Rotavirus capsid protein VP5* permeabilizes membranes

Journal of Virology

Volumn 73, Issue 4, 1999, Pages 3147-3153

  Denisova, Evgeniya ^a   Dowling, William ^a   Lamonica, Rachel ^a   Shaw, Robert ^a,b   Scarlata, Suzanne ^a   Ruggeri, Franco ^c   Mackow, Erich R ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CARBOXYFLUORESCEIN; CHOLESTEROL; DIVALENT CATION; EPITOPE; NEUTRALIZING ANTIBODY; PROTEIN HYDROLYSATE;

ARTICLE; CELL LINE; CELL VACUOLE; CONCENTRATION RESPONSE; FUSION GENE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; ROTAVIRUS; TEMPERATURE DEPENDENCE; VIRION; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION;

EID: 0032976078     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.4.3147-3153.1999     Document Type: Article

References (60)

1. Arias, C. F., P. Romero, V. Alvarez, and S. Lopez. 1996. Trypsin activation pathway of rotavirus infectivity. J. Virol. 70:5832-5839.
2. Blumenthal, R., P. Seth, M. C. Willingham, and I. Pastan. 1986. pH-dependent lysis of liposomes by adenovirus. Biochemistry 25:2231-2237.
3. Butko, P., K. Huang, M. Pusztai-Carey, and W. K. Surewicz. 1996. Membrane permeabilization induced by cytolytic delta-endotoxin CytA from Bacillus thuringiensis var. israelensis. Biochemistry 35:11355-11360.
4. Charpilienne, A., M. J. Abad, F. Michelangeli, F. Alvarado, M. Vasseur, J. Cohen, and M. C. Ruiz. 1997. Solubilized and cleaved VP7, the outer glycoprotein of rotavirus, induces permeabilization of cell membrane vesicles. J. Gen. Virol. 78:1367-1371.
5. Chow, M., J. F. Newman, D. Filman, J. M. Hogle, D. J. Rowlands, and F. Brown. 1987. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327:482-486.
6. Cleverley, D. Z., and J. Lenard. 1998. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 95:3425-3430.
7. Cohen, J., J. Laporte, A. Charpilienne, and R. Scherrer. 1979. Activation of rotavirus RNA polymerase by calcium chelation. Arch. Virol. 60:177-186.
8. Cotten, M., M. Saltik, M. Kursa, E. Wagner, G. Maass, and M. L. Birnstiel. 1994. Psoralen treatment of adenovirus particles eliminates virus replication and transcription while maintaining the endosomolytic activity of the virus capsid. Virology 205:254-261.
9. 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.
10. Crawford, S. E., M. Labbe, J. Cohen, M. H. Burroughs, Y. J. Zhou, and M. K. Estes. 1994. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J. Virol. 68:5945-5922.
11. 2+ concentration to initiate their replication cycle. J. Virol. 71: 9065-9074.
12. Curry, S., M. Chow, and J. M. Hogle. 1996. The poliovirus 135S particle is infectious. J. Virol. 70:7125-7131.
13. Espejo, R. T., S. Lopez, and C. Arias. 1981. Structural polypeptides of simian rotavirus SA11 and the effect of trypsin. J. Virol. 37:156-160.
14. Estes, M. K. 1996. Rotaviruses and their replication, p. 1329-1352. In B. N. Fields and D. M. Knipe (ed.), Virology, 3rd ed. Raven Press, New York, N.Y.
15. Estes, M. K., D. Y. Graham, and B. B. Mason. 1981. Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J. Virol. 39:879-888.
16. Falconer, M. M., J. M. Gilbert, A. M. Roper, H. B. Greenberg, and J. S. Gavora. 1995. Rotavirus-induced fusion from without in tissue culture cells. J. Virol. 69:5582-5591.
17. Fiore, L., H. B. Greenberg, and E. R. Mackow. 1991. The VP8* fragment of VP4 is the rhesus rotavirus hemagglutinin. Virology 181:553-563.
18. Fricks, C. E., and J. M. Hogle. 1990. Cell-induced conformational change in poliovirus: externatization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64:1934-1945.
19. Fukuhara, N., O. Yoshie, S. Kitaoka, T. Konno, and N. Ishida. 1987. Evidence for endocytosis-independent infection by human rotavirus. Arch. Virol. 97:93-99.
20. Gilbert, J., and H. Greenberg. 1998. Cleavage of rhesus rotavirus VP4 after arginine 247 is essential for rotavirus-like particle-induced fusion from without. J. Virol. 72:5323-5327.
21. Gilbert, J., and H. Greenberg. 1997. Virus-like particle-induced fusion form without in tissue culture cells: role of outer-layer proteins VP4 and VP7. J. Virol. 71:4555-4563.
22. Greber, U. F., M. Willetts, P. Webster, and A. Helenius. 1993. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75:477-486.
23. 22a. Hargland, R. P. 1990. Polar tracers, p. 331-338. In M. T. Z. Spence (ed.), Handbook of fluorescent probes and research chemicals, 6th ed. Molecular Probes, Inc., Portland, Ore.
24. Honda, M., P. C. Hu, C. H. Huang, H. Matsui, and S. M. Lemon. 1996. A replication-deficient adenovirus enhances liposome-mediated nucleic acid transfer into a stable cell line expressing T7 RNA polymcrase. J. Virol. Methods 58:41-51.
25. 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.
26. 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.
27. Kapikian, A. Z., and R. M. Chanock. 1996. Rotaviruses, p. 1353-1404. In B. N. Fields and D. M. Knipe (ed.), Virology, 3rd ed, vol. 2. Raven Press, New York, N.Y.
28. Keljo, D. J., M. Kuhn, and A. Smith. 1988. Acidification of endosomes is not important for the entry of rotavirus into the cell. J. Pediatr. Gastroenterol. Nutr. 7:257-263.
29. Kielian, M. 1995. Membrane fusion and the alphavirus life cycle. Adv. Virus Res. 45:113-151.
30. Kielian, M., and A. Helenius. 1985. pH-induced alterations in the fusogenic spike protein of Semliki Forest virus. J. Cell Biol. 101:2284-2291.
31. Kielian, M., M. R. Klimjack, S. Ghosh, and W. A. Duffus. 1996. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus. J. Cell Biol. 134:863-872.
32. Lawton, J. A., M. K. Estes, and B. V. Prasad. 1997. Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nat. Struct. Biol. 4:118-121.
33. Levy-Mintz, P., and M. Kielian. 1991. Mutagenesis of the putative fusion domain of the Semliki Forest virus spike protein. J. Virol. 65:4292-4300.
34. Liprandi, F., Z. Moros, M. Gerder, J. E. Ludert, F. H. Pujol, M. C. Ruiz, F. Michelangeli, A. Charpilienne, and J. Cohen. 1997. Productive penetration of rotavirus in cultured cells induces coentry of the translation inhibitor alpha-sarcin. Virology 237:430-438.
35. Lopez, S., I. Lopez, P. Romero, E. Mendez, X. Soberon, and C. F. Arias. 1991. Rotavirus YM gene 4: analysis of its deduced amino acid sequence and prediction of the secondary structure of the VP4 protein. J. Virol. 65:3738-3745.
36. Mackow, E. R., J. W. Barnett, H. Chan, and H. B. Greenberg. 1989. The rhesus rotavirus outer capsid protein VP4 functions as a hemagglutinin and is antigenically conserved when expressed by a haculovirus recombinant. J. Virol. 63:1661-1668.
37. Mackow, E. R., R. D. Shaw, S. M. Matsui, P. T. Vo, M. N. Dang, and H. B. Greenberg. 1988. The rhesus rotavirus gene encoding protein VP3: location of amino acids involved in homologous and heterologous rotavirus neutralization and identification of a putative fusion region. Proc. Natl. Acad. Sci. USA 85:645-649.
38. Mackow, E. R., P. T. Vo, R. Broome, D. Bass, and H. B. Greenberg. 1990 Immunization with baculovirus-expressed VP4 protein passively protects against simian and murine rotavirus challenge. J. Virol. 64:1698-1703.
39. Mackow, E. R., M. V. Yamanaka, M. N. Dang, and H. B. Greenberg. 1990 DNA amplification-restricted transcription-translation: rapid analysis of rhesus rotavirus neutralization sites. Proc. Natl. Acad. Sci. USA 87:518-522.
40. Moscufo, N., A. G. Yafal, A. Rogove, J. Hogle, and M. Chow. 1993. A mutation in VP4 defines a new step in the late stages of cell entry by poliovirus. J. Virol. 67:5075-5078.
41. Nandi, P., A. Charpilienne, and J. Cohen. 1992. Interaction of rotavirus particles with liposomes. J. Virol. 66:3363-3367.
42. Nibert, M. L., L. A. Schiff, and B. N. Fields. 1991. Mammalian reoviruscs contain a myristoylated structural protein. J. Virol. 65:1960-1967.
43. Offit, P. A., and G. Blavat. 1986. Identification of the two rotavirus genes determining neutralization specificities. J. Virol. 57:376-378.
44. Offit, P. A., H. F. Clark, G. Blavat, and H. B. Greenberg. 1986. Reassortant rotaviruses containing structural proteins vp3 and vp7 from different parents induce antibodies protective against each parental serotype. J. Virol. 60:491-496.
45. Patton, J. T., J. Hua, and E. A. Mansell. 1993. Location of intrachain disulfide bonds in the VP5** and VP8** trypsin cleavage fragments of the rhesus rotavirus spike protein VP4. J. Virol. 67:4848-4855.
46. Prasad, B. V., and W. Chiu. 1994. Structure of rotavirus. Curr. Top. Microbiol. Immunol. 185:9-29.
47. Prasad, B. V., R. Rothnagel, C. Q. Zeng, J. Jakana, J. A. Lawton, W. Chiu, and M. K. Estes. 1996. Visualization of ordered genomic RNA and localization of transcriptional complexes in rotavirus. Nature 382:471-473.
48. Prasad, B. V., G. J. Wang, J. P. Clerx, and W. Chiu. 1988. Three-dimensional structure of rotavirus J. Mol. Biol. 199:269-275.
49. Rodriguez, E., and E. Everitt. 1996. Adenovirus uncoating and nuclear establishment are not affected by weak base amines. J. Virol. 70:3470-3477.
50. Ruiz, M. C., M. J. Abad, A. Charpilienne, J. Cohen, and F. Michelangeli. 1997. Cell lines susceptible to infection are permeabilized by cleaved and solubilized outer layer proteins of rotavirus. J. Gen. Virol. 78:2883-2893.
51. Ruiz, M. C., S. R. Alonso-Torre, A. Charpilienne, M. Vasseur, F. Michelangeli, J. Cohen, and F. Alvarado. 1994. Rotavirus interaction with isolated membrane vesicles. J. Virol. 68:4009-4016.
52. 2+ that solubilizes outer capsid proteins from rotavirus particles is dependent on the strain. J. Virol. 70: 4877-4883.
53. Seth, P. 1994. Mechanism of adenovirus-mediated endosome lysis: role of the intact adenovirus capsid structure. Biochem. Biophys. Res. Commun. 205:1318-1324.
54. Shaw, A. L., R. Rothnagel, D. Chen, R. F. Ramig, W. Chiu, and B. V. Prasad. 1993. Three-dimensional visualization of the rotavirus hemagglutinin structure. Cell 74:693-701.
55. Shaw, R. D., D. L. Stoner-Ma, M. K. Estes, and H. B. Greenberg. 1985. Specific enzyme-linked immunoassay for rotavirus serotypes 1 and 3. J. Clin. Microbiol. 22:286-291.
56. 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.
57. Suzuki, H., S. Kitaoka, T. Konno, T. Sato, and N. Ishida. 1985. Two modes of human rotavirus entry into MA 104 cells. Arch. Virol. 85:25-34.
58. Suzuki, H., S. Kitaoka, T. Sato, T. Konno, Y. Iwasaki, Y. Numazaki, and N. Ishida. 1986. Further investigation on the mode of entry of human rotavirus into cells. Arch. Virol. 91:135-144.
59. Tosteson, M. T., and M. Chow. 1997. Characterization of the ion channels formed by poliovirus in planar lipid membranes. J. Virol. 71:507-511.
60. Yeager, M., J. A. Berriman, T. S. Baker, and A. R. Bellamy. 1994. Three-dimensional structure of the rotavirus haemagglutinin VP4 by cryo-electron microscopy and difference map analysis. EMBO J. 13:1011-1018.