Integrin-using rotaviruses bind α2β1 integrin α2 I domain via VP4 DGE sequence and recognize αXβ2 and αVβ3 by using VP7 during cell entry

Journal of Virology

Volumn 77, Issue 18, 2003, Pages 9969-9978

  Graham, Kate L ^a   Halasz, Peter ^a   Tan, Yan ^a   Hewish, Marilyn J ^a   Takada, Yoshikazu ^b   Mackow, Erich R ^c,d   Robinson, Martyn K ^e   Coulson, Barbara S ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UCB PHARMA   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; INTEGRIN; PROTEIN VP4; PROTEIN VP5; SIALIC ACID; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 2; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENETIC REASSORTMENT; GENETIC TRANSFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ROTAVIRUS; SEROTYPE; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS STRAIN;

AMINO ACID MOTIFS; ANTIGENS, VIRAL; CAPSID PROTEINS; CELL LINE; COLLAGEN; FIBRINOGEN; HUMANS; INTEGRIN ALPHA2; INTEGRIN ALPHAVBETA3; INTEGRIN ALPHAXBETA2; OLIGOPEPTIDES; ROTAVIRUS;

EID: 0141458927     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.18.9969-9978.2003     Document Type: Article

References (55)

1. Barton, E. S., J. C. Forrest, J. L. Connolly, J. D. Chappell, Y. Liu, F. J. Schnell, A. Nusrat, C. A. Parkos, and T. S. Dermody. 2001. Junction adhesion molecule is a receptor for reovirus. Cell 104:441-451.
2. Bergelson, J. M., B. M. Chan, R. W. Finberg, and M. E. Hemler. 1993. The integrin VLA-2 binds echovirus 1 and extracellular matrix ligands by different mechanisms. J. Clin. Investig. 92:232-239.
3. Bergelson, J. M., N. F. St. John, S. Kawaguchi, R. Pasqualini, F. Berdichevsky, M. E. Hemler, and R. W. Finberg. 1994. The I domain is essential for echovirus 1 interaction with VLA-2. Cell Adhes. Commun. 2:455-464.
4. 2+ gradient during entry of rotavirus into MA104 cells. J. Virol. 76:13083-13087.
5. Chen, D., J. W. Burns, M. K. Estes, and R. F. Ramig. 1989. Phenotypes of rotavirus reassortants depend upon the recipient genetic background. Proc. Natl. Acad. Sci. USA 86:3743-3747.
6. Chen, D., V. Magnuson, S. Hill, C. Arnaud, B. Steffensen, and R. J. Klebe. 1992. Regulation of integrin gene expression by substrate adherence. J. Biol. Chem. 267:23502-23506.
7. Ciarlet, M., S. E. Crawford, E. Cheng, S. E. Blutt, D. A. Rice, J. M. Bergelson, and M. K. Estes. 2002. VLA-2 (α2β1) integrin promotes rotavirus entry into cells but is not necessary for rotavirus attachment. J. Virol. 76:1109-1123.
8. Ciarlet, M., J. E. Ludert, M. Iturriza-Gomara, F. Liprandi, J. J. Gray, U. Desselberger, and M. K. Estes. 2002. Initial interaction of rotavirus strains with N-acetylneuraminic (sialic) acid residues on the cell surface correlates with VP4 genotype, not species of origin. J. Virol. 76:4087-4095.
9. Coulson, B. S. 1997. Effects of workshop monoclonal antibodies on rotavirus infection of cells, p. 391-393. In T. Kishimoto, H. Kikutani, A. E. G. Kr. von dem Borne, S. M. Goyert, D. Y. Mason, M. Miyasaka, L. Moretta, K. Okumura, S. Shaw, T. A. Springer, K. Sugamura, and H. Zola (ed.), Leucocyte typing VI. Garland Publishing, Inc., New York, N.Y.
10. Coulson, B. S., and C. Kirkwood. 1991. Relation of VP7 amino acid sequence to monoclonal antibody neutralization of rotavirus and rotavirus monotype. J. Virol. 65:5968-5974.
11. Coulson, B. S., S. L. Londrigan, and D. J. Lee. 1997. Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proc. Natl. Acad. Sci. USA 94:5389-5394.
12. Coulson, B. S., L. E. Unicomb, G. A. Pitson, and R. F. Bishop. 1987. Simple and specific enzyme immunoassay using monoclonal antibodies for serotyping human rotaviruses. J. Clin. Microbiol. 25:509-515.
13. Davison, E., R. M. Diaz, I. R. Hart, G. Santis, and J. F. Marshall. 1997. Integrin α5β1-mediated adenovirus infection is enhanced by the integrin-activating antibody TS2/16. J. Virol. 71:6204-6207.
14. Delorme, C., H. Brussow, J. Sidoti, N. Roche, K. A. Karlsson, J. R. Neeser, and S. Teneberg. 2001. Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J. Virol. 75:2276-2287.
15. Denisova, E., W. Dowling, R. LaMonica, R. Shaw, S. Scarlata, F. Ruggeri, and E. R. Mackow. 1999. Rotavirus capsid protein VP5* permeabilizes membranes. J. Virol. 73:3147-3153.
16. Dormitzer, P. R., Z. Y. Sun, O. Blixt, J. C. Paulson, G. Wagner, and S. C. Harrison. 2002. Specificity and affinity of sialic acid binding by the rhesus rotavirus VP8* core. J. Virol. 76:10512-10517.
17. Dowling, W., E. Denisova, R. LaMonica, and E. R. Mackow. 2000. Selective membrane permeabilization by the rotavirus VP5* protein is abrogated by mutations in an internal hydrophobic domain. J. Virol. 74:6368-6376.
18. Faull, R. J., J. Wang, D. I. Leavesley, W. Puzon, G. R. Russ, D. Vestweber, and Y. Takada. 1996. A novel activating anti-β1 integrin monoclonal antibody binds to the cysteine-rich repeats in the β1 chain. J. Biol. Chem. 271:25099-25106.
19. 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.
20. Guerrero, C. A., E. Mendez, S. Zarate, P. Isa, S. Lopez, and C. F. Arias. 2000. Integrin alpha(v)beta(3) mediates rotavirus cell entry. Proc. Natl. Acad. Sci. USA 97:14644-14649.
21. Guerrero, C. A., S. Zarate, G. Corkidi, S. Lopez, and C. F. Arias. 2000. Biochemical characterization of rotavirus receptors in MA104 cells. J. Virol. 74:9362-9371.
22. Guo, C. T., O. Nakagomi, M. Mochizuki, H. Ishida, M. Kiso, Y. Ohta, T. Suzuki, D. Miyamoto, K. I. Hidari, and Y. Suzuki. 1999. Ganglioside GM(1a) on the cell surface is involved in the infection by human rotavirus KUN and MO strains. J. Biochem. (Tokyo) 126:683-688.
23. Hewish, M. J., Y. Takada, and B. S. Coulson. 2000. Integrins α2β1 and α4β1 can mediate SAll rotavirus attachment and entry into cells. J. Virol. 74:228-236.
24. Hoshino, Y., R. W. Jones, and A. Z. Kapikian. 1998. Serotypic characterization of outer capsid spike protein VP4 of vervet monkey rotavirus SA11 strain. Arch. Virol. 143:1233-1244.
25. Jiang, R., B. Gao, K. Prasad, L. E. Greene, and E. Eisenberg. 2000. Hsc70 chaperones clathrin and primes it to interact with vesicle membranes. J. Biol. Chem. 275:8439-8447.
26. Jolly, C. L., B. M. Beisner, E. Ozser, and I. H. Holmes. 2001. Non-lytic extraction and characterisation of receptors for multiple strains of rotavirus. Arch. Virol. 146:1307-1323.
27. Kalica, A. R., J. Flores, and H. B. Greenberg. 1983. Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology 125:194-205.
28. Kaljot, K. T., R. D. Shaw, D. H. Rubin, and H. B. Greenberg. 1988. Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J. Virol. 62:1136-1144.
29. Kamata, T., and Y. Takada. 1994. Direct binding of collagen to the I domain of integrin alpha 2 beta 1 (VLA-2, CD49b/CD29) in a divalent cation-independent manner. J. Biol. Chem. 269:26006-26010.
30. Kawaguchi, S., and M. E. Hemler. 1993. Role of the alpha subunit cytoplasmic domain in regulation of adhesive activity mediated by the integrin VLA-2. J. Biol. Chem. 268:16279-16285.
31. Kirkwood, C. D., R. F. Bishop, and B. S. Coulson. 1998. Attachment and growth of human rotaviruses RV-3 and S12/85 in Caco-2 cells depend on VP4. J. Virol. 72:9348-9352.
32. Kool, D. A., S. M. Matsui, H. B. Greenberg, and I. H. Holmes. 1992. Isolation and characterization of a novel reassortant between avian Ty-1 and simian RRV rotaviruses. J. Virol. 66:6836-6839.
33. Lazdins, I., B. S. Coulson, C. Kirkwood, M. Dyall-Smith, P. J. Masendycz, S. Sonza, and I. H. Holmes. 1995. Rotavirus antigenicity is affected by the genetic context and glycosylation of VP7. Virology 209:80-89.
34. Londrigan, S. L., M. J. Hewish, M. J. Thomson, G. M. Sanders, H. Mustafa, and B. S. Coulson. 2000. Growth of rotaviruses in continuous human and monkey cell lines that vary in their expression of integrins. J. Gen. Virol. 81:2203-2213.
35. Londrigan, S. L., K. L. Graham, Y. Takada, P. Halasz, and B. S. Coulson. 2003. Monkey rotavirus binding to α2β1 integrin requires the α2 I domain and is facilitated by the homologous β1 subunit. J. Virol. 77:9486-9501.
36. Marjomaki, V., V. Pietiainen, H. Matilainen, P. Upla, J. Ivaska, L. Nissinen, H. Reunanen, P. Huttunen, T. Hyypia, and J. Heino. 2002. Internalization of echovirus 1 in caveolae. J. Virol. 76:1856-1865.
37. Meier, O., K. Boucke, S. V. Hammer, S. Keller, R. P. Stidwill, S. Hemmi, and U. F. Greber. 2002. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 158:1119-1131.
38. Mendez, E., C. F. Arias, and S. Lopez. 1996. Interactions between the two surface proteins of rotavirus may alter the receptor-binding specificity of the virus. J. Virol. 70:1218-1222.
39. Nagesha, H. S., L. E. Brown, and I. H. Holmes. 1989. Neutralizing monoclonal antibodies against three serotypes of porcine rotavirus. J. Virol. 63:3545-3549.
40. Nagesha, H. S., and I. H. Holmes. 1991. VP4 relationships between porcine and other rotavirus serotypes. Arch. Virol. 116:107-118.
41. Ng, T., D. Shima, A. Squire, P. I. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker. 1999. PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18:3909-3923.
42. Ortlepp, S., P. E. Stephens, N. Hogg, C. G. Figdor, and M. K. Robinson. 1995. Antibodies that activate beta 2 integrins can generate different ligand binding states. Eur. J. Immunol. 25:637-643.
43. Pesavento, J. B., A. M. Billingsley, E. J. Roberts, R. F. Ramig, and B. V. Prasad. 2003. Structures of rotavirus reassortants demonstrate correlation of altered conformation of the VP4 spike and expression of unexpected VP4-associated phenotypes. J. Virol. 77:3291-3296.
44. Ramachandran, M., J. R. Gentsch, U. D. Parashar, S. Jin, P. A. Woods, J. L. Holmes, C. D. Kirkwood, R. F. Bishop, H. B. Greenberg, S. Urasawa, G. Gerna, B. S. Coulson, K. Taniguchi, J. S. Bresee, and R. I. Glass. 1998. Detection and characterization of novel rotavirus strains in the United States. J. Clin. Microbiol. 36:3223-3229.
45. Rolsma, M. D., T. B. Kuhlenschmidt, H. B. Gelberg, and M. S. Kuhlenschmidt. 1998. Structure and function of a gangliosidc receptor for porcine rotavirus. J. Virol. 72:9079-9091.
46. Ruoslahti, E., and J. C. Reed. 1994. Anchorage dependence, integrins, and apoptosis. Cell 77:477-478.
47. Shaw, R. D., P. T. Vo, P. A. Offit, B. S. Coulson, and H. B. Greenberg. 1986. Antigenic mapping of the surface proteins of rhesus rotavirus. Virology 155:434-451.
48. Staatz, W. D., K. F. Fok, M. M. Zutter, S. P. Adams, B. A. Rodriguez, and S. A. Santoro. 1991. Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1 integrin in collagen. J. Biol. Chem. 266:7363-7367.
49. Steele, A. D., and B. Ivanoff. 2003. Rotavirus strains circulating in Africa during 1996-1999: emergence of G9 strains and P[6] strains. Vaccine 21:361-367.
50. Stupack, D. G., and D. A. Cheresh. 2002. Gct a ligand, get a life: integrins, signaling and cell survival. J. Cell Sci. 115:3729-3738.
51. Tang, B., J. M. Gilbert, S. M. Matsui, and H. B. Greenberg. 1997. Comparison of the rotavirus gene 6 from different species by sequence analysis and localization of subgroup-specific epitopes using site-directed mutagenesis. Virology 237:89-96.
52. Thain, A., K. Gaston, O. Jenkins, and A. R. Clarke. 1996. A method for the separation of GST fusion proteins from co-purifying GroEL. Trends Genet. 12:209-210.
53. Tyler, K. L., P. Clarke, R. L. DeBiasi, D. Kominsky, and G. J. Poggioli. 2001. Reoviruses and the host cell. Trends Microbiol. 9:560-564.
54. Wary, K. K., A. Mariotti, C. Zurzolo, and F. G. Giancotti. 1998. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94:625-634.
55. Zarate, S., R. Espinosa, P. Romero, C. A. Guerrero, C. F. Arias, and S. Lopez. 2000. Integrin α2β1 mediates the cell attachment of the rotavirus neuraminidase-resistant variant nar3. Virology 278:50-54.