K13 blocks KSHV lytic replication and deregulates vIL6 nad hIL6 expression: A model of lytic replication induced clonal selection in viral oncogenesis

PLoS ONE

Volumn 2, Issue 10, 2007, Pages

  Zhao, Jinshun ^a   Punj, Vasu ^a   Matta, Hittu ^a   Mazzacurati, Lucia ^a   Schamus, Sandra ^a   Yang, Yanqiang ^a   Yang, Tianbing ^b   Hong, Yan ^a   Chaudhary, Preet M ^a  

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

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HYDROLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR K13; UNCLASSIFIED DRUG; IMMEDIATE EARLY PROTEIN; VIRUS PROTEIN;

ARTICLE; CARCINOGENESIS; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CLONAL VARIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; KAPOSI SARCOMA; MOLECULAR CLONING; NONHUMAN; PROTEIN EXPRESSION; VIRION; VIRUS REACTIVATION; VIRUS REPLICATION; CELL LINE; CHEMISTRY; DNA REPLICATION; GENE EXPRESSION PROFILING; METABOLISM; NEOPLASM; VIROLOGY; VIRUS GENE;

HUMAN HERPESVIRUS 8;

CELL LINE; DNA REPLICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE EXPRESSION REGULATION, VIRAL; GENE SILENCING; GENES, VIRAL; HERPESVIRUS 8, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERLEUKIN-6; NEOPLASMS; RNA, SMALL INTERFERING; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 42449155531     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001067     Document Type: Article

References (75)

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. Science 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. 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.
4. Nicholas J (2007) Human herpesvirus 8-encoded Proteins with potential roles in virus-associated neoplasia. Front Biosci 12: 265-281.
5. Montaner S, Sodhi A, Molinolo A, Bugge TH, Sawai ET, et al. (2003) Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3: 23-36.
6. Sodhi A, Montaner S, Gutkind JS (2004) Does dysregulated expression of a deregulated viral GPCR trigger Kaposi's sarcomagenesis? Faseb J 18: 422-427.
7. Grisotto MG, Garin A, Martin AP, Jensen KK, Chan P, et al. (2006) The human herpesvirus 8 chemokine receptor vGPCR triggers autonomous proliferation of endothelial cells. J Clin Invest 116: 1264-1273.
8. Moore PS, Boshoff C, Weiss RA, Chang Y (1996) Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274: 739 1744.
9. Nicholas J, Ruvolo VR, Burns WH, Sandford G, Wan X, et al. (1997) Kaposi's sarcoma-associated human herpesvirus-8 encodes homologucs of macrophage inflammatory protein-1 and interleukin-6. Nat Med 3: 287-292.
10. Aoki Y, Jones KD, Tosato G (2000) Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6. J Hematother Stem Cell Res 9: 137-145.
11. Paulose-Murphy M, Ha NK, Xiang C, Chen Y, Gillim L, et al. (2001) Transcription program of human herpesvirus 8 (kaposi's sarcoma-associated herpesvirus). J Virol 75: 4843-4853.
12. Jenner RG, Alba 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.
13. Deng H, Chu JT, Rettig MB, Martinez-Maza O, Sun R (2002) Rta of the human herpesvirus 8/Kaposi sarcoma-associated herpesvirus up-regulates human interleukin-6 gene expression. Blood 100: 1919-1921.,
14. Miles SA, Rezai AR, Salazar-Gonzalez JF, Vander Meyden M, Stevens RH, et al. (1990) AIDS Kaposi sarcoma-derived cells produce and respond to interleukin 6. Proc Natl Acad Sci U S A 87: 4068-4072.
15. Burger R, Wendler J, Antoni K, Helm G, Kalden JR, et al. (1994) Interleukin-6 production in B-cell neoplasias and Castleman's disease: evidence, for an additional paracrine loop. Ann Hematol 69: 25-31.
16. Chatterjee M, Osborne J, Bestetti G, Chang Y, Moore PS (2002) Viral IL-6 induced cell proliferation and immune evasion of interferon activity. Science 298: 1432-1435.
17. Jones KD, Aoki Y, Chang Y, Moore PS, Yarchoan R, et al. (1999) Involvement of interleukiq-10 (IL-10) and viral IL-6 in the spontaneous growth of Kaposi's sarcoma herpesvirus-associated infected primary effusion lymphoma cells. Blood 94: 2871-2879.
18. Aoki Y, Jaffe ES, Chang Y, Jones K, Teruya-Feldstein J, et al. (1999) Angiogenesis,and hematopoiesis induced by Kaposi's sarcoma-associated herpesvirus-encoded interleukin-6. Blood 93: 4034-4043.
19. Foussat A, Wijdenes J, Bouchet I, Gaidano G, Neipel F, et al. (1999) Human interleukin-6 is in vivo an autocrine growth factor for human herpesvirus-8-infected malignant B lymphocytes. Eur Cytokine Netw 10: 501-508.
20. Liu C, Okruzhnov Y, Li H, Nicholas J (2001) Human herpesvirus 8 (HHV-8)-encoded cytokines induce expression of and autocrine signaling by vascular endothelial growth factor (VEGF) in HHV-8-infected primary-effusion lymphoma cell lines and mediate VEGF-independent antiapoptotic effects. J Virol 75: 10933-10940.
21. Cohen T, Nahari D, Cerem, LW, Neufeld G, Levi B-Z (1996) Interleukin 6 Induces the Expression of Vascular Endothelial Growth Factor. pp 736-741.
22. Molden J, Chang Y, You Y, Moore PS, Goldsmith MA (1997) A Kaposi's sarcoma-associated herpesvirus-encoded cytokine homolog (vIL-6) activates signaling through the shared gp130 receptor subunit. J Biol Chem 272: 19625-19631.
23. Li H, Nicholas J (2002) Identification of amino acid residues of gp130 signal transducer and gp80 alpha receptor subunit that are involved in ligand binding and signaling by human herpesvirus 8-encoded interleukin-6. J Virol 76: 5627-5636.
24. Parravicini C, Chandran B, Corbellino M, Berti E, Paulli M, et al. (2000) Differential viral protein expression in Kaposi's sarcoma-associated herpesvirus-infected diseases: Kaposi's sarcoma, primary effusion lymphoma, and multicentric Castleman's disease. Am J Pathol 156: 743-749.
25. Schulz TF (2006) The pleiotropic effects of Kaposi's sarcoma herpesvirus. J Pathol 208: 187-198.
26. Staskus KA, Sun R, Miller G, Racz P, Jaslowski A, et al. (1999) Cellular tropism and viral interleukin-6 expression distinguish human herpesvirus 8 involvement in Kaposi's sarcoma, primary effusion lymphoma and multicentric Castkeman's disease. J Virol 73: 4181-4187.
27. Cannon JS, Nicholas J, Orenstein JM, Mann RB, Murray PG, et al. (1999) Heterogeneity ofviral IL-6 expression in HHV-8-asssociated diseases. J Infect Dis 180: 824-828.
28. Brousset P, Cesarman E, Meggetto F, Lamant L, Delsol G (2001) Colocalization of the viral interleukin-6 with latent nuclear antigen-1 of human herpesvirus-8 in endothelial spindle cells of Kaposi's Sarcoma and lymphoid cells of multicentric Castleman's disease. Hum Pathol 32: 95-100.
29. Sturzl M, Hohenadl C, Zietz C, Castanos-Velez E, Wunderlich A, et al. (1999) Expression of K13/v-FLIP gene of human herpesvirus 8 and apoptosis in Kaposi's sarcoma spindle cells. J Natl Cancer Inst 91: 1725-1733.
30. 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.
31. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, et al. (1997) Vital FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386: 517-521.
32. Chugh P, Matta H, Schamus S, Zachariah S, Kumar A, et al. (2005) Constitutive NF-kappaB activation, normal Fas-induced apoptosis, and increased incidence of lymphoma in human herpes virus 8 K13 transgenic mice. Proc Natl Acad Sci U S A 102: 12885-12890.
33. Field N, Low W, Daniels. M, Howell S, Daviet L, et al. (2003) KSHV vFLIP binds to IKK{garnma} to activate IKK. J Cell Sci 116: 3721-3728.
34. Chaudhary PM, Jasmin A, Eby W, Hood L (1999) Modulation of the NF-kappa B pathway by vitally encoded death effector domains-containing proteins. Oncogene 18: 5738-5746.
35. Liu L, Eby MT, Rathore N, Sinha SK, Kumar A, et al. (2002) The Human Herpes Virus 8-encoded Viral FLICE Inhibitory Protein Physically Associates with and Persistently Activates the Ikappa B Kinase Complex. J Biol Chem 277: 13745-13751.
36. Sun Q, Matta H, Chaudhary PM (2003) The human herpes virus 8-encoded viral RICE inhibitory protein protects against growth factor withdrawal-induced apoptosis via NF-kappa B activation. Blood 101: 1956-1961.
37. Sun Q, Zachariah S, Chaudhary PM (2003) The human herpes virus 8-encoded viral FLICE-inhibitory, protein induces cellular transformation via NF-kappaB activation. Journal of Biological Chemistry 278: 52437-52445.
38. Sun Q, Matta H, Lu G, Chaudhary PM (2006) Induction of IL-8 expression by human herpesvirus 8 encoded vFLIP K13 via NF-kappaB activation. Oncogene 25: 2717-2726.
39. An J, Sun Y, Sun R, Rettig MB (2003) Kaposi's sarcoma-associated herpesvirus encoded vFLIP induces cellular IL-6 expression the role of the NF-kappaB and JNK/API pathways. Oncogene 22: 3371-3385.
40. Guasparri I, Keller SA, Cesarman E (2004) KSHV vFLIP is essential for the survival of infected lymphoma cells. J Exp Med 199: 993-1003.
41. Renne R, Zhong W, Herndier B, McGrath M, Abbey N, et al. (1996) Lytic growth of Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in culture. Nat Med 2: 342-346.
42. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, et al. (2003) Global changes in Kaposi's sarcoma-associated virus gone expression patterns following expression of a tetracycline-inducible Rta transactivator. J Virot 77: 4205-4220.
43. Picard D (2000) Posttranslational regulation of proteins by fusions to steroid-binding domains. Methods Enzymol 327: 385-401.
44. Matta H, Surabhi RM, Zhao J, Punj V, Sun Q, et al. (2007) Induction of spindle cell morphology in human vascular endothelial cells by human heipesvirus 8-encoded viral-FLICE inhibitory protein K13. Oncogene 26: 1656-1660.
45. Krishnan HH, Naranatt PP, Smith MS, Zeng L, Bloomer C, 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 prmiary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J Virol 78: 3601-3620.
46. Inoue N, Winter J, Lal RB, Offermann Mk, Noyano S (2003) Characterization of entry mechanisms of human herpesvirus 8 by using an Rta-dependent reporter cell line. J Virol 77: 8147-8152.
47. 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.
48. 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.
49. Sun R, Lin SF, Gradoville L, Yuan Y, Zhu F, 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.
50. Brown HJ, Song MJ, Deng H, Wu T-T, Cheng G, et al, (2003) NF-(kappa)B Inhibits Gammnaherpesvirus Lytic Replication. J Virol 77: 8532-8540.
51. Hibi M, Murakami M, Saito M, Hirano T, Taga T, et al. (1990) Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell 63: 1149-1157.
52. Lan K, Kuppers DA, Verma SC, Robertson ES (2004) Kaposi's sarcoma-associated herpesvirus-encoded latency-associated nuclear antigen inhibits lytic replication by targeting Rta: a potential mechanism for virus-mediated control of latency. J Virol 78: 6585-6594.
53. Lee BS, Paulose-Murphy M, Chung YH, Connlole M, Zeichner S, et al. (2002) Suppression of tetradecanoy phorbol acetate-induced lytic reactivation of Kaposi's sarcoma-associated herpesvirus by K1 signal transduction. J Virol 76: 12185-12199.
54. Cannon V, Cesarman E, Boshoff C (2006) KSHV G protein-coupled receptor inhibits lytic gene transcription in primary-effusion lymphoma cells via p21-mediated inhibition of Cdk2. Blood 107: 277-284.
55. Lukac DM, Garibyan L, Kirshner JR, Palmeri D, Ganem D (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.
56. 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.
57. Chang PJ, Sheild D, Gradoville L, Cho MS, Chen LW, et al. (2002) Open reading frame 50 protein of Kaposi's sarcoma-associated herpesvirus directly activates the viral PAN and K12 genes by binding to related reoponse elements J Virol 76: 3168-3178.
58. Song MJ, Deng H, Sim R (2003) Comparative study of regulation of RTA-responsive genes in Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8. J Virol 77: 9451-9462.
59. Grossmann C, Podgrabinska S, Skobe M, Ganem D (2006) Activation of NF-kappaB by the latent vFLIP gene of Kaposi's sarcoma-associated herpesvirus is required for the spindle shape of virus-infected endothelial cells and contributes to their proinflammatory phenotype. J Virol 80: 7179-7185.
60. Ensoli B, Gallo RC (1995) AIDS-associated Kaposi's sarcoma: a new perspective of its pathogenesis and treatment. Proc Assoc Am Physicians 107: 8-18.
61. Grundhoff A, Ganem D (2001) Mechanisms governing expression of the v-FLIP gene of Kaposi's sarcoma-associated herpesvirus. J Virol 75: 1857-1863.
62. Ganem D (2006) KSHV infection and the pathogenesis of Kaposi's sarcoma. Annual Review of Pathology-Mechanisms of Disease 1: 273-296.
63. Grundhoff A, Ganem D (2004) Inefficient establishment of KSHV latency suggests an additional role for continued lytic replication in Kaposi sarcoma pathogenesis. J Clin Invest 113: 124-136.
64. Kaaya EE, Parravicini C, Sundelin B, Mgaya E, Kitinya J, et al. (1992) Spindle cell ploidy and proliferation in endemic and epidemic African Kaposi's sarcoma. Eur J Cancer 28A: 1890-1894.
65. Wabinga HR Parkin DM, Wabwire-Mangen F, Mugerwa JW (1993) Cancar in Kampala, Uganda, in 1989-91: changes in incidence in the era of AIDS. Int J Cancer 54: 26-36.
66. Qunibi W, Al-Furayh O, Almeshari K, Lin SF, Sun R, et al. (1998) Serologic association of human herpesvirus eight with posttransplant Kaposi's sarcoma in Saudi Arabia. Transplantation 65: 583-585.
67. Hayward GS (2003) Initiation of angiogenic Kaposi's sarcoma lesions. Cancer Cell 3: 1-3.
68. Andreoni M, Goletti D, Pezzotti P, Pozzetto A, Monini P, et al. (2001) Prevalence, incidence and correlates of HHV-8/KSHV infection and Kaposi's sarcoma in renal and liver transplant recipients. J Infect 43: 195-199.
69. Sirianni MC, Vincenzi L, Topino S, Giovannetti A, Mazzetta F, et al. (2002 NK cell activity controls human herpesvirus 8 latent infection and is restored upon highly active antiretroviral therapy in AIDS patients with regressing Kaposi's sarcoma. Eur J Immunol 32: 2711-2720.
70. Jenkins FJ, Hoffman LJ, Liegey-Dougall A (2002) Reactivation of and primary infection with human herpesvirus 8 among solid-organ transplant recipients. J Infect Dis 185: 1238-1243.
71. Lam KM, Syed N, Whittle H, Crawford DH (1991) Circulating Epstein-Barr virus-carrying B cells in acute malaria. Lancet. 337: 876-878.
72. Babcock GJ, Decker LL, Freeman RB, Thorley-Lawson DA (1999) Epstein-barr virus-infected resting memory B cells, not proliferating lymphoblasts, accumulate in the peripheral blood of immunosuppressed patients. J Exp Med 190: 567-576.
73. Evan G, Littlewood T (1998) A matter of life and cell death. Science 281: 1317-1322.
74. Evan GI, Vousden KH (2001) Proliferation, cell cycle and apoptosis in cancer. Nature 411: 342-348.
75. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-title quantitative PCR and the 2(- Delta Delta CM) Method. Methods 25: 402-408.