RAGE binds preamyloid IAPP intermediates and mediates pancreatic β cell proteotoxicity

Journal of Clinical Investigation

Volumn 128, Issue 2, 2018, Pages 682-698

  Abedini, Andisheh ^a   Cao, Ping ^b   Plesner, Annette ^c   Zhang, Jinghua ^a   He, Meilun ^a   Derk, Julia ^a   Patil, Sachi A ^a   Rosario, Rosa ^a   Lonier, Jacqueline ^a   Song, Fei ^a   Koh, Hyunwook ^a   Li, Huilin ^a   Raleigh, Daniel P ^b   Schmidt, Ann Marie ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c NOVO NORDISK A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ADVANCED GLYCATION END PRODUCT RECEPTOR ANTAGONIST; AMYLIN; AMYLOID; BLOCKING ANTIBODY; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; INSULIN; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN S100B; SOLUBLE RECEPTOR FOR ADVANCED GLYCATION ENDPRODUCT; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; AGER PROTEIN, HUMAN; AGER PROTEIN, MOUSE; AGER PROTEIN, RAT; LIGAND;

AMYLOIDOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTIC SMOOTH MUSCLE CELL; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CORRELATIONAL STUDY; CYTOTOXICITY; EX VIVO STUDY; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GLUCOSE INTOLERANCE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; INS-1 832/13 CELL LINE; MALE; METABOLIC DISORDER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PANCREAS ISLET DISEASE; PANCREATITIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN MISFOLDING; PROTEOTOXICITY; RECEPTOR BINDING; RECEPTOR UPREGULATION; TOXICITY; ANIMAL; C57BL MOUSE; CELL LINE; CYTOLOGY; GENETICS; INFLAMMATION; INSULINOMA; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS; PANCREAS ISLET; PROTEIN FOLDING; RAT; SMOOTH MUSCLE CELL; TRANSGENIC MOUSE; UPREGULATION;

AMYLOID; AMYLOIDOSIS; ANIMALS; APOPTOSIS; CELL LINE; DIABETES MELLITUS, TYPE 2; HUMANS; INFLAMMATION; INSULIN-SECRETING CELLS; INSULINOMA; ISLET AMYLOID POLYPEPTIDE; ISLETS OF LANGERHANS; LIGANDS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCYTES, SMOOTH MUSCLE; PANCREAS; PROTEIN FOLDING; RATS; RECEPTOR FOR ADVANCED GLYCATION END PRODUCTS; UP-REGULATION;

EID: 85041467951     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85210     Document Type: Article

References (77)

1. Chiti F, Dobson CM. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem. 2006;75:333–366.
2. Cooper GJ, Willis AC, Clark A, Turner RC, Sim RB, Reid KB. Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc Natl Acad Sci U S A. 1987;84(23):8628–8632.
3. Eisenberg D, Jucker M. The amyloid state of proteins in human diseases. Cell. 2012;148(6):1188–1203.
4. 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.
5. Kahn SE, Andrikopoulos S, Verchere CB. Islet amyloid: a long-recognized but underappreciated pathological feature of type 2 diabetes. Diabetes. 1999;48(2):241–253.
6. Westermark P, Andersson A, Westermark GT. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. PhysiolRev. 2011;91(3):795–826.
7. Westermark P, Wernstedt C, Wilander E, Hayden DW, O’Brien TD, Johnson KH. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a Neuropeptide-like protein also present in normal islet cells. Proc NatlAcadSciUSA. 1987;84(11):3881–3885.
8. Clark A, et al. Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: quantitative changes in the pancreas in type 2 diabetes. Diabetes Res. 1988;9(4):151–159.
9. 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.
10. Jurgens CA, et al. β-cell loss and β-cell apoptosis in human type 2 diabetes are related to islet amyloid deposition. Am J Pathol. 2011;178(6):2632–2640.
11. Ashcroft FM, Rorsman P. Diabetes mellitus and the beta cell: the last ten years. Cell. 2012;148(6):1160–1171.
12. Halban PA, et al. β-cell failure in type 2 diabetes: postulated mechanisms and prospects for prevention and treatment. J Clin Endocrinol Metab. 2014;99(6):1983–1992.
13. Hieronymus L, Griffin S. Role of amylin in type 1 and type 2 diabetes. Diabetes Educ. 2015; 41(1 Suppl):47S–56S.
14. Li Z, Kelly L, Heiman M, Greengard P, Friedman JM. Hypothalamic amylin acts in concert with leptin to regulate food intake. CellMetab. 2015;22(6):1059–1067.
15. Kahn SE, et al. Evidence of cosecretion of islet amyloid polypeptide and insulin by beta-cells. Diabetes. 1990;39(5):634–638.
16. Lutz TA. Control of energy homeostasis by amylin. Cell Mol Life Sci. 2012;69(12):1947–1965.
17. Akter R, et al. Islet amyloid polypeptide: Structure, function, and pathophysiology. JDiabetes Res. 2016;2016:2798269.
18. Westermark P. Quantitative studies on amyloid in the islets of Langerhans. Ups J Med Sci. 1972;77(2):91–94.
19. Abedini A, et al. Time-resolved studies define the nature of toxic IAPP intermediates, providing insight for anti-amyloidosis therapeutics. Elife. 2016;5:e12977.
20. Potter KJ, et al. Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts. Proc Natl Acad Sci U S A. 2010;107(9):4305–4310.
21. Bram Y, et al. Apoptosis induced by islet amyloid polypeptide soluble oligomers is neutralized by diabetes-associated specific antibodies. SciRep. 2014;4:4267.
22. Despa S, et al. Hyperamylinemia contributes to cardiac dysfunction in obesity and diabetes: a study in humans and rats. Circ Res. 2012;110(4):598–608.
23. Westermark GT, Westermark P, Berne C, Kors-gren O. Widespread amyloid deposition in transplanted human pancreatic islets. N Engl J Med. 2008;359(9):977–979.
24. 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.
25. Kapurniotu A. Amyloidogenicity and cytotoxicity of islet amyloid polypeptide. Biopolymers. 2001;60(6):438–459.
26. Matveyenko AV, Butler PC. Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes. ILAR J. 2006;47(3):225–233.
27. Huang CJ, et al. 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. 2007;56(8):2016–2027.
28. Kim J, et al. Amyloidogenic peptide oligomer accumulation in autophagy-deficient beta cells induces diabetes. J Clin Invest. 2014;124(8):3311–3324.
29. Shigihara N, et al. Human IAPP-induced pancreatic beta cell toxicity and its regulation by autophagy. J Clin Invest. 2014;124(8):3634–3644.
30. Rivera JF, et al. Human- IAPP disrupts the autophagy/lysosomal pathway in pancreatic beta-cells: protective role of p62-positive cytoplasmic inclusions. CellDeathDiffer. 2011;18(3):415–426.
31. Hull RL, Zraika S, Udayasankar J, Aston-Mourney K, Subramanian SL, Kahn SE. Amyloid formation in human IAPP transgenic mouse islets and pancreas, and human pancreas, is not associated with endoplasmic reticulum stress. Diabetologia. 2009;52(6):1102–1111.
32. Aston-Mourney K, Hull RL, Zraika S, Udayasankar J, Subramanian SL, Kahn SE. Exendin-4 increases islet amyloid deposition but offsets the resultant beta cell toxicity in human islet amyloid polypeptide transgenic mouse islets. Diabetologia. 2011;54(7):1756–1765.
33. Park YJ, et al. Deletion of Fas protects islet beta cells from cytotoxic effects of human islet amyloid polypeptide. Diabetologia. 2012;55(4):1035–1047.
34. Zhang S, Liu J, Dragunow M, Cooper GJ. Fibril-logenic amylin evokes islet beta-cell apoptosis through linked activation of a caspase cascade and JNK1. JBiolChem. 2003;278(52):52810–52819.
35. Casas S, Gomis R, Gribble FM, Altirriba J, Knuutila S, Novials A. Impairment of the ubiquitin-proteasome pathway is a downstream endoplasmic reticulum stress response induced by extracellular human islet amyloid polypeptide and contributes to pancreatic beta-cell apoptosis. Diabetes. 2007;56(9):2284–2294.
36. Trikha S, Jeremic AM. Distinct internalization pathways of human amylin monomers and its cytotoxic oligomers in pancreatic cells. PLoS One. 2013;8(9):e73080.
37. Matveyenko AV, Butler PC. Beta-cell deficit due to increased apoptosis in the human islet amyloid polypeptide transgenic (HIP) rat recapitulates the metabolic defects present in type 2 diabetes. Diabetes. 2006;55(7):2106–2114.
38. Zraika S, et al. Oxidative stress is induced by islet amyloid formation and time-dependently mediates amyloid-induced beta cell apoptosis. Diabetologia. 2009;52(4):626–635.
39. Abedini A, Schmidt AM. Mechanisms of islet amyloidosis toxicity in type 2 diabetes. FEBSLett. 2013;587(8):1119–1127.
40. Masters SL, et al. Activation of the NLRP3 inflam-masome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol. 2010;11(10):897–904.
41. Park YJ, et al. The role of caspase-8 in amyloid-induced beta cell death in human and mouse islets. Diabetologia. 2014;57(4):765–775.
42. Westwell-Roper C, et al. IL-1 blockade attenuates islet amyloid polypeptide-induced proinflammatory cytokine release and pancreatic islet graft dysfunction. JImmunol. 2011;187(5):2755–2765.
43. Gurlo T, et al. CHOP contributes to, but is not the only mediator of, IAPP induced beta-cell apoptosis. MolEndocrinol. 2016;30(4):446–454.
44. Meier DT, Morcos M, Samarasekera T, Zraika S, Hull RL, Kahn SE. Islet amyloid formation is an important determinant for inducing islet inflammation in high-fat-fed human IAPP transgenic mice. Diabetologia. 2014;57(9):1884–1888.
45. Westwell-Roper CY, Ehses JA, Verchere CB. Resident macrophages mediate islet amyloid polypeptide-induced islet IL-1beta production and beta-cell dysfunction. Diabetes. 2014;63(5):1698–1711.
46. 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.
47. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier JL. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab. 2001;280(5):E685–E694.
48. Zhu Y, et al. Inhibition of the receptor for advanced glycation endproducts (RAGE) protects pancreatic beta-cells. Biochem Biophys Res Commun. 2011;404(1):159–165.
49. Costal F, et al. Dual effect of advanced glycation end products in pancreatic islet apoptosis. Diabetes Metab Res Rev. 2013;29(4):296–307.
50. Lee BW, Chae HY, Kwon SJ, Park SY, Ihm J, Ihm SH. RAGE ligands induce apoptotic cell death of pancreatic beta-cells via oxidative stress. Int J Mol Med. 2010;26(6):813–818.
51. Liu M, et al. Hyperamylinemia Increases IL-1beta Synthesis in the Heart via Peroxidative Sarcolem-mal Injury. Diabetes. 2016;65(9):2772–2783.
52. Toure F, et al. Formin mDia1 mediates vascular remodeling via integration of oxidative and signal transduction pathways. Circ Res. 2012;110(10):1279–1293.
53. Couce M, et al. Treatment with growth hormone and dexamethasone in mice transgenic for human islet amyloid polypeptide causes islet amyloidosis and beta-cell dysfunction. Diabetes. 1996;45(8):1094–1101.
54. Butler AE, Janson J, Soeller WC, Butler PC. Increased beta-cell apoptosis prevents adaptive increase in beta-cell mass in mouse model of type 2 diabetes: evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes. 2003;52(9):2304–2314.
55. Muff R, Buhlmann N, Fischer JA, Born W. An amylin receptor is revealed following co-trans-fection of a calcitonin receptor with receptor activity modifying proteins-1 or -3. Endocrinology. 1999;140(6):2924–2927.
56. Bucciantini M, et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature. 2002;416(6880):507–511.
57. Schmidt AM, Sahagan B, Nelson RB, Selmer J, Rothlein R, Bell JM. The role of RAGE in amyloid-beta peptide-mediated pathology in Alzheimer’s disease. Curr Opin Investig Drugs. 2009;10(7):672–680.
58. Sturchler E, Galichet A, Weibel M, Leclerc E, Heizmann CW. Site-specific blockade of RAGE-Vd prevents amyloid-beta oligomer neurotoxicity. J Neurosci. 2008;28(20):5149–5158.
59. Yan SD, et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer’s disease. Nature. 1996;382(6593):685–691.
60. Yan SD, et al. Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med. 2000;6(6):643–651.
61. Sasaki N, et al. Advanced glycation end products (AGE) and their receptor (RAGE) in the brain of patients with Creutzfeldt-Jakob disease with prion plaques. Neurosci Lett. 2002;326(2):117–120.
62. Cluck MW, Chan CY, Adrian TE. The regulation of amylin and insulin gene expression and secretion. Pancreas. 2005;30(1):1–14.
63. Young A. Historical background. Adv Pharmacol. 2005;52:1–18.
64. Gedulin BR, Rink TJ, Young AA. Dose-response for glucagonostatic effect of amylin in rats. Metabolism. 1997;46(1):67–70.
65. Wang F, Adrian TE, Westermark GT, Ding X, Gasslander T, Permert J. Islet amyloid polypeptide tonally inhibits beta-, alpha-, and delta-cell secretion in isolated rat pancreatic islets. Am J Physiol. 1999;276(1 Pt 1):E19–24.
66. Eriksson J, et al. Early metabolic defects in persons at increased risk for non-insulin-dependent diabetes mellitus. NEnglJMed. 1989;321(6):337–343.
67. Eriksson J, Nakazato M, Miyazato M, Shiomi K, Matsukura S, Groop L. Islet amyloid polypeptide plasma concentrations in individuals at increased risk of developing type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia. 1992;35(3):291–293.
68. Stridsberg M, Berne C, Sandler S, Wilander E, Oberg K. Inhibition of insulin secretion, but normal peripheral insulin sensitivity, in a patient with a malignant endocrine pancreatic tumour producing high amounts of an islet amyloid polypeptide-like molecule. Diabetologia. 1993;36(9):843–849.
69. Alonso LC, et al. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes. 2007;56(7):1792–1801.
70. Khadra A, Schnell S. Development, growth and maintenance of beta-cell mass: models are also part of the story. Mol Aspects Med. 2015;42:78–90.
71. Pancreatic Islets - Hyperplasia. National Toxicology Program. https://ntp.niehs.nih.gov/nnl/endocrine/pancreatic_islets/hyperpl/index.htm. Updated July 24, 2014. Accessed Novemeber 22, 2017.
72. Manesso E, et al. Dynamics of beta-cell turnover: evidence for beta-cell turnover and regeneration from sources of beta-cells other than beta-cell replication in the HIP rat. Am J Physiol Endocrinol Metab. 2009;297(2):E323–E330.
73. Teta M, Long SY, Wartschow LM, Rankin MM, Kushner JA. Very slow turnover of beta-cells in aged adult mice. Diabetes. 2005;54(9):2557–2567.
74. Hohmeier HE, Mulder H, Chen G, Henkel-Rieger R, Prentki M, Newgard CB. Isolation of INS-1derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes. 2000;49(3):424–430.
75. Park L, et al. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med. 1998;4(9):1025–1031.
76. Rampersad SN. Multiple applications of Alamar Blue as an indicator of metabolic function and cellular health in cell viability bioassays. Sensors (Basel). 2012;12(9):12347–12360.
77. Brett J, et al. Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol. 1993;143(6):1699–1712.