Reduction in hepatic secondary bile acids caused by short-term antibiotic-induced dysbiosis decreases mouse serum glucose and triglyceride levels

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Kuno, Takuya ^a,b   Hirayama Kurogi, Mio ^a   Ito, Shingo ^a,c   Ohtsuki, Sumio ^a,c  

^a KUMAMOTO UNIVERSITY   (Japan)

^b OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^c JAPAN AGENCY FOR MEDICAL RESEARCH AND DEVELOPMENT   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; CYTOCHROME P450; DEOXYCHOLIC ACID; LITHOCHOLIC ACID; TRIACYLGLYCEROL;

ANIMAL; BLOOD; C57BL MOUSE; DRUG EFFECT; DYSBIOSIS; GENETICS; GLUCOSE BLOOD LEVEL; LIVER; MALE; METABOLISM; MOUSE;

ANIMALS; ANTI-BACTERIAL AGENTS; BLOOD GLUCOSE; CYTOCHROME P-450 ENZYME SYSTEM; DEOXYCHOLIC ACID; DYSBIOSIS; LITHOCHOLIC ACID; LIVER; MALE; MICE; MICE, INBRED C57BL; TRIGLYCERIDES;

EID: 85040834694     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-19545-1     Document Type: Article

References (57)

1. Sommer, F. & Bäckhed, F. The gut microbiota-masters of host development and physiology. Nat. Rev. Microbiol. 11, 227-238 (2013).
2. Power, S. E., O'Toole, P. W., Stanton, C., Ross, R. P. & Fitzgerald, G. F. Intestinal microbiota, diet and health. Br. J. Nutr. 111, 387-402 (2014).
3. Mikkelsen, K. H., Knop, F. K., Frost, M., Hallas, J. & Pottegård, A. Use of Antibiotics and Risk of Type 2 Diabetes: A Population-Based Case-Control Study. J. Clin. Endocrinol. Metab. 100, 3633-3640 (2015).
4. Patel, N., Bindra, R. S., Modi, N. & Desai, S. Levofloxacin induced hypoglycemia in a non-diabetic patient. Int. J. Med. Sci. Public Health 2, 1110-1113 (2013).
5. Arpaci, D., Toço?lu, A. G., Açikgöz, B. S. & Tamer, A. Hypoglycemia caused by ciprofloxacin in a non-diabetic elderly patient: a case report. Turk. J. Geriatr. 17, 426-430 (2014).
6. Chai, G. et al. Trends of outpatient prescription drug utilization in US children, 2002-2010. Pediatrics 130, 23-31 (2012).
7. Sharland, M. The use of antibacterials in children: a report of the Specialist Advisory Committee on Antimicrobial Resistance (SACAR) Paediatric Subgroup. J. Antimicrob. Chemother. 60, i15-i26 (2007).
8. Bailey, L. C. et al. Association of antibiotics in infancy with early childhood obesity. JAMA Pediatr. 168, 1063-1069 (2014).
9. Schwartz, B. S. et al. Antibiotic use and childhood body mass index trajectory. Int. J. Obes. 40, 615-621 (2016).
10. Kuno, T., Hirayama-Kurogi, M., Ito, S. & Ohtsuki, S. Effect of Intestinal Flora on Protein Expression of Drug-Metabolizing Enzymes and Transporters in the Liver and Kidney of Germ-Free and Antibiotics-Treated Mice. Mol. Pharm. 13, 2691-2701 (2016).
11. Mazein, A. et al. Regulation and feedback of cholesterol metabolism. Nat. Preced. (2011).
12. Thorens, B. GLUT2, glucose sensing and glucose homeostasis. Diabetologia 58, 221-232 (2015).
13. Hylemon, P. B. et al. Bile acids as regulatory molecules. J. Lipid Res. 50, 1509-1520 (2009).
14. Ridlon, J. M., Kang, D. J., Hylemon, P. B. & Bajaj, J. S. Bile Acids and the Gut Microbiome. Curr. Opin. Gastroenterol. 30, 332-338 (2014).
15. Hirano, S. & Masuda, N. Enhancement of the 7 alpha-dehydroxylase activity of a gram-positive intestinal anaerobe by Bacteroides and its significance in the 7-dehydroxylation of ursodeoxycholic acid. J. Lipid Res. 23, 1152-1158 (1982).
16. Fiorucci, S. & Distrutti, E. Bile Acid-Activated Receptors, Intestinal Microbiota, and the Treatment of Metabolic Disorders. Trends Mol. Med. 21, 702-714 (2015).
17. Ridlon, J. M., Kang, D.-J. & Hylemon, P. B. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47, 241-259 (2006).
18. Wong, K. E. et al. Involvement of the vitamin D receptor in energy metabolism: regulation of uncoupling proteins. Am. J. Physiol.-Endocrinol. Metab. 296, E820-E828 (2009).
19. Zhou, J. et al. A novel pregnane X receptor-mediated and sterol regulatory element-binding protein-independent lipogenic pathway. J. Biol. Chem. 281, 15013-15020 (2006).
20. Moreau, A., Vilarem, M. J., Maurel, P. & Pascussi, J. M. Xenoreceptors CAR and PXR activation and consequences on lipid metabolism, glucose homeostasis, and inflammatory response. Mol. Pharm. 5, 35-41 (2007).
21. Staudinger, J. L. et al. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc. Natl. Acad. Sci. 98, 3369-3374 (2001).
22. Gnerre, C., Blättler, S., Kaufmann, M. R., Looser, R. & Meyer, U. A. Regulation of CYP3A4 by the bile acid receptor FXR: evidence for functional binding sites in the CYP3A4 gene. Pharmacogenet. Genomics 14, 635-645 (2004).
23. Sueyoshi, T., Kawamoto, T., Zelko, I., Honkakoski, P. & Negishi, M. The repressed nuclear receptor CAR responds to phenobarbital in activating the human CYP2B6 gene. J. Biol. Chem. 274, 6043-6046 (1999).
24. Drocourt, L., Ourlin, J.-C., Pascussi, J.-M., Maurel, P. & Vilarem, M.-J. Expression of CYP3A4, CYP2B6, andCYP2C9 Is Regulated by the Vitamin D Receptor Pathway in Primary Human Hepatocytes. J. Biol. Chem. 277, 25125-25132 (2002).
25. Goodwin, B., Moore, L. B., Stoltz, C. M., McKee, D. D. & Kliewer, S. A. Regulation of the human CYP2B6 gene by the nuclear pregnane X receptor. Mol. Pharmacol. 60, 427-431 (2001).
26. Hubbert, M. L., Zhang, Y., Lee, F. Y. & Edwards, P. A. Regulation of hepatic Insig-2 by the farnesoid X receptor. Mol. Endocrinol. 21, 1359-1369 (2007).
27. Konishi, T. et al. Oral vancomycin hydrochloride therapy for postoperative methicillin-cephem-resistantStaphylococcus aureus enteritis. Surg. Today 27, 826-832 (1997).
28. Prasad, Y. R. et al. Enhanced intestinal absorption of vancomycin with Labrasol and D-?-tocopheryl PEG 1000 succinate in rats. Int. J. Pharm. 250, 181-190 (2003).
29. Adachi, Y. et al. Enteric coated polymyxin B in the treatment of hyperammonemia and endotoxemia in liver cirrhosis. Gastroenterol. Jpn. 17, 550-557 (1982).
30. Zavascki, A. P., Goldani, L. Z., Li, J. & Nation, R. L. Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J. Antimicrob. Chemother. 60, 1206-1215 (2007).
31. Brook, I. Pathogenicity of the Bacteroides fragilis group. Ann. Clin. Lab. Sci. 19, 360-376 (1989).
32. García-Cañaveras, J. C., Donato, M. T., Castell, J. V. & Lahoz, A. Targeted profiling of circulating and hepatic bile acids in human, mouse, and rat using a UPLC-MRM-MS-validated method. J. Lipid Res. 53, 2231-2241 (2012).
33. Li, T., Francl, J. M., Boehme, S. & Chiang, J. Y. Regulation of cholesterol and bile acid homeostasis by the cholesterol 7?-hydroxylase/ steroid response element-binding protein 2/microRNA-33a axis in mice. Hepatology 58, 1111-1121 (2013).
34. Chen, J., Rider, D. A. & Ruan, R. Identification of valid housekeeping genes and antioxidant enzyme gene expression change in the aging rat liver. J. Gerontol. A. Biol. Sci. Med. Sci. 61, 20-27 (2006).
35. Suzuki-Yagawa, Y., Kawakami, K. & Nagano, K. Housekeeping Na, K-ATPase alpha 1 subunit gene promoter is composed of multiple cis elements to which common and cell type-specific factors bind. Mol. Cell. Biol. 12, 4046-4055 (1992).
36. Guinovart, J. J. et al. Bridging the gap between glucose phosphorylation and glycogen synthesis in the liver. Biochem. Soc. Trans. 25, 157-160 (1997).
37. García-Rocha, M. et al. Intracellular distribution of glycogen synthase and glycogen in primary cultured rat hepatocytes. Biochem. J. 357, 17-24 (2001).
38. Adeva-Andany, M. M., González-Lucán, M., Donapetry-García, C., Fernández-Fernández, C. & Ameneiros-Rodríguez, E. Glycogen metabolism in humans. BBA Clin. 5, 85-100 (2016).
39. Sun, T., Yi, H., Yang, C., Kishnani, P. S. & Sun, B. Starch Binding Domain-containing Protein 1 Plays a Dominant Role in Glycogen Transport to Lysosomes in Liver. J. Biol. Chem. 291, 16479-16484 (2016).
40. Anderson, A. The induction of CYP2B proteins in rodents by phenobarbital-like inducers: what has been discovered and what remains to be learned. Acta Chim. Slov. 55, 45-52 (2008).
41. Martignoni, M., Groothuis, G. M. & de Kanter, R. Species differences between mouse, rat, dog, monkey and human CYP-mediated drug metabolism, inhibition and induction. Expert Opin. Drug Metab. Toxicol. 2, 875-894 (2006).
42. Lepesheva, G. I. & Waterman, M. R. Sterol 14?-demethylase cytochrome P450 (CYP51), a P450 in all biological kingdoms. Biochim. Biophys. Acta BBA-Gen. Subj. 1770, 467-477 (2007).
43. Membrez, M. et al. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J. 22, 2416-2426 (2008).
44. Fiorucci, S., Cipriani, S., Baldelli, F. & Mencarelli, A. Bile acid-activated receptors in the treatment of dyslipidemia and related disorders. Prog. Lipid Res. 49, 171-185 (2010).
45. Makishima, M. et al. Vitamin D receptor as an intestinal bile acid sensor. Science 296, 1313-1316 (2002).
46. Sayin, S. I. et al. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab. 17, 225-235 (2013).
47. Huang, W. et al. Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration. Science 312, 233-236 (2006).
48. Lambert, G. et al. The farnesoid X-receptor is an essential regulator of cholesterol homeostasis. J. Biol. Chem. 278, 2563-2570 (2003).
49. Song, P., Zhang, Y. & Klaassen, C. D. Dose-Response of Five Bile Acids on Serum and Liver Bile Acid Concentrations and Hepatotoxicty in Mice. Toxicol. Sci. 123, 359-367 (2011).
50. Delzenne, N. M., Calderon, P. B., Taper, H. S. & Roberfroid, M. B. Comparative hepatotoxicity of cholic acid, deoxycholic acid and lithocholic acid in the rat: in vivo and in vitro studies. Toxicol. Lett. 61, 291-304 (1992).
51. Mazmanian, S. K., Round, J. L. & Kasper, D. L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453, 620-625 (2008).
52. Furusawa, Y. et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446-450 (2013).
53. Sekirov, I. et al. Antibiotic-Induced Perturbations of the Intestinal Microbiota Alter Host Susceptibility to Enteric Infection. Infect. Immun. 76, 4726-4736 (2008).
54. Kawauchi, S. et al. Downregulation of CYP3A and P-Glycoprotein in the Secondary Inflammatory Response of Mice With Dextran Sulfate Sodium-Induced Colitis and Its Contribution to Cyclosporine A Blood Concentrations. J. Pharmacol. Sci. 124, 180-191 (2014).
55. Parks, D. J. et al. Bile acids: natural ligands for an orphan nuclear receptor. Science 284, 1365-1368 (1999).
56. Nakamura, K. et al. Large-scale multiplex absolute protein quantification of drug-metabolizing enzymes and transporters in human intestine, liver, and kidney microsomes by SWATH-MS: Comparison with MRM/SRM and HR-MRM/PRM. PROTEOMICS 16, 2106-2117 (2016).
57. Sherman, B. T. et al. DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics 8, 426 (2007).