Tyrosine Phosphorylation of the Janus Kinase 2 Activation Loop Is Essential for a High-Activity Catalytic State but Dispensable for a Basal Catalytic State

Biochemistry

Volumn 43, Issue 14, 2004, Pages 4272-4283

  Chatti, Kiranam ^a   Farrar, William L ^b   Duhé, Roy J ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; CHEMICAL ACTIVATION; ENZYMES; MUTAGENESIS; PHYSIOLOGY; SIGNALING; SUBSTRATES;

INTRACELLULAR PROPAGATION; TYROSINE PHOSPHORYLATION;

CATALYSIS;

ADENOSINE TRIPHOSPHATE; CYTOKINE; GLUTAMIC ACID; JANUS KINASE 2; LYSINE; MUTANT PROTEIN; PHENYLALANINE; RECOMBINANT PROTEIN; TYROSINE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BACULOVIRUS EXPRESSION SYSTEM; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; BACULOVIRIDAE; CATALYSIS; ENZYME ACTIVATION; GENETIC VECTORS; JANUS KINASE 2; MODELS, CHEMICAL; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PHOSPHOTYROSINE; PRECIPITIN TESTS; PROTEIN KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SPODOPTERA; TYROSINE;

ANIMALIA; JANUS; UNIDENTIFIED BACULOVIRUS;

EID: 1842479256     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036109b     Document Type: Article

References (50)

1. Rodig, S. J., Meraz, M. A., White, J. M., Lampe, P. A., Riley, J. K., Arthur, C. D., King, K. L., Sheehan, K. C. F., Yin, L., Pennica, D., Johnson, E. M., Jr., and Schreiber, R. D. (1998) Disruption of the Jak1 gene demonstrates obligatory and non-redundant roles of the JAKs in cytokine-induced biological responses, Cell 93, 373-383.
2. Parganas, E., Wang, D., Stravopodis, D., Topham, D. J., Marine, J.-C., Teglund, S., Vanin, E. F., Bodner, S., Colamonici, O. R., van Deursen, J. M. A., Grosveld, G., and Ihle, J. N. (1998) JAK2 is essential for signaling through a variety of cytokine receptors, Cell 93, 385-395.
3. Neubauer, H., Cumano, A., Müller, M., Wu, H., Huffstadt, U., and Pfeffer, K. (1998) JAK2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis, Cell 93, 397-409.
4. Nosaka T., van Deursen, J. M. A., Tripp, R. A., Thierfelder, W. E., Witthuhn, B. A., McMickle, A. P., Doherty, P. C., Grosveld, Grrosveld, G.C., and Ihle, J.N. (1995) Defective lymphoid development in mice lacking JAK3, Science 270, 800-802.
5. Park, S. Y., Saijo, K., Takahashi, T., Osawa, M., Arase, H., Hirayama, N., Miyake, K., Nakauchi, H., Shirasawa, T., and Saito, T. (1995) Developmental defects of lymphoid cells in JAK3 kinase-deficient mice, Immunity 3, 771-782.
6. Thomis, D. C., Gurniak, C. B., Tivol, E., Sharpe, A. H., and Berg, L. J. (1995) Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking JAK3, Science 270, 794-797.
7. Shimoda, K., Kato, K., Aoki, K., Matsuda, T., Miyamoto, A., Shibamori, M., Yamashita, M., Numata, A., Takase, K., Kobayashi, S., Shibata, S., Asano, Y., Gondo, H., Sekiguchi, K., Nakayama, K., Nakayama, T., Okamura, T., Okamura, S., Niho, Y., and Nakayama, K. (2000) TYK2 plays a restricted role in IFNα signaling, although it is required for IL-12-mediated T cell function, Immunity 13, 561-571.
8. Karaghiosoff, M., Neubauer, H., Lassnig, C., Kovarik, P., Schindler, H., Pircher, H., McCoy, B., Bogdan, C., Decker, T., Brem, G., Pfeffer, K., and Müller, M. (2000) Partial impairment of cytokine responses in TYK2-deficient mice, Immunity 13, 549-560.
9. Rui, H., Kirken, R. A., and Farrar, W. L. (1994) Activation of receptor-associated tyrosine kinase JAK2 by Prolactin, J. Biol. Chem. 269, 5364-5368.
10. c chain sufficient for JAK kinase activation and induction of proliferation in T cells, Mol. Cell. Biol. 16, 309-317.
11. DaSilva, L., Howard, O. M. Z., Rui, H., Kirken, R. A., and Farrar, W. L. (1994) Growth signaling and JAK2 association mediated by membrane-proximal cytoplasmic regions of prolactin receptors, J. Biol. Chem. 269, 18267-18270.
12. c chain of the receptor for granulocyte-macrophage colony stimulating factor, and its activation requires the membrane-proximal region, Mol. Cell. Biol. 14, 4335-4341.
13. Zhuang, H., Niu, Z., He, T.-C., Patel, S. V., and Wojchowski, D. M. (1995) Erythropoietin-dependent inhibition of apoptosis is supported by carboxyl-truncated receptor forms and blocked by dominant-negative forms of JAK2, J. Biol. Chem. 270, 14500-14504.
14. Briscoe, J., Rogers, N. C., Witthuhn, B. A., Watling, D., Harpur, A. G., Wilks, A. F., Stark, G. R., Ihle, J. N., and Kerr, I. M. (1996) Kinase-negative mutants of JAK1 can sustain interferon-γ-inducible gene expression but not an antiviral state, EMBO J. 15, 799-809.
15. Krishnan, K., Pine, R., and Krolewski, J. J. (1997) Kinase-deficient forms of JAK1 and TYK2 inhibit interferon-α signaling in a dominant manner, Eur. J. Biochem. 247, 298-305.
16. Gauzzi, M. C., Velazquez, L., McKendry, R., Mogensen, K. E., Fellous, M., and Pellegrini, S. (1996) Interferon-α-dependent activation of TYK2 requires phosphorylation of positive regulatory tyrosines by another kinase, J. Biol. Chem. 271, 20494-20500.
17. Zhou, Y.-J., Hanson, E. P., Chen, Y.-Q., Magnuson, K., Chen, M., Swann, P. G., Wange, R. L., Changelian, P. S., and O'Shea, J. J. (1997) Distinct tyrosine phosphorylation sites in JAK3 kinase domain positively and negatively regulate its enzymatic activity, Proc. Natl. Acad. Sci. U.S.A. 94, 13850-13855.
18. Liu, K. D., Gaffen, S. L., Goldsmith, M. A., and Greene, W. C. (1997) Janus kinases in interleukin-2 mediated signaling: JAK1 and JAK3 are differentially regulated by tyrosine phosphorylation, Curr. Biol. 7, 817-826.
19. 1007 in the kinase activation loop, Mol. Cell. Biol. 17, 2497-2501.
20. Heyeck, S. D., Wilcox, H. M., Bunnell, S. C., and Berg, L. J. (1997) Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity, J. Biol. Chem. 272, 25401-25408.
21. Cunningham, M. E., Stephens, R. M., Kaplan, D. R., and Greene, L. A. (1997) Autophosphorylation of activation loop tyrosines regulates signaling by the TRK nerve growth factor receptor, J. Biol. Chem. 272, 10957-10967.
22. Kishimoto, K., Matsumoto, K., and Ninomiya-Tsuji, J. (2000) TAK1 mitogen-activated protein kinase kinase kinase is activated by autophosphorylation within its activation loop. J. Biol. Chem, 275, 7359-7364.
23. Gayko, U., Cleghon, V., Copeland, T., Morrison, D. K., and Perrimon, N. (1999) Synergistic activities of multiple phosphotyrosine residues mediate full signaling from the Drosophila Torso receptor tyrosine kinase, Proc. Natl. Acad. Sci. U.S.A. 96, 523-528.
24. Favelyukis, S., Till, J. H., Hubbard, S. R., and Miller, W. T. (2001) Structure and autoregulation of the insulin-like growth factor-1 receptor kinase, Nat. Struct. Biol. 8, 1058-1063.
25. Till, J., Becerra, M., Watty, A., Lu, Y., Ma, Y., Neubert, T., Burden, S., and Hubbard, S. R. (2002) Crystal structure of the MuSK tyrosine kinase. Insights into receptor autoregulation, Structure (Cambridge) 10, 1187-1196.
26. Hubbard, S. R., Wei, L., Ellis, L., and Hendrickson, W. A. (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor, Nature 372, 746-754.
27. Hubbard, S. R. (1997) Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analogue, EMBO J. 16, 5573-5581.
28. Yu, C.-L., Jove, R., and Burakoff, S. J. (1997) Constitutive activation of the Janus kinase-STAT pathway in T lymphoma overexpressing the Lck protein tyrosine kinase, J. Immunol. 159, 5206-5210.
29. Shuai, K., Halpern, J., ten Hoeve, J., Rao, X., and Sawyers, C. L. (1996) Constitutive activation of STAT5 by the BCR-ABL oncogene in chronic myelogenous leukemia, Oncogene 13, 247-254.
30. Murakami, Y., Nakano, S., Niho, Y., Hamasaki, N., and Izuhara, K. (1998) Constitutive activation of JAK-2 and TYK-2 in a v-src-transformed human gallbladder adenocarcinoma cell line, J. Cell. Physiol. 175, 220-228.
31. Danial, N. N., Pernis, A., and Rothman, P. B. (1995) JAK-STAT signaling induced by the v-abl oncogene, Science 269, 1875-1877.
32. Mohammadi, M., Schlessinger, J., and Hubbard, S. R. (1996) Structure of the FGF receptor tyrosine kinase domain reveals a novel autoinhibitory mechanism, Cell 86, 577-587.
33. Saylor, P., Hanna, E., and Adams, J. A. (1998) Mutations in the activation loop tyrosine of the oncoprotein v-Fps, Biochemistry 37, 17875-17881.
34. Leon, B. C., Tsigelny, I., and Adams, J. A. (2001) Electrostatic environment surrounding the activation loop phosphotyrosine in the oncoprotein v-Fps, Biochemistry 40, 10078-10086.
35. Kendall, R. L., Rutledge, R. Z., Mao, X., Tebben, A. J., Hungate, R. W., and Thomas, K. A. (1999) Vascular endothelial growth factor receptor KDR tyrosine kinase activity is increased by autophosphorylation of two activation loop tyrosine residues, J. Biol. Chem. 274, 6453-6460.
36. Zhang, J., Kimura, T., and Siraganian, R. P. (1998) Mutations in the activation loop tyrosines of protein tyrosine kinase Syk abrogate intracellular signaling but not kinase activity, J. Immunol. 161, 4366-4374.
37. Duhé, R. J., Clark, E. A., and Farrar, W. L. (2002) Characterization of the in vitro kinase activity of a partially purified soluble GST/ JAK2 fusion protein, Mol. Cell. Biochem. 236, 23-35.
38. Duhé, R. J., Rui, H., Greenwood, J. D., Garvey, K., and Farrar, W. L. (1995) Cloning of the gene encoding rat JAK2, a protein tyrosine kinase, Gene 158, 281-285.
39. Duhé, R. J., and Farrar, W. L. (1995) Characterization of active and inactive forms of the JAK2 protein-tyrosine kinase produced via the baculovirus expression vector system, J. Biol. Chem. 270, 23084-23089.
40. Olsen, H., Hedengran Faulds, M. A., Saharinen, P., Silvennoinen, O., and Haldosen, L. A. (2002) Effects of hyperactive JAK2 signaling in mammary epithelial cells, Biochem. Biophys. Res. Commun. 296, 139-144.
41. Rui, L., Gunter, D. R., Herrington, J., and Carter-Su, C. (2000) Differential binding to and regulation of JAK2 by the SH2 domain and N-terminal region of SH2-Bβ, Mol. Cell. Biol. 20, 3168-3177.
42. Carrera, A. C., Alexandrov, K., and Roberts, T. M. (1993) The conserved lysine of the catalytic domain of protein kinases is actively involved in the phosphotransfer reaction and not required for anchoring ATP, Proc. Natl. Acad. Sci. U.S.A. 90, 442-446.
43. Robinson, M. J., Harkins, P. C., Zhang, J., Baer, R., Haycock, J. W., Cobb, M. H., and Goldsmith, E. J. (1996) Mutation of position 52 in ERK2 creates a nonproductive binding mode for adenosine 5′-triphosphate, Biochemistry 35, 5641-5646.
44. Hanks, S. K., Quinn, A. M., and Hunter, T. (1988) The protein kinase family: Conserved features and deduced phylogeny of the catalytic domains, Science 241, 42-52.
45. Cruz, P. E., Martins, P. C., Alves, P. M., Peixoto, C. C., Santos, H., Moreira, J. L., and Carrondo, M. J. T. (1999) Proteolytic activity in infected and noninfected insect cells: Degradation of HIV-1 Pr55gag particles, Biotechnol. Bioeng. 65, 133-143.
46. Burt, C. T., Glonek, T., and Bárány, M. (1976) Analysis of phosphate metabolites, the intracellular pH, and the state of adenosine triphosphate in intact muscle by phosphorus nuclear magnetic resonance, J. Biol. Chem. 251, 2584-2591.
47. Miller, D. S., and Horowitz, S. B. (1986) Intracellular compartmentalization of adenosine triphophate, J. Biol. Chem. 261, 13911-13915.
48. Albery, W. J., and Knowles, J. R. (1976) Evolution of enzyme function and the development of catalytic efficiency, Biochemistry 15, 5631-5640.
49. Saharinen, P., Vihinen, M., and Silvennoinen, O. (2003) Autoinhibition of JAK2 tyrosine kinase is dependent on specific regions in its pseudokinase domain, Mol. Cell. Biol. 14, 1448-1459.
50. Saharinen, P., Takaluoma, K., and Silvennoinen, O. (2000) Regulation of the Jak2 tyrosine kinase by its pseudokinase domain, Mol. Cell. Biol. 20, 3387-3395.