Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2015, Article ID 515307, 13 pages
http://dx.doi.org/10.1155/2015/515307
Review Article

Mechanistic Contributions of Biological Cofactors in Islet Amyloid Polypeptide Amyloidogenesis

1Department of Chemistry, Pharmaqam, University of Quebec in Montreal, Montreal, QC, Canada H3C 3P8
2Quebec Network for Research on Protein Function, Structure, and Engineering (PROTEO), Canada
3Biophysics Unit (CSIC, UPV/EHU) and Department of Biochemistry and Molecular Biology, Faculty of Science and Technology, University of the Basque Country, 48080 Bilbao, Spain

Received 5 November 2014; Revised 26 January 2015; Accepted 9 February 2015

Academic Editor: Ehud Gazit

Copyright © 2015 Phuong Trang Nguyen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. Chiti and C. M. Dobson, “Protein misfolding, functional amyloid, and human disease,” Annual Review of Biochemistry, vol. 75, pp. 333–366, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. J. W. Kelly, “The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways,” Current Opinion in Structural Biology, vol. 8, no. 1, pp. 101–106, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Sekijima, R. L. Wiseman, J. Matteson et al., “The biological and chemical basis for tissue-selective amyloid disease,” Cell, vol. 121, no. 1, pp. 73–85, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Coelho, L. F. Maia, A. M. Da Silva et al., “Tafamidis for transthyretin familial amyloid polyneuropathy: a randomized, controlled trial,” Neurology, vol. 79, no. 8, pp. 785–792, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. F. E. Cohen and J. W. Kelly, “Therapeutic approaches to protein-misfolding diseases,” Nature, vol. 426, no. 6968, pp. 905–909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. M. B. Pepys and G. M. Hirschfield, “C-reactive protein: a critical update,” The Journal of Clinical Investigation, vol. 111, no. 12, pp. 1805–1812, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Kisilevsky, “The relation of proteoglycans, serum amyloid P and Apo E to amyloidosis current status, 2000,” Amyloid, vol. 7, no. 1, pp. 23–25, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. V. Bellotti and F. Chiti, “Amyloidogenesis in its biological environment: challenging a fundamental issue in protein misfolding diseases,” Current Opinion in Structural Biology, vol. 18, no. 6, pp. 771–779, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. A. T. Alexandrescu, “Amyloid accomplices and enforcers,” Protein Science, vol. 14, no. 1, pp. 1–12, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. J. B. Ancsin, “Amyloidogenesis: historical and modern observations point to heparan sulfate proteoglycans as a major culprit,” Amyloid, vol. 10, no. 2, pp. 67–79, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. G. P. Gellermann, T. R. Appel, A. Tannert et al., “Raft lipids as common components of human extracellular amyloid fibrils,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 18, pp. 6297–6302, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. E. L. Opie, “The relation Oe diabetes mellitus to lesions of the pancreas. Hyaline degeneration of the islands Oe langerhans,” The Journal of Experimental Medicine, vol. 5, no. 5, pp. 527–540, 1901. View at Publisher · View at Google Scholar
  13. E. T. Bell, “Hyalinization of the islets of Langerhans in nondiabetic individuals,” The American Journal of Pathology, vol. 35, no. 4, pp. 801–805, 1959. View at Google Scholar · View at Scopus
  14. J. C. Ehrlich and I. M. Ratner, “Amyloidosis of the islets of Langerhans. A restudy of islet hyalin in diabetic and non-diabetic individuals,” The American Journal of Pathology, vol. 38, pp. 49–59, 1961. View at Google Scholar · View at Scopus
  15. P. Westermark, C. Wernstedt, E. Wilander, D. W. Hayden, T. D. O'Brien, and K. H. Johnson, “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,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 11, pp. 3881–3885, 1987. View at Publisher · View at Google Scholar · View at Scopus
  16. G. J. S. Cooper, A. C. Willis, A. Clark, R. C. Turner, R. B. Sim, and K. B. M. Reid, “Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 23, pp. 8628–8632, 1987. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Lukinius, E. Wilander, G. T. Westermark, U. Engstrom, and P. Westermark, “Co-localization of islet amyloid polypeptide and insulin in the B cell secretory granules of the human pancreatic islets,” Diabetologia, vol. 32, no. 4, pp. 240–244, 1989. View at Publisher · View at Google Scholar · View at Scopus
  18. E. T. A. S. Jaikaran, M. R. Nilsson, and A. Clark, “Pancreatic β-cell granule peptides form heteromolecular complexes which inhibit islet amyloid polypeptide fibril formation,” Biochemical Journal, vol. 377, no. 3, pp. 709–716, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Westermark, “Amyloid in the islets of Langerhans: thoughts and some historical aspects,” Upsala Journal of Medical Sciences, vol. 116, no. 2, pp. 81–89, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. J. R. Brender, S. Salamekh, and A. Ramamoorthy, “Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective,” Accounts of Chemical Research, vol. 45, no. 3, pp. 454–462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Khemtémourian, J. A. Killian, J. W. Höppener, and M. F. M. Engel, “Recent insights in islet amyloid polypeptide-induced membrane disruption and its role in β-cell death in type 2 diabetes mellitus,” Experimental Diabetes Research, vol. 2008, Article ID 421287, 9 pages, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. M. F. M. Engel, “Membrane permeabilization by Islet Amyloid Polypeptide,” Chemistry and Physics of Lipids, vol. 160, no. 1, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Cao, P. Marek, H. Noor et al., “Islet amyloid: from fundamental biophysics to mechanisms of cytotoxicity,” FEBS Letters, vol. 587, no. 8, pp. 1106–1118, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. J. C. Hutton, “Insulin secretory granule biogenesis and the proinsulin-processing endopeptidases,” Diabetologia, vol. 37, supplement 2, pp. S48–S56, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Westermark, A. Andersson, and G. T. Westermark, “Islet amyloid polypeptide, islet amyloid, and diabetes mellitus,” Physiological Reviews, vol. 91, no. 3, pp. 795–826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Betsholtz, L. Christmansson, U. Engstrom et al., “Sequence divergence in a specific region of islet amyloid polypeptide (IAPP) explains differences in islet amyloid formation between species,” FEBS Letters, vol. 251, no. 1-2, pp. 261–264, 1989. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Westermark, U. Engstrom, K. H. Johnson, G. T. Westermark, and C. Betsholtz, “Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 13, pp. 5036–5040, 1990. View at Publisher · View at Google Scholar · View at Scopus
  28. J. A. Williamson and A. D. Miranker, “Direct detection of transient alpha-helical states in islet amyloid polypeptide,” Protein Science, vol. 16, no. 1, pp. 110–117, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. N. F. Dupuis, C. Wu, J.-E. Shea, and M. T. Bowers, “Human islet amyloid polypeptide monomers form ordered β-hairpins: a possible direct amyloidogenic precursor,” Journal of the American Chemical Society, vol. 131, no. 51, pp. 18283–18292, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. S. M. Patil, S. Xu, S. R. Sheftic, and A. T. Alexandrescu, “Dynamic α-helix structure of micelle-bound human amylin,” The Journal of Biological Chemistry, vol. 284, no. 18, pp. 11982–11991, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. R. P. R. Nanga, J. R. Brender, J. Xu, K. Hartman, V. Subramanian, and A. Ramamoorthy, “Three-dimensional structure and orientation of rat islet amyloid polypeptide protein in a membrane environment by solution NMR spectroscopy,” Journal of the American Chemical Society, vol. 131, no. 23, pp. 8252–8261, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. R. P. R. Nanga, J. R. Brender, S. Vivekanandan, and A. Ramamoorthy, “Structure and membrane orientation of IAPP in its natively amidated form at physiological pH in a membrane environment,” Biochimica et Biophysica Acta—Biomembranes, vol. 1808, no. 10, pp. 2337–2342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. R. P. R. Nanga, J. R. Brender, J. Xu, G. Veglia, and A. Ramamoorthy, “Structures of rat and human islet amyloid polypeptide IAPP1−19 in micelles by NMR spectroscopy,” Biochemistry, vol. 47, no. 48, pp. 12689–12697, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. J. Wimalawansa, “Amylin, calcitonin gene-related peptide, calcitonin, and adrenomedullin: a peptide superfamily,” Critical Reviews in Neurobiology, vol. 11, no. 2-3, pp. 167–239, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. M. C. Chapter, C. M. White, A. DeRidder, W. Chadwick, B. Martin, and S. Maudsley, “Chemical modification of class II G protein-coupled receptor ligands: frontiers in the development of peptide analogs as neuroendocrine pharmacological therapies,” Pharmacology & Therapeutics, vol. 125, no. 1, pp. 39–54, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. D. L. Hay, D. R. Poyner, and P. M. Sexton, “GPCR modulation by RAMPs,” Pharmacology & Therapeutics, vol. 109, no. 1-2, pp. 173–197, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Christopoulos, K. J. Perry, M. Morfis et al., “Multiple amylin receptors arise from receptor activity-modifying protein interaction with the calcitonin receptor gene product,” Molecular Pharmacology, vol. 56, no. 1, pp. 235–242, 1999. View at Google Scholar · View at Scopus
  38. G. Paxinos, S. Y. Chai, G. Christopoulos et al., “In vitro autoradiographic localization of calcitonin and amylin binding sites in monkey brain,” Journal of Chemical Neuroanatomy, vol. 27, no. 4, pp. 217–236, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. B. R. Gedulin, T. J. Rink, and A. A. Young, “Dose-response for glucagonostatic effect of amylin in rats,” Metabolism: Clinical and Experimental, vol. 46, no. 1, pp. 67–70, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. W. A. Scherbaum, “The role of amylin in the physiology of glycemic control,” Experimental and Clinical Endocrinology & Diabetes, vol. 106, no. 2, pp. 97–102, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Naot and J. Cornish, “The role of peptides and receptors of the calcitonin family in the regulation of bone metabolism,” Bone, vol. 43, no. 5, pp. 813–818, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Zidverc-Trajkovic, D. Stanimirovic, R. Obrenovic et al., “Calcitonin gene-related peptide levels in saliva of patients with burning mouth syndrome,” Journal of Oral Pathology & Medicine, vol. 38, no. 1, pp. 29–33, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. T. A. Lutz, “The role of amylin in the control of energy homeostasis,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 298, no. 6, pp. R1475–R1484, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Tycko and R. B. Wickner, “Molecular structures of amyloid and prion fibrils: consensus versus controversy,” Accounts of Chemical Research, vol. 46, no. 7, pp. 1487–1496, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. R. Nelson, M. R. Sawaya, M. Balbirnie et al., “Structure of the cross-β spine of amyloid-like fibrils,” Nature, vol. 435, no. 7043, pp. 773–778, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. O. S. Makin and L. C. Serpell, “Structures for amyloid fibrils,” The FEBS Journal, vol. 272, no. 23, pp. 5950–5961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. A. T. Petkova, R. D. Leapman, Z. Guo, W.-M. Yau, M. P. Mattson, and R. Tycko, “Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils,” Science, vol. 307, no. 5707, pp. 262–265, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Luca, W.-M. Yau, R. Leapman, and R. Tycko, “Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR,” Biochemistry, vol. 46, no. 47, pp. 13505–13522, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. J. J. W. Wiltzius, S. A. Sievers, M. R. Sawaya et al., “Atomic structure of the cross-β spine of islet amyloid polypeptide (amylin),” Protein Science, vol. 17, no. 9, pp. 1467–1474, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Bedrood, Y. Li, J. M. Isas et al., “Fibril structure of human islet amyloid polypeptide,” The Journal of Biological Chemistry, vol. 287, no. 8, pp. 5235–5241, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. S.-H. Shim, R. Gupta, Y. L. Ling, D. B. Strasfeld, D. P. Raleigh, and M. T. Zanni, “Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 16, pp. 6614–6619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. J. W. Kelly, “Mechanisms of amyloidogenesis,” Nature Structural Biology, vol. 7, no. 10, pp. 824–826, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Lee, E. K. Culyba, E. T. Powers, and J. W. Kelly, “Amyloid-β forms fibrils by nucleated conformational conversion of oligomers,” Nature Chemical Biology, vol. 7, no. 9, pp. 602–609, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. S. B. Prusiner, “Novel proteinaceous infectious particles cause scrapie,” Science, vol. 216, no. 4542, pp. 136–144, 1982. View at Publisher · View at Google Scholar · View at Scopus
  55. J. D. Harper and P. T. Lansbury Jr., “Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins,” Annual Review of Biochemistry, vol. 66, pp. 385–407, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Bourgault, S. Choi, J. N. Buxbaum, J. W. Kelly, J. L. Price, and N. Reixach, “Mechanisms of transthyretin cardiomyocyte toxicity inhibition by resveratrol analogs,” Biochemical and Biophysical Research Communications, vol. 410, pp. 707–713, 2011. View at Google Scholar
  57. R. Kayed, E. Head, J. L. Thompson et al., “Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis,” Science, vol. 300, no. 5618, pp. 486–489, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Bemporad and F. Chiti, “Protein misfolded oligomers: experimental approaches, mechanism of formation, and structure-toxicity relationships,” Chemistry & Biology, vol. 19, no. 3, pp. 315–327, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Abedini and D. P. Raleigh, “A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides,” Protein Engineering, Design & Selection, vol. 22, no. 8, pp. 453–459, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. N. F. Dupuis, C. Wu, J.-E. Shea, and M. T. Bowers, “The amyloid formation mechanism in human IAPP: dimers have beta-strand monomer-monomer interfaces,” Journal of the American Chemical Society, vol. 133, no. 19, pp. 7240–7243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. Y. L. Ling, D. B. Strasfeld, S.-H. Shim, D. P. Raleigh, and M. T. Zanni, “Two-dimensional infrared spectroscopy provides evidence of an intermediate in the membrane-catalyzed assembly of diabetic amyloid,” The Journal of Physical Chemistry B, vol. 113, no. 8, pp. 2498–2505, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. S. B. Padrick and A. D. Miranker, “Islet amyloid: phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis,” Biochemistry, vol. 41, no. 14, pp. 4694–4703, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. K. Yanagi, M. Ashizaki, H. Yagi, K. Sakurai, Y.-H. Lee, and Y. Goto, “Hexafluoroisopropanol induces amyloid fibrils of islet amyloid polypeptide by enhancing both hydrophobic and electrostatic interactions,” The Journal of Biological Chemistry, vol. 286, no. 27, pp. 23959–23966, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. J. D. Knight and A. D. Miranker, “Phospholipid catalysis of diabetic amyloid assembly,” Journal of Molecular Biology, vol. 341, no. 5, pp. 1175–1187, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. I. Saraogi, J. A. Hebda, J. Becerril, L. A. Estroff, A. D. Miranker, and A. D. Hamilton, “Synthetic α-helix mimetics as agonists and antagonists of islet amyloid polypeptide aggregation,” Angewandte Chemie—International Edition, vol. 49, no. 4, pp. 736–739, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Kumar, M. A. Brown, A. Nath, and A. D. Miranker, “Folded small molecule manipulation of islet amyloid polypeptide,” Chemistry & Biology, vol. 21, no. 6, pp. 775–781, 2014. View at Publisher · View at Google Scholar
  67. S. Kumar and A. D. Miranker, “A foldamer approach to targeting membrane bound helical states of islet amyloid polypeptide,” Chemical Communications (Cambridge, England), vol. 49, no. 42, pp. 4749–4751, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Hassanpour, C. A. de Carufel, S. Bourgault, and P. Forgione, “Synthesis of 2,5-diaryl-substituted thiophenes as helical mimetics: towards the modulation of islet amyloid polypeptide (IAPP) amyloid fibril formation and cytotoxicity,” Chemistry, vol. 20, no. 9, pp. 2522–2528, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. I. D. Young, L. Ailles, S. Narindrasorasak, R. Tan, and R. Kisilevsky, “Localization of the basement membrane heparan sulfate proteoglycan in islet amyloid deposits in type II diabetes mellitus,” Archives of Pathology & Laboratory Medicine, vol. 116, no. 9, pp. 951–954, 1992. View at Google Scholar · View at Scopus
  70. R. L. Hull, S. Zraika, J. Udayasankar et al., “Inhibition of glycosaminoglycan synthesis and protein glycosylation with WAS-406 and azaserine result in reduced islet amyloid formation in vitro,” American Journal of Physiology—Cell Physiology, vol. 293, no. 5, pp. C1586–C1593, 2007. View at Publisher · View at Google Scholar · View at Scopus
  71. G. T. Westermark and P. Westermark, “Localized amyloids important in diseases outside the brain—lessons from the islets of Langerhans and the thoracic aorta,” The FEBS Journal, vol. 278, no. 20, pp. 3918–3929, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. G. M. Castillo, J. A. Cummings, W. Yang et al., “Sulfate content and specific glycosaminoglycan backbone of perlecan are critical for perlecan's enhancement of islet amyloid polypeptide (amylin) fibril formation,” Diabetes, vol. 47, no. 4, pp. 612–620, 1998. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Jha, S. M. Patil, J. Gibson, C. E. Nelson, N. N. Alder, and A. T. Alexandrescu, “Mechanism of amylin fibrillization enhancement by heparin,” The Journal of Biological Chemistry, vol. 286, no. 26, pp. 22894–22904, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. H. Wang, P. Cao, and D. P. Raleigh, “Amyloid formation in heterogeneous environments: islet amyloid polypeptide glycosaminoglycan interactions,” Journal of Molecular Biology, vol. 425, no. 3, pp. 492–505, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. C. A. de Carufel, P. T. Nguyen, S. Sahnouni, and S. Bourgault, “New insights into the roles of sulfated glycosaminoglycans in islet amyloid polypeptide amyloidogenesis and cytotoxicity,” Biopolymers, vol. 100, no. 6, pp. 645–655, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. T. Konno, S. Oiki, and T. Morii, “Synergistic action of polyanionic and non-polar cofactors in fibrillation of human islet amyloid polypeptide,” FEBS Letters, vol. 581, no. 8, pp. 1635–1638, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Abedini, S. M. Tracz, J.-H. Cho, and D. P. Raleigh, “Characterization of the heparin binding site in the N-terminus of human pro-islet amyloid polypeptide: implications for amyloid formation,” Biochemistry, vol. 45, no. 30, pp. 9228–9237, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. J. R. Bishop, M. Schuksz, and J. D. Esko, “Heparan sulphate proteoglycans fine-tune mammalian physiology,” Nature, vol. 446, no. 7139, pp. 1030–1037, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. K. W. Moremen, M. Tiemeyer, and A. V. Nairn, “Vertebrate protein glycosylation: diversity, synthesis and function,” Nature Reviews Molecular Cell Biology, vol. 13, no. 7, pp. 448–462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. T. M. Handel, Z. Johnson, S. E. Crown, E. K. Lau, M. Sweeney, and A. E. Proudfoot, “Regulation of protein function by glycosaminoglycans—as exemplified by chemokines,” Annual Review of Biochemistry, vol. 74, pp. 385–410, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. N. S. Ihrcke, L. E. Wrenshall, B. J. Lindman, and J. L. Platt, “Role of heparan sulfate in immune system-blood vessel interactions,” Immunology Today, vol. 14, no. 10, pp. 500–505, 1993. View at Publisher · View at Google Scholar · View at Scopus
  82. J. D. Esko and S. B. Selleck, “Order out of chaos: assembly of ligand binding sites in heparan sulfate,” Annual Review of Biochemistry, vol. 71, pp. 435–471, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. J. McLaurin, T. Franklin, X. Zhang, J. Deng, and P. E. Fraser, “Interactions of Alzheimer amyloid-β peptides with glycosaminoglycans: effects on fibril nucleation and growth,” European Journal of Biochemistry, vol. 266, no. 3, pp. 1101–1110, 1999. View at Publisher · View at Google Scholar · View at Scopus
  84. J. A. Cohlberg, J. Li, V. N. Uversky, and A. L. Fink, “Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from α-synuclein in vitro,” Biochemistry, vol. 41, no. 5, pp. 1502–1511, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Bourgault, J. P. Solomon, N. Reixach, and J. W. Kelly, “Sulfated glycosaminoglycans accelerate transthyretin amyloidogenesis by quaternary structural conversion,” Biochemistry, vol. 50, no. 6, pp. 1001–1015, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. J. P. Solomon, S. Bourgault, E. T. Powers, and J. W. Kelly, “Heparin binds 8 kDa gelsolin cross-β-sheet oligomers and accelerates amyloidogenesis by hastening fibril extension,” Biochemistry, vol. 50, no. 13, pp. 2486–2498, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Relini, S. de Stefano, S. Torrassa et al., “Heparin strongly enhances the formation of β2-microglobulin amyloid fibrils in the presence of type I collagen,” The Journal of Biological Chemistry, vol. 283, no. 8, pp. 4912–4920, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. N. Motamedi-Shad, E. Monsellier, S. Torrasa, A. Relini, and F. Chiti, “Kinetic analysis of amyloid formation in the presence of heparan sulfate: faster unfolding and change of pathway,” The Journal of Biological Chemistry, vol. 284, no. 43, pp. 29921–29934, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Y. Suk, F. Zhang, W. E. Balch, R. J. Linhardt, and J. W. Kelly, “Heparin accelerates gelsolin amyloidogenesis,” Biochemistry, vol. 45, no. 7, pp. 2234–2242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. K. Park and C. B. Verchere, “Identification of a heparin binding domain in the N-terminal cleavage site of pro-islet amyloid polypeptide. Implications for islet amyloid formation,” The Journal of Biological Chemistry, vol. 276, no. 20, pp. 16611–16616, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. R. L. Hull, M. J. Peters, S. P. Perigo, C. K. Chan, T. N. Wight, and M. G. Kinsella, “Overall sulfation of heparan sulfate from pancreatic islet β-TC3 cells increases maximal fibril formation but does not determine binding to the amyloidogenic peptide islet amyloid polypeptide,” The Journal of Biological Chemistry, vol. 287, no. 44, pp. 37154–37164, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. F. Meng, A. Abedini, B. Song, and D. P. Raleigh, “Amyloid formation by pro-islet amyloid polypeptide processing intermediates: examination of the role of protein heparan sulfate interactions and implications for islet amyloid formation in type 2 diabetes,” Biochemistry, vol. 46, no. 43, pp. 12091–12099, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Noy, I. Solomonov, O. Sinkevich, T. Arad, K. Kjaer, and I. Sagi, “Zinc-amyloid β interactions on a millisecond time-scale stabilize non-fibrillar Alzheimer-related species,” Journal of the American Chemical Society, vol. 130, no. 4, pp. 1376–1383, 2008. View at Publisher · View at Google Scholar · View at Scopus
  94. G. Yamin, C. B. Glaser, V. N. Uversky, and A. L. Fink, “Certain metals trigger fibrillation of methionine-oxidized α-synuclein,” The Journal of Biological Chemistry, vol. 278, no. 30, pp. 27630–27635, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. M. F. Calabrese, C. M. Eakin, J. M. Wang, and A. D. Miranker, “A regulatable switch mediates self-association in an immunoglobulin fold,” Nature Structural & Molecular Biology, vol. 15, no. 9, pp. 965–971, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Hane and Z. Leonenko, “Effect of metals on kinetic pathways of amyloid-beta aggregation,” Biomolecules, vol. 4, no. 1, pp. 101–116, 2014. View at Publisher · View at Google Scholar
  97. M. C. Foster, R. D. Leapman, M. X. Li, and I. Atwater, “Elemental composition of secretory granules in pancreatic islets of Langerhans,” Biophysical Journal, vol. 64, no. 2, pp. 525–532, 1993. View at Publisher · View at Google Scholar · View at Scopus
  98. J. R. Brender, K. Hartman, R. P. R. Nanga et al., “Role of zinc in human islet amyloid polypeptide aggregation,” Journal of the American Chemical Society, vol. 132, no. 26, pp. 8973–8983, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. J. R. Brender, J. Krishnamoorthy, G. M. L. Messina et al., “Zinc stabilization of prefibrillar oligomers of human islet amyloid polypeptide,” Chemical Communications, vol. 49, no. 32, pp. 3339–3341, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. G. A. Rutter and F. Chimienti, “SLC30A8 mutations in type 2 diabetes,” Diabetologia, vol. 58, no. 1, pp. 31–36, 2015. View at Publisher · View at Google Scholar
  101. R. Sladek, G. Rocheleau, J. Rung et al., “A genome-wide association study identifies novel risk loci for type 2 diabetes,” Nature, vol. 445, no. 7130, pp. 881–885, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. C. A. Aspinwall, S. A. Brooks, R. T. Kennedy, and J. R. T. Lakey, “Effects of intravesicular H+ and extracellular H+ and Zn2+ on insulin secretion in pancreatic beta cells,” The Journal of Biological Chemistry, vol. 272, no. 50, pp. 31308–31314, 1997. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Salamekh, J. R. Brender, S.-J. Hyung et al., “A two-site mechanism for the inhibition of IAPP amyloidogenesis by zinc,” Journal of Molecular Biology, vol. 410, no. 2, pp. 294–306, 2011. View at Publisher · View at Google Scholar · View at Scopus
  104. B. Ward, K. Walker, and C. Exley, “Copper(II) inhibits the formation of amylin amyloid in vitro,” Journal of Inorganic Biochemistry, vol. 102, no. 2, pp. 371–375, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. P. J. Marek, V. Patsalo, D. F. Green, and D. P. Raleigh, “Ionic strength effects on amyloid formation by amylin are a complicated interplay among debye screening, ion selectivity, and hofmeister effects,” Biochemistry, vol. 51, no. 43, pp. 8478–8490, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. J. Guan, H.-L. Zhao, Y. Sui et al., “Histopathological correlations of islet amyloidosis with apolipoprotein e polymorphisms in type 2 diabetic chinese patients,” Pancreas, vol. 42, no. 7, pp. 1129–1137, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. S. B. Charge, M. M. Esiri, C. A. Bethune, B. C. Hansen, and A. Clark, “Apolipoprotein E is associated with islet amyloid and other amyloidoses: implications for Alzheimer's disease,” The Journal of Pathology, vol. 179, no. 4, pp. 443–447, 1996. View at Publisher · View at Google Scholar
  108. K. R. Bales, J. C. Dodart, R. B. DeMattos, D. M. Holtzman, and S. M. Paul, “Apolipoprotein E, amyloid, and Alzheimer disease,” Molecular Interventions, vol. 2, no. 6, pp. 363–375, 2002. View at Publisher · View at Google Scholar · View at Scopus
  109. J. Vidal, C. B. Verchere, S. Andrikopoulos et al., “The effect of apolipoprotein E deficiency on islet amyloid deposition in human islet amyloid polypeptide transgenic mice,” Diabetologia, vol. 46, no. 1, pp. 71–79, 2003. View at Google Scholar · View at Scopus
  110. P. Lei, W.-H. Wu, R.-W. Li et al., “Prevention and promotion effects of apolipoprotein E4 on amylin aggregation,” Biochemical and Biophysical Research Communications, vol. 368, no. 2, pp. 414–418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. P. Westermark, Z.-C. Li, G. T. Westermark, A. Leckström, and D. F. Steiner, “Effects of beta cell granule components on human islet amyloid polypeptide fibril formation,” FEBS Letters, vol. 379, no. 3, pp. 203–206, 1996. View at Publisher · View at Google Scholar · View at Scopus
  112. S. Gilead, H. Wolfenson, and E. Gazit, “Molecular mapping of the recognition interface between the islet amyloid polypeptide and insulin,” Angewandte Chemie—International Edition, vol. 45, no. 39, pp. 6476–6480, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. A. C. Susa, C. Wu, S. L. Bernstein et al., “Defining the molecular basis of amyloid inhibitors: human islet amyloid polypeptide-insulin interactions,” Journal of the American Chemical Society, vol. 136, no. 37, pp. 12912–12919, 2014. View at Publisher · View at Google Scholar
  114. M. F. M. Engel, L. Khemtémourian, C. C. Kleijer et al., “Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 16, pp. 6033–6038, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. S. Janciauskiene and B. Ahrén, “Fibrillar islet amyloid polypeptide differentially affects oxidative mechanisms and lipoprotein uptake in correlation with cytotoxicity in two insulin-producing cell lines,” Biochemical and Biophysical Research Communications, vol. 267, no. 2, pp. 619–625, 2000. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Lorenzo, B. Razzaboni, G. C. Weir, and B. A. Yankner, “Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus,” Nature, vol. 368, no. 6473, pp. 756–760, 1994. View at Publisher · View at Google Scholar · View at Scopus
  117. J. J. Meier, R. Kayed, C.-Y. Lin 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,” American Journal of Physiology—Endocrinology and Metabolism, vol. 291, no. 6, pp. E1317–E1324, 2006. View at Publisher · View at Google Scholar · View at Scopus
  118. J. Janson, W. C. Soeller, P. C. Roche et al., “Spontaneous diabetes mellitus in transgenic mice expressing human islet amyloid polypeptide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 14, pp. 7283–7288, 1996. View at Publisher · View at Google Scholar · View at Scopus
  119. Y. Bram, A. Frydman-Marom, I. Yanai et al., “Apoptosis induced by islet amyloid polypeptide soluble oligomers is neutralized by diabetes-associated specific antibodies,” Scientific Reports, vol. 4, article 4267, 2014. View at Publisher · View at Google Scholar · View at Scopus
  120. J. Janson, R. H. Ashley, D. Harrison, S. McIntyre, and P. C. Butler, “The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles,” Diabetes, vol. 48, no. 3, pp. 491–498, 1999. View at Publisher · View at Google Scholar · View at Scopus
  121. K. Pillay and P. Govender, “Amylin uncovered: a review on the polypeptide responsible for type II diabetes,” BioMed Research International, vol. 2013, Article ID 826706, 17 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  122. A. Abedini and A. M. Schmidt, “Mechanisms of islet amyloidosis toxicity in type 2 diabetes,” FEBS Letters, vol. 587, no. 8, pp. 1119–1127, 2013. View at Publisher · View at Google Scholar · View at Scopus
  123. L. Caillon, O. Lequin, and L. Khemtémourian, “Evaluation of membrane models and their composition for islet amyloid polypeptide-membrane aggregation,” Biochimica et Biophysica Acta, vol. 1828, no. 9, pp. 2091–2098, 2013. View at Publisher · View at Google Scholar · View at Scopus
  124. T. A. Mirzabekov, M.-C. Lin, and B. L. Kagan, “Pore formation by the cytotoxic islet amyloid peptide amylin,” The Journal of Biological Chemistry, vol. 271, no. 4, pp. 1988–1992, 1996. View at Publisher · View at Google Scholar · View at Scopus
  125. D. J. Fawthrop, A. R. Boobis, and D. S. Davies, “Mechanisms of cell death,” Archives of Toxicology, vol. 65, no. 6, pp. 437–444, 1991. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Orrenius, M. J. McCabe Jr., and P. Nicotera, “Ca2+-dependent mechanisms of cytotoxicity and programmed cell death,” Toxicology Letters, vol. 64-65, pp. 357–364, 1992. View at Publisher · View at Google Scholar · View at Scopus
  127. S. Zhang, J. Liu, E. L. Saafi, and G. J. S. Cooper, “Induction of apoptosis by human amylin in RINm5F islet β-cells is associated with enhanced expression of p53 and p21WAF1/CIP1,” FEBS Letters, vol. 455, no. 3, pp. 315–320, 1999. View at Publisher · View at Google Scholar · View at Scopus
  128. C. Mlynarczyk and R. Fahraeus, “Endoplasmic reticulum stress sensitizes cells to DNA damage-induced apoptosis through p53-dependent suppression of p21(CDKN1A.),” Nature Communications, vol. 5, article 5067, 2014. View at Publisher · View at Google Scholar
  129. Y. J. Park, S. Lee, T. J. Kieffer et al., “Deletion of Fas protects islet beta cells from cytotoxic effects of human islet amyloid polypeptide,” Diabetologia, vol. 55, no. 4, pp. 1035–1047, 2012. View at Publisher · View at Google Scholar · View at Scopus
  130. X.-L. Li, G. Xu, T. Chen et al., “Phycocyanin protects INS-1E pancreatic beta cells against human islet amyloid polypeptide-induced apoptosis through attenuating oxidative stress and modulating JNK and p38 mitogen-activated protein kinase pathways,” International Journal of Biochemistry and Cell Biology, vol. 41, no. 7, pp. 1526–1535, 2009. View at Publisher · View at Google Scholar · View at Scopus
  131. S. Zraika, R. L. Hull, J. Udayasankar et al., “Oxidative stress is induced by islet amyloid formation and time-dependently mediates amyloid-induced beta cell apoptosis,” Diabetologia, vol. 52, no. 4, pp. 626–635, 2009. View at Publisher · View at Google Scholar · View at Scopus
  132. B. Gedulin, G. J. S. Cooper, and A. A. Young, “Amylin secretion from the perfused pancreas: dissociation from insulin and abnormal elevation in insulin-resistant diabetic rats,” Biochemical and Biophysical Research Communications, vol. 180, no. 2, pp. 782–789, 1991. View at Publisher · View at Google Scholar · View at Scopus
  133. C.-J. Huang, C.-Y. Lin, L. Haataja 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, vol. 56, no. 8, pp. 2016–2027, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. C.-J. Huang, L. Haataja, T. Gurlo et al., “Induction of endoplasmic reticulum stress-induced beta-cell apoptosis and accumulation of polyubiquitinated proteins by human islet amyloid polypeptide,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 293, no. 6, pp. E1656–E1662, 2007. View at Publisher · View at Google Scholar · View at Scopus
  135. N. Shigihara, A. Fukunaka, A. Hara et al., “Human IAPP-induced pancreatic β cell toxicity and its regulation by autophagy,” The Journal of Clinical Investigation, vol. 124, no. 8, pp. 3634–3644, 2014. View at Publisher · View at Google Scholar
  136. J. D. Esko, T. E. Stewart, and W. H. Taylor, “Animal cell mutants defective in glycosaminoglycan biosynthesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 10, pp. 3197–3201, 1985. View at Publisher · View at Google Scholar · View at Scopus
  137. E. Sandwall, P. O'Callaghan, X. Zhang, U. Lindahl, L. Lannfelt, and J.-P. Li, “Heparan sulfate mediates amyloid-beta internalization and cytotoxicity,” Glycobiology, vol. 20, no. 5, pp. 533–541, 2010. View at Publisher · View at Google Scholar · View at Scopus
  138. T. Saridaki, M. Zampagni, B. Mannini et al., “Glycosaminoglycans (GAGs) suppress the toxicity of HypF-N prefibrillar aggregates,” Journal of Molecular Biology, vol. 421, no. 4-5, pp. 616–630, 2012. View at Publisher · View at Google Scholar · View at Scopus
  139. E. Evangelisti, C. Cecchi, R. Cascella et al., “Membrane lipid composition and its physicochemical properties define cell vulnerability to aberrant protein oligomers,” Journal of Cell Science, vol. 125, no. 10, pp. 2416–2427, 2012. View at Publisher · View at Google Scholar · View at Scopus
  140. S. Trikha and A. M. Jeremic, “Clustering and internalization of toxic amylin oligomers in pancreatic cells require plasma membrane cholesterol,” The Journal of Biological Chemistry, vol. 286, no. 41, pp. 36086–36097, 2011. View at Publisher · View at Google Scholar · View at Scopus
  141. M. Calamai and F. S. Pavone, “Partitioning and confinement of GM1 ganglioside induced by amyloid aggregates,” FEBS Letters, vol. 587, no. 9, pp. 1385–1391, 2013. View at Publisher · View at Google Scholar · View at Scopus
  142. M. F. M. Sciacca, J. R. Brender, D.-K. Lee, and A. Ramamoorthy, “Phosphatidylethanolamine enhances amyloid fiber-dependent membrane fragmentation,” Biochemistry, vol. 51, no. 39, pp. 7676–7684, 2012. View at Publisher · View at Google Scholar · View at Scopus
  143. E. C. Lee, E. Ha, S. Singh et al., “Copper(II)-human amylin complex protects pancreatic cells from amylin toxicity,” Physical Chemistry Chemical Physics, vol. 15, no. 30, pp. 12558–12571, 2013. View at Publisher · View at Google Scholar · View at Scopus
  144. J. A. Hebda, M. Magzoub, and A. D. Miranker, “Small molecule screening in context: lipid-catalyzed amyloid formation,” Protein Science, vol. 23, no. 10, pp. 1341–1348, 2014. View at Publisher · View at Google Scholar
  145. H. Wang and D. P. Raleigh, “The ability of insulin to inhibit the formation of amyloid by pro-islet amyloid polypeptide processing intermediates is significantly reduced in the presence of sulfated glycosaminoglycans,” Biochemistry, vol. 53, no. 16, pp. 2605–2614, 2014. View at Publisher · View at Google Scholar · View at Scopus
  146. J. A. Hebda, I. Saraogi, M. Magzoub, A. D. Hamilton, and A. D. Miranker, “A peptidomimetic approach to targeting pre-amyloidogenic states in type II diabetes,” Chemistry & Biology, vol. 16, no. 9, pp. 943–950, 2009. View at Publisher · View at Google Scholar · View at Scopus