Apoptosis induced by islet amyloid polypeptide soluble oligomers is neutralized by diabetes-associated specific antibodies

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Bram, Yaron ^a   Frydman Marom, Anat ^a   Yanai, Inbal ^a   Gilead, Sharon ^a   Shaltiel Karyo, Ronit ^a   Amdursky, Nadav ^a   Gazit, Ehud ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLIN; ANTIBODY; AUTOANTIBODY; NEUTRALIZING ANTIBODY;

APOPTOSIS; CELL MEMBRANE PERMEABILITY; CHEMISTRY; DRUG EFFECTS; HUMAN; IMMUNOLOGY; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY;

ANTIBODIES; ANTIBODIES, NEUTRALIZING; APOPTOSIS; AUTOANTIBODIES; CELL MEMBRANE PERMEABILITY; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN-SECRETING CELLS; ISLET AMYLOID POLYPEPTIDE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY;

EID: 84897795266     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep04267     Document Type: Article

References (56)

1. Eisenberg, D. & Jucker, M. The amyloid state of proteins in human diseases. Cell 148, 1188-1203 (2012).
2. Haass, C. The molecular significance of amyloid beta-peptide for Alzheimer's disease. Eur. Arch. Psychiatry Clin. Neurosci. 246, 118-123 (1996). (Pubitemid 26130269)
3. Conway, K. A.,Harper, J. D.&Lansbury, P. T. Accelerated in vitro fibril formation by amutant alpha-synuclein linked to early-onset Parkinson disease. Nat.Med. 4, 1318-1320 (1998). (Pubitemid 28512115)
4. Chuang, L. M. et al. Role of S20G mutation of amylin gene in insulin secretion, insulin sensitivity, and type 2 diabetes mellitus in Taiwanese patients. Diabetologia. 41, 1250-1251 (1998).
5. Terry, R. D. et al. Physical basis of cognitive alterations in alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Annals of Neurology. 30, 572-580 (1991).
6. Dickson, D. W. et al. Identification of normal and pathological aging in prospectively studied nondemented elderly humans. Neurobiol. Aging. 13, 179-189 (1992).
7. Snowdon, D. A. Aging and Alzheimer's disease: lessons from the Nun Study. Gerontologist 37, 150-156 (1997). (Pubitemid 27181271)
8. Bucciantini, M. et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507-511 (2002). (Pubitemid 34288846)
9. Lambert, M. P. et al. Diffusible, nonfibrillar ligands derived from Ab1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95, 6448-6453 (1998).
10. Dahlgren, K. N. et al. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 277, 32046-32053 (2002). (Pubitemid 34969015)
11. Walsh, D. M. et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (2002). (Pubitemid 34288854)
12. Quist, A. et al. Amyloid ion channels: a common structural link for proteinmisfolding disease. Proc. Natl. Acad. Sci. U. S. A. 102, 10427-10432 (2005). (Pubitemid 41061570)
13. Bucciantini, M. et al. Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J. Biol. Chem. 279, 31374-31382 (2004). (Pubitemid 39037804)
14. Sciacca, M. F. et al. Two-step mechanism of membrane disruption by Ab through membrane fragmentation and pore formation. Biophys. J. 103, 702-710 (2012).
15. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003). (Pubitemid 36444329)
16. Opie, E. L. On the relation of chronic interstitial pancreatitis to the islands of Langerhans and to diabetes melutus. J. Exp. Med. 5, 397-428 (1901).
17. SE, W. A. Zur Kenntnis der feineren Veränderungen des Pankreas bei Diabetes mellitus. Wien. Klin. Wochenshr. 14, 968-972 (1901).
18. Bell, E. T. Hyalinization of the islets of Langerhans in nondiabetic individuals. Am. J. Pathol. 35, 801-805 (1959).
19. Westermark, P. Mast cells in the islets of Langerhans in insular amyloidosis. Virchows Arch. A Pathol. Pathol. Anat. 354, 17-23 (1971).
20. Westermark, P., Wernstedt, C., Wilander, E. & Sletten, K. A novel peptide in the calcitonin gene related peptide family as an amyloid fibril protein in the endocrine pancreas. Biochem. Biophys. Res. Commun. 140, 827-831 (1986). (Pubitemid 17207764)
21. Westermark, P. et al. 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. Natl. Acad. Sci. U. S. A. 84, 3881-3885 (1987). (Pubitemid 17088383)
22. Westermark, P., Wernstedt, C., O'Brien, T. D., Hayden, D. W. & Johnson, K. H. Islet amyloid in type 2 human diabetes mellitus and adult diabetic cats contains a novel putative polypeptide hormone. Am. J. Pathol. 127, 414-417 (1987). (Pubitemid 17089802)
23. Cooper, G. J. et al. Amylin found in amyloid deposits in human type 2 diabetes mellitus may be a hormone that regulates glycogen metabolism in skeletalmuscle. Proc. Natl. Acad. Sci. U. S. A. 85, 7763-7766 (1988).
24. Westermark, P. & Grimelius, L. The pancreatic islet cells in insular amyloidosis in human diabetic and non-diabetic adults. Acta Pathol. Microbiol. Scand. A 81, 291-300 (1973).
25. Westermark, P. & Wilander, E. The influence of amyloid deposits on the islet volume in maturity onset diabetes mellitus. Diabetologia 15, 417-421 (1978). (Pubitemid 9046993)
26. Röcken, C., Linke, R. & Saeger, W. Immunohistology of islet amyloid polypeptide in diabetes mellitus: Semi-qantitative studies in a post-mortem series. Virchows Archiv. A 421, 339-344 (1992).
27. Sakagashira, S. et al. S20G Mutant amylin exhibits increased in vitro amyloidogenicity and increased intracellular cytotoxicity compared to wild-type amylin. Am. J. Pathol. 157, 2101-2109 (2000).
28. Lorenzo, A., Razzaboni, B., Weir, G. C. & Yankner, B. A. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368, 756-760 (1994). (Pubitemid 24153418)
29. Westermark, P., Wilander, E.,Westermark, G. T. & Johnson, K. H. Islet amyloid polypeptide-like immunoreactivity in the islet B cells of Type 2 (non-insulindependent) diabetic and non-diabetic individuals. Diabetologia 30, 887-892 (1987). (Pubitemid 18003672)
30. Westermark, P. Fine structure of islets of Langerhans in insular amyloidosis. Virchows Archiv. A 359, 1-18 (1973).
31. Janson, J. et al. Spontaneous diabetes mellitus in transgenic mice expressing human islet amyloid polypeptide. Proc. Natl. Acad. Sci. U. S. A. 93, 7283-7288 (1996). (Pubitemid 26243541)
32. Butler, A. E., Janson, J., Soeller, W. C. & Butler, P. C. Increased b-cell apoptosis prevents adaptive increase in b-cell mass in mouse model of Type 2 diabetes: Evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes 52, 2304-2314 (2003). (Pubitemid 37059501)
33. Janson, J., Ashley, R. H.,Harrison, D., McIntyre, S. & Butler, P. C. Themechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediatesized toxic amyloid particles. Diabetes 48, 491-498 (1999). (Pubitemid 29106861)
34. Dinarello, C. A., Donath, M. Y. & Mandrup-Poulsen, T. Role of IL-1b in type 2 diabetes. Curr. Opin. Endocrinol. Diabetes. Obes. 17, 314-321 (2010).
35. Masters, S. L. et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat. Immunol. 11, 897-904 (2010).
36. Patil, S. M., Xu, S., Sheftic, S. R. & Alexandrescu, A. T. Dynamic alpha-helix structure ofmicelle-bound human amylin. J. Biol. Chem. 284, 11982-11991 (2009).
37. Nanga, R. P. R., Brender, J. R., Vivekanandan, S. & Ramamoorthy, A. Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in amembrane environment. Biochim. Biophys. Acta 1808, 2337-2342 (2011).
38. Apostolidou, M., Jayasinghe, S. A. & Langen, R. Structure of alpha-helical membrane-bound human islet amyloid polypeptide and its implications for membrane-mediated misfolding. J. Biol. Chem. 283, 17205-17210 (2008).
39. Brender, J. R. et al. Amyloid fiber formation and membrane disruption are separate processes localized in two distinct regions of IAPP, the type-2-diabetesrelated peptide. J. Am. Chem. Soc. 130, 6424-6429 (2008). (Pubitemid 351706103)
40. Wiltzius, J. J., Sievers, S. A., Sawaya, M. R. & Eisenberg, D. Atomic structures of IAPP (amylin) fusions suggest amechanism for fibrillation and the role of insulin in the process. Protein Sci. 18, 1521-1530 (2009).
41. Westermark, P., Engstrom, U., Johnson, K. H.,Westermark, G. T. & Betsholtz, C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc. Natl. Acad. Sci. U. S. A. 87, 5036-5040 (1990).
42. Nanga, R. P. R., Brender, J. R., Xu, J., Veglia, G. & Ramamoorthy, A. Structures of rat and human islet amyloid polypeptide IAPP1219 in micelles by NMR spectroscopy. Biochemistry 47, 12689-12697 (2008).
43. Mirzabekov, T. A., Lin, M. C. & Kagan, B. L. Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 271, 1988-1992 (1996). (Pubitemid 26047780)
44. Last, N. B. &Miranker, A. D. Commonmechanism unites membrane poration by amyloid and antimicrobial peptides. Proc. Natl. Acad. Sci. U. S. A. 110, 6382-6387 (2013).
45. Volles, M. J. & Lansbury, P. T. Vesicle permeabilization by protofibrillar a-Synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 41, 4595-4602 (2002). (Pubitemid 34275660)
46. Soura, V. et al. Visualization of co-localization in Ab42-administered neuroblastoma cells reveals lysosome damage and autophagosome accumulation related to cell death. Biochem. J. 441, 579-590 (2012).
47. Fandrich, M., Meinhardt, J. & Grigorieff, N. Structural polymorphism of Alzheimer Abeta and other amyloid fibrils. Prion 3, 89-93 (2009).
48. Conway, K. A. et al. Acceleration of oligomerization, not fibrillization, is a shared property of both a-synuclein mutations linked to early-onset Parkinson's disease: Implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. U. S. A. 97, 571-576 (2000). (Pubitemid 30070350)
49. Lashuel, H. A., Hartley, D., Petre, B. M., Walz, T. & Lansbury, P. T., Jr. Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418, 291 (2002). (Pubitemid 34790672)
50. Kayed, R. et al. Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer. J. Biol. Chem. 284, 4230-4237 (2009).
51. Magzoub, M. &Miranker, A. D. Concentration-dependent transitions govern the subcellular localization of islet amyloid polypeptide. FASEB J. 26, 1228-1238 (2012).
52. Demuro, A. et al. Calcium Dysregulation and Membrane Disruption as a Ubiquitous Neurotoxic Mechanism of Soluble Amyloid Oligomers. J. Biol. Chem. 280, 17294-17300 (2005). (Pubitemid 41389198)
53. Yoshiike, Y., Kayed, R.,Milton, S. C., Takashima, A. & Glabe, C. G. Pore-forming proteins share structural and functional homology with amyloid oligomers. Neuromolecular Med. 9, 270-275 (2007). (Pubitemid 350129702)
54. Kellner, A. et al. Autoantibodies against beta-amyloid are common in Alzheimer's disease and help control plaque burden. Ann. Neurol. 65, 24-31 (2009).
55. Papachroni, K. K. et al. Autoantibodies to alpha-synuclein in inherited Parkinson's disease. J. Neurochem. 101, 749-756 (2007). (Pubitemid 46633311)
56. Yanamandra, K. et al. Alpha-synuclein Reactive antibodies as diagnostic biomarkers in blood sera of Parkinson's disease patients. PLoS ONE. 6, e18513 (2011).