Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

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

Elena Ruggeri A , Keith F. DeLuca B , Cesare Galli C D , Giovanna Lazzari D , Jennifer G. DeLuca B and Elaine M. Carnevale A E
+ Author Affiliations
- Author Affiliations

A Department of Biomedical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, 1601 Campus Delivery, Fort Collins, CO 80523, USA.

B Department of Biochemistry and Molecular Biology, College of Natural Sciences, Colorado State University, 1870 Campus Delivery, Fort Collins, CO 80523, USA.

C Department of Veterinary Medical Sciences, University of Bologna, Via Tolara di sopra, 50, 40064, Ozzano Emilia (Bologna), Italy.

D Avantea srl, Laboratory of Reproductive Technologies, Via Porcellasco 7f, 26100 Cremona, Italy.

E Corresponding author. Email: elaine.carnevale@colostate.edu

Reproduction, Fertility and Development 27(6) 944-956 https://doi.org/10.1071/RD14468
Submitted: 25 November 2014  Accepted: 18 February 2015   Published: 24 March 2015

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 48 h (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 48 h (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.

Additional keywords: actin, maternal aging, oocyte senescence, tubulin.


References

Altermatt, J. L., Suh, T. K., Stokes, J. E., and Carnevale, E. M. (2009). 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. 21, 615–623.
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).CrossRef | 1:CAS:528:DC%2BD1MXksF2rtbc%3D&md5=21ee49d7434170275d715474414153b4CAS | 19383268PubMed |

Asch, R., Simerly, C., Ord, T., Ord, V. A., and Schatten, G. (1995). 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. 10, 1897–1906.
| 1:STN:280:DyaK28%2FjtlWktw%3D%3D&md5=0804001c3319dd584a8c71f3c6601851CAS | 8583008PubMed |

Barrett, S. L., and Albertini, D. F. (2007). Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte. Biol. Reprod. 76, 949–957.
Allocation of gamma-tubulin between oocyte cortex and meiotic spindle influences asymmetric cytokinesis in the mouse oocyte.CrossRef | 1:CAS:528:DC%2BD2sXlvFGmsrg%3D&md5=ee6f25f39fb0b5937ee24104605141e6CAS | 17287496PubMed |

Barrett, S. L., and Albertini, D. F. (2010). Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence. J. Assist. Reprod. Genet. 27, 29–39.
Cumulus cell contact during oocyte maturation in mice regulates meiotic spindle positioning and enhances developmental competence.CrossRef | 20039198PubMed |

Battaglia, D. E., Goodwin, P., Klein, N. A., and Soules, M. R. (1996). Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 11, 2217–2222.
Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women.CrossRef | 1:STN:280:DyaK2s%2FpvV2itQ%3D%3D&md5=bc108b9e8bc1dda6d5897d8d627e1a12CAS | 8943533PubMed |

Brunet, S., and Maro, B. (2005). Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130, 801–811.
Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space.CrossRef | 1:CAS:528:DC%2BD28Xkt12nsw%3D%3D&md5=3600679dc24dbda167f14ad39cd50c5fCAS | 16322540PubMed |

Butts, S. F., Owen, C., Mainigi, M., Senapati, S., Seifer, D. B., and Dokras, A. (2014). 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. 102, 1041–1047e1.
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.CrossRef | 25086790PubMed |

Carnevale, E. M. (2008). The mare model for follicular maturation and reproductive aging in the woman. Theriogenology 69, 23–30.
The mare model for follicular maturation and reproductive aging in the woman.CrossRef | 1:CAS:528:DC%2BD2sXhsVSmu7nN&md5=b1d730b243c0636c9f9498a2aecbc1f0CAS | 17976712PubMed |

Carnevale, E. M., and Ginther, O. J. (1992). Relationships of age to uterine function and reproductive efficiency in mares. Theriogenology 37, 1101–1115.
Relationships of age to uterine function and reproductive efficiency in mares.CrossRef | 1:STN:280:DC%2BD283pvFyksw%3D%3D&md5=1d59d21e6ce65edf1bc2f7e3a516408aCAS | 16727108PubMed |

Carnevale, E., and Ginther, O. (1995). Defective oocytes as a cause of subfertility in old mares. Biol. Reprod. Monogr. 1, 209–214.

Carnevale, E. M., Bergfelt, D. R., and Ginther, O. J. (1993). Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares. Anim. Reprod. Sci. 31, 287–299.
Aging effects on follicular activity and concentrations of FSH, LH, and progesterone in mares.CrossRef | 1:CAS:528:DyaK3sXltV2nsb0%3D&md5=447aae172b61b197d75fb8805cae2dfaCAS |

Carnevale, E. M., Maclellan, L. J., Ruggeri, E., and Albertini, D. F. (2012). Meiotic spindle configurations in metaphase II oocytes from young and old mares. J. Equine Vet. Sci. 32, 410–411.
Meiotic spindle configurations in metaphase II oocytes from young and old mares.CrossRef |

Choi, Y. H., Love, C. C., Love, L. B., Varner, D. D., Brinsko, S., and Hinrichs, K. (2002). 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 123, 455–465.
Developmental competence in vivo and in vitro of in vitro-matured equine oocytes fertilized by intracytoplasmic sperm injection with fresh or frozen–thawed spermatozoa.CrossRef | 1:CAS:528:DC%2BD38Xit1Cls7o%3D&md5=f48afb639292ba8079fca99a04430adbCAS | 11882023PubMed |

Combelles, C. M., Cekleniak, N. A., Racowsky, C., and Albertini, D. F. (2002). Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes. Hum. Reprod. 17, 1006–1016.
Assessment of nuclear and cytoplasmic maturation in in-vitro matured human oocytes.CrossRef | 1:STN:280:DC%2BD387pt1eisw%3D%3D&md5=a9cce9bbb258a98851de93cb1dfa59e9CAS | 11925398PubMed |

Coticchio, G., Guglielmo, M. C., Dal Canto, M., Fadini, R., Mignini Renzini, M., De Ponti, E., Brambillasca, F., and Albertini, D. F. (2013). Mechanistic foundations of the metaphase II spindle of human oocytes matured in vivo and in vitro. Hum. Reprod. 28, 3271–3282.
Mechanistic foundations of the metaphase II spindle of human oocytes matured in vivo and in vitro.CrossRef | 1:CAS:528:DC%2BC3sXhvVSht7bN&md5=ce19aff4c0ce6186cc2b75933cd34779CAS | 24129615PubMed |

Coticchio, G., Guglielmo, M. C., Albertini, D. F., Dal Canto, M., Mignini Renzini, M., De Ponti, E., and Fadini, R. (2014). Contributions of the actin cytoskeleton to the emergence of polarity during maturation in human oocytes. Mol. Hum. Reprod. 20, 200–207.
Contributions of the actin cytoskeleton to the emergence of polarity during maturation in human oocytes.CrossRef | 1:CAS:528:DC%2BC2cXis1WqsL8%3D&md5=ec2ab5bbc077c69850427de93b595382CAS | 24258450PubMed |

Delimitreva, S., Tkachenko, O. Y., Berenson, A., and Nayudu, P. L. (2012). 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 77, 1297–1311.
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?CrossRef | 1:CAS:528:DC%2BC38XjvVemurg%3D&md5=5e3bd485b390d0140f4df211a808b8d6CAS | 22225695PubMed |

Dell’Aquila, M. E., Masterson, M., Maritato, F., and Hinrichs, K. (2001). 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. 60, 79–88.
Influence of oocyte collection technique on initial chromatin configuration, meiotic competence, and male pronucleus formation after intracytoplasmic sperm injection (ICSI) of equine oocytes.CrossRef | 1:CAS:528:DC%2BD3MXlvFWis7w%3D&md5=91ebc681fe8b5d0fd7b2ce527e0325daCAS | 11550271PubMed |

Desouza, M., Gunning, P. W., and Stehn, J. R. (2012). The actin cytoskeleton as a sensor and mediator of apoptosis. BioArchitecture 2, 75–87.
The actin cytoskeleton as a sensor and mediator of apoptosis.CrossRef | 22880146PubMed |

Galli, C., Crotti, G., Turini, P., Duchi, R., Mari, G., Zavaglia, G., Duchamp, G., Daels, P., and Lazzari, G. (2002). Frozen–thawed embryos produced by ovum pick up of immature oocytes and ICSI are capable to establish pregnancies in the horse. Theriogenology 58, 705–708.
Frozen–thawed embryos produced by ovum pick up of immature oocytes and ICSI are capable to establish pregnancies in the horse.CrossRef |

Ginther, O. J. (1992). ‘Reproductive Biology of the Mare: Basic and Applied Aspects.’ 2nd edn. (Equiservices: Cross Plains, WI.)

Gourlay, C. W., and Ayscough, K. R. (2005). Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J. Cell Sci. 118, 2119–2132.
Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast.CrossRef | 1:CAS:528:DC%2BD2MXlsFCgurc%3D&md5=7afab94ea640c47d54f7349790972105CAS | 15855235PubMed |

Grøndahl, C., Hansen, T. H., Hossaini, A., Heinze, I., Greve, T., and Hyttel, P. (1997). Intracytoplasmic sperm injection of in vitro-matured equine oocytes. Biol. Reprod. 57, 1495–1501.
Intracytoplasmic sperm injection of in vitro-matured equine oocytes.CrossRef | 9408260PubMed |

Hara, H., Hwang, I. S., Kagawa, N., Kuwayama, M., Hirabayashi, M., and Hochi, S. (2012). High incidence of multiple aster formation in vitrified–warmed bovine oocytes after in vitro fertilization. Theriogenology 77, 908–915.
High incidence of multiple aster formation in vitrified–warmed bovine oocytes after in vitro fertilization.CrossRef | 1:STN:280:DC%2BC383mtFyhtg%3D%3D&md5=61e24ca632affa657ba2698e6b0fc30aCAS | 22115806PubMed |

Heffner, L. J. (2004). Advanced maternal age: how old is too old? N. Engl. J. Med. 351, 1927–1929.
Advanced maternal age: how old is too old?CrossRef | 1:CAS:528:DC%2BD2cXps1Wltr0%3D&md5=261eced8cdfa70a158bd1a5eb98bb2adCAS | 15525717PubMed |

Hinrichs, K., Love, C. C., Brinsko, S. P., Choi, Y. H., and Varner, D. D. (2002). 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. 67, 256–262.
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.CrossRef | 1:CAS:528:DC%2BD38XkvV2itbs%3D&md5=8ca2c1edf7cb8c4afcce842ade174499CAS | 12080025PubMed |

Holubcová, Z., Howard, G., and Schuh, M. (2013). Vesicles modulate an actin network for asymmetric spindle positioning. Nat. Cell Biol. 15, 937–947.
Vesicles modulate an actin network for asymmetric spindle positioning.CrossRef | 23873150PubMed |

Khaitlina, S. Y. (2014). Intracellular transport based on actin polymerization. Biochemistry (Mosc.) 79, 917–927.
Intracellular transport based on actin polymerization.CrossRef | 1:CAS:528:DC%2BC2cXhsFCgs7nJ&md5=23ac64907800332fe91810095c3bac17CAS | 25385019PubMed |

Kim, N. H., Simerly, C., Funahashi, H., Schatten, G., and Day, B. N. (1996). Microtubule organization in porcine oocytes during fertilization and parthenogenesis. Biol. Reprod. 54, 1397–1404.
Microtubule organization in porcine oocytes during fertilization and parthenogenesis.CrossRef | 1:CAS:528:DyaK28XjtV2ju70%3D&md5=a3a1ca1ce4ae623fcd763d70b1ae5b06CAS | 8724370PubMed |

Kuliev, A., Cieslak, J., Ilkevitch, Y., and Verlinsky, Y. (2003). Chromosomal abnormalities in a series of 6733 human oocytes in preimplantation diagnosis for age-related aneuploidies. Reprod. Biomed. Online 6, 54–59.
Chromosomal abnormalities in a series of 6733 human oocytes in preimplantation diagnosis for age-related aneuploidies.CrossRef | 12626143PubMed |

Lamash, N. E., and Eliseikina, M. G. (2006). Rearrangement of the actin–spectrin cytoskeleton during oocyte maturation of the starfish Asterias amurensis. Russ. J. Mar. Biol. 32, 115–119.
Rearrangement of the actin–spectrin cytoskeleton during oocyte maturation of the starfish Asterias amurensis.CrossRef |

Mau-Holzmann, U. A. (2005). Somatic chromosomal abnormalities in infertile men and women. Cytogenet. Genome Res. 111, 317–336.
Somatic chromosomal abnormalities in infertile men and women.CrossRef | 1:STN:280:DC%2BD2MrhvVeltQ%3D%3D&md5=55a91b3d63efbaefcb7f4c806746854aCAS | 16192711PubMed |

Messinger, S. M., and Albertini, D. F. (1991). Centrosome and microtubule dynamics during meiotic progression in the mouse oocyte. J. Cell. Sci. 100, 289–298.
| 1721916PubMed |

Palermo, G. D., Kocent, J., Monahan, D., Neri, Q. V., and Rosenwaks, Z. (2014). Treatment of male infertility. Methods Mol. Biol. 1154, 385–405.
Treatment of male infertility.CrossRef | 24782020PubMed |

Rambags, B. P., van Boxtel, D. C., Tharasanit, T., Lenstra, J. A., Colenbrander, B., and Stout, T. A. (2014). Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro. Theriogenology 81, 959–965.
Advancing maternal age predisposes to mitochondrial damage and loss during maturation of equine oocytes in vitro.CrossRef | 1:CAS:528:DC%2BC2cXjsF2gurc%3D&md5=ad6e368a68b30907f0750967a230eb4dCAS | 24576711PubMed |

Santella, L., Limatola, N., and Chun, J. T. (2014). Actin cytoskeleton and fertilization in starfish eggs. In ‘Sexual Reproduction in Animals and Plants.’ (Eds Sawada, Hitoshi, Inoue, Naokazu, Iwano, Megumi.) pp. 141–155. (Springer: New York, NY.)

Schatten, G. (1994). The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization. Dev. Biol. 165, 299–335.
The centrosome and its mode of inheritance: the reduction of the centrosome during gametogenesis and its restoration during fertilization.CrossRef | 1:CAS:528:DyaK2MXhvVylu7Y%3D&md5=359db4ebc83fd52ecb3454027f8e346eCAS | 7958403PubMed |

Schatten, G., Simerly, C., and Schatten, H. (1985). 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. USA 82, 4152–4156.
Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization.CrossRef | 1:CAS:528:DyaL2MXksFWrsr0%3D&md5=6bd94458e0245ee6b20a2bc1f5a331eaCAS | 3889922PubMed |

Schatten, G., Simerly, C., and Schatten, H. (1986). 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. 466, 945–948.
Microtubules in mouse oocytes, zygotes, and embryos during fertilization and early development: unusual configurations and arrest of mammalian fertilization with microtubule inhibitors.CrossRef | 1:STN:280:DyaL283mslWmsA%3D%3D&md5=8e97c1271ab7ca4d598d15e14e7cfee9CAS | 3460464PubMed |

Sessions-Bresnahan, D. R., Graham, J. K., and Carnevale, E. M. (2014). Validation of a heterologous fertilization assay and comparison of fertilization rates of equine oocytes using in vitro fertilization, perivitelline, and intracytoplasmic sperm injections. Theriogenology 82, 274–282.
Validation of a heterologous fertilization assay and comparison of fertilization rates of equine oocytes using in vitro fertilization, perivitelline, and intracytoplasmic sperm injections.CrossRef | 1:STN:280:DC%2BC2cjhsFGmsg%3D%3D&md5=cd33761f83898cca878104b36986c0ccCAS | 24815920PubMed |

Squires, E. L., Carnevale, E. M., McCue, P. M., and Bruemmer, J. E. (2003). Embryo technologies in the horse. Theriogenology 59, 151–170.
Embryo technologies in the horse.CrossRef | 1:STN:280:DC%2BD3s%2FjslCquw%3D%3D&md5=b05c0ec24e00625abbac0511260575d8CAS | 12499026PubMed |

Stoop, D., Cobo, A., and Silber, S. (2014). Fertility preservation for age-related fertility decline. Lancet 384, 1311–1319.
Fertility preservation for age-related fertility decline.CrossRef | 25283572PubMed |

Sun, Q. Y., and Schatten, H. (2006). Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131, 193–205.
Regulation of dynamic events by microfilaments during oocyte maturation and fertilization.CrossRef | 1:CAS:528:DC%2BD28XisFals7k%3D&md5=8f44128ce99432992f73b3e2420d6f0aCAS | 16452714PubMed |

Tilly, J. L. (2001). Commuting the death sentence: how oocytes strive to survive. Nat. Rev. Mol. Cell Biol. 2, 838–848.
Commuting the death sentence: how oocytes strive to survive.CrossRef | 1:CAS:528:DC%2BD3MXotlartLk%3D&md5=fdfb53d5a3ccce46a633f403c2cb978bCAS | 11715050PubMed |

Tremoleda, J. L., Schoevers, E. J., Stout, T. A., Colenbrander, B., and Bevers, M. M. (2001). Organisation of the cytoskeleton during in vitro maturation of horse oocytes. Mol. Reprod. Dev. 60, 260–269.
Organisation of the cytoskeleton during in vitro maturation of horse oocytes.CrossRef | 1:CAS:528:DC%2BD3MXmslSjsrc%3D&md5=246989094b9b7209bcba141e3e3e1aefCAS | 11553927PubMed |

Tremoleda, J. L., Van Haeften, T., Stout, T. A., Colenbrander, B., and Bevers, M. M. (2003). Cytoskeleton and chromatin reorganization in horse oocytes following intracytoplasmic sperm injection: patterns associated with normal and defective fertilization. Biol. Reprod. 69, 186–194.
Cytoskeleton and chromatin reorganization in horse oocytes following intracytoplasmic sperm injection: patterns associated with normal and defective fertilization.CrossRef | 1:CAS:528:DC%2BD3sXkvFCntL8%3D&md5=a5dc856819d724da5bf2d0e42d0bccdeCAS | 12646492PubMed |

Vasilev, F., Chun, J. T., Gragnaniello, G., Garante, E., and Santella, L. (2012). Effects of ionomycin on egg activation and early development in starfish. PLoS ONE 7, e39231.
Effects of ionomycin on egg activation and early development in starfish.CrossRef | 1:CAS:528:DC%2BC38XptFaks7o%3D&md5=366343a59af3d0f37b7bf33dc195b5e2CAS | 22723970PubMed |

Yi, K., and Li, R. (2012). Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation. Cytoskeleton (Hoboken) 69, 727–737.
Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation.CrossRef | 1:CAS:528:DC%2BC38XhsFGqtL%2FE&md5=8b84ae4e1f636ee80f27415ed4eea790CAS | 22753278PubMed |

Yi, K., Rubinstein, B., Unruh, J. R., Guo, F., Slaughter, B. D., and Li, R. (2013). Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J. Cell Biol. 200, 567–576.
Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes.CrossRef | 1:CAS:528:DC%2BC3sXjvVygs78%3D&md5=f7bad8d6955e3b2dde5d85f5c9975cc0CAS | 23439682PubMed |

Yu, X. J., Yi, Z., Gao, Z., Qin, D., Zhai, Y., Chen, X., Ou-Yang, Y., Wang, Z. B., Zheng, P., Zhu, M. S., Wang, H., Sun, Q. Y., Dean, J., and Li, L. (2014). The subcortical maternal complex controls symmetric division of mouse zygotes by regulating F-actin dynamics. Nat. Commun. 5, 4887.
The subcortical maternal complex controls symmetric division of mouse zygotes by regulating F-actin dynamics.CrossRef | 1:CAS:528:DC%2BC2MXksVektbw%3D&md5=80878c3bf631881085172054c7f18a4bCAS | 25208553PubMed |



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