Meiotic competence of equine oocytes and pronucleus formation after intracytoplasmic sperm injection (ICSI) as related to granulosa cell apoptosis.
Abstract: Follicle atresia and granulosa cell apoptosis may be related to oocyte meiotic and developmental competence. We analyzed the relationships among granulosa cell apoptosis, initial cumulus morphology, oocyte nuclear maturation in vitro, and pronucleus formation after intracytoplasmic sperm injection (ICSI) in the horse. For each follicle, the size was measured and granulosa cells were used for DNA laddering analysis. Oocytes were evaluated for cumulus morphology, cultured for in vitro maturation, and submitted to ICSI. Apoptosis was categorized as absent, intermediate, or advanced according to the relative concentrations of two DNA fragments at 900 and 360 base pairs (bp). In 98 oocyte-follicle pairs, 52 oocytes were classified as expanded (Exp), 39 as compact (Cp), and 7 as having a partial (P) cumulus. Advanced apoptosis was detected in 55% (54/98) of follicles; 37% (36/98) of follicles showed an intermediate level of apoptosis; and 8 follicles (8%) were nonapoptotic. Follicle size was not significantly correlated with granulosa cell apoptosis (P > 0.05). Significantly more Exp than Cp oocytes originated from follicles with advanced apoptosis (P < 0.001). The proportion of oocytes maturing in vitro was significantly higher in oocytes issuing from apoptotic follicles than in oocytes issuing from healthy follicles (P < 0.05). The proportion of normally (two pronuclei) or abnormally fertilized oocytes (one or greater than two pronuclei, or partially decondensed sperm) did not differ in relation to granulosa cell apoptosis. We conclude that, in the mare, granulosa cell apoptosis is related to cumulus expansion and an increase in oocyte meiotic competence but has no effect on the proportion of meiotically competent oocytes that activate after ICSI. These results provide selection criteria for horse oocytes used in assisted reproductive techniques so that embryo production may be maximized.
Publication Date: 2003-01-08 PubMed ID: 12606481DOI: 10.1095/biolreprod.102.009852Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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The study investigates the relation between follicle atresia and granulosa cell apoptosis on oocyte meiotic and developmental competence in the horse, specifically in the context of intracytoplasmic sperm injection (ICSI). The research suggests that granulosa cell apoptosis is tied to cumulus expansion and an increase in oocyte meiotic competence, but does not affect the percentage of meiotically competent oocytes that activate after ICSI.
Study Methods and Data Collection
- The researchers collected data from 98 oocyte-follicle pairs to analyse the relationship among granulosa cell apoptosis, initial cumulus morphology, oocyte nuclear maturation in vitro, and pronucleus formation following ICSI.
- The methods used included measuring each follicle size and DNA laddering analysis of granulosa cells.
- Oocytes were assessed for cumulus morphology, cultured for in vitro maturation, and submitted to ICSI.
- Apoptosis level in the granulosa cells was categorized as either absent, intermediate, or advanced based on the relative concentrations of two DNA fragments at 900 and 360 base pairs. This was observed in 54 out of 98 follicles.
Observations and Findings
- No significant correlation was found between the size of the follicle and granulosa cell apoptosis.
- Expanded oocytes were found in follicles with advanced apoptosis rather than Compact oocytes.
- The proportion of oocytes maturing in vitro was noticeably higher in oocytes from apoptotic follicles than those from healthy follicles.
- The study found no correlation between varying rates of granulosa cell apoptosis and the number of normally or abnormally fertilized oocytes.
Conclusions and Implications
- The study concludes that granulosa cell apoptosis plays a role in cumulus expansion and enhancing oocyte meiotic competence, but does not impact the ratio of meiotically competent oocytes activated following ICSI.
- These findings can provide crucial selection criteria for horse oocytes used in assisted reproductive techniques, potentially aiding in maximizing embryo production.
Cite This Article
APA
Dell'Aquila ME, Albrizio M, Maritato F, Minoia P, Hinrichs K.
(2003).
Meiotic competence of equine oocytes and pronucleus formation after intracytoplasmic sperm injection (ICSI) as related to granulosa cell apoptosis.
Biol Reprod, 68(6), 2065-2072.
https://doi.org/10.1095/biolreprod.102.009852 Publication
Researcher Affiliations
- Department of Animal Production--Section of Reproductive Biology and Veterinary Obstetrics, University of Bari, 70010 Valenzano, Bari, Italy. e.dellaquila@veterinaria.uniba.it
MeSH Terms
- Animals
- Apoptosis / physiology
- Cell Nucleus / physiology
- Cell Separation
- Chromatin / genetics
- DNA / genetics
- DNA Fragmentation / physiology
- Female
- Fertilization in Vitro
- Granulosa Cells / physiology
- Horses
- Male
- Meiosis / physiology
- Nucleosomes / physiology
- Oocytes / physiology
- Ovarian Follicle / anatomy & histology
- Ovarian Follicle / physiology
- Sperm Injections, Intracytoplasmic
- Sperm Maturation / physiology
- Zygote / physiology
Citations
This article has been cited 9 times.- Ortiz I, Dorado J, Pereira B, Diaz-Jimenez M, Consuegra C, Gosalvez J, Hidalgo M. DNA fragmentation of equine cumulus cells from Cumulus-Oocyte complexes submitted to vitrification and its relationship to the developmental competence of the oocyte. Reprod Domest Anim 2022 Oct;57 Suppl 5(Suppl 5):64-67.
- Mastrorocco A, Cacopardo L, Martino NA, Fanelli D, Camillo F, Ciani E, Roelen BAJ, Ahluwalia A, Dell'Aquila ME. One-step automated bioprinting-based method for cumulus-oocyte complex microencapsulation for 3D in vitro maturation. PLoS One 2020;15(9):e0238812.
- Martino NA, Dell'Aquila ME, Filioli Uranio M, Rutigliano L, Nicassio M, Lacalandra GM, Hinrichs K. Effect of holding equine oocytes in meiosis inhibitor-free medium before in vitro maturation and of holding temperature on meiotic suppression and mitochondrial energy/redox potential. Reprod Biol Endocrinol 2014 Oct 11;12:99.
- Ambruosi B, Uranio MF, Sardanelli AM, Pocar P, Martino NA, Paternoster MS, Amati F, Dell'Aquila ME. In vitro acute exposure to DEHP affects oocyte meiotic maturation, energy and oxidative stress parameters in a large animal model. PLoS One 2011;6(11):e27452.
- Cremonesi F, Anderson K, Lange-Consiglio A. Efficacy of tuohy needle in oocytes collection from excised mare ovaries. Vet Med Int 2010 Aug 5;2010.
- Lange Consiglio A, Dell'Aquila ME, Fiandanese N, Ambruosi B, Cho YS, Bosi G, Arrighi S, Lacalandra GM, Cremonesi F. Effects of leptin on in vitro maturation, fertilization and embryonic cleavage after ICSI and early developmental expression of leptin (Ob) and leptin receptor (ObR) proteins in the horse. Reprod Biol Endocrinol 2009 Oct 16;7:113.
- Hasegawa J, Yanaihara A, Iwasaki S, Mitsukawa K, Negishi M, Okai T. Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI. J Assist Reprod Genet 2007 Oct;24(10):463-6.
- Minervini F, Giannoccaro A, Fornelli F, Dell'Aquila ME, Minoia P, Visconti A. Influence of mycotoxin zearalenone and its derivatives (alpha and beta zearalenol) on apoptosis and proliferation of cultured granulosa cells from equine ovaries. Reprod Biol Endocrinol 2006 Nov 30;4:62.
- Dell'Aquila ME, Caillaud M, Maritato F, Martoriati A, Gérard N, Aiudi G, Minoia P, Goudet G. Cumulus expansion, nuclear maturation and connexin 43, cyclooxygenase-2 and FSH receptor mRNA expression in equine cumulus-oocyte complexes cultured in vitro in the presence of FSH and precursors for hyaluronic acid synthesis. Reprod Biol Endocrinol 2004 Jun 22;2:44.
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