The first step: Activation of the Semliki Forest virus spike protein precursor causes a localized conformational change in the trimeric spike

Journal of Molecular Biology

Volumn 283, Issue 1, 1998, Pages 71-81

  Ferlenghi, Ilaria ^a   Gowen, Brent ^a,c   De Haas, Felix ^a   Mancini, Erika J ^a   Garoff, Henrik ^b   Sjöberg, Mathilda ^b   Fuller, Stephen D ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Conformational change; Cryo electron microscopy; Image reconstruction; Membrane fusion; Virus structure

Indexed keywords

HYBRID PROTEIN; VIRUS PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; SEMLIKI FOREST ALPHAVIRUS; VIRUS ACTIVATION; VIRUS CAPSID; VIRUS NUCLEOCAPSID; VIRUS PARTICLE;

ALPHAVIRUS; MIRIDAE; RNA VIRUSES; SEMLIKI FOREST VIRUS;

EID: 0032538274     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2066     Document Type: Article

References (54)

1. Anthony, R. P. & Brown, D. T. (1991). Sindbis virus membrane fusion is mediated by a reduction of glycoprotein disulphide bridges at the cell surface. J. Virol. 65, 1187-1194.
2. Anthony, R. P., Paredes, A. M. & Brown, D. T. (1992). Disulphide bonds are essential for the stability of the Sindbis virus envelope. J. Virol. 190, 330-336.
3. Baker, D. & Agard, D. A. (1994). Influenza hemagglutinin: kinetic control of protein function. Structure, 2, 907-910.
4. Baker, T. S. & Cheng, R. H. (1996). A model-based method for determining orientations of biological molecules by cryoelectron microscopy. J. Struct. Biol. 116, 120-130.
5. Berglund, P., Sjöberg, M., Garoff, H., Atkins, G. J., Sheahan, B. J. & Liljeström, P. (1993). Semliki Forest virus expression system: production of conditionally infectious recombinant particles. Biotechnology, 11, 916-920.
6. Böttcher, B., Kiselev, N. A., Stel'mashchuk, V. Y., Perevozchikova, N. A., Borisov, A. V. & Crowther, R. A. (1997a). Three-dimensional structure of the infectious bursal disease virus determined by electron cryomicroscopy. J. Virol. 71, 325-330.
7. Böttcher, B., Wynne, S. A. & Crowther, R. A. (1997b). Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature, 386, 88-91.
8. Bron, R., Wahlberg, J. M., Garoff, H. & Wilschut, J. (1993). Membrane fusion of Semliki Forest virus in a model system: correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J. 12, 693-701.
9. Carr, C. M. & Kim, P. S. (1993). A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell, 73, 823-832.
10. Carr, C. M., Chaudhry, C. & Kim, P. S. (1997). Influenza haemagglutinin is spring-loaded by a metastable native conformation. Proc. Natl Acad. Sci. USA, 94, 14306-14313.
11. Cheng, R., Kühn, R., Olson, N., Rossmann, M. & Baker, T. (1995). Nucleocapsid and glycoprotein organization in an enveloped virus. Cell, 80, 621-630.
12. Choi, H. K., Tong, L., Minor, W., Dumas, P., Boege, U., Rossmann, M. G. & Wengler, G. (1991). Structure of the Sindbis virus core protein reveals a chymotrypsin-like serine protease and the organization of the virion. Nature, 354, 37-43.
13. Choi, H.-K., Lu, G., Lee, S., Wengler, G. & Rossmann, M. G. (1997). Structure of the Semliki Forest virus core protein. Proteins Struct. Funct. Genet. 27, 345-359.
14. deCurtis, I. & Simons, K. (1988). Dissection of Semliki Forest virus glycoprotein delivery from the transGolgi network to the cell surface in permeablized BHK cells. Proc. Natl Acad. Sci. USA, 85, 8052-8056.
15. Denault, J.-B. & Leduc, R. (1996). Furin/PACE/SPC1: a convertase involved in exocytic and endocytic processing of precursor proteins. FEBS Letters, 379, 113-116.
16. DeTulleo, L. & Kirchhausen, T. (1998). The clathrin endocytic pathway in virus infection. EMBO J. 17, 4585-4593.
17. Fuller, S. D. (1987). The T = 4 envelope of Sindbis virus is organized by complementary interactions with a T = 3 icosahedral capsid. Cell, 48, 923-934.
18. Fuller, S. D. (1994). Illuminating fusion. Structure, 2, 903-906.
19. Fuller, S. D. (1995). Cryo-electron microscopy reveals mechanisms for the control of virion size and suggests their application to HIV. Saibo, 27, 447-452.
20. Fuller, S. D., Berriman, J. A., Butcher, S. J. & Gowen, B. E. (1995). Low pH induces the swivelling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell, 81, 715-725.
21. Fuller, S. D., Butcher, S. J., Cheng, R. H. & Baker, T. S. (1996). Three-dimensional reconstruction of icosahedral particles: the uncommon line. J. Struct. Biol. 116, 48-55.
22. Garoff, H., Frischauf, A.-M., Simons, K., Lehrach, H. & Delius, H. (1980). Nucleotide sequence of cDNA coding for Semliki Forest virus membrane glycoproteins. Nature, 288, 236-241.
23. Garoff, H., Kondor-Koch, C. & Riedel, H. (1982). Structure and assembly of alphaviruses. Curr. Topics Microbiol. Immunol. 99, 1-50.
24. Griffiths, G., Pfeiffer, S., Simons, K. & Matlin, K. (1985). Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane. J. Cell Biol. 101, 949-964.
25. Griffiths, G., Fuller, S. D., Back, R., Pfeiffer, S. & Simons, K. (1988). The dynamic nature of the Golgi complex. J. Cell Biol. 108, 277-97.
26. Griffiths, G., Quinn, P. & Warren, G. (1983). Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from the medial to the trans Golgi in baby hamster kidney cells infected with Semliki Forest virus. J. Cell Biol. 96, 835-850.
27. Guirakhoo, F., Heinz, F. X., Mandl, C. W., Holzmann, H. & Kunz, C. (1991). Fusion activity of flaviviruses: comparison of mature and immature (prM-containing) tick-borne encephalitis virions. J. Gen. Virol. 72, 1323-1329.
28. Kenney, J. M., Sjöberg, M., Garoff, H. & Fuller, S. D. (1994). Fusion activation of the Semliki Forest virus spike complex. Structure, 2, 823-832.
29. Kielian, M. (1995). Membrane fusion and the alphavirus life cycle. Advan. Virus Res. 45, 113-151.
30. Kielian, M. & Helenius, A. (1986). Entry of alphaviruses. In The Togaviridae and Flaviviridae (Schlesinger, S. & Schlesinger, M. J., eds), pp. 91-119, Plenum Publishing Inc., New York.
31. Kielian, M., Jungerwirth, S., Sayad, K. U. & DeCandido, S. (1990). Biosynthesis, maturation, and acid-activation of the Semliki Forest virus fusion protein. J. Virol. 64, 4614-4624.
32. Mancini, E. J., de Haas, F. & Fuller, S. D. (1997). High resolution icosahedral reconstruction: fulfilling the promise of cryo-electron microscopy. Structure, 5, 741-750.
33. Marquardt, T. & Helenius, A. (1992). Misfolding and aggregation of newly synthesized proteins in the endoplasmic reticulum. J. Cell Biol. 117, 505-13.
34. Paredes, A. M., Brown, D. T., Rothnagel, R., Chiu, W., Schoepp, R. J., Johnston, R. E. & Prasad, B. V. V. (1993). Three-dimensional structure of a membrane-containing virus. Proc. Natl Acad. Sci. USA, 90, 9095-9099.
35. Paredes, A. M., Heidner, H., Thuman-Commike, P., Prassad, B. V. P., Johnson, R. E. & Chiu, W. (1998). Structural localization of the E3 glycoprotein in attenuated Sindbis virus mutants. J. Virol. 72, 1534-1541.
36. Renz, D. & Brown, D. T. (1976). Characterization of Sindbis virus temperature-sensitive mutants in cultured BHK-21 and Aedes albopictus (mosquito) cells. J. Virol. 30, 281-298.
37. Ruigrok, R. W. H., Aitken, A., Calder, L. J., Martin, S. R., Skehel, J. J., Wharton, S. A., Weis, W. & Wiley, D. C. (1988). Studies on the structure of the influenza virus haemagglutinin at the pH of membrane fusion. J. Gen. Virol. 69, 2785-2795.
38. Salminen, A., Wahlberg, J. M., Lobigs, M., Liljestrom, P. & Garoff, H. (1992). Membrane fusion process of Semliki Forest virus. II: Cleavage-dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol 116, 349-57.
39. Sheehan, B., Fuller, S. D., Pique, M. E. & Yeager, M. (1996). AVS software for visualization in molecular microscopy. J. Struct. Biol. 116, 99-105.
40. Simons, K. & Fuller, S. D. (1987). The budding of enveloped viruses: a paradigm for membrane sorting? In Biological Organization: Macromolecular Interactions at High Resolution (Burnett, R. M. & Vogel, H. J., eds), pp. 139-150, Academic Press, Orlando.
41. Smeckens, S. P. (1993). Processing of protein precursors by a novel family of subtilisin related mamalian endoproteases. Bio/Technology, 11, 182-186.
42. Smith, T. J., Cheng, R. H., Olson, N. H., Peterson, P., Chase, E., Kuhn, R. J. & Baker, T. S. (1995). Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy. Proc. Natl Acad. Sci. USA, 92, 10648-10652.
43. Stadler, K., Allison, S. L., Schalich, J. & Heinz, F. X. (1997). Proteolytic activation of tick-borne encephalitis virus by furin. J. Virol. 71, 8475-8481.
44. Stewart, P. L., Burnett, R. M., Cyrklaff, M. & Fuller, S. D. (1991). Image reconstruction reveals the complex molecular organization of adenovirus. Cell, 67, 145-154.
45. van Heel, M. (1987). Similarity measures between images. Ultramicroscopy, 21, 95-100.
46. Vénien-Bryan, C. & Fuller, S. D. (1994). The organization of the spike complex of Semliki Forest virus. J. Mol. Biol. 236, 572-583.
47. Wahlberg, J. M. & Garoff, H. (1992). Membrane fusion process of Semliki Forest virus. I. Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J. Cell Biol. 116, 339-48.
48. Wahlberg, J. M., Bron, R., Wilschut, J. & Garoff, H. (1992). Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J. Virol. 66, 7309-18.
49. White, J., Kartenbeck, J. & Helenius, A. (1980). Fusion of Semliki Forest virus with the plasma membrane can be induced by low pH. J. Cell Biol. 87, 264-272.
50. White, J. M. (1990). Viral and cellular fusion protein. Annu. Rev. Physiol. 52, 675-697.
51. White, J. M. (1992). Membrane fusion. Science, 258, 917-924.
52. White, J. M., Kielian, M. & Helenius, A. (1983). Membrane fusion proteins of enveloped animal viruses. Quart. Rev. Biophys. 16, 151-195.
53. Wiley, D. C. & Skehel, J. J. (1987). The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56, 365-394.
54. Wiley, R. L., Bonifacino, J. S., Potts, B. J., Martin, M. A. & Klausner, R. D. (1988). Biosynthesis, cleavge, and degredation of the human immunodeficiency virus I envelope glycoprotein gp160. Proc. Natl Acad. Sci. USA, 85, 9580-9584.