O-GlcNAcylation modulates the self-aggregation ability of the fourth microtubule-binding repeat of tau

Biochemical and Biophysical Research Communications

Volumn 375, Issue 1, 2008, Pages 59-62

  Yu, Chun Hui ^a,b   Si, Tong ^a   Wu, Wei Hui ^a   Hu, Jia ^a   Du, Jin Tang ^a   Zhao, Yu Fen ^a   Li, Yan Mei ^a  

^a Tsinghua University   (China)

^b BEIHUA UNIVERSITY   (China)

Author keywords

Aggregation; Alzheimer's disease; Microtubule binding repeat; O GlcNAcylation; Tau

Indexed keywords

TAU PROTEIN;

ACYLATION; ARTICLE; CIRCULAR DICHROISM; HUMAN; MICROTUBULE; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; TURBIDITY;

ACETYLGLUCOSAMINE; ACYLATION; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; HUMANS; MICROTUBULES; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN CONFORMATION; REPETITIVE SEQUENCES, AMINO ACID; SERINE; TAU PROTEINS;

EID: 50949099668     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2008.07.101     Document Type: Article

References (33)

1. Mandelkow E. Alzheimer's disease-the tangled tale of tau. Nature 402 (1999) 588-589
2. Kopke Y.C.T.E., Shaikh S., Alonso A.C., Iqbal K., and Grundke-Iqbal I. Microtubule associated protein tau: abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J. Biol. Chem. 268 (1993) 24374-24384
3. 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
4. Grundke-Iqbal I., Iqbal K., Tung Y.C., Quinlan M., Wisniewski H.M., Binder L.I., et al. Abnormal phosphorylation of the microtubule-associated protein τ (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83 (1986) 49130-49170
5. Gong C.X., Liu F., Grundke-Iqbal I., and Iqbal K. Post-translational modifications of tau protein in Alzheimer's disease. J. Neural Transm. 112 (2005) 813-838
6. Lee G., Cowan N., and Kirschner M. The primary structure and heterogeneity of tau protein from mouse brain. Science 239 (1988) 285-288
7. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., and Hof P.R. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Rev. 33 (2000) 95-130
8. Friedhoff P., von Bergen M., Mandelkow E.M., and Mandelkow E. Structure of tau protein and assembly into paired helical filaments. Biochim. Biophys. Acta 1502 (2000) 122-132
9. Friedhoff P., von Bergen M., Mandelkow E.M., Davies P., and Mandelkow E. A nucleated assembly mechanism of Alzheimer paired helical filaments. Proc. Natl. Acad. Sci. USA 95 (1998) 15712-15717
10. Wille H., Drewes G., Biernat J., Mandelkow E.-M., and Mandelkow E. Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro. J. Cell Biol. 118 (1992) 573-584
11. Hiraoka S., Yao T.M., Minoura K., Tomoo K., Sumida M., Taniguchi T., and Ishida T. Conformational transition state is responsible for assembly of microtubule-binding domain of tau protein. Biochem. Biophys. Res. Commun. 315 (2004) 659-663
12. Minoura K., Yao T.M., Tomoo K., Sumida M., Sasaki M., Taniguchi T., and Ishida T. Different associational and conformational behaviors between the second and third repeat fragments in the tau microtubule-binding domain. Eur. J. Biochem. 271 (2004) 545-552
13. Liu F., Iqbal K., Grundke-Iqbal I., Hart G.W., and Gong C.X. O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 101 (2004) 10804-10809
14. Wells L., Vosseller K., and Hart G.W. Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc. Science 291 (2001) 2376-2378
15. Wu W.G., Pasternack L., Huang D.H., Koeller K.M., Lin C.C., Seitz O., and Wong C.H. Structural study on O-glycopeptides: glycosylation-induced conformational changes of O-GlcNAc, O-LacNAc, O-sialyl-LacNAc, and O-sialyl-lewis-X peptides of the mucin domain of MAdCAM-1. J. Am. Chem. Soc. 121 (1999) 2409-2417
16. Simanek E.E., Huang D.H., Pasternack L., Machajewski T.D., Seitz O., Millar D.S., Dyson H.J., and Wong C.H. Glycosylation of threonine of the repeating unit of RNA polymerase II with beta-linked N-acetylglucosame leads to a turnlike structure. J. Am. Chem. Soc. 120 (1998) 11567-11575
17. Du J.T., Li Y.M., Ma Q.F., Qiang W., Zhao Y.F., Abe H., Kanazawa K., Qin X.R., Aoyagi R., Ishizuka Y., Nemoto T., and Nakanishi H. Synthesis and conformational properties of phosphopeptides related to the human tau protein. Regul. Pept. 130 (2005) 48-56
18. Zhou L.X., Zeng Z.Y., Du J.T., Zhao Y.F., and Li Y.M. The self-assembly ability of the first microtubule-binding repeat from tau and its modulation by phosphorylation. Biochem. Biophys. Res. Commun. 348 (2006) 637-642
19. Du J.T., Yu C.H., Zhou L.X., Wu W.H., Lei P., Li Y., Zhao Y.F., Nakanishi H., and Li Y.M. Phosphorylation modulates the local conformation and self-aggregation ability of a peptide from the fourth tau microtubule-binding repeat. FEBS J. 274 (2007) 5012-5020
20. Alonso A.D., Zaidi T., Novak M., Grundke-Iqbal I., and Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. USA 98 (2001) 6923-6928
21. Haase C., Stieler J.T., Arendt T., and Holzer M. Pseudophosphorylation of tau protein alters its ability for self-aggregation. J. Neurochem. 88 (2004) 1509-1520
22. Bancher C., Brunner C., Lassmann H., Budka H., Jellinger K., Wiche G., Seitelberger F., Grundke-Iqbal I., and Wisniewski H.M. Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res. 856 (2000) 163-175
23. Gordon-Krajcer W., Yang L.S., and Ksiezak-Reding H. Conformation of paired helical filaments blocks dephosphorylation of epitopes shared with fetal tau except Ser199/202 and Ser202/Thr205. Brain Res. 856 (2000) 163-175
24. Litersky J.M., Johnson G.V.W., Jakes R., Goedert M., Lee M., and Seubert P. Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356. Biochem. J. 316 (1996) 655-660
25. Fields G.B., and Noble R.L. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 35 (1990) 161-214
26. Muhlradt P.F., Kiess M., Meyer H., Sussmuth R., and Jung G. Isolation structure elucidation and synthesis of a macrophage stimulatory lipopeptide from Mycoplasma fermentans acting at picomolar concentration. J. Exp. Med. 185 (1997) 1951-1958
27. Yi H.Q., Gruszczynska-Biegala J., Wood D., Zhao Z.F., and Zolkiewska A. Cooperation of the metalloprotease disintegrin and cysteine-rich domains of ADAM12 during inhibition of myogenic differentiation. J. Biol. Chem. 280 (2005) 23475-23483
28. Scaramozzino F., Peterson D.W., Farmer P., Gerig J.T., Graves D.J., and Lew J. TMAO promotes fibrillization and microtubule assembly activity in the C-terminal repeat region of tau. Biochemistry 45 (2006) 3684-3691
29. Barghorn S., and Mandelkow E. Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments. Biochemistry 41 (2002) 14885-14896
30. Chiba T., Hagihara Y., Higurashi T., Hasegawa K., Naiki H., and Goto Y. Amyloid fibril formation in the context of full-length protein. J. Biol. Chem. 47 (2003) 47016-47024
31. Hart G.W., Housley M.P., and Slawson C. Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446 (2007) 1017-1022
32. Dias W.B., and Hart G.W. O-GlcNAc modification in diabetes and Alzheimer's disease. Mol. Biosyst. 3 (2007) 766-772
33. Liang F.C., Chen R.P.Y., Lin C.C., Huang K.T., and Chan S.I. Tuning the conformation properties of a peptide by glycosylation and phosphorylation. Biochem. Biophys. Res. Commun. 342 (2006) 482-488