Gene expression phenotypes for lipid metabolism and intramuscular fat in skeletal muscle of cattle

Journal of Animal Science

Volumn 91, Issue 3, 2013, Pages 1112-1128

  De Jager, N ^a,b,c   Hudson, N J ^a,b,c   Reverter, A ^a,b,c   Barnard, R ^c   Cafe, L M ^a,d   Greenwood, P L ^a,d   Dalrymple, B P ^a,b,c  

^a Australian Cooperative Research Centre for Beef Genetic Technologies ^*  (Australia)

^b CSIRO   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

Beef cattle; Fatty acid synthesis; Gene expression phenotype; Intramuscular fat percentage; Tenderness genotype; Triacylglyceride synthesis

Indexed keywords

MUSCLE PROTEIN; RNA;

ANIMAL; ANIMAL DISEASE; ARTICLE; CATTLE; DNA MICROARRAY; DNA SEQUENCE; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC MARKER; GENETICS; LIPID METABOLISM; MALE; MEAT; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY; SKELETAL MUSCLE;

ANIMALS; CATTLE; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC MARKERS; LIPID METABOLISM; MALE; MEAT; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MUSCLE, SKELETAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

EID: 84882596534     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-5409     Document Type: Article

References (62)

1. Barendse, W. 2011. Haplotype analysis improved evidence for candidate genes for intramuscular fat percentage from a genome wide association study of cattle. PLoS ONE 6:e29601.
2. Barendse, W., B. Harrison, R. Bunch, and M. Thomas. 2008. Variation at the calpain 3 gene is associated with meat tenderness in zebu and composite breeds of cattle. BMC Genet. 9:41.
3. Barendse, W. J. 2002. DNA markers for meat tenderness, International Patent Publ. WO 02/064820 A1.
4. Bartle, S. J., R. L. Preston, R. E. Brown, and R. J. Grant. 1992. Trenbolone acetate/estradiol combinations in feedlot steers: Dose-response and implant carrier effects. J. Anim. Sci. 70:1326-1332.
5. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate-A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57:289-300.
6. Bolormaa, S., L. R. Neto, Y. D. Zhang, R. J. Bunch, B. E. Harrison, M. E. Goddard, and W. Barendse. 2011. A genome-wide association study of meat and carcass traits in Australian cattle. J. Anim. Sci. 89:2297-2309.
7. Bonnet, M., Y. Faulconnier, C. Leroux, C. Jurie, I. Cassar-Malek, D. Bauchart, P. Boulesteix, D. Pethick, J. F. Hocquette, and Y. Chilliard. 2007. Glucose-6-phosphate dehydrogenase and leptin are related to marbling differences among Limousin and Angus or Japanese Black x Angus steers. J. Anim. Sci. 85:2882-2894.
8. Bryant, T. C., T. E. Engle, M. L. Galyean, J. J. Wagner, J. D. Tatum, R. V. Anthony, and S. B. Laudert. 2010. Effects of ractopamine and trenbolone acetate implants with or without estradiol on growth performance, carcass characteristics, adipogenic enzyme activity, and blood metabolites in feedlot steers and heifers. J. Anim. Sci. 88:4102-4119.
9. Cafe, L. M., D. W. Hennessy, H. Hearnshaw, S. G. Morris, and P. L. Greenwood. 2006. Influences of nutrition during pregnancy and lactation on birth weights and growth to weaning of calves sired by Piedmontese or Wagyu bulls. Aust. J. Exp. Agric. 46:245-255.
10. Cafe, L. M., B. L. McIntyre, D. L. Robinson, G. H. Geesink, W. Barendse, and P. L. Greenwood. 2010a. Production and processing studies on calpain-system gene markers for tenderness in Brahman cattle: 1. Growth, efficiency, temperament, and carcass characteristics. J. Anim. Sci. 88:3047-3058.
11. Cafe, L. M., B. L. McIntyre, D. L. Robinson, G. H. Geesink, W. Barendse, D. W. Pethick, J. M. Thompson, and P. L. Greenwood. 2010b. Production and processing studies on calpain-system gene markers for tenderness in Brahman cattle: 2. Objective meat quality. J. Anim. Sci. 88:3059-3069.
12. Cafe, L. M., D. L. Robinson, D. M. Ferguson, B. L. McIntyre, G. H. Geesink, and P. L. Greenwood. 2011. Cattle temperament: Persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits. J. Anim. Sci. 89:1452-1465.
13. Chen, X., S. W. Cushman, L. K. Pannell, and S. Hess. 2005. Quantitative proteomic analysis of the secretory proteins from rat adipose cells using a 2D liquid chromatography-MS/MS approach. J. Proteome Res. 4:570-577.
14. Cherel, P., F. Herault, A. Vincent, P. Le Roy, and M. Damon. 2012. Genetic variability of transcript abundance in pig skeletal muscle at slaughter: Relationships with meat quality traits. J. Anim. Sci. 90:699-708.
15. Cunningham, B. A., J. T. Moncur, J. T. Huntington, and W. B. Kinlaw. 1998. "Spot 14" protein: A metabolic integrator in normal and neoplastic cells. Thyroid 8:815-825.
16. De Jager, N., N. J. Hudson, A. Reverter, Y.-H. Wang, S. H. Nagaraj, L. M. Cafe, P. L. Greenwood, R. T. Barnard, K. P. Kongsuwan, and B. P. Dalrymple. 2011. Chronic exposure to anabolic steroids induces the muscle expression of oxytocin and a more than fiftyfold increase in circulating oxytocin in cattle. Physiol. Genomics 43:467-478.
17. Donkor, J., M. Sariahmetoglu, J. Dewald, D. N. Brindley, and K. Reue. 2007. Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J. Biol. Chem. 282:3450-3457.
18. Du, M., J. Tong, J. Zhao, K. R. Underwood, M. Zhu, S. P. Ford, and P. W. Nathanielsz. 2010. Fetal programming of skeletal muscle development in ruminant animals. J. Anim. Sci. 88:E51-E60.
19. Duckett, S. K., S. L. Pratt, and E. Pavan. 2009. Corn oil or corn grain supplementation to steers grazing endophyte-free tall fescue. II. Effects on subcutaneous fatty acid content and lipogenic gene expression. J. Anim. Sci. 87:1120-1128.
20. Eberlein, A., C. Kalbe, T. Goldammer, R. M. Brunner, C. Kuehn, and R. Weikard. 2010. Analysis of structure and gene expression of bovine CCDC3 gene indicates a function in fat metabolism. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 156:19-25.
21. Eberlein, A., C. Kalbe, T. Goldammer, R. M. Brunner, C. Kuehn, and R. Weikard. 2011. Annotation of novel transcripts putatively relevant for bovine fat metabolism. Mol. Biol. Rep. 38:2975-2986.
22. Eden, E., D. Lipson, S. Yogev, and Z. Yakhini. 2007. Discovering motifs in ranked lists of DNA sequences. PLoS Comput. Biol. 3:e39.
23. Eden, E., R. Navon, I. Steinfeld, D. Lipson, and Z. Yakhini. 2009. Gorilla: A tool for discovery and visualization of enriched go terms in ranked gene lists. BMC Bioinformatics 10:48.
24. Goll, D. E., V. F. Thompson, R. G. Taylor, and A. Ouali. 1998. The calpain system and skeletal muscle growth. Can. J. Anim. Sci. 78:503-512.
25. Graugnard, D. E., L. L. Berger, D. B. Faulkner, and J. J. Loor. 2010. High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned angus cattle. Br. J. Nutr. 103:953-963.
26. Graugnard, D. E., P. Piantoni, M. Bionaz, L. L. Berger, D. B. Faulkner, and J. J. Loor. 2009. Adipogenic and energy metabolism gene networks in longissimus lumborum during rapid post-weaning growth in Angus and Angus x Simmental cattle fed high-starch or low-starch diets. BMC Genomics 10:142.
27. Greenwood, P. L., and L. M. Cafe. 2007. Prenatal and pre-weaning growth and nutrition of cattle: Long-term consequences for beef production. Animal 1:1283-1296.
28. Greenwood, P. L., L. M. Cafe, H. Hearnshaw, D. W. Hennessy, J. M. Thompson, and S. G. Morris. 2006. Long-term consequences of birth weight and growth to weaning on carcass, yield and beef quality characteristics of Piedmontese- and Wagyu-sired cattle. Aust. J. Exp. Agric. 46:257-269.
29. Greenwood, P. L., H. Hearnshaw, L. M. Cafe, D. W. Hennessy, and G. S. Harper. 2004a. Nutrition in utero and pre-weaning has long-term consequences for growth and size of Piedmonteseand Wagyu-sired steers. J. Anim. Sci. 82(Suppl. 1):408-409.
30. Greenwood, P. L., H. Hearnshaw, G. Kelly, and D. W. Hennessy. 2004b. Nutrition of Wagyu- and Piedmontese-sired fetuses alters newborn longissimus muscle cellular characteristics. J. Anim. Sci. 82(Suppl. 1):251.
31. Guillou, H., D. Zadravec, P. G. Martin, and A. Jacobsson. 2010. The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice. Prog. Lipid Res. 49:186-199.
32. Harris, T. E., and B. N. Finck. 2011. Dual function lipin proteins and glycerolipid metabolism. Trends Endocrinol. Metab. 22:226-233.
33. Hocquette, J. F., F. Gondret, E. Baéza, F. Médale, C. Jurie, and D. W. Pethick. 2010. Intramuscular fat content in meat-producing animals: Development, genetic and nutritional control, and identification of putative markers. Animal 4:303-319.
34. Hong, Y. H., D. Hishikawa, H. Miyahara, H. Tsuzuki, Y. Nishimura, C. Gotoh, K. C. Choi, Y. Hokari, Y. Takagi, H. G. Lee, K. K. Cho, S. G. Roh, and S. Sasaki. 2005. Up-regulation of adipogenin, an adipocyte plasma transmembrane protein, during adipogenesis. Mol. Cell. Biochem. 276:133-141.
35. Hudson, N. J., A. Reverter, and B. P. Dalrymple. 2009a. A differential wiring analysis of expression data correctly identifies the gene containing the causal mutation. PLoS Comput. Biol. 5:e1000382.
36. Hudson, N. J., A. Reverter, Y. Wang, P. L. Greenwood, and B. P. Dalrymple. 2009b. Inferring the transcriptional landscape of bovine skeletal muscle by integrating co-expression networks. PLoS ONE 4:e7249.
37. Hunter, R. A. 2010. Hormonal growth promotant use in the Australian beef industry. Anim. Prod. Sci. 50:637-659.
38. Jeong, J., E. G. Kwon, S. K. Im, K. S. Seo, and M. Baik. 2012. Expression of fat deposition and fat removal genes is associated with intramuscular fat content in longissimus dorsi muscle of Korean cattle steers. J. Anim. Sci. 90:2044-2053.
39. Kim, N. K., D. Lim, S. H. Lee, Y. M. Cho, E. W. Park, C. S. Lee, B. S. Shin, T. H. Kim, and D. Yoon. 2011. Heat shock protein b1 and its regulator genes are negatively correlated with intramuscular fat content in the longissimus thoracis muscle of Hanwoo (Korean cattle) steers. J. Agric. Food Chem. 59:5657-5664.
40. Kuryl, J., W. Kapelanski, M. Pierzchala, S. Grajewska, and M. Bocian. 2003. Preliminary observations on the effect of calpastatin gene (cast) polymorphism on carcass traits in pigs. Anim. Sci. Pap. Rep. 21:87-95.
41. Lee, S. H., Y. M. Cho, S. H. Lee, B. S. Kim, N. K. Kim, Y. H. Choy, K. H. Kim, D. Yoon, S. K. Im, S. J. Oh, and E. W. Park. 2008. Identification of marbling-related candidate genes in m-longissimus dorsi of high- and low marbled Hanwoo (Korean native cattle) steers. BMB Rep. 41:846-851.
42. Lee, S. H., C. Gondro, J. van der Werf, N. K. Kim, D. J. Lim, E. W. Park, S. J. Oh, J. P. Gibson, and J. M. Thompson. 2010. Use of a bovine genome array to identify new biological pathways for beef marbling in Hanwoo (Korean cattle). BMC Genomics 11:623.
43. Lee, S. H., E. W. Park, Y. M. Cho, S. K. Kim, J. H. Lee, J. T. Jeon, C. S. Lee, S. K. Im, S. J. Oh, J. M. Thompson, and D. Yoon. 2007. Identification of differentially expressed genes related to intramuscular fat development in the early and late fattening stages of Hanwoo steers. J. Biochem. Mol. Biol. 40:757-764.
44. Lehnert, S. A., A. Reverter, K. A. Byrne, Y. Wang, G. S. Nattrass, N. J. Hudson, and P. L. Greenwood. 2007. Gene expression studies of developing bovine longissimus muscle from two different beef cattle breeds. BMC Dev. Biol. 7:95.
45. Lim, D., N. K. Kim, H. S. Park, S. H. Lee, Y. M. Cho, S. J. Oh, T. H. Kim, and H. Kim. 2011. Identification of candidate genes related to bovine marbling using protein-protein interaction networks. Int. J. Biol. Sci. 7:992-1002.
46. Mariasegaram, M., A. Reverter, W. Barris, S. A. Lehnert, B. Dalrymple, and K. Prayaga. 2010. Transcription profiling provides insights into gene pathways involved in horn and scurs development in cattle. BMC Genomics 11:370.
47. Oort, P. J., C. H. Warden, T. K. Baumann, T. A. Knotts, and S. H. Adams. 2007. Characterization of Tusc5, an adipocyte gene coexpressed in peripheral neurons. Mol. Cell. Endocrinol. 276:24-35.
48. Perry, D., W. R. Shorthose, D. M. Ferguson, and J. M. Thompson. 2001. Methods used in the CRC program for the determination of carcass yield and beef quality. Aust. J. Exp. Agric. 41:953-957.
49. Pickworth, C. L., S. C. Loerch, S. G. Velleman, J. L. Pate, D. H. Poole, and F. L. Fluharty. 2011. Adipogenic differentiation statespecific gene expression as related to bovine carcass adiposity. J. Anim. Sci. 89:355-366.
50. Reiling, B. A., and D. D. Johnson. 2003. Effects of implant regimens (trenbolone acetate-estradiol administered alone or in combination with zeranol) and vitamin D3 on fresh beef color and quality. J. Anim. Sci. 81:135-142.
51. Reverter, A., D. J. Johnston, D. M. Ferguson, D. Perry, M. E. Goddard, H. M. Burrow, V. H. Oddy, J. M. Thompson, and B. M. Bindon. 2003. Genetic and phenotypic characterization of animal, carcass, and meat quality traits from temperate and tropically adapted beef breeds. 4. Correlations among animal, carcass, and meat quality traits. Aust. J. Agric. Res. 54:149-158.
52. Sallman Almen, M., N. Bringeland, R. Fredriksson, and H. B. Schioth. 2012. The dispanins: A novel gene family of ancient origin that contains 14 human members. PLoS ONE 7:e31961.
53. Serao, N. V. L., R. Veroneze, A. M. F. Ribeiro, L. L. Verardo, J. B. Neto, E. Gasparino, C. F. Campos, P. S. Lopes, and S. E. F. Guimaraes. 2011. Candidate gene expression and intramuscular fat content in pigs. J. Anim. Breed. Genet. 128:28-34.
54. Shehzad, A., W. Iqbal, O. Shehzad, and Y. S. Lee. 2012. Adiponectin: Regulation of its production and its role in human diseases. Hormones (Athens) 11:8-20.
55. Wang, X., C. Xue, H. Liu, Y. Xu, R. Zhao, Z. Jiang, M. V. Dodson, and J. Chen. 2009a. Differential display of expressed genes reveals a novel function of SFRS18 in regulation of intramuscular fat deposition. Int. J. Biol. Sci. 5:28-33.
56. Wang, Y. H., N. I. Bower, A. Reverter, S. H. Tan, N. De Jager, R. Wang, S. M. McWilliam, L. M. Cafe, P. L. Greenwood, and S. A. Lehnert. 2009b. Gene expression patterns during intramuscular fat development in cattle. J. Anim. Sci. 87:119-130.
57. Wang, Y. H., K. A. Byrne, A. Reverter, G. S. Harper, M. Taniguchi, S. M. McWilliam, H. Mannen, K. Oyama, and S. A. Lehnert. 2005. Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mamm. Genome 16:201-210.
58. Wheeler, T. L., L. V. Cundiff, and R. M. Koch. 1994. Effect of marbling degree on beef palatability in Bos taurus and Bos indicus cattle. J. Anim. Sci. 72:3145-3151.
59. White, S. N., E. Casas, T. L. Wheeler, S. D. Shackelford, M. Koohmaraie, D. G. Riley, C. C. Chase, D. D. Johnson, J. W. Keele, and T. P. Smith. 2005. A new single nucleotide polymorphism in capn1 extends the current tenderness marker test to include cattle of bos indicus, bos taurus, and crossbred descent. J. Anim. Sci. 83: 2001-2008.
60. Williams, J. E., D. G. Wagner, L. E. Walters, G. W. Horn, G. R. Waller, P. L. Sims, and J. J. Guenther. 1983. Effect of production systems on performance, body composition and lipid and mineral profiles of soft tissue in cattle. J. Anim. Sci. 57:1020-1028.
61. Wolcott, M. L., and D. J. Johnston. 2009. The impact of genetic markers for tenderness on steer carcass and feedlot exit and heifer puberty traits in Brahman cattle. In: Proc. 18th Conf. Assoc. Adv. Anim. Breed. Genet., Barossa Valley, South Australia. p. 159-162.
62. Zhou, H., Y. Xiao, R. Li, S. Hong, S. Li, L. Wang, R. Zeng, and K. Liao. 2009. Quantitative analysis of secretome from adipocytes regulated by insulin. Acta Biochim. Biophys. Sin. (Shanghai) 41:910-921.