Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-26T18:41:41.429Z Has data issue: false hasContentIssue false
  • English
  • Français

Are there consistent relationships between major connective tissue components, intramuscular fat content and muscle fibre types in cattle muscle?

Published online by Cambridge University Press:  16 January 2020

A. Listrat Open the ORCID record for A. Listrat [Opens in a new window] ,
M. Gagaoua Open the ORCID record for M. Gagaoua [Opens in a new window] ,
J. Normand Open the ORCID record for J. Normand [Opens in a new window] ,
D. J. Andueza ,
D. Gruffat Open the ORCID record for D. Gruffat [Opens in a new window] ,
G. Mairesse ,
G. Chesneau ,
B.-P. Mourot ,
C. Gobert  and
B. Picard Open the ORCID record for B. Picard [Opens in a new window]
A. Listrat*
Affiliation:
Université Clermont Auvergne, INRAe, VetAgro Sup, 1213 UMR Herbivores, F-63122Saint-Genès-Champanelle, France
M. Gagaoua
Affiliation:
Université Clermont Auvergne, INRAe, VetAgro Sup, 1213 UMR Herbivores, F-63122Saint-Genès-Champanelle, France Food Quality and Sensory Science Department, Teagasc Ashtown Food Research Centre, Ashtown, Dublin 15, Ireland
J. Normand
Affiliation:
Institut de l’Elevage, Service Qualité des Viandes, 23 Rue Jean Baldassini, F-69007Lyon, France
D. J. Andueza
Affiliation:
Université Clermont Auvergne, INRAe, VetAgro Sup, 1213 UMR Herbivores, F-63122Saint-Genès-Champanelle, France
D. Gruffat
Affiliation:
Université Clermont Auvergne, INRAe, VetAgro Sup, 1213 UMR Herbivores, F-63122Saint-Genès-Champanelle, France
G. Mairesse
Affiliation:
Valorex, La Messayais, F-35210Combourtillé, France
G. Chesneau
Affiliation:
Valorex, La Messayais, F-35210Combourtillé, France
B.-P. Mourot
Affiliation:
Valorex, La Messayais, F-35210Combourtillé, France
C. Gobert
Affiliation:
Elivia, Le Lion d’Angers, ZI La Coudère, F-49220Le Lion-d’Angers, France
B. Picard
Affiliation:
Université Clermont Auvergne, INRAe, VetAgro Sup, 1213 UMR Herbivores, F-63122Saint-Genès-Champanelle, France
*
†E-mail: anne.listrat@inrae.fr
Get access

Abstract

Intramuscular connective tissue (IMCT) is mainly composed of several fibrils (known as total collagen (TCol)) linked between each other by different chemical cross-links (CLs), the whole being embedded in a matrix of proteoglycans (PGs). In the field of beef quality, there is limited information on the role of CLs and PGs. Accordingly, several authors suggest that, to investigate the role of IMCT, it is important to investigate them just like TCol and insoluble collagen (ICol). In muscle, there are two other components, the muscle fibres and intramuscular fat (IMF) content. There are limited data on the relationships between these three components of muscle and then on possibility to independently manipulate these characteristics in order to control the final quality of meat. The present study aimed to investigate whether consistent relationships exist between these different components of muscle. Therefore, the present study compared four muscles of two cattle types (dairy and beef) to determine associations between TCol, ICol, CLs and PGs. Data were analysed across and within muscle (M) and animal type (AT) based on residuals. There was a strong M and AT effect for all muscle characteristics and an interaction M × AT for type I muscle fibres and IMF. Correlations between TCol, ICol and their CLs were M- and AT-independent. Total proteoglycans were positively correlated with TCol and ICol in a muscle-dependent manner irrespective of AT, but no correlation was found with CLs. On the contrary, CLs were negatively correlated with the ratio TPGs : TCol in an M-dependent manner, irrespective of AT. TCol, ICol and CLs were positively and negatively correlated with type IIA and IIB+X muscle fibres only in longissimus thoracis (LT) muscle, regardless the AT. Insoluble collagen was the only parameter of IMCT to be correlated with type I muscle fibres but only in LT muscle, irrespective of AT. There was no correlation between PGs and muscle fibre types, but PGs were the only IMCT component to be related with IMF in an M-dependent manner, irrespective of AT. Finally, there was no correlation between muscle fibre types and IMF content within M and AT. This study revealed that there is a strong relationship between IMCT components irrespective of M, an M-dependent relationship between the IMCT components and muscle fibre types and few (only with PGs) or no relationship between IMF and IMCT and muscle fibres.

Keywords

beefdairycollagencross-linksproteoglycans
Type
Research Article
Information
animal , Volume 14 , Issue 6 , June 2020 , pp. 1204 - 1212
Copyright
© The Animal Consortium 2020

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.)

Footnotes

*

These two authors contributed equally to this work.

References

Andueza, D, Listrat, A, Durand, D, Normand, J, Mourot, BP and Gruffat, D 2019. Prediction of beef meat fatty acid composition by visible-near-infrared spectroscopy was improved by preliminary freeze-drying. Meat Science 158, 107910.CrossRefGoogle ScholarPubMed
Bailey, AJ and Light, ND 1989. Connective tissue in meat and meat products. Elsevier Science (London, England and New-York, USA).Google Scholar
Christensen, M, Ertbjerg, P, Failla, S, Sanudo, C, Richardson, RI, Nute, GR, Olleta, JL, Panea, B, Alberti, P, Juarez, M, Hocquette, JF and Williams, JL 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.CrossRefGoogle ScholarPubMed
Cristancho, AG and Lazar, MA 2011. Forming functional fat: a growing understanding of adipocyte differentiation. Nature Reviews Molecular Cell Biology 12, 722–734.CrossRefGoogle ScholarPubMed
Depalle, B, Qin, Z, Shefelbine, SJ and Buehler, MJ 2015. Influence of cross-link structure, density and mechanical properties in the mesoscale deformation mechanisms of collagen fibrils. Journal of the Mechanical Behavior of Biomedical Materials 52, 1–13.CrossRefGoogle ScholarPubMed
Dubost, A, Micol, D, Meunier, B, Lethias, C and Listrat, A 2013. Relationships between structural characteristics of bovine intramuscular connective tissue assessed by image analysis and collagen and proteoglycan content. Meat Science 93, 378–386.CrossRefGoogle ScholarPubMed
Etherington, DJ 1977. The dissolution of insoluble bovine collagens by cathepsin BI, collagenolytic cathepsin and pepsin: the influence of collagen type, age and chemical purity on susceptibility. Connective Tissue Research 5, 135–145.CrossRefGoogle Scholar
Folch, J, Lees, M and Sloane Stanley, GH 1957. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry 226, 497–509.Google ScholarPubMed
Gagaoua, M, Claudia Terlouw, EM, Boudjellal, A and Picard, B 2015. Coherent correlation networks among protein biomarkers of beef tenderness: what they reveal. Journal of Proteomics 128, 365–374.CrossRefGoogle ScholarPubMed
Gagaoua, M, Terlouw, EMC and Picard, B 2017. The study of protein biomarkers to understand the biochemical processes underlying beef color development in young bulls. Meat Science 134, 18–27.CrossRefGoogle Scholar
Gagaoua, M, Terlouw, EMC, Micol, D, Hocquette, JF, Moloney, AP, Nuernberg, K, Bauchart, D, Boudjellal, A, Scollan, ND, Richardson, RI and Picard, B 2016. Sensory quality of meat from eight different types of cattle in relation with their biochemical characteristics. Journal of Integrative Agriculture 15, 1550–1563.CrossRefGoogle Scholar
Gillies, AR and Lieber, RL 2011. Structure and function of the skeletal muscle extracellular matrix. Muscle & Nerve 44, 318–331.Google ScholarPubMed
Guy, F, Prache, S, Thomas, A, Bauchart, D and Andueza, D 2011. Prediction of lamb meat fatty acid composition using near-infrared reflectance spectroscopy (NIRS). Food Chemistry 127, 1280–1286.CrossRefGoogle Scholar
Hayes, S, Kamma-Lorger, CS, Boote, C, Young, RD, Quantock, AJ, Rost, A, Khatib, Y, Harris, J, Yagi, N, Terrill, N and Meek, KM 2013. The effect of riboflavin/UVA collagen cross-linking therapy on the structure and hydrodynamic behaviour of the ungulate and rabbit corneal stroma. PLoS ONE 8, e52860.CrossRefGoogle ScholarPubMed
Iozzo, RV and Schaefer, L 2015. Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biology 42, 11–55.CrossRefGoogle ScholarPubMed
Kalamajski, S and Oldberg, Å 2010. The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biology 29, 248–253.CrossRefGoogle ScholarPubMed
Kovanen, V, Suominen, H and Heikkinen, E 1984. Collagen of slow twitch and fast twitch muscle fibres in different types of rat skeletal muscle. European Journal of Applied Physiology and Occupational Physiology 52, 235–242.CrossRefGoogle ScholarPubMed
Kuypers, R and Kurth, LB 1995. Collagen’s contribution to meat texture. In CSIRO Meat Industry Research Conference, Australia, pp. 11B-11–11B-18.Google Scholar
Lefaucheur, L 2010. A second look into fibre typing – relation to meat quality. Meat Science 84, 257–270.CrossRefGoogle ScholarPubMed
Lepetit, J 2007. A theoretical approach of the relationships between collagen content, collagen cross-links and meat tenderness. Meat Science 76, 147–159.CrossRefGoogle ScholarPubMed
Listrat, A, Gagaoua, M and Picard, B 2019. Study of the chronology of expression of ten extracellular matrix molecules during the myogenesis in cattle to better understand sensory properties of meat. Foods 8, 97–112.CrossRefGoogle ScholarPubMed
Listrat, A, Lebret, B, Louveau, I, Astruc, T, Bonnet, M, Lefaucheur, L, Picard, B and Bugeon, J 2016. How muscle structure and composition influence meat and flesh quality. The Scientific World Journal 2016, 3182746.CrossRefGoogle ScholarPubMed
Ngapo, TM, Berge, P, Culioli, J and De Smet, S 2002. Perimysial collagen crosslinking in Belgian Blue double-muscled cattle. Food Chemistry 77, 15–26.CrossRefGoogle Scholar
Nishimura, T, Hattori, A and Takahashi, K 1996. Relationship between degradation of proteoglycans and weakening of the intramuscular connective tissue during post-mortem ageing of beef. Meat Science 42, 251–260.CrossRefGoogle ScholarPubMed
Nishiumi, T, Fukuda, T and Nishimura, T 1997. Isolation and characterization of a small proteoglycan associated with porcine intramuscular connective tissue. Journal of Agricultural and Food Chemistry 45, 2978–2983.CrossRefGoogle Scholar
Picard, B, Barboiron, C, Chadeyron, D and Jurie, C 2011. Protocol for high-resolution electrophoresis separation of myosin heavy chain isoforms in bovine skeletal muscle. Electrophoresis 32, 1804–1806.CrossRefGoogle ScholarPubMed
Picard, B and Cassar-Malek, I 2009. Evidence for expression of IIb myosin heavy chain isoform in some skeletal muscles of Blonde d’Aquitaine bulls. Meat Science 82, 30–36.CrossRefGoogle ScholarPubMed
Purslow, PP 2005. Intramuscular connective tissue and its role in meat quality. Meat Science 70, 435–447.CrossRefGoogle ScholarPubMed
Purslow, PP 2010. Muscle fascia and force transmission. Journal of Bodywork and Movement Therapies 14, 411–417.CrossRefGoogle ScholarPubMed
Reese, SP, Underwood, CJ and Weiss, JA 2013. Effects of decorin proteoglycan on fibrillogenesis, ultrastructure, and mechanics of type I collagen gels. Matrix Biology: Journal of the International Society for Matrix Biology 32, 414–423CrossRefGoogle ScholarPubMed
Rhee, M, Wheeler, T, Shackelford, S and Koohmaraie, M 2004. Variation in palatability and biochemical traits within and among eleven beef muscles. Journal of Animal Science 82, 534–550.CrossRefGoogle ScholarPubMed
Saneyasu, T, Akhtar, R and Sakai, T 2016. Molecular cues guiding matrix stiffness in liver fibrosis. BioMed Research International 2016, 11.CrossRefGoogle ScholarPubMed
Seideman, SC 1986. Methods of expressing collagen characteristics and their relationship to meat tenderness and muscle fiber types. Journal of Food Science 51, 273–276.CrossRefGoogle Scholar
Torrescano, G, Sanchez-Escalante, A, Gimenez, B, Roncales, P and Beltran, JA 2003. Shear values of raw samples of 14 bovine muscles and their relation to muscle collagen characteristics. Meat Science 64, 85–91.CrossRefGoogle ScholarPubMed