Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Proteomic Assessment of the Relevant Factors Affecting Pork Meat Quality Associated with Longissimus dorsi Muscles in Duroc Pigs

  • Cho, Jin Hyoung (Department of Dental Pharmacology, School of Dentistry and Institute of Dental Bioscience, BK21 plus, Chonbuk National University) ;
  • Lee, Ra Ham (Department of Dental Pharmacology, School of Dentistry and Institute of Dental Bioscience, BK21 plus, Chonbuk National University) ;
  • Jeon, Young-Joo (Department of Dental Pharmacology, School of Dentistry and Institute of Dental Bioscience, BK21 plus, Chonbuk National University) ;
  • Park, Seon-Min (Pohang Center for Evaluation of Biomaterials) ;
  • Shin, Jae-Cheon (Pohang Center for Evaluation of Biomaterials) ;
  • Kim, Seok-Ho (Aging Research Institute, Korea Research Institute of Bioscience & BioTechnology) ;
  • Jeong, Jin Young (Division of Animal Genomics and Bioinformatics, National Institute of Animal science, Rural Development Administration) ;
  • Kang, Hyun-sung (Department of Animal Science and Technology, Sunchon National University) ;
  • Choi, Nag-Jin (Department of Animal Science, College of Agricultural and Life Science, Chonbuk National University) ;
  • Seo, Kang Seok (Department of Animal Science and Technology, Sunchon National University) ;
  • Cho, Young Sik (Department of Pharmacy, Keimyung University) ;
  • Kim, MinSeok S. (Department of Biomedical Engineering, Konyang University) ;
  • Ko, Sungho (Department of Applied Bioscience, CHA University) ;
  • Seo, Jae-Min (Department of Prosthodontics, School of Dentistry and Institute of Oral Bio-Science and Research Institute of Clinical Medicine, Chonbuk National University) ;
  • Lee, Seung-Youp (Cluster for Craniofacial Development and Regeneration Research, Institute of Oral Biosciences and School of Dentistry, Chonbuk National University) ;
  • Shim, Jung-Hyun (Department of Pharmacy, College of Pharmacy and Natural Medicine Research Institute, Mokpo National University) ;
  • Chae, Jung-Il (Department of Dental Pharmacology, School of Dentistry and Institute of Dental Bioscience, BK21 plus, Chonbuk National University)
  • Received : 2016.01.19
  • Accepted : 2016.03.29
  • Published : 2016.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

Meat quality is a complex trait influenced by many factors, including genetics, nutrition, feeding environment, animal handling, and their interactions. To elucidate relevant factors affecting pork quality associated with oxidative stress and muscle development, we analyzed protein expression in high quality longissimus dorsi muscles (HQLD) and low quality longissimus dorsi muscles (LQLD) from Duroc pigs by liquid chromatography-tandem mass spectrometry (LC-MS/MS)-based proteomic analysis. Between HQLD (n = 20) and LQLD (n = 20) Duroc pigs, 24 differentially expressed proteins were identified by LC-MS/MS. A total of 10 and 14 proteins were highly expressed in HQLD and LQLD, respectively. The 24 proteins have putative functions in the following seven categories: catalytic activity (31%), ATPase activity (19%), oxidoreductase activity (13%), cytoskeletal protein binding (13%), actin binding (12%), calcium ion binding (6%), and structural constituent of muscle (6%). Silver-stained image analysis revealed significant differential expression of lactate dehydrogenase A (LDHA) between HQLD and LQLD Duroc pigs. LDHA was subjected to in vitro study of myogenesis under oxidative stress conditions and LDH activity assay to verification its role in oxidative stress. No significant difference of mRNA expression level of LDHA was found between normal and oxidative stress condition. However, LDH activity was significantly higher under oxidative stress condition than at normal condition using in vitro model of myogenesis. The highly expressed LDHA was positively correlated with LQLD. Moreover, LDHA activity increased by oxidative stress was reduced by antioxidant resveratrol. This paper emphasizes the importance of differential expression patterns of proteins and their interaction for the development of meat quality traits. Our proteome data provides valuable information on important factors which might aid in the regulation of muscle development and the improvement of meat quality in longissimus dorsi muscles of Duroc pigs under oxidative stress conditions.

Keywords

References

  1. Bendixen, E. 2005. The use of proteomics in meat science. Meat Sci. 71:138-149. https://doi.org/10.1016/j.meatsci.2005.03.013
  2. Bouzid, M. A., O. Hammouda, R. Matran, S. Robin, and C. Fabre. 2014. Changes in oxidative stress markers and biological markers of muscle injury with aging at rest and in response to an exhaustive exercise. PLoS One 9:e90420. https://doi.org/10.1371/journal.pone.0090420
  3. Brocks, L., B. Hulsegge, and G. Merkus. 1998. Histochemical characteristics in relation to meat quality properties in the Longissimus Lumborum of fast and lean growing lines of Large White pigs. Meat Sci. 50:411-420. https://doi.org/10.1016/S0309-1740(98)00053-9
  4. Fan, J., T. Hitosugi, T. W. Chung, J. Xie, Q. Ge, T. L. Gu, R. D. Polakiewicz, G. Z. Chen, T. J. Boggon, S. Lonial, F. R. Khuri, S. Kang, and J. Chen. 2011. Tyrosine phosphorylation of lactate dehydrogenase A is important for NADH/NAD(+) redox homeostasis in cancer cells. Mol. Cell. Biol. 31:4938-4950. https://doi.org/10.1128/MCB.06120-11
  5. Frisby, J., D. Raftery, J. P. Kerry, and D. Diamond. 2005. Development of an autonomous, wireless pH and temperature sensing system for monitoring pig meat quality. Meat Sci. 70:329-336. https://doi.org/10.1016/j.meatsci.2005.01.023
  6. Gramolini, A. O. and B. J. Jasmin. 1999. Expression of the utrophin gene during myogenic differentiation. Nucleic Acids Res. 27:3603-3609. https://doi.org/10.1093/nar/27.17.3603
  7. Guo, K., J. Wang, V. Andres, R. C. Smith, and K. Walsh. 1995. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol. Cell. Biol. 15:3823-3829. https://doi.org/10.1128/MCB.15.7.3823
  8. Gurnett, C. A., D. M. Desruisseau, K. McCall, R. Choi, Z. I. Meyer, M. Talerico, S. E. Miller, J. S. Ju, A. Pestronk, A. M. Connolly, T. E. Druley, C. C. Weihl, and M. B. Dobbs. 2010. Myosin binding protein C1: a novel gene for autosomal dominant distal arthrogryposis type 1. Hum. Mol. Genet. 19:1165-1173. https://doi.org/10.1093/hmg/ddp587
  9. Halevy, O., B. G. Novitch, D. B. Spicer, S. X. Skapek, J. Rhee, G. J. Hannon, D. Beach, and A. B. Lassar. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267:1018-1021. https://doi.org/10.1126/science.7863327
  10. Hollung, K., E. Veiseth, X. Jia, E. M. Faergestad, and K. I. Hildrum. 2007. Application of proteomics to understand the molecular mechanisms behind meat quality. Meat Sci. 77:97-104. https://doi.org/10.1016/j.meatsci.2007.03.018
  11. Hwang, I. H., B. Y. Park, J. H. Kim, S. H. Cho, and J. M. Lee. 2005. Assessment of postmortem proteolysis by gel-based proteome analysis and its relationship to meat quality traits in pig longissimus. Meat Sci. 69:79-91. https://doi.org/10.1016/j.meatsci.2004.06.019
  12. Jia, X., K. Hollung, M. Therkildsen, K. I. Hildrum, and E. Bendixen. 2006. Proteome analysis of early post-mortem changes in two bovine muscle types: M. longissimus dorsi and M. semitendinosis. Proteomics 6:936-944. https://doi.org/10.1002/pmic.200500249
  13. Julve, J., J. C. Escola-Gil, A. Marzal-Casacuberta, J. Ordonez-Llanos, F. Gonzalez-Sastre, and F. Blanco-Vaca. 2000. Increased production of very-low-density lipoproteins in transgenic mice overexpressing human apolipoprotein A-II and fed with a high-fat diet. Biochim. Biophys. Acta 1488:233-244. https://doi.org/10.1016/S1388-1981(00)00127-X
  14. Kanter, M. M., G. R. Lesmes, L. A. Kaminsky, J. La Ham-Saeger, and N. D. Nequin. 1988. Serum creatine kinase and lactate dehydrogenase changes following an eighty kilometer race. Relationship to lipid peroxidation. Eur. J. Appl. Physiol. Occup. Physiol. 57:60-63. https://doi.org/10.1007/BF00691239
  15. Kislinger, T., A. O. Gramolini, Y. Pan, K. Rahman, D. H. MacLennan, and A. Emili. 2005. Proteome dynamics during C2C12 myoblast differentiation. Mol. Cell. Proteomics 4:887-901. https://doi.org/10.1074/mcp.M400182-MCP200
  16. Lametsch, R. and E. Bendixen. 2001. Proteome analysis applied to meat science: characterizing postmortem changes in porcine muscle. J. Agric. Food Chem. 49:4531-4537. https://doi.org/10.1021/jf010103g
  17. Lametsch, R., P. Roepstorff, and E. Bendixen. 2002. Identification of protein degradation during post-mortem storage of pig meat. J. Agric. Food Chem. 50:5508-5512. https://doi.org/10.1021/jf025555n
  18. Langen, R. C., J. L. Van Der Velden, A. M. Schols, M. C. Kelders, E. F. Wouters, and Y. M. Janssen-Heininger. 2004. Tumor necrosis factor-alpha inhibits myogenic differentiation through MyoD protein destabilization. FASEB J. 18:227-237. https://doi.org/10.1096/fj.03-0251com
  19. Lee, E. J., A. Malik, S. Pokharel, S. Ahmad, B. A. Mir, K. H. Cho, J. Kim, J. C. Kong, D. M. Lee, K. Y. Chung, S. H. Kim, and I. Choi. 2014. Identification of genes differentially expressed in myogenin knock-down bovine muscle satellite cells during differentiation through RNA sequencing analysis. PLoS ONE 9:e92447. https://doi.org/10.1371/journal.pone.0092447
  20. Liu, Q. C., X. H. Zha, H. Faralli, H. Yin, C. Louis-Jeune, E. Perdiguero, E. Pranckeviciene, P. Munoz-Canoves, M. A. Rudnicki, M. Brand, C. Perez-Iratxeta, and F. J. Dilworth. 2012. Comparative expression profiling identifies differential roles for Myogenin and p38alpha MAPK signaling in myogenesis. J. Mol. Cell Biol. 4:386-397. https://doi.org/10.1093/jmcb/mjs045
  21. Monin, G., E. Lambooy, and R. Klont. 1995. Influence of temperature variation on the metabolism of pig muscle in situ and after excision. Meat Sci. 40:149-158. https://doi.org/10.1016/0309-1740(94)00044-8
  22. Montesano, A., L. Luzi, P. Senesi, N. Mazzocchi, and I. Terruzzi. 2013. Resveratrol promotes myogenesis and hypertrophy in murine myoblasts. J. Transl. Med. 11:310. https://doi.org/10.1186/1479-5876-11-310
  23. Morzel, M., C. Chambon, M. Hamelin, V. Sante-Lhoutellier, T. Sayd, and G. Monin. 2004. Proteome changes during pork meat ageing following use of two different pre-slaughter handling procedures. Meat Sci. 67:689-696. https://doi.org/10.1016/j.meatsci.2004.01.008
  24. Mullen, A. M., P. C. Stapleton, D. Corcoran, R. M. Hamill, and A. White. 2006. Understanding meat quality through the application of genomic and proteomic approaches. Meat Sci. 74:3-16. https://doi.org/10.1016/j.meatsci.2006.04.015
  25. Pette, D. 2002. The adaptive potential of skeletal muscle fibers. Can. J. Appl. Physiol. 27:423-448. https://doi.org/10.1139/h02-023
  26. Picard, B., C. Berri, L. Lefaucheur, C. Molette, T. Sayd, and C. Terlouw. 2010. Skeletal muscle proteomics in livestock production. Brief. Funct. Genomics 9:259-278. https://doi.org/10.1093/bfgp/elq005
  27. Qiu, H., X. Xu, B. Fan, M. F. Rothschild, Y. Martin, and B. Liu. 2010. Investigation of LDHA and COPB1 as candidate genes for muscle development in the MYOD1 region of pig chromosome 2. Mol. Biol. Rep. 37:629-636. https://doi.org/10.1007/s11033-009-9882-y
  28. Sayd, T., M. Morzel, C. Chambon, M. Franck, P. Figwer, C. Larzul, P. Le Roy, G. Monin, P. Cherel, and E. Laville. 2006. Proteome analysis of the sarcoplasmic fraction of pig semimembranosus muscle: implications on meat color development. J. Agric. Food Chem. 54:2732-2737. https://doi.org/10.1021/jf052569v
  29. Spangenburg, E. E. and F. W. Booth. 2003. Molecular regulation of individual skeletal muscle fibre types. Acta Physiol. Scand. 178:413-424. https://doi.org/10.1046/j.1365-201X.2003.01158.x
  30. Stentz, R., R. J. Bongaerts, A. P. Gunning, M. Gasson, and C. Shearman. 2010. Controlled release of protein from viable Lactococcus lactis cells. Appl. Environ. Microbiol. 76:3026-3031. https://doi.org/10.1128/AEM.00021-10
  31. Wheeler, T. L., L. V. Cundiff, S. D. Shackelford, and M. Koohmaraie. 2005. Characterization of biological types of cattle (Cycle VII): Carcass, yield, and longissimus palatability traits. J. Anim. Sci. 83:196-207. https://doi.org/10.2527/2005.831196x
  32. Wu, R. E., W. C. Huang, C. C. Liao, Y. K. Chang, N. W. Kan, and C. C. Huang. 2013. Resveratrol protects against physical fatigue and improves exercise performance in mice. Molecules 18:4689-4702. https://doi.org/10.3390/molecules18044689
  33. Yan, J. X., R. Wait, T. Berkelman, R. A. Harry, J. A. Westbrook, C. H. Wheeler, and M. J. Dunn. 2000. A modified silver staining protocol for visualization of proteins compatible with matrixassisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21:3666-3672. https://doi.org/10.1002/1522-2683(200011)21:17<3666::AID-ELPS3666>3.0.CO;2-6
  34. Zuo, X., L. Echan, P. Hembach, H. Y. Tang, K. D. Speicher, D. Santoli, and D. W. Speicher. 2001. Towards global analysis of mammalian proteomes using sample prefractionation prior to narrow pH range two-dimensional gels and using onedimensional gels for insoluble and large proteins. Electrophoresis 22:1603-1615. https://doi.org/10.1002/1522-2683(200105)22:9<1603::AID-ELPS1603>3.0.CO;2-I

Cited by

  1. Contribution of Early-Postmortem Proteome and Metabolome to Ultimate pH and Pork Quality vol.5, pp.1, 2016, https://doi.org/10.22175/mmb.11709
  2. Effect of Knotweed in Diet on Physiological Changes in Pig vol.11, pp.2, 2016, https://doi.org/10.3390/agriculture11020169