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PloS one2017; 12(11); e0186247; doi: 10.1371/journal.pone.0186247

Skeletal muscle mitochondrial bioenergetics and associations with myostatin genotypes in the Thoroughbred horse.

Abstract: Variation in the myostatin (MSTN) gene has been reported to be associated with race distance, body composition and skeletal muscle fibre composition in the horse. The aim of the present study was to test the hypothesis that MSTN variation influences mitochondrial phenotypes in equine skeletal muscle. Mitochondrial abundance and skeletal muscle fibre types were measured in whole muscle biopsies from the gluteus medius of n = 82 untrained (21 ± 3 months) Thoroughbred horses. Skeletal muscle fibre type proportions were significantly (p < 0.01) different among the three MSTN genotypes and mitochondrial content was significantly (p T (C) and the SINE insertion 227 bp polymorphism (I). Evaluation of mitochondrial complex activities indicated higher combined mitochondrial complex I+III and II+III activities in the presence of the C-allele / I allele (p ≤ 0.05). The restoration of complex I+III and complex II+III activities following addition of exogenous coenzyme Q1 (ubiquinone1) (CoQ1) in vitro in the TT/NN (homozygous T allele/homozygous no insertion) cohort indicated decreased coenzyme Q in these animals. In addition, decreased gene expression in two coenzyme Q (CoQ) biosynthesis pathway genes (COQ4, p ≤ 0.05; ADCK3, p ≤ 0.01) in the TT/NN horses was observed. This study has identified several mitochondrial phenotypes associated with MSTN genotype in untrained Thoroughbred horses and in addition, our findings suggest that nutritional supplementation with CoQ may aid to restore coenzyme Q activity in TT/NN horses.
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Publication Date: 2017-11-30 PubMed ID: 29190290PubMed Central: PMC5708611DOI: 10.1371/journal.pone.0186247Google 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 explored the impact of myostatin (MSTN) genetic variations on the mitochondrial characteristics in horse muscle tissue. The study demonstrated a significant link between MSTN variations and mitochondrial activity, and proposed this may be potential area of focus for nutritional supplementation.

Objective of the Research

The study aimed to explore the possible influence of myostatin (MSTN) variation on mitochondrial features in the skeletal muscles of untrained Thoroughbred horses. The hypothesis was based on the previous reports suggesting an association between MSTN gene variation and several physical attributes in horses, such as their capability for racing over different distances, body composition, and skeletal muscle fiber composition.

Research Methodology

  • The research was conducted on whole muscle biopsies from the gluteus medius of 82 untrained Thoroughbred horses, aged 21 ± 3 months.
  • Researchers analyzed the mitochondrial abundance and skeletal muscle fibre types in these samples.
  • They specifically looked for the presence of MSTN genotypes, including the C-allele of SNP g.66493737C>T and the SINE insertion 227 bp polymorphism.

Findings of the Research

  • The skeletal muscle fibre type proportions were found to be significantly different among the horses, depending on their MSTN genotype.
  • Notably, mitochondrial content was found to be significantly lower in horses carrying the combined presence of the C-allele and the SINE insertion polymorphism.
  • Upon evaluation of mitochondrial complex activities, they exhibited higher combined mitochondrial complex I+III and II+III activities in horses with the C-allele and the SINE insertion polymorphism.
  • The team also observed decreased gene regulations within two coenzyme Q (CoQ) biosynthesis pathway genes (COQ4 and ADCK3) in the TT/NN horses, indicating decreased coenzyme Q levels in them.

Conclusions and Implications

  • The results of this study reveal several mitochondrial phenotypes associated with differences in MSTN genotype in untrained Thoroughbred horses.
  • The findings suggest that dietary supplementation with coenzyme Q (CoQ) may assist in the restoration of coenzyme Q activity in horses carrying certain MSTN genotypes, particularly TT/NN genotype horses. This could eventually contribute to the improvement of the horses’ physical performance.

Cite This Article

APA
Rooney MF, Porter RK, Katz LM, Hill EW. (2017). Skeletal muscle mitochondrial bioenergetics and associations with myostatin genotypes in the Thoroughbred horse. PLoS One, 12(11), e0186247. https://doi.org/10.1371/journal.pone.0186247

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 12
Issue: 11
Pages: e0186247
PII: e0186247

Researcher Affiliations

Rooney, Mary F
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland.
  • School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute (TBSI), Trinity College Dublin, Dublin 2, Ireland.
Porter, Richard K
  • School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute (TBSI), Trinity College Dublin, Dublin 2, Ireland.
Katz, Lisa M
  • UCD School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland.
Hill, Emmeline W
  • UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland.

MeSH Terms

  • Age Factors
  • Animals
  • Energy Metabolism
  • Female
  • Genotype
  • Horses / genetics
  • Horses / metabolism
  • Male
  • Mitochondria, Muscle / metabolism
  • Muscle, Skeletal / metabolism
  • Myostatin / genetics
  • Phenotype
  • Physical Conditioning, Animal
  • Polymorphism, Single Nucleotide
  • Short Interspersed Nucleotide Elements

Conflict of Interest Statement

A patent application (EP17190252.1) entitled “A Genotype specific Nutritional Supplement for Horses” has been submitted to the European Patent Office, based on these research findings. All authors of this manuscript are named on this patent application. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

References

This article includes 90 references
  1. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member.. Nature 1997 May 1;387(6628):83-90.
    doi: 10.1038/387083a0pubmed: 9139826google scholar: lookup
  2. Joulia-Ekaza D, Cabello G. Myostatin regulation of muscle development: molecular basis, natural mutations, physiopathological aspects.. Exp Cell Res 2006 Aug 1;312(13):2401-14.
    doi: 10.1016/j.yexcr.2006.04.012pubmed: 16793037google scholar: lookup
  3. Zhu X, Hadhazy M, Wehling M, Tidball JG, McNally EM. Dominant negative myostatin produces hypertrophy without hyperplasia in muscle.. FEBS Lett 2000 May 26;474(1):71-5.
    pubmed: 10828454doi: 10.1016/s0014-5793(00)01570-2google scholar: lookup
  4. Yang J, Ratovitski T, Brady JP, Solomon MB, Wells KD, Wall RJ. Expression of myostatin pro domain results in muscular transgenic mice.. Mol Reprod Dev 2001 Nov;60(3):351-61.
    doi: 10.1002/mrd.1097pubmed: 11599046google scholar: lookup
  5. Girgenrath S, Song K, Whittemore LA. Loss of myostatin expression alters fiber-type distribution and expression of myosin heavy chain isoforms in slow- and fast-type skeletal muscle.. Muscle Nerve 2005 Jan;31(1):34-40.
    doi: 10.1002/mus.20175pubmed: 15468312google scholar: lookup
  6. Amthor H, Macharia R, Navarrete R, Schuelke M, Brown SC, Otto A, Voit T, Muntoni F, Vrbóva G, Partridge T, Zammit P, Bunger L, Patel K. Lack of myostatin results in excessive muscle growth but impaired force generation.. Proc Natl Acad Sci U S A 2007 Feb 6;104(6):1835-40.
    doi: 10.1073/pnas.0604893104pmc: PMC1794294pubmed: 17267614google scholar: lookup
  7. Ploquin C, Chabi B, Fouret G, Vernus B, Feillet-Coudray C, Coudray C, Bonnieu A, Ramonatxo C. Lack of myostatin alters intermyofibrillar mitochondria activity, unbalances redox status, and impairs tolerance to chronic repetitive contractions in muscle.. Am J Physiol Endocrinol Metab 2012 Apr 15;302(8):E1000-8.
    doi: 10.1152/ajpendo.00652.2011pubmed: 22318951google scholar: lookup
  8. Mathieu O, Krauer R, Hoppeler H, Gehr P, Lindstedt SL, Alexander RM, Taylor CR, Weibel ER. Design of the mammalian respiratory system. VII. Scaling mitochondrial volume in skeletal muscle to body mass.. Respir Physiol 1981 Apr;44(1):113-28.
    pubmed: 7232882doi: 10.1016/0034-5687(81)90079-7google scholar: lookup
  9. Cunningham EP, Dooley JJ, Splan RK, Bradley DG. Microsatellite diversity, pedigree relatedness and the contributions of founder lineages to thoroughbred horses.. Anim Genet 2001 Dec;32(6):360-4.
    pubmed: 11736806doi: 10.1046/j.1365-2052.2001.00785.xgoogle scholar: lookup
  10. Hill EW, Bradley DG, Al-Barody M, Ertugrul O, Splan RK, Zakharov I, Cunningham EP. History and integrity of thoroughbred dam lines revealed in equine mtDNA variation.. Anim Genet 2002 Aug;33(4):287-94.
    pubmed: 12139508doi: 10.1046/j.1365-2052.2002.00870.xgoogle scholar: lookup
  11. Bower MA, Campana MG, Whitten M, Edwards CJ, Jones H, Barrett E, Cassidy R, Nisbet RE, Hill EW, Howe CJ, Binns M. The cosmopolitan maternal heritage of the Thoroughbred racehorse breed shows a significant contribution from British and Irish native mares.. Biol Lett 2011 Apr 23;7(2):316-20.
    doi: 10.1098/rsbl.2010.0800pmc: PMC3061175pubmed: 20926431google scholar: lookup
  12. Jones JH, Longworth KE, Lindholm A, Conley KE, Karas RH, Kayar SR, Taylor CR. Oxygen transport during exercise in large mammals. I. Adaptive variation in oxygen demand.. J Appl Physiol (1985) 1989 Aug;67(2):862-70.
    pubmed: 2793686doi: 10.1152/jappl.1989.67.2.862google scholar: lookup
  13. Jones JH, Lindstedt SL. Limits to maximal performance.. Annu Rev Physiol 1993;55:547-69.
    pubmed: 8466184doi: 10.1146/annurev.ph.55.030193.002555google scholar: lookup
  14. Young LE, Marlin DJ, Deaton C, Brown-Feltner H, Roberts CA, Wood JL. Heart size estimated by echocardiography correlates with maximal oxygen uptake.. Equine Vet J Suppl 2002 Sep;(34):467-71.
    doi: 10.1111/j.2042-3306.2002.tb05467.xpubmed: 12405735google scholar: lookup
  15. Kayar SR, Hoppeler H, Lindstedt SL, Claassen H, Jones JH, Essen-Gustavsson B, Taylor CR. Total muscle mitochondrial volume in relation to aerobic capacity of horses and steers.. Pflugers Arch 1989 Feb;413(4):343-7.
    pubmed: 2928085doi: 10.1007/bf00584481google scholar: lookup
  16. Binns MM, Boehler DA, Lambert DH. Identification of the myostatin locus (MSTN) as having a major effect on optimum racing distance in the Thoroughbred horse in the USA.. Anim Genet 2010 Dec;41 Suppl 2:154-8.
    pubmed: 21070290doi: 10.1111/j.1365-2052.2010.02126.xgoogle scholar: lookup
  17. Hill EW, Gu J, Eivers SS, Fonseca RG, McGivney BA, Govindarajan P, Orr N, Katz LM, MacHugh DE. A sequence polymorphism in MSTN predicts sprinting ability and racing stamina in thoroughbred horses.. PLoS One 2010 Jan 20;5(1):e8645.
    doi: 10.1371/journal.pone.0008645pmc: PMC2808334pubmed: 20098749google scholar: lookup
  18. Hill EW, McGivney BA, Gu J, Whiston R, Machugh DE. A genome-wide SNP-association study confirms a sequence variant (g.66493737C>T) in the equine myostatin (MSTN) gene as the most powerful predictor of optimum racing distance for Thoroughbred racehorses.. BMC Genomics 2010 Oct 11;11:552.
    doi: 10.1186/1471-2164-11-552pmc: PMC3091701pubmed: 20932346google scholar: lookup
  19. Tozaki T, Miyake T, Kakoi H, Gawahara H, Sugita S, Hasegawa T, Ishida N, Hirota K, Nakano Y. A genome-wide association study for racing performances in Thoroughbreds clarifies a candidate region near the MSTN gene.. Anim Genet 2010 Dec;41 Suppl 2:28-35.
    pubmed: 21070273doi: 10.1111/j.1365-2052.2010.02095.xgoogle scholar: lookup
  20. van den Hoven R, Gür E, Schlamanig M, Hofer M, Onmaz AC, Steinborn R. Putative regulation mechanism for the MSTN gene by a CpG island generated by the SINE marker Ins227bp.. BMC Vet Res 2015 Jun 23;11:138.
    pmc: PMC4476204pubmed: 26100061doi: 10.1186/s12917-015-0428-3google scholar: lookup
  21. Tozaki T, Sato F, Hill EW, Miyake T, Endo Y, Kakoi H, Gawahara H, Hirota K, Nakano Y, Nambo Y, Kurosawa M. Sequence variants at the myostatin gene locus influence the body composition of Thoroughbred horses.. J Vet Med Sci 2011 Dec;73(12):1617-24.
    pubmed: 21836385doi: 10.1292/jvms.11-0295google scholar: lookup
  22. Petersen JL, Mickelson JR, Rendahl AK, Valberg SJ, Andersson LS, Axelsson J, Bailey E, Bannasch D, Binns MM, Borges AS, Brama P, da Câmara Machado A, Capomaccio S, Cappelli K, Cothran EG, Distl O, Fox-Clipsham L, Graves KT, Guérin G, Haase B, Hasegawa T, Hemmann K, Hill EW, Leeb T, Lindgren G, Lohi H, Lopes MS, McGivney BA, Mikko S, Orr N, Penedo MC, Piercy RJ, Raekallio M, Rieder S, Røed KH, Swinburne J, Tozaki T, Vaudin M, Wade CM, McCue ME. Genome-wide analysis reveals selection for important traits in domestic horse breeds.. PLoS Genet 2013;9(1):e1003211.
    doi: 10.1371/journal.pgen.1003211pmc: PMC3547851pubmed: 23349635google scholar: lookup
  23. Petersen JL, Valberg SJ, Mickelson JR, McCue ME. Haplotype diversity in the equine myostatin gene with focus on variants associated with race distance propensity and muscle fiber type proportions.. Anim Genet 2014 Dec;45(6):827-35.
    doi: 10.1111/age.12205pmc: PMC4211974pubmed: 25160752google scholar: lookup
  24. Rivero JL, Serrano AL, Barrey E, Valette JP, Jouglin M. Analysis of myosin heavy chains at the protein level in horse skeletal muscle.. J Muscle Res Cell Motil 1999 Feb;20(2):211-21.
    pubmed: 10412092doi: 10.1023/a:1005461214800google scholar: lookup
  25. Ledwith A, McGowan CM. Muscle biopsy: a routine diagnostic procedure.. Equine Veterinary Education 2004;16(2):62–7.
  26. Hill EW, Fonseca RG, McGivney BA, Gu J, MacHugh DE, Katz LM. MSTN genotype (g.66493737C/T) association with speed indices in Thoroughbred racehorses.. J Appl Physiol (1985) 2012 Jan;112(1):86-90.
    doi: 10.1152/japplphysiol.00793.2011pubmed: 22016373google scholar: lookup
  27. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid.. Anal Biochem 1985 Oct;150(1):76-85.
    pubmed: 3843705doi: 10.1016/0003-2697(85)90442-7google scholar: lookup
  28. Srere PA. Citrate synthase: [EC 4.1.3.7. Citrate oxaloacetate-lyase (CoA-acetylating)]. Methods in Enzymology Volume 13: Academic Press; 1969. p. 3–11.
  29. Ragan C, Wilson M, Darley-Usmar V, Lowe P. Subfractionation of mitochondria and isolation of the proteins of oxidative phosphorylation.. Mitochondria: a practical approach 1987:79–112.
  30. Hatefi Y. Resolution of complex II and isolation of succinate dehydrogenase (EC 1.3.99.1).. Methods Enzymol 1978;53:27-35.
    pubmed: 713837doi: 10.1016/s0076-6879(78)53009-7google scholar: lookup
  31. Wharton DC, Tzagoloff A. Cytochrome oxidase from beef heart mitochondria.. Methods in enzymology 1967;10:245–50.
  32. Powers WJ, Haas RH, Le T, Videen TO, Hershey T, McGee-Minnich L, Perlmutter JS. Normal platelet mitochondrial complex I activity in Huntington's disease.. Neurobiol Dis 2007 Jul;27(1):99-101.
    doi: 10.1016/j.nbd.2007.04.008pmc: PMC2140002pubmed: 17543533google scholar: lookup
  33. King TE. Preparations of succinate—cytochrome c reductase and the cytochrome bc 1 particle, and reconstitution of succinate-cytochrome c reductase.. Methods in enzymology 1967;10:216–25.
  34. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA. Primer3Plus, an enhanced web interface to Primer3.. Nucleic Acids Res 2007 Jul;35(Web Server issue):W71-4.
    pmc: PMC1933133pubmed: 17485472doi: 10.1093/nar/gkm306google scholar: lookup
  35. Hemmings KM, Parr T, Daniel ZC, Picard B, Buttery PJ, Brameld JM. Examination of myosin heavy chain isoform expression in ovine skeletal muscles.. J Anim Sci 2009 Dec;87(12):3915-22.
    doi: 10.2527/jas.2009-2067pubmed: 19684280google scholar: lookup
  36. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  37. Cappelli K, Felicetti M, Capomaccio S, Spinsanti G, Silvestrelli M, Supplizi AV. Exercise induced stress in horses: selection of the most stable reference genes for quantitative RT-PCR normalization.. BMC Mol Biol 2008 May 19;9:49.
    pmc: PMC2412902pubmed: 18489742doi: 10.1186/1471-2199-9-49google scholar: lookup
  38. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.. Nature 1970 Aug 15;227(5259):680-5.
    pubmed: 5432063doi: 10.1038/227680a0google scholar: lookup
  39. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis.. Nat Methods 2012 Jul;9(7):671-5.
    pmc: PMC5554542pubmed: 22930834doi: 10.1038/nmeth.2089google scholar: lookup
  40. Kirby DM, Thorburn DR, Turnbull DM, Taylor RW. Biochemical assays of respiratory chain complex activity.. Methods Cell Biol 2007;80:93-119.
    doi: 10.1016/S0091-679X(06)80004-Xpubmed: 17445690google scholar: lookup
  41. Jonckheere AI, Smeitink JA, Rodenburg RJ. Mitochondrial ATP synthase: architecture, function and pathology.. J Inherit Metab Dis 2012 Mar;35(2):211-25.
    doi: 10.1007/s10545-011-9382-9pmc: PMC3278611pubmed: 21874297google scholar: lookup
  42. Ogata T. A histochemical study of the red and white muscle fibers. Part 1. Activity of the succinoxydase system in muscle fibers.. Acta Medica 1958;Okayama(12):216–27.
  43. Ingjer F. Effects of endurance training on muscle fibre ATP-ase activity, capillary supply and mitochondrial content in man.. J Physiol 1979 Sep;294:419-32.
    pmc: PMC1280565pubmed: 159945doi: 10.1113/jphysiol.1979.sp012938google scholar: lookup
  44. Greene HM, Wickler SJ, Tucker RL, London C. Fiber type composition of the middle gluteal muscle of mules.. Journal of Equine Veterinary Science 1995;15(9):388–91.
    doi: 10.1016/S0737-0806(07)80482-5google scholar: lookup
  45. Zierath JR, Hawley JA. Skeletal muscle fiber type: influence on contractile and metabolic properties.. PLoS Biol 2004 Oct;2(10):e348.
    doi: 10.1371/journal.pbio.0020348pmc: PMC521732pubmed: 15486583google scholar: lookup
  46. Serrano AL, Quiroz-Rothe E, Rivero JL. Early and long-term changes of equine skeletal muscle in response to endurance training and detraining.. Pflugers Arch 2000 Dec;441(2-3):263-74.
    pubmed: 11211112doi: 10.1007/s004240000408google scholar: lookup
  47. Lagier-Tourenne C, Tazir M, López LC, Quinzii CM, Assoum M, Drouot N, Busso C, Makri S, Ali-Pacha L, Benhassine T, Anheim M, Lynch DR, Thibault C, Plewniak F, Bianchetti L, Tranchant C, Poch O, DiMauro S, Mandel JL, Barros MH, Hirano M, Koenig M. ADCK3, an ancestral kinase, is mutated in a form of recessive ataxia associated with coenzyme Q10 deficiency.. Am J Hum Genet 2008 Mar;82(3):661-72.
    doi: 10.1016/j.ajhg.2007.12.024pmc: PMC2427193pubmed: 18319074google scholar: lookup
  48. Mollet J, Delahodde A, Serre V, Chretien D, Schlemmer D, Lombes A, Boddaert N, Desguerre I, de Lonlay P, de Baulny HO, Munnich A, Rötig A. CABC1 gene mutations cause ubiquinone deficiency with cerebellar ataxia and seizures.. Am J Hum Genet 2008 Mar;82(3):623-30.
    doi: 10.1016/j.ajhg.2007.12.022pmc: PMC2427298pubmed: 18319072google scholar: lookup
  49. Salviati L, Trevisson E, Rodriguez Hernandez MA, Casarin A, Pertegato V, Doimo M, Cassina M, Agosto C, Desbats MA, Sartori G, Sacconi S, Memo L, Zuffardi O, Artuch R, Quinzii C, Dimauro S, Hirano M, Santos-Ocaña C, Navas P. Haploinsufficiency of COQ4 causes coenzyme Q10 deficiency.. J Med Genet 2012 Mar;49(3):187-91.
    doi: 10.1136/jmedgenet-2011-100394pmc: PMC3983946pubmed: 22368301google scholar: lookup
  50. Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses.. Nat Rev Genet 2012 Mar 13;13(4):227-32.
    doi: 10.1038/nrg3185pmc: PMC3654667pubmed: 22411467google scholar: lookup
  51. de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C. Global signatures of protein and mRNA expression levels.. Mol Biosyst 2009 Dec;5(12):1512-26.
    doi: 10.1039/b908315dpmc: PMC4089977pubmed: 20023718google scholar: lookup
  52. Maier T, Güell M, Serrano L. Correlation of mRNA and protein in complex biological samples.. FEBS Lett 2009 Dec 17;583(24):3966-73.
    doi: 10.1016/j.febslet.2009.10.036pubmed: 19850042google scholar: lookup
  53. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. Global quantification of mammalian gene expression control.. Nature 2011 May 19;473(7347):337-42.
    doi: 10.1038/nature10098pubmed: 21593866google scholar: lookup
  54. Vogel C, Abreu Rde S, Ko D, Le SY, Shapiro BA, Burns SC, Sandhu D, Boutz DR, Marcotte EM, Penalva LO. Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line.. Mol Syst Biol 2010 Aug 24;6:400.
    pmc: PMC2947365pubmed: 20739923doi: 10.1038/msb.2010.59google scholar: lookup
  55. Vinogradov AD, King TE. The Keilin-Hartree heart muscle preparation.. Methods Enzymol 1979;55:118-27.
    pubmed: 156830doi: 10.1016/0076-6879(79)55017-4google scholar: lookup
  56. Capaldi RA. Arrangement of proteins in the mitochondrial inner membrane.. Biochim Biophys Acta 1982 Nov 30;694(3):291-306.
    pubmed: 6295486doi: 10.1016/0304-4157(82)90009-0google scholar: lookup
  57. Slater EC. The mechanism of the conservation of energy of biological oxidations.. Eur J Biochem 1987 Aug 3;166(3):489-504.
    pubmed: 3038543doi: 10.1111/j.1432-1033.1987.tb13542.xgoogle scholar: lookup
  58. Davey GP, Clark JB. Threshold effects and control of oxidative phosphorylation in nonsynaptic rat brain mitochondria.. J Neurochem 1996 Apr;66(4):1617-24.
    pubmed: 8627318doi: 10.1046/j.1471-4159.1996.66041617.xgoogle scholar: lookup
  59. Farge G, Touraille S, Debise R, Alziari S. The respiratory chain complex thresholds in mitochondria of a Drosophila subobscura mutant strain.. Biochimie 2002 Dec;84(12):1189-97.
    pubmed: 12628295doi: 10.1016/s0300-9084(02)00038-xgoogle scholar: lookup
  60. Rossignol R, Faustin B, Rocher C, Malgat M, Mazat JP, Letellier T. Mitochondrial threshold effects.. Biochem J 2003 Mar 15;370(Pt 3):751-62.
    pmc: PMC1223225pubmed: 12467494doi: 10.1042/bj20021594google scholar: lookup
  61. Li C, White SH, Warren LK, Wohlgemuth SE. Effects of aging on mitochondrial function in skeletal muscle of American American Quarter Horses.. J Appl Physiol (1985) 2016 Jul 1;121(1):299-311.
    doi: 10.1152/japplphysiol.01077.2015pmc: PMC5040552pubmed: 27283918google scholar: lookup
  62. Bergamini C, Moruzzi N, Sblendido A, Lenaz G, Fato R. A water soluble CoQ10 formulation improves intracellular distribution and promotes mitochondrial respiration in cultured cells.. PLoS One 2012;7(3):e33712.
    doi: 10.1371/journal.pone.0033712pmc: PMC3303850pubmed: 22432044google scholar: lookup
  63. Bhagavan HN, Chopra RK. Plasma coenzyme Q10 response to oral ingestion of coenzyme Q10 formulations.. Mitochondrion 2007 Jun;7 Suppl:S78-88.
    doi: 10.1016/j.mito.2007.03.003pubmed: 17482886google scholar: lookup
  64. Gin P, Clarke CF. Genetic evidence for a multi-subunit complex in coenzyme Q biosynthesis in yeast and the role of the Coq1 hexaprenyl diphosphate synthase.. J Biol Chem 2005 Jan 28;280(4):2676-81.
    doi: 10.1074/jbc.M411527200pubmed: 15548532google scholar: lookup
  65. Johnson A, Gin P, Marbois BN, Hsieh EJ, Wu M, Barros MH, Clarke CF, Tzagoloff A. COQ9, a new gene required for the biosynthesis of coenzyme Q in Saccharomyces cerevisiae.. J Biol Chem 2005 Sep 9;280(36):31397-404.
    doi: 10.1074/jbc.M503277200pubmed: 16027161google scholar: lookup
  66. Desbats MA, Lunardi G, Doimo M, Trevisson E, Salviati L. Genetic bases and clinical manifestations of coenzyme Q10 (CoQ 10) deficiency.. J Inherit Metab Dis 2015 Jan;38(1):145-56.
    doi: 10.1007/s10545-014-9749-9pubmed: 25091424google scholar: lookup
  67. Trevisson E, DiMauro S, Navas P, Salviati L. Coenzyme Q deficiency in muscle.. Curr Opin Neurol 2011 Oct;24(5):449-56.
    doi: 10.1097/WCO.0b013e32834ab528pubmed: 21844807google scholar: lookup
  68. Quinzii CM, Kattah AG, Naini A, Akman HO, Mootha VK, DiMauro S, Hirano M. Coenzyme Q deficiency and cerebellar ataxia associated with an aprataxin mutation.. Neurology 2005 Feb 8;64(3):539-41.
    doi: 10.1212/01.WNL.0000150588.75281.58pubmed: 15699391google scholar: lookup
  69. Miles MV, Miles L, Tang PH, Horn PS, Steele PE, DeGrauw AJ, Wong BL, Bove KE. Systematic evaluation of muscle coenzyme Q10 content in children with mitochondrial respiratory chain enzyme deficiencies.. Mitochondrion 2008 Mar;8(2):170-80.
    doi: 10.1016/j.mito.2008.01.003pubmed: 18313367google scholar: lookup
  70. Sacconi S, Trevisson E, Salviati L, Aymé S, Rigal O, Redondo AG, Mancuso M, Siciliano G, Tonin P, Angelini C, Auré K, Lombès A, Desnuelle C. Coenzyme Q10 is frequently reduced in muscle of patients with mitochondrial myopathy.. Neuromuscul Disord 2010 Jan;20(1):44-8.
    doi: 10.1016/j.nmd.2009.10.014pubmed: 19945282google scholar: lookup
  71. Duncan AJ, Bitner-Glindzicz M, Meunier B, Costello H, Hargreaves IP, López LC, Hirano M, Quinzii CM, Sadowski MI, Hardy J, Singleton A, Clayton PT, Rahman S. A nonsense mutation in COQ9 causes autosomal-recessive neonatal-onset primary coenzyme Q10 deficiency: a potentially treatable form of mitochondrial disease.. Am J Hum Genet 2009 May;84(5):558-66.
    doi: 10.1016/j.ajhg.2009.03.018pmc: PMC2681001pubmed: 19375058google scholar: lookup
  72. Borekova M, Hojerova J, Koprda V, Bauerova K. Nourishing and health benefits of coenzyme Q10-a review.. Czech journal of food sciences 2008;26(4):229–41.
  73. Littarru GP, Tiano L. Clinical aspects of coenzyme Q10: an update.. Nutrition 2010 Mar;26(3):250-4.
    doi: 10.1016/j.nut.2009.08.008pubmed: 19932599google scholar: lookup
  74. Cooke M, Iosia M, Buford T, Shelmadine B, Hudson G, Kerksick C, Rasmussen C, Greenwood M, Leutholtz B, Willoughby D, Kreider R. Effects of acute and 14-day coenzyme Q10 supplementation on exercise performance in both trained and untrained individuals.. J Int Soc Sports Nutr 2008 Mar 4;5:8.
    pmc: PMC2315638pubmed: 18318910doi: 10.1186/1550-2783-5-8google scholar: lookup
  75. Kon M, Kimura F, Akimoto T, Tanabe K, Murase Y, Ikemune S, Kono I. Effect of Coenzyme Q10 supplementation on exercise-induced muscular injury of rats.. Exerc Immunol Rev 2007;13:76-88.
    pubmed: 18198662
  76. Kon M, Tanabe K, Akimoto T, Kimura F, Tanimura Y, Shimizu K, Okamoto T, Kono I. Reducing exercise-induced muscular injury in kendo athletes with supplementation of coenzyme Q10.. Br J Nutr 2008 Oct;100(4):903-9.
    pubmed: 18284711doi: 10.1017/s0007114508926544google scholar: lookup
  77. Mizuno K, Tanaka M, Nozaki S, Mizuma H, Ataka S, Tahara T, Sugino T, Shirai T, Kajimoto Y, Kuratsune H, Kajimoto O, Watanabe Y. Antifatigue effects of coenzyme Q10 during physical fatigue.. Nutrition 2008 Apr;24(4):293-9.
    doi: 10.1016/j.nut.2007.12.007pubmed: 18272335google scholar: lookup
  78. Linnane AW, Degli Esposti M, Generowicz M, Luff AR, Nagley P. The universality of bioenergetic disease and amelioration with redox therapy.. Biochim Biophys Acta 1995 May 24;1271(1):191-4.
    pubmed: 7599207doi: 10.1016/0925-4439(95)00027-2google scholar: lookup
  79. Linnane AW, Kopsidas G, Zhang C, Yarovaya N, Kovalenko S, Papakostopoulos P, Eastwood H, Graves S, Richardson M. Cellular redox activity of coenzyme Q10: effect of CoQ10 supplementation on human skeletal muscle.. Free Radic Res 2002 Apr;36(4):445-53.
    pubmed: 12069109doi: 10.1080/10715760290021306google scholar: lookup
  80. Morisco C, Trimarco B, Condorelli M. Effect of coenzyme Q10 therapy in patients with congestive heart failure: a long-term multicenter randomized study.. Clin Investig 1993;71(8 Suppl):S134-6.
    pubmed: 8241697doi: 10.1007/bf00226854google scholar: lookup
  81. Folkers K, Simonsen R. Two successful double-blind trials with coenzyme Q10 (vitamin Q10) on muscular dystrophies and neurogenic atrophies.. Biochim Biophys Acta 1995 May 24;1271(1):281-6.
    pubmed: 7599221doi: 10.1016/0925-4439(95)00040-bgoogle scholar: lookup
  82. Caso G, Kelly P, McNurlan MA, Lawson WE. Effect of coenzyme q10 on myopathic symptoms in patients treated with statins.. Am J Cardiol 2007 May 15;99(10):1409-12.
    doi: 10.1016/j.amjcard.2006.12.063pubmed: 17493470google scholar: lookup
  83. Spurney CF, Rocha CT, Henricson E, Florence J, Mayhew J, Gorni K, Pasquali L, Pestronk A, Martin GR, Hu F, Nie L, Connolly AM, Escolar DM. CINRG pilot trial of coenzyme Q10 in steroid-treated Duchenne muscular dystrophy.. Muscle Nerve 2011 Aug;44(2):174-8.
    pmc: PMC3136634pubmed: 21698649doi: 10.1002/mus.22047google scholar: lookup
  84. Bonetti A, Solito F, Carmosino G, Bargossi AM, Fiorella PL. Effect of ubidecarenone oral treatment on aerobic power in middle-aged trained subjects.. J Sports Med Phys Fitness 2000 Mar;40(1):51-7.
    pubmed: 10822909
  85. Braun B, Clarkson PM, Freedson PS, Kohl RL. Effects of coenzyme Q10 supplementation on exercise performance, VO2max, and lipid peroxidation in trained cyclists.. Int J Sport Nutr 1991 Dec;1(4):353-65.
    pubmed: 1844568doi: 10.1123/ijsn.1.4.353google scholar: lookup
  86. Snider IP, Bazzarre TL, Murdoch SD, Goldfarb A. Effects of coenzyme athletic performance system as an ergogenic aid on endurance performance to exhaustion.. Int J Sport Nutr 1992 Sep;2(3):272-86.
    pubmed: 1338584doi: 10.1123/ijsn.2.3.272google scholar: lookup
  87. Sinatra ST, Chopra RK, Jankowitz S, Horohov DW, Bhagavan HN. Coenzyme Q10 in equine serum: response to supplementation.. Journal of Equine Veterinary Science 2013;33(2):71–3.
  88. Sinatra ST, Jankowitz SN, Chopra RK, Bhagavan HN. Plasma coenzyme Q10 and tocopherols in thoroughbred race horses: Effect of coenzyme Q10 supplementation and exercise.. Journal of Equine Veterinary Science 2013;34(2):265–9.
  89. Horohov DW, Sinatra ST, Chopra RK, Jankowitz S, Betancourt A, Bloomer RJ. The effect of exercise and nutritional supplementation on proinflammatory cytokine expression in young racehorses during training.. Journal of Equine Veterinary Science 2012;32(12):805–15.
  90. Rooney MF, Hill EW, Katz LM, Porter RK. MSTN genotype variation affects skeletal muscle mitochondrial abundance and fibre composition in untrained Thoroughbred horses.. Biochimica et Biophysica Acta (BBA)—Bioenergetics 2016;1857, Supplement:e31n.
    doi: 10.1016/j.bbabio.2016.04.064google scholar: lookup

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