Maternally recruited Aurora C kinase is more stable than Aurora B to support mouse oocyte maturation and early development

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 33, 2012, Pages

  Schindler, Karen ^a,b   Davydenko, Olga ^a   Fram, Brianna ^a   Lampson, Michael A ^a   Schultz, Richard M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; AURORA C KINASE; MESSENGER RNA;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BLASTOCYST; CELL DIVISION; CONTROLLED STUDY; CYTOKINESIS; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME STABILITY; FEMALE; FEMALE SUBFERTILITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOTYPE; IMMUNOCYTOCHEMISTRY; MEIOSIS; MOUSE; NEWBORN; NONHUMAN; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; BASE SEQUENCE; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENZYME STABILITY; FEMALE; MEIOSIS; MICE; MOLECULAR SEQUENCE DATA; OOCYTES; OOGENESIS; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; RNA, MESSENGER, STORED;

EID: 84865155384     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120517109     Document Type: Article

References (43)

1. Gopalan G, Chan CS, Donovan PJ (1997) A novel mammalian, mitotic spindle-associated kinase is related to yeast and fly chromosome segregation regulators. J Cell Biol 138:643-656. (Pubitemid 27349844)
2. Yanai A, Arama E, Kilfin G, Motro B (1997) ayk1, a novel mammalian gene related to Drosophila aurora centrosome separation kinase, is specifically expressed during meiosis. Oncogene 14:2943-2950. (Pubitemid 27315663)
3. Tseng TC, Chen SH, Hsu YP, Tang TK (1998) Protein kinase profile of sperm and eggs: Cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol 17:823-833.
4. Baldini E, et al. (2011) Aurora kinases are expressed in medullary thyroid carcinoma (MTC) and their inhibition suppresses in vitro growth and tumorigenicity of the MTC derived cell line TT. BMC Cancer 11:411.
5. Price DM, Kanyo R, Steinberg N, Chik CL, Ho AK (2009) Nocturnal activation of aurora C in rat pineal gland: Its role in the norepinephrine- induced phosphorylation of histone H3 and gene expression. Endocrinology 150:2334-2341.
6. Yan X, et al. (2005) Cloning and characterization of a novel human Aurora C splicing variant. Biochem Biophys Res Commun 328:353-361. (Pubitemid 40164676)
7. Yan X, et al. (2005) Aurora C is directly associated with Survivin and required for cytokinesis. Genes Cells 10:617-626. (Pubitemid 40867492)
8. Slattery SD, Mancini MA, Brinkley BR, Hall RM (2009) Aurora-C kinase supports mitotic progression in the absence of Aurora-B. Cell Cycle 8:2984-2994.
9. Sasai K, et al. (2004) Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil Cytoskeleton 59:249-263. (Pubitemid 40012993)
10. Fernández-Miranda G, et al. (2011) Genetic disruption of aurora B uncovers an essential role for aurora C during early mammalian development. Development 138:2661-2672.
11. Kimmins S, et al. (2007) Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol Endocrinol 21:726-739.
12. Ben Khelifa M, et al. (2011) A new AURKC mutation causing macrozoospermia: Implications for human spermatogenesis and clinical diagnosis. Mol Hum Reprod 17:762-768.
13. Shuda K, Schindler K, Ma J, Schultz RM, Donovan PJ (2009) Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol Reprod Dev 76:1094-1105.
14. Swain JE, Ding J, Wu J, Smith GD (2008) Regulation of spindle and chromatin dynamics during early and late stages of oocyte maturation by aurora kinases. Mol Hum Reprod 14:291-299. (Pubitemid 351804030)
15. Lane SI, Chang HY, Jennings PC, Jones KT (2010) The Aurora kinase inhibitor ZM447439 accelerates first meiosis in mouse oocytes by overriding the spindle assembly checkpoint. Reproduction 140:521-530.
16. Gautschi O, et al. (2008) Aurora kinases as anticancer drug targets. Clin Cancer Res 14:1639-1648. (Pubitemid 351471713)
17. Vogt E, Kipp A, Eichenlaub-Ritter U (2009) Aurora kinase B, epigenetic state of centromeric heterochromatin and chiasma resolution in oocytes. Reprod Biomed Online 19:352-368.
18. Yang KT, et al. (2010) Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mice. Mol Biol Cell 21:2371-2383.
19. Sharif B, et al. (2010) The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. J Cell Sci 123:4292-4300.
20. Nguyen HG, Chinnappan D, Urano T, Ravid K (2005) Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: Identification of an aneuploidy-promoting property. Mol Cell Biol 25:4977-4992. (Pubitemid 40781099)
21. Stewart S, Fang G (2005) Destruction box-dependent degradation of aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Res 65:8730-8735. (Pubitemid 41377361)
22. Yabe T, et al. (2009) The maternal-effect gene cellular island encodes aurora B kinase and is essential for furrow formation in the early zebrafish embryo. PLoS Genet 5:e1000518.
23. Severson AF, Hamill DR, Carter JC, Schumacher J, Bowerman B (2000) The aurora-related kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase and is required for cytokinesis. Curr Biol 10:1162-1171.
24. Giet R, Glover DM (2001) Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152:669-682.
25. Hauf S, et al. (2003) The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J Cell Biol 161:281-294. (Pubitemid 36529847)
26. Golbus MS, Stein MP (1976) Qualitative patterns of protein synthesis in the mouse oocyte. J Exp Zool 198:337-342.
27. Downs SM (1990) Protein synthesis inhibitors prevent both spontaneous and hormone-dependent maturation of isolated mouse oocytes. Mol Reprod Dev 27:235-243.
28. Avo Santos M, et al. (2011) A role for Aurora C in the chromosomal passenger complex during human preimplantation embryo development. Hum Reprod 26:1868-1881.
29. Richter JD (2007) CPEB: A life in translation. Trends Biochem Sci 32:279-285.
30. Chen J, et al. (2011) Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev 25:755-766.
31. Hu HM, Chuang CK, Lee MJ, Tseng TC, Tang TK (2000) Genomic organization, expression, and chromosome localization of a third aurora-related kinase gene, Aie1. DNA Cell Biol 19:679-688.
32. Xu Z, Williams CJ, Kopf GS, Schultz RM (2003) Maturation-associated increase in IP3 receptor type 1: Role in conferring increased IP3 sensitivity and Ca2+ oscillatory behavior in mouse eggs. Dev Biol 254:163-171. (Pubitemid 36268988)
33. Oh JS, Susor A, Conti M (2011) Protein tyrosine kinase Wee1B is essential for metaphase II exit in mouse oocytes. Science 332:462-465.
34. Murai S, Stein P, Buffone MG, Yamashita S, Schultz RM (2010) Recruitment of Orc6l, a dormant maternal mRNA in mouse oocytes, is essential for DNA replication in 1-cell embryos. Dev Biol 341:205-212.
35. Anger M, Stein P, Schultz RM (2005) CDC6 requirement for spindle formation during maturation of mouse oocytes. Biol Reprod 72:188-194. (Pubitemid 40013770)
36. Tsafriri A, Chun SY, Zhang R, Hsueh AJ, Conti M (1996) Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: Studies using selective phosphodiesterase inhibitors. Dev Biol 178:393-402. (Pubitemid 26365046)
37. Chatot CL, Ziomek CA, Bavister BD, Lewis JL, Torres I (1989) An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 86:679-688. (Pubitemid 19183391)
38. Ma P, Schultz RM (2008) Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 319:110-120.
39. Schindler K, Schultz RM (2009) CDC14B acts through FZR1 (CDH1) to prevent meiotic maturation of mouse oocytes. Biol Reprod 80:795-803.
40. Duncan FE, Chiang T, Schultz RM, Lampson MA (2009) Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol Reprod 81:768-776.
41. Igarashi H, Knott JG, Schultz RM, Williams CJ (2007) Alterations of PLCbeta1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev Biol 312:321-330. (Pubitemid 350180761)
42. Stein P, Schindler K (2011) Mouse oocyte microinjection, maturation and ploidy assessment. J Vis Exp 53:e2851.
43. Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20:1522-1528.