Abstract
Growth rate is a fundamental parameter of an organism’s life history and varies 30-fold across bird species. To explore how whole-organism growth rate and the metabolic rate of cultured muscle cells are connected, two lines of Japanese quail (Coturnix coturnix japonica), one that had been artificially selected for fast growth for over 60 generations and a control line were used to culture myoblasts. In line with previous work, myoblasts from the fast growth line had significantly higher rates of oxygen consumption, glycolytic flux, and higher mitochondrial volume than myoblasts from the control line, indicating that an increase in growth rate is associated with a concomitant increase in cellular metabolic rates and that mitochondrial density contributes to the differences in rates of metabolism between the lines. We reared chicks from two hybrid lines with reciprocal parental configurations for growth rate to explore the effect of maternally inherited mitochondrial DNA on rates of growth and metabolism. Growth rates of chicks, cellular basal oxygen consumption, glycolytic flux, and mitochondrial volume in myoblasts from chicks from both reciprocal crosses were intermediate to the fast and control lines. This indicates that genes in the nucleus have a strong influence on metabolic rates at the cellular level, compared with maternally inherited mitochondrial DNA.
Similar content being viewed by others
Abbreviations
- mtDNA:
-
Mitochondrial DNA
- C:
-
Control line of quail
- F:
-
Fast line of quail
- CFFM :
-
Females from a control line of quail crossed with males from the fast line
- FFCM :
-
Females from the fast line of quail crossed with males from the control line
- CS:
-
Chicken Serum
- HS:
-
Horse Serum
- AbAm:
-
Antibiotic/Antimycotic
- OCR:
-
Oxygen consumption rates
- FCCP:
-
Carbonylcyanide-p-trifluoromethoxyphenylhydrazone
- RCR:
-
Respiratory control ratio
- ECAR:
-
Extracellular acidification rates
- K :
-
Growth rate constant (K)
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- BMR:
-
Basal metabolic rate
References
Aggrey SE, Marks HL (2003) Effect of long-term divergent selection on growth characteristics in Japanese Quail. Poult Sci 82:538–542
Anthony NB, Nestor KE, Bacon WL (1986) Growth curves of Japanese Quail as modified by divergent selection for 4-week body weight. Poult Sci 65:1825–1833
Arnqvist G, Dowling DK, Eady P et al (2010) Genetic architecture of metabolic rate: environment specific epistasis between mitochondrial and nuclear genes in an insect. Evolution (NY) 64:3354–3363. doi:10.1111/j.1558-5646.2010.01135.x
Austin SH, Robinson TR, Robinson WD, Ricklefs RE (2011) Potential biases in estimating the rate parameter of sigmoid growth functions. Methods Ecol Evol 2:43–51. doi:10.1111/j.2041-210X.2010.00055.x
Ballard JWO, Rand DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annu Rev Ecol Evol Syst 36:621–642. doi:10.1146/annurev.ecolsys.36.091704.175513
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744. doi:10.1046/j.1365-294X.2003.02063.x
Ballard JWO, Melvin RG, Katewa SD, Maas K (2007) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution (NY) 61:1735–1747. doi:10.1111/j.1558-5646.2007.00133.x
Blier PU, Dufresne F, Burton RS (2001) Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet 17:400–406
Brand MD, Nicholls DG (2011) Assessing mitochondrial dysfunction in cells. Biochem J 435:297–312. doi:10.1042/BJ20110162
Brooks GA (2010) What does glycolysis make and why is it important? J Appl Physiol 108:1450–1451. doi:10.1152/japplphysiol.00308.2010
Brown GC (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504:46–57
Bulit F, Barrionuevo M, Massoni V (2014) Insights into life history theory: a brood size manipulation on a southern hemisphere species, Tachycineta leucorrhoa, reveals a fast pace of life. J Avian Biol 45:225–234. doi:10.1111/j.1600-048X.2013.00266.x
Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J Comp Physiol B 143:191–198. doi:10.1007/BF00797698
Chacko BK, Kramer PA, Ravi S et al (2014) The Bioenergetic Health Index: a new concept in mitochondrial translational research. Clin Sci 127:367–373. doi:10.1042/CS20140101
Chakravarthy MV, Spangenburg EE, Booth FW (2001) Culture in low levels of oxygen enhances in vitro proliferation potential of satellite cells from old skeletal muscles. Cell Mol Life Sci 58:1150–1158. doi:10.1007/PL00000929
Choi AI, Ricklefs RE, Shea RE (1993) Skeletal muscle growth, enzyme activities and the development of thermogenesis: a comparison between altricial and precocial birds. Physiol Zool 66:455–473
Coutinho LL, Morris J, Marks HL et al (1993) Delayed somite formation in a quail line exhibiting myofiber hyperplasia is accompanied by delayed expression of myogenic regulatory factors and myosin heavy chain. Development 117:563–569
Das J (2006) The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays 28:890–901. doi:10.1002/bies.20463
Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116. doi:10.1111/j.1469-185X.2010.00136.x
Ekstrand MI, Falkenberg M, Rantanen A et al (2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 13:935–944. doi:10.1093/hmg/ddh109
Fell DA (1992) Metabolic control analysis: a survey of its theoretical and experimental development. Biochem J 286:313–330
Ferrick DA, Neilson A, Beeson C (2008) Advances in measuring cellular bioenergetics using extracellular flux. Drug Discov Today 13:268–274. doi:10.1016/j.drudis.2007.12.008
Fries AC (2009) The molecular evolution of mitochondrial oxidative phosphorylation genes in the Order Passeriformes. Master of Science Thesis. The Ohio State University, USA
Gerencser AA, Neilson A, Choi SW et al (2009) Quantitative microplate-based respirometry with correction for oxygen diffusion. Anal Chem 81:6868–6878. doi:10.1021/ac900881z
Halevy O, Piestun Y, Allouh MZ et al (2004) Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 231:489–502. doi:10.1002/dvdy.20151
Harper JM, Wang M, Galecki AT et al (2011) Fibroblasts from long-lived bird species are resistant to multiple forms of stress. J Exp Biol 214:1902–1910. doi:10.1242/jeb.054643
Hawke TJ, Garry DJ (2010) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551
Hill BG, Benavides GA, Lancaster JR Jr et al (2013) Integration of cellular bioenergetics with mitochondrial quality control and autophagy. Biol Chem 393:1485–1512. doi:10.1515/hsz-2012-0198.Integration
Holmes DJ, Flückiger R, Austad SN (2001) Comparative biology of aging in birds: an update. Exp Gerontol 36:869–883
Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199:257–274. doi:10.1006/jtbi.1999.0955
Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87:1175–1213. doi:10.1152/physrev.00047.2006
Hyánková L, Knizetová H, Dedková L, Hort J (2001) Divergent selection for shape of growth curve in Japanese quail. 1. Responses in growth parameters and food conversion. Br Poult Sci 42:583–589. doi:10.1080/0007166012008837
Jimenez AG, Harper JM, Queenborough SA, Williams JB (2013) Linkages between the life-history evolution of tropical and temperate birds and the resistance of cultured skin fibroblasts to oxidative and non-oxidative chemical injury. J Exp Biol 216:1373–1380. doi:10.1242/jeb.079889
Jimenez AG, Cooper-Mullin C, Anthony NB, Williams JB (2014a) Cellular metabolic rates in cultured primary dermal fibroblasts and myoblast cells from fast-growing and control Coturnix quail. Comp Biochem Physiol A Mol Integr Physiol 171:23–30. doi:10.1016/j.cbpa.2014.02.006
Jimenez AG, Van Brocklyn J, Wortman M, Williams JB (2014b) Cellular metabolic rate is influenced by life-history traits in tropical and temperate birds. PLoS One 9:e87349. doi:10.1371/journal.pone.0087349
Jimenez AG, Cooper-Mullin C, Calhoon EA, Williams JB (2014c) Physiological underpinnings associated with differences in pace of life and metabolic rate in north temperate and neotropical birds. J Comp Physiol B 184:545–561. doi:10.1007/s00360-014-0825-0
Khaldari M, Pakdel A, Mehrabani Yeganeh H et al (2010) Response to selection and genetic parameters of body and carcass weights in Japanese quail selected for 4-week body weight. Poult Sci 89:1834–1841. doi:10.3382/ps.2010-00725
Krebs HA (1950) Body size and tissue respiration. Biochim Biophys Acta 4:249–269. doi:10.1016/0006-3002(50)90032-1
Londono G (2014) Basal metabolism in tropical birds: latitude, altitude, and the “pace of life”. Funct Ecol 29:338–346
Martin AW, Fuhrman FA (2014) The relationship between summated tissue respiration and metabolic rate in the mouse and dog. Physiol Zool 28:18–34
Martin TE, Lloyd P, Bosque C et al (2011) Growth rate variation among passerine species in tropical and temperate sites: an antagonistic interaction between parental food provisioning and nest predation risk. Evolution 65:1607–1622. doi:10.1111/j.1558-5646.2011.01227.x
Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495
McBride HM, Neuspiel M, Wasiak S (2006) Mitochondria: more than just a powerhouse. Curr Biol 16:R551–R560. doi:10.1016/j.cub.2006.06.054
McConnell H, Owicki JC, Parce JW et al (1992) The cytosensor microphysiometer: biological applications of silicon technology. Science 257:1906–1912
Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260. doi:10.1016/S0169-5347(01)02124-3
Miettinen TP, Pessa HKJ, Caldez MJ et al (2014) Identification of transcriptional and metabolic programs related to mammalian cell size. Curr Biol 24:598–608. doi:10.1016/j.cub.2014.01.071
Millward DJ, Garlick PJ (1976) The energy cost of growth. Proc Nutr Soc 35:339–349
Nicholls DG, Darley-Usmar VM, Wu M et al (2010) Bioenergetic profile experiment using C2C12 myoblast cells. J Vis Exp 3–7. doi: 10.3791/2511
Pagliarini DJ, Calvo SE, Chang B et al (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112–123. doi:10.1016/j.cell.2008.06.016
Parrinello S, Samper E, Krtolica A et al (2003) Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 5:741–747. doi:10.1038/ncb1024
Pohjoismäki JLO, Wanrooij S, Hyvärinen AK et al (2006) Alterations to the expression level of mitochondrial transcription factor A, TFAM, modify the mode of mitochondrial DNA replication in cultured human cells. Nucleic Acids Res 34:5815–5828. doi:10.1093/nar/gkl703
Pohjoismäki JLO, Boettger T, Liu Z et al (2012) Oxidative stress during mitochondrial biogenesis compromises mtDNA integrity in growing hearts and induces a global DNA repair response. Nucleic Acids Res 40:6595–6607. doi:10.1093/nar/gks301
Porter RK, Joyce OJ, Farmer MK et al (1999) Indirect measurement of mitochondrial proton leak and its application. Int J Obes Relat Metab Disord 23(Suppl 6):S12–S18
Ricklefs RE (1969) Preliminary models for growth rates in altricial birds. Ecology 50:1031–1039
Ricklefs RE (1984) The optimization of growth rate in altricial birds. Ecology 65:1602–1616
Ricklefs RE (2010) Embryo growth rates in birds and mammals. Funct Ecol 24:588–596. doi:10.1111/j.1365-2435.2009.01684.x
Ricklefs RE, Marks HL (1985) Anatomical response to selection for 4-week body mass in Japanese Quail. Auk 102:323–333
Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468
Robinson WD, Hau M, Klasing KC et al (2010) Diversification of life histories in new world birds. Auk 127:253–262. doi:10.1525/auk.2010.127.2.253
Roff DA (1992) Evolution of life histories: theory and analysis. Routledge, Chapman and Hall Inc, New York
Rubin H (1975) Central role for magnesium in coordinate control of metabolism and growth in animal cells Cell Biology. Proc Natl Acad Sci 72:3551–3555
Sahlin K (2008) Response to point:counterpoint on “lactic acid”. J Appl Physiol 105:336
Sansbury BE, Jones SP, Riggs DW et al (2011) Bioenergetic function in cardiovascular cells: the importance of the reserve capacity and its biological regulation. Chem Biol Interact 191:288–295. doi:10.1016/j.cbi.2010.12.002
Scheffler IE (2007) Mitochondria, Second edn. Wiley, Hoboken
Selman C, Blount JD, Nussey DH, Speakman JR (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends Ecol Evol 27:570–577. doi:10.1016/j.tree.2012.06.006
Shea RE, Choi I, Ricklefs RE (1995) Growth rate and function of skeletal muscles in Japanese Quail selected for 4-week body mass. Physiol Zool 68:1045–1076
Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc Lond B Biol Sci 363:375–398. doi:10.1098/rstb.2007.2145
Stager M, Cerasale DJ, Dor R et al (2014) Signatures of natural selection in the mitochondrial genomes of Tachycineta swallows and their implications for latitudinal patterns of the “pace of life”. Gene 546:104–111. doi:10.1016/j.gene.2014.05.019
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Steyermark AC, Miamen AG, Feghahati HS, Lewno AW (2005) Physiological and morphological correlates of among-individual variation in standard metabolic rate in the leopard frog Rana pipiens. J Exp Biol 208:1201–1208. doi:10.1242/jeb.01492
Stier A, Delestrade A, Zahn S et al (2014) Elevation impacts the balance between growth and oxidative stress in coal tits. Oecologia 175:791–800. doi:10.1007/s00442-014-2946-2
Tieleman BI, Versteegh MA, Fries A et al (2009) Genetic modulation of energy metabolism in birds through mitochondrial function. Proc R Soc B 276:1685–1693. doi:10.1098/rspb.2008.1946
Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930. doi:10.1111/j.1365-294X.2012.05664.x
Toews DPL, Mandic M, Richards JG, Irwin DE (2014) Migration, mitochondria, and the yellow-rumped warbler. Evolution 68:241–255. doi:10.1111/evo.12260
Tronstad K, Nooteboom M, Nilsson L et al (2014) Regulation and quantification of cellular mitochondrial morphology and content. Curr Pharm Des 20:5634–5652. doi:10.2174/1381612820666140305230546
Umminger BL (1977) Relation of whole blood sugar concentrations in vertebrates to standard metabolic rate. Comp Biochem Physiol 56:457–460
Velleman SG, Liu X, Nestor KE, McFarland DC (2000) Heterogeneity in growth and differentiation characteristics in male and female satellite cells isolated from turkey lines with different growth rates. Comp Biochem Physiol A Mol Integr Physiol 125:503–509
Velleman SG, Coy CS, Anderson JW et al (2003) Effect of selection for growth rate and inheritance on posthatch muscle development in turkeys. Poult Sci 82:1365–1372
Vock R, Weibel ER, Hoppeler H et al (1996) Design of the oxygen and substrate pathways. V. Structural basis of vascular substrate supply to muscle cells. J Exp Biol 199:1675–1688
Weibel ER, Hoppeler H (2005) Exercise-induced maximal metabolic rate scales with muscle aerobic capacity. J Exp Biol 208:1635–1644. doi:10.1242/jeb.01548
Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Natl Acad Sci USA 104:9340–9345. doi:10.1073/pnas.0702212104
Wiley C, Beeson C (2002) Continuous measurement of glucose utilization in heart myoblasts. Anal Biochem 304:139–146. doi:10.1006/abio.2002.5613
Williams JB, Tieleman BI, Visser GH, Ricklefs RE (2007) Does growth rate determine the rate of metabolism in shorebird chicks living in the Arctic? Physiol Biochem Zool 80:500–513. doi:10.1086/520126
Williams JB, Miller RA, Harper JM, Wiersma P (2010) Functional linkages for the pace of life, life-history, and environment in birds. Integr Comp Biol 50:855–868. doi:10.1093/icb/icq024
Wu M, Neilson A, Swift AL et al (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292:C125–C136. doi:10.1152/ajpcell.00247.2006
Xun Z, Rivera-Sánchez S, Ayala-Peña S et al (2012) Targeting of XJB-5-131 to mitochondria suppresses oxidative DNA damage and motor decline in a mouse model of Huntington’s disease. Cell Rep 2:1137–1142. doi:10.1016/j.celrep.2012.10.001
Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54:1177–1191. doi:10.1369/jhc.6R6995.2006
Zhang J, Nuebel E, Wisidagama DR et al (2012) Measuring metabolism in cultured cells, including human pluripotent stem cells and differentiated cells. Nat Protoc 7:1068–1085. doi:10.1038/nprot.2012.048
Acknowledgments
We are grateful to Drs. David Denlinger, Peter Reiser, and Bob Ricklefs for their helpful comments. Dr. Harry Itagaki suggested that we cross the fast and the control lines to explore how this might affect metabolism of cells. Thanks to Dr. Sandra G. Velleman, Cynthia Coy and Dr. Jim Van Brocklyn for their help with the cell culture, and Dr. Ajit Divikaruni, Dr. David Ferrick, and several anonymous reviewers for their insightful comments that have improved this manuscript. We would like to thank Andrew Sudimack for his help with processing the Japanese quail, and The Ohio State University Campus Microscopy and Imaging Facility for allowing us to use their confocal microscope. This work was funded by the National Science Foundation IBN 0212587 (JBW).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I. D. Hume.
Rights and permissions
About this article
Cite this article
Cooper-Mullin, C., Jimenez, A.G., Anthony, N.B. et al. The metabolic rate of cultured muscle cells from hybrid Coturnix quail is intermediate to that of muscle cells from fast-growing and slow-growing Coturnix quail. J Comp Physiol B 185, 547–557 (2015). https://doi.org/10.1007/s00360-015-0906-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-015-0906-8