Extracellular signal-regulated kinase activity is sustained early during human cytomegalovirus infection

Journal of Virology

Volumn 72, Issue 11, 1998, Pages 9173-9180

  Rodems, Steven M ^a,b   Spector, Deborah H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Aurora Biosciences Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATASE; PROTEIN KINASE INHIBITOR; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMEDIATE EARLY GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VIRUS GENE; VIRUS REPLICATION;

EID: 0031707104     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.11.9173-9180.1998     Document Type: Article

References (74)

1. Alessi, D. R., A. Cuenda, P. Cohen, D. T. Dudley, and A. R. Saltiel. 1995. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270:27489-27494.
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. Benn, J., F. Su, M. Doria, and R. J. Schneider. 1996. Hepatitis B virus HBx protein induces transcription factor AP-1 by activation of extracellular signal-regulated and c-Jun N-terminal mitogen-activated protein kinases. J. Virol. 70:4978-4985.
4. Blenis, J. 1993. Signal transduction via the MAP kinases: proceed at your own RSK. Proc. Natl. Acad. Sci. USA 90:5889-5892.
5. Boldogh, I., S. AbuBakar, and T. Albrecht. 1990. Activation of proto-oncogenes: an immediate early event in human cytomegalovirus infection. Science 247:561-564.
6. Boldogh, I., S. AbuBakar, C. Z. Deng, and T. Albrecht. 1991. Transcriptional activation of cellular oncogenes fos, jun, and myc by human cytomegalovirus. J. Virol. 65:1568-1571.
7. Briant, L., V. Robert-Hebmann, V. Sivan, A. Brunet, J. Pouyssegur, and C. Devaux. 1998. Involvement of extracellular signal-regulated kinase module in HIV-mediated CD4 signals controlling activation of nuclear factor-kappa B and AP-1 transcription factors. J. Immunol. 160:1875-1885.
8. Britt, W., and C. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields et al. (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
9. Bruder, J. T., and I. Kovesdi. 1997. Adenovirus infection stimulates the Raf/MAPK signaling pathway and induces interleukin-8 expression. J. Virol. 71:398-404.
10. Cahill, M. A., A. Nordheim, and R. Janknecht. 1994. Co-occurrence of CArG boxes and TCF sites within viral genomes. Biochem. Biophys. Res. Commun. 205:545-551.
11. Camps, M., A. Nichols, C. Gillieron, B. Antonsson, M. Muda, C. Chabert, U. Boschert, and S. Arkinstall. 1998. Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science 280:1262-1265.
12. Chan, Y. J., C. J. Chiou, Q. Huang, and G. S. Hayward. 1996. Synergistic interactions between overlapping binding sites for the serum response factor and ELK-1 proteins mediate both basal enhancement and phorbol ester responsiveness of primate cytomegalovirus major immediate-early promoters in monocyte and T-lymphocyte cell types. J. Virol. 70:8590-8605.
13. Cobb, M. H., J. E. Hepler, M. Cheng, and D. Robbins. 1994. The mitogen-activated protein kinases, ERK1 and ERK2. Semin. Cancer Biol. 5:261-268.
14. DeMarchi, J. M. 1981. Human cytomegalovirus DNA: restriction enzyme cleavage maps and map locations for immediate-early, early, and late RNAs. Virology 114:23-28.
15. Dudley, D. T., L. Pang, S. J. Decker, A. J. Bridges, and A. R. Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92:7686-7689.
16. Frost, J. A., T. D. Geppert, M. H. Cobb, and J. R. Feramisco. 1994. A requirement for extracellular signal-regulated kinase (ERK) function in the activation of AP-1 by Ha-Ras, phorbol 12-myristate 13-acetate, and serum. Proc. Natl. Acad. Sci. USA 91:3844-3848.
17. Groom, L. A., A. A. Sneddon, D. R. Alessi, S. Dowd, and S. M. Keyse. 1996. Differential regulation of the MAP, SAP and RK/p38 kinases by Pyst1, a novel cytosolic dual-specificity phosphatase. EMBO J. 15:3621-3632.
18. Hagemeier, C., S. M. Walker, P. J. G. Sissons, and J. H. Sinclair. 1992. The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently trans-activate the c-fos, c-myc and hsp70 promoters via basal promoter elements. J. Gen. Virol. 73:2385-2393.
19. Harel, N. Y., and J. C. Alwine. 1998. Phosphorylation of the human cytomegalovirus 86-kilodalton immediate-early protein IE2. J. Virol. 72:5481-5492.
20. Haystead, T. A., J. E. Weiel, D. W. Litchfield, Y. Tsukitani, E. H. Fischer, and E. G. Krebs. 1990. Okadaic acid mimics the action of insulin in stimulating protein kinase activity in isolated adipocytes. The role of protein phosphatase 2a in attenuation of the signal. J. Biol. Chem. 265:16571-16580.
21. Hill, C. S., and R. Treisman. 1995. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 80:199-211.
22. Hirai, K., F. Maeda, and Y. Watanabe. 1977. Expression of early virus functions in human cytomegalovirus infected HEL cells: effect of ultraviolet light-irradiation of the virus. J. Gen. Virol. 38:121-133.
23. Hunter, T. 1995. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225-236.
24. Janknecht, R., W. H. Ernst, and A. Nordheim. 1995. SAP1α is a nuclear target of signaling cascades involving ERKs. Oncogene 10:1209-1216.
25. Janknecht, R., W. H. Ernst, V. Pingoud, and A. Nordheim. 1993. Activation of ternary complex factor Elk-1 by MAP kinases. EMBO J. 12:5097-5104.
26. Johnson, G. L., and R. R. Vaillancourt. 1994. Sequential protein kinase reactions controlling cell growth and differentiation. Curr. Opin. Cell Biol. 6:230-238.
27. Karin, M. 1994. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6:415-424.
28. Koval, V., C. Clark, M. Vaishnav, S. A. Spector, and D. H. Spector. 1991. Human cytomegalovirus inhibits human immunodeficiency virus replication in cells productively infected by both viruses. J. Virol. 65:6969-6978.
29. 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.
30. Lang, D., S. Gebert, H. Arlt, and T. Stamminger. 1995. Functional interaction between the human cytomegalovirus 86-kilodalton IE2 protein and the cellular transcription factor CREB. J. Virol. 69:6030-6037.
31. Lannuzel, A., J. V. Barnier, C. Hery, V. T. Huynh, B. Guibert, F. Gray, J. D. Vincent, and M. Tardieu. 1997. Human immunodeficiency virus type 1 and its coat protein gp120 induce apoptosis and activate JNK and ERK mitogen-activated protein kinases in human neurons. Ann. Neurol. 42:847-856.
32. Lavoie, J. N., G. L'Allemain, A. Brunet, R. Muller, and J. Pouyssegur. 1996. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J. Biol. Chem. 271:20608-20616.
33. Lazar, D. F., R. J. Wiese, M. J. Brady, C. C. Mastick, S. B. Waters, K. Yamauchi, J. E. Pessin, P. Cuatrecasas, and A. R. Saltiel. 1995. Mitogen-activated protein kinase kinase inhibition does not block the stimulation of glucose utilization by insulin. J. Biol. Chem. 270:20801-20807.
34. Marais, R., J. Wynne, and R. Treisman. 1993. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73:381-393.
35. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
36. McDonough, S. H., and D. H. Spector. 1983. Transcription in human fibroblasts permissively infected by human cytomegalovirus strain AD169. Virology 125:31-46.
37. Meloche, S. 1995. Cell cycle reentry of mammalian fibroblasts is accompanied by the sustained activation of p44mapk and p42mapk isoforms in the G1 phase and their inactivation at the G1/S transition. J. Cell Physiol. 163:577-588.
38. Misra-Press, A., C. S. Rim, H. Yao, M. S. Roberson, and P. J. Stork. 1995. A novel mitogen-activated protein kinase phosphatase. Structure, expression, and regulation. J. Biol. Chem. 270:14587-14596.
39. Mocarski, E. S. 1996. Cytomegaloviruses and their replication, p. 2447-2492. In B. N. Fields, D. M. Knipe and P. M. Howley, et al. (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
40. Muda, M., U. Boschert, R. Dickinson, J. C. Martinou, I. Martinou, M. Camps, W. Schlegel, and S. Arkinstall. 1996. MKP-3, a novel cytosolic protein-tyrosine phosphatase that exemplifies a new class of mitogen-activated protein kinase phosphatase. J. Biol. Chem. 271:4319-4326.
41. Muda, M., U. Boschert, A. Smith, B. Antonsson, C. Gillieron, C. Chabert, M. Camps, I. Martinou, A. Ashworth, and S. Arkinstall. 1997. Molecular cloning and functional characterization of a novel mitogen-activated protein kinase phosphatase, MKP-4. J. Biol. Chem. 272:5141-5151.
42. Muda, M., A. Theodosiou, N. Rodrigues, U. Boschert, M. Camps, C. Gillieron, K. Davies, A. Ashworth, and S. Arkinstall. 1996. The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J. Biol. Chem. 271:27205-27208.
43. Mumby, M. 1995. Regulation by tumour antigens defines a role for PP2A in signal transduction. Semin. Cancer Biol. 6:229-237.
44. Pang, L., T. Sawada, S. J. Decker, and A. R. Saltiel. 1995. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270:13585-13588.
45. Patarca, R. 1996. Protein phosphorylation and dephosphorylation in physiologic and oncologic processes. Crit. Rev. Oncog. 7:343-432.
46. Pende, M., T. L. Fisher, P. B. Simpson, J. T. Russell, J. Blenis, and V. Gallo. 1997. Neurotransmitter- and growth factor-induced cAMP response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ribosomal S6 kinase pathway. J. Neurosci. 17:1291-1301.
47. Price, M. A., A. E. Rogers, and R. Treisman. 1995. Comparative analysis of the ternary complex factors Elk-1, SAP-1a and SAP-2 (ERP/NET). EMBO J. 14:2589-2601.
48. Ray, L. B., and T. W. Sturgill. 1988. Insulin-stimulated microtubule-associated protein kinase is phosphorylated on tyrosine and threonine in vivo. Proc. Natl. Acad. Sci. USA 85:3753-3757.
49. Robinson, M. J., and M. H. Cobb. 1997. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9:180-186.
50. Rodems, S. M., C. L. Clark, and D. H. Spector. 1998. Separate DNA elements containing ATF/CREB and IE86 binding sites differentially regulate the human cytomegalovirus UL112-113 promoter at early and late times in the infection. J. Virol. 72:2697-2707.
51. Rodems, S. M., and D. H. Spector. Unpublished data.
52. Ruderman, J. V. 1993. MAP kinase and the activation of quiescent cells. Curr. Opin. Cell Biol. 5:207-213.
53. Sambucetti, L. C., J. M. Cherrington, G. W. G. 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.
54. Schwartz, R., B. Helmich, and D. H. Spector. 1996. CREB and CREB-binding proteins play an important role in the IE2 86-kilodalton protein-mediated transactivation of the human cytomegalovirus 2.2-kilobase RNA promoter. J. Virol. 70:6955-6966.
55. Schwartz, R., M. H. Sommer, A. Scully, and D. H. Spector. 1994. Site-specific binding of the human cytomegalovirus IE2 86-kilodalton protein to an early gene promoter. J. Virol. 68:5613-5622.
56. Shelbourn, S. L., J. G. Sissons, and J. H. Sinclair. 1989. Expression of oncogenic ras in human teratocarcinoma cells induces partial differentiation and permissiveness for human cytomegalovirus infection. J. Gen. Virol. 70:367-374.
57. Sinclair, J. H., J. Baillie, L. A. Bryant, J. A. Taylor-Wiedeman, and J. G. Sissons. 1992. Repression of human cytomegalovirus major immediate early gene expression in a monocytic cell line. J. Gen. Virol. 73:433-435.
58. Staprans, S. I., D. K. Rabert, and D. H. Spector. 1988. Identification of sequence requirements and trans-acting functions necessary for regulated expression of a human cytomegalovirus early gene. J. Virol. 62:3463-3473.
59. Stinski, M. F. 1978. Sequence of protein synthesis in cells infected by human cytomegalovirus: early and late virus-induced polypeptides. J. Virol. 26:686-701.
60. Sun, H., C. H. Charles, L. F. Lau, and N. K. Tonks. 1993. MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75:487-493.
61. Tamashiro, J. C., L. J. Hock, and D. H. Spector. 1982. Construction of a cloned library of the EcoRI fragments from the human cytomegalovirus genome (strain AD169). J. Virol. 42:547-557.
62. Taylor-Wiedeman, J., J. G. Sissons, L. K. Borysiewicz, and J. H. Sinclair. 1991. Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J. Gen. Virol. 72:2059-2064.
63. Taylor-Wiedeman, J., P. Sissons, and J. Sinclair. 1994. Induction of endogenous human cytomegalovirus gene expression after differentiation of monocytes from healthy carriers. J. Virol. 68:1597-1604.
64. Treisman, R. 1994. Ternary complex factors: growth factor regulated transcriptional activators. Curr. Opin. Genet. Dev. 4:96-101.
65. Wade, E. J., K. M. Klucher, and D. H. Spector. 1992. An AP-1 binding site is the predominant cis-acting regulatory element in the 1.2-kilobase early RNA promoter of human cytomegalovirus. J. Virol. 66:2407-2417.
66. Ward, Y., S. Gupta, P. Jensen, M. Wartmann, R. J. Davis, and K. Kelly. 1994. Control of MAP kinase activation by the mitogen-induced threonine/ tyrosine phosphatase PAC1. Nature 367:651-654.
67. Wathen, M. W., and M. F. Stinski. 1982. Temporal patterns of human cytomegalovirus transcription: mapping the viral RNAs synthesized at immediate early, early, and late times after infection. J. Virol. 41:462-477.
68. Wathen, M. W., D. R. Thomsen, and M. F. Stinski. 1981. Temporal regulation of human cytomegalovirus transcription at immediate early and early times after infection. J. Virol. 38:446-459.
69. Weinshenker, B. G., S. Wilton, and G. P. Rice. 1988. Phorbol ester-induced differentiation permits productive human cytomegalovirus infection in a monocytic cell line. J. Immunol. 140:1625-1631.
70. Whalen, S. G., R. C. Marcellus, A. Whalen, N. G. Ahn, R. P. Ricciardi, and P. E. Branton. 1997. Phosphorylation within the transactivation domain of adenovirus E1A protein by mitogen-activated protein kinase regulates expression of early region 4. J. Virol. 71:3545-3553.
71. Wright, D. A., S. I. Staprans, and D. H. Spector. 1988. Four phosphoproteins with common amino termini are encoded by human cytomegalovirus AD169. J. Virol. 62:331-340.
72. Xing, J., D. D. Ginty, and M. E. Greenberg. 1996. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273:959-963.
73. Xing, J., J. M. Kornhauser, Z. Xia, E. A. Thiele, and M. E. Greenberg. 1998. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell. Biol. 18:1946-1955.
74. 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.