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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2003 Aug 29;358(1436):1331–1339. doi: 10.1098/rstb.2003.1322

The basis and significance of pre-patterning in mammals.

Richard L Gardner 1, Timothy J Davies 1
PMCID: PMC1693237  PMID: 14511479

Abstract

The second polar body (Pb) provides an enduring marker of the animal pole of the zygote, thereby revealing that the axis of bilateral symmetry of the early blastocyst is aligned with the zygote's animal-vegetal axis. That this relationship is biologically significant appeared likely when subsequent studies showed that the equator of the blastocyst tended to correspond with the plane of first cleavage. However, this cleavage plane varies both with respect to the position of the second Pb and to the distribution of components of the fertilizing sperm that continue to mark the point where it entered the egg. It also maps too variably on the blastocyst to play a causal role in early patterning. The zygote has been found transiently to exhibit bilateral symmetry before regaining an essentially spherical shape prior to first cleavage. Marking experiments indicate that the plane of bilateral symmetry of the blastocyst is aligned with, and the plane of first cleavage is typically orthogonal to, the zygote's bilateral plane. The bilateral symmetry of the zygote bears no consistent relationship either to the point of sperm entry or to the distribution of the pronuclei, and may therefore be a manifestation of intrinsic organization of the egg. Finally, the two-cell blastomere inheriting the sperm entry point has not been found to differ consistently in fate from the one that does not.

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Selected References

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  1. Blickstein I., Verhoeven H. C., Keith L. G. Zygotic splitting after assisted reproduction. N Engl J Med. 1999 Mar 4;340(9):738–739. doi: 10.1056/NEJM199903043400916. [DOI] [PubMed] [Google Scholar]
  2. Davies T. J., Gardner R. L. The plane of first cleavage is not related to the distribution of sperm components in the mouse. Hum Reprod. 2002 Sep;17(9):2368–2379. doi: 10.1093/humrep/17.9.2368. [DOI] [PubMed] [Google Scholar]
  3. Derom C., Vlietinck R., Derom R., Van den Berghe H., Thiery M. Increased monozygotic twinning rate after ovulation induction. Lancet. 1987 May 30;1(8544):1236–1238. doi: 10.1016/s0140-6736(87)92688-2. [DOI] [PubMed] [Google Scholar]
  4. Gardner R. L., Davies T. J. Is the plane of first cleavage related to the point of sperm entry in the mouse? Reprod Biomed Online. 2003 Mar;6(2):157–160. doi: 10.1016/s1472-6483(10)61703-8. [DOI] [PubMed] [Google Scholar]
  5. Gardner R. L. Experimental analysis of second cleavage in the mouse. Hum Reprod. 2002 Dec;17(12):3178–3189. doi: 10.1093/humrep/17.12.3178. [DOI] [PubMed] [Google Scholar]
  6. Gardner R. L., Meredith M. R., Altman D. G. Is the anterior-posterior axis of the fetus specified before implantation in the mouse? J Exp Zool. 1992 Dec 15;264(4):437–443. doi: 10.1002/jez.1402640409. [DOI] [PubMed] [Google Scholar]
  7. Gardner R. L. Patterning is initiated before cleavage in the mouse. Ann Anat. 2002 Nov;184(6):577–581. doi: 10.1016/S0940-9602(02)80100-5. [DOI] [PubMed] [Google Scholar]
  8. Gardner R. L. Specification of embryonic axes begins before cleavage in normal mouse development. Development. 2001 Mar;128(6):839–847. doi: 10.1242/dev.128.6.839. [DOI] [PubMed] [Google Scholar]
  9. Gardner R. L. The early blastocyst is bilaterally symmetrical and its axis of symmetry is aligned with the animal-vegetal axis of the zygote in the mouse. Development. 1997 Jan;124(2):289–301. doi: 10.1242/dev.124.2.289. [DOI] [PubMed] [Google Scholar]
  10. Gardner R. L. The initial phase of embryonic patterning in mammals. Int Rev Cytol. 2001;203:233–290. doi: 10.1016/s0074-7696(01)03009-1. [DOI] [PubMed] [Google Scholar]
  11. Graham C. F., Deussen Z. A. Features of cell lineage in preimplantation mouse development. J Embryol Exp Morphol. 1978 Dec;48:53–72. [PubMed] [Google Scholar]
  12. Hall J. G. Twins and twinning. Am J Med Genet. 1996 Jan 22;61(3):202–204. doi: 10.1002/(SICI)1096-8628(19960122)61:3<202::AID-AJMG2>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]
  13. Howlett S. K., Bolton V. N. Sequence and regulation of morphological and molecular events during the first cell cycle of mouse embryogenesis. J Embryol Exp Morphol. 1985 Jun;87:175–206. [PubMed] [Google Scholar]
  14. KILE J. C., Jr An improved method for the artificial insemination of mice. Anat Rec. 1951 Jan;109(1):109–117. doi: 10.1002/ar.1091090108. [DOI] [PubMed] [Google Scholar]
  15. Kelly S. J., Mulnard J. G., Graham C. F. Cell division and cell allocation in early mouse development. J Embryol Exp Morphol. 1978 Dec;48:37–51. [PubMed] [Google Scholar]
  16. Krzanowska H. Rapidity of removal in vitro of the cumulus oophorus and the zona pellucida in different strains of mice. J Reprod Fertil. 1972 Oct;31(1):7–14. doi: 10.1530/jrf.0.0310007. [DOI] [PubMed] [Google Scholar]
  17. Piotrowska K., Wianny F., Pedersen R. A., Zernicka-Goetz M. Blastomeres arising from the first cleavage division have distinguishable fates in normal mouse development. Development. 2001 Oct;128(19):3739–3748. doi: 10.1242/dev.128.19.3739. [DOI] [PubMed] [Google Scholar]
  18. Piotrowska K., Zernicka-Goetz M. Role for sperm in spatial patterning of the early mouse embryo. Nature. 2001 Jan 25;409(6819):517–521. doi: 10.1038/35054069. [DOI] [PubMed] [Google Scholar]
  19. Piotrowska Karolina, Zernicka-Goetz Magdalena. Early patterning of the mouse embryo--contributions of sperm and egg. Development. 2002 Dec;129(24):5803–5813. doi: 10.1242/dev.00170. [DOI] [PubMed] [Google Scholar]
  20. Plusa Berenika, Grabarek Joanna B., Piotrowska Karolina, Glover David M., Zernicka-Goetz Magdalena. Site of the previous meiotic division defines cleavage orientation in the mouse embryo. Nat Cell Biol. 2002 Oct;4(10):811–815. doi: 10.1038/ncb860. [DOI] [PubMed] [Google Scholar]
  21. Plusa Berenika, Piotrowska Karolina, Zernicka-Goetz Magdalena. Sperm entry position provides a surface marker for the first cleavage plane of the mouse zygote. Genesis. 2002 Mar;32(3):193–198. doi: 10.1002/gene.10027. [DOI] [PubMed] [Google Scholar]
  22. Schinzel A. A., Smith D. W., Miller J. R. Monozygotic twinning and structural defects. J Pediatr. 1979 Dec;95(6):921–930. doi: 10.1016/s0022-3476(79)80278-4. [DOI] [PubMed] [Google Scholar]
  23. Smith L. J. Embryonic axis orientation in the mouse and its correlation with blastocyst relationships to the uterus. II. Relationships from 4 1/4 to 9 1/2 days. J Embryol Exp Morphol. 1985 Oct;89:15–35. [PubMed] [Google Scholar]
  24. Smith L. J. Embryonic axis orientation in the mouse and its correlation with blastocyst relationships to the uterus. Part 1. Relationships between 82 hours and 4 1/4 days. J Embryol Exp Morphol. 1980 Feb;55:257–277. [PubMed] [Google Scholar]
  25. Sutovsky P., Moreno R. D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod. 2000 Aug;63(2):582–590. doi: 10.1095/biolreprod63.2.582. [DOI] [PubMed] [Google Scholar]
  26. Szymonowicz W., Preston H., Yu V. Y. The surviving monozygotic twin. Arch Dis Child. 1986 May;61(5):454–458. doi: 10.1136/adc.61.5.454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wenstrom K. D., Syrop C. H., Hammitt D. G., Van Voorhis B. J. Increased risk of monochorionic twinning associated with assisted reproduction. Fertil Steril. 1993 Sep;60(3):510–514. doi: 10.1016/s0015-0282(16)56169-x. [DOI] [PubMed] [Google Scholar]

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