Characterization of paired helical filaments by scanning transmission electron microscopy

Microscopy Research and Technique

Volumn 67, Issue 3-4, 2005, Pages 126-140

  Ksiezak Reding, Hanna ^a   Wall, Joseph S ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Alzheimer's disease; Neurofibrillary tangles; Synthetic filaments; Tau; Tauopathies

Indexed keywords

HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; NEURODEGENERATIVE DISEASES;

ALZHEIMERS DISEASE; HYPERPHOSPHORYLATED; NEURODEGENERATIVE DISORDERS; NEUROFIBRILLARY TANGLES; PAIRED HELICAL FILAMENTS; SCANNING TRANSMISSION ELECTRON MICROSCOPY; SYNTHETIC FILAMENTS; TAU; TAU PROTEINS; TAUOPATHIES;

SCANNING ELECTRON MICROSCOPY;

ARACHIDONIC ACID; DODECYL SULFATE SODIUM; DYE; NANOVAN; REAGENT; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; BIOCHEMISTRY; CORTICOBASAL DEGENERATION; DEGENERATIVE DISEASE; HUMAN; IMAGE ANALYSIS; MICROTUBULE; NEUROFIBRILLARY TANGLE; NIEMANN PICK DISEASE; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVIEW; SCANNING TRANSMISSION ELECTRON MICROSCOPY; STAINING; STRUCTURE ANALYSIS; TAUOPATHY; ULTRASTRUCTURE;

EID: 24144465828     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.20188     Document Type: Review

References (92)

1. Arai T, Guo JP, McGeer PL. 2005. Proteolysis of non-phosphorylated and phosphorylated tau by thrombin. J Biol Chem 280:5145-5153.
2. Askanas V, Engel WK. 2002. Inclusion-body myositis and myopathies: different etiologies, possibly similar pathogenic mechanisms. Review. Curr Opin Neurol 15:525-531.
3. Balbach JJ, Ishii Y, Antzutkin ON, Leapman RD, Rizzo NW, Dyda F, Reed J, Tycko R. 2000. Amyloid fibril formation by A beta 16-22, a seven-residue fragment of the Alzheimer's beta-amyloid peptide, and structural characterization by solid state NMR. Biochemistry 39:13748-13759.
4. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, Seitelberger F, Grundke-Iqbal I, Iqbal K, Wisniewski HM. 1989. Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 477:90-99.
5. Barghorn S, Mandelkow E. 2002. Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments. Biochemistry 41:14885-14896.
6. 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.
7. Barghorn S, Davies P, Mandelkow E. 2004. Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on beta-structure in the core domain. Biochemistry 43:1694-1703.
8. Baxa U, Taylor KL, Wall JS, Simon MN, Cheng N, Wickner RB, Steven AC. 2003. Architecture of Ure2p prion filaments: the N-terminal domains form a central core fiber. J Biol Chem 278:43717-43727.
9. Berriman J, Serpell LC, Oberg KA, Fink AL, Goedert M, Crowther RA. 2003. Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-beta structure. Proc Natl Acad Sci U S A 100:9034-9038.
10. Blake C, Serpell L. 1996. Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous beta-sheet helix. Structure 4:989-998.
11. Braak H, Braak E. 1991. Neuropathological staging of Alzheimer's disease-related changes. Acta Neuropathol 82:239-259.
12. Buee L, Delacourte A. 1999. Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick's disease. Review. Brain Pathol 9:681-693.
13. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. 2000. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Review. Brain Res Brain Res Rev 33:95-130.
14. Cardoso I, Goldsbury CS, Muller SA, Olivieri V, Wirtz S, Damas AM, Aebi U, Saraiva MJ. 2002. Transthyretin fibrillogenesis entails the assembly of monomers: a molecular model for in vitro assembled transthyretin amyloid-like fibrils. J Mol Biol 317:683-695.
15. Cork LC, Powers RE, Selkoe DJ, Davies P, Geyer JJ, Price DL. 1988. Neurofibrillary tangles and senile plaques in aged bears. J Neuropathol Exp Neurol 47:629-641.
16. Crowther RA. 1991. Straight and paired helical filaments in Alzheimer's disease have a common structural unit. Proc Natl Acad Sci U S A 88:2288-2292.
17. Crowther T, Goedert M, Wischik CM. 1989. The repeat region of microtubule-associated protein tau forms part of the core of the paired helical filament of Alzheimer's disease. Review. Ann Med 21:127-132.
18. 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.
19. Dickson DW, Ksiezak-Reding H, Liu W-K, Davies P, Crowe A, Yen S-HC. 1992. 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 84:596-605.
20. Drewes G. 2004. MARKing tau for tangles and toxicity. Review. Trends Biochem Sci 29:548-555.
21. Drewes G, Lichtenberg-Kraag B, Doring F, Mandelkow EM, Biernat J, Goris J, Doree M, Mandelkow E. 1992. Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J 11:2131-2138.
22. Ducruix A, Giege R. 1992. Crystallization of nucleic acids and proteins. A practical approach. New York: IRL Press, Oxford University Press, p 82-89.
23. Friedhoff P, von Bergen M, Mandelkow EM, Davies P, Mandelkow E. 1998. A nucleated assembly mechanism of Alzheimer paired helical filaments. Proc Natl Acad Sci U S A 95:15712-15717.
24. Giannetti AM, Lindwall G, Chau MF, Radeke MJ, Feinstein SC, Kohlstaedt LA. 2000. Fibers of tau fragments, but not full length tau, exhibit a cross beta-structure: implications for the formation of paired helical filaments. Protein Sci 9:2427-2435.
25. Glenner GG, Wong CW. 1984. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
26. Goedert M, Jakes R. 2005. Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 1739:240-250.
27. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. 1989a. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3:519-526.
28. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA. 1989b. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J 8:393-399.
29. Goedert M, Spillantini MG, Cairns NJ, Crowther RA. 1992. Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8:159-168.
30. Goedert M, Jakes R, Spillantini MG, Hasegawa M, Smith MJ, Crowther RA. 1996a. Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383:550-553.
31. Goedert M, Spillantini MG, Hasegawa M, Jakes R, Crowther RA, Klug A. 1996b. Molecular dissection of the neurofibrillary lesions of Alzheimer's disease. Review. Cold Spring Harbor Symp Quant Biol 61:565-573.
32. Gomez-Ramos A, Smith MA, Perry G, Avila J. 2004. Tau phosphorylation and assembly. Review. Acta Neurobiol Exp (Wars) 64: 33-39.
33. Gordon-Krajcer W, Yang L-S, Ksiezak-Reding H. 2000. Conformation of paired helical filaments blocks dephosphorylation of epitopes shared with fetal tau except Ser 199/202 and Ser202/Thr205. Brain Res 856:163-175.
34. Goux WJ. 2002. The conformations of filamentous and soluble tau associated with Alzheimer paired helical filaments. Biochemistry 41:13798-13806.
35. Goux WJ, Kopplin L, Nguyen AD, Leak K, Rutkofsky M, Shanmuganandam VD, Sharma D, Inouye H, Kirschner DA. 2004. The formation of straight and twisted filaments from short tau peptides. J Biol Chem 279:26868-26875.
36. Greenberg SG, Davies P. 1990. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci U S A 87:5827-5831.
37. Hagestedt B, Lichtenberg B, Wille H, Mandelkow EM, Mandelkow E. 1989. Tau protein becomes long and stiff upon phosphorylation: correlation between paracrystalline structure and degree of phosphorylation. J Cell Biol 109:1643-1651.
38. Hasegawa M, Crowther RA, Jakes R, Goedert M. 1997. Alzheimer-like changes in microtubule-associated protein tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation, - and filament assembly depend on the degree of sulfation. J Biol Chem 272:33118-33124.
39. Ikonomovic MD, Armstrong DM, Yen SH, Obcemea C, Vidic B. 1995. Atomic force microscopy of paired helical filaments isolated from the autopsied brains of patients with Alzheimer's disease and immunolabeled against microtubule-associated protein tau. Am J Pathol 147:516-528.
40. Iqbal K, Zaidi T, Thompson CH, Merz PA, Wisniewski HM. 1984. Alzheimer paired helical filaments: bulk isolation, solubility, and protein composition. Acta Neuropathol (Berl) 62:167-177.
41. Kajava AV, Baxa U, Wickner RB, Steven AC. 2004. A model for Ure2p prion filaments and other amyloids: the parallel superpleated beta-structure. Proc Natl Acad Sci U S A 101:7885-7890.
42. 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.
43. Kidd M. 1963. Paired helical filaments in electron microscopy of Alzheimer's disease. Nature 197:192-193.
44. King ME, Ahuja V, Binder LI, Kuret J. 1999. Ligand-dependent tau filament formation: implications for Alzheimer's disease progression. Biochemistry 38:14851-1489.
45. King ME, Gamblin TC, Kuret J, Binder LI. 2000. Differential assembly of human tau isoforms in the presence of arachidonic acid. J Neurochem 74:1749-1757.
46. King ME, Ghoshal N, Wall JS, Binder LI, Ksiezak-Reding H. 2001. Structural analysis of Pick's disease-derived and in vitro-assembled tau filaments. Am J Pathol 158:1481-1490.
47. Kirschner DA, Abraham C, Selkoe DJ. 1986. X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation. Proc Natl Acad Sci U S A 83:503-507.
48. Kondo J, Honda T, Mori H, Hamada Y, Miura R, Ogawara M, Ihara Y 1988. The carboxyl third of tau is tightly bound to paired helical filaments. Neuron 1:827-834.
49. Ksiezak-Reding H, Wall JS. 1994. Mass and physical dimensions differ in two distinct populations of paired helical filaments. Neurobiol Aging 15:11-19.
50. Ksiezak-Reding H, Yen S-H. 1991. Structural stability of paired helical filaments requires microtubule-binding domains of tau: a model for self-association. Neuron 6:717-728.
51. Ksiezak-Reding H, Binder LI, Yen S-H. 1990. Alzheimer disease proteins (A68) share epitopes with tau but show distinct biochemical properties. J Neurosci Res 25:420-430.
52. Ksiezak-Reding H, Morgan K, Dickson DW. 1994. Tau immunoreactivity and SDS solubility of two populations of paired helical filaments that differ in morphology. Brain Res 649:185-196.
53. Ksiezak-Reding H, Tracz E, Yang LS, Dickson DW, Simon M, Wall JS. 1996. Ultrastructural instability of paired helical filaments from corticobasal degeneration as examined by scanning transmission electron microscopy. Am J Pathol 149:639-651.
54. Ksiezak-Reding H, Yang G, Simon M, Wall JS. 1998. Assembled tau filaments differ from native paired helical filaments as determined by scanning transmission electron microscopy (STEM). Brain Res 814:86-98.
55. Lashuel HA, Petre BM, Wall J, Simon M, Nowak RJ, Walz T, Lansbury Jr PT. 2002. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J Mol Biol 322:1089-1102.
56. Lashuel HA, Hartley DM, Petre BM, Wall JS, Simon MN, Walz T, Lansbury Jr PT. 2003. Mixtures of wild-type and a pathogenic (E22G) form of Abeta40 in vitro accumulate protofibrils, including amyloid pores. J Mol Biol 332:795-808.
57. Lee VM, Balin BJ, Otvos L Jr, Trojanowski JQ. 1991. A68: a major subunit of paired helical filaments and derivatized forms of normal tau. Science 251:675-678.
58. Lee VM, Goedert M, Trojanowski JQ. 2001. Neurodegenerative tauopathies. Review. Annu Rev Neurosci 24:1121-1159.
59. Lindwall G, Cole RD. 1984. The purification of tau protein and the occurrence of two phosphorylation states of tau in brain. J Biol Chem 259:12241-12245.
60. Margittai M, Langen R. 2004. Template-assisted filament growth by parallel stacking of tau. Proc Natl Acad Sci U S A 101:10278-10283.
61. Maurage CA, Bussiere T, Sergeant N, Ghesteem A, Figarella-Branger D, Ruchoux MM, Pellissier JF, Delacourte A. 2004. Tau aggregates are abnormally phosphorylated in inclusion body myositis and have an immunoelectrophoretic profile distinct from other tauopathies. Neuropathol Appl Neurobiol 30:624-634.
62. Mercken M, Grynspan F, Nixon RA. 1995. Differential sensitivity to proteolysis by brain calpain of adult human tau, fetal human tau and PHF-tau. FEBS Lett 368:10-14.
63. Perez M, Valpuesta JM, Medina M, Montejo de Garcini E, Avila J. 1996. Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction. J Neurochem 67:1183-1190.
64. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R. 2005. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307:262-265.
65. Pollanen MS, Markiewicz P, Bergeron C, Goh MC. 1994. Twisted ribbon structure of paired helical filaments revealed by atomic force microscopy. Am J Pathol 144:869-873.
66. Rissman RA, Poon WW, Blurton-Jones M, Oddo S, Torp R, Vitek MP, LaFerla FM, Rohn TT, Cotman CW. 2004. Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J Clin Invest 114:121-130.
67. Ruben GC, Novak M, Edwards PC, Iqbal K. 1995. Alzheimer paired helical filaments, untreated and pronase digested, studied by vertical platinum-carbon replication and high resolution transmission electron microscopy. Brain Res 675:1-12.
68. Sadqi M, Hernandez F, Pan U, Perez M, Schaeberle MD, Avila J, Munoz V. 2002. Alpha-helix structure in Alzheimer's disease aggregates of tau-protein. Biochemistry 41:7150-7155.
69. Safar J, Wille H, Itri V, Groth D, Serban H, Torchia M, Cohen FE, Prusiner SB. 1998. Eight prion strains have PrP(Sc) molecules with different conformations. Nat Med 4:1157-1165.
70. Schneider A, Biernat J, von Bergen M, Mandelkow E, Mandelkow EM. 1999. Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 38:3549-3558.
71. Schultz C, Dehghani F, Hubbard GB, Thal DR, Struckhoff G, Braak E, Braak H. 2000. Filamentous tau pathology in nerve cells, astrocytes, and oligodendrocytes of aged baboons. J Neuropathol Exp Neurol 59:39-52.
72. Schweers O, Schonbrunn-Hanebeck E, Marx A, Mandelkow E. 1994. Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for β-structure. J Biol Chem 269:24290-24297.
73. 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 U S A 92:8463-8467.
74. Seitz A, Kojima H, Oiwa K, Mandelkow EM, Song YH, Mandelkow E. 2002. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 21:4896-4905.
75. Selkoe DJ, Ihara Y, Salazar FJ. 1982. Alzheimer's disease: insolubility of partially purified paired helical filaments in sodium dodecyl sulfate and urea. Science 215:1243-1245.
76. Spillantini MG, Goedert M, Crowther RA, Murrell JR, Farlow MR, Ghetti B. 1997. Familial multiple system tauopathy with presenile dementia: a disease with abundant neuronal and glial tau filaments. Proc Natl Acad Sci U S A 94:4113-4118.
77. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS. 2004. Conformational variations in an infectious protein determine prion strain differences. Nature 428:323-328.
78. Tracz E, Dickson DW, Hainfeld JF, Ksiezak-Reding H. 1997. Paired helical filaments in corticobasal degeneration: the fine fibrillary structure with NanoVan. Brain Res 773:33-44.
79. Vincent I, Zheng JH, Dickson DW, Kress Y, Davies P. 1998. Mitotic phosphoepitopes precede paired helical filaments in Alzheimer's disease. Neurobiol Aging 19:287-296.
80. von Bergen M, Friedhoff P, Biernat J, Heberle J, Mandelkow EM, Mandelkow E. 2000. Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif ((306)VQI-VYK(311)) forming beta structure. Proc Natl Acad Sci U S A 97:5129-5134.
81. von Bergen M, Barghorn S, Biernat J, Mandelkow EM, Mandelkow E. 2005. Tau aggregation is driven by a transition from random coil to beta sheet structure. Biochim Biophys Acta 1739:158-166.
82. Wakabayashi K, Oyanagi K, Makifuchi T, Ikuta F, Homma A, Homma Y, Horikawa Y, Tokiguchi S. 1994. Corticobasal degeneration: etiopathological significance of the cytoskeletal alterations. Acta Neuropathol (Berl) 87:545-553.
83. West MW, Wang W, Patterson J, Mancias JD, Beasley JR, Hecht MH. 1999. De novo amyloid proteins from designed combinatorial libraries. Proc Natl Acad Sci U S A 96:11211-11216.
84. Wille DM, Drewes G, Biernat J, Mandelkow EM, 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.
85. Wilson DM, Binder L. 1997. Free fatty acids stimulate the polymerization of tau and amyloid β peptides: in vitro evidence for a common effector of pathogenesis in Alzheimer's disease. Am J Pathol 150:2181-2195.
86. Wischik CM, Crowther RA, Stewart M, Roth M. 1985. Subunit structure of paired helical filaments in Alzheimer's disease. J Cell Biol 100:1905-1912.
87. Wischik CM, Novak M, Thogersen HC, Edwards PC, Runswick MJ, Jakes R, Walker JE, Milstein C, Roth M, Klug A. 1988a. Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci U S A 85:4506-4510.
88. Wischik CM, Novak M, Edwards PC, Klug A, Tichelaar W, Crowther RA. 1988b. Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci U S A 85:4884-4888.
89. Yang L-S, Ksiezak-Reding H. 1995. Calpain-induced proteolysis of normal human tau and tau associated with paired helical filaments. Eur J Biochem 233:9-17.
90. Yang L-S, Ksiezak-Reding H. 1998. Ubiquitin immunoreactivity of paired helical filaments differs in Alzheimer's disease and cortico-basal degeneration. Acta Neuropathol 96:520-526.
91. Yang L-S, Gordon-Krajcer W, Ksiezak-Reding H. 1997. Tau released from paired helical filaments with formic acid or guanidine is susceptible to calpain-mediated proteolysis. J Neurochem 69:1548-1558.
92. Yen S-H, Kress Y. 1983. The effect of chemical reagents or the proteases on the ultrastructure of paired helical filaments. In: Katzman R, editor. Banbury report 15: biological aspects of Alzheimer's disease. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, p 155-165.