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Food, fibre and pharmaceuticals from animals
REVIEW

Gene expression-based approaches to beef quality research

S. A. Lehnert A C , Y. H. Wang A , S. H. Tan A B and A. Reverter A
+ Author Affiliations
- Author Affiliations

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

B Present address: Centre for Diabetes and Endocrine Research, University of Queensland, Princess Alexandra Hospital, Ipswich Road, Woolloongabba, Qld 4102, Australia.

C Corresponding author. Email: sigrid.lehnert@csiro.au

Australian Journal of Experimental Agriculture 46(2) 165-172 https://doi.org/10.1071/EA05226
Submitted: 24 August 2005  Accepted: 6 February 2005   Published: 3 March 2006

Abstract

Advances in mammalian genomics have permitted the application of gene expression profiling approaches to gene discovery for meat quality traits in cattle. The first custom cDNA microarray based on the transcriptome of bovine muscle and fat tissue was developed and applied to animal experimentation and cell culture experimentation between 1999 and 2005. Complementary DNA microarray tools for beef quality research were developed in parallel with bioinformatics tools that permit the analysis of microarray data obtained from complex experimental designs commonly encountered in large animal research. In addition, tools were designed to link gene expression data with gene function in the bovine, such as in vitro models of bovine adipogenesis and bioinformatics tools to map gene networks from expression data. The application of these genomics tools to the study of beef quality has yielded novel knowledge of genes and molecules involved in the processes of intramuscular adipogenesis and protein turnover. This review summarises the current state of knowledge and important lessons derived from bovine genomics initiatives in Australia and around the world.


Acknowledgments

This research was supported by the Cooperative Research Center for Cattle and Beef Quality and its core partners: The University of New England, NSW Agriculture, CSIRO and Queensland Department of Primary Industries; as well as by Meat and Livestock Australia (BSC.010). The authors would like to thank their many colleagues in the CRC for Cattle and Beef Quality and CSIRO Livestock Industries, without whom this work would not have been possible. In particular, the support of Drewe Ferguson, Paul Greenwood and Greg Harper has been invaluable. The authors would also like to acknowledge Peter Willadsen and Brian Dalrymple for constructive comments on the manuscript.


References


Allingham PG, Harper GS, Hunter RA (1998) Effect of growth path on the tenderness of the semitendinosus muscle of Brahman-cross steers. Meat Science 48, 65–73.
Crossref | GoogleScholarGoogle Scholar | open url image1

Aso H, Abe H, Nakajima I, Ozutsumi K, Yamaguchi T, Takamori Y, Kodama A, Hoshino FB, Takano S (1995) A preadipocyte clonal line from bovine intramuscular adipose tissue: nonexpression of GLUT-4 protein during adipocyte differentiation. Biochemical and Biophysical Research Communications 213, 369–375.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bai Q, McGillivray C, da Costa N, Dornan S, Evans G, Stear MJ, Chang KC (2003) Development of a porcine skeletal muscle cDNA microarray: analysis of differential transcript expression in phenotypically distinct muscles. BMC Genomics 4, 8.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boleman SJ, Boleman SL, Miller RK, Taylor JF, Cross HR , et al. (1997) Consumer evaluation of beef of known categories of tenderness. Journal of Animal Science 75, 1521–1524.
PubMed |
open url image1

Boney CM, Moats-Staats BM, Stiles AD, D’Ercole AJ (1994) Expression of insulin-like growth factor-I (IGF-I) and IGF-binding proteins during adipogenesis. Endocrinology 135, 1863–1868.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bortoluzzi S, Rampoldi L, Simionati B, Zimbello R, Barbon A , et al. (1998) A comprehensive, high-resolution genomic transcript map of human skeletal muscle. Genome Research 8, 817–825.
PubMed |
open url image1

Bouley J, Meunier B, Chambon C, De Smet S, Hocquette JF, Picard B (2005) Proteomic analysis of bovine skeletal muscle hypertrophy. Proteomics 5, 490–500.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Byrne KA, Wang YH, Lehnert SA, Harper GS, McWilliam SM, Bruce HL, Reverter A (2005) Gene expression profiling of muscle tissue in Brahman steers during nutritional restriction. Journal of Animal Science 83, 1–12.
PubMed |
open url image1

Campbell WG, Gordon SE, Carlson CJ, Pattison JS, Hamilton MT, Booth FW (2001) Differential global gene expression in red and white skeletal muscle. American Journal of Physiology. Cell Physiology 280, C763–C768.
PubMed |
open url image1

Childs KD, Goad DW, Allan MF, Pomp D, Krehbiel C, Geisert RD, Morgan JB, Malayer JR (2002) Differential expression of NAT1 translational repressor during development of bovine intramuscular adipocytes. Physiological Genomics 10, 49–56.
PubMed |
open url image1

Deveaux V, Cassar-Malek I, Picard B (2001) Comparison of contractile characteristics of muscle from Holstein and double-muscled Belgian Blue foetuses. Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology 131, 21–29.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dransfield E, Martin JF, Bauchart D, Abouelkaram S, Lepetit J, Culioli J, Jurie C, Picard B (2003) Meat quality and composition of three muscles from French Cull cows and young bulls. Animal Science 76, 387–399. open url image1

Green H, Meuth M (1974) An established pre-adipose cell line and its differentiation in culture. Cell 3, 127–133.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B , et al. (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nature Genetics 17, 71–74.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Harper GS (1999) Trends in skeletal muscle biology and the understanding of toughness in beef. Australian Journal of Agricultural Research 50, 1105–1129.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hausman DB, DiGirolamo M, Bartness TJ, Hausman GJ, Martin RJ (2001) The biology of white adipocyte proliferation. Obesity Reviews 2, 239–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Koohmaraie M, Kent MP, Shackelford SD, Veiseth E, Wheeler TL (2002) Meat tenderness and muscle growth: is there any relationship? Meat Science 62, 345–352.
Crossref | GoogleScholarGoogle Scholar | open url image1

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

Maxfield EK, Sinclair KD, Dunne LD, Broadbent PJ, Robinson JJ, Stewart E, Kyle DG, Maltin CA (1998) Temporary exposure of ovine embryos to an advanced uterine environment does not affect fetal weight but alters fetal muscle development. Biology of Reproduction 59, 321–325.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pethick DW, Fergusson DM, Gardner GE, Hocquette JF, Thompson JM, Warner R (2005) Muscle metabolism in relation to genotypic and environmental influences on consumer defined quality of red meat. In ‘Indicators of milk and beef quality’. pp. 95–110. (Wageningen Academic Publishers: Wageningen)

Picard B, Lefaucheur L, Berri C, Duclos MJ (2002) Muscle fibre ontogenesis in farm animal species. Reproduction, Nutrition, Development 42, 415–431.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143–147.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reverter A, Byrne KA, Bruce 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 red high-, medium-, and low-quality diets. Journal of Animal Science 81, 1900–1910.
PubMed |
open url image1

Reverter A, Wang YH, Byrne KA, Tan SH, Harper GS, Lehnert SA (2004) Joint analysis of multiple cDNA microarray studies via multivariate mixed models applied to genetic improvement of beef cattle. Journal of Animal Science 82, 3430–3439.
PubMed |
open url image1

Reverter A, McWilliam SM, Barris W, Dalrymple BP (2005a) A rapid method for computationally inferring transcriptome coverage and microarray sensitivity. Bioinformatics 21, 80–89.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Reverter A, Barris W, Moreno N, McWilliam SM, Wang Y, Harper GS, Lehnert SA, Dalrymple BP (2005b) Construction of networks of gene interactions and regulation from bovine skeletal muscle expression data. Australian Journal of Experimental Agriculture 45, 821–829.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robelin J, Lacourt A, Bechet D, Ferrara M, Briand Y, Geay Y (1991) Muscle differentiation in the bovine fetus: a histological and histochemical approach. Growth, Development, and Aging 55, 151–160. open url image1

Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA (2000) Inhibition of adipogenesis by Wnt signaling. Science 289, 950–953.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N , et al. (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature 422, 297–302.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Suchyta SP, Sipkovsky S, Kruska R, Jeffers A, McNulty A , et al. (2003) Development and testing of a high-density cDNA microarray resource for cattle. Physiological Genomics 15, 158–164.
PubMed |
open url image1

Sudre K, Leroux C, Pietu G, Cassar-Malek I, Petit E, Listrat A, Auffray C, Picard B, Martin P, Hocquette JF (2003) Transcriptome analysis of two bovine muscles during ontogenesis. Journal of Biochemistry 133, 745–756.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sudre K, Leroux C, Cassar-Malek I, Hocquette JF, Martin P (2005a) A collection of bovine cDNA probes for gene expression profiling in muscle. Molecular and Cellular Probes 19, 61–70.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sudre K, Cassar-Malek I, Listrat A, Ueda Y, Leroux C, Jurie C, Auffray C, Renand G, Martin P, Hocquette JF (2005b) Biochemical and transcriptomic analyses of two bovine skeletal muscles in Charolais bulls divergently selected for muscle growth. Meat Science 70, 267–277.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tan SH, Reverter A, Wang Y, Byrne KA, McWilliam SM, Lehnert SA (2006) Gene expression profiling of bovine in vitro adipogenesis using a cDNA microarray. Functional & Integrative Genomics 6,
Crossref | GoogleScholarGoogle Scholar | open url image1

Taniguchi M, Mannen H, Oyama K, Shimakura Y, Oka A, Watanabe H, Kojima T, Komatsu M, Harper GS, Tsuji S (2004) Differences in stearoyl-coA desaturase mRNA levels between Japanese Black and Holstein cattle. Livestock Production Science 87, 215–220.
Crossref | GoogleScholarGoogle Scholar | 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

Wang YH, Byrne KA, Reverter A, Harper GS, Taniguchi M, Mcwilliam SM, Mannen H, Oyama K, Lehnert SA (2005a) Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mammalian Genome 16, 201–210.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang YH, Reverter A, Mannen H, Taniguchi M, Harper GS, Oyama K, Byrne KA, Oka A, Tsuji S, Lehnert SA (2005b) Transcriptional profiling of muscle tissue in growing Japanese Black cattle to identify genes involved with the development of intramuscular fat. Australian Journal of Experimental Agriculture 45, 809–820.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wegner J, Albrecht E, Fiedler I, Teuscher F, Papstein HJ, Ender K (2000) Growth- and breed-related changes of muscle fiber characteristics in cattle. Journal of Animal Science 78, 1485–1496.
PubMed |
open url image1

Yu SL, Jung KC, Lee YJ, Lee JH, Yoon DH, Lee SH, Choi KD, Sang BC (2004) Identification of differentially-expressed genes in skeletal muscles in Hanwoo (Korean cattle) using cDNA microarray. In ‘Proceedings of the 29th international conference on animal genetics’. p. 70. (International Society for Animal Genetics)

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