Muscle-fibre types in porcine longissimus muscle of different genotypes and their association with the status of energy metabolism
Xiao-Ming Men A B , Bo Deng B , Zi-Wei Xu A B C and Xin Tao BA State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi 214122, Jiangsu, China.
B Institute of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China.
C Corresponding author. Email: xzwfyz@sina.com
Animal Production Science 52(5) 305-312 https://doi.org/10.1071/AN11185
Submitted: 30 August 2011 Accepted: 13 January 2012 Published: 20 March 2012
Abstract
To study the difference in muscle-fibre types in porcine muscle among different genotypes and its association with energy metabolism, composition of myosin heavy chain (MyHC) mRNA and energy metabolism indices were determined in the longissimus muscle (LM). Pig breeds included Jinhua (JHP), Zhongbai (ZBP), Duroc × Zhongbai cross (DZP) and Duroc × Yorkshire × Landrace cross (DYL). JHP pigs were found to have the highest proportions of MyHC I, IIa and IIx mRNA (P < 0.05), creatine kinase (CK) activity (P < 0.05) and the lowest glycolytic potential (GP) compared with the other genotypes. The proportions of MyHC I and IIa mRNA increased in the order of DYL < DZP < ZBP < JHP, whereas the trend was opposite for MyHC IIb mRNA. The proportions of MyHC I, IIa and IIx mRNA were positively correlated with CK activity and the turnover ratio of creatine phosphate (CP) (P < 0.01), and negatively correlated with GP, glucose-6-phosphate (G-6-P) and lactate (LA) contents (P < 0.01), with the trends being opposite for MyHC IIb mRNA. The results indicate that muscle-fibre type in porcine LM is influenced by the genetic background of pigs. For example, JHP pigs had more of Types I, IIa and IIx fibres than did other genotypes. Proportions of Types I, IIa and IIx fibres were positively correlated with CK reaction (ATP-CP) capacity and negatively correlated with GP. These data provide some evidence for exploring the effective mechanism of muscle-fibre type on pork quality.
Additional keywords: energy metabolism, pig genotypes, muscle-fibre types, myosin heavy chain.
References
Baldwin KM, Klinkerfuss GH, Terjung RL, Mole PA, Holloszy JO (1972) Respiratory capacity of white, red, and intermediate muscle: adaptative response to exercise. The American Journal of Physiology 222, 373–378.Bee G, Biolley C, Guex G, Herzog W, Lonergan SM, Huff-Lonergan E (2006) Effects of available dietary carbohydrate and preslaughter treatment on glycolytic potential, protein degradation, and quality traits of pig muscles. Journal of Animal Science 84, 191–203.
Bendall JR (1951) The shortening of rabbit muscles during rigor mortis: its relation to the breakdown of adenosine triphosphate and creatine phosphate and to muscular contraction. The Journal of Physiology 114, 71–88.
Berg EP, Allee GL (2001) Creatine monohydrate supplemented in swine finishing diets and fresh pork quality: I. A controlled laboratory experiment. Journal of Animal Science 79, 3075–3080.
Bottinelli R, Reggiani C (2000) Human skeletal muscle fibers: molecular and functional diversity. Progress in Biophysics and Molecular Biology 73, 195–262.
| Human skeletal muscle fibers: molecular and functional diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvV2rs7k%3D&md5=c5ce347beedffaaa57b5b32d73a1f9edCAS |
Brooke MH, Kaiser KK (1970) Muscle fiber types: how many and what kind? Archives of Neurology 23, 369–379.
| Muscle fiber types: how many and what kind?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M%2FisFWgtQ%3D%3D&md5=ddb387138270ce33ff61ce319f80129aCAS |
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.
| The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqs7g%3D&md5=55061b87db810d6e373f917870cb19f8CAS |
Ceddia RB, Sweeney G (2003) Creatine supplementation increases glucose oxidation and AMK phosphorylation and reduces lactate production in L6 rat skeletal muscle cells. The Journal of Physiology 555, 409–421.
| Creatine supplementation increases glucose oxidation and AMK phosphorylation and reduces lactate production in L6 rat skeletal muscle cells.Crossref | GoogleScholarGoogle Scholar |
Chang KC, Fernandes K (1997) Developmental expression and 5′end cDNA cloning of the porcine 2x and 2b myosin heavy chain genes. DNA and Cell Biology 16, 1429–1437.
| Developmental expression and 5′end cDNA cloning of the porcine 2x and 2b myosin heavy chain genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmvFyktg%3D%3D&md5=c8a0d9716be285243fc9bfe3eef399f3CAS |
Chang KC, Fernandes K, Gldspink G (1993) In vivo expression and molecular characterization of the porcine slow myosin heavy chain. Journal of Cell Science 106, 331–341.
Chang KC, Fernandes K, Dauncey MJ (1995) Molecular characterization of a developmentally regulated porcine skeletal myosin heavy chain gene and its 5′ regulatory region. Journal of Cell Science 108, 1779–1789.
Chartrin P, Bernadet MD, Guy G, Mourot J, Hocquette JF, Rideau N, Duclos MJ, Baéza E (2006) Does overfeeding enhance genotype effects on energy metabolism and lipid deposition in breast muscle of ducks? Comparative Biochemistry and Physiology 145A, 413–418.
Choe JH, Choi YM, Lee SH, Shin HG, Ryu YC, Hong KC, Kim BC (2008) The relation between glycogen, lactate content and muscle fiber type composition, and their influence on postmortem glycolytic rate and pork quality. Meat Science 80, 355–362.
| The relation between glycogen, lactate content and muscle fiber type composition, and their influence on postmortem glycolytic rate and pork quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVagu7%2FL&md5=44e1171ce23bceb1fc25435927cded83CAS |
Choi YM, Ryu YC, Kim BC (2007) Influence of myosin heavy- and light-chain isoforms on early postmortem glycolytic rate and pork quality. Meat Science 76, 281–288.
| Influence of myosin heavy- and light-chain isoforms on early postmortem glycolytic rate and pork quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit12lsbg%3D&md5=a0dd3afda2adf11ba580000a9c91fa73CAS |
Cox RD, Buckingham ME (1992) Actin and myosin genes are transcriptionally regulated during mouse skeletal muscle development. Developmental Biology 149, 228–234.
| Actin and myosin genes are transcriptionally regulated during mouse skeletal muscle development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xls1Wlsg%3D%3D&md5=00323929879d1ff318964dc248ddecb2CAS |
da Costa N, Blackley R, Alzuherri H, Chang KC (2002) Quantifying the temporospatial expression of postnatal porcine skeletal myosin heavy chain genes. The Journal of Histochemistry and Cytochemistry 50, 353–364.
| Quantifying the temporospatial expression of postnatal porcine skeletal myosin heavy chain genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvF2mtrs%3D&md5=b0477108e7d31334518da182fb5ce771CAS |
Essén-Gustavsson B, Henriksson J (1984) Enzyme levels in pools of microdissected human muscle fibres of identified type. Adaptive response to exercise. Acta Physiologica Scandinavica 120, 505–515.
| Enzyme levels in pools of microdissected human muscle fibres of identified type. Adaptive response to exercise.Crossref | GoogleScholarGoogle Scholar |
Field ML, Clark JF, Henderson C, Seymor AM, Radda GK (1994) Alterations in the myocardial creatine kinase system during chronic anaemic hypoxia. Cardiovascular Research 28, 86–91.
| Alterations in the myocardial creatine kinase system during chronic anaemic hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFGls7Y%3D&md5=c6ce0b9977ee5e0f91f641a3f6bae8eaCAS |
Fürst W, Hallström S (1992) Simultaneous determination of myocardial nucleotides, nucleosides, purine bases and creatine phosphate by ion pair high-performance liquid chromatography. Journal of Chromatography. A 578, 39–44.
| Simultaneous determination of myocardial nucleotides, nucleosides, purine bases and creatine phosphate by ion pair high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar |
Guo J, Shan T, Wu T, Zhu LN, Ren Y, An S, Wang Y (2011) Comparisons of different muscle metabolic enzymes and muscle fiber types in Jinhua and Landrace pigs. Journal of Animal Science 89, 185–191.
| Comparisons of different muscle metabolic enzymes and muscle fiber types in Jinhua and Landrace pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotl2ktQ%3D%3D&md5=e3507ecdfd3144868f6bf716f42a1b98CAS |
Hamilton DN, Ellis M, Hemann MD, McKeith FK, Miller KD, Purser KW (2002) The impact of longissimus glycolytic potential and short-term feeding of magnesium sulfate heptahydrate prior to slaughter on carcass characteristics and pork quality. Journal of Animal Science 80, 1586–1592.
Han JZ, Gu ZY, Wu JS, Chen QF (2007) Effects and mechanism: creatine monohydrate on carcass characteristics and meat quality of finishing swine. Journal of the Chinese Cereals and Oils Association 22, 101–106.
Henckel P, Karlsson A, Jensen MT, Oksbjerg N, Petersen JS (2002) Metabolic conditions in porcine longissimus muscle immediately pre-slaughter and its influence on peri- and postmortem energy metabolism. Meat Science 62, 145–155.
| Metabolic conditions in porcine longissimus muscle immediately pre-slaughter and its influence on peri- and postmortem energy metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1Ohu70%3D&md5=9a9927cb8254c64d88cc4e88ee5b5ca0CAS |
Hou MD, Zeng SY (2000) Biochemical methods to appraise meat quality. Food Science 21, 121–123.
Hu HM, Wang JY, Zhu RS, Guo JF, Wu Y (2008) Effect of myosin heavy chain composition of muscles on meat quality in Laiwu pigs and Duroc. Science in China. Series C, Life Sciences 51, 127–132.
| Effect of myosin heavy chain composition of muscles on meat quality in Laiwu pigs and Duroc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVylsbo%3D&md5=2c6fa378ec37b49d15f7c244b4d81026CAS |
Huan YJ, Zhou GH, Zhao GM, Xu XL, Peng ZQ (2005) Changes in flavor compounds of dry-cured Chinese Jinhua ham during processing. Meat Science 71, 291–299.
| Changes in flavor compounds of dry-cured Chinese Jinhua ham during processing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVCnsb0%3D&md5=5adc25652271cbda858aa4c628ae2127CAS |
Jankala H, Harjola VP, Petersen NE, Harkonen M (1997) Myosin heavy chain mRNA transform to faster isoforms in immobilized skeletal muscle: a quantitative PCR. Journal of Applied Physiology 82, 977–982.
Kim NK, Lim JH, Song MJ, Kim OH, Park BY, Kim MJ, Hwang IH, Lee CS (2008) Comparisons of longissimus muscle metabolic enzymes and muscle fiber types in Korean and western pig breeds. Meat Science 78, 455–460.
| Comparisons of longissimus muscle metabolic enzymes and muscle fiber types in Korean and western pig breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVClsbo%3D&md5=bb7f8d72c32aaba326d206382e79b860CAS |
Larzul C, Lefaucheur L, Ecolan P, Gogue J, Talmant A, Sellier P, Le Roy P, Monin G (1997) Phenotypic and genetic parameters for longissimus muscle fibre characteristics in relations to growth, carcass, and meat quality traits in large white pigs. Journal of Animal Science 75, 3126–3137.
Lefaucheur L (2010) A second look into fiber typing - relation to meat quality. Meat Science 84, 257–270.
| A second look into fiber typing - relation to meat quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGlt7bO&md5=bb8f86b1c0433194f1f9e5996b8a9bdaCAS |
Li L-A, Xia D, Bao E-D, Wei S, Xiao J, Bao J-W, Chen W-H, Chen J, Hartung J, Zhao R-Q (2008) Erhualian and Pertrain pigs exhibit distinct behavioral, endocrine and biochemical responses during transport. Livestock Science 113, 169–177.
| Erhualian and Pertrain pigs exhibit distinct behavioral, endocrine and biochemical responses during transport.Crossref | GoogleScholarGoogle Scholar |
Maddock RJ, Bindner BS, Carr SN, McKeith FK, Berg EP, Savell JW (2002) Creatine monohydrate supplementation and the quality of fresh pork in normal and halothane carrier pigs. Journal of Animal Science 80, 997–1004.
Men XM, Deng B, Xu ZW, Liu MH, Qi KK (2011) Characteristics of ATP-CP system status in postmortem muscle and their associations with pork quality traits. Scientia Agricultura Sinca 44, 1457–1465.
Miller KD, Ellis M, Bidner B, McKeith FK, Wilson ER (2000) Porcine longissimus glycolytic potential level effects on growth performance, carcass, and meat quality characteristic. Journal of Muscle Foods 11, 169–181.
| Porcine longissimus glycolytic potential level effects on growth performance, carcass, and meat quality characteristic.Crossref | GoogleScholarGoogle Scholar |
Monin G, Sellier P (1985) Pork of low technological quality with a normal rate of muscle pH fall in the immediate post-mortem period: the case of the Hampshire breed. Meat Science 13, 49–63.
| Pork of low technological quality with a normal rate of muscle pH fall in the immediate post-mortem period: the case of the Hampshire breed.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbmvFWjuw%3D%3D&md5=0bfa18029a9391d33aaf34f4e8f33b51CAS |
Monin G, Mejenes-Quijano A, Talmant A, Sellier P (1987) Influence of breed and muscle metabolic type on muscle glycolytic potential and meat pH in pigs. Meat Science 20, 149–158.
| Influence of breed and muscle metabolic type on muscle glycolytic potential and meat pH in pigs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbmvFGitg%3D%3D&md5=21dd9c5eb18c5bcd10bf9b7bece22dc7CAS |
O’Quinn PR, Andrews BS, Goodband RD, Unruh JA, Nelssen JL, Woodworth JC, Tokach MD, Owen KQ (2000) Effects of modified tall oil and creatine monohydrate on growth performance, carcass characteristics, and meat quality of growing-finishing pigs. Journal of Animal Science 78, 2376–2382.
Saks V, Kongas O, Vendelin M, Kay L (2000) Role of creatine/phosphocreatine system in the regulation of mitochondrial respiration. Acta Physiologica Scandinavica 168, 635–641.
| Role of creatine/phosphocreatine system in the regulation of mitochondrial respiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFKlsbg%3D&md5=e06b6f8034e6174de4df63b0a501c93cCAS |
Scheffler TL, Park S, Gerrard DE (2011) Lessons to learn about postmortem metabolism using the AMPKγ3R200Q mutation in the pig. Meat Science 89, 244–250.
| Lessons to learn about postmortem metabolism using the AMPKγ3R200Q mutation in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlagtLc%3D&md5=d6c5546a4c6d71aec18e871e70c643a7CAS |
Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiologica Scandinavica 178, 413–424.
| Molecular regulation of individual skeletal muscle fibre types.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1Crt7g%3D&md5=508432e2d721e560f6381f686068a179CAS |
Tanabe R, Muroya S, Chikuni K (1999) Expression of myosin heavy chain isoforms in porcine muscle determined by multiplex PCR. Journal of Food Science 64, 222–225.
| Expression of myosin heavy chain isoforms in porcine muscle determined by multiplex PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVSiurY%3D&md5=96fcb3782305f33179638a84c1c4aaf1CAS |
Tanabe R, Murakami T, Kawahara T, Yamashiro R, Mitsumoto M, Muroya S, Nakajima I, Chikuni K (2001) Composition of myosin heavy chain isoforms in relation to meat texture in Duro, Landrace and Meishan pigs. Journal of Animal Science 72, 230–237.
Vaarmann A, Fortin D, Veksler V, Momken I, Ventura-Clapier R, Garnier A (2008) Mitochondrial biogenesis in fast skeletal muscle of CK deficient mice. Biochimica et Biophysica Acta 1777, 39–47.
| Mitochondrial biogenesis in fast skeletal muscle of CK deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivFWrtQ%3D%3D&md5=2cc87d043932f6b4abd1f9541dd4dbb8CAS |
Van Daele DJ (2010) Quantitative PCR analysis of laryngeal muscle fiber types. Journal of Communication Disorders 43, 327–334.
| Quantitative PCR analysis of laryngeal muscle fiber types.Crossref | GoogleScholarGoogle Scholar |
Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of the creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine’ circuit for cellular energy homeostasis. The Biochemical Journal 281, 21–40.
Walsh B, Tonkonogi M, Söderlund K, Hultman E, Saks V, Sahlin K (2001) The role of phosphorylcreatine in the regulation of mitochondrial respiration in human skeletal muscle. The Journal of Physiology 537, 971–978.
| The role of phosphorylcreatine in the regulation of mitochondrial respiration in human skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVGktQ%3D%3D&md5=47367de9e699c05dd054300da4b23d5fCAS |
Zhou YM, Deng WB (2009) ‘SPSS 16.0 and statistical data analysis.’ (Southwest University of Finance and Press: Chengdu, China) [In Chinese]
Zhou GH, Zhao GM (2007) Biochemical changes during processing of traditional Jinhua ham. Meat Science 77, 114–120.
| Biochemical changes during processing of traditional Jinhua ham.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvVOgsbk%3D&md5=4da75f5bb6d49dd0ae5d885a2f56bc6bCAS |
Zierath JR, Hawley JA (2004) Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biology 2, e348
| Skeletal muscle fiber type: influence on contractile and metabolic properties.Crossref | GoogleScholarGoogle Scholar |