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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

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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.

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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

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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).

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The authors declare that they have no conflict of interest.

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Correspondence to Clara Cooper-Mullin.

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Communicated by I. D. Hume.

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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

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  • DOI: https://doi.org/10.1007/s00360-015-0906-8

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