Virology Journal | |
The modulation of apoptosis by oncogenic viruses | |
Marcela Lizano1  Joaquín Manzo-Merino1  Adriana Contreras-Paredes1  Alma Mariana Fuentes-González1  | |
[1] Unidad de Investigación Biomédica en Cáncer. Instituto Nacional de Cancerología, México/Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Av. San Fernando 22, col. Sección XVI, Tlalpan, C.P. 14080, Mexico City, Mexico | |
关键词: Oncogene; Cancer; Virus; Apoptosis; | |
Others : 1149888 DOI : 10.1186/1743-422X-10-182 |
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received in 2013-01-10, accepted in 2013-05-27, 发布年份 2013 | |
【 摘 要 】
Transforming viruses can change a normal cell into a cancer cell during their normal life cycle. Persistent infections with these viruses have been recognized to cause some types of cancer. These viruses have been implicated in the modulation of various biological processes, such as proliferation, differentiation and apoptosis. The study of infections caused by oncogenic viruses had helped in our understanding of several mechanisms that regulate cell growth, as well as the molecular alterations leading to cancer. Therefore, transforming viruses provide models of study that have enabled the advances in cancer research. Viruses with transforming abilities, include different members of the Human Papillomavirus (HPV) family, Hepatitis C virus (HCV), Human T-cell Leukemia virus (HTLV-1), Epstein Barr virus (EBV) and Kaposi’s Sarcoma Herpesvirus (KSHV).
Apoptosis, or programmed cell death, is a tightly regulated process that plays an important role in development and homeostasis. Additionally, it functions as an antiviral defense mechanism. The deregulation of apoptosis has been implicated in the etiology of diverse diseases, including cancer. Oncogenic viruses employ different mechanisms to inhibit the apoptotic process, allowing the propagation of infected and damaged cells. During this process, some viral proteins are able to evade the immune system, while others can directly interact with the caspases involved in apoptotic signaling. In some instances, viral proteins can also promote apoptosis, which may be necessary for an accurate regulation of the initial stages of infection.
【 授权许可】
2013 Fuentes-González et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]McLaughlin-Drubin M, Munger K: Viruses associated with human cancer. Biochim Biophys Acta 2008, 1782(suppl 3):127-150.
- [2]The Nobel prizes. http://www.nobelprize.org webcite
- [3]zur Hausen H: Viruses in human cancers. Science 1991, 254:1167-1173.
- [4]Rous P: A Transmissible Avian Neoplasm. (Sarcoma of the Common Fowl.). J Exp Med 1910, 12:696-705.
- [5]Shope RE, Hurst EW: Infectious Papillomatosis of Rabbits: With a Note on the Histopathology. J Exp Med 1933, 58:607-624.
- [6]Bittner JJ: Some Possible Effects of Nursing on the Mammary Gland Tumor Incidence in Mice. Science 1936, 84:162.
- [7]Gross L: “Spontaneous” leukemia developing in C3H mice following inoculation in infancy, with AK-leukemic extracts, or AK-embryos. Proc Soc Exp Biol Med 1951, 76:27-32.
- [8]Epstein MA, Barr YM, Achong BG: Studies with Burkitt’s lymphoma. Wistar Inst Symp Monogr 1965, 4:69-82.
- [9]Beral V: Cancer of the cervix: a sexually transmitted infection? Lancet 1974, 1:1037-1040.
- [10]zur Hausen H, Meinhof W, Scheiber W, Bornkamm GW: Attempts to detect virus-secific DNA in human tumors. I. Nucleic acid hybridizations with complementary RNA of human wart virus. Int J Cancer 1974, 13:650-656.
- [11]D’Souza G, Dempsey A: The role of HPV in head and neck cancer and review of the HPV vaccine. Prev Med 2011, 53(Suppl 1):S5-S11.
- [12]Vogel CL, Anthony PP, Mody N, Barker LF: Hepatitis-associated antigen in Ugandan patients with hepatocellular carcinoma. Lancet 1970, 2:621-624.
- [13]Vogel CL, Anthony PP, Sadikali F, Barker LF, Peterson MR: Hepatitis-associated antigen and antibody in hepatocellular carcinoma: results of a continuing study. J Natl Cancer Inst 1972, 48:1583-1588.
- [14]Lavanchy DJ: Viral hepatitis: Global goals for vaccination. Clin Virol 2012, 55:296-302.
- [15]Hu WT, Li HC, Lee SK, Ma HC, Yang CH, Chen HL, Lo SY: Both core and F proteins of hepatitis C virus could enhance cell proliferation in transgenic mice. Biochem Biophys Res Commun 2013, 435:147-152.
- [16]Raab-Traub N: Novel mechanisms of EBV-induced oncogenesis. Curr Opin Virol 2012, 2:453-458.
- [17]Molyneux EM, Rochford R, Griffin B, Newton R, Jackson G, Menon G, Harrison CJ, Israels T, Bailey S: Burkitt’s lymphoma. Lancet 2012, 379:1234-1244.
- [18]Uchida E, Honma R, Igarashi A, Kurata M, Imadome K, Omoto E, Miura O, Arai A: Sequential monitoring of plasma EBV-DNA level in a patient with EBV-positive Hodgkin lymphoma. Rinsho Ketsueki 2012, 53:87-91.
- [19]Chan SL, Ma BB: Novel systemic therapeutic for nasopharyngeal carcinoma. Expert Opin Ther Targets 2012, 16(Suppl 1):S63-S68.
- [20]Cheng TC, Hsieh SS, Hsu WL, Chen YF, Ho HH, Sheu LF: Expression of Epstein-Barr nuclear antigen 1 in gastric carcinoma cells is associated with enhanced tumorigenicity and reduced cisplatin sensitivity. Int J Oncol 2010, 36:151-160.
- [21]Fukumoto H, Kanno T, Hasegawa H, Katano H: Pathology of Kaposi’s Sarcoma-Associated Herpesvirus Infection. Front Microbiol 2011, 2:175.
- [22]Chakraborty S, Veettil MV, Chandran B: Kaposi’s Sarcoma Associated Herpesvirus Entry into Target Cells. Front Microbiol 2012, 3:6.
- [23]zur Hausen H: Papillomaviruses in human cancers. Proc Assoc Am Physicians 1999, 111:581-587.
- [24]Kostareli E, Holzinger D, Hess J: New Concepts for Translational Head and Neck Oncology: Lessons from HPV-Related Oropharyngeal Squamous Cell Carcinomas. Front Oncol 2012, 2:36.
- [25]Hunt R, Hwa C, Tzu J, Patel R, Tyring SK, Stein J: Multiple human papillomavirus-16 associated digital squamous-cell carcinomas in an immunocompetent woman with prior human papillomavirus-related genital carcinoma. Dermatol Online J 2011, 17:20.
- [26]Stoppa G, Rumiato E, Saggioro D: Ras signaling contributes to survival of human T-cell leukemia/lymphoma virus type 1 (HTLV-1) Tax-positive T-cells. Apoptosis 2012, 17:219-228.
- [27]Kuo CY, Tsai JI, Chou TY, Hung MJ, Wu CC, Hsu SL, Hwang GY: Apoptosis induced by hepatitis B virus X protein in a CCL13-HBx stable cell line. Oncol Rep 2012, 28:127-132.
- [28]Tang H, Grise H: Cellular and molecular biology of HCV infection and hepatitis. Clin Sci (Lond) 2009, 117:49-65.
- [29]Vermeulen K, Van Bockstaele DR, Berneman ZN: Apoptosis: mechanisms and relevance in cancer. Ann Hematol 2005, 84:627-639.
- [30]Hacker G: The morphology of apoptosis. Cell Tissue Res 2000, 301:5-17.
- [31]Kitagawa K, Niikura Y: Caspase-independent mitotic death (CIMD). Cell Cycle 2008, 7:1001-1005.
- [32]Lamkanfi M, Festjens N, Declercq W, Vanden Berghe T, Vandenabeele P: Caspases in cell survival, proliferation and differentiation. Cell Death Differ 2007, 14:44-55.
- [33]Reed JC: Mechanisms of apoptosis. Am J Pathol 2000, 157:1415-1430.
- [34]Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW: Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 2002, 9:423-432.
- [35]Hill MM, Adrain C, Duriez PJ, Creagh EM, Martin SJ: Analysis of the composition, assembly kinetics and activity of native Apaf-1 apoptosomes. EMBO J 2004, 23:2134-2145.
- [36]Kuranaga E: Caspase signaling in animal development. Dev Growth Differ 2011, 53:137-148.
- [37]Srinivasula SM, Ashwell JD: IAPs: what’s in a name? Mol Cell 2008, 30:123-135.
- [38]Shi Y: Caspase activation, inhibition, and reactivation: a mechanistic view. Protein Sci 2004, 13:1979-1987.
- [39]Vaux DL, Silke J: IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 2005, 6:287-297.
- [40]Lockshin MD: Future trends for treatment of APS. J Autoimmun 2000, 15:261-264.
- [41]Jha K, Shukla M, Pandey M: Survivin expression and targeting in breast cancer. Surg Oncol 2012, 21:125-131.
- [42]Bandala E, Espinosa M, Maldonado V, Melendez-Zajgla J: Inhibitor of apoptosis-1 (IAP-1) expression and apoptosis in non-small-cell lung cancer cells exposed to gemcitabine. Biochem Pharmacol 2001, 62:13-19.
- [43]zur Hausen H: Papillomavirus infections:a major cause of human cancers. Biochim Biophys Acta 1996, 1288:F55-F78.
- [44]Lizano M, Berumen J, Garcia-Carranca A: HPV-related carcinogenesis: basic concepts, viral types and variants. Arch Med Res 2009, 40:428-434.
- [45]Schlecht NF, Kulaga S, Robitaille J, Ferreira S, Santos M, Miyamura RA, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL, Franco EL: Persistent human papillomavirus infection as a predictor of cervical intraepithelial neoplasia. JAMA 2001, 286:3106-3114.
- [46]Woodman CB, Collins SI, Young LS: The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer 2007, 7:11-22.
- [47]Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S: Human papillomavirus and cervical cancer. Lancet 2007, 370:890-907.
- [48]Pientong C, Wongwarissara P, Ekalaksananan T, Swangphon P, Kleebkaow P, Kongyingyoes B, Siriaunkgul S, Tungsinmunkong K, Suthipintawong C: Association of human papillomavirus type 16 long control region mutation and cervical cancer. Virol J 2013, 10:30-37.
- [49]Lagunas-Martinez A, Madrid-Marina V, Gariglio P: Modulation of apoptosis by early human papillomavirus proteins in cervical cancer. Biochim Biophys Acta 2010, 1805:6-16.
- [50]Garnett TO, Duerksen-Hughes PJ: Modulation of apoptosis by human papillomavirus (HPV) oncoproteins. Arch Virol 2006, 151:2321-2335.
- [51]Arechaga-Ocampo E, Pereira-Suarez AL, del Moral-Hernandez O, Cedillo-Barron L, Rodriguez-Sastre MA, Castillo-Alvarez A, Lopez-Bayghen E, Villegas-Sepulveda N: HPV + cervical carcinomas and cell lines display altered expression of caspases. Gynecol Oncol 2008, 108:10-18.
- [52]Munger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, Zacny VL: Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 2001, 20:7888-7898.
- [53]Howes KA, Ransom N, Papermaster DS, Lasudry JG, Albert DM, Windle JJ: Apoptosis or retinoblastoma: alternative fates of photoreceptors expressing the HPV-16 E7 gene in the presence or absence of p53. Genes Dev 1994, 8:1300-1310.
- [54]Thyrell L, Sangfelt O, Zhivotovsky B, Pokrovskaja K, Wang Y, Einhorn S, Grander D: The HPV-16 E7 oncogene sensitizes malignant cells to IFN-alpha-induced apoptosis. J Interferon Cytokine Res 2005, 25:63-72.
- [55]Kaznelson DW, Bruun S, Monrad A, Gjerlov S, Birk J, Ropke C, Norrild B: Simultaneous human papilloma virus type 16 E7 and cdk inhibitor p21 expression induces apoptosis and cathepsin B activation. Virology 2004, 320:301-312.
- [56]Stoppler H, Stoppler MC, Johnson E, Simbulan-Rosenthal CM, Smulson ME, Iyer S, Rosenthal DS, Schlegel R: The E7 protein of human papillomavirus type 16 sensitizes primary human keratinocytes to apoptosis. Oncogene 1998, 17:1207-1214.
- [57]Yuan H, Fu F, Zhuo J, Wang W, Nishitani J, An DS, Chen IS, Liu X: Human papillomavirus type 16 E6 and E7 oncoproteins upregulate c-IAP2 gene expression and confer resistance to apoptosis. Oncogene 2005, 24:5069-5078.
- [58]Thompson DA, Zacny V, Belinsky GS, Classon M, Jones DL, Schlegel R, Munger K: The HPV E7 oncoprotein inhibits tumor necrosis factor alpha-mediated apoptosis in normal human fibroblasts. Oncogene 2001, 20:3629-3640.
- [59]Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM: The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990, 63:1129-1136.
- [60]Thomas M, Banks L: Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 1998, 17:2943-2954.
- [61]Filippova M, Parkhurst L, Duerksen-Hughes PJ: The human papillomavirus 16 E6 protein binds to Fas-associated death domain and protects cells from Fas-triggered apoptosis. J Biol Chem 2004, 279:25729-25744.
- [62]Garnett TO, Filippova M, Duerksen-Hughes PJ: Accelerated degradation of FADD and procaspase 8 in cells expressing human papilloma virus 16 E6 impairs TRAIL-mediated apoptosis. Cell Death Differ 2006, 13:1915-1926.
- [63]Gross-Mesilaty S, Reinstein E, Bercovich B, Tobias KE, Schwartz AL, Kahana C, Ciechanover A: Basal and human papillomavirus E6 oncoprotein-induced degradation of Myc proteins by the ubiquitin pathway. Proc Natl Acad Sci USA 1998, 95:8058-8063.
- [64]Underbrink MP, Howie HL, Bedard KM, Koop JI, Galloway DA: E6 proteins from multiple human betapapillomavirus types degrade Bak and protect keratinocytes from apoptosis after UVB irradiation. J Virol 2008, 82:10408-10417.
- [65]Kabsch K, Alonso A: The human papillomavirus type 16 E5 protein impairs TRAIL- and FasL-mediated apoptosis in HaCaT cells by different mechanisms. J Virol 2002, 76:12162-12172.
- [66]Crusius K, Rodriguez I, Alonso A: The human papillomavirus type 16 E5 protein modulates ERK1/2 and p38 MAP kinase activation by an EGFR-independent process in stressed human keratinocytes. Virus Genes 2000, 20:65-69.
- [67]Moody CA, Fradet-Turcotte A, Archambault J, Laimins LA: Human papillomaviruses activate caspases upon epithelial differentiation to induce viral genome amplification. Proc Natl Acad Sci USA 2007, 104:19541-19546.
- [68]Blachon S, Demeret C: The regulatory E2 proteins of human genital papillomaviruses are pro-apoptotic. Biochimie 2003, 85:813-819.
- [69]Frattini MG, Hurst SD, Lim HB, Swaminathan S, Laimins LA: Abrogation of a mitotic checkpoint by E2 proteins from oncogenic human papillomaviruses correlates with increased turnover of the p53 tumor suppressor protein. EMBO J 1997, 16:318-331.
- [70]Desaintes C, Demeret C, Goyat S, Yaniv M, Thierry F: Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. EMBO J 1997, 16:504-514.
- [71]Thierry F, Demeret C: Direct activation of caspase 8 by the proapoptotic E2 protein of HPV18 independent of adaptor proteins. Cell Death Differ 2008, 15:1356-1363.
- [72]Wang W, Fang Y, Sima N, Li Y, Li W, Li L, Han L, Liao S, Han Z, Gao Q, et al.: Triggering of death receptor apoptotic signaling by human papillomavirus 16 E2 protein in cervical cancer cell lines is mediated by interaction with c-FLIP. Apoptosis 2011, 16:55-66.
- [73]Bellanger S, Tan CL, Xue YZ, Teissier S, Thierry F: Tumor suppressor or oncogene? A critical role of the human papillomavirus (HPV) E2 protein in cervical cancer progression. Am J Cancer Res 2011, 1:373-389.
- [74]Desaintes C, Goyat S, Garbay S, Yaniv M, Thierry F: Papillomavirus E2 induces p53-independent apoptosis in HeLa cells. Oncogene 1999, 18:4538-4545.
- [75]Parkin DM: Global cancer statistics in the year 2000. Lancet Oncol 2001, 2:533-543.
- [76]Santos-Lopez G, Sosa-Jurado F, Vallejo-Ruiz V, Melendez-Mena D, Reyes-Leyva J: Prevalence of hepatitis C virus in the Mexican population: a systematic review. J Infect 2008, 56:281-290.
- [77]Aguilera Guirao A, Romero Yuste S, Regueiro BJ: Epidemiology and clinical manifestations of viral hepatitis. Enferm Infecc Microbiol Clin 2006, 24:264-276.
- [78]Bosch FX, Ribes J, Diaz M, Cleries R: Primary liver cancer: worldwide incidence and trends. Gastroenterology 2004, 127(1):S5-S16.
- [79]Kew MC: Epidemiology of chronic hepatitis B virus infection, hepatocellular carcinoma. Pathol Biol 2010, 58:273-277.
- [80]Simmonds P, Bukh J, Combet C, Deleage G, Enomoto N, Feinstone S, Halfon P, Inchauspe G, Kuiken C, Maertens G, et al.: Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 2005, 42:962-973.
- [81]Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W: Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med 2009, 15:31-33.
- [82]Lin C, Lindenbach BD, Pragai BM, McCourt DW, Rice CM: Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini. J Virol 1994, 68:5063-5073.
- [83]Hassan M, Selimovic D, Ghozlan H, Abdel-kader O: Hepatitis C virus core protein triggers hepatic angiogenesis by a mechanism including multiple pathways. Hepatology 2009, 49:1469-1482.
- [84]Cocquerel L, Quinn ER, Flint M, Hadlock KG, Foung SK, Levy S: Recognition of native hepatitis C virus E1E2 heterodimers by a human monoclonal antibody. J Virol 2003, 77:1604-1609.
- [85]Steinmann E, Penin F, Kallis S, Patel AH, Bartenschlager R, Pietschmann T: Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog 2007, 3:e103.
- [86]Kolykhalov AA, Mihalik K, Feinstone SM, Rice CM: Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3’ nontranslated region are essential for virus replication in vivo. J Virol 2000, 74:2046-2051.
- [87]Lam AM, Frick DN: Hepatitis C virus subgenomic replicon requires an active NS3 RNA helicase. J Virol 2006, 80:404-411.
- [88]Koch JO, Bartenschlager R: Modulation of hepatitis C virus NS5A hyperphosphorylation by nonstructural proteins NS3, NS4A, and NS4B. J Virol 1999, 73:7138-7146.
- [89]Egger D, Wolk B, Gosert R, Bianchi L, Blum HE, Moradpour D, Bienz K: Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 2002, 76:5974-5984.
- [90]Evans MJ, Rice CM, Goff SP: Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc Natl Acad Sci USA 2004, 101:13038-13043.
- [91]Ranjith-Kumar CT, Kim YC, Gutshall L, Silverman C, Khandekar S, Sarisky RT, Kao CC: Mechanism of de novo initiation by the hepatitis C virus RNA-dependent RNA polymerase: role of divalent metals. J Virol 2002, 76:12513-12525.
- [92]Fischer R, Baumert T, Blum HE: Hepatitis C virus infection and apoptosis. World J Gastroenterol 2007, 13:4865-4872.
- [93]Balachandran S, Roberts PC, Kipperman T, Bhalla KN, Compans RW, Archer DR, Barber GN: Alpha/beta interferons potentiate virus-induced apoptosis through activation of the FADD/Caspase-8 death signaling pathway. J Virol 2000, 74:1513-1523.
- [94]Schaefer U, Voloshanenko O, Willen D, Walczak H: TRAIL: a multifunctional cytokine. Front Biosci 2007, 12:3813-3824.
- [95]Fischer R, Schmitt M, Bode JG, Haussinger D: Expression of the peripheral-type benzodiazepine receptor and apoptosis induction in hepatic stellate cells. Gastroenterology 2001, 120:1212-1226.
- [96]Machida K, Tsukiyama-Kohara K, Seike E, Tone S, Shibasaki F, Shimizu M, Takahashi H, Hayashi Y, Funata N, Taya C, et al.: Inhibition of cytochrome c release in Fas-mediated signaling pathway in transgenic mice induced to express hepatitis C viral proteins. J Biol Chem 2001, 276:12140-12146.
- [97]Ruggieri A, Harada T, Matsuura Y, Miyamura T: Sensitization to Fas-mediated apoptosis by hepatitis C virus core protein. Virology 1997, 229:68-76.
- [98]Saito K, Meyer K, Warner R, Basu A, Ray RB, Ray R: Hepatitis C virus core protein inhibits tumor necrosis factor alpha-mediated apoptosis by a protective effect involving cellular FLICE inhibitory protein. J Virol 2006, 80:4372-4379.
- [99]Otsuka M, Kato N, Lan K, Yoshida H, Kato J, Goto T, Shiratori Y, Omata M: Hepatitis C virus core protein enhances p53 function through augmentation of DNA binding affinity and transcriptional ability. J Biol Chem 2000, 275:34122-34130.
- [100]Machida K, Cheng KT, Lai CK, Jeng KS, Sung VM, Lai MM: Hepatitis C virus triggers mitochondrial permeability transition with production of reactive oxygen species, leading to DNA damage and STAT3 activation. J Virol 2006, 80:7199-7207.
- [101]Sudha G, Yamunadevi S, Tyagi N, Das S, Srinivasan N: Structural and molecular basis of interaction of HCV non-structural protein 5A with human casein kinase 1alpha and PKR. BMC Struct Biol 2012, 12:28.
- [102]Machida K, Tsukiyama-Kohara K, Seike E, Tone S, Shibasaki F, Shimizu M, Takahashi H, Hayashi Y, Funata N, Taya C, Yonekawa H, Kohara M: Inhibition of Cytochrome c Release in Fas-mediated Signaling Pathway in Transgenic Mice Induced to Express Hepatitis C. J Bol Chem 2001, 276:12140-12146.
- [103]Ciccaglione AR, Marcantonio C, Costantino A, Equestre M, Rapicetta M: Expression of HCV E1 protein in baculovirus-infected cells: effects on cell viability and apoptosis induction. Intervirology 2003, 46:121-126.
- [104]Ciccaglione AR, Marcantonio C, Tritarelli E, Equestre M, Magurano F, Costantino A, Nicoletti L, Rapicetta M: The transmembrane domain of hepatitis C virus E1 glycoprotein induces cell death. Virus Res 2004, 104:1-9.
- [105]Erdtmann L, Franck N, Lerat H, Le Seyec J, Gilot D, Cannie I, Gripon P, Hibner U, Guguen-Guillouzo C: The hepatitis C virus NS2 protein is an inhibitor of CIDE-B-induced apoptosis. J Biol Chem 2003, 278:18256-18264.
- [106]Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J: Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005, 437:1167-1172.
- [107]Nomura-Takigawa Y, Nagano-Fujii M, Deng L, Kitazawa S, Ishido S, Sada K, Hotta H: Non-structural protein 4A of Hepatitis C virus accumulates on mitochondria and renders the cells prone to undergoing mitochondria-mediated apoptosis. J Gen Virol 2006, 87:1935-1945.
- [108]Chung YL, Sheu ML, Yen SH: Hepatitis C virus NS5A as a potential viral Bcl-2 homologue interacts with Bax and inhibits apoptosis in hepatocellular carcinoma. Int J Cancer 2003, 107:65-73.
- [109]Matsuoka M: Human T-cell leukemia virus type I and adult T-cell leukemia. Oncogene 2003, 22:5131-5140.
- [110]Nicot C, Harrod RL, Ciminale V, Franchini G: Human T-cell leukemia/lymphoma virus type 1 nonstructural genes and their functions. Oncogene 2005, 24:6026-6034.
- [111]Gaudray G, Gachon F, Basbous J, Biard-Piechaczyk M, Devaux C, Mesnard JM: The complementary strand of the human T-cell leukemia virus type 1 RNA genome encodes a bZIP transcription factor that down-regulates viral transcription. J Virol 2002, 76:12813-12822.
- [112]Toufaily C, Landry S, Leib-Mosch C, Rassart E, Barbeau B: Activation of LTRs from different human endogenous retrovirus (HERV) families by the HTLV-1 tax protein and T-cell activators. Viruses 2011, 3:2146-2159.
- [113]Mori N, Fujii M, Cheng G, Ikeda S, Yamasaki Y, Yamada Y, Tomonaga M, Yamamoto N: Human T-cell leukemia virus type I tax protein induces the expression of anti-apoptotic gene Bcl-xL in human T-cells through nuclear factor-kappaB and c-AMP responsive element binding protein pathways. Virus Genes 2001, 22:279-287.
- [114]Waldele K, Silbermann K, Schneider G, Ruckes T, Cullen BR, Grassmann R: Requirement of the human T-cell leukemia virus (HTLV-1) tax-stimulated HIAP-1 gene for the survival of transformed lymphocytes. Blood 2006, 107:4491-4499.
- [115]Mukherjee S, Negi VS, Keitany G, Tanaka Y, Orth K: In vitro activation of the IkappaB kinase complex by human T-cell leukemia virus type-1 Tax. J Biol Chem 2008, 283:15127-15133.
- [116]Xiao G, Cvijic ME, Fong A, Harhaj EW, Uhlik MT, Waterfield M, Sun SC: Retroviral oncoprotein Tax induces processing of NF-kappaB2/p100 in T cells: evidence for the involvement of IKKalpha. EMBO J 2001, 20:6805-6815.
- [117]Suzuki T, Hirai H, Yoshida M: Tax protein of HTLV-1 interacts with the Rel homology domain of NF-kappa B p65 and c-Rel proteins bound to the NF-kappa B binding site and activates transcription. Oncogene 1994, 9:3099-3105.
- [118]Bex F, McDowall A, Burny A, Gaynor R: The human T-cell leukemia virus type 1 transactivator protein Tax colocalizes in unique nuclear structures with NF-kappaB proteins. J Virol 1997, 71:3484-3497.
- [119]Hirai H, Fujisawa J, Suzuki T, Ueda K, Muramatsu M, Tsuboi A, Arai N, Yoshida M: Transcriptional activator Tax of HTLV-1 binds to the NF-kappa B precursor p105. Oncogene 1992, 7:1737-1742.
- [120]Jeong SJ, Pise-Masison CA, Radonovich MF, Park HU, Brady JN: Activated AKT regulates NF-kappaB activation, p53 inhibition and cell survival in HTLV-1-transformed cells. Oncogene 2005, 24:6719-6728.
- [121]Tomita M, Kikuchi A, Akiyama T, Tanaka Y, Mori N: Human T-cell leukemia virus type 1 tax dysregulates beta-catenin signaling. J Virol 2006, 80:10497-10505.
- [122]Saggioro D, Silic-Benussi M, Biasiotto R, D’Agostino DM, Ciminale V: Control of cell death pathways by HTLV-1 proteins. Front Biosci 2009, 14:3338-3351.
- [123]Epstein MA, Barr YM, Achong BG: A Second Virus-Carrying Tissue Culture Strain (Eb2) of Lymphoblasts from Burkitt’s Lymphoma. Pathol Biol (Paris) 1964, 12:1233-1234.
- [124]Kutok JL, Wang F: Spectrum of Epstein-Barr virus-associated diseases. Annu Rev Pathol 2006, 1:375-404.
- [125]Given D, Yee D, Griem K, Kieff E: DNA of Epstein-Barr virus. V. Direct repeats of the ends of Epstein-Barr virus DNA. J Virol 1979, 30:852-862.
- [126]Cai X, Schafer A, Lu S, Bilello JP, Desrosiers RC, Edwards R, Raab-Traub N, Cullen BR: Epstein-Barr virus microRNAs are evolutionarily conserved and differentially expressed. PLoS Pathog 2006, 2(Suppl 3):e23.
- [127]van den Bosch CA: Is endemic Burkitt’s lymphoma an alliance between three infections and a tumour promoter? Lancet Oncol 2004, 5:738-746.
- [128]Polack A, Hortnagel K, Pajic A, Christoph B, Baier B, Falk M, Mautner J, Geltinger C, Bornkamm GW, Kempkes B: c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1. Proc Natl Acad Sci USA 1996, 93:10411-10416.
- [129]Kennedy G, Komano J, Sugden B: Epstein-Barr virus provides a survival factor to Burkitt’s lymphomas. Proc Natl Acad Sci USA 2003, 100:14269-14274.
- [130]Yamamoto N, Takizawa T, Iwanaga Y, Shimizu N, Yamamoto N: Malignant transformation of B lymphoma cell line BJAB by Epstein-Barr virus-encoded small RNAs. FEBS Lett 2000, 484:153-158.
- [131]Nanbo A, Inoue K, Adachi-Takasawa K, Takada K: Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt’s lymphoma. EMBO J 2002, 21:954-965.
- [132]Meurs EF, Galabru J, Barber GN, Katze MG, Hovanessian AG: Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 1993, 90:232-236.
- [133]Komano J, Maruo S, Kurozumi K, Oda T, Takada K: Oncogenic role of Epstein-Barr virus-encoded RNAs in Burkitt’s lymphoma cell line Akata. J Virol 1999, 73:9827-9831.
- [134]Panagopoulos D, Victoratos P, Alexiou M, Kollias G, Mosialos G: Comparative analysis of signal transduction by CD40 and the Epstein-Barr virus oncoprotein LMP1 in vivo. J Virol 2004, 78:13253-13261.
- [135]Mosialos G, Birkenbach M, Yalamanchili R, VanArsdale T, Ware C, Kieff E: The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 1995, 80:389-399.
- [136]Eliopoulos AG, Caamano JH, Flavell J, Reynolds GM, Murray PG, Poyet JL, Young LS: Epstein-Barr virus-encoded latent infection membrane protein 1 regulates the processing of p100 NF-kappaB2 to p52 via an IKKgamma/NEMO-independent signalling pathway. Oncogene 2003, 22:7557-7569.
- [137]Nguyen HQ, Magaret AS, Kitahata MM, Van Rompaey SE, Wald A, Casper C: Persistent Kaposi sarcoma in the era of highly active antiretroviral therapy: characterizing the predictors of clinical response. AIDS 2008, 22:937-945.
- [138]Mesri EA, Cesarman E, Boshoff C: Kaposi’s sarcoma and its associated Herpesvirus. Nat Rev Cancer 2010, 10:707-719.
- [139]Lebbe C, Porcher R, Marcelin AG, Agbalika F, Dussaix E, Samuel D, Varnous S, Euvrard S, Bigorie A, Creusvaux H, Legendre C, Frances C: Human herpesvirus 8 (HHV8) transmission and related morbidity in organ recipients. Am J Transplant 2013, 13:207-213.
- [140]Dupin N, Diss TL, Kellam P, Tulliez M, Du MQ, Sicard D, Weiss RA, Isaacson PG, Boshoff C: HHV-8 is associated with a plasmablastic variant of Castleman disease that is linked to HHV-8-positive plasmablastic lymphoma. Blood 2000, 100:3415-3418.
- [141]Wu W, Vieira J, Fiore N, Banerjee P, Sieburg M, Rochford R, Harrington W Jr, Feuer G: KSHV/HHV-8 infection of human hematopoietic progenitor (CD34+) cells: persistence of infection during hematopoiesis in vitro and in vivo. Blood 2006, 108:141-151.
- [142]Sharma-Walia N, Paul AG, Bottero V, Sadagopan S, Veettil MV, Kerur N, Chandran B: Kaposi’s sarcoma associated herpes virus (KSHV) induced COX-2: a key factor in latency, inflammation, angiogenesis, cell survival and invasion. LoS Pathog 2010, 6:e1000777.
- [143]Renne R, Lagunoff M, Zhong W, Ganem D: The size and conformation of Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) DNA in infected cells and virions. J Virol 1996, 70:8151-8154.
- [144]Lagunoff M, Ganem D: The structure and coding organization of the genomic termini of Kaposi’s sarcoma-associated herpesvirus. Virology 1997, 236:147-154.
- [145]Russo JJ, Bohenzky RA, Chien MC, Chen J, Yan M, Maddalena D, Parry JP, Peruzzi D, Edelman IS, Chang Y, Moore PS: Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci USA 1996, 93:14862-14867.
- [146]Cai X, Lu S, Zhang Z, Gonzalez CM, Damania B, Cullen BR: Kaposi’s sarcoma-associated herpes virus expresses an array of viral microRNA latently infected cells. Proc Natl Acad Sci USA 2005, 102:5570-5575.
- [147]Ganem D: KSHV infection and the pathogenesis of Kaposi’s sarcoma. Annu Rev Pathol 2006, 1:273-296.
- [148]Radkov SA, Kellam P, Boshoff C: The latent nuclear antigen of Kaposi sarcoma-associated herpesvirus targets the retinoblastoma-E2F pathway and with the oncogene Hras transforms primary rat cells. Nature Med 2000, 6:1121-1127.
- [149]Fujimuro M, Wu FY, ApRhys C, Kajumbula H, Young DB, Hayward GS, Hayward SD: A novel viral mechanism for dysregulation of β-catenin in Kaposi’s sarcomaassociated herpesvirus latency. Nature Med 2003, 9:300-306.
- [150]Di Bartolo DL, Cannon M, Liu YF, Renne R, Chadburn A, Boshoff C, Cesarman E: KSHV LANA inhibits TGF-beta signaling through epigenetic silencing of the TGF-beta type II receptor. Blood 2008, 111:4731-4740.
- [151]McCormick C, Ganem D: The kaposin B protein of KSHV activates the p38/MK2 pathway and stabilizes cytokine mRNAs. Science 2005, 307:739-741.
- [152]Bieleski L, Talbot SJ: Kaposi’s Sarcoma-Associated Herpesvirus vCyclin Open Reading Frame Contains an Internal Ribosome. J Virol 2001, 75:1864-1869.
- [153]Ojala PM, Ojala PM, Yamamoto K, Castaños-Vélez E, Biberfeld P, Korsmeyer SJ, Mäkelä TP: The apoptotic v-cyclin-CDK6 complex phosphorylates and inactivates Bcl-2. Nature Cell Biol. 2000, 2:819-825.
- [154]Bagnéris C, Ageichik AV, Cronin N, Wallace B, Collins M, Boshoff C, Waksman G, Barrett T: Crystal structure of a vFlip-IKKgamma complex: insights into viral activation of the IKK signalosome. Mol Cell 2008, 30:620-623.
- [155]Jaber T, Yuan Y: A Virally Encoded Small Peptide Regulates RTA Stability and Facilitates Kaposi’s Sarcoma-Associated Herpesvirus Lytic Replication. J Virol 2013, 87:3461-3470.
- [156]Chandriani S, Xu Y, Ganem D: The lytic transcriptome of Kaposi’s sarcoma-associated herpesvirus reveals extensive transcription of noncoding regions, including regions antisense to important genes. J Virol 2010, 84:7934-7942.
- [157]Song MJ, Deng H, Sun R: Comparative study of regulation of RTA-responsive genes in Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8. J Virol 2003, 77:9451-9462.
- [158]Lang SM, Bynoe MO, Karki R, Tartell MA, Means RE: Kaposi’s Sarcoma Associated Herpesvirus K3 and K5 Proteins Down Regulate Both DC-SIGN and DC-SIGNR. PLoS One 2013, 8:e58056.
- [159]Zhou F, Xue M, Qin D, Zhu X, Wang C, Zhu J, Hao T, Cheng L, Chen X, Bai Z, Feng N, Gao SJ, Lu C: HIV-1 Tat promotes Kaposi’s sarcoma-associated herpesvirus (KSHV) vIL-6-induced angiogenesis and tumorigenesis by regulating PI3K/PTEN/AKT/GSK-3β signaling pathway. PLoS One 2013, 8:e53145.
- [160]Young Bong C, John N: Bim nuclear translocation and inactivation by viral interferon regulatory factor. PLoS Pathog 2010, 5:6. e1001031
- [161]Lüttichau HR: The herpesvirus 8 encoded chemokines vCCL2 (vMIP-II) and vCCL3 (vMIP-III) target the human but not the murine lymphotactin receptor. Virol J 2008, 21:50.
- [162]Young Bong C, John N: Autocrine and Paracrine Promotion of Cell Survival and Virus Replication by Human Herpesvirus 8 Chemokines. J Virol 2008, 83:6501-6513.
- [163]Polstra AM, Goudsmit J, Cornelissen M: Latent and lytic HHV-8 mRNA expression in PBMCs and Kaposi’s sarcoma skin biopsies of AIDS Kaposi’s sarcoma patients. J Med Virol 2003, 70:624-627.
- [164]Moore PS: KSHV manipulation of the cell cycle and apoptosis. In Human Herpesviruses. Biology, Therapy, and Immunoprophylaxis. Edited by Arvin A, Campadelli-Fiume G, Mocarski E, Moore PS, Roizman B, Whitley R, Yamanishi K. Cambridge: Cambridge University Press; 2007. Chapter 30
- [165]Samols MA, Skalsky RL, Mal-donado AM, Riva A, Lopez MC, Baker HV, Renne R: Identification of cellular genes targeted by KSHV-encoded microRNAs. PLoSPathog 2007, 3:65.
- [166]Lei X, Bai Z, Ye F, Huang Y, Gao SJ: Regulation of herpesvirus lifecycle by viral microRNAs. Virulence 2010, 1:433-435.
- [167]Ziegelbauer JM, Sullivan CS, Ganem D: Tandem array based expression screens identify host mRNA targets of virus encoded microRNAs. Nat Genet 2009, 41:130-134.
- [168]Kang H, Wiedmer A, Yuan Y, Robertson E, Lieberman PM: Coordination of KSHV latent and lytic gene control by CTCF-cohesin mediated chromosome conformation. PLoS Pathog 2011, 7:e1002140.
- [169]Flanagan AM, Letai A: BH3 domains define selective inhibitory interactions with BHRF-1 and KSHV BCL-2. Cell Death Differ 2008, 15:580-588.
- [170]Shin YC, Nakamura H, Liang X, Feng P, Chang H, Kowalk TF, Jung JU: Inhibition of the ATM/p53 signal transduction pathway by Kaposi’s sarcoma-associated herpesvirus interferon regulatory factor 1. J Virol 2006, 80:2257-2266.
- [171]Tomlinson CC, Damania B: The K1 protein of Kaposi’s sarcoma-associated herpesvirus activates the Akt signaling pathway. J Virol 2008, 78:1918-1927.