Tau isoforms which contain the domain encoded by exon 6 and their role in neurite elongation

Journal of Cellular Biochemistry

Volumn 91, Issue 5, 2004, Pages 880-895

  Luo, Min Hua ^a,b   Leski, Michael L ^c   Andreadis, Athena ^a,d  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Central South University   (China)

^c MCLEAN HOSPITAL   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Alternative splicing; Isoform localization in SH SY5Y cells; Isoform variants; MAP tau; Neurite elongation

Indexed keywords

ISOPROTEIN; TAU PROTEIN; ANTIBODY; FLAG PEPTIDE; PEPTIDE; RETINOIC ACID; TUBULIN;

ARTICLE; EXON; NERVE FIBER GROWTH; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BRAIN LEVEL; CELL DIFFERENTIATION; CELL DIVISION; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; CYTOLOGY; DRUG EFFECT; FETUS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOLOGY; LIVER; MOLECULAR GENETICS; NERVE CELL; NEURITE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE HOMOLOGY; SKELETAL MUSCLE; SPINAL CORD; TUMOR CELL LINE; WESTERN BLOTTING;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; BRAIN CHEMISTRY; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; EXONS; FETUS; GENE EXPRESSION; GENETIC VECTORS; HUMANS; LIVER; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; NEURITES; NEURONS; PEPTIDES; PROTEIN ISOFORMS; SEQUENCE HOMOLOGY, AMINO ACID; SPINAL CORD; TAU PROTEINS; TRANSFECTION; TRETINOIN; TUBULIN;

EID: 3142695169     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20029     Document Type: Article

References (57)

1. Andreadis A, Brown WM, Kosik K. 1992. Structure and novel exons of the human tau gene. Biochemistry 31:10626-10633.
2. Andreadis A, Nisson P, Kosik KS, Watkins P. 1993. The exon trapping assay partly discriminates against alternatively spliced exons. Nucl Acids Res 21:2217-2221.
3. Bahr BA, Vicente JS. 1998. Age-related phosphorylation and fragmentation events influence the distribution profiles of distinct tau isoforms in mouse brain. J Neuropathol Exp Neurol 57:111-121.
4. Billingsley ML, Kincaid RL. 1997. Regulated phosphorylation and dephosphorylation of tau protein: Effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem J 323:577-591.
5. Black MM, Slaughter T, Moshiah S, Obrocka M, Fischer I. 1996. Tau is enriched on dynamic microtubules in the distal region of growing axons. J Neurosci 16:3601-3619.
6. Brandt R, Léger J, Lee G. 1995. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J Cell Biol 131:1327-1340.
7. Caceres A, Kosik KS. 1990. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463.
8. Caceres A, Potrebic S, Kosik KS. 1991. The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J Neurosci 11:1515-1523.
9. 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.
10. Chen J, Kanai Y, Cowan NJ, Hirokawa N. 1992. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360:674-677.
11. 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.
12. 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 VM, Reed L, Trojanowski JQ, Zhukareva V, Bird T, Schellenberg G, 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 USA 95:13103-13107.
13. Couchie D, Mavilia C, Georgieff IS, Liem RKH, Shelanski ML, Nuñez J. 1992. Primary structure of high molecular weight tau present in the peripheral nervous system. Proc Natl Acad Sci USA 89:4378-4381.
14. D'Souza I, Poorkaj P, Hong M, Nochlin D, Lee VM, Bird TD, Schellenberg GD. 1999. Missense and silent tau gene mutations cause frontotemporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc Natl Acad Sci USA 96:5598-5603.
15. 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.
16. DiTella M, Feiguin F, Morfini G, Cáceres A. 1994. Microfilament-associated growth cone component depends upon tau for its intracellular localization. Cell Motil Cytoskel 29:117-130.
17. Encinas M, Iglesias M, Liu Y, Wang H, Muhaisen A, Cena V, Gallego C, Cornella JX. 2000. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J Neurochem 75:991-1003.
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. Frappier TF, Georgieff IS, Brown K, Shelanski ML. 1994. Tau regulation of microtubule-microtubule spacing and bundling. J Neurochem 63:2288-2294.
20. Furukawa K, D'Souza I, Crudder CH, Onodera H, Itoyama Y, Poorkaj P, Bird TD, Schellenberg GD. 2000. Proapoptotic effects of tau mutations in chromosome 17 frontotemporal dementia and parkinsonism. Neuroreport 11:57-60.
21. Gao QS, Memmott J, Lafyatis R, Stamm S, Screaton G, Andreadis A. 2000. Complex regulation of tau exon 10, whose missplicing causes frontotemporal dementia. J Neurochem 74:490-500.
22. 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.
23. 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 isoforms in human brain. EMBO J 8:393-399.
24. 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.
25. Gorath M, Stahnke T, Mronga T, Goldbaum O, Richter-Landsberg C. 2001. Developmental changes of tau protein and mRNA in cultured rat brain oligodendrocytes. Glia 36:89-101.
26. Grabowski PJ, Black DL. 2001. Alternative RNA splicing in the nervous system. Prog Neurobiol 65:289-308.
27. Grover A, Houlden H, Baker M, Adamson J, Lewis J, Prihar G, Pickering-Brown S, Duff K, Hutton M. 1999. 5′ splice site mutations in tau associated with the inherited dementia FTDP-17 affect a stem-loop structure that regulatesalternative splicing of exon 10. J Biol Chem 274:15134-15143.
28. Himmler A. 1989. Structure of the bovine tau gene: Alternatively spliced transcripts generate a gene family. Mol Cell Biol 9:1389-1396.
29. Himmler A, Drechsel D, Kirschner MW, Martin DW. 1989. Tau consists of a set of proteins with repreated C-terminal microtubule-binding domains and variable N-terminal domains. Mol Cell Biol 9:1381-1388.
30. Hirokawa N. 1994. Microtubule organization and dynamics dependent on microtubule- associated proteins. Curr Opin Cell Biol 6:74-81.
31. 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 P, 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.
32. Ikegami S, Harada A, Hirokawa N. 2000. Muscle weakness, hyperactivity, and impairment in fear conditioning in tau-deficient mice. Neurosci Lett 279:129-132.
33. 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.
34. Kanai Y, Hirokawa N. 1995. Sorting mechanisms of tau and MAP2 in neurons: Suppressed axonal transit of MAP2 and locally regulated microtubule binding. Neuron 14:421-432.
35. Kempf M, Clement A, Faissner A, Lee G, Brandt R. 1996. Tau binds to the distal axon early in development of polarity in a microtubule- and microfilament-dependent manner. J Neurosci 16:5583-5592.
36. Kosik KS, Orecchio LD, Bakalis S, Neve RL. 1989. Developmentally regulated expression of specific tau sequences. Neuron 2:1389-1397.
37. Lee G, Neve RL, Kosik KS. 1989. The microtubule binding domain of human tau protein. Neuron 2:1615-1624.
38. Lee G, Newman ST, Gard DL, Band H, Panchamoorthy G. 1998. Tau interacts with src-family non-receptor tyrosine kinases. J Cell Sci 111:3167-3177.
39. Liu CW, Lee G, Jay DG. 1999. Tau is required for neurite outgrowth and growth cone motility of chick sensory neurons. Cell Motil Cytoskel 43:232-242.
40. LoPresti P, Szuchet S, Papasozomenos SC, Zinkowski RP, Binder LI. 1995. Functional implications for the microtubule-associated protein tau: Localization in oligodendrocytes. Proc Natl Acad Sci USA 92:10369-10373.
41. Lovestone S, Reynolds CH. 1997. The phosphorylation of tau: A critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78:309-324.
42. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP. 1999. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399:784-788.
43. Luo M, Memmott J, Andreadis A. 2004. Novel Isoforms of Tau that lack the microtubule-binding domain. Submitted.
44. Maccioni RB, Tapia L, Cambiazo V. 1995. Functional organization of tau proteins during neuronal differentiation and development. Braz J Med Biol Res 28:827-841.
45. Mandelkow EM, Biernat J, Drewes G, Gustke N, Trinczek B, Mandelkow E. 1995. Tau domains, phosphorylation, and interactions with microtubules. Neurobiol Aging 16:355-362.
46. Nuydens R, Dispersyn G, de Jong M, van den Kieboom G, Borgers M, Geerts H. 1997. Aberrant tau phosphorylation and neurite retraction during NGF deprivation in PC12 cells. Biochem Biophys Res Commun 240:687-691.
47. Nuñez J, Fischer I. 1997. Microtubule-associated proteins MAPs in the peripheral nervous system during development and regeneration. J Mol Neurosci 8:207-222.
48. Poorkaj P, Kas A, D'Souza I, Zhou Y, Pham Q, Stone M, Olson MV, Schellenberg GD. 2001. A genomic sequence analysis of the mouse and human microtubule-associated protein tau. Mamm Genome 12:700-712.
49. Sayas CL, Moreno-Flores MT, Avila J, Wandosell F. 1999. The neurite retraction induced by lysophosphatidic acid increases Alzheimer's disease-like Tau phosphorylation. J Biol Chem 274:37046-37052.
50. 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.
51. Teng KK, Georgieff IS, Aletta JM, Nuñez J, Shelanski ML, Greene LA. 1993. Characterization of a PC12 cell subclone (PC12-C41) with enhanced neurite outgrowth capacity: Implications for a modulatory role of high molecular weight tau in neuritogenesis. J Cell Sci 106:611-626.
52. Uberti D, Rizzini C, Spano PF, Memo M. 1997. Characterization of tau proteins in human neuroblastoma SHSY5Y cell line. Neurosci Lett 235:149-153.
53. Wang Y, Loomis PA, Zinkowski RP, Binder LI. 1993. A novel tau transcript in cultured human neuroblastoma cells expressing nuclear tau. J Cell Biol 121:257-267.
54. Wei ML, Andreadis A. 1998. Splicing of a regulated exon reveals additional complexity in the axonal MAP tau. J Neurochem 70:1346-1356.
55. Wei ML, Memmott J, Screaton G, Andreadis A. 2000. The splicing determinants of a regulated exon in the axonal MAP tau reside within the exon and in its upstream intron. Brain Res Mol Brain Res 80:207-218.
56. Zhang J, Johnson GV. 2000. Tau protein is hyperphosphorylated in a site-specific manner in apoptotic neuronal PC12 cells. J Neurochem 75:2346-2357.
57. Zhao Z, Ho L, Suh J, Qin W, Pyo H, Pompl P, Ksiezak-Reding H, Pasinetti GM. 2003. A role of P301L tau mutant in anti-apoptotic gene expression, cell cycle and apoptosis. Mol Cell Neurosci 24:367-379.