Origins of interspecies variation in mammalian muscle metabolic enzymes

Physiological Genomics

Volumn 43, Issue 14, 2011, Pages 873-883

  Kocha, K M ^a   Genge, C E ^a   Moyes, C D ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Coactivator 1 ; Cytochrome c oxidase; Lactate dehydrogenase; Mitochondria; Nuclear respiratory factor 1; Peroxisome proliferator activated receptor ; Scaling

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 4 1; MESSENGER RNA; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CASTOR CANADENIS; CAVIA PORCELLUS; CHIPMUNK; DNA SEQUENCE; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; MAMMAL; MARMOTA MONAX; MERIONES UNGUICALATUS; MOUSE; MUSCLE METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROMYSCUS; PHODOPUS; PRIORITY JOURNAL; PROMOTER REGION; RAT; RODENT; SCURIUS CAROLINENSIS; SOLEUS MUSCLE; SPECIES; SYRIAN HAMSTER; TAMIASCIURUS HUDSONICUS; TIBIALIS ANTERIOR MUSCLE; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; BIOCATALYSIS; CELL LINE; DNA; ENZYMES; GENE EXPRESSION REGULATION; HUMANS; MAMMALS; MICE; MOLECULAR SEQUENCE DATA; MULTIVARIATE ANALYSIS; MUSCLE, SKELETAL; PROMOTER REGIONS, GENETIC; RNA; RNA, MESSENGER; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

MAMMALIA; RODENTIA;

EID: 79961005320     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00025.2011     Document Type: Article

References (46)

1. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB, Williams RS, Yan Z. Exercise stimulates PGC-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593, 2005.
2. Amat R, Planavila A, Chen S, Iglesias R, Giralt M, Villarroya F. SIRT1 controls the transcription of the peroxisome proliferator-activated receptor-gamma co-activator-1α (PGC-1α) gene in skeletal muscle through the PGC-1α autoregulatory loop and interaction with MyoD. J Biol Chem 284: 21872-21880, 2009.
3. Baar K, Wende A, Jones T, Marison M, Nolte L, Chen M, Kelly D, Holloszy J. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J 16: 1879-1886, 2002.
4. Burness GP, Leary SC, Hochachka PW, Moyes CD. Allometric scaling of RNA, DNA, and enzyme levels: an intraspecific study. Am J Physiol Regul Integr Comp Physiol 277: R1164-R1170, 1999.
5. Buroker N, Ning X, Portman M. Cardiac PPARα protein expression is constant as alternate nuclear receptors and PGC-1 coordinately increase during the postnatal metabolic transition. PPAR Res 2008: 279531, 2008.
6. Cao W, Daniel K, Robidoux J, Puigserver P, Medvedev A, Bai X, Floering L, Spiegelman B, Collins S. p38 mitogen-activated protein kinase is the central regulator of cyclic amp-dependent transcription of the brown fat uncoupling protein 1 gene. Microbiology 24: 3057-3067, 2004.
7. Daitoku H, Yamagata K, Matsuzaki H, Hatta M, Fukamizu A. Regulation of PGC-1 promoter activity by protein kinase B and the forkhead transcription factor FKHR. Diabetes 52: 642-649, 2003.
8. Dalziel A, Moore S, Moyes C. Mitochondrial enzyme content in the muscles of high performance fish: evolution and variation among fiber types. Am J Physiol Regul Integr Comp Physiol 288: R163-R172, 2005.
9. Darveau CA, Suarez RK, Andrews RD, Hochachka PW. Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417: 166-170, 2002.
10. Davies R, Moyes CD. Allometric scaling in centrarchid fish: origins of intra-and inter-specific variation in oxidative and glycolytic enzyme levels in muscle. J Exp Biol 210: 3798-3804, 2007.
11. Dermitzakis E, Clark A. Evolution of transcription factor binding sites in mammalian gene regulatory regions: conservation and turnover. Mol Biol Evol 19: 1114-1121, 2002.
12. Dermitzakis ET, Reymond A, Lyle R, Scamuffa N, Ucla C, Deutsch S, Stevenson BJ, Flegel V, Bucher P, Jongeneel CV, Antonarakis S. Numerous potentially functional but non-genic conserved sequences on human chromosome 21. Nature 420: 578-582, 2002.
13. Dhar S, Ongwijitwat S, Wong-Riley M. Nuclear respiratory factor 1 regulates all ten nuclear-encoded subunits of cytochrome c oxidase in neurons. J Biol Chem 283: 3120-3129, 2007.
14. Edgerton VA, Roy RR. Regulation of skeletal muscle fiber size, shape and function. J Biomech 24: 237-254, 1991.
15. Emmett B, Hochachka PW. Scaling of oxidative and glycolytic enzymes in mammals. Resp Phys 45: 261-272, 1981.
16. Glazier D. Beyond the '3/4-power law': variation in intra-and interspecific scaling of metabolic rate in animals. Biol Rev 80: 1-52, 2005.
17. Gugneja S, Scarpulla RC. Serine phosphorylation within a concise amino-terminal domain in nuclear respiratory factor 1 enhances DNA binding. J Biol Chem 272: 18732-18739, 1997.
18. Handschin C, Rhee J, Lin J, Tarr P, Spiegelman B. An autoregulatory loop controls peroxisome proliferator-activated receptor coactivator 1 expression in muscle. Proc Nat Acad Sci USA 100: 7111-7116, 2003.
19. Hochachka PW, Darveau CA, Andrews RD, Suarez RK. Allometric cascade: A model for resolving body mass effects on metabolism. Comp Biochem Phys 134: 675-691, 2003.
20. Hock MB, Kralli A. Transcriptional control of mitochondrial biogenesis and function. Annu Rev Physiol 71: 177-203, 2009.
21. Hondares E, Mora O, Yubero P, Rodriguez de la Concepcion M, Iglesias R, Giralt M, Villarroya F. Thiazolidinediones and rexinoids induce peroxisome proliferator-activated receptor-coactivator (PGC)-1α gene transcription: an autoregulatory loop controls PGC-1α expression in adipocytes via peroxisome proliferator-activated receptor-gamma coactivation. Endocrinology 147: 2829-2838, 2006.
22. Irrcher I, Ljubicic V, Kiran A, Hood D. AMP-activated protein kinaseregulated activation of the PGC-1α promoter in skeletal muscle cells. PLos ONE 3: 10, 2008.
23. Garland T, Bennett A, Rezende E. Phylogenetic approaches in comparative physiology. J Exp Biol 208: 3015-3035, 2005.
24. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106: 847-856, 2000.
25. Lin J, Wu H, Tarr P, Zhang C, Wu Z, Boss O, Michael L, Puigserver P, Isotani E, Olson E, Spiegelman B. Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibers. Nature 418: 797-801, 2002.
26. Liu J, Hoglund A, Karlsson P, Lindblad J, Qaisar R, Aare S, Bengtsson E, Larsson L. Myonuclear domain size and myosin isoform expression in muscle fibres from mammals representing a 100-fold difference in body size. Exp Physiol 94: 117-129, 2008.
27. Mattick JS. Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep 2: 986-991, 2001.
28. McNab B. An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol 151: 5-28, 2008.
29. Moyes C, Genge C. Scaling of muscle metabolic enzymes: an historical prospective. Comp Biochem Physiol A Mol Integr Physiol 156: 344-350, 2010.
30. Moyes C, Hood D. Origins and consequences of mitochondrial variation. Ann Rev Physiol 65: 177-201, 2003.
31. Moyes C, LeMoine CM. Control of muscle bioenergetic gene expression: implications for allometric scaling relationships of glycolytic and oxidative enzymes. J Exp Biol 208: 1601-1610, 2005.
32. Ralston E, Hall Z. Restricted distribution of mRNA produced from a single nucleus in hybrid myotubules. J Cell Biol 119: 1063-1068, 1992.
33. Rodgers J, Lerin C, Gerhart-Hines Z, Puigserver P. Metabolic adaptations through the PGC-1α and SIRT1 pathways. FEBS Lett 582: 46-53, 2008.
34. Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta [Epub ahead of print] doi:10.1016/j.bbamcr2010.09.019.
35. Scassa ME, Guberman AS, Ceruti JM, Canepa ET. Hepatic nuclear factor 3 and nuclear factor 1 regulate 5-aminolevulinate synthase gene expression and are involved in insulin repression. J Biol Chem 279: 28082-28092, 2004.
36. Somero GN, Childress JJ. A violation of the metabolism-size scaling paradigm: activities of glycolytic enzymes in muscle increase in largersize fish. Physiol Zool 53: 322-327, 1980.
37. Sparks L, Xie H, Koza R, Mynatt R, Hulver M, Bray G, Smith S. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54: 1926-1933, 2005.
38. Springer M, Murphy W. Mammalian evolution and biomedicine: new views from phylogeny. Biol Rev 82: 375-392, 2007.
39. Tseng BS, Kasper CE, Edgerton VR. Cytoplasm-to-myonucleus ratios and succinate dehydrogenase activities in adult rat slow and fast muscle fibers. Cell Tiss Res 275: 39-49, 1994.
40. Vardhanabhuti S, Wang J, Hannenhalli S. Position and distance specificity are important determinants of cis-regulatory motifs in addition to evolutionary conservation. Nucl Acids Res 35: 3203-3213, 2007.
41. Weibel ER, Bacigalupe LD, Schmitt B, Hoppeler H. Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir Physiol Neurobiol 140: 115-132, 2004.
42. West GB, Brown JH, Enquist BJ. A general model for the origin of allometric scaling in biology. Science 276: 122-126, 1997.
43. White C, Seymour R. Mammalian basal metabolic rate is proportional to body mass 2/3. Proc Nat Acad Sci USA 100: 4046-4049, 2003.
44. Wright D, Han D, Garcia-Roves P, Geiger P, Jones T, Holloszy J. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1α expression. J Biol Chem 282: 194-199, 2007.
45. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla R, Spiegelman B. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.
46. Wulf A, Harneit A, Kroger M, Kebenko M, Wetzel M, Weitzel J. T3-mediated expression of PGC-1α via a far upstream located thyroid hormone response element. Mol Cell Endocrinol 287: 90-95, 2008