Autophagy protein ATG16L1 prevents necroptosis in the intestinal epithelium

Journal of Experimental Medicine

Volumn 214, Issue 12, 2017, Pages 3687-3705

  Matsuzawa Ishimoto, Yu ^a   Shono, Yusuke ^b   Gomez, Luis E ^a   Hubbard Lucey, Vanessa M ^a   Cammer, Michael ^a   Neil, Jessica ^a   Dewan, M Zahidunnabi ^a   Lieberman, Sophia R ^b   Lazrak, Amina ^b   Marinis, Jill M ^c   Beal, Allison ^c   Harris, Philip A ^c   Bertin, John ^c   Liu, Chen ^d   Ding, Yi ^e   van den Brink, Marcel R M ^b,f   Cadwell, Ken ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c GLAXOSMITHKLINE   (United States)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATG16L1 PROTEIN; AUTOPHAGY RELATED PROTEIN; CASPASE 3; CASPASE 8; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ATG16L1 PROTEIN, MOUSE; CARRIER PROTEIN; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN, MOUSE;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL FUNCTION; CELL PROTECTION; CONTROLLED STUDY; GRAFT VERSUS HOST REACTION; INFLAMMATORY BOWEL DISEASE; MOUSE; NECROPTOSIS; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; SMALL INTESTINE EPITHELIUM; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; AUTOPHAGY; C57BL MOUSE; CALICIVIRUS INFECTION; CELL SURVIVAL; EPITHELIUM CELL; GENE DELETION; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HOMEOSTASIS; INTESTINE MUCOSA; METABOLISM; MITOCHONDRION; MUTATION; NECROSIS; NOROVIRUS; ORGANOID; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE; VIROLOGY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CALICIVIRIDAE INFECTIONS; CARRIER PROTEINS; CELL SURVIVAL; CYTOPROTECTION; EPITHELIAL CELLS; GENE DELETION; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HOMEOSTASIS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MUTATION; NECROSIS; NOROVIRUS; ORGANOIDS; PANETH CELLS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85036529844     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20170558     Document Type: Article

References (60)

1. Adolph, T.E., M.F. Tomczak, L. Niederreiter, H.J. Ko, J. Böck, E. Martinez-Naves, J.N. Glickman, M. Tschurtschenthaler, J. Hartwig, S. Hosomi, et al. 2013. Paneth cells as a site of origin for intestinal inflammation. Nature. 503:272-276. https://doi.org/10.1038/nature12599
2. Benjamin, J.L., R. Sumpter Jr., B. Levine, and L.V. Hooper. 2013. Intestinal epithelial autophagy is essential for host defense against invasive bacteria. Cell Host Microbe. 13:723-734. https://doi.org/10.1016/j.chom.2013.05.004
3. Berry, D.L., and E.H. Baehrecke. 2007. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell. 131:1137-1148. https://doi.org/10.1016/j.cell.2007.10.048
4. Blaser, H., C. Dostert, T.W. Mak, and D. Brenner. 2016. TNF and ROS crosstalk in inflammation. Trends Cell Biol. 26:249-261. https://doi.org/10.1016/j.tcb.2015.12.002
5. Blazar, B.R., W.J. Murphy, and M. Abedi. 2012. Advances in graft-versus-host disease biology and therapy. Nat. Rev. Immunol. 12:443-458. https://doi.org/10.1038/nri3212
6. Cadwell, K. 2015. The virome in host health and disease. Immunity. 42:805-813. https://doi.org/10.1016/j.immuni.2015.05.003
7. Cadwell, K. 2016. Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis. Nat. Rev. Immunol. 16:661-675. https://doi.org/10.1038/nri.2016.100
8. Cadwell, K., J.Y. Liu, S.L. Brown, H. Miyoshi, J. Loh, J.K. Lennerz, C. Kishi, W. Kc, J.A. Carrero, S. Hunt, et al. 2008. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature. 456:259-263. https://doi.org/10.1038/nature07416
9. Cadwell, K., K.K. Patel, N.S. Maloney, T.C. Liu, A.C. Ng, C.E. Storer, R.D. Head, R. Xavier, T.S. Stappenbeck, and H.W. Virgin. 2010. Virus-plussusceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell. 141:1135-1145. https://doi.org/10.1016/j.cell.2010.05.009
10. Chen, S.Y., L.Y. Chiu, M.C. Maa, J.S. Wang, C.L. Chien, and W.W. Lin. 2011. zVAD-induced autophagic cell death requires c-Src-dependent ERK and JNK activation and reactive oxygen species generation. Autophagy. 7:217-228. https://doi.org/10.4161/auto.7.2.14212
11. Conway, K.L., P. Kuballa, J.H. Song, K.K. Patel, A.B. Castoreno, O.H. Yilmaz, H.B. Jijon, M. Zhang, L.N. Aldrich, E.J. Villablanca, et al. 2013. Atg16l1 is required for autophagy in intestinal epithelial cells and protection of mice from Salmonella infection. Gastroenterology. 145:1347-1357. https://doi.org/10.1053/j.gastro.2013.08.035
12. Cooke, K.R., W. Krenger, G. Hill, T.R. Martin, L. Kobzik, J. Brewer, R. Simmons, J.M. Crawford, M.R. van den Brink, and J.L. Ferrara. 1998. Host reactive donor T cells are associated with lung injury after experimental allogeneic bone marrow transplantation. Blood. 92:2571-2580
13. Degterev, A., Z. Huang, M. Boyce, Y. Li, P. Jagtap, N. Mizushima, G.D. Cuny, T.J. Mitchison, M.A. Moskowitz, and J. Yuan. 2005. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1:112-119. https://doi.org/10.1038/nchembio711
14. Diamanti, M.A., J. Gupta, M. Bennecke, T. De Oliveira, M. Ramakrishnan, A.K. Braczynski, B. Richter, P. Beli, Y. Hu, M. Saleh, et al. 2017. IKKa controls ATG16L1 degradation to prevent ER stress during inflammation. J. Exp. Med. 214:423-437. https://doi.org/10.1084/jem.20161867
15. Fang, H., M. Tan, M. Xia, L. Wang, and X. Jiang. 2013. Norovirus P particle efficiently elicits innate, humoral and cellular immunity. PLoS One. 8:e63269. https://doi.org/10.1371/journal.pone.0063269
16. Fischer, J.C., M. Bscheider, G. Eisenkolb, C.C. Lin, A. Wintges, V. Otten, C.A. Lindemans, S. Heidegger, M. Rudelius, S. Monette, et al. 2017. RIG-I/MAVS and STI NG signaling promote gut integrity during irradiationand immune-mediated tissue injury. Sci. Transl. Med. 9:9. https://doi.org/10.1126/scitranslmed.aag2513
17. Gold, R., M. Schmied, G. Giegerich, H. Breitschopf, H.P. Hartung, K.V. Toyka, and H. Lassmann. 1994. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab. Invest. 71:219-225
18. Goodall, M.L., B.E. Fitzwalter, S. Zahedi, M. Wu, D. Rodriguez, J.M. Mulcahy-Levy, D.R. Green, M. Morgan, S.D. Cramer, and A. Thorburn. 2016. The autophagy machinery controls cell death switching between apoptosis and necroptosis. Dev. Cell. 37:337-349. https://doi.org/10.1016/j.devcel.2016.04.018
19. Grasl-Kraupp, B., B. Ruttkay-Nedecky, H. Koudelka, K. Bukowska, W. Bursch, and R. Schulte-Hermann. 1995. In situ detection of fragmented DNA (TUN EL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology. 21:1465-1468
20. Günther, C., E. Martini, N. Wittkopf, K. Amann, B. Weigmann, H. Neumann, M.J. Waldner, S.M. Hedrick, S. Tenzer, M.F. Neurath, and C. Becker. 2011. Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature. 477:335-339. https://doi.org/10.1038/nature10400
21. Hill, G.R., and J.L. Ferrara. 2000. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood. 95:2754-2759
22. Hitomi, J., D.E. Christofferson, A. Ng, J. Yao, A. Degterev, R.J. Xavier, and J. Yuan. 2008. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell. 135:1311-1323. https://doi.org/10.1016/j.cell.2008.10.044
23. Holler, E., K. Landfried, J. Meier, M. Hausmann, and G. Rogler. 2010. The role of bacteria and pattern recognition receptors in GVHD. Int. J. Inflamm. 2010:814326. https://doi.org/10.4061/2010/814326
24. Hou, W., J. Han, C. Lu, L.A. Goldstein, and H. Rabinowich. 2010. Autophagic degradation of active caspase-8: a crosstalk mechanism between autophagy and apoptosis. Autophagy. 6:891-900. https://doi.org/10.4161/auto.6.7.13038
25. Hubbard-Lucey, V.M., Y. Shono, K. Maurer, M.L. West, N.V. Singer, C.G. Ziegler, C. Lezcano, A.C. Motta, K. Schmid, S.M. Levi, et al. 2014. Autophagy gene Atg16L1 prevents lethal T cell alloreactivity mediated by dendritic cells. Immunity. 41:579-591. https://doi.org/10.1016/j.immuni.2014.09.011
26. Imagawa, Y., T. Saitoh, and Y. Tsujimoto. 2016. Vital staining for cell death identifies Atg9a-dependent necrosis in developmental bone formation in mouse. Nat. Commun. 7:13391. https://doi.org/10.1038/ncomms13391
27. Kaiser, W.J., J.W. Upton, A.B. Long, D. Livingston-Rosanoff, L.P. Daley-Bauer, R. Hakem, T. Caspary, and E.S. Mocarski. 2011. RIP3 mediates the embryonic lethality of caspase-8-deficient mice. Nature. 471:368-372. https://doi.org/10.1038/nature09857
28. Kernbauer, E., Y. Ding, and K. Cadwell. 2014. An enteric virus can replace the beneficial function of commensal bacteria. Nature. 516:94-98. https://doi.org/10.1038/nature13960
29. Kim, Y.G., J.H. Park, T. Reimer, D.P. Baker, T. Kawai, H. Kumar, S. Akira, C. Wobus, and G. Núñez. 2011. Viral infection augments Nod1/2 signaling to potentiate lethality associated with secondary bacterial infections. Cell Host Microbe. 9:496-507. https://doi.org/10.1016/j.chom.2011.05.006
30. Koo, B.K., D.E. Stange, T. Sato, W. Karthaus, H.F. Farin, M. Huch, J.H. van Es, and H. Clevers. 2011. Controlled gene expression in primary Lgr5 organoid cultures. Nat. Methods. 9:81-83. https://doi.org/10.1038/nmeth.1802
31. Lassen, K.G., P. Kuballa, K.L. Conway, K.K. Patel, C.E. Becker, J.M. Peloquin, E.J. Villablanca, J.M. Norman, T.C. Liu, R.J. Heath, et al. 2014. Atg16L1 T300A variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense. Proc. Natl. Acad. Sci. USA. 111:7741-7746. https://doi.org/10.1073/pnas.1407001111
32. Leach, M.W., A.G. Bean, S. Mauze, R.L. Coffman, and F. Powrie. 1996. Inflammatory bowel disease in C.B-17 scid mice reconstituted with the CD45RBhigh subset of CD4+ T cells. Am. J. Pathol. 148:1503-1515
33. Liu, Y., S. Shoji-Kawata, R.M. Sumpter Jr., Y. Wei, V. Ginet, L. Zhang, B. Posner, K.A. Tran, D.R. Green, R.J. Xavier, et al. 2013. Autosis is a Na+, K+-ATPase-regulated form of cell death triggered by autophagy-inducing peptides, starvation, and hypoxia-ischemia. Proc. Natl. Acad. Sci. USA. 110:20364-20371. https://doi.org/10.1073/pnas.1319661110
34. Lu, W., J. Sun, J.S. Yoon, Y. Zhang, L. Zheng, E. Murphy, M.P. Mattson, and M.J. Lenardo. 2016. Mitochondrial protein PGAM5 regulates mitophagic protection against cell necroptosis. PLoS One. 11:e0147792. https://doi.org/10.1371/journal.pone.0147792
35. Mariño, G., M. Niso-Santano, E.H. Baehrecke, and G. Kroemer. 2014. Selfconsumption: the interplay of autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 15:81-94. https://doi.org/10.1038/nrm3735
36. McCartney, S.A., L.B. Thackray, L. Gitlin, S. Gilfillan, H.W. Virgin, and M. Colonna. 2008. MDA-5 recognition of a murine norovirus. PLoS Pathog. 4:e1000108. https://doi.org/10.1371/journal.ppat.1000108
37. Mizumura, K., S.M. Cloonan, K. Nakahira, A.R. Bhashyam, M. Cervo, T. Kitada, K. Glass, C.A. Owen, A. Mahmood, G.R. Washko, et al. 2014. Mitophagy-dependent necroptosis contributes to the pathogenesis of COPD. J. Clin. Invest. 124:3987-4003. https://doi.org/10.1172/JCI74985
38. Murphy, J.M., P.E. Czabotar, J.M. Hildebrand, I.S. Lucet, J.G. Zhang, S. Alvarez-Diaz, R. Lewis, N. Lalaoui, D. Metcalf, A.I. Webb, et al. 2013. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity. 39:443-453. https://doi.org/10.1016/j.immuni.2013.06.018
39. Murthy, A., Y. Li, I. Peng, M. Reichelt, A.K. Katakam, R. Noubade, M. Roose-Girma, J. DeVoss, L. Diehl, R.R. Graham, and M. van Lookeren Campagne. 2014. A Crohn's disease variant in Atg16l1 enhances its degradation by caspase 3. Nature. 506:456-462. https://doi.org/10.1038/nature13044
40. Oberst, A., C.P. Dillon, R. Weinlich, L.L. McCormick, P. Fitzgerald, C. Pop, R. Hakem, G.S. Salvesen, and D.R. Green. 2011. Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis. Nature. 471:363-367. https://doi.org/10.1038/nature09852
41. Pasparakis, M., and P. Vandenabeele. 2015. Necroptosis and its role in inflammation. Nature. 517:311-320. https://doi.org/10.1038/nature14191
42. Patel, K.K., H. Miyoshi, W.L. Beatty, R.D. Head, N.P. Malvin, K. Cadwell, J.L. Guan, T. Saitoh, S. Akira, P.O. Seglen, et al. 2013. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. EMBO J. 32:3130-3144. https://doi.org/10.1038/emboj.2013.233
43. Ramanan, D., and K. Cadwell. 2016. Intrinsic defense mechanisms of the intestinal epithelium. Cell Host Microbe. 19:434-441. https://doi.org/10.1016/j.chom.2016.03.003
44. Randow, F., and R.J. Youle. 2014. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe. 15:403-411. https://doi.org/10.1016/j.chom.2014.03.012
45. Remijsen, Q., V. Goossens, S. Grootjans, C. Van den Haute, N. Vanlangenakker, Y. Dondelinger, R. Roelandt, I. Bruggeman, A. Goncalves, M.J. Bertrand, et al. 2014. Depletion of RIPK3 or MLKL blocks TNF-driven necroptosis and switches towards a delayed RIPK1 kinase-dependent apoptosis. Cell Death Dis. 5:e1004. https://doi.org/10.1038/cddis.2013.531
46. Samara, C., P. Syntichaki, and N. Tavernarakis. 2008. Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ. 15:105-112. https://doi.org/10.1038/sj.cdd.4402231
47. Sato, T., 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, and H. Clevers. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 459:262-265. https://doi.org/10.1038/nature07935
48. Sato, T., D.E. Stange, M. Ferrante, R.G. Vries, J.H. Van Es, S. Van den Brink, W.J. Van Houdt, A. Pronk, J. Van Gorp, P.D. Siersema, and H. Clevers. 2011. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology. 141:1762-1772. https://doi.org/10.1053/j.gastro.2011.07.050
49. Saveljeva, S., S.L. Mc Laughlin, P. Vandenabeele, A. Samali, and M.J. Bertrand. 2015. Endoplasmic reticulum stress induces ligand-independent TNFR1-mediated necroptosis in L929 cells. Cell Death Dis. 6:e1587. https://doi.org/10.1038/cddis.2014.548
50. Simmons, A.N., R. Kajino-Sakamoto, and J. Ninomiya-Tsuji. 2016. TAK1 regulates Paneth cell integrity partly through blocking necroptosis. Cell Death Dis. 7:e2196. https://doi.org/10.1038/cddis.2016.98
51. Sun, L., H. Wang, Z. Wang, S. He, S. Chen, D. Liao, L. Wang, J. Yan, W. Liu, X. Lei, and X. Wang. 2012. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell. 148:213-227. https://doi.org/10.1016/j.cell.2011.11.031
52. Tait, S.W., A. Oberst, G. Quarato, S. Milasta, M. Haller, R. Wang, M. Karvela, G. Ichim, N. Yatim, M.L. Albert, et al. 2013. Widespread mitochondrial depletion via mitophagy does not compromise necroptosis. Cell Reports. 5:878-885. https://doi.org/10.1016/j.celrep.2013.10.034
53. Takahashi, N., L. Duprez, S. Grootjans, A. Cauwels, W. Nerinckx, J.B. DuHadaway, V. Goossens, R. Roelandt, F. Van Hauwermeiren, C. Libert, et al. 2012. Necrostatin-1 analogues: critical issues on the specificity, activity and in vivo use in experimental disease models. Cell Death Dis. 3:e437. https://doi.org/10.1038/cddis.2012.176
54. Tschurtschenthaler, M., T.E. Adolph, J.W. Ashcroft, L. Niederreiter, R. Bharti, S. Saveljeva, J. Bhattacharyya, M.B. Flak, D.Q. Shih, G.M. Fuhler, et al. 2017. Defective ATG16L1-mediated removal of IRE1α drives Crohn's disease-like ileitis. J. Exp. Med. 214:401-422. https://doi.org/10.1084/jem.20160791
55. Vaishnava, S., C.L. Behrendt, A.S. Ismail, L. Eckmann, and L.V. Hooper. 2008. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc. Natl. Acad. Sci. USA. 105:20858-20863. https://doi.org/10.1073/pnas.0808723105
56. Wang, Z., H. Jiang, S. Chen, F. Du, and X. Wang. 2012. The mitochondrial phosphatase PGAM5 functions at the convergence point of multiple necrotic death pathways. Cell. 148:228-243. https://doi.org/10.1016/j.cell.2011.11.030
57. Wlodarska, M., A.D. Kostic, and R.J. Xavier. 2015. An integrative view of microbiome-host interactions in inflammatory bowel diseases. Cell Host Microbe. 17:577-591. https://doi.org/10.1016/j.chom.2015.04.008
58. Yui, S., T. Nakamura, T. Sato, Y. Nemoto, T. Mizutani, X. Zheng, S. Ichinose, T. Nagaishi, R. Okamoto, K. Tsuchiya, et al. 2012. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 18:618-623. https://doi.org/10.1038/nm.2695
59. Zhang, D.W., J. Shao, J. Lin, N. Zhang, B.J. Lu, S.C. Lin, M.Q. Dong, and J. Han. 2009. RIP3, an energy metabolism regulator that switches TNFinduced cell death from apoptosis to necrosis. Science. 325:332-336. https://doi.org/10.1126/science.1172308
60. Zhu, X., J.S. Messer, Y. Wang, F. Lin, C.M. Cham, J. Chang, T.R. Billiar, M.T. Lotze, D.L. Boone, and E.B. Chang. 2015. Cytosolic HMGB1 controls the cellular autophagy/apoptosis checkpoint during inflammation. J. Clin. Invest. 125:1098-1110. https://doi.org/10.1172/JCI76344