Antibiotics-induced depletion of mice microbiota induces changes in host serotonin biosynthesis and intestinal motility

Journal of Translational Medicine

Volumn 15, Issue 1, 2017, Pages

  Ge, Xiaolong ^a   Ding, Chao ^a   Zhao, Wei ^b   Xu, Lizhi ^a   Tian, Hongliang ^a   Gong, Jianfeng ^a   Zhu, Minsheng ^b   Li, Jieshou ^a   Li, Ning ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

Antibiotics; Bile acids; Gut motility; Intestinal microbiota; Serotonin

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; BILE ACID; DEOXYCHOLIC ACID; METRONIDAZOLE; NEOMYCIN; OXYGENASE; SEROTONIN; TRYPTOPHAN HYDROXYLASE 1; UNCLASSIFIED DRUG; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; C57BL 6 MOUSE; CECUM; CONTROLLED STUDY; DEFECATION HABIT; DYSBIOSIS; FECES ANALYSIS; GASTROINTESTINAL TRANSIT; HOST; INTESTINE FLORA; INTESTINE MOTILITY; MALE; MOUSE; NONHUMAN; SMOOTH MUSCLE; SMOOTH MUSCLE CONTRACTILITY; SPECIES COMPOSITION; SPECIES DIVERSITY; SPECIES RICHNESS; WATER CONTENT; WILD TYPE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FECES; GASTROINTESTINAL MOTILITY; METABOLISM; METABOLOME; MICROFLORA; MUSCLE CONTRACTION; ORGAN SIZE; PATHOLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; BILE ACIDS AND SALTS; CECUM; FECES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL MOTILITY; MALE; METABOLOME; MICE, INBRED C57BL; MICROBIOTA; MUSCLE CONTRACTION; ORGAN SIZE; SEROTONIN;

EID: 85010211585     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-016-1105-4     Document Type: Article

References (37)

1. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107-33.
2. Sommer F, Backhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol. 2013;11:227-38.
3. Yang J, Tan Q, Fu Q, Zhou Y, Hu Y, Tang S, et al. Gastrointestinal microbiome and breast cancer: correlations, mechanisms and potential clinical implications. Breast Cancer. 2016. doi: 10.1007/s12282-016-0734-z.
4. Zhu L, Liu W, Alkhouri R, Baker RD, Bard JE, Quigley EM, et al. Structural changes in the gut microbiome of constipated patients. Physiol Genomics. 2014;46:679-86.
5. Quigley EM. The enteric microbiota in the pathogenesis and management of constipation. Best Pract Res Clin Gastroenterol. 2011;25:119-26.
6. Barbara G, Stanghellini V, Brandi G, Cremon C, Di Nardo G, De Giorgio R, et al. Interactions between commensal bacteria and gut sensorimotor function in health and disease. Am J Gastroenterol. 2005;100:2560-8.
7. Barbara G, Feinle-Bisset C, Ghoshal UC, Quigley EM, Santos J, Vanner S, et al. The intestinal microenvironment and functional gastrointestinal disorders. Gastroenterology. 2016. doi: 10.1053/j.gastro.2016.02.028.
8. Gershon MD. 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr Opin Endocrinol Diabetes Obes. 2013;20:14-21.
9. Heredia DJ, Dickson EJ, Bayguinov PO, Hennig GW, Smith TK. Localized release of serotonin (5-hydroxytryptamine) by a fecal pellet regulates migrating motor complexes in murine colon. Gastroenterology. 2009;136:1328-38.
10. Fukumoto S, Tatewaki M, Yamada T, Fujimiya M, Mantyh C, Voss M, et al. Short-chain fatty acids stimulate colonic transit via intraluminal 5-HT release in rats. Am J Physiol Regul Integr Comp Physiol. 2003;284:R1269-76.
11. Xu L, Yu BP, Chen JG, Luo HS. Mechanisms mediating serotonin-induced contraction of colonic myocytes. Clin Exp Pharmacol Physiol. 2007;34:120-8.
12. Yano JM, Yu K, Donaldson GP, Shastri GG, Ann P, Ma L, et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell. 2015;161:264-76.
13. Alemi F, Poole DP, Chiu J, Schoonjans K, Cattaruzza F, Grider JR, et al. The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice. Gastroenterology. 2013;144:145-54.
14. Ghaffari K, Savadkuhi ST, Honar H, Riazi K, Shafaroodi H, Moezi L, et al. Obstructive cholestasis alters intestinal transit in mice: role of opioid system. Life Sci. 2004;76:397-406.
15. Kawamata Y, Fujii R, Hosoya M, Harada M, Yoshida H, Miwa M, et al. A G protein-coupled receptor responsive to bile acids. J Biol Chem. 2003;278:9435-40.
16. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J Clin Invest. 2015;125:926-38.
17. Hintze KJ, Cox JE, Rompato G, Benninghoff AD, Ward RE, Broadbent J, et al. Broad scope method for creating humanized animal models for animal health and disease research through antibiotic treatment and human fecal transfer. Gut Microbes. 2014;5:183-91.
18. Seki E, De Minicis S, Osterreicher CH, Kluwe J, Osawa Y, Brenner DA, et al. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med. 2007;13:1324-32.
19. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med. 2010;16:228-31.
20. Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, Wheadon M, et al. Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science. 2015;347:266-9.
21. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174-80.
22. Xu H, Hao W, Zhou Q, Wang W, Xia Z, Liu C, et al. Plaque bacterial microbiome diversity in children younger than 30 months with or without caries prior to eruption of second primary molars. PLoS ONE. 2014;9:e89269.
23. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537-41.
24. Li Z, Chalazonitis A, Huang YY, Mann JJ, Margolis KG, Yang QM, et al. Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. J Neurosci. 2011;31:8998-9009.
25. Nezami BG, Mwangi SM, Lee JE, Jeppsson S, Anitha M, Yarandi SS, et al. MicroRNA 375 mediates palmitate-induced enteric neuronal damage and high-fat diet-induced delayed intestinal transit in mice. Gastroenterology. 2014;146:473-83.
26. He WQ, Peng YJ, Zhang WC, Lv N, Tang J, Chen C, et al. Myosin light chain kinase is central to smooth muscle contraction and required for gastrointestinal motility in mice. Gastroenterology. 2008;135:610-20.
27. He WQ, Qiao YN, Peng YJ, Zha JM, Zhang CH, Chen C, et al. Altered contractile phenotypes of intestinal smooth muscle in mice deficient in myosin phosphatase target subunit 1. Gastroenterology. 2013;144:1456-65.
28. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA. 2011;108:5354-9.
29. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118:229-41.
30. Chen JJ, Li Z, Pan H, Murphy DL, Tamir H, Koepsell H, et al. Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: abnormal intestinal motility and the expression of cation transporters. J Neurosci. 2001;21:6348-61.
31. Rao SS, Rattanakovit K, Patcharatrakul T. Diagnosis and management of chronic constipation in adults. Nat Rev Gastroenterol Hepatol. 2016;13:295-305.
32. Khoruts A, Sadowsky MJ. Understanding the mechanisms of faecal microbiota transplantation. Nat Rev Gastroenterol Hepatol. 2016;13(9):508-16.
33. Tian H, Ding C, Gong J, Ge X, McFarland LV, Gu L, et al. Treatment of slow transit constipation with fecal microbiota transplantation: a pilot study. J Clin Gastroenterol. 2016;50:865-70.
34. Vandeputte D, Falony G, Vieira-Silva S, Tito RY, Joossens M, Raes J. Stool consistency is strongly associated with gut microbiota richness and composition, enterotypes and bacterial growth rates. Gut. 2016;65:57-62.
35. Hadizadeh F, Walter S, Belheouane M, Bonfiglio F, Heinsen FA, Andreasson A, et al. Stool frequency is associated with gut microbiota composition. Gut. 2016. doi: 10.1136/gutjnl-2016-311935.
36. Barrett KE. Endogenous and exogenous control of gastrointestinal epithelial function: building on the legacy of Bayliss and Starling. J Physiol. 2016. doi: 10.1113/JP272227.
37. Lundgren O. 5-hydroxytryptamine, enterotoxins, and intestinal fluid secretion. Gastroenterology. 1998;115:1009-12.