Amyloid-β and the failure to form mitochondrial cristae: A biomimetic study involving artificial membranes

Journal of Alzheimer's Disease

Volumn 28, Issue 1, 2012, Pages 33-48

  Khalifat, Nada ^a   Puff, Nicolas ^a,b   Dliaa, Mariam ^a   Angelova, Miglena I ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

Author keywords

Alzheimer's disease; biophysical phenomena; fluorescence polarization; lipid bilayers; liposomes; micromanipulation; mitochondria; pH gradient; videomicroscopy

Indexed keywords

AMYLOID BETA PROTEIN[1-42];

ALZHEIMER DISEASE; ARTICLE; ARTIFICIAL MEMBRANE; BIOMIMETICS; DEHYDRATION; FLUORESCENCE; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE FLUIDITY; MITOCHONDRION; PRIORITY JOURNAL;

EID: 84855787755     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-110389     Document Type: Article

References (66)

1. Mattson MP (2004) Pathways towards and away from Alzheimers disease. Nature 430, 631-639. (Pubitemid 39061671)
2. LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-β in Alzheimers disease. Nat Rev Neurosci 8, 499-509.
3. Wirths O, Multhaup G, Bayer TA (2004) A modified β-amyloid hypothesis: Intraneuronal accumulation of the β-amyloid peptide -the first step of a fatal cascade. J Neurochem 91, 513-520. (Pubitemid 39431147)
4. Swerdlow RH, Burns JM, Khan SM (2010) The Alzheimers disease mitochondrial cascade hypothesis. J Alzheimers Dis 20(Suppl 2), S265-S279.
5. Swerdlow RH, Khan SM (2004) A "mitochondrial cascade hypothesis" for sporadic Alzheimers disease. Med Hypotheses 63, 8-20. (Pubitemid 38887104)
6. Castellani R, Hirai K, Aliev G, Drew KL, Nunomura A, Takeda A, Cash AD, Obrenovich ME, Perry G, Smith MA (2002) Role of mitochondrial dysfunction in Alzheimers disease. J Neurosci Res 70, 357-360. (Pubitemid 35222373)
7. Manczak M, Anekonda TS, Henson E, Park BS, Quinn J, Reddy PH (2006) Mitochondria are a direct site of Ab accumulation in Alzheimers disease neurons: Implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 15, 1437-1449.
8. Reddy PH, Beal MF (2008) Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimers disease. Trends Mol Med 14, 45-53.
9. Caspersen C, Wang N, Yao J, Sosunov A, Chen X, Lustbader JW, Xu HW, Stern D, McKhann G, Yan SD (2005) Mitochondrial Aβ: A potential focal point for neuronal metabolic dysfunction in Alzheimers disease. FASEB J 19, 2040-2041. (Pubitemid 41759758)
10. Chen JX, Yan SS (2010) Role of mitochondrial amyloid-beta in Alzheimers disease. J Alzheimers Dis 20(Suppl 2), 569-578.
11. Chen JX, Yan SD (2007) Amyloid-beta-induced mitochondrial dysfunction. J Alzheimers Dis 12, 177-184.
12. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimers disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
13. Hansson Petersen CA, Alikhani N, Behbahani H, Wiehager B, Pavlov PF, Alafuzoff I, Leinonen V, Ito A, Winblad B, Glaser E, Ankarcrona M (2008) The amyloid β-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc Natl Acad Sci U S A 105, 13145-13150.
14. Yamaguchi H, Yamazaki T, Ishiguro K, Shoji M, Nakazato Y, Hirai S (1992) Ultrastructural localization of Alzheimer amyloid beta/A4 protein precursor in the cytoplasm of neurons and senile plaque-associated astrocytes. Acta Neuropathol 85, 15-22.
15. Hirai K, Aliev G, Nunomura A, Fujioka H, Russell RL, Atwood CS, Johnson AB, Kress Y, Vinters HV, Tabaton M, Shimohama S, Cash AD, Siedlak SL, Harris PLR, Jones PK, Petersen RB, Perry G, SmithMA(2001) Mitochondrial abnormalities in Alzheimers disease. J Neurosci 21, 3017-3023.
16. Baloyannis SJ, Costa V, Michmizos D (2004) Mitochondrial alterations in Alzheimers disease.AmJ Alzheimers Dis Other Demen 19, 89-93.
17. Baloyannis SJ (2006) Mitochondrial alterations in Alzheimers disease. J Alzheimers Dis 9, 119-126.
18. Trimmer PA, Swerdlow RH, Parks JK, Keeney P, Bennett JP, Miller SW, Davis RE, ParkerWD(2000) Abnormal mitochondrial morphology in sporadic Parkinsons and Alzheimers disease cybrid cell lines. Exp Neurol 162, 37-50. (Pubitemid 30170099)
19. Sayre LM, Perry G, Smith MA (2008) Oxidative stress and neurotoxicity. Chem Res Toxicol 21, 172-188. (Pubitemid 351219718)
20. Lea PJ, Temkin RJ, Freeman KB, Mitchell GA, Robinson BH (1994) Variations in mitochondrial ultrastructure and dynamics observed by high resolution scanning electron microscopy (HRSEM). Microsc Res Tech 27, 269-277. (Pubitemid 24073422)
21. Logan DC (2006) The mitochondrial compartment. J Exp Bot 57, 1225-1243.
22. Mannella CA, Marko M, Penczek P, Barnard D, Frank J (1994) The internal compartmentation of rat-liver mitochondria: Tomographic study using the high-voltage transmission electron microscope. Microsc Res Tech 27, 278-283. (Pubitemid 24073423)
23. Mannella CA, Pfeiffer DR, Bradshaw PC, Moraru II, Slepchenko B, Loew LM, Hsieh CE, Buttle K, Marko M (2001) Topology of the mitochondrial inner membrane: Dynamics and bioenergetic implications. IUBMB Life 52, 93-100. (Pubitemid 33731561)
24. Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 1762, 140-147. (Pubitemid 43006021)
25. MannellaCA(2006) Structure and dynamics of the mitochondrial inner membrane cristae. Biochim Biophys Acta 1763, 542-548. (Pubitemid 44015951)
26. Khalifat N, Puff N, Bonneau S, Fournier JB, Angelova MI (2008) Membrane deformation under local pH gradient: Mimicking mitochondrial cristae dynamics. Biophys J 95, 4924-4933.
27. Fournier JB, Khalifat N, Puff N, Angelova MI (2009) Chemically triggered ejection of membrane tubules controlled by intermonolayer friction. Phys Rev Let 102, 018102.
28. Angelova MI, Dimitrov DS (1986) Liposome electroformation. Faraday Discuss. Chem Soc 81, 303-311 discussion 345-349.
29. Angelova MI, Dimitrov DS (1988) A mechanism of liposome electroformation. Prog Colloid Polym Sci 76, 59-67.
30. Angelova MI, Soĺeau S, Ḿeĺeard P, Faucon J-F, Bothorel P (1992)AC field controlled formation of giant fluctuating vesicles and bending elasticity measurements. Springer Proc Phys 66, 178-182.
31. MacDonald RC, MacDonald RI, Menco BPM, Takeshita K, Subbarao NK, Hu L-r (1991) Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim Biophys Acta 1061, 297-303.
32. Krasnowska EK, Gratton E, Parasassi T (1998) Prodan as a membrane surface fluorescence probe: Partitioning between water and phospholipid phases. Biophys J 74, 1984-1993. (Pubitemid 28157933)
33. Parasassi T, Krasnowska EK, Bagatolli L, Gratton E (1998) Laurdan and prodan as polarity-sensitive fluorescent membrane probes. J Fluoresc 08, 365-373. (Pubitemid 128545086)
34. Lentz BR (1993) Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem Phys Lip 64, 99-116. (Pubitemid 23290868)
35. Kremer JJ, Pallitto MM, Sklansky DJ, Murphy RM (2000) Correlation of β-amyloid aggregate size and hydrophobicity with decreased bilayer fluidity of model membranes. Biochem 39, 10309-10318. (Pubitemid 30663053)
36. Ege C, Lee KYC (2004) Insertion of Alzheimers A-beta 40 peptide into lipid monolayers. Biophys J 87, 1732-1740. (Pubitemid 39167029)
37. Benseny-Cases N, Ćocera M, Cladera J (2007) Conversion of non-fibrillar beta-sheet oligomers into amyloid fibrils in Alzheimers disease amyloid peptide aggregation. Biochem Biophys Res Commun 361, 916-921. (Pubitemid 47263455)
38. Hortschansky P, Schroeckh V, Christopeit T, Zandomeneghi G, Fändrich M (2005) The aggregation kinetics of Alzheimers β-amyloid peptide is controlled by stochastic nucleation. Protein Sci 14, 1753-1759. (Pubitemid 40994145)
39. Khurana R, Coleman C, Ionescu-Zanetti C, Carter SA, Krishna V, Grover RK, Roy R, Singh S (2005) Mechanism of thioflavin T binding to amyloid fibrils. J Struct Biol 151, 229-238. (Pubitemid 41338730)
40. Levine H, III (1993) Thioflavine T interaction with synthetic Alzheimers disease beta-amyloid peptides: Detection of amyloid aggregation in solution. Protein Sci 2, 404-410.
41. Levine H (1997) Stopped-flowkinetics reveal multiple phases of thioflavin T binding to Alzheimer β (1-40) amyloid fibrils. Arch Biochem Biophys 342, 306-316.
42. Jarrett JT, Berger EP, Lansbury PT (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimers disease. Biochem 32, 4693-4697. (Pubitemid 23162022)
43. Chauhan A, Ray I, Chauhan VPS (2000) Interaction of amyloid beta-protein with anionic phospholipids: Possible involvement of Lys28 and C-terminus aliphatic amino acids. Neurochem Res 25, 423-429. (Pubitemid 30161491)
44. Bokvist M, Lindström F, Watts A, Gröbner G (2004) Two types of Alzheimers β-amyloid (1-40) peptide membrane interactions: Aggregation preventing transmembrane anchoring versus accelerated surface fibril formation. J Mol Biol 335, 1039-1049. (Pubitemid 38091609)
45. Wood SJ, Maleeff B, Hart T, Wetzel R (1996) Physical, morphological and functional differences between pH 5.8 and 7.4 aggregates of the Alzheimers amyloid peptideAβ. J Mol Biol 256, 870-877. (Pubitemid 26108825)
46. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, TeplowDB(1999) Amyloid β-Protein Fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274, 25945-25952.
47. Arispe N, Pollard HB, Rojas E (1993) Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein A beta P-(1-40) in bilayer membranes. Proc Natl Acad Sci U S A 90, 10573-10577. (Pubitemid 23347084)
48. Arispe N, Diaz JC, Simakova O (2007) Aβ ion channels. Prospects for treating Alzheimers disease with Aβ channel blockers. Biochim Biophys Acta 1768, 1952-1965. (Pubitemid 47125852)
49. Capone R, Quiroz FG, Prangkio P, Saluja I, Sauer AM, Bautista MR, Turner RS, Yang J, Mayer M (2009) Amyloid-β-induced ion flux in artificial lipid bilayers and neuronal cells: Resolving a controversy. Neurotox Res 16, 1-13.
50. Jang H, Zheng J, Nussinov R (2007) Models of beta-amyloid ion channels in the membrane suggest that channel formation in the bilayer is a dynamic process. Biophys J 93, 1938-1949. (Pubitemid 47437578)
51. Jang H, Zheng J, Lal R, Nussinov R (2008) New structures help the modeling of toxic amyloid β ion channels. Trends Biochem Sci 33, 91-100.
52. Kremer JJ, Sklansky DJ, Murphy RM (2001) Profile of changes in lipid bilayer structure caused by β-amyloid peptide. Biochem 40, 8563-8571. (Pubitemid 32667263)
53. Muller WE, Eckert GP, Scheuer K, Cairns NJ, Maras A, Gattaz WF (1998) Effects of beta-amyloid peptides on the fluidity of membranes from frontal and parietal lobes of human brain. High potencies of A beta 1-42 and A beta 1-43. Amyloid 5, 10-15. (Pubitemid 128691211)
54. Müller WE, Koch S, Eckert A, Hartmann H, ScheuerK(1995) β-amyloid peptide decreases membrane fluidity. Brain Res 674, 133-136.
55. Du H, Guo L, Yan S, Sosunov AA, McKhann GM, ShiDu Yan S (2010) Early deficits in synaptic mitochondria in an Alzheimers disease mouse model. Proc Natl Acad Sci U S A 107, 18670-18675.
56. McLaurin J, Chakrabartty A (1997) Characterization of the interactions of Alzheimer beta-amyloid peptides with phospholipid membranes. Eur J Biochem 245, 355-363. (Pubitemid 27171258)
57. Waschuk SA, Elton EA, Darabie AA, Fraser PE, McLaurin J (2001) Cellular membrane composition defines Aβ-lipid interactions. J Biol Chem 276, 33561-33568.
58. Kakio A, Yano Y, Takai D, Kuroda Y, Matsumoto O, Kozutsumi Y, Matsuzaki K (2004) Interaction between amyloid beta-protein aggregates and membranes. J Pept Sci 10, 612-621. (Pubitemid 39409620)
59. Matsuzaki K (2007) Physicochemical interactions of amyloid β-peptide with lipid bilayers. Biochim Biophys Acta 1768, 1935-1942. (Pubitemid 47135568)
60. Varnier A, Kermarrec F, Blesneac I, Moreau C, Liguori L, Lenormand JL, Picollet-Dhahan N (2010) A simple method for the reconstitution of membrane proteins into giant unilamellar vesicles. J Membr Biol 233, 85-92.
61. Mecocci P, Cherubini A, Beal MF, Cecchetti R, Chionne F, Polidori MC, Romano G, Senin U (1996) Altered mitochondrial membrane fluidity in AD brain. Neurosci Lett 207, 129-132. (Pubitemid 26116548)
62. Moreira PI, Santos MS, Moreno A, Oliveira C (2001) Amyloid beta-peptide promotes permeability transition pore in brain mitochondria. Biosci Rep 21, 789-800.
63. Moreira PI, Santos MS, Moreno A, Rego AC, Oliveira C (2002) Effect of amyloid beta-peptide on permeability transition pore: A comparative study. J Neurosci Res 69, 257-267. (Pubitemid 34734156)
64. Boldogh IR, Pon LA (2007) Mitochondria on the move. Trends Cell Biol 17, 502-510. (Pubitemid 47562767)
65. Pizzo P, Pozzan T (2007) Mitochondria-endoplasmic reticulum choreography: Structure and signaling dynamics. Trends Cell Biol 17, 511-517. (Pubitemid 47562768)
66. Mannella CA, Buttle K, Rath BK, Marko M (1998) Electron microscopic tomography of rat-liver mitochondria and their interactions with the endoplasmic reticulum. BioFactors 8, 225-228. (Pubitemid 29021352)