Neurobiology of Aging
Volume 30, Issue 10 , Pages 1587-1600 , October 2009

Thiamine deficiency induces oxidative stress and exacerbates the plaque pathology in Alzheimer's mouse model

  • Saravanan S. Karuppagounder

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • ,
  • Hui Xu

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • ,
  • Qingli Shi

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • ,
  • Lian H. Chen

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • ,
  • Steve Pedrini

      Affiliations

    • Thomas Jefferson University, Farber Institute for the Neurosciences, 900 Walnut Street, Suite 467, Philadelphia, PA 19107, United States
    • ,
  • David Pechman

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • ,
  • Harriet Baker

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • ,
  • M. Flint Beal

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, 525E, 68th Street, New York, NY 10021, United States
    • ,
  • Sam E. Gandy

      Affiliations

    • Thomas Jefferson University, Farber Institute for the Neurosciences, 900 Walnut Street, Suite 467, Philadelphia, PA 19107, United States
    • ,
  • Gary E. Gibson

      Affiliations

    • Department of Neurology and Neurosciences, Weill Medical College of Cornell University, Burke Medical Research Institute, 785 Mamaroneck Avenue, White Plains, NY 10605, United States
    • Corresponding Author InformationCorresponding author. Tel.: +1 914 597 2291; fax: +1 914 597 2757.

Received 24 May 2007 ,Revised 11 December 2007 ,Accepted 14 December 2007.

References 

  1. Abrahamson EE, Ikonomovic MD, Ciallella JR, Hope CE, Paljug WR, Isanski BA, et al. Caspase inhibition therapy abolishes brain trauma-induced increases in Abeta peptide: implications for clinical outcome. Exp. Neurol. 2006;197(2):437–450
  2. Beeson JG, Shelton ER, Chan HW, Gage FH. Age and damage induced changes in amyloid protein precursor immunohistochemistry in the rat brain. J. Comp. Neurol. 1994;342(1):69–77
  3. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron. 1997;19(4):939–945
  4. Boren J, Ramos-Montoya A, Bosch KS, Vreeling H, Jonker A, Centelles JJ, et al. In situ localization of transketolase activity in epithelial cells of different rat tissues and subcellularly in liver parenchymal cells. J. Histochem. Cytochem. 2006;54(2):191–199
  5. Bubber P, Ke ZJ, Gibson GE. Tricarboxylic acid cycle enzymes following thiamine deficiency. Neurochem. Int. 2004;45(7):1021–1028
  6. Bubber P, Haroutunian V, Fisch G, Blass JP, Gibson GE. Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann. Neurol. 2005;57(5):695–703
  7. Bush AI, Pettingell WH, Multhaup G, d Paradis M, Vonsattel JP, Gusella JF, et al. Rapid induction of Alzheimer A beta amyloid formation by zinc. Science. 1994;265(5177):1464–1467
  8. Buxbaum JD, Thinakaran G, Koliatsos V, O’Callahan J, Slunt HH, Price DL, et al. Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J. Neurosci. 1998;18(23):9629–9637
  9. Calingasan NY, Gandy SE, Baker H, Sheu KF, Kim KS, Wisniewski HM, et al. Accumulation of amyloid precursor protein-like immunoreactivity in rat brain in response to thiamine deficiency. Brain Res. 1995;677(1):50–60
  10. Calingasan NY, Gandy SE, Baker H, Sheu KF, Smith JD, Lamb BT, et al. Novel neuritic clusters with accumulations of amyloid precursor protein and amyloid precursor-like protein 2 immunoreactivity in brain regions damaged by thiamine deficiency. Am. J. Pathol. 1996;149(3):1063–1071
  11. Calingasan NY, Gandy SE, Gibson GE. Thiamine deficiency alters APP but not presenilin-1 immunoreactivity in vulnerable brain regions. Neuroreport. 1997;8(11):2631–2634
  12. Calingasan NY, Chun WJ, Park LC, Uchida K, Gibson GE. Oxidative stress is associated with region-specific neuronal death during thiamine deficiency. J. Neuropathol. Exp. Neurol. 1999;58(9):946–958
  13. Calingasan NY, Huang PL, Chun HS, Fabian A, Gibson GE. Vascular factors are critical in selective neuronal loss in an animal model of impaired oxidative metabolism. J. Neuropathol. Exp. Neurol. 2000;59(3):207–217
  14. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, et al. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 2001;276(24):21562–21570
  15. Chornyy S, Parkhomenko J, Chorna N. Thiamine deficiency caused by thiamine antagonists triggers upregulation of apoptosis inducing factor gene expression and leads to caspase 3-mediated apoptosis in neuronally differentiated rat PC-12 cells. Acta Biochim. Pol. 2007;54(2):315–322
  16. Conte V, Uryu K, Fujimoto S, Yao Y, Rokach J, Longhi L, et al. Vitamin E reduces amyloidosis and improves cognitive function in Tg2576 mice following repetitive concussive brain injury. J. Neurochem. 2004;90(3):758–764
  17. Cullen KM, Halliday GM. Neurofibrillary tangles in chronic alcoholics. Neuropathol. Appl. Neurobiol. 1995;21(4):312–318
  18. de Vrij FM, Fischer DF, van Leeuwen FW, Hol EM. Protein quality control in Alzheimer's disease by the ubiquitin proteasome system. Prog. Neurobiol. 2004;74(5):249–270
  19. Estus S, Golde TE, Kunishita T, Blades D, Lowery D, Eisen M, et al. Potentially amyloidogenic, carboxyl-terminal derivatives of the amyloid protein precursor. Science. 1992;255(5045):726–728
  20. Gabuzda D, Busciglio J, Chen LB, Matsudaira P, Yankner BA. Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J. Biol. Chem. 1994;269(18):13623–13628
  21. Gallant M, Rak M, Szeghalmi A, Del Bigio MR, Westaway D, Yang J, et al. Focally elevated creatine detected in amyloid precursor protein (APP) transgenic mice and Alzheimer disease brain tissue. J. Biol. Chem. 2006;281(1):5–8
  22. Gandy S. The role of cerebral amyloid beta accumulation in common forms of Alzheimer disease. J. Clin. Invest. 2005;115(5):1121–1129
  23. Gandy S, Doeven MK, Poolman B. Alzheimer disease: presenilin springs a leak. Nat. Med. 2006;12(10):1121–1123
  24. Gibson G, Blass J. Thiamine-dependent processes and treatment strategies in neurodegenerations. Antioxid. Redox. Signal. 2007;9(10):1605–1619
  25. Gibson GE, Huang HM. Mitochondrial enzymes and endoplasmic reticulum calcium stores as targets of oxidative stress in neurodegenerative diseases. J. Bioenerg. Biomembr. 2004;36(4):335–340
  26. Gibson G, Barclay L, Blass J. The role of the cholinergic system in thiamin deficiency. Ann. N.Y. Acad. Sci. 1982;378:382–403
  27. Gibson GE, Sheu KF, Blass JP, Baker A, Carlson KC, Harding B, et al. Reduced activities of thiamine-dependent enzymes in the brains and peripheral tissues of patients with Alzheimer's disease. Arch. Neurol. 1988;45(8):836–840
  28. Gibson GE, Haroutunian V, Zhang H, Park LC, Shi Q, Lesser M, et al. Mitochondrial damage in Alzheimer's disease varies with apolipoprotein E genotype. Ann. Neurol. 2000;48(3):297–303
  29. Gibson GE, Blass JP, Beal MF, Bunik V. The alpha-ketoglutarate-dehydrogenase complex: a mediator between mitochondria and oxidative stress in neurodegeneration. Mol. Neurobiol. 2005;31(1–3):43–63
  30. Golde TE, Estus S, Younkin LH, Selkoe DJ, Younkin SG. Processing of the amyloid protein precursor to potentially amyloidogenic derivatives. Science. 1992;255(5045):728–730
  31. Gotz J, Chen F, van Dorpe J, Nitsch RM. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science. 2001;293(5534):1491–1495
  32. Gotz J, Ittner LM, Schonrock N. Alzheimer's disease and frontotemporal dementia: prospects of a tailored therapy?. Med. J. Aust. 2006;185(7):381–384
  33. Halliday G, Cullen K, Harding A. Neuropathological correlates of memory dysfunction in the Wernicke–Korsakoff syndrome. Alcohol Alcohol. 1994;2:245–251
  34. Karuppagounder S, Shi Q, Xu H, Gibson GE. Changes in inflammatory processes associated with selective vulnerability following mild impairment of oxidative metabolism. Neurobiol. Dis. 2007;26:353–362
  35. Ke ZJ, Gibson GE. Selective response of various brain cell types during neurodegeneration induced by mild impairment of oxidative metabolism. Neurochem. Int. 2004;45(2–3):361–369
  36. Ke ZJ, DeGiorgio LA, Volpe BT, Gibson GE. Reversal of thiamine deficiency-induced neurodegeneration. J. Neuropathol. Exp. Neurol. 2003;62(2):195–207
  37. Li F, Calingasan NY, Yu F, Mauck WM, Toidze M, Almeida CG, et al. Increased plaque burden in brains of APP mutant MnSOD heterozygous knockout mice. J. Neurochem. 2004;89(5):1308–1312
  38. Liu JY, Timm DE, Hurley TD. Pyrithiamine as a substrate for thiamine pyrophosphokinase. J. Biol. Chem. 2006;281(10):6601–6607
  39. Mair RG. On the role of thalamic pathology in diencephalic amnesia. Rev. Neurosci. 1994;5(2):105–140
  40. McGuinness MP, Orth JM. Gonocytes of male rats resume migratory activity postnatally. Eur. J. Cell Biol. 1992;59(1):196–210
  41. Melov S, Adlard PA, Morten K, Johnson F, Golden TR, Hinerfeld D, et al. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS ONE. 2007;2(6):e536
  42. Morre DJ, Lawrence J, Safranski K, Hammond T, Morre DM. Experimental basis for separation of membrane vesicles by preparative free-flow electrophoresis. J. Chromatogr A. 1994;668(1):201–213
  43. Nathan C, Calingasan N, Nezezon J, Ding A, Lucia MS, La Perle K, et al. Protection from Alzheimer's-like disease in the mouse by genetic ablation of inducible nitric oxide synthase. J. Exp. Med. 2005;202(9):1163–1169
  44. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron. 2003;39(3):409–421
  45. Puchtler H, Sweat F. Congo red as a stain for fluorescence microscopy of amyloid. J. Histochem. Cytochem. 1965;13(8):693–694
  46. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, et al. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci. 2005;25(46):10637–10647
  47. Santiard-Baron D, Langui D, Delehedde M, Delatour B, Schombert B, Touchet N, et al. Expression of human FE65 in amyloid precursor protein transgenic mice is associated with a reduction in beta-amyloid load. J. Neurochem. 2005;93(2):330–338
  48. 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(3):279–288
  49. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, Sena-Esteves M, et al. Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron. 2007;54(5):721–737
  50. Uryu K, Laurer H, McIntosh T, Pratico D, Martinez D, Leight S, et al. Repetitive mild brain trauma accelerates Abeta deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis. J. Neurosci. 2002;22(2):446–454
  51. Velliquette RA, O’Connor T, Vassar R. Energy inhibition elevates beta-secretase levels and activity and is potentially amyloidogenic in APP transgenic mice: possible early events in Alzheimer's disease pathogenesis. J. Neurosci. 2005;25(47):10874–10883
  52. Wang JJ, Hua Z, Fentress HM, Singleton CK. JNK1 is inactivated during thiamine deficiency-induced apoptosis in human neuroblastoma cells. J. Nutr. Biochem. 2000;11(4):208–215
  53. Wang J, Tanila H, Puolivali J, Kadish I, van Groen T. Gender differences in the amount and deposition of amyloidbeta in APPswe and PS1 double transgenic mice. Neurobiol. Dis. 2003;14(3):318–327
  54. Wang X, Wang B, Fan Z, Shi X, Ke ZJ, Luo J. Thiamine deficiency induces endoplasmic reticulum stress in neurons. Neuroscience. 2007;144(3):1045–1056
  55. Yamamoto M, Kiyota T, Horiba M, Buescher JL, Walsh SM, Gendelman HE, et al. Interferon-gamma and tumor necrosis factor-alpha regulate amyloid-beta plaque deposition and beta-secretase expression in Swedish mutant APP transgenic mice. Am. J. Pathol. 2007;170(2):680–692
  56. Yao J, Petanceska SS, Montine TJ, Holtzman DM, Schmidt SD, Parker CA, et al. Aging, gender and APOE isotype modulate metabolism of Alzheimer's Abeta peptides and F-isoprostanes in the absence of detectable amyloid deposits. J. Neurochem. 2004;90(4):1011–1018

PII: S0197-4580(07)00488-5

doi: 10.1016/j.neurobiolaging.2007.12.013

Neurobiology of Aging
Volume 30, Issue 10 , Pages 1587-1600 , October 2009

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