The human cytomegalovirus UL55 (gB) and UL75 (gH) glycoprotein ligands initiate the rapid activation of Sp1 and NF-κb during infection

Journal of Virology

Volumn 71, Issue 7, 1997, Pages 5051-5059

  Yurochko, Andrew D ^a   Hwang, Eung Soo ^a   Rasmussen, Lucy ^b   Keay, Susan ^c   Pereira, Lenore ^d   Huang, Eng Shang ^a,e  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR; VIRUS GLYCOPROTEIN; VIRUS RECEPTOR;

ARTICLE; CELL ACTIVATION; CYTOMEGALOVIRUS; MODEL; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; VIRUS ENVELOPE; VIRUS TRANSCRIPTION;

EID: 0030994219     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.7.5051-5059.1997     Document Type: Article

References (79)

1. Albrecht, T., I. Boldogh, M. P. Fons, and T. Valyi-Nagy. 1993. Activation of proto-oncogenes and cell activation signals in the initiation and progression of human cytomegalovirus infection, p. 384-411. In Y. Becker, G. Darai, and E. S. Huang (ed.), Molecular aspects of human cytomegalovirus diseases. Springer-Verlag KG, Berlin, Germany.
2. Albrecht, T., M. P. Fons, I. Boldogh, S. AbuBaker, C. Z. Deng, and D. Millinoff. 1991. Metabolic and cellular effects of human cytomegalovirus infection. Transplant. Proc. 23:48-55.
3. Baeuerle, P., and D. Baltimore. 1989. A 65-kD subunit of active NF-κB is required tor inhibition by IκB. Genes Dev. 3:1689-1698.
4. Baeuerle, P. A., and D. Baltimore. 1988. IκB: a specific inhibitor of the NF-κB transcription factor. Science 242:540-546.
5. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141-179.
6. Bergelson, J. M., and R. W. Finberg. 1993. Integrins as receptors for virus attachment and cell entry. Trends Microbiol. 1:287-288.
7. Berridge, M. J. 1987. Inositol triphosphate and diacylglycerol: two interacting second messengers. Annu. Rev. Biochem. 56:159-193.
8. Boldogh, I., S. Abubakar, and T. Albrecht. 1990. Activation of proto-oncogenes: an immediate early event in human cytomegalovirus. Science 247: 561-564.
9. Boldogh, I., M. P. Fons, and T. Albrecht. 1993. Increased levels of sequence-specific DNA-binding proteins in human cytomegalovirus-infected cells. Biochem. Biophys. Res. Commun. 197:1505-1510.
10. Britt, W. J., and D. Auger. 1986. Synthesis and processing of the envelope gp55-116 complex of human cytomegalovirus. J. Virol. 58:185-191.
11. 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.
12. Chen, L. I., T. Nishinaka, K. Kwan, I. Kitabayashi, K. Yokoyama, Y.-H. F. Fu, S. Grunwald, and R. Chiu. 1994. The retinoblastoma gene product RB stimulates Sp1-mediated transcription by liberating Sp1 from a negative regulator. Mol. Cell. Biol. 14:4380-4389.
13. Cherrington, J. M., and E. S. Mocarski. 1989. Human cytomegalovirus ie1 transactivates the α promoter-enhancer via an 18-base-pair repeat element. J. Virol. 63:1435-1440.
14. Cogswell, P. C., R. I. Scheinman, and A. S. Baldwin, Jr. 1993. Promoter of the human NF-κB p50/p105 gene. Regulation by NF-κB subunits and by c-REL. J. Immunol. 150:2794-2804.
15. Compton, T. 1995. Towards a definition of the HCMV entry pathway. Scand. J. Infect. Dis. 99(Suppl.):30-32.
16. Compton, T., R. R. Nepomuceno, and D. M. Nowlin. 1992. Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 191:387-395.
17. Compton, T., D. M. Nowlin, and N. R. Cooper. 1993. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834-841.
18. 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.
19. Cranage, M. P., G. L. Smith, S. E. Bell, H. Hart, C. Brown, A. T. Bankier, P. Tomlinson, B. G. Barrell, and T. G. Minson. 1988. Identification and expression of a human cytomegalovirus glycoprotein with homology to the Epstein-Barr virus BXLF2 product, varicella-zoster virus gpIII, and herpes simplex virus type 1 glycoprotein H. J. Virol. 62:1416-1422.
20. Dalgliesh, A. G., P. C. L. Beverley, P. R. Clapham, D. H. Crawford, M. F. Greaves, and R. A. Weiss. 1984. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312:763-766.
21. Dangoria, N. S., W. C. Breau, H. A. Anderson, D. M. Cishek, and L. C. Norkin. 1996. Extracellular simian virus 40 induces an ERK/MAP kinase-independent signalling pathway that activates primary response genes and promotes virus entry. J. Gen. Virol. 77:2173-2182.
22. Demarchi, F., F. d'Adda di Fagagna, A. Falaschi, and M. Giacca. 1996. Activation of transcription factor NF-κB by the Tat protein of human immunodeficiency virus type 1. J. Virol. 70:4427-4437.
23. Dynan, W. S., and D. Tjian. 1983. The promoter-specific transcription factor SpI binds to upstream sequences in the SV40 early promoter. Cell 35:79-87.
24. Dynan, W. S., and R. Tjian. 1983. Isolation of transcription factors that discriminate between different promoters recognized by RNA polymerase II. Cell 32:669-680.
25. Finco, T. S., and A. S. Baldwin, Jr. 1995. Mechanistic aspects of NF-κB regulation: the emerging role of phosphorylation and proteolysis. Immunity 3:263-272.
26. Franzoso, G., L. Carlson, K. Brown, M. B. Daucher, P. Bressler, and U. Siebenlist. 1996. Activation of the serum response factor by p65/NF-κB. EMBO J. 15:3403-3412.
27. Fujii, M., T. Minamino, M. Nomura, K. I. Miyamoto, J. Tanaka, and M. Seiki. 1996. Selective activation of the proto-oncogene c-jun promoter by the transforming protein v-Rel. Oncogene 12:2193-2202.
28. Ghazal, P., and J. A. Nelson. 1993. Transcription factors and viral regulatory proteins as potential mediators of human cytomegalovirus pathogenesis, p. 360-383. In Y. Becker, G. Darai, and E. S. Huang (ed.), Molecular aspects of human cytomegalovirus diseases. Springer-Verlag KG, Berlin, Germany.
29. Gibson, W. 1993. Molecular biology of human cytomegalovirus, p. 303-329. In Y. Becker, G. Darai, and E. S. Huang (ed.), Molecular aspects of human cytomegalovirus diseases. Springer-Verlag KG, Berlin, Germany.
30. Haskill, S., A. A. Beg, S. M. Tompkins, J. S. Morris, A. D. Yurochko, A. Sampson-Johannes, K. Mondal, P. Ralph, and A. S. Baldwin, Jr. 1991. Characterization of an immediate-early gene induced in adherent monocytes that encodes IκB-like activity. Cell 65:1281-1289.
31. Huang, E.-S. 1975. Human cytomegalovirus. III. Virus-induced DNA polymerase. J. Virol. 16:298-310.
32. Huang, E.-S., S.-T. Chen, and J. S. Pagano. 1973. Human cytomegalovirus. I. Purification and characterization of viral DNA. J. Virol. 12:1473-1481.
33. Huang, E.-S., and T. F. Kowalik. 1993. The pathogenicity of human cytomegalovirus: an overview, p. 1-45. In Y. Becker, G. Darai, and E. S. Huang (ed.), Molecular aspects of human cytomegalovirus diseases. Springer-Verlag KG, Berlin, Germany.
34. Hwang, E. S., J. Y. Seoh, C. G. Park, Y. H. Kook, and C. Y. Cha. 1992. Characterization of monoclonal antibodies against human cytomegalovirus (HCMV) glycoproteins. J. Korean Soc. Microbiol. 27:545-553.
35. Jahn, G., and M. Mach. 1990. Human cytomegalovirus phosphoproteins and glycoproteins and their coding regions. Curr. Top. Microbiol. Immunol. 154:171-185.
36. Kadonaga, J. T., K. R. Carner, F. R. Masiarz, and R. Tjian. 1987. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell 51:1079-1090.
37. Kaye, J. F., U. A. Compel, and A. C. Minson. 1992. Glycoprotein H of human cytomegalovirus (HCMV) forms a stable complex with HCMV UL115 gene product. J. Gen. Virol. 73:2693-2698.
38. Keay, S., and B. Baldwin. 1991. Anti-idiotypic antibodies that mimic gp86 of human cytomegalovirus inhibit viral fusion but not attachment. J. Virol. 65:5124-5128.
39. Keay, S., and B. Baldwin. 1992. The human fibroblast receptor for gp86 of human cytomegalovirus is a phosphorylated glycoprotein. J. Virol. 66:4834-4838.
40. i mediated by the 92.5-kDa putative cell membrane receptor for HCMV gp86. Am. J. Physiol. 269:C11-C21.
41. Keay, S., and B. R. Baldwin. 1996. Evidence for the role of cell phosphorylation in human cytomegalovirus/host cell fusion. J. Gen. Virol. 77:2597-2604.
42. Keay, S., T. C. Merigan, and L. Rasmussen. 1989. Identification of cell surface receptors for the 86-kilodalton glycoprotein of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 86:10100-10103.
43. Keay, S., L. Rasmussen, and L. Merigan. 1988. Syngeneic monoclonal antiidiotypic antibodies that bear the internal image of a human cytomegalovirus neutralization epitope. J. Immunol. 140:944-948.
44. Kerry, J. A., M. A. Priddy, T. L. Staley, T. R. Jones, and R. M. Stenberg. 1997. The role of ATF in regulating human cytomegalovirus DNA polymerase (UL54) promoter during viral infection. J. Virol. 71:2120-2126.
45. Kessler, D. J., M. P. Duyao, D. B. Spicer, and G. E. Sonenshein. 1992. NF-κB-like factors mediate interleukin 1 induction of c-myc gene transcription in fibroblasts. J. Exp. Med. 176:787-792.
46. Kim, S.-J., U. S. Onwuta, Y. I. Lee, R. Li, M. R. Botchan, and P. D. Robbins. 1992. The retinoblastoma gene product regulates Sp1-mediated transcription. Mol. Cell. Biol. 12:2455-2463.
47. Kingsley, C., and A. Winoto. 1992. Cloning of GT box-binding proteins: a novel Sp1 multigene family regulating T-cell receptor gene expression. Mol. Cell. Biol. 12:4251-4261.
48. Klatzmann, D., E. Champagne, S. Chamaret, J. Gruest, D. Guetard, T. Hercend, J.-C. Gluckman, and L. Montagnier. 1984. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312:767-768.
49. Kowalik, T. F., B. Wing, J. S. Haskill, J. C. Azizkhan, A. S. Baldwin, Jr., and E.-S. Huang. 1993. Multiple mechanisms are implicated in the regulation of NF-κB activity during human cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 90:1107-1111.
50. 1 activation of NF-κB: involvement of the protein kinase C pathway. J. Virol. 70:2525-2532.
51. Majello, B., P. De Luca, G. Hagen, G. Suske, and L. Lania. 1994. Different members of the Sp1 multigene family exert opposite transcriptional regulation of the long terminal repeal of HIV-1. Nucleic Acids Res. 22:4914-4921.
52. Majello, B., P. De Luca, G. Suske, and L. Lania. 1995. Differential transcriptional regulation of c-myc promoter through the same DNA binding sites targeted by Sp1-like proteins. Oncogene 10:1841-1848.
53. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/ NGF receptor family. Cell 87:427-436.
54. Navarro, D., P. Paz, S. Tugizov, K. Topp, J. La Vail, and L. Pereira. 1993. Glycoprotein B of human cytomegalovirus promotes virion penetration into cells, transmission of infection from cell to cell, and fusion of infected cells. Virology 197:143-158.
55. Nowlin, D. M., N. R. Cooper, and T. Compton. 1991. Expression of a human cytomegalovirus receptor correlates with infectibility of cells. J. Virol. 65: 3114-3121.
56. Otto, M., A. Gunther, H. Fan, O. Rick, and R. T. Huang. 1994. Identification of annexin 33 kDa in cultured cells as a binding protein of influenza virus. FEBS Lett. 356:125-129.
57. Pachl, C., W. S. Probert, K. M. Hermsen, F. R. Masiarz, L. Rasmussen, T. C. Merigan, and R. R. Spaete. 1989. The human cytomegalovirus strain Towne glycoprotein H encodes glycoprotein p86. Virology 169:418-426.
58. Pereira, L. 1994. Function of glycoprotein B homologues of the family Herpesviridae. Infect. Agents Dis. 3:9-28.
59. Qadri, I., D. Navarro, P. Paz, and L. Pereira. 1992. Assembly of conformation-dependent neutralizing domains on glycoprotein B of human cytomegalovirus. J. Gen. Virol. 73:2913-2921.
60. 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.
61. Rasmussen, L. E., R. M. Nelson, D. C. Kelsall, and T. C. Merigan. 1984. Murine monoclonal antibody to a single protein neutralizes the infectivity of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 81:876-880.
62. Sambucetti, L. C., J. M. Cherrington, G. W. Wilkinson, and E. S. Mocarski. 1989. NF-κB activation of the cytomegalovirus enhancer is mediated by a viral transactivator and by T cell stimulation. EMBO J. 8:4251-4258.
63. Scheinman, R. I., A. A. Beg, and A. S. Baldwin, Jr. 1993. NF-κB p100 (Lyt-10) is a component of H2TF1 and can function as an IκB-like molecule. Mol. Cell. Biol. 13:6089-6101.
64. Siebenlist, U., G. Franzoso, and K. Brown. 1994. Structure, regulation and function of NF-κB. Annu. Rev. Cell Biol. 10:405-455.
65. Sinclair, A. J., and P. J. Farrell. 1995. Host cell requirements for efficient infection of quiescent primary B lymphocytes by Epstein-Barr virus. J. Virol. 69:5461-5468.
66. Stenberg, R. M. 1993. Immediate-early genes of human cytomegalovirus: organization and function, p. 330-359. In Y. Becker, G. Darai, and E. S. Huang (ed.), Molecular aspects of human cytomegalovirus diseases. Springer-Verlag KG, Berlin, Germany.
67. Su, F., and R. J. Schneider. 1996. Hepatitis B virus HBx protein activates transcription factor NF-κB by acting on multiple cytoplasmic inhibitors of rel-related proteins. J. Virol. 70:4558-4566.
68. Tanner, J. E., C. Alfieri, T. A. Chatila, and F. Diaz-Mitoma. 1996. Induction of interleukin-6 after stimulation of human B-cell CD21 by Epstein-Barr virus glycoproteins gp350 and gp220. J. Virol. 70:570-575.
69. Thanos, D., and T. Maniatis. 1995. NF-κB: a lesson in family values. Cell 80:529-532.
70. Udvadia, A. J., K. T. Rogers, P. D. R. Higgins, Y. Murata, K. H. Martin, P. A. Humphrey, and J. M. Horowitz. 1993. Sp-1 binds promoter elements regulated by the RB protein and Sp-1-mediated transcription is stimulated by RB coexpression. Proc. Natl. Acad. Sci. USA 90:3265-3269.
71. Udvania, A. J., D. J. Templeton, and J. M. Horowitz. 1995. Functional interactions between the retinoblasloma (Rb) protein and Sp-family members: superactivation by Rb requires amino acids necessary for growth suppression. Proc. Natl. Acad. Sci. USA 92:3953-3957.
72. Wickham, T. J., P. Mathias, D. A. Cheresh, and G. R. Nemerow. 1993. Integrins αVβ3 and αVβ5 promote adenovirus internalization but not virus attachment. Cell 73:309-319.
73. Wing, B. A., and E.-S. Huang. Unpublished data.
74. Wing, B. A., G. C. Y. Lee, and E.-S. Huang. 1996. The human cytomegalovirus UL94 open reading frame encodes a conserved herpesvirus capsid/ tegument-associated virion protein that is expressed with true late kinetics. J. Virol. 70:3339-3345.
75. Wright, J. F., A. Kurosky, and S. Wasi. 1994. An endothelial cell-surface form of annexin II binds human cytomegalovirus. Biochem. Biophys. Res. Commun. 198:983-989.
76. Yurochko, A. D. 1997. Adhesion molecules as signal transduction molecules, p. 155-180. In L. C. Paul and T. Issekutz (ed.), Targeting cell adhesion molecules for therapeutic application. Marcel Dekker, Inc., New York, N.Y.
77. Yurochko, A. D., and E.-S. Huang. Unpublished results.
78. Yurochko, A. D., T. F. Kowalik, S.-M. Huong, and E.-S. Huang. 1995. Human cytomegalovirus upregulates NF-κB activity by transactivating the NF-κB p105/p50 and p65 promoters. J. Virol. 69:5391-5400.
79. Yurochko, A. D., M. W. Mayo, E. E. Poma, A. S. Baldwin, Jr., and E.-S. Huang. 1997. Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-κB promoters. J. Virol. 71:4638-4648.