Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-19T06:24:12.517Z Has data issue: false hasContentIssue false
  • English
  • Français

Mitochondrial abundance and function in muscle from beef steers with divergent residual feed intakes

Published online by Cambridge University Press:  11 October 2019

E. E. Fernandez Open the ORCID record for E. E. Fernandez [Opens in a new window] ,
J. W. Oltjen  and
R. D. Sainz
E. E. Fernandez*
Affiliation:
Department of Animal Science, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
J. W. Oltjen
Affiliation:
Department of Animal Science, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
R. D. Sainz
Affiliation:
Department of Animal Science, University of California, Davis, 1 Shields Ave, Davis, CA 95616, USA
*
†E-mail: [email protected]
Get access

Abstract

The objective of this study was to evaluate the relationship between muscle mitochondrial function and residual feed intake (RFI) in growing beef cattle. A 56-day feeding trial was conducted with 81 Angus × Hereford steers (initial BW = 378 ± 43 kg) from the University of California Sierra Foothills Research Station (Browns Valley, CA, USA). All steers were individually fed the same finishing ration (metabolizable energy = 3.28 Mcal/kg DM). Average daily gain (ADG), DM intake (DMI) and RFI were 1.82 ± 0.27, 8.89 ± 1.06 and 0.00 ± 0.55 kg/day, respectively. After the feeding trial, the steers were categorized into high, medium and low RFI groups. Low RFI steers consumed 13.6% less DM (P < 0.05) and had a 14.1% higher G : F ratio (P < 0.05) than the high RFI group. No differences between RFI groups were found in age, ADG or BW (P > 0.10). The most extreme individuals from the low and high RFI groups were selected to assess mitochondrial function (n = 5 low RFI and n = 6 high RFI). Mitochondrial respiration was measured using an oxygraph (Hansatech Instruments Ltd., Norfolk, UK). State 3 and State 4 respiration rates were similar between both groups (P > 0.10). Respiratory control ratios (RCRs, i.e., State 3 : State 4 oxygen uptakes) declined with animal age and were greater in low RFI steers (4.90) as compared to high RFI steers (4.26) when adjusted for age by analysis of covariance (P = 0.003). Mitochondrial complex II activity levels per gram of muscle were 42% greater in low RFI steers than in high RFI steers (P = 0.004). These data suggest that skeletal muscle mitochondria have greater reserve respiratory capacity and show greater coupling between respiration and phosphorylation in low RFI than in high RFI steers.

Keywords

bioenergeticsmetabolismbeef productionproton leakfeed efficiency
Type
Research Article
Information
animal , Volume 14 , Issue 3 , March 2020 , pp. 560 - 565
Copyright
© The Animal Consortium 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acetoze, G, Weber, KL, Ramsey, JJ and Rossow, HA 2015. Relationship between liver mitochondrial respiration and proton leak in low and high RFI steers from two linages of RFI angus bulls. International Scholarly Research Notices 2015, 194014. doi: 10.1155/2015/194014CrossRefGoogle Scholar
Affourtit, C, Quinlan, CL and Brand, MD (ed. Palmeira, CM and Moreno, AJ 2012. Measurement of proton leak and electron leak in isolated mitochondria. In Mitochondrial bioenergetics. Methods in molecular biology (ed. ), pp. 165–182. Humana Press, New York, NY, USA.CrossRefGoogle Scholar
Bottje, W, Pumford, NR, Ojano-Dirain, C, Iqbal, M and Lassiter, K 2006. Feed efficiency and mitochondrial function. Poultry Science 85, 8–14.CrossRefGoogle ScholarPubMed
Bottje, W, Tang, ZX, Iqbal, M, Cawthon, D, Okimoto, R, Wing, T and Cooper, M 2002. Association of mitochondrial function with feed efficiency within a single genetic line of male broilers. Poultry Science 81, 546–555CrossRefGoogle ScholarPubMed
Brand, MD, Chien, LF, Ainscow, EK, Rolfe, DFS and Porter, RK 1994. The causes and functions of mitochondrial proton leak. Biochimica et Biophysica Acta 1187, 132–139.CrossRefGoogle ScholarPubMed
Brown, DR, DeNise, SK and McDaniel, RG 1988. Mitochondrial respiratory metabolism and performance of cattle. Journal of Animal Science 66, 1347–1354.CrossRefGoogle ScholarPubMed
Casal, A, Garcia-Roche, M, Navajas, EA, Cassina, A and Carriquiry, M 2018. Hepatic mitochondrial function in Hereford steers with divergent residual feed intake phenotypes. Journal of Animal Science 96, 4431–4443.CrossRefGoogle ScholarPubMed
Castro Bulle, FCP, Paulino, PV, Sanches, AC and Sainz, RD 2007. Growth, carcass quality and protein and energy metabolism in beef cattle with different growth potentials and residual feed intakes. Journal of Animal Science 85, 928–936.CrossRefGoogle ScholarPubMed
Chabi, B, Ljubicic, V, Menzies, KJ, Huang, JH, Saleem, A and Hood, DA 2008. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7, 2–12.CrossRefGoogle ScholarPubMed
Commonwealth Scientific and Industrial Research Organization 1990. Feeding standards for Australian livestock. Ruminants. CSIRO Publications, East Melbourne, Victoria, Australia.Google Scholar
Estabrook, RW 1967. [7] Mitochondria respiratory control and the polarographic measurement of ADP : O ratios. Methods in Enzymology 10, 41–47.CrossRefGoogle Scholar
Ferguson, M, Mockett, RJ, Shen, Y, Orr, WC and Sohal, RS 2005. Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanocaster. Biochemical Journal 390, 501–511.CrossRefGoogle Scholar
Fernandez Guerra, E, Oltjen, J and Sainz, R 2018. Relationships between mitochondrial function and residual feed intake in beef steers. Journal of Animal Science 96 (suppl. 3), 60.CrossRefGoogle Scholar
Figueiredo, PA, Powers, SK, Ferreira, RM, Appell, HJ and Duarte, JA 2009. Aging impairs skeletal muscle mitochondrial bioenergetic function. The Journals of Gerontology Series A: Biological Sciences Medical Sciences 64A, 21–33.CrossRefGoogle Scholar
Freyssenet, A, Berthon, P and Denis, C 1996. Mitochondrial biogenesis in skeletal muscle in response to endurance exercises. Archives of Physiology and Biochemistry 104, 129–141.CrossRefGoogle ScholarPubMed
Herd, RM, Oddy, VH and Richardson, EC 2004. Biological basis for variation in residual feed intake in beef cattle. 1. Review of potential mechanisms. Australian Journal of Experimental Agriculture 44, 423–430.CrossRefGoogle Scholar
Iqbal, M, Pumford, NR, Tang, ZX, Lassiter, K, Ojan-Dirian, C, Wing, T, Cooper, M and Bottje, W 2005. Compromised liver mitochondrial function and complex activity in low feed efficient broilers are associated with higher oxidative stress and differential protein expression. Poultry Science 54, 933–941.CrossRefGoogle Scholar
Koch, RM, Swiger, LA, Chambers, D and Gregory, KE 1963. Efficiency of feed use in beef cattle. Journal of Animal Science 22, 486–494.CrossRefGoogle Scholar
Kolath, WH, Kerley, MS, Golden, JW and Keisler, DH 2006. The relationship between mitochondrial function and residual feed intake in Angus steers. Journal of Animal Science 84, 861–865.CrossRefGoogle ScholarPubMed
Lancaster, PA, Carstens, GE, Michal, JJ, Brennan, KM, Johnson, KA and Davis, ME 2014. Relationships between residual feed intake and hepatic mitochondrial function in growing beef cattle. Journal of Animal Science 92, 3134–3141.CrossRefGoogle ScholarPubMed
Larsen, S, Nielsen, J, Hansen, LB, Nielsen, LB, Wibrand, F, Stride, N, Schroder, HD, Boushel, R, Helge, JW, Dela, F and Hey-Mogensen, M 2012. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. Journal of Physiology 590, 3349–3360.CrossRefGoogle ScholarPubMed
Nkrumah, JD, Okine, EK, Mathison, GW, Schmid, K, Li, C, Basarab, JA, Price, MA, Wang, Z and Moore, SS 2006. Relationships of feedlot efficiency, performance, and feeding behavior with metabolic rate, methane production, and energy partitioning in beef cattle. Journal of Animal Science 84, 145–153.CrossRefGoogle ScholarPubMed
Ojano-Dirain, C, Iqbal, M, Wing, T, Cooper, M and Bottje, W 2005a. Glutathione and respiratory chain complex activity in duodenal mitochondria of broilers with low and high feed efficiency. Poultry Science 84, 785–788.Google ScholarPubMed
Ojano-Dirain, C, Pumford, NR, Iqbal, M, Wing, T, Cooper, M and Bottje, WG 2005b. Biochemical evaluation of mitochondrial respiratory chain in duodenum of low and high feed efficient broilers. Poultry Science 84, 1926–1934CrossRefGoogle ScholarPubMed
Ojano-Dirain, C, Tinsley, NB, Wing, T, Cooper, M and Bottje, W 2007. Membrane potential and hydrogen peroxide production in duodenal mitochondria in broilers chickens (Gallus gallus) with low and high feed efficiency. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 147, 934–941CrossRefGoogle ScholarPubMed
Pfleger, J, He, M and Abdellatif, M 2015. Mitochondrial complex II is a source of the reserve respiratory capacity that is regulated by metabolic sensors and promotes cell survival. Cell Death and Disease 6, e1835. doi: 10.1038/cddis.2015.202.CrossRefGoogle ScholarPubMed
Ramsey, JJ, Hagopian, K, Kenny, TM, Koomson, EK, Bevilacqua, L, Weindruch, R and Harper, ME 2004. Proton leak and hydrogen peroxide production in liver mitochondria from energy-restricted rats. The American Journal of Physiology-Endocrinology and Metabolism 286, E31–E40.CrossRefGoogle ScholarPubMed
Richardson, EC, Herd, RM, Archer, JA and Arthur, PF 2004. Metabolic differences in Angus steers divergently selected for residual feed intake. Australian Journal of Experimental Agriculture 44, 441–452.CrossRefGoogle Scholar
Rolfe, DFS and Brown, GC 1997. Cellular energy utilization and molecular origins of standard metabolic rate in mammals. Physiological Reviews 77, 731–758.CrossRefGoogle Scholar
Sainz, RD, Cruz, GD, Mendes, E, Magnabosco, CU, Farjalla, YB, Araujo, FRC, Gomes, RC and Leme, PR 2013. Performance, efficiency and estimated maintenance energy requirements of Bos Taurus and Bos indicus cattle. In Energy and protein metabolism and nutrition in sustainable animal production (ed. Oltjen, JW, Kebreab, E and Lapierre, H), pp. 69–70. Wageningen Academic Publishers, Wageningen, Netherlands.CrossRefGoogle Scholar
Spinazzi, M, Casarin, A, Pertegato, V, Salviati, L and Angelini, C 2012. Assessment of Mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nature Protocols 7, 1235–1246. doi: 10.1038/nprot.2012.058.CrossRefGoogle ScholarPubMed
Taylor, CR 1987. Structural and functional limits to oxidative peroxisome proliferator-activated receptor (PPAR) in mediating metabolism: insights from scaling. Annual Reviews of Physiology 49, 135–146.CrossRefGoogle Scholar
Watt, IN, Montgomery, MG, Runswick, MJ, Leslie, AGW and Walker, JE 2010. Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proceedings of the National Academy of Sciences of the United States of America 39, 16823–16827.CrossRefGoogle Scholar
Zurlo, F, Larson, K, Bogardus, C and Ravussin, E 1990. Skeletal muscle metabolism is a major determinant of resting energy expenditure. The Journal of Clinical Investigation 86, 1423–1427.CrossRefGoogle ScholarPubMed