From mitochondrial dysfunction to amyloid beta formation: Novel insights into the pathogenesis of Alzheimer's disease

Molecular Neurobiology

Volumn 46, Issue 1, 2012, Pages 186-193

  Leuner, Kristina ^a   Müller, Walter E ^b   Reichert, Andreas S ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Aging; Alzheimer's disease; Amyloid beta formation; Mitochondrial dysfunction

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E4; CALCIUM; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE; GAMMA SECRETASE; MITOCHONDRIAL DNA; OLIGOMER; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TAU PROTEIN;

AGING; ALZHEIMER DISEASE; ARTICLE; BRAIN MITOCHONDRION; COGNITIVE DEFECT; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; INFLAMMATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN PHOSPHORYLATION; RISK FACTOR; SOMATIC MUTATION; SYNAPSE;

EID: 84868127393     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-012-8307-4     Document Type: Article

References (73)

1. Qiu C, Kivipelto M, von Strauss E (2009) Epidemiology of Alzheimer's disease: occurrence, determinants, and strategies toward intervention. Dialogues Clin Neurosci 2:111-128
2. Querfurth HW, LaFerla FM (2010) Alzheimer's disease. N Engl J ed 4:329-344
3. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 2:101-112 (Pubitemid 46432529)
4. Leuner K, Hauptmann S, Abdel-Kader R, Scherping I, Keil U, Strosznajder JB, Eckert A, Muller WE (2007) Mitochondrial dysfunction: the first domino in brain aging and Alzheimer's disease? Antioxid Redox Signal 10:1659-1675 (Pubitemid 47462969)
5. Mao P, Reddy PH (2011) Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in Alzheimer's disease: implications for early intervention and therapeutics. Biochim Biophys Acta 11:1359-1370
6. Starkov AA (2008) The role of mitochondria in reactive oxygen species metabolism and signaling. Ann NY Acad Sci 37-52
7. Drose S, Brandt U (2008) The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J Biol Chem 31:21649-21654
8. Mattson MP, Magnus T (2006) Ageing and neuronal vulnerability. Nat Rev Neurosci 4:278-294
9. Scherz-Shouval R, Elazar Z (2011) Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 1:30-38
10. Clark TA, Lee HP, Rolston RK, Zhu X, MarlattMW, Castellani RJ, Nunomura A, Casadesus G, Smith MA, Lee HG et al (2010) Oxidative stress and its implications for future treatments and management of Alzheimer disease. Int J Biomed Sci 3:225-227
11. Leutner S, Schindowski K, Frolich L, Maurer K, Kratzsch T, Eckert A, Muller WE (2005) Enhanced ROS-generation in lymphocytes from Alzheimer's patients. Pharmacopsychiatry 6:312-315 (Pubitemid 41815688)
12. Leutner S, Eckert A, Muller WE (2001) ROS generation, lipid peroxidation and antioxidant enzyme activities in the aging brain. J Neural Transm 108(8-9):955-967 (Pubitemid 32802093)
13. Baek BS, Kwon HJ, Lee KH, Yoo MA, Kim KW, Ikeno Y, Yu BP, Chung HY (1999) Regional difference of ROS generation, lipid peroxidation, and antioxidant enzyme activity in rat brain and their dietary modulation. Arch Pharm Res 4:361-366
14. Butterfield DA, Howard B, Yatin S, Koppal T, Drake J, Hensley K, Aksenov M, Aksenova M, Subramaniam R, Varadarajan S et al (1999) Elevated oxidative stress in models of normal brain aging and Alzheimer's disease. Life Sci 65(18-19):1883-1892 (Pubitemid 29506923)
15. Gilmer LK, Ansari MA, Roberts KN, Scheff SW (2010) Agerelated changes in mitochondrial respiration and oxidative damage in the cerebral cortex of the Fischer 344 rat. Mech Ageing Dev 2:133-143
16. Marchi S, Giorgi C, Suski JM, Agnoletto C, Bononi A, Bonora M, De Marchi E, Missiroli S, Patergnani S, Poletti F et al. (2012) Mitochondria-ROS crosstalk in the control of cell death and aging. J Signal Transduct 329635
17. Manczak M, Jung Y, Park BS, Partovi D, Reddy PH (2005) Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J Neurochem 3:494-504 (Pubitemid 40189453)
18. Kushnareva Y, Murphy AN, Andreyev A (2002) Complex Imediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem J (Pt 2): 45-553
19. Andreyev AI, Kushnareva YE, Starkov AA (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 2:200-214 (Pubitemid 40512329)
20. Brown GC, Borutaite V (2004) Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim Biophys Acta 1658(1-2):44-49 (Pubitemid 39013232)
21. Blalock EM, Chen KC, Sharrow K, Herman JP, Porter NM, Foster TC, Landfield PW (2003) Gene Microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 9:3807-3819 (Pubitemid 36958487)
22. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damage in the ageing human brain. Nature 6994:883-891 (Pubitemid 38843301)
23. Dencher NA, Frenzel M, Reifschneider NH, Sugawa M, Krause F (2007) Proteome alterations in rat mitochondria caused by aging. Ann NY Acad Sci 291-298 (Pubitemid 47092664)
24. Frenzel M, Rommelspacher H, Sugawa MD, Dencher NA (2010) Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp Gerontol 45(7-8):563-572
25. Leuner K, Hauptmann S, Abdel-Kader R, Scherping I, Keil U, Strosznajder JB, Eckert A, Muller WE (2007) Mitochondrial ysfunction: the first domino in brain aging and Alzheimer's disease? Antioxid Redox Signal 10:1659-1675 (Pubitemid 47462969)
26. Cocco T, Pacelli C, Sgobbo P, Villani G (2009) Control of OXPHOS efficiency by complex I in brain mitochondria. Neurobiol Aging 4:622-629
27. Cocco T, Sgobbo P, Clemente M, Lopriore B, Grattagliano I, Di Paola M, Villani G (2005) Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine. Free Radic Biol Med 6:796-805 (Pubitemid 40249750)
28. Pagani L, Eckert A (2011) Amyloid-Beta interaction with mitochondria. Int J Alzheimers Dis 925050
29. Swerdlow RH (2011) Brain aging, Alzheimer's disease, and mitochondria. Biochim Biophys Acta 12:1630-1639
30. Santos RX, Correia SC, Wang X, Perry G, Smith MA, Moreira PI, Zhu X (2010) A synergistic dysfunction of mitochondrial fission/ fusion dynamics and mitophagy in Alzheimer's disease. J Alzheimers Dis S401-S412
31. Tabaton M, Tamagno E (2007) The molecular link between betaand gamma-secretase activity on the amyloid beta precursor protein. Cell Mol Life Sci 17:2211-2218 (Pubitemid 47347960)
32. Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, Guglielmotto M, Santoro G, Davit A, Danni O, Smith MA et al (2005) Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J Neurochem 3:628-636 (Pubitemid 40189465)
33. Gwon AR, Park JS, Arumugam TV, Kwon YK, Chan SL, Kim SH, Baik SH, Yang S, Yun YK, Choi Y et al (2012) Oxidative lipid modification of nicastrin enhances amyloidogenic gammasecretase activity in Alzheimer's disease. Aging Cell
34. Leuner K, Schutt T, Kurz C, Eckert SH, Schiller C, Occhipinti A, Mai S, Jendrach M, Eckert GP, Kruse SE et al (2012) Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid Redox Signal 16:1421-1433
35. Kruse SE, Watt WC, Marcinek DJ, Kapur RP, Schenkman KA, Palmiter RD (2008) Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metab 4:312-320 (Pubitemid 351455216)
36. Chen L, Yoo SE, Na R, Liu Y, Ran Q (2012) Cognitive impairment and increased Abeta levels induced by paraquat exposure are attenuated by enhanced removal of mitochondrial H(2)O(2). Neurobiol Aging 2:432-26
37. Imanishi H, Yokota M, Mori M, Shimizu A, Nakada K, Hayashi J (2011) Nuclear but not mitochondrial DNA involvement in respiratory complex I defects found in senescence-accelerated mouse strain, SAMP8. Exp Anim 4:397-404
38. Poon HF, Joshi G, Sultana R, Farr SA, Banks WA, Morley JE, Calabrese V, Butterfield DA (2004) Antisense directed at the A beta region of APP decreases brain oxidative markers in aged senescence accelerated mice. Brain Res 1:86-96 (Pubitemid 38942865)
39. Jellinger KA (2011) Interaction between alpha-synuclein and other proteins in neurodegenerative disorders. Scientific World Journal 1893-1907
40. Jucker M, Walker LC (2011) Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 4:532-540
41. Kazmierczak A, Strosznajder JB, Adamczyk A (2008) Alpha-Synuclein enhances secretion and toxicity of amyloid beta peptides in PC12 cells. Neurochem Int 53(6-8):263-269
42. Perluigi M, Butterfield DA (2012) Oxidative stress and Down syndrome: A route toward Alzheimer-like dementia. Curr Gerontol Geriatr Res 724904
43. Bush A, Beail N (2004) Risk factors for dementia in people with down syndrome: issues in assessment and diagnosis. Am J Ment Retard 2:83-97
44. Zana M, Janka Z, Kalman J (2007) Oxidative stress: A bridge between Down's syndrome and Alzheimer's disease. Neurobiol Aging 5:648-676 (Pubitemid 46349350)
45. Bambrick LL, Fiskum G (2008) Mitochondrial dysfunction in mouse trisomy 16 brain. Brain Res 9-16 (Pubitemid 350296061)
46. Valenti D, Manente GA, Moro L, Marra E, Vacca RA (2011) Deficit of complex I activity in human skin fibroblasts with chromosome 21 trisomy and overproduction of reactive oxygen species by mitochondria: involvement of the cAMP/PKA signalling pathway. Biochem J 3:679-688
47. Guglielmotto M, Aragno M, Autelli R, Giliberto L, Novo E, Colombatto S, Danni O, Parola M, Smith MA, Perry G et al (2009) The upregulation of BACE1 mediated by hypoxia and ischemic injury: role of oxidative stress and HIF1alpha. J Neurochem 4:1045-1056
48. Sun X, He G, Qing H, Zhou W, Dobie F, Cai F, Staufenbiel M, Huang LE, SongW(2006) Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression. Proc Natl Acad Sci U S A 49:18727-18732 (Pubitemid 44913478)
49. Zhang X, Zhou K, Wang R, Cui J, Lipton SA, Liao FF, Xu H, Zhang YW (2007) Hypoxia-inducible factor 1alpha (HIF-1alpha)-mediated hypoxia increases BACE1 expression and beta-amyloid generation. J Biol Chem 15:10873-10880 (Pubitemid 47100783)
50. Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GR, Chandel NS (2007) The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 6:1029-1036 (Pubitemid 46955707)
51. Schneider JA, Wilson RS, Bienias JL, Evans DA, Bennett DA (2004) Cerebral infarctions and the likelihood of dementia from Alzheimer disease pathology. Neurology 7:1148-1155 (Pubitemid 38456510)
52. Schneider JA, Arvanitakis Z, Leurgans SE, Bennett DA (2009) The neuropathology of probable Alzheimer disease and mild cognitive impairment. Ann Neurol 2:200-208
53. Chen HK, Ji ZS, Dodson SE, Miranda RD, Rosenblum CI, Reynolds IJ, Freedman SB, Weisgraber KH, Huang Y, Mahley RW (2011) Apolipoprotein E4 domain interaction mediates detrimental effects on mitochondria and is a potential therapeutic target for Alzheimer disease. J Biol Chem 7:5215-5221
54. Guglielmotto M, Monteleone D, Giliberto L, Fornaro M, Borghi R, Tamagno E, Tabaton M (2011) Amyloid-beta activates the expression of BACE1 through the JNK pathway. J Alzheimers Dis 4:871-883
55. Buggia-Prevot V, Sevalle J, Rossner S, Checler F (2008) NFkappaB-dependent control of BACE1 promoter transactivation by Abeta42. J Biol Chem 15:10037-10047
56. Hauptmann S, Scherping I, Drose S, Brandt U, Schulz KL, Jendrach M, Leuner K, Eckert A, Muller WE (2009) Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging 10:1574-1586
57. Eckert A, Hauptmann S, Scherping I, Rhein V, Muller-Spahn F, Gotz J, Muller WE (2008) Soluble beta-amyloid leads to mitochondrial defects in amyloid precursor protein and tau transgenic mice. Neurodegener Dis 5(3-4):157-159 (Pubitemid 351347837)
58. Rhein V, Song X, Wiesner A, Ittner LM, Baysang G, Meier F, Ozmen L, Bluethmann H, Drose S, Brandt U et al (2009) Amyloidbeta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc Natl Acad Sci U S A 47:20057-20062
59. Eckert A, Hauptmann S, Scherping I, Meinhardt J, Rhein V, Drose S, Brandt U, Fandrich M, Muller WE, Gotz J (2008) Oligomeric and fibrillar species of beta-amyloid (A beta 42) both impair mitochondrial function in P301L tau transgenic mice. J Mol Med (Berl) 11:1255-1267
60. Yao J, Irwin RW, Zhao L, Nilsen J, Hamilton RT, Brinton RD (2009) Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 34:14670-14675
61. Gillardon F, Rist W, Kussmaul L, Vogel J, Berg M, Danzer K, Kraut N, Hengerer B (2007) Proteomic and functional alterations in brain mitochondria from Tg2576 mice occur before amyloid plaque deposition. Proteomics 4:605-616 (Pubitemid 46362624)
62. Fu YJ, Xiong S, Lovell MA, Lynn BC (2009) Quantitative proteomic analysis of mitochondria in aging PS-1 transgenic mice. Cell Mol Neurobiol 5:649-664
63. Hansson Petersen CA, Alikhani N, Behbahani H, Wiehager B, Pavlov PF, Alafuzoff I, Leinonen V, Ito A, Winblad B, Glaser E et al (2008) The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc Natl Acad Sci U S A 35:13145-13150
64. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M et al (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 5669:448-452 (Pubitemid 38495942)
65. Hansson CA, Frykman S, Farmery MR, Tjernberg LO, Nilsberth C, Pursglove SE, Ito A,Winblad B, Cowburn RF, Thyberg J et al (2004) Nicastrin, presenilin, APH-1, and PEN-2 form active gammasecretase complexes in mitochondria. J Biol Chem 49:51654-51660 (Pubitemid 40017916)
66. Falkevall A, Alikhani N, Bhushan S, Pavlov PF, Busch K, Johnson KA, Eneqvist T, Tjernberg L, Ankarcrona M, Glaser E (2006) Degradation of the amyloid beta-protein by the novel mitochondrial peptidasome, PreP. J Biol Chem 39:29096-29104 (Pubitemid 44507053)
67. Alikhani N, Guo L, Yan S, Du H, Pinho CM, Chen JX, Glaser E, Yan SS (2011) Decreased proteolytic activity of the mitochondrial amyloid-beta degrading enzyme, PreP peptidasome, in Alzheimer's disease brain mitochondria. J Alzheimers Dis 1:75-87
68. David DC, Hauptmann S, Scherping I, Schuessel K, Keil U, Rizzu P, Ravid R, Drose S, Brandt U, Muller WE et al (2005) Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L Tau transgenic mice. J Biol Chem 25:23802-23814 (Pubitemid 40884866)
69. Fukui H, Diaz F, Garcia S, Moraes CT (2007) Cytochrome c oxidase deficiency in neurons decreases both oxidative stress and amyloid formation in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 35:14163-14168 (Pubitemid 350003352)
70. Pickrell AM, Fukui H, Moraes CT (2009) The role of cytochrome c oxidase deficiency in ROS and amyloid plaque formation. J Bioenerg Biomembr 5:453-456
71. Finsterer J (2009) Mitochondrial disorders, cognitive impairment and dementia. J Neurol Sci 283(1-2):143-148
72. Salsano E, Giovagnoli AR, Morandi L, Maccagnano C, Lamantea E, Marchesi C, Zeviani M, Pareyson D (2011) Mitochondrial dementia: A sporadic case of progressive cognitive and behavioral decline with hearing loss due to the rare m.3291T>C MELAS mutation. J Neurol Sci 300(1-2):165-168
73. Kaido M, Fujimura H, Soga F, Toyooka K, Yoshikawa H, Nishimura T, Higashi T, Inui K, Imanishi H, Yorifuji S et al (1996) Alzheimer-type pathology in a patient with mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes (MELAS). Acta Neuropathol 3:312-318 (Pubitemid 26278964)