Gender Difference in Intestinal Bile Acid Profiles in C57BL/6 Mice

  • ZHANG Cong-cong ,
  • WU Jun-fang ,
  • WANG Yu-lan
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  • 1. State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan(Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences), Wuhan 430071, China;
    2. University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2018-04-17

  Online published: 2018-08-28

Abstract

Gut microbiota is important for human health. The complex relationship between intestinal flora and bile acid profile has been studied previously. However, few previous studies have determined the profile and functions of bile acids in different intestinal segments, and whether they are related to the distribution of intestinal flora. In this paper, we measured the distribution of bile acids in different intestinal segments of male and female C57BL/6 mice with ultra-high performance liquid chromatography coupled with triple quadrupole mass spectrometry (UPLC-QqQ-MS) based targeted metabonomics analysis and nuclear magnetic resonance (NMR) based untargeted metabonomics analysis. Gender difference in distributions of bile acids were observed, which was more evident in the lower parts of intestine than in the upper part of intestine, especially in the cecum segment. This might be related to the abundance of gut microflora in different intestine segments. This study provided metabolic phenotypes of bile acids in mice of different genders, and demonstrated their interactions with gut microbiota.

Cite this article

ZHANG Cong-cong , WU Jun-fang , WANG Yu-lan . Gender Difference in Intestinal Bile Acid Profiles in C57BL/6 Mice[J]. Chinese Journal of Magnetic Resonance, 2018 , 35(3) : 328 -337 . DOI: 10.11938/cjmr20182633

References

[1] XU J, GORDON J I. Honor thy symbionts[J]. Proc Natl Acad Sci U S A, 2003, 100(18):10452-10459.
[2] MARTIN F P, DUMAS M E, WANG Y L, et al. A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model[J]. Mol Syst Biol, 2007, 3:112.
[3] CLAUS S P, TSANG T M, WANG Y L, et al. Systemic multicompartmental effects of the gut microbiome on mouse metabolic phenotypes[J]. Mol Syst Biol, 2008, 4:219.
[4] WIKOFF W R, ANFORA A T, LIU J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites[J]. Proc Natl Acad Sci U S A, 2009, 106(10):3698-3703.
[5] PARLESAK A, SCHAECKELER S, MOSER L, et al. Conjugated primary bile salts reduce permeability of endotoxin through intestinal epithelial cells and synergize with phosphatidylcholine in suppression of inflammatory cytokine production[J]. Crit Care Med, 2007, 35(10):2367-2374.
[6] RAMIREZ-PEREZ O, CRUZ-RAMON V, CHINCHILLA-LOPEZ P, et al. The role of the gut microbiota in bile acid metabolism[J]. Ann Hepatol, 2017, 16(Suppl. 1:s3-105.):s15-s20.
[7] SAYIN S I, WAHLSTROM A, FELIN J, et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist[J]. Cell Metab, 2013, 17(2):225-235.
[8] WAHLSTROM A, SAYIN S I, MARSCHALL H U, et al. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism[J]. Cell Metab, 2016, 24(1):41-50.
[9] STALEY C, WEINGARDEN A R, KHORUTS A, et al. Interaction of gut microbiota with bile acid metabolism and its influence on disease states[J]. Appl Microbiol Biotechnol, 2017, 101(1):47-64.
[10] HOFMANN A F. The continuing importance of bile acids in liver and intestinal disease[J]. Arch Intern Med, 1999, 159(22):2647-2658.
[11] RAO A, KOSTERS A, MELLS J E, et al. Inhibition of ileal bile acid uptake protects against nonalcoholic fatty liver disease in high-fat diet-fed mice[J]. Sci Transl Med, 2016, 8(357):357ra122.
[12] THOMAS C, PELLICCIARI R, PRUZANSKI M, et al. Targeting bile-acid signalling for metabolic diseases[J]. Nat Rev Drug Discov, 2008, 7(8):678-693.
[13] NAGENGAST F, GRUBBEN M, VAN MUNSTER I. Role of bile acids in colorectal carcinogenesis[J]. Eur J Cancer, 1995, 31(7,8):1067-1070.
[14] RAMALHO R M, VIANA R J, LOW W C, et al. Bile acids and apoptosis modulation:an emerging role in experimental Alzheimer's disease[J]. Trends Mol Med, 2008, 14(2):54-62.
[15] WATANABE M, HOUTEN S M, WANG L, et al. Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1c[J]. J Clin Invest, 2004, 113(10):1408-1418.
[16] JIANG C T, XIE C, LV Y, et al. Intestine-selective farnesoid X receptor inhibition improves obesity-related metabolic dysfunction[J]. Nat Commun, 2015, 6:10166.
[17] XIE G X, WANG Y X, WANG X N, et al. Profiling of serum bile acids in a healthy Chinese population using UPLC-MS/MS[J]. J Proteome Res, 2015, 14(2):850-859.
[18] BENNION L J, DROBNY E, KNOWLER W C, et al. Sex differences in the size of bile acid pools[J]. Metabolism, 1978, 27(8):961-969.
[19] NICKEN P, HAMSCHER G, BREVES G, et al. Uptake of the colon carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by different segments of the rat gastrointestinal tract:its implication in colorectal carcinogenesis[J]. Toxicol Lett, 2010, 196(1):60-66.
[20] YUAN B F, ZHU Q F, GUO N, et al. Comprehensive profiling of fecal metabolome of mice by integrated chemical isotope labeling-mass spectrometry analysis[J]. Anal Chem, 2018, 90(5):3512-3520.
[21] GARCIA-CANAVERAS J C, DONATO M T, CASTELL J V, et al. Targeted profiling of circulating and hepatic bile acids in human, mouse, and rat using a UPLC-MRM-MS-validated method[J]. J Lipid Res, 2012, 53(10):2231-2241.
[22] CHEN L, SONG K, WANG Y L. Effects of attenuated salmonella typhimurium infection on fecal metabonome in mice[J]. Chinese J Magn Reson, 2014, 31(3):349-363. 陈璐, 宋侃, 王玉兰. 感染减毒鼠伤寒沙门氏菌对小鼠粪样代谢组的影响-WIPM和Bruker 500 MHz核磁共振波谱仪检测结果的比较[J]. 波谱学杂志, 2014, 31(3):349-363.
[23] WANT E J, COEN M, MASSON P, et al. Ultra performance liquid chromatography-mass spectrometry profiling of bile acid metabolites in biofluids:application to experimental toxicology studies[J]. Anal Chem, 2010, 82(12):5282-5289.
[24] HU Y L, HAO F H, WANG Y L. NMR-based metabonomic analyses on spleen tissues of 4T1 tumor-bearing mice subjected to chemotherapies with different drug delivery strategies[J]. Chinese J Magn Reson, 2018, 35(1):8-21. 胡依黎, 豪富华, 王玉兰. 基于NMR的4T1荷瘤小鼠脾脏受不同给药方式影响的代谢组学研究[J]. 波谱学杂志, 2018, 35(1):8-21.
[25] SONG Y P, LI N, XUE H S, et al. Metabonomics analysis of brown adipose and white adipose tissues[J]. Chinese J Magn Reson, 2016, 33(2):208-223. 宋懿朋, 李宁, 薛海斯, 等. 棕色脂肪组织和白色脂肪组织的代谢组学研究[J]. 波谱学杂志, 2016, 33(2):208-223.
[26] TAKAHASHI S, FUKAMI T, MASUO Y, et al. Cyp2c70 is responsible for the species difference in bile acid metabolism between mice and humans[J]. J Lipid Res, 2016, 57(12):2130-2137.
[27] FALANY C N, JOHNSON M R, BARNES S, et al. Glycine and taurine conjugation of bile acids by a single enzyme. Molecular cloning and expression of human liver bile acid CoA:amino acid N-acyltransferase[J]. J Biol Chem, 1994, 269(30):19375-19379.
[28] FALANY C, FORTINBERRY H, LEITER E, et al. Cloning, expression, and chromosomal localization of mouse liver bile acid CoA:amino acid N-acyltransferase[J]. J Lipid Res, 1997, 38(6):1139-1148.
[29] ZHANG R, BARNES S, DIASIO R B. Differential intestinal deconjugation of taurine and glycine bile acid N-acyl amidates in rats[J]. Am J Physiol, 1992, 262(2):G351-G358.
[30] MULLER V M, ZIETEK T, ROHM F, et al. Gut barrier impairment by high-fat diet in mice depends on housing conditions[J]. Mol Nutr Food Res, 2016, 60(4):897-908.
[31] WU J F, XU W X, MING Z P, et al. Metabolic changes reveal the development of schistosomiasis in mice[J]. PLoS Negl Trop Dis, 2010, 4(8):e807.
[32] WANG Y L, TANG H R, NICHOLSON J K, et al. A metabonomic strategy for the detection of the metabolic effects of chamomile (Matricaria recutita L.) ingestion[J]. J Agric Food Chem, 2005, 53(2):191-196.
[33] TIAN Y, ZHANG L M, WANG Y L, et al. Age-related topographical metabolic signatures for the rat gastrointestinal contents[J]. J Proteome Res, 2012, 11(2):1397-1411.
[34] RIDLON J M, KANG D J, HYLEMON P B. Bile salt biotransformations by human intestinal bacteria[J]. J Lipid Res, 2006, 47(2):241-259.
[35] TIAN Y, TANG H R. Identification and structural determination of saccharides in rat feces[J]. Chinese J Magn Reson, 2012, 29(3):361-371. 田园, 唐惠儒. 大鼠粪样中几种糖类物质的结构确定[J]. 波谱学杂志, 2012, 29(3):361-371.
[36] DEN BESTEN G D, VAN EUNEN K, GROEN A K, et al. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism[J]. J Lipid Res, 2013, 54(9):2325-2340.
[37] BACKHED F, LEY R E, SONNENBURG J L, et al. Host-bacterial mutualism in the human intestine[J]. science, 2005, 307(5717):1915-1920.
[38] ZHAO Y, WU J F, LI J V, et al. Gut microbiota composition modifies fecal metabolic profiles in mice[J]. J Proteome Res, 2013, 12(6):2987-2999.
[39] FRAHER M H, O'TOOLE P W, QUIGLEY E M. Techniques used to characterize the gut microbiota:a guide for the clinician[J]. Nat Rev Gastroenterol Hepatol, 2012, 9(6):312-322.
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