Inhibition of PTPs by H2O2 regulates the activation of distinct MAPK pathways

Free Radical Biology and Medicine

Volumn 33, Issue 8, 2002, Pages 1121-1132

  Lee, Kyoungmun ^a   Esselman, Walter J ^a  

^a Michigan State University ^*  (United States)

Author keywords

CD45; Free radicals; H2O2; HePTP; Jurkat; MAPK; PTP; ROS; SHP 1

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 3 DIMETHYLAMINO 1 PHENYL 6 PYRIDAZONE; HYDROGEN PEROXIDE; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C INHIBITOR; PROTEIN KINASE C INHIBITOR; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE PHOSPHATASE; RO 318425; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

ANTIGENS, CD45; ENZYME INHIBITORS; ESTRENES; HUMANS; HYDROGEN PEROXIDE; INDOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MALEIMIDES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOLIPASE C; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE-PHOSPHATASE; PYRIMIDINES; PYRROLIDINONES; REACTIVE OXYGEN SPECIES; RECOMBINANT FUSION PROTEINS; SHP1 PROTEIN TYROSINE PHOSPHATASE; SRC-FAMILY KINASES; T-LYMPHOCYTES; TRANSFECTION;

EID: 0037108204     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(02)01000-6     Document Type: Article

References (74)

1. Kamata H., Hirata H. Redox regulation of cellular signaling. Cell. Signal. 11:1999;1-14.
2. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82:2002;47-95.
3. Rhee S.G., Bae Y.S., Lee S., Kwon J. Hydrogen peroxide a key messenger that modulates protein phosphorylation through cysteine oxidation . Science's STKE. 2000;. http://stke.sciencemag.org.
4. Thannickal V.J., Fanburg B.L. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 279:2000;L1005-L1028.
5. Pani G., Colavitti R., Borrello S., Galeotti T. Endogenous oxygen radicals modulate protein tyrosine phosphorylation and JNK-1 activation in lectin-stimulated thymocytes. Biochem. J. 347:2000;173-181.
6. Los M., Schenk H., Hexel K., Baeuerle P.A., Droge W., Schulze-Osthoff K. IL-2 gene-expression and NF-κB activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J. 14:1995;3731-3740.
7. Devadas S., Zaritskaya L., Rhee S.G., Oberley L., Williams M.S. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation selective regulation of mitogen-activated protein kinase activation and Fas ligand expression . J. Exp. Med. 195:2002;59-70.
8. Baggiolini M., Wymann M.P. Turning on the respiratory burst. Trends Biochem. Sci. 15:1990;69-72.
9. Matheny H.E., Deem T.L., Cook-Mills J.M. Lymphocyte migration through monolayers of endothelial cell lines involves VCAM-1 signaling via endothelial cell NADPH oxidase. J. Immunol. 164:2000;6550-6559.
10. Weyand C.M. New insights into the pathogenesis of rheumatoid arthritis. Rheumatology. 39:2000;3-8.
11. Glass C.K., Witztum J.L. Atherosclerosis. The road ahead. Cell. 104:2001;503-516.
12. van der Ven A.J.A.M., Blom H.J., Peters W., Jacobs L.E.H., Verver T.J.G., Koopmans P.P., Demacker P., van der Meer J.W.M. Glutathione homeostasis is disturbed in CD4-positive lymphocytes of HIV-seropositive individuals. Eur. J. Clin. Invest. 28:1998;187-193.
13. Monte M., Davel L.E., deLustig E.S. Hydrogen peroxide is involved in lymphocyte activation mechanisms to induce angiogenesis. Eur. J. Cancer. 33:1997;676-682.
14. Finkel T. Oxygen radicals and signaling. Curr. Opin. Cell Biol. 10:1998;248-253.
15. Peters G.H., Frimurer T.M., Olsen O.H. Electrostatic evaluation of the signature motif (H/V)CX5R(S/T) in protein-tyrosine phosphatases. Biochemistry. 37:1998;5383-5393.
16. Denu J.M., Tanner K.G. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide evidence for a sulfenic acid intermediate and implications for redox regulation . Biochemistry. 37:1998;5633-5642.
17. Herrlich P., Bohmer F.D. Redox regulation of signal transduction in mammalian cells. Biochem. Pharmacol. 59:2000;35-41.
18. Sattler M., Verma S., Shrikhande G., Byrne C.H., Pride Y.B., Winkler T., Greenfield E.A., Salgia R., Griffin J.D. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J. Biol. Chem. 275:2000;24273-24278.
19. 2 on protein tyrosine phosphatase activity in HER14 cells. Free Radic. Biol. Med. 16:1994;399-403.
20. Secrist J.P., Burns L.A., Karnitz L., Koretzky G.A., Abraham R.T. Stimulatory effects of the protein tyrosine phosphatase inhibitor, pervanadate, on T cell activation events. J. Biol. Chem. 268:1993;5886-5893.
21. Fialkow L., Chan C.K., Rotin D., Grinstein S., Downey G.P. Activation of the mitogen-activated protein kinase signaling pathway in neutrophils. Role of oxidants. J. Biol. Chem. 269:1994;31234-31242.
22. Cunnick J.M., Dorsey J.F., Mei L., Wu J. Reversible regulation of SHP-1 tyrosine phosphatase activity by oxidation. Biochem. Mol. Biol. Int. 45:1998;887-894.
23. Mahadev K., Zilbering A., Zhu L., Goldstein B.J. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1B in vivo and enhances the early insulin action cascade. J. Biol. Chem. 276:2001;21938-21942.
24. Lee S.R., Kwon K.S., Kim S.R., Rhee S.G. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273:1998;15366-15372.
25. Cuncic C., Detich N., Ethier D., Tracey A.S., Gresser M.J., Ramachandran C. Vanadate inhibition of protein tyrosine phosphatases in Jurkat cells modulation by redox state . J. Biol. Inorg. Chem. 4:1999;354-359.
26. Koretzky G.A., Picus J., Thomas M.L., Weiss A. Tyrosine phosphatase CD45 is essential for coupling T cell antigen receptor to the phosphatidyl inositol pathway. Nature. 346:1990;66-68.
27. Wang Y., Liang L.Z., Esselman W.J. Regulation of the calcium/NF-AT T cell activation pathway by the D2 domain of CD45. J. Immunol. 164:2000;2557-2564.
28. Penninger J.M., Irie-Sasaki J., Sasaki T., Oliveira-dos-Santos A.J. CD45 new jobs for an old acquaintance . Nat. Immunol. 2:2001;389-396.
29. Trowbridge I.S., Thomas M.L. CD45 an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development . Ann. Rev. Immunol. 12:1994;85-116.
30. D'Oro U., Sakaguchi K., Appella E., Ashwell J.D. Mutational analysis of Lck in CD45-negative T cells dominant role of tyrosine 394 phosphorylation in kinase activity . Mol. Cell. Biol. 16:1996;4996-5003.
31. D'Oro U., Ashwell J.D. Cutting edge the CD45 tyrosine phosphatase is an inhibitor of Lck activity in thymocytes . J. Immunol. 162:1999;1879-1883.
32. Matthews R.J., Bowne D.B., Flores E., Thomas M.L. Characterization of hematopoietic intracellular protein tyrosine phosphatases description of a phosphatase containing an SH2 domain and another enriched in proline-, glutamic acid-, serine-, and threonine-rich sequences . Mol. Cell. Biol. 12:1992;2396-2405.
33. Pani G., Fischer K.D., MlinaricRascan I., Siminovitch K.A. Signaling capacity of the T cell antigen receptor is negatively regulated by the PTP1C tyrosine phosphatase. J. Exp. Med. 184:1996;839-852.
34. Binstadt B.A., Billadeau D.D., Jevremovic D., Williams B.L., Fang N., Yi T.L., Koretzky G.A., Abraham R.T., Leibson P.J. SLP-76 is a direct substrate of SHP-1 recruited to killer cell inhibitory receptors. J. Biol. Chem. 273:1998;27518-27523.
35. Plas D.R., Johnson R., Pingel J.T., Matthews R.J., Dalton M., Roy G., Chan A.C., Thomas M.L. Direct regulation of ZAP-70 by SHP-1 in T cell antigen receptor signaling. Science. 272:1996;1173-1176.
36. Zanke B., Suzuki H., Kishihara K., Mizzen L., Minden M., Pawson A., Mak T.W. Cloning and expression of an inducible lymphoid-specific, protein tyrosine phosphatase (HePTPase). Eur. J. Immunol. 22:1992;235-239.
37. Saxena M., Williams S., Gilman J., Mustelin T. Negative regulation of T cell antigen receptor signal transduction by hematopoietic tyrosine phosphatase (HePTP). J. Biol. Chem. 273:1998;15340-15344.
38. Saxena M., Williams S., Brockdorff J., Gilman J., Mustelin T. Inhibition of T cell signaling by mitogen-activated protein kinase-targeted hematopoietic tyrosine phosphatase (HePTP). J. Biol. Chem. 274:1999;11693-11700.
39. Gronda M., Arab S., Iafrate B., Suzuki H., Zanke B.W. Hematopoietic protein tyrosine phosphatase suppresses extracellular stimulus-regulated kinase activation. Mol. Cell. Biol. 21:2001;6851-6858.
40. 2 role in cell survival following oxidant injury . J. Biol. Chem. 271:1996;4138-4142.
41. Houslay M.D., Kolch W. Cell-type specific integration of cross-talk between extracellular signal-regulated kinase and cAMP signaling. Mol. Pharmacol. 58:2000;659-668.
42. Robinson M.J., Cobb M.H. Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9:1997;180-186.
43. Rincon M. MAP kinase signaling pathways in T cells. Curr. Opin. Immunol. 13:2001;339-345.
44. Brockdorff J., Williams S., Couture C., Mustelin T. Dephosphorylation of ZAP-70 and inhibition of T cell activation by activated SHP1. Eur. J. Immunol. 29:1999;2539-2550.
45. 2-induced ERK1/2 phosphorylation without the requirement for MEK1/2 phosphorylation. Cell. Signal. 13:2001;645-652.
46. Ostergaard H.L., Shackelford D.A., Hurley T.R., Johnson P., Hyman R., Sefton B.M., Trowbridge I.S. Expression of CD45 alters phosphorylation of the lck-encoded tyrosine protein kinase in murine lymphoma T cell lines. Proc. Natl. Acad. Sci. USA. 86:1989;8959-8963.
47. Mustelin T., Pessa-Morikawa T., Autero M., Gassmann M., Andersson L.C., Gahmberg C.G., Burn P. Regulation of the p59fyn protein tyrosine kinase by the CD45 phosphotyrosine phosphatase. Eur. J. Immunol. 22:1992;1173-1178.
48. Sefton B.M., Taddie J.A. Role of tyrosine kinases in lymphocyte-activation. Curr. Opin. Immunol. 6:1994;372-379.
49. Franklin R.A., Atherfold P.A., McCubrey J.A. Calcium-induced ERK activation in human T lymphocytes occurs via p56(Lck) and CaM-kinase. Mol. Immunol. 37:2000;675-683.
50. Nishibe S., Wahl M.I., Hernandezsotomayor S.M.T., Tonks N.K., Rhee S.G., Carpenter G. Increase of the catalytic activity of phospholipase C-γ-1 by tyrosine phosphorylation. Science. 250:1990;1253-1256.
51. Siegel J.N., Klausner R.D., Rapp U.R., Samelson L.E. T cell antigen receptor engagement stimulates c-Raf phosphorylation and induces c-Raf-associated kinase activity via a protein kinase C-dependent pathway. J. Biol. Chem. 265:1990;18472-18480.
52. Hunter T. Protein kinases and phosphatases the yin and yang of protein phosphorylation and signaling . Cell. 80:1995;225-236.
53. Neel B.G., Tonks N.K. Protein tyrosine phosphatases in signal transduction. Curr. Opin. Cell. Biol. 9:1997;193-204.
54. Alonso A., Saxena M., Williams S., Mustelin T. Inhibitory role for dual specificity phosphatase VHR in T cell antigen receptor and CD28-induced Erk and Jnk activation. J. Biol. Chem. 276:2001;4766-4771.
55. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
56. Gu Y., Xu Y.C., Wu R.F., Souza R.F., Nwariaku F.E., Terada L.S. TNF-α activates c-Jun amino terminal kinase through p47(phox). Exp. Cell Res. 272:2002;62-74.
57. Denu J.M., Dixon J.E. Protein tyrosine phosphatases mechanisms of catalysis and regulation . Curr. Opin. Chem. Biol. 2:1998;633-641.
58. Fortin J.F., Barbeau B., Robichaud G.A., Pare M.E., Lemieux A.M., Tremblay M.J. Regulation of nuclear factor of activated T cells by phosphotyrosyl-specific phosphatase activity a positive effect on HIV-1 long terminal repeat-driven transcription and a possible implication of SHP-1 . Blood. 97:2001;2390-2400.
59. Gross S., Knebel A., Tenev T., Neininger A., Gaestel M., Herrlich P., Bohmer F.D. Inactivation of protein-tyrosine phosphatases as mechanism of UV-induced signal transduction. J. Biol. Chem. 274:1999;26378-26386.
60. KonKozlowski M., Pani G., Pawson T., Siminovitch K.A. The tyrosine phosphatase PTP1C associates with Vav, Grb2, and mSos1 in hematopoietic cells. J. Biol. Chem. 271:1996;3856-3862.
61. Kaminuma O., Deckert M., Elly C., Liu Y.C., Altman A. Vav-Rac1-mediated activation of the c-Jun N-terminal kinase/c- Jun/AP-1 pathway plays a major role in stimulation of the distal NFAT site in the interleukin-2 gene promoter. Mol. Cell. Biol. 21:2001;3126-3136.
62. Pettiford S.M., Herbst R. The MAP kinase ERK2 is a specific substrate of the protein tyrosine phosphatase HePTP. Oncogene. 19:2000;858-869.
63. Hardwick J.S., Sefton B.M. Activation of the Lck tyrosine protein kinase by hydrogen peroxide requires the phosphorylation of Tyr-394. Proc. Natl. Acad. Sci. USA. 92:1995;4527-4531.
64. Hardwick J.S., Sefton B.M. The activated form of the Lck tyrosine protein kinase in cells exposed to hydrogen peroxide is phosphorylated at both Tyr-394 and Tyr-505. J. Biol. Chem. 272:1997;25429-25432.
65. Chiang G.G., Sefton B.M. Specific dephosphorylation of the Lck tyrosine protein kinase at Tyr-394 by the SHP-1 protein-tyrosine phosphatase. J. Biol. Chem. 276:2001;23173-23178.
66. Cuevas B., Lu Y.L., Watt S., Kumar R., Zhang J.Y., Siminovitch K.A., Mills G.B. SHP-1 regulates Lck-induced phosphatidylinositol 3-kinase phosphorylation and activity. J. Biol. Chem. 274:1999;27583-27589.
67. Pei D., Lorenz U., Klingmuller U., Neel B.G., Walsh C.T. Intramolecular regulation of protein tyrosine phosphatase SH-PTP1 a new function for Src homology 2 domains . Biochemistry. 33:1994;15483-15493.
68. Fry A.M., Lanier L.L., Weiss A. Phosphotyrosines in the killer cell inhibitory receptor motif of NKB1 are required for negative signaling and for association with protein tyrosine phosphatase 1C. J. Exp. Med. 184:1996;295-300.
69. Perez-Villar J.J., Whitney G.S., Bowen M.A., Hewgill D.H., Aruffo A.A., Kanner S.B. CD5 negatively regulates the T cell antigen receptor signal transduction pathway involvement of SH2-containing phosphotyrosine phosphatase SHP-1 . Mol. Cell. Biol. 19:1999;2903-2912.
70. Shasby D.M., Yorek M., Shasby S.S. Exogenous oxidants initiate hydrolysis of endothelial cell inositol phospholipids. Blood. 72:1988;491-499.
71. Qin S.F., Inazu T., Yamamura H. Activation and tyrosine phosphorylation of p72(Syk) as well as calcium mobilization after hydrogen peroxide stimulation in peripheral-blood lymphocytes. Biochem. J. 308:1995;347-352.
72. vanDijk M.C.M., Hilkmann H., vanBlitterswijk W.J. Platelet-derived growth factor activation of mitogen-activated protein kinase depends on the sequential activation of phosphatidylcholine-specific phospholipase C, protein kinase C-zeta, and Raf-1. Biochem. J. 325:1997;303-307.
73. Cai H., Smola U., Wixler V., EisenmannTappe I., DiazMeco M.T., Moscat J., Rapp U., Cooper G.M. Role of diacylglycerol-regulated protein kinase C isotypes in growth factor activation of the Raf-1 protein kinase. Mol. Cell. Biol. 17:1997;732-741.
74. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17:1998;2596-2606.