ERK1/2 and MEK1/2 induced by Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) early during infection of target cells are essential for expression of viral genes and for establishment of infection

Journal of Virology

Volumn 79, Issue 16, 2005, Pages 10308-10329

  Sharma Walia, Neelam ^a   Krishnan, Harinivas H ^a   Naranatt, Pramod P ^a   Zeng, Ling ^a   Smith, Marilyn S ^a   Chandran, Bala ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE 5; ENVELOPE GLYCOPROTEIN GB; ENVELOPE PROTEIN; FOCAL ADHESION KINASE; HEPARIN; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; MYC PROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN ANTIBODY; PROTEIN KINASE C ZETA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; STAT1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN; VIRUS DNA; VIRUS GLYCOPROTEIN;

ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INDUCTION; ENZYME INHIBITION; FIBROBLAST; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE TARGETING; HERPES; HOST CELL; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMEDIATE EARLY GENE; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TARGET CELL; TRANSCRIPTION REGULATION; VIRUS ADSORPTION; VIRUS CULTURE; VIRUS DNA CELL DNA INTERACTION; VIRUS GENE; VIRUS INACTIVATION; VIRUS VIRULENCE;

ACTIVE TRANSPORT, CELL NUCLEUS; DNA; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 8, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE 7; OPEN READING FRAMES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR AP-1; VIRAL PROTEINS;

HUMAN HERPESVIRUS 8; KAPOSI SARCOMA ASSOCIATED HERPESVIRUS; LANA;

EID: 23244461927     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.16.10308-10329.2005     Document Type: Article

References (74)

1. Abe, J., M. Kusuhara, R. J. Ulevitch, B. C. Berk, and J. D. Lee. 1996. Big mitogen-activated protein kinase 1 (BMK1) is a redox-sensitive kinase. J. Biol. Chem. 271:16586-16590.
2. Akula, S. M., F. Z. Wang, J. Vieira, and B. Chandran. 2001. Human herpesvirus 8 (HHV-8/KSHV) infection of target cells involves interaction with heparan sulfate. Virology 282:245-255.
3. Akula, S. M., N. P. Pramod, F. Z. Wang, and B. Chandran. 2001. Human herpesvirus envelope-associated glycoprotein B interacts with heparan sulfate-like moieties. Virology 284:235-249.
4. Akula, S. M., N. P. Pramod, F. Z. Wang, and B. Chandran. 2002. Integrin α3β1 (CD 49c/29) is a cellular receptor for Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 108:407-419.
5. Akula, S. M., N. P. Pramod, N. S. Walia, F. Z. Wang, B. Fegley, and B. Chandran. 2003. Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) infection of human fibroblast cells occurs through endocytosis. J. Virol. 77:7978-7990.
6. Andrade, A. A., P. N. Silva, A. C. Pereira, L. P. De Sousa, P. C. Ferreira, R. T. Gazzinelli, E. G. Kroon, C. Ropert, and C. A. Bonjardim. 2004. The vaccinia virus-stimulated mitogen-activated protein kinase (MAPK) pathway is required for virus multiplication. Biochem. J. 381:437-446.
7. Angel, P., M. Imagawa, R. Chiu, B. Stein, R. J. Imbra, H. J. Rahmsdorf, C. Jonat, P. Herrlich, and M. Karin. 1987. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 49:729-739.
8. Antman, K., and Y. Chang. 2000. Kaposi's sarcoma. N. Engl. J. Med. 342:1027-1038.
9. Bechtel, J. T., Y. Liang, J. Hvidding, and D. Ganem. 2003. Host range of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 77:6474-6481.
10. Birkmann, A., K. Mahr, A. Ensser, S. Yaguboglu, F. Titgemeyer, B. Fleckenstein, and F. Neipel. 2001. Cell surface heparan sulfate is a receptor for human herpesvirus 8 and interacts with envelope glycoprotein K8.1. J. Virol. 75:11583-11593.
11. Blasig, C., C. Zietz, B. Haar, F. Neipel, S. Esser, N. H. Brockmeyer, E. Tschachler, S. Colombini, B. Ensoli, and M. Sturzl. 1997. Monocytes in Kaposi's sarcoma lesions are productively infected by human herpesvirus 8. J. Virol. 71:7963-7968.
12. Blenis, J. 1993. Signal transduction via the MAP kinases: proceed at your own RSK. Proc. Natl. Acad. Sci. USA 90:5889-5892.
13. Chandran, B., C. Bloomer, S. R. Chan, L. Zhu, E. Goldstein, and R. Horvat. 1998. Human herpesvirus-8 ORF K8.1 gene encodes immunogenic glycoproteins generated by spliced transcripts. Virology 249:140-149.
14. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
15. Chung, T. W., Y. C. Lee, and C. H. Kim. 2004. Hepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3K/AKT pathways: involvement of invasive potential. FASEB J. 18:1123-1125.
16. Diamond, C., S. J. Brodie, J. N. Krieger, M. L. Huang, D. M. Koelle, K. Diem, D. Muthui, and L. Corey. 1998. Human herpesvirus 8 in the prostate glands of men with Kaposi's sarcoma. J. Virol. 72:6223-6227.
17. Dourmishev, L. A., A. L. Dourmishev, D. Palmeri, R. A. Schwartz, and D. M. Lukac. 2003. Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) epidemiology and pathogenesis. Microbiol. Mol. Biol. Rev. 67:175-212.
18. English, J. M., G. Pearson, R. Baer, and M. H. Cobb. 1998. Identification of substrates and regulators of the mitogen-activated protein kinase ERK5 using chimeric protein kinases. J. Biol. Chem. 273:3854-3860.
19. Favata, M. F., K. Y. Horiuchi, E. J. Manos, A. J. Daulerio, D. A. Stradley, W. S. Feeser, D. E. Van Dyk, W. J. Pitts, R. A. Earl, F. Hobbs, R. A. Copeland, R. L. Magolda, P. A. Scherle, and J. M. Trzaskos. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273:18623-18632.
20. Fincham, V. J., M. James, M. C. Frame, and S. J. Winder. 2000. Active ERK/MAP kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-Src. EMBO J. 19:2911-2923.
21. Ganem, D. 1997. KSHV and Kaposi's sarcoma: the end of the beginning? Cell 91:157-160.
22. Ganem, D. 1998. Human herpesvirus 8 and its role in the genesis of Kaposi's sarcoma. Curr. Clin. Top. Infect. Dis. 18:237-251.
23. Inoue, N., J. Winter, R. B. Lal, M. K. Offermann, and S. Koyano. 2003. Characterization of entry mechanisms of human herpesvirus 8 by using an Rta-dependent reporter cell line. J. Virol. 77:8147-8152.
24. Jacque, J. M., A. Mann, H. Enslen, N. Sharova, B. Brichacek, R. J. Davis, and M. Stevenson. 1998. Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase. EMBO J. 17:2607-2618.
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. Janknecht, R., W. H., Ernst, and A. Nordheim. 1995. SAP1α is a nuclear target of signaling cascades involving ERKs. Oncogene 10:1209-1216.
27. Johnson, R. A., X. L. Ma, A. D. Yurochko, and E. S. Huang. 2001. The role of MKK1/2 kinase activity in human cytomegalovirus infection. J. Gen. Virol. 82:493-497.
28. Kamakura, S., T. Moriguchi, and E. Nishida. 1999. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases. Identification and characterization of a signaling pathway to the nucleus. J. Biol. Chem. 274:26563-26571.
29. Kato, Y., R. I. Tapping, S. Huang, M. H. Watson, R. J. Ulevitch, and J. D. Lee. 1998. BMK1/ERK5 is required for cell proliferation induced by epidermal growth factor. Nature 395:713-716.
30. Kato, Y., V. V. Kravchenko, R. I. Tapping, J. Han, R. J. Ulevitch, and J. D. Lee. 1997. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 16:7054-7066.
31. Kong, X., San Juan, H., A. Behera, M. E. Peeples, J. Wu, R. F. Lockey, and S. S. Mohapatra. 2004. ERK-1/2 activity is required for efficient RSV infection. FEBS Lett. 559:33-38.
32. Krishnan, H. H., P. P. Naranatt, M. S. Smith, L. Zeng, C. Bloomer, and B. Chandran. 2004. Concurrent expression of latent and a limited number of lytic genes with immune modulation and antiapoptotic function by Kaposi's sarcoma-associated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J. Virol. 78:3601-3620.
33. Le Doux, J. M., N. Landazuri, M. L. Yarmunsh, and J. R. Morgan. 2001. Complexation of retrovirus with cationic and anionic polymers increases the efficiency of gene transfer. Hum. Gene Ther. 12:1611-1621.
34. Lenormand, P., J. M. Brondello, A. Brunet, and J. Pouysségur. 1998. Growth factor-induced p42/p44 MAPK nuclear translocation and retention requires both MAPK activation and neosynthesis of nuclear anchoring proteins. Cell Biol. 142:625-633.
35. Lukac, D. M., L. Garibyan, J. R. Kirshner, D. Palmeri, and D. Ganem. 2001. DNA binding by Kaposi's sarcoma-associated herpesvirus lytic switch protein is necessary for transcriptional activation of two viral delayed early promoters. J. Virol. 75:6786-6799.
36. Luna, R. E., F. Zhou, A. Baghian, V. Chouljenko, B. Forghani, S. J. Gao, and K. G. Kousoulas. 2004. Kaposi's sarcoma-associated herpesvirus glycoprotein K8.1 is dispensable for virus entry. J. Virol. 78:6389-6398.
37. 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.
38. McCarthy, S. A., D. Chen, B. S. Yang, J. J. Garcia Ramirez, H. Cherninski, X. R. Chen, M. Klagsbrun, C. A. Hauser, M. C. Ostrowski, and M. McMahon. 1997. Rapid phosphorylation of Ets-2 accompanies mitogen-activated protein kinase activation and the induction of heparin-binding epidermal growth factor gene expression by oncogenic Raf-1. Mol. Cell. Biol. 17:2401-2412.
39. Means, R. E., S. Ishido, X. Alvarez, and J. U. Jung. 2002. Multiple endocytic trafficking pathways of MHC class I molecules induced by a herpesvirus protein. EMBO J. 21:1638-1649.
40. Moore, P. S., and Y. Chang. 2001. Kaposi's sarcoma associated herpesvirus, p. 2803-2833. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
41. Nakamura, H., M. Lu, Y. Gwack, J. Souvlis, S. L. Zeichner, and J. U. Jung. 2003. Global changes in KSHV gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J. Virol. 77:4205-4220.
42. Naranatt, P. P., H. H. Krishnan, M. S. Smith, and B. Chandran. 2005. Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) modulates the microtubule dynamics via rhoA-GTP-diaphenous-2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J. Virol. 79:1191-1206.
43. Naranatt, P. P., H. H. Krishnan, S. R. Svojanovsky, C. Bloomer, S. Mathur, and B. Chandran. 2004. Host gene induction and transcriptional reprogramming in Kaposi's sarcoma-associated herpesvirus (KSHV/HHV-8) infected endothelial, fibroblast and B cells: insights into modulation events early during infection. Cancer Res. 64:72-84.
44. Naranatt, P. P., S. M. Akula, C. A. Zien, H. H. Krishnan, and B. Chandran. 2003. Kaposi's sarcoma-associated herpesvirus induces the phosphatidylinositol 3-kinase-PKC-ζ-MEK-ERK signaling pathway in target cells early during infection: implications for infectivity. J. Virol. 77:1524-1539.
45. Neipel, F., J. C. Albrecht, and B. Fleckenstein. 1997. Cell-homologous genes in the Kaposi's sarcoma-associated rhadinovirus human herpesvirus 8: determinants of its pathogenicity? J. Virol. 71:4187-4192.
46. Okuno, T., Y. B. Jiang, K. Ueda, K. Nishimura, T. Tamura, and K. Yamanishi. 2002. Activation of human herpesvirus 8 open reading frame K5 independent of ORF50 expression. Virus Res. 90:77-89.
47. Pleschka, S., T. Wolff, C. Ehrhardt, G. Hobom, O. Planz, U. R. Rapp, and S. Ludwig. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell Biol. 3:301-305.
48. 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.
49. Renne, R., D. Blackbourn, D. Whitby, J. Levy, and D. Ganem. 1998. Limited transmission of Kaposi's sarcoma-associated herpesvirus in cultured cells. J. Virol. 72:5182-5188.
50. Russo, J. J., R. A. Bohenzky, M. C. Chien, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93:14862-14867.
51. Sarid, R., J. S. Wiezorek, P. S. Moore, and Y. Chang. 1999. Characterization and cell cycle regulation of the major Kaposi's sarcoma-associated herpes-virus (human herpesvirus 8) latent genes and their promoter. J. Virol. 73:1438-1446.
52. Schulz, T. F., J. Sheldon, and J. Greensill. 2002. Kaposi's sarcoma associated herpesvirus (KSHV) or human herpesvirus 8 (HHV8). Virus Res. 82:115-126.
53. Schulz, T. F., Y. Chang, and P. S. Moore. 1998. Kaposi's sarcoma associated herpesvirus (human herpesvirus 8), p. 87-134. In D. J. McCance (ed.), Human tumor viruses. American Society for Microbiology, Washington, D.C.
54. Sharma-Walia, N., P. P. Naranatt, H. H. Krishnan, L. Zeng, and B. Chandran. 2004. Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 envelope glycoprotein gB induces the integrin-dependent focal adhesion kinase-Src-phosphatidylinositol 3-kinase-rho GTPase signal pathways and cytoskeletal rearrangements. J. Virol. 78:4207-4223.
55. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
56. Sontag, E., S. Fedorov, C. Kamibayashi, D. Robbins, M. Cobb, and M. Mumby. 1993. The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the map kinase pathway and induces cell proliferation. Cell. 75:887-897.
57. Spear, P. G. 1993. Entry of alphaherpesviruses into cells. Semin. Virol. 4:167-180.
58. Stupack, D. G., S. Y. Cho, and R. L. Klemke. 2000. Molecular signaling mechanisms of cell migration and invasion. Immunol. Res. 21:83-88.
59. Sun, R., S. F. Lin, K. Staskus, L. Gradoville, E. Grogan, A. Haase, and G. Miller. 1999. Kinetics of Kaposi's sarcoma-associated herpesvirus gene expression. J. Virol. 73:2232-2242.
60. Tomescu, C., W. K. Law, and D. H. Kedes. 2003. Surface downregulation of major histocompatibility complex class 1, PE-CAM, and ICAM-1 following de novo infection of endothelial cells with Kaposi's sarcoma-associated herpesvirus. J. Virol. 77:9669-9684.
61. Ueda, K., H. Arakawa, and Y. Nakamura. 2003. Dual-specificity phosphatase 5 (DUSP5) as a direct transcriptional target of tumor suppressor p53. Oncogene 22:5586-5591.
62. Vieira, J., O. Hearn, L. E. Kimball, B. Chandran, and L. Corey. 2001. Activation of KSHV (HHV-8) lytic replication by human cytomegalovirus. J. Virol. 75:1378-1386.
63. Volmat, V., M. Camps, S. Arkinstall, J. Pouysségur, and P. Lenormand. 2001. The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. J. Cell Sci. 114:3433-3443.
64. Wang, F.-Z., S. M. Akula, N. P. Pramod, L. Zeng, and B. Chandran. 2001. Human herpesvirus 8 envelope glycoprotein K8.1A interaction with the target cells involves heparan sulfate. J. Virol. 75:7517-7527.
65. Wang, F.-Z., S. M. Akula, N. S. Walia, L. Zeng, and B. Chandran. 2003. Human herpesvirus 8 envelope glycoprotein B mediates cell adhesion via its RGD sequence. J. Virol. 77:3131-3147.
66. Wang, S. E., F. Y. Wu, H. Chen, M. Shamay, Q. Zheng, and G. S. Hayward. 2004. Early activation of the Kaposi's sarcoma-associated herpesvirus RTA, RAP, and MTA promoters by the tetradecanoyl phorbol acetate-induced API pathway. J. Virol. 78:4248-4267.
67. Wang, Y., O. T. Chong, and Y. Yuan. 2004. Differential regulation of K8 gene expression in immediate-early and delayed-early stages of Kaposi's sarcoma-associated herpesvirus. Virology 325:149-163.
68. West, J. T., and C. Wood. 2003. The role of Kaposi's sarcoma-associated herpesvirus/human herpesvirus-8 regulator of transcription activation (RTA) in control of gene expression. Oncogene 22:5150-5163.
69. Whitby, D., M. R. Howard, M. Tenant-Flowers, N. S. Brink, A. Copas, C. Boshoff, T. Hatzioannou, F. E. Suggett, D. M Aldam, and A. S. Denton. 1995. Detection of Kaposi sarcoma associated herpesvirus in peripheral blood of HIV-infected individuals and progression to Kaposi's sarcoma. Lancet 346:799-802.
70. WuDunn, D., and P. G. Spear. 1989. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 63:52-58.
71. Xu, S., D. Robbins, J. Frost, A. Dang, C. Lange-Carter, and M. H. Cobb. 1995. MEKK1 phosphorylates MEK1 and MEK2 but does not cause activation of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 92:6808-6812.
72. Yang, X., and D. Gabuzda. 1999. Regulation of human immunodeficiency virus type 1 infectivity by the ERK mitogen-activated protein kinase signaling pathway. J. Virol. 73:3460-3466.
73. Yung, Y., Y. Dolginov, Z. Yao, H. Rubinfeld, D. Michael, T. Hanoch, E. Roubini, Z. Lando, D. Zharhary, and R. Seger. 1997. Detection of ERK activation by a novel monoclonal antibody. FEBS Lett. 408:292-296.
74. Zhu, L., V. Puri, and B. Chandran. 1999. Characterization of human herpesvirus-8 K8.1 A/B glycoproteins by monoclonal antibodies. Virology 262:237-249.