasts Fibroblasts - virology Flaviviridae Flaviviridae - immunology Flaviviridae - physiology Flaviviridae Infections Flaviviridae Infections - immunology Flaviviridae Infections - virology HEK293 Cells Hepatitis A VIrus Cellular Receptor 1 Humans Insect Vectors Insect Vectors - virology Interferon-beta Interferon-beta - biosynthesis Interferon-beta - immunology Interferon-Induced Helicase, IFIH1 Keratinocytes Keratinocytes - virology Lectins, C-Type Lectins, C-Type - genetics Lectins, C-Type - metabolism Life Sciences Membrane Glycoproteins Membrane Glycoproteins - genetics Membrane Glycoproteins - metabolism Microbiology and Parasitology Myxovirus Resistance Proteins Myxovirus Resistance Proteins - biosynthesis Phagosomes Phagosomes - immunology Proto-Oncogene Proteins Proto-Oncogene Proteins - genetics Proto-Oncogene Proteins - metabolism Receptor Protein-Tyrosine Kinases Receptor Protein-Tyrosine Kinases - genetics Receptor Protein-Tyrosine Kinases - metabolism Receptors, Cell Surface Receptors, Cell Surface - genetics Receptors, Cell Surface - metabolism Receptors, Immunologic Receptors, Virus Receptors, Virus - genetics Receptors, Virus - metabolism RNA Interference RNA, Small Interfering Skin Skin - immunology Skin - virology Toll-Like Receptor 3 Toll-Like Receptor 3 - genetics Toll-Like Receptor 3 - immunology Toll-Like Receptor 3 - metabolism Toll-Like Receptor 7 Toll-Like Receptor 7 - immunology Ubiquitins Ubiquitins - biosynthesis Vero Cells Virology Virus Internalization Virus Replication Virus-Cell Interactions |
| Title | Biology of Zika Virus Infection in Human Skin Cells |
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