Identification of microtubule-associated protein tau isoforms in Alzheimer's paired helical filaments

Brain Research Bulletin

Volumn 43, Issue 5, 1997, Pages 501-508

  McLaughlin, Lea ^a   Zemlan, Frank P ^a   Dean, Gary E ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

A68; AD66; Neurofibrillary tangles; PHF tau

Indexed keywords

TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; HUMAN; HUMAN TISSUE; MICROTUBULE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

EID: 0030838124     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0361-9230(97)80003-2     Document Type: Article

References (54)

1. Alzheimer A. Uber eine eigenartige erkankung der hirnrinde. Allg. Z. Psychiatry. 64:1907;146-148.
2. Arriagada P. V., Growdon J. H., Hedley-Whyte E. T., Hyman B. J. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology. 42:1992;631-639.
3. Binder L. I., Frankfurter A., Rebhun L. The distribution of tau in the mammalian central nervous system. J. Cell. Biol. 101:1985;1371-1378.
4. Bondareff W., Wischik C. M., Novak M., Amos W. B., Klug A., Roth A. Molecular analysis of neurofibrillary degeneration in Alzheimer's disease. An immunohistochemical study. Am. J. Pathol. 137:1990;711-723.
5. 396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron. 10:1993;1089-1099.
6. Caputo C. B., Salama A. I. The amyloid proteins of Alzheimer's disease as potential targets for drug therapy. Neurobiol. Aging. 10:1989;451-461.
7. Caputo C. B., Wischik C. M., Novak M., Scott C. W., Brunner W. F., Montejo de Garcini E., Lo M. M. S., Norris T. E., Salama A. I. Immunological characterization of the region of tau protein that is bound to Alzheimer paired helical filaments. Neurobiol. Aging. 13:1992;267-274.
8. Cotman C. W., Geddes J. W., Kahle J. S. Axon sprouting in the rodent and Alzheimer's brain. A reactivation of developmental mechanisms? Prog. Brain Res. 83:1990;427-434.
9. Couchie D., Nunez J. An immunological characterization of microtubule-associated proteins specific for the immature brain. FEBS Lett. 188:1985;331-335.
10. Crowther J., Goedert M., Wischik C. M. The repeat region of microtubule-associated protein tau forms part of the core of the paired helical filament of Alzheimer's disease. Ann. Med. 21:1989;127-132.
11. Dickson D. W., Kseizak-Reding H., Liu W.-K., Crowe A., Yen S.-H. C. Immunocytochemistry of neurofibrillary tangles with antibodies to subregions of tau protein: Identification of hidden and cleaved tau epitopes and a new phosphorylation site. Acta Neuropathol. 84:1992;596-605.
12. Endoh R., Ogawara M., Iwatsubo T., Nakano I., Mori H. Lack of carboxy terminal sequences of tau in ghost tangles of Alzheimer's disease. Brain Res. 601:1993;164-172.
13. Goedert M., Wischik C. M., Crowther R. A., Walker J. E., Klug A. Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer's disease: Identification as the microtubule-associated protein tau. Proc. Natl. Acad. Sci. USA. 85:1988;4051-4055.
14. Goedert M., Spillanti M. G., Jakes R., Rutherford D., 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.
15. Goedert M., Spillatini M. G., Jakes R. Localization of the Alz-50 epitope in recombinant human microtubule-associated protein tau. Neurosci. Lett. 126:1991;149-154.
16. Goedert M., Spillantini M. G., Cairns N. J., Crowther R. A. Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron. 8:1992;159-168.
17. Greenberg S. G., Davies P. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. USA. 87:1990;5827-5831.
18. τ proteins display the same biochemical properties as normal. J. Biol. Chem. 267:1992;564-569.
19. Grundke-Iqbal I., Iqbal K., Quinlan M., Tung Y.-C., Zaidi M. S., Wisneiwski H. M. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 261:1986;6084-6089.
20. Grundke-Iqbal I., Iqbal K., Tung Y.-C., Quinlan M., Wisniewski H. M., Binder L. I. Abnormal phosphorylation of the microtubule-associated protein τ (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA. 83:1986;4913-4917.
21. Harrington C. R., Mukaetova-Ladinska E. B., Hills R., Edwards P. C., Montejo de Garcini E., Novak M., Wischik C. M. Measurement of distinct immunocytochemical presentations of tau protein in Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 88:1991;5842-5846.
22. Hasegawa M., Morishima-Kawashima M., Takio K., Suzuki M., Titani K., Ihara Y. Protein sequence and mass spectrophotometric analyses of tau in the Alzheimer's disease brain. J. Biol. Chem. 267:1992;17047-17054.
23. Himmler A., Drechsel D., Kirschner M. W., Martin D. W. Jr. Tau consists of a set of proteins with repeated carboxy-terminal microtubule binding domains and variable amino-terminal domains. Mol. Cell Biol. 9:1989;1381-1388.
24. Hunter T. Protein kinase families. Methods Enzymol. 200:1991;3-37.
25. Kanemaru K., Takio K., Miura R., Titani K., Ihara Y. Fetal-type phosphorylation of the τ in paired helical filaments. J. Neurochem. 58:1992;1667-1675.
26. Kidd M. Paired helical filaments in electron microscopy of Alzheimer's disease. Nature. 197:1963;192-193.
27. Kondo J., Honda T., Mori H., Hamada Y., Miura R., Ogawara M., Ihara Y. The carboxy third of tau is tightly bound to paired helical filaments. Neuron. 1:1988;827-834.
28. Konigsberg W. H., Henderson L. Removal of sodium dodecylsulfate from proteins by ion-pair extraction. Methods Enzymol. 91:1983;254-259.
29. Kosik K. S., Joachim C. L., Selkoe D. J. Microtubule-associated protein tau is a major antigenic component of paired helical filaments in Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 83:1986;4044-4048.
30. Kosik K. S., Orrechio L. D., Binder L., Trojanowski J. Q., Lee V. M.-Y., Lee G. Epitopes that span the tau molecule are shared with paired helical filaments. Neuron. 1:1988;817-825.
31. Kosik K. S., Orrechio L. D., Bakalis S., Neve R. L. Developmentally regulated expression of specific tau sequences. Neuron. 2:1989;1389-1397.
32. Kseizak-Reding H., Dickson D. W., Davies P., Yen S.-H. Recognition of tau epitopes by anti-neurofilament antibodies that bind to Alzheimer neurofibrillary tangles. Proc. Natl. Acad. Sci. USA. 84:1987;3810-3814.
33. Ksiezak-Reding H., Liu W. K., Yen S.-H. Phosphate analysis and dephosphorylation of modified tau associated with paired helical filaments. Brain Res. 597:1992;209-219.
34. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
35. Lee V. M.-Y., Balin B. J., Otvos L Jr., Trojanowski J. Q. A68: A major subunit of paired helical filaments and derivatized forms of normal tau. Science. 251:1991;675-678.
36. Lichtenberg-Kraag B., Mandelkow E.-M., Biernat J., Steiner B., Schroter C., Gustke N., Meyer H. E., Mandelkow E. Phosphorylation dependent epitopes of neurofilament antibodies on tau protein and relationship with Alzheimer tau. Proc. Natl. Acad. Sci. USA. 89:1992;5384-5388.
37. Lindwall G., Cole R. D. Phosphorylation affects the ability of tau protein to promote microtubule assembly. J. Biol. Chem. 259:1984;5301-5305.
38. Lindwall G., Cole R. D. The purification of tau protein and the occurrence of two phosphorylation states of tau in brain. J. Biol. Chem. 259:1984;12241-12245.
39. Mori H., Hamada Y., Kawaguchi M., Honda T., Kondo J., Ihara Y. A distinct form of tau is selectively incorporated into Alzheimer's paired helical filaments. Biochem. Biophys. Res. Commun. 159:1989;1221-1226.
40. Nieto A., Correas I., Lopez-Otin C., Avila J. Tau-related protein present in paired helical filaments has a decreased tubulin binding capacity as compared with microtubule-associated protein tau. Biochem. Biophys. Acta. 1096:1991;197-204.
41. Novak M., Wischik C. M., Edwards P. C., Pannell R., Milstein C. Characterization of the first monoclonal antibody against the pronase resistant core of the Alzheimer paired helical filament. Prog. Clin. Biol. Res. 317:1989;755-761.
42. Novak M., Jakes R., Edwards P., Milstein C., Wischik C. M. Difference between the tau protein of Alzheimer's paired helical filament core and normal tau revealed by epitope analysis of monoclonal antibodies 423 and 7.51. Proc. Natl. Acad. Sci. USA. 88:1991;5837-5841.
43. O'Farrell P. Z., Goodman H. M., O'Farrell P. H. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 12:1977;1133-1142.
44. Schagger H., von Jagow G. Tricine-sodium dodecylsulfate-poly- acrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:1987;368-379.
45. Selkoe D. J. Biochemistry of altered brain proteins in Alzheimer's disease. Annu. Rev. Neurosci. 12:1989;463-490.
46. Smith M. A., Taneda S., Richey P. L., Miyata S., Yan S.-D., Stern D., Sayre L. M., Monnier V. M., Perry G. Advanced Maillard reaction end products are associated with Alzheimer's disease pathology. Proc. Natl. Acad. Sci. USA. 91:1994;5710-5714.
47. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:1979;4350-4354.
48. Ueda K., Masilah E., Saitoh T., Bakalis S. L., Scoble H., Kosik K. S. Alz-50 recognizes a phosphorylated epitope of tau proteins. J. Neurosci. 10:1990;3295-3304.
49. Vogelsang G. D., Zemlan F. P., Dean G. E. Purification and solubilization of paired helical filaments from Alzheimer. Brain. J. Neurochem. 54:1990;148-155.
50. Wischik C. M., Novak M., Thorgersen H., Edwards P. C., Runswick M. J., Jakes R., Walker J. E., Milstein C., Roth M., Klug A. Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 85:1988;4506-4510.
51. Wischik C. M., Novak M., Edwards P. C., Klug A., Tichelarr W., Crowther R. A. Structural characterization of the core of the paired helical filament of Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 85:1989;4884-4888.
52. Wolozin B., Scicutella A., Davies P. Reexpresion of a developmentally regulated antigen in Down syndrome and Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 85:1988;6202-6206.
53. Yan 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., Stern D. Glycated tau protein in Alzheimer's disease: A mechanism for induction of oxidant stress. Proc. Natl. Acad. Sci. USA. 91:1994;7787-7791.
54. Zenlan F. P., Dean G. E. Monoclonal antibody PHF-9 recognizes phosphorylated serine 404 or tau protein and labels paired helical filaments. J. Neurosci. Research. 46:1996;90-97.