Degradation of islet amyloid polypeptide by neprilysin

Diabetologia

Volumn 55, Issue 11, 2012, Pages 2989-2998

  Guan, H ^a   Chow, K M ^a   Shah, R ^b   Rhodes, C J ^b   Hersh, L B ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b University of Chicago ^*  (United States)

Author keywords

Beta cell apoptosis; Cleavage; Human islet amyloid polypeptide; Islet amyloid; Neprilysin; Type 2 diabetes mellitus

Indexed keywords

ALANINE; AMYLIN; ARGININE; ASPARAGINE; ISOLEUCINE; LEUCINE; MEMBRANE METALLOENDOPEPTIDASE; PHENYLALANINE;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INHIBITION KINETICS; MASS SPECTROMETRY; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN INTERACTION; RAT;

AMINO ACID SEQUENCE; AMYLOID; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; DIABETES MELLITUS, TYPE 2; ENZYME ACTIVATION; GREEN FLUORESCENT PROTEINS; HUMANS; INSULIN-SECRETING CELLS; INSULINOMA; MOLECULAR SEQUENCE DATA; NEPRILYSIN; PANCREATIC NEOPLASMS; RATS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TRANSFECTION;

EID: 84867514335     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-012-2678-y     Document Type: Article

References (46)

1. Gotz J, Ittner LM, Lim YA (2009) Common features between diabetes mellitus and Alzheimer's disease. Cell Mol Life Sci 66:1321-1325
2. Haataja L, Gurlo T, Huang CJ, Butler PC (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr Rev 29:303-316
3. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297:353-356
4. Sanke T, Bell GI, Sample C, Rubenstein AH, Steiner DF (1988) An islet amyloid peptide is derived from an 89-amino acid precursor by proteolytic processing. J Biol Chem 263:17243-17246
5. Kahn SE, D'Alessio DA, Schwartz MW et al (1990) Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes 39:634-638
6. Moore CX, Cooper GJ (1991) Co-secretion of amylin and insulin from cultured islet beta-cells: Modulation by nutrient secretagogues, islet hormones and hypoglycemic agents. Biochem Biophys Res Commun 179:1-9
7. Butler PC, Chou J, Carter WB et al (1990) Effects of meal ingestion on plasma amylin concentration in NIDDMand nondiabetic humans. Diabetes 39:752-756
8. Westermark P, Engstrom U, Johnson KH,Westermark GT, Betsholtz C (1990) Islet amyloid polypeptide: Pinpointing amino acid residues linked to amyloid fibril formation. Proc Natl Acad Sci U S A 87:5036-5040
9. Scheuner D, Kaufman RJ (2008) The unfolded protein response: A pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 29:317-333
10. Bennett RG, Duckworth WC, Hamel FG (2000) Degradation of amylin by insulin-degrading enzyme. J Biol Chem 275:36621-36625
11. Bennett RG, Hamel FG, DuckworthWC(2003) An insulin-degrading enzyme inhibitor decreases amylin degradation, increases amylininduced cytotoxicity, and increases amyloid formation in insulinoma cell cultures. Diabetes 52:2315-2320
12. Zraika S, Aston-Mourney K, Marek P et al (2010) Neprilysin impedes islet amyloid formation by inhibition of fibril formation rather than peptide degradation. J Biol Chem 285:18177-18183
13. Zraika S, Hull RL, Udayasankar J et al (2007) Identification of the amyloid-degrading enzyme neprilysin in mouse islets and potential role in islet amyloidogenesis. Diabetes 56:304-310
14. Hersh LB, Rodgers DW (2008) Neprilysin and amyloid beta peptide degradation. Curr Alzheimer Res 5:225-231
15. Marzban L, Trigo-Gonzalez G, Zhu X et al (2004) Role of beta-cell prohormone convertase (PC)1/3 in processing of pro-islet amyloid polypeptide. Diabetes 53:141-148
16. Michael DJ, Geng X, Cawley NX et al (2004) Fluorescent cargo proteins in pancreatic beta-cells: Design determines secretion kinetics at exocytosis. Biophys J 87:L03-L05
17. Guan H, Liu Y, Daily A et al (2009) Peripherally expressed neprilysin reduces brain amyloid burden: A novel approach for treating Alzheimer's disease. J Neurosci Res 87:1462-1473
18. Leahy DJ, Dann CE 3rd, Longo P, Perman B, Ramyar KX (2000) A mammalian expression vector for expression and purification of secreted proteins for structural studies. Protein Expr Purif 20:500-506
19. Aricescu AR, Lu W, Jones EY (2006) A time-and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr D Biol Crystallogr 62:1243-1250
20. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with imagej. Biophotonics Int 11:36-42
21. Daily A, Nath A, Hersh LB (2006) Tat peptides inhibit neprilysin. J Neurovirol 12:153-160
22. Folk JE, Schirmer EW (1963) The porcine pancreatic carboxypeptidase a system. I. Three forms of the active enzyme. J Biol Chem 238:3884-3894
23. Meng F, Marek P, Potter KJ, Verchere CB, Raleigh DP (2008) Rifampicin does not prevent amyloid fibril formation by human islet amyloid polypeptide but does inhibit fibril thioflavin-T interactions: Implications for mechanistic studies of beta-cell death. Biochemistry 47:6016-6024
24. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB (2000) Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and-independent glucose-stimulated insulin secretion. Diabetes 49:424-430
25. Liu Y, Peterson DA, Kimura H, Schubert D (1997) Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 69:581-593
26. Huang CJ, Lin CY, Haataja L et al (2007) High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated beta-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 56:2016-2027
27. Law E, Lu S, Kieffer TJ et al (2010) Differences between amyloid toxicity in alpha and beta cells in human and mouse islets and the role of caspase-3. Diabetologia 53:1415-1427
28. Chow KM, Gakh O, Payne IC et al (2009) Mammalian pitrilysin: Substrate specificity and mitochondrial targeting. Biochemistry 48:2868-2877
29. Devault A, Nault C, Zollinger M et al (1988) Expression of neutral endopeptidase (enkephalinase) in heterologous COS-1 cells. Characterization of the recombinant enzyme and evidence for a glutamic acid residue at the active site. J Biol Chem 263:4033-4040
30. Li C, Hersh LB (1995) Neprilysin: Assay methods, purification, and characterization. Methods Enzymol 248:253-263
31. Howell S, Nalbantoglu J, Crine P (1995) Neutral endopeptidase can hydrolyze beta-amyloid(1-40) but shows no effect on betaamyloid precursor protein metabolism. Peptides 16:647-652
32. Iwata N, Tsubuki S, Takaki Y et al (2001) Metabolic regulation of brain Abeta by neprilysin. Science 292:1550-1552
33. Johnson KH, O'Brien TD, Betsholtz C, Westermark P (1989) Islet amyloid, islet-amyloid polypeptide, and diabetes mellitus. N Engl J Med 321:513-518
34. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52:102-110
35. Zhao HL, Lai FM, Tong PC et al (2003) Prevalence and clinicopathological characteristics of islet amyloid in chinese patients with type 2 diabetes. Diabetes 52:2759-2766
36. Clark A, Wells CA, Buley ID et al (1988) Islet amyloid, increased A-cells, reduced B cells and exocrine fibrosis: Quantitative changes in the pancreas in type 2 diabetes. Diabetes Res 9:151-159
37. Jurgens CA, Toukatly MN, Fligner CL et al (2011) Beta-cell loss and beta-cell apoptosis in human type 2 diabetes are related to islet amyloid deposition. Am J Pathol 178:2632-2640
38. Schneider HM, Storkel S, Will W (1980) Amyloid of islets of Langerhans and its relation to diabetes mellitus (author's transl). Dtsch Med Wochenschr 105:1143-1147 [article in German]
39. Janson J, Ashley RH, Harrison D, McIntyre S, Butler PC (1999) The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48:491-498
40. Lin CY, Gurlo T, Kayed R et al (2007) Toxic human islet amyloid polypeptide (h-IAPP) oligomers are intracellular, and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPPinduced beta-cell apoptosis in h-IAPP transgenic mice. Diabetes 56:1324-1332
41. Gurlo T, Ryazantsev S, Huang CJ et al (2010) Evidence for proteotoxicity in beta cells in type 2 diabetes: Toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway. Am J Pathol 176:861-869
42. Konarkowska B, Aitken JF, Kistler J, Zhang S, Cooper GJ (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells. Febs J 273:3614-3624
43. Meier JJ, Kayed R, Lin CY et al (2006) Inhibition of human IAPP fibril formation does not prevent beta-cell death: Evidence for distinct actions of oligomers and fibrils of human IAPP. Am J Physiol Endocrinol Metab 291:E1317-E1324
44. Westermark P, Andersson A, Westermark GT (2011) Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol Rev 91:795-826
45. Trikha S, Jeremic AM (2011) Clustering and internalization of toxic amylin oligomers in pancreatic cells require plasma membrane cholesterol. J Biol Chem 286:36086-36097
46. Aston-Mourney K, Hull RL, Zraika S, Udayasankar J, Subramanian SL,Kahn SE (2011) Exendin-4 increases islet amyloid deposition but offsets the resultant beta cell toxicity in human islet amyloid polypeptide transgenic mouse islets. Diabetologia 54:1756-1765