Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation

Antioxidants and Redox Signaling

Volumn 16, Issue 12, 2012, Pages 1421-1433

  Leuner, Kristina ^a,b   Schütt, Tanja ^a   Kurz, Christopher ^a   Eckert, Schamim H ^a   Schiller, Carola ^a   Occhipinti, Angelo ^a,c   Mai, Sören ^a   Jendrach, Marina ^a   Eckert, Gunter P ^a   Kruse, Shane E ^d   Palmiter, Richard D ^d   Brandt, Ulrich ^a   Dröse, Stephan ^a   Wittig, Ilka ^a   Willem, Michael ^e,f   Haass, Christian ^e,f   Reichert, Andreas S ^a,c   Müller, Walter E ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c Frankfurt Institute for Molecular Life Sciences   (Germany)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^f UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CITRININ; REACTIVE OXYGEN METABOLITE; ROTENONE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; HUMAN CELL; IN VIVO STUDY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIMYCIN A; ASPARTIC ACID ENDOPEPTIDASES; CELL LINE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; MICE; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; ROTENONE;

EID: 84860198618     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4173     Document Type: Article

References (61)

1. Anandatheerthavarada HK and Devi L. Amyloid precursor protein and mitochondrial dysfunction in Alzheimer's disease. Neuroscientist 13: 626-638, 2007. (Pubitemid 350077307)
2. Andreyev AI, Kushnareva YE, and Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochem Mosc 70: 200-214, 2005. (Pubitemid 40512329)
3. Behl C. Apoptosis and Alzheimer's disease. J Neural Transm 107: 1325-1344, 2000.
4. Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, and Rossignol R. Mitochondrial bioenergetics and structural network organization. J Cell Sci 120: 838-848, 2007. (Pubitemid 46523485)
5. Bishop NA, Lu T, and Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature 464: 529-535, 2010.
6. Blalock EM, Chen KC, Sharrow K, Herman JP, Porter NM, Foster TC, and Landfield PW. Gene Microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 23: 3807-3819, 2003. (Pubitemid 36958487)
7. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, Price DL, and Wong PC. BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat Neurosci 4: 233-234, 2001. (Pubitemid 32194867)
8. Choi WS, Kruse SE, Palmiter RD, and Xia ZG. Mitochondrial complex I inhibition is not required for dopaminergic neuron death induced by rotenone, MPP+ , or paraquat. Proc Natl Acad Sci USA 105: 15136-15141, 2008.
9. David DC, Hauptmann S, Scherping I, Schuessel K, Keil U, Rizzu P, Ravid R, Drose S, Brandt U, Muller WE, Eckert A, and Gotz J. Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L Tau transgenic mice. J Biol Chem 280: 23802-23814, 2005. (Pubitemid 40884866)
10. Devi L, Prabhu BM, Galati DF, Avadhani NG, and Anandatheerthavarada HK. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J Neurosci 26: 9057-9068, 2006. (Pubitemid 44319397)
11. Du H, Guo L, Yan SQ, Sosunov AA, McKhann GM, and Yan SS. Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc Natl Acad Sci USA 107: 18670-18675, 2010.
12. Eckert A, Steiner B, Marques C, Leutz S, Romig H, Haass C, and Muller WE. Elevated vulnerability to oxidative stressinduced cell death and activation of caspase-3 by the Swedish amyloid precursor protein mutation. J Neurosci Res 64: 183-192, 2001.
13. Finsterer J. Mitochondrial disorders, cognitive impairment and dementia. J Neurol Sci 283: 143-148, 2009.
14. Fukui H, Diaz F, Garcia S, and Moraes CT. 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 USA 104: 14163-14168, 2007. (Pubitemid 350003352)
15. Fukumoto H, Cheung BS, Hyman BT, and Irizarry MC. Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch Neurol 59: 1381-1389, 2002. (Pubitemid 35014802)
16. Guglielmotto M, Aragno M, Autelli R, Giliberto L, Novo E, Colombatto S, Danni O, Parola M, Smith MA, Perry G, Tamagno E, and Tabaton M. The up-regulation of BACE1 mediated by hypoxia and ischemic injury: role of oxidative stress and HIF1 alpha. J Neurochem 108: 1045-1056, 2009.
17. Haass C and Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid betapeptide. Nat Rev Mol Cell Biol 8: 101-112, 2007. (Pubitemid 46432529)
18. Hauptmann S, Scherping I, Drose S, Brandt U, Schulz KL, Jendrach M, Leuner K, Eckert A, and Muller WE. Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging 30: 1574-1586, 2009.
19. Holsinger RM, McLean CA, Beyreuther K, Masters CL, and Evin G. Increased expression of the amyloid precursor betasecretase in Alzheimer's disease. Ann Neurol 51: 783-786, 2002. (Pubitemid 34568861)
20. Holsinger RM, McLean CA, Collins SJ, Masters CL, and Evin G. Increased beta-Secretase activity in cerebrospinal fluid of Alzheimer's disease subjects. Ann Neurol 55: 898-899, 2004. (Pubitemid 38702591)
21. Hutter E, Unterluggauer H, Garedew A, Jansen-Durr P, and Gnaiger E. High-resolution respirometry-a modern tool in aging research. Exp Gerontol 41: 103-109, 2006. (Pubitemid 43031375)
22. Jendrach M, Mai S, Pohl S, Voth M, and Bereiter-Hahn J. Short-and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress. Mitochondrion 8: 293-304, 2008.
23. Jendrach M, Pohl S, Voth M, Kowald A, Hammerstein P, and Bereiter-Hahn J. Morpho-dynamic changes of mitochondria during ageing of human endothelial cells. Mech Ageing Dev 126: 813-821, 2005. (Pubitemid 40693304)
24. Kaido M, Fujimura H, Soga F, Toyooka K, Yoshikawa H, Nishimura T, Higashi T, Inui K, Imanishi H, Yorifuji S, and Yanagihara T. Alzheimer-type pathology in a patient with mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes (MELAS). Acta Neuropathol 92: 312-318, 1996. (Pubitemid 26278964)
25. Keil U, Bonert A, Marques CA, Scherping I, Weyermann J, Strosznajder JB, Muller-Spahn F, Haass C, Czech C, Pradier L, Muller WE, and Eckert A. Amyloid beta-induced changes in nitric oxide production and mitochondrial activity lead to apoptosis. J Biol Chem 279: 50310-50320, 2004. (Pubitemid 39577847)
26. Kruse SE, Watt WC, Marcinek DJ, Kapur RP, Schenkman KA, and Palmiter RD. Mice with mitochondrial complex I deficiency develop a fatal encephalomyopathy. Cell Metabol 7: 312-320, 2008. (Pubitemid 351455216)
27. Kushnareva Y, Murphy AN, and Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P) + oxidation-reduction state. Biochem J 368: 545-553, 2002. (Pubitemid 35454532)
28. Li Q and Sudhof TC. Cleavage of amyloid-beta precursor protein and amyloid-beta precursor-like protein by BACE 1. J Biol Chem 279: 10542-10550, 2004. (Pubitemid 38372665)
29. Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ. Protein Measurement with the Folin Phenol Reagent. J Biol Chem 193: 265-275, 1951.
30. Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, and Yankner BA. Gene regulation and DNA damage in the ageing human brain. Nature 429: 883-891, 2004. (Pubitemid 38843301)
31. Luo Y, Bolon B, Kahn S, Bennett BD, Babu-Khan S, Denis P, Fan W, Kha H, Zhang J, Gong Y, Martin L, Louis JC, Yan Q, Richards WG, Citron M, and Vassar R. Mice deficient in BACE1, the Alzheimer's beta-secretase, have normal phenotype and abolished beta-amyloid generation. Nat Neurosci 4: 231-232, 2001. (Pubitemid 32194866)
32. Manczak M, Jung Y, Park BS, Partovi D, and Reddy PH. Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J Neurochem 92: 494-504, 2005. (Pubitemid 40189453)
33. Mattson MP. Pathways towards and away from Alzheimer's disease. Nature 430: 631-639, 2004. (Pubitemid 39061671)
34. Mattson MP. Neuronal life-and-death signaling, apoptosis, and neurodegenerative disorders. Antioxid Redox Signal 8: 1997-2006, 2006. (Pubitemid 46489627)
35. Mattson MP. Mitochondrial regulation of neuronal plasticity. Neurochem Res 32: 707-715, 2007. (Pubitemid 46481300)
36. Mattson MP, Barger SW, Begley JG, and Mark RJ. Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol 46: 187-216, 1995.
37. Mattson MP, Gleichmann M, and Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 60: 748-766, 2008.
38. Mattson MP and Magnus T. Ageing and neuronal vulnerability. Nat Rev Neurosci 7: 278-294, 2006.
39. Mü ller WE, Eckert A, Kurz C, Eckert GP, and Leuner K. Mitochondrial dysfunction: common final pathway in brain aging and Alzheimer's disease-therapeutic aspects. Mol Neurobiol 41: 159-171, 2010.
40. Nakahara H, Kanno T, Inai Y, Utsumi K, Hiramatsu M, Mori A, and Packer L. Mitochondrial dysfunction in the senescence accelerated mouse (SAM). Free Radic Biol Med 24: 85-92, 1998. (Pubitemid 28006439)
41. Navarro A and Boveris A. Brain mitochondrial dysfunction in aging: conditions that improve survival, neurological performance and mitochondrial function. Front Biosci 12: 1154-1163, 2007. (Pubitemid 46846884)
42. O'Connor T, Sadleir KR, Maus E, Velliquette RA, Zhao J, Cole SL, Eimer WA, Hitt B, Bembinster LA, Lammich S, Lichtenthaler SF, Hebert SS, De Strooper B, Haass C, Bennett DA, and Vassar R. Phosphorylation of the translation initiation factor eIF2alpha increases BACE1 levels and promotes amyloidogenesis. Neuron 60: 988-1009, 2008.
43. Paradies G, Petrosillo G, Paradies V, and Ruggiero FM. Oxidative stress, mitochondrial bioenergetics, and cardiolipin in aging. Free Radic Biol Med 48: 1286-1295, 2010.
44. Pavlov PF, Petersen CH, Glaser E, and Ankarcrona M. Mitochondrial accumulation of APP and Abeta: significance for Alzheimer disease pathogenesis. J Cell Mol Med 3: 4137-4145, 2009.
45. Petrosillo G, Matera M, Casanova G, Ruggiero FM, and Paradies G. Mitochondrial dysfunction in rat brain with aging Involvement of complex I, reactive oxygen species and cardiolipin. Neurochem Int 53: 126-131, 2008.
46. Querfurth HW and LaFerla FM. Alzheimer's disease. N Engl J Med 362: 329-344, 2010.
47. Reddy PH. Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp Neurol 218: 286-292, 2009.
48. Reddy PH, Manczak M, Mao P, Calkins MJ, Reddy AP, and Shirendeb U. Amyloid-beta and mitochondria in aging and Alzheimer's disease: implications for synaptic damage and cognitive decline. J Alzheimers Dis 20 Suppl 2: S499-S512, 2010.
49. Rhein V, Song XM, Wiesner A, Ittner LM, Baysang G, Meier F, Ozmen L, Bluethmann H, Drose S, Brandt U, Savaskan E, Czech C, Gotz J, and Eckert A. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc Natl Acad Sci USA 106: 20057-20062, 2009.
50. Salsano E, Giovagnoli AR, Morandi L, Maccagnano C, Lamantea E, Marchesi C, Zeviani M, and Pareyson D. Mitochondrial dementia: a sporadic case of progressive cognitive and behavioral decline with hearing loss due to the rare m.3291T >CMELAS mutation. J Neurol Sci 300: 165-168, 2011.
51. Su B, Wang XL, Bonda D, Perry G, Smith M, and Zhu XW. Abnormal Mitochondrial Dynamics-A Novel Therapeutic Target for Alzheimer's Disease? Mol Neurobiol 41: 87-96, 2010.
52. Su B, Wang XL, Zheng L, Perry G, Smith MA, and Zhu XW. Abnormal mitochondrial dynamics and neurodegenerative diseases. Biochim Biophys Acta 1802: 135-142, 2010.
53. Sun X, He G, Qing H, Zhou W, Dobie F, Cai F, Staufenbiel M, Huang LE, and Song W. Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression. Proc Natl Acad Sci USA 103: 18727-18732, 2006. (Pubitemid 44913478)
54. Swerdlow RH and Kish SJ. Mitochondria in Alzheimer's disease. Int Rev Neurobiol 53: 341-385, 2002.
55. Tamagno E, Guglielmotto M, Aragno M, Borghi R, Autelli R, Giliberto L, Muraca G, Danni O, Zhu XW, Smith MA, Perry G, Jo DG, Mattson MP, and Tabaton M. Oxidative stress activates a positive feedback between the gamma-and betasecretase cleavages of the beta-amyloid precursor protein. J Neurochem 104: 683-695, 2008.
56. Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, GuglielmottoM, Santoro G,DavitA,Danni O,SmithMA, PerryG, and Tabaton M. Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J Neurochem 92: 628-636, 2005. (Pubitemid 40189465)
57. Verkaart S, Koopman WJH, Cheek J, Emst-de Vries SE, van den Heuvel LWPJ, Smeitink JAM, and Willems PHGM. Mitochondrial and cytosolic thiol redox state are not detectably altered in isolated human NADH: ubiquinone oxidoreductase deficiency. Biochim Biophys Acta 1772: 1041-1051, 2007. (Pubitemid 47314228)
58. Wang X, Su B, Lee HG, Li X, Perry G, Smith MA, and Zhu X. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J Neurosci 29: 9090-9103, 2009.
59. Wang X, Su B, Siedlak SL, Moreira PI, Fujioka H, Wang Y, Casadesus G, and Zhu X. Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc Natl Acad Sci USA 105: 19318-19323, 2008.
60. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, Beach T, Sue L, Wong P, Price D, Li R, and Shen Y. Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9: 3-4, 2003. (Pubitemid 36098241)
61. Yao J, Irwin RW, Zhao L, Nilsen J, Hamilton RT, and Brinton RD. Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 106: 14670-14675, 2009.