Molecular evolution of τ protein: Implications for Alzheimer's disease

Journal of Neurochemistry

Volumn 67, Issue 4, 1996, Pages 1622-1632

  Nelson, Peter T ^a,b   Stefansson, Kari ^a   Gulcher, Jeffrey ^a   Saper, Clifford B ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Animal models; Dementia; Exon splicing; Neurofibrillary tangle; Paired helical filaments; Pseudogene

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; DEMENTIA; GOAT; NEUROFIBRILLARY TANGLE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PSEUDOGENE; RHESUS MONKEY;

ANIMALIA; CAPRA HIRCUS; MACACA MULATTA; OVIS ARIES; PRIMATES; UNGULATA;

EID: 0029830646     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.67041622.x     Document Type: Article

References (58)

1. Andreadis A., Brown W. M., and Kosik K. S. (1992) Structure and novel exons of the human tau gene. Biochemistry 31, 10626-10633.
2. Baas P. W., Pienkowski T. P., and Kosik K. S. (1991) Processes induced by tau expression in Sf9 cells have an axon-like microtubule organization. J. Cell Biol. 115, 1333-1344.
3. Bard J. A., Nawoschik S. P., O'Dowd B. F., George S. R., Branchek T. A., and Weinshank R. L. (1995) The human serotonin 5-hydroxytryptamine 1D receptor pseudogene is transcribed. Gene 153, 295-296.
4. Biernat J., Mandelkow E.-M., Schroter C., Lichtenberg-Kraag B., Steiner B., Berling B., Meyer H., Mercken M., Vandermeeren A., Goedert M., and Mandelkow E. (1992) The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO J. 11, 1593-1597.
5. Braak E., Braak H., and Mandelkow E.-M. (1994a) A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. 87, 554-567.
6. Braak H., Braak E., and Strothjohann M. (1994b) Abnormally phosphorylated tau protein related to the formation of neurofibrillary tangles and neuropil threads in the cerebral cortex of sheep and goat. Neurosci. Lett. 171, 1-4.
7. Brandt R. and Lee G. (1993) Functional organization of microtubule-associated protein tau. J. Biol. Chem. 268, 3414-3419.
8. Brandt R. and Lee G. (1994) Orientation, assembly, and stability of microtubule bundles induced by a fragment of tau protein. Cell Motil. Cytoskeleton 28, 143-154.
9. Brion J., Passareiro H., Nunez J., and Flament-Durand J. (1985) Immunological determinants of tau proteins are present in neurofibrillary tangles of Alzheimer's disease. Arch. Biol. 95, 229-235.
10. Caceres A. and Kosik K. S. (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
11. Chen W.-T., Liu W.-K., and Yen S.-H. (1994) Expression of tau exon 8 in different species. Neurosci. Lett. 172, 167-170.
12. Cleveland D. W., Hwo S., and Kirschner M. W. (1977) Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J. Mol. Biol. 116, 207-225.
13. Cole G. and Neal J. W. (1990) The brain in aged elephants. J. Neuropathol. Exp. Neurol. 49, 190-192.
14. Cork L. C., Powers R. E., Selkoe D. J., Davies P., Geyer J. J., and Price D. L. (1988) Neurofibrillary tangles and senile plaques in aged bears. J. Neuropathol. Exp. Neurol. 47, 629-641.
15. Correll A., Martin-Villa J. M., Varela P., Vicario J. L., Martinez-Laso J., and Arvaiz-Villena A. (1991) Exon-2 nucleotide sequences, polymorphism, and haplotype distribution of a new HLA-DRB gene: HLA-DRB. Mol. Immunol. 28, 533-543.
16. Crowther R. A., Oleson O. F., Jakes R., and Goedert M. (1992) The microtubule binding repeats of tau protein assemble into filaments like those found in Alzheimer's disease. FEBS Lett. 309, 199-202.
17. Crowther R. A., Olesen O. F., Smith M. J., Jakes R., and Goedert M. (1994) Assembly of Alzheimer-like filaments from full-length tau protein. FEBS Lett. 337, 135-138.
18. Crowther T., Goedert M., and Wischik C. M. (1989) The repeat region of micro-tubule associated protein tau forms part of the core of the paired helical filament of Alzheimer's disease. Ann. Med. 21, 127-132.
19. Delacourte A. and Defossez A. (1986) Alzheimer's disease: Tau proteins, the promoting factors of microtubule assembly, are major components of paired helical filaments. J. Neural. Sci. 76, 173-186.
20. Dickson D. W., Crystal H. A., Bevona C., Honer W., Vincent I., and Davies P. (1995) Correlations of synaptic and pathological markers with cognitive of the elderly. Neurobiol. Aging 16, 285-304.
21. Frautschy S. A., Baird A., and Cole G. M. (1991) Effects of injected Alzheimer B-amyloid cores in rat brain. Proc. Natl. Acad. Sci. USA 88, 8362-8366.
22. Gearing M., Rebeck G. W., Hyman B. T., Tigges J., and Mirra S. S. (1994) Neuropathology and apolipoprotein E profile of aged chimpanzees: implications for Alzheimer's disease. Proc. Natl. Acad. Sci. USA 91, 9382-9386.
23. Geddes J. W., Bondada V., and Keller J. N. (1994) Effects of intrahippocampal colchicine administration on the levels and localization of microtubule-associated proteins, tau and MAP2. Brain Res. 633, 1-8.
24. Goedert M. and Jakes R. (1990) Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J. 9, 4225-4230.
25. Goedert M., Spillantini M. G., Jakes R., Rutherford D., and Crowther R. A. (1989a) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526.
26. Goedert M., Spillantini M. G., Potier M. C., Ulrich J., and Crowther R. A. (1989b) Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J. 8, 393-399.
27. Goedert M., Spillantini M. G., Cairns N. J., and Crowther R. A. (1992) Tau-protein of Alzheimer paired helical filaments - abnormal phosphorylation of all six brain isoforms. Neuron 8, 159-168.
28. Greenberg S. G. and Schein J. (1989) Isolation of relatively specific paired helical filament antibody. Soc. Neurosci. Abstr. 15, 1038.
29. Greenwood J. A., Scott C. W., Spreen R. C., Caputo C. B., and Johnson G. V. W. (1994) Casein kinase II preferentially phosphorylates human tau isoforms containing an amino-terminal insert. Identification of threonine 39 as the primary phosphate receptor. J. Biol. Chem. 269, 4373-4380.
30. Grundke-Iqbal I., Iqbal K., Tung Y.-C., Quinlan M., Wisniewski H. M., and Binder L. I. (1986) Abnormal phosphorylation of the microtubule-associated protein t(tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83, 4913-4917.
31. Gustke N., Trinczek B., Biernat J., Mandelkow E.-M., and Mandelkow E. (1994) Domains of tau protein and interactions with microtubules. Biochemistry 33, 9511-9522.
32. Himmler A. (1989) Structure of the bovine tau gene: allernatively spliced transcripts generate a protein family. Mol. Cell. Biol. 9, 1389-1396.
33. Kosik K. S., Orecchio L. D., Bakalis S., and Neve R. L. (1989) Developmentally regulated expression of specific Tau sequences. Neuron 2, 1389-1397.
34. Lee G., Cowan N., and Kirschner M. (1988) The primary structure and heterogeneity of tau protein from mouse brain. Science 239, 285-288.
35. Lewin B. (1994) Genes V, pp. 717-720. Oxford University Press, New York.
36. Li W.-H. and Tanimura M. (1987) The molecular clock runs more slowly in man than in apes and monkeys. Nature 326, 93-96.
37. Liu W.-K., Dickson D. W., and Yen S.-H. (1993) Heterogeneity of tau proteins in Alzheimer's disease. Am. J. Pathol. 142, 387-394.
38. Loomis P. A., Howard T. H., Castleberry R. P., and Binder L. I. (1990) Identification of nuclear tau isoforms in human neuroblastoma cells. Proc. Natl. Acad. Sci. USA 87, 8422-8426.
39. Marotta C. A., Chou W.-G., Majocha R. E., Watkins R., LaBonne C., and Zain S. B. (1989) Overexpression of amyloid precursor protein A4 (beta-amyloid) immunoreactivity in genetically transformed cells: implications for a cellular model of Alzheimer amyloidosis. Proc. Natl. Acad Sci. USA 86, 337-341.
40. Minghetti P. P. and Dugaiczyk A. (1993) The emergence of new DNA repeats and the divergence of primates. Proc. Natl. Acad. Sci. USA 90, 1872-1876.
41. Muma N. A., Troncoso J. C., Hoffman P. N., Koo E. H., and Price D. L. (1988) Aluminum neurotoxicity: altered expression of cytoskeletal genes. Brain Res. Mol. Brain Res. 3, 115-122.
42. Nelson P. T. and Saper C. B. (1995) Ultrastructure of neurofibrillary tangles in the cerebral cortex of sheep. Neurobiol. Aging 16, 315-323.
43. Nelson P. T., Marton L., and Saper C. B. (1993) Alz-50 immunohistochemistry in the normal sheep striatum: a light and electron microscope study. Brain Res. 600, 285-297.
44. Nelson P. T., Greenberg S. G., and Saper C. B. (1994) Neurofibrillary tangles in the cerebral cortex of sheep. Neurosci. Lett. 170, 187-190.
45. Neve R. L., Harris P., Kosik K. S., Kurnit D. M., and Donlan T. A. (1986) Identification of cDNA clones for the human microtubule-associated protein, tau, and chromosomal localization of the genes for tau and microtubule-associated protein 2. Mol. Brain Res. 1, 271-280.
46. Nguyen T., Sunahara R., Marchese A., Van Tol H. H. M., Seeman P., and O'Dowd B. F. (1991) Transcription of a human dopamine D5 pseudogene. Biochem. Biophys. Res. Commun. 181, 16-21.
47. Steiner B., Mandelkow E. M., Biernat J., Gustke N., Meyer H. E., Schmidt B., Mieskes G., Soling H. D., Drechsel D., Kirschner M. W. et al. (1990) Phosphorylation of microtubule-associated protein tau: identification of the site for Ca++ calmodulin dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J. 9, 3539-3544.
48. Su J. H., Cummings B. J., and Cotman C. W. (1994) Early phosphorylation of tau in Alzheimer's disease occurs at Ser-202 and is preferentially located within neurites. Clin. Neurosci. Neuropathol. 5, 2358-2362.
49. Szendrei G. I., Lee V. M. Y., and Otvos L. (1993) Recognition of the minimal epitope of monoclonal antibody tau-1 depends upon the presence of a phosphate group but not its location. J. Neurosci. Res. 34, 243-249.
50. Walker L. C., Kitt C. A., Struble R. G., Wagster M. V., Price D. L., and Cork L. C. (1988) Neural basis of memory decline in aged monkeys. Neurobiol. Aging 9, 657-666.
51. Wang Y., Loomis P. A., Zinkowski R. P., and Binder L. I. (1993) A novel tau-transcript in cultured human neuroblastoma cells expressing nuclear-tau. J. Cell Biol. 121, 257-267.
52. Weingarten M. D., Lockwood A, H., Hwo S.-Y., and Kirschner M. W. (1975) A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. USA 72, 1858-1862.
53. Wille H., Drewes G., Biernat J., Mandelkow E., and Mandelkow E. (1992) Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro. J. Cell Biol. 118, 573-584.
54. Wischik C. M., Novak M., Edwards P. C., Klug A., Tichelaar W., and Crowther R. A. (1988) Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. USA 85, 4884-4888.
55. Wisniewski H., Terry R. D., and Hirano A. (1970a) Neurofibrillary pathology. J. Neuropathol. Exp. Neurol. 29, 163-176.
56. Wisniewski H. M., Johnson A. B., Raine C. S., Kay W. J., and Terry R. D. (1970b) Senile plaques and cerebral amyloidosis in aged dogs. A histochemical and ultrastructural study. Lab. Invest. 23, 287-296.
57. Wisniewski H. M., Ghetti B., and Terry R. D. (1973) Neuritic (senile) plaques and filamentous changes in aged Rhesus monkeys. J. Neuropathol. Exp. Neurol. 32, 566-584.
58. Wolozin B. L., Pruchnicki A., Dickson D. W., and Davies P. (1986) A neuronal antigen in the brains of Alzheimer patients. Science 232, 648-650.