Mutations in the carboxyl-terminal hydrophobic sequence of human cytomegalovirus glycoprotein B alter transport and protein chaperone binding

Journal of Virology

Volumn 70, Issue 11, 1996, Pages 8029-8040

  Zheng, Zhenwei ^a   Maidji, Ekaterina ^a   Tugizov, Sharof ^a   Pereira, Lenore ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; CALRETICULIN; CHAPERONE; VIRUS GLYCOPROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; GENE MUTATION; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION;

EID: 0029798646     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.11.8029-8040.1996     Document Type: Article

References (66)

1. Bergeron, J. J., M. B. Brenner, D. Y. Thomas, and D. B. Williams. 1994. Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem. Sci. 19:124-128.
2. Billstrom, M. A., and W. J. Britt. 1995. Postoligomerization folding of human cytomegalovirus glycoprotein B: identification of folding intermediates and importance of disulfide bonding. J. Virol. 69:7015-7022.
3. Bonifacino, J. S., and S. J. Lippincott. 1991. Degradation of proteins within the endoplasmic reticulum. Curr. Opin. Cell Biol. 3:592-600.
4. Boppana, S. B., M. A. Polis, A. A. Kramer, W. J. Britt, and S. Koenig. 1995. Virus-specific antibody responses to human cytomegalovirus (HCMV) in human immunodeficiency virus type 1-infected persons with HCMV retinitis. J. Infect. Dis. 171:182-185.
5. Britt, W. J., and L. G. Vugler. 1989. Processing of the gp55-116 envelope glycoprotein complex (gB) of human cytomegalovirus. J. Virol. 63:403-410.
6. Britt, W. J., and L. G. Vugler. 1990. Antiviral antibody responses in mothers and their newborn infants with clinical and subclinical congenital cytomegalovirus infections. J. Infect. Dis. 161:214-219.
7. Britt, W. J., and L. G. Vugler. 1992. Oligomerization of the human cytomegalovirus major envelope glycoprotein complex gB (gp55-116). J. Virol. 66: 6747-6754.
8. Chee, M. S., A. T. Bankier, S. Beck, R. Bohni, C. M. Brown, R. Cerny, T. Horsnell, C. A. Hutchison, T. Kouzarides, J. A. Martignetti, E. Preddie, S. C. Satchwell, P. Tomlinson, K. M. Weston, and B. G. Barrell. 1990. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr. Top. Microbiol. Immunol. 154:125-170.
9. Chen, W., J. Helenius, I. Braakman, and A. Helenius. 1995. Cotranslational folding and calnexin binding during glycoprotein synthesis. Proc. Natl. Acad. Sci. USA 92:6229-6233.
10. Cranage, M. P., T. Kouzarides, A. T. Bankier, S. Satchwell, K. Weston, P. Tomlinson, B. Barrell, H. Hart, S. E. Bell, A. C. Minson, and G. L. Smith. 1986. Identification of the human cytomegalovirus glycoprotein B gene and induction of neutralizing antibodies via its expression in recombinant vaccinia virus. EMBO J. 5:3057-3063.
11. Creighton, T. E. 1983. An empirical approach to protein conformation stability and flexibility, Biopolymers 22:49-58.
12. David, V., F. Hochstenbach, S. Rajagopalan, and M. B. Brenner. 1993. Interaction with newly synthesized and retained proteins in the endoplasmic reticulum suggests a chaperone function for human integral membrane protein IP90 (calnexin). J. Biol. Chem. 268:9585-9592.
13. Drew, L. 1988. Cytomegalovirus infection in patients with AIDS. J. Infect. Dis. 158:449-456.
14. Drew, W. L., E. S. Sweet, R. C. Miner, and E. S. Mocarski. 1984. Multiple infections by Cytomegalovirus in patients with acquired immunodeficiency syndrome. J. Infect. Dis. 150:952-953.
15. Freeman, W. R., D. E. Henderly, B. K. Lipson, N. A. Rao, and A. M. Levine. 1989. Retinopathy before the diagnosis of AIDS. Ann. Ophthalmol. 21:468-474.
16. Gething, M. J., and J. Sambrook. 1992. Protein folding in the cell. Nature (London) 355:33-45.
17. Hammond, C., I. Braakman, and A. Helenius. 1994. Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91:913-917.
18. Hammond, C., and A. Helenius. 1994. Folding of VSV G protein: sequential interaction with BiP and calnexin. Science 266:456-458.
19. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
20. Helenius, A., T. Marquardt, and I. Braakman. 1993. The endoplasmic reticulum as a protein folding compartment. Trends Cell Biol. 2:227-231.
21. Holland, G. N. 1994. AIDS: retinal and choroidal infections, p. 415-433. In H. Lewis and S. J. Ryan (ed.), Medical and surgical retina: advances, controversies, and management. Mosby, St. Louis.
22. Jackson, M. R., D. M. Cohen, P. A. Peterson, and D. B. Williams. 1994. Regulation of MHC class I transport by the molecular chaperone, calnexin (p88, IP90). Science 263:384-387.
23. Kim, P. S., and P. Arvan. 1995. Calnexin and BiP act as sequential molecular chaperones during thyroglobulin folding in the endoplasmic reticulum. J. Cell Biol. 128:29-38.
24. Klausner, R. D., and R. Sitia. 1990. Protein degradation in the endoplasmic reticulum. Cell 62:611-614.
25. Kornfeld, R., and S. Kornfeld. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664.
26. Kozutsumi, Y., M. Segal, K. Normington, M. J. Gething, and J. Sambrook. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature (London) 332: 462-464.
27. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
28. Meyers, J. D. 1985. Cytomegalovirus infection after organ allografting, p. 201. In B. Roizman and C. Lopez (ed.), The herpesviruses. Plenum Publishing Corp., New York.
29. Moss, B., O. Elroy-Stein, T. Mizukami, W. A. Alexander, and T. R. Fuertes. 1990. New mammalian expression vectors. Nature (London) 348:91-92.
30. Nauseef, W. M., S. J. McCormick, and R. A. Clark. 1995. Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J. Biol. Chem. 270:4741-4747.
31. Navarro, D., P. Paz, S. Tugizov, K. Topp, J. LaVail, and L. Pereira. 1993. Glycoprotein B of human Cytomegalovirus promotes virion penetration into cells, the transmission of infection from cell to cell, and fusion of infected cells. Virology 197:143-158.
32. Navarro, D., I. Qadri, and L. Pereira. 1991. A mutation in the ectodomain of herpes simplex virus I glycoprotein B causes defective processing and retention in the endoplasmic reticulum. Virology 184:253-264.
33. Otteken, A., and B. Moss. 1996. Calreticulin interacts with newly synthesized human immunodeficiency virus type 1 envelope glycoprotein, suggesting a chaperone function similar to that of calnexin. J. Biol. Chem. 271:97-103.
34. Ou, W. J., P. H. Cameron, D. Y. Thomas, and J. J. Bergeron. 1993. Association of folding intermediates of glycoproteins with calnexin during protein maturation. Nature (London) 364:771-776.
35. Pass, R. F., A. M. August, M. Dworsky, and D. W. Reynolds. 1982. Cytomegalovirus infection in a day-care center. N. Engl. J. Med. 307:477-479.
36. Pass, R. F., S. Stagno, G. J. Myers, and C. A. Alford. 1980. Outcome of symptomatic congenital Cytomegalovirus infection: results of long-term longitudinal follow-up. Pediatrics 66:758-762.
37. Pellett, P. E., K. G. Kousoulas, L. Pereira, and B. Roizman. 1985. Anatomy of the herpes simplex virus 1 strain F glycoprotein B gene: primary sequence and predicted protein structure of the wild type and of monoclonal antibody-resistant mutants. J. Virol. 53:243-253.
38. Pereira, L. 1994. Function of glycoprotein B homologues of the family Herpesviridae. Infect. Agents Dis. 3:9-28.
39. Pereira, L., M. Hoffman, M. Tatsuno, and D. Dondero. 1984. Polymorphism of human Cytomegalovirus glycoproteins characterized by monoclonal antibodies. Virology 139:73-86.
40. Pereira, L., S. Stagno, M. Hoffman, and J. E. Volanakis. 1983. Cytomegalovirus-infected cell polypeptides immune-precipitated by sera from children with congenital and perinatal infections. Infect. Immun. 39:100-108.
41. Peterson, J. R., A. Ora, P. N. Van, and A. Helenius. 1995. Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol. Biol. Cell 6:1173-1184.
42. Qadri, I., C. Gimeno, D. Navarro, and L. Pereira. 1991. Mutations in conformation-dependent domains of herpes simplex virus 1 glycoprotein B affect the antigenic properties, dimerization, and transport of the molecule. Virology 180:135-152.
43. Qadri, I., D. Navarro, P. Paz, and L. Pereira. 1992. Assembly of conformation-dependent neutralizing domains on human cytomegalovirus glycoprotein B. J. Gen. Virol. 73:2913-2921.
44. Rajagopalan, S., and M. B. Brenner. 1994. Calnexin retains unassembled major histocompatibility complex class I free heavy chains in the endoplasmic reticulum. J. Exp. Med. 180:407-412.
45. Ramakrishnan, M., S. Tugizov, L. Pereira, and A. S. Lee. 1995. Conformation-defective herpes simplex virus 1 glycoprotein B trans-activates the promoter of the grp94 gene that codes for the 94 kDa stress protein in the endoplasmic reticulum. DNA Cell Biol. 14:373-384.
46. Rasile, L., K. Ghosh, K. Raviprakash, and H. P. Ghosh. 1993. Effects of deletions in the carboxy-terminal hydrophobic region of herpes simplex virus glycoprotein gB on intracellular transport and membrane anchoring. J. Virol. 67:4856-4866.
47. Rasmussen, L., M. Nelson, M. Neff, and T. C. Merigan. 1988. Characterization of two different human cytomegalovirus glycoproteins which are targets for virus neutralizing antibody. Virology 163:309-318.
48. Reschke, M., B. Reis, K. Noding, D. Rohsiepe, A. Richter, T. Mockenhaupt, W. Garten, and K. Radsak. 1995. Constitutive expression of human cytomegalovirus glycoprotein B (gpUL55) with mutagenized carboxy-terminal hydrophobic domains. J. Gen. Virol. 76:113-122.
49. Romagnoli, P., and R. N. Germain. 1995. Inhibition of invariant chain (Ii)-calnexin interaction results in enhanced degradation of Ii but does not prevent the assembly of alpha beta Ii complexes. J. Exp. Med. 182:2027-2036.
50. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
51. Spaete, R. R., A. Saxena, P. I. Scott, G. J. Song, W. S. Probert, W. J. Britt, W. Gibson, L. Rasmussen, and C. Pachl. 1990. Sequence requirements for proteolytic processing of glycoprotein B of human cytomegalovirus strain Towne. J. Virol. 64:2922-2931.
52. Spaete, R. R., R. M. Thayer, W. S. Probert, F. R. Masiarz, S. H. Chamberlain, L. Rasmussen, T. C. Merigan, and C. Pachl. 1988. Human cytomegalovirus strain Towne glycoprotein B is processed by proteolytic cleavage. Virology 167:207-225.
53. Stagno, S., R. F. Pass, M. E. Dworsky, R. E. Henderson, E. G. Moore, P. D. Walton, and C. A. Alford. 1982. Congenital cytomegalovirus infection. N. Engl. J. Med. 306:945-949.
54. Tarentino, A. L., C. M. Gomez, and T. H. Plummer. 1985. Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry 24:4665-4671.
55. Tatu, U., C. Hammond, and A. Helenius. 1995. Folding and oligomerization of influenza hemagglutinin in the ER and the intermediate compartment. EMBO J. 14:1340-1348.
56. Tector, M., and R. D. Salter, 1995. Calnexin influences folding of human class I histocompatibility proteins but not their assembly with beta 2-microglobulin. J. Biol. Chem. 270:19638-19542.
57. Tugizov, S., D. Navarro, P. Paz, Y. Wang, I. Qadri, and L. Pereira. 1994. Function of human cytomegalovirus glycoprotein B: syncytium formation in cells constitutively expressing gB is blocked by virus-neutralizing antibodies. Virology 201:263-276.
58. Tugizov, S., Y. Wang, I. Qadri, D. Navarro, E. Maidji, and L. Pereira. 1995. Mutated forms of human cytomegalovirus glycoprotein B are impaired in inducing syncytium formation. Virology 209:580-591.
59. Vey, M., W. Schafer, B. Reis, R. Ohuchi, W. Britt, W. Garten, H. D. Klenk, and K. Radsak. 1995. Proteolytic processing of human cytomegalovirus glycoprotein B (gpUL55) is mediated by the human endoprotease furin. Virology 206:746-749.
60. Wada, I., S. Imai, M. Kai, F. Sakane, and H. Kanoh. 1995. Chaperone function of calreticulin when expressed in the endoplasmic reticulum as the membrane-anchored and soluble forms. J. Biol. Chem. 270:20298-20304.
61. Ward, C. L., S. Omura, and R. R. Kopito. 1995. Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83:121-127.
62. Ware, F, E., A. Vassilakos, P. A. Peterson, M. R. Jackson, M. A. Lehrman, and D. B. Williams. 1995. The molecular chaperone calnexin binds Glc1Man9GlcNAc2 oligosaccharide as an initial step in recognizing unfolded glycoproteins. J. Biol. Chem. 270:4697-4704.
63. Weiss, C. D., and J. M. White. 1993. Characterization of stable Chinese hamster ovary cells expressing wild-type, secreted, and glycosylphosphatidylinositol-anchored human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 67:7060-7066.
64. Wooden, S. K., L.-J. Li, D. Navarro, I. Qadri, L. Pereira, and A. S. Lee. 1991. Transactivation of the grp78 promoter by malfolded proteins, glycosylation block, and calcium ionophore is mediated through a proximal region containing a CCAAT motif which interacts with CTF/NF-1. Mol. Cell. Biol. 11:5612-5623.
65. Yamashita, Y., K. Shimokata, S. Mizuno, T. Daikoku, T. Tsurumi, and Y. Nishiyama. 1996. Calnexin acts as a molecular chaperone during the folding of glycoprotein B of human cytomegalovirus. J. Virol. 70:2237-2246.
66. Zheng, Z., and L. Pereira. Unpublished observations.