Hsp70 negatively controls rotavirus protein bioavailability in Caco-2 cells infected by the rotavirus RF strain

Journal of Virology

Volumn 81, Issue 3, 2007, Pages 1297-1304

  Broquet, Alexis H ^a,b   Lenoir, Christelle ^a,b   Gardet, Agnès ^a,b   Sapin, Catherine ^a,b   Chwetzoff, Serge ^a,b,d   Jouniaux, Anne Marie ^a,b   Lopez, Susana ^c   Trugnan, Germain ^a,b   Bachelet, Maria ^a,b   Thomas, Ginette ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b HÔPITAL SAINT ANTOINE   (France)

^c INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^d CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; PROTEASOME INHIBITOR; PROTEIN VP2; PROTEIN VP4; PROTEIN VP6; SMALL INTERFERING RNA; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BIOAVAILABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; ROTAVIRUS; UBIQUITINATION; VIROGENESIS; VIRUS INFECTION; VIRUS MORPHOGENESIS;

CACO-2 CELLS; GENE EXPRESSION REGULATION, VIRAL; HSP70 HEAT-SHOCK PROTEINS; HUMANS; ROTAVIRUS; VIRAL PROTEINS;

ROTAVIRUS;

EID: 33846484215     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01336-06     Document Type: Article

References (42)

1. Beere, H. M., B. B. Wolf, K. Cain, D. D. Mosser, A. Mahboubi, T. Kuwana, P. Tailor, R. I. Morimoto, G. M. Cohen, and D. R. Green. 2000. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2:469-475.
2. Brenner, B. G., and M. A. Wainberg. 1999. Heat shock protein-based therapeutic strategies against human immunodeficiency virus type 1 infection. Infect. Dis. Obstet. Gynecol. 7:80-90.
3. Broquet, A. H., G. Thomas, J. Masliah, G. Trugnan, and M. Bachelet. 2003. Expression of the molecular chaperone Hsp70 in detergent-resistant microdomains correlates with its membrane delivery and release. J. Biol. Chem. 278:21601-21606.
4. Bukau, B., and A. L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92:351-366.
5. Burns, J. W., H. B. Greenberg, R. D. Shaw, and M. K. Estes. 1988. Functional and topographical analyses of epitopes on the hemagglutinin (VP4) of the simian rotavirus SA11. J. Virol. 62:2164-2172.
6. Chromy, L. R., J. M. Pipas, and R. L. Garcea. 2003. Chaperone-mediated in vitro assembly of polyomavirus capsids. Proc. Natl. Acad. Sci. USA 100:10477-10482.
7. Ciarlet, M., and M. K. Estes. 2001. Interactions between rotavirus and gastrointestinal cells. Curr. Opin. Microbiol. 4:435-441.
8. 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. 76:4467-4482.
9. Dormitzer, P. R., E. B. Nason, B. V. Prasad, and S. C. Harrison. 2004. Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430:1053-1058.
10. Dormitzer, P. R., Z. Y. Sun, G. Wagner, and S. C. Harrison. 2002. The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J. 21:885-897.
11. Elbashir, S. M., J. Harborth, K. Weber, and T. Tuschl. 2002. Analysis of gene function in:somatic mammalian cells using small interfering RNAs. Methods 26:199-213.
12. Elbert, M., D. Cohen, and A. Musch. 2006. PAR1b promotes cell-cell adhesion and inhibits dishevelled-mediated transformation of Madin-Darby canine kidney cells. Mol. Biol. Cell 17:3345-3355.
13. Esser, C., S. Alberti, and J. Hohfeld. 2004. Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim. Biophys. Acta 1695:171-188.
14. Glotzer, J. B., M. Saltik, S. Chiocca, A. I. Michou, P. Moseley, and M. Cotten. 2000. Activation of heat-shock response by an adenovirus is essential for virus replication. Nature 407:207-211.
15. Guerrero, C. A., D. Bouyssounade, S. Zarate, P. Isa, T. Lopez, R. Espinosa, P. Romero, E. Mendez, S. Lopez, and C. F. Arias. 2002. Heat shock cognate protein 70 is involved in rotavirus cell entry. J. Virol. 76:4096-4102.
16. Haglund, K., and I. Dikic. 2005. Ubiquitylation and cell signaling. EMBO J. 24:3353-3359.
17. Hartl, F. U., and M. Hayer-Hartl. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852-1858.
18. Heymann, J. B., K. Iwasaki, Y. I. Yim, N. Cheng, D. M. Belnap, L. E. Greene, E. Eisenberg, and A. C. Steven. 2005. Visualization of the binding of Hsc70 ATPase to clathrin baskets: implications for an uncoating mechanism. J. Biol. Chem. 280:7156-7161.
19. Hoeller, D., N. Crosetto, B. Blagoev, C. Raiborg, R. Tikkanen, S. Wagner, K. Kowanetz, R. Breitling, M. Mann, H. Stenmark, and I. Dikic. 2006. Regulation of ubiquitin-binding proteins by monoubiquitination. Nat. Cell Biol. 8:163-169.
20. Jindal, S., and R. A. Young. 1992. Vaccinia virus infection induces a stress response that leads to association of Hsp70 with viral proteins. J. Virol. 66:5357-5362.
21. Jourdan, N., M. Maurice, D. Delautier, A. M. Quero, A. L. Servin, and G. Trugnan. 1997. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 71:8268-8278.
22. Kohli, E., L. Maurice, J. F. Vautherot, C. Bourgeois, J. B. Bour, J. Cohen, and P. Pothier. 1992. Localization of group-specific epitopes on the major capsid protein of group A rotavirus. J. Gen. Virol. 73:907-914.
23. Kojima, K., M. W. Musch, H. Ren, D. L. Boone, B. A. Hendrickson, A. Ma, and E. B. Chang. 2003. Enteric flora and lymphocyte-derived cytokines determine expression of heat shock proteins in mouse colonic epithelial cells. Gastroenterology 124:1395-1407.
24. L'Haridon, R., and R. Scherrer. 1976. In vitro culture of a rotavirus associated with neonatal calf diarrhea. Ann. Rech. Vet. 7:373-381.
25. Liu, J. S., S. R. Kuo, A. M. Makhov, D. M. Cyr, J. D. Griffith, T. R. Broker, and L. T. Chow. 1998. Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J. Biol. Chem. 273:30704-30712.
26. Macejak, D. G., and R. B. Luftig. 1991. Association of HSP70 with the adenovirus type 5 fiber protein in infected HEp-2 cells. Virology 180:120-125.
27. Macejak, D. G., and P. Sarnow. 1992. Association of heat shock protein 70 with enterovirus capsid precursor P1 in infected human cells. J. Virol. 66:1520-1527.
28. McDonough, H., and C. Patterson. 2003. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 8:303-308.
29. Monnier, N., K. Higo-Moriguchi, Z. Y. Sun, B. V. Prasad, K. Taniguchi, and P. R. Dormitzer. 2006. High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. J. Virol. 80:1513-1523.
30. Nejmeddine, M., G. Trugnan, C. Sapin, E. Kohli, L. Svensson, S. Lopez, and J. Cohen. 2000. Rotavirus spike protein VP4 is present at the plasma membrane and is associated with microtubules in infected cells. J. Virol. 74:3313-3320.
31. Phillips, B., K. Abravaya, and R. I. Morimoto. 1991. Analysis of the specificity and mechanism of transcriptional activation of the human hsp70 gene during infection by DNA viruses. J. Virol. 65:5680-5692.
32. Piron, M., P. Vende, J. Cohen, and D. Poncet. 1998. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J. 17:5811-5821.
33. Roseto, A., R. Scherrer, J. Cohen, M. C. Guillemin, A. Charpilienne, C. Feynerol, and J. Peries. 1983. Isolation and characterization of anti-rotavirus immunoglobulins secreted by cloned hybridoma cell lines. J. Gen. Virol. 64:237-240.
34. Santoro, M. G. 1994. Heat shock proteins and virus replication: hsp70s as mediators of the antiviral effects of prostaglandins. Experientia 50:1039-1047.
35. Sapin, C., O. Colard, O. Delmas, C. Tessier, M. Breton, V. Enouf, S. Chwetzoff, J. Ouanich, J. Cohen, C. Wolf, and G. Trugnan. 2002. Rafts promote assembly and atypical targeting of a nonenveloped virus, rotavirus, in Caco-2 cells. J. Virol. 76:4591-4602.
36. Wang, H. G., S. Takayama, U. R. Rapp, and J. C. Reed. 1996. Bcl-2 interacting protein, BAG-1, binds to and activates the kinase Raf-1. Proc. Natl. Acad. Sci. USA 93:7063-7068.
37. Welch, W. J. 1992. Mammalian stress response: cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol. Rev. 72:1063-1081.
38. Welchman, R. L., C. Gordon, and R. J. Mayer. 2005. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat. Rev. Mol. Cell. Biol. 6:599-609.
39. 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.
40. Yoder, J. D., and P. R. Dormitzer. 2006. Alternative intermolecular contacts underlie the rotavirus VP5* two- to three-fold rearrangement. EMBO J. 25:1559-1568.
41. Zarate, S., M. A. Cuadras, R. Espinosa, P. Romero, K. O. Juarez, M. Camacho-Nuez, C. F. Arias, and S. Lopez. 2003. Interaction of rotaviruses with Hsc70 during cell entry is mediated by VP5. J. Virol. 77:7254-7260.
42. Zweibaum, A., H. P. Hauri, E. Sterchi, I. Chantret, K. Haffen, J. Bamat, and B. Sordat. 1984. Immunohistological evidence, obtained with monoclonal antibodies, of small intestinal brush border hydrolases in human colon cancers and foetal colons. Int. J. Cancer 34:591-598.