Glycogen synthase kinase-3 regulation of chromatin segregation and cytokinesis in mouse preimplantation embryos

Molecular Reproduction and Development

Volumn 74, Issue 2, 2007, Pages 178-188

  Acevedo, Nicole ^a   Wang, Xia ^a   Dunn, Rodney L ^b   Smith, Gary D ^a,b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c NONE   (United States)

Author keywords

Chromatin segregation; Cytokinesis; Embryo; Glycogen synthase kinase 3

Indexed keywords

ALSTERPAULLONE; ENZYME ANTIBODY; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3ALPHA ANTIBODY; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOGEN SYNTHASE KINASE 3BETA ANTIBODY; ISOPROTEIN; LITHIUM CHLORIDE; SERINE; THREONINE; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BLASTOCYST; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINESIS; CYTOPLASM; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; IMMUNONEUTRALIZATION; KARYOKINESIS; MEIOSIS; MICROINJECTION; MICRONUCLEUS; MITOSIS; MITOSIS INHIBITION; MOUSE; NONHUMAN; OOCYTE; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PRONUCLEUS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; ZYGOTE;

ANIMALS; BLASTOCYST; CELL CYCLE; CELL DIVISION; CHROMATIN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOGEN SYNTHASE KINASE 3; IMMUNOHISTOCHEMISTRY; MICE; MITOTIC SPINDLE APPARATUS; OOCYTES;

MAMMALIA;

EID: 33846027876     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.20495     Document Type: Article

References (65)

1. Alvarez B, Garrido E, Garcia-Sanz JA, Carrera AC. 2003. Phosphoinositide 3-kinase activation regulates cell division time by coordinated control of cell mass and cell cycle progression rate. J Biol Chem 278:26466-26473.
2. Bain J, McLauchlan H, Elliott M, Cohen P. 2003. The specificities of protein kinase inhibitors: An update. Biochem J 371:199-204.
3. Battaglia DE, Goodwin P, Klein NA, Soules MR. 1996. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod 11:2217-2222.
4. Berridge MJ, Downes CP, Hanley MR. 1989. Neural and developmental actions of lithium: A unifying hypothesis. Cell 59:411-419.
5. Bertrand JA, Thieffine S, Vulpetti A, Cristiani C, Valsasina B, Knapp S, Kalisz HM, Flocco M. 2003. Structural characterization of the GSK-3beta active site using selective and non-selective ATP-mimetic inhibitors. J Mol Biol 333:393-407.
6. 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.
7. Ciemerych MA. 1995. Chromatin condensation activity and cortical activity during the first three cell cycles of a mouse embryo. Mol Reprod Dev 41:416-424.
8. Ciemerych MA, Czolowska R. 1993. Differential chromatin condensation of female and male pronuclei in mouse zygotes. Mol Reprod Dev 34:73-80.
9. Cohen P, Frame S. 2001. The renaissance of GSK3. Nat Rev Mol Cell Biol 2:769-776.
10. Collas P, Le Guellec K, Tasken K. 1999. The A-kinase-anchoring protein AKAP95 is a multivalent protein with a key role in chromatin condensation at mitosis. J Cell Biol 147:1167-1180.
11. Corson DW, Fein A. 1983. Quantitative pressure injection of picoliter volumes into Limulus ventral photoreceptors. Biophys J 44:299-304.
12. Davidson EH, Cameron RA, Ransick A. 1998. Specification of cell late in the sea urchin embryo: Summary and some proposed mechanisms. Development 125:3269-3290.
13. Davies SP, Reddy H, Caivano M, Cohen P. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105.
14. Delaval B, Ferrand A, Conte N, Larroque C, Hernandez-Verdun D, Prigent C, Birnbaum D. 2004. Aurora B -TACC1 protein complex in cytokinesis. Oncogene 23:4516-4522.
15. do Carmo Avides M, Tavares A, Glover DM. 2001. Polo kinase and Asp are needed to promote the mitotic organizing activity of centrosomes. Nat Cell Biol 3:421-424.
16. Dominguez I, Itoh K, Sokol SY. 1995. Role of glycogen synthase kinase 3 beta as a negative regulator of dorsoventral axis formation in Xenopus embryos. Proc Natl Acad Sci USA 92:8498-8502.
17. Doxsey S. 2001. Re-evaluating centrosome function. Nat Rev Mol Cell Biol 2:688-698.
18. Embi N, Rylatt DB, Cohen P. 1980. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur J Biochem 107:519-527.
19. Emily-Fenouil F, Ghiglione C, Lhomond G, Lepage T, Gache C. 1998. GSK3beta/shaggy mediates patterning along the animal-vegetal axis of the sea urchin embryo. Development 125:2489-2498.
20. Gebauer F, Richter JD. 1997. Synthesis and function of Mos: The control switch of vertebrate oocyte meiosis. Bioessays 19:23-28.
21. Generoso WM, Katoh M, Cain KT, Hughes LA, Foxworth LB, Mitchell TJ, Bishop JB. 1989. Chromosome malsegregation and embryonic lethality induced by treatment of normally ovulated mouse oocytes with nocodazole. Mutat Res 210:313-322.
22. Guadagno TM, Ferrell JE, Jr. 1998. Requirement for MAPK activation for normal mitotic progression in Xenopus egg extracts. Science 282:1312-1315.
23. Hannak E, Kirkham M, Hyman AA, Oegema K. 2001. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J Cell Biol 155:1109-1116.
24. Haraguchi S, Naito K, Sato E. 1998. MAP kinase cascade, but not ERKs, activated during early cleavage of mouse embryos. Mol Reprod Dev 51:148-155.
25. Hedgepeth CM, Conrad LJ, Zhang J, Huang HC, Lee VM, Klein PS. 1997. Activation of the Wnt signaling pathway: A molecular mechanism for lithium action. Dev Biol 185:82-91.
26. Hedgepeth CM, Deardorff MA, Klein PS. 1999a. Xenopus axin interacts with glycogen synthase kinase-3 beta and is expressed in the anterior midbrain. Mech Dev 80:147-151.
27. Hedgepeth CM, Deardorff MA, Rankin K, Klein PS. 1999b. Regulation of glycogen synthase kinase 3beta and downstream Wnt signaling by axin. Mol Cell Biol 19:7147-7157.
28. Hoenich KP, Luo J, Rubie EA, Tsao MS, Jin O, Woodgett JR. 2000. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406:86-90.
29. Horne MM, Guadagno TM. 2003. A requirement for MAP kinase in the assembly and maintenance of the mitotic spindle. J Cell Biol 161:1021-1028.
30. Inoue S. 1981. Cell division and the mitotic spindle. J Cell Biol 91:131s-147s.
31. Josefsberg LB, Galiani D, Lazar S, Kaufman O, Seger R, Dekel N. 2003. Maturation-promoting factor governs mitogen-activated protein kinase activation and interphase suppression during meiosis of rat oocytes. Biol Reprod 68:1282-1290.
32. Kaufman MH. 1973. Timing of the first cleavage division of haploid mouse eggs, and the duration of its component stages. J Cell Sci 13:553-566.
33. Klein PS, Melton DA. 1996. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93:8455-8459.
34. Lawitts JA, Biggers JD. 1993. Culture of preimplantation embryos. Methods Enzymol 225:153-164.
35. Leost M, Schultz C, Link A, Wu YZ, Biernat J, Mandelkow EM, Bibb JA, Snyder GL, Greengard P, Zaharevitz DW, Gussio R, Senderowicz AM, Sausville EA, Kunick C, Meijer L. 2000. Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25. Eur J Biochem 267:5983-5994.
36. Liu Y, Obata K, Yamanaka H, Dai Y, Fukuoka T, Tokunaga A, Noguchi K. 2004. Activation of extracellular signal-regulated protein kinase in dorsal horn neurons in the rat neuropathic intermittent claudication model. Pain 109:64-72.
37. Loberg RD, Vesely E, Brosius FC, III. 2002. Enhanced glycogen synthase kinase-3beta activity mediates hypoxia-induced apoptosis of vascular smooth muscle cells and is prevented by glucose transport and metabolism. J Biol Chem 277:41667-41673.
38. Lovestone S, Hartley CL, Pearce J, Anderton BH. 1996. Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: The effects on the organization and stability of microtubules. Neuroscience 73:1145-1157.
39. Lovestone S, Davis DR, Webster MT, Kaech S, Brion JP, Matus A, Anderton BH. 1999. Lithium reduces tau phosphorylation: Effects in living cells and in neurons at therapeutic concentrations. Biol Psychiatry 45:995-1003.
40. Lu Q, Dunn RL, Angeles R, Smith GD. 2002. Regulation of spindle formation by active mitogen-activated protein kinase and protein phosphatase 2A during mouse oocyte meiosis. Biol Reprod 66:29-37.
41. Masui Y, Markert CL. 1971. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177:129-145.
42. Nasmyth K, Peters JM, Uhlmann F. 2001. Splitting the chromosome: Cutting the ties that bind sister chromatids. Novartis Found Symp 237:113-133; discussion 133-8, 158-163.
43. Ossipova O, Bardeesy N, DePinho RA, Green JB. 2003. LKB1 (XEEK1) regulates Wnt signaling in vertebrate development. Nat Cell Biol 5:889-894.
44. Phiel CJ. Klein PS. 2001. Molecular targets of lithium action. Annu Rev Pharmacol Toxicol 41:789-813.
45. Pierce SB, Kimelman D. 1995. Regulation of Spemann organizer formation by the intracellular kinase Xgsk-3. Development 121:755-765.
46. Roberts EC, Shapiro PS, Nahreini TS, Pages G, Pouyssegur J, Ahn NG. 2002. Distinct cell cycle timing requirements for extracellular signal-regulated kinase and phosphoinositide 3-kinase signaling pathways in somatic cell mitosis. Mol Cell Biol 22:7226-7241.
47. Robinson MJ, Cobb MH. 1997. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 9:180-186.
48. Ryves WJ, Harwood AJ. 2001. Lithium inhibits glycogen synthase kinase-3 by competition for magnesium. Biochem Biophys Res Commun 280:720-725.
49. Sang H, Lu Z, Li Y, Ru B, Wang W, Chen J. 2001. Phosphorylation of tau by glycogen synthase kinase 3beta in intact mammalian cells influences the stability of microtubules. Neurosci Lett 312:141-144.
50. Song L, De Sarno P, Jope RS. 2002. Central role of glycogen synthase kinase-3beta in endoplasmic reticulum stress-induced caspase-3 activation. J Biol Chem 277:44701-44708.
51. Stambolic V, Ruel L, Woodgett JR. 1996. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signaling in intact cells. Curr Biol 6:1664-1668.
52. Sumoy L, Kiefer J, Kimehnan D. 1999. Conservation of intracellular Wnt signaling components in dorsal-ventral axis formation in zebrafish. Dev Genes Evol 209:48-58.
53. Sun F, Betzendahl I, Pacchierotti F, Ranaldi R, Smitz J, Cortvrindt R, Eichenlaub-Ritter U. 2005. Aneuploidy in mouse metaphase II oocytes exposed in vivo and in vitro in preantral follicle culture to nocodazole. Mutagenesis 20:65-75.
54. Tatebayashi Y, Haque N, Tung YC, Iqbal K, Grundke-Iqbal I. 2004. Role of tau phosphorylation by glycogen synthase kinase-3beta in the regulation of organelle transport. J Cell Sci 117:1653-1663.
55. Tournebizc R, Andersen SS, Verde F, Doree M, Karsenti E, Hyman AA. 1997. Distinct roles of PP1 and PP2A-like phosphatases in control of microtubule dynamics during mitosis. Embo J 16:5537-5549.
56. Verlhac MH, de Pennart H, Maro B, Cohb MH, Clarke HJ. 1993. MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 158:330-340.
57. Verlhac MH, Kubiak JZ, Weber M, Geraud G, Colledge WH, Evans MJ, Maro B. 1996. Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122:815-822.
58. Vonica A, Weng W, Gumbiner BM, Venuti JM. 2000. TCF is the nuclear effector of the beta-catenin signal that patterns the sea urchin animal-vegetal axis. Dev Biol 217:230-243.
59. Wakefield JG, Stephens DJ, Tavare JM. 2003. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J Cell Sci 116:637-646.
60. Wang X, Liu XT, Dunn R, Ohl DA, Smith GD. 2003. Glycogen synthase kinase-3 regulates mouse oocyte homologue segregation. Mol Reprod Dev 64:96-105.
61. Welsh GI, Proud CG. 1993. Glycogen synfhase kinase-3 is rapidly inactivated in response to insulin and phosphorylates eukaryotic initiation factor elF-2B. Biochem J 294:625-629.
62. Winston NJ, Maro B. 1995. Calmodulin-dependent protein kinase II is activated transiently in ethanol-stimulated mouse oocytes. Dev Biol 170:350-352.
63. Woodgett JR. 1990. Molecular cloning and expression of glycogen synthase kinase-3/factor A. Embo J 9:2431-2438.
64. Yu Y, Xia P, Li S, Yan Y, Tan J. 2002. Determination and synchronisation of G1-phase of the cell cycle in 2- and 4-cell mouse embryos. Zygote 10:245-251.
65. Zhang F, Phiel CJ, Spece L, Gurvich N, Klein PS. 2003. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J Biol Chem 278:33067-33077.