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Molecular changes in mitochondrial respiratory activity and metabolic enzyme activity in muscle of four pig breeds with distinct metabolic types

Journal of Bioenergetics and Biomembranes volume 48, pages 55–65 (2016)Cite this article

Abstract

Skeletal muscles are metabolically active and have market value in meat-producing farm animals. A better understanding of biological pathways affecting energy metabolism in skeletal muscle could advance the science of skeletal muscle. In this study, comparative pathway-focused gene expression profiling in conjunction with muscle fiber typing were analyzed in skeletal muscles from Duroc, Pietrain, and Duroc–Pietrain crossbred pigs. Each breed type displayed a distinct muscle fiber-type composition. Mitochondrial respiratory activity and glycolytic and oxidative enzyme activities were comparable among genotypes, except for significantly lower complex I activity in Pietrain pigs homozygous-positive for malignant hyperthermia syndrome. At the transcriptional level, lactate dehydrogenase B showed breed specificity, with significantly lower expression in Pietrain pigs homozygous-positive for malignant hyperthermia syndrome. A similar mRNA expression pattern was shown for several subunits of oxidative phosphorylation complexes, including complex I, complex II, complex IV, and ATP synthase. Significant correlations were observed between mRNA expression of genes in focused pathways and enzyme activities in a breed-dependent manner. Moreover, expression patterns of pathway-focused genes were well correlated with muscle fiber-type composition. These results stress the importance of regulation of transcriptional rate of genes related to oxidative and glycolytic pathways in the metabolic capacity of muscle fibers. Overall, the results further the breed-specific understanding of the molecular basis of metabolic enzyme activities, which directly impact meat quality.

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References

  • Acín-Pérez R, Fernández-Silva P, Peleato ML, Pérez-Martos A, Enriquez JA (2008) Respiratory active mitochondrial supercomplexes. Mol Cell 32:529–539

    Article  Google Scholar 

  • Anderson EJ, Neufer PD (2006) Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation. American Journal of Physiology Cell Physiology 290:C844–C851

    Article  CAS  Google Scholar 

  • Arany Z et al. (2007) The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab 5:35–46

    Article  CAS  Google Scholar 

  • Bonnefoy N, Fiumera HL, Dujardin G, Fox TD (2009) Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes. Biochim Biophys Acta 1793:60–70

    Article  CAS  Google Scholar 

  • Cannino G, Di Liegro CM, Rinaldi AM (2007) Nuclear-mitochondrial interaction. Mitochondrion 7:359–366

    Article  CAS  Google Scholar 

  • de Bari L, Moro L, Passarella S (2013) Prostate cancer cells metabolize d-lactate inside mitochondria via a D-lactate dehydrogenase which is more active and highly expressed than in normal cells. FEBS Lett 587:467–473

    Article  Google Scholar 

  • Dudkina N, Boekema E, Braun H-P (2014) Respiratory Chain Supercomplexes in Mitochondria. In: Hohmann-Marriott MF (ed) The Structural Basis of Biological Energy Generation. Springer, Netherlands, pp. 217–229

    Chapter  Google Scholar 

  • Enns GM et al. (2005) Relationship of primary mitochondrial respiratory chain dysfunction to fiber type abnormalities in skeletal muscle. Clin Genet 68:337–348

    Article  CAS  Google Scholar 

  • Fantin VR, St-Pierre J, Leder P (2006) Attenuation of LDH-a expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9:425–434

    Article  CAS  Google Scholar 

  • Fernandez X, Lefaucheur L, Candek M (1995) Comparative study of two classifications of muscle fibres: consequences for the photometric determination of glycogen according to fibre type in red and white muscle of the pig. Meat Sci 41:225–235

    Article  CAS  Google Scholar 

  • Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82:893–922

    Article  CAS  Google Scholar 

  • Fujii J et al. (1991) Identification of a mutation in porcine ryanodine receptor associated with malignant hyperthermia. Science 253:448–451

    Article  CAS  Google Scholar 

  • Gabriel-Costa D et al. (2015) Lactate up-regulates the expression of lactate oxidation complex-related genes in left ventricular cardiac tissue of rats. PLoS One 10:e0127843

    Article  Google Scholar 

  • Gellerich FN et al. (2010) The regulation of OXPHOS by extramitochondrial calcium. Biochim Biophys Acta 1797:1018–1027

    Article  CAS  Google Scholar 

  • Giulivi C et al. (2011) Basal bioenergetic abnormalities in skeletal muscle from ryanodine receptor malignant hyperthermia-susceptible R163C knock-in mice. J Biol Chem 286:99–113

    Article  CAS  Google Scholar 

  • Gladden LB (2004) Lactate metabolism: a new paradigm for the third millennium. J Physiol 558:5–30

    Article  CAS  Google Scholar 

  • Griffiths EJ, Rutter GA (2009) Mitochondrial calcium as a key regulator of mitochondrial ATP production in mammalian cells. Biochim Biophys Acta 1787:1324–1333

    Article  CAS  Google Scholar 

  • Gueguen N, Lefaucheur L, Fillaut M, Vincent A, Herpin P (2005) Control of skeletal muscle mitochondria respiration by adenine nucleotides: differential effect of ADP and ATP according to muscle contractile type in pigs. Comp Biochem Physiol B Biochem Mol Biol 140:287–297

    Article  CAS  Google Scholar 

  • Hocquette JF, Ortigues-Marty I, Vermorel M (2001) Manipulation of tissue energy metabolism in meat-producing ruminants. Asian Australas J Anim Sci 14:720–732

    Article  Google Scholar 

  • Huber K, Petzold J, Rehfeldt C, Ender K, Fiedler I (2007) Muscle energy metabolism: structural and functional features in different types of porcine striated muscles. J Muscle Res Cell Motil 28:249–258

    Article  CAS  Google Scholar 

  • Huff-Lonergan E, Lonergan SM (2005) Mechanisms of water-holding capacity of meat: the role of postmortem biochemical and structural changes. Meat Sci 71:194–204

    Article  CAS  Google Scholar 

  • Jager S, Handschin C, St-Pierre J, Spiegelman BM (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 104:12017–12022

    Article  Google Scholar 

  • Kang C, Li Ji L (2012) Role of PGC-1alpha signaling in skeletal muscle health and disease. Ann N Y Acad Sci 1271:110–117

    Article  CAS  Google Scholar 

  • Karlsson A, Essen-Gustavsson B, Lundstrom K (1994) Muscle glycogen depletion pattern in halothane-gene-free pigs at slaughter and its relation to meat quality. Meat Sci 38:91–101

    Article  CAS  Google Scholar 

  • Kim NK et al. (2008) Comparisons of longissimus muscle metabolic enzymes and muscle fiber types in Korean and western pig breeds. Meat Sci 78:455–460

    Article  CAS  Google Scholar 

  • Krischek C, Natter R, Wigger R, Wicke M (2011) Adenine nucleotide concentrations and glycolytic enzyme activities in longissimus muscle samples of different pig genotypes collected before and after slaughter. Meat Sci 89:217–220

    Article  CAS  Google Scholar 

  • Lanner JT, Georgiou DK, Joshi AD, Hamilton SL (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2:a003996

    Article  CAS  Google Scholar 

  • Leberer E, Pette D (1984) Lactate dehydrogenase isozymes in type I, IIA and IIB fibres of rabbit skeletal muscles. Histochemistry 80:295–298

    Article  CAS  Google Scholar 

  • Lin J et al. (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418:797–801. doi:10.1038/nature00904

    Article  CAS  Google Scholar 

  • Mili S, Pinol-Roma S (2003) LRP130, a pentatricopeptide motif protein with a noncanonical RNA-binding domain, is bound in vivo to mitochondrial and nuclear RNAs. Mol Cell Biol 23:4972–4982

    Article  CAS  Google Scholar 

  • Mourier A, Ruzzenente B, Brandt T, Kuhlbrandt W, Larsson NG (2014) Loss of LRPPRC causes ATP synthase deficiency. Hum Mol Genet 23:2580–2592

    Article  CAS  Google Scholar 

  • Neupert W, Herrmann JM (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76:723–749

    Article  CAS  Google Scholar 

  • O’Neill HM et al. (2011) AMP-activated protein kinase (AMPK) beta1beta2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proc Natl Acad Sci U S A 108:16092–16097

    Article  Google Scholar 

  • O’Neill HM, Holloway GP, Steinberg GR (2013) AMPK regulation of fatty acid metabolism and mitochondrial biogenesis: implications for obesity. Mol Cell Endocrinol 366:135–151

    Article  Google Scholar 

  • Peter J, Sawaki S, Barnard R, Edgerton V, Gillespie C (1971) Lactate dehydrogenase isoenzymes: distribution in fast-twitch red, fast-twitch white, and slow-twitch intermediate fibers of guinea pig skeletal muscle. Arch Biochem Biophys 144:304–307

    Article  CAS  Google Scholar 

  • Picard M, Hepple RT, Burelle Y (2012) Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function. American Journal of Physiology Cell Physiology 302:C629–C641

    Article  CAS  Google Scholar 

  • Schon EA, Dencher NA (2009) Heavy breathing: energy conversion by mitochondrial respiratory supercomplexes. Cell Metab 9:1–3

    Article  CAS  Google Scholar 

  • Schwerzmann K, Hoppeler H, Kayar SR, Weibel ER (1989) Oxidative capacity of muscle and mitochondria: correlation of physiological, biochemical, and morphometric characteristics. Proc Natl Acad Sci U S A 86:1583–1587

    Article  CAS  Google Scholar 

  • Shen Q, Underwood K, Means W, McCormick R, Du M (2007) The halothane gene, energy metabolism, adenosine monophosphate-activated protein kinase, and glycolysis in postmortem pig longissimus dorsi muscle. J Anim Sci 85:1054–1061

    Article  CAS  Google Scholar 

  • Smits P, Smeitink J, van den Heuvel L (2010) Mitochondrial translation and beyond: processes implicated in combined oxidative phosphorylation deficiencies. J Biomed Biotechnol 2010:737385

    Article  Google Scholar 

  • Voos W, Rottgers K (2002) Molecular chaperones as essential mediators of mitochondrial biogenesis. Biochim Biophys Acta 1592:51–62

    Article  CAS  Google Scholar 

  • Werner C, Opalka JR, Gellerich FN, Wicke M (2005) The influence of mitochondrial function on meat quality in Turkey and swine. Arch Tierz Dummenstorf 48:106–111

    Google Scholar 

  • Werner C, Natter R, Schellander K, Wicke M (2010a) Mitochondrial respiratory activity in porcine longissimus muscle fibers of different pig genetics in relation to their meat quality. Meat Sci 85:127–133

    Article  CAS  Google Scholar 

  • Werner C, Natter R, Wicke M (2010b) Changes of the activities of glycolytic and oxidative enzymes before and after slaughter in the longissimus muscle of pietrain and duroc pigs and a duroc-pietrain crossbreed. J Anim Sci 88:4016–4025

    Article  CAS  Google Scholar 

  • Wojtaszewski JF, Jorgensen SB, Hellsten Y, Hardie DG, Richter EA (2002) Glycogen-dependent effects of 5-aminoimidazole-4-carboxamide (AICA)-riboside on AMP-activated protein kinase and glycogen synthase activities in rat skeletal muscle. Diabetes 51:284–292

    Article  CAS  Google Scholar 

  • Wojtaszewski JF et al. (2003) Regulation of 5’AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am J Physiol Endocrinol Metab 284:E813–E822

    Article  CAS  Google Scholar 

  • Wu Z et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115–124

    Article  CAS  Google Scholar 

  • Yue G et al. (2003) Linkage and QTL mapping for Sus scrofa chromosome 6. J Anim Breed Genet 120:45–55

    Article  CAS  Google Scholar 

  • Zhang CS et al. (2014) The lysosomal v-ATPase-ragulator complex is a common activator for AMPK and mTORC1, acting as a switch between catabolism and anabolism. Cell Metab 20:526–540

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Measurements of mitochondrial respiratory activity and metabolic enzyme activity were supported by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG) in a project initiated and led by Prof. Dr. Michael Wicke (Department of Animal Science, Quality of Food of Animal Origin, Georg-August-University Goettingen) who has left us forever.

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Authors and Affiliations

  1. Leibniz Institute for Farm Animal Biology (FBN), Institute for Genome Biology, Wilhelm-Stahl-Allee 2, 18196, Dummerstorf, Germany

    Xuan Liu, Nares Trakooljul, Eduard Muráni, Klaus Wimmers & Siriluck Ponsuksili

  2. Institute of Food Quality and Food Safety, University of Veterinary Medicine Hannover, D-30173, Hannover, Germany

    Carsten Krischek

  3. Insititute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, Bonn, Germany

    Karl Schellander

  4. Department of Animal Sciences, Quality of Food of Animal Origin, Georg-August-University Goettingen, Goettingen, Germany

    Michael Wicke

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  1. Xuan Liu
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  2. Nares Trakooljul
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  3. Eduard Muráni
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  4. Carsten Krischek
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  6. Michael Wicke
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Correspondence to Siriluck Ponsuksili.

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Michael Wicke is deceased.

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Liu, X., Trakooljul, N., Muráni, E. et al. Molecular changes in mitochondrial respiratory activity and metabolic enzyme activity in muscle of four pig breeds with distinct metabolic types. J Bioenerg Biomembr 48, 55–65 (2016). https://doi.org/10.1007/s10863-015-9639-3

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  • DOI: https://doi.org/10.1007/s10863-015-9639-3

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