The Variable Success of in Vitro Maturation: Can We Do Better?

Overview

Journal Anim Reprod

Date 2022 Oct 17

PMID 36249849

Authors

Alberto M Luciano

Federica Franciosi

Rodrigo G Barros

Cecilia Dieci

Valentina Lodde

Affiliations

Soon will be listed here.

Abstract

The efficiency of assisted reproductive technologies, consisting of the transfer of embryos obtained through maturation, fertilization and early embryo culture is still limited. The quality of the oocytes is pivotal for assisted reproductive efficiency and the maturation of the oocyte represents the first key limiting step of the embryo production system. At the time of removal from the antral follicles, the oocyte is still completing the final growth and differentiation steps, needed to provide the so-called developmental competence, i.e. the machinery required to sustain fertilization and embryo development. In mono-ovular species only one oocyte per cycle is available for procreation, therefore the current assisted reproduction techniques strive to overcome this natural boundary. However, the success is still limited and overall the effectiveness does not exceed the efficiency achieved in millions of years of mammalian evolution. One of the problems lies in the intrinsic heterogeneity of the oocytes that are subjected to maturation and in the lack of dedicated approaches to finalize the differentiation process. In this review we will try to overview some of the salient aspects of current practices by emphasizing the most critical and fundamental features in oocyte differentiation that should be carefully considered for improving current techniques.

Citing Articles

Porcine sperm bind to an oviduct glycan coupled to glass surfaces as a model of sperm interaction with the oviduct.

Soto-Heras S, Volz L, Bovin N, Miller D Sci Rep. 2025; 15(1):4680.

PMID: 39920342 PMC: 11806115. DOI: 10.1038/s41598-025-88986-2.

Lack of effect of cyclic adenosine monophosphate modulation during prematuration in vitro on development to the blastocyst stage and expression of specific genes associated with lineage commitment.

Desenzi R, Cuellar C, Hoorn Q, Batista A, Silva Jr R, Hansen P JDS Commun. 2025; 6(1):171-174.

PMID: 39877180 PMC: 11770304. DOI: 10.3168/jdsc.2024-0625.

Vitamin C Improves Oocyte In Vitro Maturation and Potentially Changes Embryo Quality in Cattle.

Wang Y, Wang A, Liu H, Yang R, Zhang B, Tang B Vet Sci. 2024; 11(8).

PMID: 39195826 PMC: 11360740. DOI: 10.3390/vetsci11080372.

IVM Advances for Early Antral Follicle-Enclosed Oocytes Coupling Reproductive Tissue Engineering to Inductive Influences of Human Chorionic Gonadotropin and Ovarian Surface Epithelium Coculture.

Peserico A, Di Berardino C, Capacchietti G, Camerano Spelta Rapini C, Liverani L, Boccaccini A Int J Mol Sci. 2023; 24(7).

PMID: 37047595 PMC: 10095509. DOI: 10.3390/ijms24076626.

Sperm selection by the oviduct: perspectives for male fertility and assisted reproductive technologies†.

Soto-Heras S, Sakkas D, Miller D Biol Reprod. 2023; 108(4):538-552.

PMID: 36625382 PMC: 10106845. DOI: 10.1093/biolre/ioac224.

References

Meijer L, Borgne A, Mulner O, Chong J, J Blow J, Inagaki N . Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem. 1997; 243(1-2):527-36. DOI: 10.1111/j.1432-1033.1997.t01-2-00527.x. View

Lonergan P, Faerge I, Hyttel P, Boland M, Fair T . Ultrastructural modifications in bovine oocytes maintained in meiotic arrest in vitro using roscovitine or butyrolactone. Mol Reprod Dev. 2003; 64(3):369-78. DOI: 10.1002/mrd.10206. View

Richard S, Baltz J . Prophase I arrest of mouse oocytes mediated by natriuretic peptide precursor C requires GJA1 (connexin-43) and GJA4 (connexin-37) gap junctions in the antral follicle and cumulus-oocyte complex. Biol Reprod. 2014; 90(6):137. DOI: 10.1095/biolreprod.114.118505. View

Diogenes M, Guimaraes A, Leme L, Mauricio M, Dode M . Effect of prematuration and maturation with fibroblast growth factor 10 (FGF10) on in vitro development of bovine oocytes. Theriogenology. 2017; 102:190-198. DOI: 10.1016/j.theriogenology.2017.06.004. View

PINCUS G, Enzmann E . THE COMPARATIVE BEHAVIOR OF MAMMALIAN EGGS IN VIVO AND IN VITRO : I. THE ACTIVATION OF OVARIAN EGGS. J Exp Med. 2009; 62(5):665-75. PMC: 2133299. DOI: 10.1084/jem.62.5.665. View

Sa Barretto L, Castro V, Garcia J, Mingoti G . Meiotic inhibition of bovine oocytes in medium supplemented with a serum replacer and hormones: effects on meiosis progression and developmental capacity. Zygote. 2010; 19(2):107-16. DOI: 10.1017/S096719941000016X. View

Dieci C, Lodde V, Franciosi F, Lagutina I, Tessaro I, Modina S . The effect of cilostamide on gap junction communication dynamics, chromatin remodeling, and competence acquisition in pig oocytes following parthenogenetic activation and nuclear transfer. Biol Reprod. 2013; 89(3):68. DOI: 10.1095/biolreprod.113.110577. View

Conti M, Hsieh M, Zamah A, Oh J . Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol Cell Endocrinol. 2011; 356(1-2):65-73. PMC: 4104635. DOI: 10.1016/j.mce.2011.11.002. View

Lodde V, Modina S, Galbusera C, Franciosi F, Luciano A . Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol Reprod Dev. 2006; 74(6):740-9. DOI: 10.1002/mrd.20639. View

10.

Jee B, Chen H, Chian R . Effect of a phosphodiesterase type 3 inhibitor in oocyte maturation medium on subsequent mouse embryo development. Fertil Steril. 2008; 91(5 Suppl):2037-42. DOI: 10.1016/j.fertnstert.2008.03.041. View

11.

Guixue Z, Luciano A, Coenen K, Gandolfi F, Sirard M . The influence of cAMP before or during bovine oocyte maturation on embryonic developmental competence. Theriogenology. 2001; 55(8):1733-43. DOI: 10.1016/s0093-691x(01)00516-7. View

12.

Conti M, Franciosi F . Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Hum Reprod Update. 2018; 24(3):245-266. PMC: 5907346. DOI: 10.1093/humupd/dmx040. View

13.

Luciano A, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F . Role of intracellular cyclic adenosine 3',5'-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod. 2003; 70(2):465-72. DOI: 10.1095/biolreprod.103.020644. View

14.

Zhang M, Su Y, Sugiura K, Xia G, Eppig J . Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science. 2010; 330(6002):366-9. PMC: 3056542. DOI: 10.1126/science.1193573. View

15.

Ozawa M, Nagai T, Somfai T, Nakai M, Maedomari N, Fahrudin M . Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap junctional communication, LH-receptor expression, and meiotic maturation of cumulus-oocyte complexes in pigs. Mol Reprod Dev. 2007; 75(5):857-66. DOI: 10.1002/mrd.20820. View

16.

Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina S, Fadini R . Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol Reprod. 2014; 91(3):61. DOI: 10.1095/biolreprod.114.118869. View

17.

Luciano A, Peluso J . Effect of in vivo gonadotropin treatment on the ability of progesterone, estrogen, and cyclic adenosine 5'-monophosphate to inhibit insulin-dependent granulosa cell mitosis in vitro. Biol Reprod. 1995; 53(3):664-9. DOI: 10.1095/biolreprod53.3.664. View

18.

Vaccari S, Weeks 2nd J, Hsieh M, Menniti F, Conti M . Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod. 2009; 81(3):595-604. PMC: 2731981. DOI: 10.1095/biolreprod.109.077768. View

19.

Donnay I, Faerge I, Grondahl C, Verhaeghe B, Sayoud H, Ponderato N . Effect of prematuration, meiosis activating sterol and enriched maturation medium on the nuclear maturation and competence to development of calf oocytes. Theriogenology. 2004; 62(6):1093-107. DOI: 10.1016/j.theriogenology.2003.12.019. View

20.

Rose R, Gilchrist R, Kelly J, Thompson J, Sutton-McDowall M . Regulation of sheep oocyte maturation using cAMP modulators. Theriogenology. 2012; 79(1):142-8. DOI: 10.1016/j.theriogenology.2012.09.020. View