Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Mitochondrial metabolism: a driver of energy utilisation and product quality?

N. J. Hudson A E , W. G. Bottje B , R. J. Hawken C , ByungWhi Kong B , R. Okimoto C and A. Reverter D
+ Author Affiliations
- Author Affiliations

A The University of Queensland, School of Agriculture and Food Sciences, Gatton, Qld 4343, Australia.

B University of Arkansas, Fayetteville, Arkansas, AR 72701, USA.

C Cobb Vantress Inc., Siloam Springs, Arkansas, AR 72761, USA.

D Commonwealth Scientific and Industrial Research Organisation, Queensland Bioscience Precinct, 306 Carmody Road, St Lucia, Brisbane, Qld 4072, Australia.

E Corresponding author. Email: n.hudson@uq.edu.au

Animal Production Science 57(11) 2204-2215 https://doi.org/10.1071/AN17322
Submitted: 15 May 2017  Accepted: 20 July 2017   Published: 23 August 2017

Abstract

High feed efficiency is a very desirable production trait as it positively influences resource utilisation, profitability and environmental considerations, albeit at the possible expense of product quality. The modern broiler is arguably the most illustrative model species as it has been transformed over the past half century into an elite feed converter. Some producers are currently reporting that 42-day-old birds gain 1 kg of wet weight for every 1.35 kg of dry weight consumed. Its large breast muscle is exclusively composed of large, low mitochondrial-content Type IIB fibres, which may contribute to low maintenance costs and high efficiency. In an effort to gain a better understanding of individual variation in chicken feed efficiency, our group has been exploring the biology of the mitochondrion at multiple levels of organisation. The mitochondrion is the organelle where much biochemical energy transformation occurs in the cell. Using Cobb-Vantress industrial birds as our primary experimental resource, we have explored the tissue content, structure and function of the mitochondrion and its relationship to growth, development, efficiency and genetic background. While much remains to be understood, recent highlights include (1) variation in muscle mitochondrial content that is associated with performance phenotypes, (2) altered muscle mitochondrial gene and protein expression in birds differing in feed efficiency, (3) variation in isolated mitochondrial function in birds differing in feed efficiency and (4) evidence for an unexpected role for the mitochondrially localised progesterone receptor in altering bird muscle metabolism. Mitochondrial function is largely conserved across the vertebrates, so the same metabolic principles appear to apply to the major production species, whether monogastric or ruminant. A speculative role for the mitochondria in aspects of meat quality and in influencing postmortem anaerobic metabolism will conclude the manuscript.

Additional keywords: feed efficiency, muscle.


References

Askew GN, Marsh RL (2002) Muscle designed for maximum short-term power output: quail flight muscle. The Journal of Experimental Biology 205, 2153–2160.

Bottje W, Kong BW, Reverter A, Waardenberg AJ, Lassiter K, Hudson NJ (2017) Progesterone signalling in broiler skeletal muscle is associated with divergent feed efficiency. BMC Systems Biology 11, 29
Progesterone signalling in broiler skeletal muscle is associated with divergent feed efficiency.CrossRef |

Bouley J, Meunier B, Chambon C, De Smet S, Hocquette JF, Picard B (2005) Proteomic analysis of bovine skeletal muscle hypertrophy. Proteomics 5, 490–500.
Proteomic analysis of bovine skeletal muscle hypertrophy.CrossRef | 1:CAS:528:DC%2BD2MXhs1Oitbk%3D&md5=ca9b7ae2a9cedd7d93ea07a3941540beCAS |

Brand MD, Chien LF, Ainscow EK, Rolfe DF, Porter RK (1994) The causes and functions of mitochondrial proton leak. Biochimica et Biophysica Acta 1187, 132–139.
The causes and functions of mitochondrial proton leak.CrossRef | 1:CAS:528:DyaK2cXmslCmsb0%3D&md5=186b38c77652ee1b230de4ca6bad714cCAS |

Brand MD, Brindle KM, Buckingham JA, Harper JA, Rolfe DF, Stuart JA (1999) The significance and mechanism of mitochondrial proton conductance. International Journal of Obesity and Related Metabolic Disorders 23, S4–S11.
The significance and mechanism of mitochondrial proton conductance.CrossRef | 1:CAS:528:DyaK1MXltFOktLs%3D&md5=a40e962778cc532b0d7873e961916e52CAS |

Bruton JD, Aydin J, Yamada T, Shabalina IG, Ivarsson N, Zhang SJ, Wada M, Tavi P, Nedergaard J, Katz A, Westerblad H (2010) Increased fatigue resistance linked to Ca2+-stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice. The Journal of Physiology 588, 4275–4288.
Increased fatigue resistance linked to Ca2+-stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice.CrossRef | 1:CAS:528:DC%2BC3cXhsVKlur7E&md5=c8fdbf050cf5382a1fd24768f37b435aCAS |

Burrin DG, Ferrell CL, Britton RA, Bauer M (1990) Level of nutrition and visceral organ size and metabolic activity in sheep. British Journal of Nutrition 64, 439–448.
Level of nutrition and visceral organ size and metabolic activity in sheep.CrossRef | 1:STN:280:DyaK3M%2FislOjtw%3D%3D&md5=0bb8170e6db05cbb999e87279de6f394CAS |

Conley KE (2016) Mitochondria to motion: optimizing oxidative phosphorylation to improve exercise performance. The Journal of Experimental Biology 219, 243–249.
Mitochondria to motion: optimizing oxidative phosphorylation to improve exercise performance.CrossRef |

Deveaux V, Cassar-Malek I, Picard B (2001) Comparison of contractile characteristics of muscle from Holstein and double-muscled Belgian Blue foetuses. Comparative Biochemistry and Physiology. A. Comparative Physiology 131, 21–29.
Comparison of contractile characteristics of muscle from Holstein and double-muscled Belgian Blue foetuses.CrossRef | 1:STN:280:DC%2BD3MnoslSrsQ%3D%3D&md5=9fb96ecc41a23ce278d88dd310d65a70CAS |

Devine CE, Ellery S, Averill S (1984) Responses of different types of ox muscle to electrical stimulation. Meat Science 10, 35–51.
Responses of different types of ox muscle to electrical stimulation.CrossRef | 1:STN:280:DC%2BC3MbmvFChsA%3D%3D&md5=2e9a1fdd4eaa01a00057180b7785522aCAS |

Diamond J, Hammond K (1992) The matches, achieved by natural selection, between biological capacities and their natural loads. Experientia 48, 551–557.
The matches, achieved by natural selection, between biological capacities and their natural loads.CrossRef | 1:STN:280:DyaK38zgslSmug%3D%3D&md5=7b369138d1314db9b1d680747b6fbc39CAS |

England EM, Matarneh SK, Oliver EM, Apaoblaza A, Scheffler TL, Shi H, Gerrard DE (2016) Excess glycogen does not resolve high ultimate pH of oxidative muscle. Meat Science 114, 95–102.
Excess glycogen does not resolve high ultimate pH of oxidative muscle.CrossRef | 1:CAS:528:DC%2BC28Xis1yhsw%3D%3D&md5=c2228d138a119b9e3d8baf2560d5163fCAS |

Essén-Gustavsson B, Lindholm A (1984) Fiber types and metabolic characteristics in muscles of wild boars, normal and halothane sensitive Swedish landrace pigs. Comparative Biochemistry and Physiology. A. Comparative Physiology 78, 67–71.
Fiber types and metabolic characteristics in muscles of wild boars, normal and halothane sensitive Swedish landrace pigs.CrossRef |

Farrar RP, Mayer LR, Starnes JW, Edington DW (1981) Selected biochemical parameters of two sizes of rat skeletal and heart muscle mitochondria at selected intervals of a 16-week endurance training program. European Journal of Applied Physiology and Occupational Physiology 46, 91–102.
Selected biochemical parameters of two sizes of rat skeletal and heart muscle mitochondria at selected intervals of a 16-week endurance training program.CrossRef | 1:CAS:528:DyaL3MXktVCntr4%3D&md5=d2cc5c343094af02d447d042a72cdc6bCAS |

Fiems LO (2012) Double muscling in cattle: genes, husbandry, carcasses and meat. Animals 2, 472–506.
Double muscling in cattle: genes, husbandry, carcasses and meat.CrossRef |

Fu L, Xu Y, Hou Y, Qi X, Zhou L, Liu H, Luan Y, Jing L, Miao Y, Zhao S, Liu H, Li X (2017) Proteomic analysis indicates that mitochondrial energy metabolism in skeletal muscle tissue is negatively correlated with feed efficiency in pigs. Scientific Reports 7, 45291
Proteomic analysis indicates that mitochondrial energy metabolism in skeletal muscle tissue is negatively correlated with feed efficiency in pigs.CrossRef | 1:CAS:528:DC%2BC2sXltlKltb8%3D&md5=ebe219006829fee85830e4ff3ff9cef2CAS |

Henriksson J (1990) The possible role of skeletal muscle in the adaptation to periods of energy deficiency. European Journal of Clinical Nutrition 44, 55–64.

Herd RM, Arthur PF (2009) Physiological basis for residual feed intake. Journal of Animal Science 87, E64–E71.
Physiological basis for residual feed intake.CrossRef | 1:STN:280:DC%2BD1M3mtVWksA%3D%3D&md5=5a063ac0eade9a09c522299df5fe5899CAS |

Hoagland M, Dodson B, Hauck J (2001) ‘Exploring the way life works: the science of biology.’ (Jones and Bartlett Publishers: Canada)

Holloszy JO (1982) Muscle metabolism during exercise. Archives of Physical Medicine and Rehabilitation 63, 231–234.

Hudson NJ (2009) Symmorphosis and livestock bioenergetics: production animal muscle has low mitochondrial volume fractions. Journal of Animal Physiology and Animal Nutrition 93, 1–6.
Symmorphosis and livestock bioenergetics: production animal muscle has low mitochondrial volume fractions.CrossRef | 1:STN:280:DC%2BD1M3psFagtw%3D%3D&md5=a5bcb3be8784898cf5b3aba6e977b952CAS |

Hudson NJ (2012) Mitochondrial treason: a novel driver of pH decline in postmortem muscle? Animal Production Science 52, 1107–1110.
Mitochondrial treason: a novel driver of pH decline in postmortem muscle?CrossRef | 1:CAS:528:DC%2BC38Xhs1Wju7zK&md5=277374041b6edfd3f7aa2e7110422720CAS |

Hudson NJ, Lehnert SA, Harper GS (2008) Obese humans as economically designed feed converters: symmorphosis and low oxidative capacity skeletal muscle. Medical Hypotheses 70, 693–697.
Obese humans as economically designed feed converters: symmorphosis and low oxidative capacity skeletal muscle.CrossRef | 1:CAS:528:DC%2BD1cXhslartb8%3D&md5=1960764c9441cc4a16e4aef350844b93CAS |

Hudson NJ, Lyons RE, Reverter A, Greenwood PL, Dalrymple BP (2013) Inferring the in vivo cellular program of developing bovine skeletal muscle from expression data. Gene Expression Patterns 13, 109–125.
Inferring the in vivo cellular program of developing bovine skeletal muscle from expression data.CrossRef | 1:CAS:528:DC%2BC3sXksFOgsbw%3D&md5=aec7abfd13d8ef76256f3de039175e30CAS |

Hudson NJ, Hawken RJ, Okimoto R, Sapp RL, Reverter A (2017) Data compression can discriminate broilers by selection line, detect haplotypes, and estimate genetic potential for complex phenotypes. Poultry Science
Data compression can discriminate broilers by selection line, detect haplotypes, and estimate genetic potential for complex phenotypes.CrossRef |

Iqbal M, Pumford NR, Tang ZX, Lassiter K, Wing T, Cooper M, Bottje W (2004) Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity. Poultry Science 83, 474–484.
Low feed efficient broilers within a single genetic line exhibit higher oxidative stress and protein expression in breast muscle with lower mitochondrial complex activity.CrossRef | 1:STN:280:DC%2BD2c7ls1agtw%3D%3D&md5=ad298b0d9bade540e71e1afdd470d2c3CAS |

Jackson SP, Green RD, Miller MF (1997) Phenotypic characterization of rambouillet sheep expressing the callipyge gene: I. Inheritance of the condition and production characteristics. Journal of Animal Science 75, 14–18.
Phenotypic characterization of rambouillet sheep expressing the callipyge gene: I. Inheritance of the condition and production characteristics.CrossRef | 1:CAS:528:DyaK2sXhtVGgu70%3D&md5=36af0ed722932ae42b7c6a81886033a1CAS |

Jain SS, Paglialunga S, Vigna C, Ludzki A, Herbst EA, Lally JS, Schrauwen P, Hoeks J, Tupling AR, Bonen A, Holloway GP (2014) High-fat diet-induced mitochondrial biogenesis is regulated by mitochondrial-derived reactive oxygen species activation of CaMKII. Diabetes 63, 1907–1913.
High-fat diet-induced mitochondrial biogenesis is regulated by mitochondrial-derived reactive oxygen species activation of CaMKII.CrossRef | 1:CAS:528:DC%2BC2cXhsV2ls7%2FF&md5=dba390dfb3d0682938a22070ffd01f15CAS |

Johnston IA, Fernandez DA, Calvo J, Vieira VL, North AW, Abercromby M, Garland T (2003) Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective. The Journal of Experimental Biology 206, 2595–2609.
Reduction in muscle fibre number during the adaptive radiation of notothenioid fishes: a phylogenetic perspective.CrossRef |

Jones AM (2014) Influence of dietary nitrate on the physiological determinants of exercise performance: a critical review. Applied Physiology, Nutrition, and Metabolism 39, 1019–1028.
Influence of dietary nitrate on the physiological determinants of exercise performance: a critical review.CrossRef | 1:CAS:528:DC%2BC2cXht1agsL3P&md5=14f64514a93acc718d3111a9f4fe8593CAS |

Jorgensen PL, Pedersen PA (2001) Structure-function relationships of Na(+), K(+), ATP, or Mg(2+) binding and energy transduction in Na,K-ATPase. Biochimica et Biophysica Acta 1505, 57–74.
Structure-function relationships of Na(+), K(+), ATP, or Mg(2+) binding and energy transduction in Na,K-ATPase.CrossRef | 1:CAS:528:DC%2BD3MXhvVagsbY%3D&md5=fa56566e96803c661af577ecd716099fCAS |

Kiessling KH (1977) Muscle structure and function in the goose, quail, pheasant, guinea hen, and chicken. Comparative Biochemistry and Physiology 57, 287–292.

Kong BW, Lassiter K, Piekarski-Welsher A, Dridi S, Reverter-Gomez A, Hudson NJ, Bottje WG (2016a) Proteomics of breast muscle tissue associated with the phenotypic expression of feed efficiency within a pedigree male broiler line: I. Highlight on mitochondria. PLoS One 11, e0155679
Proteomics of breast muscle tissue associated with the phenotypic expression of feed efficiency within a pedigree male broiler line: I. Highlight on mitochondria.CrossRef |

Kong RS, Liang G, Chen Y, Stothard P, Guan LL (2016b) Transcriptome profiling of the rumen epithelium of beef cattle differing in residual feed intake. BMC Genomics 17, 592
Transcriptome profiling of the rumen epithelium of beef cattle differing in residual feed intake.CrossRef |

Krauss S, Zhang CY, Lowell BB (2005) The mitochondrial uncoupling-protein homologues. Nature Reviews. Molecular Cell Biology 6, 248–261.
The mitochondrial uncoupling-protein homologues.CrossRef | 1:CAS:528:DC%2BD2MXhslSlsLk%3D&md5=982e4f5f92e2582f4d2de9534e430abaCAS |

Kuttappan VA, Brewer VB, Apple JK, Waldroup PW, Owens CM (2012) Influence of growth rate on the occurrence of white striping in broiler breast fillets. Poultry Science 91, 2677–2685.
Influence of growth rate on the occurrence of white striping in broiler breast fillets.CrossRef | 1:CAS:528:DC%2BC38Xhs1Wns7jM&md5=56e2be01ddd52d298b0430f78a9e10dcCAS |

Lefaucheur L, Milan D, Ecolan P, Le Callennec C (2004) Myosin heavy chain composition of different skeletal muscles in Large White and Meishan pigs. Journal of Animal Science 82, 1931–1941.
Myosin heavy chain composition of different skeletal muscles in Large White and Meishan pigs.CrossRef | 1:CAS:528:DC%2BD2cXlsFWksro%3D&md5=7231a9e39f76bd6fe58569d6b10d763bCAS |

Lefaucheur L, Lebret B, Ecolan P, Louveau I, Damon M, Prunier A, Billon Y, Sellier P, Gilbert H (2011) Muscle characteristics and meat quality traits are affected by divergent selection on residual feed intake in pigs. Journal of Animal Science 89, 996–1010.
Muscle characteristics and meat quality traits are affected by divergent selection on residual feed intake in pigs.CrossRef | 1:CAS:528:DC%2BC3MXntFKlt78%3D&md5=3a54e508fb3d162cc8eec06273de1eb8CAS |

Lehnert SA, Reverter A, Byrne KA, Wang Y, Nattrass GS, Hudson NJ, Greenwood PL (2007) Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Developmental Biology 7, 95
Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds.CrossRef |

Liu S, Wang SZ, Li ZH, Li H (2007) Association of single nucleotide polymorphism of chicken uncoupling protein gene with muscle and fatness traits. Journal of Animal Breeding and Genetics 124, 230–235.
Association of single nucleotide polymorphism of chicken uncoupling protein gene with muscle and fatness traits.CrossRef | 1:CAS:528:DC%2BD2sXhtVent7%2FP&md5=1a1f748068ad5b8b554f91aa9ca8c016CAS |

Mathieu O, Krauer R, Hoppeler H, Gehr P, Lindstedt SL, Alexander RM, Taylor CR, Weibel ER (1981) Design of the mammalian respiratory system. VII. Scaling mitochondrial volume in skeletal muscle to body mass. Respiration Physiology 44, 113–128.
Design of the mammalian respiratory system. VII. Scaling mitochondrial volume in skeletal muscle to body mass.CrossRef | 1:STN:280:DyaL3M3gtVGgsg%3D%3D&md5=3c71c3365cf60896a6d5a9f1e3befa64CAS |

Mathieu-Costello O, Suarez RK, Hochachka PW (1992) Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle. Respiration Physiology 89, 113–132.
Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle.CrossRef | 1:STN:280:DyaK38zptVKitA%3D%3D&md5=14dcaddb693559416e1d6a6fa3bc79f3CAS |

Mitchell P (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191, 144–148.
Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism.CrossRef | 1:CAS:528:DyaF38XjtlarsA%3D%3D&md5=289e49a66ec9b9a5c0e426a227cb01d9CAS |

Monin G, Mejenes-Quijano A, Talmant A, Sellier P (1987) Influence of breed and muscle metabolic type on muscle glycolytic potential and meat pH in pigs. Meat Science 20, 149–158.
Influence of breed and muscle metabolic type on muscle glycolytic potential and meat pH in pigs.CrossRef | 1:STN:280:DC%2BC3MbmvFGitg%3D%3D&md5=6d311f76e5ac059ee70c6928a2750895CAS |

Nagy KA (2005) Field metabolic rate and body size. The Journal of Experimental Biology 208, 1621–1625.
Field metabolic rate and body size.CrossRef |

Nicholls DG, Bernson VS, Heaton GM (1978) The identification of the component in the inner membrane of brown adipose tissue mitochondria responsible for regulating energy dissipation. Experientia. Supplementum 32, 89–93.
The identification of the component in the inner membrane of brown adipose tissue mitochondria responsible for regulating energy dissipation.CrossRef | 1:STN:280:DyaE1c7mvFWktw%3D%3D&md5=752b76c93497d8002744a72860c7b247CAS |

Rea SL, Graham BH, Nakamaru-Ogiso E, Kar A, Falk MJ (2010) Bacteria, yeast, worms, and flies: exploiting simple model organisms to investigate human mitochondrial diseases. Developmental Disabilities Research Reviews 16, 200–218.
Bacteria, yeast, worms, and flies: exploiting simple model organisms to investigate human mitochondrial diseases.CrossRef |

Rehfeldt C, Henning M, Fiedler I (2008) Consequences of pig domestication for skeletal muscle growth and cellularity. Livestock Science 116, 30–41.
Consequences of pig domestication for skeletal muscle growth and cellularity.CrossRef |

Rekaya R, Sapp RL, Wing T, Aggrey SE (2013) Genetic evaluation for growth, body composition, feed efficiency, and leg soundness. Poultry Science 92, 923–929.
Genetic evaluation for growth, body composition, feed efficiency, and leg soundness.CrossRef | 1:STN:280:DC%2BC3svksVeqtw%3D%3D&md5=7516f0e3bc4237686a2bdaaa423659efCAS |

Reverter A, Okimoto R, Sapp R, Bottje WG, Hawken R, Hudson NJ (2017) Chicken muscle mitochondrial content appears co-ordinately regulated and is associated with performance phenotypes. Biology Open 6, 50–58.
Chicken muscle mitochondrial content appears co-ordinately regulated and is associated with performance phenotypes.CrossRef |

Reyer H, Hawken R, Murani E, Ponsuksili S, Wimmers K (2015) The genetics of feed conversion efficiency traits in a commercial broiler line. Scientific Reports 5, 16387
The genetics of feed conversion efficiency traits in a commercial broiler line.CrossRef | 1:CAS:528:DC%2BC2MXhvVWmsLbJ&md5=6a15fc4da03d30b3c2d23c0827e45dc3CAS |

Rucker R, Chowanadisai W, Nakano M (2009) Potential physiological importance of pyrroloquinoline quinone. Alternative Medicine Review 14, 268–277.

Scheffler TL, Park S, Gerrard DE (2011) Lessons to learn about postmortem metabolism using the AMPKgamma3(R200Q) mutation in the pig. Meat Science 89, 244–250.
Lessons to learn about postmortem metabolism using the AMPKgamma3(R200Q) mutation in the pig.CrossRef | 1:CAS:528:DC%2BC3MXptlagtLc%3D&md5=efefba92164cd6fd2026f381d7f89c35CAS |

Scheffler TL, Matarneh SK, England EM, Gerrard DE (2015) Mitochondria influence postmortem metabolism and pH in an in vitro model. Meat Science 110, 118–125.
Mitochondria influence postmortem metabolism and pH in an in vitro model.CrossRef | 1:CAS:528:DC%2BC2MXht1Gru7vJ&md5=30943ee9076106e0edc7563763e083efCAS |

Shabalina IG, Hoeks J, Kramarova TV, Schrauwen P, Cannon B, Nedergaard J (2010) Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochimica et Biophysica Acta 1797, 968–980.
Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects.CrossRef | 1:CAS:528:DC%2BC3cXnvV2qtrY%3D&md5=1d5cc1c8c9ebe9e67a41b8c747d60c89CAS |

Sharma P, Bottje W, Okimoto R (2008) Polymorphisms in uncoupling protein, melanocortin 3 receptor, melanocortin 4 receptor, and pro-opiomelanocortin genes and association with production traits in a commercial broiler line. Poultry Science 87, 2073–2086.
Polymorphisms in uncoupling protein, melanocortin 3 receptor, melanocortin 4 receptor, and pro-opiomelanocortin genes and association with production traits in a commercial broiler line.CrossRef | 1:STN:280:DC%2BD1cnitVKhtA%3D%3D&md5=e698f0ad3d4476e6379047d9de159294CAS |

Siegel MP, Kruse SE, Percival JM, Goh J, White CC, Hopkins HC, Kavanagh TJ, Szeto HH, Rabinovitch PS, Marcinek DJ (2013) Mitochondrial-targeted peptide rapidly improves mitochondrial energetics and skeletal muscle performance in aged mice. Aging Cell 12, 763–771.
Mitochondrial-targeted peptide rapidly improves mitochondrial energetics and skeletal muscle performance in aged mice.CrossRef | 1:CAS:528:DC%2BC3sXhsVektrvK&md5=01d49bd8552a35890a0d837b8e32558aCAS |

Srivastava S, Kashiwaya Y, King MT, Baxa U, Tam J, Niu G, Chen X, Clarke K, Veech RL (2012) Mitochondrial biogenesis and increased uncoupling protein 1 in brown adipose tissue of mice fed a ketone ester diet. The FASEB Journal 26, 2351–2362.
Mitochondrial biogenesis and increased uncoupling protein 1 in brown adipose tissue of mice fed a ketone ester diet.CrossRef | 1:CAS:528:DC%2BC38XpslSmsrw%3D&md5=e68f876baf78f9bfa243283513754a42CAS |

St-Pierre J, Brand MD, Boutilier RG (2000) Mitochondria as ATP consumers: cellular treason in anoxia. Proceedings of the National Academy of Sciences, USA 97, 8670–8674.
Mitochondria as ATP consumers: cellular treason in anoxia.CrossRef | 1:CAS:528:DC%2BD3cXlt1GnsLY%3D&md5=def0f991d01222c6f6bb77dcf9b74349CAS |

Szarski H (1983) Cell size and the concept of wasteful and frugal evolutionary strategies. Journal of Theoretical Biology 105, 201–209.
Cell size and the concept of wasteful and frugal evolutionary strategies.CrossRef | 1:STN:280:DyaL2c%2FptFKktA%3D%3D&md5=77129b502d0bb112d1aa44e58c65eeb7CAS |

Tornroth-Horsefield S, Neutze R (2008) Opening and closing the metabolite gate. Proceedings of the National Academy of Sciences, USA 105, 19565–19566.
Opening and closing the metabolite gate.CrossRef |

van den Broek NM, Ciapaite J, De Feyter HM, Houten SM, Wanders RJ, Jeneson JA, Nicolay K, Prompers JJ (2010) Increased mitochondrial content rescues in vivo muscle oxidative capacity in long-term high-fat-diet-fed rats. The FASEB Journal 24, 1354–1364.
Increased mitochondrial content rescues in vivo muscle oxidative capacity in long-term high-fat-diet-fed rats.CrossRef | 1:CAS:528:DC%2BC3cXlslSiu70%3D&md5=7f746930dfab8e1b64ab9e5f754c8a9cCAS |

Wang S, Wang X, Ye Z, Xu C, Zhang M, Ruan B, Wei M, Jiang Y, Zhang Y, Wang L, Lei X, Lu Z (2015) Curcumin promotes browning of white adipose tissue in a norepinephrine-dependent way. Biochemical and Biophysical Research Communications 466, 247–253.
Curcumin promotes browning of white adipose tissue in a norepinephrine-dependent way.CrossRef | 1:CAS:528:DC%2BC2MXhsFSitbvN&md5=8d4b6964792bd106e0312e114aef5512CAS |

Weibel ER, Taylor CR, Bolis L (1998) ‘Muscle energy balance in sound production and flight.’ (Cambridge University Press)

Weibel ER, Taylor CR, Hoppeler H (1991) The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proceedings of the National Academy of Sciences, USA 88, 10357–10361.
The concept of symmorphosis: a testable hypothesis of structure-function relationship.CrossRef | 1:STN:280:DyaK38%2Flt1aluw%3D%3D&md5=a3a7f2c11d2ba265cdb63f35704a4ba0CAS |

White CR, Seymour RS (2003) Mammalian basal metabolic rate is proportional to body mass2/3. Proceedings of the National Academy of Sciences, USA 100, 4046–4049.
Mammalian basal metabolic rate is proportional to body mass2/3.CrossRef | 1:CAS:528:DC%2BD3sXivFSqurk%3D&md5=f4d055e833b038b87653ae1a5a747b23CAS |

Williams TM, Dobson GP, Mathieu-Costello O, Morsbach D, Worley MB, Phillips JA (1997) Skeletal muscle histology and biochemistry of an elite sprinter, the African cheetah. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 167, 527–535.
Skeletal muscle histology and biochemistry of an elite sprinter, the African cheetah.CrossRef | 1:CAS:528:DyaK2sXnslynt7k%3D&md5=e3ad2b6dd897710037b5d3ee34e7ded3CAS |

Young A (1997) Ageing and physiological functions. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 352, 1837–1843.
Ageing and physiological functions.CrossRef | 1:STN:280:DyaK1c7itFeksg%3D%3D&md5=dc920f5853c7f5fa1f2e94e96ee676d0CAS |



Rent Article (via Deepdyve) Export Citation