The pathophysiology of triose phosphate isomerase dysfunction in alzheimer's disease

Histology and Histopathology

Volumn 28, Issue 1, 2013, Pages 43-51

  Tajes, Marta ^a   Guivernau, Biuse ^a   Ramos Fernández, Eva ^a   Bosch Morató, Mònica ^a   Palomer, Ernest ^a   Guix, Francesc X ^a   Muñoz, Francisco J ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Alzheimer's disease; Methylglyoxal; Nitrotyrosination; Oxidative stress; Triosephosphate isomerase

Indexed keywords

TRIOSEPHOSPHATE ISOMERASE;

ALZHEIMER DISEASE; ENZYMOLOGY; HUMAN; METABOLISM; NITROSATION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

ALZHEIMER DISEASE; HUMANS; NITROSATION; OXIDATIVE STRESS; TRIOSE-PHOSPHATE ISOMERASE;

EID: 84872179819     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (73)

1. Ahmed N., Battah S., Karachalias N., Babaei-Jadidi R., Horányi M., Baróti K., Hollan S. and Thornalley P.J. (2003). Increased formation of methylglyoxal and proteins glycation, oxidation and nitrosation in triosephosphate isomerase deficiency. Biochim. Biophys. Acta 1639, 121-132.
2. Ationu A., Humphries A., Lalloz M.R., Arya R., Wild B., Warrilow J., Morgan J., Bellinghan A.J. and Layton D.M. (1999). Reversal of metabolic block in glycolysis by enzyme replacement in triosephosphate isomerase- deficient cells. Blood 94, 3193-3198.
3. Ball M.J., Fisman M., Hachinski V., Blume W., Fox A., Kral V.A., Kirshen A.J., Fox H. and Merskey H. (1985). A new definition of Alzheimer's disease: a hippocampal dementia. Lancet 1, 14-16.
4. Beckman J.S., Beckman T.W., Chen J., Marshall P.A. and Freeman B.A. (1990). Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 87, 1620-1624.
5. Bolaños J.P., Almeida A. and Moncada S. (2010). Glycolysis: a bioenergetic or a survival pathway? Trends Biochem. Sci. 35, 145-149.
6. Bonnet D., Pavlovic S., Lehmann J. and Rommelspacher H. (2004). The strong inhibition of triosephosphate isomerase by the natural betacarbolines may explain their neurotoxic actions. Neuroscience 127, 443-453.
7. Braak E., Braak H. and Mandelkow E.M. (1994). A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. 87, 554-567.
8. Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q. and Lee V.M. (1993). Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099.
9. Butterfield D.A. and Boyd-Kimball D. (2004). Amyloid beta-peptide (1- 42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain. Pathol. 14, 426-432.
10. Butterfield D.A., Perluigi M. and Sultana R. (2006). Oxidative stress in Alzheimer's disease brain: new insights from redox proteomics. Eur. J. Pharmacol. 545, 39-50.
11. Butterfield D.A., Reed T.T., Perluigi M., De Marco C., Coccia R., Keller J.N., Markesbery W.R. and Sultana R. (2007). Elevated levels of 3-nitrotyrosine in brain from subjects with amnestic mild cognitive impairment: implications for the role of nitration in the progression of Alzheimer's disease. Brain. Res. 1148, 243-248.
12. Castegna A., Thongboonkerd V., Klein J.B., Lynn B., Markesbery W.R. and Butterfield D.A. (2003). Proteomic identification of nitrated proteins in Alzheimer's disease brain. J. Neurochem. 85, 1394-1401.
13. Coma M., Guix F.X., Uribesalgo I., Espuña G., Solé M., Andreu D. and Muñoz F.J. (2005). Lack of oestrogen protection in amyloidmediated endothelial damage due to protein nitrotyrosination. Brain 128, 1613-1621.
14. Contreras C.F., Canales M.A., Alvarez A., De Ferrari G.V. and Inestrosa N.C. (1999). Molecular modeling of the amyloid-beta-peptide using the homology to a fragment of triosephosphate isomerase that forms amyloid in vitro. Protein Eng. 12, 959-966.
15. Cuajungco M.P., Goldstein L.E., Nunomura A., Smith M.A., Lim J.T., Atwood C.S., Huang X., Farrag Y.W., Perry G. and Bush A.I. (2000). Evidence that the beta-amyloid plaques of Alzheimer's disease represent the redox-silencing and entombment of abeta by zinc. J Biol. Chem. 275, 19439-19442.
16. Di Monte D.A., Chan P. and Sandy M.S. (1992). Glutathione in Parkinson's disease: a link between oxidative stress and mitochondrial damage?. Ann. Neurol. 32 Suppl 111-115.
17. Eber S.W., Pekrun A., Bardosi A., Gahr M., Krietsch W.K., Krüger J., Matthei R. and Schröter W. (1991). Triosephosphate isomerase deficiency: haemolytic anaemia, myopathy with altered mitochondria and mental retardation due to a new variant with accelerated enzyme catabolism and diminished specific activity. Eur. J. Pediatr. 150, 761-766.
18. Guix F.X., Uribesalgo I., Coma M. and Muñoz F.J. (2005). The physiology and pathophysiology of nitric oxide in the brain. Prog. Neurobiol, 76, 126-152.
19. Guix F.X., Ill-Raga G., Bravo R., Nakaya T., de Fabritis G., Coma M., Miscione G.P., Villà-Freixa J., Suzuki T., Fernández-Busquets X., Valverde M.A., de Strooper B. and Muñoz F.J. (2009). Amyloiddependent triosephosphate isomerase nitrotyrosination induces glycation and tau fibrillation. Brain 132, 1335-1345.
20. Halliwell B. (1992). Reactive oxygen species and the central nervous system. J. Neurochem, 59, 1609-1623.
21. Hensley K., Maidt M.L., Yu Z., Sang H., Markesbery W.R. and Floyd R.A. (1998). Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J. Neurosci. 18, 8126-8132.
22. Hipkiss A.R. (2011). Energy metabolism and ageing regulation: metabolically driven deamidation of triosephosphate isomerase may contribute to proteostatic dysfunction. Ageing Res. Rev. 10, 498-502.
23. Hollán S., Fujii H., Hirono A., Hirono K., Karro H., Miwa S., Harsányi V., Gyódi E. and Inselt-Kovács M. (1993). Hereditary triosephosphate isomerase (TPI) deficiency: two severely affected brothers one with and one without neurological symptoms. Hum. Genet. 92, 486-490.
24. Hoyer S. (1996). Oxidative metabolism deficiencies in brains of patients with Alzheimer's disease. Acta Neurol. Scand. Suppl. 165, 18-24.
25. 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. and Bush A.I. (1999). The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 38, 7609-7616.
26. Illenberger S., Zheng-Fischhöfer Q., Preuss U., Stamer K., Baumann K., Trinczek B., Biernat J., Godemann R., Mandelkow E.M. and Mandelkow E. (1998). The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol. Biol. Cell 9, 1495-1512.
27. Ill-Raga G., Ramos-Fernández E., Guix F.X., Tajes M., Bosch-Morató M., Palomer E., Godoy J., Belmar S., Cerpa W., Simpkins J.W., Inestrosa N.C. and Muñoz F.J. (2010). Amyloid-ß peptide fibrils induce nitro-oxidative stress in neuronal cells. J. Alzheimers Dis. 22, 641-652.
28. Imbimbo B.P., Lombard J. and Pomara N. (2005). Pathophysiology of Alzheimer's disease. Neuroimaging Clin. N. Am. 15, 727-753.
29. Ischiropoulos H., Zhu L., Chen J., Tsai M., Martin J.C., Smith C.D. and Beckman J.S. (1992). Peroxynitrite- mediated tyrosine nitration catalyzed by superoxide dismutase. Arch. Biochem. Biophys. 298, 431.
30. Kelly B.L. and Ferreira A. (2006). Beta-Amyloid-induced dynamin 1 degradation is mediated by N-methyl-D-aspartate receptors in hippocampal neurons. J. Biol. Chem. 281, 28079-28089.
31. Kikuchi S., Shinpo K., Moriwaka F., Makita Z., Miyata T. and Tashiro K. (1999). Neurotoxicity of methylglyoxal and 3-deoxyglucosone on cultured cortical neurons: synergism between glycation and oxidative stress, possibly involved in neurodegenerative diseases. J. Neurosci. Res. 57, 280-289.
32. Kummer M.P., Hermes M., Delekarte A., Hammerschmidt T., Kumar S., Terwel D., Walter J., Pape H.C., König S., Roeber S., Jessen F., Klockgether T., Korte M. and Heneka M.T. (2011). Nitration of tyrosine 10 critically enhances amyloid ' aggregation and plaque formation. Neuron 71, 833-844.
33. Kusaka T., Ueno M., Miki T., Kanenishi K., Nagai Y., Huang C.L., Okamoto Y., Ogawa T., Onodera M., Itoh S., Akiguchi I. and Sakamoto H. (2007). Accumulation of triosephosphate isomerase, with sequence homology to Beta amyloid peptides, in vessel walls of the newborn piglet hippocampus. Microsc. Res. Tech. 70, 648-655.
34. Levy-Lahad E., Wasco W., Poorkaj P., Romano D.M., Oshima J.M., Pettingell W.H., Yu C., Jondro P.D., Schmidt S.D., Wang K., Crowley A.C., Fu Y.-H., Guenette S.Y., Galas D., Nemens E., Wijsman E.M., Bird T.D., Schellenberg G.D. and Tanzi, R.E. (1995). Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269, 973-977.
35. Maes D., Zeelen J.P., Thanki N., Beaucamp N., Alvarez M., Thi M.H., Backmann J., Martial J.A., Wyns L., Jaenicke R. and Wierenga R.K. (1999). The crystal structure of triosephosphate isomerase (TIM) from Thermotoga maritima: a comparative thermostability structural analysis of ten different TIM structures. Proteins 37, 441-453.
36. Mainfroid V., Mande S.C., Hol W.G., Martial J.A. and Goraj K. (1996). Stabilization of human triosephosphate isomerase by improvement of the stability of individual alpha-helices in dimeric as well as monomeric forms of the protein. Biochemistry 35, 4110-4117.
37. Malenka R.C. and Malinow R.(2011). Alzheimer's disease: Recollection of lost memories. Nature 469, 44-45.
38. Mattson M.P., Cheng B., Davis D., Bryant K., Lieberburg I. and Rydel R.E. (1992). Beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12, 376-389.
39. Miranda S., Opazo C., Larrondo L.F., Muñoz F.J., Ruiz F., Leighton F. and Inestrosa N.C. (2000). The role of oxidative stress in the toxicity induced by amyloid beta-peptide in Alzheimer's disease. Prog. Neurobiol., 62, 633-648.
40. Moreno F.J., Muñoz-Montaño J.R. and Avila J. (1996). Glycogen synthase kinase 3 phosphorylation of different residues in the presence of different factors: analysis on tau protein. Mol. Cell. Biochem. 165, 47-54.
41. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Titani K. and Ihara Y. (1995). Proline-directed and non-prolinedirected phosphorylation of PHF-tau. J. Biol. Chem. 270, 823-829.
42. Muñoz F.J., Opazo C., Gil-Gómez G., Tapia G., Fernández V., Valverde M.A. and Inestrosa N.C. (2002). Vitamin E but not 17beta-estradiol protects against vascular toxicity induced by beta-amyloid wild type and the Dutch amyloid variant. J. Neurosci. 22, 3081-3089.
43. Nagano N., Orengo C.A. and Thornton J.M. (2002). One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321, 741-765.
44. Oláh J., Orosz F., Keserü G.M., Kovári Z., Kovács J., Hollán S. and Ovádi J. (2002). Triosephosphate isomerase deficiency: a neurodegenerative misfolding disease. Biochem. Soc. Trans. 30, 30-38.
45. Oláh J., Orosz F., Puskás L.G., Hackler L.Jr., Horányi M., Hollán S. and Ovádi J. (2005). Triosephosphate isomerase deficiency: consequences of an inherited mutation at mRNA, protein and metabolic levels. Biochem. J. 392, 675-683.
46. Omar R. and Pappolla M. (1993). Oxygen free radicals as inducers of heat shock protein synthesis in cultured human neuroblastoma cells: relevance to neurodegenerative disease. Eur. Arch. Psychiatry Clin. Neurosci. 242, 262-267.
47. Orosz F., Oláh J. and Ovádi J. (2006). Triosephosphate isomerase deficiency: facts and doubts. IUBMB Life 58, 703-715.
48. Orosz F., Oláh J. and Ovádi J. (2009). Triosephosphate isomerase deficiency: new insights into an enigmatic disease. Biochim.Biophys. Acta 1792, 1168-1174.
49. Ovadi J., Orosz F. and Hollán S. (2004). Functional aspects of cellular microcompartimentation in the development of neuro degeneration: mutation induced aberrant protein-protein associations. Mol. Cell. Biochem. 256-257, 83-93.
50. Pompliano D.L., Peyman A. and Knowles J.R. (1990). Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexible loop in triosephosphate isomerase. Biochemistry 29, 3186-3194.
51. Praticò D., Uryu K., Leight S., Trojanoswki J.Q. and Lee V.M. (2001). Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci. 21, 4183-4187.
52. Rice P.A., Goldman A., Steitz T.A. (1990). A helix-turn-strand structural motif common in alpha-beta proteins. Proteins 8, 334-340.
53. Richard J.P. (1993). Mechanism for the formation of methylglyoxal from triosephosphates. Biochem. Soc. Trans. 21, 549-553.
54. Richard J.P. (2008). Restoring a metabolic pathway. ACS Chem. Biol. 3, 605-607.
55. Rodríguez-Almazán C., Arreola R., Rodríguez-Larrea D., Aguirre-López B., de Gómez-Puyou M.T., Pérez-Montfort R., Costas M., Gómez-Puyou A. and Torres-Larios A. (2008). Structural basis of human triosephosphate isomerase deficiency: mutation E104D is related to alterations of a conserved water network at the dimer interface. J. Biol. Chem. 283, 23254-23263.
56. Rogaev E.I., Sherrington R., Rogaeva E.A., Levesque G., Ikeda M., Liang Y., Chi H., Lin C., Holman K., Tsuda T., Mar L., Sorbi S., Nacmias B., Piacentini S., Amaducci L., Chumakov I., Cohen D., Lannfelt L., Fraser P.E., Rommens J.M. and St. George-Hyslob P.H. (1995). Familial Alzheimer's disease in kindreds with missense mutation in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376, 775-778.
57. Saunders A.M., Schmader K, Breitner J.C., Benson M.D., Brown W.T., Goldfarb L., Goldgaber D., Manwaring M.G., Szymanski M.H., McCown N., Dole K.C., Schmechel D.E., Strittmatter W.J. and Roses A.D. (1993). Apolipoprotein E epsilon 4 allele distributions in lateonset Alzheimer's disease and in other amyloid-forming diseases. Lancet 342, 710-711.
58. Schliebs R. and Arendt T. (2011). The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 221, 555-563.
59. Schneider A.S. (2000). Triosephosphate isomerase deficiency: historical perspectives and molecular aspects. Baillieres Best Pract. Res. Clin. Haematol. 13, 119-140.
60. Schon E.A., Bonilla E. and DiMauro S. (1997). Mitochondrial DNA mutations and pathogenesis. J. Bioenerg. Biomembr. 29, 131-149.
61. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J. and Sabatini B.L. (2007). Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 27, 2866-2875.
62. Sherrington R., Rogaev E.I., Liang Y., Rogaeva E.A., Levesque G., Ikeda, M., Chi H., Lin C., Li G., Holman K., Tsuda T., Mar L., Foncin J.F., Bruni A.C., Montesi M.P., Sorbi S., Rainero I., Pinessi L., Nee L., Chumakov Y., Pollen D., Wasco W., Hainus J.L., Da Silva R., Pericak-Vance M., Tanzi R.E., Roses A.D., Fraser P.E., Rommens J.M. and St. George-Hyslop P.H. (1995) Cloning of a novel gene bearing missense mutations in early onset familial Alzheimer disease. Nature 375, 754-760.
63. Smith M.A., Richey Harris P.L., Sayre L.M., Beckman J.S. and Perry G. (1997). Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci. 17, 2653-2657.
64. Stamler J.S., Singel D.J. and Loscalzo J. (1992). Biochemistry of nitric oxide and its redox-activated forms. Science 258, 1898-1902.
65. Tanzi R.E., Vaula G., Romano D.M., Mortilla M., Huang T.L., Tupler R.G., Wasco W., Hyman B.T., Haines J.L., Jenkins B.J., Kalaitsidaki M., Warren A.C., McInnis M.G., Antonarakis S.E., Karlinsky H., Percy M.E., Connor L., Growdon J., Crapper-McLachlan D.R., Gusella J.F. and St. George-Hyslop P.H. (1992). Assessment of amyloid beta-protein precursor gene mutations in a large set of familial and sporadic Alzheimer disease cases. Am. J. Hum. Genet., 51, 273-282.
66. Thakur S.S., Deepalakshmi P.D., Gayathri P., Banerjee M., Murthy M.R. and Balaram P. (2009). Detection of the protein dimers, multiple monomeric states and hydrated forms of Plasmodium falciparum triosephosphate isomerase in the gas phase. Protein Eng. Des. Sel. 22, 289-304.
67. Valentin C., Cohen-Solal M., Maguat L., Horányi M., Inselt-Kovács M. and Hollán S. (2000). Identical germ-line mutations in the triosephosphate isomerase alleles of two brothers are associated with distinct clinical phenotypes. C.R. Acad. Sci. 3. 323, 245-250.
68. Varadarajan S., Yatin S., Kanski J., Jahanshahi F. and Butterfield D.A. (1999). Methionine residue 35 is important in amyloid beta-peptideassociated free radical oxidative stress. Brain Res. Bull. 50, 133-141.
69. Wang H.W., Pasternak J.F., Kuo H., Ristic H., Lambert M.P., Chromy B., Viola K.L., Klein W.L., Stine W.B., Krafft G.A. and Trommer B.L. (2002). Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res. 924, 133-140.
70. Wasco W. and Tanzi R.E. (1995). Molecular genetics of amyloid and apolipoprotein E in Alzheimer's disease. In: Neurobiology of Alzheimer's Disease. Bios. Sci. Publ. pp 51-76.
71. Wierenga R.K., Kapetaniou E.G. and Venkatesan R. (2010). Triosephosphate isomerase: a highly evolved biocatalyst. Cell. Mol. Life Sci. 67, 3961-3982.
72. Yoshida H. and Ihara Y. (1993). Tau in paired helical filaments is functionally distinct from fetal tau: assembly incompetence of paired helical filament-tau. J. Neurochem., 61, 1183-1186.
73. Yu J.T., Chang R.C. and Tan L. (2009). Calcium dysregulation in Alzheimer's disease: from mechanisms to therapeutic opportunities. Prog. Neurobiol. 89, 240-255.