Permeability transition pore-mediated mitochondrial superoxide flashes mediate an early inhibitory effect of amyloid beta1-42 on neural progenitor cell proliferation

Neurobiology of Aging

Volumn 35, Issue 5, 2014, Pages 975-989

  Hou, Yan ^a   Ghosh, Paritosh ^a   Wan, Ruiqian ^a   Ouyang, Xin ^a   Cheng, Heping ^b   Mattson, Mark P ^a,c   Cheng, Aiwu ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b PEKING UNIVERSITY   (China)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid peptide; ERK; Mitochondrial permeability transition pore; Neurogenesis; SOD

Indexed keywords

ALZHEIMER'S DISEASE; AMYLOID Β-PEPTIDE; ERK; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NEUROGENESIS; SOD;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CYTOCHROMES C; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; NEURONS; NUCLEAR PORE; PEPTIDE FRAGMENTS; PERMEABILITY; REACTIVE OXYGEN SPECIES; STEM CELLS; SUPEROXIDES;

EID: 84893738283     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.11.002     Document Type: Article

References (89)

1. Anantharaman M., Tangpong J., Keller J.N., Murphy M.P., Markesbery W.R., Kiningham K.K., St Clair D.K. Beta-amyloid mediated nitration of manganese superoxide dismutase: implication for oxidative stress in an APPNLH/NLH X PS-1P264L/P264L double knock-in mouse model of Alzheimer's disease. Am. J. Pathol. 2006, 168:1608-1618.
2. Begley J.G., Duan W., Chan S., Duff K., Mattson M.P. Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice. J.Neurochem. 1999, 72:1030-1039.
3. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol. Rev. 1999, 79:1127-1155.
4. Bernardi P., Forte M. The mitochondrial permeability transition pore. Novartis Found. Symp. 2007, 287:157-164.
5. Bizon J.L., Lee H.J., Gallagher M. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 2004, 3:227-234.
6. Bonda D.J., Wang X., Perry G., Nunomura A., Tabaton M., Zhu X., Smith M.A. Oxidative stress in Alzheimer disease: a possibility for prevention. Neuropharmacology 2010, 59:290-294.
7. Bruce A.J., Malfroy B., Baudry M. beta-Amyloid toxicity in organotypic hippocampal cultures: protection by EUK-8, a synthetic catalytic free radical scavenger. Proc. Natl. Acad. Sci. U.S.A 1996, 93:2312-2316.
8. Butterfield D.A., Reed T., Sultana R. Roles of 3-nitrotyrosine- and 4-hydroxynonenal-modified brain proteins in the progression and pathogenesis of Alzheimer's disease. Free Radic. Res. 2011, 45:59-72.
9. Caspersen C., Wang N., Yao J., Sosunov A., Chen X., Lustbader J.W., Xu H.W., Stern D., McKhann G., Yan S.D. Mitochondrial abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J. 2005, 19:2040-2041.
10. Cheng A., Chan S.L., Milhavet O., Wang S., Mattson M.P. p38 MAP kinase mediates nitric oxide-induced apoptosis of neural progenitor cells. J.Biol. Chem. 2001, 276:43320-43327.
11. Cheng A., Tang H., Cai J., Zhu M., Zhang X., Rao M., Mattson M.P. Gap junctional communication is required to maintain mouse cortical neural progenitor cells in a proliferative state. Dev. Biol. 2004, 272:203-216.
12. Cheng A., Shin-ya K., Wan R., Tang S.C., Miura T., Tang H., Khatri R., Gleichman M., Ouyang X., Liu D., Park H.R., Chiang J.Y., Mattson M.P. Telomere protection mechanisms change during neurogenesis and neuronal maturation: newly generated neurons are hypersensitive to telomere and DNA damage. J.Neurosci. 2007, 27:3722-3733.
13. Cheng A., Coksaygan T., Tang H., Khatri R., Balice-Gordon R.J., Rao M.S., Mattson M.P. Truncated tyrosine kinase B brain-derived neurotrophic factor receptor directs cortical neural stem cells to a glial cell fate by a novel signaling mechanism. J.Neurochem. 2007, 100:1515-1530.
14. Cho S., Szeto H.H., Kim E., Kim H., Tolhurst A.T., Pinto J.T. Anovel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J.Biol. Chem. 2007, 282:4634-4642.
15. Cotman C.W., Su J.H. Mechanisms of neuronal death in Alzheimer's disease. Brain Pathol. 1996, 6:493-506.
16. Crews L., Adame A., Patrick C., Delaney A., Pham E., Rockenstein E., Hansen L., Masliah E. Increased BMP6 levels in the brains of Alzheimer's disease patients and APP transgenic mice are accompanied by impaired neurogenesis. J.Neurosci. 2010, 30:12252-12262.
17. Crompton M., Virji S., Doyle V., Johnson N., Ward J.M. The mitochondrial permeability transition pore. Biochem. Soc. Symp. 1999, 66:167-179.
18. Demars M., Hu Y.S., Gadadhar A., Lazarov O. Impaired neurogenesis is an early event in the etiology of familial Alzheimer's disease in transgenic mice. J.Neurosci. Res. 2010, 88:2103-2117.
19. Donovan M.H., Yazdani U., Norris R.D., Games D., German D.C., Eisch A.J. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J.Comp. Neurol. 2006, 495:70-83.
20. Dumont M., Lin M.T., Beal M.F. Mitochondria and antioxidant targeted therapeutic strategies for Alzheimer's disease. J.Alzheimers Dis. 2010, 20:S633-S643.
21. Dupret D., Revest J.M., Koehl M., Ichas F., De Giorgi F., Costet P., Abrous D.N., Piazza P.V. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 2008, 3:e1959.
22. Ermini F.V., Grathwohl S., Radde R., Yamaguchi M., Staufenbiel M., Palmer T.D., Jucker M. Neurogenesis and alterations of neural stem cells in mouse models of cerebral amyloidosis. Am. J. Pathol. 2008, 172:1520-1528.
23. Esposito L., Raber J., Kekonius L., Yan F., Yu G.Q., Bien-Ly N., Puoliväli J., Scearce-Levie K., Masliah E., Mucke L. Reduction in mitochondrial superoxide dismutase modulates Alzheimer's disease-like pathology and accelerates the onset of behavioral changes in human amyloid precursor protein transgenic mice. J.Neurosci. 2006, 26:5167-5179.
24. Essers M.A., Weijzen S., de Vries-Smits A.M., Saarloos I., de Ruiter N.D., Bos J.L., Burgering B.M. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J. 2004, 23:4802-4812.
25. Faure A., Verret L., Bozon B., El Tannir El Tayara N., Ly M., Kober F., Dhenain M., Rampon C., Delatour B. Impaired neurogenesis, neuronal loss, and brain functional deficits in the APPxPS1-Ki mouse model of Alzheimer's disease. Neurobiol. Aging 2011, 32:407-418.
26. Finkel T., Holbrook N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247.
27. Gabuzda D., Busciglio J., Chen L.B., Matsudaira P., Yankner B.A. Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J.Biol. Chem. 1994, 269:13623-13628.
28. Gan L., Qiao S., Lan X., Chi L., Luo C., Lien L., Yan Liu Q., Liu R. Neurogenic responses to amyloid-beta plaques in the brain of Alzheimer's disease-like transgenic (pPDGF-APPSw,Ind) mice. Neurobiol. Dis. 2008, 29:71-80.
29. Gibson G.E., Shi Q. Amitocentric view of Alzheimer's disease suggests multi-faceted treatments. J.Alzheimers Dis. 2010, 20:S591-S607.
30. Goedert M., Spillantini M.G. Acentury of Alzheimer's disease. Science 2006, 314:777-781.
31. Goodman Y., Mattson M.P. Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury. Exp. Neurol. 1994, 128:1-12.
32. Gotoh Y., Cooper J.A. Reactive oxygen species- and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction. J.Biol. Chem. 1998, 273:17477-17482.
33. Green D.R., Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004, 305:626-629.
34. Guo Q., Sopher B.L., Furukawa K., Pham D.G., Robinson N., Martin G.M., Mattson M.P. Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide: involvement of calcium and oxyradicals. J.Neurosci. 1997, 17:4212-4222.
35. Gwon A.R., Park J.S., Arumugam T.V., Kwon Y.K., Chan S.L., Kim S.H., Baik S.H., Yang S., Yun Y.K., Choi Y., Kim S., Tang S.C., Hyun D.H., Cheng A., Dann C.E., Bernier M., Lee J., Markesbery W.R., Mattson M.P., Jo D.G. Oxidative lipid modification of nicastrin enhances amyloidogenic γ-secretase activity in Alzheimer's disease. Aging Cell 2012, 11:559-568.
36. Halagappa V.K., Guo Z., Pearson M., Matsuoka Y., Cutler R.G., Laferla F.M., Mattson M.P. Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 2007, 26:212-220.
37. Halestrap A.P. What is the mitochondrial permeability transition pore?. J.Mol. Cell Cardiol. 2009, 46:821-831.
38. Hamilton L.K., Aumont A., Julien C., Vadnais A., Calon F., Fernandes K.J. Widespread deficits in adult neurogenesis precede plaque and tangle formation in the 3xTg mouse model of Alzheimer's disease. Eur. J. Neurosci. 2010, 32:905-920.
39. Hardy J. Ahundred years of Alzheimer's disease research. Neuron 2006, 52:3-13.
40. Hashimoto T., Elder C.M., Okun M.S., Patrick S.K., Vitek J.L. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J.Neurosci. 2003, 23:1916-1923.
41. Haughey N.J., Nath A., Chan S.L., Borchard A.C., Rao M.S., Mattson M.P. Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J.Neurochem. 2002, 83:1509-1524.
42. Haughey N.J., Liu D., Nath A., Borchard A.C., Mattson M.P. Disruption of neurogenesis in the subventricular zone of adult mice, and in human cortical neuronal precursor cells in culture, by amyloid beta-peptide: implications for the pathogenesis of Alzheimer's disease. Neuromolecular Med. 2002, 1:125-135.
43. Hausenloy D., Wynne A., Duchen M., Yellon D. Transient mitochondrial permeability transition pore opening mediates preconditioning-induced protection. Circulation 2004, 109:1714-1717.
44. Hensley K., Carney J.M., Mattson M.P., Aksenova M., Harris M., Wu J.F., Floyd R.A., Butterfield D.A. Amodel for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A 1994, 91:3270-3274.
45. Hou Y., Ouyang X., Wan R., Cheng H., Mattson M.P., Cheng A. Mitochondrial superoxide production negatively regulates neural progenitor proliferation and cerebral cortical development. Stem Cells 2012, 30:2535-2547.
46. Huang X., Atwood C.S., Hartshorn M.A., Multhaup G., Goldstein L.E., Scarpa R.C., Cuajungco M.P., Gray D.N., Lim J., Moir R.D., Tanzi R.E., Bush A.I. The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 1999, 38:7609-7616.
47. Jin Y., Yan E.Z., Fan Y., Zong Z.H., Qi Z.M., Li Z. Sodium ferulate prevents amyloid-beta-induced neurotoxicity through suppression of p38 MAPK and upregulation of ERK-1/2 and Akt/protein kinase B in rat hippocampus. Acta Pharmacol. Sin. 2005, 26:943-951.
48. Jin K., Galvan V., Xie L., Mao X.O., Gorostiza O.F., Bredesen D.E., Greenberg D.A. Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw,Ind) mice. Proc. Natl. Acad. Sci. U.S.A 2004, 101:13363-13367.
49. Jo D.G., Arumugam T.V., Woo H.N., Park J.S., Tang S.C., Mughal M., Hyun D.H., Park J.H., Choi Y.H., Gwon A.R., Camandola S., Cheng A., Cai H., Song W., Markesbery W.R., Mattson M.P. Evidence that gamma-secretase mediates oxidative stress-induced beta-secretase expression in Alzheimer's disease. Neurobiol. Aging 2010, 31:917-925.
50. Keil U., Bonert A., Marques C.A., Scherping I., Weyermann J., Strosznajder J.B., Müller-Spahn F., Haass C., Czech C., Pradier L., Müller W.E., Eckert A. Amyloid beta-induced changes in nitric oxide production and mitochondrial activity lead to apoptosis. J.Biol. Chem. 2004, 279:50310-50320.
51. Keller J.N., Kindy M.S., Holtsberg F.W., St Clair D.K., Yen H.C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J.Neurosci. 1998, 18:687-697.
52. Kempermann G., Gast D., Gage F.H. Neuroplasticity in old age: sustained fivefold induction of hippocampal neurogenesis by long-term environmental enrichment. Ann. Neurol. 2002, 52:135-143.
53. Klein W.L., Krafft G.A., Finch C.E. Targeting small Aβ oligomers: the solution to an Alzheimer's disease conundrum?. Trends Neurosci. 2001, 24:219-224.
54. Kwak Y.D., Brannen C.L., Qu T., Kim H.M., Dong X., Soba P., Majumdar A., Kaplan A., Beyreuther K., Sugaya K. Amyloid precursor protein regulates differentiation of human neural stem cells. Stem Cells Dev. 2006, 15:381-389.
55. Lathia J.D., Rao M.S., Mattson M.P., Ffrench-Constant C. The microenvironment of the embryonic neural stem cell: lessons from adult niches?. Dev. Dyn. 2007, 236:3267-3282.
56. Lathia J.D., Okun E., Tang S.C., Griffioen K., Cheng A., Mughal M.R., Laryea G., Selvaraj P.K., ffrench-Constant C., Magnus T., Arumugam T.V., Mattson M.P. Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J.Neurosci. 2008, 28:13978-13984.
57. Lazarov O., Mattson M.P., Peterson D.A., Pimplikar S.W., van Praag H. When neurogenesis encounters aging and disease. Trends Neurosci. 2010, 33:569-579.
58. Lee J., Duan W., Mattson M.P. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J.Neurochem. 2002, 82:1367-1375.
59. Lustbader J.W., Cirilli M., Lin C., Xu H.W., Takuma K., Wang N., Caspersen C., Chen X., Pollak S., Chaney M., Trinchese F., Liu S., Gunn-Moore F., Lue L.F., Walker D.G., Kuppusamy P., Zewier Z.L., Arancio O., Stern D., Yan S.S., Wu H. ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 2004, 304:448-452.
60. Ma D.K., Kim W.R., Ming G.L., Song H. Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis. Ann. N. Y. Acad. Sci. 2009, 1170:664-673.
61. Mark R.J., Hensley K., Butterfield D.A., Mattson M.P. Amyloid beta-peptide impairs ion-motive ATPase activities: evidence for a role in loss of neuronal Ca2+ homeostasis and cell death. J.Neurosci. 1995, 15:6239-6249.
62. Mark R.J., Pang Z., Geddes J.W., Uchida K., Mattson M.P. Amyloid beta-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J.Neurosci. 1997, 17:1046-1054.
63. Martinou J.C., Green D.R. Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell. Biol. 2001, 2:63-67.
64. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
65. Mattson M.P., Gleichmann M., Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 2008, 60:748-766.
66. Mazur-Kolecka B., Golabek A., Nowicki K., Flory M., Frackowiak J. Amyloid-beta impairs development of neuronal progenitor cells by oxidative mechanisms. Neurobiol. Aging 2006, 27:1181-1192.
67. Mirochnic S., Wolf S., Staufenbiel M., Kempermann G. Age effects on the regulation of adult hippocampal neurogenesis by physical activity and environmental enrichment in the APP23 mouse model of Alzheimer disease. Hippocampus 2009, 19:1008-1018.
68. Murphy E., Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol. Rev. 2008, 88:581-609.
69. Owusu-Ansah E., Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 2009, 461:537-541.
70. Parachikova A., Nichol K.E., Cotman C.W. Short-term exercise in aged Tg2576 mice alters neuroinflammation and improves cognition. Neurobiol. Dis. 2008, 30:121-129.
71. Pendergrass W., Wolf N., Poot M. Efficacy of MitoTracker Green and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry A 2004, 61:162-169.
72. Petronilli V., Miotto G., Canton M., Brini M., Colonna R., Bernardi P., Di Lisa F. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys. J. 1999, 76:725-734.
73. Rasola A., Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 2007, 12:815-833.
74. Rodríguez J.J., Jones V.C., Tabuchi M., Allan S.M., Knight E.M., LaFerla F.M., Oddo S., Verkhratsky A. Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer's disease. PLoS One 2008, 3:e2935.
75. Samuels I.S., Karlo J.C., Faruzzi A.N., Pickering K., Herrup K., Sweatt J.D., Saitta S.C., Landreth G.E. Deletion of ERK2 mitogen-activated protein kinase identifies its key roles in cortical neurogenesis and cognitive function. J.Neurosci. 2008, 28:6983-6995.
76. Schieke S.M., Phillips D., McCoy J.P., Aponte A.M., Shen R.F., Balaban R.S., Finkel T. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J.Biol. Chem. 2006, 281:27643-27652.
77. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., Sabatini B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J.Neurosci. 2007, 27:2866-2875.
78. Shruster A., Eldar-Finkelman H., Melamed E., Offen D. Wnt signaling pathway overcomes the disruption of neuronal differentiation of neural progenitor cells induced by oligomeric amyloid ß-peptide. J.Neurochem. 2010, 116:522-529.
79. Sotthibundhu A., Li Q.X., Thangnipon W., Coulson E.J. Abeta(1-42) stimulates adult SVZ neurogenesis through the p75 neurotrophin receptor. Neurobiol. Aging 2009, 30:1975-1985.
80. Tamagno E., Robino G., Obbili A., Bardini P., Aragno M., Parola M., Danni O. H2O2 and 4-hydroxynonenal mediate amyloid beta-induced neuronal apoptosis by activating JNKs and p38MAPK. Exp. Neurol. 2003, 180:144-155.
81. Tamagno E., Guglielmotto M., Aragno M., Borghi R., Autelli R., Giliberto L., Muraca G., Danni O., Zhu X., Smith M.A., Perry G., Jo D.G., Mattson M.P., Tabaton M. Oxidative stress activates a positive feedback between the gamma- and beta-secretase cleavages of the beta-amyloid precursor protein. J.Neurochem. 2008, 104:683-695.
82. van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 1999, 2:266-270.
83. Verret L., Jankowsky J.L., Xu G.M., Borchelt D.R., Rampon C. Alzheimer's-type amyloidosis in transgenic mice impairs survival of newborn neurons derived from adult hippocampal neurogenesis. J.Neurosci. 2007, 27:6771-6780.
84. Wang W., Fang H., Groom L., Cheng A., Zhang W., Liu J., Wang X., Li K., Han P., Zheng M., Yin J., Wang W., Mattson M.P., Kao J.P., Lakatta E.G., Sheu S.S., Ouyang K., Chen J., Dirksen R.T., Cheng H. Superoxide flashes in single mitochondria. Cell 2008, 134:279-290.
85. Wen P.H., Hof P.R., Chen X., Gluck K., Austin G., Younkin S.G., Younkin L.H., DeGasperi R., Gama Sosa M.A., Robakis N.K., Haroutunian V., Elder G.A. The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp. Neurol. 2004, 188:224-237.
86. Zhang C., McNeil E., Dressler L., Siman R. Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer's disease. Exp. Neurol. 2007, 204:77-87.
87. Zhao Y., Xiao Z., Gao Y., Chen B., Zhao Y., Zhang J., Dai J. Insulin rescues ES cell-derived neural progenitor cells from apoptosis by differential regulation of Akt and ERK pathways. Neurosci. Lett. 2007, 429:49-54.
88. Zhou L., Miller C.A. Mitogen-activated protein kinase signaling, oxygen sensors and hypoxic induction of neurogenesis. Neurodegener Dis. 2006, 3:50-55.
89. Zoratti M., Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta 1995, 1241:139-176.