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Hyper-polyploid embryos survive after implantation in mice

Published online by Cambridge University Press:  10 March 2020

Hiroyuki Imai ,
Tokuko Iwamori ,
Ken Takeshi Kusakabe ,
Yasuo Kiso ,
Etsuro Ono  and
Kiyoshi Kano Open the ORCID record for Kiyoshi Kano [Opens in a new window]
Hiroyuki Imai
Affiliation:
Department of Biomedicine, Graduate School of Medical Science, Kyushu University, Fukuoka, Japan Laboratory of Veterinary Developmental Biology, United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi, Japan
Tokuko Iwamori
Affiliation:
Department of Biomedicine, Graduate School of Medical Science, Kyushu University, Fukuoka, Japan
Ken Takeshi Kusakabe
Affiliation:
Laboratory of Veterinary Anatomy, United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi, Japan
Yasuo Kiso
Affiliation:
Laboratory of Veterinary Anatomy, United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi, Japan
Etsuro Ono
Affiliation:
Department of Biomedicine, Graduate School of Medical Science, Kyushu University, Fukuoka, Japan
Kiyoshi Kano*
Affiliation:
Laboratory of Veterinary Developmental Biology, United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi, Japan
*
Author for correspondence: Kiyoshi Kano, Laboratory of Veterinary Developmental Biology, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1, Yoshida, Yamaguchi City, Yamaguchi Prefecture, Japan. Tel: +81 83 933 5883. E-mail: [email protected]
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Summary

Polyploids generated by natural whole genome duplication have served as a dynamic force in vertebrate evolution. As evidence for evolution, polyploid organisms exist generally, however there have been no reports of polyploid organisms in mammals. In mice, polyploid embryos under normal culture conditions normally develop to the blastocyst stage. Nevertheless, most tetraploid embryos degenerate after implantation, indicating that whole genome duplication produces harmful effects on normal development in mice. Most previous research on polyploidy has mainly focused on tetraploid embryos. Analysis of various ploidy outcomes is important to comprehend the effects of polyploidization on embryo development. The purpose of this present study was to discover the extent of the polyploidization effect on implantation and development in post-implantation embryos. This paper describes for the first time an octaploid embryo implanted in mice despite hyper-polyploidization, and indicates that these mammalian embryos have the ability to implant, and even develop, despite the harmfulness of extreme whole genome duplication.

Keywords

EmbryoImplantationMouseOctaploidPolyploid
Type
Short Communication
Information
Zygote , Volume 28 , Issue 3 , June 2020 , pp. 247 - 249
Copyright
© Cambridge University Press 2020

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References

Eakin, GS and Behringer, RR (2003) Tetraploid development in the mouse. Dev Dyn 228, 751–66.CrossRefGoogle ScholarPubMed
Eakin, GS, Hadjantonakis, AK, Papaioannou, VE and Behringer, RR (2005) Developmental potential and behavior of tetraploid cells in the mouse embryo. Dev Biol 228, 150–9.CrossRefGoogle Scholar
Gazzo, E, Pena, F, Valdez, F, Chung, A, Velit, M, Ascenzo, M and Escudero, E (2019) Blastocyst contractions are strongly related with aneuploidy, lower implantation rates, and slow-cleaving embryos: a time lapse study. JBRA Assist Reprod doi: 10.5935/1518-0557.20190053. [Epub ahead of print]CrossRefGoogle Scholar
Graham, CF (1970) Parthenogenetic mouse blastocysts. Nature 226, 165–7.CrossRefGoogle ScholarPubMed
Holland, PW, Garcia-Fernandez, J, Williams, NA and Sidow, A (1994) Gene duplications and origins of vertebrate development. Dev Suppl 1994, 125–33.Google Scholar
Horii, T, Yamamoto, M, Morita, S, Kimura, M, Nagao, Y and Hatada, I (2015) p53 supresses tetraploid development in mice. Sci Rep 5, 8907.CrossRefGoogle Scholar
Hu, M, Zhao, Z, TuanMu, LC, Wei, H, Gao, H, Li, L, Ying, J and Zhang, S (2015) Analysis of imprinted gene expression and implantation in haploid androgenetic mouse embryos. Andrologia 47, 102–8.CrossRefGoogle ScholarPubMed
Imai, H, Kano, K, Fujii, W, Takasawa, K, Wakitani, S, Hiyama, M, Nishino, K, Kusakabe, KT and Kiso, Y (2015) Tetraploid embryonic stem cells maintain pluripotency and differentiation potency into three germ layers. PLoS One 10, e0130585.CrossRefGoogle ScholarPubMed
Imai, H, Fujii, W, Kusakabe, KT, Kiso, Y and Kano, K (2019) Aggregation recovers developmental plasticity in mouse polyploid embryos. Reprod Fertil Dev 31, 404–11.CrossRefGoogle ScholarPubMed
Jiao, Y, Wichett, NJ, Ayyampalayam, S, Chanderbali, AS, Landherr, L, Ralph, PE, Tomsho, LP, Hu, Y, Liang, H, Soltis, PS, Soltis, DE, Clifton, SW, Schlarbaum, SE, Schuster, SC, Ma, H, Leebens-Mack, J and dePamphilis, CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100.CrossRefGoogle ScholarPubMed
Kawaguchi, J, Kano, K and Naito, K (2009) Expression profiling of tetraploid mouse embryos in developmental stages using a cDNA microarray analysis. J Reprod Dev 55, 670–5.CrossRefGoogle ScholarPubMed
Kawai, S, Takagi, Y, Kaneko, S and Kunosawa, T (2011) Effect of three types of mixed anesthetic agents alternate of ketamine in mice. Exp Anim 60, 481–7.CrossRefGoogle ScholarPubMed
Kukharenko, VI (2018) Disturbance of the epithelial-mesenchymal transition as a cause of the defective development of human spontaneous abortions with abnormal karyotype. Bull Exp Biol Med 165, 581–3.CrossRefGoogle ScholarPubMed
Lei, L, Guan, N, Zu, YN, Zhang, QH, Shen, JL and Jin, LH (2009) Developmental pattern of hexaploidy mouse embryos produced by blastomere fusion of diploid and tetraploid embryos at the 2-cell stage. Zygote 17, 125–30.CrossRefGoogle Scholar
Liu, L, Czerwiec, E and Keefe, DL (2004) Effect of ploidy and parental genome composition on expression of Oct-4 protein in mouse embryos. Gene Expr Patterns 4, 433–41.CrossRefGoogle ScholarPubMed
Ohno, S (1970) Evolution by gene duplication. Springer, Berlin, Heidelberg.CrossRefGoogle Scholar
Olzer, S, Ersoy, AO, Oztas, E, Topcu, V, Celen, S and Danisman, N (2015) The unprecedented recurrent diploid/tetraploid mosaicism of trisomy-18 (mixoploidy; 4n+18/2n+18): clinical report. Am J Med Genet A 167, 1650–3.Google Scholar
Panopoulou, G and Poustka, AJ (2005) Timing and mechanism of ancient vertebrate genome duplication -the adventure of hypothesis. Trends Genet 21, 559–67.CrossRefGoogle ScholarPubMed
Park, MR, Hwang, KC, Bui, HT, Cho, SG, Park, C, Oh, JW and Kim, JH (2012) Altered gene expression profiles in mouse tetraploid blastocysts. J Reprod Dev 58, 344–52.CrossRefGoogle ScholarPubMed
Robertson, SA, Care, AS and Moldenhauer, LM (2018) Regulatory T cells in embryo implantation and the immune response to pregnancy. J Clin Invest 128, 4224–35.CrossRefGoogle Scholar
Schmid, M, Steinlein, C, Tian, Q, Hanlon Newell, AE, Gessler, M, Olson, SB, Rosenwald, A, Kneitz, B and Fedorov, LM (2014) Mosaic variegated aneuploidy in mouse BubR1 deficeint embryos and pregnancy loss in human. Chromosome Res 22, 375–92.CrossRefGoogle Scholar
Selmecki, AM, Maruvka, YE, Richmond, PA, Guillet, M, Shoresh, N, Sorenson, AL, De, S, Kishony, R, Michor, F, Dowell, R and Pellman, D (2015) Polyploidy can drive rapid adaptation in yeast. Nature 519, 349–52.CrossRefGoogle ScholarPubMed
Wen, B, Li, R, Cheng, K, Li, E, Zhang, S, Xiang, J, Wang, Y and Han, J (2017) Tetraploid embryonic stem cells can contribute to the development of chimeric fetuses and chimeric extraembryonic tissues. Sci Rep 7, 3030.CrossRefGoogle ScholarPubMed
Wu, BJ, Zhao, LX, Zhu, CC, Chen, YL, Wei, MY, Bao, SQ, Sun, SC and Li, XH (2017) Altered apoptosis/autophagy and epigenetic modifications cause the impaired postimplantation octaploid embryonic development in mice. Cell Cycle 16, 82–90.CrossRefGoogle ScholarPubMed