Tau isoform regulation is region- and cell-specific in mouse brain

Journal of Comparative Neurology

Volumn 511, Issue 6, 2008, Pages 788-803

  McMillan, Pamela ^a,b   Korvatska, Elena ^b   Poorkaj, Parvoneh ^a   Evstafjeva, Zana ^b   Robinson, Linda ^b   Greenup, Lynne ^a,b   Leverenz, James ^a,b,c   Schellenberg, Gerard D ^a,b,c   D'Souza, Ian ^d  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d Seattle Institute for Cardiac Research   (United States)

Author keywords

3 repeat and 4 repeat tau; Alzheimer's disease; Frontotemporal dementia; Phosphorylation; Splicing; Tauopathy

Indexed keywords

TAU PROTEIN; ISOPROTEIN; MAPT PROTEIN, HUMAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXON; FRONTAL CORTEX; FRONTOTEMPORAL DEMENTIA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC VARIABILITY; HIPPOCAMPUS; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RNA SPLICING; TRANSGENIC MOUSE; WILD TYPE; AGING; ANIMAL; BRAIN; COMPARATIVE STUDY; CYTOLOGY; FRONTAL LOBE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; NEWBORN; PHOSPHORYLATION; SPECIES DIFFERENCE; SYNAPTIC MEMBRANE; ULTRASTRUCTURE;

AGING; ANIMALS; ANIMALS, NEWBORN; BRAIN; EXONS; FRONTAL LOBE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; HUMANS; MICE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; PROTEIN ISOFORMS; SPECIES SPECIFICITY; SYNAPTIC MEMBRANES; TAU PROTEINS;

EID: 58749088408     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21867     Document Type: Article

References (86)

1. Andorfer C, Kress Y, Espinoza M, de Silva R, Tucker KL, Barde YA, Duff K, Davies P. 2003. Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J Neurochem 86:582-590.
2. Andorfer C, Acker CM, Kress Y, Hof PR, Duff K, Davies P. 2005. Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 25:5446-5454.
3. Andreadis A. 2005. Tau gene alternative splicing: expression patterns, regulation and modulation of function in normal brain and neurodegenerative diseases. Biochim Biophys Acta 1739:91-103.
4. Arai T, Ikeda K, Akiyama H, Shikamoto Y, Tsuchiya K, Yagishita S, Beach T, Rogers J, Schwab C, Mcgeer PL. 2001. Distinct isoforms of tau aggregated in neurons and glial cells in brains of patients with Pick's disease, corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol 101:167-173.
5. Aronov S, Aranda G, Behar L, Ginzburg I. 2001. Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targeting signal. J Neurosci 21:6577-6587.
6. Baker M, Litvan I, Houlden H, Adamson J, Dickson D, Perez-Tur J, Hardy J, Lynch T, Bigio E, Hutton M. 1999. Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum Mol Genet 8:711-715.
7. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR. 2000. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33:95-130.
8. Bullmann T, de Silva R, Holzer M, Mori H, Arendt T. 2007. Expression of embryonic tau protein isoforms persist during adult neurogenesis in the hippocampus. Hippocampus 17:98-102.
9. Bunker JM, Wilson L, Jordan MA, Feinstein SC. 2004. Modulation of microtubule dynamics by tau in living cells: implications for development and neurodegeneration. Mol Biol Cell 15:2720-2728.
10. Butner KA, Kirschner MW. 1991. Tau protein binding to microtubules through a flexible array of distributed weak sites. J Cell Biol 115:717-730.
11. Clark LN, Poorkaj P, Wszolek Z, Geschwind DH, Nasreddine ZS, Miller B, Li D, Payami H, Awert F, Markopoulou K, Andreadis A, D'Souza I, Lee VMY, Reed L, Trojanowski JQ, Zhukareva V, Bird T, Schellenberg GD, Wilhelmsen KC. 1998. Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc Natl Acad Sci U S A 95:13103-13107.
12. Conrad C, Andreadis A, Trojanowski J, Dickson D, Kang D, Chen X, Wiederholt W, Hansen L, Masliah E, Thal L, Katzman R, Xia Y, Saitoh T. 1997. Genetic evidence for the involvement of Tau in progressive supranuclear palsy. Ann Neurol 41:277-281.
13. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP. 2001. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114:1179-1187.
14. de Silva R, Lashley T, Gibb G, Hanger D, Hope A, Reid A, Bandopadhyay R, Utton M, Strand C, Jowett T, Khan N, Anderton B, Wood N, Holton J, Revesz T, Lees A. 2003. Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubule-binding repeat domains as demonstrated by new specific monoclonal antibodies. Neuropathol Appl Neurobiol 29:288-302.
15. Denk F, Wade-Martins R. 2007. Knock-out and transgenic mouse models of tauopathies. Neurobiol Aging (in press).
16. Di Maria E, Tabaton M, Vigo T, Abbruzzese G, Bellone E, Donati C, Frasson E, Marchese R, Montagna P, Munoz DG, Pramstaller PP, Zanusso G, Ajmar F, Mandich P. 2000. Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy. Ann Neurol 47:374-377.
17. Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ. 2006. Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 495:70-83.
18. Drechsel DN, Hyman AA, Cobb MH, Kirschner MW. 1992. Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141-1154.
19. D'Souza I, Schellenberg GD. 2000. Determinants of 4 repeat tau expression: Coordination between enhancing and inhibitory splicing sequences for exon 10 inclusion. J Biol Chem 275:17700-17709.
20. D'Souza I and Schellenberg GD. 2002. Tau exon 10 expression involves a bipartite intron 10 regulatory sequence and a weak 3' splice site. J Biol Chem 277:26587-26599.
21. D'Souza I, Poorkaj P, Hong M, Nochlin D, Lee VMY, Bird TD, Schellenberg GD. 1999. Missense and silent tau gene mutations cause front temporal dementia with parkinsonism - chromosome 17 type by affecting multiple alternative RNA splicing regulatory elements. Proc Natl Acad Sci U S A 96:5598-5603.
22. Feinstein SC and Wilson L. 2005. Inability of tau to properly regulate neuronal microtubule dynamics: a loss-of-function mechanism by which tau might mediate neuronal cell death. Biochim Biophys Acta 1739:268-279.
23. Feng RB, Rampon C, Tang YP, Shrom D, Jin J, Kim M, Sopher B, Martin GM, Kim SH, Langdon RB, Sisodia SS, Tsien JZ. 2001. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32:911-926.
24. Forman MS, Lal D, Zhang B, Dabir DV, Swanson E, Lee VMY, Trojanowski JQ. 2005. Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration. J Neurosci 25:3539-3550.
25. Fujino Y, Wang DS, Thomas N, Espinoza M, Davies P, Dickson DW. 2005. Increased frequency of argyrophilic grain disease in Alzheimer disease with 4R-tau-specific immunohistochemistry. J Neuropathol Exp Neurol 64:209-214.
26. Goedert M, Jakes R. 1990. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J 9:4225-4230.
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 mRNA's in human brain. EMBO J 8:393-399.
29. Goedert M, Spillantini MG, Crowther RA. 1992. Cloning of a big tau microtubule-associated protein characteristic of the peripheral nervous system. Proc Natl Acad Sci U S A 89:1983-1987.
30. Goode BL, Feinstein SC. 1994. Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau. J Cell Biol 124:769-782.
31. Goode BL, Denis PE, Panda D, Radeke MJ, Miller HP, Wilson L, Feinstein SC. 1997. Functional interactions between the proline-rich and repeat regions of tau enhance microtubule binding and assembly. Mol Biol Cell 8:353-365.
32. Goode BL, Chau M, Denis PE, Feinstein SC. 2000. Structural and functional differences between 3-repeat and 4-repeat tau isoforms. J Biol Chem 275:38182-38189.
33. Goris A, WilliamsGray CH, Clark GR, Foltynie T, Lewis SJG, Brown J, Ban M, Spillantini MG, Compston A, Burn DJ, Chinnery PF, Barker RA, Sawcer SJ. 2007. Tau and alpha-synuclein in susceptibility to, and dementia in, Parkinson's disease. Ann Neurol 62:145-153.
34. Gotz J, Probst A, Spillantini MG, Schafer T, Jakes R, Burki K, Goedert M. 1995. Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. EMBO J 14:1304-1313.
35. Gotz J. 2001. Tau and transgenic animal models. Brain Res Rev 35:266-286.
36. Gould E, Gross CG. 2002. Neurogenesis in adult mammals: some progress and problems. J Neurosci 22:619-623.
37. Grover A, Houlden H, Baker M, Adamson J, Lewist J, Prihart G, Pickering-Brown S, Duff K, Hutton M. 1999. 5′ splice mutations in tau associated with the inherited dementia FTDP-17 affect a stem-loop structure that regulates alternative splicing of exon 10. J Biol Chem 274:15134-15143.
38. Gustke N, Trinczek B, Biernat J, Mandelkow EM, Mandelkow E. 1994. Domains of tau protein and interactions with microtubules. Biochemistry 33:9511-9522.
39. Hanger DP, Gibb GM, de Silva R, Boutajangout A, Brion JP, Revesz T, Lees AJ, Anderton BH. 2002. The complex relationship between soluble and insoluble tau in tauopathies revealed by efficient dephosphorylation and specific antibodies. FEBS Lett 531:538-542.
40. Higgins JJ, Golbe LI, Debiase A, Jankovic J, Factor SA, Adler RL. 2000. An extended 5′-tau susceptibility haplotype in progressive supranuclear palsy. Neurology 55:1364-1367.
41. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VMY. 1998. Mutation-specific functional impairments in distinct Tau isoforms of hereditary FTDP-17. Science 282:1914-1917.
42. Houlden H, Baker M, Morris HR, MacDonald N, Pickering-Brown S, Adamson J, Lees AJ, Rossor MN, Quinn NP, Kertesz A, Khan MN, Hardy J, Lantos PL, George-Hyslop PS, Munoz DG, Mann D, Lang AE, Bergeron C, Bigio EH, Litvan I, Bhatia KP, Dickson D, Wood NW, Hutton M. 2001. Corticobasal degeneration and progressive supranuclear palsy share a common tau haplotype. Neurology 56:1702-1706.
43. Hughes A, Mann D, Pickering-Brown S. 2003. Tau haplotype frequency in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Exp Neurol 181:12-16.
44. 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 P, 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.
45. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, Lee VMY. 1999. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24:751-762.
46. Janke C, Beck M, Stahl T, Holzer M, Brauer K, Bigl V, Arendt T. 1999. Phylogenetic diversity of the expression of the microtubule-associated protein tau: implications for neurodegenerative disorders. Mol Brain Res 68:119-128.
47. Jin KL, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA. 2004. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci U S A 101:343-347.
48. Kampers T, Pangalos M, Geerts H, Wiech H, Mandelkow E. 1999. Assembly of paired helical filaments from mouse tau: implications for the neurofibrillary pathology in transgenic mouse models for Alzheimer's disease. FEBS Lett 451:39-44.
49. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VML, Lee G. 1988. Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1:817-826.
50. Kosik KS, Orecchio LD, Bakalis S, Neve RL. 1989. Developmentally regulated expression of specific tau sequences. Neuron 2:1389-1397.
51. Lee G, Neve RL, Kosik KS. 1989. The microtubule binding domain of tau protein. Neuron 2:1615-1624.
52. Lee VMY, Goedert M, Trojanowski JQ. 2001. Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
53. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van, Slegtenhorst M, Gwinn-Hardy K, Murphy MP, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin W-L, Yen S-H, Dickson DW, Davies P, Hutton M. 2000. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25:402-405.
54. Lu M, Kosik KS. 2001. Competition for microtubule-binding with dual expression of tau missense and splice isoforms. Mol Biol Cell 12:171-184.
55. Mandelkow E, von Bergen M, Biernat J, Mandelkow EM. 2007. Structural principles of tau and the paired helical filaments of Alzheimer's disease. Brain Pathol 17:83-90.
56. Matsuo ES, Shin RW, Billingsley ML, vad deVoorde A, Oconnor M, Trojanowski JQ, Lee VMY. 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.
57. Mirra SM, Hart MN, Terry RD. 1993. Making the diagnosis of Alzheimer's disease. A primer for practicing pathologists. Arch Pathol Lab Med 117:132-144.
58. Muyrers JPP, Zhang Y, Testa G, Stewart AF. 1999. Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res 27:1555-1557.
59. Myers AJ, Kaleem M, Marlowe L, Pittman AM, Lees AJ, Fung HC, Duck-worth J, Leung D, Gibson A, Morris CM, de Silva R, Hardy J. 2005. The H1c haplotype at the MAPT locus is associated with Alzheimer's disease. Hum Mol Genet 14:2399-2404.
60. Panda D, Miller HP, Wilson L. 1999. Rapid treadmilling of brain microtubules free of microtubule-associated proteins in vitro and its suppression by tau. Proc Natl Acad Sci U S A 96:12459-12464.
61. Panda D, Samuel JC, Massie M, Feinstein SC, Wilson L. 2003. Differential regulation of microtubule dynamics by three- and four-repeat tau: Implications for the onset of neurodegenerative disease. Proc Natl Acad Sci U S A 100:9548-9553.
62. Pastor P, Ezquerra M, Perez JC, Chakraverty S, Norton J, Racette BA, McKeel D, Perlmutter JS, Tolosa E, Goate AM. 2004. Novel haplotypes in 17q21 are associated with progressive supranuclear palsy. Ann Neurol 56:249-258.
63. Pittman AM, Myers AJ, Duckworth J, Bryden L, Hanson M, Abou-Sleiman P, Wood NW, Hardy J, Lees A, de Silva R. 2004. The structure of the tau haplotype in controls and in progressive supranuclear palsy. Hum Mol Genet 13:1267-1274.
64. 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.
65. Poorkaj P, Peterson KR, Schellenberg GD. 2000. Single-step conversion of P1 and P1 artificial chromosome clones into yeast artificial chromosomes. Genomics 68:106-110.
66. Poorkaj P, Tsuang D, Wijsman EM, Nemens E, Garruto RM, Craig U, Anderson L-J, Bird TD, Plato CC, Weiderholt W, Galasko D, Schellenberg GD. 2001a. Tau is a susceptibility gene for amyotropic lateral sclerosis-parkinsonism dementia complex of Guam. Arch Neurol 58: 1871-1878.
67. Poorkaj P, Kas A, D'Souza I, Zhou Y, Pham O, Olson MV, Schellenberg GD. 2001b. A genomic sequence analysis of the mouse and human microtubule-associated protein tau. Mamm Genome 12:700-712.
68. Poorkaj P, Muma NA, Zhukareva V, Cochran EJ, Shannon KM, Hurtig H, Koller WC, Bird TD, Trojanowski JQ, Lee VMY, Schellenberg GD. 2002. A R5L tau mutation in a subject with a progressive supranuclear palsy phenotype. Ann Neurol 52:511-516.
69. Rademakers R, Melquist S, Cruts M, Theuns J, Del-Favero J, Poorkaj P, Baker M, Sleegers K, Crook R, De Pooter T, Kacem SB, Adamson J, Van den Bossche D, Van den Broeck M, Gass J, Corsmit E, DeRijk P, Thomas N, Engelborghs S, Heckman M, Litvan I, Crook J, De Deyn PP, Dickson D, Schellenberg GD, Van Broeckhoven C, Hutton ML. 2005. High-density SNP haplotyping suggests altered regulation of tau gene expression in progressive supranuclear palsy. Hum Mol Genet 14: 3281-3292.
70. Rao MS, Shetty AK. 2004. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19:234-246.
71. Reed LA, Wszolek ZK, Hutton M. 2001. Phenotypic correlations in FTDP-17. Neurobiol Aging 22:89-107.
72. Sennvik K, Boekhoorn K, Lasrado R, Terwel D, Verhaeghe S, Korr H, Schmitz C, Tomiyama T, Mori H, Krugers H, Joels M, Ramakers GJ, Lucassen PJ, Van Leuven F. 2007. Tau-4R suppresses proliferation and promotes neuronal differentiation in the hippocampus of tau knockin/knockout mice. FASEB J 21:2149-2161.
73. Stanford PM, Halliday GM, Brooks WS, Kwok BJ, Storet CE, Creasey H, Morris JGL, Fulham MJ, Schofield PRj. 2000. Progressive supranuclear palsy caused by a novel silent mutation in exon 10 of the tau gene. Brain 123:880-893.
74. Sumi SM, Bird TD, Nochlin D, Raskind MA. 1992. Familial presenile dementia with psychosis associated with cortical neurofibrillary tangles and neurodegeneration of the amygdala. Neurology 42:120-127.
75. Sundar PD, Yu CE, Sieh W, Steinbart E, Garruto RM, Oyanagi K, Craig UK, Bird TD, Wijsman EM, Galasko DR, Schellenberg GD. 2007. Two sites in the MAPT region confer genetic risk for Guam ALS/PDC and dementia. Hum Mol Genet 16:295-306.
76. Takuma H, Arawaka S, Mori H. 2003. Isoforms changes of tau protein during development in various species. Dev Brain Res 142:121-127.
77. Trinczek B, Biernat J, Baumann K, Mandelkow EM, Mandelkow E. 1995. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol Biol Cell 6:1887-1902.
78. Utton MA, Connell J, Asuni AA, van Slegtenhorst M, Hutton M, de Silva R, Lees AJ, Miller CCJ, Anderton BH. 2002. The slow axonal transport of the microtubule-associated protein tau and the transport rates of different isoforms and mutants in cultured neurons. J. Neurosci. 22: 6394-6400.
79. van Swieten JC, Bronner IF, Azmani A, Severijnen LA, Kamphorst W, Ravid R, Rizzu P, Willemsen R, Heutink P. 2007. The DeltaK280 mutation in MAP tau favors exon 10 skipping in vivo. J Neuropathol Exp Neurol 66:17-25.
80. Wang J, Sarov M, Rientjes J, Fu J, Hollak H, Kranz H, Xie W, Stewart AF, Zhang Y. 2006. An improved recombineering approach by adding RecA to lambda Red recombination. Mol Biotechnol 32:43-53.
81. Winton MJ, Joyce S, Zhukareva V, Practico D, Perl DP, Galasko D, Craig U, Trojanowski JQ, Lee VMY. 2006. Characterization of tau pathologies in gray and white matter of Guam parkinsonism-dementia complex. Acta Neuropathol 111:401-412.
82. Zabetian CP, Hutter CM, Factor SA, Nutt JG, Higgins DS, Griffith A, Roberts JW, Leis BC, Kay DM, Yearout D, Montimurro JS, Edwards KL, Samii A, Payami H. 2007. Association analysis of MAPT H1 haplotype and subhaplotypes in Parkinson's disease. Ann Neurol 62:137-144.
83. Zhang Y, Buchholz F, Muyrers JPP, Stewart AF. 1998. A new logic for DNA engineering using recombination in Escherichia coli. Nat Genet 20: 123-128.
84. Zhang Y, Muyrers JPP, Rientjes J, Stewart AF. 2003. Phage annealing proteins promote oligonucleotide-directed mutagenesis in Escherichia coli and mouse ES cells. BMC Mol Biol 4:1-14.
85. Zhukareva V, Mann D, Pickering-Brown S, Uryu K, Shuck T, Shah K, Grossman M, Miller BL, Hulette CM, Feinstein SC, Trojanowski JQ, Lee VMY. 2002. Sporadic Pick's disease: a tauopathy characterized by a spectrum of pathological tau isoforms in gray and white matter. Ann Neurol 51:730-739.
86. Zhukareva V, Joyce S, Schuck T, Van Deerlin V, Hurtig H, Albin R, Gilman S, Chin S, Miller B, Trojanowski JQ, Lee VMY. 2006. Unexpected abundance of pathological tau in progressive supranuclear palsy white matter. Ann Neurol 60:335-345.