Aberrant expression of maternal Plk1 and Dctn3 results in the developmental failure of human in-vivo- and in-vitro-matured oocytes

Scientific Reports

Volumn 5, Issue , 2015, Pages 8192-

  Fan, Yong ^a   Zhao, Hong Cui ^b,c,d   Liu, Jianqiao ^a   Tan, Tao ^e   Ding, Ting ^b,c   Li, Rong ^b,c,d   Zhao, Yue ^b,d   Yan, Jie ^b,c   Sun, Xiaofang ^a   Yu, Yang ^b,c,d   Qiao, Jie ^b,c,d  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b PEKING UNIVERSITY THIRD HOSPITAL   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d Beijing Key Laboratory of Reproductive Endocrinology and Assisted Reproduction   (China)

^e National Engineering Research Center of Biomedicine and Animal Science   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; DYNACTIN; MICROTUBULE ASSOCIATED PROTEIN; ONCOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE; SMALL INTERFERING RNA;

ANEUPLOIDY; ANTAGONISTS AND INHIBITORS; CLUSTER ANALYSIS; CYTOKINESIS; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GENETICS; HUMAN; METABOLISM; OOCYTE; RNA INTERFERENCE; ZYGOTE;

ANEUPLOIDY; CELL CYCLE PROTEINS; CLUSTER ANALYSIS; CYTOKINESIS; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; OOCYTES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; ZYGOTE;

EID: 84923086495     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08192     Document Type: Article

References (57)

1. Steptoe, P. C. & Edwards, R. G. Birth after the reimplantation of a human embryo. Lancet 2, 366 (1978).
2. Cha, K. Y. et al. Pregnancy after in vitro fertilization of human follicular oocytes collected from nonstimulated cycles, their culture in vitro and their transfer in a donor oocyte program. Fertil Steril 55, 109-113 (1991).
3. Basatemur, E. & Sutcliffe, A. Health of IVM children. J Assist Reprod Genet 28, 489-493 (2011).
4. Racowsky, C. et al. Standardization of grading embryo morphology. Fertil Steril 94, 1152-1153 (2010).
5. Bar-Yoseph,H. et al.Morphological embryo assessment: reevaluation. Fertil Steril 95, 1624-1628 (2011).
6. Montag, M., Liebenthron, J. & Koster, M. Which morphological scoring system is relevant in human embryo development? Placenta 32, S252-256 (2011).
7. Yakut, T., Karkucak, M., Sher, G. & Keskintepe, L. Comparison of aneuploidy frequencies between in vitro matured and unstimulated cycles oocytes by metaphase comparative genomic hybridization (mCGH). Mol Biol Rep 39, 6187-6191 (2012).
8. Zhang, X. Y. et al. Chromosome abnormality rates in human embryos obtained from in-vitro maturation and IVF treatment cycles. Reprod Biomed Online 21, 552-559 (2010).
9. Hassold, T., Hall, H. & Hunt, P. The origin of human aneuploidy: where we have been, where we are going. Hum Mol Genet 16, R203-208 (2007).
10. Mehta, R. H., Sridhar, H., Vijay Kumar, B. R. & Anand Kumar, T. C. High incidence of oligozoospermia and teratozoospermia in human semen infected with the aerobic bacterium Streptococcus faecalis. Reprod Biomed Online 5, 17-21 (2002).
11. Qiao, J. et al. The root of reduced fertility in aged women and possible therapentic options: Current status and future perspects. Mol Aspects Med 38, 54-85 (2014).
12. Fragouli, E. & Wells, D. Aneuploidy screening for embryo selection. Semin Reprod Med 30, 289-301 (2012).
13. Lamb, N. E., Sherman, S. L. & Hassold, T. J. Effect of meiotic recombination on the production of aneuploid gametes in humans. Cytogenet Genome Res 111, 250-255 (2005).
14. Hodges, C. A., LeMaire-Adkins, R. & Hunt, P. A. Coordinating the segregation of sister chromatids during the first meiotic division: evidence for sexual dimorphism. J Cell Sci 114, 2417-2426 (2001).
15. Fragouli, E. et al. The origin and impact of embryonic aneuploidy. Hum Genet 132, 1001-1013 (2013).
16. Sgura, A. et al. Micronuclei, centromere-positive micronuclei and chromosome nondisjunction in cytokinesis blocked human lymphocytes following mitomycin C or vincristine treatment. Mutat Res 392, 97-107 (1997).
17. Kamino, H. et al. B-cell linker protein prevents aneuploidy by inhibiting cytokinesis. Cancer Sci 99, 2444-2454 (2008).
18. Rosario, C. O. et al. Plk4 is required for cytokinesis and maintenance of chromosomal stability. Proc Natl Acad Sci U S A 107, 6888-6893 (2010).
19. Salem, H. et al. Nek7 kinase targeting leads to early mortality, cytokinesis disturbance and polyploidy. Oncogene 29, 4046-4057 (2010).
20. Gisselsson, D. et al. Generation of trisomies in cancer cells by multipolar mitosis and incomplete cytokinesis. Proc Natl Acad Sci U S A 107, 20489-20493 (2010).
21. Hognas, G. et al. Cytokinesis failure due to derailed integrin traffic induces aneuploidy and oncogenic transformation in vitro and in vivo. Oncogene 31, 3597-3606 (2012).
22. Hayashi, M. T. & Karlseder, J. DNA damage associated with mitosis and cytokinesis failure. Oncogene 32, 4593-4601 (2013).
23. Dobson, A. T. et al. The unique transcriptome through day 3 of human preimplantation development. Hum Mol Genet 13, 1461-1470 (2004).
24. Requena, A. et al. The impact of in-vitro maturation of oocytes on aneuploidy rate. Reprod Biomed Online 18, 777-783 (2009).
25. Chen, R. et al. Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell 148, 1293-1307 (2012).
26. Yan, L. et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 20, 1131-1139 (2013).
27. Tang, F. et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6, 377-382 (2009).
28. Xue, Z. et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500, 593-597 (2013).
29. Liu, N., Liu, L. & Pan, X. Single-cell analysis of the transcriptome and its application in the characterization of stem cells and early embryos. Cell Mol Life Sci 71, 2707-2715 (2014).
30. Nothias, J. Y., Majumder, S., Kaneko, K. J. & DePamphilis, M. L. Regulation of gene expression at the beginning of mammalian development. J Biol Chem 270, 22077-22080 (1995).
31. Terasawa, M. et al. Caenorhabditis elegans ortholog of the p24/p22 subunit, DNC-3, is essential for the formation of the dynactin complex by bridging DNC-1/ p150(Glued) and DNC-2/dynamitin. Genes Cells 15, 1145-1157 (2010).
32. Hammesfahr, B. & Kollmar, M. Evolution of the eukaryotic dynactin complex, the activator of cytoplasmic dynein. BMC Evol Biol 12, 95 (2012).
33. Abba, M. C. et al. Breast cancer molecular signatures as determined by SAGE: correlation with lymph node status. Mol Cancer Res 5, 881-890 (2007).
34. Elias, S. et al. Huntingtin regulates mammary stem cell division and differentiation. Stem Cell Reports 2, 491-506 (2014).
35. Ikenaka, K. et al. dnc-1/dynactin 1 knockdown disrupts transport of autophagosomes and induces motor neuron degeneration. PLoS One 8, e54511 (2013).
36. Payne, C., Rawe, V., Ramalho-Santos, J., Simerly, C. & Schatten, G. Preferentially localized dynein and perinuclear dynactin associate with nuclear pore complex proteins tomediate genomic union duringmammalian fertilization. J Cell Sci 116, 4727-4738 (2003).
37. Echeverri, C. J., Paschal, B. M., Vaughan, K. T. & Vallee, R. B. Molecular characterization of the 50-kD subunit of dynactin reveals function for the complex in chromosome alignment and spindle organization during mitosis. J Cell Biol 132, 617-633 (1996).
38. Yeh, T. Y. et al.Dynactin helps target Polo-like kinase 1 to kinetochores via its left-handed beta-helical p27 subunit. EMBO J 32, 1023-1035 (2013).
39. Lee, K. S., Oh, D. Y., Kang, Y. H. & Park, J. E. Self-regulated mechanism of Plk1 localization to kinetochores: lessons from the Plk1-PBIP1 interaction. Cell Div 3, 4 (2008).
40. Lane, H. A. & Nigg, E. A. Antibody microinjection reveals an essential role for human polo-like kinase 1 (Plk1) in the functional maturation of mitotic centrosomes. J Cell Biol 135, 1701-1713 (1996).
41. Terasawa, M. et al. Caenorhabditis elegans ortholog of the p24/p22 subunit, DNC-3, is essential for the formation of the dynactin complex by bridging DNC-1/p150(Glued) and DNC-2/dynamitin. Genes Cells 15, 1145-1157 (2010).
42. Melkonian, K. A., Maier, K. C., Godfrey, J. E., Rodgers, M. & Schroer, T. A. Mechanism of dynamitin-mediated disruption of dynactin. J Biol Chem 282, 19355-19364 (2007).
43. Luo, J. et al. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 137, 835-848 (2009).
44. Lu, L. Y. & Yu, X. The balance of Polo-like kinase 1 in tumorigenesis. Cell Div 4, 4 (2009).
45. Arnaud, L., Pines, J. & Nigg, E. A. GFP tagging reveals human Polo-like kinase 1 at the kinetochore/centromere region of mitotic chromosomes. Chromosoma 107, 424-429 (1998).
46. Xu, Y.W. et al. High follicle-stimulating hormone increases aneuploidy in human oocytes matured in vitro. Fertil Steril 95, 99-104 (2011).
47. Jones, K. T. & Lane, S. I. Molecular causes of aneuploidy in mammalian eggs. Development 140, 3719-3730 (2013).
48. Nagaoka, S. I., Hodges, C. A., Albertini, D. F. & Hunt, P. A. Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr Biol 21, 651-657 (2011).
49. Anckaert, E., De Rycke, M. & Smitz, J. Culture of oocytes and risk of imprinting defects. Hum Reprod Update 19, 52-66 (2013).
50. El Hajj, N. & Haaf, T. Epigenetic disturbances in in vitro cultured gametes and embryos: implications for human assisted reproduction. Fertil Steril 99, 632-641 (2013).
51. Eppig, J. J. & Downs, S. M. Chemical signals that regulate mammalian oocyte maturation. Biol Reprod 30, 1-11 (1984).
52. Younis, A. I., Brackett, B. G. & Fayrer-Hosken, R. A. Influence of serum and hormones on bovine oocyte maturation and fertilization in vitro. Gamete Res 23, 189-201 (1989).
53. Yu, Y. et al. Optimal timing of oocyte maturation and its relationship with the spindle assembly and developmental competence of in vitro matured human oocytes. Fertil Steril 96, 73-78 e71 (2011).
54. Assou, S. et al. The human cumulus - oocyte complex gene-expression profile. Hum Reprod 21, 1705-1719 (2006).
55. Wang, L., Feng, Z., Wang, X. & Zhang, X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136-138 (2010).
56. Yu, Y. et al . Effects of combined epidermal growth factor, brain-derived neurotrophic factor and insulin-like growth factor-1 on human oocyte maturation and early fertilized and cloned embryo development. Hum Reprod 27, 2146-2159 (2012).
57. Fan, Y. et al. Improved efficiency of microsurgical enucleated tripronuclear zygotes development and embryonic stem cell derivation by supplementing epidermal growth factor, brain-derived neurotrophic factor, and insulin-like growth factor-1. Stem Cells Dev 23, 563-575 (2014).