DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites

Molecular and Cellular Biology

Volumn 20, Issue 1, 2000, Pages 389-401

  Soldaini, Elisabetta ^a,d   John, Susan ^a   Moro, Stefano ^b,e   Bollenbacher, Julie ^a   Schindler, Ulrike ^c   Leonard, Warren J ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c AMGEN INC   (United States)

^d CHIRON VACCINES   (Italy)

^e UNIVERSITY OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; STAT5 PROTEIN;

ARTICLE; BINDING SITE; DNA SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 0033988447     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.1.389-401.2000     Document Type: Article

References (41)

1. Azam, M., H. Erdjument-Bromage, B. L. Kreider, M. Xia, F. Quelle, R. Basu, C. Saris, P. Tempst, J. N. Ihle, and C. Schindler. 1995. Interleukin-3 signals through multiple isoforms of Stat5. EMBO J. 14:1402-1411.
2. Baldwin, A. S. J. 1987. Methylation interference assay for analysis of DNA-protein interactions, p. 12.3.1-12.3.4. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 2. Greene Publishing Associates/ Wiley-Interscience, New York, N.Y.
3. Beadling, C., J. Ng, J. W. Babbage, and D. A. Cantrell. 1996. Interleukin-2 activation of STAT5 requires the convergent action of tyrosine kinases and a serine/threonine kinase pathway distinct from the Raf1/ERK2 MAP kinase pathway. EMBO J. 15:101-112.
4. Becker, S., B. Groner, and C. W. Muller. 1998. Three-dimensional structure of the Stat3β homodimer bound to DNA. Nature 394:145-151.
5. Bergad, P. L., H.-M. Shih, H. C. Towle, S. J. Schwarzenberg, and S. A. Berry. 1995. Growth hormone induction of hepatic serine protease inhibitor 2.1 transcription is mediated by a Stat5-related factor binding synergistically to two γ-activated sites. J. Biol. Chem. 270:24903-24910.
6. Boucheron, C., S. Dumon, S. C. R. Santos, R. Moriggl, L. Hennighausen, S. Gisselbrecht, and F. Gouilieux. 1998. A single amino acid in the DNA binding regions of STAT5A and STAT5B confers distinct DNA binding specificities. J. Biol. Chem. 273:33936-33941.
7. Chen, X., U. Vinkemeier, Y. Zhao, D. Jeruzalmi, J. E. Darnell, Jr., and J. Kuriyan. 1998. Crystal structure of a tyrosine phosphorylated STAT-1 dimer bound to DNA. Cell 93:827-839.
8. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
9. Decker, T., P. Kovarik, and A. Meinke. 1997. GAS elements: A few nucleotides with a major impact on cytokine-induced gene expression. J. Interferon Cytokine Res. 17:121-134.
10. Grillot, D. A. M., M. González-García, D, Ekhterae, L. Duan, N. Inohara, S. Otha, M. F. Seldin, and G. Núñez. 1997. Genomic organization, promoter region analysis, and chromosome localization of the mouse bcl-x gene. J. Immunol. 158:4750-4757.
11. Horvath, C. M., Z. Wen, and J. E. Darnell, Jr. 1995. A STAT protein domain that determines DNA sequence recognition suggests a novel DNA-binding domain. Genes Dev. 9:984-994.
12. Hou, J., U. Schindler, W. J. Henzel, S. C. Wong, and McKnight. 1995. Identification and purification of human Stat proteins activated in response to interleukin-2. Immunity 2:321-329.
13. Ihle, J. N. 1996. STATs: signal transducers and activators of transcription. Cell 84:331-334.
14. Imada, K., E. T. Bloom, H. Nakajima, J. A. Horvath-Arcidiacono, G. B. Udy, H. Davey, and W. J. Leonard. 1998. Stat5b is essential for natural killer cell-mediated proliferation and cytolytic activity. J. Exp. Med. 188:2067-2074.
15. 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.
16. Laskowski, R. A., M. W. Macarthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
17. Leonard, W. J., and J. J. O'Shea. 1998. Jaks and STATs: Biological implications. Annu. Rev. Immunol. 16:293-322.
18. Levitt, M., M. Hirshberg, R. Sharon, and V. Daggett. 1995. Potential-energy function and parameters for simulations of the molecular-dynamics of proteins and nucleic-acids in solution. Comput. Phys. Commun. 91:215-231.
19. Lin, J.-X., J. Mietz, W. S. Modi, S. John, and W. J. Leonard. 1996. Cloning of human Stat5B. Reconstitution of interleukin-2-induced Stat5A and Stat5B DNA binding activity in COS-7 cells. J. Biol. Chem. 271:10738-10744.
20. Liu, X., G. W. Robinson, F. Gouilleux, B. Groner, and L. Hennighausen. 1995. Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proc. Natl. Acad. Sci. USA 92:8831-8835.
21. Liu, X., G. W. Robinson, K. U. Wagner, L. Garrett, A. Wynshaw-Boris, and L. Hennighausen. 1997. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev. 9:2266-2278.
22. Meeker, T. C., J. Loeb, M. Ayres, and W. Sellers. 1990. The human Pim-1 gene is selectively transcribed in different hemato-lymphoid cell lines in spite of a G+C-rich housekeeping promoter. Mol. Cell. Biol. 10:1680-1688.
23. Meyer, W. K.-H., P. Reichenbach, U. Schindler, E. Soldaini, and M. Nabholz. 1997. Interaction of STAT5 dimers on two low affinity binding sites mediates interleukin 2 (IL-2) stimulation of 1L-2 receptor a gene transcription. J. Biol. Chem. 272:31821-31828.
24. Mohamadi, F., N. G. J. Richards, W. C. Guida, R. Liskamp, M. Lipton, C. Caufield, G. Chang, T. Hendrickson, and W. C. Still. 1990. MacroModel-An integrated software system for modeling organic and bioorganic molecules using molecular mechanics. J. Comput. Chem. 11:440-450.
25. Moriggl, R., D. J. Topham, S. Teglund, V. Sexl, C. McKay, D. Wang, A. Hoffmeyer, J. van Deursen, M. Y. Sangster, K. D. Bunting, G. C. Grosveld, and J. N. Ihle. 1999. Stat5 is required for IL-2-induced cell cycle progression of peripheral T cells. Immunity 10:249-259.
26. Mui, A. L., H. Wakao, A. M. O'Farrell, N. Harada, and A. Miyajima. 1995. Interleukin-3, granulocyte-macrophage colony stimulating factor and interleukin-5 transduce signals through two STAT5 homologues. EMBO J. 14: 1166-1175.
27. 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.
28. Needleman, S. B., and C. D. Wunsch. 1970. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48:443-453.
29. Pollock, R., and R. Treisman. 1990. A sensitive method for the determination of protein-DNA binding specificities. Nucleic Acids Res. 18:6197-6204.
30. Schindler, U., P. Wu, M. Rothe, M. Brasseur, and S. L. McKnight. 1995. Components of a Stat recognition code: evidence for two layers of molecular selectivity. Immunity 2:689-697.
31. Silva, C. M., and H. Lu. 1996. Characterization and cloning of STAT5 from IM-9 cells and its activation by growth hormone. Mol. Endocrinol. 10:508-518.
32. -/- mice: a direct role for Stat5 in Bcl-X(L) induction. Cell 98:181-191.
33. Teglund, S., C. McKay, E. Schuetz, J. M. van Dursen, 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.
34. Tijan, R., and T. Maniatis. 1994. Transcriptional activation: a complex puzzle with few easy pieces. Cell 77:5-8.
35. Udy, G. B., R. P. Towers, R. G. Snell, R. J. Wilkins, S.-H. Park, P. A. Ram, D. J. Waxman, and H. W. Davey. 1997. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad. Sci. USA 94:7239-7244.
36. Verdier, F., R. Rabionet, F. Gouilleux, C. Beisenherz-Huss, P. Varlet, O. Muller, P. Mayeux, C. Lacombe, S. Gisselbrecht, and S. Chretien. 1998. A sequence of the CIS promoter interacts preferentially with two associated STAT5A dimers: a distinct biochemical difference between STAT5A and STAT5B. Mol. Cell. Biol. 18:5852-5860.
37. 2-terminal domains stabilizes binding of two dimers to tandem DNA sites. EMBO J. 15:5616-5626.
38. Vinkemeier, U., I. Moarefi, J. E. Darnell, Jr., and J. Kuriyan. 1998. Structure of the amino-terminal protein interaction domain of Stat4. Science 279: 1048-1052.
39. Weiner, S. J., P. A. Kollman, D. T. Nguyen, and D. A. Case. 1986. An all-atom force field for stimulation of protein and nucleic acids. J. Comput. Chem. 7:230-252.
40. Xu, X., Y.-L. Sun, and T. Hoey. 1996. Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science 273:794-797.
41. Ye, S.-K., K. Maki, T. Kitamura, S. Sunaga, K. Akashi, J. Domen, I. L. Weissman, T. Honjo, and K. Ikuta. 1999. Induction of germline transcription in the TCRγ locus by Stat5: implications for accessibility control by the IL-7 receptor. Immunity 11:213-223.