Neurobiology of Aging
Volume 29, Issue 7 , Pages 969-980 , July 2008

Oxidative stress triggers the amyloidogenic pathway in human vascular smooth muscle cells

  • Mireia Coma

      Affiliations

    • Laboratory of Molecular Physiology and Channelopathies, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain
  • ,
  • Francesc X. Guix

      Affiliations

    • Laboratory of Molecular Physiology and Channelopathies, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain
  • ,
  • Gerard Ill-Raga

      Affiliations

    • Laboratory of Molecular Physiology and Channelopathies, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain
  • ,
  • Iris Uribesalgo

      Affiliations

    • Laboratory of Molecular Physiology and Channelopathies, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain
  • ,
  • Francesc Alameda

      Affiliations

    • Servei d′Anatomia Patològica, Hospital del Mar, Universitat Autònoma de Barcelona, Barcelona 08003, Spain
  • ,
  • Miguel A. Valverde

      Affiliations

    • Laboratory of Molecular Physiology and Channelopathies, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain
  • ,
  • Francisco J. Muñoz

      Affiliations

    • Laboratory of Molecular Physiology and Channelopathies, Universitat Pompeu Fabra, Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain
    • Corresponding Author InformationCorresponding author at: Laboratorio de Fisiologia Molecular i Canalopaties, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, C/Dr. Aiguader, 80, Barcelona 08003, Spain. Tel.: +34 93 542 28 84; fax: +34 93 542 28 02.

Received 26 July 2006 ,Revised 1 December 2006 ,Accepted 13 January 2007.

References 

  1. Attems J. Sporadic cerebral amyloid angiopathy: pathology, clinical implications, and possible pathomechanisms. Acta Neuropathol. (Berl.). 2005;110:345–359
  2. Badger AM, Bradbeer JN, Votta B, Lee JC, Adams JL, Griswold DE. Pharmacological profile of SB 203580, a selective inhibitor of cytokine suppressive binding protein/p38 kinase, in animal models of arthritis, bone resorption, endotoxin shock and immune function. J. Pharmacol. Exp. Ther. 1996;279:1453–1461
  3. Behl C, Davis JB, Lesley R, Schubert D. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell. 1994;77:817–827
  4. Bennett BL, Sasaki DT, Murray BW, O’Leary EC, Sakata ST, Xu W, et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U S A. 2001;98:13681–13686
  5. Buxbaum JD, Liu KN, Luo Y, Slack JL, Stocking KL, Peschon JJ, et al. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 1998;273:27765–27767
  6. Castano EM, Prelli F, Soto C, Beavis R, Matsubara E, Shoji M, et al. The length of amyloid-beta in hereditary cerebral hemorrhage with amyloidosis, Dutch type. Implications for the role of amyloid-beta 1-42 in Alzheimer's disease. J. Biol. Chem. 1996;271:32185–32191
  7. Christensen MA, Zhou W, Qing H, Lehman A, Philipsen S, Song W. Transcriptional regulation of BACE1, the beta-amyloid precursor protein beta-secretase, by Sp1. Mol. Cell Biol. 2004;24:865–874
  8. Coma M, Guix FX, Uribesalgo I, Espuna G, Sole M, Andreu D, et al. Lack of oestrogen protection in amyloid-mediated endothelial damage due to protein nitrotyrosination. Brain. 2005;128:1613–1621
  9. Coria F, Moreno A, Torres A, Ahmad I, Ghiso J. Distribution of Alzheimer's disease amyloid protein precursor in normal human and rat nervous system. Neuropathol. Appl. Neurobiol. 1992;18:27–35
  10. Davis-Salinas J, Van Nostrand WE. Amyloid beta-protein aggregation nullifies its pathologic properties in cultured cerebrovascular smooth muscle cells. J. Biol. Chem. 1995;270:20887–20890
  11. Frackowiak J, Potempska A, LeVine H, Haske T, Dickson D, Mazur-Kolecka B. Extracellular deposits of A beta produced in cultures of Alzheimer disease brain vascular smooth muscle cells. J. Neuropathol. Exp. Neurol. 2005;64:82–90
  12. Frackowiak J, Sukontasup T, Potempska A, Mazur-Kolecka B. Lysosomal deposition of Abeta in cultures of brain vascular smooth muscle cells is enhanced by iron.. Brain Res. 2004;1002:67–75
  13. Frackowiak J, Zoltowska A, Wisniewski HM. Non-fibrillar beta-amyloid protein is associated with smooth muscle cells of vessel walls in Alzheimer disease. J. Neuropathol. Exp. Neurol. 1994;53:637–645
  14. Ghiso J, Frangione B. Cerebral amyloidosis, amyloid angiopathy, and their relationship to stroke and dementia. J. Alzheimers Dis. 2001;3:65–73
  15. Grabowski TJ, Cho HS, Vonsattel JP, Rebeck GW, Greenberg SM. Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann. Neurol. 2001;49:697–705
  16. Harper JD, Lansbury PT. Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu. Rev. Biochem. 1997;66:385–407
  17. Herzig MC, Van Nostrand WE, Jucker M. Mechanism of cerebral beta-amyloid angiopathy: murine and cellular models. Brain Pathol. 2006;16:40–54
  18. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004;5:347–360
  19. Lammich S, Kojro E, Postina R, Gilbert S, Pfeiffer R, Jasionowski M, et al. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl. Acad. Sci. U S A. 1999;96:3922–3927
  20. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, van Duinen SG, et al. Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science. 1990;248:1124–1126
  21. Mattson MP, Magnus T. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 2006;7:278–294
  22. McDonald DR, Bamberger ME, Combs CK, Landreth GE. beta-Amyloid fibrils activate parallel mitogen-activated protein kinase pathways in microglia and THP1 monocytes. J. Neurosci. 1998;18:4451–4460
  23. McGowan E, Pickford F, Kim J, Onstead L, Eriksen J, Yu C, et al. Abeta42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron. 2005;47:191–199
  24. Miao J, Vitek MP, Xu F, Previti ML, Davis J, Van Nostrand WE. Reducing cerebral microvascular amyloid-beta protein deposition diminishes regional neuroinflammation in vasculotropic mutant amyloid precursor protein transgenic mice. J. Neurosci. 2005;25:6271–6277
  25. Mielke K, Herdegen T. JNK and p38 stresskinases—degenerative effectors of signal-transduction-cascades in the nervous system. Prog. Neurobiol. 2000;61:45–60
  26. Miranda S, Opazo C, Larrondo LF, Munoz FJ, Ruiz F, Leighton F, et al. The role of oxidative stress in the toxicity induced by amyloid beta-peptide in Alzheimer's disease. Prog. Neurobiol. 2000;62:633–648
  27. Misonou H, Morishima-Kawashima M, Ihara Y. Oxidative stress induces intracellular accumulation of amyloid beta-protein (Abeta) in human neuroblastoma cells. Biochemistry. 2000;39:6951–6959
  28. Munoz FJ, Opazo C, Gil-Gomez G, Tapia G, Fernandez V, Valverde MA, et al. Vitamin E but not 17 beta-estradiol protects against vascular toxicity induced by beta-amyloid wild type and the Dutch amyloid variant. J. Neurosci. 2002;22:3081–3089
  29. Perry G, Roder H, Nunomura A, Takeda A, Friedlich AL, Zhu X, et al. Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport. 1999;10:2411–2415
  30. Rouse J, Cohen P, Trigon S, Morange M, Alonso-Llamazares A, Zamanillo D, et al. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell. 1994;78:1027–1037
  31. Sambamurti K, Kinsey R, Maloney B, Ge YW, Lahiri DK. Gene structure and organization of the human beta-secretase (BACE) promoter. FASEB J. 2004;18:1034–1036
  32. Selkoe DJ. The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell Biol. 1998;8:447–453
  33. Shinkai Y, Yoshimura M, Ito Y, Odaka A, Suzuki N, Yanagisawa K, et al. Amyloid beta-proteins 1–40 and 1–42(43) in the soluble fraction of extra- and intracranial blood vessels. Ann. Neurol. 1995;38:421–428
  34. Smith MA, Nunomura A, Zhu X, Takeda A, Perry G. Metabolic, metallic, and mitotic sources of oxidative stress in Alzheimer disease. Antioxid. Redox. Signal. 2000;2:413–420
  35. Tamagno E, Bardini P, Obbili A, Vitali A, Borghi R, Zaccheo D, et al. Oxidative stress increases expression and activity of BACE in NT2 neurons. Neurobiol. Dis. 2002;10:279–288
  36. Tamagno E, Guglielmotto M, Bardini P, Santoro G, Davit A, Di Simone D, et al. Dehydroepiandrosterone reduces expression and activity of BACE in NT2 neurons exposed to oxidative stress. Neurobiol. Dis. 2003;14:291–301
  37. Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, Guglielmotto M, et al. Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J. Neurochem. 2005;92:628–636
  38. Tamagno E, Robino G, Obbili A, Bardini P, Aragno M, Parola M, et al. H2O2 and 4-hydroxynonenal mediate amyloid beta-induced neuronal apoptosis by activating JNKs and p38MAPK. Exp. Neurol. 2003;180:144–155
  39. Tong XK, Nicolakakis N, Kocharyan A, Hamel E. Vascular remodeling versus amyloid beta-induced oxidative stress in the cerebrovascular dysfunctions associated with Alzheimer's disease. J. Neurosci. 2005;25:11165–11174
  40. Tong Y, Zhou W, Fung V, Christensen MA, Qing H, Sun X, et al. Oxidative stress potentiates BACE1 gene expression and Abeta generation. J. Neural Transm. 2004;
  41. Tournier C, Thomas G, Pierre J, Jacquemin C, Pierre M, Saunier B. Mediation by arachidonic acid metabolites of the H2O2-induced stimulation of mitogen-activated protein kinases (extracellular-signal-regulated kinase and c-Jun NH2-terminal kinase). Eur. J. Biochem. 1997;244:587–595
  42. van Dorpe J, Smeijers L, Dewachter I, Nuyens D, Spittaels K, Van Den HC, et al. Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the london mutant of human APP in neurons. Am. J. Pathol. 2000;157:1283–1298
  43. van Duinen SG, Castano EM, Prelli F, Bots GT, Luyendijk W, Frangione B. Hereditary cerebral hemorrhage with amyloidosis in patients of Dutch origin is related to Alzheimer disease. Proc. Natl. Acad. Sci. U S A. 1987;84:5991–5994
  44. Van Nostrand WE, Melchor J, Wagner M, Davis J. Cerebrovascular smooth muscle cell surface fibrillar A beta. Alteration of the proteolytic environment in the cerebral vessel wall. Ann. N Y Acad. Sci. 2000;903:89–96
  45. Van Nostrand WE, Melchor JP, Ruffini L. Pathologic amyloid beta-protein cell surface fibril assembly on cultured human cerebrovascular smooth muscle cells. J. Neurochem. 1998;70:216–223
  46. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 1999;286:735–741
  47. Wang X, Martindale JL, Liu Y, Holbrook NJ. The cellular response to oxidative stress: influences of mitogen-activated protein kinase signaling pathways on cell survival. Biochem. J. 1998;333(Pt 2):291–300
  48. Wisniewski HM, Frackowiak J, Mazur-Kolecka B. In vitro production of beta-amyloid in smooth muscle cells isolated from amyloid angiopathy-affected vessels. Neurosci. Lett. 1995;183:120–123
  49. Wisniewski HM, Wegiel J, Vorbrodt AW, Mazur-Kolecka B, Frackowiak J. Role of perivascular cells and myocytes in vascular amyloidosis. Ann. N Y Acad. Sci. 2000;903:6–18
  50. Wisniewski T, Ghiso J, Frangione B. Peptides homologous to the amyloid protein of Alzheimer's disease containing a glutamine for glutamic acid substitution have accelerated amyloid fibril formation. Biochem. Biophys. Res. Commun. 1991;180:1528
  51. Wolfe MS, Haass C. The Role of presenilins in gamma-secretase activity. J. Biol. Chem. 2001;276:5413–5416
  52. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT, Selkoe DJ. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature. 1999;398:513–517
  53. Zhu X, Castellani RJ, Takeda A, Nunomura A, Atwood CS, Perry G, et al. Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer disease: the ‘two hit’ hypothesis. Mech. Ageing Dev. 2001;123:39–46
  54. Zhu X, Lee HG, Raina AK, Perry G, Smith MA. The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals. 2002;11:270–281
  55. Zlokovic BV. Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends. Neurosci. 2005;28:202–208

PII: S0197-4580(07)00011-5

doi: 10.1016/j.neurobiolaging.2007.01.009

Neurobiology of Aging
Volume 29, Issue 7 , Pages 969-980 , July 2008