Diet-induced obesity causes metabolic impairment independent of alterations in gut barrier integrity

Molecular Nutrition and Food Research

Volumn 59, Issue 5, 2015, Pages 968-978

  Kless, Caroline ^a   Müller, Veronika Maria ^a   Schüppel, Valentina Luise ^a   Lichtenegger, Martina ^a   Rychlik, Michael ^a   Daniel, Hannelore ^a   Klingenspor, Martin ^a   Haller, Dirk ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Diet induced obesity; Glucose tolerance; Gut barrier integrity; High fat diet; Mouse strains

Indexed keywords

MUS;

GLUCOSE;

ADIPOSE TISSUE; AKR MOUSE; ANIMAL; C57BL MOUSE; COLON; ENDOTOXEMIA; HOMEOSTASIS; IMMUNOLOGY; LIPID DIET; LIVER; MALE; METABOLISM; MOUSE; OBESITY; SPECIES DIFFERENCE;

ADIPOSE TISSUE; ANIMALS; COLON; DIET, HIGH-FAT; ENDOTOXEMIA; GLUCOSE; HOMEOSTASIS; LIVER; MALE; MICE; MICE, INBRED AKR; MICE, INBRED C57BL; OBESITY; SPECIES SPECIFICITY;

EID: 84928763605     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400840     Document Type: Article

References (40)

1. Bhatheja, R., Bhatt, D. L., Clinical outcomes in metabolic syndrome. J. Cardiovasc. Nurs. 2006, 21, 298-305.
2. Korner, J., Woods, S. C., Woodworth, K. A., Regulation of energy homeostasis and health consequences in obesity. Am. J. Med. 2009, 122, S12-18.
3. Malik, V. S., Willett, W. C., Hu, F. B., Global obesity: trends, risk factors and policy implications. Nat. Rev. Endocrinology 2013, 9, 13-27.
4. Xu, H., Barnes, G. T., Yang, Q., Tan, G. et al., Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Investig. 2003, 112, 1821-1830.
5. Bournat, J. C., Brown, C. W., Mitochondrial dysfunction in obesity. Curr. Opin. Endocrinol. Diabetes Obes. 2010, 17, 446-452.
6. Musso, G., Gambino, R., Cassader, M., Obesity, diabetes, and gut microbiota: the hygiene hypothesis expanded? Diabetes Care 2010, 33, 2277-2284.
7. Ridaura, V. K., Faith, J. J., Rey, F. E., Cheng, J. et al., Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013, 341, 1241214.
8. Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M. et al., Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007, 56, 1761-1772.
9. Brun, P., Castagliuolo, I., di Leo, V., Buda, A. et al., Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292, G518-525.
10. Kaliannan, K., Hamarneh, S. R., Economopoulos, K. P., Nasrin Alam, S. et al., Intestinal alkaline phosphatase prevents metabolic syndrome in mice. Proc. Natl. Acad. Sci. USA 2013, 110, 7003-7008.
11. Cani, P. D., Bibiloni, R., Knauf, C., Waget, A. et al., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 2008, 57, 1470-1481.
12. deLa Serre, C. B., Ellis, C. L., Lee, J., Hartman, A. L. et al., Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G440-448.
13. Suzuki, T., Hara, H., Dietary fat and bile juice, but not obesity, are responsible for the increase in small intestinal permeability induced through the suppression of tight junction protein expression in LETO and OLETF rats. Nutr. Metab. 2010, 7, 19.
14. West, D. B., Boozer, C. N., Moody, D. L., Atkinson, R. L. et al., Dietary obesity in nine inbred mouse strains. Am. J. Physiol. 1992, 262, R1025-1032.
15. West, D. B., Waguespack, J., McCollister, S., Dietary obesity in the mouse: interaction of strain with diet composition. Am. J. Physiol. 1995, 268, R658-665.
16. Montgomery, M. K., Hallahan, N. L., Brown, S. H., Liu, M. et al., Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia 2013, 56, 1129-1139.
17. Winzell, M. S., Ahren, B., The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 2004, 53(Suppl 3), S215-219.
18. York, B., Lei, K., West, D. B., Inherited non-autosomal effects on body fat in F2 mice derived from an AKR/J x SWR/J cross. Mamm. Genome 1997, 8, 726-730.
19. Hesse, D., Dunn, M., Heldmaier, G., Klingenspor, M. et al., Behavioural mechanisms affecting energy regulation in mice prone or resistant to diet-induced obesity. Physiol. Behav. 2010, 99, 370-380.
20. Serino, M., Luche, E., Gres, S., Baylac, A. et al., Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut 2012, 61, 543-553.
21. Kirpich, I. A., Feng, W., Wang, Y., Liu, Y. et al., The type of dietary fat modulates intestinal tight junction integrity, gut permeability, and hepatic toll-like receptor expression in a mouse model of alcoholic liver disease. Alcohol Clin. Exp. Res. 2012, 36, 835-846.
22. Kim, K. A., Gu, W., Lee, I. A., Joh, E. H. et al., High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PloS One 2012, 7, e47713.
23. Ruiz, P. A., Shkoda, A., Kim, S. C., Sartor, R. B. et al., IL-10 gene-deficient mice lack TGF-beta/Smad-mediated TLR2 degradation and fail to inhibit proinflammatory gene expression in intestinal epithelial cells under conditions of chronic inflammation. Ann. N. Y. Acad. Sci. 2006, 1072, 389-394.
24. Gruber, L., Kisling, S., Lichti, P., Martin, F. P. et al., High fat diet accelerates pathogenesis of murine Crohn's disease-like ileitis independently of obesity. PloS One 2013, 8, e71661.
25. Parlesak, A., Schafer, C., Schutz, T., Bode, J. C. et al., Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J. Hepatol. 2000, 32, 742-747.
26. Lam, Y. Y., Ha, C. W., Campbell, C. R., Mitchell, A. J. et al., Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PloS One 2012, 7, e34233.
27. Flores, C. A., Cid, L. P., Sepulveda, F. V., Strain-dependent differences in electrogenic secretion of electrolytes across mouse colon epithelium. Exp. Physiol. 2010, 95, 686-698.
28. Lee, Y. S., Li, P., Huh, J. Y., Hwang, I. J. et al., Inflammation is necessary for long-term but not short-term high-fat diet-induced insulin resistance. Diabetes 2011, 60, 2474-2483.
29. Turner, N., Kowalski, G. M., Leslie, S. J., Risis, S. et al., Distinct patterns of tissue-specific lipid accumulation during the induction of insulin resistance in mice by high-fat feeding. Diabetologia 2013, 56, 1638-1648.
30. Stenman, L. K., Holma, R., Korpela, R., High-fat-induced intestinal permeability dysfunction associated with altered fecal bile acids. World J. Gastroenterol. 2012, 18, 923-929.
31. Badman, M. K., Kennedy, A. R., Adams, A. C., Pissios, P. et al., A very low carbohydrate ketogenic diet improves glucose tolerance in ob/ob mice independently of weight loss. Am. J. Physio. Endocrinol. Metab. 2009, 297, E1197-1204.
32. Borghjid, S., Feinman, R. D., Response of C57Bl/6 mice to a carbohydrate-free diet. Nutr. Metab. 2012, 9, 69.
33. Jornayvaz, F. R., Jurczak, M. J., Lee, H. Y., Birkenfeld, A. L. et al., A high-fat, ketogenic diet causes hepatic insulin resistance in mice, despite increasing energy expenditure and preventing weight gain. Am. J. Physiol. Endocrinol. Metab. 2010, 299, E808-815.
34. deWit, N. J., Bosch-Vermeulen, H., deGroot, P. J., Hooiveld, G. J. et al., The role of the small intestine in the development of dietary fat-induced obesity and insulin resistance in C57BL/6J mice. BMC Med. Genomics 2008, 1, 14.
35. Ding, S., Chi, M. M., Scull, B. P., Rigby, R. et al., High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PloS One 2010, 5, e12191.
36. Shoelson, S. E., Lee, J., Goldfine, A. B., Inflammation and insulin resistance. J. Clin. Invest. 2006, 116, 1793-1801.
37. Tilg, H., Moschen, A. R., Microbiota and diabetes: an evolving relationship. Gut 2014, 63, 1513-1521.
38. Ley, R. E., Backhed, F., Turnbaugh, P., Lozupone, C. A. et al., Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 2005, 102, 11070-11075.
39. Qin, J., Li, Y., Cai, Z., Li, S. et al., A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012, 490, 55-60.
40. Ma, B. W., Bokulich, N. A., Castillo, P. A., Kananurak, A. et al., Routine habitat change: a source of unrecognized transient alteration of intestinal microbiota in laboratory mice. PloS One 2012, 7, e47416.