Unphosphorylated MARCKS is involved in neurite initiation induced by insulin-like growth factor-I in SH-SY5Y cells

Journal of Cellular Physiology

Volumn 209, Issue 3, 2006, Pages 1029-1038

  Shiraishi, Mitsuya ^a   Tanabe, Atsuhiro ^a   Saito, Naoaki ^b   Sasaki, Yasuharu ^a  

^a KITASATO UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN; CYCLOSPORIN A; F ACTIN; MARCKS PROTEIN; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SOMATOMEDIN C; WORTMANNIN;

ARTICLE; CELL MEMBRANE; CELL STIMULATION; CONTROLLED STUDY; CYTOSKELETON; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LAMELLIPODIUM; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTINS; ANDROSTADIENES; CELL LINE, TUMOR; CELL MEMBRANE; CHROMONES; ENZYME INHIBITORS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MORPHOLINES; NEURITES; NEUROBLASTOMA; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 33750528518     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20814     Document Type: Article

References (51)

1. Albert KA, Walaas SI, Wang JK, Greengard P. 1986. Widespread occurrence of "87 kDa," a major specific substrate for protein kinase C. Proc Natl Acad Sci USA 83:2822-2826.
2. Anlar B, Sullivan KA, Feldman EL. 1999. Insulin-like growth factor-I and central nervous system development. Horm Metab Res 31:120-125.
3. Arbuzova A, Schmitz AA, Vergeres G. 2002. Cross-talk unfolded: MARCKS proteins. Biochem J 362:1-12.
4. Bito H, Furuyashiki T, Ishihara H, Shibasaki Y, Ohashi K, Mizuno K, Maekawa M, Ishizaki T, Narumiya S. 2000. A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26:431-441.
5. Calabrese B, Halpain S. 2005. Essential role for the PKC target MARCKS in maintaining dendritic spine morphology. Neuron 48:77-90.
6. Clarke PR, Siddhanti SR, Cohen P, Blackshear PJ. 1993. Okadaic acid-sensitive protein phosphatases dephosphorylate MARCKS, a major protein kinase C substrate. FEBS Lett 336:37-42.
7. Dehmelt L, Smart FM, Ozer RS, Halpain S. 2003. The role of microtubule-associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation. J Neurosci 23:9479-9490.
8. Dent EW, Gertler FB. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209-227.
9. Disatnik MH, Boutet SC, Pacio W, Chan AY, Ross LB, Lee CH, Rando TA. 2004. The bi-directional translocation of MARCKS between membrane and cytosol regulates integrin-mediated muscle cell spreading. J Cell Sci 117:4469-4479.
10. Gallant C, You JY, Sasaki Y, Grabarek Z, Morgan KG. 2005. MARCKS is a major PKC-dependent regulator of calmodulin targeting in smooth muscle. J Cell Sci 118:3595-3605.
11. 2 on phospholipid membranes by basic/aromatic regions of proteins. Biophys J 86:2188-2207.
12. Govek EE, Newey SE, Van Aelst L. 2005. The role of the Rho GTPases in neuronal development. Genes Dev 19:1-49.
13. Hartwig JH, Thelen M, Rosen A, Janmey PA, Nairn AC, Aderem A. 1992. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356:618-622.
14. Hirose M, Ishizaki T, Watanabe N, Uehata M, Kranenburg O, Moolenaar WH, Matsumura F, Maekawa M, Bito H, Narumiya S. 1998. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol 141:1625-1636.
15. Ikenoya M, Hidaka H, Hosoya T, Suzuki M, Yamamoto N, Sasaki Y. 2002. Inhibition of rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific Rho-kinase inhibitor. J Neurochem 81:9-16.
16. Ivankovic-Dikic I, Grönroos E, Blaukat A, Earth BU, Dikic I. 2000. Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat Cell Biol 2:574-581.
17. Katoh H, Aoki J, Ichikawa A, Negishi M. 1998. p160 RhoA-binding kinase ROKα induces neurite retraction. J Biol Chem 273:2489-2492.
18. Kim J, Shishido T, Jiang X, Aderem A, McLaughlin S. 1994. Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles. J Biol Chem 269:28214-28219.
19. Kim B, Leventhal PS, Saltiel AR, Feldman EL. 1997. Insulin-like growth factor-I-mediated neurite outgrowth in vitro requires mitogen-activated protein kinase activation. J Biol Chem 272:21268-21273.
20. Kim B, Cheng HL, Margolis B, Feldman EL. 1998. Insulin receptor substrate 2 and Shc play different roles in insulin-like growth factor I signaling. J Biol Chem 273:34543-34550.
21. Kim B, van Golen CM, Feldman EL. 2004. Insulin-like growth factor-I signaling in human neuroblastoma cells. Oncogene 23:130-141.
22. Kimpinski K, Mearow K. 2001. Neurite growth promotion by nerve growth factor and insulin-like growth factor-1 in cultured adult sensory neurons: Role of phosphoinositide 3-kinase and mitogen activated protein kinase. J Neurosci Res 63:486-499.
23. Kurihara S, Hakuno F, Takahashi S. 2000. Insulin-like growth factor-I-dependent signal transduction pathways leading to the induction of cell growth and differentiation of human neuroblastoma cell line SH-SY5Y: The roles of MAP kinase pathway and PI 3-kinase pathway. Endocr J 47:739-751.
24. 2 at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149:1455-1472.
25. Li G, O'Connor KL, Greeley GH Jr, Blackshear PJ, Townsend CM Jr, Evers BM. 2005. Myristoylated alanine-rich C kinase substrate-mediated neurotensin release via protein kinase C-δ downstream of the Rho/ROK pathway. J Biol Chem 280:8351-8357.
26. McLaughlin S, Aderem A. 1995. The myristoyl-electrostatic switch: A modulator of reversible protein-membrane interactions. Trends Biochem Sci 20:272-276.
27. McLaughlin S, Murray D. 2005. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438:605-611.
28. McNamara RK, Lenox RH. 1997. Comparative distribution of myristoylated alanine-rich C kinase substrate (MARCKS) and F1/GAP-43 gene expression in the adult rat brain. J Comp Neurol 379:48-71.
29. Meyer G, Feldman EL. 2002. Signaling mechanisms that regulate actin-based motility processes in the nervous system. J Neurochem 83:490-503.
30. Meyer GE, Shelden E, Kim B, Feldman EL. 2001. Insulin-like growth factor I stimulates motility in human neuroblastoma cells. Oncogene 20:7542-7550.
31. Meyer G, Kim B, van Golen C, Feldman EL. 2005. Cofilin activity during insulin-like growth factor I-stimulated neuroblastoma cell motility. Cell Mol Life Sci 62:461-470.
32. Nagumo H, Ikenoya M, Sakurada K, Furuya K, Ikuhara T, Hiraoka H, Sasaki Y. 2001. Rho-associated kinase phosphorylates MARCKS in human neuronal cells. Biochem Biophys Res Commun 280:605-609.
33. Nimnual AS, Taylor LJ, Bar-Sagi D. 2003. Redox-dependent downregulation of Rho by Rac. Nat Cell Biol 5:236-241.
34. Nusser N, Gosmanova E, Zheng Y, Tigyi G. 2002. Nerve growth factor signals through TrkA, phosphatidylinositol 3-kinase, and Rac1 to inactivate RhoA during the initiation of neuronal differentiation of PC12 cells. J Biol Chem 277:35840-35846.
35. Ohmori S, Sakai N, Shirai Y, Yamamoto H, Miyamoto E, Shimizu N, Saito N. 2000. Importance of protein kinase C targeting for the phosphorylation of its substrate, myristoylated alanine-rich C-kinase substrate. J Biol Chem 275:26449-26457.
36. Sander EE, ten Klooster JP, van Delft S, van der Kammen RA, Collard JG. 1999. Rac downregulates Rho activity: Reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J Cell Biol 147:1009-1022.
37. Sebök A, Nusser N, Debreceni B, Guo Z, Santas MF, Szeberenyi J, Tigyi G. 1999. Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J Neurochem 73:949-960.
38. Seki K, Chen HC, Huang KP. 1995. Dephosphorylation of protein kinase C substrates, neurogranin, neuromodulin, and MARCKS, by calcineurin and protein phosphatases 1 and 2A. Arch Biochem Biophys 316:673-679.
39. Stumpo DJ, Bock CB, Turtle JS, Blackshear PJ. 1995. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc Natl Acad Sci USA 92:944-948.
40. Subramaniam S, Shahani N, Strelau J, Laliberté C, Brandt R, Kaplan D, Unsicker K. 2005. Insulin-like growth factor 1 inhibits extracellular signal-regulated kinase to promote neuronal survival via the phosphatidylinositol 3-kinase/protein kinase A/c-Raf pathway. J Neurosci 25:2838-2852.
41. Swierczynski SL, Blackshear PJ. 1996. Myristoylation-dependent and electrostatic interactions exert independent effects on the membrane association of the myristoylated alanine-rich protein kinase C substrate protein in intact cells. J Biol Chem 271:23424-23430.
42. Takai A, Sasaki K, Nagai H, Mieskes G, Isobe M, Isono K, Yasumoto T. 1995. Inhibition of specific binding of okadaic acid to protein phosphatase 2A by microcystin-LR, calyculin-A and tautomycin: Method of analysis of interactions of tight-binding ligands with target protein. Biochem J 306:657-665.
43. Tanabe A, Kamisuki Y, Hidaka H, Suzuki M, Negishi M, Takuwa Y. 2006. PKC phosphorylates MARCKS Ser159 not only directly but also through RhoA/ROCK. Biochem Biophys Res Commun 345:156-161.
44. Tatsumi S, Mabuchi T, Katano T, Matsumura S, Abe T, Hidaka H, Suzuki M, Sasaki Y, Minami T, Ito S. 2005. Involvement of Rho-kinase in inflammatory and neuropathic pain through phosphorylation of myristoylated alanine-rich C-kinase substrate (MARCKS). Neuroscience 131:491-498.
45. Thelen M, Rosen A, Nairn AC, Aderem A. 1991. Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane. Nature 351:320-322.
46. Wang J, Arbuzova A, Hangyás-Mihályné G, McLaughlin S. 2001. The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate. J Biol Chem 276:5012-5019.
47. Wohnsland F, Schmitz AA, Steinmetz MO, Aebi U, Vergères G. 2000. Interaction between actin and the effector peptide of MARCKS-related protein. Identification of functional amino acid segments. J Biol Chem 275:20873-20879.
48. Yamada T, Sakisaka T, Hisata S, Baba T, Takai Y. 2005. RA-RhoGAP, Rap-activated Rho GTPase-activating protein implicated in neurite outgrowth through Rho. J Biol Chem 280:33026-33034.
49. Yamaguchi Y, Katoh H, Yasui H, Mori K, Negishi M. 2001. RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J Biol Chem 276:18977-18983.
50. Yarmola EG, Edison AS, Lenox RH, Bubb MR. 2001. Actin filament cross-linking by MARCKS: Characterization of two actin-binding sites within the phosphorylation site domain. J Biol Chem 276:22351-22358.
51. Yin HL, Janmey PA. 2003. Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761-789.