Furin processing and proteolytic activation of Semliki Forest virus

Journal of Virology

Volumn 77, Issue 5, 2003, Pages 2981-2989

  Zhang, Xinyong ^a   Fugère, Martin ^b   Day, Robert ^b   Kielian, Margaret ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; FURIN; GLYCOPROTEIN E1; PROTEIN E2; PROTEIN P62; PROTEIN PRECURSOR; PROTEINASE; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN;

ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; MEMBRANE FUSION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; SEMLIKI FOREST ALPHAVIRUS; VIRUS CELL INTERACTION; VIRUS INFECTION;

ANIMALS; CELL LINE; CRICETINAE; DIMERIZATION; FURIN; HYDROGEN-ION CONCENTRATION; MEMBRANE FUSION; PROTEIN PRECURSORS; SEMLIKI FOREST VIRUS; SUBTILISINS; VIRAL ENVELOPE PROTEINS; VIRUS ACTIVATION;

EID: 0037369080     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.5.2981-2989.2003     Document Type: Article

References (54)

1. Abrami, L., M. Fivaz, E. Decroly, N. G. Seidah, F. Jean, G. Thomas, S. H. Leppla, J. T. Buckley, and F. G. van der Goot. 1998. The pore-forming toxin proaerolysin is activated by furin. J. Biol. Chem. 273:32656-32661.
2. Andersson, H., B.-U. Barth, M. Ekström, and H. Garoff. 1997. Oligomerization-dependent folding of the membrane fusion protein of Semliki Forest virus. J. Virol. 71:9654-9663.
3. 2+-independent endoprotease activity from peripheral blood lymphocytes: involvement in HIV-1 gp160 maturation. Biochemistry 40:4800-4810.
4. Bergeron, F., R. Leduc, and R. Day. 2000. Subtilase-like pro-protein convertases: from molecular specificity to therapeutic applications. J. Mol. Endocrinol. 24:1-22.
5. Bravo, D. A., J. B. Gleason, R. I. Sanchez, R. A. Roth, and R. S. Fuller. 1994. Accurate and efficient cleavage of the human insulin proreceptor by the human proprotein-processing protease furin. Characterization and kinetic parameters using the purified, secreted soluble protease expressed by a recombinant baculovirus. J. Biol. Chem. 269:25830-25837.
6. Carleton, M., H. Lee, M. Mulvey, and D. T. Brown. 1997. Role of glycoprotein PE2 in formation and maturation of the Sindbis virus spike. J. Virol. 71:1558-1566.
7. deCurtis, I., and K. Simons. 1988. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells. Proc. Natl. Acad. Sci. USA 85:8052-8056.
8. Demaurex, N., W. Furuya, S. D'Souza, J. S. Bonifacino, and S. Grinstein. 1998. Mechanism of acidification of the trans-Golgi network (TGN). In situ measurements of Ph using retrieval of TGN38 and furin from the cell surface. J. Biol. Chem. 273:2044-2051.
9. Dubois, C. M., F. Blanchette, M. H. Laprise, R. Leduc, F. Grondin, and N. G. Seidah. 2001. Evidence that furin is an authentic transforming growth factor-β1-converting enzyme. Am. J. Pathol. 158:305-316.
10. Dubois, C. M., M. H. Laprise, F. Blanchette, L. E. Gentry, and R. Leduc. 1995. Processing of transforming growth factor beta 1 I precursor by human furin convertase. J. Biol. Chem. 270:10618-10624.
11. Duffus, W. A., P. Levy-Mintz, M. R. Klimjack, and M. Kielian. 1995. Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly. J. Virol. 69:2471-2479.
12. Ferlenghi, I., B. Gowen, F. D. Haas, E. J. Mancini, H. Garoff, M. Sjoberg, and S. D. Fuller. 1998. The first step: maturation of the Semliki Forest virus spike occurs through a dramatic localized conformational change. J. Mol. Biol. 283:71-81.
13. Fugere, M., P. C. Limperis, V. Beaulieu-Audy, F. Gagnon, P. Lavigne, K. Klarskov, R. Leduc, and R. Day. 2002. Inhibitory potency and specificity of subtilase-like pro-protein convertase (SPC) prodomains. J. Biol. Chem. 277: 7648-7656.
14. Gibbons, D. L., A. Ahn, P. K. Chatterjee, and M. Kielian. 2000. Formation and characterization of the trimeric form of the fusion protein of Semliki Forest virus. J. Virol. 74:7772-7780.
15. Glomb-Reinmund, S., and M. Kielian. 1998. fus-1, a Ph shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J. Virol. 72:4281-4287.
16. Gonzalez-Reyes, L., M. B. Ruiz-Arguello, B. Garcia-Barreno, L. Calder, J. A. Lopez, J. P. Albar, J. J. Skehel, D. C. Wiley, and J. A. Melero. 2001. Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc. Natl. Acad. Sci. USA 98:9859-9864.
17. Gordon, V. M., R. Benz, K. Fujii, S. H. Leppla, and R. K. Tweten. 1997. Clostridium septicum alpha-toxin is proteolytically activated by furin. Infect. Immun. 65:4130-4134.
18. Gordon, V. M., K. R. Klimpel, N. Arora, M. A. Henderson, and S. H. Leppla. 1995. Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect. Immun. 63:82-87.
19. Gordon, V. M., A. Rehemtulla, and S. H. Leppla. 1997. A role for PACE4 in the proteolytic activation of anthrax toxin protective antigen. Infect. Immun. 65:3370-3375.
20. Gu, M., J. Rappaport, and S. H. Leppla. 1995. Furin is important but not essential for the proteolytic maturation of gp160 of HIV-1. FEBS Lett. 365:95-97.
21. Heinz, F. X., and S. L. Allison. 2000. Structures and mechanisms in flavivirus fusion. Adv. Virus Res. 55:231-269.
22. Inocencio, N. M., J. F. Sucic, J. M. Moehring, M. J. Spence, and T. J. Moehring. 1997. Endoprotease activities other than furin and PACE4 with a role in processing of HIV-I gp160 glycoproteins in CHO-K1 cells. J. Biol. Chem. 272:1344-1348.
23. Jain, S. K., S. DeCandido, and M. Kielian. 1991. Processing of the p62 envelope precursor protein of Semliki Forest virus. J. Biol. Chem. 266:5756-5761.
24. Kielian, M. 1995. Membrane fusion and the alphavirus life cycle. Adv. Virus Res. 45:113-151.
25. Kielian, M., S. Jungerwirth, K. U. Sayad, and S. DeCandido. 1990. Biosynthesis, maturation, and acid activation of the Semliki Forest virus fusion protein. J. Virol. 64:4614-4624.
26. Klenk, H. D., and W. Garten. 1994. Host cell proteases controlling virus pathogenicity. Trends Microbiol. 2:39-43.
27. Klenk, H. D., R. Rott, M. Orlich, and J. Blodorn. 1975. Activation of influenza A viruses by trypsin treatment. Virology 68:426-439.
28. Klimstra, W. B., H. W. Heidner, and R. E. Johnston. 1999. The furin protease cleavage recognition sequence of Sindbis virus PE2 can mediate virion attachment to cell surface heparan sulfate. J. Virol. 73:6299-6306.
29. Lescar, J., A. Roussel, M. W. Wien, J. Navaza, S. D. Fuller, G. Wengler, and F. A. Rey. 2001. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105:137-148.
30. Liu, B., N. Amizuka, D. Goltzman, and S. A. Rabbani. 1995. Inhibition of processing of parathyroid hormone-related peptide by anti-sense furin: effect in vitro and in vivo on rat Leydig (H-500) tumor cells. Int. J. Cancer 63:276-281.
31. Lobigs, M., and H. Garoff. 1990. Fusion function of the Semliki Forest virus spike is activated by proteolytic cleavage of the envelope glycoprotein precursor p62. J. Virol. 64:1233-1240.
32. Lobigs, M., J. M. Wahlberg, and H. Garoff. 1990. Spike protein oligomerization control of Semliki Forest virus fusion. J. Virol. 64:5214-5218.
33. Lu, Y. E., C. H. Eng, S. G. Shome, and M. Kielian. 2001. In vivo generation and characterization of a soluble form of the Semliki Forest virus fusion protein. J. Virol. 75:8329-8339.
34. Marquardt, M. T., and M. Kielian. 1996. Cholesterol-depleted cells that are relatively permissive for Semliki Forest virus infection. Virology 224:198-205.
35. McCune, J. M., L. B. Rabin, M. B. Feinberg, M. Lieberman, J. C. Kosek, G. R. Reyes, and I. L. Weissman. 1988. Endoproteolytic cleavage of gp160 is required for the activation of human immunodeficiency virus. Cell 53:55-67.
36. Moehring, J. M., N. M. Inocencio, B. J. Robertson, and T. J. Moehring. 1993. Expression of mouse furin in a Chinese hamster cell resistant to Pseudomonas exotoxin A and viruses complements the genetic lesion. J. Biol. Chem. 268:2590-2594.
37. Molinari, M., and A. Helenius. 2000. Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288:331-333.
38. Molloy, S. S., E. D. Anderson, F. Jean, and G. Thomas. 1999. Bi-cycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol. 9:28-35.
39. Moulard, M., and E. Decroly. 2000. Maturation of HIV envelope glycoprotein precursors by cellular endoproteases. Biochim. Biophys. Acta 1469:121-132.
40. Nakayama, K. 1997. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J. 327:625-635.
41. Phalen, T., and M. Kielian. 1991. Cholesterol is required for infection by Semliki Forest virus. J. Cell Biol. 112:615-623.
42. Pletnev, S. V., W. Zhang, S. Mukhopadhyay, B. R. Fisher, R. Hernandez, D. T. Brown, T. S. Baker, M. G. Rossmann, and R. J. Kuhn. 2001. Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold. Cell 105:127-136.
43. Raghunath, M., E. A. Putnam, T. Ritty, D. Hamstra, E. S. Park, M. Tschodrich-Rotter, R. Peters, A. Rehemtulla, and D. M. Milewicz. 1999. Carboxy-terminal conversion of profibrillin to fibrillin at a basic site by PACE/furin-like activity required for incorporation in the matrix. J. Cell Sci. 112:1093-1100.
44. Salminen, A., J. M. Wahlberg, M. Lobigs, P. Liljeström, and H. Garoff. 1992. Membrane fusion process of Semliki Forest virus. II. Cleavage-dependent reorganization of the spike protein complex controls virus entry. J. Cell Biol. 116:349-357.
45. Sariola, M., J. Saraste, and E. Kuismanen. 1995. Communication of post-Golgi elements with early endocytic pathway: regulation of endoproteolytic cleavage of Semliki Forest virus p62 precursor. J. Cell Sci. 108:2465-2475.
46. Skehel, J. J., and D. C. Wiley. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69:531-569.
47. Smit, J. M., W. B. Klimstra, K. D. Ryman, R. Bittman, R. E. Johnston, and J. Wilschut. 2001. PE2 cleavage mutants of Sindbis virus: correlation between viral infectivity and pH-dependent membrane fusion activation of the spike heterodimer. J. Virol. 75:11196-11204.
48. Stadler, 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.
49. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
50. Vashishtha, M., T. Phalen, M. T. Marquardt, J. S. Ryu, A. C. Ng, and M. Kielian. 1998. A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J. Cell Biol. 140:91-99.
51. Wahlberg, J. M., W. A. M. Boere, and H. Garoff. 1989. The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation. J. Virol. 63:4991-4997.
52. Wahlberg, J. M., R. Bron, J. Wilschut, and H. Garoff. 1992. Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein. J. Virol. 66:7309-7318.
53. Watson, D. G., J. M. Moehring, and T. J. Moehring. 1991. A mutant CHO-K1 strain with resistance to Pseudomonas exotoxin A and alphaviruses fails to cleave Sindbis virus glycoprotein PE2. J. Virol. 65:2332-2339.
54. Zhang, W., S. Mukhopadhyay, S. V. Pletnev, T. S. Baker, R. J. Kuhn, and M. G. Rossmann. 2002. Placement of the structural proteins in Sindbis virus. J. Virol. 76:11645-11658.