Early N-terminal changes and caspase-6 cleavage of tau in Alzheimer's disease

Journal of Neuroscience

Volumn 24, Issue 36, 2004, Pages 7895-7902

  Horowitz, Peleg M ^a,d   Patterson, Kristina R ^a   Guillozet Bongaarts, Angela L ^a   Reynolds, Matthew R ^a   Carroll, Christopher A ^b   Weintraub, Susan T ^b   Bennett, David A ^c   Cryns, Vincent L ^a   Berry, Robert W ^a   Binder, Lester I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Caspase; Neurofibrillary tangle; Tau; Truncation; Tyrosine phosphorylation

Indexed keywords

CASPASE 3; CASPASE 6; EPITOPE; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN ANTIBODY; TAU PROTEIN; TAU PROTEIN 12; TAU PROTEIN 5A6; TAU PROTEIN 9G3 PY18; TAU PROTEIN ANTIBODY; TYROSINE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLINICAL ARTICLE; HUMAN; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMINO ACID SUBSTITUTION; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; APOPTOSIS; CASPASE 6; CASPASES; COHORT STUDIES; DISEASE PROGRESSION; EPITOPES; FEMALE; HUMANS; MALE; MICROSCOPY, FLUORESCENCE; NERVE TISSUE PROTEINS; NEUROFIBRILLARY TANGLES; NEURONS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FYN; RECOMBINANT PROTEINS; SINGLE-BLIND METHOD; SRC-FAMILY KINASES; TAU PROTEINS; TEMPORAL LOBE;

EID: 4544248870     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1988-04.2004     Document Type: Article

References (52)

1. Abraha A, Ghoshal N, Gamblin TC, Cryns V, Berry RW, Kuret J, Binder LI (2000) C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J Cell Sci 113:3737-3745.
2. Bennett DA, Wilson RS, Schneider JA, Evans DA, Beckett LA, Aggarwal NT, Barnes LL, Fox JH, Bach J (2002) Natural history of mild cognitive impairment in older persons. Neurology 59:198-205.
3. Berry RW, Abraha A, Lagalwar S, LaPointe N, Gamblin TC, Cryns VL, Binder LI (2003) Inhibition of tau polymerization by its carboxy-terminal caspase cleavage fragment. Biochemistry 42:8325-8331.
4. Bondareff W, Harrington C, Wischik CM, Hauser DL, Roth M (1994) Immunohistochemical staging of neurofibrillary degeneration in Alzheimer's disease. J Neuropathol Exp Neurol 53:158-164.
5. Braak H, Braak E (1995) Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol Aging 16:271-278.
6. Canu N, Dus L, Barbato C, Ciotti MT, Brancolini C, Rinaldi AM, Novak M, Cattaneo A, Bradbury A, Calissano P (1998) Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis. J Neurosci 18:7061-7074.
7. Carmel G, Mager EM, Binder LI, Kuret J (1996) The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J Biol Chem 271:32789-32795.
8. Chung CW, Song YH, Kim IK, Yoon WJ, Ryu BR, Jo DG, Woo HN, Kwon YK, Kim HH, Gwag BJ, Mook-Jung IH, Jung YK (2001) Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol Dis 8:162-172.
9. Cohen GM (1997) Caspases: the executioners of apoptosis. Biochem J 326:1-16.
10. Cotman CW, Su JH (1996) Mechanisms of neuronal death in Alzheimer's disease. Brain Pathol 6:493-506.
11. Cryns V, Yuan J (1998) Proteases to die for. Genes Dev 12:1551-1570.
12. Desjardins P, Ledoux S (1998) Expression of ced-3 and ced-9 homologs in Alzheimer's disease cerebral cortex. Neurosci Lett 244:69-72.
13. Dickson DW, Ksiezak-Reding H, Liu WK, Davies P, Crowe A, Yen SH (1992) Immunocytochemistry of neurofibrillary tangles with antibodies to sub-regions of tau protein: identification of hidden and cleaved tau epitopes and a new phosphorylation site. Acta Neuropathol 84:596-605.
14. Duyckaerts C, Colle MA, Dessi F, Piette F, Hauw JJ (1998) Progression of Alzheimer histopathological changes. Acta Neurol Belg 98:180-185.
15. Endoh R, Ogawara M, Iwatsubo T, Nakano I, Mori H (1993) Lack of the carboxyl terminal sequence of tau in ghost tangles of Alzheimer's disease. Brain Res 601:164-172.
16. Fasulo L, Ovecka M, Kabat J, Bradbury A, Novak M, Cattaneo A (1996) Overexpression of Alzheimer's PHF core tau fragments: implications for the tau truncation hypothesis. Alzheimer's Res 2:195-200.
17. Fasulo L, Visintin M, Novak M, Cattaneo A (1998) Tau truncation in Alzheimer's disease: expression of a fragment encompassing PHF core tau induces apoptosis in COS cells. Alzheimer's Reports 1:25-32.
18. Fasulo L, Ugolini G, Visintin M, Bradbury A, Brancolini C, Verzillo V, Novak M, Cattaneo A (2000) The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J Neurochem 75:624-633.
19. Friedhoff P, von Bergen M, Mandelkow EM, Mandelkow E (2000) Structure of tau protein and assembly into paired helical filaments. Biochim Biophys Acta 1502:122-132.
20. Gamblin TC, Berry RW, Binder LI (2003a) Tau polymerization: role of the amino terminus. Biochemistry 42:2252-2257.
21. Gamblin TC, Chen F, Abraha A, Miller R, Fu Y, Garcia-Sierra F, Lagalwar S, Berry RW, Binder LI, Cryns VL (2003b) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 100:10032-10037.
22. Garcia-Sierra F, Ghoshal N, Quinn B, Berry R, Binder LI (2003) Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease. J Alzheimer's Disease 5:65-77.
23. Ghoshal N, Garcia-Sierra F, Fu Y, Beckett LA, Mufson EJ, Kuret J, Berry RW, Binder LI (2001) Tau-66: evidence for a novel tau conformation in Alzheimer's disease. J Neurochem 77:1372-1385.
24. Ghoshal N, Garcia-Sierra F, Wuu J, Leurgans S, Bennett DA, Berry RW, Binder LI (2002) Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease. Exp Neurol 177:475-493.
25. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA (1989) 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.
26. Hwang DY, Chae KR, Kang TS, Hwang JH, Lim CH, Kang HK, Goo JS, Lee MR, Lim HJ, Min SH, Cho JY, Hong JT, Song CW, Paik SG, Cho JS, Kim YK (2002) Alterations in behavior, amyloid beta-42, caspase-3, and Cox-2 in mutant PS2 transgenic mouse model of Alzheimer's disease. FASEB J 16:805-813.
27. Hyman BT, Van Hoesen GW, Wolozin BL, Davies P, Kromer LJ, Damasio AR (1988) Alz-50 antibody recognizes Alzheimer-related neuronal changes. Ann Neurol 23:371-379.
28. Jicha GA, Bowser R, Kazam IG, Davies P (1997) Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res 48:128-132.
29. Johnson GV, Seubert P, Cox TM, Motter R, Brown JP, Galasko D (1997) The tau protein in human cerebrospinal fluid in Alzheimer's disease consists of proteolytically derived fragments. J Neurochem 68:430-433.
30. Johnson GVW, Hartigan JA (1998) Tau protein in normal and Alzheimer's disease brain: an update. Alzheimer's Disease Rev 3:125-141.
31. Johnson GVW, Jenkins SM (1996) Tau protein in normal and Alzheimer's disease brain. Alzheimer's Disease Rev 1:38-54.
32. Kitamura Y, Shimohama S, Kamoshima W, Ota T, Matsuoka Y, Nomura Y, Smith MA, Perry G, Whitehouse PJ, Taniguchi T (1998) Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease. Brain Res 780:260-269.
33. Kordower JH, Chu Y, Stebbins GT, DeKosky ST, Cochran EJ, Bennett D, Mufson EJ (2001) Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Ann Neurol 49:202-213.
34. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VM, Lee G (1988) Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1:817-825.
35. LeBlanc A, Liu H, Goodyer C, Bergeron C, Hammond J (1999) Caspase-6 role in apoptosis of human neurons, amyloidogenesis, and Alzheimer's disease. J Biol Chem 274:23426-23436.
36. Lee G, Thangavel R, Sharma VM, Litersky JM, Bhaskar K, Fang SM, Do LH, Andreadis A, Van Hoesen G, Ksiezak-Reding H (2004) Phosphorylation of tau by fyn: implications for Alzheimer's disease. J Neurosci 24:2304-2312.
37. Mitchell TW, Mufson EJ, Schneider JA, Cochran EJ, Nissanov J, Han LY, Bienias JL, Lee VM, Trojanowski JQ, Bennett DA, Arnold SE (2002) Parahippocampal tau pathology in healthy aging, mild cognitive impairment, and early Alzheimer's disease. Ann Neurol 51:182-189.
38. Mufson EJ, Chen EY, Cochran EJ, Beckett LA, Bennett DA, Kordower JH (1999) Entorhinal cortex beta-amyloid load in individuals with mild cognitive impairment. Exp Neurol 158:469-490.
39. Novak M, Kabat J, Wischik CM (1993) Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament. EMBO J 12:365-370.
40. 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.
41. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A (2002) Tau is essential to beta-amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 99:6364-6369.
42. 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.
43. Rohn TT, Head E, Su JH, Anderson AJ, Bahr BA, Cotman CW, Cribbs DH (2001) Correlation between caspase activation and neurofibrillary tangle formation in Alzheimer's disease. Am J Pathol 158:189-198.
44. Rohn TT, Rissman RA, Davis MC, Kim YE, Cotman CW, Head E (2002) Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Neurobiol Dis 11:341-354.
45. Smale G, Nichols NR, Brady DR, Finch CE, Horton Jr WE (1995) Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 133:225-230.
46. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D, Ghayur T, Brady KD, Wong WW (1997) Substrate specificities of caspase family proteases. J Biol Chem 272:9677-9682.
47. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, Houtzager VM, Nordstrom PA, Roy S, Vaillancourt JP, Chapman KT, Nicholson DW (1997) A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 272:17907-17911.
48. Uboga NV, Price JL (2000) Formation of diffuse and fibrillar tangles in aging and early Alzheimer's disease. Neurobiol Aging 21:1-10.
49. Wilson RS, Beckett LA, Barnes LL, Schneider JA, Back J, Evans DA, Bennett DA (2002) Individual differences in rates of change in cognitive abilities of older persons. Psychol Aging 17:179-193.
50. Wischik CM, Novak M, Edwards PC, Klug A, Tichelaar W, Crowther RA (1988a) Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci USA 85:4884-4888.
51. Wischik CM, Novak M, Thogersen HC, Edwards PC, Runswick MJ, Jakes R, Walker JE, Milstein C, Roth M, Klug A (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.
52. Zhang Y, Goodyer C, LeBlanc A (2000) Selective and protracted apoptosis in human primary neurons microinjected with active caspase-3, -6, -7, and -8. J Neurosci 20:8384-8389.