Central role of the PPARγ gene network in coordinating beef cattle intramuscular adipogenesis in response to weaning age and nutrition

Gene Regulation and Systems Biology

Volumn 2014, Issue 8, 2014, Pages 17-32

  Moisá, Sonia J ^a   Shike, Daniel W ^a   Faulkner, Dan B ^b   Meteer, William T ^a   Keisler, Duane ^c   Loor, Juan J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Adipogenesis; Marbling; Nutrition; Transcriptomics; Weaning

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ADIPOGENESIS; AGE; ANIMAL TISSUE; ARTICLE; BEEF CATTLE; BODY COMPOSITION; CARBOHYDRATE DIET; CEBPA GENE; CONTROLLED STUDY; DGAT2 GENE; ELOVL6 GENE; FASN GENE; GENE; GENE FUNCTION; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC ASSOCIATION; INSIG1 GENE; LIPID STORAGE; LONGISSIMUS MUSCLE; NONHUMAN; NUTRITIONAL STATUS; PCK1 GENE; PHENOTYPE; PPAR GAMMA GENE; PROTEIN EXPRESSION; SCD GENE; SKELETAL MUSCLE; SREBF1 GENE; THRSP GENE; ZFP423 GENE;

EID: 84892512661     PISSN: None     EISSN: 11776250     Source Type: Journal    
DOI: 10.4137/GRSB.S11782     Document Type: Article

References (87)

1. Gregoire FM, Smas CM, Sul HS. Understanding adipocyte differentiation. Physiol Rev. Jul 1998;78(3):783-809.
2. Rosen ED, Hsu CH, Wang X, et al. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev. Jan 1, 2002;16(1):22-6.
3. Wu Z, Rosen ED, Brun R, et al. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell. Feb 1999;3(2):151-8.
4. Lengi AJ, Corl BA. Factors influencing the differentiation of bovine preadipocytes in vitro. J Anim Sci. Jun 2010;88(6):1999-2008.
5. Grant AC, Ortiz-Colon G, Doumit ME, Buskirk DD. Optimization of in vitro conditions for bovine subcutaneous and intramuscular preadipocyte differentiation. J Anim Sci. Jan 2008;86(1):73-82.
6. Vernon RG. Lipid metabolism in the adipose tissue of ruminant animals. Prog Lipid Res. 1980;19(1/2):23-106.
7. Aguiari P, Leo S, Zavan B, et al. High glucose induces adipogenic differentiation of muscle-derived stem cells. Proc Natl Acad Sci U S A. Jan 29, 2008;105(4): 1226-31.
8. Meyer DL, Kerley MS, Walker EL, et al. Growth rate, body composition, and meat tenderness in early vs. traditionally weaned beef calves. J Anim Sci. Dec 2005;83(12):2752-61.
9. Meteer WT, Retallick, KM, Faulkner, DB, Adcock, JW, and Shike, DW. Effects of weaning age and source of energy on beef calf performance, carcass characteristics, and economics. Professional Animal Scientist. 2013(29):469-81.
10. Graugnard DE, Berger LL, Faulkner DB, Loor JJ. High-starch diets induce precocious adipogenic gene network up-regulation in longissimus lumborum of early-weaned Angus cattle. Br J Nutr. Apr 2010;103(7):953-63.
11. Powell MR, Keisler DH. A potential strategy for decreasing milk production in the ewe at weaning using a growth hormone release blocker. J Anim Sci. Jul 1995;73(7):1901-5.
12. Lalman DL, Williams JE, Hess BW, Thomas MG, Keisler DH. Effect of dietary energy on milk production and metabolic hormones in thin, primiparous beef heifers. J Anim Sci. Mar 2000;78(3):530-8.
13. Moisa SJ, Shike DW, Meteer WT, Keisler D, Faulkner DB, Loor JJ. Yin yang 1 and adipogenic gene network expression in longissimus muscle of beef cattle in response to nutritional management. Gene Regul Syst Bio. 2013;7:71-83.
14. Blanco M, Villalba D, Ripoll G, Sauerwein H, Casasus I. Effects of pre-weaning concentrate feeding on calf performance, carcass and meat quality of autumn-born bull calves weaned at 90 or 150 days of age. Animal. May 2008;2(5):779-89.
15. USDA. United States Standards for Grades of Carcass Beef: United States Department of Agriculture; 1997.
16. Govoni KE, Hoagland TA, Zinn SA. The ontogeny of the somatotropic axis in male and female Hereford calves from birth to one year of age. J Anim Sci. Nov 2003;81(11):2811-7.
17. Oksbjerg N, Gondret F, Vestergaard M. Basic principles of muscle development and growth in meat-producing mammals as affected by the insulin-like growth factor (IGF) system. Domest Anim Endocrinol. Oct 2004;27(3):219-40.
18. Richards MW, Wettemann RP, Schoenemann HM. Nutritional anestrus in beef cows: concentrations of glucose and nonesterified fatty acids in plasma and insulin in serum. J Anim Sci. Sep 1989;67(9):2354-62.
19. Lehrke M, Lazar MA. The many faces of PPARgamma. Cell. Dec 16, 2005;123(6): 993-9.
20. Linhart HG, Ishimura-Oka K, DeMayo F, et al. C/EBPalpha is required for differentiation of white, but not brown, adipose tissue. Proc Natl Acad Sci U S A. Oct 23, 2001;98(22):12532-7.
21. Du M, Yin J, Zhu MJ. Cellular signaling pathways regulating the initial stage of adipogenesis and marbling of skeletal muscle. Meat Sci. Sep 2010;86(1):103-9.
22. Key CN, Perkins SD, Bratcher CL, Kriese-Anderson LA, Brandebourg TD. Grain feeding coordinately alters expression patterns of transcription factor and metabolic genes in subcutaneous adipose tissue of crossbred heifers. J Anim Sci. Jun 2013;91(6):2616-27.
23. Hata K, Nishimura R, Ikeda F, et al. Differential roles of Smad1 and p38 kinase in regulation of peroxisome proliferator-activating receptor gamma during bone morphogenetic protein 2-induced adipogenesis. Mol Biol Cell. Feb 2003;14(2):545-55.
24. Yasmeen R, Jeyakumar SM, Reichert B, Yang F, Ziouzenkova O. The contribution of vitamin A to autocrine regulation of fat depots. Biochim Biophys Acta. Jan 2012;1821(1):190-7.
25. Takahashi A, Morita M, Yokoyama K, Suzuki T, Yamamoto T. Tob2 inhibits peroxisome proliferator-activated receptor gamma2 expression by equestering Smads and C/EBPalpha during adipocyte differentiation. Mol Cell Biol. Dec 2012;32(24):5067-77.
26. Brivanlou AH, Darnell JE, Jr. Signal transduction and the control of gene expression. Science. Feb 1, 2002;295(5556):813-8.
27. Gupta RK, Arany Z, Seale P, et al. Transcriptional control of preadipocytedetermination by Zfp423. Nature. Mar 25, 2010;464(7288):619-23.
28. Massague J, Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. Apr 17, 2000;19(8):1745-54.
29. Yost TJ, Jensen DR, Haugen BR, Eckel RH. Effect of dietary macronutrient composition on tissue-specific lipoprotein lipase activity and insulin action in normal-weight subjects. Am J Clin Nutr. Aug 1998;68(2):296-302.
30. Steger DJ, Grant GR, Schupp M, et al. Propagation of adipogenic signals through an epigenomic transition state. Genes Dev. May 15, 2010;24(10):1035-44.
31. Ceseña TI. Regulation of the acetylation of C/EBPβ and its functional consequences. Michigan: Cellular and Molecular Biology, University of Michigan; 2008.
32. Gerin I, Bommer GT, Lidell ME, Cederberg A, Enerback S, Macdougald OA. On the role of FOX transcription factors in adipocyte differentiation and insulin-stimulated glucose uptake. J Biol Chem. Apr 17, 2009;284(16):10755-63.
33. Williams CB, Bennett GL, Keele JW. Simulated influence of postweaning production system on performance of different biological types of cattle: II. Carcass composition, retail product, and quality. J Anim Sci. Mar 1995;73(3):674-85.
34. Davie JR, Chadee DN. Regulation and regulatory parameters of histone modifications. J Cell Biochem Suppl. 1998;30-31:203-13.
35. Yu C, Markan K, Temple KA, Deplewski D, Brady MJ, Cohen RN. The nuclear receptor corepressorsNCoR and SMRT decrease peroxisome proliferator-activated receptor gamma transcriptional activity and repress 3T3-L1 adipogenesis. J Biol Chem. Apr 8, 2005;280(14):13600-5.
36. Sutanto MM, Ferguson KK, Sakuma H, Ye H, Brady MJ, Cohen RN. The silencing mediator of retinoid and thyroid hormone receptors (SMRT) regulates adipose tissue accumulation and adipocyte insulin sensitivity in vivo. J Biol Chem. Jun 11, 2010;285(24):18485-95.
37. Toubal A, Clement K, Fan R, et al. SMRT-GPS2 corepressor pathway dysregulation coincides with obesity-linked adipocyte inflammation. J Clin Invest. Jan 2, 2013;123(1):362-79.
38. Jack BH, Pearson RC, Crossley M. C-terminal binding protein: A metabolic sensor implicated in regulating adipogenesis. Int J Biochem Cell Biol. May 2011;43(5):693-6.
39. Li L, Xie X, Qin J, et al. The nuclear orphan receptor COUP-TFII plays an essential role in adipogenesis, glucose homeostasis, and energy metabolism. Cell Metab. Jan 7, 2009;9(1):77-87.
40. Lin FJ, Qin J, Tang K, Tsai SY, Tsai MJ. Coup d'Etat: an orphan takes control. Endocr Rev. Jun 2011;32(3):404-21.
41. Cawthorn WP, Bree AJ, Yao Y, et al. Wnt6, Wnt10a and Wnt10b inhibit adi-pogenesis and stimulate osteoblastogenesis through a beta-catenin-dependent mechanism. Bone. Feb 2012;50(2):477-89.
42. Okamura M, Kudo H, Wakabayashi K, et al. COUP-TFII acts downstream of Wnt/beta-catenin signal to silence PPARgamma gene expression and repress adipogenesis. Proc Natl Acad Sci U S A. Apr 7, 2009;106(14):5819-24.
43. Yao Y, Suraokar M, Darnay BG, et al. BSTA promotes mTORC2-mediated phosphorylation of Akt1 to suppress expression of FoxC2 and stimulate adipocyte differentiation. Sci Signal. Jan 8, 2013;6(257):ra2.
44. Davis KE, Moldes M, Farmer SR. The forkhead transcription factor FoxC2inhib-its white adipocyte differentiation. J Biol Chem. Oct 8, 2004;279(41):42453-61.
45. Bruemmer D. Targeting angiogenesis as treatment for obesity. Arterioscler Thromb Vasc Biol. Feb 2012;32(2):161-2.
46. Chilliard Y, Delavaud C, Bonnet M. Leptin expression in ruminants: nutritional and physiological regulations in relation with energy metabolism. Domest Anim Endocrinol. Jul 2005;29(1):3-22.
47. Geary TW, McFadin EL, MacNeil MD, et al. Leptin as a predictor of carcass composition in beef cattle. J Anim Sci. Jan 2003;81(1):1-8.
48. Yamada T, Kawakami S, Nakanishi N. Fat depot-specific differences in angio-genic growth factor gene expression and its relation to adipocyte size in cattle. J Vet Med Sci. Aug 2010;72(8):991-7.
49. Bonnet M, Faulconnier Y, Leroux C, et al. Glucose-6-phosphate dehydrogenase and leptin are related to marbling differences among Limousin and Angus or Japanese Black x Angus steers. J Anim Sci. Nov 2007;85(11):2882-94.
50. Fu Y, Luo N, Klein RL, Garvey WT. Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J Lipid Res. Jul 2005;46(7):1369-79.
51. Combs TP, Wagner JA, Berger J, et al. Induction of adipocyte complement-related protein of 30 kilodaltons by PPARgamma agonists: a potential mechanism of insulin sensitization. Endocrinology. Mar 2002;143(3):998-1007.
52. Shetty S, Ramos-Roman MA, Cho YR, et al. Enhanced fatty acid flux triggered by adiponectin overexpression. Endocrinology. Jan 2012;153(1):113-22.
53. Matsubara M, Maruoka S, Katayose S. Inverse relationship between plasma adi-ponectin and leptin concentrations in normal-weight and obese women. Eur J Endocrinol. Aug 2002;147(2):173-80.
54. Graugnard DE, Piantoni P, Bionaz M, Berger LL, Faulkner DB, Loor JJ. 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. 2009;10:142.
55. La B, Oh D, Lee Y, et al. Association of bovine fatty acid composition with novel missense nucleotide polymorphism in the thyroid hormone-responsive(THRSP) gene. Anim Genet. May 14, 2012;44(1):118.
56. Wang YH, Byrne KA, Reverter A, et al. Transcriptional profiling of skeletal muscle tissue from two breeds of cattle. Mamm Genome. Mar 2005;16(3):201-10.
57. Wang YH, Bower NI, Reverter A, et al. Gene expression patterns during intra-muscular fat development in cattle. J Anim Sci. Jan 2009;87(1):119-30.
58. Bennett MK, Seo YK, Datta S, Shin DJ, Selective bind-ing of sterol regulatory element-binding protein isoforms and co-regulatory proteins to promoters for lipid metabolic genes in liver. J Biol Chem. Jun 6, 2008;283(23):15628-37.
59. Jeong YS, Kim D, Lee YS, et al. Integrated expression profiling and genome-wide analysis of ChREBP targets reveals the dual role for ChREBP in glucose-regulated gene expression. PLoS One. 2011;6(7):e22544.
60. Sun J, Gao Y, Liu D, et al. Haplotype combination of the bovine INSIG1 gene sequence variants and association with growth traits in Nanyang cattle. Genome.Jun 2012;55(6):429-36.
61. Munekata K, Sakamoto K. Forkhead transcription factor Foxo1 is essential for adipocyte differentiation. In Vitro Cell Dev Biol Anim. Dec 2009;45(10):642-51.
62. Fan W, Imamura T, Sonoda N, et al. FOXO1 transrepresses peroxisome proliferator-activated receptor gamma transactivation, coordinating an insulin-induced feed-forward response in adipocytes. J Biol Chem. May 1, 2009;284(18):12188-97.
63. Nakae J, Kitamura T, Kitamura Y, Biggs WH, 3rd, Arden KC, Accili D. The forkhead transcription factor Foxo1 regulates adipocyte differentiation. Dev Cell. Jan 2003;4(1):119-29.
64. Housley MP, Rodgers JT, Udeshi ND, et al. O-GlcNAc regulates FoxO activation in response to glucose. J Biol Chem. Jun 13, 2008;283(24):16283-92.
65. Harvatine KJ, Bauman DE. SREBP1 and thyroid hormone responsive spot 14 (S14) are involved in the regulation of bovine mammary lipid synthesis during diet-induced milk fat depression and treatment with CLA. J Nutr. Oct 2006;136(10):2468-74.
66. Colbert CL, Kim CW, Moon YA, et al. Crystal structure of Spot 14, a modulator of fatty acid synthesis. Proc Natl Acad Sci U S A. Nov 2, 2010;107(44):18820-5.
67. Kim CW, Moon YA, Park SW, Cheng D, Kwon HJ, Horton JD. Induced polymerization of mammalian acetyl-CoA carboxylase by MIG12 provides a tertiary level of regulation of fatty acid synthesis. Proc Natl Acad Sci U S A. May 25, 2010;107(21):9626-31.
68. Inoue J, Yamasaki K, Ikeuchi E, et al. Identification of MIG12 as a mediator for stimulation of lipogenesis by LXR activation. Mol Endocrinol. Jun 2011;25(6):995-1005.
69. Smith SB, Crouse JD. Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J Nutr. Apr 1984;114(4):792-800.
70. Smith SB. Contribution of the pentose cycle to lipogenesis in bovine adipose tissue. Arch Biochem Biophys. Feb 15, 1983;221(1):46-56.
71. Hanson RW, Ballard FJ. The relative significance of acetate and glucose as precursors for lipid synthesis in liver and adipose tissue from ruminants. Biochem J.Nov 1967;105(2):529-36.
72. Smith S. The animal fatty acid synthase: one gene, one polypeptide, seven enzymes. FASEB J. Dec 1994;8(15):1248-59.
73. Jurie C, Cassar-Malek I, Bonnet M, et al. Adipocyte fatty acid-binding protein and mitochondrial enzyme activities in muscles as relevant indicators of mar-bling in cattle. J Anim Sci. Oct 2007;85(10):2660-9.
74. Amri EZ, Bertrand B, Ailhaud G, Grimaldi P. Regulation of adipose cell differentiation. I. Fatty acids are inducers of the aP2 gene expression. J Lipid Res.Sep 1991;32(9):1449-56.
75. Deiuliis J, Shin J, Murphy E, et al. Bovine adipose triglyceride lipase is not altered and adipocyte fatty acid-binding protein is increased by dietary flaxseed.Lipids. Nov 2010;45(11):963-73.
76. Waters SM, Kelly JP, O'Boyle P, Moloney AP, Kenny DA. Effect of level and duration of dietary n-3 polyunsaturated fatty acid supplementation on the tran-scriptional regulation of Delta9-desaturase in muscle of beef cattle. J Anim Sci. Jan 2009;87(1):244-52.
77. Archibeque SL, Lunt DK, Gilbert CD, Tume RK, Smith SB. Fatty acid indices of stearoyl-CoA desaturase do not reflect actual stearoyl-CoA desaturase enzyme activities in adipose tissues of beef steers finished with corn-, flaxseed-, or sorghum-based diets. J Anim Sci. May 2005;83(5):1153-66.
78. Chung KY, Lunt DK, Kawachi H, Yano H, Smith SB. Lipogenesis and stearoyl-CoA desaturase gene expression and enzyme activity in adipose tissue of short-and long-fed Angus and Wagyu steers fed cornor hay-based diets. J Anim Sci. Feb 2007;85(2):380-7.
79. Morcillo S, Martin-Nunez GM, Rojo-Martinez G, et al. ELOVL6 genetic variation is related to insulin sensitivity: a new candidate gene in energy metabolism.PLoS One. 2011;6(6):e21198.
80. Vincent A, Louveau I, Gondret F, Lebret B, Damon M. Mitochondrial function, fatty acid metabolism, and immune system are relevant features of pig adiposetissue development. Physiol Genomics. Nov 15, 2012;44(22):1116-24.
81. Beale EG, Harvey BJ, Forest C. PCK1 and PCK2 as candidate diabetes and obesity genes. Cell Biochem Biophys. 2007;48(2-3):89-95.
82. Beale EG, Hammer RE, Antoine B, Forest C. Disregulated glyceroneogenesis: PCK1 as a candidate diabetes and obesity gene. Trends Endocrinol Metab. Apr 2004;15(3):129-35.
83. Millward CA, Desantis D, Hsieh CW, et al. Phosphoenolpyruvate carboxykinase (Pck1) helps regulate the triglyceride/fatty acid cycle and development of insulin resistance in mice. J Lipid Res. Jun 2010;51(6):1452-63.
84. Semenkovich CF, Wims M, Noe L, Etienne J, Chan L. Insulin regulation of lipoprotein lipase activity in 3T3-L1 adipocytes is mediated at posttranscrip-tional and posttranslational levels. J Biol Chem. May 25, 1989;264(15):9030-8.
85. Payne VA, Au WS, Gray SL, et al. Sequential regulation of diacylglycerol acyltransferase 2 expression by CAAT/enhancer-binding protein beta (C/ EBPbeta) and C/EBPalpha during adipogenesis. J Biol Chem. Jul 20, 2007;282(29):21005-14.
86. Lozeman FJ, Middleton CK, Deng J, et al. Characterization of microsomal diacylglycerol acyltransferase activity from bovine adipose and muscle tissue. Comp Biochem Physiol B Biochem Mol Biol. Aug 2001;130(1):105-15.
87. Kennedy EP. Biosynthesis of complex lipids. Fed Proc. Dec 1961;20:934-40.