The human cytomegalovirus UL37 immediate-early regulatory protein is an integral membrane N-glycoprotein which traffics through the endoplasmic reticulum and Golgi apparatus

Journal of Virology

Volumn 70, Issue 10, 1996, Pages 7198-7208

  Al Barazi, Hebah O ^a   Colberg Poley, Anamaris M ^a  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOSIDASE;

ARTICLE; CONFORMATIONAL TRANSITION; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GOLGI COMPLEX; HUMAN CYTOMEGALOVIRUS; IMMEDIATE EARLY GENE; INTRACELLULAR TRANSPORT; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN GLYCOSYLATION; PROTEIN TRANSPORT;

EID: 0029814503     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.10.7198-7208.1996     Document Type: Article

References (55)

1. Al-Barazi, H. O., and A. M. Colberg-Poley. Unpublished observations.
2. Arlt, H., D. Lang, S. Gebert, and T. Stamminger. 1994. Identification of binding sites for the 86-kilodalton IE2 protein of human cytomegalovirus within an IE2-responsive viral early promoter. J. Virol. 68:4117-4125.
3. Britt, W. J., and C. A. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia.
4. Britt, W. J., and D. Auger. 1986. Synthesis and processing of the envelope gp55-116 complex of human cytomegalovirus. J. Virol. 58:185-191.
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. 1992. Oligomerization of the human major envelope glycoprotein complex gB (gp55-116). J. Virol. 66:6747-6754.
7. Chee, M. S., A. T. Bankier, S. Beck, R. Bohni, C. M. Brown, R. Cerny, T. Horsnell, C. A. Hutchison III, 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. 154:125-169.
8. Chiou, C-J., J. Zong, I. Waheed, and G. S. Hayward. 1993. Identification and mapping of dimerization and DNA-binding domains in the C terminus of the IE2 regulatory protein of human cytomegalovirus. J. Virol. 67:6201-6214.
9. Colberg-Poley, A. M. Functional roles of immediate early proteins encoded by the human cytomegalovirus UL36-38, UL115-119, TRS1/IRS1 and US3 loci. Intervirology, in press.
10. Colberg-Poley, A. M., and L. D. Santomenna. 1988. Selective induction of chromosomal gene expression by human cytomegalovirus. Virology 166:217-228.
11. Colberg-Poley, A. M., L. D. Santomenna, P. P. Harlow, P. A. Benfield, and D. J. Tenney. 1992. Human cytomegalovirus US3 and UL36-38 immediate-early proteins regulate gene expression. J. Virol. 66:95-105.
12. 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.
13. Doms, R. W., and A. Helenius. 1986. Quaternary structure of influenza virus hemagglutinin after acid treatment. J. Virol. 60:833-839.
14. Earl, P. L., R. W. Doms, and B. Moss. 1990. Oligomeric structure of the human immunodeficiency virus type 1 envelope glycoprotein. Proc. Natl. Acad. Sci. USA 87:648-652.
15. Freeze, H. H. 1995. Preparative analysis of glycoconjugates, p. 17.13.1-17.13.16. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 3. John Wiley & Sons, Inc., New York.
16. Furnari, B. A., E. Poma, T. F. Kowalik, S.-M. Huong, and E.-S. Huang. 1993. Human cytomegalovirus immediate-early gene 2 protein interacts with itself and with several novel cellular proteins. J. Virol. 67:4981-4991.
17. Gibson, W. 1981. Immediate-early proteins of human cytomegalovirus strains AD169, Davis, and Towne differ in electrophoretic mobility. Virology 112:350-354.
18. Compels, U. A., J. Nicholas, G. Lawrence, M. Jones, B. J. Thomson, M. E. D. Martin, S. Efstathiou, M. Craxton, and H. A. Macaulay. 1995. The DNA sequence of human herpesvirus-6: structure, coding content and genome evolution. Virology 209:29-51.
19. Gretch, D. R., B. Kari, L. Rasmussen, R. Gehrz, and M. Stinski. 1988. Identification and characterization of three distinct families of glycoprotein complexes present in the envelopes of human cytomegalovirus. J. Virol. 62:875-881.
20. 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.
21. Hermiston, T. W., C. L. Malone, P. R. Witte, and M. F. Stinski. 1987. Identification and characterization of the human cytomegalovirus immediate-early region 2 gene that stimulates gene expression from an inducible promoter. J. Virol. 61:3214-3221.
22. Hillson, D. A., N. Lambert, and R. B. Freedman. 1984. Formation and isomerization of disulfide bonds in protein-protein disulfide isomerase. Methods Enzymol. 107:281-294.
23. Iskenderian, A. C., L. Huang, A. Reilly, R. M. Stenberg, and D. G. Anders. 1996. Four of eleven loci required for transient complementation of human cytomegalovirus DNA replication cooperate to activate expression of replication genes. J. Virol. 70:383-392.
24. Jackson, M. R., T. Nilsson, and P. A. Peterson. 1993. Retrieval of transmembrane proteins to the endoplasmic reticulum. J. Cell Biol. 121:317-333.
25. Kari, B., and G. Gehrz. 1988. Isolation and characterization of a human cytomegalovirus glycoprotein containing a high content of O-linked oligosaccharides. Arch. Virol. 98:171-188.
26. Kouzarides, T., A. T. Bankier, S. C. Satchwell, E. Preddy, and B. G. Barrell. 1988. An immediate early gene of human cytomegalovirus encodes a potential membrane glycoprotein. Virology 165:151-164.
27. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
28. LaFemina, R. L., M. C. Pizzorno, J. D. Mosca, and G. S. Hayward. 1989. Expression of the acidic nuclear immediate early protein (IE1) of human cytomegalovirus in stable cell lines and its preferential association with metaphase chromosomes. Virology 172:584-600.
29. Lang, D., and T. Stamminger. 1993. The 86-kilodalton IE-2 protein of human cytomegalovirus is a sequence-specific DNA-binding protein that interacts directly with the negative autoregulatory response element located near the cap site of the IE-1/2 enhancer-promoter. J. Virol. 67:323-331.
30. Leatham, M. P., P. R. Witte, and M. F. Stinski. 1991. Alternate promoter selection within a human cytomegalovirus immediate-early and early transcription unit (UL119-115) defines true late transcripts containing open reading frames for putative glycoproteins. J. Virol. 65:6144-6153.
31. Lemmon, M. A., J. M. Flanagan, H. R. Treutlein, J. Zhang, and D. A. Engelman. 1992. Sequence specificity in the dimerization of transmembrane α-helices. Biochemistry 31:12719-12725.
32. Macias, M. P., and M. F. Stinski. 1993. An in vitro system for human cytomegalovirus immediate early 2 protein (IE2)-mediated site-dependent repression of transcription and direct binding of IE2 to the major immediate early promoter. Proc. Natl. Acad. Sci. USA 90:707-711.
33. Martin, M. E. D., J. Nicholas, B. J. Thomson, C. Newman, and R. W. Honess. 1991. Identification of a transactivating function mapping to the putative immediate-early locus of human herpesvirus 6. J. Virol. 65:5381-5390.
34. Martin, R. G. 1961. A method for determining the sedimentation behavior of enzymes: application to protein mixtures. J. Biol. Chem. 236:1372-1381.
35. Mocarski, E. S., Jr. 1996. Cytomegaloviruses and their replication, p. 2447-2492. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia.
36. Nicholas, J., and M. E. D. Martin. 1994. Nucleotide sequence analysis of a 38.5-kilobase-pair region of the genome of human herpesvirus 6 encoding human cytomegalovirus immediate-early gene homologs and transactivating functions. J. Virol. 68:597-610.
37. Otto, S. M., G. Sullivan-Tailyour, C. L. Malone, and M. F. Stinski. 1988. Subcellular localization of the major immediate early protein (IE1) of human cytomegalovirus at early times after infection. Virology 162:478-482.
38. Pari, G. S., A. K. Field, and J. A. Smith. 1995. Potent antiviral activity of an antisense oligonucleotide complementary to the intron-exon boundary of human cytomegalovirus genes UL36 and UL37. Antimicrob. Agents Chemother. 39:1157-1161.
39. Pari, G. S., M. A. Kacica, and D. G. Anders. 1993. Open reading frames UL44, IRS1/TRS1, and UL36-38 are required for transient complementation of human cytomegalovirus oriLyt-dependent DNA synthesis. J. Virol. 67:2575-2582.
40. Pereira, L., M. Hoffman, D. Gallo, and N. Cremer. 1982. Monoclonal antibodies to human cytomegalovirus: three surface membrane proteins with unique immunological and electrophoretic properties specify cross-reactive determinants. Infect. Immun. 36:924-932.
41. Radsak, K., K. H. Brücher, W. Britt, H. Shiou, D. Schneider, and A. Kollert. 1990. Nuclear compartmentation of glycoprotein B of human cytomegalovirus. Virology 177:515-522.
42. Rasmussen, L., J. Mullenax R. Nelson, and T. C. Merigan. 1985. Viral polypeptides detected by a complement-dependent neutralizing murine monoclonal antibody to human cytomegalovirus. J. Virol. 55:274-280.
43. Rey, M. A., B. Krust, A. G. Laurent, L. Montagnier, and A. G. Hovanessian. 1989. Characterization of human immunodeficiency virus type 2 envelope glycoproteins: dimerization of the glycoprotein precursor during processing. J. Virol. 63:647-658.
44. Smith, J. A., and G. S. Pari. 1995. Expression of human cytomegalovirus UL36 and UL37 genes is required for viral DNA replication. J. Virol. 69:1925-1931.
45. Tanford, C., and J. A. Reynolds. 1976. Characterization of membrane proteins in detergent solutions. Biochim. Biophys. Acta 457:133-170.
46. Tenney, D. J., and A. M. Colberg-Poley. 1990. RNA analysis and isolation of cDNAs derived from the human cytomegalovirus immediate-early region at 0.24 map units. Intervirology 31:203-214.
47. Tenney, D. J., and A. M. Colberg-Poley. 1991. Expression of the human cytomegalovirus UL36-38 immediate early region during permissive infection. Virology 182:199-210.
48. Tenney, D. J., and A. M. Colberg-Poley. 1991. Human cytomegalovirus UL36-38 and US3 immediate-early genes: temporally regulated expression of nuclear, cytoplasmic, and polysome-associated transcripts during infection. J. Virol. 65:6724-6734.
49. Tenney, D. J., L. D. Santomenna, K. B. Goudie, and A. M. Colberg-Poley. 1993. The human cytomegalovirus US3 immediate-early protein lacking the putative lransmcmbrane domain regulates gene expression. Nucleic Acids Res. 21:2931-2937.
50. Tkacz, J. S., and J. O. Lampen. 1975. Tunicamycin inhibition of polyisoprenyl N-acetylglucosaminyl pyrophosphate formation in calf liver microsomes. Biochem. Biophys. Res. Commun. 65:248-255.
51. Wada, I. D. Rindress, P. H. Cameron, W.-J. Ou, J. J. Dohery, D. Louvard, A. Bell, D. Dingard, D. Y. Thomas, and J. J. M. Bergeron. 1991. SSRα and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J. Biol. Chem. 266:19599-19610.
52. Walter, P., and G. Blobel. 1983. Preparation of microsomal membranes for cotranslational protein translocation. Methods Enzymol. 96:84-93.
53. Weston, K. 1988. An enhancer element in the short unique region of human cytomegalovirus regulates the production of a group of abundant immediate early transcripts. Virology 162:406-416.
54. Zhang, H., H. O. Al-Barazi, and A. M. Colberg-Poley. The acidic domain of the human cytomegalovirus UL37 immediate early glycoprotein is dispensable for its transactivating activity and localization but is not for its synergism. Virology, in press.
55. Zhang, H., and A. M. Colberg-Poley. Unpublished observations.