RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection
Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection of virus and for mounting a cascade of defense measures which include the production of type 1 interferon (IFN). Hence, a thorough understan...
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| Published in | PLoS neglected tropical diseases Vol. 5; no. 1; p. e926 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
04.01.2011
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection of virus and for mounting a cascade of defense measures which include the production of type 1 interferon (IFN). Hence, a thorough understanding of the innate immune response during DV infection would be essential for our understanding of the DV pathogenesis. A recent application of the microarray to dengue virus type 1 (DV1) infected lung carcinoma cells revealed the increased expression of both extracellular and cytoplasmic pattern recognition receptors; retinoic acid inducible gene-I (RIG-I), melanoma differentiation associated gene-5 (MDA-5) and Toll-like receptor-3 (TLR3). These intracellular RNA sensors were previously reported to sense DV infection in different cells. In this study, we show that they are collectively involved in initiating an effective IFN production against DV. Cells silenced for these genes were highly susceptible to DV infection. RIG-I and MDA5 knockdown HUH-7 cells and TLR3 knockout macrophages were highly susceptible to DV infection. When cells were silenced for only RIG-I and MDA5 (but not TLR3), substantial production of IFN-β was observed upon virus infection and vice versa. High susceptibility to virus infection led to ER-stress induced apoptosis in HUH-7 cells. Collectively, our studies demonstrate that the intracellular RNA virus sensors (RIG-I, MDA5 and TLR3) are activated upon DV infection and are essential for host defense against the virus. |
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| AbstractList | Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection of virus and for mounting a cascade of defense measures which include the production of type 1 interferon (IFN). Hence, a thorough understanding of the innate immune response during DV infection would be essential for our understanding of the DV pathogenesis. A recent application of the microarray to dengue virus type 1 (DV1) infected lung carcinoma cells revealed the increased expression of both extracellular and cytoplasmic pattern recognition receptors; retinoic acid inducible gene-I (RIG-I), melanoma differentiation associated gene-5 (MDA-5) and Toll-like receptor-3 (TLR3). These intracellular RNA sensors were previously reported to sense DV infection in different cells. In this study, we show that they are collectively involved in initiating an effective IFN production against DV. Cells silenced for these genes were highly susceptible to DV infection. RIG-I and MDA5 knockdown HUH-7 cells and TLR3 knockout macrophages were highly susceptible to DV infection. When cells were silenced for only RIG-I and MDA5 (but not TLR3), substantial production of IFN-β was observed upon virus infection and vice versa. High susceptibility to virus infection led to ER-stress induced apoptosis in HUH-7 cells. Collectively, our studies demonstrate that the intracellular RNA virus sensors (RIG-I, MDA5 and TLR3) are activated upon DV infection and are essential for host defense against the virus. Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection of virus and for mounting a cascade of defense measures which include the production of type 1 interferon (IFN). Hence, a thorough understanding of the innate immune response during DV infection would be essential for our understanding of the DV pathogenesis. A recent application of the microarray to dengue virus type 1 (DV1) infected lung carcinoma cells revealed the increased expression of both extracellular and cytoplasmic pattern recognition receptors; retinoic acid inducible gene-I (RIG-I), melanoma differentiation associated gene-5 (MDA-5) and Toll-like receptor-3 (TLR3). These intracellular RNA sensors were previously reported to sense DV infection in different cells. In this study, we show that they are collectively involved in initiating an effective IFN production against DV. Cells silenced for these genes were highly susceptible to DV infection. RIG-I and MDA5 knockdown HUH-7 cells and TLR3 knockout macrophages were highly susceptible to DV infection. When cells were silenced for only RIG-I and MDA5 (but not TLR3), substantial production of IFN- beta was observed upon virus infection and vice versa. High susceptibility to virus infection led to ER-stress induced apoptosis in HUH-7 cells. Collectively, our studies demonstrate that the intracellular RNA virus sensors (RIG-I, MDA5 and TLR3) are activated upon DV infection and are essential for host defense against the virus. Dengue fever, dengue haemmorhagic fever and dengue shock syndrome, which are caused by dengue virus infection, are a major public health problem in many parts of the world, especially South East Asia. The investigation of host cell transcriptional changes in response to virus infection using DNA microarray technology has been an area of great interest. In our previous study, we used microarray technology to study expression of individual human genes in relation to dengue virus infection. Most of the genes that were upregulated were type 1 interferon related genes. To gain a better understanding of the innate immune response to dengue virus, we knocked down RIG-I, MDA5 and TLR3 genes in HUH-7 cells. Silencing these genes using siRNA technology resulted in significant increase in viral replication. This increase in viral load induced ER stress leading to apoptosis. This study demonstrates a synergistic role for RIG-I, MDA5 and TLR3 in restricting dengue virus infection. Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection of virus and for mounting a cascade of defense measures which include the production of type 1 interferon (IFN). Hence, a thorough understanding of the innate immune response during DV infection would be essential for our understanding of the DV pathogenesis. A recent application of the microarray to dengue virus type 1 (DV1) infected lung carcinoma cells revealed the increased expression of both extracellular and cytoplasmic pattern recognition receptors; retinoic acid inducible gene-I (RIG-I), melanoma differentiation associated gene-5 (MDA-5) and Toll-like receptor-3 (TLR3). These intracellular RNA sensors were previously reported to sense DV infection in different cells. In this study, we show that they are collectively involved in initiating an effective IFN production against DV. Cells silenced for these genes were highly susceptible to DV infection. RIG-I and MDA5 knockdown HUH-7 cells and TLR3 knockout macrophages were highly susceptible to DV infection. When cells were silenced for only RIG-I and MDA5 (but not TLR3), substantial production of IFN-β was observed upon virus infection and vice versa. High susceptibility to virus infection led to ER-stress induced apoptosis in HUH-7 cells. Collectively, our studies demonstrate that the intracellular RNA virus sensors (RIG-I, MDA5 and TLR3) are activated upon DV infection and are essential for host defense against the virus. Dengue fever, dengue haemmorhagic fever and dengue shock syndrome, which are caused by dengue virus infection, are a major public health problem in many parts of the world, especially South East Asia. The investigation of host cell transcriptional changes in response to virus infection using DNA microarray technology has been an area of great interest. In our previous study, we used microarray technology to study expression of individual human genes in relation to dengue virus infection. Most of the genes that were upregulated were type 1 interferon related genes. To gain a better understanding of the innate immune response to dengue virus, we knocked down RIG-I, MDA5 and TLR3 genes in HUH-7 cells. Silencing these genes using siRNA technology resulted in significant increase in viral replication. This increase in viral load induced ER stress leading to apoptosis. This study demonstrates a synergistic role for RIG-I, MDA5 and TLR3 in restricting dengue virus infection. Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection of virus and for mounting a cascade of defense measures which include the production of type 1 interferon (IFN). Hence, a thorough understanding of the innate immune response during DV infection would be essential for our understanding of the DV pathogenesis. A recent application of the microarray to dengue virus type 1 (DV1) infected lung carcinoma cells revealed the increased expression of both extracellular and cytoplasmic pattern recognition receptors; retinoic acid inducible gene-I (RIG-I), melanoma differentiation associated gene-5 (MDA-5) and Toll-like receptor-3 (TLR3). These intracellular RNA sensors were previously reported to sense DV infection in different cells. In this study, we show that they are collectively involved in initiating an effective IFN production against DV. Cells silenced for these genes were highly susceptible to DV infection. RIG-I and MDA5 knockdown HUH-7 cells and TLR3 knockout macrophages were highly susceptible to DV infection. When cells were silenced for only RIG-I and MDA5 (but not TLR3), substantial production of IFN-β was observed upon virus infection and vice versa. High susceptibility to virus infection led to ER-stress induced apoptosis in HUH-7 cells. Collectively, our studies demonstrate that the intracellular RNA virus sensors (RIG-I, MDA5 and TLR3) are activated upon DV infection and are essential for host defense against the virus. |
| Author | Xu, Shengli Liu, Ding Xiang Wong, Hui Hui Thien, Peiling Nasirudeen, A M A Lam, Kong-Peng |
| AuthorAffiliation | University of California, Berkeley, United States of America 1 Institute of Molecular and Cell Biology, Singapore, Singapore 2 School of Biological Sciences, Nanyang Technological University, Singapore, Singapore 3 Immunology Group, Bioprocessing Technology Institute, Singapore, Singapore |
| AuthorAffiliation_xml | – name: 1 Institute of Molecular and Cell Biology, Singapore, Singapore – name: 2 School of Biological Sciences, Nanyang Technological University, Singapore, Singapore – name: 3 Immunology Group, Bioprocessing Technology Institute, Singapore, Singapore – name: University of California, Berkeley, United States of America |
| Author_xml | – sequence: 1 givenname: A M A surname: Nasirudeen fullname: Nasirudeen, A M A email: nasir@alumni.nus.edu.sg organization: Institute of Molecular and Cell Biology, Singapore, Singapore. nasir@alumni.nus.edu.sg – sequence: 2 givenname: Hui Hui surname: Wong fullname: Wong, Hui Hui – sequence: 3 givenname: Peiling surname: Thien fullname: Thien, Peiling – sequence: 4 givenname: Shengli surname: Xu fullname: Xu, Shengli – sequence: 5 givenname: Kong-Peng surname: Lam fullname: Lam, Kong-Peng – sequence: 6 givenname: Ding Xiang surname: Liu fullname: Liu, Ding Xiang |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21245912$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2011 Nasirudeen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Nasirudeen AMA, Wong HH, Thien P, Xu S, Lam K-P, et al. (2011) RIG-I, MDA5 and TLR3 Synergistically Play an Important Role in Restriction of Dengue Virus Infection. PLoS Negl Trop Dis 5(1): e926. doi:10.1371/journal.pntd.0000926 Nasirudeen et al. 2011 |
| Copyright_xml | – notice: 2011 Nasirudeen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Nasirudeen AMA, Wong HH, Thien P, Xu S, Lam K-P, et al. (2011) RIG-I, MDA5 and TLR3 Synergistically Play an Important Role in Restriction of Dengue Virus Infection. PLoS Negl Trop Dis 5(1): e926. doi:10.1371/journal.pntd.0000926 – notice: Nasirudeen et al. 2011 |
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| DOI | 10.1371/journal.pntd.0000926 |
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| DocumentTitleAlternate | Dengue Virus Signaling through RIG-I, MDA5, TLR3 |
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| Editor | Harris, Eva |
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| Keywords | Toll-Like Receptor 3 DEAD-box RNA Helicases Interferons Dengue Humans Mice, Inbred C57BL Cells, Cultured Gene Silencing Macrophages Reverse Transcriptase Polymerase Chain Reaction Dengue Virus Animals Hepatocytes Mice Apoptosis |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: AMAN DXL. Performed the experiments: AMAN HHW PT. Analyzed the data: AMAN HHW DXL. Contributed reagents/materials/analysis tools: AMAN HHW PT SX KPL. Wrote the paper: AMAN DXL. |
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| Snippet | Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early detection... Dengue virus (DV) infection is one of the most common mosquito-borne viral diseases in the world. The innate immune system is important for the early... |
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| SubjectTerms | Animals Apoptosis Cells, Cultured Cytokines DEAD Box Protein 58 DEAD-box RNA Helicases - immunology DEAD-box RNA Helicases - metabolism Dengue - immunology Dengue - pathology Dengue fever Dengue virus Dengue Virus - immunology Dengue Virus - pathogenicity Dengue virus type 1 Gene Silencing Genes Genetic engineering Hepatitis Hepatocytes - virology Humans Immune response Immune system Immunology/Cellular Microbiology and Pathogenesis Immunology/Immune Response Immunology/Immunity to Infections Immunology/Innate Immunity Infections Interferon Interferon-Induced Helicase, IFIH1 Interferons - immunology Interferons - metabolism Macrophages - virology Melanoma Mice Mice, Inbred C57BL Microbiology/Cellular Microbiology and Pathogenesis Microbiology/Innate Immunity Pattern recognition Receptors, Immunologic Reverse Transcriptase Polymerase Chain Reaction Sensors Toll-Like Receptor 3 - immunology Toll-Like Receptor 3 - metabolism Tropical diseases Vector-borne diseases Viral diseases Viral infections Viruses West Nile virus |
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| Title | RIG-I, MDA5 and TLR3 synergistically play an important role in restriction of dengue virus infection |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/21245912 https://www.proquest.com/docview/1288107190 https://search.proquest.com/docview/845765962 https://search.proquest.com/docview/876227394 https://pubmed.ncbi.nlm.nih.gov/PMC3014945 https://doaj.org/article/7889acaadf3c4bf9b2f4432587cbce2c http://dx.doi.org/10.1371/journal.pntd.0000926 |
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