The association of tissue transglutaminase with human recombinant tau results in the formation of insoluble filamentous structures

Brain Research

Volumn 745, Issue 1-2, 1997, Pages 21-31

  Appelt, Denah M ^a   Balin, Brian J ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Human recombinant tau htau 40; Insoluble filament; Neurofibrillary tangle; Paired helical filament; Transglutaminase

Indexed keywords

PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RECOMBINANT PROTEIN; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; NEUROFIBRILLARY TANGLE; NEUROFILAMENT; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; ULTRASTRUCTURE;

ALZHEIMER DISEASE; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HIPPOCAMPUS; HUMANS; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; NEUROFILAMENT PROTEINS; RECOMBINANT PROTEINS; TAU PROTEINS; TRANSGLUTAMINASES;

EID: 0031015814     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(96)01121-3     Document Type: Article

References (44)

1. Appelt, D.M., Kopen, G.C., Boyne, L.J. and Balin, B.J., Localization of transglutaminase in hippocampal neurons: Implications for Alzheimer's Disease, J. Histochem. Cytochem., 44 (1996) in press.
2. Appelt, D.M., Kopen, G.C., Boyne, L.J. and Balin, B.J., Tissue transglutaminase catalyzes the in vitro formation of insoluble structures from human recombinant tau, Soc. Neurosci. Abstr., 21:296.9A (1995) 743.
3. Barsigian, C., Stern, A.M. and Martinez, J., Tissue (type II) transglutaminase covalently incorporates itself, fibrinogen, or fibronectin into high molecular weight complexes on the extracellular surface of isolated hepatocytes, J. Biol Chem., 266 (1991) 22501-22509.
4. Binder, L.I., Frankfurter, A. and Rebhun, L.I., The distribution of tau in the mammalian central nervous system, J. Cell Biol., 101 (1985) 1371-1378.
5. Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72 (1976) 248-295.
6. Byrd, J.C. and Lichti, U., Two types of transglutaminase in the PC12 pheochromocytoma cell line, Stimulation by sodium butyrate, J. Biol. Chem., 262 (1987) 11699-11705.
7. Crowther, R.A., Oleson, O.F., Jakes, R. and Goedert, M., The microtubule binding repeats of tau protein assemble into filaments like those found in Alzheimer's disease, FEBS Lett., 309 (1992) 199-202.
8. Crowther, R.A., Oleson, O.F., Smith, M.J., Jakes, R. and Goedert, M., Assembly of Alzheimer-like filaments from full-length tau protein, FEBS Lett., 337 (1994) 135-138.
9. Dudek, S.M. and Johnson, G.V.W., Transglutaminse catalyzes the formation of sodium dodecyl sulfate-insoluble, Alz 50-reactive polymers of tau, J. Neurochem., 61 (1993) 1159-1162.
10. Facchiano, F., Benfenati, F., Valtorta, F. and Luini A., Covalent modification of synapsin 1 by a tetanus-toxin-activated transglutaminase, J. Biol. Chem., 268 (1993) 4588-4591.
11. Fesus, L., Thomazy, V. and Falus, A., Induction and activation of tissue transglutaminase during programmed cell death, FEBS Lett., 224 (1987) 104-108.
12. Folk, J.E. and Finlayson, J.S., The ε-(γ-glutamyl)lysine crosslink and the catalytic role of transglutaminases, Adv. Protein Chem., 31 (1977) 1-133.
13. Gache, Y., Guilleminot, J., Ricolfi, F., Theiss, G. and Nunez, J., A tau-related protein of 130 kDa is present in Alzheimer brain, J. Neurochem., 58 (1992) 2005-2010.
14. Gilad, G.M. and Varon, E., Transglutaminase activity in rat brain: characterization, distribution and changes with age, J. Neurochem., 4 (1985) 1522-1526.
15. 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., 9 (1990) 4225-4230.
16. Greenberg, S.G. and 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.
17. Grundke-Iqbal, I., Iqbal, K., Tung, Y.C., Quinlan, M., Wisniewski, H.M. and Binder, L.I., Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology, Proc. Natl. Acac. Sci. USA, 83 (1986) 4913-4917.
18. Grundke-Iqbal, I., Iqbal, K., Quinlan, M., Tung, Y.C., Zaidi, M.S. and Wisniewski, H.M., Microtubule-associated protein tau. A component of Alzheimer paired helical filaments, J. Biol. Chem., 261 (1986) 6084-6089.
19. Hand, D., Campoy, F.J., Clark, S., Fisher, A. and Haynes, L.W., Activity and distribution of tissue transglutaminase in association with nerve muscle synapses, J. Neurochem., 61 (1993) 1064-1072.
20. Iwaki, T., Miyanzono, M., Hitotsumatsu, T. and Tateishi, J., An immunohistochemical study of tissue transglutaminase in gliomas with reference to their cell dying processes, Am. J. Pathol., 145 (1994) 776-781.
21. Khachaturian, Z.S., Cotman, C.W. and Pettegrew, J.W., Calcium, membranes, aging, and Alzheimer's disease, Ann. NY Acad. Sci., 568 (1989) 1-292.
22. Korner, G. and Bachrach, U., Activation and de novo synthesis of transglutaminase in cultured glioma cells, J. Cell. Physiol., 124 (1985) 379-385.
23. Ksiezak-Reding, H., Binder, L.I. and Yen, S.-H., Alzheimer disease proteins (A68) share epitopes with tau but show distinct biochemical properties, J. Neurosci. Res., 25 (1990) 420-430.
24. Ledesma, M.D., Bonay, P., Colaco, C. and Avila, J., Analysis of microtubule-associated protein tau glycation in paired helical filaments, J. Biol. Chem., 269 (1994) 21614-21619.
25. Lee, V.M.-Y., Balin, B.J., Otvos, L. and Trojanowski, J.Q., A68 - a major subunit of paired helical filaments and derivatized forms of normal tau, Science, 251 (1991) 675-678.
26. Loesser, K. and Franzini-Armstrong, C., A simple method for freeze-drying of macromolecules and macromolecular complexes, J. Struct. Biol., 103 (1990) 48-56.
27. LeMosy, E.K., ErickSon, H.P., Beyer, W.F., Radek, J.T., Jeong, J.-M., Murthy, S.N.P. and Lorand, L., Visualization of purified fibronectin-transglutaminase complexes, J. Biol. Chem., 267 (1992) 7880-7885.
28. Lorand, L., Transglutaminase-mediated cross-linking of proteins and cell aging: the erythrocyte and lens models, Adv. Exp. Med. Biol., 231 (1988) 79-94.
29. Maccioni, R.B. and Seeds, N.W., Transglutaminase and neuronal differentiation, Mol. Cell. Biochem., 69 (1986) 161-168.
30. Miller, C.J. and Anderton, B.H., Transglutaminase and the neuronal cytoskeleton in Alzheimer's disease, J. Neurochem., 46 (1986) 1912-1922.
31. Miller, M.L. and Johnson, G.W., Transglutaminase cross-linking of the τ protein, J. Neurochem., 65 (1995) 1760-1770.
32. Mould, A.P., Holmes, D.F., Kadler, K.E. and Chapman, J.A., Mica sandwich technique for preparing macromolecules for rotary shadowing, J. Ultrastruct. Res., 91 (1985) 66-76.
33. Piacentini, M., Anniccchiarico-Petruzzelli, M., Oliverio, S., Piredda, L., Siedler, J.L. and Melini, G., Phenotype-specific 'tissue' transglutaminase regulation in human neuroblastoma cells in response to retinoic acid: correlation with cell death by apoptosis, Int. J. Cancer, 52 (1992) 271-278.
34. Price, D.L., Koo, E.H. and Unterbeck, A., Cellular and molecular biology of Alzheimer's disease, Bioessays, 10 (1989) 69-74.
35. Reichelt, K.L. and Poulsen E., Gamma-glutamylamino transferase and TGase in subcellular fractions of rat cortex and in cultured astrocytes, J. Neurochem., 59 (1992) 500-504.
36. Selkoe, D.J., Biochemistry of altered brain proteins in Alzheimer's disease, Annu. Rev. Neurosci., 12 (1989) 463-90.
37. Selkoe, D.J., Abraham, C. and Ihara, Y., Brain transglutaminase: In vitro crosslinking of human neurofilament proteins into insoluble polymers, Proc. Natl. Acad. Sci. USA, 79 (1982) 6070-6074.
38. Selkoe, D.J., Ihara, Y and Salazar, F.J., Alzheimer's disease: Insolubility of partially purified paired helical filaments in sodium dodecyl sulfate and urea, Science, 215 (1982) 1243-1245.
39. Smith, M.A., Siedlak, S.L., Richey, R.L., Nagaraj, R.H., Elhammer, A. and Perry, G., Quantitative solubilization and analysis of insoluble paired helical filaments from Alzheimer disease, Brain Res., 717 (1996) 99-108.
40. 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, 92 (1995) 2016-2020.
41. Tomei, L.D. and Cope, P.O., Apoptosis: The molecular basis of cell death, In Current Communications in Cell and Molecular Biology, Cold Spring Harbor Lab Press, 1991, 295 pp.
42. Wisniewski, K., Jervis, G.A., Moreta, R.C. and Wisniewski, H.M., Alzheimer neurofibrillary tangles in diseases other than senile and presenile dementia, Ann. Neurol., 5 (1979) 288-294.
43. Wille, H., Drewes, G, Biernat, J., Mandelkow, E.M. and Mandelkow, E., Alzheimer-like paired helical filaments and antiparallel dimers formed form microtubule-associated protein tau in vitro, J. Cell. Biol., 118 (1992) 573-584.
44. 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. and Stern, A.M., Glycated tau protein in Alzheimer Disease: A mechanism for induction of oxidant stress, Proc. Natl. Acad. Sci. USA, 91 (1994) 7787-7791.