Distinct roles for extracellular signal-regulated kinase 1 (ERK1) and ERK2 in the structure and production of a primate gammaherpesvirus

Journal of Virology

Volumn 86, Issue 18, 2012, Pages 9721-9736

  Woodson, Evonne N ^a   Kedes, Dean H ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME LOCALIZATION; GENE EXPRESSION; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHADINOVIRUS; SIGNAL TRANSDUCTION; VIRION; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS REPLICATION;

ANIMALS; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; HOST-PATHOGEN INTERACTIONS; MACACA MULATTA; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; RHADINOVIRUS; RNA, SMALL INTERFERING; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8; MACACA MULATTA; MIRIDAE; PRIMATES; RHADINOVIRUS;

EID: 84866170670     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00695-12     Document Type: Article

References (81)

1. Adang LA, Parsons CH, Kedes DH. 2006. Asynchronous progression through the lytic cascade and variations in intracellular viral loads revealed by high-throughput single-cell analysis of Kaposi's sarcoma-associated herpesvirus infection. J. Virol. 80:10073-10082.
2. Alexander L, et al. 2000. The primary sequence of rhesus monkey rhadinovirus isolate 26-95: sequence similarities to Kaposi's sarcomaassociated herpesvirus and rhesus monkey rhadinovirus isolate 17577. J. Virol. 74:3388-3398.
3. Andrade AA, et al. 2004. The vaccinia virus-stimulated mitogenactivated protein kinase (MAPK) pathway is required for virus multiplication. Biochem. J. 381:437-446.
4. Barber SA, et al. 2002. Visna virus-induced activation of MAPK is required for virus replication and correlates with virus-induced neuropathology. J. Virol. 76:817-828.
5. Bechtel JT, Winant RC, Ganem D. 2005. Host and viral proteins in the virion of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79:4952-4964.
6. Ben-Levy R, Hooper S, Wilson R, Paterson HF, Marshall CJ. 1998. Nuclear export of the stress-activated protein kinase p38 mediated by its substrate MAPKAP kinase-2. Curr. Biol. 8:1049-1057.
7. Bermudez O, Pages G, Gimond C. 2010. The dual-specificity MAP kinase phosphatases: critical roles in development and cancer. Am. J. Physiol. Cell Physiol. 299: C189-C202.
8. Cai Y, Liu Y, Zhang X. 2007. Suppression of coronavirus replication by inhibition of the MEK signaling pathway. J. Virol. 81:446-456.
9. Cartier C, et al. 1997. Association of ERK2 mitogen-activated protein kinase with human immunodeficiency virus particles. J. Virol. 71:4832-4837.
10. Cesarman E, Chang Y, Moore PS, Said JW, Knowles DM. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 332:1186-1191.
11. Chang Y, et al. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
12. Chen J, Stinski MF. 2002. Role of regulatory elements and the MAPK/ERK or p38 MAPK pathways for activation of human cytomegalovirus gene expression. J. Virol. 76:4873-4885.
13. Cohen A, Brodie C, Sarid R. 2006. An essential role of ERK signalling in TPA-induced reactivation of Kaposi's sarcoma-associated herpesvirus. J. Gen. Virol. 87:795-802.
14. Damania B, et al. 2004. Comparison of the Rta/Orf50 transactivator proteins of gamma-2-herpesviruses. J. Virol. 78:5491-5499.
15. Desrosiers RC, et al. 1997. A herpesvirus of rhesus monkeys related to the human Kaposi's sarcoma-associated herpesvirus. J. Virol. 71:9764-9769.
16. DeWire SM, McVoy MA, Damania B. 2002. Kinetics of expression of rhesus monkey rhadinovirus (RRV) and identification and characterization of a polycistronic transcript encoding the RRV Orf50/Rta, RRV R8, and R8.1 genes. J. Virol. 76:9819-9831.
17. DeWire SM, Money ES, Krall SP, Damania B. 2003. Rhesus monkey rhadinovirus (RRV): construction of a RRV-GFP recombinant virus and development of assays to assess viral replication. Virology 312:122-134.
18. Diao L, et al. 2005. Activation of c-Jun N-terminal kinase (JNK) pathway by HSV-1 immediate early protein ICP0. Exp. Cell Res. 308:196-210.
19. Dittmer DP, et al. 2005. Whole-genome transcription profiling of rhesus monkey rhadinovirus. J. Virol. 79:8637-8650.
20. Duffy C, et al. 2006. Characterization of a UL49-null mutant: VP22 of herpes simplex virus type 1 facilitates viral spread in cultured cells and the mouse cornea. J. Virol. 80:8664-8675.
21. Dupin N, et al. 2000. HHV-8 is associated with a plasmablastic variant of Castleman disease that is linked to HHV-8-positive plasmablastic lymphoma. Blood 95:1406-1412.
22. Dupin N, et al. 1999. Distribution of human herpesvirus-8 latently infected cells in Kaposi's sarcoma, multicentric Castleman's disease, and primary effusion lymphoma. Proc. Natl. Acad. Sci. U. S. A. 96:4546-4551.
23. Favata MF, et al. 1998. Identification of a novel inhibitor of mitogenactivated protein kinase kinase. J. Biol. Chem. 273:18623-18632.
24. Ford PW, et al. 2006. Raf/MEK/ERK signalling triggers reactivation of Kaposi's sarcoma-associated herpesvirus latency. J. Gen. Virol. 87:1139-1144.
25. Gupta P, et al. 2011. Mechanism of host cell MAPK/ERK-2 incorporation into lentivirus particles: characterization of the interaction between MAPK/ERK-2 and proline-rich-domain containing capsid region of structural protein Gag. J. Mol. Biol. 410:681-697.
26. Hemonnot B, et al. 2004. The host cell MAP kinase ERK-2 regulates viral assembly and release by phosphorylating the p6gag protein of HIV-1. J. Biol. Chem. 279:32426-32434.
27. Hui EK. 2002. Virion-associated protein kinases. Cell. Mol. Life Sci. 59:920-931.
28. Jacqué JM, et al. 1998. Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase. EMBO J. 17:2607-2618.
29. Järviluoma A, Ojala PM. 2006. Cell signaling pathways engaged by KSHV. Biochim. Biophys. Acta 1766:140-158.
30. Johnson RA, Huong SM, Huang ES. 2000. Activation of the mitogenactivated protein kinase p38 by human cytomegalovirus infection through two distinct pathways: a novel mechanism for activation of p38. J. Virol. 74:1158-1167.
31. Kalejta RF. 2008. Tegument proteins of human cytomegalovirus. Microbiol. Mol. Biol. Rev. 72:249-265.
32. Krens SF, Corredor-Adamez M, He S, Snaar-Jagalska BE, Spaink HP. 2008. ERK1 and ERK2 MAPK are key regulators of distinct gene sets in zebrafish embryogenesis. BMC Genomics 9: 196. doi:10.1186/1471-2164-9-196.
33. Krens SF, et al. 2008. Distinct functions for ERK1 and ERK2 in cell migration processes during zebrafish gastrulation. Dev. Biol. 319:370-383.
34. Krishnan HH, et al. 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.
35. Krishnan HH, Sharma-Walia N, Streblow DN, Naranatt PP, Chandran B. 2006. Focal adhesion kinase is critical for entry of Kaposi's sarcomaassociated herpesvirus into target cells. J. Virol. 80:1167-1180.
36. Kuang E, Tang Q, Maul GG, Zhu F. 2008. Activation of p90 ribosomal S6 kinase by ORF45 of Kaposi's sarcoma-associated herpesvirus and its role in viral lytic replication. J. Virol. 82:1838-1850.
37. Kuang E, Wu F, Zhu F. 2009. Mechanism of sustained activation of ribosomal S6 kinase (RSK) and ERK by kaposi sarcoma-associated herpesvirus ORF45: multiprotein complexes retain active phosphorylated ERK AND RSK and protect them from dephosphorylation. J. Biol. Chem. 284:13958-13968.
38. Lefloch R, Pouyssegur J, Lenormand P. 2008. Single and combined silencing of ERK1 and ERK2 reveals their positive contribution to growth signaling depending on their expression levels. Mol. Cell. Biol. 28:511-527.
39. Lloyd AC. 2006. Distinct functions for ERKs? J. Biol. 5:13. doi:10.1186/jbiol46.
40. Lyman MG, Randall JA, Calton CM, Banfield BW. 2006. Localization of ERK/MAP kinase is regulated by the alphaherpesvirus tegument protein Us2. J. Virol. 80:7159-7168.
41. Marchi M, et al. 2008. The N-terminal domain of ERK1 accounts for the functional differences with ERK2. PLoS One 3:e3873. doi:10.1371/journal.pone.0003873.
42. Marzluff WF, Jr, Murphy EC, Jr, Huang RC. 1973. Transcription of ribonucleic acid in isolated mouse myeloma nuclei. Biochemistry 12:3440-3446.
43. Mazzucchelli C, et al. 2002. Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34:807-820.
44. Memar OM, Rady PL, Tyring SK. 1995. Human herpesvirus-8: detection of novel herpesvirus-like DNA sequences in Kaposi's sarcoma and other lesions. J. Mol. Med. (Berl.) 73:603-609.
45. Miller G, et al. 1997. Selective switch between latency and lytic replication of Kaposi's sarcoma herpesvirus and Epstein-Barr virus in dually infected body cavity lymphoma cells. J. Virol. 71:314-324.
46. Monick M, Staber J, Thomas K, Hunninghake G. 2001. Respiratory syncytial virus infection results in activation of multiple protein kinase C isoforms leading to activation of mitogen-activated protein kinase. J. Immunol. 166:2681-2687.
47. Naranatt PP, Akula SM, Zien CA, Krishnan HH, Chandran B. 2003. Kaposi's sarcoma-associated herpesvirus induces the phosphatidylinositol 3-kinase-PKC-zeta-MEK-ERK signaling pathway in target cells early during infection: implications for infectivity. J. Virol. 77:1524-1539.
48. Naranatt PP, et al. 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.
49. Newcomb WW, et al. 2000. Isolation of herpes simplex virus procapsids from cells infected with a protease-deficient mutant virus. J. Virol. 74:1663-1673.
50. O'Connor CM, Damania B, Kedes DH. 2003. De novo infection with rhesus monkey rhadinovirus leads to the accumulation of multiple intranuclear capsid species during lytic replication but favors the release of genome-containing virions. J. Virol. 77:13439-13447.
51. O'Connor CM, Kedes DH. 2006. Mass spectrometric analyses of purified rhesus monkey rhadinovirus reveal 33 virion-associated proteins. J. Virol. 80:1574-1583.
52. O'Connor CM, Kedes DH. 2007. Rhesus monkey rhadinovirus: a model for the study of KSHV. Curr. Top. Microbiol. Immunol. 312:43-69.
53. Ott DE. 1997. Cellular proteins in HIV virions. Rev. Med. Virol. 7:167-180.
54. Pagès G, et al. 1999. Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice. Science 286:1374-1377.
55. Pagès G, Pouyssegur J. 2004. Study of MAPK signaling using knockout mice. Methods Mol. Biol. 250:155-166.
56. Pan H, Xie J, Ye F, Gao SJ. 2006. Modulation of Kaposi's sarcomaassociated herpesvirus infection and replication by MEK/ERK, JNK, and p38 multiple mitogen-activated protein kinase pathways during primary infection. J. Virol. 80:5371-5382.
57. Pleschka S, et al. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell Biol. 3:301-305.
58. Rady PL, et al. 1995. Herpesvirus-like DNA sequences in classic Kaposi's sarcomas. J. Med. Virol. 47:179-183.
59. Rady PL, et al. 1995. Herpesvirus-like DNA sequences in non-Kaposi's sarcoma skin lesions of transplant patients. Lancet 345:1339-1340.
60. Rahaus M, Desloges N, Wolff MH. 2006. Varicella-zoster virus influences the activities of components and targets of the ERK signalling pathway. J. Gen. Virol. 87:749-758.
61. Reeves MB, Breidenstein A, Compton T. 2012. Human cytomegalovirus activation of ERK and myeloid cell leukemia-1 protein correlates with survival of latently infected cells. Proc. Natl. Acad. Sci. U. S. A. 109:588-593.
62. Rodems SM, Spector DH. 1998. Extracellular signal-regulated kinase activity is sustained early during human cytomegalovirus infection. J. Virol. 72:9173-9180.
63. Roux PP, Blenis J. 2004. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68:320-344.
64. Rubinfeld H, Seger R. 2005. The ERK cascade: a prototype of MAPK signaling. Mol. Biotechnol. 31:151-174.
65. Sadagopan S, et al. 2007. Kaposi's sarcoma-associated herpesvirus induces sustained NF-kappaB activation during de novo infection of primary human dermal microvascular endothelial cells that is essential for viral gene expression. J. Virol. 81:3949-3968.
66. Schümann M, Dobbelstein M. 2006. Adenovirus-induced extracellular signal-regulated kinase phosphorylation during the late phase of infection enhances viral protein levels and virus progeny. Cancer Res. 66:1282-1288.
67. Searles RP, Bergquam EP, Axthelm MK, Wong SW. 1999. Sequence and genomic analysis of a rhesus macaque rhadinovirus with similarity to Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J. Virol. 73:3040-3053.
68. Seger R, Krebs EG. 1995. The MAPK signaling cascade. FASEB J. 9:726-735.
69. Sharma-Walia N, et al. 2005. 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. J. Virol. 79:10308-10329.
70. Staudt MR, Dittmer DP. 2007. The Rta/Orf50 transactivator proteins of the gamma-herpesviridae. Curr. Top. Microbiol. Immunol. 312:71-100.
71. Vantaggiato C, et al. 2006. ERK1 and ERK2 mitogen-activated protein kinases affect Ras-dependent cell signaling differentially. J. Biol. 5: 14. doi: 10.1186/jbiol38.
72. Wang SE, et al. 2004. Early activation of the Kaposi's sarcoma-associated herpesvirus RTA, RAP, andMTApromoters by the tetradecanoyl phorbol acetate-induced AP1 pathway. J. Virol. 78:4248-4267.
73. Winkler M, Stamminger T. 1996. A specific subform of the human cytomegalovirus transactivator protein pUL69 is contained within the tegument of virus particles. J. Virol. 70:8984-8987.
74. Xie J, Ajibade AO, Ye F, Kuhne K, Gao SJ. 2008. Reactivation of Kaposi's sarcoma-associated herpesvirus from latency requires MEK/ERK, JNK and p38 multiple mitogen-activated protein kinase pathways. Virology 371:139-154.
75. Xie J, Pan H, Yoo S, Gao SJ. 2005. Kaposi's sarcoma-associated herpesvirus induction of AP-1 and interleukin 6 during primary infection mediated by multiple mitogen-activated protein kinase pathways. J. Virol. 79:15027-15037.
76. Yang X, Gabuzda D. 1999. Regulation of human immunodeficiency virus type 1 infectivity by the ERK mitogen-activated protein kinase signaling pathway. J. Virol. 73:3460-3466.
77. Yao Y, et al. 2003. Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation. Proc. Natl. Acad. Sci. U. S. A. 100:12759-12764.
78. Yoon S, Seger R. 2006. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24:21-44.
79. Yu F, et al. 2007. Systematic identification of cellular signals reactivating Kaposi sarcoma-associated herpesvirus. PLoS Pathog. 3: e44. doi:10.1371/journal.ppat.0030044.
80. Yu XK, et al. 2003. Three-dimensional structures of the A, B, and C capsids of rhesus monkey rhadinovirus: insights into gammaherpesvirus capsid assembly, maturation, and DNA packaging. J. Virol. 77:13182-13193.
81. Zhu FX, Chong JM, Wu L, Yuan Y. 2005. Virion proteins of Kaposi's sarcoma-associated herpesvirus. J. Virol. 79: 800-811