Interactions between gut microbiota and host metabolism predisposing to obesity and diabetes

Annual Review of Medicine

Volumn 62, Issue , 2011, Pages 361-380

  Musso, Giovanni ^a   Gambino, Roberto ^b   Cassader, Maurizio ^b  

^a GRADENIGO HOSPITAL   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

endotoxin; energy homeostasis; gut flora; microbiome; TLR4

Indexed keywords

BILE ACID; CELL PROTEIN; CHOLINE; ENDOTOXIN; FASTING INDUCED ADIPOSE FACTOR; FATTY ACID; GLYCAN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; STARCH; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ABSORPTION; ACTINOBACTERIA; ARTICLE; BACILLUS; BACTEROIDES THETAIOTAOMICRON; BACTEROIDETES; BILE ACID METABOLISM; CARBOHYDRATE METABOLISM; CLOSTRIDIUM; DIABETES MELLITUS; ENDOTOXEMIA; ENERGY BALANCE; ENERGY METABOLISM; ENTEROHEPATIC CIRCULATION; FATTY ACID OXIDATION; FERMENTATION; FIRMICUTES; HUMAN; IMMUNE SYSTEM; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN SENSITIVITY; INTESTINE FLORA; INTESTINE TRANSIT TIME; LACTOBACILLUS; LIPID STORAGE; LIPID TRANSPORT; LIPOGENESIS; METABOLISM; MICROBIAL DEGRADATION; MOUSE; MYCOPLASMA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PATHOGENESIS; PRIORITY JOURNAL; RISK FACTOR; STAPHYLOCOCCUS AUREUS;

ANGIOPOIETINS; ANIMALS; BILE ACIDS AND SALTS; CARBOHYDRATE METABOLISM; CHOLINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; ENDOTOXEMIA; ENERGY METABOLISM; GASTROINTESTINAL TRACT; HUMANS; INFLAMMATION; LINOLEIC ACIDS, CONJUGATED; METAGENOME; MICE; OBESITY; RATS; TOLL-LIKE RECEPTOR 4;

EID: 79551577263     PISSN: 00664219     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-med-012510-175505     Document Type: Article

References (98)

1. Ley RE, Lozupone CA, Hamady M, et al. 2008. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6:776-88
2. Bjorneklett A, Viddal KO, Midtvedt T, et al. 1981. Intestinal and gastric bypass. Changes in intestinal microecology after surgical treatment of morbid obesity in man. Scand. J. Gastroenterol. 16:681-87
3. Nishizawa Y, Imaizumi T, Tanishita H, et al. 1988. Relationship of fat deposition and intestinal microflora in VMH rats. Int. J. Obes. 12:103-10
4. Andoh A, Benno Y, Kanauchi O, et al. 2009. Recent advances in molecular approaches to gut microbiota in inflammatory bowel disease. Curr. Pharm. Des. 15:2066-73
5. Deng W, Xi D, Mao H, et al. 2008. The use of molecular techniques based on ribosomal RNA and DNA for rumen microbial ecosystem studies: a review. Mol. Biol. Rep. 35:265-74
6. Ley RE, Bäckhed F, Turnbaugh P, et al. 2005. Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 102:11070-75
7. Turnbaugh PJ, Bäckhed F, Fulton L, et al. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213-23
8. Ley RE, Turnbaugh PJ, Klein S, et al. 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444:1022-23
9. Zhang H, DiBaise JK, Zuccolo A, et al. 2009. Human gut microbiota in obesity and after gastric bypass. Proc. Natl. Acad. Sci. USA 106:2365-70
10. Duncan SH, Lobley GE, Holtrop G, et al. 2008. Human colonic microbiota associated with diet, obesity and weight loss. Int. J. Obesity 32:1720-24
11. Santacruz A, Marcos A, Wärnberg J, et al. 2009. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring) 17:1906-15
12. Nadal I, Santacruz A, Marcos A, et al. 2009. Shifts in clostridia, bacteroides and immunoglobulin-coating fecal bacteria associated with weight loss in obese adolescents. Int. J. Obesity 33:758-67
13. Turnbaugh PJ, Hamady M, Yatsunenko T, et al. 2009. A core gut microbiome in obese and lean twins. Nature 457:480-84
14. Wu X, Ma C, Han L, et al. 2010. Molecular characterisation of the faecal microbiota in patients with type II diabetes. Curr. Microbiol. 61:69-78
15. Larsen N, Vogensen FK, van den Berg FW, et al. 2010. Gut microbiota in human adults with type 2 diabetes differs from nondiabetic adults. PLoS One 5:e9085
16. Kalliomaki M, Collado MC, Salminen S, et al. 2008. Early differences in fecal microbiota composition in children may predict overweight. Am. J. Clin. Nutr. 87:534-38
17. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, et al. 2009. High fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137:1716-24
18. Dethlefsen L, Huse S, Sogin ML, et al. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6:2383-400
19. Membrez M, Blancher F, Jaquet M, et al. 2008. Gut microbiota modulation with norfloxacin and ampicillin enhances glucose tolerance in mice. FASEB J. 22:2416-26
20. Chou CJ, Membrez M, Blancher F, 2008. Gut decontamination with norfloxacin and ampicillin enhances insulin sensitivity in mice. Nestle Nutr. Workshop Ser. 62:127-40
21. Hooper LV, Midtvedt T, Gordon JI. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22:283-307
22. Manson JM, Rauch M, Gilmore MS. 2007. The commensal microbiology of the gastrointestinal tract. In Gastrointestinal Microbiota and Regulation of the Immune System, ed. GB Huffnagle, MC Noverr, pp. 15-28. New York: Landes Biosci
23. Zocco MA, Ainora ME, Gasbarrini G, et al. 2007. Bacteroides thetaiotaomicron in the gut: molecular aspects of their interaction. Dig. Liver Dis. 39:707-12
24. D'Elia JN, Salyers AA. 1996. Contribution of a neopullulanase, a pullulanase, and an alpha-glucosidase to growth of Bacteroides thetaiotaomicron on starch. J. Bacteriol. 178:7173-79
25. Martens EC, Koropatkin NM, Smith TJ, et al. 2009. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J. Biol. Chem. 284:24673-77
26. Mahowald MA, Rey FE, Seedorf H, et al. 2009 Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc. Natl. Acad. Sci. USA 106:5859-64
27. Hoskins LC, Boulding ET. 1976. Degradation of blood group antigens in human colon ecosystems. II. A gene interaction in man that affects the fecal population density of certain enteric bacteria. J. Clin. Invest. 57:74-82
28. Bergman EN. 1990. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol. Rev. 70:567-90
29. Flint HJ, Bayer EA, Rincon MT, et al. 2008. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microb. 6:121-31
30. Louis P, Flint HJ. 2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol. Lett. 294:1-8
31. Louis P, Scott KP, Duncan SH, et al. 2007. Understanding the effects of diet on bacterial metabolism in the large intestine. J. Appl. Microbiol. 102:1197-208
32. Elia M, Cummings JH. 2007. Physiological aspects of energy metabolism and gastrointestinal effects of carbohydrates. Eur. J. Clin. Nutr. 61(Suppl. 1):S40-74
33. Duncan SH, Belenguer A, Holtrop G, et al. 2007. Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Appl. Environ. Microbiol. 73:1073-78
34. Brinkworth GD, Noakes M, Clifton PM, et al. 2009. Comparative effects of very low-carbohydrate, high-fat and high-carbohydrate, low-fat weight-loss diets on bowel habit and faecal short-chain fatty acids and bacterial populations. Br. J. Nutr. 101:1493-502
35. Walker AW, Duncan SH, McWilliam Leitch EC, et al. 2005. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon. Appl. Environ. Microbiol. 71:3692-700
36. Flint HJ. 2006. The significance of prokaryote diversity in the human gastronintestinal tract. In Prokaryotic Diversity: Mechanisms and Significance. Proc. Soc. Gen. Microbiol. Symp. 66, ed. NALogan, HM Lappin-Scott, PCF Oyston, pp. 65-90. Paris: Lavoisier
37. Mortensen FV, Nielsen H, Aalkjaer C, et al. 1994. Short chain fatty acids relax isolated resistance arteries from the human ileum by a mechanism dependent on anion-exchange. Pharmacol. Toxicol. 75:181-85
38. Brown AJ, Goldsworthy SM, Barnes AA, et al. 2003. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 278:11312-19
39. Baddini Feitoza A, Fernandes Pereira A, Ferreira da Costa N, et al. 2009. Conjugated linoleic acid (CLA): effect modulation of body composition and lipid profile. Nutr. Hosp. 24:422-28
40. Devillard E, McIntosh FM, Duncan SH, et al. 2007. Metabolism of linoleic acid by human gut bacteria: different routes for biosynthesis of conjugated linoleic acid. J. Bacteriol. 189:2566-70
41. McIntosh FM, Shingfield KJ, Devillard E, et al. 2009. Mechanism of conjugated linoleic acid and vaccenic acid formation in human faecal suspensions and pure cultures of intestinal bacteria. Microbiology 155(Pt. 1):285-94
42. Gorissen L, Raes K, Weckx S, et al. 2010. Production of conjugated linoleic acid and conjugated linolenic acid isomers by Bifidobacterium species. Appl. Microbiol. Biotechnol. 87:2257-66
43. Devillard E, McIntosh FM, Paillard D, et al. 2009. Differences between human subjects in the composition of the faecal bacterial community and faecal metabolism of linoleic acid. Microbiology 155(Pt. 2):513-20
44. Wall R, Ross RP, Shanahan F, et al. 2009. Metabolic activity of the enteric microbiota influences the fatty acid composition of murine and porcine liver and adipose tissues. Am. J. Clin. Nutr. 89:1393-401
45. Fukushima M, Yamada A, Endo T, et al. 1999. Effects of a mixture of organisms, Lactobacillus acidophilus or Streptococcus faecalis on delta-6 desaturase activity in the livers of rats fed a fat and cholesterol enriched diet. Nutrition 15:373-78
46. Ridlon JM, Kang DJ, Hylemon PB. 2006. Bile salt biotransformations by human intestinal bacteria. J. Lipid. Res. 47:241-59
47. Fukiya S, Arata M, Kawashima H, et al. 2009. Conversion of cholic acid and chenodeoxycholic acid into their 7-oxo derivatives by Bacteroides intestinalis AM-1 isolated from human feces. FEMS Microbiol. Lett. 293:263-70
48. Keitel V, Kubitz R, Häussinger D. 2008. Endocrine and paracrine role of bile acids. World J. Gastroenterol. 14:5620-29
49. Lefebvre P, Cariou B, Lien F, et al. 2009. Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 89:147-91
50. Kars M, Yang L, Gregor MF, et al. 2010. Tauroursodeoxycholic acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women. Diabetes 59:1899-905
51. Martin FP, Dumas ME, Wang Y, et al. 2007. A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model. Mol. Syst. Biol. 112:1-16
52. Martin FP, Wang Y, Sprenger N, et al. 2008. Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Mol. Syst. Biol. 4:1-15
53. Velagapudi VR, Hezaveh R, Reigstad CS, et al. 2010. The gut microbiota modulates host energy and lipid metabolism in mice. J. Lipid Res. 51:1101-12
54. Buchman A, Dubin M, Moukarzel A, et al. 1995. Choline deficiency: a cause of hepatic steatosis during parenteral nutrition that can be reversed with intravenous choline supplementation. Hepatology 22:1399-403
55. Dumas ME, Barton RH, Toye A, et al. 2006. Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice. Proc. Natl. Acad. Sci. USA 103:12511-16
56. Bäckhed F, Ding H, Wang T, et al. 2004. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 101:15718-23
57. Hooper LV, Wong MH, Thelin A, et al. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881-84
58. Stappenbeck TS, Hooper LV, Gordon JI. 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 99:15451-55
59. Musso G, Gambino R, Cassader M. 2009. Recent insights into hepatic lipid metabolism in non-alcoholic fatty liver disease (NAFLD). Prog. Lipid Res. 48:1-26
60. Backhed F, Manchester JK, Semenkovich CF, et al. 2007. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc. Natl. Acad. Sci. USA 104:979-84
61. Turnbaugh PJ, Backhed F, Fulton L, et al. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213-23
62. Turnbaugh PJ, Ley RE, Mahowald MA, et al. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027-31
63. Dutton S, Trayhurn P. 2008. Regulation of angiopoietin-like protein 4/fasting-induced adipose factor (Angptl4/FIAF) expression in mouse white adipose tissue and 3T3-L1 adipocytes. Br. J. Nutr. 100:18-26
64. Kersten S. 2005. Regulation of lipid metabolism via angiopoietin-like proteins. Biochem. Soc. Trans. 33(Pt. 5):1059-62
65. Musso G, Gambino R, Cassader M. 2010. Emerging molecular targets for the treatment of nonalcoholic fatty liver disease. Annu. Rev. Med. 61:375-92
66. Xiong Y, Miyamoto N, Shibata K, et al. 2004 Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc. Natl. Acad. Sci. USA 101:1045-50
67. Halldén G, Aponte GW. 1997. Evidence for a role of the gut hormone PYY in the regulation of intestinal fatty acid-binding protein transcripts in differentiated subpopulations of intestinal epithelial cell hybrids. J. Biol. Chem. 272:12591-600
68. Samuel BS, Shaito A, Motoike T, et al. 2008. 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 105:16767-72
69. Seki E, Brenner DA. 2008. TLR and adaptor molecules in liver disease: update. Hepatology 48:322-35
70. Shi H, Kokoeva MV, Inouye K, et al. 2006. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116:3015-25
71. Seki E, De Minicis S, Osterreicher CH, et al. 2007. TLR4 enhances TGF-βsignaling and hepatic fibrosis. Nat. Med. 13:1324-32
72. Cani PD, Amar J, Iglesias MA, et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56:1761-72
73. Cani PD, Bibiloni R, Knauf C, et al. 2008. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470-81
74. Mehta NN, McGillicuddy FC, Anderson PD, et al. 2010. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 59:172-81
75. Thuy S, Ladurner R, Volynets V, et al. 2008. Nonalcoholic fatty liver disease in humans is associated with increased plasma endotoxin and plasminogen activator inhibitor 1 concentrations and with fructose intake. J. Nutr. 138:1452-55
76. Sabaté JM, Jouët P, Harnois F, et al. 2008. High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis. Obes. Surg. 18:371-77
77. Ruiz AG, Casafont F, Crespo J, et al. 2007. Lipopolysaccharide-binding protein plasma levels and liver TNF-alpha gene expression in obese patients: evidence for the potential role of endotoxin in the patho-genesis of nonalcoholic steatohepatitis. Obes. Surg. 17:1374-80
78. Rivera CA, Adegboyega P, van Rooijen N, et al. 2007. Toll-like receptor-4 signaling and Kupffer cells play pivotal roles in the pathogenesis of nonalcoholic steatohepatitis. J. Hepatol. 47:571-79
79. Amar J, Burcelin R, Ruidavets JB, et al. 2008. Energy intake is associated with endotoxemia in apparently healthy men. Am. J. Clin. Nutr. 87:1219-23
80. Ghanim H, Abuaysheh S, Sia CL, et al. 2009. Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells after a high-fat, high-carbohydrate meal: implications for insulin resistance. Diabetes Care 32:2281-87
81. Erridge C, Attina T, Spickett CM, et al. 2007. A high-fat meal induces low-grade endotoxemia: evidence of a novel mechanism of postprandial inflammation. Am. J. Clin. Nutr. 86:1286-92
82. DeopurkarR, Ghanim H, Friedman J, et al. 2010. Differential effects of cream, glucose and orange juice on inflammation, endotoxin and the expression of toll like receptor-4 and suppressor of cytokine signaling-3. Diab. Care 33:991-7
83. Ghanim H, Sia CL, Upadhyay M, et al. 2010. Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and Toll-like receptor expression. Am. J. Clin. Nutr. 91:940-49
84. Brun P, Catsagliuolo I, Di Leo V, et al. 2007. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G518-G525
85. Farhadi A, Gundlapalli S, Shaikh M, et al. 2008. Susceptibility to gut leakiness: a possible mechanism for endotoxaemia in nonalcoholic steatohepatitis. Liver Int. 28:1026-33
86. MieleL,ValenzaV,La TorreG, et al. 2009. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology 49:1877-87
87. Sharma R, Young C, Neu J. 2010. Molecular modulation of intestinal epithelial barrier: contribution of microbiota. J. Biomed. Biotechnol. doi:10.1155/2010/305879
88. Cani PD, Possemiers S, Van de Wiele T, et al. 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58:1091-103
89. Ghoshal S, Witta J, Zhong J, et al. 2009. Chylomicrons promote intestinal absorption of lipopolysaccha-rides. J. Lipid Res. 50:90-97
90. Zipris D. 2008. Innate immunity and its role in type 1 diabetes. Curr. Opin. Endocrinol. Diab. Obes. 15:326-31
91. Mordes JP, Bortell R, Blankenhorn EP, et al. 2004. Rat models of type 1 diabetes: genetics, environment, and autoimmunity. ILAR J. 45:278-91
92. Like AA, Guberski DL, Butler L. 1991. Influence of environmental viral agents on frequency and tempo of diabetes mellitus in BB/Wor rats. Diabetes 40:259-62
93. Brugman S, Klatter FA, Visser JT, et al. 2006. Antibiotic treatment partially protects against type 1 diabetes in the Bio-Breeding diabetes-prone rat: Is the gut flora involved in the development of type 1 diabetes? Diabetologia 49:2105-8
94. Schwartz RF, Neu J, Schatz D, et al. 2007. Comment on: Brugman S et al. (2006). Antibiotic treatment partially protects against type 1 diabetes in the Bio-Breeding diabetes-prone rat: Is the gut flora involved in the development of type 1 diabetes? Diabetologia 50:220-21
95. Calcinaro FDS, Marinaro M, Candeloro P, et al. 2005. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the nonobese diabetic mouse. Diabetologia 48:1565-75
96. Valladares R, Sankar D, Li N, et al. 2010. Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats. PLoS One 5:e10507
97. Wen L, Ley RE, Volchkov PY, et al. 2008. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455:1109-13
98. Rea MC, Clayton E, O'Connor PM, et al. 2007. Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains. J. Med. Microbiol. 56(Pt. 7):940-46