Modulated induction of tau proteins in cultured human neuroblastoma cells

Brain Research

Volumn 707, Issue 2, 1996, Pages 256-265

  Ko, Li Wen ^b   Liu, Wan Kyng ^b   Georgieff, Irene S ^a,c   Yen, Shu Hui C ^b  

^a WYETH RESEARCH   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c Columbia University ^*  (United States)

Author keywords

Alzheimer's disease; Human neuroblastoma culture; Neurofibrillary degeneration; Paired helical filament; Phosphorylation; Tau

Indexed keywords

TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; NEUROBLASTOMA; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0030040586     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-8993(95)01268-0     Document Type: Article

References (76)

1. Alonso, A.C., Zaidi, T., Grundke-Iqbal, I. and Iqbal, K., Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease, Proc. Natl. Acad. Sci. USA, 91 (1994) 5562-5566.
2. Bancher, C., Brunner, C., Lassmann, H., Budka, H., Jellinger, K., Wiche, G., Seitelberger, F., Grundke-Iqbal, I., Iqbal, K. and Wisniewski, H.M., Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease, Brain Res., 477 (1989) 90-99.
3. Baudier, J. and Cole, R.D., Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by a calcium/calmodulin-dependent kinase and modulated by phospholipids, J. Biol. Chem., 262 (1987) 17577-17583.
4. Binder, L.I., Frankfurter, A. and Rebhun, L., The distribution of tau polypeptides in the mammalian central nervous system, J. Cell Biol., 101 (1985) 1371-1378.
5. Brion, J.P., Flament-Durand, J. and Dustin, P., Alzheimer's disease and tau proteins, Lancet, 2 (1986) 1098.
6. Butler, M. and Shelanski, M.L., Microheterogeneity of microtubule-associated tau protein is due to differences in phosphorylation, J. Neurochem., 47 (1986) 1517-1522.
7. Chen, W.-T., Liu, W.-K. and Yen, S.-H., Expression of tau exon 8 in different species, Neurosci. Lett., 172 (1994) 167-170.
8. Chiang, M.F., Liu, W.-K. and Yen, S.-H., Reversible heat stress-related loss of phosphorylated Alzheimer-type epitopes in tau proteins of human neuroblastoma cells, J. Neurosci., 13 (1993) 4854-4860.
9. Cleveland, D.W., Spiegelman, B. and Kirschner, M., Conservation of microtubule-associated proteins, J. Biol. Chem., 254 (1979) 12670-12678.
10. Couchie, D. and Nunez, J., Immunological characterization of microtubule-associated proteins specific for the immature brain, FEBS Lett., 188 (1985) 331-335.
11. Couchie, D., Mavilia, C., Georgieff, I.S., Liem, R.K.H., Shelanski, M.L. and Nunez, J., Primary structure of high molecular weight tau present in the peripheral nervous system, Proc. Natl. Acad. Sci. USA, 89 (1992) 4378-4381.
12. De Boni, U. and Crapper McLachlan, D.R., Controlled induction of paired helical filaments of the Alzheimer type in cultured human neurons by glutamate and aspartate, J. Neurol. Sci., 68 (1985) 105-118.
13. Drubin, D.G., Kirschner, M.W. and Feinstein, S., Microtubule-associated tau protein induction by nerve growth factor during neurite outgrowth in PC12 cells. In G.G. Borisy, D.W. Cleveland and D.B. Murphy (Eds.), Molecular Biology of the Cytoskeleton, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, 1984, pp. 343-355.
14. Drubin, D., Kobayashi, S., Kellogg, D. and Kirschner, M., Regulation of microtubule protein levels during cellular morphogenesis in nerve growth factor-treated PC12 cells, J. Cell Biol., 106 (1988) 1583-1591.
15. Dupont-Wallois, L., Sautiere, P.E., Cocquerelle, C., Bailleul, B., Delacourte, A. and Caillet-Boudin, M.L., Shift from fetal-type to Alzheimer-type phosphorylated tau proteins in SKNSH-SY 5Y cells treated with okadaic acid, FEBS Lett., 357 (1995) 197-201.
16. Fisher, G.H., Payan, I.L., Chou, S.J., Man, E.H., Cerwinski, S., Martin, T., Emory, C. and Frey, W.H., II, Racemized D-aspartate in Alzheimer neurofibrillary tangles, Brain Res. Bull., 28 (1992) 127-131.
17. Francon, J., Lennon, A.M., Fellous, A., Mareck, A., Pierre, P.N. and Nunez, J., Heterogeneity of microtubule associated proteins and brain development, Eur. J. Biochem., 129 (1982) 465-471.
18. Gache, Y., Guilleminot, J., Bridoux, A.M. and Nunez, J., Heterogeneity of the high molecular weight tau proteins in N115 neuroblastoma cells, J. Neurochem., 61 (1993) 873-880.
19. Georgieff, I., Liem, R.K.H., Mellado, W., Nunez, J. and Shelanski, M.L., High molecular weight tau: preferential localization in the peripheral nervous system, J. Cell Sci., 100 (1991) 55-60.
20. Georgieff, I.S., Liem, R.K.H., Couchie, D., Mavilia, C., Nunez, J. and Shelanski, M.L., Expression of high molecular weight tau in the central and peripheral nervous system, J. Cell Sci., 105 (1993) 729-737.
21. Goedert, M., Tau protein and the neurofibrillary pathology of Alzheimer's disease, Trends Biochem. Sci., 16 (1993) 460-465.
22. Goedert, M. and Jakes, R., Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization, EMBO J., 13 (1990):4225-4230.
23. Goedert, M., Spillantini, M.G. and Jakes, R., Localization of the Alz-50 epitope in recombinant human microtubule-associated protein tau, Neurosci. Lett., 126 (1991) 149-154.
24. Goedert, M., Spillantini, M.G., Cairns, N.J. and Crowther, R.A., Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms, Neuron, 8 (1992) 159-168.
25. Goedert, M., Spillantini, M.G., Jakes, R., Rutherford, D. and Crowther, R.A., Multiple isoforms of human microtubule associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease, Neuron, 3 (1989) 519-526.
26. tauPHF proteins display the same biochemical properties as normal tau, J. Biol. Chem., 267 (1992) 564-569.
27. Grundke-Iqbal, I., Iqbal, K., Quinlan, M., Tung, Y.-C., Zaidi, M. and Wisniewski, H.M., Microtubule-associated protein tau. A component of Alzheimer paired helical filaments, J. Biol. Chem., 261 (1986) 6084-6089.
28. Grundke-Iqbal, I., Iqbal, K., Tung, Y.-C., Quinlan, M., Wisniewski, H.M. and Binder, L.I., Abnormal phosphorylation of microtubule-associated protein tau in Alzheimer cytoskeletal pathology, Proc. Natl. Acad. Sci., USA 83 (1986) 4913-4917.
29. Himmler, A., Structure of the bovine tau gene: alternative spliced transcripts generate a protein family, Mol. Cell. Biol., 9 (1989) 1389-1396.
30. Ihara, Y., Nukina, N., Miura, R. and Ogawara, M., Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer's disease, J. Biochem. (Tokyo), 99 (1986) 1807-1810.
31. Iqbal, K. and Grundke-Iqbal, I., Ubiquitination and abnormal phosphorylation of paired helical filaments in Alzheimer's disease, Mol. Neurobiol., 5 (1992) 399-410.
32. Jakes, R., Novak, M., Davison, M. and Wischik, C.M., Identification of 3-and 4-repeat tau isoforms within the PHF in Alzheimer's disease, EMBO J., 10 (1991) 2725-2729.
33. Katzman, R., Alzheimer's disease, N. Engl. J. Med., 314 (1986) 964-973.
34. Kenessey, A., Yen, S.-H., Liu, W.-K., Yang, X.-R. and Dunlop, D.S., Detection of D-aspartate in tau proteins associated with Alzheimer paired helical filaments, Brain Res., 675 (1995) 183-189.
35. Kidd, M., Paired helical filaments in electron microscopy of Alzheimer's disease, Nature, 197 (1963) 192-193.
36. Ko, L., Sheu, K.-F.R. and Blass, J.P., Expression of intermediate filament components in IMR32K cells that develop epitopes associated with neurofibrillary tangles of Alzheimer's disease, J. Cell Biol., 111 (1990) 41a (207).
37. Ko, L., Sheu, K.-F.R., Young, O. and Blass, J.P., Induction of epitopes associated with neurofibrillary tangles in clonal mouse neuroblastoma (S20Y) cells, Acta Neuropathol. (Berl.), 81 (1990) 30-40.
38. Ko, L., Sheu, K.-F.R., Young, O., Thaler, H. and Blass, J.P., Expression of cultured human neuroblastoma cells of epitopes associated with affected neurons in Alzheimer's disease, Am. J. Pathol., 136 (1990) 867-879.
39. Kosik, K.S., Joachim, C.L. and Selkoe, D.J., Microtubule-associated protein tau is a major antigenic component of paired helical filaments in Alzheimer disease, Proc. Natl. Acad. Sci. USA, 83 (1986) 4044-4048.
40. Kosik, K.S., Orecchio, L.D., Binder, L.I., Trojanowski, J.Q., Lee, V.M.-Y. and Lee, G., Epitopes that span the tau molecule are shared with paired helical filaments, Neuron, 1 (1988) 817-825.
41. Kosik, K.S., Orecchio, L.D., Bakalis, S. and Neve, R.L., Developmentally regulated expression of specific tau sequences, Neuron, 2 (1989) 1389-1397.
42. Ksiezak-Reding, H., Binder, L.I. and Yen, S.H., Alzheimer disease proteins (A69) share epitopes with tau but show distinct biochemical properties, J. Neurosci. Res., 25 (1990) 420-430.
43. Ksiezak-Reding, H., Chien, C-H., Lee, V.M.-Y. and Yen, S.-H., Mapping of the Alz 50 epitope in microtubule-associated proteins tau, J. Neurosci. Res., 25 (1990) 412-419.
44. Langui, D., Anderton, B.H., Brion, J.P. and Ulrich, J., Effect of aluminum chloride on cultured cells from rat brain hemispheres, Brain Res., 438 (1988) 67-76.
45. Lee, G., Cowan, N. and Kirschner, M., The primary structure and heterogeneity of tau protein from mouse brain, Science, 239 (1988) 285-288.
46. Lee, V.M.-Y., Balin, B., Otvos, L. and Trojanowski, J., A68: a major subunit of paired helical filaments and derivatized form of normal tau, Science, 251 (1991) 675-678.
47. Lindwall, G. and Cole, R.D., Phosphorylation affects the ability of tau protein to promote microtubule assembly, J. Biol. Chem., 259 (1984) 5301-5305.
48. Liu, W.-K., Ksiezak-Reding, H. and Yen, S.-H., Abnormal tau proteins from Alzheimer's disease brains. Purification and amino acid analysis, J. Biol. Chem., 266 (1991) 21723-21727.
49. Liu, W.-K., Dickson, D.W. and Yen, S.-H., Heterogeneity of tau proteins in Alzheimer's disease. Evidence for increased expression of an isoform and preferential distribution of a phosphorylated isoform in neurites, Am. J. Pathol., 142 (1993) 387-394.
50. Liu, W.-K., Dickson, D.W. and Yen, S.-H., Amino acid residues 226-240 of tau, which encompass the first Lys-Ser-Pro site of tau, are partially phosphorylated in Alzheimer paired helical filament-tau, J. Neurochem., 62 (1994) 1055-1061.
51. Mareck, A., Fellous, A., Francon, J. and Nunez, J., Changes in composition and activity of microtubule-associated proteins during brain development, Nature, 284 (1980) 353-355.
52. Mavilia, C., Couchie, D. and Nunez, J., Diversity of high-molecular-weight tau proteins in different regions of the nervous system, J. Neurochem., 63 (1994) 2300-2306.
53. Mori, H., Kondo, J. and Ihara, Y., Ubiquitin is a component of paired helical filaments in Alzheimer's disease, Science, 235 (1987) 1641-1644.
54. Morishima, M. and Ihara, Y., Posttranslational modifications of tau in paired helical filaments, Dementia, 5 (1994) 282-288.
55. Novak, M., Truncated tau protein as a new marker for Alzheimer's disease, Acta Virol., 38 (1994) 173-189.
56. Nukina, N. and Ihara, Y., One of the antigenic determinants of paired helical filaments is related to tau protein, J. Biochem., 99 (1986) 1541-1544.
57. Nunez, J., Differential expression of microtubule components during brain development, Dev. Neurosci., 8 (1986) 421-457.
58. Oblinger, M.M., Argasinski, A., Wong, J. and Kosik, K.S., Tau gene expression in rat sensory neurons during development and regeneration, J. Neurosci., 11 (1991) 2453-2459.
59. Olmsted, J.B., Microtubule-associated proteins, Annu. Rev. Cell Biol., 2 (1986) 421-457.
60. Parysek, L.M. and Goldman, R.D., Distribution of a novel 57 kDa intermediate filament (IF) protein in the nervous system, J. Neurosci., 8 (1988) 555-563.
61. Peng, A., Binder, L.I. and Black, M.M., Biochemical and immunological analysis of cytoskeletal domains of neurons, J. Cell Biol., 102 (1986) 252-262.
62. Perry, G., Friedman, R., Shaw, G. and Chau, V., Ubiquitin is detected in neurofibrillary tangles and senile plaque neuntes of Alzheimer's disease brains, Proc. Natl. Acad. Sci. USA, 84 (1987) 3033-3036.
63. Potier, M.-M., de Nechaud, B. and Gros, F., Peripherin, a new member of the intermediate filament protein family, Dev. Neurosci., 6 (1984) 335-344.
64. Smith, M.A., Taneda, S., Richey, P.L., Miyata, S., Yan, S.-D., Stern, D., Sayre, L.M., Monnier, V.M. and Perry, G., Advanced Maillard reaction end products are associated with Alzheimer disease pathology, Proc. Natl. Acad. Sci. USA, 91 (1994) 5710-5714.
65. Teng, K.K., Georgieff, I.S., Aletta, J.M., Nunez, J., Shelanski, M.L. and Greene, L.A., Characterization of PC12 cell subclone (PC12-C41) with enhanced neurite outgrowth capacity: implications for a modulatory role of high molecular weight tau in neuritogenesis, J. Cell Sci., 106 (1993) 611-626.
66. Terry, R.D., Gonatas, N.K. and Weiss, M. Ultrastructural studies in Alzheimer's disease presenile dementia, Am. J. Pathol, 44 (1964) 269-297.
67. Terry, R.D. and Katzman, R., Senile dementia of the Alzheimer type, Ann. Neurol., 14 (1983) 497-506.
68. Tucker, R.P., Binder, L.I., Viereck, C., Hemmings, B.A. and Matus, A.I., The sequential appearance of low-and high-molecular-weight forms of MAP2 in the developing cerebellum, J. Neurosci., 8 (1988) 4503-4512.
69. Vincent, I., Rosado, M., Kim, E. and Davies, P. Increased production of paired helical filament epitopes in a cell culture system reduces the turnover of tau, J. Neurochem., 62 (1994) 715-723.
70. Wiche, G., Oberkanins, C. and Himmler, A. Molecular structure and function of microtubule associated proteins, Int. Rev. Cytol., 124 (1990) 217-273.
71. Wille, H., Mandelkow, E.-M., Dingus, J., Vallee, R.B., Binder, L.I. and Mandelkow, E., Domain structure and antiparallel dimers of microtubule-associated protein 2 (MAP2), J. Struct. Biol., 108 (1992) 49-61.
72. Wisniewski, H.M., Narang, H.K. and Terry, R.D., Neurofibrillary tangles of paired helical filaments, J. Neurol. Sci., 27 (1976) 173-181.
73. Wolozin, B.L., Pruchnicki, A., Dickson, D.W. and Davies, P., A neuronal antigen in the brains of Alzheimer's patients, Science, 232 (1986) 648-650.
74. Wood, J.G., Mirra, S.S., Pollack, N.J. and Binder, L.I., Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau, Proc. Natl. Acad. Sci. USA, 83 (1986) 4040-4043.
75. Van, S.-D., Chen, X., Schmidt, A.-M., Brett, J., Godman, G., Zou, Y.-S., Scott, C.W., Caputo, C., Frappier, T., Smith, M.A., Perry, G., Yen, S.-H. and Stern, D. Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress, Proc. Natl. Acad. Sci. USA, 91 (1994) 7787-7791.
76. Yen, S.-H., Dickson, D.W., Liu, W.-K., Ksiezak-Reding, H., Microtubule-associated protein tau to paired helical filaments and Alzheimer neurofibrillary tangles: an overview. In F. Ikuda (Ed), Neuropathology in Brain Research, Elsevier Science Publishers, Amsterdam, 1991, pp.33-44.