Glucose intolerance and reduced proliferation of pancreatic β-cells in transgenic pigs with impaired glucose-dependent insulinotropic polypeptide function

Diabetes

Volumn 59, Issue 5, 2010, Pages 1228-1238

  Renner, Simone ^a   Fehlings, Christiane ^a   Herbach, Nadja ^a   Hofmann, Andreas ^b   Von Waldthausen, Dagmar C ^a   Kessler, Barbara ^a   Ulrichs, Karin ^c   Chodnevskaja, Irina ^c   Moskalenko, Vasiliy ^c   Amselgruber, Werner ^d   Göke, Burkhard ^e   Pfeifer, Alexander ^b   Wanke, Rüdiger ^a   Wolf, Eckhard ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^d UNIVERSITY OF HOHENHEIM   (Germany)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; GASTRIC INHIBITORY POLYPEPTIDE; GLUCOSE; INCRETIN; INSULIN; LENTIVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL POPULATION; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; IMPAIRED GLUCOSE TOLERANCE; INSULIN LIKE ACTIVITY; INSULIN RELEASE; INTRAVENOUS GLUCOSE TOLERANCE TEST; MALE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; STEREOLOGY; SWINE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; INSULIN; INSULIN-SECRETING CELLS; RECEPTORS, GLUCAGON; SWINE;

EID: 77951829073     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0519     Document Type: Article

References (42)

1. Baggio LL, Drucker DJ. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007;132:2131-2157
2. Mayo KE, Miller LJ, Bataille D, Dalle S, Goke B, Thorens B, Drucker DJ. International Union of Pharmacology. XXXV. The glucagon receptor family. Pharmacol Rev 2003;55:167-194
3. Holst JJ, Gromada J. Role of incretin hormones in the regulation of insulin secretion in diabetic and nondiabetic humans. Am J Physiol Endocrinol Metab 2004;287:E199-E206 (Pubitemid 38943883)
4. Saxena R, Hivert MF, Langenberg C, Tanaka T, Pankow JS, Vollenweider P, Lyssenko V, Bouatia-Naji N, Dupuis J, Jackson AU, Kao WH, Li M, Glazer NL, Manning AK, Luan J, Stringham HM, Prokopenko I, Johnson T, Grarup N, Boesgaard TW, Lecoeur C, Shrader P, O'Connell J, Ingelsson E, Couper DJ, Rice K, Song K, Andreasen CH, Dina C, Kottgen A, Le Bacquer O, Pattou F, Taneera J, Steinthorsdottir V, Rybin D, Ardlie K, Sampson M, Qi L, van Hoek M, Weedon MN, Aulchenko YS, Voight BF, Grallert H, Balkau B, Bergman RN, Bielinski SJ, Bonnefond A, Bonnycastle LL, Borch-Johnsen K, Bottcher Y, Brunner E, Buchanan TA, Bumpstead SJ, Cavalcanti-Proenca C, Charpentier G, Chen YD, Chines PS, Collins FS, Cornelis M, G JC, Delplanque J, Doney A, Egan JM, Erdos MR, Firmann M, Forouhi NG, Fox CS, Goodarzi MO, Graessler J, Hingorani A, Isomaa B, Jorgensen T, Kivimaki M, Kovacs P, Krohn K, Kumari M, Lauritzen T, Levy-Marchal C, Mayor V, McAteer JB, Meyre D, Mitchell BD, Mohlke KL, Morken MA, Narisu N, Palmer CN, Pakyz R, Pascoe L, Payne F, Pearson D, Rathmann W, Sandbaek A, Sayer AA, Scott LJ, Sharp SJ, Sijbrands E, Singleton A, Siscovick DS, Smith NL, Sparso T, Swift AJ, Syddall H, Thorleifsson G, Tonjes A, Tuomi T, Tuomilehto J, Valle TT, Waeber G, Walley A, Waterworth DM, Zeggini E, Zhao JH, Illig T, Wichmann HE, Wilson JF, van Duijn C, Hu FB, Morris AD, Frayling TM, Hattersley AT, Thorsteinsdottir U, Stefansson K, Nilsson P, Syvanen AC, Shuldiner AR, Walker M, Bornstein SR, Schwarz P, Williams GH, Nathan DM, Kuusisto J, Laakso M, Cooper C, Marmot M, Ferrucci L, Mooser V, Stumvoll M, Loos RJ, Altshuler D, Psaty BM, Rotter JI, Boerwinkle E, Hansen T, Pedersen O, Florez JC, McCarthy MI, Boehnke M, Barroso I, Sladek R, Froguel P, Meigs JB, Groop L, Wareham NJ, Watanabe RM: Genetic variation in GIPR influences the glucose and insulin responses to an oral glucose challenge. Nat Genet 2010;42:142-148
5. Ehses JA, Casilla VR, Doty T, Pospisilik JA, Winter KD, Demuth HU, Pederson RA, McIntosh CH. Glucose-dependent insulinotropic polypeptide promotes beta-(INS-1) cell survival via cyclic adenosine monophosphate-mediated caspase-3 inhibition and regulation of p38 mitogen-activated protein kinase. Endocrinology 2003;144:4433-4445 (Pubitemid 37204843)
6. Trumper A, Trumper K, Horsch D. Mechanisms of mitogenic and antiapoptotic signaling by glucose-dependent insulinotropic polypeptide in beta(INS-1)-cells. J Endocrinol 2002;174:233-246 (Pubitemid 34965762)
7. Trumper A, Trumper K, Trusheim H, Arnold R, Goke B, Horsch D. Glucose-dependent insulinotropic polypeptide is a growth factor for beta (INS-1) cells by pleiotropic signaling. Mol Endocrinol 2001;15:1559-1570
8. Kim SJ, Winter K, Nian C, Tsuneoka M, Koda Y, McIntosh CH. Glucose-dependent insulinotropic polypeptide (GIP) stimulation of pancreatic beta-cell survival is dependent upon phosphatidylinositol 3-kinase (PI3K)/protein kinase B (PKB) signaling, inactivation of the forkhead transcription factor Foxo1, and down-regulation of bax expression. J Biol Chem 2005;280:22297-22307 (Pubitemid 40827886)
9. Yusta B, Baggio LL, Estall JL, Koehler JA, Holland DP, Li H, Pipeleers D, Ling Z, Drucker DJ. GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 2006;4:391-406 (Pubitemid 44752565)
10. Meier JJ, Hucking K, Holst JJ, Deacon CF, Schmiegel WH, Nauck MA. Reduced insulinotropic effect of gastric inhibitory polypeptide in first-degree relatives of patients with type 2 diabetes. Diabetes 2001;50:2497-2504 (Pubitemid 33642767)
11. Nauck MA, Heimesaat MM, Orskov C, Holst JJ, Ebert R, Creutzfeldt W. Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J Clin Invest 1993;91:301-307 (Pubitemid 23037285)
12. Drucker DJ, Nauck MA. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006;368:1696-1705
13. Nauck MA, Baller B, Meier JJ. Gastric inhibitory polypeptide and glucagon-like peptide-1 in the pathogenesis of type 2 diabetes. Diabetes 2004;53(Suppl. 3):S190-S196 (Pubitemid 39564543)
14. Miyawaki K, Yamada Y, Yano H, Niwa H, Ban N, Ihara Y, Kubota A, Fujimoto S, Kajikawa M, Kuroe A, Tsuda K, Hashimoto H, Yamashita T, Jomori T, Tashiro F, Miyazaki J, Seino Y. Glucose intolerance caused by a defect in the entero-insular axis: a study in gastric inhibitory polypeptide receptor knockout mice. Proc Natl Acad Sci U S A 1999;96:14843-14847 (Pubitemid 30019727)
15. Hansotia T, Drucker DJ. GIP and GLP-1 as incretin hormones: lessons from single and double incretin receptor knockout mice. Regul Pept 2005;128:125-134 (Pubitemid 40380913)
16. Herbach N, Goeke B, Schneider M, Hermanns W, Wolf E, Wanke R. Overexpression of a dominant negative GIP receptor in transgenic mice results in disturbed postnatal pancreatic islet and beta-cell development. Regul Pept 2005;125:103-117 (Pubitemid 39593715)
17. Hofmann A, Kessler B, Ewerling S, Weppert M, Vogg B, Ludwig H, Stojkovic M, Boelhauve M, Brem G, Wolf E, Pfeifer A. Efficient transgenesis in farm animals by lentiviral vectors. EMBO Rep 2003;4:1054-1060 (Pubitemid 37527423)
18. Pfeifer A, Ikawa M, Dayn Y, Verma IM. Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc Natl Acad Sci U S A 2002;99:2140-2145 (Pubitemid 34169028)
19. Klose R, Kemter E, Bedke T, Bittmann I, Kelsser B, Endres R, Pfeffer K, Schwinzer R, Wolf E. Expression of biologically active human TRAIL in transgenic pigs. Transplantation 2005;80:222-230 (Pubitemid 41061679)
20. Larsen MO, Rolin B, Ribel U, Wilken M, Deacon CF, Svendsen O, Gotfredsen CF, Carr RD. Valine pyrrolidide preserves intact glucose-dependent insulinotropic peptide and improves abnormal glucose tolerance in minipigs with reduced beta-cell mass. Exp Diabesity Res 2003;4:93-105 (Pubitemid 37080777)
21. Moritz MW, Dawe EJ, Holliday JF, Elliott S, Mattei JA, Thomas AL. Chronic central vein catheterization for intraoperative and long-term venous access in swine. Lab Anim Sci 1989;39:153-155
22. Kobayashi K, Kobayashi N, Okitsu T, Yong C, Fukazawa T, Ikeda H, Kosaka Y, Narushima M, Arata T, Tanaka N. Development of a porcine model of type 1 diabetes by total pancreatectomy and establishment of a glucose tolerance evaluation method. Artif Organs 2004;28:1035-1042 (Pubitemid 40378880)
23. Krickhahn M, Meyer T, Buhler C, Thiede A, Ulrichs K. Highly efficient isolation of porcine islets of Langerhans for xenotransplantation: numbers, purity, yield and in vitro function. Ann Transplant 2001;6:48-54
24. Ricordi C, Socci C, Davalli AM, Staudacher C, Baro P, Vertova A, Sassi I, Gavazzi F, Pozza G, Di Carlo V. Isolation of the elusive pig islet. Surgery 1990;107:688-694
25. van der Burg MP, Graham JM. Iodixanol density gradient preparation in university of wisconsin solution for porcine islet purification. Scientific-World Journal 2003;3:1154-1159
26. Latif ZA, Noel J, Alejandro R. A simple method of staining fresh and cultured islets. Transplantation 1988;45:827-830
27. Jones KH, Senft JA. An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J Histochem Cytochem 1985;33:77-79
28. Scherle W. A simple method for volumetry of organs in quantitative stereology. Mikroskopie 1970;26:57-60
29. Bonner-Weir S, Baxter LA, Schuppin GT, Smith FE. A second pathway for regeneration of adult exocrine and endocrine pancreas: a possible recapitulation of embryonic development. Diabetes 1993;42:1715-1720 (Pubitemid 23346407)
30. Petrik J, Reusens B, Arany E, Remacle C, Coelho C, Hoet JJ, Hill DJ. A low protein diet alters the balance of islet cell replication and apoptosis in the fetal and neonatal rat and is associated with a reduced pancreatic expression of insulin-like growth factor-II. Endocrinology 1999;140:4861-4873 (Pubitemid 30666156)
31. Xu G, Stoffers DA, Habener JF, Bonner-Weir S. Exendin-4 stimulates both β-cell replication and neogenesis, resulting in increased β-cell mass and improved glucose tolerance in diabetic rats. Diabetes 1999;48:2270-2276 (Pubitemid 30395416)
32. Herbach N, Rathkolb B, Kemter E, Pichl L, Klaften M, de Angelis MH, Halban PA, Wolf E, Aigner B, Wanke R. Dominant-negative effects of a novel mutated Ins2 allele causes early-onset diabetes and severe β-cell loss in Munich Ins2C95S mutant mice. Diabetes 2007;56:1268-1276 (Pubitemid 46715607)
33. Iatropoulos MJ, Williams GM. Proliferation markers. Exp Toxicol Pathol 1996;48:175-181
34. Hui H, Dotta F, Di Mario U, Perfetti R. Role of caspases in the regulation of apoptotic pancreatic islet beta-cells death. J Cell Physiol 2004;200:177-200 (Pubitemid 38880203)
35. Verbeke G, Molenberghs G. Linear Mixed Models for Longitudinal Data. New York, Springer, 2001
36. Bock T, Kyhnel A, Pakkenberg B, Buschard K. The postnatal growth of the beta-cell mass in pigs. J Endocrinol 2003;179:245-252 (Pubitemid 37461354)
37. Pamir N, Lynn FC, Buchan AM, Ehses J, Hinke SA, Pospisilik JA, Miyawaki K, Yamada Y, Seino Y, McIntosh CH, Pederson RA. Glucose-dependent insulinotropic polypeptide receptor null mice exhibit compensatory changes in the enteroinsular axis. Am J Physiol Endocrinol Metab 2003;284:E931-E939 (Pubitemid 36444028)
38. Hansotia T, Baggio LL, Delmeire D, Hinke SA, Yamada Y, Tsukiyama K, Seino Y, Holst JJ, Schuit F, Drucker DJ. Double incretin receptor knockout (DIRKO) mice reveal an essential role for the enteroinsular axis in transducing the glucoregulatory actions of DPP-IV inhibitors. Diabetes 2004;53:1326-1335 (Pubitemid 38569020)
39. Preitner F, Ibberson M, Franklin I, Binnert C, Pende M, Gjinovci A, Hansotia T, Drucker DJ, Wollheim C, Burcelin R, Thorens B. Glucoincretins control insulin secretion at multiple levels as revealed in mice lacking GLP-1 and GIP receptors. J Clin Invest 2004;113:635-645 (Pubitemid 38542513)
40. Shaffer C. Incretin mimetics vie for slice of type 2 diabetes market. Nat Biotechnol 2007;25:263 (Pubitemid 46398752)
41. Medarova Z, Moore A. MRI as a tool to monitor islet transplantation. Nat Rev Endocrinol 2009;5:444-452
42. Larsen MO, Rolin B. Use of the Gottingen minipig as a model of diabetes, with special focus on type 1 diabetes research. ILAR J 2004;45:303-313