Molecular and cytotoxic properties of hIAPP17-29 and rIAPP17-29 fragments: A comparative study with the respective full-length parent polypeptides

European Journal of Medicinal Chemistry

Volumn 81, Issue , 2014, Pages 442-455

  Tomasello, Marianna Flora ^a   Sinopoli, Alessandro ^b   Attanasio, Francesco ^a   Giuffrida, Maria Laura ^a   Campagna, Tiziana ^a   Milardi, Danilo ^a   Pappalardo, Giuseppe ^a  

^a CNR   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

Amyloid; Confocal microscopy; Mitochondria; Model membranes; Spectroscopy; Type 2 diabetes

Indexed keywords

AMINO ACID; AMYLIN; BUFFER; PEPTIDE FRAGMENT; SOLVENT;

ARTICLE; BETA SHEET; CIRCULAR DICHROISM; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOTOXICITY; FLUORESCENCE; GENE SEQUENCE; HUMAN; HYPOTHESIS; LIGHT SCATTERING; MEMBRANE MODEL; MOLECULAR DYNAMICS; NONHUMAN; PANCREAS ISLET BETA CELL; PH; PHYSIOLOGICAL PROCESS; RAT; ANIMAL; CELL DEATH; CELL SURVIVAL; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE;

ANIMALS; CELL DEATH; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; ISLET AMYLOID POLYPEPTIDE; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; RATS; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

EID: 84901326400     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2014.05.038     Document Type: Article

References (69)

1. J.D. Sipe Amyloidosis Crit. Rev. Clin. Lab. Sci. 31 1994 325 354
2. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 336
3. A. Clark, C.A. Wells, I.D. Buley, J.K. Cruickshank, R.I. Vanhagan, D.R. Matthews, G.J.S. Cooper, R.R. Holmann, and R.C. Turner Islet amyloid, increased A-cells, reduced B-cells and exocrine fibrosis: quantitative changes in the pancreas in type 2 diabetes Diab. Res. 9 1988 151 159 (Pubitemid 19105415)
4. M.R. Hayden, S.C. Tyagi, M.M. Kerklo, and M.R. Nicolls Type 2 diabetes mellitus as a conformational disease JOP 6 2005 287 302 (Pubitemid 41581749)
5. P. Westermark, E. Wilander, G.T. Westermark, and K.H. Johnson Islet amyloid polypeptide-like immunoreactivity in the islet B cells of Type 2 (non-insulin-dependent) diabetic and non-diabetic individuals Diabetologia 30 1987 887 892 (Pubitemid 18003672)
6. P. Westermark, A. Andersson, and G.T. Westermark Islet amyloid polypeptide, islet amyloid, and diabetes mellitus Physiol. Rev. 91 2011 795 826
7. G. Liu, A. Prabhakar, D. Aucoin, M. Simon, S. Sparks, K.J. Robbins, A. Sheen, S.A. Petty, and N. Lazo Mechanistic studies of peptide self-assembly: transient α-helices to stable β-sheets J. Am. Chem. Soc. 132 2010 18223 18232
8. A. Kapurniotu Amyloidogenicity and cytotoxicity of islet amyloid polypeptide Biopolymers 60 2001 438 459 (Pubitemid 35000911)
9. R. Kayed, J. Bernhagen, N. Greenfield, K. Sweimeh, H. Brunner, W. Voelter, and A. Kapurniotu Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro J. Mol. Biol. 287 1999 781 796 (Pubitemid 29176513)
10. M.D. Kirkitadze, G. Bitan, and D.B. Teplow Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies J. Neurosci. Res. 69 2002 567 577 (Pubitemid 34966869)
11. D.M. Walsh, and D.J. Selkoe Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration Protein Pept. Lett. 11 2004 213 228 (Pubitemid 38689025)
12. L. Haataja, T. Gurlo, C.J. Huang, and P.C. Butler Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocr. Rev. 29 2008 303 316 (Pubitemid 351679701)
13. T. Gurlo, S. Ryazantsev, C.J. Huang, M.W. Yeh, H.A. Reber, O.J. Hines, T.D. O'Brien, C.G. Glabe, and P.C. Butler 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 2010 861 869
14. 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 Acc. Chem. Res. 45 2012 454 462
15. M.F. Engel Membrane permeabilization by islet amyloid polypeptide Chem. Phys. Lipids 160 2009 1 10
16. S. Zhang, J. Liu, E.L. Saafi, and G.J. Cooper Induction of apoptosis by human amylin in RINm5F islet beta-cells is associated with enhanced expression of p53 and p21WAF1/CIP1 FEBS Lett. 455 1999 315 320 (Pubitemid 29333059)
17. S. Zraika, R.L. Hull, J. Udayasankar, K. Aston-Mourney, S.L. Subramanian, R. Kisilevsky, W.A. Szarek, and S.E. Kahn Oxidative stress is induced by islet amyloid formation and time-dependently mediates amyloid-induced beta cell apoptosis Diabetologia 52 2009 626 635
18. S.L. Subramanian, R.L. Hull, S. Zraika, K. Aston-Mourney, J. Udayasankar, and S.E. Kahn cJUN N-terminal kinase (JNK) activation mediates islet amyloid-induced beta cell apoptosis in cultured human islet amyloid polypeptide transgenic mouse islets Diabetologia 55 2012 166 174
19. N. Sánchez de Groot, I. Pallarés, F.X. Avilés, J. Vendrell, and S. Ventura Prediction of "hot spots" of aggregation in disease-linked polypeptides BMC Struct. Biol. 5 2005 18
20. A. Abedini, and D.P. Raleigh Destabilization of human IAPP amyloid fibrils by proline mutations outside of the putative amyloidogenic domain: is there a critical amyloidogenic domain in human IAPP? J. Mol. Biol. 355 2006 274 281 (Pubitemid 41782003)
21. A. Fox, T. Snollaerts, C.E. Casanova, A. Calciano, L.A. Nogaj, and D.A. Moffet Selection for nonamyloidogenic mutants of islet amyloid polypeptide (IAPP) identifies an extended region for amyloidogenicity Biochemistry 49 2010 7783 7789
22. E.T.A.S. Jaikaran, C.E. Higham, L.C. Serpell, J. Zurdo, M. Gross, A. Clark, and P.E. Fraser Identification of a novel human islet amyloid polypeptide beta-sheet domain and factors influencing fibrillogenesis J. Mol. Biol. 308 2001 515 525 (Pubitemid 33027616)
23. R. Azriel, and E. Gazit Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation J. Biol. Chem. 276 2001 34156 34161
24. K. Tenidis, M. Waldner, J. Bernhagen, W. Fischle, M. Bergmann, M. Weber, M.L. Merkle, W. Voelter, H. Brunner, and A. Kapurniotu Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties J. Mol. Biol. 295 2000 1055 1071
25. L.A. Scrocchi, Y. Chen, K.S. Waschu, F. Wang, S. Cheung, A.A. Darabie, J. McLaurin, and P.E. Fraser Design of peptide-based inhibitors of human islet amyloid polypeptide fibrillogenesis J. Mol. Biol. 318 2002 697 706 (Pubitemid 34729362)
26. G. Pappalardo, D. Milardi, A. Magrì, F. Attanasio, G. Impellizzeri, C. La Rosa, D. Grasso, and E. Rizzarelli Environmental factors differently affect human and rat IAPP: conformational preferences and membrane interactions of IAPP 17-29 peptide derivates Chem. Eur. J. 13 2007 10204 10215
27. A. Mazzaglia, N. Micali, L.M. Scolaro, F. Attanasio, A. Magrí, G. Pappalardo, and V. Villari Aggregation properties of the peptide fragments derived from the 17-29 region of the human and rat IAPP: a comparative study with two PEG-conjugated variants of the human sequence J. Phys. Chem. B 114 2010 705 713
28. A.V. Matveyenco, and P.C. Butler Islet amyloid polypeptide (IAPP) transgenic rodents as models for type 2 diabetes ILAR J. 47 2006 225 233 (Pubitemid 43986031)
29. P. Cao, P. Marek, H. Noor, V. Patsalo, L.H. Tu, H. Wang, A. Abedini, and D.P. Raleigh Islet amyloid: from fundamental biophysics to mechanisms of cytotoxicity FEBS Lett. 587 2013 1106 1118
30. A. Perczel, and M. Hallosi G.D. Fasman, Circular Dichroism and the Conformational Analysis of Biomolecules 1996 Plenum Press New York 285 380
31. N. Micali, V. Villari, G.M. Consoli, F. Cunsolo, and C. Geraci Vesicle-to-micelle transition in aqueous solutions of amphiphilic calixarene derivatives Phys. Rev. E. Stat. Nonlin. Soft Matter Phys. 73 2006 n° 051904
32. 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 48 1999 491 498 (Pubitemid 29106861)
33. S. Janciauskiene, and B. Ahrén Different sensitivity to the cytotoxic action of IAPP fibrils in two insulin-producing cell lines, HIT-T15 and RINm5F cells Biochem. Biophys. Res. Commun. 251 1998 888 893 (Pubitemid 28512806)
34. M. Magzoub, and A.D. Miranker Concentration-dependent transitions govern the subcellular localization of islet amyloid polypeptide FASEB J. 26 2012 1228 1238
35. J.M. Dypbukt, M. Ankarcrona, M. Burkitt, A. Sjöholm, K. Ström, S. Orrenius, and P. Nicotera Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines J. Biol. Chem. 269 1994 30553 30560
36. B. Konarkowska, J.F. Aitken, J. Kistler, S. Zhang, and G.J. Cooper Thiol reducing compounds prevent human amylin-evoked cytotoxicity FEBS J. 272 2005 4949 4959 (Pubitemid 41415118)
37. M. Wakabayashi, and K. Matsuzaki Ganglioside-induced amyloid formation by human islet amyloid polypeptide in lipid rafts FEBS Lett. 583 2009 2854 2858
38. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489 (Pubitemid 36444329)
39. P. Westermark, U. Engström, K.H. Jonshon, G.T. Westermark, and C. Betsholtz Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation Proc. Natl. Acad. Sci. U. S. A. 87 1990 5036 5040
40. A.D. Abedini, and P. Raleigh The role of His-18 in amyloid formation by human islet amyloid polypeptide Biochemistry 44 2005 16284 16291
41. 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 J. Biol. Chem. 286 2011 23959 23966
42. H. Naiki, K. Higuchi, M. Hosokawa, and T. Takeda Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1 Anal. Biochem 177 1989 244 249 (Pubitemid 19088253)
43. H. LeVine 3rd Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution Protein Sci. 2 1993 404 410
44. K.J. Potter, L.A. Scrocchi, G.L. Warnock, Z. Ao, M.A. Younker, L. Rosenberg, M. Lipsett, C.B. Verchere, and P.E. Fraser Amyloid inhibitors enhance survival of cultured human islets Biochim. Biophys. Acta 1790 2009 566 574
45. C.E. Higham, E.T. Jaikaran, P.E. Fraser, M. Gross, and A. Clark Preparation of synthetic human islet amyloid polypeptide (IAPP) in a stable conformation to enable study of conversion to amyloid-like fibrils FEBS Lett. 470 2000 55 60 (Pubitemid 30155623)
46. X. Zhang, B. Cheng, H. Gong, C. Li, H. Chen, L. Zheng, and K. Huang Porcine islet amyloid polypeptide fragments are refractory to amyloid formation FEBS Lett. 585 2011 71 77
47. P. Cao, L.H. Tu, A. Abedini, O. Levsh, R. Akter, V. Patsalo, A.M. Schmidt, and D.P. Raleigh Sensitivity of amyloid formation by human islet amyloid polypeptide to mutations at residue 20 J. Mol. Biol. 421 2012 282 295
48. N.G.N. Milton, and J.R. Harris Fibril formation and toxicity of the non-amyloidogenic rat amylin peptide Micron 44 2013 246 253
49. Y.A. Lim, L.M. Ittner, Y.L. Lim, and J. Götz Human but not rat amylin shares neurotoxic properties with Abeta42 in long-term hippocampal and cortical cultures FEBS Lett. 582 2008 2188 2194
50. S. Luca, W.M. Yau, R. Leapman, and R. Tycko Peptide conformation and supramolecular organization in amylin fibrils: constraints from solid-state NMR Biochemistry 46 2007 13505 13522 (Pubitemid 350209947)
51. S. Salamekh, J.R. Brender, S.J. Hyung, R.P. Nanga, S. Vivekanandan, B.T. Ruotolo, and A. Ramamoorthy A two-site mechanism for the inhibition of IAPP amyloidogenesis by zinc J. Mol. Biol. 410 2011 294 306
52. 2+ in apoptosis evoked by human amylin in pancreatic islet beta-cells Biochem. J. 343 1999 53 61 (Pubitemid 29473877)
53. S. Trikha, and A.M. Jeremic Clustering and internalization of toxic amylin oligomers in pancreatic cells require plasma membrane cholesterol J. Biol. Chem. 286 2011 36086 36097
54. J.F. Paulsson, S.W. Schultz, M. Köhler, I. Leibiger, P.O. Berggren, and G.T. Westermark Real-time monitoring of apoptosis by caspase-3-like protease induced FRET reduction triggered by amyloid aggregation Exp. Diabetes Res. 2008 865850
55. A. Abedini, and A.M. Schmidt Mechanisms of islet amyloidosis toxicity in type 2 diabetes FEBS Lett. 587 2013 1119 1127
56. A. Nath, A.D. Miranker, and E. Rhoades A membrane-bound antiparallel dimer of rat islet amyloid polypeptide Angew. Chem. Int. Ed. Engl. 50 2011 10859 10862
57. N.B. Last, E. Rhoades, and A.D. Miranker Islet amyloid polypeptide demonstrates a persistent capacity to disrupt membrane integrity Proc. Natl. Acad. Sci. U. S. A. 108 2011 9460 9465
58. T.A. Mirzabekov, M.C. Lin, and B.L. Kagan Pore formation by the cytotoxic islet amyloid peptide amylin J. Biol. Chem. 271 1996 1988 1992 (Pubitemid 26047780)
59. J.D. Knight, J.A. Hebda, and A.D. Miranker Conserved and cooperative assembly of membrane-bound alpha-helical states of islet amyloid polypeptide Biochemistry 45 2006 9496 9508 (Pubitemid 44223253)
60. M.F.M. Engel, L. Khemtemourian, C.C. Kleijer, H.J.D. Meeldijk, J. Jacobs, A.J. Verkleij, B. de Kruijff, J.A. Killian, and J.W. Höppener Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane Proc. Natl. Acad. Sci. U. S. A. 105 2008 6033 6038 (Pubitemid 351758394)
61. P. Li, D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91 1997 479 489 (Pubitemid 27508237)
62. P. Gubellini, B. Picconi, M. Di Filippo, and P. Calabresi Downstream mechanisms triggered by mitochondrial dysfunction in the basal ganglia: from experimental models to neurodegenerative diseases Biochim. Biophys. Acta 1802 2010 151 161
63. M. Stefani, and C.M. Dobson Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81 2003 678 699 (Pubitemid 37491594)
64. M. Bucciantini, G. Calloni, F. Chiti, L. Formigli, D. Nosi, C.M. Dobson, and M. Stefani Prefibrillar amyloid protein aggregates share common features of cytotoxicity J. Biol. Chem. 279 2004 31374 31382 (Pubitemid 39037804)
65. M.F.M. Sciacca, D. Milardi, G.M.L. Messina, G. Marletta, and J.R. Brender Cations as switches of amyloid-mediated membrane disruption mechanisms: calcium and IAPP Biophys. J. 104 2013 173 184
66. D. Milardi, M.F.M. Sciacca, M. Pappalardo, D.M. Grasso, and C. La Rosa The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragment LANFLVH Eur. Biophys. J. 40 2011 1 12
67. V. Villari, and N. Micali Light scattering as spectroscopic tool for the study of disperse systems useful in pharmaceutical sciences J. Pharm. Sci. 97 2008 1703 1730
68. B. Chu Laser Light Scattering-basic Principle and Practice 1991 San Diego Academic
69. T.J. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays Immunol. Methods 65 1983 55 63