Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-18T01:58:26.907Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  10 July 2018

T. Ran ,
Y. Liu ,
J. Z. Jiao ,
C. S. Zhou ,
S. X. Tang ,
M. Wang ,
Z. X. He ,
Z. L. Tan ,
W. Z. Yang  and
K. A. Beauchemin
T. Ran
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China Lethbridge Research Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta T1J 4B1, Canada
Y. Liu
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China
J. Z. Jiao
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China
C. S. Zhou*
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
S. X. Tang
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
M. Wang
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
Z. X. He
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China
Z. L. Tan
Affiliation:
Key Laboratory for Agro-Ecological Processes in Subtropical Region, and National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, and South-Central Experimental Station of Animal Nutrition and Feed Science in Ministry of Agriculture, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, Hunan 410125, P.R. China Hunan Co-Innovation Center of Animal Production Safety, CICAPS, Changsha, Hunan 410128, P.R. China
W. Z. Yang
Affiliation:
Lethbridge Research Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta T1J 4B1, Canada
K. A. Beauchemin
Affiliation:
Lethbridge Research Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta T1J 4B1, Canada
*
†E-mail: [email protected]
Get access

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.

Keywords

short-chain fatty acidsgut nutrient chemosensingfeeding system developmental changesgoat
Type
Research Article
Information
animal , Volume 13 , Issue 3 , March 2019 , pp. 509 - 517
Copyright
© The Animal Consortium 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 11303–11311.Google Scholar
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, 11312–11319.Google Scholar
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, 2554–2562.Google Scholar
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, 770–773.Google Scholar
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, 2280–2287.Google Scholar
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, 4561–4569.Google Scholar
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, 1261–1266.Google Scholar
Hansen, HS, Rosenkilde, MM, Holst, JJ and Schwartz, TW 2012. GPR119 as a fat sensor. Trends in Pharmacological Sciences 33, 374–381.Google Scholar
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, 90–94.Google Scholar
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, 1–6.Google Scholar
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, 173–176.Google Scholar
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, 888–900.Google Scholar
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, 135–142.Google Scholar
Lane, MA, Baldwin, RL and Jesse, BW 2002. Developmental changes in ketogenic enzyme gene expression during sheep rumen development. Journal of Animal Science 80, 1538–1544.Google Scholar
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, 106–112.Google Scholar
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, 903–912.Google Scholar
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, 402–408.Google Scholar
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, R283–R293.Google Scholar
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, 1932–1945.Google Scholar
Nguyen, CA, Akiba, Y and Kaunitz, JD 2012. Recent advances in gut nutrient chemosensing. Current Medicinal Chemistry 19, 28–34.Google Scholar
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, 1047–1052.Google Scholar
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, 167–175.Google Scholar
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, 2333–2341.Google Scholar
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, 111–119.Google Scholar
Rasoamanana, R, Darcel, N, Fromentin, G and Tome, D 2012. Nutrient sensing and signalling by the gut. The Proceedings of the Nutrition Society 71, 446–455.Google Scholar
Reimann, F, Tolhurst, G and Gribble, FM 2012. G-protein-coupled receptors in intestinal chemosensation. Cell Metabolism 15, 421–431.Google Scholar
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, 62–70.Google Scholar
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, 251–262.Google Scholar
Tolhurst, G, Reimann, F and Gribble, FM 2012. Intestinal sensing of nutrients. Handbook of Experimental Pharmacology 209, 309–335.Google Scholar
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, 7388–7398.Google Scholar
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.Google Scholar
Supplementary material: File

Ran et al. supplementary material

Ran et al. supplementary material 1

Download Ran et al. supplementary material(File)
File 14.8 KB