Human IAPP-induced Pancreatic β cell toxicity and its regulation by autophagy

Journal of Clinical Investigation

Volumn 124, Issue 8, 2014, Pages 3634-3644

  Shigihara, Nayumi ^a   Fukunaka, Ayako ^a   Hara, Akemi ^a   Komiya, Koji ^a   Honda, Akira ^a   Uchida, Toyoyoshi ^a   Abe, Hiroko ^a   Toyofuku, Yukiko ^a   Tamaki, Motoyuki ^a   Ogihara, Takeshi ^a   Miyatsuka, Takeshi ^a   Hiddinga, Henry J ^b   Sakagashira, Setsuya ^b   Koike, Masato ^a   Uchiyama, Yasuo ^a   Yoshimori, Tamotsu ^a,c   Eberhardt, Norman L ^b   Fujitani, Yoshio ^a   Watada, Hirotaka ^a  

^a JUNTENDO UNIVERSITY   (Japan)

^b MAYO CLINIC   (United States)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; INSULIN; MICRORNA; OLIGOMER; PROTEIN P62; ATG7 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BODY WEIGHT; CELL CYCLE; CELL DIVISION; CELL INCLUSION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DETERIORATION; GENE TARGETING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMPAIRED GLUCOSE TOLERANCE; INS 1 CELL LINE; INSULIN RELEASE; LIPID DIET; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; CELL LINE; CELL SURVIVAL; DEFICIENCY; DIABETES MELLITUS, TYPE 2; GENETICS; INSULIN RESISTANCE; KNOCKOUT MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXICITY; TRANSGENIC MOUSE;

ANIMALS; AUTOPHAGY; CELL CYCLE; CELL LINE; CELL SURVIVAL; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; RECOMBINANT PROTEINS;

EID: 84905460021     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI69866     Document Type: Article

References (63)

1. Kahn SE. The relative contributions of insulin resistance and β-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia. 2003;46(1):3-19.
2. Brunzell JD, et al. Relationships between fasting plasma glucose levels and insulin secretion during intravenous glucose tolerance tests. J Clin Endocrinol Metab. 1976;42(2):222-229.
3. Jensen CC, Cnop M, Hull RL, Fujimoto WY, Kahn SE, American Diabetes Association GSG. β-Cell function is a major contributor to oral glucose tolerance in high-risk relatives of four ethnic groups in the US. Diabetes. 2002;51(7):2170-2178.
4. Kloppel G, Lohr M, Habich K, Oberholzer M, Heitz PU. Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv Synth Pathol Res. 1985;4(2):110-125.
5. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52(1):102-110.
6. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic β-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab. 2008;10(suppl 4):32-42.
7. Hull RL, Westermark GT, Westermark P, Kahn SE. Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes. J Clin Endocrinol Metab. 2004;89(8):3629-3643.
8. O'Brien TD, Butler PC, Westermark P, Johnson KH. Islet amyloid polypeptide: a review of its biology and potential roles in the pathogenesis of diabetes mellitus. Vet Pathol. 1993;30(4):317-332.
9. Costes S, Langen R, Gurlo T, Matveyenko AV, Butler PC. β-Cell failure in type 2 diabetes: a case of asking too much of too few? Diabetes. 2013;62(2):327-335.
10. Hartter E, et al. Basal and stimulated plasma levels of pancreatic amylin indicate its cosecretion with insulin in humans. Diabetologia. 1991;34(1):52-54.
11. Westermark P, Engstrom U, Johnson KH, Westermark GT, Betsholtz C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc Natl Acad Sci U S A. 1990;87(13):5036-5040.
12. Betsholtz C, et al. Sequence divergence in a specific region of islet amyloid polypeptide (IAPP) explains differences in islet amyloid formation between species. FEBS Lett. 1989;251(1-2):261-264.
13. Matveyenko AV, Butler PC. Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes. ILAR J. 2006;47(3):225-233.
14. Butler AE, Jang J, Gurlo T, Carty MD, Soeller WC, Butler PC. Diabetes due to a progressive defect in β-cell mass in rats transgenic for human islet amyloid polypeptide (HIP Rat): a new model for type 2 diabetes. Diabetes. 2004;53(HIP Rat):1509-1516.
15. Janson J, et al. Spontaneous diabetes mellitus in transgenic mice expressing human islet amyloid polypeptide. Proc Natl Acad Sci U S A. 1996;93(14):7283-7288.
16. Verchere CB, et al. Islet amyloid formation associated with hyperglycemia in transgenic mice with pancreatic β cell expression of human islet amyloid polypeptide. Proc Natl Acad Sci U S A. 1996;93(8):3492-3496.
17. Hiddinga HJ, et al. Expression of wild-type and mutant S20G hIAPP in physiologic knock-in mouse models fails to induce islet amyloid formation, but induces mild glucose intolerance. J Diabetes Investig. 2012;3(2):138-147.
18. O'Brien TD, Butler PC, Kreutter DK, Kane LA, Eberhardt NL. Human islet amyloid polypeptide expression in COS-1 cells. A model of intracellular amyloidogenesis. Am J Pathol. 1995;147(3):609-616.
19. D'Alessio DA, et al. Pancreatic expression and secretion of human islet amyloid polypeptide in a transgenic mouse. Diabetes. 1994;43(12):1457-1461.
20. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147(4):728-741.
21. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular selfdigestion. Nature. 2008;451(7182):1069-1075.
22. Williams A, et al. Aggregate-prone proteins are cleared from the cytosol by autophagy: therapeutic implications. Curr Top Dev Biol. 2006;76:89-101.
23. Yu WH, et al. Macroautophagy - a novel β-amyloid peptide-generating pathway activated in Alzheimer's disease. J Cell Biol. 2005;171(1):87-98.
24. Boland B, et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci. 2008;28(27):6926-6937.
25. Ventruti A, Cuervo AM. Autophagy and neurodegeneration. Curr Neurol Neurosci Rep. 2007;7(5):443-451.
26. Ebato C, et al. Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet. Cell Metab. 2008;8(4):325-332.
27. Jung HS, et al. Loss of autophagy diminishes pancreatic β cell mass and function with resultant hyperglycemia. Cell Metab. 2008;8(4):318-324.
28. Huang CJ, et al. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated β-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes. 2007;56(8):2016-2027.
29. Lorenzo A, Razzaboni B, Weir GC, Yankner BA. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature. 1994;368(6473):756-760.
30. Sakagashira S, et al. S20G mutant amylin exhibits increased in vitro amyloidogenicity and increased intracellular cytotoxicity compared to wild-type amylin. Am J Pathol. 2000;157(6):2101-2109.
31. Morita S, et al. Autophagy protects against human islet amyloid polypeptide-associated apoptosis. J Diabetes Investig. 2011;2(1):48-55.
32. Komatsu M, Kageyama S, Ichimura Y. p62/SQSTM1/A170: physiology and pathology. Pharmacol Res. 2012;66(6):457-462.
33. Komatsu M, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131(6):1149-1163.
34. Bjorkoy G, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005;171(4):603-614.
35. Abe H, et al. Exendin-4 improves β-cell function in autophagy-deficient β-cells. Endocrinology. 2013;154(12):4512-4524.
36. Su H, et al. Gamma-protocadherins regulate the functional integrity of hypothalamic feeding circuitry in mice. Dev Biol. 2010;339(1):38-50.
37. Quan W, et al. Role of hypothalamic proopihumanxs omelanocortin neuron autophagy in the control of appetite and leptin response. Endocrinology. 2012;153(4):1817-1826.
38. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H. Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol. 1984;133(4):1710-1715.
39. Komatsu M, et al. Impairment of starvationinduced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005;169(3):425-434.
40. Meier JJ, et al. Inhibition of human IAPP fibril formation does not prevent β-cell death: evidence for distinct actions of oligomers and fibrils of human IAPP. Am J Physiol Endocrinol Metab. 2006;291(6):E1317-E1324.
41. Glabe CG. Structural classification of toxic amyloid oligomers. J Biol Chem. 2008;283(44):29639-29643.
42. Kayed R, et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science. 2003;300(5618):486-489.
43. Hiddinga HJ, Eberhardt NL. Intracellular amyloidogenesis by human islet amyloid polypeptide induces apoptosis in COS-1 cells. Am J Pathol. 1999;154(4):1077-1088.
44. Paulsson JF, Andersson A, Westermark P, Westermark GT. Intracellular amyloid-like deposits contain unprocessed pro-islet amyloid polypeptide (proIAPP) in β cells of transgenic mice overexpressing the gene for human IAPP and transplanted human islets. Diabetologia. 2006;49(6):1237-1246.
45. Gurlo T, et al. Evidence for proteotoxicity in β cells in type 2 diabetes: toxic islet amyloid polypeptide oligomers form intracellularly in the secretory pathway. Am J Pathol. 2010;176(2):861-869.
46. Ahren B, Oosterwijk C, Lips CJ, Hoppener JW. Transgenic overexpression of human islet amyloid polypeptide inhibits insulin secretion and glucose elimination after gastric glucose gavage in mice. Diabetologia. 1998;41(11):1374-1380.
47. Janson J, Ashley RH, Harrison D, McIntyre S, Butler PC. The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes. 1999;48(3):491-498.
48. Wicksteed B, et al. Conditional gene targeting in mouse pancreatic ss-Cells: analysis of ectopic Cre transgene expression in the brain. Diabetes. 2010;59(12):3090-3098.
49. Schmitz O, Brock B, Rungby J. Amylin agonists: a novel approach in the treatment of diabetes. Diabetes. 2004;53(suppl 3):S233-S238.
50. Rivera JF, et al. Human-IAPP disrupts the autophagy/lysosomal pathway in pancreatic β-cells: protective role of p62-positive cytoplasmic inclusions. Cell Death Differ. 2011;18(3):415-426.
51. Haataja L, Gurlo T, Huang CJ, Butler PC. Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr Rev. 2008;29(3):303-316.
52. Zraika S, et al. Toxic oligomers and islet β cell death: guilty by association or convicted by circumstantial evidence? Diabetologia. 2010;53(6):1046-1056.
53. Laganowsky A, et al. Atomic view of a toxic amyloid small oligomer. Science. 2012;335(6073):1228-1231.
54. Heldt CL, Kurouski D, Sorci M, Grafeld E, Lednev IK, Belfort G. Isolating toxic insulin amyloid reactive species that lack β-sheets and have wide pH stability. Biophys J. 2011;100(11):2792-2800.
55. Steneberg P, et al. The type 2 diabetes-associated gene ide is required for insulin secretion and suppression of α-synuclein levels in β-cells. Diabetes. 2013;62(6):2004-2014.
56. Kawarabayashi T, et al. Accumulation of β-amyloid fibrils in pancreas of transgenic mice. Neurobiol Aging. 1996;17(2):215-222.
57. Miklossy J, et al. β amyloid and hyperphosphorylated tau deposits in the pancreas in type 2 diabetes. Neurobiol Aging. 2010;31(9):1503-1515.
58. Bjorkoy G, Lamark T, Johansen T. p62/SQSTM1: a missing link between protein aggregates and the autophagy machinery. Autophagy. 2006;2(2):138-139.
59. Itakura E, Mizushima N. p62 Targeting to the autophagosome formation site requires selfoligomerization but not LC3 binding. J Cell Biol. 2011;192(1):17-27.
60. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A. 1998;95(5):2509-2514.
61. Nakayama M, et al. Multiple pathways of TWEAK-induced cell death. J Immunol. 2002;168(2):734-743.
62. Tamaki M, et al. The diabetes-susceptible gene SLC30A8/ZnT8 regulates hepatic insulin clearance. J Clin Invest. 2013;123(10):4513-4524.
63. Fukunaka A, et al. Tissue nonspecific alkaline phosphatase is activated via a two-step mechanism by zinc transport complexes in the early secretory pathway. J Biol Chem. 2011;286(18):16363-16373.