Carboxypeptidase E mediates palmitate-induced β-cell ER stress and apoptosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 24, 2008, Pages 8452-8457

  Jeffrey, Kristin D ^a   Alejandro, Emilyn U ^a   Luciani, Dan S ^a   Kalynyak, Tatyana B ^a   Hu, Xiaoke ^a   Li, Hong ^a   Lin, Yalin ^a   Townsend, R Reid ^b   Polonsky, Kenneth S ^b   Johnson, James D ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

2D difference gel electrophoresis proteomics; Free fatty acids; Hyperproinsulinemia; Mechanisms of cell lipotoxicity; Type 2 diabetes

Indexed keywords

CARBOXYPEPTIDASE H; FATTY ACID; INSULIN; PALMITIC ACID; PROINSULIN; SHORT HAIRPIN RNA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS; CARBOXYPEPTIDASE H; CELL SURVIVAL; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; HUMANS; HYPERGLYCEMIA; HYPERINSULINISM; INSULIN-SECRETING CELLS; MICE; MICE, MUTANT STRAINS; PALMITATES; PROTEOME;

EID: 46149098906     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0711232105     Document Type: Article

References (58)

1. Unger RH (1995) Lipotoxicity in the pathogenesis of obesity-dependent NIDDM. Genetic and clinical implications. Diabetes 44:863-870.
2. Paolisso G, et al. (1995) A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 38:1213-1217.
3. Bollheimer LC, Skelly RH, Chester MW, McGarry JD, Rhodes CJ (1998) Chronic exposure to free fatty acid reduces pancreatic beta cell insulin content by increasing basal insulin secretion that is not compensated for by a corresponding increase in proinsulin biosynthesis translation. J Clin Invest 101:1094-1101.
4. Furukawa H, Carroll RJ, Swift HH, Steiner DF (1999) Long-term elevation of free fatty acids leads to delayed processing of proinsulin and prohormone convertases 2 and 3 in the pancreatic beta-cell line MIN6. Diabetes 48:1395-1401.
5. Paolisso G, et al. (1995) Opposite effects of short- and long-term fatty acid infusion on insulin secretion in healthy subjects. Diabetologia 38:1295-1299.
6. Biden TJ, Robinson D, Cordery D, Hughes WE, Busch AK (2004) Chronic effects of fatty acids on pancreatic beta-cell function: New insights from functional genomics. Diabetes 53 Suppl 1:S159-S165.
7. Maedler K, et al. (2001) Distinct effects of saturated and monounsaturated fatty acids on beta-cell turnover and function. Diabetes 50:69-76.
8. Lupi R, et al. (2002) Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: Evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 51:1437-1442.
9. Zhou YP, Grill V (1995) Long term exposure to fatty acids and ketones inhibits B-cell functions in human pancreatic islets of Langerhans. J Clin Endocrinol Metab 80:1584-1590.
10. Unger RH, Zhou YT (2001) Lipotoxicity of beta-cells in obesity and in other causes of fatty acid spillover. Diabetes 50 Suppl 1:S118-S121.
11. Kharroubi I, et al. (2004) Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress. Endocrinology 145:5087-5096.
12. Eitel K, et al. (2002) Different role of saturated and unsaturated fatty acids in beta-cell apoptosis. Biochem Biophys Res Commun 299:853-856.
13. Shimabukuro M, Zhou YT, Levi M, Unger RH (1998) Fatty acid-induced beta cell apoptosis: A link between obesity and diabetes. Proc Natl Acad Sci USA 95:2498-2502.
14. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY (2003) Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 52:726-733.
15. Listenberger LL, et al. (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 100:3077-3082.
16. Cnop M, Hannaert JC, Hoorens A, Eizirik DL, Pipeleers DG (2001) Inverse relationship between cytotoxicity of free fatty acids in pancreatic islet cells and cellular triglyceride accumulation. Diabetes 50:1771-1777.
17. 2+- signaling in pancreatic beta-cells. Mol Cell Endocrinol 212:1-9.
18. Maestre I, et al. (2003) Mitochondrial dysfunction is involved in apoptosis induced by serum withdrawal and fatty acids in the beta-cell line INS-1. Endocrinology 144:335-345.
19. Carlsson C, Borg LA, Welsh N (1999) Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140:3422-3428.
20. Zhou YP, Grill VE (1995) Palmitate-induced beta-cell insensitivity to glucose is coupled to decreased pyruvate dehydrogenase activity and enhanced kinase activity in rat pancreatic islets. Diabetes 44:394-399.
21. Zhou YP, Berggren PO, Grill V (1996) A fatty acid-induced decrease in pyruvate dehydrogenase activity is an important determinant of beta-cell dysfunction in the obese diabetic db/db mouse. Diabetes 45:580-586.
22. Assimacopoulos-Jeannet F, et al. (1997) Fatty acids rapidly induce the carnitine palmitoyltransferase I gene in the pancreatic beta-cell line INS-1. J Biol Chem 272:1659-1664.
23. Joseph JW, et al. (2004) Free fatty acid-induced beta-cell defects are dependent on uncoupling protein 2 expression. J Biol Chem 279:51049-51056.
24. Yoshikawa H, et al. (2001) Effects of free fatty acids on beta-cell functions: A possible involvement of peroxisome proliferator-activated receptors alpha or pancreatic/duodenal homeobox. Metabolism 50:613-618.
25. Johnson JD, et al. (2003) Increased islet apoptosis in Pdx1+/- mice. J Clin Invest 111:1147-1160.
26. Ozcan U, et al. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306:457-461.
27. Karaskov E, et al. (2006) Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 147:3398-3407.
28. Naggert JK, et al. (1995) Hyperproinsulinaemia in obese fat/fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat Genet 10:135-142.
29. Johnson JD, et al. (2004) RyR2 and calpain-10 delineate a novel apoptosis pathway in pancreatic islets. J Biol Chem 279:24794-24802.
30. Kleinfeld AM, et al. (1996) Increases in serum unbound free fatty acid levels following coronary angioplasty. Am J Cardiol 78:1350-1354.
31. Cistola DP, Small DM (1991) Fatty acid distribution in systems modeling the normal and diabetic human circulation. A 13C nuclear magnetic resonance study. J Clin Invest 87:1431-1441.
32. Fricker LD, Snyder SH (1982) Enkephalin convertase: purification and characterization of a specific enkephalin-synthesizing carboxypeptidase localized to adrenal chromaffin granules. Proc Natl Acad Sci USA 79:3886-3890.
33. Guest PC, Ravazzola M, Davidson HW, Orci L, Hutton JC (1991) Molecular heterogeneity and cellular localization of carboxypeptidase H in the islets of Langerhans. Endocrinology 129:734-740.
34. Larsson-Nyren G, Sehlin J (1993) Interaction between perchlorate and nifedipine on insulin secretion from mouse pancreatic islets. Biosci Rep 13:107-117.
35. Kahn SE, et al. (1996) Proinsulin levels predict the development of non-insulin-dependent diabetes mellitus (NIDDM) in Japanese-American men. Diabet Med 13:S63-S66.
36. Nijpels G, Popp-Snijders C, Kostense PJ, Bouter LM, Heine RJ (1996) Fasting proinsulin and 2-h post-load glucose levels predict the conversion to NIDDM in subjects with impaired glucose tolerance: The Hoorn Study. Diabetologia 39:113-118.
37. Støy J, et al. (2007) Insulin gene mutations as a cause of permanent neonatal diabetes. Proc Natl Acad Sci USA 104:15040-15044.
38. Harding HP, Ron D (2002) Endoplasmic reticulum stress and the development of diabetes: A review. Diabetes 51 Suppl 3:S455-S461.
39. Fricker LD, Berman YL, Leiter EH, Devi LA (1996) Carboxypeptidase E activity is deficient in mice with the fat mutation. Effect on peptide processing. J Biol Chem 271:30619-30624.
40. Chen H, et al. (2001) Missense polymorphism in the human carboxypeptidase E gene alters enzymatic activity. Hum Mutat 18:120-131.
41. Wang H, Kouri G, Wollheim CB (2005) ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity. J Cell Sci 118:3905-3915.
42. Oyadomari S, Araki E, Mori M (2002) Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7:335-345.
43. Wei Y, Wang D, Topczewski F, Pagliassotti MJ (2006) Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol 291:E275-E281.
44. Ramos-Castaneda J, et al. (2005) Deficiency of ATP2C1, a Golgi ion pump, induces secretory pathway defects in endoplasmic reticulum (ER)-associated degradation and sensitivity to ER stress. J Biol Chem 280:9467-9473.
45. Oyadomari S, et al. (2006) Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell 126:727-739.
46. Roche E, et al. (1999) Palmitate and oleate induce the immediate-early response genes c-fos and nur-77 in the pancreatic beta-cell line INS-1. Diabetes 48:2007-2014.
47. Hardy S, et al. (2003) Saturated fatty acid-induced apoptosis in MDA-MB-231 breast cancer cells. A role for cardiolipin. J Biol Chem 278:31861-31870.
48. Itoh Y, et al. (2003) Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422:173-176.
49. Steneberg P, Rubins N, Bartoov-Shifman R, Walker MD, Edlund H (2005) The FFA receptor GPR40 links hyperinsulinemia, hepatic steatosis, and impaired glucose homeostasis in mouse. Cell Metab 1:245-258.
50. Treinies I, Shrake C, Koester A (2006) GPR40 knock-out mice do not develop obesity-induced glucose intolerance. Diabetologia 49:87-88.
51. 2+ currents and the size of the readily releasable granule pool in mouse pancreatic beta-cells. J Physiol 557:935-948.
52. Warnotte C, Gilon P, Nenquin M, Henquin JC (1994) Mechanisms of the stimulation of insulin release by saturated fatty acids. A study of palmitate effects in mouse beta-cells. Diabetes 43:703-711.
53. 2+ on enzyme activity and stability. J Biol Chem 269:11192-11195.
54. Song L, Fricker LD (1996) Tissue distribution and characterization of soluble and membrane-bound forms of metallocarboxypeptidase D. J Biol Chem 271:28884-28889.
55. Berman Y, Mzhavia N, Polonskaia A, Devi LA (2001) Impaired prohormone convertases in Cpe(fat)/Cpe(fat) mice. J Biol Chem 276:1466-1473.
56. Day R, et al. (1998) Prodynorphin processing by proprotein convertase 2. Cleavage at single basic residues and enhanced processing in the presence of carboxypeptidase activity. J Biol Chem 273:829-836.
57. Steiner DF, et al. (1971) Isolation and characterization of proinsulin C-peptide from bovine pancreas. J Biol Chem 246:1365-1374.
58. Johnson JD, Misler S (2002) Nicotinic acid-adenine dinucleotide phosphate-sensitive calcium stores initiate insulin signaling in human β-cells. Proc Natl Acad Sci USA 99:14566-14571.