SRF phosphorylation by glycogen synthase kinase-3 promotes axon growth in hippocampal neurons

Journal of Neuroscience

Volumn 34, Issue 11, 2014, Pages 4027-4042

  Li, Cong L ^a   Sathyamurthy, Aruna ^a   Oldenborg, Anna ^a   Tank, Dharmesh ^a   Ramanan, Narendrakumar ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Axon growth; Filopodia; GSK 3; Neurite outgrowth; Serum response factor

Indexed keywords

ACTIN BINDING PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; LAMININ; MEGAKARYOBLASTIC LEUKEMIA 1 PROTEIN; MEGAKARYOBLASTIC LEUKEMIA 2 PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; POLY DEXTRO LYSINE; PROTEIN VP16; SERINE; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELK 1; UNCLASSIFIED DRUG; VINCULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ENZYME INHIBITION; GENE MUTATION; GENE SILENCING; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LUCIFERASE ASSAY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PHOSPHORYLATION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; STAINING;

AXON GROWTH; FILOPODIA; GSK-3; NEURITE OUTGROWTH; SERUM RESPONSE FACTOR;

ANIMALS; AXONS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, TRANSGENIC; NESTIN; NEURONS; PHOSPHORYLATION; PSEUDOPODIA; SERINE; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VINCULIN;

EID: 84896754223     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4677-12.2014     Document Type: Article

References (73)

1. Alabed YZ, Pool M, Ong Tone S, Sutherland C, Fournier AE (2010) GSK-3 beta regulates myelin-dependent axon outgrowth inhibition through CRMP4. J Neurosci 30:5635-5643. CrossRef Medline
2. Badiani P, Corbella P, Kioussis D, Marvel J, Weston K (1994) Dominant interfering alleles define a role for c-Myb in T-cell development. Genes Dev 8:770-782. CrossRef Medline
3. Bechard M, Dalton S (2009) Subcellular localization of glycogen synthase kinase 3beta controls embryonic stem cell self-renewal. Mol Cell Biol 29:2092-2104. CrossRef Medline
4. Bhat RV, Budd Haeberlein SL, Avila J (2004) Glycogen synthase kinase 3: a drug target for CNS therapies. J Neurochem 89:1313-1317. CrossRef Medline
5. Bijur GN, Jope RS (2003) Glycogen synthase kinase-3 beta is highly activated in nuclei and mitochondria. Neuroreport 14:2415-2419. CrossRef Medline
6. Caspi M, Zilberberg A, Eldar-Finkelman H, Rosin-Arbesfeld R (2008) Nuclear GSK-3beta inhibits the canonical Wnt signalling pathway in a beta-catenin phosphorylation-independent manner. Oncogene 27:3546-3555. CrossRef Medline
7. Cen B, Selvaraj A, Burgess RC, Hitzler JK, Ma Z, Morris SW, Prywes R (2003) Megakaryoblastic leukemia 1, a potent transcriptional coactivator for serum response factor (SRF), is required for serum induction of SRF target genes. Mol Cell Biol 23:6597-6608. CrossRef Medline
8. Cen B, Selvaraj A, Prywes R (2004) Myocardin/MKL family of SRF coactivators: key regulators of immediate early and muscle specific gene expression. J Cell Biochem 93:74-82. CrossRef Medline
9. Cesari F, Brecht S, Vintersten K, Vuong LG, Hofmann M, Klingel K, Schnorr JJ, Arsenian S, Schild H, Herdegen T, Wiebel FF, Nordheim A (2004) Mice deficient for the ets transcription factor elk-1 show normal immune responses and mildly impaired neuronal gene activation. Mol Cell Biol 24:294-305. CrossRef Medline
10. Cho JH, Johnson GV (2003) Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites: differential impact on microtubule binding. J Biol Chem 278:187-193. CrossRef Medline
11. Cohen P, Frame S (2001) The renaissance of GSK-3. Nat Rev Mol Cell Biol 2:769-776. CrossRef Medline
12. Cohen P, Goedert M (2004) GSK-3 inhibitors: development and therapeutic potential. Nat Rev Drug Discov 3:479-487. CrossRef Medline
13. Contestabile A, Bonanomi D, Burgaya F, Girault JA, Valtorta F (2003) Localization of focal adhesion kinase isoforms in cells of the central nervous system. Int J Dev Neurosci 21:83-93. CrossRef Medline
14. Cooper SJ, Trinklein ND, Nguyen L, Myers RM (2007) Serum response factor binding sites differ in three human cell types. Genome Res 17:136-144. CrossRef Medline
15. Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17:267-310. CrossRef Medline
16. Dehmelt L, Halpain S (2004) Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol 58:18-33. CrossRef Medline
17. de Lima AD, Merten MD, Voigt T (1997) Neuritic differentiation and synaptogenesis in serum-free neuronal cultures of the rat cerebral cortex. J Comp Neurol 382:230-246. CrossRef Medline
18. Dent EW, Kwiatkowski AV, Mebane LM, Philippar U, Barzik M, Rubinson DA, Gupton S, Van Veen JE, Furman C, Zhang J, Alberts AS, Mori S, Gertler FB (2007) Filopodia are required for cortical neurite initiation. Nat Cell Biol 9:1347-1359. CrossRef Medline
19. Doble BW, Woodgett JR (2003) GSK-3: tricks of the trade for a multitasking kinase. J Cell Sci 116:1175-1186. CrossRef Medline
20. Etkin A, Alarcón JM, Weisberg SP, Touzani K, Huang YY, Nordheim A, Kandel ER (2006) A role in learning for SRF: deletion in the adult forebrain disruptsLTDand the formation of an immediate memory of a novel context. Neuron 50:127-143. CrossRef Medline
21. Frame S, Cohen P, Biondi RM (2001) A common phosphate binding site explains the unique substrate specificity of GSK-3 and its inactivation by phosphorylation. Mol Cell 7:1321-1327. CrossRef Medline
22. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, Filbin MT (2004) Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44:609-621. CrossRef Medline
23. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, Debanne D, Dargent B (2003) A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 300:2091-2094. CrossRef Medline
24. Garrido JJ, Simón D, Varea O, Wandosell F (2007) GSK-3 alpha and GSK-3 beta are necessary for axon formation. FEBS Lett 581:1579-1586. CrossRef Medline
25. Gineitis D, Treisman R (2001) Differential usage of signal transduction pathways defines two types of serum response factor target gene. J Biol Chem 276:24531-24539. CrossRef Medline
26. Gonzalez-Billault C, Jimenez-Mateos EM, Caceres A, Diaz-Nido J, Wandosell F, Avila J (2004) Microtubule-associated protein 1B function during normal development, regeneration, and pathological conditions in the nervous system. J Neurobiol 58:48-59. CrossRef Medline
27. Goold RG, Gordon-Weeks PR (2005) TheMAPkinase pathway is upstream of the activation of GSK-3beta that enables it to phosphorylate MAP1B and contributes to the stimulation of axon growth. Mol Cell Neurosci 28:524-534. CrossRef Medline
28. Goold RG, Owen R, Gordon-Weeks PR (1999) Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J Cell Sci 112:3373-3384. Medline
29. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, SchwartzMA (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466:263-266. CrossRef Medline
30. He X, Saint-Jeannet JP, Woodgett JR, Varmus HE, Dawid IB (1995) Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos. Nature 374:617-622. CrossRef Medline
31. Humphries JD, Wang P, Streuli C, Geiger B, Humphries MJ, Ballestrem C (2007) Vinculin controls focal adhesion formation by direct interactions with talin and actin. J Cell Biol 179:1043-1057. CrossRef Medline
32. Hur EM, Saijilafu, Lee BD, Kim SJ, Xu WL, Zhou FQ (2011) GSK-3 controls axon growth via CLASP-mediated regulation of growth cone microtubules. Genes Dev 25:1968-1981. CrossRef Medline
33. Iyer D, Chang D, Marx J, Wei L, Olson EN, Parmacek MS, Balasubramanyam A, Schwartz RJ (2006) Serum response factor MADS box serine-162 phosphorylation switches proliferation and myogenic gene programs. Proc Natl Acad Sci U S A 103:4516-4521. CrossRef Medline
34. Jaynes JB, O'Farrell PH (1991) Active repression of transcription by the engrailed homeodomain protein. EMBO J 10:1427-1433. Medline
35. Kang T, Wei Y, Honaker Y, Yamaguchi H, Appella E, Hung MC, Piwnica-Worms H (2008) GSK-3 beta targets Cdc25A for ubiquitin-mediated proteolysis, and GSK-3 beta inactivation correlates with Cdc25A overproduction in human cancers. Cancer Cell 13:36-47. CrossRef Medline
36. Kemp PR, Metcalfe JC (2000) Four isoforms of serum response factor that increase or inhibit smooth-muscle-specific promoter activity. Biochem J 345:445-451. CrossRef Medline
37. Kim WY, Zhou FQ, Zhou J, Yokota Y, Wang YM, Yoshimura T, Kaibuchi K, Woodgett JR, Anton ES, Snider WD (2006) Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52:981-996. CrossRef Medline
38. Kim WY, Wang X, Wu Y, Doble BW, Patel S, Woodgett JR, Snider WD (2009) GSK-3 is a master regulator of neural progenitor homeostasis. Nat Neurosci 12:1390-1397. CrossRef Medline
39. Knöll B, Kretz O, Fiedler C, Alberti S, Schütz G, Frotscher M, Nordheim A (2006) Serum response factor controls neuronal circuit assembly in the hippocampus. Nat Neurosci 9:195-204. CrossRef Medline
40. Kress GJ, Dowling MJ, Eisenman LN, Mennerick S (2010) Axonal sodium channel distribution shapes the depolarized action potential threshold of dentate granule neurons. Hippocampus 20:558-571. CrossRef Medline
41. Lonze BE, Riccio A, Cohen S, Ginty DD (2002) Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 34:371-385. CrossRef Medline
42. Lu PP, Ramanan N (2011) Serum response factor is required for cortical axon growth but is dispensable for neurogenesis and neocortical lamination. J Neurosci 31:16651-16664. CrossRef Medline
43. Meijer L, Skaltsounis AL, Magiatis P, Polychronopoulos P, Knockaert M, Leost M, Ryan XP, Vonica CA, Brivanlou A, Dajani R, Crovace C, Tarricone C, Musacchio A, Roe SM, Pearl L, Greengard P (2003) GSK-3-selective inhibitors derived from Tyrian purple indirubins. Chem Biol 10:1255-1266. CrossRef Medline
44. Miano JM (2003) Serum response factor: toggling between disparate programs of gene expression. J Mol Cell Cardiol 35:577-593. CrossRef Medline
45. Miralles F, Posern G, Zaromytidou AI, Treisman R (2003) Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113:329-342. CrossRef Medline
46. Misra RP, Rivera VM, Wang JM, Fan PD, Greenberg ME (1991) The serum response factor is extensively modified by phosphorylation following its synthesis in serum-stimulated fibroblasts. Mol Cell Biol 11:4545-4554. CrossRef Medline
47. Moiseyeva EP, Weller PA, Zhidkova NI, Corben EB, Patel B, Jasinska I, Koteliansky VE, Critchley DR (1993) Organization of the human gene encoding the cytoskeletal protein vinculin and the sequence of the vinculin promoter. J Biol Chem 268:4318-4325. Medline
48. Mokalled MH, Johnson A, Kim Y, Oh J, Olson EN (2010) Myocardinrelated transcription factors regulate the Cdk5/Pctaire1 kinase cascade to control neurite outgrowth, neuronal migration and brain development. Development 137:2365-2374. CrossRef Medline
49. Obenauer JC, Cantley LC, Yaffe MB (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31:3635-3641. CrossRef Medline
50. O' Sullivan NC, Pickering M, Di Giacomo D, Loscher JS, Murphy KJ (2010) Mkl transcription cofactors regulate structural plasticity in hippocampal neurons. Cereb Cortex 20:1915-1925. CrossRef Medline
51. Owen R, Gordon-Weeks PR (2003) Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol Cell Neurosci 23:626-637. CrossRef Medline
52. Pellegrini L, Tan S, Richmond TJ (1995) Structure of serum response factor core bound to DNA. Nature 376:490-498. CrossRef Medline
53. Polleux F, Snider W (2010) Initiating and growing an axon. Cold Spring Harb Perspect Biol 2:a001925. CrossRef Medline
54. Ramanan N, Shen Y, Sarsfield S, Lemberger T, Schütz G, Linden DJ, GintyDD (2005) SRF mediates activity-induced gene expression and synaptic plasticity but not neuronal viability. Nat Neurosci 8:759-767. CrossRef Medline
55. Rivera VM, Miranti CK, Misra RP, Ginty DD, Chen RH, Blenis J, Greenberg ME (1993) A growth factor-induced kinase phosphorylates the serum response factor at a site that regulates its DNA-binding activity. Mol Cell Biol 13:6260-6273. CrossRef Medline
56. Schratt G, Philippar U, Berger J, Schwarz H, Heidenreich O, Nordheim A (2002) Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. J Cell Biol 156:737-750. CrossRef Medline
57. Selvaraj A, Prywes R (2003) Megakaryoblastic leukemia-1/2, a transcriptional co-activator of serum response factor, is required for skeletal myogenic differentiation. J Biol Chem 278:41977-41987. CrossRef Medline
58. Sharrocks AD (2001) The ETS-domain transcription factor family. Nat Rev Mol Cell Biol 2:827-837. CrossRef Medline
59. Shiota J, Ishikawa M, Sakagami H, Tsuda M, Baraban JM, Tabuchi A (2006) Developmental expression of the SRF co-activator MAL in brain: role in regulating dendritic morphology. J Neurochem 98:1778-1788. CrossRef Medline
60. Smith-Hicks C, Xiao B, Deng R, Ji Y, Zhao X, Shepherd JD, Posern G, Kuhl D, Huganir RL, Ginty DD, Worley PF, Linden DJ (2010) SRF binding to SRE 6.9 in the Arc promoter is essential for LTD in cultured Purkinje cells. Nat Neurosci 13:1082-1089. CrossRef Medline
61. Stern S, Debre E, Stritt C, Berger J, Posern G, Knöll B (2009) A nuclear actin function regulates neuronal motility by serum response factor-dependent gene transcription. J Neurosci 29:4512-4518. CrossRef Medline
62. Stern S, Haverkamp S, Sinske D, Tedeschi A, Naumann U, Di Giovanni S, Kochanek S, Nordheim A, Knöll B (2013) The transcription factor serum response factor stimulates axon regeneration through cytoplasmic localization and cofilin interaction. J Neurosci 33:18836-18848. CrossRef Medline
63. Stevens GR, Zhang C, Berg MM, Lambert MP, Barber K, Cantallops I, Routtenberg A, Klein WL (1996) CNS neuronal focal adhesion kinase forms clusters that co-localize with vinculin. J Neurosci Res 46:445-455. CrossRef Medline
64. Treisman R (1987) Identification and purification of a polypeptide that binds to the c-fos serum response element. EMBO J 6:2711-2717. Medline
65. Twomey C, McCarthy JV (2006) Presenilin-1 is an unprimed glycogen synthase kinase-3beta substrate. FEBS Lett 580:4015-4020. CrossRef Medline
66. Vickers ER, Sharrocks AD (2002) The use of inducible engrailed fusion proteins to study the cellular functions of eukaryotic transcription factors. Methods 26:270-280. CrossRef Medline
67. Vickers ER, Kasza A, Kurnaz IA, Seifert A, Zeef LA, O'Donnell A, Hayes A, Sharrocks AD (2004) Ternary complex factor-serum response factor complex-regulated gene activity is required for cellular proliferation and inhibition of apoptotic cell death. Mol Cell Biol 24:10340-10351. CrossRef Medline
68. Wickramasinghe SR, Alvania RS, Ramanan N, Wood JN, Mandai K, Ginty DD (2008) Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons. Neuron 58:532-545. CrossRef Medline
69. Xu W, Baribault H, Adamson ED (1998) Vinculin knockout results in heart and brain defects during embryonic development. Development 125: 327-337. Medline
70. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K (2005) GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120:137-149. CrossRef Medline
71. Zhou FQ, Snider WD (2006) Intracellular control of developmental and regenerative axon growth. Philos Trans R Soc Lond B Biol Sci 361:1575-1592. CrossRef Medline
72. Zhou FQ, Zhou J, Dedhar S, Wu YH, SniderWD (2004) NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897-912. CrossRef Medline
73. Ziegler WH, Liddington RC, Critchley DR (2006) The structure and regulation of vinculin. Trends Cell Biol 16:453-460. CrossRef Medline