Cellular responses of novel human pancreatic β-cell line, 1.1B4 to hyperglycemia

Islets

Volumn 5, Issue 4, 2013, Pages 170-177

  Vasu, Srividya ^a   McClenaghan, Neville H ^a   McCluskey, Jane T ^a   Flatt, Peter R ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

1.1B4; Diabetes; Glucose; Mechanisms; Toxicity

Indexed keywords

ALANINE; ANTIOXIDANT; CALCIUM; FORSKOLIN; GLUCAGON LIKE PEPTIDE 1; GLUCOKINASE; GLUCOSE; INSULIN; POTASSIUM CHLORIDE; TRANSCRIPTION FACTOR PDX 1;

APOPTOSIS; ARTICLE; COMET ASSAY; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; HUMAN; HYPERGLYCEMIA; INSULIN RELEASE; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION;

1.1B4; DIABETES; GLUCOSE; MECHANISMS; TOXICITY;

APOPTOSIS; CELL LINE; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; GLUCOKINASE; GLUCOSE; HUMANS; HYPERGLYCEMIA; INSULIN; INSULIN-SECRETING CELLS;

EID: 84890238001     PISSN: 19382014     EISSN: 19382022     Source Type: Journal    
DOI: 10.4161/isl.26184     Document Type: Article

References (47)

1. Poitout V, Robertson RP. Minireview: Secondary beta-cell failure in type 2 diabetes - a convergence of glucotoxicity and lipotoxicity. Endocrinology 2002; 143:339-42; PMID:11796484; http://dx.doi.org/10.1210/en.143.2.339
2. Del Prato S. Role of glucotoxicity and lipotoxicity in the pathophysiology of Type 2 diabetes mellitus and emerging treatment strategies. Diabet Med 2009; 26:1185-92; PMID:20002468; http://dx.doi.org/10.1111/j.1464- 5491.2009.02847.x
3. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J Biol Chem 2004; 279:42351-4; PMID:15258147; http://dx.doi.org/10.1074/jbc.R400019200
4. Robertson R, Zhou H, Zhang T, Harmon JS. Chronic oxidative stress as a mechanism for glucose toxicity of the beta cell in type 2 diabetes. Cell Biochem Biophys 2007; 48:139-46; PMID:17709883; http://dx.doi.org/10.1007/s12013-007- 0026-5
5. Brunner Y, Schvartz D, Priego-Capote F, Couté Y, Sanchez JC. Glucotoxicity and pancreatic proteomics. J Proteomics 2009; 71:576-91; PMID:19027091; http://dx.doi.org/10.1016/j.jprot.2008.10.002
6. Araki E, Oyadomari S, Mori M. Endoplasmic reticulum stress and diabetes mellitus. Intern Med 2003; 42:7-14; PMID:12583611; http://dx.doi.org/10.2169/ internalmedicine.42.7
7. Thivolet CH, Demidem A, Haftek M, Durand A, Bertrand J. Structure, function, and immunogenicity of human insulinoma cells. Diabetes 1988; 37:1279-86; PMID:2457530; http://dx.doi.org/10.2337/diabetes.37.9.1279
8. Gueli N, Toto A, Palmieri G, Carmenini G, Delpino A. In vitro growth of a cell line originated from a human insulinoma. J Exp Clin Cancer Res 1987; 6:281-5
9. Thivolet C, Chatelain P, Haftek M, Durand A, Pugeat M. [Morphologic and functional study of a human insulin-secreting cell line]. C R Acad Sci III 1986; 303:381-6; PMID:3022894
10. Zalzman M, Anker-Kitai L, Efrat S. Differentiation of human liver-derived, insulin-producing cells toward the beta-cell phenotype. Diabetes 2005; 54:2568-75; PMID:16123344; http://dx.doi.org/10.2337/diabetes.54.9.2568
11. Segev H, Fishman B, Ziskind A, Shulman M, Itskovitz-Eldor J. Differentiation of human embryonic stem cells into insulin-producing clusters. Stem Cells 2004; 22:265-74; PMID:15153604; http://dx.doi.org/10.1634/stemcells. 22-3-265
12. Gartner W, Koc F, Nabokikh A, Daneva T, Niederle B, Luger A, Wagner L. Long-term in vitro growth of human insulin-secreting insulinoma cells. Neuroendocrinology 2006; 83:123-30; PMID:16888402; http://dx.doi.org/10.1159/ 000094875
13. Ravassard P, Hazhouz Y, Pechberty S, Bricout-Neveu E, Armanet M, Czernichow P, Scharfmann R. A genetically engineered human pancreatic β cell line exhibiting glucose-inducible insulin secretion. J Clin Invest 2011; 121:3589-97; PMID:21865645; http://dx.doi.org/10.1172/JCI58447
14. McCluskey JT, Hamid M, Guo-Parke H, McClenaghan NH, Gomis R, Flatt PR. Development and functional characterization of insulin-releasing human pancreatic beta cell lines produced by electrofusion. J Biol Chem 2011; 286:21982-92; PMID:21515691; http://dx.doi.org/10.1074/jbc.M111.226795
15. Vasu S, McClenaghan NH, McCluskey JT, Flatt PR. Effects of lipotoxicity on a novel insulin-secreting human pancreatic β-cell line, 1.1B4. Biol Chem 2013; 394:909-18; PMID:23492555
16. Sachdeva MM, Claiborn KC, Khoo C, Yang J, Groff DN, Mirmira RG, Stoffers DA. Pdx1 (MODY4) regulates pancreatic beta cell susceptibility to ER stress. Proc Natl Acad Sci U S A 2009; 106:19090-5; PMID:19855005; http://dx.doi.org/10. 1073/pnas.0904849106
17. Eizirik DL, Korbutt GS, Hellerström C. Prolonged exposure of human pancreatic islets to high glucose concentrations in vitro impairs the beta-cell function. J Clin Invest 1992; 90:1263-8; PMID:1401063; http://dx.doi.org/10. 1172/JCI115989
18. Tanaka Y, Gleason CE, Tran PO, Harmon JS, Robertson RP. Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc Natl Acad Sci U S A 1999; 96:10857-62; PMID:10485916; http://dx.doi.org/10.1073/pnas.96.19.10857
19. Kooptiwut S, Kebede M, Zraika S, Visinoni S, Aston-Mourney K, Favaloro J, Tikellis C, Thomas MC, Forbes JM, Cooper ME, et al. High glucose-induced impairment in insulin secretion is associated with reduction in islet glucokinase in a mouse model of susceptibility to islet dysfunction. J Mol Endocrinol 2005; 35:39-48; PMID:16087720; http://dx.doi.org/10.1677/jme.1.01720
20. Dubois M, Vacher P, Roger B, Huyghe D, Vandewalle B, Kerr-Conte J, Pattou F, Moustaïd-Moussa N, Lang J. Glucotoxicity inhibits late steps of insulin exocytosis. Endocrinology 2007; 148:1605-14; PMID:17204559; http://dx.doi.org/10.1210/en.2006-1022
21. Ahmed M, Muhammed SJ, Kessler B, Salehi A. Mitochondrial proteome analysis reveals altered expression of voltage dependent anion channels in pancreatic β-cells exposed to high glucose. Islets 2010; 2:283-92; PMID:21099326; http://dx.doi.org/10.4161/isl.2.5.12639
22. Maris M, Ferreira GB, D'Hertog W, Cnop M, Waelkens E, Overbergh L, Mathieu C. High glucose induces dysfunction in insulin secretory cells by different pathways: a proteomic approach. J Proteome Res 2010; 9:6274-87; PMID:20942503; http://dx.doi.org/10.1021/pr100557w
23. Heit JJ. Calcineurin/NFAT signaling in the beta-cell: From diabetes to new therapeutics. Bioessays 2007; 29:1011-21; PMID:17876792; http://dx.doi.org/10.1002/bies.20644
24. Vozzi C, Ullrich S, Charollais A, Philippe J, Orci L, Meda P. Adequate connexin-mediated coupling is required for proper insulin production. J Cell Biol 1995; 131:1561-72; PMID:8522612; http://dx.doi.org/10.1083/jcb.131.6.1561
25. Hauge-Evans AC, Squires PE, Persaud SJ, Jones PM. Pancreatic beta-cell-to-beta-cell interactions are required for integrated responses to nutrient stimuli: enhanced Ca2+ and insulin secretory responses of MIN6 pseudoislets. Diabetes 1999; 48:1402-8; PMID:10389845; http://dx.doi.org/10. 2337/diabetes.48.7.1402
26. Sato T, Haimovici R, Kao R, Li AF, Roy S. Downregulation of connexin 43 expression by high glucose reduces gap junction activity in microvascular endothelial cells. Diabetes 2002; 51:1565-71; PMID:11978657; http://dx.doi.org/10.2337/diabetes.51.5.1565
27. Heit JJ, Apelqvist AA, Gu X, Winslow MM, Neilson JR, Crabtree GR, Kim SK. Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 2006; 443:345-9; PMID:16988714; http://dx.doi.org/10.1038/nature05097
28. Klee P, Allagnat F, Pontes H, Cederroth M, Charollais A, Caille D, Britan A, Haefliger JA, Meda P. Connexins protect mouse pancreatic β cells against apoptosis. J Clin Invest 2011; 121:4870-9; PMID:22056383; http://dx.doi.org/10.1172/JCI40509
29. McTaggart JS, Clark RH, Ashcroft FM. The role of the KATP channel in glucose homeostasis in health and disease: more than meets the islet. J Physiol 2010; 588:3201-9; PMID:20519313; http://dx.doi.org/10.1113/jphysiol.2010.191767
30. Jonas JC, Bensellam M, Duprez J, Elouil H, Guiot Y, Pascal SMA. Glucose regulation of islet stress responses and beta-cell failure in type 2 diabetes. Diabetes Obes Metab 2009; 11(Suppl 4):65-81; PMID:19817790; http://dx.doi.org/ 10.1111/j.1463-1326.2009.01112.x
31. Laybutt DR, Sharma A, Sgroi DC, Gaudet J, Bonner-Weir S, Weir GC. Genetic regulation of metabolic pathways in beta-cells disrupted by hyperglycemia. J Biol Chem 2002; 277:10912-21; PMID:11782487; http://dx.doi.org/10.1074/jbc. M111751200
32. Lin P, Chen L, Li D, Liu J, Yang N, Sun Y, Xu Y, Fu Y, Hou X. Adiponectin reduces glucotoxicity-induced apoptosis of INS-1 rat insulin-secreting cells on a microfluidic chip. Tohoku J Exp Med 2009; 217:59-65; PMID:19155609; http://dx.doi.org/10.1620/tjem.217.59
33. Poitout V, Amyot J, Semache M, Zarrouki B, Hagman D, Fontes G. Glucolipotoxicity of the pancreatic beta cell. Biochim Biophys Acta 2010; 1801:289-298.
34. Goehring I, Sauter NS, Catchpole G, Assmann A, Shu L, Zien KS, Moehlig M, Pfeiffer AF, Oberholzer J, Willmitzer L, et al. Identification of an intracellular metabolic signature impairing beta cell function in the rat beta cell line INS-1E and human islets. Diabetologia 2011; 54:2584-94; PMID:21796486; http://dx.doi.org/10.1007/s00125-011-2249-7
35. Greenman IC, Gomez E, Moore CE, Herbert TP. Distinct glucose-dependent stress responses revealed by translational profiling in pancreatic beta-cells. J Endocrinol 2007; 192:179-87; PMID:17210755; http://dx.doi.org/10.1677/joe.1. 06898
36. Karunakaran U, Kim HJ, Kim JY, Lee IK. Guards and culprits in the endoplasmic reticulum: Glucolipotoxicity and beta-cell failure in type II diabetes. Exp Diabetes Res 2012; 2012:639762.
37. Ron D. Translational control in the endoplasmic reticulum stress response. J Clin Invest 2002; 110:1383-8; PMID:12438433
38. Laybutt DR, Kaneto H, Hasenkamp W, Grey S, Jonas JC, Sgroi DC, Groff A, Ferran C, Bonner-Weir S, Sharma A, et al. Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to beta-cell survival during chronic hyperglycemia. Diabetes 2002; 51:413-23; PMID:11812749; http://dx.doi.org/10.2337/diabetes.51.2.413
39. Couté Y, Brunner Y, Schvartz D, Hernandez C, Masselot A, Lisacek F, Wollheim CB, Sanchez JC. Early activation of the fatty acid metabolism pathway by chronic high glucose exposure in rat insulin secretory beta-cells. Proteomics 2010; 10:59-71; PMID:19882656; http://dx.doi.org/10.1002/pmic. 200900080
40. Lim S, Rashid MA, Jang M, Kim Y, Won H, Lee J, Woo JT, Kim YS, Murphy MP, Ali L, et al. Mitochondria-targeted antioxidants protect pancreatic β-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity. Cell Physiol Biochem 2011; 28:873-86; PMID:22178940; http://dx.doi.org/10.1159/000335802
41. Shi XL, Ren YZ, Wu J. Intermittent high glucose enhances apoptosis in INS-1 cells. Exp Diabetes Res 2011; 2011:754673.
42. Kaneko Y, Kimura T, Taniguchi S, Souma M, Kojima Y, Kimura Y, Kimura H, Niki I. Glucose-induced production of hydrogen sulfide may protect the pancreatic beta-cells from apoptotic cell death by high glucose. FEBS Lett 2009; 583:377-82; PMID:19100738; http://dx.doi.org/10.1016/j.febslet.2008.12.026
43. Chen J, Saxena G, Mungrue IN, Lusis AJ, Shalev A. Thioredoxin-interacting protein: a critical link between glucose toxicity and beta-cell apoptosis. Diabetes 2008; 57:938-44; PMID:18171713; http://dx.doi.org/10.2337/db07-0715
44. Wang Y, Gao L, Li Y, Chen H, Sun Z. Nifedipine protects INS-1 beta-cell from high glucose-induced ER stress and apoptosis. Int J Mol Sci 2011; 12:7569-80; PMID:22174617; http://dx.doi.org/10.3390/ijms12117569
45. Flatt PR, Bailey CJ. Abnormal plasma glucose and insulin responses in heterozygous lean (ob/+) mice. Diabetologia 1981; 20:573-7; PMID:7026332; http://dx.doi.org/10.1007/BF00252768
46. Lenzen S, Tiedge M, Flatt PR, Bailey CJ, Panten U. Defective regulation of glucokinase in rat pancreatic islet cell tumours. Acta Endocrinol (Copenh) 1987; 115:514-20; PMID:2820174
47. Lees Murdock DJ, Barnett YA, Barnett CR. DNA damage and cytotoxicity in pancreatic β-cells expressing human CYP2E1. Biochem Pharmacol 2004; 68:523-30; PMID:15242818; http://dx.doi.org/10.1016/j.bcp.2004.04.008