publication . Article . 2017

RIG-I/MAVS and STING signaling promote gut integrity during irradiation- and immune-mediated tissue injury

Alexander Wintges; Ulrich Kalinke; Hendrik Poeck; Hendrik Poeck; Gabriel Eisenkolb; Gabriel Eisenkolb; Stefan Lienenklaus; Melissa D. Docampo; Marcel R.M. van den Brink; Sebastien Monette; ...
Open Access
  • Published: 19 Apr 2017 Journal: Science Translational Medicine, volume 9, page eaag2513 (issn: 1946-6234, eissn: 1946-6242, Copyright policy)
  • Publisher: American Association for the Advancement of Science (AAAS)
  • Country: Germany
Abstract
The molecular pathways that regulate the tissue repair function of type I interferon (IFN-I) during acute tissue damage are poorly understood. We describe a protective role for IFN-I and the RIG-I/MAVS signaling pathway during acute tissue damage in mice. Mice lacking mitochondrial antiviral-signaling protein (MAVS) were more sensitive to total body irradiation- and chemotherapy-induced intestinal barrier damage. These mice developed worse graft-versus-host disease (GVHD) in a preclinical model of allogeneic hematopoietic stem cell transplantation (allo-HSCT) than did wild-type mice. This phenotype was not associated with changes in the intestinal microbiota but...
Subjects
Medical Subject Headings: chemical and pharmacologic phenomenasurgical procedures, operative
free text keywords: General Medicine, Medicine(all), Journal Article, Article, Adaptor Proteins, Signal Transducing, Animals, DEAD Box Protein 58, Graft vs Host Disease, Hematopoietic Stem Cell Transplantation, Intestines, Membrane Proteins, Mice, Mice, Inbred C57BL, Mice, Knockout, Neutrophil Infiltration, Organoids, Polymerase Chain Reaction, Transplantation, Homologous, Immune system, RIG-I, Transplantation, Stimulator of interferon genes, Interferon, medicine.drug, medicine, Immunology, Sting, Signal transduction, Biology, Interferon type I
Funded by
EC| CBM-INNATE
Project
CBM-INNATE
Regulation and Function of CARD9 / BCL10 / MALT1 Signalosomes in Innate Immunity and Inflammation
  • Funder: European Commission (EC)
  • Project Code: 322865
  • Funding stream: FP7 | SP2 | ERC
,
NIH| Strategies to Enhance Lymphoid Recovery After Radiation-Induced Injury
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI080455-02
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Mucosal Immunity and Microbiota in Intestinal Graft-versus-Host Disease
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 9R01AI100288-06A1
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Strategies to enhance immune reconstitution after bone marrow transplant
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01HL069929-12
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
,
NIH| MARROW TRANSPLANTATION IN LEUKEMIA AND OTHER DISEASES
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5P01CA023766-14
  • Funding stream: NATIONAL CANCER INSTITUTE
45 references, page 1 of 3

Abdullah, Z, Schlee, M, Roth, S, Mraheil, MA, Barchet, W, Böttcher, J, Hain, T, Geiger, S, Hayakawa, Y, Fritz, JH, Civril, F, Hopfner, KP, Kurts, C, Ruland, J, Hartmann, G, Chakraborty, T, Knolle, PA. RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 2012; 31: 4153-4164 [OpenAIRE] [PubMed]

Hornung, V, Ellegast, J, Kim, S, Brzozka, K, Jung, A, Kato, H, Poeck, H, Akira, S, Conzelmann, KK, Schlee, M, Endres, S, Hartmann, G. 5′-Triphosphate RNA is the ligand for RIG-I. Science. 2006; 314: 994-997 [OpenAIRE] [PubMed]

Pichlmair, A, Schulz, O, Tan, CP, Näslund, TI, Liljeström, P, Weber, F, Reis e Sousa, C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science. 2006; 314: 997-1001 [PubMed]

Barber, GN. STING-dependent cytosolic DNA sensing pathways. Trends Immunol. 2014; 35: 88-93 [PubMed]

Poeck, H, Bscheider, M, Gross, O, Finger, K, Roth, S, Rebsamen, M, Hannesschläger, N, Schlee, M, Rothenfusser, S, Barchet, W, Kato, H, Akira, S, Inoue, S, Endres, S, Peschel, C, Hartmann, G, Hornung, V, Ruland, J. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1b production. Nat Immunol. 2010; 11: 63-69 [PubMed]

Yoneyama, M, Onomoto, K, Jogi, M, Akaboshi, T, Fujita, T. Viral RNA detection by RIG-I-like receptors. Curr Opin Immunol. 2015; 32: 48-53 [OpenAIRE] [PubMed]

Pothlichet, J, Meunier, I, Davis, BK, Ting, JPY, Skamene, E, von Messling, V, Vidal, SM. Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLOS Pathog. 2013; 9: e1003256 [OpenAIRE] [PubMed]

Franchi, L, Eigenbrod, T, Muñoz-Planillo, R, Ozkurede, U, Kim, YG, Chakrabarti, A, Gale, M, Silverman, RH, Colonna, M, Akira, S, Nuñez, G. Cytosolic double-stranded RNA activates the NLRP3 inflammasome via MAVS-induced membrane permeabilization and K+ efflux. J Immunol. 2014; 193: 4214-4222 [OpenAIRE] [PubMed]

Gregorio, J, Meller, S, Conrad, C, Di Nardo, A, Homey, B, Lauerma, A, Arai, N, Gallo, RL, Digiovanni, J, Gilliet, M. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med. 2010; 207: 2921-2930 [OpenAIRE] [PubMed]

Sun, L, Miyoshi, H, Origanti, S, Nice, TJ, Barger, AC, Manieri, NA, Fogel, LA, French, AR, Piwnica-Worms, D, Piwnica-Worms, H, Virgin, HW, Lenschow, DJ, Stappenbeck, TS. Type I interferons link viral infection to enhanced epithelial turnover and repair. Cell Host Microbe. 2015; 17: 85-97 [OpenAIRE] [PubMed]

Yang, JY, Kim, MS, Kim, E, Cheon, JH, Lee, YS, Kim, Y, Lee, SH, Seo, SU, Shin, SH, Choi, SS, Kim, B, Chang, SY, Ko, HJ, Bae, JW, Kweon, MN. Enteric viruses ameliorate gut inflammation via toll-like receptor 3 and toll-like receptor 7-mediated interferon-β production. Immunity. 2016; 44: 889-900 [OpenAIRE] [PubMed]

Peterson, LW, Artis, D. Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nat Rev Immunol. 2014; 14: 141-153 [OpenAIRE] [PubMed]

Heidegger, S, van den Brink, MRM, Haas, T, Poeck, H. The role of pattern-recognition receptors in graft-versus-host disease and graft-versus-leukemia after allogeneic stem cell transplantation. Front Immunol. 2014; 5: 337 [OpenAIRE] [PubMed]

Blazar, BR, Murphy, WJ, Abedi, M. Advances in graft-versus-host disease biology and therapy. Nat Rev Immunol. 2012; 12: 443-458 [OpenAIRE] [PubMed]

Jenq, RR, van den Brink, MRM. Allogeneic haematopoietic stem cell transplantation: Individualized stem cell and immune therapy of cancer. Nat Rev Cancer. 2010; 10: 213-221 [PubMed]

45 references, page 1 of 3
Abstract
The molecular pathways that regulate the tissue repair function of type I interferon (IFN-I) during acute tissue damage are poorly understood. We describe a protective role for IFN-I and the RIG-I/MAVS signaling pathway during acute tissue damage in mice. Mice lacking mitochondrial antiviral-signaling protein (MAVS) were more sensitive to total body irradiation- and chemotherapy-induced intestinal barrier damage. These mice developed worse graft-versus-host disease (GVHD) in a preclinical model of allogeneic hematopoietic stem cell transplantation (allo-HSCT) than did wild-type mice. This phenotype was not associated with changes in the intestinal microbiota but...
Subjects
Medical Subject Headings: chemical and pharmacologic phenomenasurgical procedures, operative
free text keywords: General Medicine, Medicine(all), Journal Article, Article, Adaptor Proteins, Signal Transducing, Animals, DEAD Box Protein 58, Graft vs Host Disease, Hematopoietic Stem Cell Transplantation, Intestines, Membrane Proteins, Mice, Mice, Inbred C57BL, Mice, Knockout, Neutrophil Infiltration, Organoids, Polymerase Chain Reaction, Transplantation, Homologous, Immune system, RIG-I, Transplantation, Stimulator of interferon genes, Interferon, medicine.drug, medicine, Immunology, Sting, Signal transduction, Biology, Interferon type I
Funded by
EC| CBM-INNATE
Project
CBM-INNATE
Regulation and Function of CARD9 / BCL10 / MALT1 Signalosomes in Innate Immunity and Inflammation
  • Funder: European Commission (EC)
  • Project Code: 322865
  • Funding stream: FP7 | SP2 | ERC
,
NIH| Strategies to Enhance Lymphoid Recovery After Radiation-Induced Injury
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01AI080455-02
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Mucosal Immunity and Microbiota in Intestinal Graft-versus-Host Disease
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 9R01AI100288-06A1
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Strategies to enhance immune reconstitution after bone marrow transplant
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01HL069929-12
  • Funding stream: NATIONAL HEART, LUNG, AND BLOOD INSTITUTE
,
NIH| MARROW TRANSPLANTATION IN LEUKEMIA AND OTHER DISEASES
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5P01CA023766-14
  • Funding stream: NATIONAL CANCER INSTITUTE
45 references, page 1 of 3

Abdullah, Z, Schlee, M, Roth, S, Mraheil, MA, Barchet, W, Böttcher, J, Hain, T, Geiger, S, Hayakawa, Y, Fritz, JH, Civril, F, Hopfner, KP, Kurts, C, Ruland, J, Hartmann, G, Chakraborty, T, Knolle, PA. RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 2012; 31: 4153-4164 [OpenAIRE] [PubMed]

Hornung, V, Ellegast, J, Kim, S, Brzozka, K, Jung, A, Kato, H, Poeck, H, Akira, S, Conzelmann, KK, Schlee, M, Endres, S, Hartmann, G. 5′-Triphosphate RNA is the ligand for RIG-I. Science. 2006; 314: 994-997 [OpenAIRE] [PubMed]

Pichlmair, A, Schulz, O, Tan, CP, Näslund, TI, Liljeström, P, Weber, F, Reis e Sousa, C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science. 2006; 314: 997-1001 [PubMed]

Barber, GN. STING-dependent cytosolic DNA sensing pathways. Trends Immunol. 2014; 35: 88-93 [PubMed]

Poeck, H, Bscheider, M, Gross, O, Finger, K, Roth, S, Rebsamen, M, Hannesschläger, N, Schlee, M, Rothenfusser, S, Barchet, W, Kato, H, Akira, S, Inoue, S, Endres, S, Peschel, C, Hartmann, G, Hornung, V, Ruland, J. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1b production. Nat Immunol. 2010; 11: 63-69 [PubMed]

Yoneyama, M, Onomoto, K, Jogi, M, Akaboshi, T, Fujita, T. Viral RNA detection by RIG-I-like receptors. Curr Opin Immunol. 2015; 32: 48-53 [OpenAIRE] [PubMed]

Pothlichet, J, Meunier, I, Davis, BK, Ting, JPY, Skamene, E, von Messling, V, Vidal, SM. Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLOS Pathog. 2013; 9: e1003256 [OpenAIRE] [PubMed]

Franchi, L, Eigenbrod, T, Muñoz-Planillo, R, Ozkurede, U, Kim, YG, Chakrabarti, A, Gale, M, Silverman, RH, Colonna, M, Akira, S, Nuñez, G. Cytosolic double-stranded RNA activates the NLRP3 inflammasome via MAVS-induced membrane permeabilization and K+ efflux. J Immunol. 2014; 193: 4214-4222 [OpenAIRE] [PubMed]

Gregorio, J, Meller, S, Conrad, C, Di Nardo, A, Homey, B, Lauerma, A, Arai, N, Gallo, RL, Digiovanni, J, Gilliet, M. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med. 2010; 207: 2921-2930 [OpenAIRE] [PubMed]

Sun, L, Miyoshi, H, Origanti, S, Nice, TJ, Barger, AC, Manieri, NA, Fogel, LA, French, AR, Piwnica-Worms, D, Piwnica-Worms, H, Virgin, HW, Lenschow, DJ, Stappenbeck, TS. Type I interferons link viral infection to enhanced epithelial turnover and repair. Cell Host Microbe. 2015; 17: 85-97 [OpenAIRE] [PubMed]

Yang, JY, Kim, MS, Kim, E, Cheon, JH, Lee, YS, Kim, Y, Lee, SH, Seo, SU, Shin, SH, Choi, SS, Kim, B, Chang, SY, Ko, HJ, Bae, JW, Kweon, MN. Enteric viruses ameliorate gut inflammation via toll-like receptor 3 and toll-like receptor 7-mediated interferon-β production. Immunity. 2016; 44: 889-900 [OpenAIRE] [PubMed]

Peterson, LW, Artis, D. Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nat Rev Immunol. 2014; 14: 141-153 [OpenAIRE] [PubMed]

Heidegger, S, van den Brink, MRM, Haas, T, Poeck, H. The role of pattern-recognition receptors in graft-versus-host disease and graft-versus-leukemia after allogeneic stem cell transplantation. Front Immunol. 2014; 5: 337 [OpenAIRE] [PubMed]

Blazar, BR, Murphy, WJ, Abedi, M. Advances in graft-versus-host disease biology and therapy. Nat Rev Immunol. 2012; 12: 443-458 [OpenAIRE] [PubMed]

Jenq, RR, van den Brink, MRM. Allogeneic haematopoietic stem cell transplantation: Individualized stem cell and immune therapy of cancer. Nat Rev Cancer. 2010; 10: 213-221 [PubMed]

45 references, page 1 of 3
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