Multiple cysteine residues are implicated in Janus kinase 2-mediated catalysis

Biochemistry

Volumn 46, Issue 51, 2007, Pages 14810-14818

  Mamoon, Naila M ^a   Smith, John K ^a   Chatti, Kiranam ^a,b   Lee, Sheeyong ^a,c   Kundrapu, Kanakadurga ^a   Duhé, Roy J ^a  

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

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; MUTAGENESIS; OXIDATION; REDOX REACTIONS;

BACULOVIRAL EXPRESSION; CYSTEINE; JANUS KINASE 2 (JAK2);

ENZYME ACTIVITY;

CYSTEINE; GLUTATHIONE TRANSFERASE; JANUS KINASE 2; RECOMBINANT ENZYME; SERINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; MUTAGENESIS; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; REDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CATALYSIS; CYSTEINE; ENZYME ACTIVATION; HUMANS; JANUS KINASE 2; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATION-REDUCTION; PROTEIN KINASE INHIBITORS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 37349100875     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701118u     Document Type: Article

References (48)

1. Diefenbach, A., Schindler, H., Rollinghoff, M., Yokoyama, W. M., and Bogdan, C. (1999) Requirement for type 2 NO synthase for IL-12 signaling in innate immunity, Science 284, 951-955.
2. Bogdan, C. (2001) Nitric oxide and the immune response, Nat. Immunol. 2, 907-916.
3. Maurice, M. M., Nakamura, H., van der Voort, E. A., van Vliet, A. I., Staal, F. J., Tak, P. P., Breedveld, F. C., and Verweij, C. L. (1997) Evidence for the role of an altered redox state in hyporesponsiveness of synovial T cells in rheumatoid arthritis, J. Immunol. 158, 1458-1465.
4. Cemerski, S., Cantagrel, A., Van Meerwijk, J. P., and Romagnoli, P. (2002) Reactive oxygen species differentially affect T cell receptor-signaling pathways, J. Biol. Chem. 277, 19585-19593.
5. Cemerski, S., van Meerwijk, J. P., and Romagnoli, P. (2003) Oxidative-stress-induced T lymphocyte hyporesponsiveness is caused by structural modification rather than proteasomal degradation of crucial TCR signaling molecules, Eur. J. Immunol. 33, 2178-2185.
6. Rane, S. G., and Reddy, E. P. (2000) Janus kinases: components of multiple signaling pathways, Oncogene 19, 5662-5679.
7. Rawlings, J. S., Rosler, K. M., and Harrison, D. A. (2004) The JAK/STAT signaling pathway, J. Cell Sci. 117, 1281-1283.
8. Duhé, R. J., Evans, G. A., Erwin, R. A., Kirken, R. A., Cox, G. W., and Farrar, W. L. (1998) Nitric oxide and thiol redox regulation of Janus kinase activity, Proc. Natl. Acad. Sci. U.S.A. 95, 126-131.
9. Bingisser, R. M., Tilbrook, P. A., Holt, P. G., and Kees, U. R. (1998) Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway, J. Immunol. 160, 5729-5734.
10. Mazzoni, A., Bronte, V., Visintin, A., Spitzer, J. H., Apolloni, E., Serafini, P., Zanovello, P., and Segal, D. M. (2002) Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism, J. Immunol. 168, 689-695.
11. Mills, C. D. (1991) Molecular basis of "suppressor" macrophages. Arginine metabolism via the nitric oxide synthetase pathway, J. Immunol. 146, 2719-2723.
12. Albina, J. E., Abate, J. A., and Henry, W. L., Jr. (1991) Nitric oxide production is required for murine resident peritoneal macrophages to suppress mitogen-stimulated T cell proliferation. Role of IFN-gamma in the induction of the nitric oxide-synthesizing pathway, J. Immunol. 147, 144-148.
13. Taylor-Robinson, A. W., Liew, F. Y., Severn, A., Xu, D., McSorley, S. J., Garside, P., Padron, J., and Phillips, R. S. (1994) Regulation of the immune response by nitric oxide differentially produced by T helper type 1 and T helper type 2 cells, Eur. J. Immunol. 24, 980-984.
14. Lejeune, P., Lagadec, P., Onier, N., Pinard, D., Ohshima, H., and Jeannin, J. F. (1994) Nitric oxide involvement in tumor-induced immunosuppression, J. Immunol. 152, 5077-5083.
15. Upham, J. W., Strickland, D. H., Bilyk, N., Robinson, B. W., and Holt, P. G. (1995) Alveolar macrophages from humans and rodents selectively inhibit T-cell proliferation but permit T-cell activation and cytokine secretion, Immunology 84, 142-147.
16. Yamauchi, A., Masutani, H., Tagaya, Y., Wakasugi, N., Mitsui, A., Nakamura, H., Inamoto, T., Ozawa, K., and Yodoi, J. (1992) Lymphocyte transformation and thiol compounds; the role of ADF/thioredoxin as an endogenous reducing agent, Mol. Immunol. 29, 263-270.
17. Yamauchi, A., and Bloom, E. T. (1993) Requirement of thiol compounds as reducing agents for IL-2-mediated induction of LAK activity and proliferation of human NK cells, J. Immunol. 151, 5535-5544.
18. Iwata, S., Hori, T., Sato, N., Ueda-Taniguchi, Y., Yamabe, T., Nakamura, H., Masutani, H., and Yodoi, J. (1994) Thiol-mediated redox regulation of lymphocyte proliferation. Possible involvement of adult T cell leukemia-derived factor and glutathione in transferrin receptor expression, J. Immunol. 152, 5633-5642.
19. Deiss, L. P., and Kimchi, A. (1991) A genetic tool used to identify thioredoxin as a mediator of a growth inhibitory signal, Science 252, 117-120.
20. Kaur, N., Lu, B., Monroe, R. K., Ward, S. M., and Halvorsen, S. W. (2005) Inducers of oxidative stress block ciliary neurotrophic factor activation of Jak/STAT signaling in neurons, J. Neurochem. 92, 1521-1530.
21. Monroe, R. K., and Halvorsen, S. W. (2006) Cadmium blocks receptor-mediated Jak/STAT signaling in neurons by oxidative stress, Free Radical Biol. Med. 41, 493-502.
22. Gorina, R., Petegnief, V., Chamorro, A., and Planas, A. M. (2005) AG490 prevents cell death after exposure of rat astrocytes to hydrogen peroxide or proinflammatory cytokines: involvement of the Jak2/STAT pathway, J. Neurochem. 92, 505-518.
23. Sandburg, E. M., and Sayeski, P. P. (2004) Jak2 tyrosine kinase mediates oxidative stress-induced apoptosis in vascular smooth muscle cells, J. Biol. Chem. 279, 34547-34552.
24. Maziere, C., Conte, M. A., and Maziere, J. C. (2001) Activation of JAK2 by the oxidative stress generated with oxidized low-density lipoprotein, Free Radical Biol. Med. 31, 1334-1340.
25. Simon, A. R., Rai, U., Fanburg, B. L., and Cochran, B. H. (1998) Activation of the JAK-STAT pathway by reactive oxygen species, Am. J. Physiol. 275, 1640-1652.
26. Carballo, M., Conde, M., El Bekay, R., Martin-Nieto, J., Camacho, M. J., Monteseirin, J., Conde, J., Bedoya, F. J., and Sobrino, F. (1999) Oxidative stress triggers STAT3 tyrosine phosphorylation and nuclear translocation in human lymphocytes, J. Biol. Chem. 274, 17580-17586.
27. Abe, J., and Berk, B. C. (1999) Fyn and JAK2 mediate Ras activation by reactive oxygen species, J. Biol. Chem. 274, 21003-21010.
28. Tonks, N. (2005) Redox redux: revisiting PTPs and the control of cell signaling, Cell 121, 667-670.
29. Meng, T. C., Fukada, T., and Tonks, N. K. (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo, Mol. Cell 9, 387-399.
30. Lamb, P., Haslam, J., Kessler, L., Seidel, H. M., Stein, R. B., and Rosen, J. (1994) Rapid activation of the interferon-gamma signal transduction pathway by inhibitors of tyrosine phosphatases, J. Interferon Res. 14, 365-373.
31. Haque, S. J., Wu, Q., Kammer, W., Friedrich, K., Smith, J. M., Kerr, I. M., Stark, G. R., and Williams, B. R. (1997) Receptor-associated constitutive protein tyrosine phosphatase activity controls the kinase function of JAK1, Proc. Natl. Acad. Sci. U.S.A. 94, 8563-8568.
32. Paget, M. S., and Buttner, M. J. (2003) Thiol-based regulatory switches, Annu. Rev. Genet. 37, 91-121.
33. Poole, L. B., Karplus, P. A., and Claiborne, A. (2004) Protein sulfenic acids in redox signaling, Annu. Rev. Pharmacol. Toxicol. 44, 325-347.
34. 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.
35. 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.
36. Chatti, K., Farrar, W. L., and Duhe, R. J. (2004) 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 43, 4272-4283.
37. Oblong, J. E., Berggren, M., Gasdaska, P. Y., and Powis, G. (1994) Site-directed mutagenesis of active site cysteines in human thioredoxin produces competitive inhibitors of human thioredoxin reductase and elimination of mitogenic properties of thioredoxin, J. Biol. Chem. 269, 11714-11720.
38. Holmgren, A. (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide, J. Biol. Chem. 254, 9627-9632.
39. Olsen, H., Hedengran Faulds, M. A., Saharinen, P., Silvennoinen, O., and Haldosen, L. A. (2002) Effects of hyperactive Janus kinase 2 signaling in mammary epithelial cells, Biochem. Biophys. Res. Commun. 296, 139-144.
40. Lucet, I. S., Fantino, E., Styles, M., Bamert, R., Patel, O., Broughton, S. E., Walter, M., Burns, C. J., Treutlein, H., Wilks, F. A., and Rossjohn, J. (2006) The structural basis of Janus kinase 2 inhibition by a potent and specific pan-Janus kinase inhibitor, Blood 107, 176-183.
41. Giles, N. M., Watts, A. B., Giles, G. I., Fry, F. H., Littlechild, J. A., and Jacob, C. (2003) Metal and redox modulation of cysteine protein function, Chem. Biol. 10, 677-693.
42. Chou, W. Y., Chang, H. P., Huang, C. H., Kuo, C. C., Tong. L., and Chang, G. G. (2000) Characterization of the functional role of Asp141, Asp194, and Asp464 residues in the Mn2+-L-malate binding of pigeon liver malic enzyme, Protein Sci. 9, 242-251.
43. Soundar, S., O'Hagan, M., Fomulu, K. S., and Colman, R. F. (2006) Identification of Mn2+-binding aspartates from alpha, beta, and gamma subunits of human NAD-dependent isocitrate dehydrogenase, J. Biol. Chem. 281, 21073-21081.
44. Huang, Y. C., Grodsky, N. B., Kim, T. K., and Colman, R. F. (2004) Ligands of the Mn2+ bound to porcine mitochondrial NADP-dependent isocitrate dehydrogenase, as assessed by mutagenesis, Biochemistry 43, 2821-2828.
45. Lai, K. S., Jin, Y., Graham, D. K., Witthuhn, B. A., Ihle, J. N., and Liu, E. T. (1995) A kinase-deficient splice variant of the human JAK3 is expressed in hematopoietic and epithelial cancer cells, J. Biol. Chem. 270, 25028-25036.
46. Veillette, A., Dumont, D., and Fournel, M. (1993) Conserved cysteine residues are critical for the enzymatic function of the lymphocyte-specific tyrosine protein kinase p56lck, J. Biol. Chem. 268, 17547-17553.
47. Oo, M. L., Senga, T., Thant, A. A., Amin, A. R., Huang, P., Mon, N. N., and Hamaguchi, M. (2003) Cysteine residues in the C-terminal lobe of Src: their role in the suppression of the Src kinase, Oncogene 22, 1411-1417.
48. Lee, J. W., Kim, J. E., Park, E. J., Kim, J. H., Lee, C. H., Lee, S. R., and Kwon, J. (2004) Two conserved cysteine residues are critical for the enzymic function of the human platelet-derived growth factor receptor-beta: evidence for different roles of Cys-822 and Cys-940 in the kinase activity, Biochem. J. 382, 631-639.