FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Sci Rep / Application of extracellular flux analysis for determining m...
Scientific reports2019; 9(1); 16778; doi: 10.1038/s41598-019-53066-9

Application of extracellular flux analysis for determining mitochondrial function in mammalian oocytes and early embryos.

Abstract: Mitochondria provide the major source of ATP for mammalian oocyte maturation and early embryo development. Oxygen Consumption Rate (OCR) is an established measure of mitochondrial function. OCR by mammalian oocytes and embryos has generally been restricted to overall uptake and detailed understanding of the components of OCR dedicated to specific molecular events remains lacking. Here, extracellular flux analysis (EFA) was applied to small groups of bovine, equine, mouse and human oocytes and bovine early embryos to measure OCR and its components. Using EFA, we report the changes in mitochondrial activity during the processes of oocyte maturation, fertilisation, and pre-implantation development to blastocyst stage in response to physiological demands in mammalian embryos. Crucially, we describe the real time partitioning of overall OCR to spare capacity, proton leak, non-mitochondrial and coupled respiration - showing that while activity changes over the course of development in response to physiological demand, the overall efficiency is unchanged. EFA is shown to be able to measure mitochondrial function in small groups of mammalian oocytes and embryos in a manner which is robust, rapid and easy to use. EFA is non-invasive and allows real-time determination of the impact of compounds on OCR, facilitating an assessment of the components of mitochondrial activity. This provides proof-of-concept for EFA as an accessible system with which to study mammalian oocyte and embryo metabolism.
Get Full Text
Publication Date: 2019-11-14 PubMed ID: 31727902PubMed Central: PMC6856134DOI: 10.1038/s41598-019-53066-9Google 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.
LinkedInCopy
  • Journal Article

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 applies extracellular flux analysis for understanding the mitochondrial function of various mammalian oocytes and early embryos, including bovines, equine, mouse and humans. The study highlights the changes in mitochondrial activity during the processes of ovule maturation, fertilization, and pre-implantation development in response to physiological demands of mammalian embryos.

Understanding Mitochondrial Function in Mammalian Oocytes and Early Embryos

  • The research focuses on how mitochondria, which are the primary source of ATP, work during the maturation of oocytes and the early stages of embryo development in mammals.
  • The overall uptake of Oxygen Consumption Rate (OCR) has generally been restricted in mammalian oocytes and embryos, hence, the particular components of OCR related to specific molecular events are not well-understood. This research applies extracellular flux analysis (EFA) to break down and understand these components.

Applying Extracellular Flux Analysis (EFA) to Measure OCR

  • EFA is applied to small groups of different types of mammalian oocytes and early embryos, including those belonging to bovine, equine, mouse and humans, in order to measure OCR and its distinct components. This allows for a more detailed understanding of mitochondrial function during crucial stages of development.
  • By using EFA, researchers can observe changes in mitochondrial activity during the processes of oocyte maturation, fertilization, and pre-implantation development. These stages respond to physiological demands in mammalian embryos.

Assessing Efficiency and Partitioning of OCR

  • Despite changes in activity in different development stages, the overall efficiency of OCR remains constant. Moreover, the partitioning of overall OCR to several components such as spare capacity, proton leak, non-mitochondrial and coupled respiration can be tracked in real-time with EFA.
  • The study proves EFA to be a useful, rapid, and robust method for examining mitochondrial function in small groups of mammalian oocytes and embryos. It is also non-invasive and permits real-time evaluation of different compound’s impact on OCR. This assessment can further clarify the different components of mitochondrial activity.

Implications and Future Directions

  • Results of the study provide a proof-of-concept for EFA as an accessible system to study mammalian oocyte and embryo metabolism. Due to its non-invasive nature, EFA presents an invaluable tool suitable for more detailed and insightful future research on the mitochondrial function in mammalian oocytes and early embryos.

Cite This Article

APA
Muller B, Lewis N, Adeniyi T, Leese HJ, Brison DR, Sturmey RG. (2019). Application of extracellular flux analysis for determining mitochondrial function in mammalian oocytes and early embryos. Sci Rep, 9(1), 16778. https://doi.org/10.1038/s41598-019-53066-9

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 9
Issue: 1
Pages: 16778
PII: 16778

Researcher Affiliations

Muller, Bethany
  • Centre for Atherothrombosis and Metabolic Disease, Hull York Medical School, University of Hull, Hull, HU6 7RX, UK.
Lewis, Niamh
  • Institute of Aging and Chronic Disease, University of Liverpool, Liverpool, UK.
Adeniyi, Tope
  • Department of Reproductive Medicine, Manchester University NHS Foundation Trust, Manchester Academic Health Sciences Centre UK, Manchester, UK.
Leese, Henry J
  • Centre for Atherothrombosis and Metabolic Disease, Hull York Medical School, University of Hull, Hull, HU6 7RX, UK.
Brison, Daniel R
  • Department of Reproductive Medicine, Manchester University NHS Foundation Trust, Manchester Academic Health Sciences Centre UK, Manchester, UK.
  • Maternal and Fetal Health Research Centre, School of Medical Sciences, University of Manchester UK, Manchester, UK.
Sturmey, Roger G
  • Centre for Atherothrombosis and Metabolic Disease, Hull York Medical School, University of Hull, Hull, HU6 7RX, UK. roger.sturmey@hyms.ac.uk.

MeSH Terms

  • Animals
  • Biosensing Techniques / methods
  • Cattle
  • Embryo, Mammalian / metabolism
  • Embryonic Development
  • Female
  • Fertilization
  • Horses
  • Humans
  • Mice
  • Mitochondria / metabolism
  • Oocytes / metabolism
  • Oxygen Consumption

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 69 references
  1. Reynier P, May-Panloup P, Chrétien MF, Morgan CJ, Jean M, Savagner F, Barrière P, Malthièry Y. Mitochondrial DNA content affects the fertilizability of human oocytes.. Mol Hum Reprod 2001 May;7(5):425-9.
    doi: 10.1093/molehr/7.5.425pubmed: 11331664google scholar: lookup
  2. Collado-Fernandez E, Picton HM, Dumollard R. Metabolism throughout follicle and oocyte development in mammals.. Int J Dev Biol 2012;56(10-12):799-808.
    doi: 10.1387/ijdb.120140ecpubmed: 23417402google scholar: lookup
  3. Cotterill M, Harris SE, Collado Fernandez E, Lu J, Huntriss JD, Campbell BK, Picton HM. The activity and copy number of mitochondrial DNA in ovine oocytes throughout oogenesis in vivo and during oocyte maturation in vitro.. Mol Hum Reprod 2013 Jul;19(7):444-50.
    doi: 10.1093/molehr/gat013pmc: PMC3690804pubmed: 23468533google scholar: lookup
  4. Jansen RP. Germline passage of mitochondria: quantitative considerations and possible embryological sequelae.. Hum Reprod 2000 Jul;15 Suppl 2:112-28.
    doi: 10.1093/humrep/15.suppl_2.112pubmed: 11041519google scholar: lookup
  5. Shoubridge EA. Mitochondrial DNA segregation in the developing embryo.. Hum Reprod 2000 Jul;15 Suppl 2:229-34.
    doi: 10.1093/humrep/15.suppl_2.229pubmed: 11041528google scholar: lookup
  6. 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.
    pubmed: 30423285doi: 10.1071/rd17387google scholar: lookup
  7. Motta PM, Nottola SA, Makabe S, Heyn R. Mitochondrial morphology in human fetal and adult female germ cells.. Hum Reprod 2000 Jul;15 Suppl 2:129-47.
    doi: 10.1093/humrep/15.suppl_2.129pubmed: 11041520google scholar: lookup
  8. Sathananthan AH, Trounson AO. Mitochondrial morphology during preimplantational human embryogenesis.. Hum Reprod 2000 Jul;15 Suppl 2:148-59.
    pubmed: 11041521doi: 10.1093/humrep/15.suppl_2.148google scholar: lookup
  9. FRIDHANDLER L, HAFEZ ES, PINCUS G. Developmental changes in the respiratory activity of rabbit ova.. Exp Cell Res 1957 Aug;13(1):132-9.
    pubmed: 13473847doi: 10.1016/0014-4827(57)90054-xgoogle scholar: lookup
  10. Houghton FD, Thompson JG, Kennedy CJ, Leese HJ. Oxygen consumption and energy metabolism of the early mouse embryo.. Mol Reprod Dev 1996 Aug;44(4):476-85.
    pubmed: 8844690doi: 10.1002/(sici)1098-2795(199608)44:4<476::aid-mrd7>3.0.co;2-igoogle scholar: lookup
  11. Thompson JG, Partridge RJ, Houghton FD, Cox CI, Leese HJ. Oxygen uptake and carbohydrate metabolism by in vitro derived bovine embryos.. J Reprod Fertil 1996 Mar;106(2):299-306.
    doi: 10.1530/jrf.0.1060299pubmed: 8699414google scholar: lookup
  12. 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
  13. Lopes AS, Greve T, Callesen H. Quantification of embryo quality by respirometry.. Theriogenology 2007 Jan 1;67(1):21-31.
    doi: 10.1016/j.theriogenology.2006.09.026pubmed: 17109946google scholar: lookup
  14. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells.. Biochem J 2011 Apr 15;435(2):297-312.
    pmc: PMC3076726pubmed: 21726199doi: 10.1042/bj20110162google scholar: lookup
  15. Brinster RL. Embryo development.. J Anim Sci 1974 May;38(5):1003-12.
    doi: 10.2527/jas1974.3851003xpubmed: 4596884google scholar: lookup
  16. Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence.. Hum Reprod 2000 Dec;15(12):2621-33.
    doi: 10.1093/humrep/15.12.2621pubmed: 11098036google scholar: lookup
  17. Mills RM, Brinster RL. Oxygen consumption of preimplantation mouse embryos.. Exp. Cell Res. 1967;47:337–344.
    doi: 10.1016/0014-4827(67)90236-4google scholar: lookup
  18. Herlitz H, Hultborn R. A microspectrophotometric technique for determination of respiration in comparison to the Cartesian diver method. Respiratory activity of rat corpus luteum cells with reference to substrate.. Acta Physiol Scand 1974 Mar;90(3):594-601.
    doi: 10.1111/j.1748-1716.1974.tb05624.xpubmed: 4857348google scholar: lookup
  19. Shiku H, Shiraishi T, Ohya H, Matsue T, Abe H, Hoshi H, Kobayashi M. Oxygen consumption of single bovine embryos probed by scanning electrochemical microscopy.. Anal Chem 2001 Aug 1;73(15):3751-8.
    doi: 10.1021/ac010339jpubmed: 11510844google scholar: lookup
  20. Goto K, Kumasako Y, Koike M, Kanda A, Kido K, Nagaki M, Otsu E, Kawabe F, Kai Y, Utsunomiya T. Prediction of the in vitro developmental competence of early-cleavage-stage human embryos with time-lapse imaging and oxygen consumption rate measurement.. Reprod Med Biol 2018 Jul;17(3):289-296.
    doi: 10.1002/rmb2.12104pmc: PMC6046524pubmed: 30013431google scholar: lookup
  21. Lopes AS, Larsen LH, Ramsing N, Løvendahl P, Räty M, Peippo J, Greve T, Callesen H. Respiration rates of individual bovine in vitro-produced embryos measured with a novel, non-invasive and highly sensitive microsensor system.. Reproduction 2005 Nov;130(5):669-79.
    doi: 10.1530/rep.1.00703pubmed: 16264096google scholar: lookup
  22. M. Obeidat Y. Monitoring Oocyte/Embryo Respiration Using Electrochemical-Based Oxygen Sensors.. Sensors Actuators B Chem 2018;276:72–81.
    doi: 10.1016/j.snb.2018.07.157google scholar: lookup
  23. 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
  24. Tejera A, Herrero J, Viloria T, Romero JL, Gamiz P, Meseguer M. Time-dependent O2 consumption patterns determined optimal time ranges for selecting viable human embryos.. Fertil Steril 2012 Oct;98(4):849-57.e1-3.
    doi: 10.1016/j.fertnstert.2012.06.040pubmed: 22835446google scholar: lookup
  25. Leese HJ, Guerif F, Allgar V, Brison DR, Lundin K, Sturmey RG. Biological optimization, the Goldilocks principle, and how much is lagom in the preimplantation embryo.. Mol Reprod Dev 2016 Sep;83(9):748-754.
    doi: 10.1002/mrd.22684pubmed: 27465801google scholar: lookup
  26. Pelletier M, Billingham LK, Ramaswamy M, Siegel RM. Extracellular flux analysis to monitor glycolytic rates and mitochondrial oxygen consumption.. Methods Enzymol 2014;542:125-49.
    pubmed: 24862264doi: 10.1016/b978-0-12-416618-9.00007-8google scholar: lookup
  27. Leese HJ. Metabolism of the preimplantation embryo: 40 years on.. Reproduction 2012 Apr;143(4):417-27.
    doi: 10.1530/REP-11-0484pubmed: 22408180google scholar: lookup
  28. Eppig JJ. Intercommunication between mammalian oocytes and companion somatic cells.. Bioessays 1991 Nov;13(11):569-74.
    doi: 10.1002/bies.950131105pubmed: 1772412google scholar: lookup
  29. Sanchez-Lazo L, Brisard D, Elis S, Maillard V, Uzbekov R, Labas V, Desmarchais A, Papillier P, Monget P, Uzbekova S. Fatty acid synthesis and oxidation in cumulus cells support oocyte maturation in bovine.. Mol Endocrinol 2014 Sep;28(9):1502-21.
    doi: 10.1210/me.2014-1049pmc: PMC5414796pubmed: 25058602google scholar: lookup
  30. Thompson JG, Lane M, Gilchrist RB. Metabolism of the bovine cumulus-oocyte complex and influence on subsequent developmental competence.. Soc Reprod Fertil Suppl 2007;64:179-90.
    pubmed: 17491147doi: 10.5661/rdr-vi-179google scholar: lookup
  31. Leese HJ, Barton AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos.. J Reprod Fertil 1984 Sep;72(1):9-13.
    doi: 10.1530/jrf.0.0720009pubmed: 6540809google scholar: lookup
  32. Clark AR, Stokes YM, Lane M, Thompson JG. Mathematical modelling of oxygen concentration in bovine and murine cumulus-oocyte complexes.. Reproduction 2006 Jun;131(6):999-1006.
    doi: 10.1530/rep.1.00974pubmed: 16735539google scholar: lookup
  33. 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
  34. 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.
    doi: 10.1262/jrd.2012-082pubmed: 22785440google scholar: lookup
  35. Heinecke JW, Shapiro BM. Respiratory burst oxidase of fertilization.. Proc Natl Acad Sci U S A 1989 Feb;86(4):1259-63.
    doi: 10.1073/pnas.86.4.1259pmc: PMC286667pubmed: 2537493google scholar: lookup
  36. Lopes AS, Lane M, Thompson JG. Oxygen consumption and ROS production are increased at the time of fertilization and cell cleavage in bovine zygotes.. Hum Reprod 2010 Nov;25(11):2762-73.
    pubmed: 20823113doi: 10.1093/humrep/deq221google scholar: lookup
  37. Campbell K, Swann K. Ca2+ oscillations stimulate an ATP increase during fertilization of mouse eggs.. Dev Biol 2006 Oct 1;298(1):225-33.
    doi: 10.1016/j.ydbio.2006.06.032pubmed: 16872595google scholar: lookup
  38. Dumollard R, Hammar K, Porterfield M, Smith PJ, Cibert C, Rouvière C, Sardet C. Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion.. Development 2003 Feb;130(4):683-92.
    doi: 10.1242/dev.00296pubmed: 12505999google scholar: lookup
  39. Van Blerkom J, Davis P, Alexander S. Inner mitochondrial membrane potential (DeltaPsim), cytoplasmic ATP content and free Ca2+ levels in metaphase II mouse oocytes.. Hum Reprod 2003 Nov;18(11):2429-40.
    doi: 10.1093/humrep/deg466pubmed: 14585897google scholar: lookup
  40. Sutovsky P, Van Leyen K, McCauley T, Day BN, Sutovsky M. Degradation of paternal mitochondria after fertilization: implications for heteroplasmy, assisted reproductive technologies and mtDNA inheritance.. Reprod Biomed Online 2004 Jan;8(1):24-33.
    doi: 10.1016/S1472-6483(10)60495-6pubmed: 14759284google scholar: lookup
  41. 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
  42. Betts DH, Madan P. Permanent embryo arrest: molecular and cellular concepts.. Mol Hum Reprod 2008 Aug;14(8):445-53.
    doi: 10.1093/molehr/gan035pmc: PMC2515101pubmed: 18511487google scholar: lookup
  43. Matwee C, Betts DH, King WA. Apoptosis in the early bovine embryo.. Zygote 2000 Feb;8(1):57-68.
    doi: 10.1017/S0967199400000836pubmed: 10840875google scholar: lookup
  44. Artley JK, Braude PR, Johnson MH. Gene activity and cleavage arrest in human pre-embryos.. Hum Reprod 1992 Aug;7(7):1014-21.
    doi: 10.1093/oxfordjournals.humrep.a137761pubmed: 1430119google scholar: lookup
  45. Almeida PA, Bolton VN. The relationship between chromosomal abnormality in the human preimplantation embryo and development in vitro.. Reprod Fertil Dev 1996;8(2):235-41.
    doi: 10.1071/RD9960235pubmed: 8726861google scholar: lookup
  46. Burruel V, Klooster K, Barker CM, Pera RR, Meyers S. Abnormal early cleavage events predict early embryo demise: sperm oxidative stress and early abnormal cleavage.. Sci Rep 2014 Oct 13;4:6598.
    pmc: PMC4194434pubmed: 25307782doi: 10.1038/srep06598google scholar: lookup
  47. Kimura N, Tsunoda S, Iuchi Y, Abe H, Totsukawa K, Fujii J. Intrinsic oxidative stress causes either 2-cell arrest or cell death depending on developmental stage of the embryos from SOD1-deficient mice.. Mol Hum Reprod 2010 Jul;16(7):441-51.
    doi: 10.1093/molehr/gaq007pubmed: 20223891google scholar: lookup
  48. Favetta LA, St John EJ, King WA, Betts DH. High levels of p66shc and intracellular ROS in permanently arrested early embryos.. Free Radic Biol Med 2007 Apr 15;42(8):1201-10.
    doi: 10.1016/j.freeradbiomed.2007.01.018pubmed: 17382201google scholar: lookup
  49. Tejera A, Castelló D, de Los Santos JM, Pellicer A, Remohí J, Meseguer M. Combination of metabolism measurement and a time-lapse system provides an embryo selection method based on oxygen uptake and chronology of cytokinesis timing.. Fertil Steril 2016 Jul;106(1):119-126.e2.
    doi: 10.1016/j.fertnstert.2016.03.019pubmed: 27037460google scholar: lookup
  50. Muoio DM. Metabolic inflexibility: when mitochondrial indecision leads to metabolic gridlock.. Cell 2014 Dec 4;159(6):1253-62.
    doi: 10.1016/j.cell.2014.11.034pmc: PMC4765362pubmed: 25480291google scholar: lookup
  51. Brand MD. Uncoupling to survive? The role of mitochondrial inefficiency in ageing.. Exp Gerontol 2000 Sep;35(6-7):811-20.
    doi: 10.1016/S0531-5565(00)00135-2pubmed: 11053672google scholar: lookup
  52. Cadenas S. Mitochondrial uncoupling, ROS generation and cardioprotection.. Biochim Biophys Acta Bioenerg 2018 Sep;1859(9):940-950.
    doi: 10.1016/j.bbabio.2018.05.019pubmed: 29859845google scholar: lookup
  53. Woods DC. Mitochondrial Heterogeneity: Evaluating Mitochondrial Subpopulation Dynamics in Stem Cells.. Stem Cells Int 2017;2017:7068567.
    doi: 10.1155/2017/7068567pmc: PMC5516713pubmed: 28757879google scholar: lookup
  54. 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
  55. Trimarchi JR, Liu L, Porterfield DM, Smith PJ, Keefe DL. Oxidative phosphorylation-dependent and -independent oxygen consumption by individual preimplantation mouse embryos.. Biol Reprod 2000 Jun;62(6):1866-74.
    doi: 10.1095/biolreprod62.6.1866pubmed: 10819794google scholar: lookup
  56. Herst PM, Berridge MV. Cell surface oxygen consumption: a major contributor to cellular oxygen consumption in glycolytic cancer cell lines.. Biochim Biophys Acta 2007 Feb;1767(2):170-7.
    pubmed: 17266920doi: 10.1016/j.bbabio.2006.11.018google scholar: lookup
  57. Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling.. Ann N Y Acad Sci 2008 Dec;1147:37-52.
    doi: 10.1196/annals.1427.015pmc: PMC2869479pubmed: 19076429google scholar: lookup
  58. Krisher RL, Prather RS. A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation.. Mol Reprod Dev 2012 May;79(5):311-20.
    doi: 10.1002/mrd.22037pmc: PMC3328638pubmed: 22431437google scholar: lookup
  59. Nickens KP, Wikstrom JD, Shirihai OS, Patierno SR, Ceryak S. A bioenergetic profile of non-transformed fibroblasts uncovers a link between death-resistance and enhanced spare respiratory capacity.. Mitochondrion 2013 Nov;13(6):662-7.
    doi: 10.1016/j.mito.2013.09.005pmc: PMC3837383pubmed: 24075934google scholar: lookup
  60. Hill BG, Dranka BP, Zou L, Chatham JC, Darley-Usmar VM. Importance of the bioenergetic reserve capacity in response to cardiomyocyte stress induced by 4-hydroxynonenal.. Biochem J 2009 Oct 23;424(1):99-107.
    doi: 10.1042/BJ20090934pmc: PMC2872628pubmed: 19740075google scholar: lookup
  61. Pfleger J, He M, Abdellatif M. Mitochondrial complex II is a source of the reserve respiratory capacity that is regulated by metabolic sensors and promotes cell survival.. Cell Death Dis 2015 Jul 30;6(7):e1835.
    doi: 10.1038/cddis.2015.202pmc: PMC4650745pubmed: 26225774google scholar: lookup
  62. Eckert JJ, Fleming TP. The effect of nutrition and environment on the preimplantation embryo.. Obstet. Gynaecol. 2011;13:43–48.
  63. Leary C, Leese HJ, Sturmey RG. Human embryos from overweight and obese women display phenotypic and metabolic abnormalities.. Hum Reprod 2015 Jan;30(1):122-32.
    doi: 10.1093/humrep/deu276pubmed: 25391239google scholar: lookup
  64. Orsi NM, Leese HJ. Amino acid metabolism of preimplantation bovine embryos cultured with bovine serum albumin or polyvinyl alcohol.. Theriogenology 2004 Jan 15;61(2-3):561-72.
    doi: 10.1016/S0093-691X(03)00206-1pubmed: 14662152google scholar: lookup
  65. Lewis N, Hinrichs K, Schnauffer K, Morganti M, Argo CM. Effect of oocyte source and transport time on rates of equine oocyte maturation and cleavage after fertilization by ICSI, with a note on the validation of equine embryo morphological classification.. Clin. Theriogenology 2016;8:25–39.
  66. 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
  67. Ruane PT, Berneau SC, Koeck R, Watts J, Kimber SJ, Brison DR, Westwood M, Aplin JD. Apposition to endometrial epithelial cells activates mouse blastocysts for implantation.. Mol Hum Reprod 2017 Sep 1;23(9):617-627.
    doi: 10.1093/molehr/gax043pubmed: 28911212google scholar: lookup
  68. Gelbaya TA, Nardo LG, Fitzgerald CT, Horne G, Brison DR, Lieberman BA. Ovarian response to gonadotropins after laparoscopic salpingectomy or the division of fallopian tubes for hydrosalpinges.. Fertil Steril 2006 May;85(5):1464-8.
    doi: 10.1016/j.fertnstert.2005.10.036pubmed: 16580673google scholar: lookup
  69. Roberts S, McGowan L, Hirst W, Brison D, Vail A, Lieberman B. Towards single embryo transfer? Modelling clinical outcomes of potential treatment choices using multiple data sources: predictive models and patient perspectives.. Health Technol Assess 2010 Jul;14(38):1-237.
    pubmed: 20684810doi: 10.3310/hta14380google scholar: lookup

Citations

This article has been cited 19 times.
  1. Siemers KM, Klein AK, Baack ML. Mitochondrial Dysfunction in PCOS: Insights into Reproductive Organ Pathophysiology.. Int J Mol Sci 2023 Aug 23;24(17).
    doi: 10.3390/ijms241713123pubmed: 37685928google scholar: lookup
  2. Satouh Y, Sato K. Reorganization, specialization, and degradation of oocyte maternal components for early development.. Reprod Med Biol 2023 Jan-Dec;22(1):e12505.
    doi: 10.1002/rmb2.12505pubmed: 36726596google scholar: lookup
  3. Mastrorocco A, Cacopardo L, Temerario L, Martino NA, Tridente F, Rizzo A, Lacalandra GM, Robbe D, Carluccio A, Dell'Aquila ME. Investigating and Modelling an Engineered Millifluidic In Vitro Oocyte Maturation System Reproducing the Physiological Ovary Environment in the Sheep Model.. Cells 2022 Nov 15;11(22).
    doi: 10.3390/cells11223611pubmed: 36429039google scholar: lookup
  4. Pladevall-Morera D, Zylicz JJ. Chromatin as a sensor of metabolic changes during early development.. Front Cell Dev Biol 2022;10:1014498.
    doi: 10.3389/fcell.2022.1014498pubmed: 36299478google scholar: lookup
  5. Kim CW, Lee HJ, Ahn D, Go RE, Choi KC. Establishment of a platform for measuring mitochondrial oxygen consumption rate for cardiac mitochondrial toxicity.. Toxicol Res 2022 Oct;38(4):511-522.
    doi: 10.1007/s43188-022-00136-2pubmed: 36277363google scholar: lookup
  6. Wang CY, Wang CH, Mai RT, Chen TW, Li CW, Chao CH. Mutant p53-microRNA-200c-ZEB2-Axis-Induced CPT1C Elevation Contributes to Metabolic Reprogramming and Tumor Progression in Basal-Like Breast Cancers.. Front Oncol 2022;12:940402.
    doi: 10.3389/fonc.2022.940402pubmed: 35936710google scholar: lookup
  7. Tan TCY, Brown HM, Thompson JG, Mustafa S, Dunning KR. Optical imaging detects metabolic signatures associated with oocyte quality†.. Biol Reprod 2022 Oct 11;107(4):1014-1025.
    doi: 10.1093/biolre/ioac145pubmed: 35863764google scholar: lookup
  8. Gonzalez Porras MA, Stojkova K, Acosta FM, Rathbone CR, Brey EM. Engineering Human Beige Adipose Tissue.. Front Bioeng Biotechnol 2022;10:906395.
    doi: 10.3389/fbioe.2022.906395pubmed: 35845420google scholar: lookup
  9. Romero-Morales AI, Robertson GL, Rastogi A, Rasmussen ML, Temuri H, McElroy GS, Chakrabarty RP, Hsu L, Almonacid PM, Millis BA, Chandel NS, Cartailler JP, Gama V. Human iPSC-derived cerebral organoids model features of Leigh syndrome and reveal abnormal corticogenesis.. Development 2022 Oct 15;149(20).
    doi: 10.1242/dev.199914pubmed: 35792828google scholar: lookup
  10. Gorczyca G, Wartalski K, Romek M, Samiec M, Duda M. The Molecular Quality and Mitochondrial Activity of Porcine Cumulus-Oocyte Complexes Are Affected by Their Exposure to Three Endocrine-Active Compounds under 3D In Vitro Maturation Conditions.. Int J Mol Sci 2022 Apr 20;23(9).
    doi: 10.3390/ijms23094572pubmed: 35562963google scholar: lookup
  11. Musson R, Gąsior Ł, Bisogno S, Ptak GE. DNA damage in preimplantation embryos and gametes: specification, clinical relevance and repair strategies.. Hum Reprod Update 2022 May 2;28(3):376-399.
    doi: 10.1093/humupd/dmab046pubmed: 35021196google scholar: lookup
  12. Gorczyca G, Wartalski K, Wiater J, Samiec M, Tabarowski Z, Duda M. Anabolic Steroids-Driven Regulation of Porcine Ovarian Putative Stem Cells Favors the Onset of Their Neoplastic Transformation.. Int J Mol Sci 2021 Oct 30;22(21).
    doi: 10.3390/ijms222111800pubmed: 34769230google scholar: lookup
  13. Tedjo W, Obeidat Y, Catandi G, Carnevale E, Chen T. Real-Time Analysis of Oxygen Gradient in Oocyte Respiration Using a High-Density Microelectrode Array.. Biosensors (Basel) 2021 Jul 29;11(8).
    doi: 10.3390/bios11080256pubmed: 34436058google scholar: lookup
  14. Mastrorocco A, Cacopardo L, Lamanna D, Temerario L, Brunetti G, Carluccio A, Robbe D, Dell'Aquila ME. Bioengineering Approaches to Improve In Vitro Performance of Prepubertal Lamb Oocytes.. Cells 2021 Jun 10;10(6).
    doi: 10.3390/cells10061458pubmed: 34200771google scholar: lookup
  15. Yureneva S, Averkova V, Silachev D, Donnikov A, Gavisova A, Serov V, Sukhikh G. Searching for female reproductive aging and longevity biomarkers.. Aging (Albany NY) 2021 Jun 22;13(12):16873-16894.
    doi: 10.18632/aging.203206pubmed: 34156973google 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-20-0494pubmed: 33539317google scholar: lookup
  17. Blanco-Prieto O, Catalán J, Trujillo-Rojas L, Peña A, Rivera Del Álamo MM, Llavanera M, Bonet S, Fernández-Novell JM, Yeste M, Rodríguez-Gil JE. Red LED Light Acts on the Mitochondrial Electron Chain of Mammalian Sperm via Light-Time Exposure-Dependent Mechanisms.. Cells 2020 Nov 26;9(12).
    doi: 10.3390/cells9122546pubmed: 33256077google scholar: lookup
  18. Sinharoy P, Aziz AH, Majewska NI, Ahuja S, Handlogten MW. Perfusion reduces bispecific antibody aggregation via mitigating mitochondrial dysfunction-induced glutathione oxidation and ER stress in CHO cells.. Sci Rep 2020 Oct 6;10(1):16620.
    doi: 10.1038/s41598-020-73573-4pubmed: 33024175google scholar: lookup
  19. Cobley JN. Mechanisms of Mitochondrial ROS Production in Assisted Reproduction: The Known, the Unknown, and the Intriguing.. Antioxidants (Basel) 2020 Sep 29;9(10).
    doi: 10.3390/antiox9100933pubmed: 33003362google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.