Quantitative analysis of the bidirectional viral G-protein-coupled receptor and lytic latency-associated nuclear antigen promoter of Kaposi's sarcoma-associated herpesvirus

Journal of Virology

Volumn 86, Issue 18, 2012, Pages 9683-9695

  Hiltona, Isaac B ^a   Dittmer, Dirk P ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LATENCY ASSOCIATED NUCLEAR ANTIGEN; LUCIFERASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; GAIN OF FUNCTION MUTATION; GENETIC REGULATION; HUMAN HERPESVIRUS 8; LOSS OF FUNCTION MUTATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; TATA BOX; TRANSACTIVATION;

ANTIGENS, VIRAL; BASE SEQUENCE; CELL LINE; GENOME, VIRAL; HERPESVIRUS 8, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, VIRUS; RNA, MESSENGER; RNA, VIRAL; TRANS-ACTIVATORS; VIRUS LATENCY;

HUMAN HERPESVIRUS 8;

EID: 84866151030     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00881-12     Document Type: Article

References (84)

1. Arnett KL, et al. 2010. Structural and mechanistic insights into cooperative assembly of dimeric Notch transcription complexes Nat. Struct. Mol. Biol. 17:1312-1317.
2. Bauer C, Osman AM, Cercignani G, Gialluca N, Paolini M. 2001. A unified theory of enzyme kinetics based upon the systematic analysis of the variations of k(cat), K(M), and k(cat)/K(M) and the relevant DeltaG(0 not equal) values-possible implications in chemotherapy and biotechnology Biochem. Pharmacol. 61:1049-1055.
3. 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.
4. Bieleski L, Hindley C, Talbot SJ. 2004. A polypyrimidine tract facilitates the expression of Kaposi's sarcoma-associated herpesvirus vFLIP through an internal ribosome entry site J. Gen. Virol. 85:615-620.
5. Bieleski L, Talbot SJ. 2001. Kaposi's sarcoma-associated herpesvirus vcyclin open reading frame contains an internal ribosome entry site J. Virol. 75:1864-1869.
6. Bu W, Carroll KD, Palmeri D, Lukac DM. 2007. Kaposi's sarcomaassociated herpesvirus/human herpesvirus 8 ORF50/Rta lytic switch protein functions as a tetramer J. Virol. 81:5788-5806.
7. Budt M, Hristozova T, Hille G, Berger K, Brune W. 2011. Construction of a lytically replicating Kaposi's sarcoma-associated herpesvirus J. Virol. 85:10415-10420.
8. Cai X, Cullen BR. 2006. Transcriptional origin of Kaposi's sarcomaassociated herpesvirus microRNAs J. Virol. 80:2234-2242.
9. Carroll KD, et al. 2006. Kaposi's sarcoma-associated herpesvirus lytic switch protein stimulates DNA binding of RBP-Jk/CSL to activate the Notch pathway J. Virol. 80:9697-9709.
10. Cave JW, Loh F, Surpris JW, Xia L, Caudy MA. 2005. A DNA transcription code for cell-specific gene activation by notch signaling Curr. Biol. 15:94-104.
11. Chang H, Dittmer DP, Shin YC, Hong Y, Jung JU. 2005. Role of Notch signal transduction in Kaposi's sarcoma-associated herpesvirus gene expression J. Virol. 79:14371-14382.
12. Chang PJ, Boonsiri J, Wang SS, Chen LY, Miller G. 2010. Binding of RBP-Jkappa (CSL) protein to the promoter of the Kaposi's sarcomaassociated herpesvirus ORF47 (gL) gene is a critical but not sufficient determinant of transactivation by ORF50 protein Virology 398:38-48.
13. Chang PJ, Miller G. 2004. Autoregulation of DNA binding and protein stability of Kaposi's sarcoma-associated herpesvirus ORF50 protein J. Virol. 78:10657-10673.
14. Chang PJ, Shedd D, Miller G. 2008. A mobile functional region of Kaposi's sarcoma-associated herpesvirus ORF50 protein independently regulates DNA binding and protein abundance J. Virol. 82:9700-9716.
15. Chang PJ, Shedd D, Miller G. 2005. Two subclasses of Kaposi's sarcomaassociated herpesvirus lytic cycle promoters distinguished by open reading frame 50 mutant proteins that are deficient in binding to DNA J. Virol. 79:8750-8763.
16. Chen J, et al. 2001. Activation of latent Kaposi's sarcoma-associated herpesvirus by demethylation of the promoter of the lytic transactivator Proc. Natl. Acad. Sci. U. S. A. 98:4119-4124.
17. Chen J, Ye F, Xie J, Kuhne K, Gao SJ. 2009. Genome-wide identification of binding sites for Kaposi's sarcoma-associated herpesvirus lytic switch protein, RTA Virology 386:290-302.
18. Chiou CJ, et al. 2002. Patterns of gene expression and a transactivation function exhibited by the vGCR (ORF74) chemokine receptor protein of Kaposi's sarcoma-associated herpesvirus J. Virol. 76:3421-3439.
19. Chow CC, Ong KM, Dougherty EJ, Simons Simons Jr SS, 2011. Inferring mechanisms from dose-response curves Methods Enzymol. 487:465-483.
20. Damania B, et al. 2004. Comparison of the Rta/Orf50 transactivator proteins of gamma-2-herpesviruses J. Virol. 78:5491-5499.
21. Dittmer D, et al. 1998. A cluster of latently expressed genes in Kaposi's sarcoma-associated herpesvirus J. Virol. 72:8309-8315.
22. Dittmer DP. 2003. Transcription profile of Kaposi's sarcoma-associated herpesvirus in primary Kaposi's sarcoma lesions as determined by realtime PCR arrays Cancer Res. 63:2010-2015.
23. Fakhari FD, Jeong JH, Kanan Y, Dittmer DP. 2006. The atencyassociated nuclear antigen of Kaposi sarcoma-associated herpesvirus induces B cell hyperplasia and lymphoma J. Clin. Invest. 116:735-742.
24. Ganem D. 2010. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine J. Clin. Invest. 120:939-949.
25. Garrett R, Grisham CM. 2010. Biochemistry, 4th ed. Brooks/Cole, Cengage Learning, Belmont, CA.
26. Godfrey A, Anderson J, Papanastasiou A, Takeuchi Y, Boshoff C. 2005. Inhibiting primary effusion lymphoma by lentiviral vectors encoding short hairpin RNA Blood 105:2510-2518.
27. Gunther T, Grundhoff A. 2010. The epigenetic landscape of latent Kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog. 6:e1000935. doi:10.1371/journal.ppat.1000935.
28. Gwack Y, Byun H, Hwang S, Lim C, Choe J. 2001. CREB-binding protein and histone deacetylase regulate the transcriptional activity of Kaposi's sarcoma-associated herpesvirus open reading frame 50 J. Virol. 75:1909-1917.
29. Herndier BG, et al. 1994. Characterization of a human Kaposi's sarcoma cell line that induces angiogenic tumors in animals AIDS 8:575-581.
30. Hsieh JJ, et al. 1996. Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2 Mol. Cell. Biol. 16:952-959.
31. Jenner RG, Alba MM, Boshoff C, Kellam P. 2001. Kaposi's sarcomaassociated herpesvirus latent and lytic gene expression as revealed byDNA arrays J. Virol. 75:891-902.
32. Jeong J, Papin J, Dittmer D. 2001. Differential regulation of the overlapping Kaposi's sarcoma-associated herpesvirus vGCR (orf74) and LANA (orf73) promoters J. Virol. 75:1798-1807.
33. Jeong JH, Hines-Boykin R, Ash JD, Dittmer DP. 2002. Tissue specificity of the Kaposi's sarcoma-associated herpesvirus latent nuclear antigen (LANA/orf73) promoter in transgenic mice J. Virol. 76:11024-11032.
34. Jeong JH, et al. 2004. Regulation and autoregulation of the promoter for the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus J. Biol. Chem. 279:16822-16831.
35. Jimenez-Ramirez C, et al. 2006. Epstein-Barr virus EBNA-3C is targeted to and regulates expression from the bidirectional LMP-1/2B promoter J. Virol. 80:11200-11208.
36. Jin Y, et al. 2012. Carboxyl-terminal amino acids 1052 to 1082 of the latency-associated nuclear antigen (LANA) interact with RBP-Jkappa and are responsible for LANA-mediated RTA repression J. Virol. 86:4956-4969.
37. Kang H, Lieberman PM. 2009. Cell cycle control of Kaposi's sarcomaassociated herpesvirus latency transcription by CTCF-cohesin interactions J. Virol. 83:6199-6210.
38. Kemmer G, Keller S. 2010. Nonlinear least-squares data fitting in Excel spreadsheets Nat. Protoc. 5:267-281.
39. Kim HD, O'Shea EK. 2008. A quantitative model of transcription factoractivated gene expression Nat. Struct. Mol. Biol. 15:1192-1198.
40. Kim HD, Shay T, O'Shea EK, Regev A. 2009. Transcriptional regulatory circuits: predicting numbers from alphabets Science 325:429-432.
41. Kirshner JR, Staskus K, Haase A, Lagunoff M, Ganem D. 1999. Expression of the open reading frame 74 (G-protein-coupled receptor) gene of Kaposi's sarcoma (KS)-associated herpesvirus: implications for KS pathogenesis J. Virol. 73:6006-6014.
42. Kovall RA, Blacklow SC. 2010. Mechanistic insights into Notch receptor signaling from structural and biochemical studies Curr. Top. Dev. Biol. 92:31-71.
43. 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.
44. Kuhlman T, Zhang Z, Saier Jr MH, Hwa T. 2007. Combinatorial transcriptional control of the lactose operon of Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 104:6043-6048.
45. Lan K, Kuppers DA, Verma SC, Robertson ES. 2004. Kaposi's sarcomaassociated herpesvirus-encoded latency-associated nuclear antigen inhibits lytic replication by targeting Rta: a potential mechanism for virusmediated control of latency J. Virol. 78:6585-6594.
46. Lan K, 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.
47. Laux G, Economou A, Farrell PJ. 1989. The terminal protein gene 2 of Epstein-Barr virus is transcribed from a bidirectional latent promoter region J. Gen. Virol. 70:3079-3084.
48. Li H, Komatsu T, Dezube BJ, Kaye KM. 2002. The Kaposi's sarcomaassociated herpesvirus K12 transcript from a primary effusion lymphoma contains complex repeat elements, is spliced, and initiates from a novel promoter J. Virol. 76:11880-11888.
49. Li Q, Zhou F, Ye F, Gao SJ. 2008. Genetic disruption of KSHV major latent nuclear antigen LANA enhances viral lytic transcriptional program Virology 379:234-244.
50. Li YY, et al. 2006. Systematic analysis of head-to-head gene organization: evolutionary conservation and potential biological relevance. PLoS Comput. Biol. 2:e74. doi:10.1371/journal.pcbi.0020074.
51. Liang Y, Chang J, Lynch SJ, Lukac DM, Ganem D. 2002. The lytic switch protein of KSHV activates gene expression via functional interaction with RBP-Jkappa (CSL), the target of the Notch signaling pathway Genes Dev. 16:1977-1989.
52. 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.
53. Lu F, Day L, Gao SJ, Lieberman PM. 2006. Acetylation of the latencyassociated nuclear antigen regulates repression of Kaposi's sarcomaassociated herpesvirus lytic transcription J. Virol. 80:5273-5282.
54. Lu J, Verma SC, Cai Q, Robertson ES. 2011. The single RBP-Jkappa site within the LANA promoter is crucial for establishing Kaposi's sarcomaassociated herpesvirus latency during primary infection J. Virol. 85:6148-6161.
55. Lukac DM, Kirshner JR, 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.
56. 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.
57. Matsumura S, Fujita Y, Gomez E, Tanese N, Wilson AC. 2005. Activation of the Kaposi's sarcoma-associated herpesvirus major latency locus by the lytic switch protein RTA (ORF50) J. Virol. 79:8493-8505.
58. Miele L. 2011. Transcription factor RBPJ/CSL: a genome-wide look at transcriptional regulation Proc. Natl. Acad. Sci. U. S. A. 108:14715-14716.
59. Moorman NJ, Willer DO, Speck SH. 2003. The gammaherpesvirus 68 latency-associated nuclear antigen homolog is critical for the establishment of splenic latency J. Virol. 77:10295-10303.
60. Nador RG, et al. 2001. Expression of Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor monocistronic and bicistronic transcripts in primary effusion lymphomas Virology 287:62-70.
61. Nakamura H, et al. 2003. Global changes in Kaposi's sarcoma-ssociated virus gene expression patterns following expression of a tetracyclineinducible Rta transactivator J. Virol. 77:4205-4220.
62. Neil H, et al. 2009. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast Nature 457:1038-1042.
63. Ong CT, et al. 2006. Target selectivity of vertebrate notch proteins Collaboration between discrete domains and CSL-binding site architecture determines activation probability. J. Biol. Chem. 281:5106-5119.
64. Ong KM, Blackford JA, Jr, Kagan BL, Simons SS, Jr, Chow CC. 2010. A theoretical framework for gene induction and experimental comparisons Proc. Natl. Acad. Sci. U. S. A. 107:7107-7112.
65. Palmeri D, Carroll KD, Gonzalez-Lopez O, Lukac DM. 2011. Kaposi's sarcoma-associated herpesvirus Rta tetramers make high-affinity interactions with repetitive DNA elements in the Mta promoter to stimulate DNA binding of RBP-Jk/CSL J. Virol. 85:11901-11915.
66. Pantry SN, Medveczky PG. 2009. Epigenetic regulation of Kaposi's sarcoma-associated herpesvirus replication Semin. Cancer Biol. 19:153-157.
67. Pearce M, Matsumura S, Wilson AC. 2005. Transcripts encoding K12, v-FLIP, v-cyclin, and the microRNA cluster of Kaposi's sarcomaassociated herpesvirus originate from a common promoter J. Virol. 79:14457-14464.
68. Persson LM, Wilson AC. 2010. Wide-scale use of Notch signaling factor CSL/RBP-Jkappa in RTA-mediated activation of Kaposi's sarcomaassociated herpesvirus lytic genes J. Virol. 84:1334-1347.
69. Rosenfeld N, Young JW, Alon U, Swain PS, Elowitz MB. 2005. Gene regulation at the single-cell level Science 307:1962-1965.
70. Russo JJ, et al. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8) Proc. Natl. Acad. Sci. U. S. A. 93:14862-14867.
71. 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.
72. Sin SH, Fakhari FD, Dittmer DP. 2010. The viral latency-associated nuclear antigen augments the B-cell response to antigen in vivo J. Virol. 84:10653-10660.
73. 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.
74. 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.
75. Staudt MR, Dittmer DP. 2006. Promoter switching allows simultaneous transcription of LANA and K14/vGPCR of Kaposi's sarcoma-associated herpesvirus Virology 350:192-205.
76. Stedman W, et al. 2008. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators EMBO J. 27:654-666.
77. Sun R, et al. 1998. A viral gene that activates lytic cycle expression of Kaposi's sarcoma-associated herpesvirus Proc. Natl. Acad. Sci. U. S. A. 95:10866-10871.
78. Talbot SJ, Weiss RA, Kellam P, Boshoff C. 1999. Transcriptional analysis of human herpesvirus-8 open reading frames 71, 72, 73, K14, and 74 in a primary effusion lymphoma cell line Virology 257:84-94.
79. Toth Z, et al. 2010. Epigenetic analysis of KSHV latent and lytic genomes. PLoS Pathog. 6:e1001013. doi:10.1371/journal.ppat.1001013.
80. Trinklein ND, et al. 2004. An abundance of bidirectional promoters in the human genome Genome Res. 14:62-66.
81. Wei W, Pelechano V, Jarvelin AI, Steinmetz LM. 2011. Functional consequences of bidirectional promoters Trends Genet. 27:267-276.
82. Wen KW, Damania B. 2010. Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis Cancer Lett. 289:140-150.
83. Wen KW, Dittmer DP, Damania B. 2009. Disruption of LANA in rhesus rhadinovirus generates a highly lytic recombinant virus J. Virol. 83:9786-9802.
84. Xu Y, et al. 2005. A Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 ORF50 deletion mutant is defective for reactivation of latent virus and DNA replication J. Virol. 79:3479-3487.