Structural insights into Alzheimer filament assembly pathways based on site-directed mutagenesis and S-glutathionylation of three-repeat neuronal Tau protein

Microscopy Research and Technique

Volumn 67, Issue 3-4, 2005, Pages 156-163

  Dinoto, Luca ^a   Deture, Michael A ^a   Purich, Daniel L ^a  

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

Author keywords

Aberrant protein polymerization; Cytoskeletal protein; Glutathione; MAP2; Microtubule associated proteins; Oxidative stress

Indexed keywords

DIMERS; NEURODEGENERATIVE DISEASES; POLYMERIZATION; SULFUR COMPOUNDS;

ABERRANT PROTEIN POLYMERIZATION; ALZHEIMER; CYTOSKELETAL PROTEINS; FILAMENT ASSEMBLY; GLUTHATHIONE; MAP2; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULES; PAIRED HELICAL FILAMENTS; STRUCTURAL INSIGHTS;

PROTEINS;

CYTOSKELETON PROTEIN; DIMER; DISULFIDE; GLUTATHIONE; MICROTUBULE ASSOCIATED PROTEIN 2; MONOMER; TAU PROTEIN;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; DISULFIDE BOND; ELECTRON MICROSCOPY; IMAGE ANALYSIS; MICROTUBULE; NEUROFIBRILLARY TANGLE; OXIDATION; OXIDATIVE STRESS; PAIRED HELICAL FILAMENT; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN POLYMERIZATION; REACTION ANALYSIS; REVIEW; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS;

EID: 24144493633     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.20195     Document Type: Review

References (65)

1. Barghorn S, Zheng-Fischhofer Q, Ackmann M, Biernat J, von Bergen M, Mandelkow EM, Mandelkow E. 2000. Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias. Biochemistry 39:11714-11721.
2. Carrell RW, Gooptu B. 1998. Conformational changes and disease-serpins, prions and Alzheimer's. Curr Opin Struct Biol 8:799-809.
3. Chau MF, Radeke MJ, de Ines C, Barasoain L, Kohlstaedt LA, Feinstein SC. 1998. The microtubule-associated protein tau cross-links to two distinct sites on each alpha and beta tubulin monomer via separate domains. Biochemistry 37:17692-17703.
4. Chirita CN, Necula M, Kuret J. 2003. Anionic micelles and vesicles induce tau fibrillization in vitro. J Biol Chem 278:25644-25650.
5. Cleland WW. 1964. Dithiothreitol, a new protective reagent for SH groups. Biochemistry 2:480-482.
6. Crowther RA. 1991. Straight and paired helical filaments in Alzheimer disease have a common structural unit. Proc Natl Acad Sci USA 88:2288-2292.
7. Crowther RA, Olesen OF, Jakes R, Goedert M. 1992. The microtubule binding repeats of tau protein assemble into filaments like those found in Alzheimer's disease. FEBS Lett 309:199-202.
8. Crowther RA, Olesen OF, Smith MJ, Jakes R, Goedert M. 1994. Assembly of Alzheimer-like filaments from full-length tau protein. FEBS Lett 337:135-138.
9. DeTure MA, Zhang EY, Bubb MR, Purich DL. 1996. In vitro polymerization of embryonic MAP-2c and fragments of the MAP-2 microtubule binding region into structures resembling paired helical filaments. J Biol Chem 271:32702-32706.
10. DeTure MA, Di Noto L, Purich DL. 2002. In vitro assembly of Alzheimer-like filaments. How a small cluster of charged residues in Tau and MAP2 controls filament morphology. J Biol Chem 277: 34755-34759.
11. DiNoto L. 2002. Biochemical investigation of Tau and MAP2 polymerization: implications for neuropathic filament assembly in Alzheimer's disease, Doctoral Dissertation, University of Florida, Gainesville, FL.
12. DiNoto L, DeTure MA, Purich DL. 2002. Disulfide-cross-linked tau and MAP2 homodimers readily promote microtubule assembly. Mol Cell Biol Res Commun 2:71-76.
13. Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E. 1997. MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89:297-308.
14. Eigen M. 1996. Prionics or the kinetic basis of prion diseases. Biophys Chem 63:A1-A18.
15. Ennulat D, Liem R, Hashim G, Shelanski ML. 1989. Two separate 18-amino acid domains of tau promote the polymerization of tubulin. J Biol Chem 264:5327-5330.
16. Friedhoff P, von Bergen M, Mandelkow E-M, Davies P, Mandelkow E. 1998a. Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution. Proc Natl Acad Sci USA 95:15712-15717.
17. Friedhoff P, Schneider A, Mandelkow EM, Mandelkow E. 1998b. A nucleated assembly mechanism of Alzheimer paired helical filaments. Biochemistry 37:10223-10230.
18. Gamblin TC, King ME, Kuret J, Berry RW, Binder LI. 2000. Oxidative regulation of fatty acid-induced tau polymerization. Biochemistry 39:14203-14210.
19. Gamblin TC, Berry RW, Binder LI. 2003. Modeling tau polymerization in vitro: a review. Biochemistry 42:15009-15017.
20. Goedert M. 2004. Tau protein and neurodegeneration. Semin Cell Dev Biol 15:45-9.
21. Goedert M, Crowther RA, Spillantini MG. 1998. Tau mutations cause frontotemporal dementias. Neuron 21:955-958.
22. Hoffmann R, Dawson NF, Wade JD, Otvos Jr L. 1997. Oxidized and phosphorylated synthetic peptides corresponding to the second and third tubulin-binding repeats of the tau protein reveal structural features of paired helical filament assembly. J Peptide Res 50:132-142.
23. Honda K, Casadesus G, Petersen RB, Perry G, Smith MA. 2004. Oxidative stress and redox-active iron in Alzheimer's disease. Ann N Y Acad Sci 1012:179-182.
24. Huang X, Atwood CS, Hartshorn MA, Multhaup G, Goldstein LE, Scarpa RC, Cuajungco MP, Gray DN, Lim J, Moir RD, Tanzi RE, Bush AI. 1999. The A beta-peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 38:7609-7616.
25. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JBJ, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P. 1998. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
26. Joly JC, Flynn G, Purich DL. 1989. The microtubule-binding fragment of microtubule-associated protein-2: location of the protease-accessible site and identification of an assembly-promoting peptide. J Cell Biol 109:2289-2294.
27. Johnson GVW, Greenwood JA. 1995. Localization and in situ phosphorylation state of nuclear tau. Neurobiol Aging 16:371-374.
28. Johnson GV, Hartigan JA. 1999. Tau protein in normal and Alzheimer's disease brain: an update. J Alzheimer's Dis 1:329-351.
29. Kampers T, Friedhoff P, Biernat J, Mandelkow EM, Mandelkow E. 1996. RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments. FEBS Lett 399:344-349.
30. Kidd M. 1963. Paired helical filaments in electron microscopy of Alzheimer's disease. Nature 197:192-193.
31. Koo EH, Lansbury PT, Kelly JW. 1999. Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc Natl Acad Sci USA 96:9989-9990.
32. Kopke E, Tung Y-C, Shaikh S, Alonso AC, Iqbal K, Grundke-Iqbal I. 1993. Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J Biol Chem 268:24374-24384.
33. Landino LM, Robinson SH, Skreslet TE, Cabral DM. 2004. Redox modulation of tau and microtubule-associated protein-2 by the glutathione/glutaredoxin reductase system. Biochem Biophys Res Commun 323:112-117.
34. Lansbury PT, Caughey B. 1995. The chemistry of scrapie infection: implications of the "ice 9" metaphor. Chem Biol 2:1-5.
35. Ledesma MD, Bonay P, Colaco C, Avila J. 1994. Analysis of microtubule-associated protein tau glycation in paired helical filaments. J Biol Chem 269:21614-21619.
36. Ledesma MD, Avila J, Correas I. 1995. Isolation of a phosphorylated soluble tau fraction from Alzheimer's disease brain. Neurobiol Aging 16:515-522.
37. Lee VM, Goedert M, Trojanowski JQ. 2001. Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
38. Lee HG, Perry G, Moreira PI, Garrett MR, Liu Q, Zhu X, Takeda A, Nunomura A, Smith MA. 2005. Tau phosphorylation in Alzheimer's disease: pathogen or protector? Trends Mol Med 11:164-169.
39. Lewis SA, Wang DH, Cowan NJ. 1988. Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science 242:936-939.
40. Makrides V, Shen TE, Bhatia R, Smith BL, Thimm J, Lal R, Feinstein SC. 2003. Microtubule-dependent oligomerization of tau: implications for physiological tau function and tauopathies. J Biol Chem 278:33298-33304.
41. Makrides V, Massie MR, Feinstein SC, Lew J. 2004. Evidence for two distinct binding sites for tau on microtubules. Proc Natl Acad Sci USA 101:6746-6751.
42. Manetto V, Perry G, Tabaton M, Mulvihill P, Fried VA, Smith HT, Gambetti P, Autilio-Gambetti L. 1988. Ubiquitin is associated with abnormal cytoplasmic filaments characteristic of neurodegenerative diseases. Proc Natl Acad Sci USA 85:4501-4505.
43. Matsuo ES, Shin RW, Billingsley ML, Van deVoorde A, O'Connor M, Trojanowski JQ, Lee VM. 1994. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13:989-1002.
44. Miller CC, Anderton BH. 1986. Transglutaminase and the neuronal cytoskeleton in Alzheimer's disease. J Neurochem 46:1912-1922.
45. Pauling L, Itano HA. 1949. Sickle cell anemia: a molecular disease. Science 110:543-548.
46. Perez M, Valpuesta JM, Medina M, Montejo de Garcini E, Avila . 1996. Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction. J Neurochem 67:1183-1190.
47. Perez M, Hernandez F, Gomez-Ramos A, Smith M, Perry G, Avila J. 2002. Formation of aberrant phosphotau fibrillar polymers in neural cultured cells. Eur J Biochem 269:1484-1489.
48. Perry G, Mulvihill P, Manetto V, Autilio-Gambetti L, Gambetti P. 1987. Immunocytochemical properties of Alzheimer straight filaments. J Neurosci 7:3736-3738.
49. Perry G, Taddeo MA, Petersen RB, Castellani RJ, Harris PL, Siedlak SL, Cash AD, Liu Q, Nunomura A, Atwood CS, Smith MA. 2003. Adventiously-bound redox active iron and copper are at the center of oxidative damage in Alzheimer disease. Biometals 16:77-81.
50. Pierre M, Nunez J. 1983. Multisite phosphorylation of tau proteins from rat brain. Biochem Biophys Res Commun 115:212-219.
51. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD. 1998. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43:815-825.
52. Prusiner SB. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216:136-144.
53. Scherzinger E, Sittler A, Schweiger K, Heiser V, Lurz R, Hasenbank R, Bates GP, Lehrach H, Wanker EE. 1999. Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc Natl Acad Sci USA 96:4604-4609.
54. Schweers O, Mandelkow EM, Biernat J, Mandelkow E. 1995. Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc Natl Acad Sci USA 92:8463-8467.
55. Singer SM, Zainelli GM, Norlund MA, Lee JM, Muma NA. 2002. Transglutaminase bonds in neurofibrillary tangles and paired helical filament tau early in Alzheimer's disease. Neurochem Int 40:17-30.
56. Smith MA, Sayre LM, Monnier VM, Perry G. 1995. Radical AGEing in Alzheimer's disease. Trends Neurosci 18:172-176.
57. Soto C. 1999. Alzheimer's and prion disease as disorders of protein conformation: implications for the design of novel therapeutic approaches. FEBS Lett 498:204-207.
58. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B. 1998. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 95:7737-7741.
59. Terry RD. 1963. The fine structure of neurofibrillary tangles in Alzheimer's disease. J Neuropathol Exp Neurol 22:629-642.
60. Thomas PJ, Qu B-H, Pedersen PL. 1995. Defective protein folding as a basis of human disease. Trends Biochem Sci 20:456-459.
61. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW. 1975. A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 72:1858-1862.
62. Wilson DM, Binder LI. 1995. Polymerization of microtubule-associated protein tau under near-physiological conditions. J Biol Chem 270:24306-24314.
63. Wilson DM, Binder LI. 1997. Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease. Am J Pathol 150:2181-2195.
64. Wischik CM, Novak M, Thogersen HC, Edwards PC, Runswick MJ, Jakes R, Walker JE, Milstein C, Roth M, Klug A. 1998. Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci USA 85:4506-4510.
65. Zhang EY, DeTure MA, Bubb MR, Caviston TL, Erdos GW, Whittaker SD, Purich DL. 1996. Self-assembly of the brain MAP-2 microtubule-binding region into polymeric structures resembling Alzheimer filaments. Biochem Biophys Res Commun 229:176-181.