Analyze Diet
Reproduction (Cambridge, England)2022; 163(4); 183-198; doi: 10.1530/REP-21-0351

Oocyte metabolic function, lipid composition, and developmental potential are altered by diet in older mares.

Abstract: Dietary supplementation is the most feasible method to improve oocyte function and developmental potential . During three experiments, oocytes were collected from maturing, dominant follicles of older mares to determine whether short-term dietary supplements can alter oocyte metabolic function, lipid composition, and developmental potential. Over approximately 8 weeks, control mares were fed hay (CON) or hay and grain products (COB). Treated mares received supplements designed for equine wellness and gastrointestinal health, flaxseed oil, and a proprietary blend of fatty acid and antioxidant support (reproductive support supplement (RSS)) intended to increase antioxidant activity and lipid oxidation. RSS was modified for individual experiments with additional antioxidants or altered concentrations of n-3 to n-6 fatty acids. Oocytes from mares supplemented with RSS when compared to COB had higher basal oxygen consumption, indicative of higher aerobic metabolism, and proportionately more aerobic to anaerobic metabolism. In the second experiment, oocytes collected from the same mares prior to (CON) and after approximately 8 weeks of RSS supplementation had significantly reduced oocyte lipid abundance. In the final experiment, COB was compared to RSS supplementation, including RSS modified to proportionately reduce n-3 fatty acids and increase n-6 fatty acids. The ability of sperm-injected oocytes to develop into blastocysts was higher for RSS, regardless of fatty acid content, than for COB. We demonstrated that short-term diet supplementation can directly affect oocyte function in older mares, resulting in oocytes with increased metabolic activity, reduced lipid content, and increased developmental potential.
Publication Date: 2022-01-28 PubMed ID: 37379450PubMed Central: PMC8942336DOI: 10.1530/REP-21-0351Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

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.

The research paper investigates the impact of dietary supplementation on the oocyte function and developmental potential of older mares. It demonstrates that short-term diet supplementation can influence the metabolic activities of oocytes, thus leading to decreased lipid content and enhanced developmental potential.

Overview of the Research

  • The study was conducted in three separate experiments with the main objective of examining whether dietary supplements can bring in changes to oocyte metabolic function, lipid composition, and developmental potential in older mares.
  • Oocytes, also known as egg cells, were collected from healthy, maturing follicles of these mares for the study.
  • Dietary control groups were fed hay only (CON) or hay mixed with grain products (COB), while the treatment groups received different supplementation, including those for equine wellness and gastrointestinal health, flaxseed oil, and a proprietary blend of fatty acid and antioxidant support termed as ‘Reproductive Support Supplement’ (RSS).

Findings from the Experiments

  • In the first experiment, it was observed that oocytes from mares that were supplemented with RSS exhibited higher basal oxygen consumption compared to those from mares that received COB. This indicated that these oocytes have higher aerobic metabolism and a higher proportion of aerobic to anaerobic metabolism.
  • The second experiment found that the lipid abundance in oocytes from the same mares decreased after 8 weeks of RSS supplementation. This suggests that RSS supplementation can significantly reduce oocyte lipid content.
  • In the final experiment, oocytes of mares receiving RSS supplement (including the ones with modified RSS) had a higher potential to develop into blastocysts than those on the COB diet, regardless of the fatty acid content in the diet.
  • This implies that RSS improves the developmental potential of oocytes, irrespective of the fatty acid content in it.

Significance and Implications of the Research

  • The study effectively demonstrates that even short-term dietary supplementation can significantly affect the function of the oocyte in older mares.
  • These alterations include increased metabolic activity, reduced lipid content, and increased developmental potential.
  • This research could open pathways for improving reproductive health and efficacy in older mares, and possibly extend to other species.

Cite This Article

APA
Catandi GD, LiPuma L, Obeidat YM, Maclellan LJ, Broeckling CD, Chen T, Chicco AJ, Carnevale EM. (2022). Oocyte metabolic function, lipid composition, and developmental potential are altered by diet in older mares. Reproduction, 163(4), 183-198. https://doi.org/10.1530/REP-21-0351

Publication

ISSN: 1741-7899
NlmUniqueID: 100966036
Country: England
Language: English
Volume: 163
Issue: 4
Pages: 183-198

Researcher Affiliations

Catandi, Giovana D
  • Equine Reproduction Laboratory, Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
LiPuma, Lance
  • Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Obeidat, Yusra M
  • Electronic Engineering Department, Hijjawi Faculty for Engineering Technology, Yarmouk University, Irbid, Jordan.
Maclellan, Lisa J
  • Equine Reproduction Laboratory, Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Broeckling, Corey D
  • Proteomics and Metabolomics Facility, Colorado State University, Fort Collins, Colorado, USA.
Chen, Tom
  • Department of Electrical and Computer Engineering, Colorado State University, Fort Collins, Colorado, USA.
  • School of Biomedical Engineering, Colorado State University, Fort Collins, Colorado, USA.
Chicco, Adam J
  • Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Carnevale, Elaine M
  • Equine Reproduction Laboratory, Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
  • Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.

MeSH Terms

  • Horses
  • Animals
  • Female
  • Male
  • Semen
  • Oocytes
  • Diet / veterinary
  • Fatty Acids
  • Antioxidants
  • Fatty Acids, Omega-6

Grant Funding

  • R21 HD097601 / NICHD NIH HHS

References

This article includes 82 references
  1. Aardema H, Lolicato F, van de Lest CH, Brouwers JF, Vaandrager AB, van Tol HT, Roelen BA, Vos PL, Helms JB, Gadella BM. Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage.. Biol Reprod 2013 Jun;88(6):164.
    doi: 10.1095/biolreprod.112.106062pubmed: 23616596google scholar: lookup
  2. Abdulhasan MK, Li Q, Dai J, Abu-Soud HM, Puscheck EE, Rappolee DA. CoQ10 increases mitochondrial mass and polarization, ATP and Oct4 potency levels, and bovine oocyte MII during IVM while decreasing AMPK activity and oocyte death.. J Assist Reprod Genet 2017 Dec;34(12):1595-1607.
    doi: 10.1007/s10815-017-1027-ypmc: PMC5714820pubmed: 28900834google scholar: lookup
  3. Babayev E, Seli E. Oocyte mitochondrial function and reproduction.. Curr Opin Obstet Gynecol 2015 Jun;27(3):175-81.
  4. Bavister BD, Squirrell JM. Mitochondrial distribution and function in oocytes and early embryos.. Hum Reprod 2000 Jul;15 Suppl 2:189-98.
    doi: 10.1093/humrep/15.suppl_2.189pubmed: 11041524google scholar: lookup
  5. Ben-Meir A, Burstein E, Borrego-Alvarez A, Chong J, Wong E, Yavorska T, Naranian T, Chi M, Wang Y, Bentov Y, Alexis J, Meriano J, Sung HK, Gasser DL, Moley KH, Hekimi S, Casper RF, Jurisicova A. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging.. Aging Cell 2015 Oct;14(5):887-95.
    doi: 10.1111/acel.12368pmc: PMC4568976pubmed: 26111777google scholar: lookup
  6. Boudoures AL, Saben J, Drury A, Scheaffer S, Modi Z, Zhang W, Moley KH. Obesity-exposed oocytes accumulate and transmit damaged mitochondria due to an inability to activate mitophagy.. Dev Biol 2017 Jun 1;426(1):126-138.
    doi: 10.1016/j.ydbio.2017.04.005pubmed: 28438607google scholar: lookup
  7. Bowtell JL, Cooke K, Turner R, Mileva KN, Sumners DP. Acute physiological and performance responses to repeated sprints in varying degrees of hypoxia.. J Sci Med Sport 2014 Jul;17(4):399-403.
    doi: 10.1016/j.jsams.2013.05.016pubmed: 23809839google scholar: lookup
  8. 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
  9. Broughton DE, Moley KH. Obesity and female infertility: potential mediators of obesity's impact.. Fertil Steril 2017 Apr;107(4):840-847.
  10. Carnevale EM. The mare model for follicular maturation and reproductive aging in the woman.. Theriogenology 2008 Jan 1;69(1):23-30.
  11. Carnevale EM. Advances in Collection, Transport and Maturation of Equine Oocytes for Assisted Reproductive Techniques.. Vet Clin North Am Equine Pract 2016 Dec;32(3):379-399.
    doi: 10.1016/j.cveq.2016.07.002pubmed: 27726987google scholar: lookup
  12. Carnevale EM, Ginther OJ. Defective oocytes as a cause of subfertility in old mares. Biology of Reproduction 52:209–214.
  13. Carnevale EM, Metcalf ES. Morphology, developmental stages and quality parameters of in vitro-produced equine embryos.. Reprod Fertil Dev 2019 Jan;31(12):1758-1770.
    doi: 10.1071/RD19257pubmed: 31718765google scholar: lookup
  14. Carnevale EM, Catandi GD, Fresa K. Equine Aging and the Oocyte: A Potential Model for Reproductive Aging in Women.. J Equine Vet Sci 2020 Jun;89:103022.
    doi: 10.1016/j.jevs.2020.103022pubmed: 32563447google scholar: lookup
  15. Catandi G, Obeidat Y, Chicco A, Chen T, Carnevale E. Basal and maximal oxygen consumption of oocytes from young and old mares. Reproduction, Fertility and Development 31:208–208.
    doi: 10.1071/RDv31n1Ab167google scholar: lookup
  16. 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-20-0494pmc: PMC7969451pubmed: 33539317google scholar: lookup
  17. Cecchino GN, Seli E, Alves da Motta EL, García-Velasco JA. The role of mitochondrial activity in female fertility and assisted reproductive technologies: overview and current insights.. Reprod Biomed Online 2018 Jun;36(6):686-697.
    doi: 10.1016/j.rbmo.2018.02.007pubmed: 29598846google scholar: lookup
  18. Chicco AJ, Le CH, Gnaiger E, Dreyer HC, Muyskens JB, D'Alessandro A, Nemkov T, Hocker AD, Prenni JE, Wolfe LM, Sindt NM, Lovering AT, Subudhi AW, Roach RC. Adaptive remodeling of skeletal muscle energy metabolism in high-altitude hypoxia: Lessons from AltitudeOmics.. J Biol Chem 2018 May 4;293(18):6659-6671.
    doi: 10.1074/jbc.RA117.000470pmc: PMC5936810pubmed: 29540485google scholar: lookup
  19. Collins A, Palmer E, Bézard J, Burke J, Duchamp G, Buckley T. A comparison of the biochemical composition of equine follicular fluid and serum at four different stages of the follicular cycle.. Equine Vet J Suppl 1997 Dec;(25):12-6.
  20. Contri A, De Amicis I, Molinari A, Faustini M, Gramenzi A, Robbe D, Carluccio A. Effect of dietary antioxidant supplementation on fresh semen quality in stallion.. Theriogenology 2011 Apr 15;75(7):1319-26.
  21. Dalbies-Tran R, Cadoret V, Desmarchais A, Elis S, Maillard V, Monget P, Monniaux D, Reynaud K, Saint-Dizier M, Uzbekova S. A Comparative Analysis of Oocyte Development in Mammals.. Cells 2020 Apr 17;9(4).
    doi: 10.3390/cells9041002pmc: PMC7226043pubmed: 32316494google scholar: lookup
  22. Das UN. Essential fatty acids: biochemistry, physiology and pathology.. Biotechnol J 2006 Apr;1(4):420-39.
    doi: 10.1002/biot.200600012pubmed: 16892270google scholar: lookup
  23. de Lorgeril M, Salen P. New insights into the health effects of dietary saturated and omega-6 and omega-3 polyunsaturated fatty acids.. BMC Med 2012 May 21;10:50.
    doi: 10.1186/1741-7015-10-50pmc: PMC3394202pubmed: 22613931google scholar: lookup
  24. Deichsel K, Palm F, Koblischke P, Budik S, Aurich C. Effect of a dietary antioxidant supplementation on semen quality in pony stallions.. Theriogenology 2008 May;69(8):940-5.
  25. Devine PJ, Perreault SD, Luderer U. Roles of reactive oxygen species and antioxidants in ovarian toxicity.. Biol Reprod 2012 Feb;86(2):27.
  26. Dhungana S, Carlson JE, Pathmasiri W, McRitchie S, Davis M, Sumner S, Appt SE. Impact of a western diet on the ovarian and serum metabolome.. Maturitas 2016 Oct;92:134-142.
  27. DiMauro S, Schon EA. Mitochondrial respiratory-chain diseases.. N Engl J Med 2003 Jun 26;348(26):2656-68.
    doi: 10.1056/NEJMra022567pubmed: 12826641google scholar: lookup
  28. Downs SM. Nutrient pathways regulating the nuclear maturation of mammalian oocytes.. Reprod Fertil Dev 2015 May;27(4):572-82.
    doi: 10.1071/RD14343pubmed: 25798589google scholar: lookup
  29. Downs SM, Mosey JL, Klinger J. Fatty acid oxidation and meiotic resumption in mouse oocytes.. Mol Reprod Dev 2009 Sep;76(9):844-53.
    doi: 10.1002/mrd.21047pmc: PMC3995453pubmed: 19455666google scholar: lookup
  30. Dunning KR, Robker RL. Promoting lipid utilization with l-carnitine to improve oocyte quality.. Anim Reprod Sci 2012 Sep;134(1-2):69-75.
  31. Dunning KR, Russell DL, Robker RL. Lipids and oocyte developmental competence: the role of fatty acids and β-oxidation.. Reproduction 2014 Jul;148(1):R15-27.
    doi: 10.1530/REP-13-0251pubmed: 24760880google scholar: lookup
  32. El-Shahat KH, Abo-El maaty AM. The effect of dietary supplementation with calcium salts of long chain fatty acids and/or L-carnitine on ovarian activity of Rahmani ewes.. Anim Reprod Sci 2010 Jan;117(1-2):78-82.
  33. 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/ani10050883pmc: PMC7278476pubmed: 32438699google scholar: lookup
  34. Foster CV, Harris RC, Snow DH. The effect of oral L-carnitine supplementation on the muscle and plasma concentrations in the Thoroughbred horse.. Comp Biochem Physiol A Comp Physiol 1988;91(4):827-35.
    doi: 10.1016/0300-9629(8890971-1pubmed: 2907450google scholar: lookup
  35. Frape DL. Equine Nutrition and Feeding. .
  36. Gaskins AJ, Chavarro JE. Diet and fertility: a review.. Am J Obstet Gynecol 2018 Apr;218(4):379-389.
    doi: 10.1016/j.ajog.2017.08.010pmc: PMC5826784pubmed: 28844822google scholar: lookup
  37. Ginther O. Reproductive biology of the mare. In Basic and Applied Aspects, vol. 75.
  38. Gonzalez-Castro RA, Carnevale EM. Association of equine sperm population parameters with outcome of intracytoplasmic sperm injections.. Theriogenology 2018 Oct 1;119:114-120.
  39. Goo S, Pham T, Han JC, Nielsen P, Taberner A, Hickey A, Loiselle D. Multiscale measurement of cardiac energetics.. Clin Exp Pharmacol Physiol 2013 Sep;40(9):671-81.
    doi: 10.1111/1440-1681.12139pubmed: 23745944google scholar: lookup
  40. Gu L, Liu H, Gu X, Boots C, Moley KH, Wang Q. Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes.. Cell Mol Life Sci 2015 Jan;72(2):251-71.
    doi: 10.1007/s00018-014-1739-4pmc: PMC4389777pubmed: 25280482google scholar: lookup
  41. Hallebeek JM, Beynen AC. Dietary fats and lipid metabolism in relation to equine health, performance and disease. PhD Thesis. The Netherlands: Department of Nutrition, Utrecht University.
  42. Hashimoto S, Morimoto N, Yamanaka M, Matsumoto H, Yamochi T, Goto H, Inoue M, Nakaoka Y, Shibahara H, Morimoto Y. Quantitative and qualitative changes of mitochondria in human preimplantation embryos.. J Assist Reprod Genet 2017 May;34(5):573-580.
    doi: 10.1007/s10815-017-0886-6pmc: PMC5427646pubmed: 28190213google scholar: lookup
  43. Hendriks WK, Colleoni S, Galli C, Paris DBBP, Colenbrander B, Stout TAE. Mitochondrial DNA replication is initiated at blastocyst formation in equine embryos.. Reprod Fertil Dev 2019 Mar;31(3):570-578.
    doi: 10.1071/RD17387pubmed: 30423285google scholar: lookup
  44. Hess T, Ross-Jones T. Omega-3 fatty acid supplementation in horses. Revista Brasileira de Zootecnia 43:677–683.
  45. Hodge LB, Rude BJ, Dinh TN, Lemley CO. Effect of ω-3 fatty acid supplementation to gestating and lactating mares: on milk IgG, mare and foal blood concentrations of IgG, insulin and glucose, placental efficiency, and fatty acid composition of milk and serum from mares and foals. Journal of Equine Veterinary Science 51:70–78.
  46. Jahangirifar M, Taebi M, Nasr-Esfahani MH, Askari GH. Dietary Patterns and The Outcomes of Assisted Reproductive Techniques in Women with Primary Infertility: A Prospective Cohort Study.. Int J Fertil Steril 2019 Jan;12(4):316-323.
    doi: 10.22074/ijfs.2019.5373pmc: PMC6186288pubmed: 30291693google scholar: lookup
  47. Jancar N, Kopitar AN, Ihan A, Virant Klun I, Bokal EV. Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilization and blastocyst development.. J Assist Reprod Genet 2007 Feb-Mar;24(2-3):91-7.
    doi: 10.1007/s10815-006-9103-8pmc: PMC3454987pubmed: 17216562google scholar: lookup
  48. Kansaku K, Itami N, Kawahara-Miki R, Shirasuna K, Kuwayama T, Iwata H. Differential effects of mitochondrial inhibitors on porcine granulosa cells and oocytes.. Theriogenology 2017 Nov;103:98-103.
  49. Karuputhula NB, Chattopadhyay R, Chakravarty B, Chaudhury K. Oxidative status in granulosa cells of infertile women undergoing IVF.. Syst Biol Reprod Med 2013 Apr;59(2):91-8.
    doi: 10.3109/19396368.2012.743197pubmed: 23278116google scholar: lookup
  50. Kermack AJ, Lowen P, Wellstead SJ, Fisk HL, Montag M, Cheong Y, Osmond C, Houghton FD, Calder PC, Macklon NS. Effect of a 6-week "Mediterranean" dietary intervention on in vitro human embryo development: the Preconception Dietary Supplements in Assisted Reproduction double-blinded randomized controlled trial.. Fertil Steril 2020 Feb;113(2):260-269.
  51. Lai Q, Xiang W, Li Q, Zhang H, Li Y, Zhu G, Xiong C, Jin L. Oxidative stress in granulosa cells contributes to poor oocyte quality and IVF-ET outcomes in women with polycystic ovary syndrome.. Front Med 2018 Oct;12(5):518-524.
    doi: 10.1007/s11684-017-0575-ypubmed: 29260383google scholar: lookup
  52. Lewis N, Hinrichs K, Leese HJ, McG Argo C, Brison DR, Sturmey R. Energy metabolism of the equine cumulus oocyte complex during in vitro maturation.. Sci Rep 2020 Feb 26;10(1):3493.
    doi: 10.1038/s41598-020-60624-zpmc: PMC7044441pubmed: 32103136google scholar: lookup
  53. Li YR, Li S, Lin CC. Effect of resveratrol and pterostilbene on aging and longevity.. Biofactors 2018 Jan;44(1):69-82.
    doi: 10.1002/biof.1400pubmed: 29210129google scholar: lookup
  54. Lindholm CR, Ertel RL, Bauwens JD, Schmuck EG, Mulligan JD, Saupe KW. A high-fat diet decreases AMPK activity in multiple tissues in the absence of hyperglycemia or systemic inflammation in rats.. J Physiol Biochem 2013 Jun;69(2):165-75.
    doi: 10.1007/s13105-012-0199-2pmc: PMC3644018pubmed: 22941749google scholar: lookup
  55. Lolicato F, Brouwers JF, de Lest CH, Wubbolts R, Aardema H, Priore P, Roelen BA, Helms JB, Gadella BM. The cumulus cell layer protects the bovine maturing oocyte against fatty acid-induced lipotoxicity.. Biol Reprod 2015 Jan;92(1):16.
    doi: 10.1095/biolreprod.114.120634pubmed: 25297544google scholar: lookup
  56. Madsen L, Rustan AC, Vaagenes H, Berge K, Dyrøy E, Berge RK. Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference.. Lipids 1999 Sep;34(9):951-63.
    doi: 10.1007/s11745-999-0445-xpubmed: 10574660google scholar: lookup
  57. May-Panloup P, Chretien MF, Malthiery Y, Reynier P. Mitochondrial DNA in the oocyte and the developing embryo.. Curr Top Dev Biol 2007;77:51-83.
    doi: 10.1016/S0070-2153(0677003-Xpubmed: 17222700google scholar: lookup
  58. Meldrum DR, Casper RF, Diez-Juan A, Simon C, Domar AD, Frydman R. Aging and the environment affect gamete and embryo potential: can we intervene?. Fertil Steril 2016 Mar;105(3):548-559.
  59. Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, Grunfeld L. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility.. Lancet 1991 Jun 8;337(8754):1375-7.
    doi: 10.1016/0140-6736(9193060-mpubmed: 1674764google scholar: lookup
  60. Nehra D, Le HD, Fallon EM, Carlson SJ, Woods D, White YA, Pan AH, Guo L, Rodig SJ, Tilly JL, Rueda BR, Puder M. Prolonging the female reproductive lifespan and improving egg quality with dietary omega-3 fatty acids.. Aging Cell 2012 Dec;11(6):1046-54.
    doi: 10.1111/acel.12006pmc: PMC5624332pubmed: 22978268google scholar: lookup
  61. Obeidat YM, Evans AJ, Tedjo W, Chicco AJ, Carnevale E, Chen TW. Monitoring oocyte/embryo respiration using electrochemical-based oxygen sensors. Sensors and Actuators: Part B 276:72–81.
    doi: 10.1016/j.snb.2018.07.157google scholar: lookup
  62. Obeidat YM, Cheng MH, Catandi G, Carnevale E, Chicco AJ, Chen TW. Design of a multi-sensor platform for integrating extracellular acidification rate with multi-metabolite flux measurement for small biological samples.. Biosens Bioelectron 2019 May 15;133:39-47.
    doi: 10.1016/j.bios.2019.02.069pmc: PMC6660976pubmed: 30909011google scholar: lookup
  63. Pasquariello R, Ermisch AF, Silva E, McCormick S, Logsdon D, Barfield JP, Schoolcraft WB, Krisher RL. Alterations in oocyte mitochondrial number and function are related to spindle defects and occur with maternal aging in mice and humans†.. Biol Reprod 2019 Apr 1;100(4):971-981.
    doi: 10.1093/biolre/ioy248pubmed: 30476005google scholar: lookup
  64. Ratchford AM, Chang AS, Chi MM, Sheridan R, Moley KH. Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes.. Am J Physiol Endocrinol Metab 2007 Nov;293(5):E1198-206.
    doi: 10.1152/ajpendo.00097.2007pubmed: 17684106google scholar: lookup
  65. Richani D, Dunning KR, Thompson JG, Gilchrist RB. Metabolic co-dependence of the oocyte and cumulus cells: essential role in determining oocyte developmental competence.. Hum Reprod Update 2021 Jan 4;27(1):27-47.
    doi: 10.1093/humupd/dmaa043pubmed: 33020823google scholar: lookup
  66. Ruiz AJ, Tibary A, Heaton RA, Hargreaves IP, Leadon DP, Bayly WM. Effects of Feeding Coenzyme Q10-Ubiquinol on Plasma Coenzyme Q10 Concentrations and Semen Quality in Stallions.. J Equine Vet Sci 2021 Jan;96:103303.
    doi: 10.1016/j.jevs.2020.103303pubmed: 33349408google scholar: lookup
  67. Satué K, Fazio E, Ferlazzo A, Medica P. Hematochemical Patterns in Follicular Fluid and Blood Stream in Cycling Mares: A Comparative Note.. J Equine Vet Sci 2019 Sep;80:20-26.
    doi: 10.1016/j.jevs.2019.06.016pubmed: 31443828google scholar: lookup
  68. Schmid-Lausigk Y, Aurich C. Influences of a diet supplemented with linseed oil and antioxidants on quality of equine semen after cooling and cryopreservation during winter.. Theriogenology 2014 Apr 15;81(7):966-73.
  69. Sessions-Bresnahan DR, Schauer KL, Heuberger AL, Carnevale EM. Effect of Obesity on the Preovulatory Follicle and Lipid Fingerprint of Equine Oocytes.. Biol Reprod 2016 Jan;94(1):15.
    doi: 10.1095/biolreprod.115.130187pubmed: 26632608google scholar: lookup
  70. Siu MK, Cheng CY. The blood-follicle barrier (BFB) in disease and in ovarian function.. Adv Exp Med Biol 2012;763:186-92.
    doi: 10.1007/978-1-4614-4711-5_9pmc: PMC4169694pubmed: 23397625google scholar: lookup
  71. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G. XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification.. Anal Chem 2006 Feb 1;78(3):779-87.
    doi: 10.1021/ac051437ypubmed: 16448051google scholar: lookup
  72. Spikings EC, Alderson J, St John JC. Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development.. Biol Reprod 2007 Feb;76(2):327-35.
    doi: 10.1095/biolreprod.106.054536pubmed: 17035641google scholar: lookup
  73. Steinberg F, Stites TE, Anderson P, Storms D, Chan I, Eghbali S, Rucker R. Pyrroloquinoline quinone improves growth and reproductive performance in mice fed chemically defined diets.. Exp Biol Med (Maywood) 2003 Feb;228(2):160-6.
    doi: 10.1177/153537020322800205pubmed: 12563022google scholar: lookup
  74. Tautenhahn R, Böttcher C, Neumann S. Highly sensitive feature detection for high resolution LC/MS.. BMC Bioinformatics 2008 Nov 28;9:504.
    doi: 10.1186/1471-2105-9-504pmc: PMC2639432pubmed: 19040729google scholar: lookup
  75. Ullah O, Zhongshu L, Ali I, Xu L, Liu H, Fang N. Effects of pterostilbene on the activation of nuclear factor erythroid 2-related factor 2 pathway during in vitro maturation of mouse oocytes. Journal of Agricultural Science 10:35.
    doi: 10.5539/jas.v10n7p35google scholar: lookup
  76. Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence.. Mitochondrion 2011 Sep;11(5):797-813.
    doi: 10.1016/j.mito.2010.09.012pubmed: 20933103google scholar: lookup
  77. Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge EA. The role of mitochondrial DNA copy number in mammalian fertility.. Biol Reprod 2010 Jul;83(1):52-62.
  78. Williams CJ, Erickson GF. Morphology and Physiology of the Ovary.. 2000;.
    pubmed: 25905186
  79. Yang W, Wang L, Wang F, Yuan S. Roles of AMP-Activated Protein Kinase (AMPK) in Mammalian Reproduction.. Front Cell Dev Biol 2020;8:593005.
    doi: 10.3389/fcell.2020.593005pmc: PMC7710906pubmed: 33330475google scholar: lookup
  80. Zachut M, Dekel I, Lehrer H, Arieli A, Arav A, Livshitz L, Yakoby S, Moallem U. Effects of dietary fats differing in n-6:n-3 ratio fed to high-yielding dairy cows on fatty acid composition of ovarian compartments, follicular status, and oocyte quality.. J Dairy Sci 2010 Feb;93(2):529-45.
    doi: 10.3168/jds.2009-2167pubmed: 20105525google scholar: lookup
  81. Zarezadeh R, Mehdizadeh A, Leroy JLMR, Nouri M, Fayezi S, Darabi M. Action mechanisms of n-3 polyunsaturated fatty acids on the oocyte maturation and developmental competence: Potential advantages and disadvantages.. J Cell Physiol 2019 Feb;234(2):1016-1029.
    doi: 10.1002/jcp.27101pubmed: 30073662google scholar: lookup
  82. Zeyner A, Harmeyer J. Metabolic functions of L-carnitine and its effects as feed additive in horses. A review.. Arch Tierernahr 1999;52(2):115-38.
    doi: 10.1080/17450399909386157pubmed: 10548966google scholar: lookup

Citations

This article has been cited 0 times.