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The genetic basis of XX-XY differences present before gonadal sex differentiation in the mouse
Abstract
There is now a substantial body of data showing that in eutherian mammals (mouse, rat, cow and man) XY conceptuses are developmentally more advanced (and consequently larger) than XX conceptuses of equivalent gestational age. This developmental difference is already discernible in the preimplantation period and it has been suggested that the more advanced development of XY embryos may be a consequence of the preimplantation expression of Y chromosomal genes such as Sry or Zfy. In the present paper sex-chromosomally variant mice were used to analyse the genetic basis of XX-XY differences as manifest at 10.5 days post coitum. The results show that the XX-XY difference is due to a combination of a Y chromosome effect and an effect of the difference in X chromosome constitution (2X v 1X). The Y effect is not dependent on the presence of Sry. In the light of this and other studies, it is concluded that the Y chromosome of most mouse strains carries a factor which accelerates preimplantation development and that the resulting developmental advantage is carried over into the postimplantation period. The retarding effect of two X chromosomes is then superimposed on this Y effect subsequent to the blastocyst stage but prior to 9.5 days post coitum.
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“Questions regarding the effects of X and Y gene imbalance have been explored over the past decade, and the data suggests that X and Y gene dose discrepancies account for several sex-biased phenotypes in the brain and periphery (Arnold, 2004; Arnold et al., 2016; Burgoyne et al., 1995).”
From Hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes: sex differences in regulation of stress responsivity (2017) · cites this paper as Burgoyne et al., 1995
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Cites
Male development of chromosomally female mice transgenic for Sry
Koopman, P. A., Gubbay, J., Vivian, N., Goodfellow, P. N., & Lovell-Badge, R. H. (1991) · Nature · doi:10.1038/351117a0 · Cited by 2,193
Gubbay, J., Collignon, J., Koopman, P. A., Capel, B., Economou, A., Münsterberg, A., Vivian, N., Goodfellow, P. N., & Lovell-Badge, R. H. (1990) · Nature · doi:10.1038/346245a0 · Cited by 1,675
Male sexual differentiation in mice lacking H–Y antigen
McLaren, A. L. D., Simpson, E., Tomonari, K., Chandler, P., & Hogg, H. (1984) · Nature · doi:10.1038/312552a0 · Cited by 225
Sex‐related differences in developmental rates of bovine embryos produced and cultured in vitro
Xu, K., Yadav, B. R., King, W. A., & BETTERIDGE, K. J. (1992) · Molecular Reproduction and Development · doi:10.1002/mrd.1080310404 · Cited by 209
Inverted repeat structure of the Sry locus in mice.
Gubbay, J., Vivian, N., Economou, A., Jackson, D., Goodfellow, P. N., & Lovell-Badge, R. H. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.17.7953 · Cited by 194
Altered sex ratio of live young after transfer of fast‐ and slow‐developing mouse embryos
Tsunoda, Y., Tokunaga, T., & SUGIE, T. (1985) · Gamete Research · doi:10.1002/mrd.1120120308 · Cited by 177
Evans, E. P., Burtenshaw, M. D., & Cattanach, B. M. (1982) · Nature · doi:10.1038/300443a0 · Cited by 176
Self-citationSex and development in bovine in-vitro fertilized embryos
Avery, B., Madison, V., & Greve, T. (1991) · Theriogenology · doi:10.1016/0093-691x(91)90306-x · Cited by 169
A Y-chromosomal effect on blastocyst cell number in mice
Burgoyne, P. S. (1993) · Development · doi:10.1242/dev.117.1.341 · Cited by 160
Self-citationMorphological development and sex of bovine in vitro‐fertilized embryos
Avery, B., Jørgensen, C. B., Madison, V., & Greve, T. (1992) · Molecular Reproduction and Development · doi:10.1002/mrd.1080320312 · Cited by 151
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- structure of the Srylocus in mice. Proc. natn. Acad. Sci. Reprod. Dev. 31 249-252.
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Metadata
- Authors
- Burgoyne, P. S., Thornhill, A. R., Boudrean, S. K., Darling, S. M., Bishop, C. E., & Evans, E. P.
- Affiliations
- National Institute for Medical Research (GB)
- MRC Mammalian Development Unit, Wolfson House, 4 Stephenson Way, London NW1 2HE, U. K.
- University College London (GB)
- Inserm (FR)
- MRC Radiobiology Unit, Chilton, Didcot, Oxon OX11 0RD, U. K.
- ORCID
- Burgoyne, P. S.
- Venue
- Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 1995-11-29
- Volume
- 350
- Issue
- 1333
- Pages
- 253-261
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- OpenAlex
- W2119156348
- Cited by
- 168
- References
- 37
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 5 · 2023: 8 · 2022: 3 · 2021: 15 · 2020: 7 · 2019: 10 · 2018: 8 · 2017: 11 · 2016: 7 · 2015: 8 · 2014: 10 · 2013: 5 · 2012: 6
- FWCI
- 1.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- preimplantation embryo development, Y chromosome, SRY, ZFY, mouse embryo, developmental rate, X chromosome dosage, gonadal sex differentiation, blastocyst
- MeSH terms
- Animals, Body Weight, Female, Embryonic and Fetal Development, Gonads, Longitudinal Studies, Male, Sex Determination Analysis, X Chromosome, Y Chromosome, Mice
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