Beta-nodavirus B2 protein induces hydrogen peroxide production, leading to Drp1-recruited mitochondrial fragmentation and cell death via mitochondrial targeting

Apoptosis

Volumn 19, Issue 10, 2014, Pages 1457-1470

  Su, Yu C ^a   Chiu, Hsuan W ^a   Hung, Jo C ^a   Hong, Jiann R ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Anti oxidants; Cell death; Hydrogen peroxide production; Mitochondrial fragmentation; Nervous necrosis virus; Oxidative stress

Indexed keywords

ACRIDINE ORANGE; BETA NODAVIRUS B2 PROTEIN; CATALASE; DYNAMIN; DYNAMIN 1 LIKE PROTEIN; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; VIRUS PROTEIN; FISH PROTEIN;

ANIMAL CELL; ARTICLE; ASSAY; CELL DAMAGE; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; EMBRYO DEATH; FEMALE; FERTILIZATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; UPREGULATION; ANIMAL; APOPTOSIS; CELL LINE; FISH DISEASE; GENETICS; METABOLISM; NODAVIRIDAE; PATHOPHYSIOLOGY; RNA VIRUS INFECTION; VETERINARY; VIROLOGY; ZEBRA FISH;

ANIMALS; APOPTOSIS; CELL LINE; DYNAMINS; FISH DISEASES; FISH PROTEINS; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA; NODAVIRIDAE; OXIDATIVE STRESS; RNA VIRUS INFECTIONS; VIRAL NONSTRUCTURAL PROTEINS; ZEBRAFISH;

EID: 84919869519     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-1016-x     Document Type: Article

References (48)

1. Ball L, Johnson K (1999) Reverse genetics of nodaviruses. Adv Virus Res 53:229-244
2. Bovo G, Nishizawa T, Maltese C, Borghesan F, Mutinelli F, Montesi F, De Mas S (1999) Viral encephalopathy and retinopathy of farmed marine fish species in Italy. Virus Res 63:143-146
3. Mori KI, Nakai T, Muroga K, Arimoto M, Mushiake K, Furusawa I (1992) Properties of a new virus belonging to nodaviridae found in larval striped jack (Pseudocaranx dentex) with nervous necrosis. Virology 187:368-371
4. Munday B, Kwang J, Moody N (2002) Betanodavirus infections of teleost fish: a review. J Fish Dis 25:127-142
5. Li H, Li W, Ding S (2002) Induction and suppression of RNA silencing by an animal virus. Science 296:1319-1321
6. Delsert C, Morin N, Comps M (1997) A fish encephalitis virus that differs from other nodaviruses by its capsid protein processing. Arch Virol 142:2359-2371
7. Wu HC, Chiu CS, Wu JL, Gong HY, Chen MC, Lu MW, Hong JR (2008) Zebrafish anti-apoptotic protein zfBcl-xL can block betanodavirus protein alpha-induced mitochondria-mediated secondary necrosis cell death. Fish Shell Immunol 24:436-449
8. Iwamoto T, Mise K, Takeda A, Okinaka Y, Mori K, Arimoto M, Okuno T, Nakai T (2005) Characterization of Striped jack nervous necrosis virus subgenomic RNA3 and biological activities of its encoded protein B2. J Gen Virol 86:2807-2816
9. Su YC, Wu JL, Hong JR (2009) Betanodavirus non-structural protein B2: a novel necrotic death factor that induces mitochondria-mediated cell death in fish cells. Virology 385:143-154
10. Chen LJ, Su YC, Hong JR (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
11. Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G, Li WX, Ding SW (2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436:1040-1043
12. Wang X, Aliyari R, Li W, Li H, Kim K, Carthew R, Atkinson P, Ding S (2006) RNA interference directs innate immunity against viruses in adult drosophila. Science 312:452-454
13. Jellinger KA (2003) General aspects of neurodegeneration. J Neural Transm Suppl 65:101-144
14. Taylor JP, Hardy J, Fischbeck KH (2002) Toxic proteins in neurodegenerative disease. Science 296:1991-1995
15. Krapfenbauer K, Engidawork E, Cairns N, Fountoulakis M, Lubee G (2003) Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders. Brain Res 967:152-160
16. Desagher S, Glowinski J, Premont J (1996) Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 16:2553-2562
17. Dringen R, Hampercht B (1997) Involvement of glutathione peroxidase and catalase in the disposal of exogenous hydrogen peroxide by cultured astroglial cells. Brain Res 759:67-75
18. Schiavone J, Hassan HM (1988) An assay for the detection of superoxide dismutase in individual Escherichia coli colonies. Anal Biochem 168:455-461
19. Shull S, Heintz NH, Periasamy M, Manohar M, Jansen YM, Marsh JP, Mossman BT (1991) Differential regulation of antioxidant enzymes in response to oxidants. J Biol Chem 266:24398-24403
20. Chen SP, Yang HL, Her GM, Lin HY, Jeng MF, Wu JL, Hong JR (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
21. Chen SP, Wu JL, Su YC, Hong JR (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
22. Su YC, Hong JR (2010) Betanodavirus B2 causes ATP depletion-induced cell death via mitochondrial targeting and complex II inhibition in vitro and in vivo. J Biol Chem 285(51):39801-39810
23. Chang CW, Su YC, Her GM, Ken CF, Hong JR (2011) Betanodavirus induces oxidative stress-mediated cell death that prevented by anti-oxidants and zfcatalase in fish cells. PLoS ONE 6:e25853
24. Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
25. Kain S, Mai K, Sinai P (1994) Human multiple tissue western blots: a new immunological tool for the analysis of tissue-specific protein expression. BioTechniques 17:982-987
26. Hong JR, Lin T, Hsu Y, Wu JL (1998) Apoptosis procedes necrosis of fish cell line by infectious pancreatic necrosis virus. Virology 250:76-84
27. Hong JR, Wu JL (2002) Induction of apoptotic death in cells via Bad gene expression by infectious pancreatic necrosis virus infection. Cell Death Differ 9:113-124
28. Hong JR, Lin GH, Lin CJ, Wang WP, Lee CC, Wu JL (2004) The phosphatidylserine receptor is required for the engulfment of dead apoptotic cell and for normal development in zebrafish. Development 131(21):5417-5427
29. Mullen PD, Brand RJ, Parlette GN (1975) Evaluation of dye exclusion and colony inhibition techniques for detection of polyoma-specific, cell-mediated immunity. J Natl Cancer Inst 54:229-231
30. Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf 2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47:1304-1309
31. Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11:872-884
32. Liesa M, Palacin M, Zorzano A (2009) Mitochondrial dynamics in mammalian health and disease. Physiol Rev 89:799-845
33. Chen XJ, Butow RA (2005) The organization and inheritance of the mitochondrial genome. Nat Rev Genet 6:815-825
34. Mozdy AD, McCaffery JM, Shaw JM (2000) Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol 151:367-380
35. Otsuga D, Keegan BR, Brisch E, Thatcher JW, Hermann GJ, Bleazard W, Shaw JM (1998) The dynamin-related GTPase, Dnm1p, controls mitochondrial morphology in yeast. J Cell Biol 143:333-349
36. Smirnova E, Griparic L, Shurland DL, van der Bliek AM (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell 12:2245-2256
37. Smirnova E, Shurland D, Ryazantsev SN, van der Bliek AM (1998) A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 143:351-358
38. Ingerman E, Perkins EM, Marino M, Mears JA, McCaffery JM, Hinshaw JE, Nunnari J (2005) Dnm1 forms spirals that are structurally tailored to fit mitochondria. J Cell Biol 170:1021-1027
39. Lackner LL, Horner LS, Nunnari J (2009) Mechanistic analysis of a dynamin effector. Science 325:874-877
40. Mears JA, Lackner LL, Fang S, Ingerman E, Nunnari J, Hinshaw JE (2011) Conformational changes in Dnm1 support a contractile mechanism for mitochondrial fission. Nat Struct Mol Biol 18:20-26
41. Legesse-Miller A, Massol RH, Kirchhausen T (2003) Constriction and Dnm1p recruitment are distinct processes in mitochondrial fission. Mol Biol Cell 14:1953-1963
42. Taguchi N, Ishihara N, Jofuku A, Oka T, Mihara K (2007) Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J Biol Chem 282:11521-11529
43. Kim H, Scimia MC, Wilkinson D, Trelles RD, Wood MR, Bowtell D, Dillin A, Mercola M, Ronai ZA (2011) Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol Cell 44:532-544
44. Cho DH, Nakamura T, Fang J, Cieplak P, Godzik A, Gu Z, Lipton SA (2009) S-Nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 324:102-105
45. Wang H, Song P, Du L, Tian W, Yue W, Liu M, Li D, Wang B, Zhu Y, Cao C, Zhou J, Chen Q (2011) Parkin ubiquitinates Drp1 for proteasome-dependent degradation: implication of dysregulated mitochondrial dynamics in Parkinson's disease. J Biol Chem 286:11649-11658
46. Figueroa-Romero C, Iniguez-Lluhi JA, Stadler J, Chang CR, Arnoult D, Keller PJ, Hong Y, Blackstone C, Feldman EL (2009) SUMOylation of the mitochondrial fission protein Drp1 occurs at multiple nonconsensus sites within the B domain and is linked to its activity cycle. FASEB J 23:3917-3927
47. Elgass K, Pakay J, Ryan MT, Palmer GS (2013) Recent advances into the understanding of mitochondrial fission. Biochim Biophys Acta 188:150-161
48. Hong JR (2013) Betanodavirus: mitochondrial disruption and necrotic cell death. World J Virol 2(1):1-5