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Amyloid Peptide Pores and the Beta Sheet Conformation

  • Bruce L. Kagan
  • Jyothi Thundimadathil
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 677)

Abstract

Over 20 clinical syndromes have been described as amyloid diseases. Pathologically, these illnesses are characterized by the deposition in various tissues of amorphous, Congo red staining deposits, referred to as amyloid. Under polarizing light microscopy, these deposits exhibit characteristic green birefringence. X-ray diffraction reveals cross-beta structure of extended amyloid fibrils. Although there is always a major protein in amyloid deposits, the predominant protein differs in each of the clinical syndromes. All the proteins exhibit the characteristic nonnative beta-sheet state. These proteins aggregate spontaneously into extended fibrils and precipitate out of solution. At least a dozen of these peptides have been demonstrated to be capable of channel formation in lipid bilayers and it has been proposed that this represents a pathogenic mechanism. Remarkably, the channels formed by these various peptides exhibit a number of common properties including irreversible, spontaneous insertion into membranes, production of large, heterogeneous single-channel conductances, relatively poor ion selectivity, inhibition of channel formation by Congo red and related dyes and blockade of inserted channels by zinc. In vivo amyloid peptides have been shown to disrupt intracellular calcium regulation, plasma membrane potential, mitochondrial membrane potential and function and long-term potentiation in neurons. Amyloid peptides also cause cytotoxicity. Formation of the beta sheet conformation from native protein structures can be induced by high protein concentrations, metal binding, acidic pH, amino acid mutation and interaction with lipid membranes. Most amyloid peptides interact strongly with membranes and this interaction is enhanced by conditions which favor beta-sheet formation. Formation of pores in these illnesses appears to be a spontaneous process and available evidence suggests several steps are critical. First, destabilization of the native structure and formation of the beta-sheet conformation must occur. This may occur in solution or may be facilitated by contact with lipid membranes. Oligomerization of the amyloid protein is then mediated by the beta strands. Amyloid monomers and extended fibrils appear to have little potential for toxicity whereas there is much evidence implicating amyloid oligomers of intermediate size in the pathogenesis of amyloid disease. Insertion of the oligomer appears to take place spontaneously although there may be a contribution of acidic pH and/or membrane potential. Very little is known about the structure of amyloid pores, but given that the amyloid peptides must acquire beta-sheet conformation to aggregate and polymerize, it has been hypothesized that amyloid pores may in fact be beta-sheet barrels similar to the pores formed by alpha-latrotoxin, Staphylococcal alpha-hemolysin, anthrax toxin and clostridial perfringolysin.

Keywords

Prion Protein Pore Formation Channel Formation Amyloid Protein Amyloid Peptide 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Sipe JD, Cohen AS. Review: history of the amyloid fibril. J Struct Biol 2000; 130:88–98.PubMedCrossRefGoogle Scholar
  2. 2.
    Anguiano M, Nowak RJ, Lansbury PT. Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes. Biochemistry 2002; 41:11338–11343.PubMedCrossRefGoogle Scholar
  3. 3.
    Hirakura Y, Kagan BL. Pore formation by beta-2-microglobulin: a mechanism for the pathogenesis of dialysis associated amyloidosis. Amyloid 2001; 8:94–100.PubMedGoogle Scholar
  4. 4.
    Sipe JD. Serum amyloid A: from fibril to function. Current status. Amyloid 2000; 7:10–12.PubMedCrossRefGoogle Scholar
  5. 5.
    Kourie JI, Hanna EA, Henry CL. Properties and modulation of alpha human atrial natriuretic peptide (alpha-hANP)-formed ion channels. Can J Physiol Pharmacol 2001; 79:654–64.PubMedCrossRefGoogle Scholar
  6. 6.
    Hirakura Y, Azimov R, Azimova R et al. Polyglutamine-induced ion channels: a possible mechanism for the neurotoxicity of huntington and other CAG repeat diseases. J Neurosci Res, 2000; 60:490–494.PubMedCrossRefGoogle Scholar
  7. 7.
    Hirakura Y, Azimov R, Azimova R et al. Ion channels with different selectivity formed by transthyretin. Biophys J 2001; 80:120a.Google Scholar
  8. 8.
    Azimova RK, Kagan BL. Ion channels formed by a fragment of alpha-synucleain (NAC) in lipid membranes. Biophs J 2003; 84:53a.Google Scholar
  9. 9.
    Hirakura Y, Carreras I, Sipe JD et al. Channel formation by serum amyloid A: a potential mechanism for amyloid pathogenesis and host defense. Amyloid 2002; 9:13–23.PubMedGoogle Scholar
  10. 10.
    Stipani V, Galluci E, Micelli S et al. Channel formation by salmon and human calcitonin in black lipid membranes. Biophys J 2001; 81:3332–3338.PubMedCrossRefGoogle Scholar
  11. 11.
    Malisauskas M, Zamotin V, Jass J et al. Amyloid protofilaments from the calcium-binding protein equine lysozyme: formation of ring and linear structures depends on pH and metal ion concentration. J Mol Biol 2003; 330:879–890.PubMedCrossRefGoogle Scholar
  12. 12.
    Bahadi R, Farrelly PV, Kenna BL et al. Channels formed with a mutant prion protein PrP(82-–146) homologous to a 7-kDa fragment in diseased brain of GSS patients. Am J Physiol Cell Physiol 2003; 285:C862–872.Google Scholar
  13. 13.
    Quist A, Doudevski J, Lin H et al. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc Natl Acad Sci USA 2005; 102:10427–10432.PubMedCrossRefGoogle Scholar
  14. 14.
    Pieri L, Bucciantini M, Guasti P et al. Synthetic lipid vesicles recruit native-like aggregates and affect the aggregation process of the prion Ure2p: Insights on vesicle permeabilization and charge selectivity. Biophys J 2009; 96:3319–3330.PubMedCrossRefGoogle Scholar
  15. 15.
    Canale C, Torrassa S, Rispoli P et al. A. Natively folded HypF-N and its early amyloid aggregates interact with phospholipid monolayers and destabilize supported phospholipid bilayers. Biophys J 2006; 91:4575–4588.PubMedCrossRefGoogle Scholar
  16. 16.
    Ceru S, Kokalj SJ, Rabzelj S et al. Size and morphology of toxic oligomers of amyloidogenic proteins: a case study of human stefin B. Amyloid 2008; 15:147–159.PubMedCrossRefGoogle Scholar
  17. 17.
    Hawkins PN, Richardson S, MacSweeney JE et al. Scintigraphic quantification and serial monitoring of human visceral amyloid deposits provide evidence for turnover and regression. Q J Med 1993; 86:365–374.PubMedGoogle Scholar
  18. 18.
    Hardy J, Alsop D. Amyloid deposition as the central event in the etiology of Alzheimer’s disease. Trends Pharmacol 1991; 12:383–388.CrossRefGoogle Scholar
  19. 19.
    Samaia HB, Mari JJ, Vallada HP et al. A prion-linked psychiatric disorder. Nature 1997; 20; 390:241.Google Scholar
  20. 20.
    Forloni G, Angeretti N, Chiesa R et al. Neurotoxicity of a prion fragment. Nature 1993; 362:543–546.PubMedCrossRefGoogle Scholar
  21. 21.
    Lorenzo A, Razzaboni B, Weir GC et al. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 1994; 368:756–760.PubMedCrossRefGoogle Scholar
  22. 22.
    Pike CJ, Burdick D, Walencewicz AJ et al. Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 1993; 13:1676–1687.PubMedGoogle Scholar
  23. 23.
    Harper JD, Lansbury PT. Models of amyloid seeding in Alzheimer’s disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Ann Rev of Biochem 1997; 66:385–407.CrossRefGoogle Scholar
  24. 24.
    Hirakura Y, Satoh Y, Hirashima N et al. Membrane perturbation by the neurotoxic Alzheimer amyloid fragment beta 25-35 requires aggregation and beta-sheet formation. Biochem Mol Biol Int 1998; 46:787–794.PubMedGoogle Scholar
  25. 25.
    Lesne S, Koh MT, Kotilinek L et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006; 440:352–357.PubMedCrossRefGoogle Scholar
  26. 26.
    Walsh DM, Klyubin I, Fadeeva JV et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002; 416:535–539.PubMedCrossRefGoogle Scholar
  27. 27.
    Lin H, Bhatia R et al. Amyloid beta protein forms ion channels: implications for Alzheimer’s disease pathophysiology. Faseb J 2001; 15:2433–2444.PubMedCrossRefGoogle Scholar
  28. 28.
    Janson J, Ashley RH, Harrison D et al The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles. Diabetes 1999; 48:491–498.PubMedCrossRefGoogle Scholar
  29. 29.
    Lashuel HA, Petre BM, Wall J et al. Alpha-synuclein, especially the Parkinson’s disease-associated mutants, forms pore-like annular and tubular protofibrils. J Mol Biol 2002; 322:1089–1102.PubMedCrossRefGoogle Scholar
  30. 30.
    Kayed R, Head E, Thompson JL et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003; 300:486–489.PubMedCrossRefGoogle Scholar
  31. 31.
    Kagan BL, Azimov R, Azimova R. Amyloid peptide channels. J Membr Biol 2004; 202:1–10.PubMedCrossRefGoogle Scholar
  32. 32.
    Capone R, Garcia-Quinn F, Prangkio R et al. Amyloid beta ion channels in artificial lipid bilayer and neuronal cells. Neurotoxicity Res 2009 (in press).Google Scholar
  33. 33.
    Fernandez A, Berry RS. Proteins with H-bond packing defects are highly interactive with lipid bilayers: Implications for amyloidogenesis. Proc Natl Acad Sci USA 2003; 100:2391–2396.PubMedCrossRefGoogle Scholar
  34. 34.
    Stefani M, Dobson CM. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med 2003; 81:678–699.PubMedCrossRefGoogle Scholar
  35. 35.
    McLaurin J, Chakrabartty A. Characterization of the interactions of Alzheimer beta-amyloid peptides with phospholipid membranes. Eur J Biochem 1997; 245:355–363.PubMedCrossRefGoogle Scholar
  36. 36.
    Wong PT, Schauerte JA, Wisser KC et al. Amyloid-beta membrane binding and permeabilization are distinct processes influenced separately by membrane charge and fluidity. J Mol Biol 2009; 386:81–96.PubMedCrossRefGoogle Scholar
  37. 37.
    Hirakura Y, Lin MC, Kagan BL. Alzheimer amyloid abeta1-42 channels: effects of solvent, pH and Congo Red. J Neurosci Res 1999; 57:458–466.PubMedCrossRefGoogle Scholar
  38. 38.
    Terzi E, Holzamann G, Seelig J. Interaction of Alzheimer beta-amyloid peptide (1–40) with lipid membranes. J Mol Biochem 1997; 36:14845–14852.Google Scholar
  39. 39.
    Boqvist M, Lindstrom F, Watts A et al. Two types of Alzheimer’s beta-amyloid (1–40) peptide membrane interaction aggregation preventing transmembrane anchoring versus accelerated fibril formation. J Mol Biol 2004; 335:1039–1049.CrossRefGoogle Scholar
  40. 40.
    Alarcon JM, Brito JA, Hermosilla T et al. Ion channel formation by Alzheimer’s disease amyloid beta-peptide (Abeta40) in unilameilar liposomes is determined by amionic phospholipds. Peptides 2006; 27:365–363.CrossRefGoogle Scholar
  41. 41.
    Hertel C, Terzi E et al. Inhibition of the electrostatic interaction between beta-amyloid peptide and membranes prevents beta-amyloid-induced toxicity. Proc Natl Acad Sci USA 1997; 94:9412–9416.PubMedCrossRefGoogle Scholar
  42. 42.
    Lau TL, Ambroggio EE et al. Amyloid-beta peptide disruption of lipid membranes and the effect of metal ions. J Mol Biol 2006; 356:759–770.PubMedCrossRefGoogle Scholar
  43. 43.
    Durell SR, Guy HR, Arispe N et al. Theoretical models of the ion channel structure of amyloid beta-protein. Biophy J 1994; 67:2137–2145.CrossRefGoogle Scholar
  44. 44.
    Jang H, Ma B, Lal R et al. Models of toxic beta-sheet channels of protegrin-1 suggest a common subunit organization motif shared with toxic Alzheimer beta-amyloid ion channels. Biophys J 2008; 95:4631–4642.PubMedCrossRefGoogle Scholar
  45. 45.
    Lee G, Pollard HB, Arispe N. Annexin 5 and apolipoprotein against Alzheimer’s amyloid beta-peptide cytoxicity by competitive inhibition of a common phosphatadylserine receptor site. Peptides 2002; 23:1249–1263.PubMedCrossRefGoogle Scholar
  46. 46.
    Kakio A, Nishimoto S, Yanagisawa K et al. Interactions of amyloid beta-protein with various gangliosides in raft-like membranes: importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid. Biochemistry 2002; 41:7385–7390.PubMedCrossRefGoogle Scholar
  47. 47.
    Yanagisawa K. Role of gangliosides in Alzheimer’s disease. Biochim Biophys Acta 2007; 1768:1943–1951.PubMedCrossRefGoogle Scholar
  48. 48.
    Yanagisawa K, Odaka A, Suzuki N et al. GM1 ganglioside-bound amyloid beta-protein (A-beta): a possible form of preamyloid in Alzheimer’s disease. Nat Med 1995; 1:1062–1066.PubMedCrossRefGoogle Scholar
  49. 49.
    Arispe N, Doh M. Plasma membrane cholesterol controls the cytotoxicity of Alzheimer’s disease AbetaP (1–40) and (1–42) peptides. FASEB J 2002; 16:1526–1536.PubMedCrossRefGoogle Scholar
  50. 50.
    Westermark P, Wilander E. The influence of amyloid deposits on the islet volume in maturity onset diabetes mellitus. Diabetologia 1978; 15:417–421.PubMedCrossRefGoogle Scholar
  51. 51.
    Mirzabekov TA, Lin MC, Kagan BL. Pore formation by the cytotoxic islet amyloid peptide amylin. J Biol Chem 1996; 271:1988–1992.PubMedCrossRefGoogle Scholar
  52. 52.
    Sakagashira S, Hiddinga HJ, Tateishi K et al. S20G mutant amylin exhibits increased in vitro amyloidogenicity and increased intracellular cytotoxicity compared to wild-type-amylin. Am J Pathol 2000; 157:2101–2109.PubMedGoogle Scholar
  53. 53.
    Jayasinghe SA, Langen R. Membrane interaction of islet amyloid polypeptide. Biochim Biophys Acta 2007; 1768:2002–2009.PubMedCrossRefGoogle Scholar
  54. 54.
    Knight JD, Miranker AD. Phospholipid catalysis of diabetic amyloid assembly. J Mol Biol 2004; 341:1175–1187.PubMedCrossRefGoogle Scholar
  55. 55.
    Knight JD, Hebda JA, Miranker AD. Conserved and cooperative assembly of membrane-bound alpha-helical states of islet amyloid polypeptide. Biochem 2006; 45:9496–9508.CrossRefGoogle Scholar
  56. 56.
    Jayasinghe SA, Langen R. Lipid membranes modulate the structure of islet amyloid polypeptide. Biochemistry 2005; 45:12113–12119.CrossRefGoogle Scholar
  57. 57.
    Sparr F, Engel MF, Sakharov DV et al. Islet amyloid polypeptide-induced membrane leakage involves uptake of lipids by forming amyloid fibers. FEBS Lett 2004; 577:117–120.PubMedCrossRefGoogle Scholar
  58. 58.
    Kayed J, Bernhagen N, Greenfield K et al. Conformational transmissions of islet amyloid polypeptide. (IAPP) in amyloid formation in vitro. J Mol Biol 1999; 287:781–796.PubMedCrossRefGoogle Scholar
  59. 59.
    DeArmond SJ, Prusiner SB. Perspectives on prion biology, prion disease pathogenesis and pharmacologic approaches to treatment. Clin Lab Med 2003; 23:1–41.PubMedCrossRefGoogle Scholar
  60. 60.
    Lin MC, Mirzebekov T, Kagan BL. Channel formation by a neurotoxic prion protein fragment. J Biol Chem 1997; 272:44–47.PubMedCrossRefGoogle Scholar
  61. 61.
    Pan KM, Baldwin M, Nguyen J et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 1993; 90:10962–10966.PubMedCrossRefGoogle Scholar
  62. 62.
    Kazlauskaite J, Sanghera N, Sylvester I et al. Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 2003; 42:3295–3304.PubMedCrossRefGoogle Scholar
  63. 63.
    Bahadi R, Farrelly PV, Kenna BL et al. Channels formed with a mutant prion protein PrP(82-–146) homologous to a 7-kDa fragment in diseased brain of GSS patients. Am J Physiol Cell Physiol 2003b; 285:C862–872.Google Scholar
  64. 64.
    Volles MJ, Lansbury PT. Vesicle permeabilization by protofibrillar AS is sensitive to Parkinson’s disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 2002; 41:4595–4602.PubMedCrossRefGoogle Scholar
  65. 65.
    Zakharov SD, Hulleman JD, Dutseva EA et al. Helical alpha-synuclein forms highly conductive ion channels. Biochemistry 2007; 46:14369–14379.PubMedCrossRefGoogle Scholar
  66. 66.
    Arispe N. Architecture of the Alzheimers Aß P ion channel pore. J Membrane Biol 2004; 197:33–48.CrossRefGoogle Scholar
  67. 67.
    Schutz GE. The structure of bacteria: outer membrane proteins. Biochim Biophys Acta 2002; 1565:308–317.CrossRefGoogle Scholar
  68. 68.
    Benz R, Schmid A, Hancock RW. Ion selectivity of gram-negative bacterial porins. J Bacteriol 1983; 153:241–252.Google Scholar
  69. 69.
    Hill K, Model K, Ryan MT et al. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 1998; 395:516–521.PubMedCrossRefGoogle Scholar
  70. 70.
    Schleiff E, Soll J, Kuchler M et al. Characterization of the translocon of the outer envelope of choloroplasts. J Cell Biol 2003; 160:541–551.PubMedCrossRefGoogle Scholar
  71. 71.
    Wimley WC. The versatile β-barrel membrane protein. Curr Opin Struct Biol 2003; 13:404–411.PubMedCrossRefGoogle Scholar
  72. 72.
    Song L, Hobaugh MR, Shustak C et al. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 1996; 274:1859–1866.PubMedCrossRefGoogle Scholar
  73. 73.
    Sekiya K, Satoh R, Danbara H et al. A ring-shaped structure with a crown formed by streptolysin O on the erythrocyte membrane. J Bacteriol 1993; 175:5953–5961.PubMedGoogle Scholar
  74. 74.
    Olofsson A, Hebert, Thiestam M. The projection structure of perfringolysin O (Clostridium perfringens theta-toxin). FEBS Lett 1993; 319:125–127.PubMedCrossRefGoogle Scholar
  75. 75.
    Sharpe JC, London E. Diptheria toxin forms pores of different sizes depending on its concentration in membranes: probable relationionship to oligomerization. J Membr Biol 1999; 171:209–221.PubMedCrossRefGoogle Scholar
  76. 76.
    Tadjibaeva G, Sabirov R, Tomita T. Flammutoxin, a cytolysin from the edible mushroom Flammulina velutipes, forms two different types of voltage-gated channels in lipid bilayer membranes. Biochem Biophys Acta 2000; 1467:431–443.PubMedCrossRefGoogle Scholar
  77. 77.
    Cabiaux V, Wolff C, Ruysschaert JM. Interaction with a lipid membrane: a key step in bacterial toxins virulence. Int J Biol Macromol 1997; 21:285–298.PubMedCrossRefGoogle Scholar
  78. 78.
    Thundimadathil J, Roeske RW, Guo L. A synthetic peptide forms voltage-gated porin-like ion channels in lipid bilayer membranes. Biochem Biophys Res Commun 2005; 330:585–590.PubMedCrossRefGoogle Scholar
  79. 79.
    Conlan S, Zhang Y et al. Biochemical and biophysical characterization of OmpG: A monomeric porin Biochemistry 2000; 39:11845–11854.PubMedCrossRefGoogle Scholar
  80. 80.
    Bainbridge G, Gokce I, Lakey JH. Voltage gating is a fundamental feature of porin and toxin β-barrel membrane channels. FEBS Lett 1998; 431:305–308.PubMedCrossRefGoogle Scholar
  81. 81.
    Berrier C, Coulombe A et al. Fast and slow kinetics of porin channels from Escherichia coli reconstituted into giant liposomes and studied by patch-clamp. FEBS Lett 1992; 306:251–256.PubMedCrossRefGoogle Scholar
  82. 82.
    Valeva A, Weisser A, Walker B et al. Molecular architecture of a toxin pore: a 15-residue sequence lines the transmembrane channel of staphylococcal alpha-toxin. EMBO J 1996; 15:1857–1864.PubMedGoogle Scholar
  83. 83.
    Thundimadathil J, Roeske RW et al. Aggregation and porin-like channel activity of a β-sheet peptide. Biochemistry 2005; 44:10259–10270.PubMedCrossRefGoogle Scholar
  84. 84.
    Thundimadathil J, Roeske RW et al. Effect of membrane mimicking environment on the conformation of a pore forming (xSxG)6 peptide, Biopolymers. Peptide Science 2006; 84:317–328.PubMedGoogle Scholar
  85. 85.
    Mirzabekov T, Lin MC, Yuan WL et al. Channel formation in planar lipid bilayers by a neurotoxic fragment of the beta-amyloid peptide. Biochem Biophys Research Commun 1994; 202:1142–1148.CrossRefGoogle Scholar
  86. 86.
    Lin MC, Kagan, BL. Electrophysiologic properties of channels induced by Abeta 25–26 in planar lipid bilayers. Peptides 2002; 23:1215–1228.PubMedCrossRefGoogle Scholar
  87. 87.
    Arispe N, Rojas E, Pollard HB. Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc Natl Acad Sci USA 1993; 90:567–571.PubMedCrossRefGoogle Scholar
  88. 88.
    Arispe N, Pollard HB, Rojas E. Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein (Abeta P(1-40)) in bilayer membraines. Proc Natl Acad Sci USA 1993; 90:10573–10577.PubMedCrossRefGoogle Scholar
  89. 89.
    Lashuel HA, Hartley DM, Petre BM et al. Mixtures of wild-type and a pathogenic (E22G) form of Abeta40 in vitro accumulate protofibrils, including amyloid pores. J Mol Biol 2003; 332:795–808.PubMedCrossRefGoogle Scholar
  90. 90.
    Kim HJ, Suh YH, Lee MH et al. Cation selective channels formed by a C-terminal fragment of beta-amyloid precursor protein. Neuroreport 1999; 10:1427–1431.PubMedCrossRefGoogle Scholar
  91. 91.
    Kourie JI, Culverson A. Prion peptide fragment PrP(106–126) forms distinct cation channel types. Neurosci Res 2000; 62:120–133.CrossRefGoogle Scholar
  92. 92.
    Wang L, Lashuel HA, Walz T et al. Murine apolipoprotein serum amyloid A in solution forms a hexamer containing a central channel. Proc Natl Acad Sci USA 2002; 99:15947–15952.PubMedCrossRefGoogle Scholar
  93. 93.
    Kourie JI. Characterization of a C-type natriuretic peptide (CNP-39)-formed cation-selective channel from platypus (Omithorhynchus anatinus) venom. J Physiol 1999; 518:359–369.PubMedCrossRefGoogle Scholar
  94. 94.
    Kourie JI. Synthetic mammalian C-type natriuretic peptide forms large cation channels. FEBS Lett 1999; 445:57–62.PubMedCrossRefGoogle Scholar
  95. 95.
    Monoi H, Futaki S, Kugimiya S et al. Poly-L-glutamine forms cation channels: relevance to the pathogenesis of the polyglutamine diseases. Biophys J 2000; 78:2892–2894.PubMedCrossRefGoogle Scholar
  96. 96.
    Ibrahim HR, Thomas U, Pellegrini A. A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action. J Biol Chem 2002; 276:43767–43774.CrossRefGoogle Scholar
  97. 97.
    Chung J, Yang H, de Beus MD et al. Cu/Zn superoxide dismutase can form pore-like structures. Biochem Biophys Res Commun 2003; 312:873–876.PubMedCrossRefGoogle Scholar

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© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine at UCLAUniversity of CaliforniaLos AngelesUSA
  2. 2.Peptisyntha, Inc.TorranceUSA

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