FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Reprod Fertil Dev / Cytoskeletal alterations associated with donor age and cultu...
Reproduction, fertility, and development2015; 27(6); 944-956; doi: 10.1071/RD14468

Cytoskeletal alterations associated with donor age and culture interval for equine oocytes and potential zygotes that failed to cleave after intracytoplasmic sperm injection.

Abstract: Intracytoplasmic sperm injection (ICSI) is an established method to fertilise equine oocytes, but not all oocytes cleave after ICSI. The aims of the present study were to examine cytoskeleton patterns in oocytes after aging in vitro for 0, 24 or 48h (Experiment 1) and in potential zygotes that failed to cleave after ICSI of oocytes from donors of different ages (Experiment 2). Cytoplasmic multiasters were observed after oocyte aging for 48h (P<0.01). A similar increase in multiasters was observed with an increased interval after ICSI for young mares (9-13 years) but not old (20-25 years) mares. Actin vesicles were observed more frequently in sperm-injected oocytes from old than young mares. In the present study, multiasters appeared to be associated with cell aging, whereas actin vesicles were associated with aging of the oocyte donor.
Get Full Text
Publication Date: 2015-03-24 PubMed ID: 25798646PubMed Central: PMC4934900DOI: 10.1071/RD14468Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article discusses a study regarding the effects of aging and time in culture on the cytoskeleton structure of equine oocytes failed to be fertilised through the intracytoplasmic sperm injection (ICSI) method. The authors also explored the differences in these structures between oocytes derived from younger and older horses.

Objective of the Study

  • The study aimed to understand how aging and in vitro culture time affects the cytoskeletal structures in horse oocytes subject to intracytoplasmic sperm injection (ICSI). It also aimed to examine the differences between the cytoskeleton in oocytes derived from younger and older horses that did not cleave after ICSI.

Methodology and Experiments

  • The research was conducted in two main experiments. In Experiment 1, the researchers examined cytoskeleton patterns in oocytes after they were aged in vitro for 0, 24, or 48 hours.
  • In Experiment 2, the team focused on potential zygotes that did not cleave after undergoing ICSI. The donor oocytes for this procedure came from females of different age groups.

Findings

  • The research found cytoplasmic multiasters (star-shaped figures formed in the cell cytoplasm) were noticed in the oocytes aged for 48 hours in vitro.
  • The number of multiasters also increased with the interval after ICSI for younger mares (9-13 years), but this was not observed in mares who were older (20-25 years).
  • Actin vesicles, small enclosed pouches that contain actin proteins that help in cell movement and structure, were observed more frequently in sperm-injected oocytes from older mares when compared to the younger ones.

Conclusion

  • The study concluded that cytoplasmic multiasters appeared to be associated with cell aging, whereas actin vesicles were associated with the age of the oocyte donor. Hence, the age factor manifests at two different cellular levels – the cell aging (indicated by multiasters) and the donor’s age (indicated by actin vesicles).

Cite This Article

APA
Ruggeri E, DeLuca KF, Galli C, Lazzari G, DeLuca JG, Carnevale EM. (2015). Cytoskeletal alterations associated with donor age and culture interval for equine oocytes and potential zygotes that failed to cleave after intracytoplasmic sperm injection. Reprod Fertil Dev, 27(6), 944-956. https://doi.org/10.1071/RD14468

Publication

Reproduction, fertility, and development
ISSN: 1448-5990
NlmUniqueID: 8907465
Country: Australia
Language: English
Volume: 27
Issue: 6
Pages: 944-956

Researcher Affiliations

Ruggeri, Elena
  • Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, 1601 Campus Delivery, Fort Collins, CO 80523, USA.
DeLuca, Keith F
  • Department of Biochemistry and Molecular Biology, College of Natural Sciences, Colorado State University, 1870 Campus Delivery, Fort Collins, CO 80523, USA.
Galli, Cesare
  • Department of Veterinary Medical Sciences, University of Bologna, Via Tolara di sopra, 50, 40064, Ozzano Emilia (Bologna), Italy.
Lazzari, Giovanna
  • Avantea srl, Laboratory of Reproductive Technologies, Via Porcellasco 7f, 26100 Cremona, Italy.
DeLuca, Jennifer G
  • Department of Biochemistry and Molecular Biology, College of Natural Sciences, Colorado State University, 1870 Campus Delivery, Fort Collins, CO 80523, USA.
Carnevale, Elaine M
  • Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, 1601 Campus Delivery, Fort Collins, CO 80523, USA.

MeSH Terms

  • Age Factors
  • Animals
  • Cytoskeleton / metabolism
  • Female
  • Fertilization in Vitro / veterinary
  • Horses
  • Male
  • Oocytes / metabolism
  • Sperm Injections, Intracytoplasmic / methods
  • Sperm Injections, Intracytoplasmic / veterinary
  • Spermatozoa / metabolism
  • Zygote / metabolism

Grant Funding

  • R01 GM088371 / NIGMS NIH HHS

References

This article includes 51 references
  1. Altermatt JL, Suh TK, Stokes JE, Carnevale EM. Effects of age and equine follicle-stimulating hormone (eFSH) on collection and viability of equine oocytes assessed by morphology and developmental competency after intracytoplasmic sperm injection (ICSI). Reprod Fertil Dev 2009;21(4):615–23.
    pubmed: 19383268
  2. Asch R, Simerly C, Ord T, Ord VA, Schatten G. The stages at which human fertilization arrests: microtubule and chromosome configurations in inseminated oocytes which failed to complete fertilization and development in humans. Hum Reprod 1995;10(7):1897–906.
    pubmed: 8583008
  3. Barrett SL, Albertini DF. Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol Reprod 2007;76(6):949–57.
    pubmed: 17287496
  4. Barrett SL, Albertini DF. Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J Assist Reprod Genet 2010;27(1):29–39.
    pmc: PMC2826619pubmed: 20039198
  5. Battaglia DE, Goodwin P, Klein NA, Soules MR. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum Reprod 1996;11(10):2217–22.
    pubmed: 8943533
  6. Brunet S, Maro B. Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 2005;130(6):801–11.
    pubmed: 16322540
  7. Butts SF, Owen C, Mainigi M, Senapati S, Seifer DB, Dokras A. Assisted hatching and intracytoplasmic sperm injection are not associated with improved outcomes in assisted reproduction cycles for diminished ovarian reserve: an analysis of cycles in the United States from 2004 to 2011. Fertil Steril 2014;102(4):1041–1047. e1.
    pmc: PMC4184996pubmed: 25086790
  8. Carnevale E, Bergfelt D, Ginther O. Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares. Animal Reproduction Science 1993;31(3):287–299.
  9. Carnevale EM, Ginther OJ. Defective oocytes as a cause of subfertility in old mares. Biol Reprod Monogr 1995;1:209–214. Equine Reproduction VI.
  10. Carnevale EM. The mare model for follicular maturation and reproductive aging in the woman. Theriogenology 2008;69(1):23–30.
    pubmed: 17976712
  11. Carnevale EM, Maclellan LJ, Ruggeri E, Albertini DF. Meiotic spindle configurations in metaphase II oocytes from young and old mares. J Equine Vet Sci 2012;32:410–411.
  12. Carnevale EM, Ginther OJ. Relationships of age to uterine function and reproductive efficiency in mares. Theriogenology 1992;37(5):1101–15.
    pubmed: 16727108
  13. Choi YH, Love CC, Love LB, Varner DD, Brinsko S, Hinrichs K. Developmental competence in vivo and in vitro of in vitro-matured equine oocytes fertilized by intracytoplasmic sperm injection with fresh or frozen-thawed spermatozoa. Reproduction 2002;123(3):455–65.
    pubmed: 11882023
  14. Combelles CM, Cekleniak NA, Racowsky C, Albertini DF. Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum Reprod 2002;17(4):1006–16.
    pubmed: 11925398
  15. Coticchio G, Guglielmo MC, Albertini DF, Dal Canto M, Mignini Renzini M, De Ponti E, Fadini R. Contributions of the actin cytoskeleton to the emergence of polarity during maturation in human oocytes. Mol Hum Reprod 2014;20(3):200–7.
    pubmed: 24258450
  16. Coticchio G, Guglielmo MC, Dal Canto M, Fadini R, Mignini Renzini M, De Ponti E, Brambillasca F, Albertini DF. Mechanistic foundations of the metaphase II spindle of human oocytes matured in vivo and in vitro. Hum Reprod 2013;28(12):3271–82.
    pubmed: 24129615
  17. Delimitreva S, Tkachenko OY, Berenson A, Nayudu PL. Variations of chromatin, tubulin and actin structures in primate oocytes arrested during in vitro maturation and fertilization—what is this telling us about the relationships between cytoskeletal and chromatin meiotic defects?. Theriogenology 2011;77(7):1297–1311.
    pubmed: 22225695
  18. Delimitreva S, Tkachenko OY, Berenson A, Nayudu PL. Variations of chromatin, tubulin and actin structures in primate oocytes arrested during in vitro maturation and fertilization--what is this telling us about the relationships between cytoskeletal and chromatin meiotic defects?. Theriogenology 2012;77(7):1297–311.
    pubmed: 22225695
  19. Dell’Aquila ME, Masterson M, Maritato F, Hinrichs K. Influence of oocyte collection technique on initial chromatin configuration, meiotic competence, and male pronucleus formation after intracytoplasmic sperm injection (ICSI) of equine oocytes. Mol Reprod Dev 2001;60(1):79–88.
    pubmed: 11550271
  20. Desouza M, Gunning PW, Stehn JR. The actin cytoskeleton as a sensor and mediator of apoptosis. Bioarchitecture 2012;2(3):75–87.
    pmc: PMC3414384pubmed: 22880146
  21. Galli C, Crotti G, Turini P, Duchi R, Mari G, Zavaglia G, Duchamp G, Daels P, Lazzari G. Frozen–thawed embryos produced by Ovum Pick Up of immature oocytes and ICSI are capable to establish pregnancies in the horse. Theriogenology 2002;58(2):705–708.
  22. Ginther OJ. Reproductive biology of the mare : basic and applied aspects. 1992. p. xiv.p. 642.
  23. Gourlay CW, Ayscough KR. Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J Cell Sci 2005;118(Pt 10):2119–32.
    pubmed: 15855235
  24. Grondahl C, Hansen TH, Hossaini A, Heinze I, Greve T, Hyttel P. Intracytoplasmic sperm injection of in vitro-matured equine oocytes. Biol Reprod 1997;57(6):1495–501.
    pubmed: 9408260
  25. Hara H, Hwang IS, Kagawa N, Kuwayama M, Hirabayashi M, Hochi S. High incidence of multiple aster formation in vitrified-warmed bovine oocytes after in vitro fertilization. Theriogenology 2012;77(5):908–15.
    pubmed: 22115806
  26. Heffner LJ. Advanced maternal age--how old is too old?. N Engl J Med 2004;351(19):1927–9.
    pubmed: 15525717
  27. Hinrichs K, Love CC, Brinsko SP, Choi YH, Varner DD. In vitro fertilization of in vitro-matured equine oocytes: effect of maturation medium, duration of maturation, and sperm calcium ionophore treatment, and comparison with rates of fertilization in vivo after oviductal transfer. Biol Reprod 2002;67(1):256–62.
    pubmed: 12080025
  28. Holubcova Z, Howard G, Schuh M. Vesicles modulate an actin network for asymmetric spindle positioning. Nat Cell Biol 2013;15(8):937–47.
    pmc: PMC3797517pubmed: 23873150
  29. Khaitlina SY. Intracellular transport based on actin polymerization. Biochemistry (Mosc) 2014;79(9):917–27.
    pubmed: 25385019
  30. Kim NH, Simerly C, Funahashi H, Schatten G, Day BN. Microtubule organization in porcine oocytes during fertilization and parthenogenesis. Biol Reprod 1996;54(6):1397–404.
    pubmed: 8724370
  31. Kuliev A, Cieslak J, Ilkevitch Y, Verlinsky Y. Chromosomal abnormalities in a series of 6733 human oocytes in preimplantation diagnosis for age-related aneuploidies. Reproductive biomedicine online 2003;6(1):54–59.
    pubmed: 12626143
  32. Lamash NE, Eliseikina MG. Rearrangement of the actin-spectrin cytoskeleton during oocyte maturation of the starfish Asterias amurensis. Russian Journal of Marine Biology 2006;32(2):115–119.
  33. Mau-Holzmann UA. Somatic chromosomal abnormalities in infertile men and women. Cytogenet Genome Res 2005;111(3–4):317–36.
    pubmed: 16192711
  34. Messinger SM, Albertini DF. Centrosome and microtubule dynamics during meiotic progression in the mouse oocyte. J Cell Sci 1991;100(Pt 2):289–98.
    pubmed: 1721916
  35. Palermo GD, Kocent J, Monahan D, Neri QV, Rosenwaks Z. Treatment of male infertility. Methods Mol Biol 2014;1154:385–405.
    pubmed: 24782020
  36. Rambags BP, van Boxtel DC, Tharasanit T, Lenstra JA, Colenbrander B, Stout TA. Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 2014;81(7):959–65.
    pubmed: 24576711
  37. Santella L, Limatola N, Chun JT. Actin Cytoskeleton and Fertilization in Starfish Eggs. 2014. pp. 141–155.
  38. Schatten G. The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev Biol 1994;165(2):299–335.
    pubmed: 7958403
  39. Schatten G, Simerly C, Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc Natl Acad Sci U S A 1985;82(12):4152–6.
    pmc: PMC397953pubmed: 3889922
  40. Schatten G, Simerly C, Schatten H. Microtubules in mouse oocytes, zygotes, and embryos during fertilization and early development: unusual configurations and arrest of mammalian fertilization with microtubule inhibitors. Ann N Y Acad Sci 1986;466:945–8.
    pubmed: 3460464
  41. Sessions-Bresnahan D, Graham J, Carnevale E. Validation of a heterologous fertilization assay and comparison of fertilization rates of equine oocytes using in vitro fertilization, perivitelline, and intracytoplasmic sperm injections. Theriogenology 2014;82:274–282.
    pubmed: 24815920
  42. Squires EL, Carnevale EM, McCue PM, Bruemmer JE. Embryo technologies in the horse. Theriogenology 2003;59(1):151–70.
    pubmed: 12499026
  43. Stoop D, Cobo A, Silber S. Fertility preservation for age-related fertility decline. Lancet 2014;384(9950):1311–9.
    pubmed: 25283572
  44. Sun QY, Schatten H. Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 2006;131(2):193–205.
    pubmed: 16452714
  45. Tilly JL. Commuting the death sentence: how oocytes strive to survive. Nat Rev Mol Cell Biol 2001;2(11):838–48.
    pubmed: 11715050
  46. Tremoleda JL, Schoevers EJ, Stout TA, Colenbrander B, Bevers MM. Organisation of the cytoskeleton during in vitro maturation of horse oocytes. Mol Reprod Dev 2001;60(2):260–9.
    pubmed: 11553927
  47. Tremoleda JL, Van Haeften T, Stout TA, Colenbrander B, Bevers MM. Cytoskeleton and chromatin reorganization in horse oocytes following intracytoplasmic sperm injection: patterns associated with normal and defective fertilization. Biol Reprod 2003;69(1):186–94.
    pubmed: 12646492
  48. Vasilev F, Chun JT, Gragnaniello G, Garante E, Santella L. Effects of ionomycin on egg activation and early development in starfish. PLoS One 2012;7(6):e39231.
    pmc: PMC3377674pubmed: 22723970
  49. Yi K, Li R. Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation. Cytoskeleton (Hoboken) 2012;69(10):727–37.
    pubmed: 22753278
  50. Yi K, Rubinstein B, Unruh JR, Guo F, Slaughter BD, Li R. Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J Cell Biol 2013;200(5):567–76.
    pmc: PMC3587830pubmed: 23439682
  51. Yu XJ, Yi Z, Gao Z, Qin D, Zhai Y, Chen X, Ou-Yang Y, Wang ZB, Zheng P, Zhu MS, Wang H, Sun QY, Dean J, Li L. The subcortical maternal complex controls symmetric division of mouse zygotes by regulating F-actin dynamics. Nat Commun 2014;5:4887.
    pmc: PMC6529946pubmed: 25208553
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.