Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-18T06:05:24.109Z Has data issue: false hasContentIssue false

New insight of some extracellular matrix molecules in beef muscles. Relationships with sensory qualities

Published online by Cambridge University Press:  16 November 2015

A. Dubost
Affiliation:
Institut National de la Recherche Agronomique (INRA), UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France
D. Micol
Affiliation:
Institut National de la Recherche Agronomique (INRA), UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France
C. Lethias
Affiliation:
Institut de Biologie et Chimie des Protéines (IBCP), FRE 3310 DyHTIT, Passage du Vercors, 69367 Lyon, Cedex 07, France
A. Listrat*
Affiliation:
Institut National de la Recherche Agronomique (INRA), UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France
Get access

Abstract

The aim of this study was to highlight the relationships between decorin, tenascin-X and type XIV collagen, three minor molecules of extracellular matrix (ECM), with some structural parameters of connective tissue and its content in total collagen, its cross-links (CLs) and its proteoglycans (PGs). In addition, we have evaluated impact of these minor molecules on beef quality traits. The relative abundance of these molecules was evaluated by western blot analysis in Longissimus thoracis (LT) and Biceps femoris (BF) muscles from Aberdeen Angus and Blond d’Aquitaine beef breeds. Decorin and tenascin-X were more abundant in BF than in LT (1.8 v. 0.5 arbitrary units (AU), respectively, P<0.001, and 1.0 v. 0.6 AU, P<0.05). There was no muscle effect for collagen XIV content. Decorin and tenascin-X relative abundance were positively correlated with perimysium and endomysium areas and with collagen characteristics (total, insoluble and CLs). Decorin was negatively correlated with total PG content and positively with tenascin-X. Collagen XIV was correlated with any of parameters measured. To assess the impact of decorin, tenascin-X and collagen XIV and of their ratios to total collagen and PGs on shear force and quality traits we realized, respectively, a multiple-linear regression analysis and a Pearson’s correlation analysis. Decorin and tenascin-X relative abundance were, respectively, negatively and positively involved in juiciness. Decorin relative abundance was also negatively involved in abnormal flavour and positively in overall liking. The ratio of decorin to total collagen and PGs was negatively correlated to juiciness, together with collagen XIV ratio to total PGs. The ratios of decorin, tenascin-X and collagen XIV to total PGs were positively correlated to sensory tenderness, negatively to abnormal beef flavour and positively to overall liking. The ratio of decorin to total collagen was also negatively correlated to abnormal flavour and positively to overall liking while its ratio to total PGs was positively correlated to beef flavour and overall liking. Results of the present study highlighted for the first time the possible role of minor ECM molecules on beef quality traits. In addition, variations of meat texture and more generally of sensory qualities would depend not only to the quantity of total collagen and of its CLs, but also of components of ECM such as decorin, tenascin-X and collagen XIV and of their ratios to total collagen and PGs.

Type
Research Article
Copyright
© The Animal Consortium 2015 

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

Barbosa, I, Garcia, S, Barbier-Chassefiere, V, Caruelle, JP, Martelly, I and Papy-Garcia, D 2003. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 13, 647653.CrossRefGoogle ScholarPubMed
Bradford, MM 1976. A rapid and sensitive method for quantification of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Cuvelier, C, Cabaraux, JF, Dufrasne, I, Clinquart, A, Hocquette, JF, Istasse, L and Hornick, JL 2006. Performance, slaughter characteristics and meat quality of young bulls from Belgian Blue, Limousin and Aberdeen Angus breeds fattened with a sugar-beet pulp or a cereal-based diet. Animal Science 82, 125132.Google Scholar
Danielson, KG, Baribault, H, Holmes, DF, Graham, H, Kadler, KE and Iozzo, RV 1997. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. Journal of Cell Biology 136, 729743.CrossRefGoogle ScholarPubMed
Dourte, LM, Pathmanathan, L, Jawad, AF, Iozzo, RV, Mienaltowski, MJ, Birk, DE and Soslowsky, LJ 2012. Influence of decorin on the mechanical, compositional, and structural properties of the mouse patellar tendon. Journal of Biomechanical Engineering 134, 18.CrossRefGoogle ScholarPubMed
Dransfield, E, Martin, JF, Bauchart, D, Abouelkaram, S, Lepetit, J, Culioli, J, Jurie, C and Picard, B 2003. Meat quality and composition of three muscles from French cull cows and young bulls. Animal Science 76, 387399.Google Scholar
Dubost, A, Micol, D, Meunier, B, Lethias, C and Listrat, A 2013a. Relationships between structural characteristics of bovine intramuscular connective tissue assessed by image analysis and collagen and proteoglycan content. Meat Science 93, 378386.CrossRefGoogle ScholarPubMed
Dubost, A, Micol, D, Picard, B, Lethias, C, Andueza, D, Bauchart, D and Listrat, A 2013b. Structural and biochemical characteristics of bovine intramuscular connective tissue and beef quality. Meat Science 95, 555561.Google Scholar
Ehnis, T, Dieterich, W, Bauer, M, Kresse, H and Schuppan, D 1997. Localization of a binding site for the proteoglycan decorin on collagen XIV (undulin). Journal of Biological Chemistry 272, 2041420419.CrossRefGoogle ScholarPubMed
Elefteriou, F, Exposito, JY, Garrone, R and Lethias, C 2001. Binding of tenascin-X to decorin. FEBS Letters 495, 4447.CrossRefGoogle ScholarPubMed
Etherington, DJ and Sims, TJ 1981. Detection and estimation of collagen. Journal of the Science of Food and Agriculture 32, 539546.Google Scholar
Farndale, RW, Sayers, CA and Barrett, AJ 1982. A direct spectrophotometric micro-assay for sulfated glycoaminoglycans in cartilage cultures. Connective Tissue Research 9, 247248.Google Scholar
Flint, FO and Pickering, K 1984. Demonstration of collagen in meat-products by an improved picro-sirius red polarization method. Analyst 109, 15051506.CrossRefGoogle Scholar
Font, B, Aubertfoucher, E, Goldschmidt, D, Eichenberger, D and Van der Rest, M 1993. Binding of collagen XIV with the dermatan sulfate side-chain of decorin. Journal of Biological Chemistry 268, 2501525018.Google Scholar
Font, B, Eichenberger, D, Rosenberg, LM and Van der Rest, M 1996. Characterization of the interactions of type XII collagen with two small proteoglycans from fetal bovine tendon, decorin and fibromodulin. Matrix Biology 15, 341348.CrossRefGoogle ScholarPubMed
Hill, F 1966. The solubility of intramuscular collagen in meat animals of various ages. Journal of Food Science 31, 161166.CrossRefGoogle Scholar
Lepetit, J 2007. A theoretical approach of the relationships between collagen content, collagen cross-links and meat tenderness. Meat Science 76, 147159.CrossRefGoogle ScholarPubMed
Lethias, C, Carisey, A, Comte, J, Cluzel, C and Exposito, JY 2006. A model of tenascin-X integration within the collagenous network. FEBS Letters 580, 62816285.CrossRefGoogle Scholar
Lethias, C, Descollonges, Y, Garrone, R and Van Der Rest, M 1993. Expression of type XIV collagen during the differenciation of fetal bovine skin: immunolabelling with monoclonal antibody is prominent in morphogenetic areas. Journal of Investigative Dermatology 101, 9299.CrossRefGoogle Scholar
Lethias, C, Elefteriou, F, Parsiegla, G, Exposito, JY and Garrone, R 2001. Identification and characterization of a conformational heparin-binding site involving two fibronectin type III modules of bovine tenascin-X. Journal of Biological Chemistry 276, 1643216438.Google Scholar
Lewis, JL, Krawczak, DA, Oegema, TR Jr and Westendorf, JJ 2010. Effect of decorin and dermatan sulfate on the mechanical properties of a neocartilage. Connective Tissue Research 51, 159170.Google Scholar
Listrat, A and Hocquette, JF 2004. Analytical limits of total and insoluble collagen content measurements and of type I and III collagen analysis by electrophoresis in bovine muscles. Meat Science 68, 127136.Google Scholar
Listrat, A, Picard, B, Jailler, R, Collignon, H, Peccatte, JR, Micol, D, Geay, Y and Dozias, D 2001. Grass valorisation and muscular characteristics of blonde d’Aquitaine steers. Animal Research 50, 105118.Google Scholar
Listrat, A, Rakadjiyski, N, Jurie, C, Picard, B, Touraille, C and Geay, Y 1999. Effect of the type of diet on muscle characteristics and meat palatability of growing Salers bulls. Meat Science 53, 115124.CrossRefGoogle ScholarPubMed
Mao, JR, Taylor, G, Dean, WB, Wagner, DR, Afzal, V, Lotz, JC, Rubin, EM and Bristow, J 2002. Tenascin-X deficiency mimics Ehlers-Danlos syndrome in mice through alteration of collagen deposition. Nature Genetics 30, 421425.Google Scholar
Margaron, Y, Bostan, L, Exposito, JY, Malbouyres, M, Trunfio-Sfarghiu, AM, Berthier, Y and Lethias, C 2010. Tenascin-X increases the stiffness of collagen gels without affecting fibrillogenesis. Biophysical Chemistry 147, 8791.Google Scholar
Ngapo, TM, Berge, P, Culioli, J and De Smet, S 2002. Perimysial collagen crosslinking in Belgian Blue double-muscled cattle. Food Chemistry 77, 1526.Google Scholar
Nishimura, T 2010. The role of intramuscular connective tissue in meat texture. Animal Science Journal 81, 2127.Google Scholar
Nishiyama, T, McDonough, AM, Bruns, RR and Burgeson, RE 1994. Type XII and type XIV collagens mediate interactions between banded collagen fibers in vitro and may modulate extracellular matrix deformability. Journal of Biological Chemistry 269, 2819328199.CrossRefGoogle ScholarPubMed
Pearce, KL, Rosenvold, K, Andersen, HJ and Hopkins, DL 2011. Water distribution and mobility in meat during the conversion of muscle to meat and ageing and the impacts on fresh meat quality attributes – a review. Meat Science 89, 111124.CrossRefGoogle ScholarPubMed
Pedersen, ME, Kulseth, MA, Kolset, SO, Velleman, S and Eggen, KH 2001. Decorin and fibromodulin expression in two bovine muscles (M-semitendinosus and M-psoas major) differing in texture. Journal of Muscle Foods 12, 117.Google Scholar
Penisson-Besnier, I, Allamand, V, Beurrier, P, Martin, L, Schalkwijk, J, van Vlijmen-Willems, I, Gartioux, C, Malfait, F, Syx, D, Macchi, L, Marcorelles, P, Arbeille, B, Croue, A, De Paepe, A and Dubas, F 2013. Compound heterozygous mutations of the TNXB gene cause primary myopathy. Neuromuscular Disorders 23, 664669.CrossRefGoogle ScholarPubMed
Scott, JE 1992. Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB Journal 6, 26392645.CrossRefGoogle ScholarPubMed
Sifre, L, Berge, P, Engel, E, Martin, JF, Bonny, JM, Listrat, A, Taylor, R and Culioli, J 2005. Influence of the spatial organization of the perimysium on beef tenderness. Journal of Agricultural and Food Chemistry 53, 83908399.Google Scholar
Svensson, L, Heineg, D, Oldberg, A 1995. Decorin-binding sites for collagen type I are mainly located in leucine-rich repeats 4-5. Journal of Biological Chemistry 270, 2071220716.Google Scholar
Totland, GK and Kryvi, H 1991. Distribution patterns of muscle fibre types in major muscles of the bull (Bos taurus). Anatomy and Embryology 184, 441450.Google Scholar
Velleman, SG 2002. Role of the extracellular matrix in muscle growth and development. Journal of Animal Science 80, E8E13.Google Scholar
Voermans, NC, Altenburg, TM, Hamel, BC, de Haan, A and van Engelen, BG 2007. Reduced quantitative muscle function in tenascin-X deficient Ehlers-Danlos patients. Neuromuscular Disorders 17, 597602.CrossRefGoogle ScholarPubMed
Voermans, NC, van Alfen, N, Pillen, S, Lammens, M, Schalkwijk, J, Zwarts, MJ, van Rooij, IA, Hamel, BC and van Engelen, BG 2009. Neuromuscular involvement in various types of Ehlers-danlos syndrome. Annals of Neurology 65, 687697.Google Scholar
Voermans, NC, Verrijp, K, Eshuis, L, Balemans, MC, Egging, D, Sterrenburg, E, van Rooij, IA, van der Laak, JA, Schalkwijk, J, van der Maarel, SM, Lammens, M and van Engelen, BG 2011. Mild muscular features in tenascin-X knockout mice, a model of Ehlers-danlos syndrome. Connective Tissue Research 52, 422432.CrossRefGoogle Scholar
Weber, IT, Harrison, RW and Iozzo, RV 1996. Model structure of decorin and implications for collagen fibrillogenesis. Journal of Biological Chemistry 271, 3176731770.Google Scholar
Woessner, JF Jr 1961. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Archives of Biochemistry and Biophysics 93, 440447.Google Scholar