Upregulation of cellular Bcl-2 by the KSHV encoded RTA promotes virion production

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Gao, Jianming ^a,b   Cai, Qiliang ^a   Lu, Jie ^a   Jha, Hem Chandra ^a   Robertson, Erle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Three Gorges University School of Medicine   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN; PROTEIN BCL 2; REPLICATION AND TRANSCRIPTION ACTIVATOR; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; RTA PROTEIN, HUMAN HERPESVIRUS 8; TRANSACTIVATOR PROTEIN;

APOPTOSIS; ARTICLE; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; UPREGULATION; VIRION; VIRUS REPLICATION; CELL LINE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NORTHERN BLOTTING; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING;

HUMAN HERPESVIRUS 8; LENTIVIRUS;

APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; HERPESVIRUS 8, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; POLYMERASE CHAIN REACTION; PROTO-ONCOGENE PROTEINS C-BCL-2; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANS-ACTIVATORS; VIRION;

EID: 80052061573     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023892     Document Type: Article

References (71)

1. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, et al. (1994) Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Sicence 266: 1865-1869.
2. 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.
3. Boshoff C, Schulz TF, Kennedy MM, Graham AK, Fisher C, et al. (1995) Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat Med 1: 1274-1278.
4. Soulier J, Grollet L, Oksenhendler E, Cacoub P, Cazals-Hatem D, et al. (1995) Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86: 1276-1280.
5. Ohtsuki Y, Iwata J, Furihata M, Takeuchi T, Sonobe H, et al. (1999) Ultrastructure of Kaposi's sarcoma-associated herpesvirus (KSHV)/human herpesvirus-8 (HHV-8) in a primary effusion lymphoma cell line treated with tetradecanoyl phorbol acetate (TPA). Med Electron Microsc 32: 94-99.
6. Wang YC, Zhang Q, Montalvo EA, (1998) Purification of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) and analyses of the structural proteins. J Virol Methods 73: 219-228.
7. Jenner RG, Albà MM, Boshoff C, Kellam P, (2001) Kaposi's sarcoma-associated herpesvirus latent and lytic gene expression as revealed by DNA arrays. J Virol 75: 891-902.
8. Sarid R, Flore O, Bohenzky RA, Chang Y, Moore PS, (1998) Transcription mapping of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) genome in a body cavity-based lymphoma cell line (BC-1). J Virol 72: 1005-1012.
9. Dittmer D, Lagunoff M, Renne R, Staskus K, Haase A, et al. (1998) A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus. J Virol 72: 8309-8315.
10. Sharp TV, Wang HW, Koumi A, Hollyman D, Endo Y, et al. (2002) K15 protein of Kaposi's sarcoma-associated herpesvirus is latently expressed and binds to HAX-1, a protein with antiapoptotic function. J Virol 76: 802-816.
11. Davis DA, Rinderknecht AS, Zoeteweij JP, Aoki Y, Read-Connole EL, et al. (2001) Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus. Blood 97: 3244-3250.
12. Haque M, Davis DA, Wang V, Widmer I, Yarchoan R, (2003) Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) contains hypoxia response elements: relevance to lytic induction by hypoxia. J Virol 77: 6761-6768.
13. Cai Q, Lan K, Verma SC, Si H, Lin D, et al. (2006) Kaposi's sarcoma-associated herpesvirus latent protein LANA interacts with HIF-1 alpha to upregulate RTA expression during hypoxia: Latency control under low oxygen conditions. J Virol 80: 7965-7975.
14. Miller G, Heston L, Grogan E, Gradoville L, Rigsby M, 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.
15. Yu Y, Black JB, Goldsmith CS, Browning PJ, Bhalla K, et al. (1999) Induction of human herpesvirus-8 DNA replication and transcription by butyrate and TPA in BCBL-1 cells. J Gen Virol 80: 83-90.
16. Bowser BS, DeWire SM, Damania B, (2002) Transcriptional regulation of the K1 gene product of Kaposi's sarcoma-associated herpesvirus. J Virol 76: 12574-12583.
17. Deng H, Song MJ, Chu JT, Sun R, (2002) Transcriptional regulation of the interleukin-6 gene of human herpesvirus 8 (Kaposi's sarcoma-associated herpesvirus). J Virol 76: 8252-8264.
18. Rimessi P, Bonaccrosi A, Stürzl M, Fabris M, Brocca-Cofano E, et al. (2001) Transcription pattern of human herpesvirus 8 open reading frame K3 in primary effusion lymphoma and Kaposi's sarcoma. J Virol 75: 7161-7174.
19. Haque M, Chen J, Ueda K, Mori Y, Nakano K, et al. (2000) Identification and analysis of the K5 gene of Kaposi's sarcoma-associated herpesvirus. J Virol 74: 2867-2875.
20. Seaman WT, Quinlivan EB, (2003) Lytic switch protein (ORF50) response element in the Kaposi's sarcoma-associated herpesvirus K8 promoter is located within but does not require a palindromic structure. Virology 310: 72-84.
21. Wang Y, Yuan Y, (2007) Essential role of RBP-Jkappa in activation of the K8 delayed-early promoter of Kaposi's sarcoma-associated herpesvirus by ORF50/RTA. Virology 359: 19-27.
22. Ueda K, Ishikawa K, Nishimura K, Sakakibara S, Do E, et al. (2002) Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) replication and transcription factor activates the K9 (vIRF) gene through two distinct cis elements by a non-DNA-binding mechanism. J Virol 76: 12044-12054.
23. Song MJ, Deng H, Sun R, (2003) Comparative study of regulation of RTA-responsive genes in Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J Virol 77: 9451-9462.
24. Liang Y, Ganem D, (2004) RBP-J (CSL) is essential for activation of the K14/vGPCR promoter of Kaposi's sarcoma-associated herpesvirus by the lytic switch protein RTA. J Virol 78: 6818-6826.
25. Wong EL, Damania B, (2006) Transcriptional regulation of the Kaposi's sarcoma-associated herpesvirus K15 gene. J Virol 80: 1385-1392.
26. Song MJ, Brown HJ, Wu TT, Sun R, (2001) Transcription activation of polyadenylated nuclear rna by rta in human herpesvirus 8/Kaposi's sarcoma-associated herpesvirus. J Virol 75: 3129-3140.
27. Song MJ, Li X, Brown HJ, Sun R, (2002) Characterization of interactions between RTA and the promoter of polyadenylated nuclear RNA in Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J Virol 76: 5000-5013.
28. Masa SR, Lando R, Sarid R, (2008) Transcriptional regulation of the open reading frame 35 encoded by Kaposi's sarcoma-associated herpesvirus. Virology 371: 14-31.
29. Gonzalez CM, Wong EL, Bowser BS, Hong GK, Kenney S, et al. (2006) Identification and characterization of the Orf49 protein of Kaposi's sarcoma-associated herpesvirus. J Virol 80: 3062-3070.
30. Sakakibara S, Ueda K, Chen J, Okuno T, Yamanishi K, (2001) Octamer-binding sequence is a key element for the autoregulation of Kaposi's sarcoma-associated herpesvirus ORF50/Lyta gene expression. J Virol 75: 6894-6900.
31. Deng H, Young A, Sun R, (2000) Auto-activation of the rta gene of human herpesvirus-8/Kaposi's sarcoma-associated herpesvirus. J Gen Virol 81: 3043-3048.
32. Byun H, Gwack Y, Hwang S, Choe J, (2002) Kaposi's sarcoma-associated herpesvirus open reading frame (ORF) 50 transactivates K8 and ORF57 promoters via heterogeneous response elements. Mol Cells 14: 185-191.
33. Wang SE, Wu FY, Yu Y, Hayward GS, (2003) CCAAT/enhancer-binding protein-alpha is induced during the early stages of Kaposi's sarcoma-associated herpesvirus (KSHV) lytic cycle reactivation and together with the KSHV replication and transcription activator (RTA) cooperatively stimulates the viral RTA, MTA, and PAN promoters. J Virol 77: 9590-9612.
34. Liu Y, Cao Y, Liang D, Gao Y, Xia T, et al. (2008) Kaposi's sarcoma-associated herpesvirus RTA activates the processivity factor ORF59 through interaction with RBP-Jkappa and a cis-acting RTA responsive element. Virology 380: 264-275.
35. Green DR, Evan GI, (2002) A matter of life and death. Cancer Cell 1: 19-30.
36. Flanagan AM, Letai A, (2008) BH3 domains define selective inhibitory interactions with BHRF-1 and KSHV BCL-2. Cell Death Differ 15: 580-588.
37. Cory S, Adam JM, (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2: 647-656.
38. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR, (2010) The BCL-2 family reunion. Mol Cell 37: 299-310.
39. Brychtová S, Brychta T, Kotrsová L, Pilka R, Tichý M, et al. (2000) Expression of Bcl-2 in dysplastic and neoplastic cervical lesions in relation to cell proliferation and HPV infection. Neoplasma 47: 143-147.
40. Tsujimoto Y, Cossman J, Jaffe E, Croce CM, (1985) Involvement of the bcl-2 gene in human follicular lymphoma. Science 228: 1440-1443.
41. Yip KW, Reed JC, (2008) Bcl-2 family proteins and cancer. Oncogene 27: 6398-6406.
42. Higashiyama M, Doi O, Kodama K, Yokouchi H, et al. (1995) High prevalence of bcl-2 oncoprotein expression in small cell lung cancer. Anticancer Res 15: 503-505.
43. Harada N, Hata H, Yoshida M, Soniki T, Nagasaki A, et al. (1998) Expression of Bcl-2 family of proteins in fresh myeloma cells. Leukemia 12: 1817-1820.
44. Leiter U, Schmid RM, Kaskel P, Peter RU, Krähn G, (2000) Antiapoptotic bcl-2 and bcl-xL in advanced malignant melanoma. Arch Dermatol Res 292: 225-232.
45. Ohmori T, Podack ER, Nishio K, Takahashi M, Miyahara Y, et al. (1993) Apoptosis of lung cancer cells caused by some anti-cancer agents (MMC, CPT-11, ADM) is inhibited by bcl-2. Biochem Biophys Res Commun 192: 30-36.
46. Harima Y, Harima K, Shikata N, Oka A, Ohnishi T, et al. (1998) Bax and Bcl-2 expressions predict response to radiotherapy in human cervical cancer. J Cancer Res Clin Oncol 124: 503-510.
47. Bourgarel-Rey V, Savry A, Hua G, Carré M, Bressin C, et al. (2009) Transcriptional down-regulation of Bcl-2 by vinorelbine: identification of a novel binding site of p53 on Bcl-2 promoter. Biochem Pharmacol 78: 1148-1156.
48. Wang XD, Ou TM, Lu YJ, Li Z, Xu Z, et al. (2010) Turning off transcription of the bcl-2 gene by stabilizing the bcl-2 promoter quadruplex with quindoline derivatives. J Med Chem 53: 4390-4398.
49. Onyshchenko MI, Gaynutdinov TI, Englund EA, Appella DH, Neumann RD, et al. (2009) Stabilization of G-quadruplex in the BCL2 promoter region in double-stranded DNA by invading short PNAs. Nucleic Acids Res 37: 7570-7580.
50. Breitschopf K, Haendeler J, Malchow P, Zeiher AM, Dimmeler S, (2000) Posttranslational modification of Bcl-2 facilitates its proteasome-dependent degradation: molecular characterization of the involved signaling pathway. Mol Cell Biol 20: 1886-1896.
51. Lan K, Kuppers DA, Verma SC, Sharma N, Murakami M, et al. (2005) Induction of Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen by the lytic transactivator RTA: a novel mechanism for establishment of latency. J Virol 79: 7453-7465.
52. Lu J, Verma SC, Murakami M, Cai Q, Kumar P, et al. (2009) Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus (KSHV) upregulates survivin expression in KSHV-Associated B-lymphoma cells and contributes to their proliferation. J Virol 83: 7129-7141.
53. He Z, Liu Y, Liang D, Wang Z, Robertson ES, et al. (2010) Cellular corepressor TLE2 inhibits replication-and-transcription- activator-mediated transactivation and lytic reactivation of Kaposi's sarcoma-associated herpesvirus. J Virol 84: 2047-2062.
54. Junn HJ, Kim JY, Seol DW, (2010) Effective knockdown of multiple target genes by expressing the single transcript harbouring multi-cistronic shRNAs. Biochem Biophys Res Commun 396: 861-865.
55. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, et al. (2003) Global changes in Kaposi's sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J Virol 77: 4205-4220.
56. Lukac DM, Kirshner J, Ganem D, (1999) Transcriptional activation by the product of open reading frame 50 of Kaposi's sarcoma-associated herpesvirus is required for lytic viral reactivation in B cells. J Virol 73: 9348-9361.
57. Lukac DM, Renne R, Kirshner JR, Ganem D, (1998) Reactivation of Kaposi's sarcoma-associated herpesvirus infection from latency by expression of the ORF 50 transactivator, a homolog of the EBV R protein. Virology 252: 304-312.
58. Wen HJ, Minhas V, Wood C, (2009) Identification and characterization of a new Kaposi's sarcoma-associated herpesvirus replication and transcription activator (RTA)-responsive element involved in RTA-mediated transactivation. J Gen Virol 90: 944-953.
59. Ballestas ME, Chatis PA, Kaye KM, (1999) Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen. Science 284: 641-644.
60. Cotter MA 2nd, Robertson ES, (1999) The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264: 254-264.
61. Moore PS, Boshoff C, Weiss RA, Chang Y, (1996) Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274: 1739-1744.
62. Moore PS, Chang Y, (2001) Molecular virology of Kaposi's sarcoma-associated herpesvirus. Philos Trans R Soc Lond B Biol Sci 356: 499-516.
63. Wang S, Liu S, Wu MH, Geng Y, Wood C, (2001) Identification of a cellular protein that interacts and synergizes with the RTA (ORF50) protein of Kaposi's sarcoma-associated herpesvirus in transcriptional activation. J Virol 75: 11961-11973.
64. Yang Z, Wood C, (2007) The transcriptional repressor K-RBP modulates RTA-mediated transactivation and lytic replication of Kaposi's sarcoma-associated herpesvirus. J Virol 81: 6294-6306.
65. Wang SE, Wu FY, Fujimuro M, Zong J, Hayward SD, et al. (2003) Role of CCAAT/enhancer-binding protein alpha (C/EBPalpha) in activation of the Kaposi's sarcoma-associated herpesvirus (KSHV) lytic-cycle replication-associated protein (RAP) promoter in cooperation with the KSHV replication and transcription activator (RTA) and RAP. J Virol 77: 600-623.
66. Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G, (2008) Viral control of mitochondrial apoptosis. PLoS Pathog 4: e1000018.
67. Cam M, Handke W, Picard-Maureau M, Brune W, (2010) Cytomegaloviruses inhibit Bak- and Bax-mediated apoptosis with two separate viral proteins. Cell Death Differ 17: 655-665.
68. Everett H, McFadden G, (1999) Apoptosis: an innate immune response to virus infection. Trends Microbiol 7: 160-165.
69. Gruffat H, Sergeant A, (1994) Characterization of the DNA-binding site repertoire for the Epstein-Barr virus transcription factor R. Nucleic Acids Res 22: 1172-1178.
70. Chen LW, Chang PJ, Delecluse HJ, Miller G, (2005) Marked variation in response of consensus binding elements for the Rta protein of Epstein-Barr virus. J Virol 79: 9635-9650.
71. Young RL, Korsmeyer S, (1993) A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol Cell Biol 13: 3686-3697.