Integrated analyses of genome-wide DNA occupancy and expression profiling identify key genes and pathways involved in cellular transformation by a marek's disease virus oncoprotein, meq

Journal of Virology

Volumn 87, Issue 16, 2013, Pages 9016-9029

  Subramaniam, Sugalesini ^a,b   Johnston, John ^c   Preeyanon, Likit ^d   Brown, Titus C ^d   Kung, Hsing Jien ^e   Cheng, Hans H ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c Michigan State University   (United States)

^d NONE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; JANUS KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; ONCOPROTEIN; PHOSPHATASE; PROTEIN C JUN; PROTEIN MEQ; STAT PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL PROLIFERATION; CELL TRANSFORMATION; CHICKEN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CREB1 GENE; DOWN REGULATION; EMBRYO; ENZYME INHIBITION; GENE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; MICROARRAY ANALYSIS; NFE2L2 GENE; NONHUMAN; NR2F1 GENE; ONCOGENE MYC; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; UPREGULATION; ZEB1 GENE;

ANIMALS; BINDING SITES; CELL LINE; CELL TRANSFORMATION, VIRAL; CHICKENS; CHROMATIN IMMUNOPRECIPITATION; DNA; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; MARDIVIRUS; MICROARRAY ANALYSIS; ONCOGENE PROTEINS, VIRAL; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

EID: 84881260786     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01163-13     Document Type: Article

References (84)

1. Osterrieder N, Kamil JP, Schumacher D, Tischer BK, Trapp S. 2006. Marek's disease virus: from miasma to model. Nat. Rev. Microbiol. 4:283-294.
2. Witter RL. 1998. Control strategies for Marek's disease: a perspective for the future. Poult. Sci. 77:1197-1203.
3. Baigent SJ, Smith LP, Nair VK, Currie RJ. 2006. Vaccinal control of Marek's disease: current challenges, and future strategies to maximize protection. Vet. Immunol. Immunopathol. 112:78-86.
4. Okazaki W, Purchase HG, Burmester BR. 1970. Protection against Marek's disease by vaccination with a herpesvirus of turkeys. Avian Dis. 14:413-429.
5. Witter RL. 1997. Increased virulence of Marek's disease virus field isolates. Avian Dis. 41:149-163.
6. Gimeno IM. 2008. Marek's disease vaccines: a solution for today but a worry for tomorrow? Vaccine 26(Suppl 3):C31-C41.
7. Morrow C, Fehler F. 2004. Marek's disease: a world-wide problem, p 49-61. In Davison F, Nair V (ed), Marek's disease. Academic Press, San Diego, CA.
8. Nair V, Kung HJ. 2004. Marek's disease virus oncogenicity: molecular mechanisms, p 32-47. In Davison F, Nair V (ed), Marek's disease. Academic Press, San Diego, CA.
9. Jones D, Lee L, Liu JL, Kung HJ, Tillotson JK. 1992. Marek disease virus encodes a basic-leucine zipper gene resembling the fos/jun oncogenes that is highly expressed in lymphoblastoid tumors. Proc. Natl. Acad. Sci. U. S. A. 89:4042-4046.
10. Lee LF, Wu P, Sui D, Ren D, Kamil J, Kung HJ, Witter RL. 2000. The complete unique long sequence and the overall genomic organization of the GA strain of Marek's disease virus. Proc. Natl. Acad. Sci. U. S. A. 97:6091-6096.
11. Lupiani B, Lee LF, Cui X, Gimeno I, Anderson A, Morgan RW, Silva RF, Witter RL, Kung HJ, Reddy SM. 2004. Marek's disease virusencoded Meq gene is involved in transformation of lymphocytes but is dispensable for replication. Proc. Natl. Acad. Sci. U. S. A. 101:11815-11820.
12. Xie Q, Anderson AS, Morgan RW. 1996. Marek's disease virus (MDV) ICP4, pp38, and meq genes are involved in the maintenance of transformation of MDCC-MSB1 MDV-transformed lymphoblastoid cells. J. Virol. 70:1125-1131.
13. Kung HJ, Xia L, Brunovskis P, Li D, Liu JL, Lee LF. 2001. Meq: an MDV-specific bZIP transactivator with transforming properties. Curr. Top. Microbiol. Immunol. 255:245-260.
14. Qian Z, Brunovskis P, Lee L, Vogt PK, Kung HJ. 1996. Novel DNA binding specificities of a putative herpesvirus bZIP oncoprotein. J. Virol. 70:7161-7170.
15. Ross NL. 1999. T-cell transformation by Marek's disease virus. Trends Microbiol. 7:22-29.
16. Levy AM, Gilad O, Xia L, Izumiya Y, Choi J, Tsalenko A, Yakhini Z, Witter R, Lee L, Cardona CJ, Kung HJ. 2005. Marek's disease virus Meq transforms chicken cells via the v-Jun transcriptional cascade: a converging transforming pathway for avian oncoviruses. Proc. Natl. Acad. Sci. U. S. A. 102:14831-14836.
17. Himly M, Foster DN, Bottoli I, Iacovoni JS, Vogt PK. 1998. The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248:295-304.
18. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
19. Valouev A, Johnson DS, Sundquist A, Medina C, Anton E, Batzoglou S, Myers RM, Sidow A. 2008. Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods 5:829-834.
20. Bailey TL, Williams N, Misleh C, Li WW. 2006. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34: W369-W373.
21. Bailey TL, Boden M, Buske FA, Frith M, Grant E, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37:W202-W208.
22. Scaffidi AK, Mutsaers SE, Moodley YP, McAnulty RJ, Laurent GJ, Thompson PJ, Knight DA. 2002. Oncostatin M stimulates proliferation, induces collagen production and inhibits apoptosis of human lung fibroblasts. Br. J. Pharmacol. 136:793-801.
23. Ohori M, Kinoshita T, Okubo M, Sato K, Yamazaki A, Arakawa H, Nishimura S, Inamura N, Nakajima H, Neya M, Miyake H, Fujii T. 2005. Identification of a selective ERK inhibitor and structural determination of the inhibitor-ERK2 complex. Biochem. Biophys. Res. Commun. 336:357-363.
24. Levy AM, Izumiya Y, Brunovskis P, Xia L, Parcells MS, Reddy SM, Lee L, Chen HW, Kung HJ. 2003. Characterization of the chromosomal binding sites and dimerization partners of the viral oncoprotein Meq in Marek's disease virus-transformed T cells. J. Virol. 77:12841-12851.
25. Wingender E, Dietze P, Karas H, Knüppel R. 1996. TRANSFAC: a database on transcription factors and their DNA binding sites. Nucleic Acids Res. 24:238-241.
26. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. 2010. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res. 38:D105-D110.
27. Zhao L, Glazov EA, Pattabiraman DR, Al-Owaidi F, Zhang P, Brown MA, Leo PJ, Gonda TJ. 2011. Integrated genome-wide chromatin occupancy and expression analyses identify key myeloid prodifferentiation transcription factors repressed by Myb. Nucleic Acids Res. 39:4664-4679.
28. Ridinger-Saison M, Boeva V, Rimmele P, Kulakovskiy I, Gallais I, Levavasseur B, Paccard C, Legoix-Ne P, Morle F, Nicolas A, Hupe P, Barillot E, Moreau-Gachelin F, Guillouf C. 2012. Spi-1/PU. 1 activates transcription through clustered DNA occupancy in erythroleukemia. Nucleic Acids Res. 40:8927-8941.
29. Li M, Ge Q, Wang W, Wang J, Lu Z. 2011. c-Jun binding site identification in K562 cells. J. Genet. Genomics 38:235-242.
30. Suchodolski PF, Izumiya Y, Lupiani B, Ajithdoss DK, Lee LF, Kung HJ, Reddy SM. 2010. Both homo and heterodimers of Marek's disease virus encoded Meq protein contribute to transformation of lymphocytes in chickens. Virology 399:312-321.
31. Verbruggen V, Ek O, Georlette D, Delporte F, Von Berg V, Detry N, Biemar F, Coutinho P, Martial JA, Voz ML, Manfroid I, Peers B. 2010. The Pax6b homeodomain is dispensable for pancreatic endocrine cell differentiation in zebrafish. J. Biol. Chem. 285:13863-13873.
32. Bard-Chapeau EA, Jeyakani J, Kok CH, Muller J, Chua BQ, Gunaratne J, Batagov A, Jenjaroenpun P, Kuznetsov VA, Wei CL, D'Andrea RJ, Bourque G, Jenkins NA, Copeland NG. 2012. Ecotopic viral integration site 1 (EVI1) regulates multiple cellular processes important for cancer and is a synergistic partner for FOS protein in invasive tumors. Proc. Natl. Acad. Sci. U. S. A. 109:2168-2173.
33. Brown AC, Smith LP, Kgosana L, Baigent SJ, Nair V, Allday MJ. 2009. Homodimerization of the Meq viral oncoprotein is necessary for induction of T-cell lymphoma by Marek's disease virus. J. Virol. 83:11142-11151.
34. Suchodolski PF, Izumiya Y, Lupiani B, Ajithdoss DK, Gilad O, Lee LF, Kung HJ, Reddy SM. 2009. Homodimerization of Marek's disease virusencoded Meq protein is not sufficient for transformation of lymphocytes in chickens. J. Virol. 83:859-869.
35. Platanias LC. 2003. Map kinase signaling pathways and hematologic malignancies. Blood 101:4667-4679.
36. De Luca A, Maiello MR, D'Alessio A, Pergameno M, Normanno N. 2012. The RAS/RAF/MEK/ERK and the PI3K/AKT signalling pathways: role in cancer pathogenesis and implications for therapeutic approaches. Expert Opin. Ther. Targets 16(Suppl 2):S17-S27.
37. Kiu H, Nicholson SE. 2012. Biology and significance of the JAK/STAT signaling pathways. Growth Factors 30:88-106.
38. Sansone P, Bromberg J. 2012. Targeting the interleukin-6/Jak/stat pathway in human malignancies. J. Clin. Oncol. 30:1005-1014.
39. Zheng CF, Guan KL. 1993. Properties of MEKs, the kinases that phosphorylate and activate the extracellular signal-regulated kinases. J. Biol. Chem. 268:23933-23939.
40. Buza JJ, Burgess SC. 2007. Modeling the proteome of a Marek's disease transformed cell line: a natural animal model for CD30 overexpressing lymphomas. Proteomics 7:1316-1326.
41. Roberts ML, Cooper NR. 1998. Activation of a ras-MAPK-dependent pathway by Epstein-Barr virus latent membrane protein 1 is essential for cellular transformation. Virology 240:93-99.
42. Dawson CW, Laverick L, Morris MA, Tramoutanis G, Young LS. 2008. Epstein-Barr virus-encoded LMP1 regulates epithelial cell motility and invasion via the ERK-MAPK pathway. J. Virol. 82:3654-3664.
43. Portis T, Longnecker R. 2004. Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/ Akt pathway. Oncogene 23:8619-8628.
44. Anderson LJ, Longnecker R. 2008. EBV LMP2A provides a surrogate pre-B cell receptor signal through constitutive activation of the ERK/ MAPK pathway. J. Gen. Virol. 89:1563-1568.
45. 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.
46. Ye FC, Blackbourn DJ, Mengel M, Xie JP, Qian LW, Greene W, Yeh IT, Graham D, Gao SJ. 2007. Kaposi's sarcoma-associated herpesvirus promotes angiogenesis by inducing angiopoietin-2 expression via AP-1 and Ets1. J. Virol. 81:3980-3991.
47. Lambert PJ, Shahrier AZ, Whitman AG, Dyson OF, Reber AJ, McCubrey JA, Akula SM. 2007. Targeting the PI3K and MAPK pathways to treat Kaposi's-sarcoma-associated herpes virus infection and pathogenesis. Expert Opin. Ther. Targets 11:589-599.
48. Cai Q, Verma SC, Lu J, Robertson ES. 2010. Molecular biology of Kaposi's sarcoma-associated herpesvirus and related oncogenesis. Adv. Virus Res. 78:87-142.
49. Chen RE, Thorner J. 2007. Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim. Biophys. Acta 1773:1311-1340.
50. Keyse SM. 2000. Protein phosphatases and the regulation of mitogenactivated protein kinase signalling. Curr. Opin. Cell Biol. 12:186-192.
51. Camps M, Nichols A, Arkinstall S. 2000. Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J. 14:6-16.
52. Owens DM, Keyse SM. 2007. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26:3203-3213.
53. Haagenson KK, Wu GS. 2010. Mitogen activated protein kinase phosphatases and cancer. Cancer Biol. Ther. 9:337-340.
54. Wu S, Wang Y, Sun L, Zhang Z, Jiang Z, Qin Z, Han H, Liu Z, Li X, Tang A, Gui Y, Cai Z, Zhou F. 2011. Decreased expression of dualspecificity phosphatase 9 is associated with poor prognosis in clear cell renal cell carcinoma. BMC Cancer 11:413. doi:10.1186/1471-2407-11 -413.
55. Westermarck J, Li SP, Kallunki T, Han J, Kähäri VM. 2001. p38 mitogen-activated protein kinase-dependent activation of protein phosphatases 1 and 2A inhibits MEK1 and MEK2 activity and collagenase 1 (MMP-1) gene expression. Mol. Cell. Biol. 21:2373-2383.
56. Mumby M. 2007. PP2A: unveiling a reluctant tumor suppressor. Cell 130:21-24.
57. Garibal J, Hollville E, Bell AI, Kelly GL, Renouf B, Kawaguchi Y, Rickinson AB, Wiels J. 2007. Truncated form of the Epstein-Barr virus protein EBNA-LP protects against caspase-dependent apoptosis by inhibiting protein phosphatase 2A. J. Virol. 81:7598-7607.
58. Mochida S, Hunt T. 2012. Protein phosphatases and their regulation in the control of mitosis. EMBO Rep. 13:197-203.
59. Sehgal PB. 2000. STAT-signalling through the cytoplasmic compartment: consideration of a new paradigm. Cell. Signal. 12:525-535.
60. Burke WM, Jin X, Lin HJ, Huang M, Liu R, Reynolds RK, Lin J. 2001. Inhibition of constitutively active Stat3 suppresses growth of human ovarian and breast cancer cells. Oncogene 20:7925-7934.
61. Hodge DR, Hurt EM, Farrar WL. 2005. The role of IL-6 and STAT3 in inflammation and cancer. Eur. J. Cancer 41:2502-2512.
62. Wu C, Guan Q, Wang Y, Zhao ZJ, Zhou GW. 2003. SHP-1 suppresses cancer cell growth by promoting degradation of JAK kinases. J. Cell. Biochem. 90:1026-1037.
63. Wu C, Sun M, Liu L, Zhou GW. 2003. The function of the protein tyrosine phosphatase SHP-1 in cancer. Gene 306:1-12.
64. Ehrmann J, Strakova N, Vrzalikova K, Hezova R, Kolar Z. 2008. Expression of STATs and their inhibitors SOCS and PIAS in brain tumors. In vitro and in vivo study. Neoplasma 55:482-487.
65. Barclay JL, Anderson ST, Waters MJ, Curlewis JD. 2009. SOCS3 as a tumor suppressor in breast cancer cells, and its regulation by PRL. Int. J. Cancer 124:1756-1766.
66. Coppola D, Parikh V, Boulware D, Blanck G. 2009. Substantially reduced expression of PIAS1 is associated with colon cancer development. J. Cancer Res. Clin. Oncol. 135:1287-1291.
67. Greenhalgh CJ, Alexander WS. 2004. Suppressors of cytokine signalling and regulation of growth hormone action. Growth Horm. IGF Res. 14: 200-206.
68. Ram PA, Waxman DJ. 1997. Interaction of growth hormone-activated STATs with SH2-containing phosphotyrosine phosphatase SHP-1 and nuclear JAK2 tyrosine kinase. J. Biol. Chem. 272:17694-17702.
69. Liu HC, Kung HJ, Fulton JE, Morgan RW, Cheng HH. 2001. Growth hormone interacts with the Marek's disease virus SORF2 protein and is associated with disease resistance in chicken. Proc. Natl. Acad. Sci. U. S. A. 98:9203-9208.
70. Wilker E, Yaffe MB. 2004. 14-3-3 Proteins-a focus on cancer and human disease. J. Mol. Cell. Cardiol. 37:633-642.
71. Freeman AK, Morrison DK. 2011. 14-3-3 Proteins: diverse functions in cell proliferation and cancer progression. Semin. Cell Dev. Biol. 22:681-687.
72. Hermeking H, Benzinger A. 2006. 14-3-3 proteins in cell cycle regulation. Semin. Cancer Biol. 16:183-192.
73. Freed E, Symons M, Macdonald SG, McCormick F, Ruggieri R. 1994. Binding of 14-3-3 proteins to the protein kinase Raf and effects on its activation. Science 265:1713-1716.
74. Irie K, Gotoh Y, Yashar BM, Errede B, Nishida E, Matsumoto K. 1994. Stimulatory effects of yeast and mammalian 14-3-3 proteins on the Raf protein kinase. Science 265:1716-1719.
75. Downward J. 1994. The GRB2/Sem-5 adaptor protein. FEBS Lett. 338: 113-117.
76. Tari AM, Lopez-Berestein G. 2001. GRB2: a pivotal protein in signal transduction. Semin. Oncol. 28:142-147.
77. Daly RJ, Binder MD, Sutherland RL. 1994. Overexpression of the Grb2 gene in human breast cancer cell lines. Oncogene 9:2723-2727.
78. Watanabe T, Shinohara N, Moriya K, Sazawa A, Kobayashi Y, Ogiso Y, Takiguchi M, Yasuda J, Koyanagi T, Kuzumaki N, Hashimoto A. 2000. Significance of the Grb2 and son of sevenless (Sos) proteins in human bladder cancer cell lines. IUBMB Life 49:317-320.
79. Giubellino A, Burke TR, Bottaro DP. 2008. Grb2 signaling in cell motility and cancer. Expert Opin. Ther. Targets 12:1021-1033.
80. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
81. Liu JL, Ye Y, Lee LF, Kung HJ. 1998. Transforming potential of the herpesvirus oncoprotein MEQ: morphological transformation, serum-independent growth, and inhibition of apoptosis. J. Virol. 72: 388-395.
82. Ohashi K, Morimura T, Takagi M, Lee SI, Cho KO, Takahashi H, Maeda Y, Sugimoto C, Onuma M. 1999. Expression of bcl-2 and bcl-x genes in lymphocytes and tumor cell lines derived from MDV-infected chickens. Acta Virol. 43:128-132.
83. Takagi M, Takeda T, Asada Y, Sugimoto C, Onuma M, Ohashi K. 2006. The presence of a short form of p53 in chicken lymphoblastoid cell lines during apoptosis. J. Vet. Med. Sci. 68:561-566.
84. Alikhani M, Alikhani Z, Graves DT. 2005. FOXO1 functions as a master switch that regulates gene expression necessary for tumor necrosis factorinduced fibroblast apoptosis. J. Biol. Chem. 280:12096-12102.