β-Barrel Topology of Alzheimer's β-Amyloid Ion Channels

Journal of Molecular Biology

Volumn 404, Issue 5, 2010, Pages 917-934

  Jang, Hyunbum ^a   Arce, Fernando Teran ^b,c   Ramachandran, Srinivasan ^b,c   Capone, Ricardo ^b,c   Lal, Ratnesh ^b,c   Nussinov, Ruth ^a,d  

^a SAIC FREDERICK INC   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

Atomic force microscopy; Molecular dynamics simulations; Toxic amyloid ion channels; U shaped motif; barrel

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; HYBRID PROTEIN; ION CHANNEL; MONOMER; OLIGOMER; PROTEIN SUBUNIT;

ALZHEIMER DISEASE; ARTICLE; ATOMIC FORCE MICROSCOPY; BETA BARREL; BETA SHEET; BETA TURN; BINDING SITE; CELL MEMBRANE; ION PERMEABILITY; LIPID BILAYER; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE;

EID: 78649529340     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.10.025     Document Type: Article

References (92)

1. Wimley W.C. The versatile β-barrel membrane protein. Curr. Opin. Struct. Biol. 2003, 13:404-411.
2. Schulz G.E. The structure of bacterial outer membrane proteins. Biochim. Biophys. Acta 2002, 1565:308-317.
3. Benz R., Schmid A., Hancock R.E. Ion selectivity of Gram-negative bacterial porins. J. Bacteriol. 1985, 162:722-727.
4. Jap B.K., Walian P.J. Biophysics of the structure and function of porins. Q. Rev. Biophys. 1990, 23:367-403.
5. Murzin A.G., Lesk A.M., Chothia C. Principles determining the structure of beta-sheet barrels in proteins: I. A theoretical analysis. J. Mol. Biol. 1994, 236:1369-1381.
6. Murzin A.G., Lesk A.M., Chothia C. Principles determining the structure of beta-sheet barrels in proteins: II. The observed structures. J. Mol. Biol. 1994, 236:1382-1400.
7. McLachlan A.D. Gene duplications in the structural evolution of chymotrypsin. J. Mol. Biol. 1979, 128:49-79.
8. Thinnes F.P., Gotz H., Kayser H., Benz R., Schmidt W.E., Kratzin H.D., Hilschmann N. Identification of human porins: I. Purification of a porin from human B-lymphocytes (Porin 31HL) and the topochemical proof of its expression on the plasmalemma of the progenitor cell. Biol. Chem. Hoppe Seyler 1989, 370:1253-1264.
9. Bay D.C., Court D.A. Origami in the outer membrane: the transmembrane arrangement of mitochondrial porins. Biochem. Cell Biol. 2002, 80:551-562.
10. Casadio R., Jacoboni I., Messina A., De Pinto V. A 3D model of the voltage-dependent anion channel (VDAC). FEBS Lett. 2002, 520:1-7.
11. Shulga N., Wilson-Smith R., Pastorino J.G. Hexokinase II detachment from the mitochondria potentiates cisplatin induced cytotoxicity through a caspase-2 dependent mechanism. Cell Cycle 2009, 8:3355-3364.
12. Abu-Hamad S., Arbel N., Calo D., Arzoine L., Israelson A., Keinan N., et al. The VDAC1 N-terminus is essential both for apoptosis and the protective effect of anti-apoptotic proteins. J. Cell Sci. 2009, 122:1906-1916.
13. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 2002, 416:507-511.
14. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., et al. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
15. Cheng I.H., Scearce-Levie K., Legleiter J., Palop J.J., Gerstein H., Bien-Ly N., et al. Accelerating amyloid-β fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J. Biol. Chem. 2007, 282:23818-23828.
16. Arispe N., Pollard H.B., Rojas E. Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [AβP-(1-40)] in bilayer membranes. Proc. Natl Acad. Sci. USA 1993, 90:10573-10577.
17. Arispe N., Rojas E., Pollard H.B. Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl Acad. Sci. USA 1993, 90:567-571.
18. Arispe N., Pollard H.B., Rojas E. β-Amyloid Ca(2+)-channel hypothesis for neuronal death in Alzheimer disease. Mol. Cell. Biochem. 1994, 140:119-125.
19. 2+ interaction with Alzheimer amyloid β protein calcium channels. Proc. Natl Acad. Sci. USA 1996, 93:1710-1715.
20. Bhatia R., Lin H., Lal R. Fresh and globular amyloid β protein (1-42) induces rapid cellular degeneration: evidence for AβP channel-mediated cellular toxicity. FASEB J. 2000, 14:1233-1243.
21. 1-42 channels: effects of solvent, pH, and Congo red. J. Neurosci. Res. 1999, 57:458-466.
22. Hirakura Y., Yiu W.W., Yamamoto A., Kagan B.L. Amyloid peptide channels: blockade by zinc and inhibition by Congo red (amyloid channel block). Amyloid 2000, 7:194-199.
23. Jang H., Zheng J., Lal R., Nussinov R. New structures help the modeling of toxic amyloidβ ion channels. Trends Biochem. Sci. 2008, 33:91-100.
24. Kawahara M., Arispe N., Kuroda Y., Rojas E. Alzheimer's disease amyloid β-protein forms Zn(2+)-sensitive, cation-selective channels across excised membrane patches from hypothalamic neurons. Biophys. J. 1997, 73:67-75.
25. Lal R., Lin H., Quist A.P. Amyloid beta ion channel: 3D structure and relevance to amyloid channel paradigm. Biochim. Biophys. Acta 2007, 1768:1966-1975.
26. Lin H., Bhatia R., Lal R. Amyloid β protein forms ion channels: implications for Alzheimer's disease pathophysiology. FASEB J. 2001, 15:2433-2444.
27. 2+-sensitive channel in reconstituted lipid vesicles. Biochemistry 1999, 38:11189-11196.
28. 25-35 in planar lipid bilayers. Peptides 2002, 23:1215-1228.
29. Quist A., Doudevski I., Lin H., Azimova R., Ng D., Frangione B., et al. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl Acad. Sci. USA 2005, 102:10427-10432.
30. 2+-sensitive channel. J. Biol. Chem. 1998, 273:13379-13382.
31. Zhu Y.J., Lin H., Lal R. Fresh and nonfibrillar amyloid β protein(1-40) induces rapid cellular degeneration in aged human fibroblasts: evidence for AβP-channel-mediated cellular toxicity. FASEB J. 2000, 14:1244-1254.
32. Diaz J.C., Simakova O., Jacobson K.A., Arispe N., Pollard H.B. Small molecule blockers of the Alzheimer Abeta calcium channel potently protect neurons from Abeta cytotoxicity. Proc. Natl Acad. Sci. USA 2009, 106:3348-3353.
33. Kayed R., Pensalfini A., Margol L., Sokolov Y., Sarsoza F., Head E., et al. Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer. J. Biol. Chem. 2009, 284:4230-4237.
34. Capone R., Garcia Quiroz F., Prangkio P., Sauer A.M., Bautista M.R., Turner R.S., et al. Amyloid-β-induced ion flux in artificial lipid bilayers and neuronal cells: resolving a controversy. Neurotox. Res. 2009, 16:1-13.
35. Mobley D.L., Cox D.L., Singh R.R., Maddox M.W., Longo M.L. Modeling amyloid β-peptide insertion into lipid bilayers. Biophys. J. 2004, 86:3585-3597.
36. Durell S.R., Guy H.R., Arispe N., Rojas E., Pollard H.B. Theoretical models of the ion channel structure of amyloid β-protein. Biophys. J. 1994, 67:2137-2145.
37. Chimon S., Ishii Y. Capturing intermediate structures of Alzheimer's β-amyloid, Aβ(1-40), by solid-state NMR spectroscopy. J. Am. Chem. Soc. 2005, 127:13472-13473.
38. Singer S.J., Dewji N.N. Evidence that Perutz's double-beta-stranded subunit structure for beta-amyloids also applies to their channel-forming structures in membranes. Proc. Natl Acad. Sci. USA 2006, 103:1546-1550.
39. Luhrs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Dobeli H., et al. 3D structure of Alzheimer's amyloid-β(1-42) fibrils. Proc. Natl Acad. Sci. USA 2005, 102:17342-17347.
40. Petkova A.T., Yau W.M., Tycko R. Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry 2006, 45:498-512.
41. 2-microglobulin fragment probed by solid-state NMR. Proc. Natl Acad. Sci. USA 2006, 103:18119-18124.
42. Ferguson N., Becker J., Tidow H., Tremmel S., Sharpe T.D., Krause G., et al. General structural motifs of amyloid protofilaments. Proc. Natl Acad. Sci. USA 2006, 103:16248-16253.
43. de Planque M.R., Raussens V., Contera S.A., Rijkers D.T., Liskamp R.M., Ruysschaert J.M., et al. β-Sheet structured β-amyloid(1-40) perturbs phosphatidylcholine model membranes. J. Mol. Biol. 2007, 368:982-997.
44. Lau T.L., Ambroggio E.E., Tew D.J., Cappai R., Masters C.L., Fidelio G.D., et al. Amyloid-β peptide disruption of lipid membranes and the effect of metal ions. J. Mol. Biol. 2006, 356:759-770.
45. Kagan B.L. Amyloidosis and protein folding. Science 2005, 307:42-43. author reply, 42-43.
46. Petosa C., Collier R.J., Klimpel K.R., Leppla S.H., Liddington R.C. Crystal structure of the anthrax toxin protective antigen. Nature 1997, 385:833-838.
47. Jang H., Zheng J., Nussinov R. Models of β-amyloid ion-channels in the membrane suggest that channel formation in the bilayer is a dynamic process. Biophys. J. 2007, 93:1938-1949.
48. Jang H., Arce F.T., Capone R., Ramachandran S., Lal R., Nussinov R. Misfolded amyloid ion channels present mobile β-sheet subunits in contrast to conventional ion channels. Biophys. J. 2009, 97:3029-3037.
49. Jang H., Arce F.T., Ramachandran S., Capone R., Azimova R., Kagan B.L., et al. Truncated β-amyloid peptide channels provide an alternative mechanism for Alzheimer's disease and Down syndrome. Proc. Natl Acad. Sci. USA 2010, 107:6538-6543.
50. Jang H., Arce F.T., Ramachandran S., Capone R., Lal R., Nussinov R. Structural convergence among diverse toxic β-sheet ion channels. J. Phys. Chem. B 2010, 114:9445-9451.
51. Motte J., Williams R.S. Age-related changes in the density and morphology of plaques and neurofibrillary tangles in Down syndrome brain. Acta Neuropathol. 1989, 77:535-546.
52. 17-42 peptide, a component of diffuse amyloid deposits of Alzheimer disease. J. Biol. Chem. 1994, 269:10987-10990.
53. Higgins L.S., Murphy G.M., Forno L.S., Catalano R., Cordell B. p3 β-amyloid peptide has a unique and potentially pathogenic immunohistochemical profile in Alzheimer's disease brain. Am. J. Pathol. 1996, 149:585-596.
54. 1-42 deposits do not lead to Alzheimer's neuritic plaques in aged dogs. Biochem. J. 1996, 313:575-580.
55. 17-42) is a major constituent of Down's syndrome cerebellar preamyloid. J. Biol. Chem. 1996, 271:33623-33631.
56. 17-42 in Alzheimer's disease activates JNK and caspase-8 leading to neuronal apoptosis. Brain 2002, 125:2036-2043.
57. Szczepanik A.M., Rampe D., Ringheim G.E. Amyloid-β peptide fragments p3 and p4 induce pro-inflammatory cytokine and chemokine production in vitro and in vivo. J. Neurochem. 2001, 77:304-317.
58. Pike C.J., Overman M.J., Cotman C.W. Amino-terminal deletions enhance aggregation of β-amyloid peptides in vitro. J. Biol. Chem. 1995, 270:23895-23898.
59. 2-microglobulin forms ion channels: implication for dialysis related amyloidosis. J. Am. Chem. Soc. 2009, 131:14938-14945.
60. Jang H., Ma B., Nussinov R. Conformational study of the protegrin-1 (PG-1) dimer interaction with lipid bilayers and its effect. BMC Struct. Biol. 2007, 7:21.
61. Capone R., Mustata M., Jang H., Arce F.T., Nussinov R., Lal R. Antimicrobial protegrin-1 (PG-1) forms ion channels: MD simulation, AFM, and electrical conductance studies. Biophys. J. 2010, 98:2644-2652.
62. Sansom M.S., Kerr I.D. Transbilayer pores formed by beta-barrels: molecular modeling of pore structures and properties. Biophys. J. 1995, 69:1334-1343.
63. 17-42 (p3) oligomers: the importance of the turn location and its conformation. Biophys. J. 2009, 97:1168-1177.
64. Miller Y., Ma B., Nussinov R. Polymorphism in Alzheimer Aβ amyloid organization reflects conformational selection in a rugged energy landscape. Chem. Rev. 2010, 110:4820-4838.
65. Zheng J., Ma B., Nussinov R. Consensus features in amyloid fibrils: sheet-sheet recognition via a (polar or nonpolar) zipper structure. Phys. Biol. 2006, 3:P1-P4.
66. 17-42 fibril architecture: tight intermolecular sheet-sheet association and intramolecular hydrated cavities. Biophys. J. 2007, 93:3046-3057.
67. 2-Microglobulin amyloid fragment organization and morphology and its comparison to Aβ suggests that amyloid aggregation pathways are sequence specific. Biochemistry 2008, 47:2497-2509.
68. 10-35): sequence effects. Proc. Natl Acad. Sci. USA 2002, 99:14126-14131.
69. Lin M.C., Mirzabekov T., Kagan B.L. Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem. 1997, 272:44-47.
70. Hirakura Y., Azimov R., Azimova R., Kagan B.L. Polyglutamine-induced ion channels: a possible mechanism for the neurotoxicity of Huntington and other CAG repeat diseases. J. Neurosci. Res. 2000, 60:490-494.
71. 2-microglobulin: a mechanism for the pathogenesis of dialysis associated amyloidosis. Amyloid 2001, 8:94-100.
72. Cerf E., Sarroukh R., Tamamizu-Kato S., Breydo L., Derclaye S., Dufrene Y.F., et al. Antiparallel beta-sheet: a signature structure of the oligomeric amyloid beta-peptide. Biochem. J. 2009, 421:415-423.
73. McLaurin J., Chakrabartty A. Characterization of the interactions of Alzheimer beta-amyloid peptides with phospholipid membranes. Eur. J. Biochem. 1997, 245:355-363.
74. Shao H., Jao S., Ma K., Zagorski M.G. Solution structures of micelle-bound amyloid β-(1-40) and β-(1-42) peptides of Alzheimer's disease. J. Mol. Biol. 1999, 285:755-773.
75. Ege C., Lee K.Y. Insertion of Alzheimer's A beta 40 peptide into lipid monolayers. Biophys. J. 2004, 87:1732-1740.
76. Smart O.S., Goodfellow J.M., Wallace B.A. The pore dimensions of gramicidin A. Biophys. J. 1993, 65:2455-2460.
77. Frishman D., Argos P. Knowledge-based protein secondary structure assignment. Proteins 1995, 23:566-579.
78. Smart J.L., Marrone T.J., McCammon J.A. Conformational sampling with Poisson-Boltzmann forces and a stochastic dynamics/Monte Carlo method: application to alanine dipeptide. J. Comput. Chem. 1997, 18:1750-1759.
79. Jang H., Woolf T.B. Multiple pathways in conformational transitions of the alanine dipeptide: an application of dynamic importance sampling. J. Comput. Chem. 2006, 27:1136-1141.
80. Sipe J.D., Cohen A.S. Review: history of the amyloid fibril. J. Struct. Biol. 2000, 130:88-98.
81. Hegde R.S., Mastrianni J.A., Scott M.R., DeFea K.A., Tremblay P., Torchia M., et al. A transmembrane form of the prion protein in neurodegenerative disease. Science 1998, 279:827-834.
82. Soong R., Brender J.R., Macdonald P.M., Ramamoorthy A. Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. J. Am. Chem. Soc. 2009, 131:7079-7085.
83. Brender J.R., Hartman K., Nanga R.P., Popovych N., de la Salud Bea R., Vivekanandan S., et al. Role of zinc in human islet amyloid polypeptide aggregation. J. Am. Chem. Soc. 2009, 132:8973-8983.
84. Brender J.R., Lee E.L., Cavitt M.A., Gafni A., Steel D.G., Ramamoorthy A. 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. 2008, 130:6424-6429.
85. Jang H., Ma B., Lal R., Nussinov R. Models of toxic β-sheet channels of protegrin-1 suggest a common subunit organization motif shared with toxic Alzheimer β-amyloid ion channels. Biophys. J. 2008, 95:4631-4642.
86. Wong P.T., Schauerte J.A., Wisser K.C., Ding H., Lee E.L., Steel D.G., Gafni A. Amyloid-beta membrane binding and permeabilization are distinct processes influenced separately by membrane charge and fluidity. J. Mol. Biol. 2009, 386:81-96.
87. Chauhan A., Ray I., Chauhan V.P. Interaction of amyloid beta-protein with anionic phospholipids: possible involvement of Lys28 and C-terminus aliphatic amino acids. Neurochem. Res. 2000, 25:423-429.
88. Zhao H., Tuominen E.K., Kinnunen P.K. Formation of amyloid fibers triggered by phosphatidylserine-containing membranes. Biochemistry 2004, 43:10302-10307.
89. Maltseva E., Kerth A., Blume A., Mohwald H., Brezesinski G. Adsorption of amyloid beta (1-40) peptide at phospholipid monolayers. ChemBioChem 2005, 6:1817-1824.
90. Yoda M., Miura T., Takeuchi H. Non-electrostatic binding and self-association of amyloid beta-peptide on the surface of tightly packed phosphatidylcholine membranes. Biochem. Biophys. Res. Commun. 2008, 376:56-59.
91. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., Karplus M. CHARMM - a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4:187-217.
92. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26:1781-1802.