Differential molecular and cellular responses of GLP-1 secreting L-cells and pancreatic alpha cells to glucotoxicity and lipotoxicity

Experimental Cell Research

Volumn 336, Issue 1, 2015, Pages 100-108

  Vasu, Srividya ^a   Charlotte Moffett, R ^a   McClenaghan, Neville H ^a   Flatt, Peter R ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

Alpha cells; Beta cells; GLP 1; Glucotoxicity; L cells; Lipotoxicity

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; GLUCOSE; MESSENGER RNA; PALMITIC ACID; PROTEIN BAX; BIOLOGICAL MARKER; INSULIN; PALMITIC ACID DERIVATIVE; SWEETENING AGENT;

APOPTOSIS; ARTICLE; CELL FUNCTION; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; GLUCAGON RELEASE; GLUCOTOXICITY; HORMONE RELEASE; HYPERGLYCEMIA; HYPERLIPIDEMIA; IN VITRO STUDY; INSULIN RELEASE; L CELL LINE; LD50; LIPOTOXICITY; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY CELL; UPREGULATION; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; MOUSE; PATHOPHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION (PROCESS); WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; GLUCAGON-LIKE PEPTIDE 1; GLUCAGON-SECRETING CELLS; GLUCOSE; HYPERGLYCEMIA; INSULIN; INSULIN-SECRETING CELLS; MICE; PALMITATES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SWEETENING AGENTS;

EID: 84943415049     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.05.022     Document Type: Article

References (55)

1. Araki E., Oyadomari S., Mori M. Endoplasmic reticulum stress and diabetes mellitus. Intern. Med. 2003, 42:7-14.
2. Bach S.P., Renehan A.G., Potten C.S. Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 2000, 21:469-476.
3. Baggio L.L., Drucker D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
4. Brunner Y., Schvartz D., Priego-Capote F., Coute Y., Sanchez J.C. Glucotoxicity and pancreatic proteomics. J. Proteomics 2009, 71:576-591.
5. Cani P.D., Hoste S., Guiot Y., Delzenne N.M. Dietary non-digestible carbohydrates promote l-cell differentiation in the proximal colon of rats. Br. J. Nutr. 2007, 98:32-37.
6. Choi S.E., Lee Y.J., Hwang G.S., Chung J.H., Lee S.J., Lee J.H., Han S.J., Kim H.J., Lee K.W., Kim Y., Jun H.S., Kang Y. Supplement of TCA cycle intermediates protects against high glucose/palmitate-induced INS-1 beta cell death. Arch. Biochem. Biophys. 2011, 505:231-241.
7. Cunha D.A., Hekerman P., Ladrière L., Bazarra-Castro A., Ortis F., Wakeham M.C., Moore F., Rasschaert J., Cardozo A.K., Bellomo E., Overbergh L., Mathieu C., Lupi R., Hai T., Herchuelz A., Marchetti P., Rutter G.A., Eizirik D.L., Cnop M. Initiation and execution of lipotoxic ER stress in pancreatic beta-cells. J. Cell Sci. 2008, 121:2308-2318.
8. Cvjetićanin T., Stojanović I., Timotijević G., Stosić-Grujicić S., Miljković D. T cells cooperate with palmitic acid in induction of beta cell apoptosis. BMC Immunol. 2009, 10(29).
9. D'Aleo V., Del Guerra S., Martano M., Bonamassa B., Canistro D., Soleti A., Valgimigli L., Paolini M., Filipponi F., Boggi U., Del Prato S., Lupi R. The non-peptidyl low molecular weight radical scavenger IAC protects human pancreatic islets from lipotoxicity. Mol. Cell. Endocrinol. 2009, 309:63-66.
10. Drucker D.J. Biologic actions and therapeutic potential of the proglucagon-derived peptides. Nat. Clin. Pract. Endocrinol. Metab. 2005, 1:22-31.
11. Flatt P.R., Bailey C.J. Abnormal plasma glucose and insulin response in heterozygous lean (ob/+) mice. Diabetologia 1981, 42:670-674.
12. Gehrmann W., Elsner M., Lenzen S. Role of metabolically generated reactive oxygen species for lipotoxicity in pancreatic beta-cells. Diabetes Obes. Metab. 2010, 12(Suppl 2):149-158.
13. Greenman I.C., Gomez E., Moore C.E., Herbert T.P. Distinct glucose-dependent stress responses revealed by translational profiling in pancreatic beta-cells. J. Endocrinol. 2007, 192:179-187.
14. Hellemans K.H., Hannaert J.C., Denys B., Steffensen K.R., Raemdonck C., Martens G.A., Van Veldhoven P.P., Gustafsson J.A., Pipeleers D. Susceptibility of pancreatic beta cells to fatty acids is regulated by LXR/PPARalpha-dependent stearoyl-coenzyme A desaturase. PloS One 2009, 4:e7266.
15. Holst J.J., Knop F.K., Vilsboll T., Krarup T., Madsbad S. Loss of incretin effect is a specific, important, and early characteristic of type 2 diabetes. Diabetes Care 2011, 34(Suppl 2):S251-S257.
16. Holst J.J. Enteroendocrine secretion of gut hormones in diabetes, obesity and after bariatric surgery. Curr. Opin. Pharmacol. 2013, 13:983-988.
17. Hong J., Abudula R., Chen J., Jeppesen P.B., Dyrskog S.E., Xiao J., Colombo M., Hermansen K. The short-term effect of fatty acids on glucagon secretion Is influenced by their chain length, spatial configuration, and degree of unsaturation: studies in vitro. Metabolism 2005, 54:1329-1336.
18. Hong J., Jeppesen P.B., Nordentoft I., Hermansen K. fatty acid-induced effect on glucagon secretion Is mediated via fatty acid oxidation. Diabetes Metab. Res. Rev. 2007, 23:202-210.
19. Hong J., Chen L., Jeppesen P.B., Nordentoft I., Hermansen K. Stevioside counteracts the alpha-cell hypersecretion caused by long-term palmitate exposure. Am. J. Physiol. Endocrinol. Metab. 2006, 290:E416-E422.
20. Irwin N., Frizelle P., Montgomery I.A., Moffett R.C., O'Harte F.P., Flatt P.R. Beneficial effects of the novel cholecystokinin agonist (pGlu-Gln)-CCK-8 in mouse models of obesity/diabetes. Diabetologia 2012, 55:2747-2758.
21. Kaltschmidt B., Kaltschmidt C., Hofmann T.G., Hehner S.P., Droge W., Schmitz M.L. The pro-or anti-apoptotic function of NF-kappaB is determined by the nature of the apoptotic stimulus. Eur. J. Biochem. 2000, 267:3828-3835.
22. Kempaiah P., Kisiel W. Human tissue factor pathway inhibitor-2 induces caspase-mediated apoptosis in a human fibrosarcoma cell line. Apoptosis 2008, 13:702-715.
23. Kooptiwut S., Kebede M., Zraika S., Visinoni S., Aston-Mourney K., Favaloro J., Tikellis C., Thomas M.C., Forbes J.M., Cooper ME Dunlop M., Proietto J., Andrikopoulos S. 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.
24. Laybutt D.R., Kaneto H., Hasenkamp W., Grey S., Jonas J.C., Sgroi D.C., Groff A., Ferran C., Bonner-Weir S., Sharma A., Sharma A., Weir G.C. Increased expression of antioxidant and antiapoptotic genes in islets that may contribute to beta-cell survival during chronic hyperglycemia. Diabetes 2002, 51:413-423.
25. Lees Murdock D.J., Barnett Y.A., Barnett C.R. DNA damage and cytotoxicity in pancreatic beta-cells expressing human CYP2E1. Biochem. Pharmacol. 2004, 68:523-530.
26. Lim S., Rashid M.A., Jang M., Kim Y., Won H., Lee J., Woo J.T., Kim Y.S., Murphy M.P., Ali L Ha J., Kim S.S. Mitochondria-targeted antioxidants protect pancreatic beta-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity. Cell. Physiol. Biochem. 2011, 28:873-886.
27. Maestre I., Jordan J., Calvo S., Reig J.A., Cena V., Soria B., Prentki M., Roche E. Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the beta-cell line INS-1. Endocrinology 2003, 144:335-345.
28. 3 on glucose homeostasis and DNA damage in type 2 diabetic mice. J. Diabetes Complicat. 2012, 26:363-368.
29. Meier J.J., Ueberberg S., Korbas S., Schneider S. Diminished glucagon suppression after beta-cell reduction is due to impaired alpha-cell function rather than an expansion of alpha-cell mass. Am. J. Physiol. Endocrinol. Metab. 2011, 300:E717-E723.
30. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
31. Nauck M.A., Heimesaat M.M., Orskov C., Holst J.J., 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. Investig. 1993, 91:301-307.
32. Nauck M.A., Baller B., Meier J.J. gastric inhibitory polypeptide and glucagon-like peptide-1 in the pathogenesis of type 2 diabetes. Diabetes 2004, 53:S190-S196.
33. Noor R., Astuti I., Mustofa Cytotoxicity of α -terpineol in HeLa cell line and its effects to apoptosis and cell cycle. J. Med. Sci. 2012, 46:1-9.
34. Piro S., Maniscalchi E.T., Monello A., Pandini G., Mascali L.G., Rabuazzo A.M., Purrello F. Palmitate affects insulin receptor phosphorylation and intracellular insulin signal in a pancreatic alpha-cell line. Endocrinology 2010, 151:4197-4206.
35. Potten C.S. The significance of spontaneous and induced apoptosis in the gastrointestinal tract of mice. Cancer Metastasis Rev. 1992, 11:179-195.
36. Raskin P. Islet-cell abnormalities in non-insulin-dependent diabetes mellitus. Am. J. Med. 1985, 79:2-5.
37. Reimann F., Gribble F.M. Glucose-sensing in glucagon-like peptide-1-secreting cells. Diabetes 2002, 51:2757-2763.
38. Reimann F., Williams L., da Silva Xavier G., Rutter G.A., Gribble F.M. Glutamine potently stimulates glucagon-like peptide-1 secretion from GLUTag cells. Diabetologia 2004, 47:1592-1601.
39. Robertson R.P. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J. Biol. Chem. 2004, 279:42351-42354.
40. Roth K.A., Hertz J.M., Gordon J.I. Mapping enteroendocrine cell populations in transgenic mice reveals an unexpected degree of complexity in cellular differentiation within the gastrointestinal tract. J. Cell Biol. 1990, 110:1791-1801.
41. Schonhoff S.E., Giel-Moloney M., Leiter A.B. Minireview: development and differentiation of gut endocrine cells. Endocrinology 2004, 145:2639-2644.
42. Shen X., Li H., Pan L., Hong J., Xiao J., Hermansen K., Jeppesen P.B., Li G. Glucotoxicity andα cell dysfunction: involvement of the PI3K/Akt pathway in glucose-induced insulin resistance in rat islets and clonal αtc1-6 cells. Endocr. Res. 2012, 37:12-24.
43. Shi X.L., Ren Y.Z., Wu J. Intermittent high glucose enhances apoptosis in INS-1 cells. Exp. Diabetes Res. 2011, 2011(2011):754673.
44. Sirota N.P., Zhanataev A.K., Kuznetsova E.A., Khizhnyak E.P., Anisina E.A., Durnev A.D. Some causes of inter-laboratory variation in the results of comet assay. Mutat. Res. 2014, 770:16-22.
45. Toft-Nielsen M.B., Damholt M.B., Madsbad S., Hilsted L.M., Hughes T.E., Michelsen B.K., Holst J.J. Determinants of the impaired secretion of glucagon-like peptide-1 in type 2 diabetic patients. J. Clin. Endocrinol. Metab. 2001, 86:3717-3723.
46. Vasu S., McClenaghan N.H., McCluskey J.T., Flatt P.R. Effects of lipotoxicity on a novel insulin-secreting Human pancreatic β-cell line 1.1B4. Biolo. Chem. 2013, 394:909-918.
47. Vasu S., McClenaghan N.H., McCluskey J.T., Flatt P.R. cellular responses of novel Human pancreatic β-cell line 1.1B4 to hyperglycemia. Islets 2013, 5:170-177.
48. Vasu S., McClenaghan N.H., McCluskey J.T., Flatt P.R. Mechanisms of toxicity by proinflammatory cytokines in a novel human pancreatic beta cell line, 1.1B4. Biochim. Biophys. Acta 2014, 1840:136-145.
49. Vasu S., Moffett C., McClenaghan N.H., Flatt P.R. Responses of GLP-1 secreting l-cells to cytotoxicity resemble pancreatic beta but not alpha cells. J. Mol. Endocrinol. 2015, 54(1):91-104. 10.1530/JME-14-0214.
50. Verdich C., Toubro S., Buermann B., Lysgard M.J., Juul H.J., Astrup A. the role of postprandial releases of insulin and incretin hormones in mean-induced satiety-effect of obesity and weight reduction. Int. J. Obes. Relat. Metab. Disord. 2001, 25:1206-1214.
51. Vilsboll T., Knop F.K., Krarup T., Johansen A., Madsbad S., Larsen S., Hansen T., Pedersen O., Holst J.J. The pathophysiology of diabetes involves a defective amplification of the late-phase insulin response to glucose by glucose-dependent insulinotropic polypeptide-regardless of etiology and phenotype. J. Clin. Endocrinol. Metab. 2003, 88:4897-4903.
52. Vilsboll T., Krarup T., Sonne J., Madsbad S., Volund A., Juul A.G., Holst J.J. Incretin secretion in relation to meal size and body weight in healthy subjects and people with type 1 and type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 2003, 88:2706-2713.
53. Vilsbøll T., Holst J.J. Incretins, insulin secretion and type 2 diabetes mellitus. Diabetologia 2004, 47:357-366.
54. 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, 12:7569-7580.
55. Yoon K.H., Ko S.H., Cho J.H., Lee J.M., Ahn Y.B., Song K.H., Yoo S.J., Kang M.I., Cha B.Y., Lee K.W., Son H.Y., Kang S.K., Kim H.S., Lee I.K., Bonner-Weir S. Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea. J. Clin. Endocrinol. Metab. 2003, 88:2300-2308.