The transmembrane domains of the prM and E proteins of yellow fever virus are endoplasmic reticulum localization signals

Journal of Virology

Volumn 78, Issue 22, 2004, Pages 12591-12602

  De Beeck, Anne Op ^a   Rouillé, Yves ^a   Caron, Mélanie ^a   Duvet, Sandrine ^b   Dubuisson, Jean ^a,c  

^a INSTITUT PASTEUR DE LILLE   (France)

^b UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^c INSTITUT DE BIOLOGIE DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CHIMERIC PROTEIN; ENVELOPE PROTEIN; GLYCAN;

ALPHA HELIX; ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; YELLOW FEVER FLAVIVIRUS;

AMINO ACID SEQUENCE; ANTIGENS, CD4; CELL MEMBRANE; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; RECOMBINANT FUSION PROTEINS; VIRAL ENVELOPE PROTEINS; YELLOW FEVER VIRUS;

EID: 7644232918     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.22.12591-12602.2004     Document Type: Article

References (69)

1. Allison, S. L., K. Stadler, C. W. Mandl, C. Kunz, and F. X. Heinz. 1995. Synthesis and secretion of recombinant tick-borne encephalitis virus protein E in soluble and particulate form. J. Virol. 69:5816-5820.
2. Allison, S. L., K. Stiasny, K. Stadler, C. W. Mandl, and F. X. Heinz. 1999. Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein E. J. Virol. 73:5605-5612.
3. Andersson, A. M., L. Melin, A. Bean, and R. F. Pettersson. 1997. A retention signal necessary and sufficient for Golgi localization maps to the cytoplasmic tail of a Bunyaviridae (Uukuniemi virus) membrane glycoprotein. J. Virol. 71:4717-4727.
4. Armstrong, J., and S. Patel. 1991. The Golgi sorting domain of coronavirus E1 protein. J. Cell Sci. 98:567-575.
5. Barlowe, C. 2003. Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol. 13:295-300.
6. Barlowe, C., L. Orci, T. Yeung, M. Hosobuchi, S. Hamamoto, N. Salama, M. F. Rexach, M. Ravazzola, M. Amherdt, and R. Schekman. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895-907.
7. Bause, E., W. Breuer, J. Schweden, R. Roeser, and R. Geyer. 1992. Effect of substrate structure on the activity of Man9-mannosidase from pig liver involved in N-linked oligosaccharide processing. Eur. J. Biochem. 208:451-457.
8. Bischoff, J., and R. Kornfeld. 1986. The use of 1-deoxymannojirimycin to evaluate the role of various α-mannosidases in oligosaccharide processing in intact cells. J. Biol. Chem. 261:4758-4765.
9. Bonifacino, J. S., P. Cosson, N. Shah, and R. D. Klausner. 1991. Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum. EMBO J. 10:2783-2793.
10. Bonifacino, J. S., C. K. Suzuki, and R. D. Klausner. 1990. A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum. Science 247:79-82.
11. Bretcher, M. S., and S. Munro. 1993. Cholesterol and Golgi apparatus. Science 261:1280-1281.
12. Cocquerel, L., S. Duvet, J.-C. Meunier, A. Pillez, R. Cacan, C. Wychowski, and J. Dubuisson. 1999. The transmembrane domain of hepatitis C virus glycoprotein E1 is a signal for static retention in the endoplasmic reticulum. J. Virol. 73:2641-2649.
13. Cocquerel, L., J.-C. Meunier, A. Pillez, C. Wychowski, and J. Dubuisson. 1998. A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. J. Virol. 72:2183-2191.
14. Cocquerel, L., A. Op de Beeck, M. Lambot, J. Roussel, D. Delgrange, A. Pillez, C. Wychowski, F. Penin, and J. Dubuisson. 2002. Topologic changes in the transmembrane domains of hepatitis C virus envelope glycoproteins. EMBO J. 21:2893-2902.
15. Cocquerel, L., C. Wychowski, F. Minner, F. Penin, and J. Dubuisson. 2000. Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a key role in the processing, subcellular localization and assembly of these envelope proteins. J. Virol. 74:3623-3633.
16. Despres, P., A. Cahour, A. Dupuy, V. Deubel, M. Bouloy, J. P. Digoutte, and M. Girard. 1987. High genetic stability of the region coding for the structural proteins of yellow fever virus strain 17D. J. Gen. Virol. 68:2245-2247.
17. Dominguez, M., K. Dejgaard, J. Fullekrug, S. Dahan, A. Fazel, J. P. Paccaud, D. Y. Thomas, J. J. Bergeron, and T. Nilsson. 1998. gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer. J. Cell Biol. 140:751-765.
18. Dubuisson, J., H. H. Hsu, R. C. Cheung, H. B. Greenberg, D. G. Russell, and C. M. Rice. 1994. Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J. Virol. 68:6147-6160.
19. Dubuisson, J., and C. M. Rice. 1996. Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin. J. Virol. 70:778-786.
20. Ferlenghi, I., M. Clarke, T. Ruttan, S. L. Allison, J. Schalich, F. X. Heinz, S. C. Harrison, F. A. Rey, and S. D. Fuller. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593-602.
21. Fiedler, K., M. Veit, M. A. Stamnes, and J. E. Rothman. 1996. Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science 273:1396-1399.
22. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83: 8122-8126.
23. Hebert, D. N., B. Foellmer, and A. Helenius. 1995. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 81:425-433.
24. Heinz, F. X., and S. L. Allison. 2000. Structures and mechanisms in flavivirus fusion. Adv. Virus Res. 55:231-269.
25. Hobman, T. C., L. Woodward, and M. G. Farquahr. 1995. Targeting of a heterodimeric membrane complex to the Golgi complex: rubella virus E2 glycoprotein contains a transmembrane Golgi retention signal. Mol. Biol. Cell 6:7-20.
26. Kappeler, F., D. R. Klopfenstein, M. Foguet, J. P. Paccaud, and H. P. Hauri. 1997. The recycling of ERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum-exit determinant interacting with COPII. J. Biol. Chem. 272:31801-31808.
27. Kmiécik, D., V. Herman, C. J. M. Stroop, J. C. Michalski, A. M. Mir, O. Labiau, A. Verbert, and R. Cacan. 1995. Catabolism of glycan moieties of lipid intermediates leads to a single Man5GlcNAc oligosaccharide isomer: a study with permeabilized CHO cells. Glycobiology 5:483-494.
28. Konishi, E., and P. W. Mason. 1993. Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the pre-membrane protein. J. Virol. 67:1672-1675.
29. Kuhn, R. J., W. Zhang, M. G. Rossmann, S. V. Pletnev, 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.
30. Kummerer, B. M., and C. M. Rice. 2002. Mutations in the yellow fever virus nonstructural protein NS2A selectively block production of infectious particles. J. Virol. 76:4773-4784.
31. Letourneur, F., and P. Cosson. 1998. Targeting to the endoplasmic reticulum in yeast cells by determinants present in transmembrane domains. J. Biol. Chem. 273:33273-33278.
32. Lindenbach, B. D., and C. M. Rice. 2001. Flaviviridae: the viruses and their replication, p. 991-1042. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins. Philadelphia, Pa.
33. Littman, D. R., Y. Thomas, P. J. Maddon, L. Chess, and R. Axel. 1985. The isolation and sequence of the gene encoding T8: a molecule defining functional classes of T lymphocytes. Cell 40:237-246.
34. Liu, W. J., H. B. Chen, and A. A. Khromykh. 2003. Molecular and functional analyses of Kunjin virus infectious cDNA clones demonstrate the essential roles for NS2A in virus assembly and for a nonconservative residue in NS3 in RNA replication. J. Virol. 77:7804-7813.
35. Liu, W. J., P. L. Sedlak, N. Kondratieva, and A. A. Khromykh. 2002. Complementation analysis of the flavivirus Kunjin NS3 and NS5 proteins defines the minimal regions essential for formation of a replication complex and shows a requirement of NS3 in cis for virus assembly. J. Virol. 76: 10766-10775.
36. Locker, J. K., J. Klumperman, V. Oorschot, M. C. Horzinek, H. J. Geuze, and P. J. M. Rottier. 1994. The cytoplasmic tail of mouse hepatitis virus M protein is essential but not sufficient for its retention in the Golgi complex. J. Biol. Chem. 269:28263-28269.
37. Lorenz, I. C., S. L. Allison, F. X. Heinz, and A. Helenius. 2002. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J. Virol. 76:5480-5491.
38. Lorenz, I. C., J. Kartenbeck, A. Mezzacasa, S. L. Allison, F. X. Heinz, and A. Helenius. 2003. Intracellular assembly and secretion of recombinant subviral particles from tick-borne encephalitis virus. J. Virol. 77:4370-4382.
39. Machamer, C. E., and J. K. Rose. 1987. A specific transmembrane domain of a coronavirus E1 glycoprotein is required for its retention in the Golgi region. J. Cell Biol. 105:1205-1214.
40. Mackenzie, J. M., and E. G. Westaway. 2001. Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J. Virol. 75:10787-10799.
41. Martire, G., G. Mottola, M. C. Pascale, N. Malagolini, I. Turrini, F. Serafini-Cessi, M. R. Jackson, and S. Bonatti. 1996. Different fate of a single reporter protein containing KDEL or KKXX targeting signals stably expressed in mammalian cells. J. Biol. Chem. 271:3541-3547.
42. Moss, B., O. Elroy-Stein, T. Mizukami, W. A. Alexander, and T. R. Fuerst. 1990. New mammalian expression vectors. Nature 348:91-92.
43. Mottola, G., N. Jourdan, G. Castaldo, N. Malagolini, A. Lahm, F. Serafini-Cessi, G. Migliaccio, and S. Bonatti. 2000. A new determinant of endoplasmic reticulum localization is contained in the juxtamembrane region of the ectodomain of hepatitis C virus glycoprotein E1. J. Biol. Chem. 275:24070-24079.
44. Munro, S. 1995. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 17:4695-4704.
45. Nishimura, N., and W. E. Balch. 1997. A di-acidic signal required for selective export from the endoplasmic reticulum. Science 277:556-558.
46. Op De Beeck, A., L. Cocquerel, and J. Dubuission. 2001. Biogenesis of hepatitis C virus envelope glycoproteins. J. Gen. Virol. 82:2589-2595.
47. Op De Beeck, A., and J. Dubuisson. 2003. Topology of hepatitis C virus envelope glycoproteins. Rev. Med. Virol. 13:233-241.
48. Op De Beeck, A., R. Molenkamp, M. Caron, A. Ben Younes, P. Bredenbeek, and J. Dubuisson. 2003. Role of the transmembrane domains of prM and E proteins in the formation of yellow fever virus envelope. J. Virol. 77:813-820.
49. Op De Beeck, A., R. Montserret, S. Duvet, L. Cocquerel, R. Cacan, B. Barberot, M. Le Maire, F. Penin, and J. Dubuisson. 2000. Role of the transmembrane domains of hepatitis C virus envelope proteins E1 and E2 in the assembly of the noncovalent E1E2 heterodimer. J. Biol. Chem. 275: 31428-31437.
50. Pascale, M. C., M. C. Erra, N. Malagolini, F. Serafini-Cessi, A. Leone, and S. Bonatti. 1992. Post-translational processing of an O-glycosylated protein, the human CD8 glycoprotein, during the intracellular transport to the plasma membrane. J. Biol. Chem. 267:25196-25201.
51. Pascale, M. C., N. Malagolini, F. Serafini-Cessi, G. Migliaccio, A. Leone, and S. Bonatti. 1992. Biosynthesis and oligosaccharide structure of human CD8 glycoprotein expressed in a rat epithelial cell line. J. Biol. Chem. 267:9940-9947.
52. Pedrazzini, E., A. Villa, and N. Borgese. 1996. A mutant cytochrome b5 with a lengthened membrane anchor escapes from the endoplasmic reticulum and reaches the plasma membrane. Proc. Natl. Acad. Sci. USA 93:4207-4212.
53. Pettersson, R. F. 1991. Protein localization and virus assembly at intracellular membranes. Curr. Top. Microbiol. Immunol. 170:67-104.
54. Popot, J.-L. 1993. Integral membrane protein structure: transmembrane α-helices as autonomous folding domains. Curr. Opin. Struct. Biol. 3:532-540.
55. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375:291-298.
56. Robertson, B., G. Myers, C. Howard, T. Brettin, J. Bukh, B. Gaschen, T. Gojobori, G. Maertens, M. Mizokami, O. Nainan, S. Netesov, K. Nishioka, T. Shini, P. Simmonds, D. Smith, L. Stuyver, and A. Weiner, for the International Committee on Virus Taxonomy. 1998. Classification, nomenclature, and database development for hepatitis C virus (HCV) and related viruses: proposals for standardization. Arch. Virol. 143:2493-2503.
57. Rothman, J. E., and F. T. Wieland. 1996. Protein sorting by transport vesicles. Science 272:227-234.
58. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
59. Sevier, C. S., O. A. Weisz, M. Davis, and C. E. Machamer. 2000. Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell 11:13-22.
60. Shin, J., R. L. Dunbrack, S. Lee, and J. L. Strominger. 1991. Signals for retention of transmembrane proteins in the endoplasmic reticulum studied with CD4 truncation mutants. Proc. Natl. Acad. Sci. USA 88:1918-1922.
61. 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.
62. Stiasny, K., S. L. Allison, A. Marchler-Bauer, C. Kunz, and F. X. Heinz. 1996. Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. J. Virol. 70:8142-8147.
63. Szczesna-Skorupa, E., and B. Kemper. 2000. Endoplasmic reticulum retention determinants in the transmembrane and linker domains of cytochrome P450 2C1. J. Biol. Chem. 275:19409-19415.
64. Weisz, O. A., A. M. Swift, and C. E. Machamer. 1993. Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J. Cell Biol. 122:1185-1196.
65. Weng, S., and R. G. Spiro. 1993. Demonstration that a kifunensine-resistant alpha-mannosidase with a unique processing action on N-linked oligosaccharides occurs in rat liver endoplasmic reticulum and various cultured cells. J. Biol. Chem. 268:25656-25663.
66. Wengler, G. 1989. Cell-associated West Nile flavivirus is covered with E+pre-M protein heterodimers which are destroyed and reorganized by proteolytic cleavage during virus release. J. Virol. 63:2521-2526.
67. Yang, M., J. Ellenberg, J. S. Bonifacino, and A. M. Weissman. 1997. The transmembrane domain of a carboxy-terminal anchored protein determines localization to the endoplasmic reticulum. J. Biol. Chem. 272:1970-1975.
68. Zhang, W., P. R. Chipman, J. Corver, P. R. Johnson, Y. Zhang, S. Mukhopadhyay, T. S. Baker, J. H. Strauss, M. G. Rossmann, and R. J. Kuhn. 2003. Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat. Struct. Biol. 10:907-912.
69. Zhang, Y., J. Corver, P. R. Chipman, 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.