A novel humanized GLP-1 receptor model enables both affinity purification and Cre-LoxP deletion of the receptor

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Jun, Lucy S ^a   Showalter, Aaron D ^a   Ali, Nosher ^a   Dai, Feihan ^b   Ma, Wenzhen ^a   Coskun, Tamer ^a   Ficorilli, James V ^a   Wheeler, Michael B ^b   Michael, M Dodson ^a   Sloop, Kyle W ^a  

^a ELI LILLY AND COMPANY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCOSE; INSULIN; GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR;

ANIMAL EXPERIMENT; ANTIBODY DETECTION; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; GENE LOCUS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; LUNG; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS; PROTEIN PURIFICATION; STOMACH; STOMACH EMPTYING; WILD TYPE; ANIMAL; DIABETES MELLITUS, TYPE 2; DISEASE MODEL; GENETICS; HUMAN; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; GLUCOSE; GLUCOSE TOLERANCE TEST; HUMANS; INSULIN; MICE; MICE, TRANSGENIC; PANCREAS; RECEPTORS, GLUCAGON;

EID: 84898798260     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093746     Document Type: Article

References (52)

1. Holst JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439.
2. Estall JL, Drucker DJ (2006) Glucagon and glucagon-like peptide receptors as drug targets. Curr Pharm Des 12: 1731-1750.
3. Nauck MA, Kleine N, Orskov C, Holst JJ, Willms B, et al. (1993) Normalization of fasting hyperglycaemia by exogenous glucagon-like peptide 1 (7-36 amide) in type 2 (non-insulin-dependent) diabetic patients. Diabetologia 36: 741-744. (Pubitemid 23218642)
4. Thorens B (1992) Expression cloning of the pancreatic beta cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc Natl Acad Sci U S A 89: 8641-8645.
5. Hansotia T, Baggio LL, Delmeire D, Hinke SA, Yamada Y, et al. (2004) Double incretin receptor knockout (DIRKO) mice reveal an essential role for the enteroinsular axis in transducing the glucoregulatory actions of DPP-IV inhibitors. Diabetes 53: 1326-1335. (Pubitemid 38569020)
6. Lamont BJ, Li Y, Kwan E, Brown TJ, Gaisano H, et al. (2012) Pancreatic GLP-1 receptor activation is sufficient for incretin control of glucose metabolism in mice. J Clin Invest 122: 388-402.
7. Chia CW, Egan JM (2008) Incretin-based therapies in type 2 diabetes mellitus. J Clin Endocrinol Metab 93: 3703-3716.
8. Monami M, Marchionni N, Mannucci E (2009) Glucagon-like peptide-1 receptor agonists in type 2 diabetes: a meta-analysis of randomized clinical trials. Eur J Endocrinol 160: 909-917.
9. Halbirk M, Norrelund H, Moller N, Holst JJ, Schmitz O, et al. (2010) Cardiovascular and metabolic effects of 48-h glucagon-like peptide-1 infusion in compensated chronic patients with heart failure. Am J Physiol Heart Circ Physiol 298: H1096-1102.
10. Mendis B, Simpson E, MacDonald I, Mansell P (2012) Investigation of the haemodynamic effects of exenatide in healthy male subjects. Br J Clin Pharmacol 74: 437-444.
11. Kim M, Platt MJ, Shibasaki T, Quaggin SE, Backx PH, et al. (2013) GLP-1 receptor activation and Epac2 link atrial natriuretic peptide secretion to control of blood pressure. Nat Med.
12. Korner M, Stockli M, Waser B, Reubi JC (2007) GLP-1 receptor expression in human tumors and human normal tissues: potential for in vivo targeting. J Nucl Med 48: 736-743. (Pubitemid 47604973)
13. Vara E, Arias-Diaz J, Garcia C, Balibrea JL, Blazquez E (2001) Glucagon-like peptide-1(7-36) amide stimulates surfactant secretion in human type II pneumocytes. Am J Respir Crit Care Med 163: 840-846. (Pubitemid 32275852)
14. Benito E, Blazquez E, Bosch MA (1998) Glucagon-like peptide-1-(7-36)amide increases pulmonary surfactant secretion through a cyclic adenosine 3′,5′-monophosphate-dependent protein kinase mechanism in rat type II pneumocytes. Endocrinology 139: 2363-2368. (Pubitemid 28513760)
15. Richter G, Feddersen O, Wagner U, Barth P, Goke R, et al. (1993) GLP-1 stimulates secretion of macromolecules from airways and relaxes pulmonary artery. Am J Physiol 265: L374-381.
16. Panjwani N, Mulvihill EE, Longuet C, Yusta B, Campbell JE, et al. (2013) GLP-1 Receptor Activation Indirectly Reduces Hepatic Lipid Accumulation But Does Not Attenuate Development of Atherosclerosis in Diabetic Male ApoE 2/2 Mice. Endocrinology 154: 127-139.
17. Turton MD, O'Shea D, Gunn I, Beak SA, Edwards CM, et al. (1996) A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379: 69-72. (Pubitemid 26008136)
18. Tushuizen ME, Bunck MC, Pouwels PJ, van Waesberghe JH, Diamant M, et al. (2006) Incretin mimetics as a novel therapeutic option for hepatic steatosis. Liver Int 26: 1015-1017. (Pubitemid 44323421)
19. Gier B, Butler PC, Lai CK, Kirakossian D, DeNicola MM, et al. (2012) Glucagon like peptide-1 receptor expression in the human thyroid gland. J Clin Endocrinol Metab 97: 121-131.
20. Bjerre Knudsen L, Madsen LW, Andersen S, Almholt K, de Boer AS, et al. (2010) Glucagon-like Peptide-1 receptor agonists activate rodent thyroid C-cells causing calcitonin release and C-cell proliferation. Endocrinology 151: 1473-1486.
21. Bullock BP, Heller RS, Habener JF (1996) Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor. Endocrinology 137: 2968-2978. (Pubitemid 26192194)
22. Campos RV, Lee YC, Drucker DJ (1994) Divergent tissue-specific and developmental expression of receptors for glucagon and glucagon-like peptide-1 in the mouse. Endocrinology 134: 2156-2164. (Pubitemid 24142957)
23. Dunphy JL, Taylor RG, Fuller PJ (1998) Tissue distribution of rat glucagon receptor and GLP-1 receptor gene expression. Mol Cell Endocrinol 141: 179-186. (Pubitemid 28393391)
24. Pyke C, Knudsen LB (2013) The Glucagon-Like Peptide-1 Receptor-or Not? Endocrinology 154: 4-8.
25. Schwenk F, Baron U, Rajewsky K (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081. (Pubitemid 26012492)
26. Otto C, Fuchs I, Kauselmann G, Kern H, Zevnik B, et al. (2009) GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol Reprod 80: 34-41.
27. Sloop KW, Cao JX, Siesky AM, Zhang HY, Bodenmiller DM, et al. (2004) Hepatic and glucagon-like peptide-1-mediated reversal of diabetes by glucagon receptor antisense oligonucleotide inhibitors. J Clin Invest 113: 1571-1581. (Pubitemid 39071680)
28. Sloop KW, Willard FS, Brenner MB, Ficorilli J, Valasek K, et al. (2010) Novel small molecule glucagon-like peptide-1 receptor agonist stimulates insulin secretion in rodents and from human islets. Diabetes 59: 3099-3107.
29. Wilson-Perez HE, Chambers AP, Ryan KK, Li B, Sandoval DA, et al. (2013) Vertical sleeve gastrectomy is effective in two genetic mouse models of glucagon-like Peptide 1 receptor deficiency. Diabetes 62: 2380-2385.
30. Kojima K, Bowersock GJ, Kojima C, Klug CA, Grizzle WE, et al. (2012) Validation of a robust proteomic analysis carried out on formalin-fixed paraffin-embedded tissues of the pancreas obtained from mouse and human. Proteomics 12: 3393-3402.
31. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21: 70-71.
32. Doyle ME, Egan JM (2007) Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol Ther 113: 546-593. (Pubitemid 46365961)
33. Drucker DJ (2006) The biology of incretin hormones. Cell Metab 3: 153-165.
34. Imeryuz N, Yegen BC, Bozkurt A, Coskun T, Villanueva-Penacarrillo ML, et al. (1997) Glucagon-like peptide-1 inhibits gastric emptying via vagal afferent-mediated central mechanisms. Am J Physiol 273: G920-927.
35. Baggio LL, Drucker DJ (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132: 2131-2157. (Pubitemid 46711096)
36. Hansotia T, Drucker DJ (2005) GIP and GLP-1 as incretin hormones: lessons from single and double incretin receptor knockout mice. Regul Pept 128: 125-134. (Pubitemid 40380913)
37. Chen Q, Miller LJ, Dong M (2010) Role of N-linked glycosylation in biosynthesis, trafficking, and function of the human glucagon-like peptide 1 receptor. Am J Physiol Endocrinol Metab 299: E62-68.
38. Goke R, Just R, Lankat-Buttgereit B, Goke B (1994) Glycosylation of the GLP-1 receptor is a prerequisite for regular receptor function. Peptides 15: 675-681. (Pubitemid 24221842)
39. Whitaker GM, Lynn FC, McIntosh CH, Accili EA (2012) Regulation of GIP and GLP1 receptor cell surface expression by N-glycosylation and receptor heteromerization. PLoS One 7: e32675.
40. Butler AE, Campbell-Thompson M, Gurlo T, Dawson DW, Atkinson M, et al. (2013) Marked Expansion of Exocrine and Endocrine Pancreas with Incretin Therapy in Humans with increased Exocrine Pancreas Dysplasia and the potential for Glucagon-producing Neuroendocrine Tumors. Diabetes.
41. Heine RJ, Fu H, Kendall DM, Moller DE (2013) Comment on: Butler et al. Marked Expansion of Exocrine and Endocrine Pancreas With Incretin Therapy in Humans With Increased Exocrine Pancreas Dysplasia and the Potential for Glucagon-Producing Neuroendocrine Tumors. Diabetes 2013; 62: 2595-2604. Diabetes 62: e16-e17.
42. Butler AE, Campbell-Thompson M, Gurlo T, Dawson DW, Atkinson M, et al. (2013) Reponse to Comments on: Butler et al. Marked Expansion of Exocrine and Endocrine Pancreas With Incretin Therapy in Humans With Increased Exocrine Pancreas Dysplasia and the Potential for Glucagon-Producing Neuroendocrine Tumors. Diabetes 2013; 62: 2595-2604. Diabetes 62: e19-e22.
43. Scrocchi LA, Brown TJ, MaClusky N, Brubaker PL, Auerbach AB, et al. (1996) Glucose intolerance but normal satiety in mice with a null mutation in the glucagon-like peptide 1 receptor gene. Nat Med 2: 1254-1258. (Pubitemid 26375413)
44. Lobbestael E, Reumers V, Ibrahimi A, Paesen K, Thiry I, et al. (2010) Immunohistochemical detection of transgene expression in the brain using small epitope tags. BMC Biotechnol 10: 16.
45. Romani-Perez M, Outeirino-Iglesias V, Gil-Lozano M, Gonzalez-Matias LC, Mallo F, et al. (2013) Pulmonary GLP-1 Receptor Increases at Birth and Exogenous GLP-1 Receptor Agonists Augmented Surfactant-Protein Levels in Litters From Normal and Nitrofen-Treated Pregnant Rats. Endocrinology 154: 1144-1155.
46. Suzuki H, Dann CT, Rajkovic A (2013) Generation of a germ cell-specific mouse transgenic CHERRY reporter, Sohlh1-mCherryFlag. Genesis 51: 50-58.
47. Tornehave D, Kristensen P, Romer J, Knudsen LB, Heller RS (2008) Expression of the GLP-1 receptor in mouse, rat, and human pancreas. J Histochem Cytochem 56: 841-851.
48. Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ, et al. (2008) Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptor-dependent and -independent pathways. Circulation 117: 2340-2350. (Pubitemid 351653542)
49. Schlatter P, Beglinger C, Drewe J, Gutmann H (2007) Glucagon-like peptide 1 receptor expression in primary porcine proximal tubular cells. Regul Pept 141: 120-128. (Pubitemid 46482693)
50. Maurel D, Comps-Agrar L, Brock C, Rives ML, Bourrier E, et al. (2008) Cell-surface protein-protein interaction analysis with time-resolved FRET and snaptag technologies: application to GPCR oligomerization. Nat Methods 5: 561-567. (Pubitemid 351761765)
51. Persani L, Calebiro D, Bonomi M (2007) Technology Insight: modern methods to monitor protein-protein interactions reveal functional TSH receptor oligomerization. Nat Clin Pract Endocrinol Metab 3: 180-190. (Pubitemid 46146970)
52. Zvonok N, Yaddanapudi S, Williams J, Dai S, Dong K, et al. (2007) Comprehensive proteomic mass spectrometric characterization of human cannabinoid CB2 receptor. J Proteome Res 6: 2068-2079. (Pubitemid 46985094)