Herpesvirus saimiri as a model for gammaherpesvirus oncogenesis

Seminars in Cancer Biology

Volumn 9, Issue 3, 1999, Pages 231-239

  Jung, Jae U ^a   Choi, Joong Kook ^a   Ensser, Armin ^b   Biesinger, Brigitte ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

Animal model; Herpesvirus saimiri; Oncogene; Transformation; Virus encoded cellular homologues

Indexed keywords

INTERLEUKIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; CARCINOGENESIS; CELL CULTURE; CELL GROWTH; HERPES VIRUS INFECTION; HERPES VIRUS SAIMIRI; LYMPHOCYTE TRANSFORMATION; LYMPHOPROLIFERATIVE DISEASE; NONHUMAN; PRIMATE; PROTO ONCOGENE; RABBIT; REVIEW; SIGNAL TRANSDUCTION; SPECIES; T LYMPHOCYTE;

EID: 0033022846     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1006/scbi.1998.0115     Document Type: Article

References (98)

1. Fleckenstein, B, Desrosiers, RC, 1982.
2. Johnson DR, Jondal M. Herpesvirus ateles and herpesvirus saimiri transform marmoset T cells into continuously proliferating cell lines that can mediate natural killer cell-like cytotoxicity. Proc Natl Acad Sci USA. 78:1981;6391-6395.
3. Neubauer RH, Briggs CJ, Noer KB, Rabin H. Identification of normal and transformed lymphocyte subsets of nonhuman primates with monoclonal antibodies to human lymphocytes. J Immunol. 130:1983;1323-1329.
4. Bertram KA, Pearson GR. Natural killer cells in relation to Herpesvirus saimiri-induced disease course and manifestations in owl monkeys. J Natl Cancer Inst. 70:1983;147-155.
5. Adolf GR. Lymphokines produced by herpesvirus-transformed marmoset monkey lymphoid cell lines. I. Characterization of a constitutively produced interferon. Virology. 137:1984;195-200.
6. Medveczky PG, Medveczky MM. Expression of interleukin 2 receptors in T cells transformed by strains of Herpesvirus saimiri representing three DNA subgroups. Intervirology. 30:1989;213-226.
7. Alexander L, Du Z, Rosenzweig M, Jung JU, Desrosiers RC. A role for natural simian immunodeficiency virus and human immunodeficiency virus type 1 nef alleles in lymphocyte activation. J Virol. 71:1997;6094-6099.
8. Ablashi DV, Schirm S, Fleckenstein B, Faggioni A, Dahlberg J, Rabin H, Loeb W, Armstrong G, Peng JW, Aulahk G. Herpesvirus saimiri-induced lymphoblastoid rabbit cell line: growth characteristics, virus persistence, and oncogenic properties. J Virol. 55:1985;623-633.
9. Rabin H, Hopkins RF, Desrosiers RC, Ortaldo JR, Djeu JY, Neubauer RH. Transformation of owl monkey T cells in vitro with Herpesvirus saimiri. Proc Natl Acad Sci USA. 81:1984;4563-4567.
10. Desrosiers RC, Silva DP, Waldron LM, Letvin NL. Nononcogenic deletion mutants of herpesvirus saimiri are defective for in vitro immortalization. J Virol. 57:1986;701-705.
11. Falk L, Johnson D, Deinhardt F. Transformation of marmoset lymphocytes in vitro with Herpesvirus ateles. Int J Cancer. 21:1978;652-657.
12. Kiyotaki M, Desrosiers RC, Letvin NL. Herpesvirus saimiri strain 11 immortalizes a restricted marmoset T8 lymphocyte subpopulation in vitro. J Exp Med. 164:1986;926-931.
13. +marmoset lymphocyte with NK function. J Immunol. 140:1988;730-736.
14. Medveczkyy P, Szomolanyi E, Desrosiers RC, Mulder C. Classification of herpesvirus saimiri into three groups based on extreme variation in a DNA region required for oncogenicity. J Virol. 52:1984;938-944.
15. Szomolanyi E, Medveczky P, Mulder C. In vitro immortalization of marmoset cells with three subgroups of herpesvirus sairairi. J Virol. 61:1987;3485-3490.
16. Biesinger B, Muller-Fleckenstein I, Simmer B, Lang G, Wittmann S, Platzer E, Desrosiers RC, Fleckenstein B. Stable growth transformation of human T lymphocytes by herpesvirus saimiri. Proc Natl Acad Sci USA. 89:1992;3116-3119.
17. Akari H, Mori K, Terao K, Otani I, Fukasawa M, Mukai R, Yoshikawa Y. In vitro immortalization of Old World monkey T lymphocytes with Herpesvirus saimiri: its susceptibility to infection with simian immunodeficiency viruses. Virology. 218:1996;382-388.
18. Feldmann G, Fickenscher H, Bodemer W, Spring M, Nißlein T, Hunsmann G, Dittmer U. Generation of herpes virus saimiri-transformed T-cell lines from macaques is restricted by reactivation of simian spuma viruses. Virology. 229:1997;106-112.
19. Meinl E, Fickenscher H, Hoch RM, Malefyt RD, de Waal M, Hart BA, Wekerle H, Hohlfeld R, Fleckenstein B. Growth transformation of antigen-specific T cell lines from rhesus monkeys by herpesvirus saimiri. Virology. 229:1997;175-182.
20. Yasukawa M, Inoue Y, Kimura N, Fujita S. Immortalization of human T cells expressing T-cell receptor gamma delta by herpesvirus saimiri. J Virol. 69:1995;8114-8117.
21. +intrathymic precursors in vitro. Int Immunol. 8:1996;1797-1805.
22. Klein JL, Fickenscher H, Holliday JE, Biesinger B, Fleckenstein B. Herpesvirus saimiri immortalized gamma delta T cell line activated by IL-12. J Immunol. 156:1996;2754-2760.
23. Mittrucker HW, Muller-Fleckenstein I, Fleckenstein B, Fleischer B. CD2-mediated autocrine growth of herpes virus saimiri-transformed human T lymphocytes. J Exp Med. 176:1992;909-913.
24. +cytotoxic T lymphocytes. J Virol. 67:1993;6317-6321.
25. Broker BM, Tsygankov AY, Muller-Fleckenstein I, Guse AH, Chitaev NA, Biesinger B, Fleckenstein B, Emmrich F. Immortalization of human T cell clones by Herpesvirus saimiri. Signal transduction analysis reveals functional CD3, CD4, and IL-2 receptors. J Immunol. 151:1993;1184-1192.
26. Broker BM, Tsygankov AY, Fickenscher H, Chitaev NA, Muller-Fleckenstein I, Fleckenstein B, Bolen JB, Emmrich F, SchuIze-Koops H. Engagement of the CD4 receptor inhibits the interleukin-2-dependent proliferation of human T cells transformed by Herpesvirus saimiri. Eur J Immunol. 24:1994;843-850.
27. Mittrucker HW, Muller-Fleckenstein I, Fleckenstein B, Fleischer B. Herpes virus saimiri-transformed human T lymphocytes: normal functional phenotype and preserved T cell receptor signalling. Int Immunol. 5:1993;985-990.
28. Weber F, Meinl E, Drexler K, Czlonkowska A, Huber S, Fickenscher H, Muller-Fleckenstein I, Fleckenstein B, Wekerle H, Hohlfeld R. Transformation of human T-cell clones by Herpesvirus saimiri: intact antigen recognition by autonomously growing myelin basic protein-specific T cells. Proc Natl Acad Sci USA. 90:1993;11049-11053.
29. De Carli M, Berthold S, Fickenscher H, Fleckenstein IM, D'Elios MM, Gao Q, Biagiotti R, Giudizi MG, Kalden JR, Fleckenstein B. Immortalization with herpesvirus saimiri modulates the cytokine secretion profile of established Th1 and Th2 human T cell clones. J Immunol. 151:1993;5022-5030.
30. +T cell clones. Role for membrane TNF-alpha/TNF-alpha receptors and CD2/CD58 interactions. J Immunol. 153:1994;4872-4879.
31. +T cells can provide polyclonal B cell help via the CD40 ligand as well as the TNF-alpha pathway and through release of lymphokines. J Immunol. 157:1996;3876-3885.
32. Albrecht JC, Nicholas J, Biller D, Cameron KR, Biesinger B, Newman C, Wittmann S, Craxton MA, Coleman H, Fleckenstein B. Primary structure of the herpesvirus saimiri genome. J Virol. 66:1992;5047-5058.
33. Neipel, F, Albrecht, JC, Fleckenstein, B, 1997, 4187, 4192.
34. Desrosiers RC, Burghoff RL, Bakker A, Kamine J. Construction of replication competent Herpesvirus saimiri deletion mutants. J Virol. 49:1984;343-348.
35. Grassmann R, Fleckenstein B. Selectable recombinant herpesvirus saimiri is capable of persisting in a human T-cell line. J Virol. 63:1989;1818-1821.
36. Duboise SM, Guo J, Desrosiers RC, Jung JU. Use of virion DNA as a cloning vector for the construction of mutant and recombinant herpesviruses. Proc Natl Acad Sci USA. 93:1996;11389-11394.
37. Knappe A, Hiller C, Thurau M, Wittmann S, Hofmann H, Fleckenstein B, F ickenscher H. The superantigen- homologous viral immediate-early gene ie 14/vsag in herpesvirus saimiri-transformed human T cells. J Virol. 71:1997;9124-9133.
38. Koomey JM, Mulder C, Burghoff RL, Fleckenstein B, Desrosiers RC. Deletion of DNA sequence in a nononcogenic variant of Herpesvirus saimiri. J Virol. 50:1984;662-665.
39. Desrosiers RC, Bakker A, Kamine J, Falk LA, Hunt RD, King NW. A region of the Herpesvirus saimiri genome required for oncogenicity. Science. 228:1985;184-187.
40. Murthy SC, Trimble JJ, Desrosiers RC. Deletion mutants of herpes virus saimiri define an open reading frame necessary for transformation. J Virol. 63:1989;3307-3314.
41. Biesinger B, Trimble JJ, Desrosiers RC, Fleckenstein B. The divergence between two oncogenic Herpesvirus saimiri strains in a genomic region related to the transforming phenotype. Virology. 176:1990;505-514.
42. Geck P, Whitaker SA, Medveczky MM, Medveczky PG. Expression of collagenlike sequences by a tumor virus, herpesvirus saimiri. J Virol. 64:1990;3509-3515.
43. Jung JU, Trimble JJ, King NW, Biesinger B, Fleckenstein BW, Desrosiers RC. Identification of transforming genes of subgroup A and C strains of Herpesvirus saimiri. Proc Natl Acad Sci U S A. 88:1991;7051-7055.
44. Kretschmer C, Murphy C, Biesinger B, Beckers J, Fickenscher H, Kirchner T, Fleckenstein B, Ruther U. A Herpes saimiri oncogene causing peripheral T-cell lymphoma in transgenic mice. Oncogene. 12:1996;1609-1616.
45. Lee H, Trimble JJ, Yoon DW, Regier D, Desrosiers RC, Jung JU. Genetic variation of herpesvirus saimiri subgroup A transforming protein and its association with cellular src. J Virol. 71:1997;3817-3825.
46. Fickenscher H, Biesinger B, Knappe A, Wittmann S, Fleckenstein B. Regulation of the herpesvirus saimiri oncogene stpC, similar to that of T-cell activation genes, in growth-transformed human T lymphocytes. J Virol. 70:1996;6012-6019.
47. Medveczky MM, Geck P, Vassallo R, Medveczky PG. Expression of the collagen-like putative oncoprotein of Herpesvirus saimiri in transformed T cells. Virus Genes. 7:1993;349-365.
48. Biesinger B, Tsygankov AY, Fickenscher H, Emmrich F, Fleckenstein B, Bolen JB, Broker BM. The product of the Herpesvirus saimiri open reading frame 1 (tip) interacts with T cell-specific kinase p56lck in transformed cells. J Biol Chem. 270:1995;4729-4734.
49. Jung JU, Lang SM, Jun T, Roberts TM, Veillette A, Desrosiers RC. Downregulation of Lck-mediated signal transduction by tip of herpesvirus saimiri. J Virol. 69:1995;7814-7822.
50. Lund T, Medveczky MM, Geck P, Medveczky PG. A herpesvirus saimiri protein required for interleukin-2 independence is associated with membranes of transformed T cells. J Virol. 69:1995;4495-4499.
51. Fickenscher H, Bokel C, Knappe A, Biesinger B, Meinl E, Fleischer B, F leckenstein B, Broker BM. Functional phenotype of transformed human alphabeta and gammadelta T cells determined by different subgroup C strains of herpesvirus Saimiri. J Virol. 71:1997;2252-2263.
52. Duboise SM, Guo J, Czajak S, Desrosiers RC, Jung JU. STP and Tip are essential for herpesvirus saimiri oncogenicity. J Virol. 72:1998;1308-1313.
53. Jung JU, Desrosiers RC. Identification and characterization of the herpesvirus saimiri oncoprotein STP-C488. J Virol. 65:1991;6953-6960.
54. Jung JU, Desrosiers RC. Distinct functional domains of STP-C488 of herpesvirus saimiri. Virology. 204:1994;751-758.
55. Jung JU, Desrosiers RC. Herpesvirus saimiri oncogene STP-C488 encodes a phosphoprotein. J Virol. 66:1992;1777-1780.
56. Murphy C, Kretschmer C, Biesinger B, Beckers J, Jung J, Desrosiers RC, Muller-Hermelink HK, Fleckenstein BW, Ruther U. Epithelial tumours induced by a herpesvirus oncogene in transgenic mice. Oncogene. 9:1994;221-226.
57. Jung JU, Desrosiers RC. Association of the viral oncoprotein STP-C488 with cellular ras. Mol Cell Biol. 15:1995;6506-6512.
58. Guo J, Williams K, Duboise SM, Alexander L, Veazey R, Jung JU. S ubstitution of ras for the herpesvirus saimiri STP oncogene in lymphocyte transformation. J Virol. 72:1998;3698-3704.
59. Lee, H, Choi, JK, Guo, J, Mosialos, G, Kaye, K, Kieff, E, Jung, JU, 1998.
60. 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. 80:1995;389-399.
61. Lund T, Medveczky MM, Neame PJ, Medveczky PG. A herpesvirus saim iri membrane protein required for interleukin-2 independence forms a stable complex with p56lck. J Virol. 70:1996;600-606.
62. Jung JU, Lang SM, Friedrich U, Jun T, Roberts TM, Desrosiers RC, Biesi nger B. Identification of Lck-binding elements in tip of herpesvirus saimiri. J Biol Chem. 270:1995;20660-20667.
63. Wiese N, Tsygankov AY, Klauenberg U, Bolen JB, Fleischer B, Broker BM. Selective activation of T cell kinase p56lck by Herpesvirus saimiri protein tip. J Biol Chem. 271:1996;847-852.
64. Lund T, Medveczky MM, Medveczky PG. Herpesvirus saimiri Tip-484 membrane protein markedly increases p56lck activity in T cells. J Virol. 71:1997;378-382.
65. Guo J, Duboise M, Lee H, Li M, Choi JK, Rosenzweig M, Jung JU. Enhanced downregulation of Lck-mediated signal transduction by a Y114 mutation of herpesvirus Saimiri tip. J Virol. 71:1997;7092-7096.
66. Duboise SM, Lee H, Guo J, Choi JK, Czajak S, Simon M, Desrosiers RC, J ung JU. Mutation of the Lck-binding motif of Tip enhances lymphoid cell activation by herpesvirus saimiri. J Virol. 72:1998;2607-2614.
67. Yoon DW, Lee H, Seol W, DeMaria M, Rosenzweig M, Jung JU. Tap: a novel cellular protein that interacts with tip of herpesvirus saimiri and induces lymphocyte aggregation. Immunity. 6:1997;571-582.
68. Gruter P, Tabernero C, von Kobbe Q, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber BK, Izaurralde E. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell. 1:1998;649-659.
69. Murthy S, Kamine J, Desrosiers RC. Viral-encoded small RNAs in herpes virus saimiri induced tumors. EMBO J. 5:1986;1625-1632.
70. Geck P, Whitaker SA, Medveczky MM, Last TJ, Medveczky PG. Small RNA expression from the oncogenic region of a highly oncogenic strain of herpesvirus saimiri. Virus Genes. 8:1994;25-34.
71. Lee SI, Steitz JA. Herpesvirus saimiri U RNAs are expressed and assembled into ribonucleoprotein particles in the absence of other viral genes. J Virol. 64:1990;3905-3915.
72. Myer VE, Lee SI, Steitz JA. Viral small nuclear ribonucleoproteins bind a protein implicated in messenger RNA destabilization. Proc Natl Acad Sci U S A. 89:1992;1296-1300.
73. Geck P, Medveczky MM, Chou CS, Brown A, Cus J, Medveczky PG. Herpesvirus saimiri small RNA and interleukin-4 mRNA AUUUA repeats compete for sequence-specific factors including a novel 70K protein. J Gen Virol. 75:1994;2293-2301.
74. Lang G, Fleckenstein B. trans activation of the thymidylate synthase promoter of herpesvirus saimiri. J Virol. 64:1990;5333-5341.
75. Fodor WL, Rollins SA, Bianco-Caron S, Rother RP, Guilmette ER, Burton WV, Albrecht JC, Fleckenstein B, Squinto SP. The complement control protein homolog of herpesvirus saimiri regulates serum complement by inhibiting C3 convertase activity. J Virol. 69:1995;3889-3892.
76. Bramley JC, Davies A, Lachmann PJ. Herpesvirus saimiri CD59-baculovirus expression and characterisation of complement inhibitory activity. Biochem Soc: Trans. 25:1997;354.
77. Rouvier E, Luciani MF, Mattei MG, Denizot F, Golstein P. CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. J Immunol. 150:1993;5445-5456.
78. Fossiez F, Banchereau J, Murray R, Van Kooten C, Garrone P, Lebecque S. Interleukin-17. Int Rev Immunol. 16:1998;541-551.
79. Yao Z, Fanslow WC, Seldin MF, Rousseau AM, Painter SL, Comeau MR, Cohen JI, Spriggs MK. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity. 3:1995;811-821.
80. Knappe A, Hiller C, Niphuis H, Fossiez F, Thurau M, Wittmann S, Kuhn E M, Lebecque S, Banchereau J, Rosenwirth B, Fleckenstein B, Heeney J, Fickenscher H. The interleukin-17 gene of herpesvirus saimiri. J Virol. 72:1998;5797-5801.
81. Thomson W, Nicholas J. Superantigen function. Nature 35. 1:1991;530.
82. Yao Z, Maraskovsky E, Spriggs MK, Cohen JI, Armitage RJ, Alderson MR. Herpesvirus saimiri open reading frame 14, a protein encoded by T lymphotropic herpesvirus, binds to MW class II molecules and stimulates T cell proliferation. J Immunol. 156:1996;3260-3266.
83. Knappe A, Thurau M, Niphuis H, Hiller C, Wittmann S, Kuhn EM, Rosenwirth B, Fleckenstein B, Heeney J, Fickenscher H. T-cell lymphoma caused by herpesvirus saimiri C488 independently of ie 14/vsag, a viral gene with superantigen homology. J Virol. 72:1998;3469-3471.
84. Duboise M, Guo J, Czajak S, Lee H, Veazey R, Desrosiers RC, Jung JU. A role for herpesvirus saimiri orf14 in transformation and persistent infe ction. J Virol. 72:1998;6770-6776.
85. Nava VE, Cheng EH, Veliuona M, Zou S, Clem RJ, Mayer ML, Hardwick JM. Herpesvirus saimiri encodes a functional homolog of the human bcl-2 oncog ene. J Virol. 71:1997;4118-4122.
86. Derfuss T, Fickenscher H, Kraft MS, Henning G, Lengenfelder D, Fleckenstein B, Meinl E. Antiapoptotic activity of the herpesvirus saimiri-encoded Bcl-2 homolog: stabilization of mitochondria and inhibition of caspase-3-like activity. J Virol. 72:1998;5897-5904.
87. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, Scaffidi C, Krammer PH, Peter ME, Tschopp J. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature. 386:1997;517-521.
88. Wallach D. Apoptosis. Placing death under control. Nature. 388:1997;123.
89. Nicholas J, Cameron KR, Honess RW. Herpesvirus saimiri encodes homologues of G protein-coupled receptors and cyclins. Nature. 355:1992;362-365.
90. Jung JU, Stager M, Desrosiers RC. Virus-encoded cyclin. Mol Cell Biol. 14:1994;7235-7244.
91. Swanton C, Mann DJ, Fleckenstein B, Neipel F, Peters G, Jones N. Herpes viral cyclin/CA6 complexes evade inhibition by CDK inhibitor proteins. Nature. 390:1997;184-187.
92. Schulze-Gahmen, U, Jung, JU, Kim, SH, 1999.
93. Ahuja SK, Murphy PM. Molecular piracy of mammalian interleukin-8 receptor type B by herpesvirus saimiri. J Biol Chem. 268:1993;20691-20694.
94. Murphy PM. The molecular biology of leukocyte chemoattractant re ceptors. Annu Rev Immunol. 12:1994;593.
95. Kilger E, Kieser A, Baumann M, Hammerschmidt W. Epstein-Barr vir us-mediated B-cell proliferation is dependent upon latent membrane protein 1, which simulates an activated CD40 receptor. EMBO J. 17:1998;1700-1709.
96. Miller CL, Burkhardt AL, Lee JH, Stealey B, Longnecker R, Bolen JB, Kieff E. Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases. Immunity. 2:1995;155-166.
97. Lee H, Veazey R, Williams K, Li M, Guo J, Neipel F, Fleckenstein B, Lackner A, Desrosiers RC, Jung JU. Deregulation of cell growth by the K1 gene of Kaposi's sarcoma-associated herpesvirus. Nat Med. 4:1998;435-440.
98. Desrosiers RC, Sasseville VG, Czajak SC, Zhang X, Mansfield KG, Kaur A, Johnson RP, Lackner AA, Jung JU. A herpesvirus of rhesus monkeys related to the human Kaposi's sarcoma-associated herpesvirus. J Virol. 71:1997;9764-9769.