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Calcium propionate supplementation improves development of rumen epithelium in calves via stimulating G protein-coupled receptors

Published online by Cambridge University Press:  26 February 2018

X. Z. Zhang
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
W. B. Chen
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
X. Wu
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
Y. W. Zhang
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
Y. M. Jiang
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
Q. X. Meng
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
Z. M. Zhou*
Affiliation:
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, P. R. China
*
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Abstract

In the present study, calcium propionate (CaP) was used as feed additive in the diet of calves to investigate their effects on rumen fermentation and the development of rumen epithelium in calves. To elucidate the mechanism in which CaP improves development of calf rumen epithelium via stimulating the messenger RNA (mRNA) expression of G protein-coupled receptors, a total of 54 male Jersey calves (age=7±1 days, BW=23.1±1.2 kg) were randomly divided into three treatment groups: control without CaP supplementation (Con), 5% CaP supplementation (5% CaP) and 10% CaP supplementation (10% CaP). The experiment lasted 160 days and was divided into three feeding stages: Stage 1 (days 0 to 30), Stage 2 (days 31 to 90) and Stage 3 (days 91 to 160). Calcium propionate supplementation percentages were calculated on a dry matter basis. In total, six calves from each group were randomly selected and slaughtered on days 30, 90 and 160 at the conclusion of each experimental feeding stage. Rumen fermentation was improved with increasing concentration of CaP supplementation in calves through the first 30 days (Stage 1). No effects of CaP supplementation were observed on rumen fermentation in calves during Stage 2 (days 31 to 90). Supplementation with 5% CaP increased propionate concentration, but not acetate and butyrate in calves during Stage 3 (days 91 to 160). The rumen papillae length of calves in the 5% CaP supplementation group was greater than that of Con groups in calves after 160 days feeding. The mRNA expression of G protein-coupled receptor 41 (GPR41) and GPR43 supplemented with 5% CaP were greater than the control group and 10% CaP group in feeding 160 days calves. 5% CaP supplementation increased the mRNA expression of cyclin D1, whereas did not increase the mRNA expression of cyclin-dependent kinase 4 compared with the control group in feeding 160-day calves. These results indicate that propionate may act as a signaling molecule to improve rumen epithelium development through stimulating mRNA expression of GPR41 and GPR43.

Type
Research Article
Copyright
© The Animal Consortium 2018 

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Footnotes

a

Present address: College of Animal Science, Inner Mongolia Agricultural University, Hohhot, 010018, P. R. China.

References

Abdoun, K, Stumpff, F and Martens, H 2006. Ammonia and urea transport across the rumen epithelium: a review. Animal Health Research Reviews 7, 4359.Google Scholar
Alexandria, VT 2002. Calcium propionate. Center for Food and Nutrition Policy (CFNP) TAP Review 8, 119.Google Scholar
Anil, MH and Forbes, JM 1980. Feeding in sheep during intraportal infusions of short-chain fatty acids and the effect of liver denervation. Journal of Physiology 298, 407417.Google Scholar
Association of Official Analytical Chemists 1990. Official methods of analysis, 15th edition. AOAC, Arlington, VA, USA.Google Scholar
Baldin, V, Lukas, J, Marcote, MJ, Pagano, M and Draetta, G 1993. Cyclin D1 is a nuclear-protein required for cell-cycle progression in G1. Genes & Development 7, 812821.Google Scholar
Bergman, EN 1975. Production and utilization of metabolites by the alimentary tract as measured in portal and hepatic. In Digestion and metabolism in the ruminant (ed. IW McDonald and ACI Warner), pp. 292305. University of New England Publishing Unit, Armidale, NSW, Australia.Google Scholar
Bergman, EN 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567590.Google Scholar
Broderick, GA and Kang, JH 1980. Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. Journal of Dairy Science 63, 6475.Google Scholar
Brown, AJ, Goldsworthy, SM and Barnes, AA 2003. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. Journal of Biological Chemistry 278, 1131211319.Google Scholar
Erwin, E, Marco, G and Emery, E 1961. Volatile fatty acid analysis of blood and rumen fluid by gas chromatography. Journal of Dairy Science 44, 17681771.Google Scholar
Gäbel, G, Aschenbach, JR and Muller, F 2002. Transfer of energy substrates across the ruminal epithelium: implications and limitations. Animal Health Research Reviews 3, 1530.Google Scholar
Gilliland, RL, Bush, LJ and Friend, JD 1962. Relation of ration composition to rumen development in early-weaned dairy calves with observations on ruminal Parakeratosis. Journal of Dairy Science 45, 12111217.Google Scholar
Gorka, P, Kowalski, ZM, Pietrzak, P, Kotunia, A, Kiljanczyk, R, Flaga, J, Holst, JJ, Guilloteau, P and Zabielski, R 2009. Effect of sodium butyrate supplementation in milk replacer and starter diet on rumen development in calves. Journal of Physiology and Pharmacology 60 (suppl. 3), 4753.Google Scholar
Graham, C and Simmons, NL 2005. Functional organization of the bovine rumen epithelium. American Journal of Physiology Regulatory Integrative & Comparative Physiology 288, R173.Google Scholar
Hamada, TS 1976. Factors influencing growth of rumen, liver and other organs in kids weaned from milk replacers to solid foods. Journal of Dairy Science 59, 11101118.Google Scholar
Hong, YH, Nishimura, Y, Hishikawa, D, Tsuzuki, H, Miyahara, H, Gotoh, C, Choi, KC, Feng, DD, Chen, C, Lee, HG, Katoh, K, Roh, SG and Sasaki, S 2005. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology 146, 50925099.Google Scholar
Krause, KM and Oetzel, GR 2006. Understanding and preventing subacute ruminal acidosis in dairy herds: a review. Animal Feed Science and Technology 126, 215236.Google Scholar
Lane, MA and Jesse, BW 1997. Effect of volatile fatty acid infusion on development of the rumen epithelium in neonatal sheep. Journal of Dairy Science 80, 740746.Google Scholar
Lee, SH and Hossner, KL 2002. Coordinate regulation of ovine adipose tissue gene express by propionate. Journal of Animal Science 80, 28402849.Google Scholar
Lesmeister, KE, Tozer, PR and Heinrichs, AJ 2004. Development and analysis of a rumen tissue sampling procedure. Journal of Dairy Science 87, 13361344.Google Scholar
Liu, Q, Wang, C, Guo, G, Yang, WZ, Dong, KH, Huang, YX, Yang, XM and He, DC 2009. Effects of calcium propionate on rumen fermentation, urinary excretion of purine derivatives and feed digestibility in steers. Journal of Agricultural Sciences 14, 201209.Google Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402408.Google Scholar
Malhi, M, Gui, HB, Yao, L, Aschenbach, JR, Gäbel, G and Shen, ZM 2013. Increased papillae growth and enhanced short-chain fatty acid absorption in the rumen of goats are associated with transient increases in cyclin D1 expression after ruminal butyrate infusion. Journal of Dairy Science 96, 76037616.Google Scholar
Mathew, OP, Ranganna, K and Yatsu, FM 2010. Butyrate, an HDAC inhibitor, stimulates interplay between different posttrans-lational modifications of histone H3 and differently alters G1-specific cell cycle proteins in vascular smooth muscle cells. Biomedicine & Pharmacotherapy 64, 733740.Google Scholar
Noble, MEM, Endicott, JA, Brown, NR and Johnson, LN 1997. The cyclin box fold: Protein recognition in cell-cycle and transcription control. Trends in Biochemical Sciences 22, 482487.Google Scholar
NRC 2000. Nutrient requirements of beef cattle, 7th edition. National Academic Press, Washington, DC, USA.Google Scholar
Pardee, AB 1989. G1 events and regulation of cell-proliferation. Science 246, 603608.Google Scholar
Penner, GB, Aschenbach, JR, Gabel, G, Rackwitz, R and Oba, M 2009. Epithelial capacity for apical uptake of short chain fattyacids is a key determinant for intraruminal pH and the susceptibility to subacute ruminal acidosis in sheep. Journal of Nutrition 139, 17141720.Google Scholar
Poul, LE, Loison, C, Struyf, S, Springael, JY, Lannoy, V, Decobeeq, ME, Brezillon, S and Detheux, M 2003. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. Journal of Biological Chemistry 278, 2548125489.Google Scholar
Roy, CC, Kien, CL and Bouthillier, L 2006. Short-chain fatty acids: ready for prime time. Nutrition in Clinical Practice 21, 351366.Google Scholar
Sakata, T and Tamate, H 1979. Rumen epithelium cell proliferation accelerated by propionate and acetate. Journal of Dairy Science 62, 4952.Google Scholar
Sander, EG, Warner, RG, Harrison, HN and Loosli, JK 1959. The stimulatory effect of sodium butyrate and sodium propionate on the development of rumen mucosa in the young calf. Journal of Dairy Science 42, 16001605.Google Scholar
Tamate, H, McGilliard, AD, Jacobson, NL and Getty, R 1962. Effect of various dietaries on the anatomical development of the stomach in the calf. Journal of Dairy Science 45, 408420.Google Scholar
Van Soest, PJ., Robertson, JB and Lewis, BA 1991. Methods for dietary, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 35833597.Google Scholar
Venkatakrishnan, AJ, Deupi, X, Lebon, G, Tate, CG, Schertler, GF and Babu, MM 2013. Molecular signatures of G-protein-coupled receptors. Nature 494, 185194.Google Scholar
Wan, R 2009. Regulation of propionate on adipogenesis of bovine intramuscular preadipocytes. China Agricultural University, Beijing, China.Google Scholar
Wang, A, Akers, RM and Jiang, H 2012. Short communication: presence of G protein-coupled receptor 43 in rumen epithelium but not in the islets of Langerhans in cattle. Journal of Dairy Science 95, 13711375.Google Scholar
Xiao, XJ, Alugongo, GM, Chuang, R, Dong, SZ, Li, SL, Yoon, I, Wu, Z.H and Cao, ZJ 2015. Effects of Saccharomyces cerevisiae fermentation products on dairy calves: ruminal fermentation, gastrointestinal morphology, and microbial community. Journal of Dairy Science 99, 54015412.Google Scholar
Xie, XX, Meng, QX, Liu, P, Wu, H, Li, SR, Ren, LP and Li, XZ 2013. Effects of a mixture of steam-flaked corn and extruded soybeans on performance, ruminal development, ruminal fermentation, and intestinal absorptive capability in veal calves. Journal of Animal Science 91, 43154321.Google Scholar
Xiong, Y, Miyamoto, N and Shibata, K 2004. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein coupled receptor GPCR41. Proceedings of the National Academy of Sciences of the United States of America 101, 10451050.Google Scholar
Yonezawa, T, Haga, S, Kobayashi, Y, Katoh, K and Obara, Y 2009. Short-chain fatty acid signaling pathways in bovine mammary epithelial cells. Regulatory Peptides 153, 3036.Google Scholar
Zhang, XZ, Meng, QX, Lu, L, Cui, ZL and Ren, LP 2015. The effect of calcium propionate supplementation on performance, meat quality, and mRNA expression of finishing steers fed a high-concentrate diet. Journal of Animal and Feed Sciences 24, 100106.Google Scholar
Zhang, XZ, Wu, X, Chen, WB, Zhang, YW, Jiang, YM, Meng, QX and Zhou, ZM 2017. Growth performance and development of internal organ, and gastrointestinal tract of calf supplementation with calcium propionate at various stages of growth period. PLoS One 12, e0179940.Google Scholar