Seasonal expressions of GPR41 and GPR43 in the colon of the wild ground squirrels (Spermophilus dauricus)

Submitted: 23 October 2021
Accepted: 2 January 2022
Published: 21 January 2022
Abstract Views: 1159
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G-protein-coupled receptor 41 (GPR41) and G-protein-coupled receptor 43 (GPR43) are important short-chain fatty acids (SCFAs) receptors. Previous studies indicated that GPR41 and GPR43 are involved in the secretion of gastrointestinal peptides, and glucose and lipid metabolism, and are closely related to obesity and type II diabetes, and other diseases. The purpose of the study was to explore the relationship between the GPR41 and GPR43 and seasonal breeding, and provide new prospects for further exploring the nutritional needs of breeding. We identified the localization and expression levels of GPR41 and GPR43 in the colon of the wild ground squirrels (Spermophilus dauricus) both in the breeding season and non-breeding season. The histological results revealed that the lumen diameter of the colon had obvious seasonal changes, and the diameter of the colonic lumen in the non-breeding season was larger than that in the breeding season. Immunohistochemical staining suggested GPR41 and GPR43 have expressed in the simple layer columnar epithelium. In addition, compared with the breeding season, the mRNA and protein expression levels of GPR41 and GPR43 in the colon were higher during the non-breeding season. In general, these results indicated GPR41 and GPR43 might play a certain role in regulating seasonal breeding.

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Savage DC. Gastrointestinal microflora in mammalian nutrition. Annu Rev Nutr 1986;6:155-78. DOI: https://doi.org/10.1146/annurev.nu.06.070186.001103
Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 2001;81:1031-64. DOI: https://doi.org/10.1152/physrev.2001.81.3.1031
Boets E, Deroover L, Houben E, Vermeulen K, Gomand SV, Delcour JA, et al. Quantification of in vivo colonic short chain fatty acid production from insulin. Nutrients 2015;7:8916-29. DOI: https://doi.org/10.3390/nu7115440
Scheppach W. Effects of short chain fatty acids on gut morphology and function. Gut 1994;35:S35-8. DOI: https://doi.org/10.1136/gut.35.1_Suppl.S35
Macia L, Thorburn AN, Binge LC, Marino E, Rogers KE, Maslowski KM, et al. Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases. Immunol Rev 2012;245:164-76. DOI: https://doi.org/10.1111/j.1600-065X.2011.01080.x
Hernández MAG, Canfora EE, Jocken JWE, Blaak EE. The short-chain fatty acid acetate in body weight control and insulin sensitivity. Nutrients 2019;11:1943. DOI: https://doi.org/10.3390/nu11081943
Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre R, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009;58:1509-17. DOI: https://doi.org/10.2337/db08-1637
Lin HV, Frassetto A, Jr EJK, Nawrocki AR, Lu MM, Kosinski JR, et al. Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One 2012;7:e35240. DOI: https://doi.org/10.1371/journal.pone.0035240
Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, et al. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 2003;278:11312-19. DOI: https://doi.org/10.1074/jbc.M211609200
Pan P, Oshima K, Huang Y-W, Agle KA, Drobyski WR, Chen X, et al. Loss of FFAR2 promotes colon cancer by epigenetic dysregulation of inflammation suppressors. Int J Cancer 2018;143:886-96. DOI: https://doi.org/10.1002/ijc.31366
Kimura I, Ichimura A, Ohue-Kitano R, Igarashi M. Free fatty acid receptors in health and disease. Physiol Rev 2020;100:171-210. DOI: https://doi.org/10.1152/physrev.00041.2018
Haraa T, Kashiharaa D, Ichimurac A, Kimuraa I, Tsujimotoa G, Hirasawa A. Role of free fatty acid receptors in the regulation of energy metabolism. Biochim Biophys Acta 2014;1841:1292-300. DOI: https://doi.org/10.1016/j.bbalip.2014.06.002
Le Poul E, Loison C, Struyf S, Springael J-Y, Lannoy V, Decobecq ME, et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J Biol Chem 2003;278:25481-89. DOI: https://doi.org/10.1074/jbc.M301403200
Karaki S-i, Tazoe H, Hayashi H, Kashiwabara H, Tooyama K, Suzuki Y, et al. Expression of the short-chain fatty acid receptor, GPR43, in the human colon. J Mol Histol 2008;39:135-42. DOI: https://doi.org/10.1007/s10735-007-9145-y
Venegas DP, Fuente MKDl, Landskron G, González MJ, Quera R, Dijkstra G, et al. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front Immunol 2019;10:277. DOI: https://doi.org/10.3389/fimmu.2019.01486
Hong Y-H, Nishimura Y, Hishikawa D, Tsuzuki H, Miyahara H, Gotoh C, et al. Acetate and propionate short chain fatty acids stimulate adipogenesis via GPCR43. Endocrinology 2005;146:5092-99. DOI: https://doi.org/10.1210/en.2005-0545
Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, et al. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 2012;61:364-71. DOI: https://doi.org/10.2337/db11-1019
Xiong Y, Miyamoto N, Shibata K, Valasek MA, Motoike T, Kedzierski RM, et al. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc Natl Acad Sci USA 2004;101:1045-50. DOI: https://doi.org/10.1073/pnas.2637002100
Kimuraa I, Inouea D, Maedaa T, Hara T, Ichimura A, Miyauchi S, et al. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc Natl Acad Sci USA 2011;108:8030-35. DOI: https://doi.org/10.1073/pnas.1016088108
Song Y, Yang X, Zhang X, Zhu J, Chen Y, et al. Seasonal expression of extracellular signal regulated kinases in the colon of wild ground squirrels (Spermophilus dauricus). Res Square 2021. Available from: https://www.researchsquare.com/article/rs-841280/v1 DOI: https://doi.org/10.21203/rs.3.rs-841280/v1
Yu W, Zhang Z, Liu P, Yang Y, Zhang H, Yuan Z, et al. Seasonal expressions of SPAG11A and androgen receptor in the epididymis of the wild ground squirrels (Citellus dauricus Brandt). Eur J Histochem 2020;64:3111. DOI: https://doi.org/10.4081/ejh.2020.3111
Yuan Z, Wang Y, Yu W, Xie W, Zhang Z, Wang J, et al. Seasonal expressions of oxytocin and oxytocin receptor in the epididymides in the wild ground squirrels (Citellus Dauricus Brandt). Gen Comp Endocrinol 2020;289:113391. DOI: https://doi.org/10.1016/j.ygcen.2020.113391
Li Q, Zhang F, Zhang S, Sheng X, Han X, Weng Q, et al. Seasonal expression of androgen receptor, aromatase, and estrogen receptor alpha and beta in the testis of the wild ground squirrel (Citellus dauricus Brandt). Eur J Histochem 2015;59:2456. DOI: https://doi.org/10.4081/ejh.2015.2456
Wang J, Liu Q, Qi H, Wang Y, Gao Q, Gao F, et al. Seasonal expressions of androgen receptor, P450arom and estrogen receptors in the epididymis of the wild ground squirrel (Citellus dauricus Brandt). Gen Comp Endocrinol 2019;270:131-38. DOI: https://doi.org/10.1016/j.ygcen.2018.10.017
Wang Y, Wang Z, Yu W, Sheng X, Zhang H, Han Y, et al. Seasonal expressions of androgen receptor, estrogen receptors and cytochrome P450 aromatase in the uteri of the wild Daurian ground squirrels (Spermophilus dauricus). Eur J Histochem 2018;62:2889. DOI: https://doi.org/10.4081/ejh.2018.2889
Yang X, Yao Y, Zhang X, Zhong J, Gao F, et al. Seasonal changes in the distinct taxonomy and function of the gut microbiota in the wild ground squirrel (Spermophilus dauricus). Animals 2021;11:2685. DOI: https://doi.org/10.3390/ani11092685
Chang SC, Shen MH, Liu CY, Pu CM, Hu JM, Huang CJ. A gut butyrate-producing bacterium Butyricicoccus pullicaecorum regulates short-chain fatty acid transporter and receptor to reduce the progression of 1,2-dimethylhydrazine-associated colorectal cancer. Oncol Lett.2020;20:327-36. DOI: https://doi.org/10.3892/ol.2020.12190
Karaki S, Mitsui R, Hayashi H, Kato I, Sugiya H, Iwanaga T, et al. Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and mucosal mast cells in rat intestine. Cell Tissue Res 2006;324:353-60. DOI: https://doi.org/10.1007/s00441-005-0140-x
Tazoe H, Otomo Y, Karaki S-I, Kato I, Fukami Y, Terasaki M, et al. Expression of short-chain fatty acid receptor GPR41 in the human colon. Biomed Res 2009;30:149-56. DOI: https://doi.org/10.2220/biomedres.30.149
Kaji I, Karaki S-i, Tanaka R, Kuwahara A. Density distribution of free fatty acid receptor 2 (FFA2)-expressing and GLP-1-producing enteroendocrine L cells in human and rat lower intestine, and increased cell numbers after ingestion of fructo-oligosaccharide. J Mol Histol 2011;42:27-38. DOI: https://doi.org/10.1007/s10735-010-9304-4
Buffa R, Capella C, Fontana P, Usellini L, Solcia E. Types of endocrine cells in the human colon and rectum. Cell Tissue Res 1978;192:227-40. DOI: https://doi.org/10.1007/BF00220741
Samuel BS, Shaito A, Motoike T, Rey FE, Backhed F, Manchester JK, et al. Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci USA 2008;105:16767-72. DOI: https://doi.org/10.1073/pnas.0808567105
Zaibi MS, Stocker CJ, O'Dowd J, Davies A, Bellahcene M, Cawthorne MA, et al. Roles of GPR41 and GPR43 in leptin secretory responses of murine adipocytes to short chain fatty acids. FEBS Lett 2010;584:2381-86. DOI: https://doi.org/10.1016/j.febslet.2010.04.027
Giroud S, Habold C, Nespolo RF, Mejías C, Terrien J, Logan SM, et al. The torpid state: Recent advances in metabolic adaptations and protective mechanisms (dagger). Front Physiol 2020;11:623665. DOI: https://doi.org/10.3389/fphys.2020.623665
Tang C, Ahmed K, Gille A, Lu S, Gröne HJ, Tunaru S, et al. Loss of FFA2 and FFA3 increases insulin secretion and improves glucose tolerance in type 2 diabetes. Nat Med 2015;21:173-7. DOI: https://doi.org/10.1038/nm.3779
Veprik A, Laufer D, Weiss S, Rubins N, Walker MD. GPR41 modulates insulin secretion and gene expression in pancreatic beta-cells and modifies metabolic homeostasis in fed and fasting states. FASEB J 2016;30:3860-69. DOI: https://doi.org/10.1096/fj.201500030R
Kimura I, Ozawa K, Inoue D, Imamura T, Kimura K, Maeda T, et al. The gut microbiota suppresses insulin-mediated fat accumulation via the short-chain fatty acid receptor GPR43. Nat Commun 2013;4:1829. DOI: https://doi.org/10.1038/ncomms2852
Chi F, Sharpley MS, Nagaraj R, Roy SS, Banerjee U. Glycolysis-independent glucose metabolism distinguishes TE from ICM fate during mammalian embryogenesis. Dev Cell 2020;53:9-26-e24. DOI: https://doi.org/10.1016/j.devcel.2020.02.015
Thompson DJG, Simpson AC, Pugh PA, Tervit HR. Requirement for glucose during in vitro culture of sheep preimplantation embryos. Mol Reprod Dev 1992;31:253-57. DOI: https://doi.org/10.1002/mrd.1080310405

How to Cite

Yang, X., Liu, X., Song, F., Wei, H., Gao, F., Zhang, H., … Yuan, Z. (2022). Seasonal expressions of GPR41 and GPR43 in the colon of the wild ground squirrels (<em>Spermophilus dauricus</em>). European Journal of Histochemistry, 66(1). https://doi.org/10.4081/ejh.2022.3351

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