Activation of the STAT6 transcription factor in Jurkat T-cells by the herpesvirus saimiri Tip protein

Journal of General Virology

Volumn 93, Issue 2, 2012, Pages

  Kim, Yuri ^a   Kwon, Eun Kyung ^a   Jeon, Ju Hong ^a   So, Insuk ^a   Kim, In Gyu ^a   Choi, Myung Sik ^a,b   Kim, Ik Sang ^a,b   Choi, Joong Kook ^c   Jung, Jae Ung ^d   Cho, Nam Hyuk ^a,b  

^a Seoul National University College of Medicine   (South Korea)

^b Seoul National University Bundang Hospital   (South Korea)

^c Chungbuk National University College of Medicine   (South Korea)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; STAT6 PROTEIN; TYROSINE KINASE INTERACTING PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; PHOSPHOPROTEIN; STAT6 PROTEIN, HUMAN; TYROSINE KINASE INTERACTING PROTEIN, SAIMIRIINE HERPESVIRUS 2;

ARTICLE; CELL NUCLEUS; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; GENE EXPRESSION; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; HERPES VIRUS SAIMIRI; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; T CELL LYMPHOMA; T LYMPHOCYTE; TRANSCRIPTION INITIATION; ACTIVE TRANSPORT; IMMUNOLOGY; LEUKEMIA CELL LINE; METABOLISM; PATHOGENICITY; PROTEIN ANALYSIS; VIROLOGY; VIRUS CELL TRANSFORMATION;

HERPESVIRIDAE; PRIMATES; SAIMIRIINE HERPESVIRUS 2;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL TRANSFORMATION, VIRAL; HERPESVIRUS 2, SAIMIRIINE; HUMANS; JURKAT CELLS; PHOSPHOPROTEINS; PROTEIN INTERACTION MAPPING; STAT6 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 84855930919     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.036087-0     Document Type: Article

References (57)

1. Benekli, M., Baer, M. R., Baumann, H. & Wetzler, M. (2003). Signal transducer and activator of transcription proteins in leukemias. Blood 101, 2940-2954.
2. Biesinger, B., Müller-Fleckenstein, I., Simmer, B., Lang, G., Wittmann, S., Platzer, E., Desrosiers, R. C. & Fleckenstein, B. (1992). Stable growth transformation of human T lymphocytes by herpesvirus saimiri. Proc Natl Acad Sci U S A 89, 3116-3119.
3. Biesinger, B., Tsygankov, A. Y., Fickenscher, H., Emmrich, F., Fleckenstein, B., Bolen, J. B. & Bröker, B. M. (1995). The product of the Herpesvirus saimiri open reading frame 1 (Tip) interacts with T cellspecific kinase p56lck in transformed cells. J Biol Chem 270, 4729-4734.
4. Bild, A. H., Turkson, J. & Jove, R. (2002). Cytoplasmic transport of Stat3 by receptor-mediated endocytosis. EMBO J 21, 3255-3263.
5. Bowman, T., Garcia, R., Turkson, J. & Jove, R. (2000). STATs in oncogenesis. Oncogene 19, 2474-2488.
6. Bromberg, J. & Darnell, J. E., Jr (2000). The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19, 2468-2473.
7. Brown, S. & Zeidler, M. P. (2008). Unphosphorylated STATs go nuclear. Curr Opin Genet Dev 18, 455-460.
8. Cai, Q., Verma, S. C., Choi, J. Y., Ma, M. & Robertson, E. S. (2010). Kaposi's sarcoma-associated herpesvirus inhibits interleukin-4-mediated STAT6 phosphorylation to regulate apoptosis and maintain latency. J Virol 84, 11134-11144.
9. Chatterjee-Kishore, M., Kishore, R., Hicklin, D. J., Marincola, F. M. & Ferrone, S. (1998). Different requirements for signal transducer and activator of transcription 1alpha and interferon regulatory factor 1 in the regulation of low molecular mass polypeptide 2 and transporter associated with antigen processing 1 gene expression. J Biol Chem 273, 16177-16183.
10. Cho, N. H., Feng, P., Lee, S. H., Lee, B. S., Liang, X., Chang, H. & Jung, J. U. (2004). Inhibition of T cell receptor signal transduction by tyrosine kinase-interacting protein of Herpesvirus saimiri. J Exp Med 200, 681-687.
11. Cho, N. H., Kingston, D., Chang, H., Kwon, E. K., Kim, J. M., Lee, J. H., Chu, H., Choi, M. S., Kim, I. S. & Jung, J. U. (2006). Association of herpesvirus saimiri Tip with lipid raft is essential for downregulation of T-cell receptor and CD4 coreceptor. J Virol 80, 108-118.
12. Choi, J. K., Ishido, S. & Jung, J. U. (2000). The collagen repeat sequence is a determinant of the degree of herpesvirus saimiri STP transforming activity. J Virol 74, 8102-8110.
13. Cui, X., Zhang, L., Luo, J., Rajasekaran, A., Hazra, S., Cacalano, N. & Dubinett, S. M. (2007). Unphosphorylated STAT6 contributes to constitutive cyclooxygenase-2 expression in human non-small cell lung cancer. Oncogene 26, 4253-4260.
14. Deutsch, H. H. J., Koettnitz, K., Chung, J. & Kalthoff, F. S. (1995). Distinct sequence motifs within the cytoplasmic domain of the human IL-4 receptor differentially regulate apoptosis inhibition and cell growth. J Immunol 154, 3696-3703.
15. Duboise, S. M., Guo, J., Czajak, S., Desrosiers, R. C. & Jung, J. U. (1998). STP and Tip are essential for herpesvirus saimiri oncogenicity. J Virol 72, 1308-1313.
16. Ensser, A., Thurau, M., Wittmann, S. & Fickenscher, H. (2003). The genome of herpesvirus saimiri C488 which is capable of transforming human T cells. Virology 314, 471-487.
17. Guiter, C., Dusanter-Fourt, I., Copie-Bergman, C., Boulland, M. L., Le Gouvello, S., Gaulard, P., Leroy, K. & Castellano, F. (2004). Constitutive STAT6 activation in primary mediastinal large B-cell lymphoma. Blood 104, 543-549.
18. Hartley, D. A. & Cooper, G. M. (2000). Direct binding and activation of STAT transcription factors by the herpesvirus saimiri protein Tip. J Biol Chem 275, 16925-16932.
19. Hartley, D. A., Amdjadi, K., Hurley, T. R., Lund, T. C., Medveczky, P. G. & Sefton, B. M. (2000). Activation of the Lck tyrosine protein kinase by the herpesvirus saimiri tip protein involves two binding interactions. Virology 276, 339-348.
20. Haura, E. B., Turkson, J. & Jove, R. (2005). Mechanisms of disease: insights into the emerging role of signal transducers and activators of transcription in cancer. Nat Clin Pract Oncol 2, 315-324.
21. Heck, E., Lengenfelder, D., Schmidt, M., Müller-Fleckenstein, I., Fleckenstein, B., Biesinger, B. & Ensser, A. (2005). T-cell growth transformation by herpesvirus saimiri is independent of STAT3 activation. J Virol 79, 5713-5720.
22. Heck, E., Friedrich, U., Gack, M. U., Lengenfelder, D., Schmidt, M., Müller-Fleckenstein, I., Fleckenstein, B., Ensser, A. & Biesinger, B. (2006). Growth transformation of human T cells by herpesvirus saimiri requires multiple Tip-Lck interaction motifs. J Virol 80, 9934-9942.
23. Hou, J., Schindler, U., Henzel, W. J., Ho, T. C., Brasseur, M. & McKnight, S. L. (1994). An interleukin-4-induced transcription factor: IL-4 Stat. Science 265, 1701-1706.
24. Ilaria, R. L., Jr & Van Etten, R. A. (1996). P210 and P190(BCR/ABL) induce the tyrosine phosphorylation and DNA binding activity of multiple specific STAT family members. J Biol Chem 271, 31704-31710.
25. Johnston, J. A., Kawamura, M., Kirken, R. A., Chen, Y. Q., Blake, T. B., Shibuya, K., Ortaldo, J. R., McVicar, D. W. & O'Shea, J. J. (1994). Phosphorylation and activation of the Jak-3 Janus kinase in response to interleukin-2. Nature 370, 151-153.
26. Jung, J. U., Lang, S. M., Friedrich, U., Jun, T., Roberts, T. M., Desrosiers, R. C. & Biesinger, B. (1995). Identification of Lckbinding elements in Tip of herpesvirus saimiri. J Biol Chem 270, 20660-20667.
27. Jung, J. U., Choi, J. K., Ensser, A. & Biesinger, B. (1999). Herpesvirus saimiri as a model for gammaherpesvirus oncogenesis. Semin Cancer Biol 9, 231-239.
28. Keegan, A. D., Nelms, K., White, M., Wang, L. M., Pierce, J. H. & Paul, W. E. (1994). An IL-4 receptor region containing an insulin receptor motif is important for IL-4-mediated IRS-1 phosphorylation and cell growth. Cell 76, 811-820.
29. Kjellen, P., Amdjadi, K., Lund, T. C., Medveczky, P. G. & Sefton, B. M. (2002). The herpesvirus saimiri Tip484 and Tip488 proteins both stimulate lck tyrosine protein kinase activity in vivo and in vitro. Virology 297, 281-288.
30. Lee, H., Choi, J. K., Li, M., Kaye, K., Kieff, E. & Jung, J. U. (1999). Role of cellular tumor necrosis factor receptor-associated factors in NF-kB activation and lymphocyte transformation by herpesvirus saimiri STP. J Virol 73, 3913-3919.
31. Lee, B. S., Lee, S. H., Feng, P., Chang, H., Cho, N. H. & Jung, J. U. (2005). Characterization of the Kaposi's sarcoma-associated herpesvirus K1 signalosome. J Virol 79, 12173-12184.
32. Levy, D. E. & Darnell, J. E., Jr (2002). Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3, 651-662.
33. Li, W. X. (2008). Canonical and non-canonical JAK-STAT signaling. Trends Cell Biol 18, 545-551.
34. Lund, T. C., Garcia, R., Medveczky, M. M., Jove, R. & Medveczky, P. G. (1997). Activation of STAT transcription factors by herpesvirus saimiri Tip-484 requires p56lck. J Virol 71, 6677-6682.
35. Lund, T. C., Prator, P. C., Medveczky, M. M. & Medveczky, P. G. (1999). The Lck binding domain of herpesvirus saimiri Tip-484 constitutively activates Lck and STAT3 in T cells. J Virol 73, 1689-1694.
36. Min, C. K., Bang, S. Y., Cho, B. A., Choi, Y. H., Yang, J. S., Lee, S. H., Seong, S. Y., Kim, K. W., Kim, S. & other authors (2008). Role of amphipathic helix of a herpesviral protein in membrane deformation and T cell receptor downregulation. PLoS Pathog 4, e1000209.
37. Murata, T., Noguchi, P. D. & Puri, R. K. (1996). IL-13 induces phosphorylation and activation of JAK2 Janus kinase in human colon carcinoma cell lines: similarities between IL-4 and IL-13 signaling. J Immunol 156, 2972-2978.
38. Murphy, C., Kretschmer, C., Biesinger, B., Beckers, J., Jung, J., Desrosiers, R. C., Müller-Hermelink, H. K., Fleckenstein, B. W. & Rüther, U. (1994). Epithelial tumours induced by a herpesvirus oncogene in transgenic mice. Oncogene 9, 221-226.
39. Park, J., Lee, B. S., Choi, J. K., Means, R. E., Choe, J. & Jung, J. U. (2002). Herpesviral protein targets a cellular WD repeat endosomal protein to downregulate T lymphocyte receptor expression. Immunity 17, 221-233.
40. Park, J., Cho, N. H., Choi, J. K., Feng, P., Choe, J. & Jung, J. U. (2003). Distinct roles of cellular Lck and p80 proteins in herpesvirus saimiri Tip function on lipid rafts. J Virol 77, 9041-9051.
41. Qin, J. Z., Kamarashev, J., Zhang, C. L., Dummer, R., Burg, G. & Döbbeling, U. (2001). Constitutive and interleukin-7-and interleukin-15-stimulated DNA binding of STAT and novel factors in cutaneous T cell lymphoma cells. J Invest Dermatol 117, 583-589.
42. Reichel, M., Nelson, B. H., Greenberg, P. D. & Rothman, P. B. (1997). The IL-4 receptor alpha-chain cytoplasmic domain is sufficient for activation of JAK-1 and STAT6 and the induction of IL-4-specific gene expression. J Immunol 158, 5860-5867.
43. Ritz, O., Guiter, C., Castellano, F., Dorsch, K., Melzner, J., Jais, J. P., Dubois, G., Gaulard, P., Möller, P. & Leroy, K. (2009). Recurrent mutations of the STAT6 DNA binding domain in primary mediastinal B-cell lymphoma. Blood 114, 1236-1242.
44. Ryan, J. J., McReynolds, L. J., Keegan, A., Wang, L. H., Garfein, E., Rothman, P., Nelms, K. & Paul, W. E. (1996). Growth and gene expression are predominantly controlled by distinct regions of the human IL-4 receptor. Immunity 4, 123-132.
45. Shao, H., Xu, X., Mastrangelo, M. A., Jing, N., Cook, R. G., Legge, G. B. & Tweardy, D. J. (2004). Structural requirements for signal transducer and activator of transcription 3 binding to phosphotyrosine ligands containing the YXXQ motif. J Biol Chem 279, 18967-18973.
46. Sheng, H., Shao, J., Morrow, J. D., Beauchamp, R. D. & DuBois, R. N. (1998). Modulation of apoptosis and Bcl-2 expression by prostaglandin E2 in human colon cancer cells. Cancer Res 58, 362-366.
47. Shi, S., Larson, K., Guo, D., Lim, S. J., Dutta, P., Yan, S. J. & Li, W. X. (2008). Drosophila STAT is required for directly maintaining HP1 localization and heterochromatin stability. Nat Cell Biol 10, 489-496.
48. Skinnider, B. F., Elia, A. J., Gascoyne, R. D., Patterson, B., Trumper, L., Kapp, U. & Mak, T. W. (2002). Signal transducer and activator of transcription 6 is frequently activated in Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood 99, 618-626.
49. Stolina, M., Sharma, S., Lin, Y., Dohadwala, M., Gardner, B., Luo, J., Zhu, L., Kronenberg, M., Miller, P. W. & other authors (2000). Specific inhibition of cyclooxygenase 2 restores antitumor reactivity by altering the balance of IL-10 and IL-12 synthesis. J Immunol 164, 361-370.
50. Wehner, L. E., Schröder, N., Kamino, K., Friedrich, U., Biesinger, B. & Rüther, U. (2001). Herpesvirus saimiri Tip gene causes T-cell lymphomas in transgenic mice. DNA Cell Biol 20, 81-88.
51. Witthuhn, B. A., Silvennoinen, O., Miura, O., Lai, K. S., Cwik, C., Liu, E. T. & Ihle, J. N. (1994). Involvement of the Jak-3 Janus kinase in signalling by interleukins 2 and 4 in lymphoid and myeloid cells. Nature 370, 153-157.
52. Xu, F., Mukhopadhyay, S. & Sehgal, P. B. (2007). Live cell imaging of interleukin-6-induced targeting of 'transcription factor' STAT3 to sequestering endosomes in the cytoplasm. Am J Physiol Cell Physiol 293, C1374-C1382.
53. Yan, S. J., Lim, S. J., Shi, S., Dutta, P. & Li, W. X. (2011). Unphosphorylated STAT and heterochromatin protect genome stability. FASEB J 25, 232-241.
54. Yang, J. & Stark, G. R. (2008). Roles of unphosphorylated STATs in signaling. Cell Res 18, 443-451.
55. Yang, J., Liao, X., Agarwal, M. K., Barnes, L., Auron, P. E. & Stark, G. R. (2007). Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkB. Genes Dev 21, 1396-1408.
56. Yu, H., Pardoll, D. & Jove, R. (2009). STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9, 798-809.
57. Zhou, S., Shoelson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. G., King, F., Roberts, T., Ratnofsky, S. & other authors (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.