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. 1990 Jun 15;268(3):539–545. doi: 10.1042/bj2680539

An insulin-sensitive cytosolic protein kinase accounts for the regulation of ATP citrate-lyase phosphorylation.

K T Yu 1, W B Benjamin 1, S Ramakrishna 1, N Khalaf 1, M P Czech 1
PMCID: PMC1131472  PMID: 2114095

Abstract

Purified rat liver ATP citrate-lyase is phosphorylated on serine residues by an insulin-stimulated cytosolic kinase activity partially purified from rat adipocytes [Yu, Khalaf & Czech (1987) J. Biol. Chem. 262, 16677-16685]. The Km for lyase phosphorylation by this hormone-sensitive kinase activity is approx. 3 microM. Two-dimensional tryptic-peptide mapping of the 32P-labelled lyase reveals that the kinase-catalysed phosphorylation occurs primarily on a specific peptide. In intact 32P-labelled adipocytes, insulin enhances the serine phosphorylation of ATP citrate-lyase by 2-3-fold. Tryptic digestion of the 32P-labelled lyase immunopurified from insulin-treated adipocytes also yields one major phosphopeptide. 32P-labelled lyase tryptic peptides derived from labelling experiments in vitro and in vivo exhibit identical electrophoretic and chromatographic migration profiles. Furthermore, radio-sequencing of the phosphopeptide from lyase 32P-labelled in vitro indicates that serine-3 from the N-terminus is phosphorylated by the insulin-stimulated cytosolic kinase, in agreement with previous studies on the position of the phosphoserine residue in ATP citrate-lyase isolated from insulin-treated cells. Taken together, the similarity in site-specific phosphorylation of ATP citrate-lyase from insulin-treated adipocytes to that catalysed by the hormone-activated cytosolic kinase in vitro strongly suggests that this kinase mediates insulin action on lyase phosphorylation in intact cells.

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  1. Alexander M. C., Kowaloff E. M., Witters L. A., Dennihy D. T., Avruch J. Purification of a hepatic 123,000-dalton hormone-stimulated 32P-peptide and its identification as ATP-citrate lyase. J Biol Chem. 1979 Aug 25;254(16):8052–8056. [PubMed] [Google Scholar]
  2. Alexander M. C., Palmer J. L., Pointer R. H., Koumjian L., Avruch J. The role of the cyclic AMP-dependent protein kinase in the glucagon-stimulated phosphorylation of ATP-citrate lyase. Biochim Biophys Acta. 1981 Apr 17;674(1):37–47. doi: 10.1016/0304-4165(81)90344-5. [DOI] [PubMed] [Google Scholar]
  3. Avruch J., Witters L. A., Alexander M. C., Bush M. A. Effects of glucagon and insulin on cytoplasmic protein phosphorylation in hepatocytes. J Biol Chem. 1978 Jul 10;253(13):4754–4761. [PubMed] [Google Scholar]
  4. Belsham G. J., Brownsey R. W., Denton R. M. Reversibility of the insulin-stimulated phosphorylation of ATP citrate lyase and a cytoplasmic protein of subunit Mr 22000 in adipose tissue. Biochem J. 1982 Apr 15;204(1):345–352. doi: 10.1042/bj2040345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Belsham G. J., Denton R. M., Tanner M. J. Use of a novel rapid preparation of fat-cell plasma membranes employing Percoll to investigate the effects of insulin and adrenaline on membrane protein phosphorylation within intact fat-cells. Biochem J. 1980 Nov 15;192(2):457–467. doi: 10.1042/bj1920457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benjamin W. B., Clayton N. L. Action of insulin and catecholamines on the phosphorylation of proteins associated with the cytosol, membranes, and "fat cake" of rat fat cells. J Biol Chem. 1978 Mar 10;253(5):1700–1709. [PubMed] [Google Scholar]
  7. Bernier M., Laird D. M., Lane M. D. Insulin-activated tyrosine phosphorylation of a 15-kilodalton protein in intact 3T3-L1 adipocytes. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1844–1848. doi: 10.1073/pnas.84.7.1844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blackshear P. J., Nemenoff R. A., Avruch J. Preliminary characterization of a heat-stable protein from rat adipose tissue whose phosphorylation is stimulated by insulin. Biochem J. 1982 Jun 15;204(3):817–824. doi: 10.1042/bj2040817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brownsey R. W., Denton R. M. Evidence that insulin activates fat-cell acetyl-CoA carboxylase by increased phosphorylation at a specific site. Biochem J. 1982 Jan 15;202(1):77–86. doi: 10.1042/bj2020077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brownsey R. W., Edgell N. J., Hopkirk T. J., Denton R. M. Studies on insulin-stimulated phosphorylation of acetyl-CoA carboxylase, ATP citrate lyase and other proteins in rat epididymal adipose tissue. Evidence for activation of a cyclic AMP-independent protein kinase. Biochem J. 1984 Mar 15;218(3):733–743. doi: 10.1042/bj2180733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Burant C. F., Treutelaar M. K., Buse M. G. In vitro and in vivo activation of the insulin receptor kinase in control and denervated skeletal muscle. J Biol Chem. 1986 Jul 5;261(19):8985–8993. [PubMed] [Google Scholar]
  12. Cobb M. H. An insulin-stimulated ribosomal protein S6 kinase in 3T3-L1 cells. J Biol Chem. 1986 Oct 5;261(28):12994–12999. [PubMed] [Google Scholar]
  13. Cobb M. H., Rosen O. M. Description of a protein kinase derived from insulin-treated 3T3-L1 cells that catalyzes the phosphorylation of ribosomal protein S6 and casein. J Biol Chem. 1983 Oct 25;258(20):12472–12481. [PubMed] [Google Scholar]
  14. Corvera S., Czech M. P. Mechanism of insulin action on membrane protein recycling: a selective decrease in the phosphorylation state of insulin-like growth factor II receptors in the cell surface membrane. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7314–7318. doi: 10.1073/pnas.82.21.7314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Czech M. P., Klarlund J. K., Yagaloff K. A., Bradford A. P., Lewis R. E. Insulin receptor signaling. Activation of multiple serine kinases. J Biol Chem. 1988 Aug 15;263(23):11017–11020. [PubMed] [Google Scholar]
  16. Ellis L., Clauser E., Morgan D. O., Edery M., Roth R. A., Rutter W. J. Replacement of insulin receptor tyrosine residues 1162 and 1163 compromises insulin-stimulated kinase activity and uptake of 2-deoxyglucose. Cell. 1986 Jun 6;45(5):721–732. doi: 10.1016/0092-8674(86)90786-5. [DOI] [PubMed] [Google Scholar]
  17. Garrison J. C., Borland M. K., Florio V. A., Twible D. A. The role of calcium ion as a mediator of the effects of angiotensin II, catecholamines, and vasopressin on the phosphorylation and activity of enzymes in isolated hepatocytes. J Biol Chem. 1979 Aug 10;254(15):7147–7156. [PubMed] [Google Scholar]
  18. Garrison J. C. The effects of glucagon, catecholamines, and the calcium ionophore A23187 on the phosphorylation of rat hepatocyte cytosolic proteins. J Biol Chem. 1978 Oct 10;253(19):7091–7100. [PubMed] [Google Scholar]
  19. Gazzano H., Kowalski A., Fehlmann M., Van Obberghen E. Two different protein kinase activities are associated with the insulin receptor. Biochem J. 1983 Dec 15;216(3):575–582. doi: 10.1042/bj2160575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Herrera R., Rosen O. M. Autophosphorylation of the insulin receptor in vitro. Designation of phosphorylation sites and correlation with receptor kinase activation. J Biol Chem. 1986 Sep 15;261(26):11980–11985. [PubMed] [Google Scholar]
  21. Hughes W. A., Brownsey R. W., Denton R. M. Studies on the incorporation of [32P]phosphate into pyruvate dehydrogenase in intact rat fat-cells. Effects of insulin. Biochem J. 1980 Nov 15;192(2):469–481. doi: 10.1042/bj1920469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Häring H. U., White M. F., Machicao F., Ermel B., Schleicher E., Obermaier B. Insulin rapidly stimulates phosphorylation of a 46-kDa membrane protein on tyrosine residues as well as phosphorylation of several soluble proteins in intact fat cells. Proc Natl Acad Sci U S A. 1987 Jan;84(1):113–117. doi: 10.1073/pnas.84.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ingebritsen T. S., Geelen M. J., Parker R. A., Evenson K. J., Gibson D. M. Modulation of hydroxymethylglutaryl-CoA reductase activity, reductase kinase activity, and cholesterol synthesis in rat hepatocytes in response to insulin and glucagon. J Biol Chem. 1979 Oct 25;254(20):9986–9989. [PubMed] [Google Scholar]
  24. Karasik A., Pepinsky R. B., Shoelson S. E., Kahn C. R. Lipocortins 1 and 2 as substrates for the insulin receptor kinase in rat liver. J Biol Chem. 1988 Aug 25;263(24):11862–11867. [PubMed] [Google Scholar]
  25. Kasuga M., Fujita-Yamaguchi Y., Blithe D. L., Kahn C. R. Tyrosine-specific protein kinase activity is associated with the purified insulin receptor. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2137–2141. doi: 10.1073/pnas.80.8.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kasuga M., Fujita-Yamaguchi Y., Blithe D. L., White M. F., Kahn C. R. Characterization of the insulin receptor kinase purified from human placental membranes. J Biol Chem. 1983 Sep 25;258(18):10973–10980. [PubMed] [Google Scholar]
  27. Kasuga M., Zick Y., Blith D. L., Karlsson F. A., Häring H. U., Kahn C. R. Insulin stimulation of phosphorylation of the beta subunit of the insulin receptor. Formation of both phosphoserine and phosphotyrosine. J Biol Chem. 1982 Sep 10;257(17):9891–9894. [PubMed] [Google Scholar]
  28. Kasuga M., Zick Y., Blithe D. L., Crettaz M., Kahn C. R. Insulin stimulates tyrosine phosphorylation of the insulin receptor in a cell-free system. Nature. 1982 Aug 12;298(5875):667–669. doi: 10.1038/298667a0. [DOI] [PubMed] [Google Scholar]
  29. Khan M. N., Savoie S., Bergeron J. J., Posner B. I. Characterization of rat liver endosomal fractions. In vivo activation of insulin-stimulable receptor kinase in these structures. J Biol Chem. 1986 Jun 25;261(18):8462–8472. [PubMed] [Google Scholar]
  30. Klarlund J. K., Bradford A. P., Milla M. G., Czech M. P. Purification of a novel insulin-stimulated protein kinase from rat liver. J Biol Chem. 1990 Jan 5;265(1):227–234. [PubMed] [Google Scholar]
  31. Klein H. H., Freidenberg G. R., Kladde M., Olefsky J. M. Insulin activation of insulin receptor tyrosine kinase in intact rat adipocytes. An in vitro system to measure histone kinase activity of insulin receptors activated in vivo. J Biol Chem. 1986 Apr 5;261(10):4691–4697. [PubMed] [Google Scholar]
  32. Kohanski R. A., Frost S. C., Lane M. D. Insulin-dependent phosphorylation of the insulin receptor-protein kinase and activation of glucose transport in 3T3-L1 adipocytes. J Biol Chem. 1986 Sep 15;261(26):12272–12281. [PubMed] [Google Scholar]
  33. Lawrence J. C., Jr, Hiken J., Burnette B., DePaoli-Roach A. A. Phosphorylation of phosphoprotein phosphatase inhibitor-2 (I-2) in rat fat cells. Biochem Biophys Res Commun. 1988 Jan 15;150(1):197–203. doi: 10.1016/0006-291x(88)90505-0. [DOI] [PubMed] [Google Scholar]
  34. Le Cam A. Insulin and glucagon regulation of protein phosphorylation in isolated hepatocytes. Persistence, reversibility, and concentration dependence of hormonal effect. Evidence for common phosphorylation sites for both hormones on the Mr = 46,000 protein. J Biol Chem. 1982 Jul 25;257(14):8376–8389. [PubMed] [Google Scholar]
  35. McKeel D. W., Jarett L. Preparation and characterization of a plasma membrane fraction from isolated fat cells. J Cell Biol. 1970 Feb;44(2):417–432. doi: 10.1083/jcb.44.2.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Nemenoff R. A., Gunsalus J. R., Avruch J. An insulin-stimulated (ribosomal S6) protein kinase from soluble extracts of H4 hepatoma cells. Arch Biochem Biophys. 1986 Feb 15;245(1):196–203. doi: 10.1016/0003-9861(86)90205-5. [DOI] [PubMed] [Google Scholar]
  37. Nilsson N. O., Strålfors P., Fredrikson G., Belfrage P. Regulation of adipose tissue lipolysis: effects of noradrenaline and insulin on phosphorylation of hormone-sensitive lipase and on lipolysis in intact rat adipocytes. FEBS Lett. 1980 Feb 25;111(1):125–130. doi: 10.1016/0014-5793(80)80776-9. [DOI] [PubMed] [Google Scholar]
  38. Novak-Hofer I., Thomas G. Epidermal growth factor-mediated activation of an S6 kinase in Swiss mouse 3T3 cells. J Biol Chem. 1985 Aug 25;260(18):10314–10319. [PubMed] [Google Scholar]
  39. Oka Y., Mottola C., Oppenheimer C. L., Czech M. P. Insulin activates the appearance of insulin-like growth factor II receptors on the adipocyte cell surface. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4028–4032. doi: 10.1073/pnas.81.13.4028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Perrotti N., Accili D., Marcus-Samuels B., Rees-Jones R. W., Taylor S. I. Insulin stimulates phosphorylation of a 120-kDa glycoprotein substrate (pp120) for the receptor-associated protein kinase in intact H-35 hepatoma cells. Proc Natl Acad Sci U S A. 1987 May;84(10):3137–3140. doi: 10.1073/pnas.84.10.3137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Petruzzelli L., Herrera R., Rosen O. M. Insulin receptor is an insulin-dependent tyrosine protein kinase: copurification of insulin-binding activity and protein kinase activity to homogeneity from human placenta. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3327–3331. doi: 10.1073/pnas.81.11.3327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pierce M. W., Palmer J. L., Keutmann H. T., Avruch J. ATP-citrate lyase. Structure of a tryptic peptide containing the phosphorylation site directed by glucagon and the cAMP-dependent protein kinase. J Biol Chem. 1981 Sep 10;256(17):8867–8870. [PubMed] [Google Scholar]
  43. Pierce M. W., Palmer J. L., Keutmann H. T., Hall T. A., Avruch J. The insulin-directed phosphorylation site on ATP-citrate lyase is identical with the site phosphorylated by the cAMP-dependent protein kinase in vitro. J Biol Chem. 1982 Sep 25;257(18):10681–10686. [PubMed] [Google Scholar]
  44. Pucci D. L., Ramakrishna S., Benjamin W. B. ATP-citrate lyase phosphorylation in rat adipose tissue. J Biol Chem. 1983 Nov 10;258(21):12907–12911. [PubMed] [Google Scholar]
  45. RODBELL M. METABOLISM OF ISOLATED FAT CELLS. I. EFFECTS OF HORMONES ON GLUCOSE METABOLISM AND LIPOLYSIS. J Biol Chem. 1964 Feb;239:375–380. [PubMed] [Google Scholar]
  46. Ramakrishna S., Benjamin W. B. Fat cell protein phosphorylation. Identification of phosphoprotein-2 as ATP-citrate lyase. J Biol Chem. 1979 Sep 25;254(18):9232–9236. [PubMed] [Google Scholar]
  47. Ramakrishna S., Benjamin W. B. Insulin action rapidly decreases multifunctional protein kinase activity in rat adipose tissue. J Biol Chem. 1988 Sep 5;263(25):12677–12681. [PubMed] [Google Scholar]
  48. Ramakrishna S., Pucci D. L., Benjamin W. B. ATP-citrate lyase kinase and cyclic AMP-dependent protein kinase phosphorylate different sites on ATP-citrate lyase. J Biol Chem. 1981 Oct 25;256(20):10213–10216. [PubMed] [Google Scholar]
  49. Ramakrishna S., Pucci D. L., Benjamin W. B. Dependence of ATP-citrate lyase kinase activity on the phosphorylation of ATP-citrate lyase by cyclic AMP-dependent protein kinase. J Biol Chem. 1983 Apr 25;258(8):4950–4956. [PubMed] [Google Scholar]
  50. Ramakrishna S., Pucci D. L., Benjamin W. B. Insulin stimulates the dephosphorylation of phosphothreonine from fat-pad ATP-citrate lyase. Biochem Biophys Res Commun. 1984 Aug 16;122(3):1047–1056. doi: 10.1016/0006-291x(84)91197-5. [DOI] [PubMed] [Google Scholar]
  51. Ranganathan N. S., Linn T. C., Srere P. A. Phosphorylation of dephospho-ATP citrate lyase by the catalytic subunit of cAMP-dependent protein kinase. J Biol Chem. 1982 Jan 25;257(2):698–702. [PubMed] [Google Scholar]
  52. 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]
  53. Sheorain V. S., Khatra B. S., Soderling T. R. Hormonal regulation of skeletal muscle glycogen synthase through covalent phosphorylation. Fed Proc. 1982 Aug;41(10):2618–2622. [PubMed] [Google Scholar]
  54. Smith C. J., Rubin C. S., Rosen O. M. Insulin-treated 3T3-L1 adipocytes and cell-free extracts derived from them incorporate 32P into ribosomal protein S6. Proc Natl Acad Sci U S A. 1980 May;77(5):2641–2645. doi: 10.1073/pnas.77.5.2641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Sobrino F., Hers H. G. The inactivation of phosphorylase and activation of glycogen synthase in the adipose tissue. Eur J Biochem. 1980 Aug;109(1):239–246. doi: 10.1111/j.1432-1033.1980.tb04789.x. [DOI] [PubMed] [Google Scholar]
  56. Sommercorn J., Mulligan J. A., Lozeman F. J., Krebs E. G. Activation of casein kinase II in response to insulin and to epidermal growth factor. Proc Natl Acad Sci U S A. 1987 Dec;84(24):8834–8838. doi: 10.1073/pnas.84.24.8834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Stadtmauer L., Rosen O. M. Phosphorylation of synthetic insulin receptor peptides by the insulin receptor kinase and evidence that the preferred sequence containing Tyr-1150 is phosphorylated in vivo. J Biol Chem. 1986 Jul 25;261(21):10000–10005. [PubMed] [Google Scholar]
  58. Strålfors P. Isoproterenol and insulin control the cellular localization of ATP citrate-lyase through its phosphorylation in adipocytes. J Biol Chem. 1987 Aug 25;262(24):11486–11489. [PubMed] [Google Scholar]
  59. Sturgill T. W., Ray L. B. Muscle proteins related to microtubule associated protein-2 are substrates for an insulin-stimulatable kinase. Biochem Biophys Res Commun. 1986 Jan 29;134(2):565–571. doi: 10.1016/s0006-291x(86)80457-0. [DOI] [PubMed] [Google Scholar]
  60. Tabarini D., Heinrich J., Rosen O. M. Activation of S6 kinase activity in 3T3-L1 cells by insulin and phorbol ester. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4369–4373. doi: 10.1073/pnas.82.13.4369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Tavaré J. M., O'Brien R. M., Siddle K., Denton R. M. Analysis of insulin-receptor phosphorylation sites in intact cells by two-dimensional phosphopeptide mapping. Biochem J. 1988 Aug 1;253(3):783–788. doi: 10.1042/bj2530783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Thomas G., Martin-Pérez J., Siegmann M., Otto A. M. The effect of serum, EGF, PGF2 alpha and insulin on S6 phosphorylation and the initiation of protein and DNA synthesis. Cell. 1982 Aug;30(1):235–242. doi: 10.1016/0092-8674(82)90029-0. [DOI] [PubMed] [Google Scholar]
  63. Tornqvist H. E., Gunsalus J. R., Nemenoff R. A., Frackelton A. R., Pierce M. W., Avruch J. Identification of the insulin receptor tyrosine residues undergoing insulin-stimulated phosphorylation in intact rat hepatoma cells. J Biol Chem. 1988 Jan 5;263(1):350–359. [PubMed] [Google Scholar]
  64. Vargas A. M., Halestrap A. P., Denton R. M. The effects of glucagon, phenylephrine and insulin on the phosphorylation of cytoplasmic, mitochondrial and membrane-bound proteins of intact liver cells from starved rats. Biochem J. 1982 Oct 15;208(1):221–229. doi: 10.1042/bj2080221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. White M. F., Maron R., Kahn C. R. Insulin rapidly stimulates tyrosine phosphorylation of a Mr-185,000 protein in intact cells. Nature. 1985 Nov 14;318(6042):183–186. doi: 10.1038/318183a0. [DOI] [PubMed] [Google Scholar]
  66. White M. F., Shoelson S. E., Keutmann H., Kahn C. R. A cascade of tyrosine autophosphorylation in the beta-subunit activates the phosphotransferase of the insulin receptor. J Biol Chem. 1988 Feb 25;263(6):2969–2980. [PubMed] [Google Scholar]
  67. Witters L. A. Insulin stimulates the phosphorylation of acetyl-CoA carboxylase. Biochem Biophys Res Commun. 1981 May 29;100(2):872–878. doi: 10.1016/s0006-291x(81)80254-9. [DOI] [PubMed] [Google Scholar]
  68. Witters L. A., Tipper J. P., Bacon G. W. Stimulation of site-specific phosphorylation of acetyl coenzyme A carboxylase by insulin and epinephrine. J Biol Chem. 1983 May 10;258(9):5643–5648. [PubMed] [Google Scholar]
  69. Yu K. T., Czech M. P. Tyrosine phosphorylation of insulin receptor beta subunit activates the receptor tyrosine kinase in intact H-35 hepatoma cells. J Biol Chem. 1986 Apr 5;261(10):4715–4722. [PubMed] [Google Scholar]
  70. Yu K. T., Czech M. P. Tyrosine phosphorylation of the insulin receptor beta subunit activates the receptor-associated tyrosine kinase activity. J Biol Chem. 1984 Apr 25;259(8):5277–5286. [PubMed] [Google Scholar]
  71. Yu K. T., Khalaf N., Czech M. P. Insulin stimulates a membrane-bound serine kinase that may be phosphorylated on tyrosine. Proc Natl Acad Sci U S A. 1987 Jun;84(12):3972–3976. doi: 10.1073/pnas.84.12.3972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Yu K. T., Khalaf N., Czech M. P. Insulin stimulates a novel Mn2+-dependent cytosolic serine kinase in rat adipocytes. J Biol Chem. 1987 Dec 5;262(34):16677–16685. [PubMed] [Google Scholar]
  73. Yu K. T., Khalaf N., Czech M. P. Insulin stimulates the tyrosine phosphorylation of a Mr = 160,000 glycoprotein in rat adipocyte plasma membranes. J Biol Chem. 1987 Jun 5;262(16):7865–7873. [PubMed] [Google Scholar]
  74. Zimmerman C. L., Appella E., Pisano J. J. Advances in the analysis of amino acid phenylthiohydantoins by high performance liquid chromatography. Anal Biochem. 1976 Sep;75(1):77–85. doi: 10.1016/0003-2697(76)90057-9. [DOI] [PubMed] [Google Scholar]

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