Aging promotes amyloid-β peptide induced mitochondrial dysfunctions in rat brain: A molecular link between aging and Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 27, Issue 4, 2011, Pages 753-765

  Sinha, Maitrayee ^a   Behera, Prajna ^a   Bhowmick, Pritha ^a   Banerjee, Kalpita ^a   Basu, Sumitran ^a   Chakrabarti, Sasanka ^a  

^a INSTITUTE OF POST GRADUATE MEDICAL EDUCATION AND RESEARCH   (India)

Author keywords

Alzheimer's disease; amyloid peptide; brain aging; cytochrome c; mitochondria; respiratory chain complexes

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN[1-42]; CYTOCHROME C;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; RAT; RESPIRATORY CHAIN;

EID: 84455173852     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-110686     Document Type: Article

References (66)

1. Bird TD (2001) Alzheimers disease and other primary dementias. In Harrisons Principles of Internal Medicine, Braunwald E, Fauci AS, Kasper DL, Hauser SL, Longo DL, Jameson JL, eds. McGraw-Hill, Inc USA, pp. 2391-2398
2. Evans DA, Funkenstein HH, Albert MS, Scherr PA, Cook NR, Chown MJ, Hebert LE, Hennekens CH, Taylor JO (1989) Prevalence of Alzheimers disease in a community population of older persons higher than previously reported. JAMA 262, 2551-2556
3. Selkoe DJ (1991) The molecular pathology of Alzheimers disease. Neuron 6, 487-498
4. Strooper BD (2010) Proteases and proteolysis in Alzheimers disease: A multifactorial view on the disease process. Physiol Rev 90, 465-494
5. Evin G, Weidemann A (2002) Biogenesis and metabolism of Alzheimers disease A amyloid peptides. Peptides 23, 1285-1297 (Pubitemid 34786707)
6. Fukuchi K, Kamino K, Deeb SS, Smith AC, Dang T, Martin GM (1992) Overexpression of amyloid precursor protein alters its normal processing and is associated with neurotoxicity. Biochem Biophys Res Commun 182, 165-173
7. Sondag CM, Dhawan G, Combs CK (2009) Beta amyloid oligomers and fibrils stimulate differential activation of primary microglia. J Neuroinflammation 6, 1-13
8. De Felice FG, Vieira MNN, Saraiva LMM, Villar JDF, Abreu JG, Liu R, Chang L, Klein WL, Ferreira1 SRT (2004) Targeting the neurotoxic species in Alzheimers disease: Inhibitors of A oligomerization. FASEB J 18, 1366-1372 (Pubitemid 39150351)
9. Nichols MR, Moss MA, Reed DK, Cratic-McDaniel S, Hoh JH, Rosenberry TT (2005) Amyloid- protofibrils differ from amyloid- aggregates induced in dilute hexafluoroisopropanol in stability and morphology. J Biol Chem 280, 2471-2480 (Pubitemid 40189347)
10. Hung LW, Ciccotosto GD, Giannakis E, Tew JD, Perez K, Masters CL, Cappai R, Wade JD, Barnham KJ (2008) Amyloid- peptide (Aβ) neurotoxicity is modulated by the rate of peptide aggregation: A dimers and trimers correlate with neurotoxicity. J Neurosci 28, 11950-11958
11. Snyder SW, Ladror US, Wade WS, Wang GT, Barrett LW, Matayoshi ED, Huffaker HJ, Krafft GA, Holzman TF (1994) Amyloid-beta aggregation: Selective inhibition of aggregation in mixtures of amyloid with different chain lengths. Biophys J 67, 1216-1228
12. El-Agnaf OM, Mahil DS, Patel BP, Austen BM (2000) Oligomerization and toxicity of β-amyloid-42 implicated in Alzheimers disease. Biochem Biophys Res Commun 273, 1003-1007 (Pubitemid 30481069)
13. Crouch PJ, Harding SME, White AR, Camakaris J, Bush AI, Masters CL (2008) Mechanisms of A mediated neurodegeneration in Alzheimers disease. Int J Biochem Cell Biol 40, 81-198
14. 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)
15. Lin TM, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative disease. Nature 443, 787-795 (Pubitemid 44622683)
16. Agostinho P, Cunha RA, Oliveira C (2010) Neuroinflammation, oxidative stress and the pathogenesis of Alzheimers disease. Curr Pharm Des 16, 2766-2778
17. Zawia NH, Lahiri DK, Cardozo-Pelaez F (2009) Epigenetics, oxidative stress and Alzheimers disease. Free Radic Biol Med 46, 1241-1249
18. Hauptmann S,Keil U, Scherping I, Bonert A, Eckert A,Müller WE(2006) Mitochondrial dysfunction in sporadic and genetic Alzheimers disease. Exp Gerontol 41, 668-673 (Pubitemid 43866354)
19. Kish SJ, Bergeron C, Rajput A, Dozic S, Mastrogiacomo F, Chang LJ, Wilson JM, DiStefano LM, Nobrega JN (1992) Brain Cytochrome oxidase in Alzheimers disease. J Neurochem 59, 776-779
20. Reddy PH, Beal MF (2005) Are mitochondria critical in the pathogenesis of Alzheimers disease? Brain Res Rev 49, 618-632 (Pubitemid 41546661)
21. Qiao H,Koya RC, NakagawaK,Tanaka H, Fujita H,Takimoto M, Kuzumaki N (2005) Inhibition of Alzheimers amyloid- peptide-induced reduction of mitochondrial membrane potential and neurotoxicity by gelsolin. Neurobiol Aging 26, 849-855 (Pubitemid 40249487)
22. Kim H, Lee JH, Lee JP, Kim EM, Chang KA, Park HC, Jeong SJ, Wittendorp MC, Seo JE, Choi SH, Suh YH (2002) Amyloid peptide induces cytochrome c release from isolated mitochondria. Neuroreport 13, 1989-1993 (Pubitemid 35398974)
23. Pagani L, Eckert A (2011) Amyloid-beta interaction with mitochondria. Int J Alzheimers Dis 12 pages. ID 925050, doi:10.4061/2011/925050
24. Rhein V, Baysang G, Rao S, Meier F, Bonert A,Müller-Spahn F, Eckert A (2009) Amyloid-beta leads to impaired cellular respiration, energy production and mitochondrial electron chain complex activities in human neuroblastoma cells. Cell Mol Neurobiol 29, 1063-1071
25. Casley CS, Canevari L, Land JM, Clark JB, SharpeMA(2002) Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J Neurochem 80, 91-100 (Pubitemid 34614581)
26. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anandatheerthavarada HK (2006) Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimers disease brain is associated with mitochondrial dysfunction. J Neurosci 26, 9057-9068 (Pubitemid 44319397)
27. Sen T, Sen N, Jana S, Khan FH, Chatterjee U, Chakrabarti S (2007) Depolarization and cardiolipin depletion in aged rat brain mitochondria: Relationship with oxidative stress and electron transport chain activity. Neurochem Int 50, 719-725 (Pubitemid 46463985)
28. Cummings BJ, Satou T, Head TE, Milgram NW, Cole GM, Savage MJ, Podlisny MB, Selkoe DJ, Siman R, Greenbergii BD, Cotmant CW (1996) Diffuse plaques contain C-terminal Aβ-42 and not Aβ-40: Evidence from cats and dogs. Neurobiol Aging 17, 653-659
29. Barnham KJ, Kenche VB, Ciccotosto GD, Smith DP, Tew DJ, Liu X, Perez K, Cranston GA, Johanssen TJ, Volitakis I, Bush AI, Masters CL, White AR, Smith JP, Cherny RA, Cappai R (2008) Platinum-based inhibitors of amyloid- as therapeutic agents for Alzheimers disease. Proc Natl Acad Sci U S A 105, 6813-6818 (Pubitemid 351754487)
30. 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
31. Jana S, Sinha M, Chanda D, Roy T, Banerjee K, Munshi S, Patro BS, Chakrabarti S (2011) Mitochondrial dysfunction mediated by quinone oxidation products of dopamine: Implications in dopamine cytotoxicity and pathogenesis of Parkinsons disease. Biochim Biophys Acta 1812, 663-673
32. Reers M, Smith TW, Chen LB (1991) J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480-4486
33. Sen T, Sen N, Tripathi G, Chatterjee U, Chakrabarti S (2006) Lipid peroxidation associated cardiolipin loss and membrane depolarization in rat brain mitochondria. Neurochem Int 49, 20-27 (Pubitemid 44275196)
34. Hinkle PC (1995) Oxygen proton and phosphate fluxes and stoichiometries In. Bioenergeties: A Practical Approach, Brown GC, Cooper CE, eds. IRL Press, Oxford pp. 1-15
35. Banerjee K, Sinha M, Pham Cle L, Jana S, Chanda D, Cappai R, Chakrabarti S (2010) Alpha-synuclein induced membrane depolarization and loss of phosphorylation capacity of isolated rat brain mitochondria: Implications in Parkinsons disease. FEBS Lett 584, 1571-1576
36. Clark JB, Bates TE, Boakye P, Kuimov A, Land JM (1997) Investigation of mitochondrial defects in brain and skeletal muscle In. Neurochemistry: A Practical Approach, Turner AJ, Bachelard HS, eds. Oxford University Press Inc, New York, pp. 151-174
37. Wharton DC, Tzagoloff A (1967) Cytochrome oxidase from beef heart mitochondria. Methods Enzymol 10, 10245-10250
38. Khan FH, Sen T, Maiti AK, Jana S, Chatterjee U, Chakrabarti S (2005) Inhibition of rat brain mitochondrial electron transport chain activity by dopamine oxidation products during extended in vitro incubation: Implications for Parkinsons disease. Biochim Biophys Acta 1741, 65-74 (Pubitemid 40824991)
39. Westermeier R (2005) Electrophoresis in Practice, Wiley VCH, Weinheim
40. Basford RE (1967) Preparation and properties of brain mitochondria. Methods Enzymol 10, 96-101
41. Clark JB, Nicklas WJ (1970) The metabolism of rat brain mitochondria: Preparation and characterization. J Biol Chem 245, 4724-4731
42. Marksteiner J, Humpel C (2008) Beta-amyloid expression, release and extracellular deposition in aged rat brain slices. Mol Psychiatry 13, 939-952
43. Jang JH, Surh YJ (2003) Protective effect of resveratrol on β- amyloid-induced oxidative PC12 cell death. Free Radic Biol Med 34, 1100-1110
44. Gao X, Tang XC (2006) Huperzine attenuates mitochondrial dysfunction inβ-amyloid-treated PC12 cells by reducing oxygen free radicals accumulation and improving mitochondrial energy metabolism. J Neurosci Res 83, 1048-1057
45. Canevari L, Clark JB, Bates TE (1999) beta-Amyloid fragment 25-35 selectively decreases complex IV activity in isolated mitochondria. FEBS Lett 457, 131-134 (Pubitemid 29387424)
46. Anandatheerthavarada HK, Biswas G, Robin MA, Avadhani NG (2003) Mitochondrial targeting and a novel transmembrane arrest of Alzheimers amyloid precursor protein impairs mitochondrial function in neuronal cells. J Cell Biol 161, 41-54 (Pubitemid 36459078)
47. Hong WK, Han EH, Kim DG, Ahn JY, Park JS, Han BG (2007) Amyloid-α-peptide reduces the expression level of mitochondrial cytochrome oxidase subunits. Neurochem Res 32, 1483-1488 (Pubitemid 47094410)
48. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K,Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Moore FG, Lue LF,Walker DG, Kuppusamy P, Zewier JL, Arancio O, Stern D, Yan SS, Wu H (2004) ABAD directly links A to mitochondrial toxicity in Alzheimers disease. Science 304, 448-452 (Pubitemid 38495942)
49. Du H, Yan SS (2010) Mitochondrial permeability transition pore in Alzheimers disease: Cyclophilin D and amyloid beta. Biochim Biophys Acta 1802, 198-204
50. Singh P, Suman S, Chandna S, Das TK (2009) Possible role of amyloid-beta, adenine nucleotide translocase and cyclophilin- D interaction in mitochondrial dysfunction of Alzheimers disease. Bioinformation 3, 440-445
51. Petersen CAH, Alikhani N, Behbahani H,Wiehager B, Pavlov PF, Alafuzoff I, Leinonen V, Ito A, Winblad B, Glaser E, Ankarcrona M (2008) The amyloid peptide is imported into mitochondria via the TOMimport machinery and localized to mitochondrial cristae. Proc Natl Acad Sci U S A 105, 13145-13150
52. Rourke BO (2000) Pathophysiological and protective role of mitochondrial ion channels. J Physiol 529, 23-36
53. Arispe N, Diaz JC, Simakova O (2007) A ion channels. Prospects for treating Alzheimers disease with A channel blockers. Biochim Biophys Acta 1768, 1952-1965 (Pubitemid 47125852)
54. Lal R, Lin H, Quist AP (2007) Amyloid beta ion channel: 3D structure and relevance to amyloid channel paradigm. Biochim Biophys Acta 1768, 1966-1975 (Pubitemid 47125855)
55. Eckert GP, Wood WG, Müller WE (2001) Effects of aging and β-amyloid on the properties of brain synaptic and mitochondrial membranes. J Neural Transm 108, 1051-1064 (Pubitemid 32802102)
56. Rodrigues CMP, Sola S, Brito MA, Brondino CD, Brites D, Moura JJG (2001) Amyloid - Peptide disrupts mitochondrial membrane lipid and protein structure: Protective pole of tauroursodeoxycholate. Biochem Biophys Res Commun 281, 468-474 (Pubitemid 32928179)
57. Schmidt C, Lepsverdize E, Chi SL, Das AM, Pizzo SV, Dityatev A, Schachner M (2008) Amyloid precursor protein and amyloid β-peptide bind toATP synthase and regulate its activity at the surface of neural cells APP, A and regulation of ATP synthase activity. Mol Psychiatry 13, 953-969
58. Bagh MB, Thakurta IG, Biswas M, Behera P, Chakrabarti S (2011) Age-related oxidative decline of mitochondrial functions in rat brain is prevented by long term oral antioxidant supplementation. Biogerontology 12, 119-131
59. Navarro A, BoverisA(2004) Rat brain and liver mitochondria develop oxidative stress and loose enzymatic activity with aging. Am J Physiol Regul Integr Comp Physiol 287, R1244-R1249 (Pubitemid 39391072)
60. Eckert A, Hauptmann S, Scherping I, Meinhardt J, Rhein V, Dröse S, Brandt U, Fändrich M, Müller WE, Götz J (2008) Oligomeric and fibrillar species of β-amyloid (Aβ42) both impair mitochondrial function in P301L tau transgenic mice. J Mol Med 86, 1255-1267
61. Chakrabarti S, Munshi S, Banerjee K, Thakurta IG, Sinha M, Bagh MB (2011) Mitochondrial Dysfunction during Brain Aging: Role of Oxidative Stress and Modulation by Antioxidant Supplementation. Aging Dis 2, 242-256
62. Nilsen J, Chen S, Irwin RW, Iwamoto S, Brinton RD (2006) Estrogen protects neuronal cells from amyloid beta-induced apoptosis via regulation of mitochondrial proteins and function. BMC Neurosci 7, 74-88
63. Phaneuf S, Leeuwenburgh C (2002) Cytochrome c release from mitochondria in the aging heart: A possible mechanism for apoptosis with age. Am J Physiol Regul Integr Comp Physiol 282, R423-R430 (Pubitemid 34664592)
64. Higgins GC, Beart PM, Shin YS, Chen MJ, Cheung NS, Nagley P (2010) Oxidative stress: Emerging mitochondrial and cellular themes and variations in neuronal injury. J Alzheimers Dis 20, S453-S473
65. NavarroA,Gomèz C, Sańchez-PinoMJ,GonzálezH, Bańdez MJ, Boveris AD, Boveris A (2005) Vitamin E at high doses improves survival, neurological performance and brain mitochondrial function in aging male mice. Am J Physiol Regul Integr Comp Physiol 289, R1392-R1399
66. Liu J, Head E, Gharib AM, Yuan W, Ingersoll RT, Hagen TM, Cotman CW, Ames BN (2002) Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: Partial reversal by feeding acetyl-L-carnitine and/or R-α- lipoic acid. Proc Natl Acad Sci U S A 99, 2356-2361 (Pubitemid 34169065)