A role for Aurora C in the chromosomal passenger complex during human preimplantation embryo development

Human Reproduction

Volumn 26, Issue 7, 2011, Pages 1868-1881

  Avo Santos, Margarida ^a   Van De Werken, Christine ^b   De Vries, Marieke ^c   Jahr, Holger ^b   Vromans, Martijn J M ^a   Laven, Joop S E ^b   Fauser, Bart C ^a   Kops, Geert J ^a   Lens, Susanne M ^a   Baart, Esther B ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Aurora C; chromosomal passenger complex; chromosome segregation; human embryos; human oocytes

Indexed keywords

AURORA B KINASE; AURORA C KINASE; BOREALIN; CHROMOSOMAL PASSENGER COMPLEX; HISTONE H3; INNER CENTROMERE PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; SURVIVIN; UNCLASSIFIED DRUG;

ARTICLE; BLASTOCYST; CHROMOSOME; CRYOPRESERVATION; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; MORULA; NUCLEOTIDE SEQUENCE; OOCYTE; PREIMPLANTATION EMBRYO; PROMETAPHASE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ZYGOTE;

EID: 79959472011     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der111     Document Type: Article

References (72)

1. Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B, Reyftmann L, Dechaud H, De Vos J, Hamamah S. The human cumulus-oocyte complex gene-expression profile. Hum Reprod 2006; 21:1705-1719. (Pubitemid 44028240)
2. Baart EB, de Rooij DG, Keegan KS, de Boer P. Distribution of Atr protein in primary spermatocytes of a mouse chromosomal mutant: a comparison of preparation techniques. Chromosoma 2000; 109:139-147. (Pubitemid 30433307)
3. Baart EB, Martini E, Van den Berg I, Macklon NS, Galjaard RJ, Fauser BC, Van Opstal D. Preimplantation genetic screening reveals a high incidence of aneuploidy and mosaicism in embryos from young women undergoing IVF. Hum Reprod 2006;21:223-233. (Pubitemid 41794315)
4. Barr AR, Gergely F. Aurora-A: the maker and breaker of spindle poles. J Cell Sci 2007;120:2987-2996. (Pubitemid 47517082)
5. Bernard M, Sanseau P, Henry C, Couturier A, Prigent C. Cloning of STK13, a third human protein kinase related to Drosophila aurora and budding yeast Ipl1 that maps on chromosome 19q13.3-ter. Genomics 1998;53:406-409. (Pubitemid 28527647)
6. Bielanska M, Tan SL, Ao A. Chromosomal mosaicism throughout human preimplantation development in vitro: incidence, type, and relevance to embryo outcome. Hum Reprod 2002;17:413-419. (Pubitemid 34168450)
7. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four-and eight-cell stages of preimplantation development. Nature 1988;332:459-461. (Pubitemid 18090251)
8. Brittle AL, Ohkura H. Centrosome maturation: Aurora lights the way to the poles. Curr Biol 2005;15:R880-R882. (Pubitemid 41566131)
9. 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.
10. Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 2006;20:1744-1754. (Pubitemid 43992883)
11. 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;21:796-805.
12. Chen HL, Tang CJ, Chen CY, Tang TK. Overexpression of an Aurora-C kinase-deficient mutant disrupts the Aurora-B/INCENP complex and induces polyploidy. J Biomed Sci 2005;12:297-310. (Pubitemid 40897637)
13. Coonen E, Derhaag JG, Dumoulin JC, Van Wissen LC, Bras M, Janssen M, Evers JL, Geraedts JP. Anaphase lagging mainly explains chromosomal mosaicism in human preimplantation embryos. Hum Reprod 2004; 19:316-324. (Pubitemid 38219999)
14. Cutts SM, Fowler KJ, Kile BT, Hii LL, O'Dowd RA, Hudson DF, Saffery R, Kalitsis P, Earle E, Choo KH. Defective chromosome segregation, microtubule bundling and nuclear bridging in inner centromere protein gene (Incenp)-disrupted mice. Hum Mol Genet 1999;8:1145-1155. (Pubitemid 29328982)
15. Daphnis DD, Delhanty JD, Jerkovic S, Geyer J, Craft I, Harper JC. Detailed FISH analysis of day 5 human embryos reveals the mechanisms leading to mosaic aneuploidy. Hum Reprod 2005;20:129-137.
16. Dieterich K, Soto Rifo R, Faure AK, Hennebicq S, Ben Amar B, Zahi M, Perrin J, Martinez D, Sele B, Jouk PS et al. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat Genet 2007;39:661-665. (Pubitemid 46676111)
17. Dieterich K, Zouari R, Harbuz R, Vialard F, Martinez D, Bellayou H, Prisant N, Zoghmar A, Guichaoua MR, Koscinski I et al. The Aurora Kinase C c.144delC mutation causes meiosis I arrest in men and is frequent in the North African population. Hum Mol Genet 2009; 18:1301-1309.
18. Dupont C, Segars J, DeCherney A, Bavister BD, Armant DR, Brenner CA. Incidence of chromosomal mosaicism in morphologically normal nonhuman primate preimplantation embryos. Fertil Steril 2010; 93:2545-2550.
19. Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 2004;6:117-131. (Pubitemid 38089210)
20. Heijnen EM, Eijkemans MJ, De Klerk C, Polinder S, Beckers NG, Klinkert ER, Broekmans FJ, Passchier J, Te Velde ER, Macklon NS et al. A mild treatment strategy for in-vitro fertilisation: a randomised non-inferiority trial. Lancet 2007;369:743-749.
21. Hohmann FP, Macklon NS, Fauser BC. A randomized comparison of two ovarian stimulation protocols with gonadotropin-releasing hormone (GnRH) antagonist cotreatment for in vitro fertilization commencing recombinant follicle-stimulating hormone on cycle day 2 or 5 with the standard long GnRH agonist protocol. J Clin Endocrinol Metab 2003; 88:166-173. (Pubitemid 36115160)
22. Hu HM, Chuang CK, Lee MJ, Tseng TC, Tang TK. Genomic organization, expression, and chromosome localization of a third aurora-related kinase gene, Aie1. DNA Cell Biol 2000;19:679-688.
23. Jeyaprakash AA, Klein UR, Lindner D, Ebert J, Nigg EA, Conti E. Structure of a Survivin-Borealin-INCENP core complex reveals how chromosomal passengers travel together. Cell 2007;131:271-285. (Pubitemid 47576137)
24. Jones GM, Cram DS, Song B, Kokkali G, Pantos K, Trounson AO. Novel strategy with potential to identify developmentally competent IVF blastocysts. Hum Reprod 2008a;23:1748-1759. (Pubitemid 352020001)
25. Jones GM, Cram DS, Song B, Magli MC, Gianaroli L, Lacham-Kaplan O, Findlay JK, Jenkin G, Trounson AO. Gene expression profiling of human oocytes following in vivo or in vitro maturation. Hum Reprod 2008b;23:1138-1144. (Pubitemid 351757345)
26. Katayama H, Brinkley WR, Sen S. The Aurora kinases: role in cell transformation and tumorigenesis. Cancer Metastasis Rev 2003; 22:451-464. (Pubitemid 36791899)
27. Kimmins S, Crosio C, Kotaja N, Hirayama J, Monaco L, Hoog C, Van Duin M, Gossen JA, Sassone-Corsi P. Differential functions of the Aurora-B and Aurora-C kinases in mammalian spermatogenesis. Mol Endocrinol 2007;21:726-739.
28. Kimura M, Matsuda Y, Yoshioka T, Okano Y. Cell cycle-dependent expression and centrosome localization of a third human aurora/Ipl1-related protein kinase, AIK3. J Biol Chem 1999;274:7334-7340.
29. Klein UR, Nigg EA, Gruneberg U. Centromere targeting of the chromosomal passenger complex requires a ternary subcomplex of Borealin, Survivin, and the N-terminal domain of INCENP. Mol Biol Cell 2006;17:2547-2558. (Pubitemid 43825493)
30. Kuijk EW, du Puy L, Van Tol HT, Haagsman HP, Colenbrander B, Roelen BA. Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev Biol 2007;7:58.
31. Li X, Sakashita G, Matsuzaki H, Sugimoto K, Kimura K, Hanaoka F, Taniguchi H, Furukawa K, Urano T. Direct association with inner centromere protein (INCENP) activates the novel chromosomal passenger protein, Aurora-C. J Biol Chem 2004;279:47201-47211. (Pubitemid 39518377)
32. Lin YS, Su LJ, Yu CT, Wong FH, Yeh HH, Chen SL, Wu JC, Lin WJ, Shiue YL, Liu HS et al. Gene expression profiles of the aurora family kinases. Gene Expr 2006;13:15-26.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408. (Pubitemid 34164012)
34. Mamo S, Gal AB, Polgar Z, Dinnyes A. Expression profiles of the pluripotency marker gene POU5F1 and validation of reference genes in rabbit oocytes and preimplantation stage embryos. BMC Mol Biol 2008;9:67.
35. Marquez C, Sandalinas M, Bahce M, Alikani M, Munne S. Chromosome abnormalities in 1255 cleavage-stage human embryos. Reprod Biomed Online 2000;1:17-26.
36. Mtango NR, Latham KE. Differential expression of cell cycle genes in rhesus monkey oocytes and embryos of different developmental potentials. Biol Reprod 2008;78:254-266. (Pubitemid 351159981)
37. Nguyen HG, Chinnappan D, Urano T, Ravid K. Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol Cell Biol 2005; 25:4977-4992. (Pubitemid 40781099)
38. Pavlok A, Kopecny V, Lucas-Hahn A, Niemann H. Transcriptional activity and nuclear ultrastructure of 8-cell bovine embryos developed by in vitro maturation and fertilization of oocytes from different growth categories of antral follicles. Mol Reprod Dev 1993;35:233-243. (Pubitemid 23207478)
39. Peters AH, Plug AW, Van Vugt MJ, de Boer P. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 1997;5:66-68. (Pubitemid 27129985)
40. Price DM, Kanyo R, Steinberg N, Chik CL, Ho AK. Nocturnal activation of aurora C in rat pineal gland: its role in the norepinephrine-induced phosphorylation of histone H3 and gene expression. Endocrinology 2009;150:2334-2341.
41. Puschendorf M, Terranova R, Boutsma E, Mao X, Isono K, Brykczynska U, Kolb C, Otte AP, Koseki H, Orkin SH et al. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat Genet 2008;40:411-420. (Pubitemid 351450889)
42. Rajkovic A, Matzuk MM. Functional analysis of oocyte-expressed genes using transgenic models. Mol Cell Endocrinol 2002;187:5-9. (Pubitemid 34436928)
43. Rambags BP, Krijtenburg PJ, Drie HF, Lazzari G, Galli C, Pearson PL, Colenbrander B, Stout TA. Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro. Mol Reprod Dev 2005; 72:77-87. (Pubitemid 41026309)
44. Ruchaud S, Carmena M, Earnshaw WC. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 2007;8:798-812. (Pubitemid 47462135)
45. Santos MA, Teklenburg G, Macklon NS, Van Opstal D, Schuring-Blom GH, Krijtenburg PJ, de Vreeden-Elbertse J, Fauser BC, Baart EB. The fate of the mosaic embryo: chromosomal constitution and development of Day 4, 5 and 8 human embryos. Hum Reprod 2010;25:1916-1926.
46. Sasai K, Katayama H, Stenoien DL, Fujii S, Honda R, Kimura M, Okano Y, Tatsuka M, Suzuki F, Nigg EA et al. Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil Cytoskeleton 2004;59:249-263. (Pubitemid 40012993)
47. Schramm RD, Paprocki AM, VandeVoort CA. Causes of developmental failure of in-vitro matured rhesus monkey oocytes: impairments in embryonic genome activation. Hum Reprod 2003;18:826-833. (Pubitemid 36426965)
48. Sharif B, Na J, Lykke-Hartmann K, McLaughlin SH, Laue E, Glover DM, Zernicka-Goetz M. The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. J Cell Sci 2010;123:4292-4300.
49. Shuda K, Schindler K, Ma J, Schultz RM, Donovan PJ. Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol Reprod Dev 2009;76:1094-1105.
50. Slattery SD, Moore RV, Brinkley BR, Hall RM. Aurora-C and Aurora-B share phosphorylation and regulation of CENP-A and Borealin during mitosis. Cell Cycle 2008;7:787-795. (Pubitemid 351520043)
51. Slattery SD, Mancini MA, Brinkley BR, Hall RM. Aurora-C kinase supports mitotic progression in the absence of Aurora-B. Cell Cycle 2009; 8:2984-2994.
52. Smits VA, Klompmaker R, Vallenius T, Rijksen G, Makela TP, Medema RH. p21 inhibits Thr161 phosphorylation of Cdc2 to enforce the G2 DNA damage checkpoint. J Biol Chem 2000;275:30638-30643.
53. Sugimoto K, Urano T, Zushi H, Inoue K, Tasaka H, Tachibana M, Dotsu M. Molecular dynamics of Aurora-A kinase in living mitotic cells simultaneously visualized with histone H3 and nuclear membrane protein importinalpha. Cell Struct Funct 2002;27:457-467. (Pubitemid 36267714)
54. Tang CJ, Lin CY, Tang TK. Dynamic localization and functional implications of Aurora-C kinase during male mouse meiosis. Dev Biol 2006; 290:398-410. (Pubitemid 43163501)
55. Tatsuka M, Katayama H, Ota T, Tanaka T, Odashima S, Suzuki F, Terada Y. Multinuclearity and increased ploidy caused by overexpression of the aurora-and Ipl1-like midbody-associated protein mitotic kinase in human cancer cells. Cancer Res 1998; 58:4811-4816. (Pubitemid 28503674)
56. Tesarik J. Involvement of oocyte-coded message in cell differentiation control of early human embryos. Development 1989;105:317-322. (Pubitemid 19053280)
57. Tesarik J, Kopecny V, Plachot M, Mandelbaum J. Activation of nucleolar and extranucleolar RNA synthesis and changes in the ribosomal content of human embryos developing in vitro. J Reprod Fertil 1986; 78:463-470. (Pubitemid 17179847)
58. Ulmer R, Rehder H, Trotnow S, Kniewald A, Kniewald T, Pfeiffer RA. Triploid embryo after in vitro fertilization. Arch Gynecol 1985; 237:101-107. (Pubitemid 16191698)
59. Uren AG, Wong L, Pakusch M, Fowler KJ, Burrows FJ, Vaux DL, Choo KH. Survivin and the inner centromere protein INCENP show similar cell-cycle localization and gene knockout phenotype. Curr Biol 2000; 10:1319-1328.
60. Vader G, Kauw JJ, Medema RH, Lens SM. Survivin mediates targeting of the chromosomal passenger complex to the centromere and midbody. EMBO Rep 2006a;7:85-92.
61. Vader G, Medema RH, Lens SM. The chromosomal passenger complex: guiding Aurora-B through mitosis. J Cell Biol 2006b;173:833-837.
62. Vagnarelli P, Earnshaw WC. Chromosomal passengers: the four-dimensional regulation of mitotic events. Chromosoma 2004; 113:211-222. (Pubitemid 39462364)
63. Vanneste E, Voet T, Le Caignec C, Ampe M, Konings P, Melotte C, Debrock S, Amyere M, Vikkula M, Schuit F et al. Chromosome instability is common in human cleavage-stage embryos. Nat Med 2009;15:577-583.
64. Viuff D, Greve T, Avery B, Hyttel P, Brockhoff PB, Thomsen PD. Chromosome aberrations in in vitro-produced bovine embryos at days 2-5 post-insemination. Biol Reprod 2000;63:1143-1148.
65. Vogt E, Kipp A, Eichenlaub-Ritter U. Aurora kinase B, epigenetic state of centromeric heterochromatin and chiasma resolution in oocytes. Reprod Biomed Online 2009;19:352-368.
66. Voullaire L, Slater H, Williamson R, Wilton L. Chromosome analysis of blastomeres from human embryos by using comparative genomic hybridization. Hum Genet 2000;106:210-217. (Pubitemid 30156426)
67. Wells D, Delhanty JD. Comprehensive chromosomal analysis of human preimplantation embryos using whole genome amplification and single cell comparative genomic hybridization. Mol Hum Reprod 2000; 6:1055-1062.
68. Yamanaka Y, Heike T, Kumada T, Shibata M, Takaoka Y, Kitano A, Shiraishi K, Kato T, Nagato M, Okawa K et al. Loss of Borealin/DasraB leads to defective cell proliferation, p53 accumulation and early embryonic lethality. Mech Dev 2008;125:441-450.
69. Yan X, Cao L, Li Q, Wu Y, Zhang H, Saiyin H, Liu X, Zhang X, Shi Q, Yu L. Aurora C is directly associated with Survivin and required for cytokinesis. Genes Cells 2005;10:617-626. (Pubitemid 40867492)
70. Yang KT, Li SK, Chang CC, Tang CJ, Lin YN, Lee SC, Tang TK. Aurora-C kinase deficiency causes cytokinesis failure in meiosis I and production of large polyploid oocytes in mouse. Mol Biol Cell 2010;21: 2371-2383.
71. 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; 70:1392-1399. (Pubitemid 38509687)
72. Zijlstra C, Kidson A, Schoevers EJ, Daemen AJ, Tharasanit T, Kuijk EW, Hazeleger W, Ducro-Steverink DW, Colenbrander B, Roelen BA. Blastocyst morphology, actin cytoskeleton quality and chromosome content are correlated with embryo quality in the pig. Theriogenology 2008;70:923-935.