Separate molecular determinants in amyloidogenic and antimicrobial peptides

Journal of Molecular Biology

Volumn 426, Issue 11, 2014, Pages 2159-2166

  Landreh, Michael ^a   Johansson, Jan ^a,b   Jörnvall, Hans ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

amyloid formation; antimicrobial peptides; discordant helices; membrane binding; peptide folding

Indexed keywords

AMYLIN; AMYLOID PROTEIN; DERMASEPTIN; POLYPEPTIDE ANTIBIOTIC AGENT;

ALPHA HELIX; ANTIMICROBIAL ACTIVITY; HUMAN; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN REFOLDING; PROTEIN SECONDARY STRUCTURE; REVIEW;

AMYLOID FORMATION; ANTIMICROBIAL PEPTIDES; DISCORDANT HELICES; MEMBRANE BINDING; PEPTIDE FOLDING;

AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84899936765     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.03.005     Document Type: Review

References (65)

1. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu Rev Biochem 75 2006 333 366
2. H.A. Lashuel, C.R. Overk, A. Oueslati, and E. Masliah The many faces of alpha-synuclein: from structure and toxicity to therapeutic target Nat Rev Neurosci 14 2013 38 48
3. D. Eisenberg, and M. Jucker The amyloid state of proteins in human diseases Cell 148 2012 1188 1203
4. C.L. Heldt, D. Kurouski, M. Sorci, E. Grafeld, I.K. Lednev, and G. Belfort Isolating toxic insulin amyloid reactive species that lack beta-sheets and have wide pH stability Biophys J 100 2011 2792 2800
5. A. Laganowsky, C. Liu, M.R. Sawaya, J.P. Whitelegge, J. Park, and M. Zhao et al. Atomic view of a toxic amyloid small oligomer Science 335 2012 1228 1231
6. V. Novitskaya, O.V. Bocharova, I. Bronstein, and I.V. Baskakov Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons J Biol Chem 281 2006 13828 13836
7. M.F. Engel, L. Khemtemourian, C.C. Kleijer, H.J. Meeldijk, J. Jacobs, and A.J. Verkleij et al. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane Proc Natl Acad Sci U S A 105 2008 6033 6038
8. L. Pieri, M. Bucciantini, D. Nosi, L. Formigli, J. Savistchenko, and R. Melki et al. The yeast prion Ure2p native-like assemblies are toxic to mammalian cells regardless of their aggregation state J Biol Chem 281 2006 15337 15344
9. A.L. Gharibyan, V. Zamotin, K. Yanamandra, O.S. Moskaleva, B.A. Margulis, and I.A. Kostanyan et al. Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways J Mol Biol 365 2007 1337 1349
10. M.F. Sciacca, S.A. Kotler, J.R. Brender, J. Chen, D.K. Lee, and A. Ramamoorthy Two-step mechanism of membrane disruption by Abeta through membrane fragmentation and pore formation Biophys J 103 2012 702 710
11. M.F. Sciacca, J.R. Brender, D.K. Lee, and A. Ramamoorthy Phosphatidylethanolamine enhances amyloid fiber-dependent membrane fragmentation Biochemistry 51 2012 7676 7684
12. N.B. Last, D.E. Schlamadinger, and A.D. Miranker A common landscape for membrane-active peptides Protein Sci 22 2013 870 882
13. M.R. Yeaman, and N.Y. Yount Mechanisms of antimicrobial peptide action and resistance Pharmacol Rev 55 2003 27 55
14. Y. He, and T. Lazaridis Activity determinants of helical antimicrobial peptides: a large-scale computational study PLoS One 8 2013 e66440
15. U.H. Durr, U.S. Sudheendra, and A. Ramamoorthy LL-37, the only human member of the cathelicidin family of antimicrobial peptides Biochim Biophys Acta 1758 2006 1408 1425
16. A. Ramamoorthy, D.K. Lee, T. Narasimhaswamy, and R.P. Nanga Cholesterol reduces pardaxin's dynamics-a barrel-stave mechanism of membrane disruption investigated by solid-state NMR Biochim Biophys Acta 1798 2010 223 227
17. L. Yang, T.A. Harroun, T.M. Weiss, L. Ding, and H.W. Huang Barrel-stave model or toroidal model? A case study on melittin pores Biophys J 81 2001 1475 1485
18. S.J. Soscia, J.E. Kirby, K.J. Washicosky, S.M. Tucker, M. Ingelsson, and B. Hyman et al. The Alzheimer's disease-associated amyloid beta-protein is an antimicrobial peptide PLoS One 5 2010 e9505
19. Y. Hirakura, I. Carreras, J.D. Sipe, and B.L. Kagan Channel formation by serum amyloid A: a potential mechanism for amyloid pathogenesis and host defense Amyloid 9 2002 13 23
20. M. Pasupuleti, M. Roupe, V. Rydengard, K. Surewicz, W.K. Surewicz, and A. Chalupka et al. Antimicrobial activity of human prion protein is mediated by its N-terminal region PLoS One 4 2009 e7358
21. N.B. Last, and A.D. Miranker Common mechanism unites membrane poration by amyloid and antimicrobial peptides Proc Natl Acad Sci U S A 110 2013 6382 6387
22. C. Code, Y.A. Domanov, J.A. Killian, and P.K. Kinnunen Activation of phospholipase A2 by temporin B: formation of antimicrobial peptide-enzyme amyloid-type cofibrils Biochim Biophys Acta 1788 2009 1064 1072
23. L. Caillon, J.A. Killian, O. Lequin, and L. Khemtemourian Biophysical investigation of the membrane-disrupting mechanism of the antimicrobial and amyloid-like peptide dermaseptin s9 PLoS One 8 2013 e75528
24. H. Jang, F.T. Arce, M. Mustata, S. Ramachandran, R. Capone, and R. Nussinov et al. Antimicrobial protegrin-1 forms amyloid-like fibrils with rapid kinetics suggesting a functional link Biophys J 100 2011 1775 1783
25. H. Chu, M. Pazgier, G. Jung, S.P. Nuccio, P.A. Castillo, and M.F. de Jong et al. Human alpha-defensin 6 promotes mucosal innate immunity through self-assembled peptide nanonets Science 337 2012 477 481
26. Y. Huang, J. Huang, and Y. Chen Alpha-helical cationic antimicrobial peptides: relationships of structure and function Protein Cell 1 2010 143 152
27. W.C. Wimley Describing the mechanism of antimicrobial peptide action with the interfacial activity model ACS Chem Biol 5 2010 905 917
28. 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
29. T. Bartels, L.S. Ahlstrom, A. Leftin, F. Kamp, C. Haass, and M.F. Brown et al. The N-terminus of the intrinsically disordered protein alpha-synuclein triggers membrane binding and helix folding Biophys J 99 2010 2116 2124
30. S. Ohta, M. Tanaka, K. Sakakura, T. Kawakami, S. Aimoto, and H. Saito Defining lipid-binding regions of human serum amyloid A using its fragment peptides Chem Phys Lipids 162 2009 62 68
31. A. Olofsson, T. Borowik, G. Grobner, and A.E. Sauer-Eriksson Negatively charged phospholipid membranes induce amyloid formation of medin via an alpha-helical intermediate J Mol Biol 374 2007 186 194
32. S.W. Glasser, A.P. Senft, J.A. Whitsett, M.D. Maxfield, G.F. Ross, and T.R. Richardson et al. Macrophage dysfunction and susceptibility to pulmonary Pseudomonas aeruginosa infection in surfactant protein C-deficient mice J Immunol 181 2008 621 628
33. H. Willander, G. Askarieh, M. Landreh, P. Westermark, K. Nordling, and H. Keranen et al. High-resolution structure of a BRICHOS domain and its implications for anti-amyloid chaperone activity on lung surfactant protein C Proc Natl Acad Sci U S A 109 2012 2325 2329
34. J. Johansson, T. Szyperski, and K. Wuthrich Pulmonary surfactant-associated polypeptide SP-C in lipid micelles: CD studies of intact SP-C and NMR secondary structure determination of depalmitoyl-SP-C(1-17) FEBS Lett 362 1995 261 265
35. H. Shao, S. Jao, K. Ma, and M.G. Zagorski Solution structures of micelle-bound amyloid beta-(1-40) and beta-(1-42) peptides of Alzheimer's disease J Mol Biol 285 1999 755 773
36. A.K. Thakur, M. Jayaraman, R. Mishra, M. Thakur, V.M. Chellgren, and I.J. Byeon et al. Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism Nat Struct Mol Biol 16 2009 380 389
37. M. Jayaraman, R. Kodali, B. Sahoo, A.K. Thakur, A. Mayasundari, and R. Mishra et al. Slow amyloid nucleation via alpha-helix-rich oligomeric intermediates in short polyglutamine-containing huntingtin fragments J Mol Biol 415 2012 881 899
38. M. Michalek, E.S. Salnikov, S. Werten, and B. Bechinger Membrane interactions of the amphipathic amino terminus of huntingtin Biochemistry 52 2013 847 858
39. A. Tossi, L. Sandri, and A. Giangaspero Amphipathic, alpha-helical antimicrobial peptides Biopolymers 55 2000 4 30
40. G. Wang, X. Li, and Z. Wang APD2: the updated antimicrobial peptide database and its application in peptide design Nucleic Acids Res 37 2009 D933 D937
41. O. Lequin, A. Ladram, L. Chabbert, F. Bruston, O. Convert, and D. Vanhoye et al. Dermaseptin S9, an alpha-helical antimicrobial peptide with a hydrophobic core and cationic termini Biochemistry 45 2006 468 480
42. A. Bhunia, R. Saravanan, H. Mohanram, M.L. Mangoni, and S. Bhattacharjya NMR structures and interactions of temporin-1Tl and temporin-1Tb with lipopolysaccharide micelles: mechanistic insights into outer membrane permeabilization and synergistic activity J Biol Chem 286 2011 24394 24406
43. A.K. Mahalka, and P.K. Kinnunen Binding of amphipathic alpha-helical antimicrobial peptides to lipid membranes: lessons from temporins B and L Biochim Biophys Acta 1788 2009 1600 1609
44. S. Maurer-Stroh, M. Debulpaep, N. Kuemmerer, M.L. de la Paz, I.C. Martins, and J. Reumers et al. Exploring the sequence determinants of amyloid structure using position-specific scoring matrices Nat Methods 7 2010 855 857
45. A.M. Fernandez-Escamilla, F. Rousseau, J. Schymkowitz, and L. Serrano Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins Nat Biotechnol 22 2004 1302 1306
46. Y. Kallberg, M. Gustafsson, B. Persson, J. Thyberg, and J. Johansson Prediction of amyloid fibril-forming proteins J Biol Chem 276 2001 12945 12950
47. E. Nordling, and M. Abraham-Nordling Colonic amyloidosis, computational analysis of the major amyloidogenic species, serum amyloid A Comput Biol Chem 39 2012 29 34
48. C. Poojari, A. Kukol, and B. Strodel How the amyloid-beta peptide and membranes affect each other: an extensive simulation study Biochim Biophys Acta 1828 2013 327 339
49. H. Jang, L. Connelly, F.T. Arce, S. Ramachandran, B.L. Kagan, and R. Lal et al. Mechanisms for the insertion of toxic, fibril-like beta-amyloid oligomers into the membrane J Chem Theory Comput 9 2013 822 833
50. A. Quist, I. Doudevski, H. Lin, R. Azimova, D. Ng, and B. Frangione et al. Amyloid ion channels: a common structural link for protein-misfolding disease Proc Natl Acad Sci U S A 102 2005 10427 10432
51. F. Tofoleanu, and N.V. Buchete Alzheimer Abeta peptide interactions with lipid membranes: fibrils, oligomers and polymorphic amyloid channels Prion 6 2012 339 345
52. A. Sandberg, L.M. Luheshi, S. Sollvander, T. Pereira de Barros, B. Macao, and T.P. Knowles et al. Stabilization of neurotoxic Alzheimer amyloid-beta oligomers by protein engineering Proc Natl Acad Sci U S A 107 2010 15595 15600
53. C. Nerelius, A. Sandegren, H. Sargsyan, R. Raunak, H. Leijonmarck, and U. Chatterjee et al. Alpha-helix targeting reduces amyloid-beta peptide toxicity Proc Natl Acad Sci U S A 106 2009 9191 9196
54. R.P. 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 Biochim Biophys Acta 1808 2011 2337 2342
55. M. Apostolidou, S.A. Jayasinghe, and R. Langen Structure of alpha-helical membrane-bound human islet amyloid polypeptide and its implications for membrane-mediated misfolding J Biol Chem 283 2008 17205 17210
56. M.F. Engel, H. Yigittop, R.C. Elgersma, D.T. Rijkers, R.M. Liskamp, and B. de Kruijff et al. Islet amyloid polypeptide inserts into phospholipid monolayers as monomer J Mol Biol 356 2006 783 789
57. J.R. Brender, E.L. Lee, M.A. Cavitt, A. Gafni, D.G. Steel, and A. Ramamoorthy Amyloid fiber formation and membrane disruption are separate processes localized in two distinct regions of IAPP, the type-2-diabetes-related peptide J Am Chem Soc 130 2008 6424 6429
58. M. Pannuzzo, A. Raudino, D. Milardi, C. La Rosa, and M. Karttunen alpha-Helical structures drive early stages of self-assembly of amyloidogenic amyloid polypeptide aggregate formation in membranes Sci Rep 3 2013 2781
59. L. Caillon, O. Lequin, and L. Khemtemourian Evaluation of membrane models and their composition for islet amyloid polypeptide-membrane aggregation Biochim Biophys Acta 1828 2013 2091 2098
60. P. Cao, A. Abedini, H. Wang, L.H. Tu, X. Zhang, and A.M. Schmidt et al. Islet amyloid polypeptide toxicity and membrane interactions Proc Natl Acad Sci U S A 110 2013 19279 19284
61. J.A. Hebda, and A.D. Miranker The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes Annu Rev Biophys 38 2009 125 152
62. J.E. Suk, S.B. Lokappa, and T.S. Ulmer The clustering and spatial arrangement of beta-sheet sequence, but not order, govern alpha-synuclein fibrillogenesis Biochemistry 49 2010 1533 1540
63. K.A. Burke, K.J. Kauffman, C.S. Umbaugh, S.L. Frey, and J. Legleiter The interaction of polyglutamine peptides with lipid membranes is regulated by flanking sequences associated with huntingtin J Biol Chem 288 2013 14993 15005
64. 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 Eng Des Sel 22 2009 453 459
65. M. Landreh, J. Johansson, and H. Jornvall C-Peptide: a molecule balancing insulin states in secretion and diabetes-associated depository conditions Horm Metab Res 45 2013 769 773