Interleukin 2 receptor signaling regulates the perforin gene through signal transducer and activator of transcription (Stat)5 activation of two enhancers

Journal of Experimental Medicine

Volumn 190, Issue 9, 1999, Pages 1297-1307

  Zhang, Jin ^a   Scordi, Irinoulla ^a   Smyth, Mark J ^b   Lichtenheld, Mathias G ^a  

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

^b AUSTIN RESEARCH INSTITUTE   (Australia)

Author keywords

Cytotoxic T lymphocyte; IL 2 receptor; Perforin; T cell activation; Transgenic mouse

Indexed keywords

INTERLEUKIN 2 RECEPTOR; PERFORIN; STAT5 PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE INDUCTION; GENE LOCUS; GENE TARGETING; HELPER CELL; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; CELL LINE; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; INTERLEUKIN-2; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; MILK PROTEINS; MOLECULAR SEQUENCE DATA; PORE FORMING CYTOTOXIC PROTEINS; RECEPTORS, INTERLEUKIN-2; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSFECTION;

EID: 0033231511     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.9.1297     Document Type: Article

References (63)

1. Liu, C.C., S. Rafii, A. Granelli-Piperno, J.A. Trapani, and J.D. Young. 1989. Perforin and serine esterase gene expression in stimulated human T cells. Kinetics, mitogen requirements, and effects of cyclosporin A. J. Exp. Med. 170:2105-2118.
2. + T cells. J. Exp. Med. 171:1269-1281.
3. + T cells. J. Immunol. 148: 3354-3360.
4. Dennert, G., and E.R. Podack. 1983. Cytolysis by H-2-specific T killer cells. Assembly of tubular complexes on target membranes. J. Exp. Med. 157:1483-1495.
5. Shiver, J.W., L. Su, and P.A. Henkart. 1992. Cytotoxicity with target DNA breakdown by rat basophilic leukemia cells expressing both cytolysin and granzyme A. Cell. 71:315-322.
6. Henkart, P.A. 1994. Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. Immunity. 1:343-346.
7. Kagi, D., B. Ledermann, K. Burki, P. Seiler, B. Odermatt, K.J. Olsen, E.R. Podack, R.M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature. 369:31-37.
8. Rossi, C.P., A. McAllister, M. Tanguy, D. Kagi, and M. Brahic. 1998. Theiler's virus infection of perforin-deficient mice. J. Virol. 72:4515-4519.
9. + T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity. Eur. J. Immunol. 24:3068-3072.
10. van den Broek, M.E., D. Kagi, F. Ossendorp, R. Toes, S. Vamvakas, W.K. Lutz, C.J. Melief, R.M. Zinkernagel, and H. Hengartner. 1996. Decreased tumor surveillance in perforin-deficient mice. J. Exp. Med. 184:1781-1790.
11. + T cells. J. Exp. Med. 186:1407-1418.
12. Geisberg, M., L.A. Terry, N. Flomenberg, and B. Dupont. 1992. Cytotoxic and proliferative allospecific T-cell clones contain perforin and mediate anti-CD3-induced cytotoxicity. Hum. Immunol. 35:239-245.
13. Smyth, M.J., Y. Norihisa, and J.R. Ortaldo. 1992. Multiple cytolytic mechanisms displayed by activated human peripheral blood T cell subsets. J. Immunol. 148:55-62.
14. Gamero, A.M., D. Ussery, D.S. Reintgen, C.A. Puleo, and J.Y. Djeu. 1995. Interleukin 15 induction of lymphokine-activated killer cell function against autologous tumor cells in melanoma patient lymphocytes by a CD18-dependent, perforin-related mechanism. Cancer Res. 55:4988-4994.
15. Ye, W., J.D. Young, and C.C. Liu. 1996. Interleukin-15 induces the expression of mRNAs of cytolytic mediators and augments cytotoxic activities in primary murine lymphocytes. Cell. Immunol. 174:54-62.
16. Waldmann, T., Y. Tagaya, and R. Bamford. 1998. Interleukin-2, interleukin-15, and their receptors. Int. Rev. Immunol. 16:205-226.
17. + T cells in vivo by IL-15. Immunity. 8:591-599.
18. Suzuki, H., T.M. Kundig, C. Furlonger, A. Wakeham, E. Timms, T. Matsuyama, R. Schmits, J.J. Simard, P.S. Ohashi, H. Griesser, et al. 1995. Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor β. Science. 268:1472-1476.
19. Youn, B.S., K.K. Kim, and B.S. Kwon. 1996. A critical role of Sp1- and Ets-related transcription factors in maintaining CTL-specific expression of the mouse perforin gene. J. Immunol. 157:3499-3509.
20. Koizumi, H., M.F. Horta, B.S. Youn, K.C. Fu, B.S. Kwon, J.D. Young, and C.C. Liu. 1993. Identification of a killer cell-specific regulatory element of the mouse perforin gene: an Ets-binding site-homologous motif that interacts with Ets-related proteins. Mol. Cell. Biol. 13:6690-6701.
21. Horta, M.F., K.C. Fu, H. Koizumi, J.D. Young, and C.C. Liu. 1996. Cell-free conversion of a ubiquitous nuclear protein into a killer-cell-specific form that binds to the NF-P enhancer element of the mouse perforin gene. Eur. J. Biochem. 238:639-646.
22. Lichtenheld, M.G., and E.R. Podack. 1992. Structure and function of the murine perforin promoter and upstream region. Reciprocal gene activation or silencing in perforin positive and negative cells. J. Immunol. 149:2619-2626.
23. Zhang, Y., and M.G. Lichtenheld. 1997. Non-killer cell-specific transcription factors silence the perforin promoter. J. Immunol. 158:1734-1741.
24. Lichtenheld, M.G., E.R. Podack, and R.B. Levy. 1995. Transgenic control of perforin gene expression. Functional evidence for two separate control regions. J. Immunol. 154:2153-2163.
25. Conzelmann, A., P. Corthesy, M. Cianfriglia, A. Silva, and M. Nabholz. 1982. Hybrids between rat lymphoma and mouse T cells with inducible cytolytic activity. Nature. 298: 170-172.
26. Garcia-Sanz, J.A., and E.R. Podack. 1993. Regulation of perforin gene expression in a T cell hybrid with inducible cytolytic activity. Eur. J. Immunol. 23:1877-1883.
27. Willerford, D.M., J. Chen, J.A. Ferry, L. Davidson, A. Ma, and F.W. Alt. 1995. Interleukin-2 receptor alpha chain regulates the size and content of the peripheral lymphoid compartment. Immunity. 3:521-530.
28. Cepero, E., H.J. Hnatyszyn, G. Kraus, and M.G. Lichtenheld. 1998. Potent inhibition of CTLA-4 expression by an anti-CTLA-4 ribozyme. Biochem. Biophys. Res. Commun. 247: 838-843.
29. Roberts, S., and D.L. Bentley. 1992. Distinct modes of transcription read through or terminate at the c-myc attenuator. EMBO (Eur. Mol. Biol. Organ.) J. 11:1085-1093.
30. Lichtenheld, M.G., and E.R. Podack. 1989. Structure of the human perforin gene. A simple gene organization with interesting potential regulatory sequences. J. Immunol. 143:4267-4274.
31. Makrigiannis, A.P., and D.W. Hoskin. 1997. Inhibition of CTL induction by rapamycin: IL-2 rescues granzyme B and perforin expression but only partially restores cytotoxic activity. J. Immunol. 159:4700-4707.
32. Moriggl, R., V. Gouilleux-Gruart, R. Jahne, S. Berchtold, C. Gartmann, X. Liu, L. Hennighausen, A. Sotiropoulos, B. Groner, and F. Gouilleux. 1996. Deletion of the carboxyl-terminal transactivation domain of MGF-Stat5 results in sustained DNA binding and a dominant negative phenotype. Mol. Cell. Biol. 16:5691-5700.
33. Quandt, K., K. Frech, H. Karas, E. Wingender, and T. Werner. 1995. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 23:4878-4884.
34. Berchtold, S., R. Moriggl, F. Gouilleux, O. Silvennoinen, C. Beisenherz, E. Pfitzner, M. Wissler, E. Stocklin, and B. Groner. 1997. Cytokine receptor-independent, constitutively active variants of STAT5. J. Biol. Chem. 272:30237-30243.
35. Leonard, W.J., and J.J. O'Shea. 1998. Jaks and STATs: biological implications. Annu. Rev. Immunol. 16:293-322.
36. Horvath, C.M., and J.E. Darnell. 1997. The state of the STATs: recent developments in the study of signal transduction to the nucleus. Curr. Opin. Cell. Biol. 9:233-239.
37. Gaffen, S.L., S.Y. Lai, W. Xu, F. Gouilleux, B. Groner, M.A. Goldsmith, and W.C. Greene. 1995. Signaling through the interleukin 2 receptor β chain activates a STAT-5-like DNA-binding activity. Proc. Natl. Acad. Sci. USA. 92:7192-7196.
38. Bright, J.J., L.D. Kerr, and S. Sriram. 1997. TGF-β inhibits IL-2-induced tyrosine phosphorylation and activation of Jak-1 and Stat 5 in T lymphocytes. J. Immunol. 159:175-183.
39. + suppressor T cell, NY4.2, in the prevention of autoimmune IDDM in NOD mice. J. Autoimmun. 10:299-307.
40. + T lymphocytes. Inhibition by transforming growth factor-β. J. Immunol. 146:3289-3297.
41. Teglund, S., C. McKay, E. Schuetz, J.M. van Deursen, D. Stravopodis, D. Wang, M. Brown, S. Bodner, G. Grosveld, and J.N. Ihle. 1998. Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell. 93:841-850.
42. Moriggl, R., D.J. Topham, S. Teglund, V. Sexl, C. McKay, D. Wang, A. Hoffmeyer, J. van Deursen, M.Y. Sangster, K.D. Bunting, et al. 1999. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity. 10:249-259.
43. Nakajima, H., X.W. Liu, A. Wynshaw-Boris, L.A. Rosenthal, K. Imada, D.S. Finbloom, L. Hennighausen, and W.J. Leonard. 1997. An indirect effect of Stat5a in IL-2-induced proliferation: a critical role for Stat5a in IL-2-mediated IL-2 receptor a chain induction. Immunity. 7:691-701.
44. Imada, K., E.T. Bloom, H. Nakajima, J.A. Horvath-Arcidiacono, G.B. Udy, H.W. Davey, and W.J. Leonard. 1998. Stat5b is essential for natural killer cell-mediated proliferation and cytolytic activity. J. Exp. Med. 188:2067-2074.
45. Fujii, H., K. Ogasawara, H. Otsuka, M. Suzuki, K. Yamamura, T. Yokochi, T. Miyazaki, H. Suzuki, T.W. Mak, S. Taki, et al. 1998. Functional dissection of the cytoplasmic sub-regions of the IL-2 receptor β chain in primary lymphocyte populations. EMBO (Eur. Mol. Biol. Organ.) J. 17:6551-6557.
46. Yu, C.R., J.R. Ortaldo, R.E. Curiel, H.A. Young, S.K. Anderson, and P. Gosselin. 1999. Role of a STAT binding site in the regulation of the human perforin promoter. J. Immunol. 162:2785-2790.
47. Akaishi, H., K. Takeda, T. Kaisho, R. Shineha, S. Satomi, J. Takeda, and S. Akira. 1998. Defective IL-2-mediated IL-2 receptor α chain expression in Stat3-deficient T lymphocytes. Int. Immunol. 10:1747-1751.
48. Nakata, M., M.J. Smyth, Y. Norihisa, A. Kawasaki, Y. Shinkai, K. Okumura, and H. Yagita. 1990. Constitutive expression of pore-forming protein in peripheral blood γ/δ T cells: implication for their cytotoxic role in vivo. J. Exp. Med. 172: 1877-1880.
49. Koizumi, H., C.C. Liu, L.M. Zheng, S.V. Joag, N.K. Bayne, J. Holoshitz, and J.D. Young. 1991. Expression of perforin and serine esterases by human γ/δ T cells. J. Exp. Med. 173: 499-502.
50. Guy-Grand, D., M. Malassis-Seris, C. Briottet, and P. Vassalli. 1991. Cytotoxic differentiation of mouse gut thymodependent and independent intraepithelial T lymphocytes is induced locally. Correlation between functional assays, presence of perforin and granzyme transcripts, and cytoplasmic granules. J. Exp. Med. 173:1549-1552.
51. Suzuki, H., G.S. Duncan, H. Takimoto, and T.W. Mak. 1997. Abnormal development of intestinal intraepithelial lymphocytes and peripheral natural killer cells in mice lacking the IL-2 receptor β chain. J. Exp. Med. 185:499-505.
52. Lodolce, J.P., D.L. Boone, S. Chai, R.E. Swain, T. Dassopoulos, S. Trettin, and A. Ma. 1998. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity. 9:669-676.
53. Sperisen, P., S.M. Wang, E. Soldaini, M. Pla, C. Rusterholz, P. Bucher, P. Corthesy, P. Reichenbach, and M. Nabholz. 1995. Mouse interleukin-2 receptor α gene expression. Interleukin-1 and interleukin-2 control transcription via distinct cis-acting elements. J. Biol. Chem. 270:10743-10753.
54. John, S., C.M. Robbins, and W.J. Leonard. 1996. An IL-2 response element in the human IL-2 receptor α chain promoter is a composite element that binds Stat5, Elf-1, HMG-I(Y) and a GATA family protein. EMBO (Eur. Mol. Biol. Organ.) J. 15: 5627-5635.
55. Meyer, W.K., P. Reichenbach, U. Schindler, E. Soldaini, and M. Nabholz. 1997. Interaction of STATS dimers on two low affinity binding sites mediates interleukin 2 (IL-2) stimulation of IL-2 receptor α gene transcription. J. Biol. Chem. 272:31821-31828.
56. Serdobova, I., M. Pla, P. Reichenbach, P. Sperisen, J. Ghysdael, A. Wilson, J. Freeman, and M. Nabholz. 1997. Elf-1 contributes to the function of the complex interleukin (IL)-2-responsive enhancer in the mouse IL-2 receptor α gene. J. Exp. Med. 185:1211-1221.
57. John, S., U. Vinkemeier, E. Soldaini, J.E. Darnell, Jr., and W.J. Leonard. 1999. The significance of tetramerization in promoter recruitment by Stat5. Mol. Cell. Biol. 19:1910-1918.
58. Duncliffe, K.N., A.G. Bert, M.A. Vadas, and P.N. Cockerill. 1997. A T cell-specific enhancer in the interleukin-3 locus is activated cooperatively by Oct and NFAT elements within a DNase I-hypersensitive site. Immunity. 6:175-185.
59. Trouche, D., P. Robin, O. Robillard, P. Sassone-Corsi, and A. Harel-Bellan. 1991. c-fos transcriptional activation by IL-2 in mouse CTL-L2 cells is mediated through two distinct signal transduction pathways converging on the same enhancer element. J. Immunol. 147:2398-2403.
60. Feuerstein, N., D. Huang, S.H. Hinrichs, D.J. Orten, N. Aiyar, and M.B. Prystowsky. 1995. Regulation of cAMP-responsive enhancer binding proteins during cell cycle progression in T lymphocytes stimulated by IL-2. J. Immunol. 154:68-79.
61. Arima, N., W.A. Kuziel, T.A. Grdina, and W.C. Greene. 1992. IL-2-induced signal transduction involves the activation of nuclear NF-κB expression. J. Immunol. 149:83-91.
62. Georgopoulos, K., S. Winandy, and N. Avitahl. 1997. The role of the Ikaros gene in lymphocyte development and homeostasis. Annu. Rev. Immunol. 15:155-176.
63. Spits, H., B. Blom, A.C. Jaleco, K. Weijer, M.C. Verschuren, J.J. van Dongen, M.H. Heemskerk, and P.C. Res. 1998. Early stages in the development of human T, natural killer and thymic dendritic cells. Immunol. Rev. 165:75-86.