Glycogen synthase kinase 3 has a proapoptotic function in Hydra gametogenesis

Developmental Biology

Volumn 278, Issue 1, 2005, Pages 1-12

  Rentzsch, Fabian ^a,b,d   Hobmayer, Bert ^a,c   Holstein, Thomas W ^a,d  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c UNIVERSITY OF INNSBRUCK   (Austria)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Apoptosis; Cnidaria; Gametogenesis; GSK3; Hydra; Nurse cell; Oogenesis; Wnt

Indexed keywords

ALSTERPAULLONE; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; LITHIUM; WNT PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; COELENTERATE; ENZYME ACTIVITY; ENZYME INHIBITION; GAMETOGENESIS; GERM LINE; METAZOON; MOLECULAR EVOLUTION; MOLECULE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; ZEBRA FISH;

ANIMALIA; CNIDARIA; DANIO RERIO; HYDRA; METAZOA;

EID: 11844286394     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.10.007     Document Type: Article

References (73)

1. S. Artavanis-Tsakonas, M.D. Rand, and R.J. Lake Notch signaling: cell fate control and signal integration in development Science 284 1999 770 776
2. R.V. Bhat, J. Shanley, M.P. Correll, W.E. Fieles, R.A. Keith, C.W. Scott, and C.M. Lee Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration Proc. Natl. Acad. Sci. U. S. A. 97 2000 11074 11079
3. S.S. Blair A role for the segment polarity gene shaggy-zeste white 3 in the specification of regional identity in the developing wing of Drosophila Dev. Biol. 162 1994 229 244
4. M. Broun, and H.R. Bode Characterization of the head organizer in hydra Development 129 2002 875 884
5. K.M. Cadigan, and R. Nusse Wnt signaling: a common theme in animal development Genes Dev. 11 1997 3286 3305
6. S. Chen, D.C. Guttridge, Z. You, Z. Zhang, A. Fribley, M.W. Mayo, J. Kitajewski, and C.Y. Wang Wnt-1 signaling inhibits apoptosis by activating beta-catenin/T cell factor-mediated transcription J. Cell Biol. 152 2001 87 96
7. D. Cook, M.J. Fry, K. Hughes, R. Sumathipala, J.R. Woodgett, and T.C. Dale Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C EMBO J. 15 1996 4526 4536
8. A.A. Culbert, M.J. Brown, S. Frame, T. Hagen, D.A. Cross, B. Bax, and A.D. Reith GSK-3 inhibition by adenoviral FRAT1 overexpression is neuroprotective and induces Tau dephosphorylation and beta-catenin stabilisation without elevation of glycogen synthase activity FEBS Lett. 507 2001 288 294
9. R. Dajani, E. Fraser, S.M. Roe, N. Young, V. Good, T.C. Dale, and L.H. Pearl Crystal structure of glycogen synthase kinase 3 beta: structural basis for phosphate-primed substrate specificity and autoinhibition Cell 105 2001 721 732
10. R. Dajani, E. Fraser, S.M. Roe, M. Yeo, V.M. Good, V. Thompson, T.C. Dale, and L.H. Pearl Structural basis for recruitment of glycogen synthase kinase 3beta to the axin-APC scaffold complex EMBO J. 22 2003 494 501
11. C.N. David A quantitative method for maceration of hydra tissue Wilhelm Roux' Arch. Entwicklungsmech. Org. 171 1973 259 268
12. V.W. Ding, R.H. Chen, and F. McCormick Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling J. Biol. Chem. 275 2000 32475 32481
13. I. Dominguez, K. Itoh, and S.Y. Sokol Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos Proc. Natl. Acad. Sci. U. S. A. 92 1995 8498 8502
14. N. Embi, D.B. Rylatt, and P. Cohen Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase Eur. J. Biochem. 107 1980 519 527
15. F. Emily-Fenouil, C. Ghiglione, G. Lhomond, T. Lepage, and C. Gache GSK3beta/shaggy mediates patterning along the animal-vegetal axis of the sea urchin embryo Development 125 1998 2489 2498
16. D.M. Ferkey, and D. Kimelman GSK-3: new thoughts on an old enzyme Dev. Biol. 225 2000 471 479
17. D.R. Foltz, M.C. Santiago, B.E. Berechid, and J.S. Nye Glycogen synthase kinase-3beta modulates notch signaling and stability Curr. Biol. 12 2002 1006 1011
18. S. Frame, and P. Cohen GSK3 takes centre stage more than 20 years after its discovery Biochem. J. 359 2001 1 16
19. E. Fraser, N. Young, R. Dajani, J. Franca-Koh, J. Ryves, R.S. Williams, M. Yeo, M.T. Webster, C. Richardson, M.J. Smalley, L.H. Pearl, A. Harwood, and T.C. Dale Identification of the Axin and Frat binding region of glycogen synthase kinase-3 J. Biol. Chem. 277 2002 2176 2185
20. G.T. Ginsburg, and A.R. Kimmel Autonomous and nonautonomous regulation of axis formation by antagonistic signaling via 7-span cAMP receptors and GSK3 in Dictyostelium Genes Dev. 11 1997 2112 2123
21. R.G. Goold, R. Owen, and P.R. Gordon-Weeks Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones J. Cell Sci. 112 Pt. 19 1999 3373 3384
22. M. Greber, C.N. David, and T. Holstein A quantitative method for separation of living hydra cells Roux's Arch. Dev. Biol. 201 1992 196 300
23. M. Hammerschmidt, F. Pelegri, M.C. Mullins, D.A. Kane, F.J. van Eeden, M. Granato, M. Brand, M. Furutani-Seiki, P. Haffter, C.P. Heisenberg, Y.J. Jiang, R.N. Kelsh, J. Odenthal, R.M. Warga, and C. Nusslein-Volhard dino And mercedes, two genes regulating dorsal development in the zebrafish embryo Development 123 1996 95 102
24. A.J. Harwood, S.E. Plyte, J. Woodgett, H. Strutt, and R.R. Kay Glycogen synthase kinase 3 regulates cell fate in Dictyostelium Cell 80 1995 139 148
25. M. Hassel, and A. Bieller Stepwise transfer from high to low lithium concentrations increases the head-forming potential in Hydra vulgaris and possibly activates the PI cycle Dev. Biol. 177 1996 439 448
26. X. He, J.P. Saint-Jeannet, J.R. Woodgett, H.E. Varmus, and I.B. Dawid Glycogen synthase kinase-3 and dorsoventral patterning in Xenopus embryos Nature 374 1995 617 622
27. M. Herold, M. Cikala, H. MacWilliams, C.N. David, and A. Bottger Cloning and characterisation of PKB and PRK homologs from Hydra and the evolution of the protein kinase family Dev. Genes Evol. 212 2002 513 519
28. M. Hetman, J.E. Cavanaugh, D. Kimelman, and Z. Xia Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal J. Neurosci. 20 2000 2567 2574
29. E. Hobmayer, M. Hatta, R. Fischer, T. Fujisawa, T.W. Holstein, and T. Sugiyama Identification of a Hydra homologue of the beta-catenin/plakoglobin/ armadillo gene family Gene 172 1996 155 159
30. B. Hobmayer, F. Rentzsch, K. Kuhn, C.M. Happel, C.C. von Laue, P. Snyder, U. Rothbacher, and T.W. Holstein WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra Nature 407 2000 186 189
31. B. Hobmayer, F. Rentzsch, and T.W. Holstein Identification and expression of HySmad1, a member of the R-Smad family of TGFbeta signal transducers, in the diploblastic metazoan Hydra Dev. Genes Evol. 211 2001 597 602
32. K.P. Hoeflich, J. Luo, E.A. Rubie, M.S. Tsao, O. Jin, and J.R. Woodgett Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation Nature 406 2000 86 90
33. T. Holstein Cnidaria-Hydrozoa 1994 Fischer Verlag Stuttgart
34. T.W. Holstein, and C.N. David Cell cycle length, cell size, and proliferation rate in hydra stem cells Dev. Biol. 142 1990 392 400
35. T.G. Honegger, D. Zürrer, and P. Tardent Oogenesis in Hydra carnea: a new model based on light and electron microscopic analysis and nurse cell differentiation Tissue Cell 21 1989 381 393
36. K. Hughes, E. Nikolakaki, S.E. Plyte, N.F. Totty, and J.R. Woodgett Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation EMBO J. 12 1993 803 808
37. J. Jia, K. Amanai, G. Wang, J. Tang, B. Wang, and J. Jiang Shaggy/GSK3 antagonizes Hedgehog signalling by regulating cubitus interruptus Nature 416 2002 548 552
38. Y. Kishimoto, K.H. Lee, L. Zon, M. Hammerschmidt, and S. Schulte-Merker The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning Development 124 1997 4457 4466
39. P.S. Klein, and D.A. Melton A molecular mechanism for the effect of lithium on development Proc. Natl. Acad. Sci. U. S. A. 93 1996 8455 8459
40. M. Knockaert, K. Wieking, S. Schmitt, M. Leost, K.M. Grant, J.C. Mottram, C. Kunick, and L. Meijer Intracellular targets of Paullones. Identification following affinity purification on immobilized inhibitor J. Biol. Chem. 277 2002 25493 25501
41. O. Krylova, M.J. Messenger, and P.C. Salinas Dishevelled-1 regulates microtubule stability: a new function mediated by glycogen synthase kinase-3beta J. Cell Biol. 151 2000 83 94
42. S.G. Kuznetsov, M. Lyanguzowa, and T.C.G. Bosch Role of epithelial cells and programmed cell death in Hydra spermatogenesis Zoology 104 2001 25 31
43. M. Leost, C. Schultz, A. Link, Y.Z. Wu, J. Biernat, E.M. Mandelkow, J.A. Bibb, G.L. Snyder, P. Greengard, D.W. Zaharevitz, R. Gussio, A.M. Senderowicz, E.A. Sausville, C. Kunick, and L. Meijer Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25 Eur. J. Biochem. 267 2000 5983 5994
44. L. Li, H. Yuan, C.D. Weaver, J. Mao, G.H. Farr III, D.J. Sussman, J. Jonkers, D. Kimelman, and D. Wu Axin and Frat1 interact with dvl and GSK, bridging Dvl to GSK in Wnt-mediated regulation of LEF-1 EMBO J. 18 1999 4233 4240
45. C.L. Littlefield, C. Finkemeier, and H.R. Bode Spermatogenesis in Hydra oligactis. II. How temperature controls the reciprocity of sexual and asexual reproduction Dev. Biol. 146 1991 292 300
46. V.J. Martin, C.L. Littlefield, W.E. Archer, and H.R. Bode Embryogenesis in hydra Biol. Bull. 192 1997 345 363
47. M.A. Miller Gametogenesis in the early-diverging cnidarian Hydra vulgaris: molecules and mechanisms 1999 University of California Irvine
48. M.A. Miller, and R.E. Steele Lemon encodes an unusual receptor protein-tyrosine kinase expressed during gametogenesis in Hydra Dev. Biol. 224 2000 286 298
49. M.A. Miller, U. Technau, K.M. Smith, and R.E. Steele Oocyte development in Hydra involves selection from competent precursor cells Dev. Biol. 224 2000 326 338
50. A. Munck, and C.N. David Cell proliferation and differentiation kinetics during spermatogenesis in Hydra carnea Roux's Arch. Dev. Biol. 194 1985 247 256
51. A. Nasevicius, T. Hyatt, H. Kim, J. Guttman, E. Walsh, S. Sumanas, Y. Wang, and S.C. Ekker Evidence for a frizzled-mediated wnt pathway required for zebrafish dorsal mesoderm formation Development 125 1998 4283 4292
52. C. Nishimiya-Fujisawa, and T. Sugiyama Genetic analysis of developmental mechanisms in hydra. XX. Cloning of interstitial stem cells restricted to the sperm differentiation pathway in Hydra magnipapillata Dev. Biol. 157 1993 1 9
53. M. Pap, and G.M. Cooper Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway J. Biol. Chem. 273 1998 19929 19932
54. C.J. Phiel, and P.S. Klein Molecular targets of lithium action Annu. Rev. Pharmacol. Toxicol. 41 2001 789 813
55. S.B. Pierce, and D. Kimelman Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3 Development 121 1995 755 765
56. M.A. Price, and D. Kalderon Proteolysis of the Hedgehog signaling effector cubitus interruptus requires phosphorylation by glycogen synthase kinase 3 and casein kinase 1 Cell 108 2002 823 835
57. L. Ruel, V. Stambolic, A. Ali, A.S. Manoukian, and J.R. Woodgett Regulation of the protein kinase activity of Shaggy (Zeste-white3) by components of the wingless pathway in Drosophila cells and embryos J. Biol. Chem. 274 1999 21790 21796
58. P.G. Sacks, and L.E. Davis Production of nerveless Hydra attenuata by hydroxyurea treatments J. Cell Sci. 37 1979 189 203
59. M.J. Seidensticker, and J. Behrens Biochemical interactions in the wnt pathway Biochim. Biophys. Acta 1495 2000 168 182
60. E. Siegfried, L.A. Perkins, T.M. Capaci, and N. Perrimon Putative protein kinase product of the Drosophila segment-polarity gene zeste-white3 Nature 345 1990 825 829
61. X. Song, C.H. Zhu, C. Doan, and T. Xie Germline stem cells anchored by adherens junctions in the Drosophila ovary niches Science 296 2002 1855 1857
62. S.E. Stachel, D.J. Grunwald, and P.Z. Myers Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish Development 117 1993 1261 1274
63. V. Stambolic, and J.R. Woodgett Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation Biochem. J. 303 Pt. 3 1994 701 704
64. R.E. Steele Developmental signaling in Hydra: what does it take to build a "simple" animal? Dev. Biol. 248 2002 199 219
65. R.E. Steele, P. Lieu, N.H. Mai, M.A. Shenk, and M.P. Sarras Response to insulin and the expression pattern of a gene encoding an insulin receptor homologue suggest a role for an insulin-like molecule in regulating growth and patterning in Hydra Dev. Genes Evol. 206 1996 247 259
66. P. Tardent Gametogenesis in the genus Hydra Am. Zool. 14 1974 447 456
67. P. Tardent Coelenterata, cnidaria F. Seidel Morphogenese der Tiere vol. 1 (A-I) 1978 VEB Gustav Fischer Verlag Jena Jena 69 415
68. U. Technau, and H.R. Bode HyBra1, a Brachyury homologue, acts during head formation in Hydra Development 126 1999 999 1010
69. U. Technau, M.A. Miller, D. Bridge, and R.E. Steele Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis Dev. Biol. 260 2003 191 206
70. E. ter Haar, J.T. Coll, D.A. Austen, H.M. Hsiao, L. Swenson, and J. Jain Structure of GSK3beta reveals a primed phosphorylation mechanism Nat. Struct. Biol. 8 2001 593 596
71. Q.M. Wang, C.J. Fiol, A.A. DePaoli-Roach, and P.J. Roach Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation J. Biol. Chem. 269 1994 14566 14574
72. M. Westerfield The Zebrafish Book 1993 University of Oregon Press Eugene, OR
73. A.H. Wikramanayake, L. Huang, and W.H. Klein beta-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo Proc. Natl. Acad. Sci. U. S. A. 95 1998 9343 9348