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Scientific reports2020; 10(1); 3493; doi: 10.1038/s41598-020-60624-z

Energy metabolism of the equine cumulus oocyte complex during in vitro maturation.

Abstract: Horses are one of the few species, beside humans, in which assisted reproductive technology has important clinical applications. Furthermore, the horse can serve as a valuable model for the study of comparative reproductive biology. Here we present the first comprehensive characterisation of energy metabolism and mitochondrial efficiency in equine cumulus-oocyte complexes (COCs) during in vitro maturation (IVM), as determined using a combination of non-invasive consumption and release assays and mitochondrial function analysis. These data reveal notable species-specific differences in the rate and kinetics of glucose consumption and glycolysis throughout IVM. Approximately 95% of glucose consumed was accounted for by lactate production; however, high concurrent oxygen consumption indicated a comparatively increased role for non-glycolytic oxidative phosphorylation. Up to 38% of equine COC oxygen consumption could be attributed to non-mitochondrial activities and there was a significant loss of spare respiratory capacity over the course of IVM. Notably, our data also revealed that current IVM protocols may be failing to satisfy the metabolic demands of the equine COC. Our findings constitute the first report on mitochondrial efficiency in the equine COC and provide new insight into comparative gamete biology as well as metabolism of the COC during in vitro maturation.
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Publication Date: 2020-02-26 PubMed ID: 32103136PubMed Central: PMC7044441DOI: 10.1038/s41598-020-60624-zGoogle Scholar: Lookup
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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.

This research presents the first detailed analysis of energy metabolism in horse cumulus-oocyte complexes (COCs) during in vitro maturation, revealing unique characteristics of glucose consumption, glycolysis, oxygen consumption and mitochondrial efficiency that suggests current maturation protocols may not meet the metabolic needs of the COC.

Study Overview

  • This study is about understanding the intricate energy metabolism of a specific reproductive cell grouping in horses, called the cumulus-oocyte complexes (COCs) during in vitro (in the lab) maturation process.
  • The purpose of this research is not only to understand this process in horses specifically, but also to use the horse as a model for studying reproduction in other species, including humans.

Methods and Findings

  • The researchers used non-invasive consumption and release assays and mitochondrial function analysis to measure energy metabolism during COC’s in vitro maturation.
  • One finding was that horse COCs displayed unique patterns of glucose consumption and glycolysis (breakdown of glucose for energy) throughout in vitro maturation, compared to other species.
  • About 95% of glucose consumed was converted into lactate (a product of glycolysis). Simultaneously, high oxygen consumption indicated a significant role of non-glycolytic oxidative phosphorylation (a different energy-producing process).
  • Up to 38% of the oxygen consumption of horse COCs, however, was attributed to non-mitochondrial activities—actions not related to the cell’s powerhouses.
  • There was a significant loss of the COCs’ reserve energy over the course of in vitro maturation.

Implications

  • These findings show that current in vitro maturation practices may be insufficient for the metabolic demands of horse COCs.
  • This creates potential for improving these protocols to better accommodate the cell group’s unique metabolism during maturation.
  • The researchers’ findings on the horse COCs’ mitochondrial efficiency were the first of their kind—bringing new insights into how gametes (reproductive cells) function and metabolize energy in horses and possibly in other species as well.

Cite This Article

APA
Lewis N, Hinrichs K, Leese HJ, McG Argo C, Brison DR, Sturmey R. (2020). Energy metabolism of the equine cumulus oocyte complex during in vitro maturation. Sci Rep, 10(1), 3493. https://doi.org/10.1038/s41598-020-60624-z

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 10
Issue: 1
Pages: 3493
PII: 3493

Researcher Affiliations

Lewis, N
  • Institute of Ageing and Chronic Disease, University of Liverpool, Cheshire, UK. n.lewis@liv.ac.uk.
Hinrichs, K
  • Texas A&M University, College Station, Texas, USA.
Leese, H J
  • Cardiovascular and Metabolic Research, Hull York Medical School, University of Hull, Hull, Yorkshire, UK.
McG Argo, C
  • Institute of Ageing and Chronic Disease, University of Liverpool, Cheshire, UK.
  • Scotland's Rural College (SRUC), Northern Faculty, Craibstone Campus, Aberdeen, AB21 9YA, Scotland.
Brison, D R
  • Maternal and Fetal Health Research, Faculty of Biology, Medicine & Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK.
Sturmey, R
  • Cardiovascular and Metabolic Research, Hull York Medical School, University of Hull, Hull, Yorkshire, UK.

MeSH Terms

  • Animals
  • Cells, Cultured
  • Cumulus Cells / cytology
  • Energy Metabolism
  • Glucose / metabolism
  • Glycolysis
  • Horses
  • In Vitro Oocyte Maturation Techniques
  • Mitochondria / metabolism
  • Oocytes / cytology
  • Oocytes / metabolism
  • Oxygen Consumption

Grant Funding

  • Biotechnology and Biological Sciences Research Council

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 61 references
  1. Leemans B, Gadella BM, Stout TA, De Schauwer C, Nelis H, Hoogewijs M, Van Soom A. Why doesn't conventional IVF work in the horse? The equine oviduct as a microenvironment for capacitation/fertilization.. Reproduction 2016 Dec;152(6):R233-R245.
    doi: 10.1530/REP-16-0420pubmed: 27651517google scholar: lookup
  2. 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 Mar;123(3):455-65.
    doi: 10.1530/rep.0.1230455pubmed: 11882023google scholar: lookup
  3. Galli C, Colleoni S, Duchi R, Lagutina I, Lazzari G. Developmental competence of equine oocytes and embryos obtained by in vitro procedures ranging from in vitro maturation and ICSI to embryo culture, cryopreservation and somatic cell nuclear transfer.. Anim Reprod Sci 2007 Mar;98(1-2):39-55.
    doi: 10.1016/j.anireprosci.2006.10.011pubmed: 17101246google scholar: lookup
  4. Claes A, Cuervo-Arango J, van den Broek J, Galli C, Colleoni S, Lazzari G, Deelen C, Beitsma M, Stout TA. Factors affecting the likelihood of pregnancy and embryonic loss after transfer of cryopreserved in vitro produced equine embryos.. Equine Vet J 2019 Jul;51(4):446-450.
    doi: 10.1111/evj.13028pubmed: 30269336google scholar: lookup
  5. Hinrichs K, Choi YH, Love LB, Varner DD, Love CC, Walckenaer BE. Chromatin configuration within the germinal vesicle of horse oocytes: changes post mortem and relationship to meiotic and developmental competence.. Biol Reprod 2005 May;72(5):1142-50.
    doi: 10.1095/biolreprod.104.036012pubmed: 15647456google scholar: lookup
  6. Roser JF, Meyers-Brown G. Superovulation in the Mare: A Work in Progress.. J. Equine Vet. Sci. 2012;32:376–386.
    doi: 10.1016/j.jevs.2012.05.055google scholar: lookup
  7. Fleming TP, Watkins AJ, Velazquez MA, Mathers JC, Prentice AM, Stephenson J, Barker M, Saffery R, Yajnik CS, Eckert JJ, Hanson MA, Forrester T, Gluckman PD, Godfrey KM. Origins of lifetime health around the time of conception: causes and consequences.. Lancet 2018 May 5;391(10132):1842-1852.
    doi: 10.1016/S0140-6736(18)30312-Xpmc: PMC5975952pubmed: 29673874google scholar: lookup
  8. Zhang JJ, Boyle MS, Allen WR, Galli C. Recent studies on in vivo fertilisation of in vitro matured horse oocytes.. Equine Vet. J. 1989;21:101–104.
    doi: 10.1111/j.2042-3306.1989.tb04691.xgoogle scholar: lookup
  9. Gerard N. Concentrations of glucose, pyruvate and lactate in relation to follicular growth, preovulatory maturation and oocyte nuclear maturation stage in the mare.. Theriogenology 2000;53:372.
  10. Leese HJ, Barton AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos.. J Reprod Fertil 1984 Sep;72(1):9-13.
    pubmed: 6540809doi: 10.1530/jrf.0.0720009google scholar: lookup
  11. Gardner DK, Leese HJ. Concentrations of nutrients in mouse oviduct fluid and their effects on embryo development and metabolism in vitro.. J Reprod Fertil 1990 Jan;88(1):361-8.
    doi: 10.1530/jrf.0.0880361pubmed: 2313649google scholar: lookup
  12. Harris SE, Gopichandran N, Picton HM, Leese HJ, Orsi NM. Nutrient concentrations in murine follicular fluid and the female reproductive tract.. Theriogenology 2005 Sep 1;64(4):992-1006.
    doi: 10.1016/j.theriogenology.2005.01.004pubmed: 16054501google scholar: lookup
  13. O'Donnell-Tormey J, Nathan CF, Lanks K, DeBoer CJ, de la Harpe J. Secretion of pyruvate. An antioxidant defense of mammalian cells.. J Exp Med 1987 Feb 1;165(2):500-14.
    doi: 10.1084/jem.165.2.500pmc: PMC2188509pubmed: 3102672google scholar: lookup
  14. Downs SM, Hudson ED. Energy substrates and the completion of spontaneous meiotic maturation.. Zygote 2000 Nov;8(4):339-51.
    doi: 10.1017/S0967199400001131pubmed: 11108555google scholar: lookup
  15. Wale PL, Gardner DK. The effects of chemical and physical factors on mammalian embryo culture and their importance for the practice of assisted human reproduction.. Hum Reprod Update 2016 Jan-Feb;22(1):2-22.
    doi: 10.1093/humupd/dmv034pubmed: 26207016google scholar: lookup
  16. Filali M, Hesters L, Fanchin R, Tachdjian G, Frydman R, Frydman N. Retrospective comparison of two media for invitro maturation of oocytes.. Reprod Biomed Online 2008 Feb;16(2):250-6.
    doi: 10.1016/S1472-6483(10)60582-2pubmed: 18284882google scholar: lookup
  17. Van Blerkom J, Antczak M, Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics.. Hum Reprod 1997 May;12(5):1047-55.
    doi: 10.1093/humrep/12.5.1047pubmed: 9194664google scholar: lookup
  18. 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 Suppl 2013 Dec;(45):39-43.
    doi: 10.1111/evj.12159pubmed: 24304402google scholar: lookup
  19. Child TJ, Phillips SJ, Abdul-Jalil AK, Gulekli B, Tan SL. A comparison of in vitro maturation and in vitro fertilization for women with polycystic ovaries.. Obstet Gynecol 2002 Oct;100(4):665-70.
    pubmed: 12383531doi: 10.1016/s0029-7844(02)02193-2google scholar: lookup
  20. Buckett WM, Chian RC, Dean NL, Sylvestre C, Holzer HE, Tan SL. Pregnancy loss in pregnancies conceived after in vitro oocyte maturation, conventional in vitro fertilization, and intracytoplasmic sperm injection.. Fertil Steril 2008 Sep;90(3):546-50.
    doi: 10.1016/j.fertnstert.2007.06.107pubmed: 17904128google scholar: lookup
  21. Walter J, Huwiler F, Fortes C, Grossmann J, Roschitzki B, Hu J, Naegeli H, Laczko E, Bleul U. Analysis of the equine "cumulome" reveals major metabolic aberrations after maturation in vitro.. BMC Genomics 2019 Jul 17;20(1):588.
    pmc: PMC6637639pubmed: 31315563doi: 10.1186/s12864-019-5836-5google scholar: lookup
  22. Hollywood K, Brison DR, Goodacre R. Metabolomics: current technologies and future trends.. Proteomics 2006 Sep;6(17):4716-23.
    doi: 10.1002/pmic.200600106pubmed: 16888765google scholar: lookup
  23. Biggers JD, Whittingham DG, Donahue RP. The pattern of energy metabolism in the mouse oöcyte and zygote.. Proc Natl Acad Sci U S A 1967 Aug;58(2):560-7.
    pmc: PMC335672pubmed: 5233459doi: 10.1073/pnas.58.2.560google scholar: lookup
  24. Kidder GM, Vanderhyden BC. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence.. Can J Physiol Pharmacol 2010 Apr;88(4):399-413.
    doi: 10.1139/Y10-009pmc: PMC3025001pubmed: 20555408google scholar: lookup
  25. Harris SE, Leese HJ, Gosden RG, Picton HM. Pyruvate and oxygen consumption throughout the growth and development of murine oocytes.. Mol Reprod Dev 2009 Mar;76(3):231-8.
    doi: 10.1002/mrd.20945pubmed: 18618608google scholar: lookup
  26. Steeves TE, Gardner DK. Metabolism of glucose, pyruvate, and glutamine during the maturation of oocytes derived from pre-pubertal and adult cows.. Mol Reprod Dev 1999 Sep;54(1):92-101.
    doi: 10.1002/(SICI)1098-2795(199909)54:1<92::AID-MRD14>3.0.CO;2-Apubmed: 10423304google scholar: lookup
  27. Sturmey RG, Leese HJ. Energy metabolism in pig oocytes and early embryos.. Reproduction 2003 Aug;126(2):197-204.
    doi: 10.1530/rep.0.1260197pubmed: 12887276google scholar: lookup
  28. Sutton ML, Cetica PD, Beconi MT, Kind KL, Gilchrist RB, Thompson JG. Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes.. Reproduction 2003 Jul;126(1):27-34.
    doi: 10.1530/rep.0.1260027pubmed: 12814344google scholar: lookup
  29. Muller B, Lewis N, Adeniyi T, Leese HJ, Brison DR, Sturmey RG. Application of extracellular flux analysis for determining mitochondrial function in mammalian oocytes and early embryos.. Sci Rep 2019 Nov 14;9(1):16778.
    pmc: PMC6856134pubmed: 31727902doi: 10.1038/s41598-019-53066-9google scholar: lookup
  30. González-Fernández L, Sánchez-Calabuig MJ, Alves MG, Oliveira PF, Macedo S, Gutiérrez-Adán A, Rocha A, Macías-García B. Expanded equine cumulus-oocyte complexes exhibit higher meiotic competence and lower glucose consumption than compact cumulus-oocyte complexes.. Reprod Fertil Dev 2018 Jan;30(2):297-306.
    doi: 10.1071/RD16441pubmed: 28679463google scholar: lookup
  31. Sutton ML, Gilchrist RB, Thompson JG. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity.. Hum Reprod Update 2003 Jan-Feb;9(1):35-48.
    doi: 10.1093/humupd/dmg009pubmed: 12638780google scholar: lookup
  32. Obeidat YM. Monitoring Oocyte/Embryo Respiration Using Electrochemical-Based Oxygen.. Sensors Actuators B. Chem. 2018;276:72–81.
    doi: 10.1016/j.snb.2018.07.157google scholar: lookup
  33. Sugimura S, Matoba S, Hashiyada Y, Aikawa Y, Ohtake M, Matsuda H, Kobayashi S, Konishi K, Imai K. Oxidative phosphorylation-linked respiration in individual bovine oocytes.. J Reprod Dev 2012;58(6):636-41.
    pubmed: 22785440doi: 10.1262/jrd.2012-082google scholar: lookup
  34. Tejera A, Herrero J, de Los Santos MJ, Garrido N, Ramsing N, Meseguer M. Oxygen consumption is a quality marker for human oocyte competence conditioned by ovarian stimulation regimens.. Fertil Steril 2011 Sep;96(3):618-623.e2.
    doi: 10.1016/j.fertnstert.2011.06.059pubmed: 21782167google scholar: lookup
  35. Davila MP, Muñoz PM, Bolaños JM, Stout TA, Gadella BM, Tapia JA, da Silva CB, Ferrusola CO, Peña FJ. Mitochondrial ATP is required for the maintenance of membrane integrity in stallion spermatozoa, whereas motility requires both glycolysis and oxidative phosphorylation.. Reproduction 2016 Dec;152(6):683-694.
    doi: 10.1530/REP-16-0409pubmed: 27798283google scholar: lookup
  36. Mookerjee SA, Gerencser AA, Nicholls DG, Brand MD. Quantifying intracellular rates of glycolytic and oxidative ATP production and consumption using extracellular flux measurements.. J Biol Chem 2017 Apr 28;292(17):7189-7207.
    doi: 10.1074/jbc.M116.774471pmc: PMC5409486pubmed: 28270511google scholar: lookup
  37. Grøndahl C, Hyttel P, Grøndahl ML, Eriksen T, Gotfredsen P, Greve T. Structural and endocrine aspects of equine oocyte maturation in vivo.. Mol Reprod Dev 1995 Sep;42(1):94-105.
    doi: 10.1002/mrd.1080420113pubmed: 8562057google scholar: lookup
  38. Cetica P, Pintos L, Dalvit G, Beconi M. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro.. Reproduction 2002 Nov;124(5):675-81.
    doi: 10.1530/rep.0.1240675pubmed: 12417006google scholar: lookup
  39. Harris SE, Adriaens I, Leese HJ, Gosden RG, Picton HM. Carbohydrate metabolism by murine ovarian follicles and oocytes grown in vitro.. Reproduction 2007 Sep;134(3):415-24.
    doi: 10.1530/REP-07-0061pubmed: 17709560google scholar: lookup
  40. Preis KA, Seidel G Jr, Gardner DK. Metabolic markers of developmental competence for in vitro-matured mouse oocytes.. Reproduction 2005 Oct;130(4):475-83.
    doi: 10.1530/rep.1.00831pubmed: 16183865google scholar: lookup
  41. Downs SM, Utecht AM. Metabolism of radiolabeled glucose by mouse oocytes and oocyte-cumulus cell complexes.. Biol Reprod 1999 Jun;60(6):1446-52.
    doi: 10.1095/biolreprod60.6.1446pubmed: 10330104google scholar: lookup
  42. Alm H, Hinrichs K. Effect of cycloheximide on nuclear maturation of horse oocytes and its relation to initial cumulus morphology.. J Reprod Fertil 1996 Jul;107(2):215-20.
    doi: 10.1530/jrf.0.1070215pubmed: 8882287google scholar: lookup
  43. Hinrichs K, Schmidt AL, Friedman PP, Selgrath JP, Martin MG. In vitro maturation of horse oocytes: characterization of chromatin configuration using fluorescence microscopy.. Biol Reprod 1993 Feb;48(2):363-70.
    doi: 10.1095/biolreprod48.2.363pubmed: 8439626google scholar: lookup
  44. Manes C, Lai NC. Nonmitochondrial oxygen utilization by rabbit blastocysts and surface production of superoxide radicals.. J Reprod Fertil 1995 May;104(1):69-75.
    doi: 10.1530/jrf.0.1040069pubmed: 7636807google scholar: lookup
  45. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parslow D, Armistead S, Lemire K, Orrell J, Teich J, Chomicz S, Ferrick DA. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells.. Am J Physiol Cell Physiol 2007 Jan;292(1):C125-36.
    doi: 10.1152/ajpcell.00247.2006pubmed: 16971499google scholar: lookup
  46. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells.. Biochem J 2011 Apr 15;435(2):297-312.
    doi: 10.1042/BJ20110162pmc: PMC3076726pubmed: 21726199google scholar: lookup
  47. Ginther OJ. Reproductive Biology of the mare: basic and applied aspects.. .
  48. Woods J, Bergfelt DR, Ginther OJ. Effects of time of insemination relative to ovulation on pregnancy rate and embryonic-loss rate in mares.. Equine Vet J 1990 Nov;22(6):410-5.
    doi: 10.1111/j.2042-3306.1990.tb04306.xpubmed: 2269264google scholar: lookup
  49. Peterson CC, Nagy KA, Diamond J. Sustained metabolic scope.. Proc Natl Acad Sci U S A 1990 Mar;87(6):2324-8.
    doi: 10.1073/pnas.87.6.2324pmc: PMC53679pubmed: 2315323google scholar: lookup
  50. Choi YH, Gibbons JR, Canesin HS, Hinrichs K. Effect of medium variations (zinc supplementation during oocyte maturation, perifertilization pH, and embryo culture protein source) on equine embryo development after intracytoplasmic sperm injection.. Theriogenology 2016 Oct 15;86(7):1782-8.
    doi: 10.1016/j.theriogenology.2016.05.037pubmed: 27377209google scholar: lookup
  51. Hinrichs K, Choi YH, Norris JD, Love LB, Bedford-Guaus SJ, Hartman DL, Velez IC. Evaluation of foal production following intracytoplasmic sperm injection and blastocyst culture of oocytes from ovaries collected immediately before euthanasia or after death of mares under field conditions.. J Am Vet Med Assoc 2012 Oct 15;241(8):1070-4.
    doi: 10.2460/javma.241.8.1070pubmed: 23039983google scholar: lookup
  52. Salgado RM, Brom-de-Luna JG, Resende HL, Canesin HS, Hinrichs K. Lower blastocyst quality after conventional vs. Piezo ICSI in the horse reflects delayed sperm component remodeling and oocyte activation.. J Assist Reprod Genet 2018 May;35(5):825-840.
    doi: 10.1007/s10815-018-1174-9pmc: PMC5984897pubmed: 29637506google scholar: lookup
  53. Leese HJ, Barton AM. Production of pyruvate by isolated mouse cumulus cells.. J Exp Zool 1985 May;234(2):231-6.
    doi: 10.1002/jez.1402340208pubmed: 3998681google scholar: lookup
  54. Ramakrishnan N, Chen R, McClain DE, Bünger R. Pyruvate prevents hydrogen peroxide-induced apoptosis.. Free Radic Res 1998 Oct;29(4):283-95.
    pubmed: 9860043doi: 10.1080/10715769800300321google scholar: lookup
  55. Lee YJ, Kang IJ, Bünger R, Kang YH. Mechanisms of pyruvate inhibition of oxidant-induced apoptosis in human endothelial cells.. Microvasc Res 2003 Sep;66(2):91-101.
    doi: 10.1016/S0026-2862(03)00052-9pubmed: 12935767google scholar: lookup
  56. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review.. Reprod Biol Endocrinol 2012 Jun 29;10:49.
    doi: 10.1186/1477-7827-10-49pmc: PMC3527168pubmed: 22748101google scholar: lookup
  57. Oyamada T, Fukui Y. Oxygen tension and medium supplements for in vitro maturation of bovine oocytes cultured individually in a chemically defined medium.. J Reprod Dev 2004 Feb;50(1):107-17.
    doi: 10.1262/jrd.50.107pubmed: 15007208google scholar: lookup
  58. Park JI, Hong JY, Yong HY, Hwang WS, Lim JM, Lee ES. High oxygen tension during in vitro oocyte maturation improves in vitro development of porcine oocytes after fertilization.. Anim Reprod Sci 2005 Jun;87(1-2):133-41.
    doi: 10.1016/j.anireprosci.2004.11.002pubmed: 15885446google scholar: lookup
  59. Lewis NL, Hinrichs K, Schnauffer K, Morganti M, McG. Argo C. Effect of oocyte source and transport time on rates of equine oocyte maturation and cleavage after fertilisation by ICSI, with a note on the validation of equine embryo morphological classification.. Clin. Theriogenology 2016;8:29–43.
  60. Choi YH, Varner DD, Hartman DL, Hinrichs K. Blastocyst production from equine oocytes fertilized by intracytoplasmic injection of lyophilized sperm.. Anim. Reprod. Sci. 2006;94:307–308.
    doi: 10.1016/j.anireprosci.2006.03.085google scholar: lookup
  61. Guerif F, McKeegan P, Leese HJ, Sturmey RG. A simple approach for COnsumption and RElease (CORE) analysis of metabolic activity in single mammalian embryos.. PLoS One 2013;8(8):e67834.
    doi: 10.1371/journal.pone.0067834pmc: PMC3744531pubmed: 23967049google scholar: lookup

Citations

This article has been cited 14 times.
  1. Zhu X, Zhao S, Xu S, Zhang D, Zhu M, Pan Q, Huang J. Granulosa Cells Improved Mare Oocyte Cytoplasmic Maturation by Providing Collagens. Front Cell Dev Biol 2022;10:914735.
    doi: 10.3389/fcell.2022.914735pubmed: 35846364google scholar: lookup
  2. Orsolini MF, Meyers SA, Dini P. An Update on Semen Physiology, Technologies, and Selection Techniques for the Advancement of In Vitro Equine Embryo Production: Section II. Animals (Basel) 2021 Nov 20;11(11).
    doi: 10.3390/ani11113319pubmed: 34828049google scholar: lookup
  3. Li Z, Song X, Yin S, Yan J, Lv P, Shan H, Cui K, Liu H, Liu Q. Single-Cell RNA-Seq Revealed the Gene Expression Pattern during the In Vitro Maturation of Donkey Oocytes. Genes (Basel) 2021 Oct 19;12(10).
    doi: 10.3390/genes12101640pubmed: 34681034google scholar: lookup
  4. Fernández-Hernández P, Marinaro F, Sánchez-Calabuig MJ, García-Marín LJ, Bragado MJ, González-Fernández L, Macías-García B. The Proteome of Equine Oviductal Fluid Varies Before and After Ovulation: A Comparative Study. Front Vet Sci 2021;8:694247.
    doi: 10.3389/fvets.2021.694247pubmed: 34422946google scholar: lookup
  5. Catandi GD, Obeidat YM, Broeckling CD, Chen TW, Chicco AJ, Carnevale EM. Equine maternal aging affects oocyte lipid content, metabolic function and developmental potential. Reproduction 2021 Apr;161(4):399-409.
    doi: 10.1530/REP-20-0494pubmed: 33539317google scholar: lookup
  6. Fernández-Hernández P, Sánchez-Calabuig MJ, García-Marín LJ, Bragado MJ, Gutiérrez-Adán A, Millet Ó, Bruzzone C, González-Fernández L, Macías-García B. Study of the Metabolomics of Equine Preovulatory Follicular Fluid: A Way to Improve Current In Vitro Maturation Media. Animals (Basel) 2020 May 19;10(5).
    doi: 10.3390/ani10050883pubmed: 32438699google scholar: lookup
  7. Walter J, Colleoni S, Lazzari G, Fortes C, Grossmann J, Roschitzki B, Laczko E, Naegeli H, Bleul U, Galli C. Maturational competence of equine oocytes is associated with alterations in their 'cumulome'. Mol Hum Reprod 2024 Sep 12;30(9).
    doi: 10.1093/molehr/gaae033pubmed: 39288330google scholar: lookup
  8. Luis-Calero M, Ortiz-Rodríguez JM, Fernández-Hernández P, Muñoz-García CC, Pericuesta E, Gutiérrez-Adán A, Marinaro F, Embade N, Conde R, Bizkarguenaga M, Millet Ó, González-Fernández L, Macías-García B. Preovulatory follicular fluid secretome added to in vitro maturation medium influences the metabolism of equine cumulus-oocyte complexes. BMC Vet Res 2024 Jun 25;20(1):272.
    doi: 10.1186/s12917-024-04129-1pubmed: 38918770google scholar: lookup
  9. Bao S, Yin T, Liu S. Ovarian aging: energy metabolism of oocytes. J Ovarian Res 2024 May 31;17(1):118.
    doi: 10.1186/s13048-024-01427-ypubmed: 38822408google scholar: lookup
  10. Bresnahan DR, Catandi GD, Peters SO, Maclellan LJ, Broeckling CD, Carnevale EM. Maturation and culture affect the metabolomic profile of oocytes and follicular cells in young and old mares. Front Cell Dev Biol 2023;11:1280998.
    doi: 10.3389/fcell.2023.1280998pubmed: 38283993google scholar: lookup
  11. Pollard CL. Can Nicotinamide Adenine Dinucleotide (NAD(+)) and Sirtuins Be Harnessed to Improve Mare Fertility?. Animals (Basel) 2024 Jan 7;14(2).
    doi: 10.3390/ani14020193pubmed: 38254361google scholar: lookup
  12. Catandi GD, Bresnahan DR, Peters SO, Fresa KJ, Maclellan LJ, Broeckling CD, Carnevale EM. Equine maternal aging affects the metabolomic profile of oocytes and follicular cells during different maturation time points. Front Cell Dev Biol 2023;11:1239154.
    doi: 10.3389/fcell.2023.1239154pubmed: 37818125google scholar: lookup
  13. Placidi M, Vergara T, Casoli G, Flati I, Capece D, Artini PG, Virmani A, Zanatta S, D'Alessandro AM, Tatone C, Di Emidio G. Acyl-Carnitines Exert Positive Effects on Mitochondrial Activity under Oxidative Stress in Mouse Oocytes: A Potential Mechanism Underlying Carnitine Efficacy on PCOS. Biomedicines 2023 Sep 6;11(9).
    doi: 10.3390/biomedicines11092474pubmed: 37760915google scholar: lookup
  14. Catandi GD, LiPuma L, Obeidat YM, Maclellan LJ, Broeckling CD, Chen T, Chicco AJ, Carnevale EM. Oocyte metabolic function, lipid composition, and developmental potential are altered by diet in older mares. Reproduction 2022 Apr 1;163(4):183-198.
    doi: 10.1530/REP-21-0351pubmed: 37379450google scholar: lookup
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