Intestinal adaptation and Reg gene expression induced by antidiabetic duodenal-jejunal bypass surgery in Zucker fatty rats

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 7, 2013, Pages

  Li, Bing ^a   Lu, Yarong ^a   Srikant, Coimbatore B ^a   Gao, Zu Hua ^a   Liu, Jun Li ^a,b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b Montreal Diabetes Research Centre   (Canada)

Author keywords

Apoptosis; Cell death; Cell proliferation; Diabetes; Immunohistochemistry; Obesity; Reg family proteins; Type

Indexed keywords

PROTEIN; REG PROTEIN; UNCLASSIFIED DRUG; LECTIN; LITHOSTATHINE; PANCREATITIS ASSOCIATED PROTEIN; PANCREATITIS-ASSOCIATED PROTEIN; REG1 PROTEIN, RAT; TUMOR ANTIGEN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; DUODENUM; DUODENUM JEJUNUM BYPASS SURGERY; EPITHELIUM; GENE EXPRESSION; HYPERGLYCEMIA; HYPERINSULINEMIA; IMMUNOHISTOCHEMISTRY; INTESTINE; INTESTINE MUCOSA; INTESTINE SURGERY; JEJUNUM; NONHUMAN; PRIORITY JOURNAL; RAT; ZUCKER RAT; ANIMAL; ATROPHY; BARIATRIC SURGERY; BIOSYNTHESIS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; MALE; METABOLISM; MORBID OBESITY; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; ANTIGENS, NEOPLASM; ATROPHY; BARIATRIC SURGERY; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; DUODENUM; GLUCOSE TOLERANCE TEST; INTESTINAL MUCOSA; JEJUNUM; LECTINS, C-TYPE; LITHOSTATHINE; MALE; OBESITY, MORBID; RATS; RATS, ZUCKER; TUMOR MARKERS, BIOLOGICAL;

MLCS; MLOWN;

EID: 84878164165     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00275.2012     Document Type: Article

References (47)

1. Bodeker H, Vasseur S, Dusetti NJ, Dagorn JC, Iovanna JL. PAP gene transcription induced by cycloheximide in AR4-2J cells involves ADPribosylation. Biochem Biophys Res Commun 251: 710-713, 1998.
2. Breen DM, Rasmussen BA, Kokorovic A, Wang R, Cheung GWC, Lam TKT. Jejunal nutrient sensing is required for duodenal-jejunal bypass surgery to rapidly lower glucose concentrations in uncontrolled diabetes. Nat Med 18: 950-955, 2012.
3. Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ, Bantle JP, Sledge I. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 122: 248-256, 2009.
4. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102-110, 2003.
5. Carracedo A, Lorente M, Egia A, Blazquez C, Garcia S, Giroux V, Malicet C, Villuendas R, Gironella M, Gonzalez-Feria L, Piris MA, Iovanna JL, Guzman M, Velasco G. The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell 9: 301-312, 2006.
6. Cheng KK, Iglesias MA, Lam KS, Wang Y, Sweeney G, Zhu W, Vanhoutte PM, Kraegen EW, Xu A. APPL1 potentiates insulin-mediated inhibition of hepatic glucose production and alleviates diabetes via Akt activation in mice. Cell Metab 9: 417-427, 2009.
7. Cui W, De Jesus K, Zhao H, Takasawa S, Shi B, Srikant CB, Liu JL. Overexpression of Reg3alpha increases cell growth and the levels of cyclin D1 and CDK4 in insulinoma cells. Growth Factors 27: 195-202, 2009.
8. Dudrick SJ, Daly JM, Castro G, Akhtar M. Gastrointestinal adaptation following small bowel bypass for obesity. Ann Surg 185: 642-648, 1977.
9. Dusetti NJ, Frigerio JM, Szpirer C, Dagorn JC, Iovanna JL. Cloning, expression and chromosomal localization of the rat pancreatitis-associated protein III gene. Biochem J 307: 9-16, 1995.
10. Dusetti NJ, Vasseur S, Ortiz EM, Romeo H, Dagorn JC, Burrone O, Iovanna JL. The pancreatitis-associated protein I promoter allows targeting to the pancreas of a foreign gene, whose expression is up-regulated during pancreatic inflammation. J Biol Chem 272: 5800-5804, 1997.
11. Endo Y, Ohta M, Kai S, Kitano S. An obese rat model of bariatric surgery with gastric banding. Obes Surg 17: 815-819, 2007.
12. Gatmaitan P, Huang H, Talarico J, Moustarah F, Kashyap S, Kirwan JP, Schauer PR, Brethauer SA. Pancreatic islet isolation after gastric bypass in a rat model: technique and initial results for a promising research tool. Surgery for obesity and related diseases. Am Soc Bariatric Surg 6: 532-537, 2010.
13. Gross DJ, Weiss L, Reibstein I, van den Brand J, Okamoto H, Clark A, Slavin S. Amelioration of diabetes in nonobese diabetic mice with advanced disease by linomide-induced immunoregulation combined with Reg protein treatment. Endocrinology 139: 2369-2374, 1998.
14. Hoffmeister A, Ropolo A, Vasseur S, Mallo GV, Bodeker H, Ritz-Laser B, Dressler GR, Vaccaro MI, Dagorn JC, Moreno S, Iovanna JL. The HMG-I/Y-related protein p8 binds to p300 and Pax2 transactivation domain-interacting protein to regulate the trans-activation activity of the Pax2A and Pax2B transcription factors on the glucagon gene promoter. J Biol Chem 277: 22314-22319, 2002.
15. Karra E, Yousseif A, Batterham RL. Mechanisms facilitating weight loss and resolution of type 2 diabetes following bariatric surgery. Trends Endocrinol Metab 21: 337-344, 2010.
16. Keidar A. Bariatric surgery for type 2 diabetes reversal: the risks. Diabetes Care 34, Suppl 2: S361-S266, 2011.
17. Klover PJ, Clementi AH, Mooney RA. Interleukin-6 depletion selectively improves hepatic insulin action in obesity. Endocrinology 146: 3417-3427, 2005.
18. Kohli R, Stefater MA, Inge TH. Molecular insights from bariatric surgery. Rev Endocr Metab Disord 12: 211-219, 2011.
19. Kurtz TW, Morris RC, Pershadsingh HA. The Zucker fatty rat as a genetic model of obesity and hypertension. Hypertension 13: 896-901, 1989.
20. Liu JL, Coschigano KT, Robertson K, Lipsett M, Guo Y, Kopchick JJ, Kumar U, Liu YL. Disruption of growth hormone receptor gene causes diminished pancreatic islet size and increased insulin sensitivity in mice. Am J Physiol Endocrinol Metab 287: E405-E413, 2004.
21. Lu Y, Ponton A, Okamoto H, Takasawa S, Herrera PL, Liu JL. Activation of the Reg family genes by pancreatic-specific IGF-I gene deficiency and after streptozotocin-induced diabetes in mouse pancreas. Am J Physiol Endocrinol Metab 291: E50-E58, 2006.
22. Masciotra L, Lechêne de la Porte P, Frigerio JM, Dusetti NJ, Dagorn JC, Iovanna JL. Immunocytochemical localization of pancreatitis-associated protein in human small intestine. Dig Dis Sci 40: 519-524, 1995.
23. Miller RA, Chu Q, Le Lay J, Scherer PE, Ahima RS, Kaestner KH, Foretz M, Viollet B, Birnbaum MJ. Adiponectin suppresses gluconeogenic gene expression in mouse hepatocytes independent of LKB1-AMPK signaling. J Clin Invest 121: 2518-2528, 2011.
24. Mistry SB, Omana JJ, Kini S. Rat models for bariatric surgery and surgery for type 2 diabetes mellitus. Obes Surg 19: 655-660, 2009.
25. Mithieux G. A synergy between incretin effect and intestinal gluconeogenesis accounting for the rapid metabolic benefits of gastric bypass surgery. Curr Diabetes Rep 12: 167-171, 2012.
26. Patti ME, McMahon G, Mun EC, Bitton A, Holst JJ, Goldsmith J, Hanto DW, Callery M, Arky R, Nose V, Bonner-Weir S, Goldfine AB. Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia 48: 2236-2240, 2005.
27. Pick A, Clark J, Kubstrup C, Levisetti M, Pugh W, Bonner-Weir S, Polonsky KS. Role of apoptosis in failure of beta-cell mass compensation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat. Diabetes 47: 358-364, 1998.
28. Pinkney JH, Johnson AB, Gale EA. The big fat bariatric bandwagon. Diabetologia 53: 1815-1822, 2010.
29. Polyzogopoulou EV, Kalfarentzos F, Vagenakis AG, Alexandrides TK. Restoration of euglycemia and normal acute insulin response to glucose in obese subjects with type 2 diabetes following bariatric surgery. Diabetes 52: 1098-1103, 2003.
30. Pories WJ. Bariatric surgery: risks and rewards. J Clin Endocrinol Metab 93: S89-96, 2008.
31. Rajas F, Bruni N, Montano S, Zitoun C, Mithieux G. The glucose-6 phosphatase gene is expressed in human and rat small intestine: regulation of expression in fasted and diabetic rats. Gastroenterology 117: 132-139, 1999.
32. Rubino F, Forgione A, Cummings DE, Vix M, Gnuli D, Mingrone G, Castagneto M, Marescaux J. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg 244: 741-749, 2006.
33. Rubino F, Zizzari P, Tomasetto C, Bluet-Pajot MT, Forgione A, Vix M, Grouselle D, Marescaux J. The role of the small bowel in the regulation of circulating ghrelin levels and food intake in the obese Zucker rat. Endocrinology 146: 1745-1751, 2005.
34. Sandi MJ, Hamidi T, Malicet C, Cano C, Loncle C, Pierres A, Dagorn JC, Iovanna JL. p8 expression controls pancreatic cancer cell migration, invasion, adhesion, and tumorigenesis. J Cell Physiol 226: 3442-3451, 2011.
35. Sansonetti A, Romeo H, Berthezene P, Scacchi P, Dusetti N, Keim V, Dagorn JC, Iovanna JL. Developmental, nutritional, and hormonal regulation of the pancreatitis-associated protein I and III gene expression in the rat small intestine. Scand J Gastroenterol 30: 664-669, 1995.
36. Service GJ, Thompson GB, Service FJ, Andrews JC, Collazo-Clavell ML, Lloyd RV. Hyperinsulinemic hypoglycemia with nesidioblastosis after gastric-bypass surgery. N Engl J Med 353: 249-254, 2005.
37. Speck M, Cho YM, Asadi A, Rubino F, Kieffer TJ. Duodenal-jejunal bypass protects GK rats from β-cell loss and aggravation of hyperglycemia and increases enteroendocrine cells coexpressing GIP and GLP-1. Am J Physiol Endocrinol Metab 300: E923-E932, 2011.
38. Takasawa S, Ikeda T, Akiyama T, Nata K, Nakagawa K, Shervani NJ, Noguchi N, Murakami-Kawaguchi S, Yamauchi A, Takahashi I, Tomioka-Kumagai T, Okamoto H. Cyclin D1 activation through ATF-2 in Reg-induced pancreatic beta-cell regeneration. FEBS Lett 580: 585-591, 2006.
39. Takaya K, Ogawa Y, Isse N, Okazaki T, Satoh N, Masuzaki H, Mori K, Tamura N, Hosoda K, Nakao K. Molecular cloning of rat leptin receptor isoform complementary DNAs-identification of a missense mutation in Zucker fatty (fa/fa) rats. Biochem Biophys Res Commun 225: 75-83, 1996.
40. Tordoff MG, Tluczek JP, Friedman MI. Effect of hepatic portal glucose concentration on food intake and metabolism. Am J Physiol Regul Integr Comp Physiol 257: R1474-R1480, 1989.
41. Troy S, Soty M, Ribeiro L, Laval L, Migrenne S, Fioramonti X, Pillot B, Fauveau V, Aubert R, Viollet B, Foretz M, Leclerc J, Duchampt A, Zitoun C, Thorens B, Magnan C, Mithieux G, Andreelli F. Intestinal gluconeogenesis is a key factor for early metabolic changes after gastric bypass but not after gastric lap-band in mice. Cell Metab 8: 201-211, 2008.
42. Wang Y, Jacovetti C, Li B, Siddique T, Xiong X, Yin H, Wang M, Zhao H, Liu JL. Coordinated age-dependent and pancreatic-specific expression of mouse Reg2, Reg3α and Reg3β genes. Growth Factors 29: 1-10, 2011.
43. Watanabe T, Yonemura Y, Yonekura H, Suzuki Y, Miyashita H, Sugiyama K, Moriizumi S, Unno M, Tanaka O, Kondo H. Pancreatic beta-cell replication and amelioration of surgical diabetes by Reg protein. Proc Natl Acad Sci USA 91: 3589-3592, 1994.
44. Wolff C, Schott C, Porschewski P, Reischauer B, Becker KF. Successful protein extraction from over-fixed and long-term stored formalin-fixed tissues. PLoS One 6: e16353, 2011.
45. Woods M, Lan Z, Li J, Wheeler MB, Wang H, Wang R. Antidiabetic effects of duodenojejunal bypass in an experimental model of diabetes induced by a high-fat diet. Br J Surg 98: 686-696, 2011.
46. Xiong X, Wang X, Li B, Chowdhury S, Lu Y, Srikant CB, Ning N, Liu JL. Pancreatic islet-specific overexpression of Reg3β protein induced the expression of pro-islet genes and protected mice against streptozotocininduced diabetes. Am J Physiol Endocrinol Metab 300: E669-E680, 2011.
47. Zhou YP, Madjidi A, Wilson ME, Nothhelfer DA, Johnson JH, Palma JF, Schweitzer A, Burant C, Blume JE, Johnson JD. Matrix metalloproteinases contribute to insulin insufficiency in Zucker diabetic fatty rats. Diabetes 54: 2612-2619, 2005.