Role of individual caspases induced by astrovirus on the processing of its structural protein and its release from the cell through a non-lytic mechanism

Virology

Volumn 401, Issue 2, 2010, Pages 322-332

  Banos Lara, Ma del Rocío ^a   Méndez, Ernesto ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Astrovirus; Capsid protein processing; Caspases; Virus release

Indexed keywords

CASPASE; CASPASE 3; CASPASE 8; CASPASE 9; PROTEIN VP90; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; ASTROVIRUS; ASTROVIRUS INFECTION; CELL FUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME STRUCTURE; GENE MAPPING; GENETIC TRANSFECTION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN SECRETION; CELL LINE; GENE SILENCING; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN PROCESSING; VIRUS ASSEMBLY; VIRUS RELEASE;

ASTROVIRIDAE; HUMAN ASTROVIRUS; MIRIDAE;

CASPASES; CELL LINE; GENE SILENCING; HUMANS; MAMASTROVIRUS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, SMALL INTERFERING; VIRAL STRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS RELEASE;

EID: 77952318926     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.02.028     Document Type: Article

References (73)

1. Austin C.D., Lawrence D.A., Peden A.A., Varfolomeev E.E., Totpal K., De Maziere A.M., Klumperman J., Arnott D., Pham V., Scheller R.H., Ashkenazi A. Death-receptor activation halts clathrin-dependent endocytosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(27):10283-10288.
2. Backes C., Kuentzer J., Lenhof H.P., Comtesse N., Meese E. GraBCas: a bioinformatics tool for score-based prediction of caspase- and granzyme B-cleavage sites in protein sequences. Nucleic Acids Res. 2005, 33(Web Server issue):W208-W213.
3. Barber G.N. Host defense, viruses and apoptosis. Cell Death Differ. 2001, 8(2):113-126.
4. Baxendale W., Mebatsion T. The isolation and characterisation of astroviruses from chickens. Avian Pathol. 2004, 33(3):364-370.
5. Behling-Kelly E., Schultz-Cherry S., Koci M., Kelley L., Larsen D., Brown C. Localization of astrovirus in experimentally infected turkeys as determined by in situ hybridization. Vet. Pathol. 2002, 39(5):595-598.
6. Bertrand R., Solary E., O'Connor P., Kohn K.W., Pommier Y. Induction of a common pathway of apoptosis by staurosporine. Exp. Cell Res. 1994, 211(2):314-321.
7. Bideshi D.K., Tan Y., Bigot Y., Federici B.A. A viral caspase contributes to modified apoptosis for virus transmission. Genes Dev. 2005, 19(12):1416-1421.
8. Deretic V., Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009, 5(6):527-549.
9. Doseff A.I. Apoptosis: the sculptor of development. Stem Cells Dev. 2004, 13(5):473-483.
10. Finkbeiner S.R., Le B.M., Holtz L.R., Storch G.A., Wang D. Detection of newly described astrovirus MLB1 in stool samples from children. Emerg. Infect. Dis. 2009, 15(3):441-444.
11. Fischer U., Janicke R.U., Schulze-Osthoff K. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ. 2003, 10(1):76-100.
12. Fuentes-Prior P., Salvesen G.S. The protein structures that shape caspase activity, specificity, activation and inhibition. Biochem. J. 2004, 384(Pt 2):201-232.
13. Gallimore C.I., Taylor C., Gennery A.R., Cant A.J., Galloway A., Lewis D., Gray J.J. Use of a heminested reverse transcriptase PCR assay for detection of astrovirus in environmental swabs from an outbreak of gastroenteritis in a pediatric primary immunodeficiency unit. J. Clin. Microbiol. 2005, 43(8):3890-3894.
14. Garcia-Calvo M., Peterson E.P., Rasper D.M., Vaillancourt J.P., Zamboni R., Nicholson D.W., Thornberry N.A. Purification and catalytic properties of human caspase family members. Cell Death Differ. 1999, 6(4):362-369.
15. Geigenmuller U., Chew T., Ginzton N., Matsui S.M. Processing of nonstructural protein 1a of human astrovirus. J. Virol. 2002, 76(4):2003-2008.
16. Germain M., Affar E.B., D'Amours D., Dixit V.M., Salvesen G.S., Poirier G.G. Cleavage of automodified poly(ADP-ribose) polymerase during apoptosis. Evidence for involvement of caspase-7. J. Biol. Chem. 1999, 274(40):28379-28384.
17. Groene W.S., Shaw R.D. Psoralen preparation of antigenically intact noninfectious rotavirus particles. J. Virol. Methods 1992, 38(1):93-102.
18. Guix S., Bosch A., Ribes E., Dora Martinez L., Pinto R.M. Apoptosis in astrovirus-infected CaCo-2 cells. Virology 2004, 319(2):249-261.
19. Guix S., Caballero S., Bosch A., Pinto R.M. C-terminal nsP1a protein of human astrovirus colocalizes with the endoplasmic reticulum and viral RNA. J. Virol. 2004, 78(24):13627-13636.
20. Hildeman D., Jorgensen T., Kappler J., Marrack P. Apoptosis and the homeostatic control of immune responses. Curr. Opin. Immunol. 2007, 19(5):516-521.
21. Hitomi J., Katayama T., Eguchi Y., Kudo T., Taniguchi M., Koyama Y., Manabe T., Yamagishi S., Bando Y., Imaizumi K., Tsujimoto Y., Tohyama M. Involvement of caspase-4 in endoplasmic reticulum stress-induced apoptosis and Abeta-induced cell death. J. Cell Biol. 2004, 165(3):347-356.
22. Hitomi J., Katayama T., Taniguchi M., Honda A., Imaizumi K., Tohyama M. Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci. Lett. 2004, 357(2):127-130.
23. Hu P., Han Z., Couvillon A.D., Exton J.H. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J. Biol. Chem. 2004, 279(47):49420-49429.
24. Inoue S., Browne G., Melino G., Cohen G.M. Ordering of caspases in cells undergoing apoptosis by the intrinsic pathway. Cell Death Differ. 2009, 16(7):1053-1061.
25. Jackson W.T., Giddings T.H., Taylor M.P., Mulinyawe S., Rabinovitch M., Kopito R.R., Kirkegaard K. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005, 3(5):e156.
26. Jiang B., Monroe S.S., Koonin E.V., Stine S.E., Glass R.I. RNA sequence of astrovirus: distinctive genomic organization and a putative retrovirus-like ribosomal frameshifting signal that directs the viral replicase synthesis. Proc. Natl. Acad. Sci. U. S. A. 1993, 90(22):10539-10543.
27. Jonassen C.M., Jonassen T.O., Saif Y.M., Snodgrass D.R., Ushijima H., Shimizu M., Grinde B. Comparison of capsid sequences from human and animal astroviruses. J. Gen. Virol. 2001, 82(Pt 5):1061-1067.
28. Kang J.J., Schaber M.D., Srinivasula S.M., Alnemri E.S., Litwack G., Hall D.J., Bjornsti M.A. Cascades of mammalian caspase activation in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 1999, 274(5):3189-3198.
29. Koopmans M.P., Bijen M.H., Monroe S.S., Vinje J. Age-stratified seroprevalence of neutralizing antibodies to astrovirus types 1 to 7 in humans in The Netherlands. Clin. Diagn. Lab. Immunol. 1998, 5(1):33-37.
30. Kuranaga E., Miura M. Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol. 2007, 17(3):135-144.
31. Li M., Li H., Li C., Zhou S., Guo L., Liu H., Jiang W., Liu X., Li P., McNutt M.A., Li G. Alpha fetoprotein is a novel protein-binding partner for caspase-3 and blocks the apoptotic signaling pathway in human hepatoma cells. Int. J. Cancer 2009, 124(12):2845-2854.
32. Lowe M., Lane J.D., Woodman P.G., Allan V.J. Caspase-mediated cleavage of syntaxin 5 and giantin accompanies inhibition of secretory traffic during apoptosis. J. Cell Sci. 2004, 117(Pt 7):1139-1150.
33. MacFarlane M. TRAIL-induced signalling and apoptosis. Toxicol. Lett. 2003, 139(2-3):89-97.
34. McLean J.E., Ruck A., Shirazian A., Pooyaei-Mehr F., Zakeri Z.F. Viral manipulation of cell death. Curr. Pharm. Des. 2008, 14(3):198-220.
35. McStay G.P., Salvesen G.S., Green D.R. Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ. 2008, 15(2):322-331.
36. Mebratu Y., Tesfaigzi Y. How ERK1/2 activation controls cell proliferation and cell death: Is subcellular localization the answer?. Cell Cycle 2009, 8(8):1168-1175.
37. Mendez E., Arias C.F. Astrovirus. Virology 2007, 982-1000. Raven Press, New York, (Vol. vol. 1., 2 vols). D.N.K.B.N. Fields, P.M. Howley (Eds.).
38. Mendez E., Fernandez-Luna T., Lopez S., Mendez-Toss M., Arias C.F. Proteolytic processing of a serotype 8 human astrovirus ORF2 polyprotein. J. Virol. 2002, 76(16):7996-8002.
39. Mendez E., Salas-Ocampo M.P., Munguia M.E., Arias C.F. Protein products of the open reading frames encoding nonstructural proteins of human astrovirus serotype 8. J. Virol. 2003, 77(21):11378-11384.
40. Mendez E., Salas-Ocampo E., Arias C.F. Caspases mediate processing of the capsid precursor and cell release of human astroviruses. J. Virol. 2004, 78(16):8601-8608.
41. Mendez E., Aguirre-Crespo G., Zavala G., Arias C.F. Association of the astrovirus structural protein VP90 with membranes plays a role in virus morphogenesis. J. Virol. 2007, 81(19):10649-10658.
42. Mendez-Toss M., Romero-Guido P., Munguia M.E., Mendez E., Arias C.F. Molecular analysis of a serotype 8 human astrovirus genome. J. Gen. Virol. 2000, 81(Pt 12):2891-2897.
43. Monroe S.S., Jiang B., Stine S.E., Koopmans M., Glass R.I. Subgenomic RNA sequence of human astrovirus supports classification of Astroviridae as a new family of RNA viruses. J. Virol. 1993, 67(6):3611-3614.
44. Montero, H., Rojas, M., Arias, C.F., Lopez, S., 2008. Rotavirus infection induces the phosphorylation of eIF2alpha but prevents the formation of stress granules. J. Virol. 82 (3), 1496-504.
45. Moser L.A., Schultz-Cherry S. Suppression of astrovirus replication by an ERK1/2 inhibitor. J. Virol. 2008, 82(15):7475-7482.
46. Moser L.A., Carter M., Schultz-Cherry S. Astrovirus increases epithelial barrier permeability independently of viral replication. J. Virol. 2007, 81(21):11937-11945.
47. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403(6765):98-103.
48. Ramuz O., Isnardon D., Devilard E., Charafe-Jauffret E., Hassoun J., Birg F., Xerri L. Constitutive nuclear localization and initial cytoplasmic apoptotic activation of endogenous caspase-3 evidenced by confocal microscopy. Int. J. Exp. Pathol. 2003, 84(2):75-81.
49. Rao R.V., Hermel E., Castro-Obregon S., del Rio G., Ellerby L.M., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J. Biol. Chem. 2001, 276(36):33869-33874.
50. Riedl S.J., Salvesen G.S. The apoptosome: signalling platform of cell death. Nat. Rev. Mol. Cell. Biol. 2007, 8(5):405-413.
51. Schulze-Osthoff K., Ferrari D., Los M., Wesselborg S., Peter M.E. Apoptosis signaling by death receptors. Eur. J. Biochem. 1998, 254(3):439-459.
52. Silva M.T., do Vale A., dos Santos N.M. Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications. Apoptosis 2008, 13(4):463-482.
53. Slee E.A., Harte M.T., Kluck R.M., Wolf B.B., Casiano C.A., Newmeyer D.D., Wang H.G., Reed J.C., Nicholson D.W., Alnemri E.S., Green D.R., Martin S.J. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 1999, 144(2):281-292.
54. Slee E.A., Adrain C., Martin S.J. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J. Biol. Chem. 2001, 276(10):7320-7326.
55. Stennicke H.R., Salvesen G.S. Biochemical characteristics of caspases-3, -6, -7, and -8. J. Biol. Chem. 1997, 272(41):25719-25723.
56. Stepczynska A., Lauber K., Engels I.H., Janssen O., Kabelitz D., Wesselborg S., Schulze-Osthoff K. Staurosporine and conventional anticancer drugs induce overlapping, yet distinct pathways of apoptosis and caspase activation. Oncogene 2001, 20(10):1193-1202.
57. Strater J., Walczak H., Pukrop T., Von Muller L., Hasel C., Kornmann M., Mertens T., Moller P. TRAIL and its receptors in the colonic epithelium: a putative role in the defense of viral infections. Gastroenterology 2002, 122(3):659-666.
58. Suliman A., Lam A., Datta R., Srivastava R.K. Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and -independent pathways. Oncogene 2001, 20(17):2122-2133.
59. Talanian R.V., Quinlan C., Trautz S., Hackett M.C., Mankovich J.A., Banach D., Ghayur T., Brady K.D., Wong W.W. Substrate specificities of caspase family proteases. J. Biol. Chem. 1997, 272(15):9677-9682.
60. Taylor M.B., Walter J., Berke T., Cubitt W.D., Mitchell D.K., Matson D.O. Characterisation of a South African human astrovirus as type 8 by antigenic and genetic analyses. J. Med. Virol. 2001, 64(3):256-261.
61. Taylor R.C., Cullen S.P., Martin S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell. Biol. 2008, 9(3):231-241.
62. Teodoro J.G., Branton P.E. Regulation of apoptosis by viral gene products. J. Virol. 1997, 71(3):1739-1746.
63. Tewari M., Quan L.T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D.R., Poirier G.G., Salvesen G.S., Dixit V.M. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995, 81(5):801-809.
64. Thornberry N.A., Rano T.A., Peterson E.P., Rasper D.M., Timkey T., Garcia-Calvo M., Houtzager V.M., Nordstrom P.A., Roy S., Vaillancourt J.P., Chapman K.T., Nicholson D.W. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 1997, 272(29):17907-17911.
65. Thornberry N.A., Chapman K.T., Nicholson D.W. Determination of caspase specificities using a peptide combinatorial library. Methods Enzymol. 2000, 322:100-110.
66. van Kuppeveld F.J., Hoenderop J.G., Smeets R.L., Willems P.H., Dijkman H.B., Galama J.M., Melchers W.J. Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. Embo J. 1997, 16(12):3519-3532.
67. Vandenabeele P., Vanden Berghe T., Festjens N. Caspase inhibitors promote alternative cell death pathways. Sci. STKE 2006, 2006(358):pe44.
68. Wang Q.H., Kakizawa J., Wen L.Y., Shimizu M., Nishio O., Fang Z.Y., Ushijima H. Genetic analysis of the capsid region of astroviruses. J. Med. Virol. 2001, 64(3):245-255.
69. Wang Z.B., Liu Y.Q., Cui Y.F. Pathways to caspase activation. Cell Biol. Int. 2005, 29(7):489-496.
70. Willcocks M.M., Carter M.J. Identification and sequence determination of the capsid protein gene of human astrovirus serotype 1. FEMS Microbiol. Lett. 1993, 114(1):1-7.
71. Wurzer W.J., Planz O., Ehrhardt C., Giner M., Silberzahn T., Pleschka S., Ludwig S. Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J. 2003, 22(11):2717-2728.
72. Yin X.M. Bid, a BH3-only multi-functional molecule, is at the cross road of life and death. Gene 2006, 369:7-19.
73. Yukioka F., Matsuzaki S., Kawamoto K., Koyama Y., Hitomi J., Katayama T., Tohyama M. Presenilin-1 mutation activates the signaling pathway of caspase-4 in endoplasmic reticulum stress-induced apoptosis. Neurochem. Int. 2008, 52(4-5):683-687.