MAP kinase activator from insulin-stimulated skeletal muscle is a protein threonine/tyrosine kinase (original) (raw)

Abstract

A 'MAP kinase activator' was purified several thousand-fold from insulin-stimulated rabbit skeletal muscle, which resembled the 'activator' from nerve growth factor-stimulated PC12 cells in that it could be inactivated by incubation with protein phosphatase 2A, but not by protein tyrosine phosphatases and its apparent molecular mass was 45-50 kDa. In the presence of MgATP, 'MAP kinase activator' converted the normal 'wild-type' 42 kDa MAP kinase from an inactive dephosphorylated form to the fully active diphosphorylated species. Phosphorylation occurred on the same threonine and tyrosine residues which are phosphorylated in vivo in response to growth factors or phorbol esters. A mutant MAP kinase produced by changing a lysine at the active centre to arginine was phosphorylated in an identical manner by the 'MAP kinase activator', but no activity was generated. The results demonstrate that 'MAP kinase activator' is a protein kinase (MAP kinase kinase) and not a protein that stimulates the autophosphorylation of MAP kinase. MAP kinase kinase is the first established example of a protein kinase that can phosphorylate an exogenous protein on threonine as well as tyrosine residues.

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  1. Adams P. D., Parker P. J. TPA-induced activation of MAP kinase. FEBS Lett. 1991 Sep 23;290(1-2):77–82. doi: 10.1016/0014-5793(91)81230-6. [DOI] [PubMed] [Google Scholar]
  2. Adler S. P., Purich D., Stadtman E. R. Cascade control of Escherichia coli glutamine synthetase. Properties of the PII regulatory protein and the uridylyltransferase-uridylyl-removing enzyme. J Biol Chem. 1975 Aug 25;250(16):6264–6272. [PubMed] [Google Scholar]
  3. Ahn N. G., Seger R., Bratlien R. L., Diltz C. D., Tonks N. K., Krebs E. G. Multiple components in an epidermal growth factor-stimulated protein kinase cascade. In vitro activation of a myelin basic protein/microtubule-associated protein 2 kinase. J Biol Chem. 1991 Mar 5;266(7):4220–4227. [PubMed] [Google Scholar]
  4. Ahn N. G., Weiel J. E., Chan C. P., Krebs E. G. Identification of multiple epidermal growth factor-stimulated protein serine/threonine kinases from Swiss 3T3 cells. J Biol Chem. 1990 Jul 15;265(20):11487–11494. [PubMed] [Google Scholar]
  5. Anderson N. G., Maller J. L., Tonks N. K., Sturgill T. W. Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase. Nature. 1990 Feb 15;343(6259):651–653. doi: 10.1038/343651a0. [DOI] [PubMed] [Google Scholar]
  6. Binétruy B., Smeal T., Karin M. Ha-Ras augments c-Jun activity and stimulates phosphorylation of its activation domain. Nature. 1991 May 9;351(6322):122–127. doi: 10.1038/351122a0. [DOI] [PubMed] [Google Scholar]
  7. Bodwell J. E., Ortí E., Coull J. M., Pappin D. J., Smith L. I., Swift F. Identification of phosphorylated sites in the mouse glucocorticoid receptor. J Biol Chem. 1991 Apr 25;266(12):7549–7555. [PubMed] [Google Scholar]
  8. Boulton T. G., Gregory J. S., Cobb M. H. Purification and properties of extracellular signal-regulated kinase 1, an insulin-stimulated microtubule-associated protein 2 kinase. Biochemistry. 1991 Jan 8;30(1):278–286. doi: 10.1021/bi00215a038. [DOI] [PubMed] [Google Scholar]
  9. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  10. Cobb M. H., Boulton T. G., Robbins D. J. Extracellular signal-regulated kinases: ERKs in progress. Cell Regul. 1991 Dec;2(12):965–978. doi: 10.1091/mbc.2.12.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cohen P., Alemany S., Hemmings B. A., Resink T. J., Strålfors P., Tung H. Y. Protein phosphatase-1 and protein phosphatase-2A from rabbit skeletal muscle. Methods Enzymol. 1988;159:390–408. doi: 10.1016/0076-6879(88)59039-0. [DOI] [PubMed] [Google Scholar]
  12. Cohen P., Holmes C. F., Tsukitani Y. Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem Sci. 1990 Mar;15(3):98–102. doi: 10.1016/0968-0004(90)90192-e. [DOI] [PubMed] [Google Scholar]
  13. Cool D. E., Tonks N. K., Charbonneau H., Fischer E. H., Krebs E. G. Expression of a human T-cell protein-tyrosine-phosphatase in baby hamster kidney cells. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7280–7284. doi: 10.1073/pnas.87.18.7280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Crews C. M., Alessandrini A. A., Erikson R. L. Mouse Erk-1 gene product is a serine/threonine protein kinase that has the potential to phosphorylate tyrosine. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8845–8849. doi: 10.1073/pnas.88.19.8845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dent P., Lavoinne A., Nakielny S., Caudwell F. B., Watt P., Cohen P. The molecular mechanism by which insulin stimulates glycogen synthesis in mammalian skeletal muscle. Nature. 1990 Nov 22;348(6299):302–308. doi: 10.1038/348302a0. [DOI] [PubMed] [Google Scholar]
  16. Goris J., Pallen C. J., Parker P. J., Hermann J., Waterfield M. D., Merlevede W. Conversion of a phosphoseryl/threonyl phosphatase into a phosphotyrosyl phosphatase. Biochem J. 1988 Dec 15;256(3):1029–1034. doi: 10.1042/bj2561029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gómez N., Cohen P. Dissection of the protein kinase cascade by which nerve growth factor activates MAP kinases. Nature. 1991 Sep 12;353(6340):170–173. doi: 10.1038/353170a0. [DOI] [PubMed] [Google Scholar]
  18. Gómez N., Tonks N. K., Morrison C., Harmar T., Cohen P. Evidence for communication between nerve growth factor and protein tyrosine phosphorylation. FEBS Lett. 1990 Oct 1;271(1-2):119–122. doi: 10.1016/0014-5793(90)80386-w. [DOI] [PubMed] [Google Scholar]
  19. Hanks S. K., Quinn A. M., Hunter T. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science. 1988 Jul 1;241(4861):42–52. doi: 10.1126/science.3291115. [DOI] [PubMed] [Google Scholar]
  20. Hardie D. G., Guy P. S. Reversible phosphorylation and inactivation of acetyl-CoA carboxylase from lactating rat mammary gland by cyclic AMP-dependent protein kinase. Eur J Biochem. 1980 Sep;110(1):167–177. doi: 10.1111/j.1432-1033.1980.tb04852.x. [DOI] [PubMed] [Google Scholar]
  21. Her J. H., Wu J., Rall T. B., Sturgill T. W., Weber M. J. Sequence of pp42/MAP kinase, a serine/threonine kinase regulated by tyrosine phosphorylation. Nucleic Acids Res. 1991 Jul 11;19(13):3743–3743. doi: 10.1093/nar/19.13.3743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hoshi M., Nishida E., Sakai H. Activation of a Ca2+-inhibitable protein kinase that phosphorylates microtubule-associated protein 2 in vitro by growth factors, phorbol esters, and serum in quiescent cultured human fibroblasts. J Biol Chem. 1988 Apr 15;263(11):5396–5401. [PubMed] [Google Scholar]
  23. Katz J. D., Ohnishi K., Lebow L. T., Bonavida B. The SJL/J T cell response to both spontaneous and transplantable syngeneic reticulum cell sarcoma is mediated predominantly by the V beta 17a+ T cell clonotype. J Exp Med. 1988 Nov 1;168(5):1553–1562. doi: 10.1084/jem.168.5.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Krieg J., Hofsteenge J., Thomas G. Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J Biol Chem. 1988 Aug 15;263(23):11473–11477. [PubMed] [Google Scholar]
  25. L'Allemain G., Sturgill T. W., Weber M. J. Defective regulation of mitogen-activated protein kinase activity in a 3T3 cell variant mitogenically nonresponsive to tetradecanoyl phorbol acetate. Mol Cell Biol. 1991 Feb;11(2):1002–1008. doi: 10.1128/mcb.11.2.1002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  27. Lavoinne A., Erikson E., Maller J. L., Price D. J., Avruch J., Cohen P. Purification and characterisation of the insulin-stimulated protein kinase from rabbit skeletal muscle; close similarity to S6 kinase II. Eur J Biochem. 1991 Aug 1;199(3):723–728. doi: 10.1111/j.1432-1033.1991.tb16176.x. [DOI] [PubMed] [Google Scholar]
  28. Lindberg R. A., Quinn A. M., Hunter T. Dual-specificity protein kinases: will any hydroxyl do? Trends Biochem Sci. 1992 Mar;17(3):114–119. doi: 10.1016/0968-0004(92)90248-8. [DOI] [PubMed] [Google Scholar]
  29. Mangum J. H., Magni G., Stadtman E. R. Regulation of glutamine synthetase adenylylation and deadenylylation by the enzymatic uridylylation and deuridylylation of the PII regulatory protein. Arch Biochem Biophys. 1973 Oct;158(2):514–525. doi: 10.1016/0003-9861(73)90543-2. [DOI] [PubMed] [Google Scholar]
  30. Nel A. E., Hanekom C., Rheeder A., Williams K., Pollack S., Katz R., Landreth G. E. Stimulation of MAP-2 kinase activity in T lymphocytes by anti-CD3 or anti-Ti monoclonal antibody is partially dependent on protein kinase C. J Immunol. 1990 Apr 1;144(7):2683–2689. [PubMed] [Google Scholar]
  31. Payne D. M., Rossomando A. J., Martino P., Erickson A. K., Her J. H., Shabanowitz J., Hunt D. F., Weber M. J., Sturgill T. W. Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J. 1991 Apr;10(4):885–892. doi: 10.1002/j.1460-2075.1991.tb08021.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Posada J., Sanghera J., Pelech S., Aebersold R., Cooper J. A. Tyrosine phosphorylation and activation of homologous protein kinases during oocyte maturation and mitogenic activation of fibroblasts. Mol Cell Biol. 1991 May;11(5):2517–2528. doi: 10.1128/mcb.11.5.2517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pulverer B. J., Kyriakis J. M., Avruch J., Nikolakaki E., Woodgett J. R. Phosphorylation of c-jun mediated by MAP kinases. Nature. 1991 Oct 17;353(6345):670–674. doi: 10.1038/353670a0. [DOI] [PubMed] [Google Scholar]
  34. Ray L. B., Sturgill T. W. Rapid stimulation by insulin of a serine/threonine kinase in 3T3-L1 adipocytes that phosphorylates microtubule-associated protein 2 in vitro. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1502–1506. doi: 10.1073/pnas.84.6.1502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sanghera J. S., Paddon H. B., Bader S. A., Pelech S. L. Purification and characterization of a maturation-activated myelin basic protein kinase from sea star oocytes. J Biol Chem. 1990 Jan 5;265(1):52–57. [PubMed] [Google Scholar]
  36. Scott J. D., Glaccum M. B., Fischer E. H., Krebs E. G. Primary-structure requirements for inhibition by the heat-stable inhibitor of the cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1613–1616. doi: 10.1073/pnas.83.6.1613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Seger R., Ahn N. G., Boulton T. G., Yancopoulos G. D., Panayotatos N., Radziejewska E., Ericsson L., Bratlien R. L., Cobb M. H., Krebs E. G. Microtubule-associated protein 2 kinases, ERK1 and ERK2, undergo autophosphorylation on both tyrosine and threonine residues: implications for their mechanism of activation. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6142–6146. doi: 10.1073/pnas.88.14.6142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Smeal T., Binetruy B., Mercola D. A., Birrer M., Karin M. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature. 1991 Dec 12;354(6353):494–496. doi: 10.1038/354494a0. [DOI] [PubMed] [Google Scholar]
  39. Sturgill T. W., Ray L. B., Erikson E., Maller J. L. Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature. 1988 Aug 25;334(6184):715–718. doi: 10.1038/334715a0. [DOI] [PubMed] [Google Scholar]
  40. Sturgill T. W., Wu J. Recent progress in characterization of protein kinase cascades for phosphorylation of ribosomal protein S6. Biochim Biophys Acta. 1991 May 17;1092(3):350–357. doi: 10.1016/s0167-4889(97)90012-4. [DOI] [PubMed] [Google Scholar]
  41. Tonks N. K., Charbonneau H., Diltz C. D., Fischer E. H., Walsh K. A. Demonstration that the leukocyte common antigen CD45 is a protein tyrosine phosphatase. Biochemistry. 1988 Nov 29;27(24):8695–8701. doi: 10.1021/bi00424a001. [DOI] [PubMed] [Google Scholar]
  42. Wu J., Rossomando A. J., Her J. H., Del Vecchio R., Weber M. J., Sturgill T. W. Autophosphorylation in vitro of recombinant 42-kilodalton mitogen-activated protein kinase on tyrosine. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9508–9512. doi: 10.1073/pnas.88.21.9508. [DOI] [PMC free article] [PubMed] [Google Scholar]