Key Golgi factors for structural and functional maturation of Bunyamwera virus

Journal of Virology

Volumn 79, Issue 17, 2005, Pages 10852-10863

  Novoa, Reyes R ^a   Calderita, Gloria ^a   Cabezas, Pilar ^a   Elliott, Richard M ^b   Risco, Cristina ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; N ACETYL BETA GLUCOSAMINIDASE; SIALIC ACID;

ANIMAL CELL; ARTICLE; BUNYAMWERA VIRUS; CARBOHYDRATE ANALYSIS; GLYCOSYLATION; NONHUMAN; PRIORITY JOURNAL; SIALYLATION; TRANS GOLGI NETWORK; VIRION; VIROGENESIS; VIRUS ASSEMBLY; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS PURIFICATION;

ACETYLGLUCOSAMINIDASE; ANIMALS; BUNYAMWERA VIRUS; CELL LINE; CERCOPITHECUS AETHIOPS; CHO CELLS; CRICETINAE; CRICETULUS; DRUG RESISTANCE, VIRAL; GLYCOPROTEINS; N-ACETYLNEURAMINIC ACID; STRUCTURE-ACTIVITY RELATIONSHIP; TRANS-GOLGI NETWORK; VERO CELLS; VIRAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

BUNYAMWERA VIRUS; ORTHOBUNYAVIRUS;

EID: 23844480674     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.17.10852-10863.2005     Document Type: Article

References (58)

1. Allison, S. L., Y. J. Tao, G. O'Riordain, C. W. Mandl, S. C. Harrison, and F. X. Heinz. 2003. Two disinct size classes of immature and mature subviral particles from tick-borne encephalitis virus. J. Virol. 77:11357-11366.
2. Allan-Bonnet, N., R. Sougrat, and J. Lippincott-Schwartz. 2004, Molecular basis for Golgi maintenance and biogenesis. Curr. Opin. Cell Biol. 16:364-372.
3. Baumeister, W. 2002. Electron tomography: towards visualizing the molecular organization of the cytoplasm. Curr. Opin. Struct. Biol. 12:679-684.
4. Bijlmakers, M. J., and M. Marsh. 2003. The on-off story of protein palmitoylation. Trends Cell Biol. 13:32-42.
5. Bonay, P., S. Munro, M. Fresno, and B. Alarcon. 1996. Intra-Golgi transport inhibition by megalomycin. J. Biol. Chem. 271:3719-3726.
6. Bridgen, A., W. Friedemann, J. K. Fazakerley, and R. M. Elliott. 2001. Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc. Natl. Acad. Sci. USA 98:664-669.
7. Cash, P., L. Hendershot, and D. H. L. Bishop. 1980. The effects of glycosylation inhibitors on the maturation and intracellular polypeptide synthesis induced by snowshoe hare bunyavirus. Virology 103:235-240.
8. Chen, W., and P. Stanley. 2003. Five Lec1 CHO cell mutants have distinct Mgat1 gene mutations that encode truncated N-acetylglucosaminyltransferase I. Glycobiology 13:43-50.
9. Cheng, R. H., R. J. Kuhn, N. H. Olson, M. G. Rossmann, H. K. Choi, T. J. Smith, and T. S. Baker. 1995. Nucleocapsid and glycoprotein organization in an enveloped virus. Cell 80:621-630.
10. Conway, J. F., R. L. Duda, N., Cheng, R. W. Hendrix, and A. C. Steven. 1995. Proteolytic and conformational control of virus capsid maturation: the bateriophage HK97 system. J. Mol. Biol. 253:86-99.
11. Cyrklaff, M., C. Risco, J. J. Fernández, M. V. Jiménez, M. Esteban, W. Baumeister, and J. L. Carrascosa. 2005. Cryo-electron tomography of vaccinia virus. Proc. Natl. Acad. Sci. USA 102:2772-2777.
12. De Ran, C. A. M., K. Staedler, G. -J. Godeke, B. Jan Bosch, and P. J. M. Rottier. 2004. Cleavage inhibition of the murine coronavirus spike protein by a furin-like enzyme affects cell-cell but not virus-cell fusion. J. Virol. 78:6048-6054.
13. Deustcher, S. L., N. Nuwayhid, P. Stanley, E. I. Briles, and C. B. Hirschberg. 1984. Translocation across Golgi vesicle membranes: a CHO glycosilation mutant deficient in CMP-sialic acid transport. Cell 39:295-299.
14. Elliott, R. M. 1997. Emerging viruses: the Bunyaviridae. Mol. Med. 3:572-577.
15. Goldsmith, C. S., L. H. Elliott, C. J. Peters, and S. R. Zaki. 1995. Ultrastructural characteristics of Sin Nombre virus, causative agent of hantavirus pulmonary syndrome. Arch. Virol. 140:2107-2122.
16. Griffiths, G., and P. Rottier. 1992. Cell biology of viruses that assemble along the biosynthetic pathway. Semin. Cell Biol. 3:367-381.
17. Grünewald, K., P. Desai, D. C. Winkler, J. B. Heymann, D. Belnap, W. Baumeister, and A. C. Steven. 2003. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302:1396-1398.
18. Helenius, A., and M. Aebi. 2001. Intracellular functions of N-linked glycans. Science 291:2364-2369.
19. Jantti, J., P. Hilden, H. Ronka, V. Makiranta, S. Keranen, and E. Kuismanen. 1997. Immunocytochemical analysis of Uukuniemi virus budding compartments: role of the intermediate compartment and the Golgi stack in virus maturation. J. Virol. 71:1162-1172.
20. Kuhn, R. J., W. Zhang, M. G. Rossman, S. V. Pletner, J. Corver, E. Lenches, C. T. Jones, S. Mukhopadhyay, P. R. Chipman, E. G. Strauss, T. S. Baker, and J. H. Strauss. 2002. Structure of dengue virus. Implications for flavivirus organization, maturation, and fusion. Cell 108:717-725.
21. Lappin, D. F., G. W. Nakitare, J. W. Palfreyman, and R. M. Elliott. 1994. Localization of Bunyamwera bunyavirus G1 glycoprotein to the Golgi requires association with G2 but not with NSm. J. Gen. Virol. 75:3441-3451.
22. Ludwig, G. V., B. A. Israe, B. M. Christensen, T. M. Yuill, and K. T. Schultz. 1991. Monoclonal antibodies directed against the envelope glycoproteins of La Crosse virus. Microb. Pathog. 11:411-421.
23. Mancini, E. J., M. Clarke, B. E. Gowen, T. Rutten, and S. D. Fuller. 2000. Cryoelectron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus. Cell 5:255-266.
24. Marsh, B. J., and K. E. Howell. 2002. The mammalian Golgi -complex debates. Nat. Rev. Mol. Cell. Biol. 3:789-795.
25. Marsh, B. J., N. Volkmann, J. R. McIntosh, and K. E. Howell. 2004. Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc. Natl. Acad. Sci. USA 101:5565-5570.
26. Matsuoka, Y., S. Y. Chen, and R. W. Compans. 1994. A signal for Golgi retention in the bunyavirus G1 glycoprotein. J. Biol. Chem. 268:22565-22573.
27. Mckenzie, J. M., M. K. Jones, and E. G. Westaway. 1999. Markers for trans-Golgi membranes and the intermediate compartment localize to induced membranes with distinct replication functions in flavivirus-infected cells. J. Virol. 73:9555-9567.
28. Meager, A., A. Ungkitchanukit, and R. C. Hughes. 1976. Variants of hamster fibroblasts resistant to Ricinus communis toxin (ricin). Biochem. J. 154:113-124.
29. Medalia, O., I. Weber, A. S. Frangakis, D. Nicastro, G. Gerish, and W. Baumeister. 2002. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298:1209-1213.
30. Mironov, A. A., P. Weidman, and A. Luini. 1997. Variations on the intracellular transport theme: maturing cisternae and trafficking tubules. J. Cell Biol. 138:481-484.
31. Mogelsvang, S., B. J. Marsh, M. S. Ladinsky, and K. E. Howell. 2004. Predicting function from structure: 3D structure studies of the mammalian Golgi complex. Traffic 5:338-345.
32. Nakitare, G. W., and R. M. Elliott. 1993. Expression of the Bunyamwera virus M genome segment and intracellular localization of NSm. Virology 195:511-520.
33. Navarro-Lérida, I., M. Martínez-Moreno, F. Roncal, F. Gavilanes, J. P. Albar, and I. Rodríguez-Crespo. 2004. Proteomic identification of brain proteins that interact with dynein light chain LC8. Proteomics 4:339-346.
34. Novoa, R. R., G. Calderita, R. Arranz, J. Fontana, H. Granzow, and C. Risco. 2005. Virus factories: associations of cells organelles for viral replication and morphogenesis. Biol. Cell. 97:147-172.
35. Opat, A. S., H. Puthalakath, J. Burke, and P. A. Gleeson. 1998. Genetic defect in N-acetylglucosaminyltransferase I gene of a ricin-resistant baby hamster kidney mutant. Biochem. J. 336:593-598.
36. Parodi, A. J. 2000. Protein glycosylaton and its role in protein folding. Annu. Rev. Biochem. 69:69-93.
37. Pelham, H. R., and J. E. Rothman. 2000. The debate about transport in the Golgi -two sides of the same coin? Cell 102:713-739.
38. Prentice, E., W. G. Jerome, T. Yoshimori, M. Mizushima, and M. R. Denison. 2004. Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 279:10136-10141.
39. Risco, C., L. Menéndez-Arias, T. D. Copeland, P. Pinto da Silva, and S, Oroszlan. 1995. Intracellular transport of murine leukemia virus during acute infection of NIH-3T3 cells: nuclear import of nucleocapsid protein and integrase. J. Cell Sci. 108:3039-3050.
40. Risco, C., J. R. Rodríguez, C. López-Iglesias, J. L. Carrascosa, M. Esteban, and D. Rodríguez. 2002. Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76:1839-1855.
41. Risco, C., J. L. Carrascosa, and T. K. Frey. 2003. Structural maturation of rubella virus in the Golgi complex. Virology 312:261-269.
42. Ronnholm, R. 1992. Localization to the Golgi complex of Uukuniemi virus glycoproteins G1 and G2 expressed from cloned cDNAs. J. Virol. 66:4525-4531.
43. Salanueva, I. J., J. L. Carrascosa, and C. Risco. 1999. Structural maturation of the transmissible gastroenteritis coronavirus. J. Virol. 73:7952-7964.
44. Salanueva, I. J., R. R. Novoa, P. Cabezas, C. López-Iglesias, J. L. Carrascosa, R. M. Elliott, and C. Risco. 2003. Polymorphism and structural maturation of Bunyamwera virus in Golgi and post-Golgi compartments. J. Virol. 77:1368-1381.
45. Schmaljohn, S., and J. W. Hooper. 2001. Bunyaviridae: the viruses and their replication, p. 1581-1602. In D. M. Knipe and P. M. Holey (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
46. Seemann, J., E. Jokitalo, M. Pypaert, and G. Warren. 2000. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407:1022-1026.
47. Shi, X., and R. M. Elliott. 2004. Analysis of N-linked glycosylation of Hantaan virus glycoproteins and the role of oligosaccharide side chains in protein folding and intracellular trafficking. J. Virol. 78:5414-5422.
48. Shi, X., D. F. Lappin, and R. M. Elliott. 2004, Mapping the Golgi targeting and retention signal of Bunyamwera virus glycoproteins. J. Virol. 78:10793-10802.
49. Spiro, R. G. 2002. Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12:43-56.
50. Staedler, K., S. L. Allison, J. Schalich, and F. X. Heinz. 1997. Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71:8475-8481.
51. Stanley, P. 1989. Chinese hamster ovary cell mutants with multiple glycosylation defects for production of glycoproteins with minimal carbohydrate heterogeneity. Mol. Cell. Biol. 9:377-383.
52. Subramaniam, S., and J. L. S, Milne. 2004. Three-dimensional electron microscopy at molecular resolution. Annu. Rev. Biophys. Biomol. Struct. 33:141-155.
53. Tritel, M., and M. D. Resh. 2000. Kinetic analysis of human immunodeficiency virus type 1 assembly reveals the presence of sequential intermediates. J. Virol. 74:5845-5855.
54. Vennema, H., G.-J. Godeke, W. A. Rossen, W. F. Voorhout, M. C. Horzinek, D.-J. E. Opstelten, and P. J. M. Rottier. 1996. Nucleocapsid-independent assembly of coronavirus-like particles by coexpression of viral envelope proteins. EMBO J. 15:2020-2028.
55. Watret, G. E., G. R. Pringle, and R. M. Elliott. 1985. Synthesis of bunyavirus-specific proteins in a continuous cell line (XTC-2) derived from Xenopus laevis. J. Gen. Virol. 66:473-482.
56. Weber, F., E. F. Dunn, A. Bridgen, and R. M. Elliott. 2001. The Bunyamwera virus nonstructural protein NSs inhibits viral RNA polymerase in a minireplicon system. Virology 281:67-74.
57. Yeager, M., E. M. Wilson-Kubalek, S. G. Weiner, P. O. Brown, and A. Rein. 1998. Supramolecular organization of immature and mature murine leukemia virus revealed by electron cryo-microscopy: Implications for retroviral assembly mechanisms. Proc. Natl. Acad. Sci. USA 95:7299-7304.
58. Zhang, Y., J. Corver, P. R. Chapman, W. Zhang, S. V. Pletnev, D. Sedlak, T. S. Baker, J. H. Strauss, R. J. Kuhn, and M. G. Rossmann. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613.