Concentration-dependent transitions govern the subcellular localization of islet amyloid polypeptide

FASEB Journal

Volumn 26, Issue 3, 2012, Pages 1228-1238

  Magzoub, Mazin ^a   Miranker, Andrew D ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amylin; Parkinson's disease

Indexed keywords

AMYLIN; CELL PENETRATING PEPTIDE;

ALPHA HELIX; ANIMAL CELL; ARTICLE; BETA SHEET; CELL CULTURE; CELLULAR DISTRIBUTION; CYTOTOXICITY; HUMAN; MITOCHONDRION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; RAT;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; COS CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; INSULIN-SECRETING CELLS; INSULINOMA; INTRACELLULAR SPACE; ISLET AMYLOID POLYPEPTIDE; MICROSCOPY, CONFOCAL; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; OXIDOREDUCTASES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RATS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, FLUORESCENCE;

EID: 84857729756     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-194613     Document Type: Article

References (71)

1. Haataja, L., Gurlo, T., Huang, C. J., and Butler, P. C. (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis. Endocr. Rev. 29, 303-316 (Pubitemid 351679701)
2. Hoppener, J. W., Ahren, B., and Lips, C. J. (2000) Islet amyloid and type 2 diabetes mellitus. N. Engl. J. Med. 343, 411-419 (Pubitemid 30626125)
3. Kahn, S. E., Andrikopoulos, S., and Verchere, C. B. (1999) Islet amyloid: a long-recognized but underappreciated pathological feature of type 2 diabetes. Diabetes 48, 241-253 (Pubitemid 29061094)
4. Clark, A., and Nilsson, M. R. (2004) Islet amyloid: a complication of islet dysfunction or an aetiological factor in Type 2 diabetes? Diabetologia. 47, 157-169 (Pubitemid 38315352)
5. Hull, R. L., Westermark, G. T., Westermark, P., and Kahn, S. E. (2004) Islet amyloid: a critical entity in the pathogenesis of type 2 diabetes. J. Clin. Endocrinol. Metab. 89, 3629-3643 (Pubitemid 39071447)
6. Kapurniotu, A. (2001) Amyloidogenicity and cytotoxicity of islet amyloid polypeptide. Biopolymers 60, 438-459
7. Westermark, P., Engstrom, U., Johnson, K. H., Westermark, G. T., and 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
8. Matveyenko, A. V., and Butler, P. C. (2006) 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 55, 2106-2114 (Pubitemid 44509986)
9. Potter, K. J., Abedini, A., Marek, P., Klimek, A. M., Butterworth, S., Driscoll, M., Baker, R., Nilsson, M. R., Warnock, G. L., Oberholzer, J., Bertera, S., Trucco, M., Korbutt, G. S., Fraser, P. E., Raleigh, D. P., and Verchere, C. B. (2010) Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts. Proc. Natl. Acad. Sci. U. S. A. 107, 4305-4310
10. Ruschak, A. M., and Miranker, A. D. (2007) Fiber-dependent amyloid formation as catalysis of an existing reaction pathway. Proc. Natl. Acad. Sci. U. S. A. 104, 12341-12346 (Pubitemid 47206139)
11. Hebda, J. A., and Miranker, A. D. (2009) The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes. Annu. Rev. Biophys. 38, 125-152
12. Wiltzius, J. J., Sievers, S. A., Sawaya, M. R., and Eisenberg, D. (2009) Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process. Protein Sci. 18, 1521-1530
13. Nath, A., Miranker, A. D., and Rhoades, E. (2011) A membrane-bound antiparallel dimer of rat islet amyloid polypeptide. Angew. Chem. Int. Ed. Engl. 50, 10859-10862
14. Williamson, J. A., Loria, J. P., and Miranker, A. D. (2009) Helix stabilization precedes aqueous and bilayer-catalyzed fiber formation in islet amyloid polypeptide. J. Mol. Biol. 393, 383-396
15. Williamson, J. A., and Miranker, A. D. (2007) Direct detection of transient alpha-helical states in islet amyloid polypeptide. Protein Sci. 16, 110-117 (Pubitemid 46036503)
16. Patil, S. M., Xu, S., Sheftic, S. R., and Alexandrescu, A. T. (2009) Dynamic alpha-helix structure of micelle-bound human amylin. J. Biol. Chem. 284, 11982-11991
17. Apostolidou, M., Jayasinghe, S. A., and Langen, R. (2008) Structure of alpha-helical membrane-bound human islet amyloid polypeptide and its implications for membrane-mediated misfolding. J. Biol. Chem. 283, 17205-17210
18. Nanga, R. P., Brender, J. R., Xu, J., Hartman, K., Subramanian, V., and Ramamoorthy, A. (2009) Three-dimensional structure and orientation of rat islet amyloid polypeptide protein in a membrane environment by solution NMR spectroscopy. J. Am. Chem. Soc. 131, 8252-8261
19. Hebda, J. A., Saraogi, I., Magzoub, M., Hamilton, A. D., and Miranker, A. D. (2009) A peptidomimetic approach to targeting pre-amyloidogenic states in type II diabetes. Chem. Biol. 16, 943-950
20. Neve, R. L., and Robakis, N. K. (1998) Alzheimer's disease: a re-examination of the amyloid hypothesis. Trends Neurosci. 21, 15-19 (Pubitemid 128766369)
21. Butler, A. E., Janson, J., Soeller, W. C., and Butler, P. C. (2003) 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 52, 2304-2314 (Pubitemid 37059501)
22. Butler, A. E., Jang, J., Gurlo, T., Carty, M. D., Soeller, W. C., and Butler, P. C. (2004) Diabetes due to a progressive defect in beta-cell mass in rats transgenic for human islet amyloid polypeptide (HIP rat): a new model for type 2 diabetes. Diabetes 53, 1509-1516 (Pubitemid 38697663)
23. Meier, J. J., Kayed, R., Lin, C. Y., Gurlo, T., Haataja, L., Jayasinghe, S., Langen, R., Glabe, C. G., and Butler, P. C. (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 (Pubitemid 44904040)
24. Janson, J., Ashley, R. H., Harrison, D., McIntyre, S., and Butler, P. C. (1999) The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 48, 491-498 (Pubitemid 29106861)
25. Last, N. B., Rhoades, E., and Miranker, A. D. (2011) Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity. Proc. Natl. Acad. Sci. U. S. A. 108, 9460-9465
26. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65, 55-63
27. McNeil, P. L., Murphy, R. F., Lanni, F., and Taylor, D. L. (1984) A method for incorporating macromolecules into adherent cells. J. Cell Biol. 98, 1556-1564 (Pubitemid 14126984)
28. Mcneil, P. L. (1989) Incorporation of macromolecules into living cells. Methods Cell Biol. 29, 153-173
29. 2+-dependent vesicle-vesicle fusion events. J. Cell Biol. 139, 63-74
30. McNeil, P. L. (2002) Repairing a torn cell surface: make way, lysosomes to the rescue. J. Cell Sci. 115, 873-879
31. Middleton, E. R., and Rhoades, E. (2010) Effects of curvature and composition on alpha-synuclein binding to lipid vesicles. Biophys. J. 99, 2279-2288
32. Luca, S., Yau, W. M., Leapman, R., and Tycko, R. (2007) Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR. Biochemistry 46, 13505-13522 (Pubitemid 350209947)
33. + channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424-430
34. O'Brien, T. D., Butler, P. C., Kreutter, D. K., Kane, L. A., and Eberhardt, N. L. (1995) Human islet amyloid polypeptide expression in COS-1 cells. A model of intracellular amyloidogenesis. Am. J. Pathol. 147, 609-616
35. Hiddinga, H. J., and Eberhardt, N. L. (1999) Intracellular amyloidogenesis by human islet amyloid polypeptide induces apoptosis in COS-1 cells. Am. J. Pathol. 154, 1077-1088 (Pubitemid 29169742)
36. Riss, T. L., and Moravec, R. A. (2004) Use of multiple assay endpoints to investigate the effects of incubation time, dose of toxin, and plating density in cell-based cytotoxicity assays. Assay Drug Dev. Technol. 2, 51-62 (Pubitemid 38647416)
37. 2+ in apoptosis evoked by human amylin in pancreatic islet beta-cells. Biochem. J. 343, 53-61
38. Rumora, L., Hadzija, M., Barisic, K., Maysinger, D., and Grubiic, T. Z. (2002) Amylin-induced cytotoxicity is associated with activation of caspase-3 and MAP kinases. Biol. Chem. 383, 1751-1758 (Pubitemid 36033089)
39. Konarkowska, B., Aitken, J. F., Kistler, J., Zhang, S., and Cooper, G. J. (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells. FEBS J. 273, 3614-3624 (Pubitemid 44086959)
40. Lim, Y. A., Ittner, L. M., Lim, Y. L., and Gotz, J. (2008) Human but not rat amylin shares neurotoxic properties with Abeta42 in long-term hippocampal and cortical cultures. FEBS Lett. 582, 2188-2194
41. Knight, J. D., Hebda, J. A., and Miranker, A. D. (2006) Conserved and cooperative assembly of membrane-bound alpha-helical states of islet amyloid polypeptide. Biochemistry 45, 9496-9508 (Pubitemid 44223253)
42. Brender, J. R., Hartman, K., Reid, K. R., Kennedy, R. T., and Ramamoorthy, A. (2008) A single mutation in the nonamyloidogenic region of islet amyloid polypeptide greatly reduces toxicity. Biochemistry 47, 12680-12688
43. Koo, B. W., Hebda, J. A., and Miranker, A. D. (2008) Amide inequivalence in the fibrillar assembly of islet amyloid polypeptide. Protein Eng. Des. Sel. 21, 147-154 (Pubitemid 351323351)
44. Nanga, R. P., Brender, J. R., Xu, J., Veglia, G., and Ramamoorthy, A. (2008) Structures of rat and human islet amyloid polypeptide IAPP(1-19) in micelles by NMR spectroscopy. Biochemistry 47, 12689-12697
45. Soong, R., Brender, J. R., Macdonald, P. M., and Ramamoorthy, A. (2009) Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. J. Am. Chem. Soc. 131, 7079-7085
46. Wang, L. H., Rothberg, K. G., and Anderson, R. G. (1993) Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell Biol. 123, 1107-1117 (Pubitemid 23352421)
47. Wadia, J. S., Stan, R. V., and Dowdy, S. F. (2004) Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10, 310-315 (Pubitemid 38667624)
48. Sampath, P., and Pollard, T. D. (1991) Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments. Biochemistry 30, 1973-1980
49. Du, D., Murray, A. N., Cohen, E., Kim, H. E., Simkovsky, R., Dillin, A., and Kelly, J. W. (2011) A kinetic aggregation assay allowing selective and sensitive amyloid-beta quantification in cells and tissues. Biochemistry 50, 1607-1617
50. Ritzel, R. A., and Butler, P. C. (2003) Replication increases beta-cell vulnerability to human islet amyloid polypeptide-induced apoptosis. Diabetes 52, 1701-1708 (Pubitemid 36792460)
51. Gurlo, T., Ryazantsev, S., Huang, C. J., Yeh, M. W., Reber, H. A., Hines, O. J., O'Brien, T. D., Glabe, C. G., and Butler, P. C. (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
52. Li, X. L., Chen, T., Wong, Y. S., Xu, G., Fan, R. R., Zhao, H. L., and Chan, J. C. (2011) Involvement of mitochondrial dysfunction in human islet amyloid polypeptide-induced apoptosis in INS-1E pancreatic beta cells: An effect attenuated by phycocyanin. Int. J. Biochem. Cell Biol. 43, 525-534
53. Casas, S., Gomis, R., Gribble, F. M., Altirriba, J., Knuutila, S., and Novials, A. (2007) 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 56, 2284-2294 (Pubitemid 47358235)
54. Mirzabekov, T. A., Lin, M. C., and Kagan, B. L. (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 271, 1988-1992 (Pubitemid 26047780)
55. Tschop, M., and Heiman, M. L. (2001) Rodent obesity models: an overview. Exp. Clin. Endocrinol. Diabetes. 109, 307-319 (Pubitemid 32885033)
56. Hoppener, J. W., Oosterwijk, C., Nieuwenhuis, M. G., Posthuma, G., Thijssen, J. H., Vroom, T. M., Ahren, B., and Lips, C. J. (1999) Extensive islet amyloid formation is induced by development of type II diabetes mellitus and contributes to its progression: pathogenesis of diabetes in a mouse model. Diabetologia 42, 427-434 (Pubitemid 29148401)
57. Shimabukuro, M., Zhou, Y. T., Levi, M., and Unger, R. H. (1998) Fatty acid-induced beta cell apoptosis: a link between obesity and diabetes. Proc. Natl. Acad. Sci. U. S. A. 95, 2498-2502 (Pubitemid 28145970)
58. 2+ concentration. J. Biol. Chem. 273, 33501-33507
59. Magzoub, M., and Graslund, A. (2004) Cell-penetrating peptides: [corrected] from inception to application. Q. Rev. Biophys. 37, 147-195 (Pubitemid 40867965)
60. Soto, C., and Castano, E. M. (1996) The conformation of Alzheimer's beta peptide determines the rate of amyloid formation and its resistance to proteolysis. Biochem. J. 314, 701-707 (Pubitemid 26074788)
61. Palm-Apergi, C., Lorents, A., Padari, K., Pooga, M., and Hallbrink, M. (2009) The membrane repair response masks membrane disturbances caused by cell-penetrating peptide uptake. FASEB J. 23, 214-223
62. Demuro, A., Mina, E., Kayed, R., Milton, S. C., Parker, I., and Glabe, C. G. (2005) Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280, 17294-17300 (Pubitemid 41389198)
63. Lin, C. Y., Gurlo, T., Kayed, R., Butler, A. E., Haataja, L., Glabe, C. G., and Butler, P. C. (2007) Toxic human islet amyloid polypeptide (h-IAPP) oligomers are intracellular, and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPP-induced beta-cell apoptosis in h-IAPP transgenic mice. Diabetes 56, 1324-1332 (Pubitemid 46715613)
64. Matveyenko, A. V., Gurlo, T., Daval, M., Butler, A. E., and Butler, P. C. (2009) Successful versus failed adaptation to high-fat diet-induced insulin resistance: the role of IAPP-induced beta-cell endoplasmic reticulum stress. Diabetes 58, 906 -916
65. Liu, M. L., and Hong, S. T. (2005) Early phase of amyloid beta42-induced cytotoxicity in neuronal cells is associated with vacuole formation and enhancement of exocytosis. Exp. Mol. Med. 37, 559-566
66. Lustbader, J. W., Cirilli, M., Lin, C., Xu, H. W., Takuma, K., Wang, N., Caspersen, C., Chen, X., Pollak, S., Chaney, M., Trinchese, F., Liu, S., Gunn-Moore, F., Lue, L. F., Walker, D. G., Kuppusamy, P., Zewier, Z. L., Arancio, O., Stern, D., Yan, S. S., and Wu, H. (2004) ABAD directly links Aβ to mitochondrial toxicity in Alzheimer's disease. Science 304, 448-452 (Pubitemid 38495942)
67. Lim, Y. A., Rhein, V., Baysang, G., Meier, F., Poljak, A., Raftery, M. J., Guilhaus, M., Ittner, L. M., Eckert, A., and Gotz, J. (2010) Aβ and human amylin share a common toxicity pathway via mitochondrial dysfunction. Proteomics 10, 1621-1633
68. Nakamura, K., Nemani, V. M., Wallender, E. K., Kaehlcke, K., Ott, M., and Edwards, R. H. (2008) Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondria. J. Neurosci. 28, 12305-12317
69. Conway, K. A., Harper, J. D., and Lansbury, P. T. J. (2000) Fibrils formed in vitro from alpha-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 39, 2552-2563 (Pubitemid 30148907)
70. Conway, K. A., Lee, S. J., Rochet, J. C., Ding, T. T., Williamson, R. E., and Lansbury, P. T. J. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both alphasynuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. U. S. A. 97, 571-576 (Pubitemid 30070350)
71. Nakamura, K., Nemani, V. M., Azarbal, F., Skibinski, G., Levy, J. M., Egami, K., Munishkina, L., Zhang, J., Gardner, B., Wakabayashi, J., Sesaki, H., Cheng, Y., Finkbeiner, S., Nussbaum, R. L., Masliah, E., and Edwards, R. H. (2011) Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein. J. Biol. Chem. 286, 20710-20726