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

Science Translational Medicine

Volumn 9, Issue 386, 2017, Pages

  Fischer, Julius C ^a   Bscheider, Michael ^a,k   Eisenkolb, Gabriel ^a,b   Lin, Chia Ching ^a   Wintges, Alexander ^a   Otten, Vera ^a   Lindemans, Caroline A ^b,c   Heidegger, Simon ^a   Rudelius, Martina ^d   Monette, Sébastien ^e   Rodriguez, Kori A Porosnicu ^b   Calafiore, Marco ^b   Liebermann, Sophie ^b   Liu, Chen ^f   Lienenklaus, Stefan ^g   Weiss, Siegfried ^h   Kalinke, Ulrich ^g   Ruland, Jürgen ^a,i,j   Peschel, Christian ^a   Shono, Yusuke ^b   Docampo, Melissa ^b,l   Velardi, Enrico ^b   Jenq, Robert R ^b   Hanash, Alan M ^b   Dudakov, Jarrod A ^b   Haas, Tobias ^a   Van Den Brink, Marcel R M ^b   Poeck, Hendrik ^a,b   more..

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e ROCKEFELLER UNIVERSITY   (United States)

^f RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^g HANNOVER MEDICAL SCHOOL   (Germany)

^h HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

ⁱ GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^j German Center for Cardiovascular Research   (Germany)

^k STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^l USA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

5' TRIPHOSPHATE RNA; ADAPTOR PROTEIN; INTERFERON; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; POLYPEPTIDE ANTIBIOTIC AGENT; REGENERATING ISLET DERIVED PROTEIN 3 GAMMA; RETINOIC ACID INDUCIBLE PROTEIN I; RNA DERIVATIVE; STING PROTEIN; UNCLASSIFIED DRUG; DDX58 PROTEIN, MOUSE; IPS-1 PROTEIN, MOUSE; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; EX VIVO STUDY; GRAFT VERSUS HOST REACTION; IMMUNE MEDIATED INJURY; IN VITRO STUDY; IN VIVO STUDY; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE INJURY; INTESTINE MUCOSA PERMEABILITY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RADIATION INJURY; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; WHOLE BODY RADIATION; ALLOTRANSPLANTATION; ANIMAL; C57BL MOUSE; CYTOLOGY; CYTOPLASM; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; INTESTINE; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RADIATION RESPONSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; DEAD BOX PROTEIN 58; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; INTERFERON TYPE I; INTESTINES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; ORGANOIDS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSPLANTATION, HOMOLOGOUS;

EID: 85018260284     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aag2513     Document Type: Article

References (45)

1. Z. Abdullah, M. Schlee, S. Roth, M. A. Mraheil, W. Barchet, J. Böttcher, T. Hain, S. Geiger, Y. Hayakawa, J. H. Fritz, F. Civril, K.-P. Hopfner, C. Kurts, J. Ruland, G. Hartmann, T. Chakraborty, P. A. Knolle, RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J. 31, 4153-4164 (2012).
2. V. Hornung, J. Ellegast, S. Kim, K. Brzozka, A. Jung, H. Kato, H. Poeck, S. Akira, K.-K. Conzelmann, M. Schlee, S. Endres, G. Hartmann, 5'-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997 (2006).
3. A. Pichlmair, O. Schulz, C. P. Tan, T. I. Näslund, P. Liljeström, F. Weber, C. Reis e Sousa, RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 314, 997-1001 (2006).
4. G. N. Barber, STING-dependent cytosolic DNA sensing pathways. Trends Immunol. 35, 88-93 (2014).
5. H. Poeck, M. Bscheider, O. Gross, K. Finger, S. Roth, M. Rebsamen, N. Hannesschläger, M. Schlee, S. Rothenfusser, W. Barchet, H. Kato, S. Akira, S. Inoue, S. Endres, C. Peschel, G. Hartmann, V. Hornung, J. Ruland, Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1β production. Nat. Immunol. 11, 63-69 (2010).
6. M. Yoneyama, K. Onomoto, M. Jogi, T. Akaboshi, T. Fujita, Viral RNA detection by RIG-I-like receptors. Curr. Opin. Immunol. 32, 48-53 (2015).
7. J. Pothlichet, I. Meunier, B. K. Davis, J. P.-Y. Ting, E. Skamene, V. von Messling, S. M. Vidal, Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLOS Pathog. 9, e1003256 (2013).
8. + efflux. J. Immunol. 193, 4214-4222 (2014).
9. J. Gregorio, S. Meller, C. Conrad, A. Di Nardo, B. Homey, A. Lauerma, N. Arai, R. L. Gallo, J. Digiovanni, M. Gilliet, Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J. Exp. Med. 207, 2921-2930 (2010).
10. L. Sun, H. Miyoshi, S. Origanti, T. J. Nice, A. C. Barger, N. A. Manieri, L. A. Fogel, A. R. French, D. Piwnica-Worms, H. Piwnica-Worms, H. W. Virgin, D. J. Lenschow, T. S. Stappenbeck, Type I interferons link viral infection to enhanced epithelial turnover and repair. Cell Host Microbe 17, 85-97 (2015).
11. J.-Y. Yang, M.-S. Kim, E. Kim, J. H. Cheon, Y.-S. Lee, Y. Kim, S.-H. Lee, S.-U. Seo, S.-H. Shin, S. S. Choi, B. Kim, S.-Y. Chang, H.-J. Ko, J.-W. Bae, M.-N. Kweon, Enteric viruses ameliorate gut inflammation via toll-like receptor 3 and toll-like receptor 7-mediated interferon-β production. Immunity 44, 889-900 (2016).
12. L. W. Peterson, D. Artis, Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14, 141-153 (2014).
13. S. Heidegger, M. R. M. van den Brink, T. Haas, H. Poeck, The role of pattern-recognition receptors in graft-versus-host disease and graft-versus-leukemia after allogeneic stem cell transplantation. Front. Immunol. 5, 337 (2014).
14. B. R. Blazar, W. J. Murphy, M. Abedi, Advances in graft-versus-host disease biology and therapy. Nat. Rev. Immunol. 12, 443-458 (2012).
15. R. R. Jenq, M. R. M. van den Brink, Allogeneic haematopoietic stem cell transplantation: Individualized stem cell and immune therapy of cancer. Nat. Rev. Cancer 10, 213-221 (2010).
16. L. Schwab, L. Goroncy, S. Palaniyandi, S. Gautam, A. Triantafyllopoulou, A. Mocsai, W. Reichardt, F. J. Karlsson, S. V. Radhakrishnan, K. Hanke, A. Schmitt-Graeff, M. Freudenberg, F. D. von Loewenich, P. Wolf, F. Leonhardt, N. Baxan, D. Pfeifer, O. Schmah, A. Schönle, S. F. Martin, R. Mertelsmann, J. Duyster, J. Finke, M. Prinz, P. Henneke, H. Häcker, G. C. Hildebrandt, G. Häcker, R. Zeiser, Neutrophil granulocytes recruited upon translocation of intestinal bacteria enhance graft-versus-host disease via tissue damage. Nat. Med. 20, 648-654 (2014).
17. S. Viaud, F. Saccheri, G. Mignot, T. Yamazaki, R. Daillère, D. Hannani, D. P. Enot, C. Pfirschke, C. Engblom, M. J. Pittet, A. Schlitzer, F. Ginhoux, L. Apetoh, E. Chachaty, P.-L. Woerther, G. Eberl, M. Berard, C. Ecobichon, D. Clermont, C. Bizet, V. Gaboriau-Routhiau, N. Cerf-Bensussan, P. Opolon, N. Yessaad, E. Vivier, B. Ryffel, C. O. Elson, J. Dorè, G. Kroemer, P. Lepage, I. G. Boneca, F. Ghiringhelli, L. Zitvogel, The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 342, 971-976 (2013).
18. X.-D. Li, Y.-H. Chiu, A. S. Ismail, C. L. Behrendt, M. Wight-Carter, L. V. Hooper, Z. J. Chen, Mitochondrial antiviral signaling protein (MAVS) monitors commensal bacteria and induces an immune response that prevents experimental colitis. Proc. Natl. Acad. Sci. U.S.A. 108, 17390-17395 (2011).
19. J. M. Breuss, J. Gallo, H. M. DeLisser, I. V. Klimanskaya, H. G. Folkesson, J. F. Pittet, S. L. Nishimura, K. Aldape, D. V. Landers, W. Carpenter, Expression of the β6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodeling. J. Cell Sci. 108 (Pt. 6), 2241-2251 (1995).
20. J. M. Breuss, N. Gillett, L. Lu, D. Sheppard, R. Pytela, Restricted distribution of integrin beta 6 mRNA in primate epithelial tissues. J. Histochem. Cytochem. 41, 1521-1527 (1993).
21. S. Vaishnava, M. Yamamoto, K. M. Severson, K. A. Ruhn, X. Yu, O. Koren, R. Ley, E. K. Wakeland, L. V. Hooper, The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255-258 (2011).
22. H. Poeck, R. Besch, C. Maihoefer, M. Renn, D. Tormo, S. S. Morskaya, S. Kirschnek, E. Gaffal, J. Landsberg, J. Hellmuth, A. Schmidt, D. Anz, M. Bscheider, T. Schwerd, C. Berking, C. Bourquin, U. Kalinke, E. Kremmer, H. Kato, S. Akira, R. Meyers, G. Hacker, M. Neuenhahn, D. Busch, J. Ruland, S. Rothenfusser, M. Prinz, V. Hornung, S. Endres, T. Tüting, G. Hartmann, 5'-Triphosphate-siRNA: Turning gene silencing and Rig-I activation against melanoma. Nat. Med. 14, 1256-1263 (2008).
23. J. A. Dudakov, A. M. Hanash, M. R. M. van den Brink, Interleukin-22: Immunobiology and pathology. Annu. Rev. Immunol. 33, 747-785 (2015).
24. J. A. Dudakov, A. M. Hanash, R. R. Jenq, L. F. Young, A. Ghosh, N. V. Singer, M. L. West, O. M. Smith, A. M. Holland, J. J. Tsai, R. L. Boyd, M. R. M. van den Brink, Interleukin-22 drives endogenous thymic regeneration in mice. Science 336, 91-95 (2012).
25. A. Dann, H. Poeck, A. L. Croxford, S. Gaupp, K. Kierdorf, M. Knust, D. Pfeifer, C. Maihoefer, S. Endres, U. Kalinke, S. G. Meuth, H. Wiendl, K. P. Knobeloch, S. Akira, A. Waisman, G. Hartmann, M. Prinz, Cytosolic RIG-I-like helicases act as negative regulators of sterile inflammation in the CNS. Nat. Neurosci. 15, 98-106 (2012).
26. T. Sato, R. G. Vries, H. J. Snippert, M. van de Wetering, N. Barker, D. E. Stange, J. H. van Es, A. Abo, P. Kujala, P. J. Peters, H. Clevers, Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
27. B.-K. Koo, H. Clevers, Stem cells marked by the R-spondin receptor LGR5. Gastroenterology 147, 289-302 (2014).
28. K. Yasuda, P. Yu, C. J. Kirschning, B. Schlatter, F. Schmitz, A. Heit, S. Bauer, H. Hochrein, H. Wagner, Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways. J. Immunol. 174, 6129-6136 (2005).
29. H. Ishikawa, Z. Ma, G. N. Barber, STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792 (2009).
30. J. Ahn, D. Gutman, S. Saijo, G. N. Barber, STING manifests self DNA-dependent inflammatory disease. Proc. Natl. Acad. Sci. U.S.A. 109, 19386-19391 (2012).
31. K. Vidal, I. Grosjean, J. P. Evillard, C. Gespach, D. Kaiserlian, Immortalization of mouse intestinal epithelial cells by the SV40-large T gene. Phenotypic and immune characterization of the MODE-K cell line. J. Immunol. Methods 166, 63-73 (1993).
32. R. J. Robb, E. Kreijveld, R. D. Kuns, Y. A. Wilson, S. D. Olver, A. L. J. Don, N. C. Raffelt, N. A. De Weerd, K. E. Lineburg, A. Varelias, K. A. Markey, M. Koyama, A. D. Clouston, P. J. Hertzog, K. P. A. Macdonald, G. R. Hill, Type I-IFNs control GVHD and GVL responses after transplantation. Blood 118, 3399-3409 (2011).
33. M. Tschurtschenthaler, J. Wang, C. Fricke, T. M. J. Fritz, L. Niederreiter, T. E. Adolph, E. Sarcevic, S. Kunzel, F. A. Offner, U. Kalinke, J. F. Baines, H. Tilg, A. Kaser, Type I interferon signalling in the intestinal epithelium affects Paneth cells, microbial ecology and epithelial regeneration. Gut 63, 1921-1931 (2014).
34. -/- mice develop colitis associated with downregulation of Gai2. Cell Res. 17, 858-868 (2007).
35. A. M. Hanash, J. A. Dudakov, G. Hua, M. H. O'Connor, L. F. Young, N. V. Singer, M. L. West, R. R. Jenq, A. M. Holland, L.W. Kappel, A. Ghosh, J.J. Tsai, U. K. Rao, N. L. Yim, O. M. Smith, E. Velardi, E. B. Hawryluk, G. F. Murphy, C. Liu, L. A. Fouser, R. Kolesnick, B. R. Blazar, M. R. M. van den Brink, Interleukin-22 protects intestinal stem cells from immunemediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 37, 339-350 (2012).
36. L. Pellegrinet, V. Rodilla, Z. Liu, S. Chen, U. Koch, L. Espinosa, K. H. Kaestner, R. Kopan, J. Lewis, F. Radtke, Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 140, 1230-1240.e7 (2011).
37. R. L. Gallo, L. V. Hooper, Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol. 12, 503-516 (2012).
38. J. Muñoz, D. E. Stange, A. G. Schepers, M. van de Wetering, B.-K. Koo, S. Itzkovitz, R. Volckmann, K. S. Kung, J. Koster, S. Radulescu, K. Myant, R. Versteeg, O. J. Sansom, J. H.van Es, N. Barker, A. van Oudenaarden, S. Mohammed, A.J. Heck, H. Clevers, The Lgr5 intestinal stem cell signature: Robust expression of proposed quiescent '+4' cell markers. EMBO J. 31, 3079-3091 (2012).
39. K. S. Yan, L. A. Chia, X. Li, A. Ootani, J. Su, J. Y. Lee, N. Su, Y. Luo, S. C. Heilshorn, M. R. Amieva, E. Sangiorgi, M. R. Capecchi, C. J. Kuo, The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc. Natl. Acad. Sci. U.S.A. 109, 466-471 (2012).
40. S. C. Nalle, J. R. Turner, Intestinal barrier loss as a critical pathogenic link between inflammatory bowel disease and graft-versus-host disease. Mucosal Immunol. 8, 720-730 (2015).
41. B. Funke, F. Lasitschka, W. Roth, R. Penzel, S. Meuer, M. Saile, N. Gretz, B. Sido, P. Schirmacher, F. Autschbach, Selective downregulation of retinoic acid-inducible gene I within the intestinal epithelial compartment in Crohn's disease. Inflamm. Bowel Dis. 17, 1943-1954 (2011).
42. D. Jankovic, J. Ganesan, M. Bscheider, N. Stickel, F. C. Weber, G. Guarda, M. Follo, D. Pfeifer, A. Tardivel, K. Ludigs, A. Bouazzaoui, K. Kerl, J. C. Fischer, T. Haas, A. Schmitt-Graff, A. Manoharan, L. Muller, J. Finke, S. F. Martin, O. Gorka, C. Peschel, J. Ruland, M. Idzko, J. Duyster, E. Holler, L. E. French, H. Poeck, E. Contassot, R. Zeiser, The Nlrp3 inflammasome regulates acute graft-versus-host disease. J. Exp. Med. 210, 1899-1910 (2013).
43. Ö. Alpdogan, S. J. Muriglan, J. M. Eng, L. M. Willis, A. S. Greenberg, B. J. Kappel, M. R. M. van den Brink, IL-7 enhances peripheral T cell reconstitution after allogeneic hematopoietic stem cell transplantation. J. Clin. Invest. 112, 1095-1107 (2003).
44. K. Neumann, M. Castiñeiras-Vilariño, U. Höckendorf, N. Hannesschlager, S. Lemeer, D. Kupka, S. Meyermann, M. Lech, H.-J. Anders, B. Kuster, D. H. Busch, A. Gewies, R. Naumann, O. Groß, J. Ruland, Clec12a is an inhibitory receptor for uric acid crystals that regulates inflammation in response to cell death. Immunity 40, 389-399 (2014).
45. T. D. Kim, T. H. Terwey, J. L. Zakrzewski, D. Suh, A. A. Kochman, M. E. Chen, C. G. King, C. Borsotti, J. Grubin, O. M. Smith, G. Heller, C. Liu, G. F. Murphy, O. Alpdogan, M. R. M. van den Brink, Organ-derived dendritic cells have differential effects on alloreactive T cells. Blood 111, 2929v2940 (2008).