Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Transcriptional profiling of muscle tissue in growing Japanese Black cattle to identify genes involved with the development of intramuscular fat

Y. H. Wang A F , A. Reverter A , H. Mannen B , M. Taniguchi B C , G. S. Harper A , K. Oyama D , K. A. Byrne A , A. Oka B , S. Tsuji B and S. A. Lehnert A
+ Author Affiliations
- Author Affiliations

A Cooperative Research Centre for Cattle and Beef Quality, CSIRO Livestock Industries, Queensland Bioscience Precinct, 306 Carmody Road, St Lucia, Brisbane, Qld 4067, Australia.

B Laboratory of Animal Breeding and Genetics, Faculty of Agriculture, Kobe University, Kobe-shi 657-8501, Japan.

C Present address: Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2P5, Canada.

D Food Resources Education and Research Center, Kobe University, Kasai, 675-2103, Japan.

E Livestock Research Center, Hyogo Prefectural Institute of Agriculture, Forestry and Fisheries, Kasai, 679-0198, Japan.

F Corresponding author. Email:yonghong.wang@csiro.au

Australian Journal of Experimental Agriculture 45(8) 809-820 https://doi.org/10.1071/EA05058
Submitted: 22 February 2005  Accepted: 9 May 2005   Published: 26 August 2005

Abstract

Japanese Black cattle are characterised by a unique ability to deposit intramuscular fat with lower melting temperature. In this study, 3 consecutive biopsies from Longissimus muscle tissue were taken and RNA isolated from 3 Japanese Black (Tajima strain) and 3 Holstein animals at age 11–20 months. The gene expression changes in these samples were analysed using a bovine fat/muscle cDNA microarray. A mixed-ANOVA model was fitted to the intensity signals. A total of 335 (4.8%) array elements were identified as differentially expressed genes in this breed × time comparison study. Genes preferentially expressed in Japanese Black are associated with mono-unsaturated fatty acid synthesis, fat deposition, adipogenesis development and muscle regulation, while examples of genes preferentially expressed in Holstein come from functional classes involved in connective tissue and skeletal muscle development. The gene expression differences detected between the Longissimus muscle of the 2 breeds give important clues to the molecular basis for the unique features of the Japanese Black breed, such as the onset and rate of adipose tissue development, metabolic differences, and signalling pathways involved in converting carbohydrate to lipid during lipogenesis. These findings will impact on industry management strategies designed to manipulate intramuscular adipose development at different development stages to gain maximum return for beef products.


Acknowledgments

This research was supported in Australia by the Cooperative Research Centre for Cattle and Beef Quality, and we acknowledge the many other resources and opportunities provided to us by the staff of the Centre. In Japan, the work was facilitated significantly by the support of Nitchiku Japan and we thank them for that support.


References


Allingham P , Brownlee G , Harper G , Brown T (2005) Synthesis of hyaluronan during growth and differentiation of 3T3-L1 adipocytes. In ‘HA 2003 Proceedings’. (Eds E Balazs, V Hascall) (in press).

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Rapp BA, Wheeler DL (2002) GenBank. Nucleic Acids Research 30, 17–20.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Börchers T , Spener F (1994) Fatty acid binding proteins. In ‘Current topics in membranes. Vol. 40.’ (Ed. D Hoekstra) pp. 261–294. (Academic Press Inc.: San Diego)

Cianzio DS, Topel DG, Whitehurst GB, Beitz DC, Self HL (1985) Adipose tissue growth and cellularity: changes in bovine adipocyte size and number. Journal of Animal Science 60, 970–976.
PubMed |
open url image1

Garcia-Cortes LA, Rico M, Groeneveld E (1998) Using coupling with the Gibbs sampler to assess convergence in animal models. Journal of Animal Science 76, 441–447.
PubMed |
open url image1

Glatz JF, Vork MM, Cistola DP, van der Vusse GJ (1993) Cytoplasmic fatty acid binding protein: significance for intracellular transport of fatty acids and putative role on signal transduction pathways. Prostaglandins, Leukotrienes, and Essential Fatty Acids 48, 33–41.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gondret F, Damon M, Jadhao SB, Houdebine LM, Herpin P, Hocquette JF (2004) Age-related changes in glucose utilization and fatty acid oxidation in a muscle-specific manner during rabbit growth. Journal of Muscle Research and Cell Motility 25, 405–410.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hawken RJ, Barris WC, McWilliam SM, Dalrymple BP (2004) An interactive bovine in silico SNP database (IBISS). Mammalian Genome 15, 819–827.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hood RL, Allen CE (1973) Cellularity of bovine adipose tissue. Journal of Lipid Research 14, 605–610.
PubMed |
open url image1

Inoue-Murayama M, Sugimoto Y, Niimi Y, Aso H (2000) Type XVIII collagen is newly transcribed during bovine adipogenesis. Differentiation 65, 281–285.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Japan Meat Grading Association (1988) ‘New beef grading standards.’ (Japan Meat Grading Association: Tokyo)

Kinlaw WB, Church JL, Harmon J, Mariash CN (1995) Direct evidence for a role of the ‘spot 14’ protein in the regulation of lipid synthesis. Journal of Biological Chemistry 270, 16615–16618.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lehnert SA, Wang YH, Byrne KA (2004) Development and application of a bovine cDNA mircroarray for expression profiling of muscle and adipose tissue. Australian Journal of Experimental Agriculture 44, 1127–1133.
Crossref | GoogleScholarGoogle Scholar | open url image1

McLachlan GJ, Bean RW, Peel D (2002) A mixture model-based approach to the clustering of microarray expression data. Bioinformatics 18, 413–422.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moody WG, Cassens RG (1968) Histochemical differentiation of red and white muscle fibers. Journal of Animal Science 27, 961–968.
PubMed |
open url image1

Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 32, 1372–1374.
PubMed |
open url image1

Nakajima I, Muroya S, Tanabe R, Chikuni K (2002) Extracellular matrix development during differentiation into adipocytes with a unique increase in type V and VI collagen. Biology of the Cell 94, 197–203.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nishimura T, Hattori A, Takahashi K (1999) Structural changes in intramuscular connective tissue during the fattening of Japanese black cattle: effect of marbling on beef tenderization. Journal of Animal Science 77, 93–104.
PubMed |
open url image1

Owens FN, Gill DR, Secrist DS, Coleman SW (1995) Review of some aspects of growth and development of feedlot cattle. Journal of Animal Science 73, 3152–3172.
PubMed |
open url image1

Peng X, Wood CL, Blalock EM, Chen KC, Landfield PW, Stromberg AJ (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics 4, 26.
Crossref | PubMed |
open url image1

Pethick DW, Harper GS, Oddy VH (2004) Growth development and nutritional manipulation of marbling in cattle: a review. Australian Journal of Experimental Agriculture 44, 705–715.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Reviews of Physiology, Biochemistry and Pharmacology 116, 1–76.
PubMed |
open url image1

Reverter A, Byrne KA, Brucet HL, Wang YH, Dalrymple BP, Lehnert SA (2003) A mixture model-based cluster analysis of DNA microarray gene expression data on Brahman and Brahman composite steers fed high-, medium-, and low-quality diets. Journal of Animal Science 81, 1900–1910.
PubMed |
open url image1

Rump R, Buhlmann C, Borchers T, Spener F (1996) Differentiation-dependent expression of heart type fatty acid-binding protein in C2C12 muscle cells. European Journal of Cell Biology 69, 135–142.
PubMed |
open url image1

Russell RG, Oteruelo FT (1981) An ultrastructural study of the differentiation of skeletal muscle in the bovine fetus. Anatomy and Embryology 162, 403–417.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Swatland HJ (1993) Developing a fiber-optic probe to combine subcutaneous fat depth and meat quality measurements. Journal of Animal Science 71, 2666–2673.
PubMed |
open url image1

Toseland CD, Campbell S, Francis I, Bugelski PJ, Mehdi N (2001) Comparison of adipose tissue changes following administration of rosiglitazone in the dog and rat. Diabetes, Obesity and Metabolism 3, 163–170.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tran PH, Peiffer DA, Shin Y, Meek LM, Brody JP, Cho KW (2002) Microarray optimizations: increasing spot accuracy and automated identification of true microarray signals. Nucleic Acids Research 30, 54e.
Crossref | GoogleScholarGoogle Scholar | open url image1

Veerkamp JH, van Moerkerk HT (1993) Fatty acid-binding protein and its relation to fatty acid oxidation. Molecular and Cellular Biochemistry 123, 101–106.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang YH, Byrne KA, Reverter A, Harper GS, Tanaiguchi M, McWilliam SM, Mannen H, Oyama K, Lehnert SA (2005) Comparison of gene expression profiles of muscle tissue in Japanese black and Holstein cattle. Mammalian Genome 16, 201–210.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang YH, McWilliam SM, Barendse W, Kata SR, Womack JE, Moore SS, Lehnert SA (2001) Mapping of 12 bovine ribosomal protein genes using a bovine radiation hybrid panel. Animal Genetics 32, 269–273.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yang A, Larsen TW, Smith SB, Tume RK (1999) Delta9 desaturase activity in bovine subcutaneous adipose tissue of different fatty acid composition. Lipids 34, 971–978.
PubMed |
open url image1

Zembayashi M (1994) Effects of nutritional planes and breeds on intramuscular-lipid deposition in M. longissimus dorsi of steers. Meat Science 38, 367–374.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zembayashi M, Nishimura K, Lunt DK, Smith SB (1995) Effect of breed type and sex on the fatty acid composition of subcutaneous and intramuscular lipids of finishing steers and heifers. Journal of Animal Science 73, 3325–3332.
PubMed |
open url image1