Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-17T17:56:38.817Z Has data issue: false hasContentIssue false
  • English
  • Français

Mouse embryonic stem cells maintain differentiation potency into somatic lineage despite alternation of ploidy

Published online by Cambridge University Press:  31 March 2022

Hiroyuki Imai ,
Wataru Fujii ,
Ken Takeshi Kusakabe ,
Yasuo Kiso  and
Kiyoshi Kano Open the ORCID record for Kiyoshi Kano [Opens in a new window]
Hiroyuki Imai
Affiliation:
Laboratory of Veterinary Anatomy, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan Laboratory of Veterinary Developmental Biology, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan
Wataru Fujii
Affiliation:
Laboratory of Applied Genetics, Graduate School of Agricultural and Life Science, The University of Tokyo, Tokyo, Japan
Ken Takeshi Kusakabe
Affiliation:
Laboratory of Veterinary Anatomy, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan
Yasuo Kiso
Affiliation:
Laboratory of Veterinary Anatomy, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan
Kiyoshi Kano*
Affiliation:
Laboratory of Veterinary Developmental Biology, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan
*
Author for correspondence: Kiyoshi Kano. Laboratory of Veterinary Developmental biology, Joint faculty of Veterinary Medicine, Yamaguchi University. 1677-1, Yoshida, Yamaguchi, 753-0841, Japan. Tel: +81 83 933 5883. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Vertebrates, including mammals, are considered to have evolved by whole genome duplications. Although some fish have been reported to be polyploids that have undergone additional genome duplication, there have been no reports of polyploid mammals due to abnormal development after implantation. Furthermore, as the number of physiologically existing tetraploid somatic cells is small, details of the functions of these ploidy-altered cells are not fully understood. In this present study, we aimed to clarify the details of the differentiation potency of tetraploids using tetraploid embryonic stem cells. To clarify the differentiation potency, we used mouse tetraploid embryonic stem cells derived from tetraploid embryos. We presented tetraploid embryonic stem cells differentiated into neural and osteocyte lineage in vitro and tetraploid cells that contributed to various tissues of chimeric embryos ubiquitously in vivo. These results revealed that mouse embryonic stem cells maintain differentiation potency after altering the ploidy. Our results provide an important basis for the differentiation dynamics of germ layers in mammalian polyploid embryogenesis.

Keywords

DifferentiationMouse embryonic stem cellsPloidyTetraploid
Type
Research Article
Information
Zygote , Volume 30 , Issue 4 , August 2022 , pp. 480 - 486
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anatskaya, O. V. and Vinogradov, A. E. (2010). Somatic polyploidy promotes cell function under stress and energy depletion: Evidence from tissue-specific mammal transcriptome. Functional and Integrative Genomics, 10(4), 433–446. doi: 10.1007/s10142-010-0180-5 CrossRefGoogle ScholarPubMed
Brodsky, V. Y. and Uryvaeva, I. V. (1985). Genome multiplication in growth and development: Biology of polyploid and polytene cells. Cambridge University Press.Google Scholar
Duncan, A. W., Taylor, M. H., Hickey, R. D., Hanlon Newell, A. E., Lenzi, M. L., Olson, S. B., Finegold, M. J. and Grompe, M. (2010). The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature, 467(7316), 707–710. doi: 10.1038/nature09414 CrossRefGoogle ScholarPubMed
Eakin, G. S., Hadjantonakis, A. K., Papaioannou, V. E. and Behringer, R. R. (2005). Developmental potential and behavior of tetraploid cells in the mouse embryo. Developmental Biology, 288(1), 150–159. doi: 10.1016/j.ydbio.2005.09.028 CrossRefGoogle ScholarPubMed
Elling, U., Taubenschmid, J., Wirnsberger, G., O’Malley, R., Demers, S. P., Vanhaelen, Q., Shukalyuk, A. I., Schmauss, G., Schramek, D., Schnuetgen, F., von Melchner, H., Ecker, J. R., Stanford, W. L., Zuber, J., Stark, A. and Penninger, J. M. (2011). Forward and reverse genetics through derivation of haploid mouse embryonic stem cells. Cell Stem Cell, 9(6), 563–574. doi: 10.1016/j.stem.2011.10.012 CrossRefGoogle ScholarPubMed
Fujikawa-Yamamoto, K., Miyagoshi, M., Luo, X. and Yamagishi, H. (2011). DNA-unstable decaploid mouse H1 (ES) cells established from DNA-stable pentaploid H1 (ES) cells polyploidized using demecolcine. Cell Proliferation, 44(2), 111–119. doi: 10.1111/j.1365-2184.2011.00734.x H1.CrossRefGoogle ScholarPubMed
Fujikawa-Yamamoto, K., Ota, T., Miyagoshi, M. and Yamagishi, H. (2012). Pluripotency of a polyploid H1 (ES) cell system without leukaemia inhibitory factor. Cell Proliferation, 45(2), 140–147. doi: 10.1111/j.1365-2184.2011.00805.x H1.CrossRefGoogle ScholarPubMed
Fujikawa-Yamamoto, K., Miyagoshi, M. and Yamagishi, H. (2013). Dodecaploid H1 embryonic stem cells abolished pluripotency in L15F10 medium both with and without leukemia inhibitory factor. Human Cell, 26(3), 97–104. doi: 10.1007/s13577-013-0063-x CrossRefGoogle ScholarPubMed
Gazzo, E., Peña, F., Valdéz, F., Chung, A., Velit, M., Ascenzo, M. and Escudero, E. (2020). Blastocyst contractions are strongly related with aneuploidy, lower implantation rates, and slow-cleaving embryos: A time lapse study. JBRA Assisted Reproduction, 24(1), 77–81. doi: 10.5935/1518-0557.20190053 Google ScholarPubMed
Hay, D. L. (1988). Placental histology and the production of human choriogonadotrophin and its subunits in pregnancy. British Journal of Obstetrics and Gynaecology, 95(12), 1268–1275. doi: 10.1111/j.1471-0528.1988.tb06817.x CrossRefGoogle ScholarPubMed
Holland, P. W. H., Garcia-Fernàndez, J., Williams, N. A. and Sidow, A. (1994). Gene duplications and the origins of vertebrate development. Development, 1994(Supplement), 125–133. doi: 10.1242/dev.1994.Supplement.125 CrossRefGoogle Scholar
Horii, T., Yamamoto, M., Morita, S., Kimura, M., Nagao, Y. and Hatada, I. (2015). p53 suppresses tetraploid development in mice. Scientific Reports, 5, 8907. doi: 10.1038/srep08907 CrossRefGoogle ScholarPubMed
Hu, D. and Cross, J. C. (2010). Development and function of trophoblast giant cells in the rodent placenta. International Journal of Developmental Biology, 54(2–3), 341–354. doi: 10.1387/ijdb.082768dh CrossRefGoogle ScholarPubMed
Imai, H., Kano, K., Fujii, W., Takasawa, K., Wakitani, S., Hiyama, M., Nishino, K., Kusakabe, K. T. and Kiso, Y. (2015). Tetraploid embryonic stem cells maintain pluripotency and differentiation potency into three germ layers. PLoS ONE, 10(6), e0130585. doi: 10.1371/journal.pone.0130585 CrossRefGoogle ScholarPubMed
Imai, H., Fujii, W., Kusakabe, K. T., Kiso, Y. and Kano, K. (2016). Effects of whole genome duplication on cell size and gene expression in mouse embryonic stem cells. Journal of Reproduction and Development, 62(6), 571–576. doi: 10.1262/jrd.2016-037 CrossRefGoogle ScholarPubMed
Imai, H., Fujii, W., Kusakabe, K. T., Kiso, Y. and Kano, K. (2019). Aggregation recovers developmental plasticity in mouse polyploid embryos. Reproduction, Fertility, and Development, 31(2), 404–411. doi: 10.1071/RD18093 CrossRefGoogle ScholarPubMed
Kaufman, M. H. and Webb, S. (1990). Postimplantation development of tetraploid mouse embryos produced by electrofusion. Development, 110(4), 1121–1132. doi: 10.1242/dev.110.4.1121 CrossRefGoogle ScholarPubMed
Kawaguchi, J., Kano, K. and Naito, K. (2009). Expression profiling of tetraploid mouse embryos in the developmental stages using a cDNA microarray analysis. Journal of Reproduction and Development, 55(6), 670–675. doi: 10.1262/jrd.09-127a CrossRefGoogle ScholarPubMed
Kondoh, H. and Takemoto, T. (2012). Axial stem cells deriving both posterior neural and mesodermal tissues during gastrulation. Current Opinion in Genetics and Development, 22(4), 374–380. doi: 10.1016/j.gde.2012.03.006 CrossRefGoogle ScholarPubMed
Leeb, M. and Wutz, A. (2011). Derivation of haploid embryonic stem cells from mouse embryos. Nature, 479(7371), 131–134. doi: 10.1038/nature10448 CrossRefGoogle ScholarPubMed
Liu, L., Czerwiec, E. and Keefe, D. L. (2004). Effect of ploidy and parental genome composition on expression of Oct-4 protein in mouse embryos. Gene Expression Patterns, 4(4), 433–441. doi: 10.1016/j.modgep.2004.01.004 CrossRefGoogle ScholarPubMed
López-Sánchez, N. and Frade, J. M. (2013). Genetic evidence for p75NTR-dependent tetraploidy in cortical projection neurons from adult mice. Journal of Neuroscience, 33(17), 7488–7500. doi: 10.1523/JNEUROSCI.3849-12.2013 CrossRefGoogle ScholarPubMed
MacKay, G. E. and West, J. D. (2005). Fate of tetraploid cells in 4n↔2n chimeric mouse blastocysts. Mechanisms of Development, 122(12), 1266–1281. doi: 10.1016/j.mod.2005.09.001 CrossRefGoogle ScholarPubMed
McGill, J. R., Lalley, P. J., Leach, R. J., Johnson, T. J. and Von Hoff, D. D. (1992). Chromosomal influence on hybrid cell proliferation. Cell Proliferation, 25(4), 345–355. doi: 10.1111/j.1365-2184.1992.tb01445.x CrossRefGoogle ScholarPubMed
Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J. C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America, 90(18), 8424–8428. doi: 10.1073/pnas.90.18.8424 CrossRefGoogle ScholarPubMed
Ohno, S. (1970). Evolution by gene duplication. Springer.CrossRefGoogle Scholar
Okada, Y., Matsumoto, A., Shimazaki, T., Enoki, R., Koizumi, A., Ishii, S., Itoyama, Y., Sobue, G. and Okano, H. (2008). Spatiotemporal recapitulation of central nervous system development by murine embryonic stem cell-derived neural stem/progenitor cells. Stem Cells, 26(12), 3086–3098. doi: 10.1634/stemcells.2008-0293 CrossRefGoogle ScholarPubMed
Panopoulou, G. and Poustka, A. J. (2005). Timing and mechanism of ancient vertebrate genome duplications – The adventure of a hypothesis. Trends in Genetics, 21(10), 559–567. doi: 10.1016/j.tig.2005.08.004 CrossRefGoogle ScholarPubMed
Park, M. R., Lee, A. R., Bui, H. T., Park, C., Park, K. K., Cho, S. G., Song, H., Kim, J. H., Nguyen, V. T. and Kim, J. H. (2011). Chromosome remodeling and differentiation of tetraploid embryos during preimplantation development. Developmental Dynamics, 240(7), 1660–1669. doi: 10.1002/dvdy.22653 CrossRefGoogle ScholarPubMed
Piferrer, F., Beaumont, A., Falguière, J. C., Flajšhans, M., Haffray, P. and Colombo, L. (2009). Polyploid fish and shellfish: Production, biology and applications to aquaculture for performance improvement and genetic containment. Aquaculture, 293(3–4), 125–156. doi: 10.1016/j.aquaculture.2009.04.036 CrossRefGoogle Scholar
Tada, M., Takahama, Y., Abe, K., Nakatsuji, N. and Tada, T. (2001). Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Current Biology, 11(19), 1553–1558. doi: 10.1016/s0960-9822(01)00459-6 CrossRefGoogle ScholarPubMed
Takemoto, T., Uchikawa, M., Yoshida, M., Bell, D. M., Lovell-Badge, R., Papaioannou, V. E. and Kondoh, H. (2011). Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature, 470(7334), 394–398. doi: 10.1038/nature09729 CrossRefGoogle ScholarPubMed
Von Hoff, D. D., Forseth, B., Clare, C. N., Hansen, K. L. and VanDevanter, D. (1990). Double minutes arise from circular extrachromosomal DNA intermediates which integrate into chromosomal sites in human HL-60 leukemia cells. Journal of Clinical Investigation, 85(6), 1887–1895. doi: 10.1172/JCI114650 CrossRefGoogle ScholarPubMed
Wang, M. J., Chen, F., Li, J. X., Liu, C. C., Zhang, H. B., Xia, Y., Yu, B., You, P., Xiang, D., Lu, L., Yao, H., Borjigin, U., Yang, G. S., Wangensteen, K. J., He, Z. Y., Wang, X. and Hu, Y. P. (2014). Reversal of hepatocyte senescence after continuous in vivo cell proliferation. Hepatology, 60(1), 349–361. doi: 10.1002/hep.27094 CrossRefGoogle ScholarPubMed
Wang, Z. Q., Kiefer, F., Urbánek, P. and Wagner, E. F. (1997). Generation of completely embryonic stem cell-derived mutant mice using tetraploid blastocyst injection. Mechanisms of Development, 62(2), 137–145. doi: 10.1016/s0925-4773(97)00655-2 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. Scientific Reports, 7(1), 3030. doi: 10.1038/s41598-017-02783-0 CrossRefGoogle Scholar
Wu, B. J., Zhao, L. X., Zhu, C. C., Chen, Y. L., Wei, M. Y., Bao, S. Q., Sun, S. C. and Li, X. H. (2017). Altered apoptosis/autophagy and epigenetic modifications cause the impaired postimplantation octaploid embryonic development in mice. Cell Cycle, 16(1), 82–90. doi: 10.1080/15384101.2016.1252884 CrossRefGoogle ScholarPubMed
Yamazaki, W., Amano, T., Bai, H., Takahashi, M. and Kawahara, M. (2016). The influence of polyploidy and genome composition on genomic imprinting in mice. Journal of Biological Chemistry, 291(40), 20924–20931. doi: 10.1074/jbc.M116.744144 CrossRefGoogle ScholarPubMed
Supplementary material: File

Imai et al. supplementary material

Figures S1-S3 and Table S1

Download Imai et al. supplementary material(File)
File 2.8 MB