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RESEARCH ARTICLE

Effect of β-carotene supplementation on the expression of lipid metabolism-related genes and the deposition of back fat in beef cattle

Q. Jin A , H. B. Zhao A , X. M. Liu A , F. C. Wan A B , Y. F. Liu A , H. J. Cheng A , W. You A , G. F. Liu A and X. W. Tan A
+ Author Affiliations
- Author Affiliations

A Shandong Key Laboratory of Animal Disease Control and Breeding, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, No.8, Sangyuan Road, Ji’nan City, Shandong Province, 250100, China.

B Corresponding author. Email: wanfc@sina.com

Animal Production Science 57(3) 513-519 https://doi.org/10.1071/AN15434
Submitted: 7 August 2015  Accepted: 7 December 2015   Published: 20 April 2016

Abstract

To evaluate the effects of β-carotene (βC) supplementation on lipid metabolism in the back fat of beef cattle, 120 continental crossbred (Simmental × local Luxi yellow cattle) steers were selected randomly from feedlots and allotted to four groups. Each steer was supplemented with 0, 600, 1200, or 1800 mg/day of βC for 90 days, and then received no βC for 60 days (depletion period). The βC levels significantly increased in steers supplemented with βC (P < 0.01), and then decreased to the control level by Day 150. Back fat thickness decreased slightly with increasing βC supplementation, and significantly differed among groups after supplementation ceased (P < 0.01 on Day 120, P < 0.05 on Day 150). Significant regression relationships between βC supplement level and both βC content in back fat tissue on Day 90 and back fat thickness on Days 90, 120, and 150 were established (P < 0.01). No significant differences in the dry matter intake or average daily gain were detected, but higher net meat percentages were observed in the 1200 and 1800 mg/day βC-supplemented groups compared with the control (P < 0.05). The mRNA expression of two fat synthesis-related genes, acetyl-CoA carboxylase and fatty acid synthase, were downregulated during the supplementation period, but upregulated during the next 60 days when the steers received no βC supplementation. In contrast, the expression of two fat hydrolysis-related genes, hormone-sensitive lipase and adipose triglyceride lipase, were upregulated during the supplementation period and downregulated in the subsequent 60 days. The results showed that βC supplementation suppresses back fat deposition in beef cattle by inhibiting fat synthesis and enhancing fat hydrolysis.

Additional keywords: beef quality, carotenoids.


References

Amengual J, Gouranton E, van Helden YG, Hessel S, Ribot J, Kramer E, Kiec-Wilk B, Razny U, Lietz G, Wyss A, Dembinska-Kiec A, Palou A, Keijer J, Landrier JF, Bonet ML, von Lintig J (2011) Beta-carotene reduces body adiposity of mice via BCMO1. PLoS One 6, e20644
Beta-carotene reduces body adiposity of mice via BCMO1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnt1Gqtb0%3D&md5=87a89c987ec5ffbc13b3cb4a4dcdeae7CAS | 21673813PubMed |

Arnett A, Daniel M, Dikeman ME (2008) Restricting vitamin A in cattle diets improves beef carcass marbling and USDA quality and yield grades. Beef Cattle Research 24–27.

Boulanger A, McLemore P, Copeland NG, Gilbert DJ, Jenkins NA, Yu SS (2003) Identification of beta-carotene 15,15ʹ-monooxygenase as a peroxisome proliferator-activated receptor target gene. The FASEB Journal 17, 1304–1306.

Brun T, Roche E, Kim KH, Prentki M (1993) Glucose regulates acetyl-CoA carboxylase gene expression in a pancreatic beta-cell line (INS-1). The Journal of Biological Chemistry 268, 18905–18911.

Condron KN, Lemenager RP, Claeys MC, Lipkie TE, Schoonmaker JP (2014) Supplemental beta-carotene I: effect on plasma vitamin A, growth, performance, and carcass characteristics of feedlot cattle. Meat Science 98, 736–743.
Supplemental beta-carotene I: effect on plasma vitamin A, growth, performance, and carcass characteristics of feedlot cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlWkur7K&md5=f536c459271e2277d2bc1ccf57ea1ba6CAS | 25108270PubMed |

Ferry G, Tellier E, Try A, Grés S, Naime I, Simon MF, Rodriguez M, Boucher J, Tack I, Gesta S (2003) Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation up-regulated expression with adipocyte differentiation and obesity. The Journal of Biological Chemistry 278, 18162–18169.
Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation up-regulated expression with adipocyte differentiation and obesity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjs1Khsro%3D&md5=8899b5540d235194b4d694c87fd46316CAS | 12642576PubMed |

Gibb D, Van Herk FH, Mir P, Loerch S, McAllister T (2011) Removal of supplemental vitamin A from barley-based diets improves marbling in feedlot heifers. Canadian Journal of Animal Science 91, 669–674.
Removal of supplemental vitamin A from barley-based diets improves marbling in feedlot heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XislWnt7o%3D&md5=9f7983ddd815e6bf16ca3d4cdf6bad62CAS |

Gong X, Tsai SW, Yan B, Rubin LP (2006) Cooperation between MEF2 and PPARgamma in human intestinal beta,beta-carotene 15,15ʹ-monooxygenase gene expression. BMC Molecular Biology 7, 7
Cooperation between MEF2 and PPARgamma in human intestinal beta,beta-carotene 15,15ʹ-monooxygenase gene expression.Crossref | GoogleScholarGoogle Scholar | 16504037PubMed |

Gorocica-Buenfil MA, Fluharty FL, Reynolds CK, Loerch SC (2007a) Effect of dietary vitamin A concentration and roasted soybean inclusion on marbling, adipose cellularity, and fatty acid composition of beef. Journal of Animal Science 85, 2230–2242.
Effect of dietary vitamin A concentration and roasted soybean inclusion on marbling, adipose cellularity, and fatty acid composition of beef.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGlsLw%3D&md5=37e2e679a762c3c8acd734e016f702d3CAS | 17468427PubMed |

Gorocica-Buenfil MA, Fluharty FL, Reynolds CK, Loerch SC (2007b) Effect of dietary vitamin A restriction on marbling and conjugated linoleic acid content in Holstein steers. Journal of Animal Science 85, 2243–2255.
Effect of dietary vitamin A restriction on marbling and conjugated linoleic acid content in Holstein steers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGlsL0%3D&md5=e1b979e671031b009b24d38e71d7d92bCAS | 17468420PubMed |

Hossain P, Kawar B, El Nahas M (2007) Obesity and diabetes in the developing world – a growing challenge. The New England Journal of Medicine 356, 213–215.
Obesity and diabetes in the developing world – a growing challenge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1yqtA%3D%3D&md5=a9e0b0589f4b7dfdc0dad88726b9e432CAS | 17229948PubMed |

Jin Q, Cheng H, Wan F, Bi Y, Liu G, Liu X, Zhao H, You W, Liu Y, Tan X (2015) Effects of feeding b-carotene on levels of b-carotene and vitamin A in blood and tissues of beef cattle and the effects on beef quality. Meat Science 110, 293–301.
Effects of feeding b-carotene on levels of b-carotene and vitamin A in blood and tissues of beef cattle and the effects on beef quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVyrs7zJ&md5=07848f238c9d5317df3af512d29c37f6CAS | 26319310PubMed |

Kabagambe E, Furtado J, Baylin A, Campos H (2005) Some dietary and adipose tissue carotenoids are associated with the risk of nonfatal acute myocardial infarction in Costa Rica. The Journal of Nutrition 135, 1763–1769.

Karadas F, Pappas AC, Surai PF, Speake BK (2005) Embryonic development within carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 141, 244–251.
Embryonic development within carotenoid-enriched eggs influences the post-hatch carotenoid status of the chicken.Crossref | GoogleScholarGoogle Scholar |

Liu XM, Fu JL, Song EL, Zang K, Wan FC, Wu NK, Wang AG (2009) Effect of nicotinamide on proliferation, differentiation, and energy metabolism in bovine preadipocytes. Asian-Australasian Journal of Animal Sciences 22, 1320–1327.
Effect of nicotinamide on proliferation, differentiation, and energy metabolism in bovine preadipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtl2jsrnL&md5=2b525291cb01046b091ba88fa42b4365CAS |

Lobo GP, Amengual J, Li HN, Golczak M, Bonet ML, Palczewski K, von Lintig J (2010) Beta,beta-carotene decreases peroxisome proliferator receptor gamma activity and reduces lipid storage capacity of adipocytes in a beta,beta-carotene oxygenase 1-dependent manner. The Journal of Biological Chemistry 285, 27891–27899.
Beta,beta-carotene decreases peroxisome proliferator receptor gamma activity and reduces lipid storage capacity of adipocytes in a beta,beta-carotene oxygenase 1-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOnsL3E&md5=e5222534054a37ed3b3c9448ed21d835CAS | 20573961PubMed |

Luisa Bonet M, Canas JA, Ribot J, Palou A (2015) Carotenoids and their conversion products in the control of adipocyte function, adiposity and obesity. Archives of Biochemistry and Biophysics 572, 112–125.
Carotenoids and their conversion products in the control of adipocyte function, adiposity and obesity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjt1eisL8%3D&md5=f6c94b46b8a14a6ec58cae1a4366f7f9CAS |

McGarry J, Foster D (1980) Regulation of hepatic fatty acid oxidation and ketone body production. Annual Review of Biochemistry 49, 395–420.
Regulation of hepatic fatty acid oxidation and ketone body production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXkvFahur4%3D&md5=24360e2db5254fe1bfab35f226833501CAS | 6157353PubMed |

Östh M, Öst A, Kjolhede P, Strålfors P (2014) The concentration of β-carotene in human adipocytes, but not the whole-body adipocyte stores, is reduced in obesity. PLoS One 9, e85610
The concentration of β-carotene in human adipocytes, but not the whole-body adipocyte stores, is reduced in obesity.Crossref | GoogleScholarGoogle Scholar | 24416432PubMed |

Parker RS (1989) Carotenoids in human blood and tissues. The Journal of Nutrition 119, 101–104.

Reynoso C, Mora O, Nieves V, Shimada A, De Mejıa EG (2004) β-Carotene and lutein in forage and bovine adipose tissue in two tropical regions of Mexico. Animal Feed Science and Technology 113, 183–190.
β-Carotene and lutein in forage and bovine adipose tissue in two tropical regions of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtV2ntrs%3D&md5=182255bb58bad221eebc9314b542ba9bCAS |

Siebert BD, Kruka ZA, Davisb J, Pitchforda WS, Harperc GS, Bottemaa CDK (2006) Effect of low vitamin A status on fat deposition and fatty acid desaturation in beef cattle. Lipids 41, 365–370.
Effect of low vitamin A status on fat deposition and fatty acid desaturation in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtV2isbs%3D&md5=c92b20dd1540943bae80e20f3c8a8905CAS | 16808150PubMed |

Strachan D, Yang A, Dillon R (1993) Effect of grain feeding on fat colour and other carcass characteristics in previously grass-fed Bos indicus steers. Australian Journal of Experimental Agriculture 33, 269–273.
Effect of grain feeding on fat colour and other carcass characteristics in previously grass-fed Bos indicus steers.Crossref | GoogleScholarGoogle Scholar |

Tanos R, Murray IA, Smith PB, Patterson A, Perdew GH (2012) Role of the Ah receptor in homeostatic control of fatty acid synthesis in the liver. Toxicological Sciences 129, 372–379.
Role of the Ah receptor in homeostatic control of fatty acid synthesis in the liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVSms7%2FN&md5=262da54fd3a82a06ddd099fd99cdacdaCAS | 22696238PubMed |

Tourniaire F, Gouranton E, von Lintig J, Keijer J, Luisa Bonet M, Amengual J, Lietz G, Landrier J-F (2009) β-Carotene conversion products and their effects on adipose tissue. Genes & Nutrition 4, 179–187.
β-Carotene conversion products and their effects on adipose tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGgtLrF&md5=29ffea824e922115ff735028db388b66CAS |

Tsutsumi C, Okuno M, Tannous L, Piantedosi R, Allan M, Goodman D, Blaner W (1992) Retinoids and retinoid-binding protein expression in rat adipocytes. The Journal of Biological Chemistry 267, 1805–1810.

Virtanen S, van’t Veer P, Kok F, Kardinaal AFM, Aro A (1996) Predictors of adipose tissue carotenoid and retinol levels in nine countries. The EURAMIC Study. American Journal of Epidemiology 144, 968–979.
Predictors of adipose tissue carotenoid and retinol levels in nine countries. The EURAMIC Study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2Fntl2muw%3D%3D&md5=ccf3d1c3acad2f48caee1bbad8d8538bCAS | 8916508PubMed |

Wakil SJ (1989) Fatty acid synthase, a proficient multifunctional enzyme. Biochemistry 28, 4523–4530.
Fatty acid synthase, a proficient multifunctional enzyme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXit1OntLw%3D&md5=1f509264491c93f9ecbdfba0adb8b1a4CAS | 2669958PubMed |

Wyss A, von Lintig J (2008) Cleavage of β-carotene to retinal. In ‘Carotenoids, volume 4: natural functions’. (Eds G Britton, S Liaaen-Jensen, H Pfander) pp. 325–340. (Birkhäuser: Basel)

Yang A, Larsen TW, Tume RK (1992) Carotenoid and retinol concentrations in serum, adipose tissue and liver and carotenoid transport in sheep, goats and cattle. Australian Journal of Agricultural Research 43, 1809–1817.
Carotenoid and retinol concentrations in serum, adipose tissue and liver and carotenoid transport in sheep, goats and cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktlKg&md5=89077be5591ccf5856b5d36bdcb05f92CAS |

Yang A, McLennan S, Armstrong J, Larsen T, Shaw F, Tume R (1993) Effect of short-term grain feeding on bovine body-fat colour: a cautionary note. Crop and Pasture Science 44, 215–220.
Effect of short-term grain feeding on bovine body-fat colour: a cautionary note.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFWku7o%3D&md5=36463a588441416610c3e551cdb98490CAS |

Zechner R, Kienesberger PC, Haemmerle G, Zimmermann R, Lass A (2009) Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores. Journal of Lipid Research 50, 3–21.
Adipose triglyceride lipase and the lipolytic catabolism of cellular fat stores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFOhsw%3D%3D&md5=371bc1812828f88be17469fa0b31df33CAS | 18952573PubMed |

Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, Riederer M, Lass A, Neuberger G, Eisenhaber F, Hermetter A (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306, 1383–1386.
Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvVektLw%3D&md5=b0e03db627a60b78c20efd3d4da831c1CAS | 15550674PubMed |