Single-nucleotide polymorphisms for matrix metalloprotease-1 can affect perimysial strength and intramuscular fat content but not growth rate of cattle
S. Christensen A B , C. Monteavaro B and P. P. Purslow B CA Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), CABA C1425FQB, Argentina.
B CIVETAN, CCT-CONICET, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil 7000, Argentina.
C Corresponding author. Email: ppurslow@gmail.com
Animal Production Science 60(16) 1869-1876 https://doi.org/10.1071/AN18789
Submitted: 31 January 2019 Accepted: 5 May 2020 Published: 16 June 2020
Abstract
Context: Single-nucleotide polymorphisms (SNPs) in the gene coding for matrix metalloprotease-1 (MMP-1) are known to affect the level of intramuscular fat found in cattle. As well as a signalling molecule affecting adipogenesis, MMP-1 is a major collagenase involved in the turnover of connective tissue.
Aims: The aim of the work was to assess whether SNPs in the gene for MMP-1 may affect the mechanical properties of intramuscular connective tissue, and therefore meat texture.
Methods: Allelic frequencies of three SNPs for MMP-1 were determined in a group of black Aberdeen Angus cattle whose growth characteristics had been traced for 450 days before slaughter. Associations between the alleles of each of the three SNPs and growth rate, killing out percentage, half-carcass weight, intramuscular fat content, cooking loss, strength of perimysium in cooked M. semitendinosus and Warner–Bratzler peak force of cooked M. longissimus dorsi were studied.
Key results: None of the SNPs studied had any effect on growth curves, and only one SNP (ss77831914) showed differences in half-carcass weight between alleles. Carcass yield and killing out percentage showed a small difference between alleles of ss7783924. No effects were found on the Warner–Bratzler peak force of M. longissimus dorsi cooked to 70°C. Two SNPs (ss77831914 and ss77831924) showed significant differences between alleles in the raw strength of perimysium in M. semitendinosus and the amount of intramuscular fat.
Conclusions: Commonly occurring SNPs of the major collagenase MMP-1 can affect the strength of intramuscular connective tissue as well as intramuscular fat content. Although these differences in connective tissue strength do not influence Warner–Bratzler measures of toughness at a cooking temperature of 70°C, they may contribute to differences in toughness in low-temperature, long-time cooking.
Implications: Because none of the SNPs had effects on the growth curves of the cattle studied, selection of animals with the relevant alleles of SNPs ss77831914 ss77831924 could be used to produce more tender meat without affecting carcass yield.
Additional keywords: adipogenesis, collagen, matrix metalloproteinases.
References
Albertí P, Panea B, Sañudo C, Olleta JL, Ripoll G, Ertbjerg P, Christensen M, Gigli S, Failla S, Concetti S, Hocquette JF (2008) Live weight, body size and carcass characteristics of young bulls of fifteen European breeds. Livestock Science 114, 19–30.| Live weight, body size and carcass characteristics of young bulls of fifteen European breeds.Crossref | GoogleScholarGoogle Scholar |
Andarawewa KL, Rio MC (2008). New insights into MMP function in adipogenesis. In ‘The cancer degradome’. (Eds D Edwards, G Hoyer-Hansen, F Blasi, BF Sloane) pp. 361–372. (Springer: New York)
Bauters D, Scroyen I, Van Hul M, Lijnen HR (2015) Gelatinase A (MMP-2) promotes murine adipogenesis. Biochimica et Biophysica Acta (BBA)-. General Subjects 1850, 1449–1456.
| Gelatinase A (MMP-2) promotes murine adipogenesis.Crossref | GoogleScholarGoogle Scholar |
Bruce HL, Aalhus JL (2017) Advances in the understanding and measurement of meat texture. In ‘New aspects of meat quality: from genes to ethics’. (Ed. PP Purslow) pp. 129–166. (Woodhead Publishing: Cambridge, MA, USA)
Buchanan FC, Fitzsimmons CJ, Van Kessel AG, Thue TD, Winkelman-Sim DC, Schmutz SM (2002) Association of missense in the bovine leptin gene with carcass fat content and leptin mRNA levels. Genetics, Selection, Evolution 34, 105–116.
| Association of missense in the bovine leptin gene with carcass fat content and leptin mRNA levels.Crossref | GoogleScholarGoogle Scholar | 11929627PubMed |
Bernard C, Cassar-Malek I, Le Cunff M, Dubroeucq H, Renand G, Hocquette JF (2007) New indicators of beef sensory quality revealed by expression of specific genes. Journal of Agricultural and Food Chemistry 55, 5229–5237.
| New indicators of beef sensory quality revealed by expression of specific genes.Crossref | GoogleScholarGoogle Scholar | 17547415PubMed |
Chen D, Li W, Du M, Cao B (2019) Adipogenesis, fibrogenesis and myogenesis related gene expression in longissimus muscle of high and low marbling beef cattle. Livestock Science 229, 188–193.
| Adipogenesis, fibrogenesis and myogenesis related gene expression in longissimus muscle of high and low marbling beef cattle.Crossref | GoogleScholarGoogle Scholar |
Christensen S, Purslow PP (2016) The role of matrix metalloproteinases in muscle and adipose tissue development and meat quality: a review. Meat Science 119, 138–146.
| The role of matrix metalloproteinases in muscle and adipose tissue development and meat quality: a review.Crossref | GoogleScholarGoogle Scholar | 27180222PubMed |
Christensen M, Purslow PP, Larsen LM (2000) The effect of cooking temperature on mechanical properties of whole meat, single muscle fibres and perimysial connective tissue. Meat Science 55, 301–307.
| The effect of cooking temperature on mechanical properties of whole meat, single muscle fibres and perimysial connective tissue.Crossref | GoogleScholarGoogle Scholar | 22061287PubMed |
Christensen M, Ertbjerg P, Failla S, Sañudo C, Richardson RI, Nute GR, Olleta JL, Panea B, Albertí P, Juárez M, Hocquette JF (2011) Relationship between collagen characteristics, lipid content and raw and cooked texture of meat from young bulls of fifteen European breeds. Meat Science 87, 61–65.
| Relationship between collagen characteristics, lipid content and raw and cooked texture of meat from young bulls of fifteen European breeds.Crossref | GoogleScholarGoogle Scholar | 20870360PubMed |
Collins A, Ke X (2012) Primer1: primer design Web service for Tetra-Primer ARMS-PCR. The Open Bioinformatics Journal 6, 55–58.
| Primer1: primer design Web service for Tetra-Primer ARMS-PCR.Crossref | GoogleScholarGoogle Scholar |
Davey CL, Gilbert KV (1974) Temperature‐dependent cooking toughness in beef. Journal of the Science of Food and Agriculture 25, 931–938.
| Temperature‐dependent cooking toughness in beef.Crossref | GoogleScholarGoogle Scholar |
Dominguez-Hernandez E, Salaseviciene A, Ertbjerg P (2018) Low-temperature long-time cooking of meat: Eating quality and underlying mechanisms. Meat Science 143, 104–113.
| Low-temperature long-time cooking of meat: Eating quality and underlying mechanisms.Crossref | GoogleScholarGoogle Scholar | 29730528PubMed |
Dunner S, Sevane N, Garcia D, O’Cortés A, Valentini A, Williams JL, Mangin B, Cañón J, Leveziel H,, GeMQual Consortium (2013a) Association of genes involved in carcass and meat quality traits in 15 European bovine breeds. Livestock Science 154, 34–44.
| Association of genes involved in carcass and meat quality traits in 15 European bovine breeds.Crossref | GoogleScholarGoogle Scholar |
Dunner S, Sevane N, Garcia D, Leveziel H, Williams JL, Mangin B, Valentini A,, GemQual Consortium (2013b) Genes involved in muscle lipid composition in 15 European Bos taurus breeds. Animal Genetics 44, 493–501.
| Genes involved in muscle lipid composition in 15 European Bos taurus breeds.Crossref | GoogleScholarGoogle Scholar | 23611291PubMed |
Gotoh T, Takahashi H, Nishimura T, Kuchida K, Mannen H (2014) Meat produced by Japanese Black cattle and Wagyu. Animal Frontiers 4, 46–54.
| Meat produced by Japanese Black cattle and Wagyu.Crossref | GoogleScholarGoogle Scholar |
Harris PV, Shorthose WR (1988) Meat texture. In ‘Developments in meat science. Vol. 4’. (Ed. RA Lawrie) pp. 45–286. (Elsevier Applied Science Publishers: London)
King DA, Wheeler TL, Shackelford SD, Koohmaraie M (2009) Comparison of palatability characteristics of beef gluteus medius and triceps brachii muscles. Journal of Animal Science 87, 275–284.
| Comparison of palatability characteristics of beef gluteus medius and triceps brachii muscles.Crossref | GoogleScholarGoogle Scholar | 18791153PubMed |
Latorre ME, Velázquez DE, Purslow PP (2018) The thermal shrinkage force in perimysium from different beef muscles is not affected by post-mortem ageing. Meat Science 135, 109–114.
| The thermal shrinkage force in perimysium from different beef muscles is not affected by post-mortem ageing.Crossref | GoogleScholarGoogle Scholar | 28968553PubMed |
Lewis GJ, Purslow PP (1989) The strength and stiffness of perimysial connective tissue isolated from cooked beef muscle. Meat Science 26, 255–269.
| The strength and stiffness of perimysial connective tissue isolated from cooked beef muscle.Crossref | GoogleScholarGoogle Scholar | 22055022PubMed |
Lewis GJ, Purslow PP, Rice AE (1991) The effect of conditioning on the strength of perimysial connective tissue dissected from cooked meat. Meat Science 30, 1–12.
| The effect of conditioning on the strength of perimysial connective tissue dissected from cooked meat.Crossref | GoogleScholarGoogle Scholar | 22061646PubMed |
Little S (2001) Amplification‐refractory mutation system (ARMS) analysis of point mutations. Current Protocols in Human Genetics 7, 9.8.1–9.8.12.
Magalhães AF, de Camargo GM, Junior GAF, Gordo DG, Tonussi RL, Costa RB, Espigolan R, Rafael MDO, Bresolin T, de Andrade WB, Takada L (2016) Genome-wide association study of meat quality traits in Nellore cattle. PLoS One 11, e0157845
| Genome-wide association study of meat quality traits in Nellore cattle.Crossref | GoogleScholarGoogle Scholar | 27494397PubMed |
McCormick RJ (1994) The flexibility of the collagen compartment of muscle. Meat Science 36, 79–91.
| The flexibility of the collagen compartment of muscle.Crossref | GoogleScholarGoogle Scholar | 22061454PubMed |
Meissburger B, Stachorski L, Roder E, Rudolfsky G, Wolfrum C (2011) Tissue inhibitor of matrix metalloproteinase 1 (TIMPS1) controls adipogenesis in obesity in mice and in humans. Diabetologia 54, 1468–1479.
| Tissue inhibitor of matrix metalloproteinase 1 (TIMPS1) controls adipogenesis in obesity in mice and in humans.Crossref | GoogleScholarGoogle Scholar | 21437772PubMed |
Miao ZG, Zhang LP, Yu X, Yang QY, Zhu MJ, Dodson MV, Du M (2016) Invited review: mesenchymal progenitor cells in intramuscular connective tissue development animal. Animal 10, 75–81.
| Invited review: mesenchymal progenitor cells in intramuscular connective tissue development animal.Crossref | GoogleScholarGoogle Scholar | 26350682PubMed |
Nishimura T (2010) The role of intramuscular connective tissue in meat texture. Animal Science Journal 81, 21–27.
| The role of intramuscular connective tissue in meat texture.Crossref | GoogleScholarGoogle Scholar | 20163668PubMed |
Nishimura T (2015) Role of extracellular matrix in development of skeletal muscle and postmortem aging of meat. Meat Science 109, 48–55.
| Role of extracellular matrix in development of skeletal muscle and postmortem aging of meat.Crossref | GoogleScholarGoogle Scholar | 26141816PubMed |
Purslow PP (2014) New developments on the role of intramuscular connective tissue in meat toughness. Annual Review of Food Science and Technology 5, 133–153.
| New developments on the role of intramuscular connective tissue in meat toughness.Crossref | GoogleScholarGoogle Scholar | 24437687PubMed |
Purslow PP, Oiseth S, Hughes J, Warner RD (2016) The structural basis of cooking loss in beef: variations with temperature and ageing. Food Research International 89, 739–748.
| The structural basis of cooking loss in beef: variations with temperature and ageing.Crossref | GoogleScholarGoogle Scholar | 28460973PubMed |
Purslow PP (2018) Contribution of collagen and connective tissue to cooked meat toughness; some paradigms reviewed. Meat Science 144, 127–134.
| Contribution of collagen and connective tissue to cooked meat toughness; some paradigms reviewed.Crossref | GoogleScholarGoogle Scholar | 29636208PubMed |
Sandrin A, Beakou A, Favier R, Lepetit J (2004) Modeling changes with ageing in the mechanical properties of beef connective tissue. In ‘Proceedings 50th International Congress of Meat Science and Technology’. (DigICoMST: Helsinki, Finland) Available at http://icomst-proceedings.helsinki.fi/papers/2004_01_55.pdf (Verified 27 May 2020)
Santiago GG, Siqueira F, Cardoso FF, Regitano LCA, Ventura R, Sollero BP, Sollero BP, Souza MD, Mokry FB, Ferreira ABR, Torres RAA (2017) Genomewide association study for production and meat quality traits in Canchim beef cattle. Journal of Animal Science 95, 3381–3390.
| Genomewide association study for production and meat quality traits in Canchim beef cattle.Crossref | GoogleScholarGoogle Scholar | 28805909PubMed |
Schenkel FS, Miller SP, Jiang Z, Mandell IB, Ye X, Li H, Wilton JW (2006) Association of a single nucleotide polymorphism in the calpastatin gene with carcass and meat quality traits of beef cattle. Journal of Animal Science 84, 291–299.
| Association of a single nucleotide polymorphism in the calpastatin gene with carcass and meat quality traits of beef cattle.Crossref | GoogleScholarGoogle Scholar | 16424255PubMed |
Sevane N, Leveziel H, Nute RG, Sañudo C, Valentini A, Williams JL, Dunner S, GemQual Consortium (2014) Phenotypic and genotypic background underlying variations in fatty acids compositions and sensory parameters in European bovine breeds. Journal of Animal Science and Biotechnology 5, 20
| Phenotypic and genotypic background underlying variations in fatty acids compositions and sensory parameters in European bovine breeds.Crossref | GoogleScholarGoogle Scholar | 24735897PubMed |
Shackelford SD, Wheeler TL, Koohmaraie M (1995) Relationship between shear force and trained sensory panel tenderness ratings of 10 major muscles from Bos indicus and Bos taurus cattle. Journal of Animal Science 73, 3333–3340.
| Relationship between shear force and trained sensory panel tenderness ratings of 10 major muscles from Bos indicus and Bos taurus cattle.Crossref | GoogleScholarGoogle Scholar | 8586592PubMed |
Shiomi T, Lemaître V, D’Armiento J, Okada Y (2010) Matrix metalloproteinases, a disintegrin and metalloproteinases, and a disintegrin and metalloproteinases with thrombospondin motifs in non‐neoplastic diseases. Pathology International 60, 477–496.
| Matrix metalloproteinases, a disintegrin and metalloproteinases, and a disintegrin and metalloproteinases with thrombospondin motifs in non‐neoplastic diseases.Crossref | GoogleScholarGoogle Scholar | 20594269PubMed |
Taylor RG (2004) Connective tissue structure, function and influence on meat quality. In ‘Encyclopedia of meat sciences’. (Ed. WK Jensen) pp. 306–13. (Elsevier: Amsterdam)
Tornberg EVA (2005) Effects of heat on meat proteins–Implications on structure and quality of meat products. Meat Science 70, 493–508.
| Effects of heat on meat proteins–Implications on structure and quality of meat products.Crossref | GoogleScholarGoogle Scholar |
Uezumi A, Ito T, Morikawa D, Shimizu N, Yoneda T, Segawa M, Yamaguchi M, Ogawa R, Matev MM, Miyagoe-Suzuki Y (2011) Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle. Journal of Cell Science 124, 3654–3664.
| Fibrosis and adipogenesis originate from a common mesenchymal progenitor in skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 22045730PubMed |
Williams JL, Dunner S, Valentini A, Mazza R, Amarger V, Checa ML, Crisa A, Razzaq N, Delourme D, Grandjean F, Marchitelli C (2009) Discovery, characterization and validation of single nucleotide polymorphisms within 206 bovine genes that may be considered as candidate genes for beef production and quality. Animal Genetics 40, 486–491.
| Discovery, characterization and validation of single nucleotide polymorphisms within 206 bovine genes that may be considered as candidate genes for beef production and quality.Crossref | GoogleScholarGoogle Scholar | 19397516PubMed |