Abstract
The relationship between factors external to the human oocyte and the developmental potential of the female gamete after meiotic maturation in vivo is discussed. The findings indicate very different intrafolliailar oxygen contents exist among follicles from the same and different patients, and marginally hypoxic conditions in some follicles are associated with a comparatively low adenosine triphosphate content and a reduction in intracellular pHfor the corresponding metaphase II-stage oocyte. For such oocytes, the finding of an increased frequency of cytoplasmic pathology and chromosomal scattering (aneuploidy) suggests a compromised developmental potential Three distinctly different patterns of cumulus cell attachment and proliferation during the first 24 hours of culture after insemination are described. As reported earlier, different cumulus cell phenotypes observed in vitro are independent of the presence of the oocyte or fertilized egg and unrelated to the degree of expansion of the cumulus at retrieval. However, developmental viability and implantation potential after in vitro fertilization-embryo transfer appear to be related to an intrinsic pattern of cumulus cell behavior in vitro. The results are discussed with respect to the role of factors external to the human oocyte that may influence or determine the ability of the oocyte to develop progressively after fertilization.
Similar content being viewed by others
References
Boue J, Boue A, Lazar P. Retrospective and prospective epidemiological studies of 1500 karyotyped spontaneous abortions. Teratology 1975;12:11–26.
Burgoyne P, Holland K, Stephens R. Incidence of numerical chromosome anomalies in human pregnancy: Estimation from induced and spontaneous abortion data. Hum Reprod 1991;6: 555–64.
Edwards RG. Causes of early embryonic loss in human pregnancy. Hum Reprod 1986;1:185–98.
Osborn J, Moor R. An assessment of the factors causing embryonic loss after fertilization in vitro. J Reprod Fertil 1988; 36(suppl): 59–72.
Van Blerkom J. Developmental failure in human reproduction associated with chromosomal abnormalities and cytoplasmic pathologies in meiotically mature oocytes. In: Van Blerkom J, ed. Biological basis of early reproductive failure in the human: Applications to medically assisted conception. New York: Oxford University Press, 1994:283–326.
Martin R, Mahadevan M, Taylor P, et al. Chromosome analysis of unfertilized human oocytes. J Reprod Fertil 1986;78:673–6.
Wramsby H, Fredga K. Chromosome analysis of human oocytes failing the cleavage after insemination in vitro. Hum Reprod 1987;2:137–42.
Gras L, McBain J, Trounson A, Kola I. The incidence of chromosomal aneuploidy in stimulated and unstimulated (natural) un-mseminated human oocytes. Hum Reprod 1992;7:1396–401.
Zenzes T, Wang P, Casper R. Evidence for a maternal predisposition to chromosome aneuploidy in multiple oocytes of some in vitro fertilization patients. Fertil Steril 1992;57:143–9.
Van Blerkom J, Henry G. Oocyte dysmorphism and aneuploidy meiotically mature human oocytes after controlled ovarian hy-perstimulation. Hum Reprod 1992;7:379–90.
Van Blerkom J, Henry G. Cytogenetic analyses of living human oocytes: Cellular basis and developmental consequences of perturbations in chromosomal organization and complement. Hum Reprod 1988;3:777–90.
Angell R, Ledger W, Yong E, Harkness L, Baird D. Cytogenetic analysis of unfertilized human oocytes. Hum Reprod 1991;6: 568–73.
Munne S, Lee A, Rosenwaks Z, Grifo J, Cohen J. Diagnosis of major chromosome aneuploidies in human preimplantation embryos. Hum Reprod 1993;8:2185–91.
Tann J, Gomez E, Sampaio M, Ruiz M, Remohi J, Pellicer A. Cytogenetic analysis of human oocytes from fertile women. Hum Reprod 1991;6:1100–3.
Eichenlaub-Ritter U, Stahl A, Luciani J. The microtubular cyto-skeleton and chromosomes of unfertilized human oocytes aged in vitro. Hum Genet 1988;80:259–64.
Acosta A, Moon S, Oehninger S, Muasher S, Rosenwaks Z, Matta J. Implantation potential of each embryo in multiple pregnancies obtained by in vitro fertilization seems to be different. Fertil Stenl 1988;50:906–11.
Conaghan J, Hardy K, Handyside A, Winston R, Leese H. Selection criteria for human embryo transfer: A comparison of pyruvate uptake and morphology. J Assist Reprod Genet 1993;10: 21–30.
Gott A, Hardy K, Winston R, Leese H. Non-invasive measurement of pyruvate and glucose uptake and lactate production by-single human preimplantation embryos. Hum Reprod 1990;5: 104–8.
Van Blerkom J, Davis P, Lee J. ATP content of human oocytes and developmental potential and outcome after 1VF-ET. Hum Reprod 1995;10:415–24.
Van Blerkom J. Developmental failure in human reproduction associated with preovulatory oogenesis and preimplantation em-bryogenesis. In: Van Blerkom J, Motta, P, ed. Ultrastructure of human gametogenesis and embryogenesis. Boston: Kluwer Academic Publishers, 1989:125–80.
Chi MY, Manchester J, Yang V, Curato A, Strickler R, Lowry, O. Contrast in levels of metabolic enzymes in human and mouse ova. Biol Reprod 1988;39:295–307.
Martin K, Hardy K, Winston R, Leese H. Activity of enzymes of energy metabolism in single human preimplantation embryos. J Reprod Fertil 1993;9:259–66.
Barnett D, Bavister B. What is the relationship between the metabolism of preimplantation embryos and their developmental competence? Mol Reprod Devel (in press).
Van Blerkom, J. Occurrence and developmental consequences of aberrant cellular organization in meiotically mature human oocytes after exogenous ovarian hyperstimulation. J Electr Micro Tech 1990;16:324–46.
Hartshorne GM. Steroid production by the cumulus: Relationship to fertilization in vitro. Hum Reprod 1989;7:742–5.
Nayudu P, Gook D, Lopata A, Sheather S, Lloyd-Smith C, Cadusch P, Johnson W. Follicular characteristics associated with viable pregnancy after in vitro fertilization in humans. Gamete Res 1987;18:37–55.
Nayudu P, Lopata A, Jones G, et al. An analysis of human oocytes and follicles from stimulated cycles: Oocyte morphology and associated follicular fluid characteristics. Hum Reprod 1989;4: 558–67.
Van Blerkom J, Davis P. Cytogenetic, cellular and developmental consequences of cryopreservation of immature and mature mouse and human oocytes. Micro Res Tech 1994;27:165–93.
Van Blerkom J. Intrinsic and extrinsic influences on the expression of molecular and cellular differentiation in human oocytes and embryos. In: Wasserman P, ed. Elements of mammalian fertilization. Boca Raton, Florida: CRC Press. 1991:81–105.
Gaulden M. Maternal age effect: The enigma of Down syndrome and other trisomic conditions. Mutat Res 1992;296:69–88.
Byatt-Smith J, Leese H, Gosden R. An investigation by mathematical modeling of whether mouse and human preimplanta-tion embryos in static culture can satisfy their demands for oxygen by diffusion. Hum Reprod 1991;6:52–57.
Van Blerkom J, Davis P, Mernam J. A retrospective analysis of unfertilized and presumed parthenogenetically activated human oocytes demonstrates a high frequency of sperm penetration. Hum Reprod 1994;9:2381–8.
Bunn F, Poyton R. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 1996 (in press).
Gregory L, Booth A, Wells C, Walker S. A study of the cumulus-corona cell complex in in vitro fertilization and embryo transfer; a prognostic indicator of the failure of implantation. Hum Reprod 1994;9:1308–17.
Goldman S, Dirnfeld M, Gonen Y, Koifman M, Lissak A, Abramovici H. Different morphology and proliferative ability of cumulus and granulosa cells originating from cystic follicles aspirated from stimulated in vitro fertilization patients. Fertil Steril 1993;59:601–4.
Laufer N, Tarlatzis B, DeCherney A, et al. Asynchrony between human cumulus-corona cell complex and oocyte maturation after human menopausal gonadotropin treatment for in vitro fertilization. Fertil Steril 1984;42:366–72.
Tamura M, Sasano H, Suzuki T, et al. Expression of epidermal growth factors and epidermal growth factor receptor in normal cycling human ovaries. Hum Reprod 1995;1:1891-6.
Kamat B, Brown L, Manseau E, Senger D, Dvorak H. Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development. Am J Pathol 1995;146:157–65.
Author information
Authors and Affiliations
Additional information
Studies of uninsemmared oocytes, cumulus cells, and follicular fluids were supported by a grant from the National Institutes of Health (HD-31907). This paper is derived from a lecture presented at the 42nd Annual Meeting of the Society for Gynecological Investigation (Chicago, 1995).
Rights and permissions
About this article
Cite this article
Van Blerkom, J. The Influence of Intrinsic and Extrinsic Factors on the Developmental Potential and Chromosomal Normality of the Human Oocyte. Reprod. Sci. 3, 3–11 (1996). https://doi.org/10.1016/1071-5576(95)00041-0
Published:
Issue Date:
DOI: https://doi.org/10.1016/1071-5576(95)00041-0