Tau phosphorylation at threonine-175 leads to fibril formation and enhanced cell death: Implications for amyotrophic lateral sclerosis with cognitive impairment

Journal of Neurochemistry

Volumn 108, Issue 3, 2009, Pages 634-643

  Gohar, May ^b   Yang, Wencheng ^b   Strong, Wendy ^b   Volkening, Kathryn ^b   Leystra Lantz, Cheryl ^b   Strong, Michael J ^a,b,c  

^a LONDON HEALTH SCIENCES CENTRE   (Canada)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Dementia; Frontotemporal dementia; Frontotemporal lobar degeneration; Motor neuron disease; Pseudophosphorylation

Indexed keywords

ALANINE; BETA TUBULIN; ISOPROTEIN; TAU PROTEIN; THIOFLAVINE; THREONINE; THREONINE 175; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL DEATH; CELL MUTANT; CELL STRAIN HEK293; COGNITIVE DEFECT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EX VIVO STUDY; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION;

AMYOTROPHIC LATERAL SCLEROSIS; BLOTTING, WESTERN; CASPASES; CELL DEATH; CELL LINE; COGNITION DISORDERS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; NEUROFIBRILS; PHOSPHORYLATION; PLASMIDS; SOLUBILITY; TAU PROTEINS; THREONINE; TRANSFECTION; TUBULIN;

EID: 58149339675     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05791.x     Document Type: Article

References (46)

1. Arai T., Hasegawa M., Akiyama H. et al. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 351, 602 611.
2. Bradford M. M. (1976) A rapid and sensitive technique for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248 254.
3. Cho J. H. Johnson G. V. (2004) Glycogen synthase kinase 3 beta induces caspase-cleaved tau aggregation in situ. J. Biol. Chem. 279, 54716 54723.
4. Chung C. W., Song Y. H., Kim I. K. et al. (2001) Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol. Dis. 8, 162 172.
5. del C. Alonso A., Zaidi T., Grundke-Iqbal I. Iqbal K. (1994) Role of abnormally phsophorylated tau in the breakdown of microtubules in Alzheimer's disease. Proc. Natl Acad. Sci. USA 91, 5562 5566.
6. del C. Alonso A., Zaidi T., Novak M., Barra H. S., Grundke-Iqbal I. Iqbal K. (2001) Interaction of tau isoforms with Alzheimer's disease abnormally hyperphosphorylated tau and in vitro phosphorylation into the disease-like protein. J. Biol. Chem. 276, 37967 37973.
7. del C. Alonso A., Li B., Grundke-Iqbal I. Iqbal K. (2006) Polymerization of hyperphosphorylated tau into filaments eliminates its inhibitory activity. Proc. Natl Acad. Sci. USA 103, 8864 8869.
8. Eidenmüller J., Fath T., Maas T., Pool M., Sontag E. Brandt R. (2001) Phosphorylation-mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein. Biochem. J. 357, 759 767.
9. Fasulo L., Ugolini G., Visintin M., Bradbury A., Brancolini C., Verzillo V., Novak M. Cattaneo A. (2000) The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J. Neurochem. 75, 624 633.
10. Forman M. S., Trojanowski J. Q. Lee V. M. (2004) Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat. Med. 10, 1055 1063.
11. Forno L. S., Langston J. W., Herrick M. K., Wilson J. D. Murayama S. (2002) Ubiquitin-positive neuronal and tau 2-positive glial inclusions in frontotemporal dementia of motor neuron type. Acta Neuropathol. 103, 599 606.
12. Friedhoff P., Schneider A., Mandelkow E.-M. Mandelkow E. (1998) Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution. Biochem. 37, 10223 10230.
13. Gamblin T. C., Chen F., Zambrano A. et al. (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc. Natl Acad. Sci. USA 100, 10032 10037.
14. Goedert M., Spillantini M. G., Jakes R., Rutherford D. Crowther R. A. (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519 526.
15. Gong C. X., Liu F., Grundke-Iqbal I. Iqbal K. (2005) Post-translational modifications of tau protein in Alzheimer's disease. J. Neural Trans. 112, 813 838.
16. Grundke-Iqbal I., Iqbal K., Quinlan M., Tung Y.-C. Zaida M. S. (1986a) Microtubule-associate protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 261, 6084 6089.
17. Grundke-Iqbal I., Iqbal K., Tung Y.-C., Quinlan M., Wisniewski H. M. Binder L. I. (1986b) Abnormal phosphorylation of the microtubule-associated protein τ (tau) in Alzheimer cytoskeletal pathology. Proc. Natl Acad. Sci. USA 83, 4913 4917.
18. Hanger D. P., Betts J. C., Loviny T. L. F., Blackstock W. P. Anderton B. H. (1998) New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament tau) from Alzheimer's disease brain using nanoelectrospray mass spectroscopy. J. Neurochem. 71, 2465 2476.
19. Himmler A., Dreschsel D., Kirschner M. W. Martin D. W. Jr. (1989) Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains. Mol. Cell. Biol. 9, 1381 1388.
20. Ince P. G., Lowe J. Shaw P. J. (1998) Amyotrophic lateral sclerosis: current issues in classification, pathogenesis and molecular pathology. Neuropathol. Appl. Neurobiol. 24, 104 117.
21. Itoh N., Ishiguro K., Arai H., Kokubo Y., Sasaki R., Narita Y. Kuzuhara S. (2003) Biochemical and ultrastructural study of neurofibrillary tangles in amyotrophic lateral sclerosis/parkinsonism-dementia complex in the Kii peninsula of Japan. J. Neuropathol. Exp. Neurol. 62, 791 798.
22. Jordan M. Wurm F. (2004) Transfection of adherent and suspended cells by calcium phosphate. Methods 33, 136 143.
23. Köpke E., Tung Y.-C., Shaikh S., del C. Alonso A., Iqbal K. Grundke-Iqbal I. (1993) Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J. Biol. Chem. 268, 24374.
24. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680 685.
25. Li B., Chohan M. O., Grundke-Iqbal I. Iqbal K. (2007) Disruption of micrtubule network by Alzheimer abnormally hyperphosphorylated tau. Acta Neuropathol. 113, 501 511.
26. Lindwall G. Cole R. D. (1984) Phosphorylation affects the ability of tau protein to promote microtubule assembly. J. Biol. Chem. 259, 5301 5305.
27. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55 63.
28. Mott R. T., Dickson D. W., Trojanowski J. Q. et al. (2005) Neuropathological, biochemical, and molecular characterization of the frontotemporal dementias. J. Neuropathol. Exp. Neurol. 64, 420 428.
29. Neary D., Snowden J. S., Gustafson L. et al. (1998) Frontotemporal lobar degeneration. A consensus on clinical diagnostic criteria. Neurology 51, 1546 1554.
30. Neumann M., Sampathu D. M., Kwong L. K. et al. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130 133.
31. Noda K., Katayama S., Watanabe C., Yamamura Y. Nakamura S. (1999) Gallyas- and tau-positive glial structures in motor neuron disease with dementia. Clin. Neuropath. 18, 218 225.
32. Rissman R. A., Poon W. W., Blurton-Jones M., Oddo S., Torp R., Vitek M. P., LaFerla F. M., Rohn T. T. Cotman C. W. (2004) Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest. 114, 121 130.
33. Santa-Maria I., Pérez M., Hernández F., Muñoz V., Moreno F. J. Avila J. (2006) In vitro tau fibrillization: mapping protein regions. Biochim. Biophys. Acta 1762, 683 692.
34. Schneider A., Biernat J., von Bergen M., Mandelkow E. Mandelkow E.-M. (1999) Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochem. 38, 3549 3558.
35. Strong M. J. (2001) The evidence for ALS as a multisystems disorder of limited phenotypic expression. Can. J. Neurol. Sci. 28, 283 298.
36. Strong M. J. (2008) The syndromes of frontotemporal dysfunction in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 9, 323 338.
37. Strong M. J., Kesavapany S. Pant H. C. (2005) The pathobiology of amyotrophic lateral sclerosis: a proteinopathy? J. Neuropathol. Exp. Neurol. 64, 649 664.
38. Strong M. J., Yang W., Strong W. L., Leystra-Lantz C., Jaffe H. Pant H. C. (2006) Tau protein hyperphosphorylation in sporadic ALS with cognitive impairment. Neurology 66, 1770 1771.
39. Taniguchi S., Suzuki N., Masuda M., Hisanaga S.-I., Iwatsubo T., Goedert M. Hasegawa M. (2005) Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins. J. Biol. Chem. 280, 7614 7623.
40. Wakayama I., Kihira Y., Yoshida S. Garruto R. M. (1993) Rare neuropil threads in amyotrophic lateral sclerosis and parkinsonism-dementia on Guam and in the Kii Peninsula of Japan. Dementia 4, 75 80.
41. Weingarten M. D., Lockwood A. H., Hwo S.-Y. Kirschner M. W. (1975) A protein factor essential for microtubule assembly. Proc. Natl Acad. Sci. USA 72, 1858 1862.
42. Wilson C. M., Grace G. M., Munoz D. G., He B. P. Strong M. J. (2001) Cognitive impairment in sporadic ALS. A pathological continuum underlying a multisystem disorder. Neurology 57, 651 657.
43. Yang W., Sopper M. M., Leystra-Lantz C. Strong M. J. (2003) Microtubule-associated tau protein positive neuronal and glial inclusions in amyotrophic lateral sclerosis. Neurology 61, 1766 1773.
44. Yang W., Ang L.-C. Strong M. J. (2005) Tau protein aggregation in the frontal and entorhinal cortices as a function of aging. Dev. Brain Res. 156, 127 138.
45. Yang W., Leystra-Lantz C. Strong M. J. (2008) Upregulation of GSK3β expression in frontal and temporal cortex of ALS with cognitive impairment (ALSci). Brain Res. 1196, 131 139.
46. Yokota O., Tsuchiya K., Oda T. et al. (2006) Amyotrophic lateral sclerosis with dementia: an autopsy case showing many Bunina bodies, tau-positive neuronal and astrocytic plaque-like pathologies, and pallido-nigral degeneration. Acta Neuropathol. 112, 633 645.