Avian reovirus S1133-induced DNA damage signaling and subsequent apoptosis in cultured cells and in chickens

Archives of Virology

Volumn 156, Issue 11, 2011, Pages 1917-1929

  Lin, Ping Yuan ^a   Liu, Hung Jen ^b   Chang, Ching Dong ^c   Chang, Chi I ^c   Hsu, Jue Liang ^c   Liao, Ming Huei ^c   Lee, Jeng Woei ^a   Shih, Wen Ling ^c  

^a TZU CHI UNIVERSITY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c NATIONAL PINGTUNG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REGULATORY PROTEIN;

ANIMAL; ANIMAL DISEASE; APOPTOSIS; ARTICLE; AVIAN ORTHOREOVIRUS; BIRD DISEASE; CELL CULTURE; CHICKEN; GENETICS; GERMFREE ANIMAL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REOVIRUS INFECTION; SIGNAL TRANSDUCTION; VIROLOGY;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELLS, CULTURED; CHICKENS; ORTHOREOVIRUS, AVIAN; POULTRY DISEASES; REOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS;

AVIAN ORTHOREOVIRUS; GALLUS GALLUS;

EID: 80255124794     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-011-1063-3     Document Type: Article

References (61)

1. Benavente J, Martinez-Costas J (2007) Avian reovirus: structure and biology. Virus Res 123: 105-119.
2. Bodelon G, Labrada L, Martinez-Costas J, Benavente J (2002) Modification of late membrane permeability in avian reovirus-infected cells: viroporin activity of the S1-encoded nonstructural p10 protein. J Biol Chem 277: 17789-17796.
3. Brenner B, Koppenhoefer U, Weinstock C, Linderkamp O, Lang F, Gulbins E (1997) Fas- or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J Biol Chem 272: 22173-22181.
4. Brune B, Zhou J, von Knethen A (2003) Nitric oxide, oxidative stress, and apoptosis. Kidney Int Suppl: S22-S24.
5. Carriere A, Carmona MC, Fernandez Y, Rigoulet M, Wenger RH, Penicaud L, Casteilla L (2004) Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect. J Biol Chem 279: 40462-40469.
6. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802-805.
7. Chan SW, Egan PA (2005) Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J 19: 1510-1512.
8. Chen YT, Lin CH, Ji WT, Li SK, Liu HJ (2008) Proteasome inhibition reduces avian reovirus replication and apoptosis induction in cultured cells. J Virol Methods 151: 95-100.
9. Choi J, Ou JH (2006) Mechanisms of liver injury. III. Oxidative stress in the pathogenesis of hepatitis C virus. Am J Physiol Gastrointest Liver Physiol 290: G847-G851.
10. Chulu JL, Lee LH, Lee YC, Liao SH, Lin FL, Shih WL, Liu HJ (2007) Apoptosis induction by avian reovirus through p53 and mitochondria-mediated pathway. Biochem Biophys Res Commun 356: 529-535.
11. Chulu JL, Huang WR, Wang L, Shih WL, Liu HJ (2010) Avian reovirus non-structural protein p17-induced G2/M cell cycle arrest and host cellular protein translation shutoff involve activation of p53-dependent pathways. J Virol 84: 7683-7694.
12. Desmyter J, Melnick JL, Rawls WE (1968) Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J Virol 2: 955-961.
13. Du F, Wang L, Zhang Y, Jiang W, Sheng H, Cao Q, Wu J, Shen B, Shen T, Zhang JZ, Bao C, Li D, Li N (2008) Role of GADD45 beta in the regulation of synovial fluid T cell apoptosis in rheumatoid arthritis. Clin Immunol 128: 238-247.
14. Flory E, Kunz M, Scheller C, Jassoy C, Stauber R, Rapp UR, Ludwig S (2000) Influenza virus-induced NF-kappaB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IkappaB kinase. J Biol Chem 275: 8307-8314.
15. Fontanier-Razzaq N, McEvoy TG, Robinson JJ, Rees WD (2001) DNA damaging agents increase gadd153 (CHOP-10) messenger RNA levels in bovine preimplantation embryos cultured in vitro. Biol Reprod 64: 1386-1391.
16. Friedman AD (1996) GADD153/CHOP, a DNA damage-inducible protein, reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res 56: 3250-3256.
17. Gargouri B, van Pelt J, El Feki Ael F, Attia H, Lassoued S (2009) Induction of Epstein-Barr virus (EBV) lytic cycle in vitro causes oxidative stress in lymphoblastoid B cell lines. Mol Cell Biochem 324: 55-63.
18. Gouvea V, Schnitzer TJ (1982) Pathogenicity of avian reoviruses: examination of six isolates and a vaccine strain. Infect Immun 38: 731-738.
19. Harkin DP, Bean JM, Miklos D, Song YH, Truong VB, Englert C, Christians FC, Ellisen LW, Maheswaran S, Oliner JD, Haber DA (1999) Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell 97: 575-586.
20. Hsieh YH, Su IJ, Wang HC, Chang WW, Lei HY, Lai MD, Chang WT, Huang W (2004) Pre-S mutant surface antigens in chronic hepatitis B virus infection induce oxidative stress and DNA damage. Carcinogenesis 25: 2023-2032.
21. Hsu CJ, Wang CY, Lee LH, Shih WL, Chang CI, Cheng HL, Chulu JL, Ji WT, Liu HJ (2006) Development and characterization of monoclonal antibodies against avian reovirus sigma C protein and their application in detection of avian reovirus isolates. Avian Pathol 35: 320-326.
22. Jones RC, Kibenge FS (1984) Reovirus-induced tenosynovitis in chickens: the effect of breed. Avian Pathol 13: 511-528.
23. Kannan R, Gukasyan HJ, Zhang W, Trousdale MD, Kim KJ, Lee VH (2004) Impairment of conjunctival glutathione secretion and ion transport by oxidative stress in an adenovirus type 5 ocular infection model of pigmented rabbits. Free Radic Biol Med 37: 229-238.
24. Kavouras JH, Prandovszky E, Valyi-Nagy K, Kovacs SK, Tiwari V, Kovacs M, Shukla D, Valyi-Nagy T (2007) Herpes simplex virus type 1 infection induces oxidative stress and the release of bioactive lipid peroxidation by-products in mouse P19N neural cell cultures. J Neurovirol 13: 416-425.
25. Kuo YF, Su YZ, Tseng YH, Wang SY, Wang HM, Chueh PJ (2010) Flavokawain B, a novel chalcone from Alpinia pricei Hayata with potent apoptotic activity: Involvement of ROS and GADD153 upstream of mitochondria-dependent apoptosis in HCT116 cells. Free Radic Biol Med 49: 214-226.
26. Labrada L, Bodelon G, Vinuela J, Benavente J (2002) Avian reoviruses cause apoptosis in cultured cells: viral uncoating, but not viral gene expression, is required for apoptosis induction. J Virol 76: 7932-7941.
27. Lassoued S, Ben Ameur R, Ayadi W, Gargouri B, Ben Mansour R, Attia H (2008) Epstein-Barr virus induces an oxidative stress during the early stages of infection in B lymphocytes, epithelial, and lymphoblastoid cell lines. Mol Cell Biochem 313: 179-186.
28. Lawrence MC, McGlynn K, Naziruddin B, Levy MF, Cobb MH (2007) Differential regulation of CHOP-10/GADD153 gene expression by MAPK signaling in pancreatic beta-cells. Proc Natl Acad Sci USA 104: 11518-11525.
29. Leutner S, Eckert A, Muller WE (2001) ROS generation, lipid peroxidation and antioxidant enzyme activities in the aging brain. J Neural Transm 108: 955-967.
30. Lin CH, Shih WL, Lin FL, Hsieh YC, Kuo YR, Liao MH, Liu HJ (2009) Bovine ephemeral fever virus-induced apoptosis requires virus gene expression and activation of Fas and mitochondrial signaling pathway. Apoptosis 14: 864-877.
31. Lin HY, Chuang ST, Chen YT, Shih WL, Chang CD, Liu HJ (2007) Avian reovirus-induced apoptosis related to tissue injury. Avian Pathol 36: 155-159.
32. Lin PY, Liu HJ, Liao MH, Chang CD, Chang CI, Cheng HL, Lee JW, Shih WL (2010) Activation of PI 3-kinase/Akt/NF-kappaB and Stat3 signaling by avian reovirus S1133 in the early stages of infection results in an inflammatory response and delayed apoptosis. Virology 400: 104-114.
33. Lin YL, Liu CC, Chuang JI, Lei HY, Yeh TM, Lin YS, Huang YH, Liu HS (2000) Involvement of oxidative stress, NF-IL-6, and RANTES expression in dengue-2-virus-infected human liver cells. Virology 276: 114-126.
34. Lu HF, Hsueh SC, Ho YT, Kao MC, Yang JS, Chiu TH, Huamg SY, Lin CC, Chung JG (2007) ROS mediates baicalin-induced apoptosis in human promyelocytic leukemia HL-60 cells through the expression of the Gadd153 and mitochondrial-dependent pathway. Anticancer Res 27: 117-125.
35. Martinez-Costas J, Gonzalez-Lopez C, Vakharia VN, Benavente J (2000) Possible involvement of the double-stranded RNA-binding core protein sigmaA in the resistance of avian reovirus to interferon. J Virol 74: 1124-1131.
36. Mayerhofer T, Kodym R (2003) Gadd153 restores resistance to radiation-induced apoptosis after thiol depletion. Biochem Biophys Res Commun 310: 115-120.
37. Nakabayashi H, Taketa K, Miyano K, Yamane T, Sato J (1982) Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res 42: 3858-3863.
38. Ni Y, Kemp MC (1995) A comparative study of avian reovirus pathogenicity: virus spread and replication and induction of lesions. Avian Dis 39: 554-566.
39. Nicolini A, Ajmone-Cat MA, Bernardo A, Levi G, Minghetti L (2001) Human immunodeficiency virus type-1 Tat protein induces nuclear factor (NF)-kappaB activation and oxidative stress in microglial cultures by independent mechanisms. J Neurochem 79: 713-716.
40. Norbury CJ, Zhivotovsky B (2004) DNA damage-induced apoptosis. Oncogene 23: 2797-2808.
41. Olive PL, Banath JP (2009) Kinetics of H2AX phosphorylation after exposure to cisplatin. Cytometry B Clin Cytom 76: 79-90.
42. Pal S, Polyak SJ, Bano N, Qiu WC, Carithers RL, Shuhart M, Gretch DR, Das A (2010) Hepatitis C virus induces oxidative stress, DNA damage and modulates the DNA repair enzyme NEIL1. J Gastroenterol Hepatol 25: 627-634.
43. Paranjpe A, Cacalano NA, Hume WR, Jewett A (2008) Mechanisms of N-acetyl cysteine-mediated protection from 2-hydroxyethyl methacrylate-induced apoptosis. J Endod 34: 1191-1197.
44. Paranjpe A, Cacalano NA, Hume WR, Jewett A (2009) N-acetyl cysteine mediates protection from 2-hydroxyethyl methacrylate induced apoptosis via nuclear factor kappa B-dependent and independent pathways: potential involvement of JNK. Toxicol Sci 108: 356-366.
45. Pauklin S, Kristjuhan A, Maimets T, Jaks V (2005) ARF and ATM/ATR cooperate in p53-mediated apoptosis upon oncogenic stress. Biochem Biophys Res Commun 334: 386-394.
46. Pereg Y, Shkedy D, de Graaf P, Meulmeester E, Edelson-Averbukh M, Salek M, Biton S, Teunisse AF, Lehmann WD, Jochemsen AG, Shiloh Y (2005) Phosphorylation of Hdmx mediates its Hdm2- and ATM-dependent degradation in response to DNA damage. Proc Natl Acad Sci USA 102: 5056-5061.
47. Ping-Yuan L, Hung-Jen L, Meng-Jiun L, Feng-Ling Y, Hsue-Yin H, Jeng-Woei L, Wen-Ling S (2006) Avian reovirus activates a novel proapoptotic signal by linking Src to p53. Apoptosis 11: 2179-2193.
48. Quadrilatero J, Hoffman-Goetz L (2004) N-Acetyl-l-cysteine prevents exercise-induced intestinal lymphocyte apoptosis by maintaining intracellular glutathione levels and reducing mitochondrial membrane depolarization. Biochem Biophys Res Commun 319: 894-901.
49. Reed LJ, Muench H (1938) A simple method of estimating fifty percent endpoints. Am J Epidemiol 27: 493-497.
50. Reisner AH, Nemes P, Bucholtz C (1975) The use of Coomassie Brilliant Blue G250 perchloric acid solution for staining in electrophoresis and isoelectric focusing on polyacrylamide gels. Anal Biochem 64: 509-516.
51. Roos WP, Kaina B (2006) DNA damage-induced cell death by apoptosis. Trends Mol Med 12: 440-450.
52. Sarkaria JN, Busby EC, Tibbetts RS, Roos P, Taya Y, Karnitz LM, Abraham RT (1999) Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 59: 4375-4382.
53. Schaefer-Klein J, Givol I, Barsov EV, Whitcomb JM, VanBrocklin M, Foster DN, Federspiel MJ, Hughes SH (1998) The EV-O-derived cell line DF-1 supports the efficient replication of avian leukosis-sarcoma viruses and vectors. Virology 248: 305-311.
54. Shih WL, Hsu HW, Liao MH, Lee LH, Liu HJ (2004) Avian reovirus sigmaC protein induces apoptosis in cultured cells. Virology 321: 65-74.
55. Shmulevitz M, Corcoran J, Salsman J, Duncan R (2004) Cell-cell fusion induced by the avian reovirus membrane fusion protein is regulated by protein degradation. J Virol 78: 5996-6004.
56. Sinclair A, Yarranton S, Schelcher C (2006) DNA-damage response pathways triggered by viral replication. Expert Rev Mol Med 8: 1-11.
57. Spagnuolo G, D'Anto V, Cosentino C, Schmalz G, Schweikl H, Rengo S (2006) Effect of N-acetyl-L-cysteine on ROS production and cell death caused by HEMA in human primary gingival fibroblasts. Biomaterials 27: 1803-1809.
58. Tang KN, Fletcher OJ, Villegas P (1987) The effect on newborn chicks of oral inoculation of reovirus isolated from chickens with tenosynovitis. Avian Dis 31: 584-590.
59. van de Zande S, Kuhn EM (2007) Central nervous system signs in chickens caused by a new avian reovirus strain: a pathogenesis study. Vet Microbiol 120: 42-49.
60. Yang F, Yan S, He Y, Wang F, Song S, Guo Y, Zhou Q, Wang Y, Lin Z, Yang Y, Zhang W, Sun S (2008) Expression of hepatitis B virus proteins in transgenic mice alters lipid metabolism and induces oxidative stress in the liver. J Hepatol 48: 12-19.
61. Zhang W, Hoffman B, Liebermann DA (2001) Ectopic expression of MyD118/Gadd45/CR6 (Gadd45beta/alpha/gamma) sensitizes neoplastic cells to genotoxic stress-induced apoptosis. Int J Oncol 18: 749-757.