Planarian GSK3s are involved in neural regeneration

Development Genes and Evolution

Volumn 218, Issue 2, 2008, Pages 89-103

  Adell, Teresa ^a   Marsal, Maria ^a   Saló, Emili ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

1 Azakenpaullone; GSK3; Planarians; Regeneration

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; HELMINTH PROTEIN; NERVE PROTEIN;

ANIMAL; ARTICLE; CENTRAL NERVOUS SYSTEM; ENZYMOLOGY; GENETICS; MORPHOGENESIS; NERVE REGENERATION; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; TURBELLARIA;

ANIMALS; BODY PATTERNING; CENTRAL NERVOUS SYSTEM; GLYCOGEN SYNTHASE KINASE 3; HELMINTH PROTEINS; MORPHOGENESIS; NERVE REGENERATION; NERVE TISSUE PROTEINS; PHENOTYPE; PHYLOGENY; PLANARIANS;

EID: 84883835546     PISSN: 0949944X     EISSN: 1432041X     Source Type: Journal    
DOI: 10.1007/s00427-007-0199-3     Document Type: Article

References (68)

1. Anderton BH (1999) Alzheimer's disease: clues from flies and worms. Curr Biol 9:R106-R109
2. Baguñà J, Ballester R (1978) The nervous system in planarians: peripheral and gastrodermal plexuses, pharynx innervation and the relationship between central nervous system structure and the aceolomate organization. J Morph 155:237-252
3. Broun M, Gee L, Reinhardt B, Bode HR (2005) Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132:2907-2916
4. Cebria F, Newmark PA (2007) Morphogenesis defects are associated with abnormal nervous system regeneration following roboA RNAi in planarians. Development 134:833-837
5. Cebria F, Nakazawa M, Mineta K, Ikeo K, Gojobori T, Agata K (2002) Dissecting planarian central nervous system regeneration by the expression of neural-specific genes. Dev Growth Differ 44:135-146
6. Cebria F, Guo T, Jopek J, Newmark P (2007) Regeneration and maintenance of the planarian midline is regulated by a slit orthologue. Dev Biol 207(2):394-406
7. Chen G, Bower KA, Ma C, Fang S, Thiele CJ, Luo J (2004) Glycogen synthase kinase 3beta (GSK3beta) mediates 6-hydroxydopamineinduced neuronal death. Faseb J 18:1162-1164
8. Dajani R, Fraser E, Roe SM, Young N, Good V, Dale TC, Pearl LH (2001) Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition. Cell 105:721-732
9. Dajani R, Fraser E, Roe SM, YeoM, Good VM, Thompson V, Dale TC, Pearl LH (2003) Structural basis for recruitment of glycogen synthase kinase 3beta to the axin-APC scaffold complex. EMBO J 22:494-501
10. Emily-Fenouil F, Ghiglione C, Lhomond G, Lepage T, Gache C (1998) GSK3beta/shaggy mediates patterning along the animalvegetal axis of the sea urchin embryo. Development 125:2489-2498
11. Farnesi R, Tei S (1980) Dugesia lugubris s.l. auricles: research into the ultrastructure and on the functional efficiency. Riv Biol 73:65-77
12. Frame S, Cohen P (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359(Pt 1):1-16
13. Fraser E, Young N, Dajani R, Franca-Koh J, Ryves J, Williams RS, Yeo M, Webster MT, Richardson C, Smalley MJ, Pearl LH, Harwood A, Dale TC (2002) Identification of the Axin and Frat binding region of glycogen synthase kinase-3. J Biol Chem 277: 2176-2185
14. Fredieu JR, Cui Y, Maier D, Danilchik MV, Christian JL (1997) Xwnt-8 and lithium can act upon either dorsal mesodermal or neurectodermal cells to cause a loss of forebrain in Xenopus embryos. Dev Biol 186: 100-114
15. Gogel S, Wakefield S, Tear G, Klambt C, Gordon-Weeks PR (2006) The Drosophila microtubule associated protein Futsch is phosphorylated by Shaggy/Zeste-white 3 at an homologous GSK3beta phosphorylation site in MAP1B. Mol Cell Neurosci 33:188-199
16. Goold RG, Gordon-Weeks PR (2004) Glycogen synthase kinase 3beta and the regulation of axon growth. Biochem Soc Trans 32:809-811
17. Guder C, Philipp I, Lengfeld T, Watanabe H, Hobmayer B, Holstein TW (2006) The Wnt code: cnidarians signal the way. Oncogene 25:7450-7460
18. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows95/98/NT. Nucleic Acids Symp Ser 41:95-98
19. 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
20. Higginbotham H, Tanaka T, Brinkman BC, Gleeson JG (2006) GSK3beta and PKCzeta function in centrosome localization and process stabilization during Slit-mediated neuronal repolarization. Mol Cell Neurosci 32:118-132
21. Inoue T, Kumamoto H, Okamoto K, Umesono Y, Sakai M, Sanchez Alvarado A, Agata K (2004) Morphological and functional recovery of the planarian photosensing system during head regeneration. Zoolog Sci 21:275-283
22. Itoh K, Krupnik VE, Sokol SY (1998) Axis determination in Xenopus involves biochemical interactions of axin, glycogen synthase kinase 3 and beta-catenin. Curr Biol 8:591-594
23. Jiang H, Guo W, Liang X, Rao Y (2005) Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120: 123-135
24. Jope RS, Johnson GV (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 29:95-102
25. 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 neurotrophininduced and hippocampal axon growth. Neuron 52:981-996
26. Kishida K, Naka KI (1967) Amino acids and the spikes from the retinal ganglion cells. Science 156:648-650
27. Kobayashi C, Saito Y, Ogawa K, Agata K (2007) Wnt signaling is required for antero-posterior patterning of the planarian brain. Dev Biol 306:714-724
28. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163
29. Kunick C, Lauenroth K, Leost M, Meijer L, Lemcke T (2004) 1-Azakenpaullone is a selective inhibitor of glycogen synthase kinase-3 beta. Bioorg Med Chem Lett 14:413-416
30. Lartillot N, Philippe H (2004) A Bayesian mixture model for acrosssite heterogeneities in the amino-acid replacement process. Mol Biol Evol 21(6):1095-1109
31. Li R (2005) Neuronal polarity: until GSK-3 do us part. Curr Biol 15: R198-R200
32. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 20:27-39
33. Marcus EA, Kintner C, Harris W (1998) The role of GSK3beta in regulating neuronal differentiation in Xenopus laevis. Mol Cell Neurosci 12:269-280
34. Marsal M, Pineda D, Salo E (2003) Gtwnt-5 a member of the wnt family expressed in a subpopulation of the nervous system of the planarian Girardia tigrina. Gene Expr Patterns 3:489-495
35. Mills J, Digicaylioglu M, Legg AT, Young CE, Young SS, Barr AM, Fletcher L, O, Connor TP, Dedhar S (2003) Role of integrin-linked kinase in nerve growth factor-stimulated neurite outgrowth. J Neurosci 23:1638-1648
36. Mineta K, Nakazawa M, Cebria F, Ikeo K, Agata K, Gojobori T (2003) Origin and evolutionary process of the CNS elucidated by comparative genomics analysis of planarian ESTs. Proc Natl Acad Sci USA 100:7666-7671
37. Miyasaka T, Ding Z, Gengyo-Ando K, Oue M, Yamaguchi H, Mitani S, Ihara Y (2005) Progressive neurodegeneration in C. elegans model of tauopathy. Neurobiol Dis 20:372-383
38. Muller WA, Teo R, Mohrlen F (2004) Patterning a multi-headed mutant in Hydractinia: enhancement of head formation and its phenotypic normalization. Int J Dev Biol 48:9-15
39. Newmark PA (2005) Opening a new can of worms: a large-scale RNAi screen in planarians. Dev Cell 8:623-624
40. Niehrs C (1999) Head in the WNT: the molecular nature of Spemann's head organizer. Trends Genet 15:314-319
41. Nogi T, Levin M (2005) Characterization of innexin gene expression and functional roles of gap-junctional communication in planarian regeneration. Dev Biol 287:314-335
42. Okamoto K, Takeuchi K, Agata K (2005) Neural projections in planarian brain revealed by fluorescent dye tracing. Zoolog Sci 22:535-546
43. Oviedo NJ, Newmark PA, Sanchez Alvarado A (2003) Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea. Dev Dyn 226:326-333
44. Parker PJ, Caudwell FB, Cohen P (1983) Glycogen synthase from rabbit skeletal muscle; effect of insulin on the state of phosphorylation of the seven phosphoserine residues in vivo. Eur J Biochem 130:227-234
45. Pineda D, Salo E (2002) Planarian Gtsix3, a member of the Six/so gene family, is expressed in brain branches but not in eye cells. Gene Expr Patterns 2:169-173
46. Plickert G, Jacoby V, Frank U, Muller W, Mokady O (2006) Wnt signaling in hydroid development: formation of the primary body axis in embryogenesis and its subsequent patterning. Dev Biol 298:368-378
47. Rosania G, Merlie J Jr., Gray N, Chang Y, Schultz P, Heald R (1999) A cyclin-dependent kinase inhibitor inducing cancer cell differentiation: biochemical identification using Xenopus egg extracts. Proc Natl Acad Sci USA 96:4797-4802
48. Salinas PC (2005) Retrograde signalling at the synapse: a role for Wnt proteins. Biochem Soc Trans 33:1295-1298
49. Salo E (2006) The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays 28:546-559
50. Salo E, Baguna J (1984) Regeneration and pattern formation in planarians. I. The pattern of mitosis in anterior and posterior regeneration in Dugesia (G) tigrina, and a new proposal for blastema formation. J Embryol Exp Morphol 83:63-80
51. Sanchez Alvarado A, Newmark P (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci USA 96:5049-5054
52. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou A (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10:55-63
53. Schaffer B, Wiedau-Pazos M, Geschwind DH (2003) Gene structure and alternative splicing of glycogen synthase kinase 3 beta (GSK-3beta) in neural and non-neural tissues. Gene 302:73-81
54. Schlesinger A, Shelton CA, Maloof JN, Meneghini M, Bowerman B (1999) Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes Dev 13:2028-2038
55. Siegfried E, Perkins LA, Capaci TM, Perrimon N (1990) Putative protein kinase product of the Drosophila segment-polarity gene zeste-white3. Nature 345:825-829
56. Singer M (1952) The influence of the nerve in regeneration of the amphibian extremity. Q Rev Biol 27:169-200
57. Suzuki M, Satoh A, Ide H, Tamura K (2005) Nerve-dependent and -independent events in blastema formation during Xenopus froglet limb regeneration. Dev Biol 286:361-375
58. Takadera T, Ohyashiki T (2007) Caspase-dependent apoptosis induced by calcineurin inhibitors was prevented by glycogen synthase kinase-3 inhibitors in cultured rat cortical cells. Brain Res 1133:20-26
59. Takadera T, Yoshikawa R, Ohyashiki T (2006) Thapsigargin-induced apoptosis was prevented by glycogen synthase kinase-3 inhibitors in PC12 cells. Neurosci Lett 408:124-128
60. Teo R, Mohrlen F, Plickert G, Muller WA, Frank U (2006) An evolutionary conserved role of Wnt signaling in stem cell fate decision. Dev Biol 289:91-99
61. Tsonis PA, Del Rio-Tsonis K, Wallace JL, Burns JC, Hofmann MC, Millan JL, Washabaugh CH (1996) Can insights into urodele limb regeneration be achieved with cell cultures and retroviruses? Int J Dev Biol 40:813-816
62. Umemori H, Linhoff MW, Ornitz DM, Sanes JR (2004) FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118:257-270
63. Umesono Y, Watanabe K, Agata K (1999) Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209:31-39
64. Weitzel HE, Illies MR, Byrum CA, Xu R, Wikramanayake AH, Ettensohn CA (2004) Differential stability of beta-catenin along the animal-vegetal axis of the sea urchin embryo mediated by dishevelled. Development 131:2947-2956
65. Welsh GI, Proud CG (1993) Glycogen synthase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor eIF-2B. Biochem J 294(Pt 3):625-629
66. Woodgett JR (1990) Molecular cloning and expression of glycogen synthase kinase-3/factor A. Embo J 9:2431-2438
67. Zhou FQ, Snider WD (2005) Cell biology. GSK-3beta and microtubule assembly in axons. Science 308:211-214
68. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD (2004) NGFinduced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897-912