Biometals

, Volume 18, Issue 4, pp 333–338 | Cite as

Protein Tyrosine Phosphatases as Targets of the Combined Insulinomimetic Effects of Zinc and Oxidants

Abstract

Zinc ions have an insulin-like (insulinomimetic) effect. A particularly sensitive target of zinc ions is protein tyrosine phosphatase 1B (PTP 1B), a key regulator of the phosphorylation state of the insulin receptor. Modulation of insulin signaling by zinc chelating agents and the recognition of temporal and spatial fluctuations of zinc suggest a physiological role of zinc in insulin signal transduction. Tyrosine phosphatases seem to be regulated jointly by insulin-induced redox (hydrogen peroxide) signaling, which results in their oxidative inactivation, and by their zinc inhibition after oxidative zinc release from other proteins. In␣diabetes, the significant oxidative stress and associated changes in zinc metabolism modify the cell’s response and sensitivity to insulin. Zinc deficiency activates stress pathways and may result in a loss of tyrosine phosphatase control, thereby causing insulin resistance.

Key words

diabetes insulin signaling PTP 1B redox zinc 

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References

  1. Anderson, RA 2003Chromium and insulin resistanceNutr Res Rev16267275CrossRefGoogle Scholar
  2. Alonso, A, Sasin, J, Bottini, N, Friedberg, I, Friedberg, I, Ostermann, A, Godzik, A, Hunter, T, Dixon, J, Mustelin, T 2004Protein tyrosine phosphatases in the human genomeCell117699711CrossRefPubMedGoogle Scholar
  3. Arslan, P, Di Virgilio, F, Beltrame, M, Tsien, RY, Pozzan, T 1985Cytosolic Ca2+ homeostasis in Ehrlich and Yoshida carcinomasJ Biol Chem26027192727PubMedGoogle Scholar
  4. Bandyopadhyay, D, Kusari, A, Kenner, KA, Liu, F, Chernoff, J, Gustafson, TA, Kusari, J 1997Protein-tyrosine phosphatase 1B complexes with the insulin receptor in vivo and is tyrosine-phosphorylated in the presence of insulinJ Biol Chem27216391645CrossRefPubMedGoogle Scholar
  5. Beattie, JH, Wood, AM, Newman, AM, Bremner, I, Choo, KHA, Michalska, AE, Duncan, JS, Trayhurn, P 1998Obesity and hyperleptinemia in metallothionein (-I and -II) null miceProc Natl Acad Sci USA95358363CrossRefPubMedGoogle Scholar
  6. Beyersmann, D, Haase, H 2001Functions of zinc in signaling, proliferation and differentiation of mammalian cellsBioMetals14331341CrossRefPubMedGoogle Scholar
  7. Brautigan, DL, Bornstein, P, Gallis, B 1981Phosphotyrosyl-protein phosphatase. Specific inhibition by ZnJ Biol Chem25665196522PubMedGoogle Scholar
  8. Byon, JC, Kusari, AB, Kusari, J 1998Protein-tyrosine phosphatase-1B acts as a negative regulator of insulin signal transductionMol Cell Biochem182101108CrossRefPubMedGoogle Scholar
  9. Chausmer, AB 1998Zinc, insulin and diabetesJ Am Coll Nutr17109115PubMedGoogle Scholar
  10. Chen, MD, Liou, SJ, Lin, PY, Yang, VC, Alexander, PS, Lin, WH 1998Effects of zinc supplementation on the plasma glucose level and insulin activity in genetically obese (ob/ob) miceBiol Trace Elem Res61303311PubMedGoogle Scholar
  11. Chen, Y, Maret, W 2001Catalytic selenols couple the redox cycles of metallothionein and glutathioneEur J Biochem26833463353CrossRefPubMedGoogle Scholar
  12. Cheng, A, Dube, N, Gu, F, Tremblay, ML 2002Coordinated action of protein tyrosine phosphatases in insulin signal transductionEur J Biochem26910501059CrossRefPubMedGoogle Scholar
  13. Coulston, L, Dandona, P 1980Insulin-like effect of zinc on adipocytesDiabetes29665667PubMedGoogle Scholar
  14. Czech, MP, Lawrence, JC,Jr, Lynn, WS 1974Evidence for electron transfer reactions involved in the Cu2+-dependent thiol activation of fat cell glucose utilizationJ Biol Chem24910011006PubMedGoogle Scholar
  15. Dadke, S, Kusari, A, Kusari, J 2001Phosphorylation and activation of protein tyrosine phosphatase (PTP) 1B by insulin receptorMol Cell Biochem221147154CrossRefPubMedGoogle Scholar
  16. Elchebly, M, Payette, P, Michaliszyn, E, Cromlish, W, Collins, S, Loy, AL, Normandin, D, Cheng, A, Himms-Hagen, J, Chan, CC, Ramachandran, C, Gresser, MJ, Tremblay, ML, Kennedy, BP 1999Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B geneScience28315441548CrossRefPubMedGoogle Scholar
  17. Fischer, EH 1999Cell signaling by protein tyrosine phosphorylationAdv Enzyme Regul39359369CrossRefPubMedGoogle Scholar
  18. Flint, AJ, Gebbink, MF, Franza, BR,Jr, Hill, DE, Tonks, NK 1993Multi-site phosphorylation of the protein tyrosine phosphatase, PTP 1B: identification of cell cycle regulated and phorbol ester stimulated sites of phosphorylationEMBO J1219371946PubMedGoogle Scholar
  19. Haase, H, Maret, W 2003Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signalingExp Cell Res291289298CrossRefPubMedGoogle Scholar
  20. Haase, H, Maret, W 2004A diferential assay for the reduced and oxidized states of metallothionein and thioneinAnal Biochem3331926CrossRefPubMedGoogle Scholar
  21. Hulley, P, Davison, A 2003Regulation of tyrosine phosphorylation cascades by phosphatases: What the actions of vanadium teach usJ Trace Elem Exp Med16281290CrossRefGoogle Scholar
  22. Imbra, RJ, Karin, M 1987Metallothionein gene expression is regulated by serum factors and activators of protein kinase CMol Cell Biol713581363PubMedGoogle Scholar
  23. Jacob, C, Maret, W, Vallee, BL 1998Selenium redox biochemistry of zinc–sulfur coordination sites in proteins and enzymesProc Natl Acad Sci USA9619101914CrossRefGoogle Scholar
  24. Johnson, TO, Ermolieff, J, Jirousek, MR 2002Protein tyrosine phosphatase 1B inhibitors for diabetesNat Rev Drug Discov1696709CrossRefPubMedGoogle Scholar
  25. Kenner, KA, Anyanwu, E, Olefsky, JM, Kusari, J 1996Protein-tyrosine phosphatase 1B is a negative regulator of insulin- and insulin-like growth factor-I-stimulated signalingJ Biol Chem2711981019816CrossRefPubMedGoogle Scholar
  26. Krieger-Brauer, HI, Medda, PK, Kather, H 1997Insulin-induced activation of NADPH-dependent H2O2 generation in human adipocyte plasma membranes is mediated by Gαi2J Biol Chem2721013510143CrossRefPubMedGoogle Scholar
  27. Marchand-Brustel, Y, Gual, P, Gremeaux, T, Gonzalez, T, Barres, R, Tanti, JF 2003Fatty acid-induced insulin resistance: role of insulin receptor substrate 1 serine phosphorylation in the retroregulation of insulin signalingBiochem Soc Trans3111521156PubMedGoogle Scholar
  28. Li, S, Whorton, AR 2003Regulation of protein tyrosine phosphatase 1B in intact cells by S-nitrosothiolsArch Biochem Biophys410269279CrossRefPubMedGoogle Scholar
  29. Mahadev, K, Motoshima, H, Wu, X, Ruddy, JM, Arnold, RS, Cheng, G, Lambeth, JD, Goldstein, BJ 2004The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transductionMol Cell Biol2418441854CrossRefPubMedGoogle Scholar
  30. Mahadev, K, Zilbering, A, Zhu, L, Goldstein, BJ 2001Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascadeJ Biol Chem2762193821942CrossRefPubMedGoogle Scholar
  31. Maret, W, Jacob, C, Vallee, BL, Fischer, EH 1999Inhibitory sites in enzymes: zinc removal and reactivation by thioneinProc Natl Acad Sci USA9619361940CrossRefPubMedGoogle Scholar
  32. Maret, W, Vallee, BL 1998Thiolate ligands in metallothionein confer redox activity on zinc clustersProc Natl Acad Sci USA9534783482CrossRefPubMedGoogle Scholar
  33. May, JM, Contoreggi, CS 1982The mechanism of the insulin-like effects of ionic zincJ Biol Chem25743624368PubMedGoogle Scholar
  34. McClung, JP, Roneker, CA, Mu, W, Lisk, DJ, Langlais, P, Liu, F, Lei, XG 2004Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidaseProc Natl Acad Sci USA10188528857CrossRefPubMedGoogle Scholar
  35. McNeill, JH, Delgatty, HL, Battell, ML 1991Insulinlike effects of sodium selenate in streptozotocin-induced diabetic ratsDiabetes4016751678PubMedGoogle Scholar
  36. Moeslein, FM, Myers, MP, Landreth, GE 1999The CLK family kinases, CLK1 and CLK2, phosphorylate and activate the tyrosine phosphatase, PTP-1BJ Biol Chem2742669726704CrossRefPubMedGoogle Scholar
  37. Nakatani, Y, Kaneto, H, Kawamori, D, Hatazaki, M, Miyatsuka, T, Matsuoka, T, Kajimoto, Y, Matsuhisa, M, Yamasaki, Y, Hori, M 2004Modulation of the JNK pathway in liver affects insulin resistance statusJ Biol Chem2794580345809CrossRefPubMedGoogle Scholar
  38. Oteiza, PI, Clegg, MS, Zago, MP, Keen, CL 2000Zinc deficiency induces oxidative stress and AP-1 activation in 3T3 cellsFree Radic Biol Med2810911099CrossRefPubMedGoogle Scholar
  39. Palmiter, RD, Findley, SD 1995Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zincEMBO14639649PubMedGoogle Scholar
  40. Quarterman, J, Mills, CF, Humphries, WR 1966The reduced secretion of, and sensitivity to insulin in zinc-deficient ratsBiochem Biophys Res Commun25354358CrossRefPubMedGoogle Scholar
  41. Quesada, AR, Byrnes, RW, Krezoski, SO, Petering, DH 1996Direct reaction of H2O2 with sulfhydryl groups in HL-60 cells: Zinc-metallothionein and other sitesArch Biochem Biophys334241250CrossRefPubMedGoogle Scholar
  42. Robertson, RP 2004Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetesJ Biol Chem2794235142354CrossRefPubMedGoogle Scholar
  43. Ross, SA, Gulve, EA, Wang, M 2004Chemistry and biochemistry of type 2 diabetesChem Rev10412551282CrossRefPubMedGoogle Scholar
  44. Salmeen, A, Andersen, JN, Myers, MP, Meng, TC, Hinks, JA, Tonks, NK, Barford, D 2003Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediateNature423769773CrossRefPubMedGoogle Scholar
  45. Samet, JM, Silbajoris, R, Wu, W, Graves, LM 1999Tyrosine phosphatases as targets in metal-induced signaling in human airway epithelial cellsAm J Respir Cell Mol Biol21357364PubMedGoogle Scholar
  46. Saurin, AT, Neubert, H, Brennan, JP, Eaton, P 2004Widespread sulfenic acid formation in tissues in response to hydrogen peroxideProc Natl Acad Sci USA1011798217987CrossRefPubMedGoogle Scholar
  47. Shisheva, A, Gefel, D, Shechter, Y 1992Insulinlike effects of zinc ion in vitro and in vivo. Preferential effects on desensitized adipocytes and induction of normoglycemia in streptozocin-induced ratsDiabetes41982988PubMedGoogle Scholar
  48. Simon, SF, Taylor, CG 2001Dietary zinc supplementation attenuates hyperglycemia in db/db miceExp Biol Med2264351Google Scholar
  49. Tang, X, Shay, NF 2001Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytesJ Nutr13114141420PubMedGoogle Scholar
  50. Montfort, RL, Congreve, M, Tisi, D, Carr, R, Jhoti, H 2003Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1BNature423773777CrossRefPubMedGoogle Scholar
  51. Xie, J, Zhu, H, Larade, K, Ladoux, A, Seguritan, A, Chu, M, Ito, S, Bronson, RT, Leiter, EH, Zhang, C-Y, Rosen, ED, Bunn, HF 2004Absence of a reductase, NCB5OR, causes insulin-deficient diabetesProc Natl Acad Sci USA1011075010755CrossRefPubMedGoogle Scholar
  52. Yang, Y, Maret, W, Vallee, BL 2001Differential fluorescence labeling of cysteinyl clusters uncovers high tissue levels of thioneinProc Natl Acad Sci USA9855565559CrossRefPubMedGoogle Scholar
  53. Zabolotny, JM, Haj, FG, Kim, Y-B, Kim, H-J, Shulman, GI, Kim, JK, Neel, BG, Kahn, BB 2004Transgenic overexpression of protein-tyrosine phosphatase 1B in muscle causes insulin resistance, but overexpression with leukocyte antigen-related phosphatase does not additively impair insulin actionJ Biol Chem2792484424851Google Scholar
  54. Zinker, BA, Rondinone, CM, Trevillyan, JM, Gum, RJ, Clampit, JE, Waring, JF, Xie, N, Wilcox, D, Jacobson, P, Frost, L, Kroeger, PE, Reilly, RM, Koterski, S, Opgenorth, TJ, Ulrich, RG, Crosby, S, Butler, M, Murray, SF, McKay, RA, Bhanot, S, Monia, BP, Jirousek, MR 2002PTP 1B antisense oligonucleotide lowers PTP 1B protein, normalizes blood glucose, and improves insulin sensitivity in diabetic miceProc Natl Acad Sci USA991135711362CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  1. 1.Institute of ImmunologyUniversity Hospital RWTH AachenGermany
  2. 2.Departments of Preventive Medicine & Community Health and AnesthesiologyUniversity of Texas Medical BranchGalvestonUSA

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