1,112
Views
34
CrossRef citations to date
0
Altmetric
Report

p38α MAPK Is a MTOC-associated protein regulating spindle assembly, spindle length and accurate chromosome segregation during mouse oocyte meiotic maturation

, , , , , , , , , & show all
Pages 4130-4143 | Published online: 15 Oct 2010

References

  • Compton DA. Spindle assembly in animal cells. Annu Rev Biochem 2000; 69:95 - 114
  • Gatlin JC, Matov A, Groen AC, Needleman DJ, Maresca TJ, Danuser G, et al. Spindle fusion requires dynein-mediated sliding of oppositely oriented micro-tubules. Curr Biol 2009; 19:287 - 296
  • Taylor SS, Scott MI, Holland AJ. The spindle checkpoint: a quality control mechanism which ensures accurate chromosome segregation. Chromosome Res 2004; 12:599 - 616
  • Kastan MB, Bartek J. Cell cycle checkpoints and cancer. Nature 2004; 432:316 - 323
  • Martin RH. Meiotic errors in human oogenesis and spermatogenesis. Reprod Biomed Online 2008; 16:523 - 531
  • Wang WH, Sun QY. Meiotic spindle, spindle checkpoint and embryonic aneuploidy. Front Biosci 2006; 11:620 - 636
  • Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 2007; 130:484 - 498
  • Brunet S, Polanski Z, Verlhac MH, Kubiak JZ, Maro B. Bipolar meiotic spindle formation without chromatin. Curr Biol 1998; 8:1231 - 1234
  • Schatten G. The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 1994; 165:299 - 335
  • Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 2001; 81:807 - 869
  • Saavedra HI, Fukasawa K, Conn CW, Stambrook PJ. MAPK mediates RAS-induced chromosome instability. J Biol Chem 1999; 274:38083 - 38090
  • Sun SC, Xiong B, Lu SS, Sun QY. MEK1/2 is a critical regulator of microtubule assembly and spindle organization during rat oocyte meiotic maturation. Mol Reprod Dev 2008; 75:1542 - 1548
  • Yu LZ, Xiong B, Gao WX, Wang CM, Zhong ZS, Huo LJ, et al. MEK1/2 regulates microtubule organization, spindle pole tethering and asymmetric division during mouse oocyte meiotic maturation. Cell Cycle 2007; 6:330 - 338
  • Lewis TS, Shapiro PS, Ahn NG. Signal transduction through MAP kinase cascades. Adv Cancer Res 1998; 74:49 - 139
  • Sasaki K, Chiba K. Induction of apoptosis in starfish eggs requires spontaneous inactivation of MAPK (extracellular signal-regulated kinase) followed by activation of p38MAPK. Mol Biol Cell 2004; 15:1387 - 1396
  • Takenaka K, Moriguchi T, Nishida E. Activation of the protein kinase p38 in the spindle assembly checkpoint and mitotic arrest. Science 1998; 280:599 - 602
  • ter Haar E, Prabhakar P, Liu X, Lepre C. Crystal structure of the p38alpha-MAPKAP kinase 2 heterodimer. J Biol Chem 2007; 282:9733 - 9739
  • Ben-Levy R, Leighton IA, Doza YN, Attwood P, Morrice N, Marshall CJ, et al. Identification of novel phosphorylation sites required for activation of MAPKAP kinase-2. EMBO J 1995; 14:5920 - 5930
  • Larochelle S, Suter B. The Drosophila melanogaster homolog of the mammalian MAPK-activated protein kinase-2 (MAPKAPK-2) lacks a proline-rich N-terminus. Gene 1995; 163:209 - 214
  • Allen M, Svensson L, Roach M, Hambor J, McNeish J, Gabel CA. Deficiency of the stress kinase p38alpha results in embryonic lethality: characterization of the kinase dependence of stress responses of enzyme-deficient embryonic stem cells. J Exp Med 2000; 191:859 - 870
  • Mikhailov A, Shinohara M, Rieder CL. Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway. J Cell Biol 2004; 166:517 - 526
  • Matsusaka T, Pines J. Chfr acts with the p38 stress kinases to block entry to mitosis in mammalian cells. J Cell Biol 2004; 166:507 - 516
  • Shiromizu T, Goto H, Tomono Y, Bartek J, Totsukawa G, Inoko A, et al. Regulation of mitotic function of Chk1 through phosphorylation at novel sites by cyclin-dependent kinase 1 (Cdk1). Genes Cells 2006; 11:477 - 485
  • Yen AH, Yang JL. Cdc20 proteolysis requires p38 MAPK signaling and Cdh1-independent APC/C ubiquitination during spindle assembly checkpoint activation by cadmium. J Cell Physiol 2010; 223:327 - 334
  • Lee K, Kenny A, Rieder CL. P38 MAP Kinase Activity Is Required during Mitosis for Timely Satisfaction of the Mitotic Checkpoint but Not for the Fidelity of Chromosome Segregation. Mol Biol Cell 2010; 21:2150 - 2160
  • Liu J, Puscheck EE, Wang F, Trostinskaia A, Barisic D, Maniere G, et al. Serine-threonine kinases and transcription factors active in signal transduction are detected at high levels of phosphorylation during mitosis in preimplantation embryos and trophoblast stem cells. Reproduction 2004; 128:643 - 654
  • Paliga AJ, Natale DR, Watson AJ. p38 mitogen-activated protein kinase (MAPK) first regulates filamentous actin at the 8–16 cell stage during preimplantation development. Biol Cell 2005; 97:629 - 640
  • Guay J, Lambert H, Gingras-Breton G, Lavoie JN, Huot J, Landry J. Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. J Cell Sci 1997; 110:357 - 368
  • Aouadi M, Binetruy B, Caron L, Le Marchand-Brustel Y, Bost F. Role of MAPKs in development and differentiation: lessons from knockout mice. Biochimie 2006; 88:1091 - 1098
  • Cuenda A, Rousseau S. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim Biophys Acta 2007; 1773:1358 - 1375
  • Villa-Diaz LG, Miyano T. Activation of p38 MAPK during porcine oocyte maturation. Biol Reprod 2004; 71:691 - 696
  • Goshima G, Wollman R, Stuurman N, Scholey JM, Vale RD. Length control of the metaphase spindle. Curr Biol 2005; 15:1979 - 1988
  • Brust-Mascher I, Sommi P, Cheerambathur DK, Scholey JM. Kinesin-5-dependent poleward flux and spindle length control in Drosophila embryo mitosis. Mol Biol Cell 2009; 20:1749 - 1762
  • Wang ZB, Ou XH, Tong JS, Li S, Wei L, Ouyang YC, et al. The SUMO pathway functions in mouse oocyte maturation. Cell Cycle 2010; 9:2640 - 2646
  • Joshi HC, Palacios MJ, McNamara L, Cleveland DW. Gamma-tubulin is a centrosomal protein required for cell cycle-dependent microtubule nucleation. Nature 1992; 356:80 - 83
  • Rieder CL. The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 1981; 84:145 - 158
  • Salmon ED, Begg DA. Functional implications of cold-stable microtubules in kinetochore fibers of insect spermatocytes during anaphase. J Cell Biol 1980; 85:853 - 665
  • Haren L, Stearns T, Luders J. Plk1-dependent recruitment of gamma-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS One 2009; 4:5976
  • Burbank KS, Mitchison TJ, Fisher DS. Slide-and-cluster models for spindle assembly. Curr Biol 2007; 17:1373 - 1383
  • Vogt E, Kirsch-Volders M, Parry J, Eichenlaub-Ritter U. Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat Res 2008; 651:14 - 29
  • Malmanche N, Maia A, Sunkel CE. The spindle assembly checkpoint: preventing chromosome missegregation during mitosis and meiosis. FEBS Lett 2006; 580:2888 - 2895
  • Tang J, Yang X, Liu X. Phosphorylation of Plk1 at Ser326 regulates its functions during mitotic progression. Oncogene 2008; 27:6635 - 6645
  • Cha H, Wang X, Li H, Fornace AJ Jr. A functional role for p38 MAPK in modulating mitotic transit in the absence of stress. J Biol Chem 2007; 282:22984 - 22992
  • Hannak E, Kirkham M, Hyman AA, Oegema K. Aurora-A kinase is required for centrosome maturation in Caenorhabditis elegans. J Cell Biol 2001; 155:1109 - 1116
  • Barr FA, Sillje HH, Nigg EA. Polo-like kinases and the orchestration of cell division. Nat Rev Mol Cell Biol 2004; 5:429 - 440
  • Yao LJ, Fan HY, Tong C, Chen DY, Schatten H, Sun QY. Polo-like kinase-1 in porcine oocyte meiotic maturation, fertilization and early embryonic mitosis. Cell Mol Biol (Noisy-le-grand) 2003; 49:399 - 405
  • Fan HY, Tong C, Teng CB, Lian L, Li SW, Yang ZM, et al. Characterization of Polo-like kinase-1 in rat oocytes and early embryos implies its functional roles in the regulation of meiotic maturation, fertilization and cleavage. Mol Reprod Dev 2003; 65:318 - 329
  • Meng XQ, Fan HY, Zhong ZS, Zhang G, Li YL, Chen DY, et al. Localization of gamma-tubulin in mouse eggs during meiotic maturation, fertilization and early embryonic development. J Reprod Dev 2004; 50:97 - 105
  • Raynaud-Messina B, Merdes A. Gamma-tubulin complexes and microtubule organization. Curr Opin Cell Biol 2007; 19:24 - 30
  • Lee J, Miyano T, Moor RM. Spindle formation and dynamics of gamma-tubulin and nuclear mitotic apparatus protein distribution during meiosis in pig and mouse oocytes. Biol Reprod 2000; 62:1184 - 1192
  • Barrett SL, Albertini DF. Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol Reprod 2007; 76:949 - 957
  • Berdnik D, Knoblich JA. Drosophila Aurora-A is required for centrosome maturation and actin-dependent asymmetric protein localization during mitosis. Curr Biol 2002; 12:640 - 647
  • Barr AR, Gergely F. Aurora-A: the maker and breaker of spindle poles. J Cell Sci 2007; 120:2987 - 2996
  • Sumara I, Gimenez-Abian JF, Gerlich D, Hirota T, Kraft C, de la Torre C, et al. Roles of polo-like kinase 1 in the assembly of functional mitotic spindles. Curr Biol 2004; 14:1712 - 1722
  • Ben-Levy R, Hooper S, Wilson R, Paterson HF, Marshall CJ. Nuclear export of the stress-activated protein kinase p38 mediated by its substrate MAPKAP kinase-2. Curr Biol 1998; 8:1049 - 1057
  • Yuan J, Xu BZ, Qi ST, Tong JS, Wei L, Li M, et al. MAPK-activated protein kinase 2 is required for mouse meiotic spindle assembly and kinetochore-microtubule attachment. PLoS One 2010; 5:11247
  • Maro B, Howlett SK, Webb M. Non-spindle microtubule organizing centers in metaphase II-arrested mouse oocytes. J Cell Biol 1985; 101:1665 - 1672
  • Silk AD, Holland AJ, Cleveland DW. Requirements for NuMA in maintenance and establishment of mammalian spindle poles. J Cell Biol 2009; 184:677 - 690
  • Houghtaling BR, Yang G, Matov A, Danuser G, Kapoor TM. Op18 reveals the contribution of nonkinetochore microtubules to the dynamic organization of the vertebrate meiotic spindle. Proc Natl Acad Sci USA 2009; 106:15338 - 15343
  • Ohi R, Burbank K, Liu Q, Mitchison TJ. Nonredundant functions of Kinesin-13s during meiotic spindle assembly. Curr Biol 2007; 17:953 - 959
  • Khodjakov A, Copenagle L, Gordon MB, Compton DA, Kapoor TM. Minus-end capture of preformed kinetochore fibers contributes to spindle morphogenesis. J Cell Biol 2003; 160:671 - 683
  • Wuhr M, Chen Y, Dumont S, Groen AC, Needleman DJ, Salic A, et al. Evidence for an upper limit to mitotic spindle length. Curr Biol 2008; 18:1256 - 1261
  • Mitchison TJ, Maddox P, Gaetz J, Groen A, Shirasu M, Desai A, et al. Roles of polymerization dynamics, opposed motors and a tensile element in governing the length of Xenopus extract meiotic spindles. Mol Biol Cell 2005; 16:3064 - 3076
  • Waters JC, Mitchison TJ, Rieder CL, Salmon ED. The kinetochore microtubule minus-end disassembly associated with poleward flux produces a force that can do work. Mol Biol Cell 1996; 7:1547 - 1558
  • Uteng M, Hentrich C, Miura K, Bieling P, Surrey T. Poleward transport of Eg5 by dynein-dynactin in Xenopus laevis egg extract spindles. J Cell Biol 2008; 182:715 - 726
  • Yang G, Cameron LA, Maddox PS, Salmon ED, Danuser G. Regional variation of microtubule flux reveals microtubule organization in the metaphase meiotic spindle. J Cell Biol 2008; 182:631 - 639
  • Wassmann K, Niault T, Maro B. Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr Biol 2003; 13:1596 - 1608
  • Yin S, Wang Q, Liu JH, Ai JS, Liang CG, Hou Y, et al. Bub1 prevents chromosome misalignment and precocious anaphase during mouse oocyte meiosis. Cell Cycle 2006; 5:2130 - 2137
  • Wei L, Liang XW, Zhang QH, Li M, Yuan J, Li S, et al. BubR1 is a spindle assembly checkpoint protein regulating meiotic cell cycle progression of mouse oocyte. Cell Cycle 2010; 9:1112 - 1121
  • Reis A, Madgwick S, Chang HY, Nabti I, Levasseur M, Jones KT. Prometaphase APCcdh1 activity prevents non-disjunction in mammalian oocytes. Nat Cell Biol 2007; 9:1192 - 1198
  • Fan HY. BubR1, a spindle assembly checkpoint protein in mammalian oocyte meiosis. Cell Cycle 2010; 9:1456 - 1465
  • Elowe S, Hummer S, Uldschmid A, Li X, Nigg EA. Tension-sensitive Plk1 phosphorylation on BubR1 regulates the stability of kinetochore microtubule interactions. Genes Dev 2007; 21:2205 - 2219
  • Li M, Li S, Yuan J, Wang ZB, Sun SC, Schatten H, et al. Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. PLoS One 2009; 4:7701
  • Sun SC, Wei L, Li M, Lin SL, Xu BZ, Liang XW, et al. Perturbation of survivin expression affects chromosome alignment and spindle checkpoint in mouse oocyte meiotic maturation. Cell Cycle 2009; 8:3365 - 3372
  • Gaetz J, Kapoor TM. Dynein/dynactin regulate metaphase spindle length by targeting depolymerizing activities to spindle poles. J Cell Biol 2004; 166:465 - 471
  • Yuan J, Li M, Wei L, Yin S, Xiong B, Li S, et al. Astrin regulates meiotic spindle organization, spindle pole tethering and cell cycle progression in mouse oocytes. Cell Cycle 2009; 8:3384 - 3395