A role for virally induced reactive oxygen species in kaposi's sarcoma herpesvirus tumorigenesis

Antioxidants and Redox Signaling

Volumn 18, Issue 1, 2013, Pages 80-90

  Ma, Qi ^a   Cavallin, Lucas E ^a   Leung, Howard J ^a   Chiozzini, Chiara ^b   Goldschmidt Clermont, Pascal J ^a   Mesri, Enrique A ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CYCLIN D1; G PROTEIN COUPLED RECEPTOR; MYC PROTEIN; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STAT3 PROTEIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; KAPOSI SARCOMA; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SARCOMAGENESIS; SPINDLE CELL; TUMOR GROWTH; VIRUS CARCINOGENESIS;

ACETYLCYSTEINE; ANGIOGENESIS INHIBITORS; ANIMALS; ANTIVIRAL AGENTS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; FREE RADICAL SCAVENGERS; GENE EXPRESSION; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; NEUROPEPTIDES; OXIDATIVE STRESS; RAC GTP-BINDING PROTEINS; REACTIVE OXYGEN SPECIES; RECEPTORS, G-PROTEIN-COUPLED; SARCOMA, KAPOSI; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

ANIMALIA; HERPESVIRIDAE; HUMAN HERPESVIRUS 8;

EID: 84870493180     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4584     Document Type: Article

References (50)

1. Agarwal A, Munoz-Najar U, Klueh U, Shih SC, and Claffey KP. N-acetyl-cysteine promotes angiostatin production and vascular collapse in an orthotopic model of breast cancer. Am J Pathol 164: 1683-1696, 2004.
2. Akira S, Nishio Y, Inoue M, Wang XJ, Wei S, Matsusaka T, Yoshida K, Sudo T, Naruto M, and Kishimoto T. Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell 77: 63-71, 1994.
3. Albini A, Morini M, D'Agostini F, Ferrari N, Campelli F, Arena G, Noonan DM, Pesce C, and De Flora S. Inhibition of angiogenesis-driven Kaposi's sarcoma tumor growth in nude mice by oral N-acetylcysteine. Cancer Res 61: 8171-8178, 2001.
4. Aoki Y, Feldman GM, and Tosato G. Inhibition of STAT3 signaling induces apoptosis and decreases survivin expression in primary effusion lymphoma. Blood 101: 1535-1542, 2003.
5. Atkuri KR, Mantovani JJ, Herzenberg LA, and Herzenberg LA. N-acetylcysteine\a safe antidote for cysteine/glutathi-one deficiency. Curr Opin Pharmacol 7: 355-359, 2007.
6. Bais C, Santomasso B, Coso O, Arvanitakis L, Raaka EG, Gutkind JS, Asch AS, Cesarman E, Gershengorn MC, and Mesri EA. G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391: 86-89, 1998.
7. Bedard K and Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007.
8. Cesarman E, Mesri EA, and Gershengorn MC. Viral G protein-coupled receptor and Kaposi's sarcoma: a model of paracrine neoplasia? J Exp Med 191: 417-422, 2000.
9. Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM, and Moore PS. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869, 1994.
10. Chung AS and Ferrara N. Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol 27: 563-584, 2011.
11. De Rosa SC, Zaretsky MD, Dubs JG, Roederer M, Anderson M, Green A, Mitra D, Watanabe N, Nakamura H, Tjioe I, Deresinski SC, Moore WA, Ela SW, Parks D, Herzenberg LA, and Herzenberg LA. N-acetylcysteine replenishes glu-tathione in HIV infection. Eur J Clin Invest 30: 915-929, 2000.
12. Dittmer DP and Krown SE. Targeted therapy for Kaposi's sarcoma and Kaposi's sarcoma-associated herpesvirus. Curr Opin Oncol 19: 452-457, 2007.
13. Gallo RC. The enigmas of Kaposi's sarcoma. Science 282: 1837-1839, 1998.
14. Ganem D. KSHV infection and the pathogenesis of Kaposi's sarcoma. Annu Rev Pathol 1: 273-296, 2006.
15. Ganem D. KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J Clin Invest 120: 939-949, 2010.
16. Gao P, Zhang H, Dinavahi R, Li F, Xiang Y, Raman V, Bhujwalla ZM, Felsher DW, Cheng L, Pevsner J, Lee LA, Semenza GL, and Dang CV. HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell 12: 230-238, 2007.
17. Herzenberg LA, De Rosa SC, Dubs JG, Roederer M, Anderson MT, Ela SW, Deresinski SC, and Herzenberg LA. Glutathione deficiency is associated with impaired survival in HIV disease. Proc Natl Acad Sci USA 94: 1967-1972, 1997.
18. Hussain SP, Hofseth LJ, and Harris CC. Radical causes of cancer. Nat Rev Cancer 3: 276-285, 2003.
19. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, and Goldschmidt-Clermont PJ. Mi-togenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652, 1997.
20. Kirshner JR, Staskus K, Haase A, Lagunoff M, and Ganem D. 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, 1999.
21. Koon HB, Bubley GJ, Pantanowitz L, Masiello D, Smith B, Crosby K, Proper J, Weeden W, Miller TE, Chatis P, Egorin MJ, Tahan SR, and Dezube BJ. Imatinib-induced regression of AIDS-related Kaposi's sarcoma. J Clin Oncol 23: 982-989, 2005.
22. Krown SE. Therapy of AIDS-associated Kaposi's sarcoma: targeting pathogenetic mechanisms. Hematol Oncol Clin North Am 17: 763-783, 2003.
23. Li X, Feng J, and Sun R. Oxidative stress induces reactivation of Kaposi's sarcoma-associated herpesvirus and death of primary effusion lymphoma cells. J Virol 85: 715-724, 2011.
24. Ma Q, Cavallin LE, Yan B, Zhu S, Duran EM, Wang H, Hale LP, Dong C, Cesarman E, Mesri EA, and Goldschmidt-Clermont PJ. Antitumorigenesis of antioxidants in a trans-genic Rac1 model of Kaposi's sarcoma. Proc Natl Acad Sci USA 106: 8683-8688, 2009.
25. Menon SG, Sarsour EH, Kalen AL, Venkataraman S, Hitch-ler MJ, Domann FE, Oberley LW, and Goswami PC. Su-peroxide signaling mediates N-acetyl-L-cysteine- induced G1 arrest: regulatory role of cyclin D1 and manganese super-oxide dismutase. Cancer Res 67: 6392-6399, 2007.
26. Mesri EA, Cesarman E, and Boshoff C. Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 10: 707-719, 2010.
27. Montaner S, Sodhi A, Molinolo A, Bugge TH, Sawai ET, He Y, Li Y, Ray PE, and Gutkind JS. 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, 2003.
28. Montaner S, Sodhi A, Ramsdell AK, Martin D, Hu J, Sawai ET, and Gutkind JS. The Kaposi's sarcoma-associated her-pesvirus G protein-coupled receptor as a therapeutic target for the treatment of Kaposi's sarcoma. Cancer Res 66: 168-174, 2006.
29. Montaner S, Sodhi A, Servitja JM, Ramsdell AK, Barac A, Sawai ET, and Gutkind JS. The small GTPase Rac1 links the Kaposi sarcoma-associated herpesvirus vGPCR to cyto-kine secretion and paracrine neoplasia. Blood 104: 2903-2911, 2004.
30. Mutlu AD, Cavallin LE, Vincent L, Chiozzini C, Eroles P, Duran EM, Asgari Z, Hooper AT, La Perle KM, Hilsher C, Gao SJ, Dittmer DP, Rafii S, and Mesri EA. In vivo-restricted and reversible malignancy induced by human herpesvirus-8 KSHV: a cell and animal model of virally induced Kaposi's sarcoma. Cancer Cell 11: 245-258, 2007.
31. Myoung J and Ganem D. Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: maintenance of tight latency with efficient reactivation upon induction. J Virol Methods 174: 12-21, 2011.
32. Nguyen HQ, Magaret AS, Kitahata MM, Van Rompaey SE, Wald A, and Casper C. Persistent Kaposi sarcoma in the era of highly active antiretroviral therapy: characterizing the predictors of clinical response. Aids 22: 937-945, 2008.
33. Owusu-Ansah E, Yavari A, Mandal S, and Banerjee U. Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat Genet 40: 356-361, 2008.
34. Punjabi AS, Carroll PA, Chen L, and Lagunoff M. Persistent activation of STAT3 by latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells. J Virol 81: 2449-2458, 2007.
35. Reiner A, Yekutieli D, and Benjamini Y. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368-375, 2003.
36. Roederer M, Staal FJ, Raju PA, Ela SW, Herzenberg LA, and Herzenberg LA. Cytokine-stimulated human immunodeficiency virus replication is inhibited by N-acetyl-L-cysteine. Proc Natl Acad Sci USA 87: 4884-4888, 1990.
37. Safai B, Johnson KG, Myskowski PL, Koziner B, Yang SY, Cunningham-Rundles S, Godbold JH, and Dupont B. The natural history of Kaposi's sarcoma in the acquired immunodeficiency syndrome. Ann Intern Med 103: 744-750, 1985.
38. Sarrazin S, Adam E, Lyon M, Depontieu F, Motte V, Land-olfi C, Lortat-Jacob H, Bechard D, Lassalle P, and Delehedde M. Endocan or endothelial cell specific molecule-1 (ESM-1): a potential novel endothelial cell marker and a new target for cancer therapy. Biochim Biophys Acta 1765: 25-37, 2006.
39. Sharma-Walia N, Paul AG, Bottero V, Sadagopan S, Veettil MV, Kerur N, and Chandran B. Kaposi's sarcoma associated herpes virus (KSHV) induced COX-2: a key factor in latency, inflammation, angiogenesis, cell survival and invasion. PLoS Pathog 6: e1000777, 2010.
40. Shin JW, Huggenberger R, and Detmar M. Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis. Blood 112: 2318-2326, 2008.
41. Sullivan RJ, Pantanowitz L, and Dezube BJ. Targeted therapy for Kaposi sarcoma. BioDrugs 23: 69-75, 2009.
42. Szatrowski TP and Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798, 1991.
43. Ushio-Fukai M. Redox signaling in angiogenesis: role of NADPH oxidase. Cardiovasc Res 71: 226-235, 2006.
44. Ushio-Fukai M and Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 264: 85-97, 2004.
45. Wade M and Wahl GM. c-Myc, genome instability, and tu-morigenesis: the devil is in the details. Curr Top Microbiol Immunol 302: 169-203, 2006.
46. Wang HW, Trotter MW, Lagos D, Bourboulia D, Henderson S, Makinen T, Elliman S, Flanagan AM, Alitalo K, and Boshoff C. Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nat Genet 36: 687-693, 2004.
47. Yang TY, Chen SC, Leach MW, Manfra D, Homey B, Wiekowski M, Sullivan L, Jenh CH, Narula SK, Chensue SW, and Lira SA. Transgenic expression of the chemokine receptor encoded by human herpesvirus 8 induces an an-gioproliferative disease resembling Kaposi's sarcoma. J Exp Med 191: 445-454, 2000.
48. Ye F, Zhou F, Bedolla RG, Jones T, Lei X, Kang T, Guadalupe M, and Gao SJ. Reactive oxygen species hydrogen peroxide mediates Kaposi's sarcoma-associated herpesvirus reactivation from latency. PLoS Pathog 7: e1002054, 2011.
49. Yoon S, Woo SU, Kang JH, Kim K, Kwon MH, Park S, Shin HJ, Gwak HS, and Chwae YJ. STAT3 transcriptional factor activated by reactive oxygen species induces IL6 in starvation-induced autophagy of cancer cells. Autophagy 6: 1125-1138, 2010.
50. Yu H and Jove R. The STATs of cancer\new molecular targets come of age. Nat Rev Cancer 4: 97-105, 2004.