Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease

Experimental Neurology

Volumn 177, Issue 2, 2002, Pages 475-493

  Ghoshal, Nupur ^a   García Sierra, Francisco ^a   Wuu, Joanne ^b   Leurgans, Sue ^b   Bennett, David A ^b,c   Berry, Robert W ^a   Binder, Lester I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Antibody; Conformation; Episodic memory; Epitope; Tau

Indexed keywords

EPITOPE; MONOCLONAL ANTIBODY; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN INJURY; BRAIN REGION; CLINICAL ARTICLE; CLINICAL TRIAL; COGNITIVE DEFECT; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HUMAN; MALE; MEMORY DISORDER; MOLECULAR BIOLOGY; NEURITIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

EID: 0036434880     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.2002.8014     Document Type: Article

References (82)

1. Abraha, A., N. Ghoshal, T. C. Gamblin, V. Cryns, R. W. Berry, J. Kuret, and L. I. Binder. 2000. C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J. Cell Sci. 113: 3737-3745.
2. Anonymous. 1997. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol. Aging 18: S1-2.
3. Arnold, S. E., B. T. Hyman, J. Flory, A. R. Damasio, and G. W. Van Hoesen. 1991. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb. Cortex 1: 103-116.
4. Arriagada, P. V., J. H. Growdon, E. T. Hedley-Whyte, and B. T. Hyman. 1992. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42: 631-639.
5. Augustinack, J. C., A. Schneider, E. M. Mandelkow, and B. T. Hy-man, 2002. Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. (Berlin) 103: 26-35.
6. Beckett, L. A., R. S. Wilson, D. A. Bennett, and M. C. Morris. 1997. Around the WORLD backward: An algorithm for scoring the MMSE WORLD item. Neurology 48: 1733-1734.
7. Bennett, D. A., K. M. Shannon, L. A. Beckett, C. G. Goetz, and R. S. Wilson. 1997. Metric properties of nurses' ratings of parkinsonian signs with a modified Unified Parkinson's Disease Rating Scale. Neurology 49: 1580-1587.
8. Bennett, D. A., K. M. Shannon, L. A. Beckett, and R. S. Wilson. 1999. Dimensionality of parkinsonian signs in aging and Alzheimer's disease. J. Gerontol. A Biol. Sci. Med. Sci. 54: M191-196.
9. Bierer, L. M., P. R. Hof, D. P. Purohit, L. Carlin, J. Schmeidler, K. L. Davis, and D. P. Perl. 1995. Neocortical neurofibrillary tangles correlate with dementia severity in Alzheimer's disease. Arch. Neurol. 52: 81-88.
10. Bondareff, W., C. Harrington, C. M. Wischik, D. L. Hauser, and M. Roth. 1994. Immunohistochemical staging of neurofibrillary degeneration in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 53: 158-164.
11. Bondareff, W., C. M. Wischik, M. Novak, and M. Roth. 1991. Sequestration of tau by granulovacuolar degeneration in Alzheimer's disease. Am. J. Pathol. 139: 641-647.
12. Braak, E., H. Braak, and E. M. Mandelkow. 1994. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. 87: 554-567.
13. Braak, H., and E. Braak. 1991. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82: 239-259.
14. Braak, H., and E. Braak. 1997. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging 18: 351-357.
15. Bruce, C. V., J. Clinton, S. M. Gentleman, G. W. Roberts, and M. C. Royston. 1992. Quantifying the pattern of beta/A4 amyloid protein distribution in Alzheimer's disease by image analysis. Neuropathol. Appl. Neurobiol. 18: 125-136.
16. Buee-Scherrer, V., O. Condamines, C. Mourton-Gilles, R. Jakes, M. Goedert, B. Pau, and A. Delacourte. 1996. AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Brain Res. Mol. Brain Res. 39: 79-88.
17. Cairns, N. J., A. Chadwick, P. J. Luthert, and P. L. Lantos. 1991. Beta-amyloid protein load is relatively uniform throughout neo-cortex and hippocampus in elderly Alzheimer's disease patients. Neurosci. Lett. 129: 115-118.
18. Carmel, G., E. M. Mager, L. I. Binder, and J. Kuret. 1996. The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J. Biol. Chem. 271: 32789-32795.
19. Chu, Y., E. J. Cochran, D. A. Bennett, E. J. Mufson, and J. H. Kordower. 2001. Down-regulation of trkA mRNA within nucleus basalis neurons in individuals with mild cognitive impairment and Alzheimer's disease. J. Comp. Neurol. 437: 296-307.
20. Condamines, O., V., L Buee-Scherrer, A. Boissier, A. Wattez, A. Delacourte, B. Pau, and C. Mourton-Gilles. 1995. New immunoassay for the mapping of neurofibrillary degeneration in Alzheimer's disease using two monoclonal antibodies against human paired helical filament tau proteins. Neurosci. Lett. 192: 81-84.
21. Cummings, B. J., and C. W. Cotman. 1995. Image analysis of beta-amyloid load in Alzheimer's disease and relation to dementia severity. Lancet 346: 1524-1528.
22. Cummings, B. J., C. J., Pike, R. Shankle, and C. W. Cotman. 1996. Beta-amyloid deposition and other measures of neuropathology predict cognitive status in Alzheimer's disease. Neurobiol. Aging 17: 921-933.
23. Defigueiredo, R. J., B. J., Cummings, P. Y., Mundkur, and C. W. Cotman. 1995. Color image analysis in neuroanatomical research: Application to senile plaque subtype quantification in Alzheimer's disease. Neurobiol. Aging 16: 211-223.
24. Delacourte, A., J. P. David, N. Sergeant, L. Buee, A. Wattez, P. Vermersch, F. Ghozali, C. Fallet-Bianco, F. Pasquier, F. Lebert, H. Petit, and C. Di Menza. 1999. The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology 52: 1158-1165.
25. Dickson, D. W., H., Ksiezak-Reding, W. K., Liu, P. Davies, A. Crowe, and S. H. Yen. 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.
26. Duvernoy, H. 1988. The Human Hippocampus: An Atlas of Applied Anatomy. Springer-Verlag, New York.
27. Endoh, R., M. Ogawara, T. Iwatsubo, I. Nakano, and H. Mori. 1993. Lack of the carboxyl terminal sequence of tau in ghost tangles of Alzheimer's disease. Brain Res. 601: 164-172.
28. Fewster, P., S. Griffin-Brooks, J. MacGregor, E. Ojalvo-Rose, and M. Ball. 1991. A topographical pathway by which histopathological lesions disseminate through the brain of patients with Alzheimer's disease. Dementia 2: 121-132.
29. Folstein, M. F., S. E. Folstein, and P. R. McHugh. 1975. "Mini-Mental State": A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12: 189-198.
30. Garcia-Sierra, F., J. J. Hauw, C. Duyckaerts, C. M. Wischik, J. Luna-Munoz, and R. Mena. 2000. The extent of neurofibrillary pathology in perforant pathway neurons is the key determinant of dementia in the very old. Acta Neuropathol. (Berlin) 100: 29-35.
31. Garcia-Sierra, F., C. M. Wischik, C. R. Harrington, J. Luna-Munoz, and R. Mena. 2001. Accumulation of C-terminally truncated tau protein associated with vulnerability of the perforant pathway in early stages of neurofibrillary pathology in Alzheimer's disease. J. Chem. Neuroanat. 22: 65-77.
32. Ghoshal, N., F. Garćia-Sierra, Y. Fu, L. A. Beckett, E. J. Mufson, J. Kuret, R. W. Berry, and L. I. Binder. 2001. Tau-66: Evidence for a novel tau conformation in Alzheimer's disease. J. Neurochem. 77: 1372-1385.
33. Ghoshal, N., J. F. Smiley, A. J. DeMaggio, M. F. Hoekstra, E. J. Cochran, L. I. Binder, and J. Kuret. 1999. A new molecular link between the fibrillar and granulovacuolar lesions of Alzheimer's disease. Am. J. Pathol. 155: 1163-1172.
34. Giasson, B. I., R. Jakes, M. Goedert, J. E. Duda, S. Leight, J. Q. Trojanowski, and V. M. Lee. 2000. A panel of epitope-specific antibodies detects protein domains distributed throughout human alpha-synuclein in Lewy bodies of Parkinson's disease. J. Neurosci. Res. 59: 528-533.
35. Gordon-Krajcer, W., L. Yang, and H. Ksiezak-Reding. 2000. Conformation of paired helical filaments blocks dephosphorylation of epitopes shared with fetal tau except Ser199/202 and Ser202/ Thr205. Brain Res. 856: 163-175.
36. Grundke-Iqbal, I., K. Iqbal, M. Quinlan, Y. C. Tung, M. S. Zaidi, and H. M. Wisniewski. 1986a. Microtubule-associated protein tau: A component of Alzheimer paired helical filaments. J. Biol. Chem. 261: 6084-6089.
37. Grundke-Iqbal, I., K. Iqbal, Y. C. Tung, M. Quinlan, H. M. Wisniewski, and L. I. Binder. 1986b. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83: 4913-4917.
38. Hensley, K., N. Hall, R. Subramaniam, P. Cole, M. Harris, M. Aksenov, M. Aksenova, S. P. Gabbita, J. F. Wu, J. M. Carney, et al. 1995. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J. Neurochem. 65: 2146-2156.
39. Hori, A., R. Weiss, and T. Schaake. 1988. Ganglioglioma containing osseous tissue and neurofibrillary tangles. Arch. Pathol. Lab. Med. 112: 653-655.
40. Hyman, B. T., G. W. Van Hoesen, A. R. Damasio, and C. L. Barnes. 1984. Alzheimer's disease: Cell-specific pathology isolates the hippocampal formation. Science 225: 1168-1170.
41. Ishizawa, K., and D. W. Dickson. 2001. Microglial activation parallels system degeneration in progressive supranuclear palsy and corticobasal degeneration. J. Neuropathol. Exp. Neurol. 60: 647-657.
42. Janota, I. 1974. Neurofibrillary tangles, granulovacuolar degeneration and argentophilic bodies in a third ventricle tumour. Acta Neuropathol. 29: 367-369.
43. Johnson, G. V. W., and J. A. Hartigan, 1998. Tau protein in normal and Alzheimer's disease brain: An update. Alzheimer's Dis. Rev. 3: 125-141.
44. King, M. E., N. Ghoshal, J. S. Wall, L. I. Binder, and H. Ksiezak-Reding, 2001. Structural analysis of Pick's disease-derived and in vitro assembled tau filaments. Am. J. Pathol. 158: 1481-1490.
45. Kordower, J. H., Y. Chu, G. T. Stebbins, S. T. DeKosky, E. J. Cochran, D. Bennett, and E. J. Mufson. 2001. Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Ann. Neurol. 49: 202-213.
46. Kosik, K. S., L. D. Orecchio, L. Binder, J. Q. Trojanowski, V. M. Lee, and G. Lee. 1988. Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1: 817-825.
47. Kudo, M. 1986. Hypothalamic gangliocytoma. Selective appearance of neurofibrillary changes, granulovacuolar degeneration, and argentophilic bodies. Acta Pathol. Jpn. 36: 1225-1229.
48. Kuret, J., G. S. Johnson, D. Cha, E. R. Christenson, A. J. DeMaggio, and M. F. Hoekstra. 1997. Casein kinase 1 is tightly associated with paired-helical filaments isolated from Alzheimer's disease brain. J. Neurochem. 69: 2506-2515.
49. Lee, V. M., M. Goedert, and J. Q. Trojanowski. 2001. Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24: 1121-1159.
50. Lewis, J., D. W. Dickson, W. L. Lin, L. Chisholm, A. Corral, G. Jones, S. H. Yen, N. Sahara, L. Skipper, D. Yager, C. Eckman, J. Hardy, M. Hutton, and E. McGowan. 2001. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293: 1487-1491.
51. LoPresti, P., S. Szuchet, S. C. Papasozomenos, R. P. Zinkowski, and L. I. Binder. 1995. Functional implications for the microtubule-associated protein tau: Localization in oligodendrocytes. Proc. Natl. Acad. Sci. USA 92: 10369-10373.
52. Markesbery, W. R., H. Z. Wang, N. W. Kowall, K. S. Kosik, and A. C. McKee. 1993. Morphometric image analysis of neuropil threads in Alzheimer's disease. Neurobiol. Aging 14: 303-307.
53. McKenzie, J. E., G. W. Roberts, and M. C. Royston. 1996. Quantifi-cation of Alzheimer-type neurofibrillary lesions by automated image analysis. Neurodegeneration 5: 251-258.
54. McKhann, G., D. Drachman, M. Folstein, R. Katzman, D. Price, and E. M. Stadlan. 1984. Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34: 939-944.
55. Mena, R., Y., Robitaille, and A. C. Cuello, 1992. New patterns of intraneuronal accumulation of the microtubular binding domain of tau in granulovacuolar degeneration. J. Geriatr. Psychiatry Neurol. 5: 132-141.
56. Mitchell, T. W., E. J. Mufson, J. A. Schneider, E. J. Cochran, J. Nissanov, L. Y. Han, J. L. Bienias, V. M. Lee, J. Q. Trojanowski, D. A. Bennett, and S. E. Arnold. 2002. Parahippocampal tau pathology in healthy aging, mild cognitive impairment, and early Alzheimer's disease. Ann. Neurol. 51: 182-189.
57. Mufson, E. J., E. Y. Chen, E. J. Cochran, L. A. Beckett, D. A. Bennett, and J. H. Kordower. 1999. Entorhinal cortex beta-amyloid load in individuals with mild cognitive impairment. Exp. Neurol. 158: 469-490.
58. Mukaetova-Ladinska, E. B., C. R. Harrington, M. Roth, and C. M. Wischik, 1993. Biochemical and anatomical redistribution of tau protein in Alzheimer's disease. Am. J. Pathol. 143: 565-578.
59. Novak, M., J. Kabat, and C. M. Wischik. 1993. Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament. EMBO J. 12: 365-370.
60. Oberc-Greenwood, M. A., P. E. McKeever, P. L. Kornblith, and B. H. Smith. 1984. A human ganglioglioma containing paired helical filaments. Hum. Pathol. 15: 834-838.
61. Perry, G., M. Kawai, M. Tabaton, M. Onorato, P. Mulvihill, P. Richey, A. Morandi, J. A. Connolly, and P. Gambetti. 1991. Neuropil threads of Alzheimer's disease show a marked alteration of the normal cytoskeleton. J. Neurosci. 11: 1748-1755.
62. Price, J. L., A. I. Ko, M. J. Wade, S. K. Tsou, D. W. McKeel, and J. C. Morris. 2001. Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch. Neurol. 58: 1395-1402.
63. Price, J. L., and J. C. Morris. 1999. Tangles and plaques in nondemented aging and "preclinical", Alzheimer's disease. Ann. Neurol. 45: 358-368.
64. Schmidt, M. L., V. Zhukareva, K. L. Newell, V. M.-Y. Lee, and J. Q. Trojanowski. 2001. Tau isoform profile and phosphorylation state in dementia pugilistica recapitulate Alzheimer's disease. Acta Neuropathol. 101: 518-524.
65. Schwab, C., A. J. DeMaggio, N. Ghoshal, L. I. Binder, J. Kuret, and P. L. McGeer. 2000. Casein kinase 1 delta is associated with pathological accumulation of tau in several neurodegenerative diseases. Neurobiol. Aging 21: 503-510.
66. Shukla, C., and L. R. Bridges. 1999. Regional distribution of tau, beta-amyloid and beta-amyloid precursor protein in the Alzheimer's brain: A quantitative immunolabelling study. NeuroReport 10: 3785-3789.
67. Shukla, C., and L. R. Bridges. 2001. Tau, beta-amyloid and beta-amyloid precursor protein distribution in the entorhinal-hippocampal alvear and perforant pathways in the Alzheimer's brain. Neurosci. Lett. 303: 193-197.
68. Singh, T. J., I. Grundke-Iqbal, and K. Iqbal. 1995. Phosphorylation of tau protein by casein kinase-1 converts it to an abnormal Alzheimer-like state. J. Neurochem. 64: 1420-1423.
69. Thal, D. R., M. Holzer, U. Rub, G. Waldmann, S. Gunzel, D. Zedlick, and R. Schober. 2000. Alzheimer-related tau-pathology in the perforant path target zone and in the hippocampal stratum oriens and radiatum correlates with onset and degree of dementia. Exp. Neurol. 163: 98-110.
70. Tomlinson, B. E., and D. Kitchener. 1972. Granulovacuolar degeneration of hippocampal pyramidal cells. J. Pathol. 106: 165-185.
71. Uboga, N. V., and J. L. Price. 2000. Formation of diffuse and fibrillar tangles in aging and early Alzheimer's disease. Neurobiol. Aging 21: 1-10.
72. Van Hoesen, G. W., B. T. Hyman, and A. R. Damasio. 1991. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus 1: 1-8.
73. Van Hoesen, G. W., and A. Solodkin. 1994. Cellular and system neuroanatomical changes in Alzheimer's disease. Ann. N. Y. Acad. Sci. 747: 12-35.
74. Vincent, I. J., and P. Davies. 1992. A protein kinase associated with paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. USA 89: 2878-2882.
75. von Bergen,M., P. Friedhoff, J. Biernat, J. Heberle, and E. Mandelkow. 2000. Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming beta structure. Proc. Natl. Acad. Sci. USA 97: 5129-5134.
76. Wilson, R. S., L. A. Beckett, L. L. Barnes, J. A. Schneider, J. Back, D. A. Evans, and D. A. Bennett, 2002. Individual differences in rates of change in cognitive abilities of older persons. Psychol. Aging. 17: 179-193.
77. Wilson, R. S., L. A. Beckett, D. A. Bennett, M. S. Albert, and D. A. Evans. 1999. Change in cognitive function in older persons from a community population: Relation to age and Alzheimer disease. Arch. Neurol. 56: 1274-1279.
78. Wilson, R. S., D. W. Gilley, D. A. Bennett, L. A. Beckett, and D. A. Evans. 2000. Person-specific paths of cognitive decline in Alzheimer's disease and their relation to age. Psychol. Aging 15: 18-28.
79. Wischik, C. M. 1989. Cell biology of the Alzheimer tangle. Curr. Opin. Cell Biol. 1: 115-122.
80. Wischik, C. M., M. Novak, P. C. Edwards, A. Klug, W. Tichelaar, and R. A. Crowther. 1988a. Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. USA 85: 4884-4888.
81. Wischik, C. M., M. Novak, H. C. Thogersen, P. C. Edwards, M. J. Runswick, R. Jakes, J. E. Walker, C. Milstein, M. Roth, and A. Klug. 1988b. Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. USA 85: 4506-4510.
82. Yasojima, K., J. Kuret, A. J. DeMaggio, E. McGeer, and P. L. McGeer. 2000. Casein kinase 1 delta mRNA is upregulated in Alzheimer disease brain. Brain Res. 865: 116-120.