Endoplasmic reticulum chaperones are involved in the morphogenesis of rotavirus infectious particles

Journal of Virology

Volumn 82, Issue 11, 2008, Pages 5368-5380

  Maruri Avidal, Liliana ^a   López, Susana ^a   Arias, Carlos F ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; CALRETICULIN; CHAPERONE; DISULFIDE; EGTAZIC ACID; GLUCOSE REGULATED PROTEIN 94; MONOCLONAL ANTIBODY; OLIGOSACCHARIDE; SINDBIS VIRUS NONSTRUCTURAL PROTEIN 4;

ANIMAL CELL; ARTICLE; CELL ORGANELLE; CHEMICAL BOND; ENDOPLASMIC RETICULUM; GENE SILENCING; HEAT TREATMENT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUALITY CONTROL; VIRUS ASSEMBLY; VIRUS INFECTION; VIRUS INFECTIVITY; VIRUS MORPHOGENESIS; VIRUS PARTICLE;

ANIMALS; CALNEXIN; CALRETICULIN; CELL LINE; DISULFIDES; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; MACACA MULATTA; MOLECULAR CHAPERONES; PROTEIN DISULFIDE-ISOMERASE; PROTEIN FOLDING; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; ROTAVIRUS; SENSITIVITY AND SPECIFICITY; VIRAL PROTEINS; VIRION; VIRUS INTERNALIZATION;

ROTAVIRUS;

EID: 43949107171     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02751-07     Document Type: Article

References (67)

1. Bergmann, C. C., D. Maass, M. S. Poruchynsky, P. H. Atkinson, and A. R. Bellamy. 1989. Topology of the non-structural rotavirus receptor glycoprotein NS28 in the rough endoplasmic reticulum. EMBO J. 8:1695-1703.
2. Buchner, J. 1999. Hsp90 & Co. - a holding for folding. Trends Biochem. Sci. 24:136-141.
3. Cabrai, C. M., Y. Liu, K. W. Moremen, and R. N. Sifers. 2002. Organizational diversity among distinct glycoprotein endoplasmic reticulum-associated degradation programs. Mol. Biol. Cell 13:2639-2650.
4. Cannon, K. S., D. N. Hebert, and A. Helenius. 1996. Glycan-dependent and -independent association of vesicular stomatitis virus G protein with calnexin. J. Biol. Chem. 271:14280-14284.
5. Choukhi, A., S. Ung, C. Wychowski, and J. Dubuisson. 1998. Involvement of endoplasmic reticulum chaperones in the folding of hepatitis C virus glycoproteins. J. Virol. 72:3851-3858.
6. Cuadras, M. A., B. B. Bordier, J. L. Zambrano, J. E. Ludert, and H. B. Greenberg. 2006. Dissecting rotavirus particle-raft interaction with small interfering RNAs: insights into rotavirus transit through the secretory pathway. J. Virol. 80:3935-3946.
7. Cuadras, M. A., D. A. Feigelstock, S. An, and H. B. Greenberg. 2002. Gene expression pattern in Caco-2 cells following rotavirus infection. J. Virol. 76:4467-1482.
8. Dormitzer, P. R., and H. B. Greenberg. 1992. Calcium chelation induces a conformational change in recombinant herpes simplex virus-1-expressed rotavirus VP7. Virology 189:828-832.
9. Ellgaard, L., M. Molinari, and A. Helenius. 1999. Setting the standards: quality control in the secretory pathway. Science 286:1882-1888.
10. Estes, M. K. 2001. Rotaviruses and their replication, p. 1747-1785. In D. M. Knipe et al. (ed.), Fields virology. Lippincott Williams & Wilkins, Philadelphia, PA.
11. Gaudin, Y. 1997. Folding of rabies virus glycoprotein: epitope acquisition and interaction with endoplasmic reticulum chaperones. J. Virol. 71:3742-3750.
12. Gething, M. J., K. McCammon, and J. Sambrook. 1986. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell 46:939-950.
13. Gonzalez, R. A., R. Espinosa, P. Romero, S. López, and C. F. Arias. 2000. Relative localization of viroplasmic and endoplasmic reticulum-resident rotavirus proteins in infected cells. Arch. Virol. 145:1963-1973.
14. Gonzalez, R. A., M. A. Torres-Vega, S. López, and C. F. Arias. 1998. In vivo interactions among rotavirus nonstructural proteins. Arch. Virol. 143:981-996.
15. Guerrero, C. A., S. Zárate, G. Corkidi, S. López, and C. F. Arias. 2000. Biochemical characterization of rotavirus receptors in MA104 cells. J. Virol. 74:9362-9371.
16. Hammond, C., and A. Helenius. 1993. A chaperone with a sweet tooth. Curr. Biol. 3:884-886.
17. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
18. Hammond, C., and A. Helenius. 1995. Quality control in the secretory pathway. Curr. Opin. Cell Biol. 7:523-529.
19. Helenius, A., and M. Aebi. 2004. Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73:1019-1049.
20. Hendershot, L., D. Bole, G. Kohler, and J. F. Kearney. 1987. Assembly and secretion of heavy chains that do not associate posttranslationally with immunoglobulin heavy chain-binding protein. J. Cell Biol. 104:761-767.
21. Hong, M., S. Luo, P. Baumeister, J. M. Huang, R. K. Gogia, M. Li, and A. S. Lee. 2004. Underglycosylation of ATF6 as a novel sensing mechanism for activation of the unfolded protein response. J. Biol. Chem. 279:11354-11363.
22. Hurtley, S. M., D. G. Bole, H. Hoover-Litty, A. Helenius, and C. S. Copeland. 1989. Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP). J. Cell Biol. 108:2117-2126.
23. Jindadamrongwech, S., C. Thepparit, and D. R. Smith. 2004. Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2. Arch. Virol. 149:915-927.
24. Kassenbrock, C. K., and R. B. Kelly. 1989. Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides. EMBO J. 8:1461-1467.
25. Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13:1211-1233.
26. Kleizen, B., and I. Braakman. 2004. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16:343-349.
27. Knarr, G., S. Modrow, A. Todd, M. J. Gething, and J. Buchner. 1999. BiP-binding sequences in HIV gp160. Implications for the binding specificity of Bip. J. Biol. Chem. 274:29850-29857.
28. Leitzgen, K., M. R. Knittler, and I. G. Haas. 1997. Assembly of immunoglobulin light chains as a prerequisite for secretion. A model for oligomerization-dependent subunit folding. J. Biol. Chem. 272:3117-3123.
29. 2+-ATPase inhibitor thapsigargin. J. Biol. Chem. 268:12003- 12009.
30. Liberek, K., J. Marszalek, D. Ang, C. Georgopoulos, and M. Zylicz. 1991. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88:2874-2878.
31. -ΔΔCT method. Methods 25:402-408.
32. López, T., M. Camacho, M. Zayas, R. Najera, R. Sánchez, C. F. Arias, and S. López. 2005. Silencing the morphogenesis of rotavirus. J. Virol. 79:184-192.
33. Ma, Y., and L. M. Hendershot. 2004. ER chaperone functions during normal and stress conditions. J. Chem. Neuroanat. 28:51-65.
34. Méndez, E., C. F. Arias, and S. López. 1996. Interactions between the two surface proteins of rotavirus may alter the receptor-binding specificity of the virus. J. Virol. 70:1218-1222.
35. Meunier, L., Y. K. Usherwood, K. T. Chung, and L. M. Hendershot. 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13:4456-4469.
36. Michelangeli, F., F. Liprandi, M. E. Chemello, M. Ciarlet, and M. C. Ruiz. 1995. Selective depletion of stored calcium by thapsigargin blocks rotavirus maturation but not the cytopathic effect. J. Virol. 69:3838-3847.
37. Mirazimi, A., M. Nilsson, and L. Svensson. 1998. The molecular chaperone calnexin interacts with the NSP4 enterotoxin of rotavirus in vivo and in vitro. J. Virol. 72:8705-8709.
38. Mirazimi, A., and L. Svensson. 1998. Carbohydrates facilitate correct disulfide bond formation and folding of rotavirus VP7. J. Virol. 72:3887-3892.
39. Mirazimi, A., and L. Svensson. 2000. ATP is required for correct folding and disulfide bond formation of rotavirus VP7. J. Virol. 74:8048-8052.
40. Mirazimi, A., C. H. von Bonsdorff, and L. Svensson. 1996. Effect of brefeldin A on rotavirus assembly and oligosaccharide processing. Virology 217:554-563.
41. Mir-Shekari, S. Y., D. A. Ashford, D. J. Harvey, R. A. Dwek, and I. T. Schulze. 1997. The glycosylation of the influenza A virus hemagglutinin by mammalian cells. A site-specific study. J. Biol. Chem. 272:4027-1036.
42. Molinari, M., K. K. Eriksson, V. Calanca, C. Galli, P. Cresswell, M. Michalak, and A. Helenius. 2004. Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell 13:125-135.
43. Molinari, M., C. Galli, V. Piccaluga, M. Pieren, and P. Paganetti. 2002. Sequential assistance of molecular chaperones and transient formation of covalent complexes during protein degradation from the ER. J. Cell Biol. 158:247-257.
44. Molinari, M., and R. Sitia. 2005. The secretory capacity of a cell depends on the efficiency of endoplasmic reticulum-associated degradation. Curr. Top. Microbiol. Immunol. 300:1-15.
45. Ohba, H., T. Harano, and T. Omura. 1981. Biosynthesis and turnover of a microsomal protein disulfide isomerase in rat liver. J. Biochem. (Tokyo) 89:901-907.
46. Pando, V., P. Isa, C. F. Arias, and S. López. 2002. Influence of calcium on the early steps of rotavirus infection. Virology 295:190-200.
47. Pelham, H. R. 1989. Control of protein exit from the endoplasmic reticulum. Annu. Rev. Cell Biol. 5:1-23.
48. Peterson, J. R., A. Ora, P. N. Van, and A. Helenius. 1995. Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol. Biol. Cell 6:1173-1184.
49. Poruchynsky, M. S., and P. H. Atkinson. 1991. Rotavirus protein rearrangements in purified membrane-enveloped intermediate particles. J. Virol. 65:4720-4727.
50. Rajagopalan, S., and M. B. Brenner. 1994. Calnexin retains unassembled major histocompatibility complex class I free heavy chains in the endoplasmic reticulum. J. Exp. Med. 180:407-412.
51. Resendez, E., Jr., J. W. Attenello, A. Gratsky, C. S. Chang, and A. S. Lee. 1985. Calcium ionophore A23187 induces expression of glucose-regulated genes and their heterologous fusion genes. Mol. Cell. Biol. 5:1212-1219.
52. Rothman, J. E. 1989. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell 59:591-601.
53. Ruddock, L. W., and M. Molinari. 2006. N-glycan processing in ER quality control. J. Cell Sci. 119:4373-4380.
54. 2+ that solubilizes outer capsid proteins from rotavirus particles is dependent on the strain. J. Virol. 70:4877-4883.
55. Satoh, M., A. Nakai, Y. Sokawa, K. Hirayoshi, and K. Nagata. 1993. Modulation of the phosphorylation of glucose-regulated protein, GRP78, by transformation and inhibition of glycosylation. Exp. Cell Res. 205:76-83.
56. Shen, J., X. Chen, L. Hendershot, and R. Prywes. 2002. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3:99-111.
57. Sitia, R., and I. Braakman. 2003. Quality control in the endoplasmic reticulum protein factory. Nature 426:891-894.
58. Snapp, E. L., A. Sharma, J. Lippincott-Schwartz, and R. S. Hegde. 2006. Monitoring chaperone engagement of substrates in the endoplasmic reticulum of live cells. Proc. Natl. Acad. Sci. USA 103:6536-6541.
59. Sullivan, D. C., L. Huminiecki, J. W. Moore, J. J. Boyle, R. Poulsom, D. Creamer, J. Barker, and R. Bicknell. 2003. EndoPDI, a novel protein-disulfide isomerase-like protein that is preferentially expressed in endothelial cells acts as a stress survival factor. J. Biol. Chem. 278:47079-47088.
60. Svensson, L., P. R. Dormitzer, C. H. von Bonsdorff, L. Maunula, and H. B. Greenberg. 1994. Intracellular manipulation of disulfide bond formation in rotavirus proteins during assembly. J. Virol. 68:5204-5215.
61. Trask, S. D., and P. R. Dormitzer. 2006. Assembly of highly infectious rotavirus particles recoated with recombinant outer capsid proteins. J. Virol. 80:11293-11304.
62. Triantafilou, K., D. Fradelizi, K. Wilson, and M. Triantafilou. 2002. GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J. Virol 76:633-643.
63. van Leeuwen, J. E., and K. P. Kearse. 1996. Calnexin associates exclusively with individual CD3 delta and T cell antigen receptor (TCR) alpha proteins containing incompletely trimmed glycans that are not assembled into multisubunit TCR complexes. J. Biol. Chem. 271:9660-9665.
64. Ware, F. E., A. Vassilakos, P. A. Peterson, M. R. Jackson, M. A. Lehrman, and D. B. Williams. 1995. The molecular chaperone calnexin binds Glc1Man9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J. Biol. Chem. 270:4697-4704.
65. Xu, A., A. R. Bellamy, and J. A. Taylor. 1998. BiP (GRP78) and endoplasmin (GRP94) are induced following rotavirus infection and bind transiently to an endoplasmic reticulum-localized virion component. J. Virol. 72:9865-9872.
66. Yoshida, H., K. Haze, H. Yanagi, T. Yura, and K. Mori. 1998. Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J. Biol. Chem. 273:33741-33749.
67. Zárate, S., R. Espinosa, P. Romero, C. A. Guerrero, C. F. Arias, and S. López. 2000. Integrin alpha2beta1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278:50-54.