Betanodavirus up-regulates chaperone GRP78 via ER stress: Roles of GRP78 in viral replication and host mitochondria-mediated cell death

Apoptosis

Volumn 16, Issue 3, 2011, Pages 272-287

  Su, Yu Chin ^a   Wu, Jen Leih ^b   Hong, Jiann Ruey ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

Author keywords

Bcl 2; ER stress; GRP78; Mitochondria; Nervous necrosis virus; siRNA

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CASPASE 12; CHAPERONE; GLUCOSE REGULATED PROTEIN 78; PROTEIN BCL 2; RNA POLYMERASE;

ANIMAL CELL; ARTICLE; BETANODAVIRUS; CELL DEATH; ENDOPLASMIC RETICULUM STRESS; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MITOCHONDRION; NODAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA VIRUS; UPREGULATION; VIRUS REPLICATION;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; CELL DEATH; CELL LINE; CELL SURVIVAL; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; EIF-2 KINASE; ENDOPLASMIC RETICULUM; FISHES; GENE KNOCKDOWN TECHNIQUES; HEAT-SHOCK PROTEINS; MITOCHONDRIA; NODAVIRIDAE; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA, VIRAL; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; UP-REGULATION; VIRAL LOAD; VIRAL PROTEINS; VIRUS REPLICATION;

BETANODAVIRUS; EPINEPHELINAE; REDSPOTTED GROUPER NERVOUS NECROSIS VIRUS; RNA VIRUSES; STRIPED JACK NERVOUS NECROSIS VIRUS;

EID: 79952194891     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-010-0565-x     Document Type: Article

References (58)

1. LA Ball KL Johnson 1999 Reverse genetics of nodaviruses Adv Virus Res 53 229 244 10582101 10.1016/S0065-3527(08)60350-4 1:CAS:528:DC%2BD3cXnt1CgtQ%3D%3D
2. BL Munday J Kwang N Moody 2002 Betanodavirus infections of teleost fish: a review J Fish Dis 25 127 142 10.1046/j.1365-2761.2002.00350.x (Pubitemid 34267855)
3. A Schneemann V Reddy JE Johson 1998 The structural and function of nodavirus particles: a paradigm for understanding chemical biology Adv Virus Res 50 381 446 9521003 10.1016/S0065-3527(08)60812-X 1:CAS:528:DyaK1cXhvVais74%3D
4. V Toffolo E Negrisolo C Maltese G Bovo P Belvedere L Colombo LD Valle 2006 Phylogeny of betanodaviruses and molecular evolution of their RNA polymerase and coat proteins Mol Phylogenet Evol 43 298 308 16990016 10.1016/j.ympev.2006.08.003 (Pubitemid 46484344)
5. K Mori T Nakai K Muroga M Arimoto K Mushiake I Furusawa 1992 Properties of a new virus belonging to nodaviridae found in larval striped jack (Pseudocaranx dentex) with nervous necrosis Virology 187 368 371 1736540 10.1016/0042-6822(92)90329-N 1:STN:280:DyaK387kt1Ghug%3D%3D
6. YX Guo T Wei K Dallmann J Kwang 2003 Induction of caspase-dependent apoptosis by betanodaviruses GGNNV and demonstration of protein alpha as an apoptosis inducer Virology 308 74 82 12706091 10.1016/S0042-6822(02)00098-3 1:CAS:528:DC%2BD3sXivFeku7c%3D (Pubitemid 36428966)
7. HC Wu CS Chiu JL Wu HY Gong MC Chen MW Lu JR Hong 2008 Zebrafish anti-apoptotic protein zfBcl-xL can block betanodavirus protein alpha-induced mitochondria-mediated secondary necrosis cell death Fish Shellfish Immunol 24 436 449 18276161 10.1016/j.fsi.2008.01.001 1:CAS:528:DC%2BD1cXjtVels7g%3D
8. LJ Chen YC Su JR Hong 2009 Betanodavirus non-structural protein B1: a novel anti-necrotic death factor that modulates cell death in early replication cycle in fish cells Virology 385 444 454 19136133 10.1016/j.virol.2008.11.048 1:CAS:528:DC%2BD1MXisFOnt7w%3D
9. BJ Fenner R Thiagarajan HK Chua J Kwang 2006 Betanodavirus B2 is an RNA interference antagonist that facilitates intracellular viral RNA accumulation J Virol 80 85 94 16352533 10.1128/JVI.80.1.85-94.2006 1:CAS:528: DC%2BD28Xjslaltrs%3D
10. T Iwamoto K Mise A Takeda Y Okinaka K Mori M Arimoto T Okuno T Nakai 2005 Characterization of Striped jack nervous necrosis virus subgenomic RNA3 and biological activities of its encoded protein B2 J Gen Virol 86 2807 2816 16186236 10.1099/vir.0.80902-0 1:CAS:528:DC%2BD2MXhtFSrsrbE (Pubitemid 41410472)
11. SP Chen JL Wu YC Su JR Hong 2007 Anti-Bcl-2 family members, zfBcl-x(L) and zfMcl-1a, prevent cytochrome c release from cells undergoing betanodavirus-induced secondary necrotic cell death Apoptosis 12 1043 1060 17245642 10.1007/s10495-006-0032-x 1:CAS:528:DC%2BD2sXkvFKit70%3D (Pubitemid 46701602)
12. HL Su CL Liao YL Lin 2002 Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response J Virol 76 4162 4171 11932381 10.1128/JVI.76.9.4162-4171.2002 1:CAS:528:DC%2BD38XivFGju7g%3D (Pubitemid 34309551)
13. HP Harding M Calfon F Urano I Novoa D Ron 2002 Transcriptional and translational control in the Mammalian unfolded protein response Annu Rev Cell Dev Biol 18 575 599 12142265 10.1146/annurev.cellbio.18.011402.160624 1:CAS:528:DC%2BD38XptVOqs70%3D (Pubitemid 35387362)
14. RJ Kaufman D Scheuner M Schroder X Shen K Lee CY Liu SM Arnold 2002 The unfolded protein response in nutrient sensing and differentiation Nat Rev Mol Cell Biol 3 411 421 12042763 10.1038/nrm829 1:CAS:528:DC%2BD38Xltlart7Y%3D (Pubitemid 34685699)
15. XD Li H Lankinen N Putkuri O Vapalahti A Vaheri 2005 Tula hantavirus triggers pro-apoptotic signals of ER stress in Vero E6 cells Virology 333 180 189 15708603 10.1016/j.virol.2005.01.002 1:CAS:528:DC%2BD2MXhtlelt70%3D (Pubitemid 40222201)
16. RV Rao DE Bredesen 2004 Misfolded proteins, endoplasmic reticulum stress and neurodegeneration Curr Opin Cell Biol 16 653 662 15530777 10.1016/j.ceb.2004.09.012 1:CAS:528:DC%2BD2cXpsVOrtbg%3D (Pubitemid 39463116)
17. BL Williams WI Lipkin 2006 Endoplasmic reticulum stress and neurodegeneration in rats neonatally infected with borna disease virus J Virol 80 8613 8626 16912310 10.1128/JVI.00836-06 1:CAS:528:DC%2BD28XovVOjtLg%3D (Pubitemid 44384872)
18. X Chen J Shen R Prywes 2002 The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi J Biol Chem 277 13045 13052 11821395 10.1074/jbc.M110636200 1:CAS:528:DC%2BD38XivFSjsbY%3D (Pubitemid 34952673)
19. K Lee W Tirasophon X Shen M Prywes R Okada RH Yoshida K Mori RJ Kaufman 2002 IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response Genes Dev 16 452 466 11850408 10.1101/gad.964702 1:CAS:528:DC%2BD38XhvFKgs7s%3D (Pubitemid 34165102)
20. E Szegezdi SE Logue AM Gorman A Samali 2006 Mediators of endoplasmic reticulum stress-induced apoptosis EMBO Rep 7 880 885 16953201 10.1038/sj.embor.7400779 1:CAS:528:DC%2BD28XptVSlsLo%3D (Pubitemid 44523966)
21. D Baltzis LK Qu S Papadopoulou JD Blais JC Bell N Sonenberg AE Koromilas 2004 Resistance to vesicular stomatitis virus infection requires a functional cross talk between the eukaryotic translation initiation factor 2 alpha kinases PERK and PKR J Virol 78 12747 12761 15542627 10.1128/JVI.78.23.12747-12761.2004 1:CAS:528:DC%2BD2cXhtVaqtbrF (Pubitemid 39507783)
22. CL Netherton JC Parsley T Wileman 2004 African swine fever virus inhibits induction of the stress-induced proapoptotic transcription factor CHOP/GADD153 J Virol 78 10825 10838 15367650 10.1128/JVI.78.19.10825-10828.2004 1:CAS:528:DC%2BD2cXotVemtLc%3D (Pubitemid 39258408)
23. B He 2006 Viruses, endoplasmic reticulum stress, and interferon responses Cell Death Differ 13 393 403 16397582 10.1038/sj.cdd.4401833 1:CAS:528:DC%2BD28Xhtl2mtL4%3D (Pubitemid 43979439)
24. DE Dimcheff MA Faasse FJ McAtee JL Portis 2004 Endoplasmic reticulum (ER) stress induced by a neurovirulent mouse retrovirus is associated with prolonged BiP binding and retention of a viral protein in the ER J Biol Chem 279 33782 33790 15178688 10.1074/jbc.M403304200 1:CAS:528:DC%2BD2cXmtFOiu7s%3D (Pubitemid 39063027)
25. KD Tardif K Mori A Siddiqui 2002 Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway J Virol 76 7453 7459 12097557 10.1128/JVI.76.15.7453-7459.2002 1:CAS:528:DC%2BD38XltlKru7o%3D (Pubitemid 34760967)
26. V Bitko S Barik 2001 An endoplasmic reticulum-specific stress-activated caspase (caspase-12) is implicated in the apoptosis of A549 epithelial cells by respiratory syncytial virus J Cell Biochem 80 441 454 11135374 10.1002/1097-4644(20010301)80:3<441::AID-JCB170>3.0.CO;2-C 1:STN:280:DC%2BD3M3islShug%3D%3D (Pubitemid 32141499)
27. SN Farrow R Brown 1996 New members of the Bcl-2 family and their protein partners Curr Opin Genet Dev 6 45 49 8791486 10.1016/S0959-437X(96)90009-X 1:CAS:528:DyaK28XhtVWgtLs%3D
28. ZN Oltvai CL Milliman SJ Korsmeyer 1993 Bcl-2 hetrodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death Cell 74 609 619 8358790 10.1016/0092-8674(93)90509-O 1:CAS:528:DyaK3sXms1eqtbs%3D (Pubitemid 23259742)
29. N Zamzami G Kroemer 2001 The mitochondrion in apoptosis: how Pandora's box opens Nat Rev Mol Cell Biol 2 67 71 11413468 10.1038/35048073 1:CAS:528:DC%2BD3MXivVWmsLw%3D (Pubitemid 33676964)
30. S Oyadomari M Mori 2004 Roles of CHOP/GADD153 in endoplasmic reticulum stress Cell Death Differ 11 381 389 14685163 10.1038/sj.cdd.4401373 1:CAS:528:DC%2BD2cXit12ntbc%3D (Pubitemid 38489416)
31. SP Chen HL Yang GM Her HY Lin MF Jeng JL Wu JR Hong 2006 Betanodavirus induces phosphatidylserine exposure and loss of mitochondrial membrane potential in secondary necrotic cells, both of which are blocked by bongkrekic acid Virology 347 379 391 16430940 10.1016/j.virol.2005.11.052 1:CAS:528: DC%2BD28XjvVaisLc%3D (Pubitemid 44316553)
32. HC Wu JL Wu HL Chu YC Su JR Hong 2010 RGNNV induces mitochondria-mediated cell death via newly synthesized protein dependent pathway in fish cells Fish Shellfish Immunol 29 457 463
33. YC Su JL Wu JR Hong 2009 Betanodavirus non-structural protein B2: a novel necrotic death factor that induces mitochondria-mediated cell death in fish cells Virology 385 143 154 19116179 10.1016/j.virol.2008.11.036 1:CAS:528:DC%2BD1MXitlWnsrs%3D
34. B Nicholson J Dunn 1974 Homologous viral interference in trout and Atlantic salmon cell cultures infected with infectious pancreatic necrosis virus J Virol 14 180 182 4836601 1:STN:280:DyaE2c3lsVCrtQ%3D%3D
35. GH Yang S Li JJ Pestka 2000 Down-regulation of the endoplasmic reticulum chaperone GRP78/BiP by vomitoxin (Deoxynivalenol) Toxicol Appl Pharmacol 162 207 217 10652249 10.1006/taap.1999.8842 1:CAS:528:DC%2BD3cXnsVWlsg%3D%3D (Pubitemid 30102098)
36. UK Laemmli 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685 5432063 10.1038/227680a0 1:CAS:528:DC%2BD3MXlsFags7s%3D
37. SR Kain K Mai P Sinai 1994 Human multiple tissue western blots: a new immunological tool for the analysis of tissue-specific protein expression Biotechniques 17 982 987 7840980 1:CAS:528:DyaK2cXmvFKntbs%3D
38. JR Hong JL Wu 2002 Induction of apoptotic death in cells via Bad gene expression by infectious pancreatic necrosis virus infection Cell Death Differ 9 113 124 11840162 10.1038/sj.cdd.4400933 1:CAS:528:DC%2BD38XitFegtro%3D
39. PC Chen JL Wu GM Her JR Hong 2010 Aquatic birnavirus induces necrotic cell death via mitochondria-mediated caspases pathway that inhibited by bongkrekic acid Fish Shellfish Immunol 28 344 353 19944168 10.1016/j.fsi.2009. 11.014 1:CAS:528:DC%2BC3cXhtlGgtrw%3D
40. PD Mullen RJ Brand GN Parlette 1975 Evaluation of dye exclusion and colony inhibition techniques for detection of polyoma-specific, cell-mediated immunity J Natl Cancer Inst 54 229 231 163318 1:STN:280:DyaE2M%2FpslGktQ%3D%3D
41. KB Mezeth S Nylund H Henrisksen S Patel AH Nerland AM Szilvay 2007 RNA-dependent RNA polymerase from Atlantic halibut nodavirus contains two signals for localization to the mitochondria Virus Res 130 43 52 17602779 10.1016/j.virusres.2007.05.014 1:CAS:528:DC%2BD2sXht12gurbP (Pubitemid 350051088)
42. DJ Miller P Ahlquist 2002 Flock house virus RNA polymerase is a transmembrane protein with amino-terminal sequences sufficient for mitochondrial localization and membrane insertion J Virol 76 9856 9867 12208963 10.1128/JVI.76.19.9856-9867.2002 1:CAS:528:DC%2BD38XntFGksLk%3D (Pubitemid 35006525)
43. M Priscilla V Wynsberghe P Ahlquist 2009 5′ cis elements direct nodavirus RNA1 recruitment to mitochondrial sites of replication complex formation J Virol 83 2976 2988 10.1128/JVI.02040-08
44. G Bovo T Nishizawa C Maltese F Borghesan F Mutinelli F Montesi S De Mas 1999 Viral encephalopathy and retinopathy of farmed marine fish species in Italy Virus Res 63 143 146 10509726 10.1016/S0168-1702(99)00068-4 1:CAS:528:DyaK1MXls12js74%3D (Pubitemid 29413003)
45. RA Mazzarella N Marcus SM Haugejorden JM Balcarek JJ Baldassare B Roy LJ Li AS Lee M Green 1994 Erp61 is GRP58, a stress-inducible luminal endoplasmic reticulum protein, but is devoid of phosphatidylinositide-specific phospholipase C activity Arch Biochem Biophys 308 454 460 8109975 10.1006/abbi.1994.1064 (Pubitemid 24171423)
46. HL Pahl 1999 Signal transduction from the endoplasmic reticulum to the cell nucleus Physiol Rev 79 683 701 10390516 1:CAS:528:DyaK1MXksFemtrw%3D (Pubitemid 29330171)
47. NJ Buchkovich TG Maquire Y Yu AW Paton JC Paton JC Alwine 2007 Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly J Virol 82 31 39 17942541 10.1128/JVI.01881-07 (Pubitemid 350309120)
48. RJ Davis 2000 Signal transduction by the JNK group of MAP kinases Cell 103 239 252 11057897 10.1016/S0092-8674(00)00116-1 1:CAS:528: DC%2BD3cXns1Cltrk%3D
49. M Lamkanfi M Kalai P Vandenabeele 2004 Caspase-12: an overview Cell Death Differ 11 365 368 14685161 10.1038/sj.cdd.4401364 1:CAS:528: DC%2BD2cXit12ntbs%3D (Pubitemid 38489413)
50. T Yoneda K Imaizumi K Oono D Yui F Gomi T Katayama M Tohyama 2001 Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress J Biol Chem 276 13935 13940 11278723 1:CAS:528:DC%2BD3MXjt12rsr0%3D
51. DT Rutkowski RJ Kaufman 2004 A trip to the ER: coping with stress Trends Cell Biol 14 20 28 14729177 10.1016/j.tcb.2003.11.001 1:CAS:528: DC%2BD2cXjtFegsw%3D%3D (Pubitemid 38076857)
52. PJ Dufresne K Thivierge S Cotton C Beauchemin C Ide E Ubalijoro JF Laliberte MG Fortin 2008 Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles Virology 374 217 227 18222516 10.1016/j.virol.2007.12.014 1:CAS:528: DC%2BD1cXks12gsbg%3D
53. DJ Miller MD Schwartz P Ahlquist 2001 Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells J Virol 75 11664 11676 11689648 10.1128/JVI.75.23.11664-11676.2001 1:CAS:528:DC%2BD3MXotlaqs7o%3D (Pubitemid 33063258)
54. SA Weeks WP Shield C Sahi EA Craig S Rospert DJ Miller 2010 A targeted analysis of cellular chaperones reveals contrasting roles for heat shock protein 70 in flock house virus RNA replication J Virol 84 330 339 19828623 10.1128/JVI.01808-09 1:CAS:528:DC%2BC3cXisVKiu78%3D
55. M Germain JP Mathai GC Shore 2002 BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria J Biol Chem 277 18053 18060 11884414 10.1074/jbc.M201235200 1:CAS:528: DC%2BD38XktVCnu7k%3D (Pubitemid 34967618)
56. +: a control point for apoptosis Science 300 135 139 12624178 10.1126/science. 1081208 1:CAS:528:DC%2BD3sXis1Cgt7Y%3D (Pubitemid 36423046)
57. MC Wei WX Zong EH Cheng T Lindsten V Panoutsakopoulou AJ Ross KA Roth GR MacGregor CB Thompson SJ Korsmeyer 2001 Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 727 730 11326099 10.1126/science.1059108 1:CAS:528:DC%2BD3MXjt1eltr0%3D (Pubitemid 32385543)
58. I Kim W Xu JC Reed 2008 Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities Nat Rev Drug Discov 7 1013 1030 19043451 10.1038/nrd2755 1:CAS:528:DC%2BD1cXhsVenu7%2FM