Neurobiology of Aging
Volume 27, Issue 7 , Pages 918-925 , July 2006

Oxidative modification and down-regulation of Pin1 in Alzheimer's disease hippocampus: A redox proteomics analysis

  • Rukhsana Sultana

      Affiliations

    • Department of Chemistry, University of Kentucky, Lexington, KY 40506, USA
    • Center of Membrane Sciences, University of Kentucky, Lexington, KY 40506, USA
  • ,
  • Debra Boyd-Kimball

      Affiliations

    • Department of Chemistry, University of Kentucky, Lexington, KY 40506, USA
    • Center of Membrane Sciences, University of Kentucky, Lexington, KY 40506, USA
  • ,
  • H. Fai Poon

      Affiliations

    • Department of Chemistry, University of Kentucky, Lexington, KY 40506, USA
    • Center of Membrane Sciences, University of Kentucky, Lexington, KY 40506, USA
  • ,
  • Jain Cai

      Affiliations

    • Department of Pharmacology, University of Louisville, School of Medicine and VAMC, Louisville, KY, USA
  • ,
  • William M. Pierce

      Affiliations

    • Department of Pharmacology, University of Louisville, School of Medicine and VAMC, Louisville, KY, USA
  • ,
  • Jon B. Klein

      Affiliations

    • Core Proteomics Laboratory, University of Louisville, Louisville, KY, USA
  • ,
  • William R. Markesbery

      Affiliations

    • Center of Membrane Sciences, University of Kentucky, Lexington, KY 40506, USA
    • Departments of Neurology and Pathology, University of Kentucky, Lexington, KY 40536, USA
  • ,
  • Xiao Zhen Zhou

      Affiliations

    • Cancer Biology Program, Department of Medicine, Beth Israel Deaconess Medical Centre, Harvard Medical School, Boston, MA 02115, USA
  • ,
  • Kun Ping Lu

      Affiliations

    • Cancer Biology Program, Department of Medicine, Beth Israel Deaconess Medical Centre, Harvard Medical School, Boston, MA 02115, USA
  • ,
  • D. Allan Butterfield

      Affiliations

    • Department of Chemistry, University of Kentucky, Lexington, KY 40506, USA
    • Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY 40506, USA
    • Center of Membrane Sciences, University of Kentucky, Lexington, KY 40506, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 859 257 3184; fax: +1 859 257 5876.

Received 3 December 2004 ,Revised 25 April 2005 ,Accepted 2 May 2005.

References 

  1. Aksenov M, Aksenova M, Butterfield DA, Markesbery WR. Oxidative modification of creatine kinase BB in Alzheimer's disease brain. J Neurochem. 2000;74(6):2520–2527
  2. Alonso A, Zaidi T, Novak M, Grundke-Iqbal I, Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA. 2001;98(12):6923–6928
  3. Boguski MS, McIntosh MW. Biomedical informatics for proteomics. Nature. 2003;422:233–237
  4. Braak E, Braak H. Alzheimer's disease: transiently developing dendritic changes in pyramidal cells of sector CA1 of the Ammon's horn. Acta Neuropathol (Berl). 1997;93(4):323–325
  5. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol (Berl). 1994;87(6):554–567
  6. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev. 2000;33(1):95–130
  7. Butterfield DA. Proteomics: a new approach to investigate oxidative stress in Alzheimer's disease brain. Brain Res. 2004;1000(1–2):1–7
  8. Butterfield DA, Boyd-Kimball D, Castegna A. Proteomics in Alzheimer's disease: insights into potential mechanisms of neurodegeneration. J Neurochem. 2003;86(6):1313–1327
  9. Butterfield DA, Kanski J. Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech Ageing Dev. 2001;122(9):945–962
  10. Butterfield DA, Lauderback CM. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic Biol Med. 2002;32(11):1050–1060
  11. Butterfield DA, Stadtman ER. Protein oxidation processes in aging brain. Adv Cell Aging Gerontol. 1997;2:161–191
  12. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, Pierce WM, et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med. 2002;33(4):562–571
  13. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, et al. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem. 2002;82(6):1524–1532
  14. Castegna A, Thongboonkerd V, Klein J, Lynn BC, Wang YL, Osaka H, et al. Proteomic analysis of brain proteins in the gracile axonal dystrophy (gad) mouse, a syndrome that emanates from dysfunctional ubiquitin carboxyl-terminal hydrolase L-1, reveals oxidation of key proteins. J Neurochem. 2004;88(6):1540–1546
  15. Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, Butterfield DA. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem. 2003;85(6):1394–1401
  16. Daly NL, Hoffmann R, Otvos LJ, Craik DJ. Role of phosphorylation in the conformation of tau peptides implicated in tau accumulation in Alzheimer's disease hippocampus. Acta Neuropathol (Berl). 2002;104:471–481
  17. Delacourte A. Pathological tau proteins of Alzheimer's disease as a biochemical marker of neurofibrillary degeneration. Biomed Pharmacother. 1994;48(7):287–295
  18. Delacourte A, Sergeant N, Wattez A, Maurage CA, Lebert F, Pasquier F, et al. Tau aggregation in the hippocampal formation: an ageing or a pathological process?. Exp Gerontol. 2002;37(10–11):1291–1296
  19. Devasahayam G, Chaturvedi V, Hanes SD. The Ess1 prolyl isomerase is required for growth and morphogenetic switching in Candida albicans. Genetics. 2002;160(1):37–48
  20. Goedert M. Alzheimer's disease. Pinning down phosphorylated tau. Nature. 1999;399(6738):739–740
  21. Gonzalez C, Farias G, Maccioni RB. Modification of tau to an Alzheimer's type protein interferes with its interaction with microtubules. Cell Mol Biol (Noisy-le-grand). 1998;44(7):1117–1127
  22. Grundke-Iqbal I, Iqbal K, Quinlan M, Tung YC, Zaidi MS, Wisniewski HM. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J Biol Chem. 1986;261(13):6084–6089
  23. Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, et al. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J Neurochem. 1995;65(5):2146–2156
  24. Holzer M, Gartner U, Stobe A, Hartig W, Gruschka H, Bruckner MK, et al. Inverse association of Pin1 and tau accumulation in Alzheimer's disease hippocampus. Acta Neuropathol (Berl). 2002;104(5):471–481
  25. Kanski J, Aksenova M, Stoyanova A, Butterfield DA. Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal cell culture systems in vitro: structure–activity studies. J Nutr Biochem. 2002;13(5):273–281
  26. Katzman R, Saitoh T. Advances in Alzheimer's disease. FASEB J. 1991;5(3):278–286
  27. Kofron JL, Kuzmic P, Kishore V, Colon-Bonilla E, Rich DH. Determination of kinetic constants for peptidyl prolyl cistrans isomerases by an improved spectrophotometric assay. Biochemistry. 1991;30(25):6127–6134
  28. Korolainen MA, Goldsteins G, Alafuzoff I, Koistinaho J, Pirttila T. Proteomic analysis of protein oxidation in Alzheimer's disease brain. Electrophoresis. 2002;23:3428–3433
  29. Kurt MA, Davies DC, Kidd M, Duff K, Howlett DR. Hyperphosphorylated tau and paired helical filament-like structures in the brains of mice carrying mutant amyloid precursor protein and mutant presenilin-1 transgenes. Neurobiol Dis. 2003;14(1):89–97
  30. Larner AJ. The cerebellum in Alzheimer's disease. Dement Geriatr Cogn Disord. 1997;8(4):203–209
  31. Lauderback CM, Hackett JM, Huang FF, Keller JN, Szweda LI, Markesbery WR, et al. The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42. J Neurochem. 2001;78(2):413–416
  32. Lee VM, Geodert M, Trojanowski JQ. Neurodegenerative tauopathies. Annu Rev Neurosci 2001;24:1121–59.
  33. Levine RL, Williams JA, Stadtman ER, Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994;233:346–357
  34. Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, et al. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature. 2003;424(6948):556–561
  35. Lu KP, Hanes SD, Hunter T. A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature. 1996;380(6574):544–547
  36. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature. 1999;399(6738):784–788
  37. Mandelkow EM, Stamer K, Vogel R, Thies E, Mandelkow E. Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses. Neurobiol Aging. 2003;24(8):1079–1085
  38. Markesbery WR. Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med. 1997;23(1):134–147
  39. Maurer MH, Feldmann RE, Bromme JO, Kalenka A. Comparison of statistical approaches for the analysis of proteome expression data of differentiating neural stem cells. J Proteome Res. 2005;4:96–100
  40. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 1984;34(7):939–944
  41. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Watanabe A, et al. Hyperphosphorylation of tau in PHF. Neurobiol Aging. 1995;16(3):365–371[discussion 371–380]
  42. Nagy Z, Esiri MM, Cato AM, Smith AD. Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol (Berl). 1997;94(1):6–15
  43. Picklo MJ, Montine TJ, Amarnath V, Neely MD. Carbonyl toxicology and Alzheimer's disease. Toxicol Appl Pharmacol. 2002;184(3):187–197
  44. Poon HF, Calabrese V, Scapagnini G, Butterfield DA. Free radicals and brain aging. Clin Geriatr Med. 2004;20(2):329–359
  45. Ramakrishnan P, Dickson DW, Davies P. Pin1 colocalization with phosphorylated tau in Alzheimer's disease and other tauopathies. Neurobiol Dis. 2003;14(2):251–264
  46. Schutkowski M, Bernhardt A, Zhou XZ, Shen M, Reimer U, Rahfeld JU, et al. Role of phosphorylation in determining the backbone dynamics of the serine/threonine-proline motif and Pin1 substrate recognition. Biochemistry. 1998;37(16):5566–5575
  47. Shen M, Stukenberg PT, Kirschner MW, Lu KP. The essential mitotic peptidyl-prolyl isomerase Pin1 binds and regulates mitosis-specific phosphoproteins. Genes Dev. 1998;12(5):706–720
  48. Smith MA. Alzheimer disease. Int Rev Neurobiol. 1998;42:1–54
  49. Smith PD, O’Hare MJ, Park DS. Emerging pathogenic role for cyclin dependent kinases in neurodegeneration. Cell Cycle. 2004;3(3):289–291
  50. Spillantini MG, Goedert M. Tau protein pathology in neurodegenerative diseases. Trends Neurosci. 1998;21(10):428–433
  51. Stadtman ER. Protein oxidation and aging. Science. 1992;257(5074):1220–1224
  52. Stadtman ER, Berlett BS. Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol. 1997;10(5):485–494
  53. Stamer K, Vogel R, Thies E, Mandelkow E, Mandelkow EM. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol. 2002;156(6):1051–1063
  54. Sultana R, Butterfield DA. Oxidatively modified GST and MRP1 in Alzheimer's disease brain: implications for accumulation of reactive lipid peroxidation products. Neurochem Res. 2004;29(12):2215–2220
  55. Sze CI, Su M, Pugazhenthi S, Jambal P, Hsu LJ, Heath J, et al. Down-regulation of WW domain-containing oxidoreductase induces tau phosphorylation in vitro. A potential role in Alzheimer's disease. J Biol Chem. 2004;279(29):30498–30506
  56. Thal DR, Holzer M, Rub U, Waldmann G, Gunzel S, Zedlick D, et al. Alzheimer-related tau-pathology in the perforant path target zone and in the hippocampal stratum oriens and radiatum correlates with onset and degree of dementia. Exp Neurol. 2000;163(1):98–110
  57. Thongboonkerd V, Luengpailin J, Cao J, Pierce WM, Cai J, Klein JB, et al. Fluoride exposure attenuates expression of Streptococcus pyogenes virulence factors. J Biol Chem. 2002;277(19):16599–16605
  58. Wang JZ, Gong CX, Zaidi T, Grundke-Iqbal I, Iqbal K. Dephosphorylation of Alzheimer paired helical filaments by protein phosphatase-2A and -2B. J Biol Chem. 1995;270(9):4854–4860
  59. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, et al. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science. 1997;278(5345):1957–1960
  60. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, Stoller G, et al. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell. 2000;6(4):873–883

PII: S0197-4580(05)00118-1

doi: 10.1016/j.neurobiolaging.2005.05.005

Neurobiology of Aging
Volume 27, Issue 7 , Pages 918-925 , July 2006