Bile-acid-mediated decrease in endoplasmic reticulum stress: A potential contributor to the metabolic benefits of ileal interposition surgery in UCD-T2DM rats

DMM Disease Models and Mechanisms

Volumn 6, Issue 2, 2013, Pages 443-456

  Cummings, Bethany P ^a   Bettaieb, Ahmed ^a   Graham, James L ^a   Kim, Jaehyoung ^b   Ma, Fangrui ^b   Shibata, Noreene ^a   Stanhope, Kimber L ^a   Giulivi, Cecilia ^a   Hansen, Frederik ^c   Jelsing, Jacob ^c   Vrang, Niels ^c   Kowala, Mark ^d   Chouinard, Michael L ^d   Haj, Fawaz G ^a   Havel, Peter J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c Gubra ApS   (Denmark)

^d ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; CHOLIC ACID; GLUCAGON LIKE PEPTIDE 1;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE ACID METABOLISM; BODY WEIGHT; CALORIC INTAKE; CELL CULTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENERGY EXPENDITURE; FAT TOLERANCE TEST; GAMMAPROTEOBACTERIA; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; ILEAL INTERPOSITION; ILEUM RESECTION; INSULIN METABOLISM; INTESTINE FLORA; LIPID METABOLISM; LIVER; LIVER CELL; MALE; MOLECULAR INTERACTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ADIPOCYTES; ANIMALS; BILE ACIDS AND SALTS; BODY WEIGHT; CECUM; CHOLIC ACID; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; EATING; ENDOPLASMIC RETICULUM STRESS; ENERGY METABOLISM; GAMMAPROTEOBACTERIA; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TOLERANCE TEST; HEPATOCYTES; ILEUM; INSULIN; INSULIN-SECRETING CELLS; LIPID METABOLISM; MALE; ORGAN SPECIFICITY; RATS; SIGNAL TRANSDUCTION;

EID: 84875142060     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.010421     Document Type: Article

References (40)

1. Baggio, L. L. and Drucker, D. J. (2007). Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 2131-2157. (Pubitemid 46711096)
2. Bootsma, A. H., Overmars, H., Van Rooij, A., Van Lint, A. E., Wanders, R. J., Van Gennip, A. H. and Vreken, P. (1999). Rapid analysis of conjugated bile acids in plasma using electrospray tandem mass spectrometry: application for selective screening of peroxisomal disorders. J. Inherit. Metab. Dis. 22, 307-310. (Pubitemid 29259501)
3. Brubaker, P. L. and Drucker, D. J. (2004). Minireview: Glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology 145, 2653-2659. (Pubitemid 38686211)
4. Buchwald, H., Avidor, Y., Braunwald, E., Jensen, M. D., Pories, W., Fahrbach, K. and Schoelles, K. (2004). Bariatric surgery: a systematic review and meta-analysis. JAMA 292, 1724-1737. (Pubitemid 39346675)
5. Cummings, B. P., Digitale, E. K., Stanhope, K. L., Graham, J. L., Baskin, D. G., Reed, B. J., Sweet, I. R., Griffen, S. C. and Havel, P. J. (2008). Development and characterization of a novel rat model of type 2 diabetes mellitus: the UC Davis type 2 diabetes mellitus UCD-T2DM rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1782-R1793.
6. Cummings, B. P., Stanhope, K. L., Graham, J. L., Baskin, D. G., Griffen, S. C., Nilsson, C., Sams, A., Knudsen, L. B., Raun, K. and Havel, P. J. (2010a). Chronic administration of the glucagon-like peptide-1 analog, liraglutide, delays the onset of diabetes and lowers triglycerides in UCD-T2DM rats. Diabetes 59, 2653-2661.
7. Cummings, B. P., Stanhope, K. L., Graham, J. L., Evans, J. L., Baskin, D. G., Griffen, S. C. and Havel, P. J. (2010b). Dietary fructose accelerates the development of diabetes in UCD-T2DM rats: amelioration by the antioxidant, alpha-lipoic acid. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R1343-R1350.
8. Cummings, B. P., Strader, A. D., Stanhope, K. L., Graham, J. L., Lee, J., Raybould, H. E., Baskin, D. G. and Havel, P. J. (2010c). Ileal interposition surgery improves glucose and lipid metabolism and delays diabetes onset in the UCD-T2DM rat. Gastroenterology 138, 2437-2446.
9. Cummings, B. P., Bettaieb, A., Graham, J. L., Stanhope, K. L., Kowala, M., Haj, F. G., Chouinard, M. L. and Havel, P. J. (2012). Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology 153, 3620-3632.
10. Folch, J., Lees, M. and Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
11. Furet, J. P., Kong, L. C., Tap, J., Poitou, C., Basdevant, A., Bouillot, J. L., Mariat, D., Corthier, G., Doré, J., Henegar, C. et al. (2010). Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59, 3049-3057.
12. Gregor, M. F., Yang, L., Fabbrini, E., Mohammed, B. S., Eagon, J. C., Hotamisligil, G. S. and Klein, S. (2009). Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 58, 693-700.
13. Harding, H. P. and Ron, D. (2002). Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51, S455-S461. (Pubitemid 35403430)
14. Hotamisligil, G. S. (2010). Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917.
15. Kalaany, N. Y. and Mangelsdorf, D. J. (2006). LXRS and FXR: the yin and yang of cholesterol and fat metabolism. Annu. Rev. Physiol. 68, 159-191.
16. Kohli, R., Kirby, M., Setchell, K. D., Jha, P., Klustaitis, K., Woollett, L. A., Pfluger, P. T., Balistreri, W. F., Tso, P., Jandacek, R. J. et al. (2010). Intestinal adaptation after ileal interposition surgery increases bile acid recycling and protects against obesity-related comorbidities. Am. J. Physiol. Gastrointest. Liver Physiol. 299, G652-G660.
17. Li, J. V., Ashrafian, H., Bueter, M., Kinross, J., Sands, C., Le Roux, C. W., Bloom, S. R., Darzi, A., Athanasiou, T., Marchesi, J. R. et al. (2011). Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 60, 1214-1223.
18. Miyata, M., Yamakawa, H., Hamatsu, M., Kuribayashi, H., Takamatsu, Y. and Yamazoe, Y. (2011). Enterobacteria modulate intestinal bile acid transport and homeostasis through apical sodium-dependent bile acid transporter (SLC10A2) expression. J. Pharmacol. Exp. Ther. 336, 188-196.
19. Morino, K., Petersen, K. F. and Shulman, G. I. (2006). Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction. Diabetes 55 Suppl. 2, S9-S15. (Pubitemid 44927027)
20. Nakatani, H., Kasama, K., Oshiro, T., Watanabe, M., Hirose, H. and Itoh, H. (2009). Serum bile acid along with plasma incretins and serum high-molecular weight adiponectin levels are increased after bariatric surgery. Metabolism 58, 1400-1407.
21. Ozcan, U., Cao, Q., Yilmaz, E., Lee, A. H., Iwakoshi, N. N., Ozdelen, E., Tuncman, G., Görgün, C., Glimcher, L. H. and Hotamisligil, G. S. (2004). Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461. (Pubitemid 39372439)
22. Ozcan, U., Yilmaz, E., Ozcan, L., Furuhashi, M., Vaillancourt, E., Smith, R. O., Görgün, C. Z. and Hotamisligil, G. S. (2006). Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140. (Pubitemid 44300242)
23. Patti, M. E., Houten, S. M., Bianco, A. C., Bernier, R., Larsen, P. R., Holst, J. J., Badman, M. K., Maratos-Flier, E., Mun, E. C., Pihlajamaki, J. et al. (2009). Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity 17, 1671-1677.
24. Paulsen, S. J., Vrang, N., Larsen, L. K., Larsen, P. J. and Jelsing, J. (2010). Stereological assessment of pancreatic beta-cell mass development in male Zucker Diabetic Fatty (ZDF) rats: correlation with pancreatic beta-cell function. J. Anat. 217, 624-630.
25. Pols, T. W., Noriega, L. G., Nomura, M., Auwerx, J. and Schoonjans, K. (2011). The bile acid membrane receptor TGR5 as an emerging target in metabolism and inflammation. J. Hepatol. 54, 1263-1272.
26. Ron, D. and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529. (Pubitemid 46985379)
27. Samuel, V. T., Petersen, K. F. and Shulman, G. I. (2010). Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277.
28. Sancho, V., Trigo, M. V., Martín-Duce, A., Gonz Lez, N., Acitores, A., Arnés, L., Valverde, I., Malaisse, W. J. and Villanueva- Peñacarrillo, M. L. (2006). Effect of GLP-1 on D-glucose transport, lipolysis and lipogenesis in adipocytes of obese subjects. Int. J. Mol. Med. 17, 1133-1137.
29. Schauer, P. R., Kashyap, S. R., Wolski, K., Brethauer, S. A., Kirwan, J. P., Pothier, C. E., Thomas, S., Abood, B., Nissen, S. E. and Bhatt, D. L. (2012). Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N. Engl. J. Med. 366, 1567-1576.
30. Scott, W. R. and Batterham, R. L. (2011). Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: understanding weight loss and improvements in type 2 diabetes after bariatric surgery. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R15-R27.
31. Shawl, A. I., Park, K. H. and Kim, U. H. (2009). Insulin receptor signaling for the proliferation of pancreatic β-cells: involvement of Ca2+ second messengers, IP3, NAADP and cADPR. Islets 1, 216-223.
32. Sjöström, L., Lindroos, A. K., Peltonen, M., Torgerson, J., Bouchard, C., Carlsson, B., Dahlgren, S., Larsson, B., Narbro, K., Sjöström, C. D. et al. (2004). Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N. Engl. J. Med. 351, 2683-2693. (Pubitemid 39665322)
33. Strader, A. D. (2006). Ileal transposition provides insight into the effectiveness of gastric bypass surgery. Physiol. Behav. 88, 277-282. (Pubitemid 44202216)
34. Swann, J. R., Want, E. J., Geier, F. M., Spagou, K., Wilson, I. D., Sidaway, J. E., Nicholson, J. K. and Holmes, E. (2011). Systemic gut microbial modulation of bile acid metabolism in host tissue compartments. Proc. Natl. Acad. Sci. USA 108 Suppl. 1, 4523-4530.
35. Thaler, J. P. and Cummings, D. E. (2009). Minireview: Hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology 150, 2518-2525.
36. Thomas, C., Pellicciari, R., Pruzanski, M., Auwerx, J. and Schoonjans, K. (2008). Targeting bile-acid signalling for metabolic diseases. Nat. Rev. Drug Discov. 7, 678-693.
37. Thomas, C., Gioiello, A., Noriega, L., Strehle, A., Oury, J., Rizzo, G., Macchiarulo, A., Yamamoto, H., Mataki, C., Pruzanski, M. et al. (2009). TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10, 167-177.
38. Torchia, E. C., Labonté, E. D. and Agellon, L. B. (2001). Separation and quantitation of bile acids using an isocratic solvent system for high performance liquid chromatography coupled to an evaporative light scattering detector. Anal. Biochem. 298, 293-298. (Pubitemid 33105245)
39. Watanabe, M., Houten, S. M., Mataki, C., Christoffolete, M. A., Kim, B. W., Sato, H., Messaddeq, N., Harney, J. W., Ezaki, O., Kodama, T. et al. (2006). Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439, 484-489. (Pubitemid 43152840)
40. Zhang, H., Di Baise, J. K., Zuccolo, A., Kudrna, D., Braidotti, M., Yu, Y., Parameswaran, P., Crowell, M. D., Wing, R., Rittmann, B. E. et al. (2009). Human gut microbiota in obesity and after gastric bypass. Proc. Natl. Acad. Sci. USA 106, 2365-2370.