Importance of autophosphorylation at Ser186 in the a-loop of salt inducible kinase 1 for its sustained kinase activity

Journal of Cellular Biochemistry

Volumn 104, Issue 5, 2008, Pages 1724-1739

  Hashimoto, Yoshiko Katoh ^a   Satoh, Tomohiro ^b   Okamoto, Mitsuhiro ^c   Takemori, Hiroshi ^a  

^a NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^b Protein Express Co Ltd   (Japan)

^c TEZUKAYAMA UNIVERSITY   (Japan)

Author keywords

Activation loop; Autophosphorylation; GSK 3 ; LKB1; Signal transduction; SIK

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHOTRANSFERASE; SERINE;

ARTICLE; CELL CULTURE; ENZYME ACTIVITY; ENZYME STRUCTURE; HELA CELL; HUMAN; HUMAN CELL; IN VITRO SELECTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

14-3-3 PROTEINS; ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; GLYCOGEN SYNTHASE KINASE 3; HELA CELLS; HUMANS; INDOLES; MICE; OXIMES; PHOSPHORYLATION; PHOSPHOSERINE; PHOSPHOTHREONINE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RATS;

EID: 50249148288     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21737     Document Type: Article

References (49)

1. Al-Hakim AK, Goransson O, Deak M, Toth R, Campbell DG, Morrice NA, Prescott AR, Alessi DR. 2005. 14-3-3 cooperates with LKB1 to regulate the activity and localization of QSK and SIK. J Cell Sci 118:5661-5673.
2. Berdeaux R, Goebel N, Banaszynski L, Takemori H, Wandless T, Shelton GD, Montminy M. 2007. SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes. Nat Med 13:597-603.
3. Boer U, Eglins J, Krause D, Schnell S, Schofl C, Knepel W. 2007. Enhancement by lithium of cAMP-induced CRE/ CREB-directed gene transcription conferred by TORC on the CREB basic leucine zipper domain. Biochem J 15: 69-77.
4. Boudeau J, Baas AF, Deak M, Morrice NA, Kieloch A, Schutkowski M, Prescott AR, Clevers HC, Alessi DR. 2003. MO25alpha/beta interact with STRADalpha/ beta enhancing their ability to bind, activate and localize LKB1 in the cytoplasm. EMBO J 22:5102-5114.
5. Crate BE, Seefeld K, Gamble J, Kemp BE, Witters LA. 1998. Functional domains of the alphal catalytic subunit of the AMP-activated protein kinase. J Biol Chem 273:35347-35354.
6. Doble BW, Woodgett JR. 2003. GSK-3: Tricks of the trade for a multi-tasking kinase. J Cell Sci 116:1175-1186.
7. Doi J, Takemori H, Lin X-Z, Horike N, Katoh Y, Okamoto M. 2002. Salt-inducible kinase represses PKA-mediated activation of human cholesterol side chain cleavage cytochrome promoter through the CREB basic leucine zipper domain. J Biol Chem 277:15629-15637.
8. Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E. 1997. MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297-308.
9. El Jamali A, Freund C, Rechner C, Scheidereit C, Dietz R, Bergmann MW. 2004. Reoxygenation after severe hypoxia induces cardiomyocyte hypertrophy in vitro: Activation of CREB downstream of GSK3beta. FASEB J 18: 1096-1098.
10. Eswarakumar VP, Lax I, Schlessinger J. 2005. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16:139-149.
11. Feldman JD, Vician L, Crispino M, Hoe W, Baudry M, Herschman HR. 2000. The salt-inducible kinase, SIK, is induced by depolarization in brain. J Neurochem 74: 2227-2238.
12. Fiol CJ, Mahrenholz AM, Wang Y, Roeske RW, Roach PJ. 1987. 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 262:14042-14048.
13. Fiol CJ, Williams JS, Chou CH, Wang QM, Roach PJ, Andrisani OM. 1994. 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 269:32187-32193.
14. Frame S, Cohen P, Biondi RM. 2001. A common phosphate binding site explains the unique substrate specificity of GSK3 and its inactivation by phosphorylation. Mol Cell 7:1321-1327.
15. Hansen TO, Rehfeld JF, Nielsen FC. 2004. GSK-3beta reduces cAMP-induced cholecystokinin gene expression by inhibiting CREB binding. Neuroreport 15:841-845.
16. 2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation. Neuron 3:59-70.
17. Hardie DG, Carling D. 1997. The AMP-activated protein kinase - Fuel gauge of the mammalian cell? Eur J Biochem 246:259-273.
18. 2+-independent activities and kinetic parameters. J Biol Chem 262:8051-8055.
19. Hers I, Tavare JM, Denton RM. 1999. The protein kinase C inhibitors bisindolylmaleimide I (GF 109203x) and IX (Ro 31-8220) are potent inhibitors of glycogen synthase kinase-3 activity. FEBS Lett 460:433-436.
20. Hong SP, Leiper FC, Woods A, Carling D, Carlson M. 2003. Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc Natl Acad Sci USA 100:8839-8843.
21. Horike N, Takemori H, Katoh Y, Doi J, Min L, Asano T, Sun XJ, Yamamoto H, Kasayama S, Muraoka M, Nonaka Y, Okamoto M. 2003. Adipose-specific expression, phosphorylation of Ser794 in insulin receptor substrate-1, and activation in diabetic animals of salt-inducible kinase-2. J Biol Chem 278:18440-18447.
22. Johnson LN, Noble ME, Owen DJ. 1996. Active and inactive protein kinases: Structural basis for regulation. Cell 85:149-158.
23. Katoh Y, Takemori H, Min L, Muraoka M, Doi J, Horike N, Okamoto M. 2004. Salt-inducible kinase-1 represses cAMP response element-binding protein activity both in the nucleus and in the cytoplasm. Eur J Biochem 271:4307-4319.
24. Katoh Y, Takemori H, Lin XZ, Tamura M, Muraoka M, Satoh T, Tsuchiya Y, Min L, Doi J, Miyauchi A, Witters LA, Nakamura H, Okamoto M. 2006. Silencing the constitutive active transcription factor CREB by the LKB1-SIK signaling cascade. FEBS J 273:2730-2748.
25. Koivisto L, Alavian K, Hakkinen L, Pelech S, McCulloch CA, Larjava H. 2003. Glycogen synthase kinase-3 regulates formation of long lamellipodia in human keratinocytes. J Cell Sci 116:3749-3760.
26. Koo SH, Flechner L, Qi L, Zhang X, Screaton RA, Jeffries S, Hedrick S, Xu W, Boussouar F, Brindle P, Takemori H, Montminy M. 2005. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 437:1109-1111.
27. Leclerc S, Garnier M, Hoessel R, Marko' D, Bibb JA, Snyder GL, Greengard P, Biernat J, Wu YZ, Mandelkow EM, Eisenbrand G, Meijer L. 2001. Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J Biol Chem 276: 251-2560.
28. Lin X, Takemori H, Katoh Y, Doi J, Horike N, Makino A, Nonaka Y, Okamoto M. 2001. Salt-inducible kinase is involved in the ACTH/cAMP-dependent protein kinase signaling in Y1 mouse adrenocortical tumor cells. Mol Endocrinol 15:1264-1276.
29. Lin-Marq N, Borel C, Antonarakis SE. 2005. Peutz-Jeghers LKB1 mutants fail to activate GSK-3beta, preventing it from inhibiting Wnt signaling. Mol Genet Genomics 273:184-196.
30. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Makela TP, Hardie DG, Alessi DR. 2004. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/ PAR-1. EMBO J 23:833-843.
31. Nayak V, Zhao K, Wyce A, Schwartz MF, Lo WS, Berger SL, Marmorstein R. 2006. Structure and dimerization of the kinase domain from yeast Snf1, a member of the Snf1/AMPK protein family. Structure 14:477-485.
32. Ossipova O, Bardeesy N, DePinho RA, Green JB. 2003. LKB1 (XEEK1) regulates Wnt signalling in vertebrate development. Nat Cell Biol 5:889-894.
33. Panneerselvam S, Marx A, Mandelkow EM, Mandelkow E. 2006. Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure 14:173-183.
34. Polychronopoulos P, Magiatis P, Skaltsounis AL, Myrianthopoulos V, Mikros E, Tarricone A, Musacchio A, Roe SM, Pearl L, Leost M, Greengard P, Meijer L. 2004. Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases. J Med Chem 47:935-946.
35. Rivers A, Gietzen KF, Vielhaber E, Virshup DM. 1998. Regulation of casein kinase I epsilon and casein kinase I delta by an in vivo futile phosphorylation cycle. J Biol Chem 273:15980-15984.
36. Sato S, Fujita N, Tsuruo T. 2002. Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J Biol Chem 277:39360-39367.
37. Schwede T, Kopp J, Guex N, Peitsch MC. 2003. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 31:3381-3385.
38. Screaton RA, Conkright MD, Katoh Y, Best JL, Canettieri G, Jeffries S, Guzman E, Niessen S, Yates JR III, Takemori H, Okamoto M, Montminy M. 2004. The CREB coactivator TORC2 functions as a calcium-and cAMP-sensitive coincidence detector. Cell 119:61-74.
39. Shankar SL, Krupski M, Parashar B, Okwuaka C, O'Guin K, Mani S, Shafit-Zagardo B. 2004. UCN-01 alters phosphorylation of Akt and GSK3beta and induces apoptosis in six independent human neuroblastoma cell lines. J Neurochem 90:702-711.
40. Spicer J, Rayter S, Young N, Elliott R, Ashworth A, Smith D. 2003. Regulation of the Wnt signalling component PAR1A by the Peutz-Jeghers syndrome kinase L KB1. Oncogene 22:4752-4756.
41. Takemori H, Okamoto M. 2008. Regulation of CREB-mediated gene expression by salt inducible kinase. J Steroid Biochem Mol Biol 108:287-291.
42. Timm T, Li XY, Biernat J, Jiao J, Mandelkow E, Vandekerckhove J, Mandelkow EM. 2003. MARKK, a Ste20-like kinase, activates the polarity-inducing kinase MARK/PAR-1. EMBO J 22:5090-5101.
43. Toker A. 1998. Signaling through protein kinase C. Front Biosci 3:D1134-D1147.
44. Tullai JW, Chen J, Schaffer ME, Kamenetsky E, Kasif S, Cooper GM. 2007. Glycogen synthase kinase-3 represses cyclic AMP response element-binding protein (CREB)-targeted immediate early genes in quiescent cells. J Biol Chem 282:9482-9491.
45. Tzivion G, Avruch J. 2002. 14-3-3proteins: Active cofactors in cellular regulation by serine/threonine phosphorylation. J Biol Chem 277:3061-3064.
46. van der Geer P, Hunter T. 1994. Phosphopeptide mapping and phosphoamino acid analysis by electrophoresis and chromatography on thin-layer cellulose plates. Electrophoresis 15:544-554.
47. van der Linden AM, Nolan KM, Sengupta P. 2007. KIN-29 SIK regulates chemoreceptor gene expression via an MEF2 transcription factor and a class II HDAC. EMBO J 26:358-370.
48. Wang Z, Takemori H, Haider SK, Nonaka Y, Okamoto M. 1999. Cloning of a novel kinase (SIK) of the SNF1/AMPK family from high salt diet-treated rat adrenal. FEBS Lett 453:135-139.
49. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D. 2003. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13: 2004-2008.