Substrate Competitive GSK-3 Inhibitors {single bond} strategy and Implications

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 3, 2010, Pages 598-603

  Eldar Finkelman, Hagit ^a   Licht Murava, Avital ^a   Pietrokovski, Shmuel ^b   Eisenstein, Miriam ^b  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

GSK 3; Inhibitors; Phosphorylation; Protein kinase; Substrate recognition

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; ADENOSINE TRIPHOSPHATE; AR A 014418; BENZAZEPIONE; CHIR 98023; CHIR 99021; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; L 803; NP 00111; PYRAZOLOPYRIDINE; PYRROLOAZEPINE; SB 41528; TDZD 8; UNCLASSIFIED DRUG;

BINDING SITE; DIABETES MELLITUS; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; FOOD INTAKE; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HUMAN; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; REVIEW; WEIGHT CHANGE;

ANIMALS; DIABETES MELLITUS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; NEURODEGENERATIVE DISEASES; PROTEIN KINASE INHIBITORS; SUBSTRATE SPECIFICITY;

EUKARYOTA;

EID: 75349098918     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2009.09.010     Document Type: Review

References (70)

1. Woodgett J.R. Molecular cloning and expression of glycogen synthase kinase-3/factorA. EMBO J. 9 (1990) 2431-2438
2. Eldar-Finkelman H. Glycogen synthase kinase-3: an emerging therapeutic target. Trends Mol. Med. 8 (2002) 126-132
3. Doble B.W., and Woodgett J.R. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116 (2003) 1175-1186
4. Jope R.S., Yuskaitis C.J., and Beurel E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 32 (2007) 577-595
5. Frame S., and Cohen P. GSK-3 takes center stage more than 20 years after its discovery. Biochem. J. 359 (2001) 1-16
6. Patel S., Doble B., and Woodgett J.R. Glycogen synthase kinase-3 in insulin and Wnt signalling: a double-edged sword?. Biochem. Soc. Trans. 32 (2004) 803-808
7. Jope R.S., and Johnson G.V. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29 (2004) 95-102
8. Gould T.D., Zarate C.A., and Manji H.K. Glycogen synthase kinase-3: a target for novel bipolar disorder treatments. J. Clin. Psychiatry 65 (2004) 10-21
9. Martinez A. Preclinical efficacy on GSK-3 inhibitors: towards a future generation of powerful drugs. Med. Res. Rev. 28 (2008) 773-796
10. Patel S., and Woodgett J. Glycogen synthase kinase-3 and cancer: good cop, bad cop?. Cancer Cell 14 (2008) 351-353
11. Woodgett J.R., and Cohen P. Multisite phosphorylation of glycogen synthase. Molecular basis for the substrate specificity of glycogen synthase kinase-3 and casein kinase-II (glycogen synthase kinase-5). Biochim. Biophys. Acta 788 (1984) 339-347
12. Fiol C.J., Mahrenholz A.M., Wang Y., Roeske R.W., and Roach P.J. Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3. J. Biol. Chem. 262 (1987) 14042-14048
13. Liberman Z., and Eldar-Finkelman H. Serine 332 phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 attenuates insulin signaling. J. Biol. Chem. 280 (2005) 4422-4428
14. Sharfi H., and Eldar-Finkelman H. Sequential phosphorylation of insulin receptor substrate-2 by glycogen synthase kinase-3 and c-Jun NH2-terminal kinase plays a role in hepatic insulin signaling. Am. J. Physiol. Endocrinol. Metab. 294 (2008) E307-E315
15. van Es J.H., Barker N., and Clevers H. You Wnt some, you lose some: oncogenes in the Wnt signaling pathway. Curr. Opin. Genet. Dev. 13 (2003) 28-33
16. Angers S., and Moon R. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 10 (2009) 468-4677
17. Cohen E.D., Tian Y., and Morrisey E.E. Wnt signaling: an essential regulator of cardiovascular differentiation, morphogenesis and progenitor self-renewal. Development 135 (2008) 789-798
18. Aberle H., Bauer A., Stappert J., Kispert A., and Kemler R. beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16 (1997) 3797-3804
19. Liu C., Li Y., Semenov M., Han C., Baeg G.H., Tan Y., Zhang Z., Lin X., and He X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108 (2002) 837-847
20. Fiol C.J., Williams J.S., Chou C.H., Wang Q.M., Roach P.J., and Andrisani O.M. A secondary phosphorylation of CREB341 at Ser129 is required for the cAMP-mediated control of gene expression. A role for glycogen synthase kinase-3 in the control of gene expression. J. Biol. Chem. 269 (1994) 32187-32193
21. Bush A.L., and Hyson R.L. Effects of lithium and deafferentation on expression of glycogen synthase kinase-3beta, NFκB, beta-catenin and pCreb in the chick cochlear nucleus. Brain Res. 1203 (2008) 18-25
22. Chu B., Soncin F., Price B.D., Stevenson M.A., and Calderwood S.K. Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271 (1996) 30847-30857
23. Beals C.R., Sheridan C.M., Turck C.W., Gardner P., and Crabtree G.R. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275 (1997) 1930-1934
24. Pasinetti G.M., and Eberstein J.A. Metabolic syndrome and the role of dietary lifestyles in Alzheimer's disease. J. Neurochem. 106 (2008) 1503-1514
25. Luchsinger J.A. Adiposity, hyperinsulinemia, diabetes and Alzheimer's disease: an epidemiological perspective. Eur. J. Pharmacol. 585 (2008) 119-129
26. Doble B.W., Patel S., Wood G.A., Kockeritz L.K., and Woodgett J.R. Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev. Cell 12 (2007) 957-971
27. MacAulay K., Doble B.W., Patel S., Hansotia T., Sinclair E.M., Drucker D.J., Nagy A., and Woodgett J.R. Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism. Cell. Metab. 6 (2007) 329-337
28. Kerkela R., Kockeritz L., Macaulay K., Zhou J., Doble B.W., Beahm C., Greytak S., Woulfe K., Trivedi C.M., Woodgett J.R., Epstein J.A., Force T., and Huggins G.S. Deletion of GSK-3beta in mice leads to hypertrophic cardiomyopathy secondary to cardiomyoblast hyperproliferation. J. Clin. Invest. 118 (2008) 3609-3618
29. Liang M.H., and Chuang D.M. Differential roles of glycogen synthase kinase-3 isoforms in the regulation of transcriptional activation. J. Biol. Chem. 281 (2006) 30479-30484
30. Liang M.H., and Chuang D.M. Regulation and function of glycogen synthase kinase-3 isoforms in neuronal survival. J. Biol. Chem. 282 (2007) 3904-3917
31. Eldar-Finkelman H., and Eisenstein M. Peptide inhibitors targeting protein kinases. Curr. Pharm. Des. 15 (2009) 2463-2470
32. Hoeflich K.P., Luo J., Rubie E.A., Tsao M.S., Jin O., and Woodgett J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-κB activation. Nature 406 (2000) 86-90
33. Ilouz R., Kowelsman N., Eisenstein M., and Eldar-Finkelman H. Identification of novel glycogen synthase kinase-3beta substrate-interacting residues suggests a common mechanism for substrate recognition. J. Biol. Chem. 281 (2006) 30621-30630
34. Dajani R., Fraser E., Roe S.M., Young N., Good V., Dale T.C., and Pearl L.H. Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 105 (2001) 721-732
35. ter Haar E., Coll J.T., Austen D.A., Hsiao H.M., Swenson L., and Jain J. Structure of GSK3beta reveals a primed phosphorylation mechanism. Nat. Struct. Biol. 8 (2001) 593-596
36. Frame S., Cohen P., and Biondi R.M. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol. Cell 7 (2001) 1321-1327
37. Plotkin B., Kaidanovich O., Talior I., and Eldar-Finkelman H. Insulin mimetic action of synthetic phosphorylated peptide inhibitors of glycogen synthase kinase-3. J. Pharmacol. Exp. Ther. (2003) 974-980
38. O. Kaidanovich-Beilien, H. Eldar-Finkelman, Long-Term Treatment with Novel Glycogen Synthase Kinase-3 Inhibitor Improves Glucose Homeostasis in Ob/Ob Mice: Molecular Characterization In Liver And Muscle, J. Pharmacol. Exp. Ther. 16 (2006) 17-24.
39. Rao R., Hao C.M., Redha R., Wasserman D.H., McGuinness O.P., and Breyer M.D. Glycogen synthase kinase 3 inhibition improves insulin-stimulated glucose metabolism but not hypertension in high-fat-fed C57BL/6J mice. Diabetologia 50 (2007) 452-460
40. Grimes C.A., and Jope R.S. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 65 (2001) 391-426
41. Hooper C., Killick R., and Lovestone S. The GSK3 hypothesis of Alzheimer's disease. J. Neurochem. 104 (2008) 1433-1439
42. Rowe M.K., Wiest C., and Chuang D.M. GSK-3 is a viable potential target for therapeutic intervention in bipolar disorder. Neurosci. Biobehav. Rev. 31 (2007) 920-931
43. Klein P.S., and Melton D.A. A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 8455-8459
44. Porsolt R.D., Le Pichon M., and Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 266 (1977) 730-732
45. Kaidanovich-beilin O., Milman A., Weizman A., Pick C., and Eldar-Finkelman H. Rapid anti-depressive like activity of specific GSK-3 inhibitor, and its effect on -catenin in the mouse hippocampus. Biol. Psychiatry 55 (2004) 781-784
46. Gould T.D., Einat H., Bhat R., and Manji H.K. AR-A014418, a selective GSK-3 inhibitor, produces antidepressant-like effects in the forced swim test. Int. J. Neuropsychopharmacol. 7 (2004) 387-390
47. O'Brien W.T., Harper A.D., Jove F., Woodgett J.R., Maretto S., Piccolo S., and Klein P.S. Glycogen synthase kinase-3beta haploinsufficiency mimics the behavioral and molecular effects of lithium. J. Neurosci. 24 (2004) 6791-6798
48. Shapira M., Licht A., Milman A., Pick C.G., Shohami E., and Eldar-Finkelman H. Role of glycogen synthase kinase-3beta in early depressive behavior induced by mild traumatic brain injury. Mol. Cell. Neurosci. 34 (2007) 571-577
49. Chen G., Bower K.A., Ma C., Fang S., Thiele C.J., and Luo J. Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamine-induced neuronal death. FASEB J. 18 (2004) 1162-1164
50. Kim W.Y., Zhou F.Q., Zhou J., Yokota Y., Wang Y.M., Yoshimura T., Kaibuchi K., Woodgett J.R., Anton E.S., and Snider W.D. Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52 (2006) 981-996
51. Mao Y., Ge X., Frank C.L., Madison J.M., Koehler A.N., Doud M.K., Tassa C., Berry E.M., Soda T., Singh K.K., Biechele T., Petryshen T.L., Moon R.T., Haggarty S.J., and Tsai L.H. Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3beta/beta-catenin signaling. Cell 136 (2009) 1017-1031
52. Sutherland C., Leighton I.A., and Cohen P. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J. 295 (1993) 15-19
53. Welsh G.I., and Proud C.G. Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem. J. 294 (1993) 625-629
54. Stambolic V., Ruel L., and Woodgett J.R. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6 (1996) 1664-1668
55. Ilouz R., Pietrokovsky S., Eisenstein M., and Eldar-Finkelman H. New insights into the autoinhibition mechanism of glycogen synthase kinase-3 beta. J. Mol. Biol. 385 (2008) 999-1007
56. Hanks S.K., and Hunter T. Protein kinases. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9 (1995) 576-596
57. Coghlan M.P., Culbert A.A., Cross D.A., Corcoran S.L., Yates J.W., Pearce N.J., Rausch O.L., Murphy G.J., Carter P.S., Roxbee Cox L., Mills D., Brown M.J., Haigh D., Ward R.W., Smith D.G., Murray K.J., Reith A.D., and Holder J.C. Selective small molecule inhibitors of glycogen synthase kinase-3 modulate glycogen metabolism and gene transcription. Chem. Biol. 7 (2000) 793-803
58. Cline G.W., Johnson K., Regittnig W., Perret P., Tozzo E., Xiano L., Damico C., and Shulman G.I. Effects of a novel glycogen synthase kinase-3 inhibitor on insulin-stimulated glucose metabolism in Zucker diabetic fatty (fa/fa) rats. Diabetes (2002) 2903-2910
59. Henriksen E.J., Kinnick T.R., Teachey M.K., O'Keefe M.P., Ring D., Johnson K.W., and Harrison S.D. Modulation of muscle insulin resistance by selective inhibition of GSK-3 in Zucker diabetic fatty rats. Am. J. Physiol. Endocrinol. Metab. 284 (2003) E892-E900
60. Bhat R., Xue Y., Berg S., Hellberg S., Ormo M., Nilsson Y., Radesater A.C., Jerning E., Markgren P.O., Borgegard T., Nylof M., Gimenez-Cassina A., Hernandez F., Lucas J.J., Diaz-Nido J., and Avila J. Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem. 278 (2003) 45937-45945
61. Leost M., Schultz C., Link A., Wu Y.Z., Biernat J., Mandelkow E.M., Bibb J.A., Snyder G.L., Greengard P., Zaharevitz D.W., Gussio R., Senderowicz A.M., Sausville E.A., Kunick C., and Meijer L. Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25. Eur. J. Biochem. 267 (2000) 5983-5994
62. Meijer L., Skaltsounis A.L., Magiatis P., Polychronopoulos P., Knockaert M., Leost M., Ryan X.P., Vonica C.A., Brivanlou A., Dajani R., Crovace C., Tarricone C., Musacchio A., Roe S.M., Pearl L., and Greengard P. GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem. Biol. 10 (2003) 1255-1266
63. Meijer L., Thunnissen A.M., White A.W., Garnier M., Nikolic M., Tsai L.H., Walter J., Cleverley K.E., Salinas P.C., Wu Y.Z., Biernat J., Mandelkow E.M., Kim S.H., and Pettit G.R. Inhibition of cyclin-dependent kinases, GSK-3beta and CK1 by hymenialdisine, a marine sponge constituent. Chem. Biol. 7 (2000) 51-63
64. Witherington J., Bordas V., Gaiba A., Garton N.S., Naylor A., Rawlings A.D., Slingsby B.P., Smith D.G., and Takle A.K. R.W. Ward, 6-aryl-pyrazolo[3,4-b]pyridines: potent inhibitors of glycogen synthase kinase-3 (GSK-3). Bioorg. Med. Chem. Lett. 13 (2003) 3055-3057
65. Martinez A., Alonso M., Castro A., Perez C., and Moreno F.J. First non-ATP competitive glycogen synthase kinase 3 beta (GSK-3beta) inhibitors: thiadiazolidinones (TDZD) as potential drugs for the treatment of Alzheimer's disease. J. Med. Chem. 45 (2002) 1292-1299
66. Rosa A.O., Egea J., Martinez A., Garcia A.G., and Lopez M.G. Neuroprotective effect of the new thiadiazolidinone NP00111 against oxygen-glucose deprivation in rat hippocampal slices: implication of ERK1/2 and PPARgamma receptors. Exp. Neurol. 212 (2008) 93-99
67. Medina M., and Castro A. Glycogen synthase kinase-3 (GSK-3) inhibitors reach the clinic. Curr. Opin. Drug Discov. Dev. 11 (2008) 533-543
68. Ring D.B., Johnson K.W., Henriksen E.J., Nuss J.M., Goff D., Kinnick T.R., Ma S.T., Reeder J.W., Samuels I., Slabiak T., Wagman A.S., Hammond M.E., and Harrison S.D. Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52 (2003) 588-595
69. Meijer L., Flajolet M., and Greengard P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol. Sci. 25 (2004) 471-480
70. Eldar-Finkelman H., and Ilouz R. Challenges and opportunities with glycogen synthase kinase-3 inhibitors for insulin resistance and Type 2 diabetes treatment. Expert Opin. Investig. Drugs 12 (2003) 1511-1519