Neuronal deletion of GSK3β increases microtubule speed in the growth cone and enhances axon regeneration via CRMP-2 and independently of MAP1B and CLASP2

BMC Biology

Volumn 12, Issue 1, 2014, Pages

  Liz, Márcia A ^a   Mar, Fernando M ^a,b   Santos, Telma E ^a   Pimentel, Helena I ^a   Marques, Ana M ^a   Morgado, Marlene M ^a   Vieira, Sílvia ^a   Sousa, Vera F ^a,b   Pemble, Hayley ^c   Wittmann, Torsten ^c   Sutherland, Calum ^d   Woodgett, James R ^e   Sousa, Mónica M ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Axon regeneration; CRMP 2; Growth cone; GSK3 ; Microtubule

Indexed keywords

CLASP2 PROTEIN, MOUSE; COLLAPSIN RESPONSE MEDIATOR PROTEIN-2; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE-ASSOCIATED PROTEIN 1B; NERVE PROTEIN; SIGNAL PEPTIDE;

ANIMAL; C57BL MOUSE; FEMALE; GENETICS; GROWTH CONE; KNOCKOUT MOUSE; MALE; METABOLISM; MICROTUBULE; MOUSE; NERVE FIBER; PHOSPHORYLATION; PHYSIOLOGY; RAT; REGENERATION; WISTAR RAT;

ANIMALS; AXONS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; GROWTH CONES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NERVE TISSUE PROTEINS; PHOSPHORYLATION; RATS; RATS, WISTAR; REGENERATION;

EID: 84927941057     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-12-47     Document Type: Article

References (64)

1. Neumann S, Woolf CJ: Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 1999, 23:83-91. 10.1016/S0896-6273(00)80755-2
2. Erturk A, Hellal F, Enes J, Bradke F: Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration. J Neurosci 2007, 27:9169-9180. 10.1523/JNEUROSCI.0612-07.2007.
3. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, Kapitein LC, Strikis D, Lemmon V, Bixby J, Hoogenraad CC, Bradke F: Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 2011, 331:928-931. 10.1126/science.1201148.
4. Rivieccio MA, Brochier C, Willis DE, Walker BA, D'Annibale MA, McLaughlin K, Siddiq A, Kozikowski AP, Jaffrey SR, Twiss JL, Ratan RR, Langley B: HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci USA 2009, 106:19599-19604. 10.1073/pnas.0907935106.
5. Cho Y, Cavalli V: HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J 2012, 31:3063-3078. 10.1038/emboj.2012.160.
6. Liu CM, Hur EM, Zhou FQ: Coordinating gene expression and axon assembly to control axon growth: potential role of GSK3 signaling. Front Mol Neurosci 2012, 5:3.
7. Hughes K, Nikolakaki E, Plyte SE, Totty NF, Woodgett JR: Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J 1993, 12:803-808.
8. Cole A, Frame S, Cohen P: Further evidence that the tyrosine phosphorylation of glycogen synthase kinase-3 (GSK3) in mammalian cells is an autophosphorylation event. Biochem J 2004, 377:249-255. 10.1042/BJ20031259.
9. Hartigan JA, Xiong WC, Johnson GV: Glycogen synthase kinase 3beta is tyrosine phosphorylated by PYK2. Biochem Biophys Res Commun 2001, 284:485-489. 10.1006/bbrc.2001.4986.
10. Lesort M, Jope RS, Johnson GV: Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J Neurochem 1999, 72:576-584. 10.1046/j.1471-4159.1999.0720576.x.
11. Simon D, Benitez MJ, Gimenez-Cassina A, Garrido JJ, Bhat RV, Diaz-Nido J, Wandosell F: Pharmacological inhibition of GSK-3 is not strictly correlated with a decrease in tyrosine phosphorylation of residues 216/279. J Neurosci Res 2008, 86:668-674. 10.1002/jnr.21523.
12. Doble BW, Woodgett JR: GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003, 116:1175-1186. 10.1242/jcs.00384.
13. Zhou FQ, Snider WD: Cell biology. GSK-3beta and microtubule assembly in axons. Science 2005, 308:211-214. 10.1126/science.1110301.
14. Dill J, Wang H, Zhou F, Li S: Inactivation of glycogen synthase kinase 3 promotes axonal growth and recovery in the CNS. J Neurosci 2008, 28:8914-8928. 10.1523/JNEUROSCI.1178-08.2008.
15. Alabed YZ, Pool M, Ong Tone S, Sutherland C, Fournier AE: GSK3 beta regulates myelin-dependent axon outgrowth inhibition through CRMP4. J Neurosci 2010, 30:5635-5643. 10.1523/JNEUROSCI.6154-09.2010.
16. McManus EJ, Sakamoto K, Armit LJ, Ronaldson L, Shpiro N, Marquez R, Alessi DR: Role that phosphorylation of GSK3 plays in insulin and Wnt signalling defined by knockin analysis. EMBO J 2005, 24:1571-1583. 10.1038/sj.emboj.7600633.
17. Hoeflich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR: Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000, 406:86-90. 10.1038/35017574.
18. Smith DS, Skene JH: A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J Neurosci 1997, 17:646-658.
19. Cao Z, Gao Y, Bryson JB, Hou J, Chaudhry N, Siddiq M, Martinez J, Spencer T, Carmel J, Hart RB, Filbin MT: The cytokine interleukin-6 is sufficient but not necessary to mimic the peripheral conditioning lesion effect on axonal growth. J Neurosci 2006, 26:5565-5573. 10.1523/JNEUROSCI.0815-06.2006.
20. Tuszynski MH, Steward O: Concepts and methods for the study of axonal regeneration in the CNS. Neuron 2012, 74:777-791. 10.1016/j.neuron.2012.05.006.
21. Renault-Mihara F, Katoh H, Ikegami T, Iwanami A, Mukaino M, Yasuda A, Nori S, Mabuchi Y, Tada H, Shibata S, Saito K, Matsushita M, Kaibuchi K, Okada S, Toyama Y, Nakamura M, Okano H: Beneficial compaction of spinal cord lesion by migrating astrocytes through glycogen synthase kinase-3 inhibition. EMBO Mol Med 2011, 3:682-696. 10.1002/emmm.201100179.
22. Patel S, Doble BW, MacAulay K, Sinclair EM, Drucker DJ, Woodgett JR: Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol Cell Biol 2008, 28:6314-6328. 10.1128/MCB.00763-08.
23. Young P, Qiu L, Wang D, Zhao S, Gross J, Feng G: Single-neuron labeling with inducible Cre-mediated knockout in transgenic mice. Nat Neurosci 2008, 11:721-728. 10.1038/nn.2118.
24. Scales TM, Lin S, Kraus M, Goold RG, Gordon-Weeks PR: Nonprimed and DYRK1A-primed GSK3 beta-phosphorylation sites on MAP1B regulate microtubule dynamics in growing axons. J Cell Sci 2009, 122:2424-2435. 10.1242/jcs.040162.
25. Trivedi N, Marsh P, Goold RG, Wood-Kaczmar A, Gordon-Weeks PR: Glycogen synthase kinase-3beta phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons. J Cell Sci 2005, 118:993-1005. 10.1242/jcs.01697.
26. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, Vermeulen W, Burgering BM, De Zeeuw CI, Grosveld F, Galjart N: Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001, 104:923-935. 10.1016/S0092-8674(01)00288-4.
27. Kumar P, Lyle KS, Gierke S, Matov A, Danuser G, Wittmann T: GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J Cell Biol 2009, 184:895-908. 10.1083/jcb.200901042.
28. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K: GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 2005, 120:137-149. 10.1016/j.cell.2004.11.012.
29. Sun G, Li Z, Wang X, Tang W, Wei Y: Modulation of MAPK and Akt signaling pathways in proximal segment of injured sciatic nerves. Neurosci Lett 2013, 534:205-210.
30. Saijilafu , Hur EM, Liu CM, Jiao Z, Xu WL, Zhou FQ: PI3K-GSK3 signalling regulates mammalian axon regeneration by inducing the expression of Smad1. Nat Commun 2013, 4:2690.
31. Seira O, Del Rio JA: Glycogen synthase kinase 3 beta (GSK3beta) at the tip of neuronal development and regeneration. Mol Neurobiol 2014, 49:931-944. 10.1007/s12035-013-8571-y.
32. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD: NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 2004, 42:897-912. 10.1016/j.neuron.2004.05.011.
33. Jiang H, Guo W, Liang X, Rao Y: Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 2005, 120:123-135.
34. Jones DM, Tucker BA, Rahimtula M, Mearow KM: The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J Neurochem 2003, 86:1116-1128. 10.1046/j.1471-4159.2003.01925.x.
35. Garrido JJ, Simon D, Varea O, Wandosell F: GSK3 alpha and GSK3 beta are necessary for axon formation. FEBS Lett 2007, 581:1579-1586. 10.1016/j.febslet.2007.03.018.
36. Wang T, Wu X, Yin C, Klebe D, Zhang JH, Qin X: CRMP-2 is involved in axon growth inhibition induced by RGMa in vitro and in vivo. Mol Neurobiol 2013, 47:903-913. 10.1007/s12035-012-8385-3.
37. Sanchez S, Sayas CL, Lim F, Diaz-Nido J, Avila J, Wandosell F: The inhibition of phosphatidylinositol-3-kinase induces neurite retraction and activates GSK3. J Neurochem 2001, 78:468-481. 10.1046/j.1471-4159.2001.00453.x.
38. Farghaian H, Turnley AM, Sutherland C, Cole AR: Bioinformatic prediction and confirmation of beta-adducin as a novel substrate of glycogen synthase kinase 3. J Biol Chem 2011, 286:25274-25283. 10.1074/jbc.M111.251629.
39. Cole AR, Knebel A, Morrice NA, Robertson LA, Irving AJ, Connolly CN, Sutherland C: GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 2004, 279:50176-50180. 10.1074/jbc.C400412200.
40. Naska S, Park KJ, Hannigan GE, Dedhar S, Miller FD, Kaplan DR: An essential role for the integrin-linked kinase-glycogen synthase kinase-3 beta pathway during dendrite initiation and growth. J Neurosci 2006, 26:13344-13356. 10.1523/JNEUROSCI.4462-06.2006.
41. Owen R, Gordon-Weeks PR: Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol Cell Neurosci 2003, 23:626-637. 10.1016/S1044-7431(03)00095-2.
42. Kim WY, Zhou FQ, Zhou J, Yokota Y, Wang YM, Yoshimura T, Kaibuchi K, Woodgett JR, Anton ES, Snider WD: Essential roles for GSK-3 s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 2006, 52:981-996. 10.1016/j.neuron.2006.10.031.
43. Hur EM, Zhou FQ: GSK3 signalling in neural development. Nat Rev Neurosci 2010, 11:539-551.
44. Hur EM, Saijilafu , Lee BD, Kim SJ, Xu WL, Zhou FQ: GSK3 controls axon growth via CLASP-mediated regulation of growth cone microtubules. Genes Dev 2011, 25:1968-1981. 10.1101/gad.17015911.
45. Soares S, von Boxberg Y, Lombard MC, Ravaille-Veron M, Fischer I, Eyer J, Nothias F: Phosphorylated MAP1B is induced in central sprouting of primary afferents in response to peripheral injury but not in response to rhizotomy. Eur J Neurosci 2002, 16:593-606. 10.1046/j.1460-9568.2002.02126.x.
46. Tortosa E, Galjart N, Avila J, Sayas CL: MAP1B regulates microtubule dynamics by sequestering EB1/3 in the cytosol of developing neuronal cells. EMBO J 2013, 32:1293-1306. 10.1038/emboj.2013.76.
47. Bouquet C, Soares S, von Boxberg Y, Ravaille-Veron M, Propst F, Nothias F: Microtubule-associated protein 1B controls directionality of growth cone migration and axonal branching in regeneration of adult dorsal root ganglia neurons. J Neurosci 2004, 24:7204-7213. 10.1523/JNEUROSCI.2254-04.2004.
48. Arimura N, Inagaki N, Chihara K, Menager C, Nakamura N, Amano M, Iwamatsu A, Goshima Y, Kaibuchi K: Phosphorylation of collapsin response mediator protein-2 by Rho-kinase. Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem 2000, 275:23973-23980. 10.1074/jbc.M001032200.
49. Mimura F, Yamagishi S, Arimura N, Fujitani M, Kubo T, Kaibuchi K, Yamashita T: Myelin-associated glycoprotein inhibits microtubule assembly by a Rho-kinase-dependent mechanism. J Biol Chem 2006, 281:15970-15979. 10.1074/jbc.M510934200.
50. Zhu LQ, Zheng HY, Peng CX, Liu D, Li HL, Wang Q, Wang JZ: Protein phosphatase 2A facilitates axonogenesis by dephosphorylating CRMP2. J Neurosci 2010, 30:3839-3848. 10.1523/JNEUROSCI.5174-09.2010.
51. Khanna R, Wilson SM, Brittain JM, Weimer J, Sultana R, Butterfield A, Hensley K: Opening Pandora's jar: a primer on the putative roles of CRMP2 in a panoply of neurodegenerative, sensory and motor neuron, and central disorders. Future Neurol 2012, 7:749-771. 10.2217/fnl.12.68.
52. Hilton GD, Ndubuizu AN, McCarthy MM: Neuroprotective effects of estradiol in newborn female rat hippocampus. Brain Res Dev Brain Res 2004, 150:191-198. 10.1016/j.devbrainres.2004.03.006.
53. Wakade C, Khan MM, De Sevilla LM, Zhang QG, Mahesh VB, Brann DW: Tamoxifen neuroprotection in cerebral ischemia involves attenuation of kinase activation and superoxide production and potentiation of mitochondrial superoxide dismutase. Endocrinology 2008, 149:367-379. 10.1210/en.2007-0899.
54. Pelech S, Sutter C, Zhang H: Kinetworks protein kinase multiblot analysis. Methods Mol Biol 2003, 218:99-111.
55. Fleming CE, Mar FM, Franquinho F, Saraiva MJ, Sousa MM: Transthyretin internalization by sensory neurons is megalin mediated and necessary for its neuritogenic activity. J Neurosci 2009, 29:3220-3232. 10.1523/JNEUROSCI.6012-08.2009.
56. Norton WT, Poduslo SE: Myelination in rat brain: method of myelin isolation. J Neurochem 1973, 21:749-757. 10.1111/j.1471-4159.1973.tb07519.x.
57. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M: Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 2004, 58:167-176.
58. Gierke S, Kumar P, Wittmann T: Analysis of microtubule polymerization dynamics in live cells. Methods Cell Biol 2010, 97:15-33.
59. Qi Y, Wang JK, McMillian M, Chikaraishi DM: Characterization of a CNS cell line, CAD, in which morphological differentiation is initiated by serum deprivation. J Neurosci 1997, 17:1217-1225.
60. Komarova Y, De Groot CO, Grigoriev I, Gouveia SM, Munteanu EL, Schober JM, Honnappa S, Buey RM, Hoogenraad CC, Dogterom M, Borisy GG, Steinmetz MO, Akhmanova A: Mammalian end binding proteins control persistent microtubule growth. J Cell Biol 2009, 184:691-706. 10.1083/jcb.200807179.
61. Pereira AJ, Maiato H: Improved kymography tools and its applications to mitosis. Methods 2010, 51:214-219. 10.1016/j.ymeth.2010.01.016.
62. Neukirchen D, Bradke F: Cytoplasmic linker proteins regulate neuronal polarization through microtubule and growth cone dynamics. J Neurosci 2011, 31:1528-1538. 10.1523/JNEUROSCI.3983-10.2011.
63. Li CH, Tam PKS: An iterative algorithm for minimum cross entropy thresholding. Pattern Recognit Lett 1998, 18:771-776.
64. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG: Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 2006, 23:635-659. 10.1089/neu.2006.23.635.