Up-regulation of Mcl-1 and bak by coronavirus infection of human, avian and animal cells modulates apoptosis and viral replication

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Zhong, Yanxin ^a   Liao, Ying ^a   Fang, Shouguo ^a   Tam, James P ^a   Liu, Ding Xiang ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAK; PROTEIN MCL 1; SMALL INTERFERING RNA; VIRUS PROTEIN; DDIT3 PROTEIN, HUMAN; MESSENGER RNA; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; AVIAN INFECTIOUS BRONCHITIS VIRUS; CHICKEN; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; FIBROBLAST; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UPREGULATION; VERO CELL; VIRUS CELL INTERACTION; VIRUS PARTICLE; VIRUS REPLICATION; ANIMAL; CERCOPITHECUS; CHICK EMBRYO; CORONAVIRUS INFECTION; DNA MICROARRAY; DOWN REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; VIROLOGY;

ANIMALIA; AVES; AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS; MAMMALIA;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; CHICKENS; CORONAVIRUS INFECTIONS; DOWN-REGULATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATIDYLINOSITOL 3-KINASES; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-BCL-2; RNA INTERFERENCE; RNA, MESSENGER; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION, GENETIC; UP-REGULATION; VERO CELLS; VIRUS REPLICATION;

EID: 84855655888     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030191     Document Type: Article

References (52)

1. Hay S, Kannourakis G, (2002) A time to kill: viral manipulation of the cell death program. J Gen Virol 83: 1547-1564.
2. Ren J, Shi M, Liu R, Yang QH, Johnson T, et al. (2005) The Birc6 (Bruce) gene regulates p53 and the mitochondrial pathway of apoptosis and is essential for mouse embryonic development. Proc Natl Acad Sci U S A 102: 565-570.
3. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, et al. (2007) ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129: 1337-1349.
4. Reed JC, (2000) Mechanisms of apoptosis. Am J Pathol 157: 1415-1430.
5. Elmore S, (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35: 495-516.
6. Assuncao Guimaraes C, Linden R, (2004) Programmed cell deaths. Apoptosis and alternative deathstyles. Eur J Biochem 271: 1638-1650.
7. Adams JM, Cory S, (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26: 61-66.
8. Galonek HL, Hardwick JM, (2006) Upgrading the BCL-2 network. Nat Cell Biol 8: 1317-1319.
9. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, et al. (2000) Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7: 1166-1173.
10. Ferri KF, Kroemer G, (2001) Organelle-specific initiation of cell death pathways. Nat Cell Biol 3: E255-263.
11. Li J, Lee B, Lee AS, (2006) Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 281: 7260-7270.
12. Leu JI, Dumont P, Hafey M, Murphy ME, George DL, (2004) Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex. Nat Cell Biol 6: 443-450.
13. Willis SN, Chen L, Dewson G, Wei A, Naik E, et al. (2005) Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19: 1294-1305.
14. Barber GN, (2001) Host defense, viruses and apoptosis. Cell Death Differ 8: 113-126.
15. O'Brien V, (1998) Viruses and apoptosis. J Gen Virol 79 (Pt 8): 1833-1845.
16. Liu C, Xu HY, Liu DX, (2001) Induction of caspase-dependent apoptosis in cultured cells by the avian coronavirus infectious bronchitis virus. J Virol 75: 6402-6409.
17. Peiris JS, Guan Y, Yuen KY, (2004) Severe acute respiratory syndrome. Nat Med 10: S88-97.
18. King DJ, Cavanagh D, (1991) Infectious Bronchitis. In: Calnek BW, Barnes HJ, Beard CW, Reid WM, Yoder HWJ, editors. Disease of Poultry Ames, Iowa Iowa State University Press pp. 471-484.
19. Picault JP, Drouin P, Guittet M, Bennejean G, Protais J, et al. (1986) Isolation, characterisation and preliminary cross-protection studies with a new pathogenic avian infectious bronchitis virus (strain PL-84084). Avian Pathol 15: 367-383.
20. Landman WJ, Feberwee A, (2004) Aerosol-induced Mycoplasma synoviae arthritis: the synergistic effect of infectious bronchitis virus infection. Avian Pathol 33: 591-598.
21. Matthijs MG, van Eck JH, Landman WJ, Stegeman JA, (2003) Ability of Massachusetts-type infectious bronchitis virus to increase colibacillosis susceptibility in commercial broilers: a comparison between vaccine and virulent field virus. Avian Pathol 32: 473-481.
22. Shen S, Wen ZL, Liu DX, (2003) Emergence of a coronavirus infectious bronchitis virus mutant with a truncated 3b gene: functional characterization of the 3b protein in pathogenesis and replication. Virology 311: 16-27.
23. Fang SG, Shen S, Tay FP, Liu DX, (2005) Selection of and recombination between minor variants lead to the adaptation of an avian coronavirus to primate cells. Biochem Biophys Res Commun 336: 417-423.
24. Xu LH, Huang M, Fang SG, Liu DX, (2011) Coronavirus infection induces DNA replication stress partly through interaction of its nonstructural protein 13 with the p125 subunit of DNA polymerase delta. J Biol Chem 286: 39546-39559.
25. Liao Y, Wang X, Huang M, Tam JP, Liu DX, (2011) Regulation of the p38 mitogen-activated protein kinase and dual-specificity phosphatase 1 feedback loop modulates the induction of interleukin 6 and 8 in cells infected with coronavirus infectious bronchitis virus. Virology 420: 106-116.
26. Liu DX, Inglis SC, (1992) Identification of two new polypeptides encoded by mRNA5 of the coronavirus infectious bronchitis virus. Virology 186: 342-347.
27. Shen S, Law YC, Liu DX, (2004) A single amino acid mutation in the spike protein of coronavirus infectious bronchitis virus hampers its maturation and incorporation into virions at the nonpermissive temperature. Virology 326: 288-298.
28. Liu DX, Inglis SC, (1991) Association of the infectious bronchitis virus 3c protein with the virion envelope. Virology 185: 911-917.
29. Shen H, Fang SG, Chen B, Chen G, Tay FP, et al. (2009) Towards construction of viral vectors based on avian coronavirus infectious bronchitis virus for gene delivery and vaccine development. J Virol Methods 160: 48-56.
30. Li FQ, Tam JP, Liu DX, (2007) Cell cycle arrest and apoptosis induced by the coronavirus infectious bronchitis virus in the absence of p53. Virology 365: 435-445.
31. Adams KW, Cooper GM, (2007) Rapid turnover of mcl-1 couples translation to cell survival and apoptosis. J Biol Chem 282: 6192-6200.
32. Cuconati A, Mukherjee C, Perez D, White E, (2003) DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells. Genes Dev 17: 2922-2932.
33. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.
34. Boulares AH, Yakovlev AG, Ivanova V, Stoica BA, Wang G, et al. (1999) Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 274: 22932-22940.
35. Kim I, Xu W, Reed JC, (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7: 1013-1030.
36. Ariyama Y, Tanaka Y, Shimizu H, Shimomura K, Okada S, et al. (2008) The role of CHOP messenger RNA expression in the link between oxidative stress and apoptosis. Metabolism 57: 1625-1635.
37. Oyadomari S, Mori M, (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11: 381-389.
38. McCullough KD, Martindale JL, Klotz LO, Aw TY, Holbrook NJ, (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21: 1249-1259.
39. Wang YC, Kulp SK, Wang D, Yang CC, Sargeant AM, et al. (2008) Targeting endoplasmic reticulum stress and Akt with OSU-03012 and gefitinib or erlotinib to overcome resistance to epidermal growth factor receptor inhibitors. Cancer Res 68: 2820-2830.
40. Longo PG, Laurenti L, Gobessi S, Sica S, Leone G, et al. (2008) The Akt/Mcl-1 pathway plays a prominent role in mediating antiapoptotic signals downstream of the B-cell receptor in chronic lymphocytic leukemia B cells. Blood 111: 846-855.
41. Shen Y, Shenk TE, (1995) Viruses and apoptosis. Curr Opin Genet Dev 5: 105-111.
42. Kurokawa M, Koyama AH, Yasuoka S, Adachi A, (1999) Influenza virus overcomes apoptosis by rapid multiplication. Int J Mol Med 3: 527-530.
43. Mi J, Li ZY, Ni S, Steinwaerder D, Lieber A, (2001) Induced apoptosis supports spread of adenovirus vectors in tumors. Hum Gene Ther 12: 1343-1352.
44. Yan H, Xiao G, Zhang J, Hu Y, Yuan F, et al. (2004) SARS coronavirus induces apoptosis in Vero E6 cells. J Med Virol 73: 323-331.
45. Kim H, Rafiuddin-Shah M, Tu HC, Jeffers JR, Zambetti GP, et al. (2006) Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 8: 1348-1358.
46. Rajalingam K, Sharma M, Lohmann C, Oswald M, Thieck O, et al. (2008) Mcl-1 is a key regulator of apoptosis resistance in Chlamydia trachomatis-infected cells. PLoS One 3: e3102.
47. Pearce AF, Lyles DS, (2009) Vesicular stomatitis virus induces apoptosis primarily through Bak rather than Bax by inactivating Mcl-1 and Bcl-XL. J Virol 83: 9102-9112.
48. Wang X, Liao Y, Yap PL, Png KJ, Tam JP, et al. (2009) Inhibition of protein kinase R activation and upregulation of GADD34 expression play a synergistic role in facilitating coronavirus replication by maintaining de novo protein synthesis in virus-infected cells. J Virol 83: 12462-12472.
49. Jiang CC, Lucas K, Avery-Kiejda KA, Wade M, deBock CE, et al. (2008) Up-regulation of Mcl-1 is critical for survival of human melanoma cells upon endoplasmic reticulum stress. Cancer Res 68: 6708-6717.
50. Dong L, Jiang CC, Thorne RF, Croft A, Yang F, et al. (2011) Ets-1 mediates upregulation of Mcl-1 downstream of XBP-1 in human melanoma cells upon ER stress. Oncogene.
51. Liu TC, Wang Y, Hallden G, Brooks G, Francis J, et al. (2005) Functional interactions of antiapoptotic proteins and tumor necrosis factor in the context of a replication-competent adenovirus. Gene Ther 12: 1333-1346.
52. Cao X, Yang M, Wei RC, Zeng Y, Gu JF, et al. (2011) Cancer targeting Gene-Viro-Therapy of liver carcinoma by dual-regulated oncolytic adenovirus armed with TRAIL gene. Gene Ther.