HIV, EBV and KSHV: Viral cooperation in the pathogenesis of human malignancies

Cancer Letters

Volumn 305, Issue 2, 2011, Pages 175-185

  Ramos da Silva, Suzane ^a   Elgui de Oliveira, Deilson ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

EBV; HIV 1; KSHV; Viral carcinogenesis; Viral cooperation

Indexed keywords

ANTIRETROVIRUS AGENT; TRANSACTIVATOR PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; APOPTOSIS; BURKITT LYMPHOMA; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CELL TRANSFORMATION; EPSTEIN BARR VIRUS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HODGKIN DISEASE; HUMAN; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; KAPOSI SARCOMA; LONG TERMINAL REPEAT; NONHODGKIN LYMPHOMA; NONHUMAN; PRIMARY CENTRAL NERVOUS SYSTEM LYMPHOMA; PRIORITY JOURNAL; SHORT SURVEY; VIRUS CARCINOGENESIS; VIRUS GENOME; VIRUS LATENCY; VIRUS REACTIVATION; VIRUS REPLICATION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79955473602     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.02.007     Document Type: Review

References (116)

1. Wood C., Harrington W.J. AIDS and associated malignancies. Cell Res. 2005, 15:947-952.
2. Elgui de Oliveira D. DNA viruses in human cancer: an integrated overview on fundamental mechanisms of viral carcinogenesis. Cancer Lett. 2007, 247:182-196.
3. Swerdlow S., Campo E., Lee Harris N., Jaffe E.S., Pileri S.A., Stein H., Thiele J., Vardiman J.W. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissue (IARC WHO Classification of Tumours) 2008, World Health Organization. fourth ed.
4. Ganem D. KSHV infection and the pathogenesis of Kaposi's sarcoma. Annu. Rev. Pathol. 2006, 1:273-296.
5. Cesarman E., Chang Y., Moore P.S., Said J.W., Knowles D.M. Kaposi's Sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 1995, 332:1186-1191.
6. Grogg K.L., Miller R.F., Dogan A. HIV infection and lymphoma. J. Clin.Pathol. 2007, 60:1365-1372.
7. Beral V., Peterman T.A., Berkelman R.L., Jaffe H.W. Kaposi's sarcoma among persons with AIDS: a sexually transmitted infection?. Lancet 1990, 335:123-128.
8. Jacobson L.P., Jenkins F.J., Springer G., Muñoz A., Shah K.V., Phair J., Zhang Z., Armenian H. Interaction of human immunodeficiency virus type 1 and human herpesvirus type 8 infections on the incidence of Kaposi's sarcoma. J. Infect. Dis. 2000, 181:1940-1949.
9. Ledergerber B., Telenti A., Egger M. Risk of HIV related Kaposi's sarcoma and non-Hodgkin's lymphoma with potent antiretroviral therapy: prospective cohort study. BMJ 1999, 319:23-24.
10. Grulich A.E., Li Y., McDonald A.M., Correll P.K., Law M.G., Kaldor J.M. Decreasing rates of Kaposi's sarcoma and non-Hodgkin's lymphoma in the era of potent combination anti-retroviral therapy. AIDS 2001, 15:629-633.
11. Rabkin C.S. AIDS and cancer in the era of highly active antiretroviral therapy (HAART). Eur. J. Cancer 2001, 37:1316-1319.
12. Besson C., Goubar A., Gabarre J., Rozenbaum W., Pialoux G., Chatelet F.P., Katlama C., Charlotte F., Dupont B., Brousse N., Huerre M., Mikol J., Camparo P., Mokhtari K., Tulliez M., Salmon-Céron D., Boué F., Costagliola D., Raphaël M. Changes in AIDS-related lymphoma since the era of highly active antiretroviral therapy. Blood 2001, 98:2339-2344.
13. Silverberg M.J., Abrams D.I. AIDS-defining and non-AIDS-defining malignancies: cancer occurrence in the antiretroviral therapy era. Curr. Opin. Oncol. 2007, 19:446-451.
14. Wilde J.T., Lee C.A., Darby S.C., Kan S.W., Giangrande P., Phillips A.N., Winter M., Spooner R., Ludlam C.A. The incidence of lymphoma in the UK haemophilia population between 1978 and 1999. AIDS 2002, 16:1803-1807.
15. International Collaboration on HIV and Cancer Highly active antiretroviral therapy and incidence of cancer in human immunodeficiency virus-infected adults. J. Natl. Cancer Inst. 2000, 92:1823-1830.
16. Diamond C., Taylor T.H., Aboumrad T., Anton-Culver H. Changes in acquired immunodeficiency syndrome-related non-Hodgkin lymphoma in the era of highly active antiretroviral therapy: incidence, presentation, treatment, and survival. Cancer 2006, 106:128-135.
17. Stevens S.J., Blank B.S., Smits P.H., Meenhorst P.L., Middeldorp J.M. High Epstein-Barr virus (EBV) DNA loads in HIV-infected patients: correlation with antiretroviral therapy and quantitative EBV serology. AIDS 2002, 16:993-1001.
18. Casper C. Defining a role for antiviral drugs in the treatment of persons with HHV-8 infection. Herpes 2006, 13:42-47.
19. Bourboulia D., Aldam D., Lagos D., Allen E., Williams I., Cornforth D., Copas A., Boshoff C. Short- and long-term effects of highly active antiretroviral therapy on Kaposi sarcoma-associated herpesvirus immune responses and viraemia. AIDS 2004, 18:485-493.
20. Gill J., Bourboulia D., Wilkinson J., Hayes P., Cope A., Marcelin A.G., Calvez V., Gotch F., Boshoff C., Gazzard B. Prospective study of the effects of antiretroviral therapy on Kaposi sarcoma - associated herpesvirus infection in patients with and without Kaposi sarcoma. J. Acquir. Immune Deficiency Syndromes 2002, 31:384-390.
21. Cattelan A.M., Calabrò M.L., Gasperini P., Aversa S.M., Zanchetta M., Meneghetti F., De Rossi A., Chieco-Bianchi L. Acquired immunodeficiency syndrome-related Kaposi's sarcoma regression after highly active antiretroviral therapy: biologic correlates of clinical outcome. J. Natl. Cancer Inst. Monogr. 2001, 28:44-49.
22. Cattelan A.M., Calabrò M.L., Aversa S.M., Zanchetta M., Meneghetti F., De Rossi A., Chieco-Bianchi L. Regression of AIDS-related Kaposi's sarcoma following antiretroviral therapy with protease inhibitors: biological correlates of clinical outcome. Eur. J. Cancer 1999, 35:1809-1815.
23. Piriou E., Jansen C.A., van Dort K., De Cuyper I., Nanlohy N.M., Lange J.M., van Oers M.H., Miedema F., van Baarle D. Reconstitution of EBV latent but not lytic antigen-specific CD4+ and CD8+ T cells after HIV treatment with highly active antiretroviral therapy. J. Immunol. 2005, 175:2010-2017.
24. Panagiotakis S.H., Soufla G., Baritaki S., Sourvinos G., Passam A., Zagoreos I., Stavrianeas N., Spandidos D.A. Concurrent CMV and EBV DNAemia is significantly correlated with a delay in the response to HAART in treatment-naive HIV type 1-positive patients. AIDS Res. Hum. Retroviruses 2007, 23:10-18.
25. Jansen C.A., Piriou E., De Cuyper I.M., van Dort K., Lange J.M., Miedema F., van Baarle D. Long-term highly active antiretroviral therapy in chronic HIV-1 infection: evidence for reconstitution of antiviral immunity. Antivir. Ther. 2006, 11:105-116.
26. Rooney C M. New insights into EBV-associated post-transplant lymphoproliferative disease. Lancet 2003, 361:192-193.
27. Tanner J.E., Alfieri C. The Epstein-Barr virus and post-transplant lymphoproliferative disease: interplay of immunosuppression, EBV, and the immune system in disease pathogenesis. Transpl. Infect. Dis. 2001, 3:60-69.
28. Della Bella S., Nicola S., Brambilla L., Riva A., Ferrucci S., Presicce P., Boneschi V., Berti E., Villa M.L. Quantitative and functional defects of dendritic cells in classic Kaposi's sarcoma. Clin. Immunol. 2006, 119:317-329.
29. Cullen B.R. HIV-1 auxiliary proteins: making connections in a dying cell. Cell 1998, 93:685-692.
30. Freed E.O. HIV-1 replication. Somat. Cell Mol. Genet. 2001, 26:13-33.
31. Davison A.J., Eberle R., Ehlers B., Hayward G.S., McGeoch D.J., Minson A.C., Pellett P.E., Roizman B., Studdert M.J., Thiry E. The order Herpesvirales. Arch. Virol. 2009, 154:171-177.
32. Swaminathan S. Molecular biology of Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus. Semin. Hematol. 2003, 40:107-115.
33. Staudt M.R., Dittmer D.P. TheRta/Orf50 transactivator proteins of the gamma-herpesviridae. Curr. Top. Microbiol. Immunol. 2007, 312:71-100.
34. Brown H.J., Song M.J., Deng H., Wu T.T., Cheng G., Sun R. NF-kappaB inhibits gammaherpesvirus lytic replication. J. Virol. 2003, 77:8532-8540.
35. Raftery M., Müller A., Schönrich G. Herpesvirus homologues of cellular genes. Virus Genes 2000, 21:65-75.
36. A Thorley-Lawson D., Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N. Engl. J. Med. 2004, 350:1328-1337.
37. Thorley-Lawson D.A. EBV the prototypical human tumor virus - just how bad is it?. J. Allergy Clin. Immunol. 2005, 116:251-261.
38. Chang Y., Cesarman E., Pessin M.S., Lee F., Culpepper J., Knowles D.M., Moore P.S. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 1994, 266:1865-1869.
39. Soulier J., Grollet L., Oksenhendler E., Cacoub P., Cazals-Hatem D., Babinet P., d'Agay M.F., Clauvel J.P., Raphael M., Degos L. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 1995, 86:1276-1280.
40. Dittmer D., Lagunoff M., Renne R., Staskus K., Haase A., Ganem D. A cluster of latently expressed genes in Kaposi's sarcoma-associated Herpesvirus. J. Virol. 1998, 72:8309-8315.
41. Talbot S.J., Weiss R.A., Kellam P., Boshoff C. Transcriptional analysis of human herpesvirus-8 open reading frames 71, 72, 73, K14, and 74 in a primary effusion lymphoma cell line. Virology 1999, 257:84-94.
42. Sarid R., Wiezorek J.S., Moore P.S., Chang Y. Characterization and cell cycle regulation of the major Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) latent genes and their promoter. J. Virol. 1999, 73:1438-1446.
43. Ballestas M.E., Chatis P.A., Kaye K.M. Efficient persistence of extrachromosomal KSHV DNA Mediated by latency-associated nuclear antigen. Science 1999, 284:641-644.
44. Ballestas M.E., Kaye K.M. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mediates episome persistence through cis-acting terminal repeat (TR) sequence and specifically binds TR DNA. J. Virol. 2001, 75:3250-3258.
45. Friborg J.J., Kong W., Hottiger M.O., Nabel G.J. p53 inhibition by the LANA protein of KSHV protects against cell death. Nature 1999, 402:889-894.
46. Fujimuro M., Hayward S.D. The latency-associated nuclear antigen of Kaposi's Sarcoma-associated herpesvirus manipulates the activity of glycogen synthase kinase-3β. J. Virol. 2003, 77:8019-8030.
47. Fujimuro M., Liu J., Zhu J., Yokosawa H., Hayward S.D. Regulation of the interaction between glycogen synthase kinase 3 and the Kaposi's Sarcoma-associated herpesvirus latency-associated nuclear antigen. J. Virol. 2005, 79:10429-10441.
48. Verma S.C., Borah S., Robertson E.S. Latency-associated nuclear antigen of Kaposi's Sarcoma-associated herpesvirus up-regulates transcription of human telomerase reverse transcriptase promoter through interaction with transcription factor Sp1. J. Virol. 2004, 78:10348-10359.
49. Knight J.S., Cotter M.A., Robertson E.S. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus transactivates the telomerase reverse transcriptase promoter. J. Biol. Chem. 2001, 276:22971-22978.
50. Zaldumbide A., Ossevoort M., Wiertz E.J.H.J., Hoeben R.C. In cis inhibition of antigen processing by the latency-associated nuclear antigen I of Kaposi sarcoma herpes virus. Mol. Immunol. 2007, 44:1352-1360.
51. Kwun H.J., da Silva S.R., Shah I.M., Blake N., Moore P.S., Chang Y. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mimics Epstein-Barr virus EBNA1 immune evasion through central repeat domain effects on protein processing. J. Virol. 2007, 81:8225-8235.
52. Thome M., Schneider P., Hofmann K., Fickenscher H., Meinl E., Neipel F., Mattmann C., Burns K., Bodmer J.L., Schröter M., Scaffidi C., Krammer P.H., Peter M.E., Tschopp J. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 1997, 386:517-521.
53. Matta H., Mazzacurati L., Schamus S., Yang T., Sun Q., Chaudhary P.M. Kaposi's Sarcoma-associated herpesvirus (KSHV) oncoprotein K13 bypasses TRAFs and directly interacts with the IkappaB kinase complex to selectively activate NF-kappaB without JNK activation. J. Biol. Chem. 2007, 282:24858-24865.
54. Guasparri I., Keller S.A., Cesarman E. KSHV vFLIP is essential for the survival of infected lymphoma cells. J. Exp. Med. 2004, 199:993-1003.
55. Sun Q., Matta H., Chaudhary P.M. The human herpes virus 8-encoded viral FLICE inhibitory protein protects against growth factor withdrawal-induced apoptosis via NF-kappa B activation. Blood 2003, 101:1956-1961.
56. Verschuren E.W., Jones N., Evan G.I. The cell cycle and how it is steered by Kaposi's sarcoma-associated herpesviruscyclin. J. Gen. Virol. 2004, 85:1347-1361.
57. Mocroft A., Kirk O., Clumeck N., Gargalianos-Kakolyris P., Trocha H., Chentsova N., Antunes F., Stellbrink H.-J., Phillips A.N., Lundgren J.D. The changing pattern of Kaposi sarcoma in patients with HIV, 1994-2003. The EuroSIDA study. Cancer 2004, 100:2644-2654.
58. Dedicoat M., Newton R. Review of the distribution of Kaposi's sarcoma-associated herpesvirus (KSHV) in Africa in relation to the incidence of Kaposi's sarcoma. Brit. J. Cancer 2003, 88:1-3.
59. Mesri E.A., Cesarman E., Boshoff C. Kaposi's sarcoma and its associated Herpesvirus. Nat. Rev. Cancer 2010, 10:707-719.
60. Chen Y.B., Rahemtullah A., Hochberg E. Primary effusion lymphoma. Oncologist 2007, 12:569-576.
61. Münz C., Moormann A. Immune escape by Epstein-Barr virus associated malignancies. Semin. Cancer Biol. 2008, 18:381-387.
62. Lee H.R., Lee S., Chaudhary P.M., Gill P., Jung J.U. Immune evasion by Kaposi's sarcoma-associated herpesvirus. Future Microbiol. 2010, 5:1349-1365.
63. van Baarle D., Nanlohy N.M., Otto S., Plunkett F.J., Fletcher J.M., Akbar A.N. Progressive telomere shortening of Epstein-Barr virus-specific memory T cells during HIV infection: contributor to exhaustion?. J. Infect. Dis. 2008, 198:1353-1357.
64. Boivin G., Gaudreau A., Routy J.P. Evaluation of the human herpesvirus 8 DNA load in blood and Kaposi's sarcoma skin lesions from AIDS patients on highly active antiretroviral therapy. AIDS 2000, 14:1907-1910.
65. Babcock G.J., Decker L.L., Volk M., Thorley-Lawson D.A. EBV persistence in memory B cells in vivo. Immunity 1998, 9:395-404.
66. Bekker V., Scherpbier H., Beld M., Piriou E., van Breda A., Lange J., van Leth F., Jurriaans S., Alders S., Wertheim-van Dillen P., van Baarle D., Kuijpers T. Epstein-Barr virus infects B and non-B lymphocytes in HIV-1-infected children and adolescents. J. Infect. Dis. 2006, 194:1323-1330.
67. Tremblay M., Meloche S., Sekaly R.P., Wainberg M.A. Complement receptor 2 mediates enhancement of human immunodeficiency virus 1 infection in Epstein-Barr virus-carrying B cells. J. Exp. Med. 1990, 171:1791-1796.
68. Staskus K.A., Sun R., Miller G., Racz P., Jaslowski A., Metroka C., Brett-Smith H., Haase A.T. Cellular tropism and viral interleukin-6 expression distinguish human herpesvirus 8 involvement in Kaposi's sarcoma, primary effusion lymphoma, and multicentric Castleman's disease. J. Virol. 1999, 73:4181-4187.
69. Stebbing J., Gazzard B., Douek D.C. Where does HIV live?. N. Engl. J. Med. 2004, 350:1872-1880.
70. Blasig C., Zietz C., Haar B., Neipel F., Esser S., Brockmeyer N.H., Tschachler E., Colombini S., Ensoli B., Sturzl M. Monocytes in Kaposi's sarcoma lesions are productively infected by human herpesvirus 8. J. Virol. 1997, 71:7963-7968.
71. Aoki Y., Tosato G. HIV-1 Tat enhances Kaposi sarcoma-associated herpesvirus (KSHV) infectivity. Blood 2004, 104:810-814.
72. Merat R., Amara A., Lebbe C., de The H., Morel P., Saib A. HIV-1 infection of primary effusion lymphoma cell line triggers Kaposi's sarcoma-associated herpesvirus (KSHV) reactivation. Int. J. Cancer 2002, 97:791-795.
73. Mercader M., Nickoloff B.J., Foreman K.E. Induction of human immunodeficiency virus 1 replication by human herpesvirus 8. Arch. Pathol. Lab. Med. 2001, 125:785-789.
74. Caselli E., Galvan M., Cassai E., Caruso A., Sighinolfi L., Di Luca D. Human herpesvirus 8 enhances human immunodeficiency virus replication in acutely infected cells and induces reactivation in latently infected cells. Blood 2005, 106:2790-2797.
75. Scala G., Quinto I., Ruocco M.R., Mallardo M., Ambrosino C., Squitieri B., Tassone P., Venuta S. Epstein-Barr virus nuclear antigen 2 transactivates the long terminal repeat of human immunodeficiency virus type 1. J. Virol. 1993, 67:2853-2861.
76. Zhang R.D., Guan M., Park Y., Tawadros R., Yang J.Y., Gold B., Wu B., Henderson E.E. Synergy between human immunodeficiency virus type 1 and Epstein-Barr virus in T lymphoblastoid cell lines. AIDS Res. Hum. Retroviruses 1997, 13:161-171.
77. Colombrino E., Rossi E., Ballon G., Terrin L., Indraccolo S., Chieco-Bianchi L., De Rossi A. Human immunodeficiency virus type 1 Tat protein modulates cell cycle and apoptosis in Epstein-Barr virus-immortalized B cells. Exp. Cell Res. 2004, 295:539-548.
78. Lin J.C. The Epstein-Barr virus DNA polymerase transactivates the human immunodeficiency virus type 1.5' long terminal repeat. Biochem. Biophys. Res. Commun. 1993, 195:242-249.
79. Hammarskjöld M.L., Simurda M.C. Epstein-Barr virus latent membrane protein transactivates the human immunodeficiency virus type 1 long terminal repeat through induction of NF-kappa B activity. J. Virol. 1992, 66:6496-6501.
80. Markovitz D.M., Kenney S., Kamine J., Smith M.S., Davis M., Huang E.S., Rosen C., Pagano J.S. Disparate effects of two herpesvirus [corrected] immediate-early gene trans-activators on the HIV-1 LTR. Virology 1989, 173:750-754.
81. Kenney S., Kamine J., Markovitz D., Fenrick R., Pagano J. An Epstein-Barr virus immediate-early gene product trans-activates gene expression from the human immunodeficiency virus long terminal repeat. Proc. Natl. Acad. Sci. USA 1988, 85:1652-1656.
82. Quinlivan E.B., Holley-Guthrie E., Mar E.C., Smith M.S., Kenney S. The Epstein-Barr virus BRLF1 immediate-early gene product transactivates the human immunodeficiency virus type 1 long terminal repeat by a mechanism which is enhancer independent. J. Virol. 1990, 64:1817-1820.
83. Mallon R., Borkowski J., Albin R., Pepitoni S., Schwartz J., Kieff E. The Epstein-Barr virus BZLF1 gene product activates the human immunodeficiency virus type 1.5' long terminal repeat. J. Virol. 1990, 64:6282-6285.
84. Hyun T.S., Subramanian C., Cotter M.A., II, Thomas R.A., Robertson E.S. Latency-associated nuclear antigen encoded by Kaposi's Sarcoma-associated herpesvirus interacts with tat and activates the long terminal repeat of human immunodeficiency virus type 1 in human cells. J. Virol. 2001, 75:8761-8771.
85. Renne R., Barry C., Dittmer D., Compitello N., Brown P.O., Ganem D. Modulation of cellular and viral gene expression by the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus. J. Virol. 2001, 75:458-468.
86. Huang L.M., Chao M.F., Chen M.Y., Shih H.M., Chiang Y.P., Chuang C.Y., Lee C.Y. Reciprocal regulatory interaction between human herpesvirus 8 and human immunodeficiency virus type 1. J. Biol. Chem. 2001, 276:13427-13432.
87. de Oliveira D.E., Ballon G., Cesarman E. NF-kappaB signaling modulation by EBV and KSHV. Trends Microbiol. 2010, 18:248-257.
88. Sun Q., Matta H., Chaudhary P. Kaposi's sarcoma associated herpes virus-encoded viral FLICE inhibitory protein activates transcription from HIV-1 long terminal repeat via the classical NF-kappaB pathway and functionally cooperates with Tat. Retrovirology 2005, 2:9-23.
89. Fiorelli V., Gendelman R., Sirianni M.C., Chang H.K., Colombini S., Markham P.D., Monini P., Sonnabend J., Pintus A., Gallo R.C., et al. Gamma-interferon produced by CD8+ T cells infiltrating Kaposi's Sarcoma induces spindle cells with angiogenic phenotype and synergy with human immunodeficiency virus-1 Tat protein: an immune response to human herpesvirus-8 infection?. Blood 1998, 91:956-967.
90. Albini A., Soldi R., Giunciuglio D., Giraudo E., Benelli R., Primo L., Noonan D., Salio M., Camussi G., Rockl W., Bussolino F. The angiogenesis induced by HIV-1 tat protein is mediated by the Flk-1/KDR receptor on vascular endothelial cells. Nat. Med. 1996, 2:1371-1375.
91. Ensoli B., Barillari G., Salahuddin S.Z., Gallo R.C., Wong-Staal F. Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 1990, 345:84-86.
92. Ensoli B., Gendelman R., Markham P., Fiorelli V., Colombini S., Raffeld M., Cafaro A., Chang H.K., Brady J.N., Gallo R.C. Synergy between basic fibroblast growth factor and HIV-1 Tat protein in induction of Kaposi's sarcoma. Nature 1994, 371:674-680.
93. Prakash O., Tang Z.Y., He Y.E., Ali M.S., Coleman R., Gill J., Farr G., Samaniego F. Human Kaposi's sarcoma cell-mediated tumorigenesis in human immunodeficiency type 1 tat-expressing transgenic mice. J. Natl. Cancer Inst. 2000, 92:721-728.
94. Barillari G., Gendelman R., Gallo R.C., Ensoli B. The Tat protein of human immunodeficiency virus type 1, a growth factor for AIDS Kaposi sarcoma and cytokine-activated vascular cells, induces adhesion of the same cell types by using integrin receptors recognizing the RGD amino acid sequence. Proc. Natl. Acad. Sci. USA 1993, 90:7941-7945.
95. Barillari G., Sgadari C., Fiorelli V., Samaniego F., Colombini S., Manzari V., Modesti A., Nair B.C., Cafaro A., Sturzl M., et al. The Tat protein of human immunodeficiency virus type-1 promotes vascular cell growth and locomotion by engaging the alpha 5beta 1 and alpha vbeta 3 integrins and by mobilizing sequestered basic fibroblast growth factor. Blood 1999, 94:663-672.
96. Rahman M.A., Kingsley L.A., Atchison R.W., Belle S., Breinig M.C., Ho M., Rinaldo C.R. Reactivation of Epstein-Barr virus during early infection with human immunodeficiency virus. J. Clin. Microbiol. 1991, 29:1215-1220.
97. Legoff J., Amiel C., Calisonni O., Fromentin D., Rajoely B., Abuaf N., Tartour E., Rozenbaum W., Bélec L., Nicolas J.C. Early impairment of CD8+ T cells immune response against Epstein-Barr virus (EBV) antigens associated with high level of circulating mononuclear EBV DNA load in HIV infection. J. Clin. Immunol. 2004, 24:125-134.
98. Astrin S.M., Laurence J. Human immunodeficiency virus activates c-myc and Epstein-Barr virus in human B lymphocytes. Ann. N.Y. Acad. Sci. 1992, 651:422-432.
99. Caselli E., Menegazzi P., Bracci A., Galvan M., Cassai E., Di Luca D. Human herpesvirus-8 (Kaposi's sarcoma-associated herpesvirus) ORF50 interacts synergistically with the tat gene product in transactivating the human immunodeficiency virus type 1 LTR. J. Gen. Virol. 2001, 82:1965-1970.
100. Caselli E., Galvan M., Santoni F., Rotola A., Caruso A., Cassai E., Luca D.D. Human herpesvirus-8 (Kaposi's sarcoma-associated virus) ORF50 increases in vitro cell susceptibility to human immunodeficiency virus type 1 infection. J. Gen. Virol. 2003, 84:1123-1131.
101. Varthakavi V., Smith R.M., Deng H., Sun R., Spearman P. Human immunodeficiency virus type-1 activates lytic cycle replication of Kaposi's sarcoma-associated herpesvirus through induction of KSHV Rta. Virology 2002, 297:270-280.
102. Zeng Y., Zhang X., Huang Z., Cheng L., Yao S., Qin D., Chen X., Tang Q., Lv Z., Zhang L., Lu C. Intracellular Tat of human immunodeficiency virus type 1 activates lytic cycle replication of Kaposi's sarcoma-associated herpesvirus: role of JAK/STAT signaling. J. Virol. 2007, 81:2401-2417.
103. Varthakavi V., Browning P.J., Spearman P. Human immunodeficiency virus replication in a primary effusion lymphoma cell line stimulates lytic-phase replication of Kaposi's sarcoma-associated Herpesvirus. J. Virol. 1999, 73:10329-10338.
104. Guo H.G., Pati S., Sadowska M., Charurat M., Reitz M. Tumorigenesis by human herpesvirus 8 vGPCR is accelerated by human immunodeficiency virus type 1 Tat. J. Virol. 2004, 78:9336-9342.
105. Pati S., Foulke J.S., Barabitskaya O., Kim J., Nair B.C., Hone D., Smart J., Feldman R.A., Reitz M. Human herpesvirus 8-encoded vGPCR activates nuclear factor of activated T cells and collaborates with human immunodeficiency virus type 1 Tat. J. Virol. 2003, 77:5759-5773.
106. Yen-Moore A., Hudnall S.D., Rady P.L., Wagner R.F., Moore T.O., Memar O., Hughes T.K., Tyring S.K. Differential expression of the HHV-8 vGCR cellular homolog gene in AIDS-associated and classic Kaposi's sarcoma: potential role of HIV-1 Tat. Virology 2000, 267:247-251.
107. Chen X., Cheng L., Jia X., Zeng Y., Yao S., Lv Z., Qin D., Fang X., Lei Y., Lu C. Human immunodeficiency virus type 1 Tat accelerates Kaposi sarcoma-associated herpesvirusKaposin A-mediated tumorigenesis of transformed fibroblasts in vitro as well as in nude and immunocompetent mice. Neoplasia 2009, 11:1272-1284.
108. Moore P.S., Gao S.J., Dominguez G., Cesarman E., Lungu O., Knowles D.M., Garber R., Pellett P.E., McGeoch D.J., Chang Y. Primary characterization of a herpesvirus agent associated with Kaposi's sarcoma. J. Virol. 1996, 70:549-558.
109. Boshoff C., Endo Y., Collins P.D., Takeuchi Y., Reeves J.D., Schweickart V.L., Siani M.A., Sasaki T., Williams T.J., Gray P.W., Moore P.S., Chang Y., Weiss R.A. Angiogenic and HIV-inhibitory functions of KSHV-encoded chemokines. Science 1997, 278:290-294.
110. Stine J.T., Wood C., Hill M., Epp A., Raport C.J., Schweickart V.L., Endo Y., Sasaki T., Simmons G., Boshoff C., Clapham P., Chang Y., Moore P., Gray P.W., Chantry D. KSHV-encoded CC chemokine vMIP-III is a CCR4 agonist, stimulates angiogenesis, and selectively chemoattracts TH2 cells. Blood 2000, 95:1151-1157.
111. Jiang Y., Xu D., Zhao Y., Zhang L. Mutual inhibition between Kaposi's sarcoma-associated herpesvirus and Epstein-Barr virus lytic replication initiators in dually-infected primary effusion lymphoma. PLoS One 2008, 3:e1569.
112. Xu D., Coleman T., Zhang J., Fagot A., Kotalik C., Zhao L., Trivedi P., Jones C., Zhang L. Epstein-Barr virus inhibits Kaposi's sarcoma-associated herpesvirus lytic replication in primary effusion lymphomas. J. Virol. 2007, 81:6068-6078.
113. Spadavecchia S., Gonzalez-Lopez O., Carroll K.D., Palmeri D., Lukac D.M. Convergence of Kaposi's sarcoma-associated herpesvirus reactivation with Epstein-Barr virus latency and cellular growth mediated by the notch signaling pathway in coinfected cells. J. Virol. 2010, 84:10488-10500.
114. Uchida J., Yasui T., Takaoka-Shichijo Y., Muraoka M., Kulwichit W., Raab-Traub N., Kikutani H. Mimicry of CD40 signals by Epstein-Barr virus LMP1 in B lymphocyte responses. Science 1999, 286:300-303.
115. Krithivas A., Young D.B., Liao G., Greene D., Hayward S.D. Human herpesvirus 8 LANA interacts with proteins of the mSin3 corepressor complex and negatively regulates Epstein-Barr virus gene expression in dually infected PEL cells. J. Virol. 2000, 74:9637-9645.
116. J.D. Novak, A.J. Cañas, The Theory Underlying Concept Maps and How to Construct Them, Technical Report IHMC CmapTools 2006-01 Rev 01-2008, Florida Institute for Human and Machine Cognition, 2008. <>. http://cmap.ihmc.us/Publications/ResearchPapers/TheoryUnderlyingConceptMaps.pdf.