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International journal of molecular sciences2025; 26(12); 5495; doi: 10.3390/ijms26125495

Biphasic CAPA-IVM Improves Equine Oocyte Quality and Subsequent Embryo Development Without Inducing Genetic Aberrations.

Abstract: In vitro maturation (IVM) of oocytes retrieved from ovum pick-up (OPU) or ovarian tissue (OT) is a standard approach for patients with specific conditions where prior hormonal stimulation is contraindicated. However, the developmental competence of oocytes matured in vitro is still inferior to that of oocytes matured in vivo. Capacitation IVM (CAPA-IVM) includes an extra step of pre-maturation culture (PMC) with c-type natriuretic peptide (CNP) as a meiotic arrestor to better synchronize cytoplasmic and nuclear maturity in oocytes by allowing the cytoplasm additional time to acquire essential components critical for optimal competency. This study aims to evaluate the effect of CAPA-IVM on equine oocyte quality and developmental competence. Immature cumulus-oocyte complexes (COCs) were retrieved from slaughterhouse ovaries and matured in vitro either in CAPA-IVM (short 6 h, long 24 h pre-maturation) or standard IVM. Mature oocytes from each group were analyzed for calcium-releasing potential ( = 52) and single-oocyte proteomics ( = 44), and embryo development ( = 229) was assessed after fertilization with piezo-drilled intracytoplasmic sperm injection (ICSI). Genetic analysis of developed blastocysts ( = 41) was performed to detect chromosomal aberrations. Our findings demonstrate that CAPA-IVM of equine COCs yields significantly higher maturation rates than controls. Moreover, short CAPA-IVM with six hours pre-maturation culture showed substantially higher embryo development potential than the control group (20/69 vs. 9/63, respectively). Genetic analysis revealed a high euploidy rate in equine blastocysts regardless of the maturation conditions. Live calcium imaging of the fertilized oocytes demonstrated that the majority of oocytes displayed non-continuous calcium oscillation patterns, irrespective of maturation conditions. Single-oocyte proteomics reveals a comparable proteomic landscape between mature oocytes subjected to short CAPA-IVM and standard IVM. However, we identified four enriched gene sets with positive enrichment scores after short CAPA-IVM, related to cytoskeleton regulation, ribosomal function, and cytosolic components. Our findings indicate that CAPA-IVM holds the potential to improve oocyte quality and competence in horses. However, further fine-tuning of culture conditions would benefit the effective use of these IVM systems. Moreover, given that the mare serves as an excellent model for human reproduction, the molecular trends identified in this study could provide valuable insights for advancing human artificial reproductive technologies.
Publication Date: 2025-06-08 PubMed ID: 40564960PubMed Central: PMC12192595DOI: 10.3390/ijms26125495Google Scholar: Lookup
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  • Journal Article

Summary

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This research evaluates the impact of a specific in-vitro maturation method, known as CAPA-IVM, on the quality and developmental competence of horse oocytes. The study reveals that this method improves oocyte quality and developmental potential without causing genetic abnormalities.

Research Background

In the world of assisted reproduction, in-vitro maturation (IVM) of oocytes is commonly used, especially in cases where prior hormonal stimulation is not advisable. The key challenge with this is that oocytes matured in a laboratory setting often don’t reach the level of developmental competence of those matured in a host organism. This research evaluates a particular IVM method known as Capacitation IVM (CAPA-IVM), which includes an additional pre-maturation step. The purpose of this step is to better synchronize the oocyte’s cytoplasmic and nuclear maturity by extending the time for cytoplasm to accrue essential components.

  • The study was carried out on immature cumulus-oocyte complexes (COCs) extracted from slaughterhouse ovaries.
  • The oocytes were matured in vitro through the CAPA-IVM technique with two forms of pre-maturation: a short 6-hour procedure and a longer 24-hour procedure. These were compared against standard IVM.
  • The matured oocytes from all three groups were subjected to several analyses: calcium-releasing potential, single-oocyte proteomics, and post-fertilization embryo development.
  • The developed blastocysts were genetically analyzed to detect chromosomal aberrations.

Key Findings

The study demonstrated that CAPA-IVM yielded significantly better maturation rates than the control samples. Furthermore, the shorter form of CAPA-IVM, with just six hours pre-maturation, showed considerably better embryo development potential than the control samples.

  • Importantly, the genetic analysis of the resulting blastocysts revealed a high rate of euploidy (normal number of chromosomes) regardless of the maturation conditions.
  • The majority of the fertilized oocytes exhibited non-continuous patterns of calcium oscillation, irrespective of the maturation technique used.
  • Proteomics analysis revealed essentially similar landscapes between mature oocytes from the short CAPA-IVM and the standard IVM, though four enriched gene sets were identified in the short CAPA-IVM, relating to cytoskeleton regulation, ribosomal function, and cytosolic components.

Implications of the Research

These findings suggest that CAPA-IVM could be a significant tool in improving the quality and developmental competency of oocytes. The evidence of high rates of euploidy indicates that this technique does not exacerbate genetic abnormalities. However, more adjustments and fine-tuning of the culture conditions may be required to make full, effective use of such IVM systems. Considering that the physiological characteristics of horse reproduction closely mirror that of humans, these findings could potentially provide valuable insights that could advance human artificial reproductive technologies.

Cite This Article

APA
Fakhar-I-Adil M, Angel-Velez D, Araftpoor E, Amin QA, Hedia M, Bühler M, Gevaert K, Menten B, Van Soom A, Chuva de Sousa Lopes SM, Stoop D, De Roo C, Smits K, Heindryckx B. (2025). Biphasic CAPA-IVM Improves Equine Oocyte Quality and Subsequent Embryo Development Without Inducing Genetic Aberrations. Int J Mol Sci, 26(12), 5495. https://doi.org/10.3390/ijms26125495

Publication

ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 26
Issue: 12
PII: 5495

Researcher Affiliations

Fakhar-I-Adil, Muhammad
  • Ghent-Fertility and Stem Cell Team (G-FaST), Department for Reproductive Medicine, Department of Human Structure and Repair, Ghent University Hospital, Corneel Heymanslaan 10, 9000 Ghent, Belgium.
Angel-Velez, Daniel
  • Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, 9820 Merelbeke, Belgium.
Araftpoor, Emin
  • VIB-UGent Center for Medical Biotechnology, Vlaams Instituut voor Biotechnologie (VIB), 9052 Ghent, Belgium.
  • Department of Biomolecular Medicine, Ghent University, 9052 Ghent, Belgium.
Amin, Qurratul Ain
  • Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, 9820 Merelbeke, Belgium.
Hedia, Mohamed
  • Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, 9820 Merelbeke, Belgium.
  • Theriogenology Department, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt.
Bühler, Marcel
  • VIB-UGent Center for Medical Biotechnology, Vlaams Instituut voor Biotechnologie (VIB), 9052 Ghent, Belgium.
  • Department of Biomolecular Medicine, Ghent University, 9052 Ghent, Belgium.
Gevaert, Kris
  • VIB-UGent Center for Medical Biotechnology, Vlaams Instituut voor Biotechnologie (VIB), 9052 Ghent, Belgium.
  • Department of Biomolecular Medicine, Ghent University, 9052 Ghent, Belgium.
Menten, Björn
  • Center for Medical Genetics, Ghent University Hospital, 9000 Ghent, Belgium.
Van Soom, Ann
  • Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, 9820 Merelbeke, Belgium.
Chuva de Sousa Lopes, Susana Marina
  • Department of Anatomy and Embryology, Leiden University Medical Center, 2333 ZA Leiden, The Netherlands.
Stoop, Dominic
  • Department for Reproductive Medicine, Women's Clinic, Ghent University Hospital, Corneel Heymanslaan 10, 9000 Ghent, Belgium.
De Roo, Chloë
  • Department for Reproductive Medicine, Women's Clinic, Ghent University Hospital, Corneel Heymanslaan 10, 9000 Ghent, Belgium.
Smits, Katrien
  • Department of Internal Medicine, Reproduction and Population Medicine, Ghent University, 9820 Merelbeke, Belgium.
Heindryckx, Björn
  • Ghent-Fertility and Stem Cell Team (G-FaST), Department for Reproductive Medicine, Department of Human Structure and Repair, Ghent University Hospital, Corneel Heymanslaan 10, 9000 Ghent, Belgium.

MeSH Terms

  • Animals
  • Horses
  • Oocytes / metabolism
  • Oocytes / cytology
  • In Vitro Oocyte Maturation Techniques / methods
  • In Vitro Oocyte Maturation Techniques / veterinary
  • Female
  • Embryonic Development
  • Blastocyst / metabolism
  • Blastocyst / cytology
  • Chromosome Aberrations
  • Cumulus Cells / cytology
  • Cumulus Cells / metabolism
  • Sperm Injections, Intracytoplasmic
  • Natriuretic Peptide, C-Type / pharmacology

Grant Funding

  • BOF.STG.2021.0042.01 / Bijzonder Onderzoeksfonds
  • 1177425N / Research Foundation - Flanders
  • 2018000504 (GOA030-18 BOF) / Bijzonder Onderzoeksfonds (BOF)

Conflict of Interest Statement

The authors declare that they have no conflicts of interest.

References

This article includes 91 references
  1. Gong X, Li H, Zhao Y. The Improvement and Clinical Application of Human Oocyte In Vitro Maturation (IVM). Reprod. Sci. 2022;29:2127–2135.
    doi: 10.1007/s43032-021-00613-3pubmed: 34076873google scholar: lookup
  2. Maclellan L, Carnevale E, Da Silva M.C, Scoggin C, Bruemmer J, Squires E. Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares. Theriogenology 2002;58:911–919.
    doi: 10.1016/S0093-691X(02)00920-2pubmed: 12212891google scholar: lookup
  3. Hinrichs K. Immature oocyte collection and maturation. In: McKinnon A.O., Squires E.L., Vaala W.E., Varner D.D., editors. Equine Reproduction. 2nd ed. Volume 2. Wiley-Blackwell; Ames, IA, USA: 2011. pp. 2931–2935.
  4. He M, Zhang T, Yang Y, Wang C. Mechanisms of Oocyte Maturation and Related Epigenetic Regulation. Front. Cell Dev. Biol. 2021;9:654028.
    doi: 10.3389/fcell.2021.654028pmc: PMC8025927pubmed: 33842483google scholar: lookup
  5. Scott T.J, Carnevale E, Maclellan L, Scoggin C, Squires E. Embryo development rates after transfer of oocytes matured in vivo, in vitro, or within oviducts of mares. Theriogenology 2001;55:705–715.
    doi: 10.1016/S0093-691X(01)00438-1pubmed: 11245260google scholar: lookup
  6. Foss R, Ortis H, Hinrichs K. Effect of potential oocyte transport protocols on blastocyst rates after intracytoplasmic sperm injection in the horse. Equine Vet. J. 2013;45:39–43.
    doi: 10.1111/evj.12159pubmed: 24304402google scholar: lookup
  7. Hyttel P, Fair T, Callesen H, Greve T. Oocyte growth, capacitation and final maturation in cattle. Theriogenology 1997;47:23–32.
  8. Hendriksen P, Vos P, Steenweg W, Bevers M, Dieleman S. Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 2000;53:11–20.
    doi: 10.1016/S0093-691X(99)00236-8pubmed: 10735058google scholar: lookup
  9. Sun G.-Y, Gong S, Kong Q.-Q, Li Z.-B, Wang J, Xu M.-T, Luo M.-J, Tan J.-H. Role of AMP-activated protein kinase during postovulatory aging of mouse oocytes. Biol. Reprod. 2020;103:534–547.
    doi: 10.1093/biolre/ioaa081pubmed: 32588041google scholar: lookup
  10. Norris R.P, Ratzan W.J, Freudzon M, Mehlmann L.M, Krall J, Movsesian M.A, Wang H, Ke H, Nikolaev V.O, Jaffe L.A. Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 2009;136:1869–1878.
    doi: 10.1242/dev.035238pmc: PMC2680110pubmed: 19429786google scholar: lookup
  11. Vaccari S, Weeks J.L, Hsieh M, Menniti F.S, Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol. Reprod. 2009;81:595–604.
  12. Hyttel P, Greve T, Callesen H. Ultrastructural aspects of oocyte maturation and fertilization in cattle. J. Reprod. Fertil. Suppl. 1989;38:35–47.
    pubmed: 2677348
  13. Zhu S, Wang Q. Metabolic control of oocyte development. Biol. Reprod. 2022;107:54–61.
    doi: 10.1093/biolre/ioac082pubmed: 35470861google scholar: lookup
  14. Leal G.R, Monteiro C.A.S, Souza-Fabjan J.M.G, de Paula Vasconcelos C.O, Nogueira L.A.G, Ferreira A.M.R, Serapião R.V. Role of cAMP modulator supplementations during oocyte in vitro maturation in domestic animals. Anim. Reprod. Sci. 2018;199:1–14.
  15. Gilchrist R.B, Ho T.M, De Vos M, Sanchez F, Romero S, Ledger W.L, Anckaert E, Vuong L.N, Smitz J. A fresh start for IVM: Capacitating the oocyte for development using pre-IVM. Hum. Reprod. Update 2023;30:3–25.
    doi: 10.1093/humupd/dmad023pubmed: 37639630google scholar: lookup
  16. Zuccotti M, Giorgi Rossi P, Martinez A, Garagna S, Forabosco A, Redi C.A. Meiotic and developmental competence of mouse antral oocytes. Biol. Reprod. 1998;58:700–704.
    doi: 10.1095/biolreprod58.3.700pubmed: 9510956google scholar: lookup
  17. Funahashi H, Cantley T.C, Day B.N. Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol. Reprod. 1997;57:49–53.
    doi: 10.1095/biolreprod57.1.49pubmed: 9209079google scholar: lookup
  18. Luciano A.M, Franciosi F, Modina S.C, Lodde V. Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism (s). Biol. Reprod. 2011;85:1252–1259.
    doi: 10.1095/biolreprod.111.092858pubmed: 21816847google scholar: lookup
  19. Nogueira D, Cortvrindt R, De Matos D, Vanhoutte L, Smitz J. Effect of phosphodiesterase type 3 inhibitor on developmental competence of immature mouse oocytes in vitro. Biol. Reprod. 2003;69:2045–2052.
    doi: 10.1095/biolreprod.103.021105pubmed: 12930710google scholar: lookup
  20. Somfai T, Kikuchi K, Onishi A, Iwamoto M, Fuchimoto D.-I, Papp Á.B, Sato E, Nagai T. Meiotic arrest maintained by cAMP during the initiation of maturation enhances meiotic potential and developmental competence and reduces polyspermy of IVM/IVF porcine oocytes. Zygote 2003;11:199–206.
    doi: 10.1017/S0967199403002247pubmed: 14640184google scholar: lookup
  21. Albuz F, Sasseville M, Lane M, Armstrong D, Thompson J, Gilchrist R. Simulated physiological oocyte maturation (SPOM): A novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. Hum. Reprod. 2010;25:2999–3011.
    doi: 10.1093/humrep/deq246pubmed: 20870682google scholar: lookup
  22. 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;55:1733–1743.
    doi: 10.1016/S0093-691X(01)00516-7pubmed: 11393223google scholar: lookup
  23. Zhang M, Su Y.-Q, Sugiura K, Xia G, Eppig J.J. Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 2010;330:366–369.
    doi: 10.1126/science.1193573pmc: PMC3056542pubmed: 20947764google scholar: lookup
  24. Franciosi F, Coticchio G, Lodde V, Tessaro I, Modina S.C, Fadini R, Dal Canto M, Renzini M.M, Albertini D.F, Luciano A.M. Natriuretic peptide precursor C delays meiotic resumption and sustains gap junction-mediated communication in bovine cumulus-enclosed oocytes. Biol. Reprod. 2014;91:61, 61–69.
    doi: 10.1095/biolreprod.114.118869pubmed: 25078681google scholar: lookup
  25. Kirillova A, Bunyaeva E, Van Ranst H, Khabas G, Farmakovskaya M, Kamaletdinov N, Nazarenko T, Abubakirov A, Sukhikh G, Smitz J.E.J. Improved maturation competence of ovarian tissue oocytes using a biphasic in vitro maturation system for patients with gynecological malignancy: A study on sibling oocytes. J. Assist. Reprod. Genet. 2021;38:1331–1340.
    doi: 10.1007/s10815-021-02118-zpmc: PMC8266929pubmed: 33619680google scholar: lookup
  26. Sanchez F, Le A.H, Ho V.N.A, Romero S, Van Ranst H, De Vos M, Gilchrist R.B, Ho T.M, Vuong L.N, Smitz J. Biphasic in vitro maturation (CAPA-IVM) specifically improves the developmental capacity of oocytes from small antral follicles. J. Assist. Reprod. Genet. 2019;36:2135–2144.
    doi: 10.1007/s10815-019-01551-5pmc: PMC6823411pubmed: 31399916google scholar: lookup
  27. Sánchez F, Lolicato F, Romero S, De Vos M, Van Ranst H, Verheyen G, Anckaert E, Smitz J.E.J. An improved IVM method for cumulus-oocyte complexes from small follicles in polycystic ovary syndrome patients enhances oocyte competence and embryo yield. Hum. Reprod. 2017;32:2056–2068.
    doi: 10.1093/humrep/dex262pubmed: 28938744google scholar: lookup
  28. Akin N, Le A.H, Ha U.D.T, Romero S, Sanchez F, Pham T.D, Nguyen M.H.N, Anckaert E, Ho T.M, Smitz J. Positive effects of amphiregulin on human oocyte maturation and its molecular drivers in patients with polycystic ovary syndrome. Hum. Reprod. 2022;37:30–43.
    doi: 10.1093/humrep/deab237pubmed: 34741172google scholar: lookup
  29. Vuong L.N, Ho V.N, Ho T.M, Dang V.Q, Phung T.H, Giang N.H, Le A.H, Pham T.D, Wang R, Smitz J. In-vitro maturation of oocytes versus conventional IVF in women with infertility and a high antral follicle count: A randomized non-inferiority controlled trial. Hum. Reprod. 2020;35:2537–2547.
    doi: 10.1093/humrep/deaa240pubmed: 32974672google scholar: lookup
  30. Vuong L.N, Le A.H, Ho V.N, Pham T.D, Sanchez F, Romero S, De Vos M, Ho T.M, Gilchrist R.B, Smitz J. Live births after oocyte in vitro maturation with a prematuration step in women with polycystic ovary syndrome. J. Assist. Reprod. Genet. 2020;37:347–357.
    doi: 10.1007/s10815-019-01677-6pmc: PMC7056678pubmed: 31902102google scholar: lookup
  31. Vuong L.N, Nguyen L.K, Le A.H, Pham H.H, Ho V.N, Le H.L, Pham T.D, Dang V.Q, Phung T.H, Smitz J. Fresh embryo transfer versus freeze-only after in vitro maturation with a pre-maturation step in women with high antral follicle count: A randomized controlled pilot study. J. Assist. Reprod. Genet. 2021;38:1293–1302.
    doi: 10.1007/s10815-021-02180-7pmc: PMC8266980pubmed: 33825118google scholar: lookup
  32. McLaughlin M, Albertini D, Wallace W, Anderson R, Telfer E. Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. MHR Basic Sci. Reprod. Med. 2018;24:135–142.
    doi: 10.1093/molehr/gay002pubmed: 29390119google scholar: lookup
  33. Xu F, Lawson M.S, Bean Y, Ting A.Y, Pejovic T, De Geest K, Moffitt M, Mitalipov S.M, Xu J. Matrix-free 3D culture supports human follicular development from the unilaminar to the antral stage in vitro yielding morphologically normal metaphase II oocytes. Hum. Reprod. 2021;36:1326–1338.
    doi: 10.1093/humrep/deab003pmc: PMC8600176pubmed: 33681988google scholar: lookup
  34. Guo Y, Jia L, Zeng H, Sun P, Su W, Li T, Liang X, Fang C. Neurotrophin-4 promotes in vitro development and maturation of human secondary follicles yielding metaphase II oocytes and successful blastocyst formation. Hum. Reprod. Open 2024;2024:hoae005.
    doi: 10.1093/hropen/hoae005pmc: PMC10873269pubmed: 38371224google scholar: lookup
  35. Cuervo-Arango J, Claes A.N, Stout T.A. Mare and stallion effects on blastocyst production in a commercial equine ovum pick-up–intracytoplasmic sperm injection program. Reprod. Fertil. Dev. 2019;31:1894–1903.
    doi: 10.1071/RD19201pubmed: 31634435google scholar: lookup
  36. Choi Y.H, Love L.B, Varner D.D, Hinrichs K. Blastocyst development in equine oocytes with low meiotic competence after suppression of meiosis with roscovitine prior to in vitro maturation. Zygote 2006;14:1–8.
    doi: 10.1017/S0967199406003534pubmed: 16700969google scholar: lookup
  37. Choi Y.H, Love L.B, Varner D.D, Hinrichs K. Holding immature equine oocytes in the absence of meiotic inhibitors: Effect on germinal vesicle chromatin and blastocyst development after intracytoplasmic sperm injection. Theriogenology 2006;66:955–963.
  38. Broothaers K, Pascottini O.B, Hedia M, Angel-Velez D, De Coster T, Peere S, Polfliet E, Van den Branden E, Govaere J, Van Soom A. Oocyte holding and in vitro maturation duration between 28 and 34 hours do not affect equine OPU-ICSI outcomes. Theriogenology 2025;233:64–69.
  39. Metcalf E.S, Masterson K.R, Battaglia D, Thompson J.G, Foss R, Beck R, Cook N.L, O’Leary T. Conditions to optimise the developmental competence of immature equine oocytes. Reprod. Fertil. Dev. 2020;32:1012–1021.
    doi: 10.1071/RD19249pubmed: 32693913google scholar: lookup
  40. Lodde V, Colleoni S, Tessaro I, Corbani D, Lazzari G, Luciano A.M, Galli C, Franciosi F. A prematuration approach to equine IVM: Considering cumulus morphology, seasonality, follicle of origin, gap junction coupling and large-scale chromatin configuration in the germinal vesicle. Reprod. Fertil. Dev. 2019;31:1793–1804.
    doi: 10.1071/RD19230pubmed: 31630726google scholar: lookup
  41. Benammar A, Derisoud E, Vialard F, Palmer E, Ayoubi J.M, Poulain M, Chavatte-Palmer P. The Mare: A Pertinent Model for Human Assisted Reproductive Technologies?. Animals 2021;11:2304.
    doi: 10.3390/ani11082304pmc: PMC8388489pubmed: 34438761google scholar: lookup
  42. Carnevale E.M, Catandi G.D, Fresa K. Equine Aging and the Oocyte: A Potential Model for Reproductive Aging in Women. J. Equine Vet. Sci. 2020;89:103022.
    doi: 10.1016/j.jevs.2020.103022pubmed: 32563447google scholar: lookup
  43. Nogueira D, Ron-El R, Friedler S, Schachter M, Raziel A, Cortvrindt R, Smitz J. Meiotic Arrest In Vitro by Phosphodiesterase 3-Inhibitor Enhances Maturation Capacity of Human Oocytes and Allows Subsequent Embryonic Development1. Biol. Reprod. 2006;74:177–184.
    doi: 10.1095/biolreprod.105.040485pubmed: 16207840google scholar: lookup
  44. Santiquet N.W, Greene A.F, Becker J, Barfield J.P, Schoolcraft W.B, Krisher R.L. A pre-in vitro maturation medium containing cumulus oocyte complex ligand-receptor signaling molecules maintains meiotic arrest, supports the cumulus oocyte complex and improves oocyte developmental competence. Mol. Hum. Reprod. 2017;23:594–606.
    doi: 10.1093/molehr/gax032pubmed: 28586460google scholar: lookup
  45. Morishita N, Shibata K, Matsunaga R, Ochi M, Horiuchi T. Novel CAPA-IVM using dibutyryl-cAMP (DBCAMP) and C-type natriuretic peptide (CNP): Bovine model study for human IVM of oocytes. Fertil. Steril. 2020;114:e353.
  46. Farghaly T, Khalifa E, Mostafa S, Hussein M, Bedaiwy M, Ahmady A. The effect of temporary meiotic attenuation on the in vitro maturation outcome of bovine oocytes. Vitr. Cell. Dev. Biology. Anim. 2015;51:662–671.
    doi: 10.1007/s11626-015-9878-ypubmed: 25784604google scholar: lookup
  47. Abdel-Ghani M.A, Sakaguchi K, Kanno C, Yanagawa Y, Katagiri S, Nagano M. Effects of pre-maturational culture duration on developmental competence of bovine small-sized oocytes. J. Reprod. Dev. 2018;64:365–369.
    doi: 10.1262/jrd.2018-004pmc: PMC6105738pubmed: 29798966google scholar: lookup
  48. Galatidou S, Petelski A.A, Pujol A, Lattes K, Latorraca L.B, Fair T, Popovic M, Vassena R, Slavov N, Barragán M. Single-cell proteomics reveals decreased abundance of proteostasis and meiosis proteins in advanced maternal age oocytes. Mol. Hum. Reprod. 2024;30:gaae023.
    doi: 10.1093/molehr/gaae023pmc: PMC12106276pubmed: 38870523google scholar: lookup
  49. Zhang H, Zhang H, Huang C, Zeng Q, Tian C, He F, Yang Y. Simple One-step Vial-based Pretreatment for Deep Single-cell Proteomics and Its Application to Oocyte Aging. bioRxiv 2024.
    doi: 10.1101/2024.12.03.626713google scholar: lookup
  50. Soto-Heras S, Paramio M.-T, Thompson J.G. Effect of pre-maturation with C-type natriuretic peptide and 3-isobutyl-1-methylxanthine on cumulus-oocyte communication and oocyte developmental competence in cattle. Anim. Reprod. Sci. 2019;202:49–57.
  51. Gong X, Shen L, Zhang H, Ai J, Gilchrist R.B, Zhao Y. CAPA-IVM improves the cytoplasmic quality of in vitro-matured oocytes from unstimulated mice. Theriogenology 2023;212:117–128.
  52. Guelman V, Patrizio P. A Color Atlas for Human Assisted Reproduction. Lippincott Williams & Wilkins; Philadelphia, PA, USA: 2003. The oocyte; pp. 25–47.
  53. Takahashi T, Igarashi H, Amita M, Hara S, Kurachi H. Cellular and molecular mechanisms of various types of oocyte aging. Reprod. Med. Biol. 2011;10:239–249.
    doi: 10.1007/s12522-011-0099-0pmc: PMC5904634pubmed: 29699098google scholar: lookup
  54. Miao Y, Ma S, Liu X, Miao D, Chang Z, Luo M, Tan J. Fate of the first polar bodies in mouse oocytes. Mol. Reprod. Dev. Inc. Gamete Res. 2004;69:66–76.
    doi: 10.1002/mrd.20148pubmed: 15278906google scholar: lookup
  55. Gilula N.B, Epstein M.L, Beers W.H. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex. J. Cell Biol. 1978;78:58–75.
    doi: 10.1083/jcb.78.1.58pmc: PMC2110163pubmed: 670298google scholar: lookup
  56. Colonna R, Mangia F. Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes. Biol. Reprod. 1983;28:797–803.
    doi: 10.1095/biolreprod28.4.797pubmed: 6860738google scholar: lookup
  57. Luciano A.M, Franciosi F, Dieci C, Lodde V. Changes in large-scale chromatin structure and function during oogenesis: A journey in company with follicular cells. Anim. Reprod. Sci. 2014;149:3–10.
  58. Gharibi S, Hajian M, Ostadhosseini S, Hosseini S, Forouzanfar M, Nasr-Esfahani M. Effect of phosphodiesterase type 3 inhibitor on nuclear maturation and in vitro development of ovine oocytes. Theriogenology 2013;80:302–312.
  59. Li H, Sutton-McDowall M, Wang X, Sugimura S, Thompson J, Gilchrist R. Extending prematuration with cAMP modulators enhances the cumulus contribution to oocyte antioxidant defence and oocyte quality via gap junctions. Hum. Reprod. 2016;31:810–821.
    doi: 10.1093/humrep/dew020pubmed: 26908844google scholar: lookup
  60. Romero S, Sánchez F, Lolicato F, Van Ranst H, Smitz J. Immature oocytes from unprimed juvenile mice become a valuable source for embryo production when using C-type natriuretic peptide as essential component of culture medium. Biol. Reprod. 2016;95:64.
    doi: 10.1095/biolreprod.116.139808pubmed: 27488026google scholar: lookup
  61. Lin T, Lee J.E, Kang J.W, Oqani R.K, Cho E.S, Kim S.B, Il Jin D. Melatonin supplementation during prolonged in vitro maturation improves the quality and development of poor-quality porcine oocytes via anti-oxidative and anti-apoptotic effects. Mol. Reprod. Dev. 2018;85:665–681.
    doi: 10.1002/mrd.23052pubmed: 30106229google scholar: lookup
  62. Altermatt J.L, Suh T.K, Stokes J.E, Carnevale E.M. 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;21:615–623.
    doi: 10.1071/RD08210pubmed: 19383268google scholar: lookup
  63. Li X, Mu Y, Elshewy N, Ding D, Zou H, Chen B, Wei Z, Cao Y, Zhou P, Zhang Z. Comparison of IVF and IVM outcomes in the same patient treated with a modified IVM protocol along with an oocytes-maturing system containing melatonin: A pilot study. Life Sci. 2021;264:118706.
    doi: 10.1016/j.lfs.2020.118706pubmed: 33152350google scholar: lookup
  64. Xi G, An L, Jia Z, Tan K, Zhang J, Wang Z, Zhang C, Miao K, Wu Z, Tian J. Natriuretic peptide receptor 2 (NPR2) localized in bovine oocyte underlies a unique mechanism for C-type natriuretic peptide (CNP)-induced meiotic arrest. Theriogenology 2018;106:198–209.
  65. Di Nisio V, Antonouli S, Damdimopoulou P, Salumets A, Cecconi S. In vivo and in vitro postovulatory aging: When time works against oocyte quality?. J. Assist. Reprod. Genet. 2022;39:905–918.
    doi: 10.1007/s10815-022-02418-ypmc: PMC9050976pubmed: 35312936google scholar: lookup
  66. Son W.-Y, Lee S.-Y, Lim J.-H. Fertilization, cleavage and blastocyst development according to the maturation timing of oocytes in in vitro maturation cycles. Hum. Reprod. 2005;20:3204–3207.
    doi: 10.1093/humrep/dei195pubmed: 16037117google scholar: lookup
  67. Yu Y, Yan J, Liu Z.C, Yan L.Y, Li M, Zhou Q, Qiao J. Optimal timing of oocyte maturation and its relationship with the spindle assembly and developmental competence of in vitro matured human oocytes. Fertil. Steril. 2011;96:73–78.e71.
  68. Zhang X.Y, Ata B, Son W.-Y, Buckett W.M, Tan S.-L, Ao A. Chromosome abnormality rates in human embryos obtained from in-vitro maturation and IVF treatment cycles. Reprod. Biomed. Online 2010;21:552–559.
    doi: 10.1016/j.rbmo.2010.05.002pubmed: 20800547google scholar: lookup
  69. Carrera C.A, González C, Díaz R.M, Gutierrez A.M, Hinrichs K. Prolonged maturation reduces cleavage and blastocyst rates after ICSI. J. Equine Vet. Sci. 2023;125:104637.
  70. Zhang J, Wei Q, Cai J, Zhao X, Ma B. Effect of C-Type Natriuretic Peptide on Maturation and Developmental Competence of Goat Oocytes Matured In Vitro. PLoS ONE 2015;10:e0132318.
  71. Bedford S.J, Kurokawa M, Hinrichs K, Fissore R.A. Intracellular calcium oscillations and activation in horse oocytes injected with stallion sperm extracts or spermatozoa. Reproduction 2003;126:489–499.
    doi: 10.1530/rep.0.1260489pubmed: 14525531google scholar: lookup
  72. Bedford S.J, Kurokawa M, Hinrichs K, Fissore R.A. Patterns of Intracellular Calcium Oscillations in Horse Oocytes Fertilized by Intracytoplasmic Sperm Injection: Possible Explanations for the Low Success of This Assisted Reproduction Technique in the Horse1. Biol. Reprod. 2004;70:936–944.
    doi: 10.1095/biolreprod.103.021485pubmed: 14656727google scholar: lookup
  73. Yeste M, Jones C, Amdani S.N, Coward K. Oocyte activation and fertilisation: Crucial contributors from the sperm and oocyte. Signal.-Mediat. Control Cell Div. Oogenesis Oocyte-Embryo Dev. 2017;59:213–239.
    pubmed: 28247051
  74. Zafar M.I, Lu S, Li H. Sperm-oocyte interplay: An overview of spermatozoon’s role in oocyte activation and current perspectives in diagnosis and fertility treatment. Cell Biosci. 2021;11:4.
    doi: 10.1186/s13578-020-00520-1pmc: PMC7789549pubmed: 33407934google scholar: lookup
  75. Kurokawa M, Fissore R.A. ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development. Mol. Hum. Reprod. 2003;9:523–533.
    doi: 10.1093/molehr/gag072pubmed: 12900511google scholar: lookup
  76. Dozortsev D, Rybouchkin A, De Sutter P, Dhont M. Sperm plasma membrane damage prior to intracytoplasmic sperm injection: A necessary condition for sperm nucleus decondensation. Hum. Reprod. 1995;10:2960–2964.
  77. Yanagida K, Katayose H, Hirata S, Yazawa H, Hayashi S, Sato A. Influence of sperm immobilization on onset of Ca2+ oscillations after ICSI. Hum. Reprod. 2001;16:148–152.
    doi: 10.1093/humrep/16.1.148pubmed: 11139554google scholar: lookup
  78. De Coster T, Zhao Y, Tšuiko O, Demyda-Peyrás S, Van Soom A, Vermeesch J, Smits K. Genome-wide equine preimplantation genetic testing enabled by simultaneous haplotyping and copy number detection. Sci. Rep. 2024;14:2003.
    doi: 10.1038/s41598-023-48103-7pmc: PMC10805710pubmed: 38263320google scholar: lookup
  79. Gu C, Li K, Li R, Li L, Li X, Dai X, He Y. Chromosomal aneuploidy associated with clinical characteristics of pregnancy loss. Front. Genet. 2021;12:667697.
    doi: 10.3389/fgene.2021.667697pmc: PMC8083898pubmed: 33936179google scholar: lookup
  80. Shilton C.A, Kahler A, Davis B.W, Crabtree J.R, Crowhurst J, McGladdery A.J, Wathes D.C, Raudsepp T, de Mestre A.M. Whole genome analysis reveals aneuploidies in early pregnancy loss in the horse. Sci. Rep. 2020;10:13314.
    doi: 10.1038/s41598-020-69967-zpmc: PMC7415156pubmed: 32769994google scholar: lookup
  81. Claes A, Stout T.A.E. Success rate in a clinical equine in vitro embryo production program. Theriogenology 2022;187:215–218.
  82. Dunkley S, Scheffler K, Mogessie B. Cytoskeletal form and function in mammalian oocytes and zygotes. Curr. Opin. Cell Biol. 2022;75:102073.
    doi: 10.1016/j.ceb.2022.02.007pubmed: 35364486google scholar: lookup
  83. Egbert J.R, Silbern I, Uliasz T.F, Lowther K.M, Yee S.-P, Urlaub H, Jaffe L.A. Phosphatases modified by LH signaling in ovarian follicles: Testing their role in regulating the NPR2 guanylyl cyclase†. Biol. Reprod. 2023;110:102–115.
    doi: 10.1093/biolre/ioad130pmc: PMC10790345pubmed: 37774352google scholar: lookup
  84. Hong Y, Lin Q, Zhang Y, Liu J, Zheng Z. Research Progress of Ribosomal Proteins in Reproductive Development. Int. J. Mol. Sci. 2024;25:13151.
    doi: 10.3390/ijms252313151pmc: PMC11642206pubmed: 39684863google scholar: lookup
  85. Angel-Velez D, De Coster T, Azari-Dolatabad N, Fernandez-Montoro A, Benedetti C, Bogado Pascottini O, Woelders H, Van Soom A, Smits K. New alternative mixtures of cryoprotectants for equine immature oocyte vitrification. Animals 2021;11:3077.
    doi: 10.3390/ani11113077pmc: PMC8614364pubmed: 34827809google scholar: lookup
  86. Leemans B, Gadella B.M, Stout T.A.E, Heras S, Smits K, Ferrer-Buitrago M, Claes E, Heindryckx B, De Vos W.H, Nelis H. Procaine Induces Cytokinesis in Horse Oocytes via a pH-Dependent Mechanism1. Biol. Reprod. 2015;93:1–17.
    doi: 10.1095/biolreprod.114.127423pubmed: 26085521google scholar: lookup
  87. Popovic M, Dheedene A, Christodoulou C, Taelman J, Dhaenens L, Van Nieuwerburgh F, Deforce D, Van den Abbeel E, De Sutter P, Menten B. Chromosomal mosaicism in human blastocysts: The ultimate challenge of preimplantation genetic testing?. Hum. Reprod. 2018;33:1342–1354.
    doi: 10.1093/humrep/dey106pubmed: 29796631google scholar: lookup
  88. Sante T, Vergult S, Volders P.-J, Kloosterman W.P, Trooskens G, De Preter K, Dheedene A, Speleman F, De Meyer T, Menten B. ViVar: A comprehensive platform for the analysis and visualization of structural genomic variation. PLoS ONE 2014;9:e113800.
  89. Raman L, Dheedene A, De Smet M, Van Dorpe J, Menten B. WisecondorX: Improved copy number detection for routine shallow whole-genome sequencing. Nucleic Acids Res. 2019;47:1605–1614.
    doi: 10.1093/nar/gky1263pmc: PMC6393301pubmed: 30566647google scholar: lookup
  90. Fernández Montoro A, Araftpoor E, De Coster T, Angel-Velez D, Bühler M, Hedia M, Gevaert K, Van Soom A, Pavani K.C, Smits K. Decoding bull fertility in vitro: A proteomics exploration from sperm to blastocyst. Reproduction 2025;169:e240296.
    doi: 10.1530/REP-24-0296pmc: PMC11949518pubmed: 40047448google scholar: lookup
  91. Kanehisa M, Furumichi M, Sato Y, Matsuura Y, Ishiguro-Watanabe M. KEGG: Biological systems database as a model of the real world. Nucleic Acids Res. 2024;53:D672–D677.
    doi: 10.1093/nar/gkae909pmc: PMC11701520pubmed: 39417505google scholar: lookup

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