Aurora kinase A is essential for meiosis in mouse oocytes

English version

Autoři: Cecilia S. Blengini ^aff001; Patricia Ibrahimian ^aff001; Michaela Vaskovicova ^aff003; David Drutovic ^aff003; Petr Solc ^aff003; Karen Schindler ^aff001
Působiště autorů: Department of Genetics; Rutgers, The State University of New Jersey, Piscataway, New Jersey, United States of America ^aff001; Human Genetics Institute of New Jersey; Piscataway, New Jersey, United States of America ^aff002; Institute of Animal Physiology and Genetics of the Czech Academy of Sciences, Libechov, Czech Republic ^aff003
Vyšlo v časopise: Aurora kinase A is essential for meiosis in mouse oocytes. PLoS Genet 17(4): e1009327. doi:10.1371/journal.pgen.1009327
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009327

Souhrn

The Aurora protein kinases are well-established regulators of spindle building and chromosome segregation in mitotic and meiotic cells. In mouse oocytes, there is significant Aurora kinase A (AURKA) compensatory abilities when the other Aurora kinase homologs are deleted. Whether the other homologs, AURKB or AURKC can compensate for loss of AURKA is not known. Using a conditional mouse oocyte knockout model, we demonstrate that this compensation is not reciprocal because female oocyte-specific knockout mice are sterile, and their oocytes fail to complete meiosis I. In determining AURKA-specific functions, we demonstrate that its first meiotic requirement is to activate Polo-like kinase 1 at acentriolar microtubule organizing centers (aMTOCs; meiotic spindle poles). This activation induces fragmentation of the aMTOCs, a step essential for building a bipolar spindle. We also show that AURKA is required for regulating localization of TACC3, another protein required for spindle building. We conclude that AURKA has multiple functions essential to completing MI that are distinct from AURKB and AURKC.

Klíčová slova:

Immunostaining – Meiosis – Metaphase – Microtubules – Oocytes – Phosphorylation – Protein kinases – Xenopus oocytes

Zdroje

1. Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet. 2012;13(7):493–504. doi: 10.1038/nrg3245 22705668

2. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nature Reviews Genetics. 2001;2(4):280–91. doi: 10.1038/35066065 11283700

3. Gruhn JR, Zielinska AP, Shukla V, Blanshard R, Capalbo A, Cimadomo D, et al. Chromosome errors in human eggs shape natural fertility over reproductive life span. Science. 2019;365(6460):1466–9. doi: 10.1126/science.aav7321 31604276

4. Manandhar G, Schatten H, Sutovsky P. Centrosome reduction during gametogenesis and its significance. Biol Reprod. 2005;72(1):2–13. doi: 10.1095/biolreprod.104.031245 15385423

5. Pimenta-Marques A, Bento I, Lopes CAM, Duarte P, Jana SC, Bettencourt-Dias M. A mechanism for the elimination of the female gamete centrosome in Drosophila melanogaster. Science. 2016:aaf4866. doi: 10.1126/science.aaf4866 27229142

6. Borrego-Pinto J, Somogyi K, Karreman MA, König J, Müller-Reichert T, Bettencourt-Dias M, et al. Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes. J Cell Biol. 2016;212(7):815–27. doi: 10.1083/jcb.201510083 27002173

7. Combelles CM, Albertini DF. Microtubule patterning during meiotic maturation in mouse oocytes is determined by cell cycle-specific sorting and redistribution of gamma-tubulin. Dev Biol. 2001;239(2):281–94. doi: 10.1006/dbio.2001.0444 11784035

8. Ma W, Viveiros MM. Depletion of pericentrin in mouse oocytes disrupts microtubule organizing center function and meiotic spindle organization. Mol Reprod Dev. 2014;81(11):1019–29. doi: 10.1002/mrd.22422 25266793

9. Baumann C, Wang X, Yang L, Viveiros MM. Error-prone meiotic division and subfertility in mice with oocyte-conditional knockdown of pericentrin. J Cell Sci. 2017;130(7):1251–62. doi: 10.1242/jcs.196188 28193732

10. So C, Seres KB, Steyer AM, Monnich E, Clift D, Pejkovska A, et al. A liquid-like spindle domain promotes acentrosomal spindle assembly in mammalian oocytes. Science. 2019;364(6447). doi: 10.1126/science.aat9557 31249032

11. Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007;130(3):484–98. doi: 10.1016/j.cell.2007.06.025 17693257

12. Clift D, Schuh M. A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun. 2015;6:7217. doi: 10.1038/ncomms8217 26147444

13. Musacchio A, Salmon ED. The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol. 2007;8(5):379–93. doi: 10.1038/nrm2163 17426725

14. Carmena M, Earnshaw WC. The cellular geography of Aurora kinases. Nature Reviews Molecular Cell Biology. 2003;4(11):842–54. doi: 10.1038/nrm1245 14625535

15. Nigg EA. Mitotic kinases as regulators of cell division and its checkpoints. Nature Reviews Molecular Cell Biology. 2001;2(1):21–32. doi: 10.1038/35048096 11413462

16. Brown JR, Koretke KK, Birkeland ML, Sanseau P, Patrick DR. Evolutionary relationships of Aurora kinases: implications for model organism studies and the development of anti-cancer drugs. BMC Evol Biol. 2004;4:39. doi: 10.1186/1471-2148-4-39 15476560

17. Barr AR, Gergely F. Aurora-A: the maker and breaker of spindle poles. J Cell Sci. 2007;120(Pt 17):2987–96. doi: 10.1242/jcs.013136 17715155

18. Cowley DO, Rivera-Perez JA, Schliekelman M, He YJ, Oliver TG, Lu L, et al. Aurora-A kinase is essential for bipolar spindle formation and early development. Mol Cell Biol. 2009;29(4):1059–71. doi: 10.1128/MCB.01062-08 19075002

19. Mori D, Yano Y, Toyo-oka K, Yoshida N, Yamada M, Muramatsu M, et al. NDEL1 phosphorylation by Aurora-A kinase is essential for centrosomal maturation, separation, and TACC3 recruitment. Mol Cell Biol. 2007;27(1):352–67. doi: 10.1128/MCB.00878-06 17060449

20. Katayama H, Sasai K, Kloc M, Brinkley BR, Sen S. Aurora kinase-A regulates kinetochore/chromatin associated microtubule assembly in human cells. Cell Cycle. 2008;7(17):2691–704. doi: 10.4161/cc.7.17.6460 18773538

21. Kinoshita K, Noetzel TL, Pelletier L, Mechtler K, Drechsel DN, Schwager A, et al. Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J Cell Biol. 2005;170(7):1047–55. doi: 10.1083/jcb.200503023 16172205

22. Balboula AZ, Nguyen AL, Gentilello AS, Quartuccio SM, Drutovic D, Solc P, et al. Haspin kinase regulates microtubule-organizing center clustering and stability through Aurora kinase C in mouse oocytes. J Cell Sci. 2016;129(19):3648–60. doi: 10.1242/jcs.189340 27562071

23. Saskova A, Solc P, Baran V, Kubelka M, Schultz RM, Motlik J. Aurora kinase A controls meiosis I progression in mouse oocytes. Cell Cycle. 2008;7(15):2368–76. doi: 10.4161/cc.6361 18677115

24. Solc P, Baran V, Mayer A, Bohmova T, Panenkova-Havlova G, Saskova A, et al. Aurora kinase A drives MTOC biogenesis but does not trigger resumption of meiosis in mouse oocytes matured in vivo. Biol Reprod. 2012;87(4):85. doi: 10.1095/biolreprod.112.101014 22837479

25. Yao LJ, Zhong ZS, Zhang LS, Chen DY, Schatten H, Sun QY. Aurora-A is a critical regulator of microtubule assembly and nuclear activity in mouse oocytes, fertilized eggs, and early embryos. Biol Reprod. 2004;70(5):1392–9. doi: 10.1095/biolreprod.103.025155 14695913

26. Ding J, Swain JE, Smith GD. Aurora kinase-A regulates microtubule organizing center (MTOC) localization, chromosome dynamics, and histone-H3 phosphorylation in mouse oocytes. Mol Reprod Dev. 2011;78(2):80–90. doi: 10.1002/mrd.21272 21274965

27. Bury L, Coelho PA, Simeone A, Ferries S, Eyers CE, Eyers PA, et al. Plk4 and Aurora A cooperate in the initiation of acentriolar spindle assembly in mammalian oocytes. J Cell Biol. 2017;216(11):3571–90. doi: 10.1083/jcb.201606077 28972102

28. Wang X, Baumann C, De La Fuente R, Viveiros MM. CEP215 and AURKA regulate spindle pole focusing and aMTOC organization in mouse oocytes. Reproduction. 2020. doi: 10.1530/REP-19-0263 31895686

29. Balboula AZ, Schindler K. Selective disruption of aurora C kinase reveals distinct functions from aurora B kinase during meiosis in mouse oocytes. PLoS Genet. 2014;10(2):e1004194. doi: 10.1371/journal.pgen.1004194 24586209

30. Schindler K, Davydenko O, Fram B, Lampson MA, Schultz RM. Maternally recruited Aurora C kinase is more stable than Aurora B to support mouse oocyte maturation and early development. Proc Natl Acad Sci U S A. 2012;109(33):E2215–22. doi: 10.1073/pnas.1120517109 22778418

31. Nguyen AL, Drutovic D, Vazquez BN, El Yakoubi W, Gentilello AS, Malumbres M, et al. Genetic Interactions between the Aurora Kinases Reveal New Requirements for AURKB and AURKC during Oocyte Meiosis. Current Biology. 2018;28(21):3458–+. doi: 10.1016/j.cub.2018.08.052 30415701

32. Wellard SR, Schindler K, Jordan PW. Aurora B and C kinases regulate chromosome desynapsis and segregation during mouse and human spermatogenesis. Journal of Cell Science. 2020;133(23):jcs248831. doi: 10.1242/jcs.248831 33172986

33. Wellard SR, Zhang Y, Shults C, Zhao X, McKay M, Murray SA, et al. Overlapping roles for PLK1 and Aurora A during meiotic centrosome biogenesis in mouse spermatocytes. EMBO reports.n/a(n/a):e51023. doi: 10.15252/embr.202051023 33615678

34. Lan ZJ, Xu X, Cooney AJ. Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol Reprod. 2004;71(5):1469–74. doi: 10.1095/biolreprod.104.031757 15215191

35. Chmatal L, Yang K, Schultz RM, Lampson MA. Spatial Regulation of Kinetochore Microtubule Attachments by Destabilization at Spindle Poles in Meiosis I. Curr Biol. 2015;25(14):1835–41. doi: 10.1016/j.cub.2015.05.013 26166779

36. Zhao X, Feng C, Yu D, Deng X, Wu D, Jin M, et al. Successive recruitment of p-CDC25B-Ser351 and p-cyclin B1-Ser123 to centrosomes contributes to the release of mouse oocytes from prophase I arrest. Dev Dyn. 2015;244(2):110–21. doi: 10.1002/dvdy.24220 25349079

37. Riabukha YA, Petrova DA, Zatsepina OV. Comparative Analysis of Number and Competence in Meiotic Maturation of Preovulatory Oocytes of C57Bl/6J Mice and Their F1 Hybrids after Stimulation with Gonadotropin. Bull Exp Biol Med. 2019;167(5):702–5. doi: 10.1007/s10517-019-04603-z 31630300

38. Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA. Quantitative Phosphoproteomics Identifies Substrates and Functional Modules of Aurora and Polo-Like Kinase Activities in Mitotic Cells. Science Signaling. 2011;4(179):rs5–rs. doi: 10.1126/scisignal.2001497 21712546

39. Little TM, Jordan PW. PLK1 is required for chromosome compaction and microtubule organization in mouse oocytes. Mol Biol Cell. 2020;31(12):1206–17. doi: 10.1091/mbc.E19-12-0701 32267211

40. Macůrek L, Lindqvist A, Lim D, Lampson MA, Klompmaker R, Freire R, et al. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature. 2008;455(7209):119–23. doi: 10.1038/nature07185 18615013

41. DeLuca KF, Meppelink A, Broad AJ, Mick JE, Peersen OB, Pektas S, et al. Aurora A kinase phosphorylates Hec1 to regulate metaphase kinetochore-microtubule dynamics. J Cell Biol. 2018;217(1):163–77. doi: 10.1083/jcb.201707160 29187526

42. Barros TP, Kinoshita K, Hyman AA, Raff JW. Aurora A activates D-TACC-Msps complexes exclusively at centrosomes to stabilize centrosomal microtubules. J Cell Biol. 2005;170(7):1039–46. doi: 10.1083/jcb.200504097 16186253

43. Vallot A, Leontiou I, Cladiere D, El Yakoubi W, Bolte S, Buffin E, et al. Tension-Induced Error Correction and Not Kinetochore Attachment Status Activates the SAC in an Aurora-B/C-Dependent Manner in Oocytes. Curr Biol. 2018;28(1):130–9 e3. doi: 10.1016/j.cub.2017.11.049 29276128

44. Hached K, Xie SZ, Buffin E, Cladière D, Rachez C, Sacras M, et al. Mps1 at kinetochores is essential for female mouse meiosis I. Development. 2011;138(11):2261–71. doi: 10.1242/dev.061317 21558374

45. Santaguida S, Tighe A, D’Alise AM, Taylor SS, Musacchio A. Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J Cell Biol. 2010;190(1):73–87. doi: 10.1083/jcb.201001036 20624901

46. Eyers PA, Erikson E, Chen LG, Maller JL. A Novel Mechanism for Activation of the Protein Kinase Aurora A. Current Biology. 2003;13(8):691–7. doi: 10.1016/s0960-9822(03)00166-0 12699628

47. Tsai MY, Wiese C, Cao K, Martin O, Donovan P, Ruderman J, et al. A Ran signalling pathway mediated by the mitotic kinase Aurora A in spindle assembly. Nat Cell Biol. 2003;5(3):242–8. doi: 10.1038/ncb936 12577065

48. Brunet S, Dumont J, Lee KW, Kinoshita K, Hikal P, Gruss OJ, et al. Meiotic regulation of TPX2 protein levels governs cell cycle progression in mouse oocytes. PLoS One. 2008;3(10):e3338. doi: 10.1371/journal.pone.0003338 18833336

49. Carmena M, Wheelock M, Funabiki H, Earnshaw WC. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol. 2012;13(12):789–803. doi: 10.1038/nrm3474 23175282

50. Carmena M, Ruchaud S, Earnshaw WC. Making the Auroras glow: regulation of Aurora A and B kinase function by interacting proteins. Curr Opin Cell Biol. 2009;21(6):796–805. doi: 10.1016/j.ceb.2009.09.008 19836940

51. Fu J, Bian M, Liu J, Jiang Q, Zhang C. A single amino acid change converts Aurora-A into Aurora-B-like kinase in terms of partner specificity and cellular function. Proceedings of the National Academy of Sciences. 2009;106(17):6939–44. doi: 10.1073/pnas.0900833106 19357306

52. Hans F, Skoufias DA, Dimitrov S, Margolis RL. Molecular distinctions between Aurora A and B: a single residue change transforms Aurora A into correctly localized and functional Aurora B. Mol Biol Cell. 2009;20(15):3491–502. doi: 10.1091/mbc.e09-05-0370 19494039

53. Zorba A, Buosi V, Kutter S, Kern N, Pontiggia F, Cho YJ, et al. Molecular mechanism of Aurora A kinase autophosphorylation and its allosteric activation by TPX2. Elife. 2014;3:e02667. doi: 10.7554/eLife.02667 24867643

54. Ferrari S, Marin O, Pagano MA, Meggio F, Hess D, El-Shemerly M, et al. Aurora-A site specificity: a study with synthetic peptide substrates. Biochem J. 2005;390(Pt 1):293–302. doi: 10.1042/BJ20050343 16083426

55. van Heesbeen R, Raaijmakers JA, Tanenbaum ME, Halim VA, Lelieveld D, Lieftink C, et al. Aurora A, MCAK, and Kif18b promote Eg5-independent spindle formation. Chromosoma. 2017;126(4):473–86. doi: 10.1007/s00412-016-0607-4 27354041

56. Ye AA, Deretic J, Hoel CM, Hinman AW, Cimini D, Welburn JP, et al. Aurora A Kinase Contributes to a Pole-Based Error Correction Pathway. Curr Biol. 2015;25(14):1842–51. doi: 10.1016/j.cub.2015.06.021 26166783

57. Seki A, Coppinger JA, Jang C-Y, Yates JR, Fang G. Bora and the Kinase Aurora A Cooperatively Activate the Kinase Plk1 and Control Mitotic Entry. Science. 2008;320(5883):1655–8. doi: 10.1126/science.1157425 18566290

58. Asteriti IA, De Mattia F, Guarguaglini G. Cross-Talk between AURKA and Plk1 in Mitotic Entry and Spindle Assembly. Frontiers in Oncology. 2015;5(283). doi: 10.3389/fonc.2015.00283 26779436

59. Joukov V, De Nicolo A. Aurora-PLK1 cascades as key signaling modules in the regulation of mitosis. Science Signaling. 2018;11(543):eaar4195. doi: 10.1126/scisignal.aar4195 30108183

60. Solc P, Kitajima TS, Yoshida S, Brzakova A, Kaido M, Baran V, et al. Multiple Requirements of PLK1 during Mouse Oocyte Maturation. PLOS ONE. 2015;10(2):e0116783. doi: 10.1371/journal.pone.0116783 25658810

61. Giet R, Uzbekov R, Cubizolles F, Le Guellec K, Prigent C. The Xenopus laevis aurora-related protein kinase pEg2 associates with and phosphorylates the kinesin-related protein XlEg5. J Biol Chem. 1999;274(21):15005–13. doi: 10.1074/jbc.274.21.15005 10329703

62. Fu J, Bian M, Xin G, Deng Z, Luo J, Guo X, et al. TPX2 phosphorylation maintains metaphase spindle length by regulating microtubule flux. J Cell Biol. 2015;210(3):373–83. doi: 10.1083/jcb.201412109 26240182

63. Mendez R, Hake LE, Andresson T, Littlepage LE, Ruderman JV, Richter JD. Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA. Nature. 2000;404(6775):302–7. doi: 10.1038/35005126 10749216

64. Hodgman R, Tay J, Mendez R, Richter JD. CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development. 2001;128(14):2815–22. 11526086

65. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil. 1989;86(2):679–88. doi: 10.1530/jrf.0.0860679 2760894

66. McGuinness BE, Anger M, Kouznetsova A, Gil-Bernabé AM, Helmhart W, Kudo NR, et al. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr Biol. 2009;19(5):369–80. doi: 10.1016/j.cub.2009.01.064 19249208

67. Yu J, Hecht NB, Schultz RM. RNA-binding properties and translation repression in vitro by germ cell-specific MSY2 protein. Biol Reprod. 2002;67(4):1093–8. doi: 10.1095/biolreprod67.4.1093 12297523

68. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, Kipp JL, et al. Postnatal regulation of germ cells by activin: The establishment of the initial follicle pool. Developmental Biology. 2006;298(1):132–48. doi: 10.1016/j.ydbio.2006.06.025 16930587

69. Dunn KW, Kamocka MM, McDonald JH. A practical guide to evaluating colocalization in biological microscopy. Am J Physiol Cell Physiol. 2011;300(4):C723–42. doi: 10.1152/ajpcell.00462.2010 21209361

70. Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006;224(Pt 3):213–32. doi: 10.1111/j.1365-2818.2006.01706.x 17210054

71. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9(7):676–82. doi: 10.1038/nmeth.2019 22743772

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