RIP3 regulates autophagy and promotes coxsackievirus B3 infection of intestinal epithelial cells

Cell Host and Microbe

Volumn 18, Issue 2, 2015, Pages 221-232

  Harris, Katharine G ^a   Morosky, Stefanie A ^a   Drummond, Coyne G ^a   Patel, Maulik ^b   Kim, Chonsaeng ^c   Stolz, Donna B ^a   Bergelson, Jeffrey M ^d   Cherry, Sara ^e   Coyne, Carolyn B ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c Korea Research Institute of Chemical Technology   (South Korea)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; PROTEIN KINASE; PROTEIN P62; RECEPTOR INTERACTING PROTEIN KINASE 3; UNCLASSIFIED DRUG; 3C PROTEASES; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK3 PROTEIN, HUMAN; VIRAL PROTEIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; COXSACKIEVIRUS B3; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; INTESTINE EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; VIRUS ENTRY; VIRUS REPLICATION; CACO-2 CELL LINE; ENTEROVIRUS B; EPITHELIUM CELL; GENE SILENCING; GENETIC SCREENING; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE; VIROLOGY;

AUTOPHAGY; CACO-2 CELLS; CYSTEINE ENDOPEPTIDASES; ENTEROVIRUS B, HUMAN; EPITHELIAL CELLS; GENE SILENCING; GENETIC TESTING; HOST-PATHOGEN INTERACTIONS; HUMANS; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RNA INTERFERENCE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84956873718     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.07.007     Document Type: Article

References (49)

1. M. Alirezaei, C.T. Flynn, M.R. Wood, and J.L. Whitton Pancreatic acinar cell-specific autophagy disruption reduces coxsackievirus replication and pathogenesis in vivo Cell Host Microbe 11 2012 298 305
2. C.A. Anderson, G. Boucher, C.W. Lees, A. Franke, M. D'Amato, K.D. Taylor, J.C. Lee, P. Goyette, M. Imielinski, A. Latiano, and et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47 Nat. Genet. 43 2011 246 252
3. J.L. Benjamin, R. Sumpter Jr., B. Levine, and L.V. Hooper Intestinal epithelial autophagy is essential for host defense against invasive bacteria Cell Host Microbe 13 2013 723 734
4. T.O. Berg, M. Fengsrud, P.E. Strømhaug, T. Berg, and P.O. Seglen Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes J. Biol. Chem. 273 1998 21883 21892
5. N. Blom, J. Hansen, D. Blaas, and S. Brunak Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks Prot. Sci. 5 1996 2203 2216
6. R.A. Bozym, K. Patel, C. White, K.H. Cheung, J.M. Bergelson, S.A. Morosky, and C.B. Coyne Calcium signals and calpain-dependent necrosis are essential for release of coxsackievirus B from polarized intestinal epithelial cells Mol. Biol. Cell 22 2011 3010 3021
7. Z. Cai, S. Jitkaew, J. Zhao, H.C. Chiang, S. Choksi, J. Liu, Y. Ward, L.G. Wu, and Z.G. Liu Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis Nat. Cell Biol. 16 2014 55 65
8. C.M. Carthy, D.J. Granville, K.A. Watson, D.R. Anderson, J.E. Wilson, D. Yang, D.W. Hunt, and B.M. McManus Caspase activation and specific cleavage of substrates after coxsackievirus B3-induced cytopathic effect in HeLa cells J. Virol. 72 1998 7669 7675
9. X. Chen, W. Li, J. Ren, D. Huang, W.T. He, Y. Song, C. Yang, W. Li, X. Zheng, P. Chen, and J. Han Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death Cell Res. 24 2014 105 121
10. Y.S. Cho, S. Challa, D. Moquin, R. Genga, T.D. Ray, M. Guildford, and F.K. Chan Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation Cell 137 2009 1112 1123
11. C.B. Coyne, and J.M. Bergelson Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions Cell 124 2006 119 131
12. C.B. Coyne, R. Bozym, S.A. Morosky, S.L. Hanna, A. Mukherjee, M. Tudor, K.S. Kim, and S. Cherry Comparative RNAi screening reveals host factors involved in enterovirus infection of polarized endothelial monolayers Cell Host Microbe 9 2011 70 82
13. D. Crowther, and J.L. Melnick The incorporation of neutral red and acridine orange into developing poliovirus particles making them photosensitive Virology 14 1961 11 21
14. M.C. de Almagro, and D. Vucic Necroptosis: Pathway diversity and characteristics Semin. Cell Dev. Biol. 39 2015 56 62
15. E. Delorme-Axford, R.B. Donker, J.F. Mouillet, T. Chu, A. Bayer, Y. Ouyang, T. Wang, D.B. Stolz, S.N. Sarkar, A.E. Morelli, and et al. Human placental trophoblasts confer viral resistance to recipient cells Proc. Natl. Acad. Sci. USA 110 2013 12048 12053
16. E. Delorme-Axford, Y. Sadovsky, and C.B. Coyne Lipid raft- and SRC family kinase-dependent entry of coxsackievirus B into human placental trophoblasts J. Virol. 87 2013 8569 8581
17. E. Delorme-Axford, S. Morosky, J. Bomberger, D.B. Stolz, W.T. Jackson, and C.B. Coyne BPIFB3 regulates autophagy and coxsackievirus B replication through a noncanonical pathway independent of the core initiation machinery MBio 5 2014 e02147
18. C.P. Dillon, R. Weinlich, D.A. Rodriguez, J.G. Cripps, G. Quarato, P. Gurung, K.C. Verbist, T.L. Brewer, F. Llambi, Y.N. Gong, and et al. RIPK1 blocks early postnatal lethality mediated by caspase-8 and RIPK3 Cell 157 2014 1189 1202
19. M. Elgendy, C. Sheridan, G. Brumatti, and S.J. Martin Oncogenic Ras-induced expression of Noxa and Beclin-1 promotes autophagic cell death and limits clonogenic survival Mol. Cell 42 2011 23 35
20. K.G. Harris, and C.B. Coyne Enter at your own risk: how enteroviruses navigate the dangerous world of pattern recognition receptor signaling Cytokine 63 2013 230 236
21. K.G. Harris, and C.B. Coyne Death waits for no man - does it wait for a virus? How enteroviruses induce and control cell death Cytokine Growth Factor Rev. 25 2014 587 596
22. S. He, L. Wang, L. Miao, T. Wang, F. Du, L. Zhao, and X. Wang Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-alpha Cell 137 2009 1100 1111
23. W.J. Kaiser, J.W. Upton, A.B. Long, D. Livingston-Rosanoff, L.P. Daley-Bauer, R. Hakem, T. Caspary, and E.S. Mocarski RIP3 mediates the embryonic lethality of caspase-8-deficient mice Nature 471 2011 368 372
24. W.J. Kaiser, L.P. Daley-Bauer, R.J. Thapa, P. Mandal, S.B. Berger, C. Huang, A. Sundararajan, H. Guo, L. Roback, S.H. Speck, and et al. RIP1 suppresses innate immune necrotic as well as apoptotic cell death during mammalian parturition Proc. Natl. Acad. Sci. USA 111 2014 7753 7758
25. K. Kirkegaard, M.P. Taylor, and W.T. Jackson Cellular autophagy: surrender, avoidance and subversion by microorganisms Nat. Rev. Microbiol. 2 2004 301 314
26. V. Kirkin, T. Lamark, T. Johansen, and I. Dikic NBR1 cooperates with p62 in selective autophagy of ubiquitinated targets Autophagy 5 2009 732 733
27. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, L. Agholme, M. Agnello, P. Agostinis, J.A. Aguirre-Ghiso, and et al. Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 2012 445 544
28. C.A. Lamb, T. Yoshimori, and S.A. Tooze The autophagosome: origins unknown, biogenesis complex Nat. Rev. Mol. Cell Biol. 14 2013 759 774
29. M. Lippai, and P. Low The role of the selective adaptor p62 and ubiquitin-like proteins in autophagy BioMed Res. Int. 2014 2014 832704
30. Y. Liu, S. Shoji-Kawata, R.M. Sumpter Jr., Y. Wei, V. Ginet, L. Zhang, B. Posner, K.A. Tran, D.R. Green, R.J. Xavier, and et al. 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 2013 20364 20371
31. B. Longdon, M.A. Brockhurst, C.A. Russell, J.J. Welch, and F.M. Jiggins The evolution and genetics of virus host shifts PLoS Pathog. 10 2014 e1004395
32. G. Mariño, M. Niso-Santano, E.H. Baehrecke, and G. Kroemer Self-consumption: the interplay of autophagy and apoptosis Nat. Rev. Mol. Cell Biol. 15 2014 81 94
33. Y. Matsuzawa, S. Oshima, Y. Nibe, M. Kobayashi, C. Maeyashiki, Y. Nemoto, T. Nagaishi, R. Okamoto, K. Tsuchiya, T. Nakamura, and M. Watanabe RIPK3 regulates p62-LC3 complex formation via the caspase-8-dependent cleavage of p62 Biochem. Biophys. Res. Commun. 456 2015 298 304
34. N. Mizushima, and B. Levine Autophagy in mammalian development and differentiation Nat. Cell Biol. 12 2010 823 830
35. K. Moriwaki, and F.K. Chan RIP3: a molecular switch for necrosis and inflammation Genes Dev. 27 2013 1640 1649
36. K. Newton, X. Sun, and V.M. Dixit Kinase RIP3 is dispensable for normal NF-kappa Bs, signaling by the B-cell and T-cell receptors, tumor necrosis factor receptor 1, and Toll-like receptors 2 and 4 Mol. Cell. Biol. 24 2004 1464 1469
37. A. Oberst, C.P. Dillon, R. Weinlich, L.L. McCormick, P. Fitzgerald, C. Pop, R. Hakem, G.S. Salvesen, and D.R. Green Catalytic activity of the caspase-8-FLIP(L) complex inhibits RIPK3-dependent necrosis Nature 471 2011 363 367
38. J.A. Rickard, J.A. O'Donnell, J.M. Evans, N. Lalaoui, A.R. Poh, T. Rogers, J.E. Vince, K.E. Lawlor, R.L. Ninnis, H. Anderton, and et al. RIPK1 regulates RIPK3-MLKL-driven systemic inflammation and emergency hematopoiesis Cell 157 2014 1175 1188
39. S.M. Robinson, G. Tsueng, J. Sin, V. Mangale, S. Rahawi, L.L. McIntyre, W. Williams, N. Kha, C. Cruz, B.M. Hancock, and et al. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers PLoS Pathog. 10 2014 e1004045
40. S. Shelly, N. Lukinova, S. Bambina, A. Berman, and S. Cherry Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus Immunity 30 2009 588 598
41. A. Stolz, A. Ernst, and I. Dikic Cargo recognition and trafficking in selective autophagy Nat. Cell Biol. 16 2014 495 501
42. D.A. Suhy, T.H. Giddings Jr., and K. Kirkegaard Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles J. Virol. 74 2000 8953 8965
43. L. Sun, H. Wang, Z. Wang, S. He, S. Chen, D. Liao, L. Wang, J. Yan, W. Liu, X. Lei, and X. Wang Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase Cell 148 2012 213 227
44. J. Wong, J. Zhang, X. Si, G. Gao, I. Mao, B.M. McManus, and H. Luo Autophagosome supports coxsackievirus B3 replication in host cells J. Virol. 82 2008 9143 9153
45. X.N. Wu, Z.H. Yang, X.K. Wang, Y. Zhang, H. Wan, Y. Song, X. Chen, J. Shao, and J. Han Distinct roles of RIP1-RIP3 hetero- and RIP3-RIP3 homo-interaction in mediating necroptosis Cell Death Differ. 21 2014 1709 1720
46. T. Yonekawa, G. Gamez, J. Kim, A.C. Tan, J. Thorburn, J. Gump, A. Thorburn, and M.J. Morgan RIP1 negatively regulates basal autophagic flux through TFEB to control sensitivity to apoptosis EMBO Rep. 16 2015 700 708
47. P.W. Yu, B.C. Huang, M. Shen, J. Quast, E. Chan, X. Xu, G.P. Nolan, D.G. Payan, and Y. Luo Identification of RIP3, a RIP-like kinase that activates apoptosis and NFkappaB Curr. Biol. 9 1999 539 542
48. L. Yu, A. Alva, H. Su, P. Dutt, E. Freundt, S. Welsh, E.H. Baehrecke, and M.J. Lenardo Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8 Science 304 2004 1500 1502
49. D.W. Zhang, J. Shao, J. Lin, N. Zhang, B.J. Lu, S.C. Lin, M.Q. Dong, and J. Han RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis Science 325 2009 332 336