Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Zhang, Xu ^a   Zhao, Yufeng ^b   Zhang, Menghui ^a   Pang, Xiaoyan ^a   Xu, Jia ^a   Kang, Chaoying ^b   Li, Meng ^b   Zhang, Chenhong ^a   Zhang, Zhiguo ^c   Zhang, Yifei ^c   Li, Xiaoying ^c   Ning, Guang ^c   Zhao, Liping ^a,b  

^a Shanghai Jiao Tong University   (China)

^b Chinese National Human Genome Center at Shanghai   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; BERBERINE; LEPTIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; RNA 16S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEROIDES; BODY FAT; BODY WEIGHT; CONTROLLED STUDY; DRUG EFFICACY; FIRMICUTES; HORMONE BLOOD LEVEL; INSULIN RESISTANCE; INTESTINE FLORA; LIPID DIET; MALE; NONHUMAN; OBESITY; PROTEIN BLOOD LEVEL; PROTEOBACTERIA; PYROSEQUENCING; RAT; TREATMENT RESPONSE;

ADIPOSITY; ANIMALS; BERBERINE; DIET, HIGH-FAT; FATTY ACIDS, VOLATILE; FECES; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; INFLAMMATION; INSULIN RESISTANCE; LEAST-SQUARES ANALYSIS; MALE; METAGENOME; OBESITY; PHENOTYPE; PHYLOGENY; RATS; RATS, WISTAR; WEIGHT GAIN;

ALLOBACULUM; BACTERIA (MICROORGANISMS); COPTIS CHINENSIS; OTUS; RATTUS;

EID: 84864560961     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042529     Document Type: Article

References (69)

1. O'Hara AM, Shanahan F, (2006) The gut flora as a forgotten organ. EMBO Rep 7: 688-693.
2. Guarner F, Malagelada JR, (2003) Gut flora in health and disease. Lancet 361: 512-519.
3. Li M, Wang B, Zhang M, Rantalainen M, Wang S, et al. (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A 105: 2117-2122.
4. Ley RE, Turnbaugh PJ, Klein S, Gordon JI, (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023.
5. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1131.
6. Larsen N, Vogensen FK, van den Berg FWJ, Nielsen DS, Andreasen AS, et al. (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5: e9085.
7. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, et al. (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470-1481.
8. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, et al. (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 101: 15718-15723.
9. Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, et al. (2007) Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772.
10. Delzenne NM, Neyrinck AM, Backhed F, Cani PD, (2011) Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat Rev Endocrinol 7: 639-646.
11. Cani P, Neyrinck A, Fava F, Knauf C, Burcelin R, et al. (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50: 2374-2383.
12. Jia W, Li H, Zhao L, Nicholson JK, (2008) Gut microbiota: a potential new territory for drug targeting. Nat Rev Drug Discov 7: 123-129.
13. Zhao L, Shen J, (2010) Whole-body systems approaches for gut microbiota-targeted, preventive healthcare. J Biotechnol 149: 183-190.
14. Tang J, Feng Y, Tsao S, Wang N, Curtain R, et al. (2009) Berberine and Coptidis rhizoma as novel antineoplastic agents: a review of traditional use and biomedical investigations. J Ethnopharmacol 126: 5-17.
15. Zhang Y, Li X, Zou D, Liu W, Yang J, et al. (2008) Treatment of type 2 diabetes and dyslipidemia with the natural plant alkaloid berberine. J Clin Endocrinol Metab 93: 2559-2565.
16. Zhang H, Wei J, Xue R, Wu J-D, Zhao W, et al. (2010) Berberine lowers blood glucose in type 2 diabetes mellitus patients through increasing insulin receptor expression. Metabolism 59: 285-292.
17. Yin J, Xing H, Ye J, (2008) Efficacy of berberine in patients with type 2 diabetes mellitus. Metabolism 57: 712-717.
18. Kong W, Wei J, Abidi P, Lin M, Inaba S, et al. (2004) Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 10: 1344-1351.
19. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, et al. (2006) Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55: 2256-2264.
20. Yin J, Gao Z, Liu D, Liu Z, Ye J, (2008) Berberine improves glucose metabolism through induction of glycolysis. Am J Physiol Endocrinol Metab 294: E148-156.
21. Ko B-S, Choi SB, Park SK, Jang JS, Kim YE, et al. (2005) Insulin sensitizing and insulinotropic action of berberine from Cortidis rhizoma. Biol Pharm Bull 28: 1431-1437.
22. Xia X, Yan J, Shen Y, Tang K, Yin J, et al. (2011) Berberine improves glucose metabolism in diabetic rats by inhibition of hepatic gluconeogenesis. PLoS One 6: e16556.
23. Lu SS, Yu YL, Zhu HJ, Liu XD, Liu L, et al. (2009) Berberine promotes glucagon-like peptide-1 (7-36) amide secretion in streptozotocin-induced diabetic rats. J Endocrinol 200: 159-165.
24. Liu Y, Hao H, Xie H, Lv H, Liu C, et al. (2009) Oxidative demethylenation and subsequent glucuronidation are the major metabolic pathways of berberine in rats. J Pharm Sci 98: 4391-4401.
25. Hua W, Ding L, Chen Y, Gong B, He J, et al. (2007) Determination of berberine in human plasma by liquid chromatography-electrospray ionization-mass spectrometry. J Pharm Biomed Anal 44: 931-937.
26. Han J, Lin H, Huang W, (2011) Modulating gut microbiota as an anti-diabetic mechanism of berberine. Med Sci Monit 17: RA164-167.
27. Xie W, Gu D, Li J, Cui K, Zhang Y, (2011) Effects and action mechanisms of berberine and Rhizoma coptidis on gut microbes and obesity in high-fat diet-fed C57BL/6J mice. PLoS One 6: e24520.
28. Crow JM, (2011) Microbiome: That healthy gut feeling. Nature 480: S88-89.
29. Zhang X, Zhao Y, Hu Y, Liu P, Zhao L, (2011) Whole-body systerms biology based on functional metagenomics: new opportunity for the modernization of traditional Chinese medicine. Mode Tradit Chin Med Mater Med 13: 202-212.
30. Chae SH, Jeong IH, Choi DH, Oh JW, Ahn YJ, (1999) Growth-inhibiting effects of Coptis japonica root-derived isoquinoline alkaloids on human intestinal bacteria. J Agric Food Chem 47: 934-938.
31. Wang T, Cai G, Qiu Y, Fei N, Zhang M, et al. (2011) Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 6: 320-329.
32. Sedova L, Seda O, Krenova D, Kren V, Kazdova L, (2004) Isotretinoin and fenofibrate induce adiposity with distinct effect on metabolic profile in a rat model of the insulin resistance syndrome. Int J Obes Relat Metab Disord 28: 719-725.
33. Lepper PM, Schumann C, Triantafilou K, Rasche FM, Schuster T, et al. (2007) Association of lipopolysaccharide-binding protein and coronary artery disease in men. J Am Coll Cardiol 50: 25-31.
34. Tesch GH, (2008) MCP-1/CCL2: a new diagnostic marker and therapeutic target for progressive renal injury in diabetic nephropathy. Am J Physiol Renal Physiol 294: F697-701.
35. Bullen JW, Bluher S, Kelesidis T, Mantzoros CS, (2007) Regulation of adiponectin and its receptors in response to development of diet-induced obesity in mice. Am J Physiol Endocrinol Metab 292: E1079-1086.
36. Haluzik M, Parizkova J, Haluzik M, (2004) Adiponectin and its role in the obesity-induced insulin resistance and related complications. Physiol Res 53: 123-130.
37. Reagan-Shaw S, Nihal M, Ahmad N, (2008) Dose translation from animal to human studies revisited. FASEB J 22: 659-661.
38. Kong WJ, Zhang H, Song DQ, Xue R, Zhao W, et al. (2009) Berberine reduces insulin resistance through protein kinase C-dependent up-regulation of insulin receptor expression. Metabolism 58: 109-119.
39. Hotamisligil GS, (2006) Inflammation and metabolic disorders. Nature 444: 860-867.
40. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, et al. (1996) IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271: 665-670.
41. Jeong HW, Hsu KC, Lee J-W, Ham M, Huh JY, et al. (2009) Berberine suppresses proinflammatory responses through AMPK activation in macrophages. Am J Physiol Endocrinol Metab 296: E955-964.
42. Zhang Q, Piao XL, Piao XS, Lu T, Wang D, et al. (2011) Preventive effect of Coptis chinensis and berberine on intestinal injury in rats challenged with lipopolysaccharides. Food Chem Toxicol 49: 61-69.
43. Zhang C, Zhang M, Wang S, Han R, Cao Y, et al. (2009) Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4: 232-241.
44. Hong SW, Kim SH, Jeun JA, Lee SJ, Kim SU, et al. (2000) Antimicrobial activity of 9-O-acyl- and 9-O-benzoyl-substituted berberrubines. Planta Med 66: 361-363.
45. Park SK, Kim MS, Roh SW, Bae JW, (2011) Blautia stercoris sp. nov., isolated from human feces. Int J Syst Evol Microbiol 62: 776-779.
46. Greetham HL, Gibson GR, Giffard C, Hippe H, Merkhoffer B, et al. (2004) Allobaculum stercoricanis gen. nov., sp. nov., isolated from canine feces. Anaerobe 10: 301-307.
47. Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, et al. (2010) Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59: 1635-1642.
48. Peng L, Li ZR, Green RS, Holzman IR, Lin J, (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 139: 1619-1625.
49. Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, et al. (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58: 1091-1103.
50. Gu LL, Li N, Gong JF, Li QR, Zhu WM, et al. (2011) Berberine ameliorates intestinal epithelial tight-junction damage and down-regulates myosin light chain kinase pathways in a mouse model of endotoxinemia. J Infect Dis 203: 1602-1612.
51. Harig JM, Soergel KH, Komorowski RA, Wood CM, (1989) Treatment of diversion colitis with short-chain-fatty acid irrigation. N Engl J Med 320: 23-28.
52. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, et al. (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461: 1282-1286.
53. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, et al. (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469: 543-547.
54. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, et al. (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 107: 14691-14696.
55. Flint HJ, (2011) Obesity and the gut microbiota. J Clin Gastroenterol 45 Suppl: S128-S132.
56. Ravussin Y, Koren O, Spor A, LeDuc C, Gutman R, et al. (2012) Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity 20: 738-747.
57. Zhang C, Zhang M, Pang X, Zhao Y, Wang L, et al. (2012) Structural resilience of the gut microbiota in adult mice under high-fat dietary perturbations. ISME J doi: 10.1038/ismej.2012.27.
58. Wang Y, Jia X, Ghanam K, Beaurepaire C, Zidichouski J, et al. (2010) Berberine and plant stanols synergistically inhibit cholesterol absorption in hamsters. Atherosclerosis 209: 111-117.
59. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, et al. (2008) Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes 32: 1720-1724.
60. Zhou L, Wang X, Shao L, Yang Y, Shang W, et al. (2008) Berberine acutely inhibits insulin secretion from beta-cells through 3′,5′-cyclic adenosine 5′-monophosphate signaling pathway. Endocrinology 149: 4510-4518.
61. Li W, Godzik A, (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
62. DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, et al. (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34: W394-399.
63. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
64. Schloss PD, Handelsman J, (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506.
65. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
66. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
67. Lozupone C, Knight R, (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
68. ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Ithaca, NY: Microcomputer Power.
69. Wold S, Sjostrom M, Eriksson L, (2001) PLS-regression: a basic tool of chemometrics. Chemometr Intell Lab 58: 109-130.