Coronavirus membrane-associated papain-like proteases induce autophagy through interacting with Beclin1 to negatively regulate antiviral innate immunity

Protein and Cell

Volumn 5, Issue 12, 2014, Pages 912-927

  Chen, Xiaojuan ^a   Wang, Kai ^a,b   Xing, Yaling ^a   Tu, Jian ^c   Yang, Xingxing ^a   Zhao, Qian ^a   Li, Kui ^d   Chen, Zhongbin ^a  

^a BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^b BENGBU MEDICAL COLLEGE   (China)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

antiviral immunity; autophagy; Beclin1; coronavirus; papain like protease; STING

Indexed keywords

BECLIN 1; BETA INTERFERON; GREEN FLUORESCENT PROTEIN; MICROTUBULE PROTEIN 1 LIGHT CHAIN 3; PAPAIN LIKE PROTEASE; PEPTIDES AND PROTEINS; PROTEINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; GAMMA INTERFERON; LIGHT CHAIN 3, HUMAN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; MPYS PROTEIN, HUMAN; PAPAIN; PAPAIN-LIKE PROTEINASE 2;

ANTIVIRAL INNATE IMMUNITY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORONAVIRUS; ENZYME ACTIVITY; EXPRESSION VECTOR; GENE SILENCING; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INNATE IMMUNITY; LUCIFERASE ASSAY; MCF 7 CELL LINE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UBIQUITINATION; UPREGULATION; VIRUS ENVELOPE; VIRUS REPLICATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN CORONAVIRUS NL63; IMMUNE EVASION; IMMUNOLOGY; LYSOSOME; MEMBRANE FUSION; METABOLISM; PHAGOSOME; SIGNAL TRANSDUCTION; VIROLOGY;

CORONAVIRUS;

APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CORONAVIRUS NL63, HUMAN; GENE EXPRESSION REGULATION; HEK293 CELLS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; INTERFERON-GAMMA; LYSOSOMES; MCF-7 CELLS; MEMBRANE FUSION; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; PAPAIN; PHAGOSOMES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 84916893906     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-014-0104-6     Document Type: Article

References (71)

1. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC (2005) The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. Journal of virology 79:15189–15198
2. Barth S, Glick D, Macleod KF (2010) Autophagy: assays and artifacts. J Pathol 221:117–124
3. Bernasconi R, Noack J, Molinari M (2012) Unconventional roles of nonlipidated LC3 in ERAD tuning and coronavirus infection. Autophagy 8:1534–1536
4. Bibeau-Poirier A, Servant MJ (2008) Roles of ubiquitination in pattern-recognition receptors and type I interferon receptor signaling. Cytokine 43:359–367
5. Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T (2005) p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603–614
6. Chen ZJ (2012) Ubiquitination in signaling to and activation of IKK. Immunol Rev 246:95–106
7. Chen Z, Wang Y, Ratia K, Mesecar AD, Wilkinson KD, Baker SC (2007) Proteolytic processing and deubiquitinating activity of papain-like proteases of human coronavirus NL63. J Virol 81:6007–6018
8. Chen Q, Fang L, Wang D, Wang S, Li P, Li M, Luo R, Chen H, Xiao S (2012) Induction of autophagy enhances porcine reproductive and respiratory syndrome virus replication. Virus Res 163:650–655
9. Choi AM, Ryter SW, Levine B (2013) Autophagy in human health and disease. New Engl J Med 368:651–662
10. Clementz MA, Chen Z, Banach BS, Wang Y, Sun L, Ratia K, Baez-Santos YM, Wang J, Takayama J, Ghosh AK et al (2010) Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J Virol 84:4619–4629
11. Cottam EM, Maier HJ, Manifava M, Vaux LC, Chandra-Schoenfelder P, Gerner W, Britton P, Ktistakis NT, Wileman T (2011) Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 7:1335–1347
12. de Haan CA, Reggiori F (2008) Are nidoviruses hijacking the autophagy machinery? Autophagy 4:276–279
13. Deretic V (2012) Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr Opin Immunol 24:21–31
14. Devaraj SG, Wang N, Chen Z, Chen Z, Tseng M, Barretto N, Lin R, Peters CJ, Tseng CT, Baker SC et al (2007) Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J Biol Chem 282:32208–32221
15. Dong X, Levine B (2013) Autophagy and viruses: adversaries or allies? J Innate Immun 5:480–493
16. Dreux M, Chisari FV (2010) Viruses and the autophagy machinery. Cell Cycle (Georgetown, Tex.) 9: 1295–1307
17. Gannage M, Dormann D, Albrecht R, Dengjel J, Torossi T, Ramer PC, Lee M, Strowig T, Arrey F, Conenello G et al (2009) Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 6:367–380
18. Glick D, Barth S, Macleod KF (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221:3–12
19. Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC (2002) RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76:3697–3708
20. Hagemeijer MC, Verheije MH, Ulasli M, Shaltiel IA, de Vries LA, Reggiori F, Rottier PJ, de Haan CA (2010) Dynamics of coronavirus replication-transcription complexes. J Virol 84:2134–2149
21. Hoyer-Hansen M, Bastholm L, Mathiasen IS, Elling F, Jaattela M (2005) Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 12:1297–1309
22. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH (2009) ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20:1992–2003
23. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720–5728
24. Kang R, Zeh HJ, Lotze MT, Tang D (2011) The Beclin1 network regulates autophagy and apoptosis. Cell Death Differ 18:571–580
25. Ke PY, Chen SS (2011) Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J Clin Investig 121:37–56
26. Kimura S, Noda T, Yoshimori T (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3:452–460
27. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445–544
28. Knoops K, Kikkert M, Worm SH, Zevenhoven-Dobbe JC, van der Meer Y, Koster AJ, Mommaas AM, Snijder EJ (2008) SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS biology 6:e226
29. Kraft C, Martens S (2012) Mechanisms and regulation of autophagosome formation. Curr Opin Cell Biol 24:496–501
30. Kroemer G, Levine B (2008) Autophagic cell death: the story of a misnomer. Nat Rev 9:1004–1010
31. Kuballa P, Nolte WM, Castoreno AB, Xavier RJ (2012) Autophagy and the immune system. Annu Rev Immunol 30:611–646
32. Kudchodkar SB, Levine B (2009) Viruses and autophagy. Rev Med Virol 19:359–378
33. Kyei GB, Dinkins C, Davis AS, Roberts E, Singh SB, Dong C, Wu L, Kominami E, Ueno T, Yamamoto A et al (2009) Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol 186:255–268
34. Levine B, Deretic V (2007) Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol 7:767–777
35. Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469:323–335
36. Li J, Liu Y, Wang Z, Liu K, Wang Y, Liu J, Ding H, Yuan Z (2011) Subversion of cellular autophagy machinery by hepatitis B virus for viral envelopment. J Virol 85:6319–6333
37. Liang C, Lee JS, Inn KS, Gack MU, Li Q, Roberts EA, Vergne I, Deretic V, Feng P, Akazawa C et al (2008) Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat Cell Biol 10:776–787
38. Liu Q, Qin Y, Zhou L, Kou Q, Guo X, Ge X, Yang H, Hu H (2012) Autophagy sustains the replication of porcine reproductive and respiratory virus in host cells. Virology 429:136–147
39. Loo YM, Gale M Jr (2011) Immune signaling by RIG-I-like receptors. Immunity 34:680–692
40. Maier HJ, Britton P (2012) Involvement of autophagy in coronavirus replication. Viruses 4:3440–3451
41. Maier HJ, Cottam EM, Stevenson-Leggett P, Wilkinson JA, Harte CJ, Wileman T, Britton P (2013) Visualizing the autophagy pathway in avian cells and its application to studying infectious bronchitis virus. Autophagy 9:496–509
42. Matsunaga K, Noda T, Yoshimori T (2009) Binding Rubicon to cross the Rubicon. Autophagy 5:876–877
43. Mehrpour M, Esclatine A, Beau I, Codogno P (2010) Overview of macroautophagy regulation in mammalian cells. Cell Res 20:748–762
44. Mihaylova MM, Shaw RJ (2011) The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13:1016–1023
45. Mizushima N (2009) Physiological functions of autophagy. Curr Topics Microbiol Immunol 335:71–84
46. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140:313–326
47. Monastyrska I, Ulasli M, Rottier PJ, Guan JL, Reggiori F, de Haan CA (2013) An autophagy-independent role for LC3 in equine arteritis virus replication. Autophagy 9:164–174
48. Munz C (2011) Beclin-1 targeting for viral immune escape. Viruses 3:1166–1178
49. Orvedahl A, Levine B (2008) Viral evasion of autophagy. Autophagy 4:280–285
50. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjorkoy G, Johansen T (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131–24145
51. Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P (2008) Regulation of macroautophagy by mTOR and Beclin1 complexes. Biochimie 90:313–323
52. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR (2004) Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279:10136–10141
53. Rabinowitz JD, White E (2010) Autophagy and metabolism. Science (New York, N.Y.) 330:1344–1348
54. Reggiori F, Monastyrska I, Verheije MH, Cali T, Ulasli M, Bianchi S, Bernasconi R, de Haan CA, Molinari M (2010) Coronaviruses Hijack the LC3-I-positive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 7:500–508
55. Richards AL, Jackson WT (2013) How positive-strand RNA viruses benefit from autophagosome maturation. J Virol 87:9966–9972
56. Shintani T, Klionsky DJ (2004) Autophagy in health and disease: a double-edged sword. Science (New York, N.Y.) 306:990–995
57. Shoji-Kawata S, Levine B (2009) Autophagy, antiviral immunity, and viral countermeasures. Biochim Biophys Acta 1793:1478–1484
58. Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J, Onderwater JJ, van der Meulen J, Koerten HK, Mommaas AM (2006) Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80:5927–5940
59. Sumpter R Jr, Levine B (2011) Selective autophagy and viruses. Autophagy 7:260–265
60. Sun L, Xing Y, Chen X, Zheng Y, Yang Y, Nichols DB, Clementz MA, Banach BS, Li K, Baker SC, Chen Z (2012a) Coronavirus papain-like proteases negatively regulate antiviral innate immune response through disruption of STING-mediated signaling. PloS One 7:e30802
61. Sun MX, Huang L, Wang R, Yu YL, Li C, Li PP, Hu XC, Hao HP, Ishag HA, Mao X (2012b) Porcine reproductive and respiratory syndrome virus induces autophagy to promote virus replication. Autophagy 8:1434–1447
62. Tang SW, Chen CY, Klase Z, Zane L, Jeang KT (2013) The cellular autophagy pathway modulates human T-cell leukemia virus type 1 replication. J Virol 87:1699–1707
63. Weidberg H, Shvets E, Elazar Z (2011) Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 80:125–156
64. Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, Luo H (2008) Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 82:9143–9153
65. Xing Y, Chen J, Tu J, Zhang B, Chen X, Shi H, Baker SC, Feng L, Chen Z (2013) The papain-like protease of porcine epidemic diarrhea virus negatively regulates type I interferon pathway by acting as a viral deubiquitinase. J Gen Virol 94:1554–1567
66. Yang ZJ, Chee CE, Huang S, Sinicrope FA (2011) The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther 10:1533–1541
67. Yang X, Chen X, Bian G, Tu J, Xing Y, Wang Y, Chen Z (2014) Proteolytic processing, deubiquitinase and interferon antagonist activities of Middle East respiratory syndrome coronavirus papain-like protease. J Gen Virol 95:614–626
68. Zhao Z, Thackray LB, Miller BC, Lynn TM, Becker MM, Ward E, Mizushima NN, Denison MR, Virgin HWT (2007) Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3:581–585
69. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, Heintz N, Yue Z (2009a) Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 11:468–476
70. Zhong Y, Wang QJ, Yue Z (2009b) Atg14L and Rubicon: yin and yang of Beclin 1-mediated autophagy control. Autophagy 5:890–891
71. Zhou H, Perlman S (2007) Mouse hepatitis virus does not induce Beta interferon synthesis and does not inhibit its induction by double-stranded RNA. J Virol 81:568–574