Reactivation of oxidized PTP1B and PTEN by thioredoxin 1

FEBS Journal

Volumn 281, Issue 16, 2014, Pages 3545-3558

  Schwertassek, Ulla ^a,c   Haque, Aftabul ^a,d   Krishnan, Navasona ^a   Greiner, Romy ^b   Weingarten, Lars ^b   Dick, Tobias P ^b   Tonks, Nicholas K ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

insulin signaling; phosphatase; reactive oxygen species; redox regulation; substrate trapping; thioredoxin 1

Indexed keywords

DISULFIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 1B; THIOL; THIOREDOXIN 1;

CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME METABOLISM; ENZYME REACTIVATION; ENZYME SPECIFICITY; IN VITRO STUDY; INTRACELLULAR SIGNALING; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; RNA INTERFERENCE;

INSULIN SIGNALING; PHOSPHATASE; REACTIVE OXYGEN SPECIES; REDOX REGULATION; SUBSTRATE TRAPPING; THIOREDOXIN 1;

CATALYTIC DOMAIN; DISULFIDES; ENZYME ACTIVATION; HEK293 CELLS; HELA CELLS; HUMANS; INSULIN; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PTEN PHOSPHOHYDROLASE; THIOREDOXINS;

EID: 84906791913     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12898     Document Type: Review

References (53)

1. Lambeth JD, (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4, 181-189.
2. Bedard K, &, Krause KH, (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87, 245-313.
3. Droge W, (2002) Free radicals in the physiological control of cell function. Physiol Rev 82, 47-95.
4. Finkel T, (2011) Signal transduction by reactive oxygen species. J Cell Biol 194, 7-15.
5. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock PB, &, Rhee SG, (1997) Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 272, 217-221.
6. Meng TC, Fukada T, &, Tonks NK, (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 9, 387-399.
7. Meng TC, Buckley DA, Galic S, Tiganis T, &, Tonks NK, (2004) Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J Biol Chem 279, 37716-37725.
8. Tonks NK, (2013) Protein tyrosine phosphatases-from housekeeping enzymes to master regulators of signal transduction. FEBS J 280, 346-378.
9. Tonks NK, (2006) Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7, 833-846.
10. Tonks NK, (2005) Redox redux: revisiting PTPs and the control of cell signaling. Cell 121, 667-670.
11. Ostman A, Frijhoff J, Sandin A, &, Bohmer FD, (2011) Regulation of protein tyrosine phosphatases by reversible oxidation. J Biochem 150, 345-356.
12. Salmeen A, Andersen JN, Myers MP, Meng TC, Hinks JA, Tonks NK, &, Barford D, (2003) Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423, 769-773.
13. Frijhoff J, Dagnell M, Godfrey R, &, Ostman A, (2013) Regulation of protein tyrosine phosphatase oxidation in cell adhesion and migration. Antioxid Redox Signal 20, 1994-2010.
14. Lee SR, Kwon KS, Kim SR, &, Rhee SG, (1998) Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J Biol Chem 273, 15366-15372.
15. Mahadev K, Zilbering A, Zhu L, &, Goldstein BJ, (2001) Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J Biol Chem 276, 21938-21942.
16. Haque A, Andersen JN, Salmeen A, Barford D, &, Tonks NK, (2011) Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147, 185-198.
17. Leslie NR, Bennett D, Lindsay YE, Stewart H, Gray A, &, Downes CP, (2003) Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J 22, 5501-5510.
18. Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, &, Rhee SG, (2004) Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci USA 101, 16419-16424.
19. Boivin B, Zhang S, Arbiser JL, Zhang ZY, &, Tonks NK, (2008) A modified cysteinyl-labeling assay reveals reversible oxidation of protein tyrosine phosphatases in angiomyolipoma cells. Proc Natl Acad Sci USA 105, 9959-9964.
20. Seo JH, Ahn Y, Lee SR, Yeol Yeo C, &, Chung Hur K, (2005) The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway. Mol Biol Cell 16, 348-357.
21. Barrett WC, DeGnore JP, Konig S, Fales HM, Keng YF, Zhang ZY, Yim MB, &, Chock PB, (1999) Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38, 6699-6705.
22. Barrett WC, DeGnore JP, Keng YF, Zhang ZY, Yim MB, &, Chock PB, (1999) Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J Biol Chem 274, 34543-34546.
23. 2. J Biol Chem 277, 20336-20342.
24. Dagnell M, Frijhoff J, Pader I, Augsten M, Boivin B, Xu J, Mandal PK, Tonks NK, Hellberg C, Conrad M, et al,. (2013) Selective activation of oxidized PTP1B by the thioredoxin system modulates PDGF-beta receptor tyrosine kinase signaling. Proc Natl Acad Sci USA 110, 13398-13403.
25. Watson WH, Pohl J, Montfort WR, Stuchlik O, Reed MS, Powis G, &, Jones DP, (2003) Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif. J Biol Chem 278, 33408-33415.
26. Collet JF, &, Messens J, (2010) Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 13, 1205-1216.
27. Schwertassek U, Balmer Y, Gutscher M, Weingarten L, Preuss M, Engelhard J, Winkler M, &, Dick TP, (2007) Selective redox regulation of cytokine receptor signaling by extracellular thioredoxin-1. EMBO J 26, 3086-3097.
28. Casagrande S, Bonetto V, Fratelli M, Gianazza E, Eberini I, Massignan T, Salmona M, Chang G, Holmgren A, &, Ghezzi P, (2002) Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc Natl Acad Sci USA 99, 9745-9749.
29. Holmgren A, &, Luthman M, (1978) Tissue distrubution and subcellular localization of bovine thioredoxin determined by radioimmunoassay. Biochemistry 17, 4071-4077.
30. Yang J, Groen A, Lemeer S, Jans A, Slijper M, Roe SM, den Hertog J, &, Barford D, (2007) Reversible oxidation of the membrane distal domain of receptor PTPalpha is mediated by a cyclic sulfenamide. Biochemistry 46, 709-719.
31. Savitsky PA, &, Finkel T, (2002) Redox regulation of Cdc25C. J Biol Chem 277, 20535-20540.
32. Sohn J, &, Rudolph J, (2003) Catalytic and chemical competence of regulation of cdc25 phosphatase by oxidation/reduction. Biochemistry 42, 10060-10070.
33. Funato Y, &, Miki H, (2014) Reversible oxidation of PRL family protein-tyrosine phosphatases. Methods 65, 184-189.
34. Chen CY, Willard D, &, Rudolph J, (2009) Redox regulation of SH2-domain-containing protein tyrosine phosphatases by two backdoor cysteines. Biochemistry 48, 1399-1409.
35. Abdelsaid MA, &, El-Remessy AB, (2012) S-Glutathionylation of LMW-PTP regulates VEGF-mediated FAK activation and endothelial cell migration. J Cell Sci 125, 4751-4760.
36. Parsons ZD, &, Gates KS, (2013) Thiol-dependent recovery of catalytic activity from oxidized protein tyrosine phosphatases. Biochemistry 52, 6412-6423.
37. Limon-Pacheco JH, Hernandez NA, Fanjul-Moles ML, &, Gonsebatt ME, (2007) Glutathione depletion activates mitogen-activated protein kinase (MAPK) pathways that display organ-specific responses and brain protection in mice. Free Radical Biol Med 43, 1335-1347.
38. Meuillet EJ, Mahadevan D, Berggren M, Coon A, &, Powis G, (2004) Thioredoxin-1 binds to the C2 domain of PTEN inhibiting PTEN's lipid phosphatase activity and membrane binding: a mechanism for the functional loss of PTEN's tumor suppressor activity. Arch Biochem Biophys 429, 123-133.
39. Kim HY, &, Kim JR, (2008) Thioredoxin as a reducing agent for mammalian methionine sulfoxide reductases B lacking resolving cysteine. Biochem Biophys Res Commun 371, 490-494.
40. Oh J, Hur MW, &, Lee CE, (2009) SOCS1 protects protein tyrosine phosphatases by thioredoxin upregulation and attenuates Jaks to suppress ROS-mediated apoptosis. Oncogene 28, 3145-3156.
41. 2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4, ra86.
42. Motohashi K, Kondoh A, Stumpp MT, &, Hisabori T, (2001) Comprehensive survey of proteins targeted by chloroplast thioredoxin. Proc Natl Acad Sci USA 98, 11224-11229.
43. Dick TP, Bangia N, Peaper DR, &, Cresswell P, (2002) Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16, 87-98.
44. Dick TP, &, Cresswell P, (2002) Thiol oxidation and reduction in major histocompatibility complex class I-restricted antigen processing and presentation. Methods Enzymol 348, 49-54.
45. Engelhard J, Christian BE, Weingarten L, Kuntz G, Spremulli LL, &, Dick TP, (2011) In situ kinetic trapping reveals a fingerprint of reversible protein thiol oxidation in the mitochondrial matrix. Free Radical Biol Med 50, 1234-1241.
46. Flint AJ, Tiganis T, Barford D, &, Tonks NK, (1997) Development of 'substrate-trapping' mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci USA 94, 1680-1685.
47. Anderie I, Schulz I, &, Schmid A, (2007) Characterization of the C-terminal ER membrane anchor of PTP1B. Exp Cell Res 313, 3189-3197.
48. Hansen SK, Cancilla MT, Shiau TP, Kung J, Chen T, &, Erlanson DA, (2005) Allosteric inhibition of PTP1B activity by selective modification of a non-active site cysteine residue. Biochemistry 31, 7704-7712.
49. Lou YW, Chen YY, Hsu SF, Chen RK, Lee CL, Khoo KH, Tonks NK, &, Meng TC, (2008) Redox regulation of the protein tyrosine phosphatase PTP1B in cancer cells. FEBS J 275, 69-88.
50. 2: a quantitative comparison between continuous low-dose and one-time high-dose treatments. Free Radical Biol Med 60, 325-335.
51. Karisch R, &, Neel BG, (2012) Methods to monitor classical protein-tyrosine phosphatase oxidation. FEBS J 280, 459-475.
52. Schwertassek U, Weingarten L, &, Dick TP, (2007) Identification of redox-active cell-surface proteins by mechanism-based kinetic trapping. Sci STKE 2007, pl8.
53. Durocher Y, Perret S, &, Kamen A, (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res 30, E9.