An autophagy-independent role for LC3 in equine arteritis virus replication

Autophagy

Volumn 9, Issue 2, 2013, Pages 164-174

  Monastyrska, Iryna ^a   Ulasli, Mustafa ^d   Rottier, Peter J M ^a   Guan, Jun Lin ^c   Reggiori, Fulvio ^b   De Haan, Cornelis A M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d GAZIANTEP UNIVERSITY   (Turkey)

Author keywords

Arterivirus; Autophagy; Double membrane vesicles; LC3; Nidoviruses

Indexed keywords

DOUBLE STRANDED RNA; MICROTUBULE ASSOCIATED PROTEIN 1; PROTEIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; EQUINE VIRAL ARTERITIS VIRUS; IMMUNOELECTRON MICROSCOPY; LIGHT CHAIN; LIGHT CHAIN 3; MEMBRANE VESICLE; NONHUMAN; PROTEIN DEPLETION; RNA REPLICATION; VIRUS REPLICATION;

EID: 84873677330     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.22743     Document Type: Article

References (53)

1. den Boon JA, Ahlquist P. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 2010; 64:241-56; PMID:20825348; http://dx.doi.org/10.1146/annurev.micro.112408.134012.
2. den Boon JA, Diaz A, Ahlquist P. Cytoplasmic viral replication complexes. Cell Host Microbe 2010; 8:77- 85; PMID:20638644; http://dx.doi.org/10.1016/j. chom.2010.06.010.
3. Mackenzie J. Wrapping things up about virus RNA replication. Traffic 2005; 6:967-77; PMID:16190978; http://dx.doi.org/10.1111/j.1600-0854.2005.00339. x.
4. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ. Nidovirales: evolving the largest RNA virus genome. Virus Res 2006; 117:17-37; PMID:16503362; http://dx.doi.org/10.1016/j.virusres.2006.01.017.
5. de Vries AAF, Horzinek MC, Rottier PJM, de Groot RJ. The genome organization of the nidovirales: Similarities and differences between arteri-, toro-, and coronaviruses. Semin Virol 1997; 8:33-47; http://dx.doi.org/10.1006/ smvy.1997.0104.
6. Pedersen KW, van der Meer Y, Roos N, Snijder EJ. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulumderived double-membrane vesicles which carry the viral replication complex. J Virol 1999; 73:2016-26; PMID:9971782.
7. van der Meer Y, van Tol H, Locker JK, Snijder EJ. ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J Virol 1998; 72:6689-98; PMID:9658116.
8. Knoops K, Bárcena M, Limpens RW, Koster AJ, Mommaas AM, Snijder EJ. Ultrastructural characterization of arterivirus replication structures: reshaping the endoplasmic reticulum to accommodate viral RNA synthesis. J Virol 2012; 86:2474-87; PMID:22190716; http://dx.doi.org/10.1128/JVI.06677-11.
9. Snijder EJ, van Tol H, Roos N, Pedersen KW. Nonstructural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex. J Gen Virol 2001; 82:985-94; PMID:11297673.
10. Lin LT, Dawson PW, Richardson CD. Viral interactions with macroautophagy: a double-edged sword. Virology 2010; 402:1-10; PMID:20413139; http://dx.doi.org/10.1016/j.virol.2010.03.026.
11. Taylor MP, Kirkegaard K. Potential subversion of autophagosomal pathway by picornaviruses. Autophagy 2008; 4:286-9; PMID:18094610.
12. Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009; 5:527- 49; PMID:19527881; http://dx.doi.org/10.1016/j.chom. 2009.05.016.
13. Sumpter R Jr., Levine B. Selective autophagy and viruses. Autophagy 2011; 7:260-5; PMID:21150267; http://dx.doi.org/10.4161/auto.7.3.14281.
14. Taylor MP, Kirkegaard K. Modification of cellular autophagy protein LC3 by poliovirus. J Virol 2007; 81:12543-53; PMID:17804493; http://dx.doi.org/10. 1128/JVI.00755-07.
15. Wong J, Zhang J, Si X, Gao G, Mao I, McManus BM, et al. Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 2008; 82:9143- 53; PMID:18596087; http://dx.doi.org/10.1128/JVI.00641-08.
16. Yoon SY, Ha YE, Choi JE, Ahn J, Lee H, Kweon HS, et al. Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. J Virol 2008; 82:11976-8; PMID:18799585; http://dx.doi.org/10.1128/JVI.01028- 08.
17. Klein KA, Jackson WT. Human rhinovirus 2 induces the autophagic pathway and replicates more efficiently in autophagic cells. J Virol 2011; 85:9651- 4; PMID:21752910; http://dx.doi.org/10.1128/JVI.00316-11.
18. Klein KA, Jackson WT. Picornavirus subversion of the autophagy pathway. Viruses 2011; 3:1549- 61; PMID:21994795; http://dx.doi.org/10.3390/v3091549.
19. Zhang Y, Li Z, Ge X, Guo X, Yang H. Autophagy promotes the replication of encephalomyocarditis virus in host cells. Autophagy 2011; 7:613- 28; PMID:21460631; http://dx.doi.org/10.4161/auto.7.6.15267.
20. O'Donnell V, Pacheco JM, LaRocco M, Burrage T, Jackson W, Rodriguez LL, et al. Foot-and-mouth disease virus utilizes an autophagic pathway during viral replication. Virology 2011; 410:142-50; PMID:21112602; http://dx.doi.org/10. 1016/j.virol.2010.10.042.
21. Huang SC, Chang CL, Wang PS, Tsai Y, Liu HS. Enterovirus 71-induced autophagy detected in vitro and in vivo promotes viral replication. J Med Virol 2009; 81:1241-52; PMID:19475621; http://dx.doi.org/10.1002/jmv.21502.
22. Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol 2012; 22:R29- 34; PMID:22240478; http://dx.doi.org/10. 1016/j.cub.2011.11.034.
23. Chen Y, Klionsky DJ. The regulation of autophagy - unanswered questions. J Cell Sci 2011; 124:161- 70; PMID:21187343; http://dx.doi.org/10.1242/jcs. 064576.
24. Kabeya Y, Mizushima N, Yamamoto A, Oshitani- Okamoto S, Ohsumi Y, Yoshimori T. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117:2805-12; PMID:15169837; http://dx.doi.org/10.1242/jcs.01131.
25. Reggiori F, Monastyrska I, Verheije MH, Calì T, Ulasli M, Bianchi S, et al. Coronaviruses Hijack the LC3-Ipositive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 2010; 7:500-8; PMID:20542253; http://dx.doi.org/10.1016/j.chom.2010.05.013.
26. de Haan CA, Molinari M, Reggiori F. Autophagyindependent LC3 function in vesicular traffic. Autophagy 2010; 6:994-6; PMID:20814233; http://dx.doi.org/10. 4161/auto.6.7.13309.
27. Calì T, Galli C, Olivari S, Molinari M. Segregation and rapid turnover of EDEM1 by an autophagy-like mechanism modulates standard ERAD and folding activities. Biochem Biophys Res Commun 2008; 371:405- 10; PMID:18452703; http://dx.doi.org/10.1016/j.bbrc.2008.04.098.
28. Knoops K, Kikkert M, Worm SH, Zevenhoven-Dobbe JC, van der Meer Y, Koster AJ, et al. SARS-coronavirus replication is supported by a reticulovesicular network of modified endoplasmic reticulum. PLoS Biol 2008; 6:e226; PMID:18798692; http://dx.doi.org/10.1371/journal.pbio.0060226.
29. Hagemeijer MC, Verheije MH, Ulasli M, Shaltiël IA, de Vries LA, Reggiori F, et al. Dynamics of coronavirus replication-transcription complexes. J Virol 2010; 84:2134-49; PMID:20007278; http://dx.doi.org/10.1128/JVI.01716-09.
30. Gillespie LK, Hoenen A, Morgan G, Mackenzie JM. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J Virol 2010; 84:10438-47; PMID:20686019; http://dx.doi.org/10.1128/ JVI.00986-10.
31. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 2006; 80:5059-64; PMID:16641297; http://dx.doi.org/10.1128/JVI.80.10.5059-5064.2006.
32. Hyde JL, Sosnovtsev SV, Green KY, Wobus C, Virgin HW, Mackenzie JM. Mouse norovirus replication is associated with virus-induced vesicle clusters originating from membranes derived from the secretory pathway. J Virol 2009; 83:9709-19; PMID:19587041; http://dx.doi.org/10.1128/JVI.00600-09.
33. Ulasli M, Verheije MH, de Haan CA, Reggiori F. Qualitative and quantitative ultrastructural analysis of the membrane rearrangements induced by coronavirus. Cell Microbiol 2010; 12:844-61; PMID:20088951; http://dx.doi.org/ 10.1111/j.1462-5822.2010.01437.x.
34. Suhy DA, Giddings TH Jr., Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 2000; 74:8953- 65; PMID:10982339; http://dx.doi.org/10.1128/JVI.74.19.8953-8965.2000.
35. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; http://dx.doi.org/10.1083/ jcb.200412022.
36. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009; 461:654-8; PMID:19794493; http://dx.doi.org/10.1038/nature08455.
37. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720- 8; PMID:11060023; http://dx.doi.org/10.1093/emboj/19.21.5720.
38. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-75; PMID:18188003.
39. Cottam EM, Maier HJ, Manifava M, Vaux LC, Chandra-Schoenfelder P, Gerner W, et al. Coronavirus nsp6 proteins generate autophagosomes from the endoplasmic reticulum via an omegasome intermediate. Autophagy 2011; 7:1335-47; PMID:21799305; http//dx.doi.org/10.4161/auto.7.11.16642.
40. Stertz S, Reichelt M, Spiegel M, Kuri T, Martínez- Sobrido L, García-Sastre A, et al. The intracellular sites of early replication and budding of SARS-coronavirus. Virology 2007; 361:304-15; PMID:17210170; http://dx.doi.org/10.1016/j.virol.2006.11.027.
41. Zhao Z, Thackray LB, Miller BC, Lynn TM, Becker MM, Ward E, et al. Coronavirus replication does not require the autophagy gene ATG5. Autophagy 2007; 3:581-5; PMID:17700057.
42. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR. Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 2004; 279:10136-41; PMID:14699140; http://dx.doi.org/10.1074/jbc. M306124200.
43. Prentice E, McAuliffe J, Lu X, Subbarao K, Denison MR. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J Virol 2004; 78:9977-86; PMID:15331731; http://dx.doi.org/10.1128/ JVI.78.18.9977-9986.2004.
44. Al-Younes HM, Al-Zeer MA, Khalil H, Gussmann J, Karlas A, Machuy N, et al. Autophagy-independent function of MAP-LC3 during intracellular propagation of Chlamydia trachomatis. Autophagy 2011; 7:814- 28; PMID:21464618; http://dx.doi.org/10.4161/auto.7.8.15597.
45. Bernasconi R, Galli C, Noack J, Bianchi S, de Haan CA, Reggiori F, et al. Role of the SEL1L:LC3-I complex as an ERAD tuning receptor in the mammalian ER. Mol Cell 2012; 46:809-19; PMID:22633958; http://dx.doi.org/10.1016/j.molcel. 2012.04.017.
46. Gosert R, Kanjanahaluethai A, Egger D, Bienz K, Baker SC. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 2002; 76:3697-708; PMID:11907209; http://dx.doi.org/10.1128/JVI.76.8.3697-3708.2002.
47. Reggiori F, de Haan CA, Molinari M. Unconventional use of LC3 by coronaviruses through the alleged subversion of the ERAD tuning pathway. Viruses 2011; 3:1610-23; PMID:21994798; http://dx.doi.org/10.3390/v3091610.
48. Hara T, Takamura A, Kishi C, Iemura S, Natsume T, Guan JL, et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 2008; 181:497-510; PMID:18443221; http://dx.doi.org/10.1083/ jcb.200712064.
49. de Vries AA, Chirnside ED, Bredenbeek PJ, Gravestein LA, Horzinek MC, Spaan WJ. All subgenomic mRNAs of equine arteritis virus contain a common leader sequence. Nucleic Acids Res 1990; 18:3241- 7; PMID:2162519; http://dx.doi.org/10.1093/nar/18.11.3241.
50. Elroy-Stein O, Moss B. Gene expression using the vaccinia virus/T7 RNA polymerase hybrid system. Curr Protoc Mol Biol 2001; Chapter 16:Unit16.19.
51. Verheije MH, Raaben M, Mari M, Te Lintelo EG, Reggiori F, van Kuppeveld FJ, et al. Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog 2008; 4:e1000088; PMID:18551169; http://dx.doi.org/10.1371/journal.ppat.1000088.
52. Castillo-Olivares J, Wieringa R, Bakonyi T, de Vries AA, Davis-Poynter NJ, Rottier PJ. Generation of a candidate live marker vaccine for equine arteritis virus by deletion of the major virus neutralization domain. J Virol 2003; 77:8470-80; PMID:12857916; http://dx.doi.org/10.1128/JVI.77.15.8470-8480. 2003.
53. Vennema H, Rijnbrand R, Heijnen L, Horzinek MC, Spaan WJ. Enhancement of the vaccinia virus/phage T7 RNA polymerase expression system using encephalomyocarditis virus 5'-untranslated region sequences. Gene 1991; 108:201-9; PMID:1660838; http://dx.doi.org/10.1016/0378-1119(91)90435-E.