Tyrosine nitration within the proline-rich region of tau in Alzheimer's disease

American Journal of Pathology

Volumn 178, Issue 5, 2011, Pages 2275-2285

  Reyes, Juan F ^a   Fu, Yifan ^a   Vana, Laurel ^a   Kanaan, Nicholas M ^b   Binder, Lester I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY TAU NY197; MONOCLONAL ANTIBODY TAU NY394; PROLINE; TAU PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NITRATION; NONHUMAN; PAIRED HELICAL FILAMENT; PATHOGENESIS; PRIORITY JOURNAL; WESTERN BLOTTING;

EID: 79959236278     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.01.030     Document Type: Article

References (50)

1. Glenner GG, Wong CW: Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 1984, 120:885-890 (Pubitemid 14104991)
2. 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, 261:6084-6089 (Pubitemid 17207447)
3. Goedert M, Wischik CM, Crowther RA, Walker JE, Klug A: Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule- associated protein tau. Proc Natl Acad Sci USA 1988, 85:4051-4055
4. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA: Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526
5. Ksiezak-Reding H, Liu WK, Yen SH: Phosphate analysis and dephosphorylation of modified tau associated with paired helical filaments. Brain Res 1992, 597:209-219 (Pubitemid 23003689)
6. Braak H, Braak E: Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991, 82:239-259
7. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT: Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42:631-639
8. Abraha A, Ghoshal N, Gamblin TC, Cryns V, Berry RW, Kuret J, Binder LI: C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J Cell Sci 2000, 113:3737-3745
9. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, Lu M, Fu Y, Garcia-Sierra F, LaPointe N, Miller R, Berry RW, Binder LI, Cryns VL: Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 2003, 100:10032-10037 (Pubitemid 37087063)
10. Park SY, Ferreira A: The generation of a 17 kDa neurotoxic fragment: an alternative mechanism by which tau mediates beta-amyloid-induced neurodegeneration. J Neurosci 2005, 25:5365-5375
11. Carmel G, Mager EM, Binder LI, Kuret J: The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J Biol Chem 1996, 271:32789-32795 (Pubitemid 27008707)
12. Horiguchi T, Uryu K, Giasson BI, Ischiropoulos H, LightFoot R, Bellmann C, Richter-Landsberg C, Lee VM, Trojanowski JQ: Nitration of tau protein is linked to neurodegeneration in tauopathies [Erratum appeared in Am J Pathol 2003, 163:2645]. Am J Pathol 2003, 163:1021-1031 (Pubitemid 37040138)
13. Reynolds MR, Berry RW, Binder LI: Nitration in neurodegeneration: deciphering the "Hows" "nYs". Biochemistry 2007, 46:7325-7336
14. Beckman JS, Chen J, Crow JP, Ye YZ: Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration. Prog Brain Res 1994, 103:371-380
15. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G: Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 1997, 17:2653-2657 (Pubitemid 27154998)
16. Beckman JS, Koppenol WH: Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996, 271:C1424-C1437
17. Thomas DD, Miranda KM, Colton CA, Citrin D, Espey MG, Wink DA: Heme proteins and nitric oxide (NO): the neglected, eloquent chemistry in NO redox signaling and regulation. Antioxid Redox Signal 2003, 5:307-317 (Pubitemid 36793014)
18. Pfeiffer S, Lass A, Schmidt K, Mayer B: Protein tyrosine nitration in mouse peritoneal macrophages activated in vitro and in vivo: evidence against an essential role of peroxynitrite. FASEB J 2001, 15:2355-2364 (Pubitemid 33063164)
19. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, Hussain P, Vecoli C, Paolocci N, Ambs S, Colton CA, Harris CC, Roberts DD, Wink DA: The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 2008, 45:18-31
20. Ischiropoulos H, al-Mehdi AB: Peroxynitrite-mediated oxidative protein modifications. FEBS Lett 1995, 364:279-282
21. Beckman JS, Carson M, Smith CD, Koppenol WH: ALS, SOD and peroxynitrite. Nature 1993, 364:584
22. Atwood CS, Perry G, Zeng H, Kato Y, Jones WD, Ling KQ, Huang X, Moir RD, Wang D, Sayre LM, Smith MA, Chen SG, Bush AI: Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 2004, 43:560-568 (Pubitemid 38082580)
23. Souza JM, Giasson BI, Chen Q, Lee VM, Ischiropoulos H: Dityrosine cross-linking promotes formation of stable alpha-synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J Biol Chem 2000, 275:18344-18349 (Pubitemid 30414790)
24. Reynolds MR, Berry RW, Binder LI: Site-specific nitration and oxidative dityrosine bridging of the tau protein by peroxynitrite: implications for Alzheimer's disease. Biochemistry 2005, 44:1690-1700 (Pubitemid 40204410)
25. Aulak KS, Koeck T, Crabb JW, Stuehr DJ: Dynamics of protein nitration in cells and mitochondria. Am J Physiol Heart Circ Physiol 2004, 286:H30-H38 (Pubitemid 38049459)
26. Gow AJ, Farkouh CR, Munson DA, Posencheg MA, Ischiropoulos H: Biological significance of nitric oxide-mediated protein modifications. Am J Physiol Lung Cell Mol Physiol 2004, 287:L262-L268 (Pubitemid 38943907)
27. Nonnis S, Cappelletti G, Taverna F, Ronchi C, Ronchi S, Negri A, Grassi E, Tedeschi G: Tau is endogenously nitrated in mouse brain: identification of a tyrosine residue modified in vivo by NO. Neurochem Res 2008, 33:518-525 (Pubitemid 351230454)
28. Giannopoulou E, Katsoris P, Polytarchou C, Papadimitriou E: Nitration of cytoskeletal proteins in the chicken embryo chorioallantoic membrane. Arch Biochem Biophys 2002, 400:188-198 (Pubitemid 34852399)
29. Kamisaki Y, Wada K, Bian K, Balabanli B, Davis K, Martin E, Behbod F, Lee YC, Murad F: An activity in rat tissues that modifies nitrotyrosine- containing proteins. Proc Natl Acad Sci USA 1998, 95:11584-11589 (Pubitemid 28460458)
30. Reynolds MR, Berry RW, Binder LI: Site-specific nitration differentially influences tau assembly in vitro. Biochemistry 2005, 44:13997-14009 (Pubitemid 41507480)
31. Reynolds MR, Reyes JF, Fu Y, Bigio EH, Guillozet-Bongaarts AL, Berry RW, Binder LI: Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J Neurosci 2006, 26:10636-10645
32. Reyes JF, Reynolds MR, Horowitz PM, Fu Y, Guillozet-Bongaarts AL, Berry R, Binder LI: A possible link between astrocyte activation and tau nitration in Alzheimer's disease. Neurobiol Dis 2008, 31:198-208
33. Binder LI, Frankfurter A, Rebhun LI: The distribution of tau in the mammalian central nervous system. J Cell Biol 1985, 101:1371-1378 (Pubitemid 16203754)
34. Hanger DP, Betts JC, Loviny TL, Blackstock WP, Anderton BH: New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry. J Neurochem 1998, 71:2465-2476 (Pubitemid 28531257)
35. Ye YZ, Strong M, Huang ZQ, Beckman JS: Antibodies that recognize nitrotyrosine. Methods Enzymol 1996, 269:201-209 (Pubitemid 26295709)
36. Mufson EJ, Lavine N, Jaffar S, Kordower JH, Quirion R, Saragovi HU: Reduction in p140-TrkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease. Exp Neurol 1997, 146:91-103 (Pubitemid 27319723)
37. LoPresti P, Szuchet S, Papasozomenos SC, Zinkowski RP, Binder LI: Functional implications for the microtubule-associated protein tau: localization in oligodendrocytes. Proc Natl Acad Sci USA 1995, 92: 10369-10373
38. Eidenmüller J, Fath T, Maas T, Pool M, Sontag E, Brandt R: Phosphorylation- mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein. Biochem J 2001, 357:759-767 (Pubitemid 32735156)
39. Pellicer EM, Sundblad A: Recuperación de antígenos por horno de microondas con buffer de ácido cítrico [Antigen retrieval by microwave oven with buffer of citric acid]. Spanish. Medicina (B Aires) 1994, 54:129-132
40. Guillozet-Bongaarts AL, Garcia-Sierra F, Reynolds MR, Horowitz PM, Fu Y, Wang T, Cahill ME, Bigio EH, Berry RW, Binder LI: Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease. Neurobiol Aging 2005, 26:1015-1022 (Pubitemid 40312665)
41. Bussière T, Hof PR, Mailliot C, Brown CD, Caillet-Boudin ML, Perl DP, Buée L, Delacourte A: Phosphorylated serine422 on tau proteins is a pathological epitope found in several diseases with neurofibrillary degeneration. Acta Neuropathol 1999, 97:221-230 (Pubitemid 29137270)
42. Steiner B, Mandelkow EM, Biernat J, Gustke N, Meyer HE, Schmidt B, Mieskes G, Söling HD, Drechsel D, Kirschner MW, Goedert M, Mandelkow E: Phosphorylation of microtubule-associated protein tau: identification of the site for Ca2(+)-calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J 1990, 9:3539-3544
43. Wang Y, Garg S, Mandelkow EM, Mandelkow E: Proteolytic processing of tau. Biochem Soc Trans, 2010, 38:955-961
44. Khuebachova M, Verzillo V, Skrabana R, Ovecka M, Vaccaro P, Panni S, Bradbury A, Novak M: Mapping the C terminal epitope of the Alzheimer's disease specific antibody MN423. J Immunol Methods 2002, 262:205-215 (Pubitemid 34450744)
45. Tremblay MA, Acker CM, Davies P: Tau phosphorylated at tyrosine 394 is found in Alzheimer's disease tangles and can be a product of the Abl-related kinase, Arg. J Alzheimers Dis 2010, 19:721-733
46. Rayala SK, Martin E, Sharina IG, Molli PR, Wang X, Jacobson R, Murad F, Kumar R: Dynamic interplay between nitration and phosphorylation of tubulin cofactor B in the control of microtubule dynamics [Erratum appeared in Proc Natl Acad Sci USA 2008, 105:399]. Proc Natl Acad Sci USA 2007, 104:19470-19475
47. Cappelletti G, Maggioni MG, Ronchi C, Maci R, Tedeschi G: Protein tyrosine nitration is associated with cold- and drug-resistant microtubules in neuronal-like PC12 cells. Neurosci Lett 2006, 401:159-164
48. Lebouvier T, Scales TM, Williamson R, Noble W, Duyckaerts C, Hanger DP, Reynolds CH, Anderton BH, Derkinderen P: The microtubule- associated protein tau is also phosphorylated on tyrosine. J Alzheimers Dis 2009, 18:1-9
49. Liu F, Liang Z, Gong CX: Hyperphosphorylation of tau and protein phosphatases in Alzheimer disease. Panminerva Med 2006, 48: 97-108 (Pubitemid 44671265)
50. Zheng-Fischhöfer Q, Biernat J, Mandelkow EM, Illenberger S, Godemann R, Mandelkow E: Sequential phosphorylation of Tau by glycogen synthase kinase-3beta and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical- filament-like conformation. Eur J Biochem 1998, 252:542-552 (Pubitemid 28156880)