Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-19T03:03:03.913Z Has data issue: false hasContentIssue false
  • English
  • Français

Restricted development of mouse triploid fetuses with disorganized expression of imprinted genes

Published online by Cambridge University Press:  16 October 2014

Wataru Yamazaki ,
Masashi Takahashi  and
Manabu Kawahara
Wataru Yamazaki
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo 060–8589, Japan.
Masashi Takahashi
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo 060–8589, Japan.
Manabu Kawahara*
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo 060–8589, Japan. Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo 060–8589, Japan.
*
All correspondence to: Manabu Kawahara. Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo 060–8589, Japan. Tel:/Fax: +81 11 706 2541. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Eukaryotic species commonly contain a diploid complement of chromosomes. The diploid state appears to be advantageous for mammals because it enables sexual reproduction and facilitates genetic recombination. Nonetheless, the effects of DNA ploidy on mammalian ontogeny have yet to be understood. The present study shows phenotypic features and expression patterns of imprinted genes in tripronucleate diandric and digynic triploid (DAT and DGT) mouse fetuses on embryonic day 10.5 (E10.5). Measurement of crown–rump length revealed that the length of DGT fetuses (1.87 ± 0.13 mm; mean ± standard error of the mean) was much smaller than that of diploid fetuses (4.81 ± 0.05 mm). However, no significant difference was observed in the crown–rump length between diploid and DAT fetuses (3.86 ± 0.43 mm). In DGT fetuses, the expression level of paternally expressed genes, Igf2, Dlk1, Ndn, and Peg3, remained significantly reduced and that of maternally expressed genes, Igf2r and Grb10, increased. Additionally, in DAT fetuses, the Igf2 mRNA expression level was approximately twice that in diploid fetuses, as expected. These results provide the first demonstration that imprinted genes in mouse triploid fetuses show distinctive expression patterns independent of the number of parental-origin haploid sets. These data suggest that both DNA ploidy and asymmetrical functions of parental genomes separately influence mammalian ontogeny.

Keywords

Fetal growthGene expressionGenomic imprintingTriploid
Type
Research Article
Information
Zygote , Volume 23 , Issue 6 , December 2015 , pp. 874 - 884
Copyright
Copyright © Cambridge University Press 2014 

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

Arvidsson, C.G., Hamberg, H., Johnsson, H., Myrdal, U., Anneren, G. & Brun, A. (1986). A boy with complete triploidy and unusually long survival. Acta Paediatr. Scand. 75, 507–10.CrossRefGoogle ScholarPubMed
Beatty, R.A. (1978). The origin of human triploidy: an integration of qualitative and quantitative evidence. Ann. Hum. Genet. 41, 299–314.CrossRefGoogle ScholarPubMed
Birger, Y., Shemer, R., Perk, J. & Razin, A. (1999). The imprinting box of the mouse Igf2r gene. Nature 397, 84–8.CrossRefGoogle ScholarPubMed
Broad, K.D., Curley, J.P. & Keverne, E.B. (2009). Increased apoptosis during neonatal brain development underlies the adult behavioral deficits seen in mice lacking a functional paternally expressed gene 3 (Peg3). Dev. Neurobiol. 69, 314–25.CrossRefGoogle ScholarPubMed
Brodsky, W.Y. & Uryvaeva, I.V. (1977). Cell polyploidy: its relation to tissue growth and function. Int. Rev. Cytol. 50, 275–332.CrossRefGoogle Scholar
Carr, D.H. (1971a). Chromosome studies in selected spontaneous abortions. Polyploidy in man. J. Med. Genet. 8, 164–74.CrossRefGoogle ScholarPubMed
Carr, D.H. (1971b). Genetic basis of abortion. Annu. Rev. Genet. 5, 65–80.CrossRefGoogle ScholarPubMed
Carriere, R. (1969). The growth of liver parenchymal nuclei and its endocrine regulation. Int. Rev. Cytol. 25, 201–77.CrossRefGoogle ScholarPubMed
Charalambous, M., Smith, F.M., Bennett, W.R., Crew, T.E., Mackenzie, F. & Ward, A. (2003). Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc. Natl. Acad. Sci. USA 100, 8292–7.CrossRefGoogle ScholarPubMed
Cuellar, O. & Uyeno, T. (1972). Triploidy in rainbow trout. Cytogenetics 11, 508–15.CrossRefGoogle ScholarPubMed
DeChiara, T.M., Efstratiadis, A. & Robertson, E.J. (1990). A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345, 78–80.CrossRefGoogle Scholar
DeChiara, T.M., Robertson, E.J. & Efstratiadis, A. (1991). Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64, 849–59.CrossRefGoogle ScholarPubMed
Doherty, A.S., Mann, M.R., Tremblay, K.D., Bartolomei, M.S. & Schultz, R.M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–35.CrossRefGoogle ScholarPubMed
Fryns, J.P., van de Kerckhove, A., Goddeeris, P. & van den Berghe, H. (1977). Unusually long survival in a case of full triploidy of maternal origin. Hum. Genet. 38, 147–55.CrossRefGoogle Scholar
Hasegawa, T., Harada, N., Ikeda, K., Ishii, T., Hokuto, I., Kasai, K., Tanaka, M., Fukuzawa, R., Niikawa, N. & Matsuo, N. (1999). Digynic triploid infant surviving for 46 days. Am. J. Med. Genet. 87, 306–10.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Henery, C.C. & Kaufman, M.H. (1992). Cleavage rate of diandric triploid mouse embryos during the preimplantation period. Mol. Reprod. Dev. 32, 251–8.CrossRefGoogle ScholarPubMed
Ilgren, E.B. (1980). Polyploidization of extraembryonic tissues during mouse embryogenesis. J. Embryol. Exp. Morphol. 59, 103–11.Google ScholarPubMed
Iliopoulos, D., Vassiliou, G., Sekerli, E., Sidiropoulou, V., Tsiga, A., Dimopoulou, D. & Voyiatzis, N. (2005). Long survival in a 69,XXX triploid infant in Greece. Genet. Mol. Res. 4, 755–9.Google Scholar
Jacobs, P.A., Angell, R.R., Buchanan, I.M., Hassold, T.J., Matsuyama, A.M. & Manuel, B. (1978). The origin of human triploids. Ann. Hum. Genet. 42, 49–57.CrossRefGoogle ScholarPubMed
Kaufman, M.H. & Speirs, S. (1987). The postimplantation development of spontaneous digynic triploid embryos in LT/Sv strain mice. Development 101, 383–91.CrossRefGoogle ScholarPubMed
Kaufman, M.H. & Webb, S. (1990). Postimplantation development of tetraploid mouse embryos produced by electrofusion. Development 110, 1121–32.CrossRefGoogle ScholarPubMed
Kaufman, M.H., Lee, K.K. & Speirs, S. (1989a). Influence of diandric and digynic triploid genotypes on early mouse embryogenesis. Development 105, 137–45.CrossRefGoogle ScholarPubMed
Kaufman, M.H., Speirs, S. & Lee, K.K. (1989b). The sex-chromosome constitution and early postimplantation development of diandric triploid mouse embryos. Cytogenet. Cell Genet. 50, 98–101.CrossRefGoogle ScholarPubMed
Kim, J., Ekram, M.B., Kim, H., Faisal, M., Frey, W.D., Huang, J.M., Tran, K., Kim, M.M. & Yu, S. (2012). Imprinting control region (ICR) of the Peg3 domain. Hum. Mol. Genet. 21, 2677–87.CrossRefGoogle ScholarPubMed
Kono, T., Sotomaru, Y., Sato, Y. & Nakahara, T. (1993). Development of androgenetic mouse embryos produced by in vitro fertilization of enucleated oocytes. Mol. Reprod. Dev. 34, 43–6.CrossRefGoogle ScholarPubMed
Li, E., Beard, C. & Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature 366, 362–5.CrossRefGoogle ScholarPubMed
Li, L., Keverne, E.B., Aparicio, S.A., Ishino, F., Barton, S.C. & Surani, M.A. (1999). Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 284, 330–3.CrossRefGoogle ScholarPubMed
Lin, S.P., Youngson, N., Takada, S., Seitz, H., Reik, W., Paulsen, M., Cavaille, J. & Ferguson-Smith, A.C. (2003). Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat. Genet. 35, 97–102.CrossRefGoogle ScholarPubMed
Lu, T.Y. & Markert, C.L. (1980). Manufacture of diploid/tetraploid chimeric mice. Proc. Natl. Acad. Sci. USA 77, 6012–6.CrossRefGoogle ScholarPubMed
Ludwig, T., Eggenschwiler, J., Fisher, P., D’Ercole, A.J., Davenport, M.L. & Efstratiadis, A. (1996). Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev. Biol. 177, 517–35.CrossRefGoogle ScholarPubMed
McGrath, J. & Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179–83.CrossRefGoogle ScholarPubMed
McKinnell, R.G. (1964). Expression of the kandiyohi gene in triploid frogs produced by nuclear transplantation. Genetics 49, 895–903.CrossRefGoogle ScholarPubMed
Moon, Y.S., Smas, C.M., Lee, K., Villena, J.A., Kim, K.H., Yun, E.J. & Sul, H.S. (2002). Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol. Cell. Biol. 22, 5585–92.CrossRefGoogle ScholarPubMed
Nagatomo, H., Kagawa, S., Kishi, Y., Takuma, T., Sada, A., Yamanaka, K., Abe, Y., Wada, Y., Takahashi, M., Kono, T. & Kawahara, M. (2013). Transcriptional wiring for establishing cell lineage specification at the blastocyst stage in cattle. Biol. Reprod. 88, 158.CrossRefGoogle ScholarPubMed
Niebuhr, E. (1974). Triploidy in man. Cytogenetical and clinical aspects. Humangenetik 21, 103–25.Google ScholarPubMed
Niemann-Seyde, S.C., Rehder, H. & Zoll, B. (1993). A case of full triploidy (69,XXX) of paternal origin with unusually long survival time. Clin. Genet. 43, 79–82.CrossRefGoogle Scholar
Obata, Y. & Kono, T. (2002). Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 277, 5285–9.CrossRefGoogle Scholar
Ogawa, H., Wu, Q., Komiyama, J., Obata, Y. & Kono, T. (2006). Disruption of parental-specific expression of imprinted genes in uniparental fetuses. FEBS Lett. 580, 5377–84.CrossRefGoogle ScholarPubMed
Pagliardini, S., Ren, J., Wevrick, R. & Greer, J.J. (2005). Developmental abnormalities of neuronal structure and function in prenatal mice lacking the Prader-Willi syndrome gene necdin. Am. J. Pathol. 167, 175–91.CrossRefGoogle ScholarPubMed
Quinn, P., Barros, C. & Whittingham, D.G. (1982). Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. J. Reprod. Fertil. 66, 161–8.CrossRefGoogle ScholarPubMed
Quinn, P., Kerin, J.F. & Warnes, G.M. (1985). Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid. Fertil. Steril. 44, 493–8.CrossRefGoogle Scholar
Saito, M., Takada, K., Yamada, T. & Fujimoto, J. (1996). Overexpression of granulocyte colony-stimulating factor in vivo decreases the level of polyploidization of mouse bone marrow megakaryocytes. Stem Cells 14, 124–31.CrossRefGoogle ScholarPubMed
Sato, A., Otsu, E., Negishi, H., Utsunomiya, T. & Arima, T. (2007). Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum. Reprod. 22, 26–35.CrossRefGoogle ScholarPubMed
Sherard, J., Bean, C., Bove, B., DelDuca, V. Jr., Esterly, K.L., Karcsh, H.J., Munshi, G., Reamer, J.F., Suazo, G., Wilmoth, D. & et al. (1986). Long survival in a 69,XXY triploid male. Am. J. Med. Genet. 25, 307–12.CrossRefGoogle Scholar
Shiura, H., Nakamura, K., Hikichi, T., Hino, T., Oda, K., Suzuki-Migishima, R., Kohda, T., Kaneko-ishino, T. & Ishino, F. (2009). Paternal deletion of Meg1/Grb10 DMR causes maternalization of the Meg1/Grb10 cluster in mouse proximal chromosome 11 leading to severe pre- and postnatal growth retardation. Hum. Mol. Genet. 18, 1424–38.CrossRefGoogle ScholarPubMed
Sotomaru, Y., Katsuzawa, Y., Hatada, I., Obata, Y., Sasaki, H. & Kono, T. (2002). Unregulated expression of the imprinted genes H19 and Igf2r in mouse uniparental fetuses. J. Biol. Chem. 277, 12474–8.CrossRefGoogle ScholarPubMed
Speirs, S. & Kaufman, M.H. (1989). Analysis of the sex-chromosome constitution of digynic triploid mouse embryos. Cytogenet. Cell Genet. 52, 151–3.CrossRefGoogle ScholarPubMed
Suemori, H., Takahashi, N. & Noguchi, S. (1995). Hoxc-9 mutant mice show anterior transformation of the vertebrae and malformation of the sternum and ribs. Mech. Dev. 51, 265–73.CrossRefGoogle ScholarPubMed
Surani, M.A., Barton, S.C. & Norris, M.L. (1984). Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548–50.CrossRefGoogle ScholarPubMed
Surani, M.A., Barton, S.C. & Norris, M.L. (1986). Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell 45, 127–36.CrossRefGoogle ScholarPubMed
Suwinska, A., Ozdzenski, W., Waksmundzka, M. & Tarkowski, A.K. (2005). Experimentally produced diploid-triploid mouse chimaeras develop up to adulthood. Mol. Reprod. Dev. 72, 362–76.CrossRefGoogle ScholarPubMed
Takagi, N. & Sasaki, M. (1976). Digynic triploidy after superovulation in mice. Nature 264, 278–81.CrossRefGoogle ScholarPubMed
Thorvaldsen, J.L., Duran, K.L. & Bartolomei, M.S. (1998). Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12, 3693–702.CrossRefGoogle ScholarPubMed
Verona, R.I., Thorvaldsen, J.L., Reese, K.J. & Bartolomei, M.S. (2008). The transcriptional status but not the imprinting control region determines allele-specific histone modifications at the imprinted H19 locus. Mol. Cell. Biol. 28, 71–82.CrossRefGoogle Scholar
Whittingham, D.G. (1971). Culture of mouse ova. J. Reprod. Fertil. Suppl. 14, 7–21.Google ScholarPubMed
Yang, T., Adamson, T.E., Resnick, J.L., Leff, S., Wevrick, R., Francke, U., Jenkins, N.A., Copeland, N.G. & Brannan, C.I. (1998). A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat. Genet. 19, 25–31.CrossRefGoogle ScholarPubMed
Supplementary material: File

Yamazaki Supplementary Material

Appendix

Download Yamazaki Supplementary Material(File)
File 42.5 KB