Characterization of in vitro glycation sites of tau

Journal of Neurochemistry

Volumn 69, Issue 4, 1997, Pages 1709-1719

  Nacharaju, Parimala ^a   Ko, Li Wen ^a   Yen, Shu Hui C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Glycation sites; Tau glycation

Indexed keywords

LYSINE; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; NEUROFIBRILLARY TANGLE; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN POLYMORPHISM; PROTEIN PROCESSING; PROTEIN PURIFICATION; SENILE PLAQUE;

EID: 0030964705     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69041709.x     Document Type: Article

References (61)

1. Agarwal K. C., Parks R. E., Widness J. A., and Schwartz R. (1985) Nonenzymatic glycosylation of erythrocytic proteins in normal and diabetic subjects: enzymes of nucleoside and nucleotide metabolism. Diabetes 34, 251-255.
2. Ancos J. G., Correas I., and Avila J. (1993) Differences in microtubule binding and self-association abilities of bovine brain tau isoforms. J. Biol. Chem. 268, 7976-7982.
3. Arai K., Iijuka S., Tada Y., Oikawa K., and Taniguchi N. (1987) Increase in the glycosylated form of erythrocyte Cu-Zn-superoxide dismutase in diabetes and close association of the nonenzymatic glycosylation with the enzyme activity. Biochim. Biophys. Acta 924, 292-296.
4. Bai Y., Ueno H., and Manning J. M. (1989) Some factors that influence the nonenzymatic glycation of peptides and polypeptides by glyceraldehyde. J. Protein Chem. 8, 299-315.
5. Brandt R. and Lee G. (1993) Functional organization of microtubule-associated tau: identification of regions which affect microtubule growth, nucleation and bundle formation in vitro. J. Biol. Chem. 268, 3414-3419.
6. Brownlee M. (1992) Glycation products and the pathogenesis of diabetes complications. Diabetes Care 15, 1835-1843.
7. Brownlee M. and Cerami A. (1981) The biochemistry of the complications of diabetes mellitus. Annu. Rev. Biochem. 50, 385-432.
8. 1c. Biochem. Biophys. Res. Commun. 67, 103-109.
9. Bunn H. F., Gabbay K. H., and Gallop P. M. (1978) The glycosylation of hemoglobin: relevance to diabetes mellitus. Science 200, 21-27.
10. Charonis A. S. and Tsilibary E. C. (1992) Structural and functional changes of laminin and type IV collagen after nonenzymic glycation. Diabetes 41 (Suppl. 2), 49-51.
11. Cleveland D. W., Hwo S.-Y., and Kirschner M. W. (1977) Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 116, 227-247.
12. Day J. F., Thorpe S. R., and Baynes J. W. (1979) Nonenzymatically glycosylated albumin: in vitro preparation and isolation from normal human serum. J. Biol. Chem. 254, 595-597.
13. ∈-(carboxymethyl)lysine in lens proteins. Biochemistry 28, 9464-9468.
14. Eble A. S., Thorpe S. R., and Baynes J. W. (1983) Nonenzymatic glucosylation and glucose-dependent cross-linking of protein. J. Biol. Chem. 258, 9406-9412.
15. Fu M., Wells-Knecht K. J., Blackledge J. A., Lyons T. J., Thorpe S. R., and Baynes J. W. (1994) Glycation, glycoxydation, and cross-linking of collagen by glucose: kinetics, mechanisms, and inhibition of late stages of the Maillard reaction. Diabetes 43, 676-683.
16. Glenner G. G. and Wong C. W. (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890.
17. 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.
18. Goedert M., Spillantini M. G., Jakes R., Rutherford D., and 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.
19. Goedert M., Spillantini M. G., Cairns N. J., and Crowther R. A. (1992) Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8, 159-168.
20. Grandhee S. K. and Monnier V. M. (1991) Mechanism of formation of the Maillard protein cross-link pentosidine: glucose, fructose, and ascorbate as pentosidine precursors. J. Biol. Chem. 266, 11649-11653.
21. Greenberg S. G. and Davies P. (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. USA 87, 5827-5831.
22. Hayase F., Nagaraj R. H., Miyata S., Njoroge F. G., and Monnier V. M. (1989) Aging of proteins: immunological detection of a glucose-derived pyrrole formed during Maillard reaction in vivo. J. Biol. Chem. 264, 3758-3764.
23. Himmler A. (1989) Structure of bovine tau gene: alternatively spliced transcripts generate a protein family. Mol. Cell. Biol. 9, 1389-1396.
24. Iberg N. and Fluckiger R. (1986) Nonenzymatic glycosylation of albumin in vivo: identification of multiple glycosylated sites. J. Biol. Chem. 261, 13542-13545.
25. Iqbal K., Grundke-Iqbal I., Zaidi T., Merz P. A., Wen G. Y., Shaikh S. S., Wisniewski H. M., Alafuzoff I., and Winblad B. (1986) Defective brain microtubule assembly in Alzheimer's disease. Lancet 2, 421-426.
26. Iqbal K., Grundke-Iqbal I., Smith A. J., George L., Tung Y., and Zaidi T. (1989) Identification and localization of tau peptide to paired helical filaments of Alzheimer's disease. Proc. Natl. Acad. Sci. USA 86, 5646-5650.
27. Keil B. (1971) Trypsin, in The Enzymes. Vol. III (Boyer P. D., ed), pp. 250-275. Academic Press, New York.
28. Kent M. J. C., Light N. D., and Bailey A. J. (1985) Evidence for glucose-mediated covalent cross-linking of collagen after glycosylation in vitro. Biochem. J. 225, 745-752.
29. Kosik K. S., Joachim C. L., and Selkoe D. J. (1986) Microtubule-associated protein tau is a major antigenic component of paired helical filaments in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 83, 4044-4048.
30. Ledesma M. D., Bonay P., Colaco C., and Avila J. (1994) Analysis of microtubule-associated protein tau glycation in paired helical filaments. J. Biol. Chem. 269, 21614-21619.
31. Ledesma M. D., Bonay P., and Avila J. (1995) τ protein from Alzheimer's disease patients is glycated at its tubulin-binding domain. J. Neurochem. 65, 1658-1664.
32. Ledesma M. D., Medina M., and Avila J. (1996) The in vitro formation of recombinant tau polymers: effect of phosphorylation and glycation. Mol. Chem. Neuropathol. 27, 249-258.
33. Lee C. K. and Manning J. M. (1973 ) Kinetics of the carbamylation of the amino groups of sickle cell hemoglobin by cyanate. J. Biol. Chem. 248, 5861-5865.
34. Lee V. M.-Y., Balin B. J., Otvos L. Jr., and Trojanowski J. Q. (1991) A68: a major subunit of paired helical filaments and derivatized forms of normal tau. Science 251, 675-678.
35. Liu W.-K., Ksiezak-Reding H., and Yen S.-H. (1991) Abnormal tau protein from Alzheimer's disease brain. J. Biol. Chem. 266, 21723-21727.
36. Lorenzi M., Cagliero E., Markey B., Henricksen T., Witztum J. L., and Sampietro T. (1984) Interaction of human endothelial cells with elevated glucose concentrations and native and glycosylated low density lipoproteins. Diabetologia 26, 218-222.
37. Masters C. L., Simms G., Weinman N. A., Multhaup G., McDonald B. L., and Beyreuther K. (1985) Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA 82, 4245-4249.
38. McPherson J. D., Shilton B. H., and Walton D. J. (1988) Evidence for glycation of horse liver alcohol dehydrogenase in vivo. Biochem. Biophys. Res. Commun. 152, 711-716.
39. Monnier V. M., Sell D. R., Nagaraj R. H., Miyata S., Grandhee S., Odetti P., and Ibrahim S. A. (1992) Maillard reaction-mediated molecular damage to extracellular matrix and other tissue proteins in diabetes, aging, and uremia. Diabetes 41, 36-41.
40. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Titani K., and Ihara Y. (1995) Proline-derived and non-proline-derived phosphorylation of PHF-tau. J. Biol. Chem. 270, 823-829.
41. Nacharaju P. and Acharya A. S. (1992) Amadori rearrangement potential of hemoglobin at its glycation sites is dependent on the three-dimensional structure of protein. Biochemistry 31, 12673-12679.
42. Nieto A., Correas I., Lopez-Otin C., and Avila J. (1991) Tau-related protein present in paired helical filaments has a decreased tubulin binding capacity as compared with microtubule-associated protein tau. Biochim. Biophys. Acta 1096, 197-204.
43. Ozols J. (1990) Amino acid analysis. Methods Enzymol. 182, 587-601.
44. Palinski W., Koschinsky T., Butler S. W., Miller E., Vlassara H., Cerami A., and Witztum J. L. (1995) Immunological evidence for the presence of advanced glycation end products in atherosclerotic lesions of euglycemic rabbits. Arterioscler. Thromb. Vasc. Biol. 15, 571-582.
45. Pande A., Garner W. H., and Spector A. (1979) Glucosylation of human lens protein and cataractogenesis. Biochem. Biophys. Res. Commun. 89, 1260-1266.
46. Reiger K. M. (1991) Nonenzymatic glycation of collagen in aging and diabetes. Proc. Soc. Exp. Biol. Med. 196, 17-29.
47. Reiger K. M., Amigable M., and Last J. A. (1992) Nonenzymatic glycation of type I collagen: the effects of aging on preferential glycation sites. J. Biol. Chem. 267, 24207-24216.
48. Robins S. P. and Bailey A. J. (1972) Age-related changes in collagen: the identification of reducible lysine-carbohydrate condensation product. Biochem. Biophys. Res. Commun. 48, 76-84.
49. Selkoe D. J., Ihara Y., and Salazar F. J. (1982) Alzheimer's disease: insolubility of partially purified paired helical filaments in sodium dodecyl sulfate and urea. Science 215, 1243-1245.
50. Shaklai N., Garlick R. L., and Bunn H. F. (1984) Nonenzymatic glycosylation of human serum albumin alters its conformation and function. J. Biol. Chem. 259, 3812-3817.
51. Shapiro R., McManus M. J., Zalut C., and Bunn H. F. (1980) Sites of nonenzymatic glycosylation of human hemoglobin A. J. Biol. Chem. 255, 3120-3127.
52. Shilton B. H. and Walton D. J. (1991) Sites of glycation of human and horse liver alcohol dehydrogenase in vivo. J. Biol. Chem. 266, 5587-5592.
53. 1c with prevalent cardiovascular disease in the original cohort of the Framingham heart study. Diabetes 41, 202-208.
54. Smith M. A., Teneda S., Richey P. L., Miyata S., Van S.-D., Stern D., Sayre L. M., Monnier V. M., and Perry G. (1994) Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc. Natl. Acad. Sci. USA 91, 5710-5714.
55. Stevens V. J., Rouzer C. A., Monnier V. M., and Cerami A. (1978) Diabetic cataract formation: potential role of glycosylation of lens crystallins. Proc. Natl. Acad. Sci. USA 75, 2918-2922.
56. Trueb B., Holenstein C. G., Fisher R. W., and Winterhalter K. H. (1980) Nonenzymatic glycosyiation of proteins: a warning. J. Biol. Chem. 255, 6717-6720.
57. Wang J.-Z., Grundke-Iqbal I., and Iqbal K. (1996) Glycosylation of microtubule-associated protein tau: an abnormal post-translational modification in Alzheimer's disease. Nat. Med. 2, 871-875.
58. Watkins N. G., Thorpe S. R., and Baynes J. W. (1985) Glycation of amino groups in proteins: studies on the specificity of modification of RNase by glucose. J. Biol. Chem. 260, 10629-10636.
59. Wille H., Drewes G., Biernat J., Mandelkow E.-M., 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.
60. 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 D. (1994) Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc. Natl. Acad. Sci. USA 91, 7787-7791.
61. Yen S.-H. and Kress Y. (1983) The effects of chemical reagents or proteases on the ultra structure of paired helical filaments, in Banbury Report, Vol. 15: Biological Aspects of Alzheimer's Disease (Katzman R., ed), pp. 155-165. Cold Spring Harbor Press, Cold Spring Harbor.