Skip to main content Accessibility help
×
×
Home

Postnatal differential expression of chemoreceptors of free fatty acids along the gastrointestinal tract of supplemental feeding v. grazing kid goats

  • T. Ran (a1) (a2), Y. Liu (a1), J. Z. Jiao (a1), C. S. Zhou (a1) (a3), S. X. Tang (a1) (a3), M. Wang (a1) (a3), Z. X. He (a1), Z. L. Tan (a1) (a3), W. Z. Yang (a2) and K. A. Beauchemin (a2)...

Abstract

The gastrointestinal tract (GIT) of animals is capable of sensing various kinds of nutrients via G-protein coupled receptor-mediated signaling transduction pathways, and the process is known as ‘gut nutrient chemosensing’. GPR40, GPR41, GPR43 and GPR119 are chemoreceptors for free fatty acids (FFAs) and lipid derivatives, but they are not well studied in small ruminants. The objective of this study is to determine the expression of GPR40, GPR41, GPR43 and GPR119 along the GIT of kid goats under supplemental feeding (S) v. grazing (G) during early development. In total, 44 kid goats (initial weight 1.35±0.12 kg) were slaughtered for sampling (rumen, abomasum, duodenum, jejunum, ileum, cecum, colon and rectum) between days 0 and 70. The expression of GPR41 and GPR43 were measured at both mRNA and protein levels, whereas GPR40 and GPR119 were assayed at protein level only. The effects of age and feeding system on their expression were variable depending upon GIT segments, chemoreceptors and expression level (mRNA or protein), and sometimes feeding system × age interactions (P<0.05) were observed. Supplemental feeding enhanced expression of GPR40, GPR41 and GPR43 in most segments of the GIT of goats, whereas G enhanced expression of GPR119. GPR41 and GPR43 were mainly expressed in rumen, abomasum and cecum, with different responses to age and feeding system. GPR41 and GPR43 expression in abomasum at mRNA level was greatly (P<0.01) affected by both age and feeding system; whereas their expression in rumen and abomasum at protein level were different, feeding system greatly (P<0.05) affected GPR41 expression, but had no effect (P>0.05) on GPR43 expression; and there were no feeding system×age interactions (P>0.05) on GPR41 and GPR43 protein expression. The expression of GPR41 and GPR43 in rumen and abomasum linearly (P<0.01) increased with increasing age (from days 0 to 70). Meanwhile, age was the main factor affecting GPR40 expression throughout the GIT. These outcomes indicate that age and feeding system are the two factors affecting chemoreceptors for FFAs and lipid derivatives expression in the GIT of kids goats, and S enhanced the expression of chemoreceptors for FFAs, whereas G gave rise to greater expression of chemoreceptors for lipid derivatives. Our results suggest that enhanced expression of chemoreceptors for FFAs might be one of the benefits of early supplemental feeding offered to young ruminants during early development.

Copyright

Corresponding author

E-mail: zcs@isa.ac.cn

References

Hide All
Briscoe, CP, Tadayyon, M, Andrews, JL, Benson, WG, Chambers, JK, Eilert, MM, Ellis, C, Elshourbagy, NA, Goetz, AS, Minnick, DT, Murdock, PR, Sauls, HR, Shabon, U, Spinage, LD, Strum, JC, Szekeres, PG, Tan, KB, Way, JM, Ignar, DM, Wilson, S and Muir, AI 2003. The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. Journal of Biological Chemistry 278, 1130311311.
Brown, AJ, Goldsworthy, SM, Barnes, AA, Eilert, MM, Tcheang, L, Daniels, D, Muir, AI, Wigglesworth, MJ, Kinghorn, I, Fraser, NJ, Pike, NB, Strum, JC, Steplewski, KM, Murdock, PR, Holder, JC, Marshall, FH, Szekeres, PG, Wilson, S, Ignar, DM, Foord, SM, Wise, A and Dowell, SJ 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.
Coverdale, JA, Tyler, HD, Quigley, JD and Brumm, JA 2004. Effect of various levels of forage and form of diet on rumen development and growth in calves. Journal of Dairy Science 87, 25542562.
Covington, DK, Briscoe, CA, Brown, AJ and Jayawickreme, CK 2006. The G-protein-coupled receptor 40 family (GPR40-GPR43) and its role in nutrient sensing. Biochemical Society Transactions 34, 770773.
Edfalk, S, Steneberg, P and Edlund, H 2008. Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 57, 22802287.
Ekberg, JH, Hauge, M, Kristensen, LV, Madsen, AN, Engelstoft, MS, Husted, AS, Sichlau, R, Egerod, KL, Timshel, P, Kowalski, TJ, Gribble, FM, Reiman, F, Hansen, HS, Howard, AD, Holst, B and Schwartz, TW 2016. GPR119, a major enteroendocrine sensor of dietary triglyceride metabolites co-acting in synergy with FFA1 (GPR40). Endocrinology 157, 45614569.
Feng, XT, Leng, J, Xie, Z, Li, SL, Zhao, W and Tang, QL 2012. GPR40: a therapeutic target for mediating insulin secretion (review). International Journal of Molecular Medicine 30, 12611266.
Hansen, HS, Rosenkilde, MM, Holst, JJ and Schwartz, TW 2012. GPR119 as a fat sensor. Trends in Pharmacological Sciences 33, 374381.
Hirasawa, A, Tsumaya, K, Awaji, T, Katsuma, S, Adachi, T, Yamada, M, Sugimoto, Y, Miyazaki, S and Tsujimoto, G 2005. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nature Medicine 11, 9094.
Ichimura, A, Hasegawa, S, Kasubuchi, M and Kimura, I 2014. Free fatty acid receptors as therapeutic targets for the treatment of diabetes. Frontiers in Pharmacology 5, 16.
Itoh, Y, Kawamata, Y, Harada, M, Kobayashi, M, Fujii, R, Fukusumi, S, Ogi, K, Hosoya, M, Tanaka, Y, Uejima, H, Tanaka, H, Maruyama, M, Satoh, R, Okubo, S, Kizawa, H, Komatsu, H, Matsumura, F, Noguchi, Y, Shinohara, T, Hinuma, S, Fujisawa, Y and Fujino, M 2003. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173176.
Jiao, JZ, Li, XP, Beauchemin, KA, Tan, ZL, Tang, SX and Zhou, CS 2015. Rumen development process in goats as affected by supplemental feeding v. grazing: age-related anatomic development, functional achievement and microbial colonisation. British Journal of Nutrition 113, 888900.
Karaki, S, Tazoe, H, Hayashi, H, Kashiwabara, H, Tooyama, K, Suzuki, Y and Kuwahara, A 2008. Expression of the short-chain fatty acid receptor, GPR43, in the human colon. Journal of Molecular Histology 39, 135142.
Lane, MA, Baldwin, RL and Jesse, BW 2002. Developmental changes in ketogenic enzyme gene expression during sheep rumen development. Journal of Animal Science 80, 15381544.
Li, HZ, Ran, T, He, ZX, Yan, QX, Tang, SX and Tan, ZL 2016. Postnatal developmental changes of the small intestinal villus height, crypt depth and hexose transporter mRNA expression in supplemental feeding and grazing goats. Small Ruminant Research 141, 106112.
Liou, AP, Lu, X, Sei, Y, Zhao, X, Pechhold, S, Carrero, RJ, Raybould, HE and Wank, S 2011. The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 140, 903912.
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402408.
Lu, ZY, Gui, HB, Yao, L, Yan, L, Martens, H, Aschenbach, JR and Shen, ZM 2015. Short-chain fatty acids and acidic pH upregulate UT-B, GPR41, and GPR4 in rumen epithelial cells of goats. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 308, R283R293.
Mace, OJ and Marshall, F 2013. Digestive physiology of the pig symposium: gut chemosensing and the regulation of nutrient absorption and energy supply. Journal of Animal Science 91, 19321945.
Nguyen, CA, Akiba, Y and Kaunitz, JD 2012. Recent advances in gut nutrient chemosensing. Current Medicinal Chemistry 19, 2834.
Nilsson, NE, Kotarsky, K, Owman, C and Olde, B 2003. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochemical and Biophysical Research Communications 303, 10471052.
Overton, HA, Babbs, AJ, Doel, SM, Fyfe, MCT, Gardner, LS, Griffin, G, Jackson, HC, Procter, MJ, Rasamison, CM, Tang-Christensen, M, Widdowson, PS, Williams, GM and Reynet, C 2006. Deorphanization of a G protein-coupled receptor for oleoylethanolamide and its use in the discovery of small-molecule hypophagic agents. Cell Metabolism 3, 167175.
Ran, T, Li, HZ, Liu, Y, Zhou, CS, Tang, SX, Han, XF, Wang, M, He, ZX, Kang, JH, Yan, QX, Tan, ZL and Beauchemin, KA 2016a. Cloning, phylogenetic analysis, and distribution of free fatty acid receptor GPR120 expression along the gastrointestinal tract of housing versus grazing kid goats. Journal of Agricultural and Food Chemistry 64, 23332341.
Ran, T, Li, HZ, Liu, Y, Tang, SX, Han, XF, Wang, M, He, ZX, Kang, JH, Yan, QX, Tan, ZL and Zhou, CS 2016b. Expression of genes related to sweet taste receptors and monosaccharides transporters along the gastrointestinal tracts at different development stages in goats. Livestock Science 188, 111119.
Rasoamanana, R, Darcel, N, Fromentin, G and Tome, D 2012. Nutrient sensing and signalling by the gut. The Proceedings of the Nutrition Society 71, 446455.
Reimann, F, Tolhurst, G and Gribble, FM 2012. G-protein-coupled receptors in intestinal chemosensation. Cell Metabolism 15, 421431.
Steinert, RE and Beglinger, C 2011. Nutrient sensing in the gut: interactions between chemosensory cells, visceral afferents and the secretion of satiation peptides. Physiology & Behavior 105, 6270.
Tazoe, H, Otomo, Y, Kaji, I, Tanaka, R, Karaki, SI and Kuwahara, A 2008. Roles of short-chain fatty acids receptors, Gpr41 and Gpr43 on colonic functions. Journal of Physiology and Pharmacology 59, 251262.
Tolhurst, G, Reimann, F and Gribble, FM 2012. Intestinal sensing of nutrients. Handbook of Experimental Pharmacology 209, 309335.
Yan, QX, Tang, SX, Tan, ZL, Han, XF, Zhou, CS, Kang, JH and Wang, M 2015. Proteomic analysis of isolated plasma membrane fractions from the mammary gland in lactating cows. Journal of Agricultural and Food Chemistry 63, 73887398.
Zeng, JY 2009. Effects of short chain fatty acids on nutrition metabolism and immune of growing goats in vitro. PhD thesis, Graduate University of Chinese Academy of Sciences, Beijing, P.R. China.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

animal
  • ISSN: 1751-7311
  • EISSN: 1751-732X
  • URL: /core/journals/animal
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Ran et al. supplementary material
Ran et al. supplementary material 1

 Word (15 KB)
15 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed