Aberrant Splicing of tau Pre-mRNA Caused by Intronic Mutations Associated with the Inherited Dementia Frontotemporal Dementia with Parkinsonism Linked to Chromosome 17

REFERENCES

• Andreadis, A., Brown, W. M., and Kosik, K. S.. 1992. Structure and novel exons of the human tau gene. Biochemistry 31:10626–10633
   PubMed Web of Science ®Google Scholar
• Black, D. L.. 1995. Finding splice sites within a wilderness of RNA. RNA 1:763–771
   PubMedGoogle Scholar
• Black, D. L., Chabot, B., and Steitz, J. A.. 1985. U2 as well as U1 small nuclear ribonucleoproteins are involved in premessenger RNA splicing. Cell 42:737–750
   PubMed Web of Science ®Google Scholar
• Blanchette, M., and Chabot, B.. 1997. A highly stable duplex structure sequesters the 5′ splice site region of hnRNP A1 alternative exon 7B. RNA 3:405–419
   PubMed Web of Science ®Google Scholar
• Chabot, B.. Synthesis and purification of RNA substrates RNA processing Hames, D., and Higgins, S. I:1–29 Oxford University Press, Oxford, United Kingdom
   Google Scholar
• Clark, L. N., Poorkaj, P., Wszolek, Z., Geschwind, D. H., Nasreddine, Z. S., Miller, B., Li, D., Payami, H., Awert, F., Markopoulou, K., Andreadis, A., D'Souza, I., Lee, V. M., Reed, L., Trojanowski, J. Q., Zhukareva, V., Bird, T., Schellenberg, G., and Wilhelmsen, K. C.. 1998. 1994. 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
   PubMed Web of Science ®Google Scholar
• Côté, J., and Chabot, B.. 1997. Natural base-pairing interactions between 5′ splice site and branch site sequences affect mammalian 5′ splice site selection. RNA 3:1248–1261
   PubMedGoogle Scholar
• Dignam, J. D., Lebovitz, R. M., and Roeder, R. G.. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475–1489
   PubMed Web of Science ®Google Scholar
• D'Souza, I., Poorkaj, P., Hong, M., Nochlin, D., Lee, V. M., Bird, T. D., and Schellenberg, G. D.. 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
   PubMed Web of Science ®Google Scholar
• Eng, F. J., and Warner, J. R.. 1991. Structural basis for the regulation of splicing of a yeast messenger RNA. Cell 65:797–804
   PubMed Web of Science ®Google Scholar
• Eperon, I. C., Ireland, D. C., Smith, R. A., Mayeda, A., and Krainer, A. R.. 1993. Pathways for selection of 5′ splice sites by U1 snRNPs and SF2/ASF. EMBO J. 12:3607–3617
   PubMedGoogle Scholar
• Eperon, L. P., Estibeiro, J. P., and Eperon, I. C.. 1986. The role of nucleotide sequences in splice site selection in eukaryotic pre-messenger RNA. Nature 324:280–282
   PubMed Web of Science ®Google Scholar
• Eperon, L. P., Graham, I. R., Griffiths, A. D., and Eperon, I. C.. 1988. Effects of RNA secondary structure on alternative splicing of pre-mRNA: is folding limited to a region behind the transcribing RNA polymerase? Cell 54:393–401
   PubMed Web of Science ®Google Scholar
• Foster, N. L., Wilhelmsen, K., Sima, A. A., Jones, M. Z., D'Amato, C. J., and Gilman, S.. 1997. Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus conference. Ann. Neurol. 41:706–715
   PubMed Web of Science ®Google Scholar
• Goedert, M.. 1998. Neurofibrillary pathology of Alzheimer's disease and other tauopathies. Prog. Brain Res. 117:287–306
   PubMedGoogle Scholar
• Goedert, M., Crowther, R. A., and Spillantini, M. G.. 1998. Tau mutations cause frontotemporal dementias. Neuron 21:955–958
   PubMed Web of Science ®Google Scholar
• Goedert, M., Spillantini, M. G., and Crowther, R. A.. 1991. Tau proteins and neurofibrillary degeneration. Brain Pathol. 1:279–286
   PubMedGoogle Scholar
• Goedert, M., Spillantini, M. G., and Davies, S. W.. 1998. Filamentous nerve cell inclusions in neurodegenerative diseases. Curr. Opin. Neurobiol. 8:619–632
   PubMed Web of Science ®Google Scholar
• Goedert, M., Spillantini, M. G., Jakes, R., Rutherford, D., and Crowther, R. A.. 1989. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3:519–526
   PubMed Web of Science ®Google Scholar
• Goguel, V., Liao, X. L., Rymond, B. C., and Rosbash, M.. 1991. U1 snRNP can influence 3′-splice site selection as well as 5′-splice site selection. Genes Dev. 5:1430–1438
   PubMedGoogle Scholar
• Goguel, V., and Rosbash, M.. 1993. Splice site choice and splicing efficiency are positively influenced by pre-mRNA intramolecular base pairing in yeast. Cell 72:893–901
   PubMed Web of Science ®Google Scholar
• Goguel, V., Wang, Y., and Rosbash, M.. 1993. Short artificial hairpins sequester splicing signals and inhibit yeast pre-mRNA splicing. Mol. Cell. Biol. 13:6841–6848
   PubMedGoogle Scholar
• Grover, A., Houlden, H., Baker, M., Adamson, J., Lewis, J., Prihar, G., Pickering-Brown, S., Duff, K., and Hutton, M.. 1999. 5′ splice site 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
   PubMed Web of Science ®Google Scholar
• Hasegawa, M., Smith, M. J., and Goedert, M.. 1998. Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett. 437:207–210
   PubMed Web of Science ®Google Scholar
• Hasegawa, M., Smith, M. J., Iijima, M., Tabira, T., and Goedert, M.. 1999. FTDP-17 mutations N279K and S305N in tau produce increased splicing of exon 10. FEBS Lett. 443:93–96
   PubMedGoogle Scholar
• Hirokawa, N.. 1998. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519–526
   PubMed Web of Science ®Google Scholar
• Hirokawa, N.. 1994. Microtubule organization and dynamics dependent on microtubule-associated proteins. Curr. Opin. Cell Biol. 6:74–81
   PubMedGoogle Scholar
• Hodges, D., and Bernstein, S. I.. 1994. Genetic and biochemical analysis of alternative RNA splicing. Adv. Genet. 31:207–281
   PubMedGoogle Scholar
• Hong, M., Zhukareva, V., Vogelsberg-Ragaglia, V., Wszolek, Z., Reed, L., Miller, B. I., Geschwind, D. H., Bird, T. D., McKeel, D., Goate, A., Morris, J. C., Wilhelmsen, K. C., Schellenberg, G. D., Trojanowski, J. Q., and Lee, V. M.. 1998. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282:1914–1917
   PubMed Web of Science ®Google Scholar
• Hutton, M., Lendon, C. L., 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, R. C., Stevens, M., de Graaff, E., Wauters, E., van Baren, J., Hillebrand, M., Joosse, M., Kwon, J. M., Nowotny, P., Heutink, P. et al. 1998. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702–705
   PubMed Web of Science ®Google Scholar
• Iijima, M., Tabira, T., Poorkaj, P., Schellenberg, G. D., Trojanowski, J. Q., Lee, V. M., Schmidt, M. L., Takahashi, K., Nabika, T., Matsumoto, T., Yamashita, Y., Yoshioka, S., and Ishino, H.. 1999. A distinct familial presenile dementia with a novel missense mutation in the tau gene. Neuroreport 10:497–501
   PubMedGoogle Scholar
• Ishihara, T., Hong, M., Zhang, B., Nakagawa, Y., Lee, M. K., Trojanowski, J. Q., and Lee, V. M.. 1999. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24:751–762
   PubMedGoogle Scholar
• Jiang, Z., Zhang, W., Rao, Y., and Wu, J. Y.. 1998. Regulation of Ich-1 pre-mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl. Acad. Sci. USA 95:9155–9160
   PubMedGoogle Scholar
• Kohtz, J. D., Jamison, S. F., Will, C. L., Zuo, P., Luhrmann, R., Garcia-Blanco, M. A., and Manley, J. L.. 1994. Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 368:119–124
   PubMed Web of Science ®Google Scholar
• Kosik, K. S.. 1990. Tau protein and neurodegeneration. Mol. Neurobiol. 4:171–179
   PubMedGoogle Scholar
• Kramer, A.. 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65:367–409
   PubMed Web of Science ®Google Scholar
• Kramer, A., Frick, M., and Keller, W.. 1987. Separation of multiple components of HeLa cell nuclear extracts required for pre-messenger RNA splicing. J. Biol. Chem. 262:17630–17640
   PubMedGoogle Scholar
• Kramer, A., and Keller, W.. 1990. Preparation and fractionation of mammalian extracts active in pre-mRNA splicing. Methods Enzymol. 181:3–19
   PubMedGoogle Scholar
• Kuo, H. C., Nasim, F. H., and Grabowski, P. J.. 1991. Control of alternative splicing by the differential binding of U1 small nuclear ribonucleoprotein particle. Science 251:1045–1050
   PubMed Web of Science ®Google Scholar
• Lee, G., Neve, R. L., and Kosik, K. S.. 1989. The microtubule binding domain of tau protein. Neuron 2:1615–1624
   PubMed Web of Science ®Google Scholar
• Lee, V. M., and Trojanowski, J. Q.. 1992. The disordered neuronal cytoskeleton in Alzheimer's disease. Curr. Opin. Neurobiol. 2:653–656
   PubMed Web of Science ®Google Scholar
• Lin, C. L., Bristol, L. A., Jin, L., Dykes-Hoberg, M., Crawford, T., Clawson, L., and Rothstein, J. D.. 1998. Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20:589–602
   PubMed Web of Science ®Google Scholar
• Mandelkow, E., and Mandelkow, E. M.. 1995. Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7:72–81
   PubMed Web of Science ®Google Scholar
• Mandelkow, E. M., Biernat, J., Drewes, G., Gustke, N., Trinczek, B., and Mandelkow, E.. 1995. Tau domains, phosphorylation, and interactions with microtubules. Neurobiol. Aging 16:355–363
   PubMed Web of Science ®Google Scholar
• Mayeda, A., and Krainer, A. R.. Mammalian in vitro splicing assays. 1997 Methods Mol. Biol.
   Google Scholar
• Moore, M. J., Query, C. C., and Sharp, P. A.. 1993. Splicing of precursors to messenger RNAs by the spliceosome RNA world. Gesteland, R., and Atkins, J. 1–30 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
   Google Scholar
• Mount, S. M.. 1982. A catalogue of splice junction sequences. Nucleic Acids Res. 10:459–472
   PubMed Web of Science ®Google Scholar
• Nakai, K., and Sakamoto, H.. 1994. Construction of a novel database containing aberrant splicing mutations of mammalian genes. Gene 141:171–177
   PubMed Web of Science ®Google Scholar
• Nandabalan, K., Price, L., and Roeder, G. S.. 1993. Mutations in U1 snRNA bypass the requirement for a cell type-specific RNA splicing factor. Cell 73:407–415
   PubMed Web of Science ®Google Scholar
• Poorkaj, P., Bird, T. D., Wijsman, E., Nemens, E., Garruto, R. M., Anderson, L., Andreadis, A., Wiederholt, W. C., Raskind, M., and Schellenberg, G. D.. 1998. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann. Neurol. 43:815–825 (Erratum, 44:428.)
   PubMed Web of Science ®Google Scholar
• Puig, O., Gottschalk, A., Fabrizio, P., and Seraphin, B.. 1999. Interaction of the U1 snRNP with nonconserved intronic sequences affects 5′ splice site selection. Genes Dev. 13:581–592
   PubMedGoogle Scholar
• Reed, R.. 1996. Initial splice-site recognition and pairing during pre-mRNA splicing. Curr. Opin. Genet. Dev. 6:215–220
   PubMed Web of Science ®Google Scholar
• Reyes, J. L., Gustafson, E. H., Luo, H. R., Moore, M. J., and Konarska, M. M.. 1999. The C-terminal region of hPrp8 interacts with the conserved GU dinucleotide at the 5′ splice site. RNA 5:206–220
   PubMedGoogle Scholar
• Reyes, J. L., Kois, P., Konforti, B. B., and Konarska, M. M.. 1996. The canonical GU dinucleotide at the 5′ splice site is recognized by p220 of the U5 snRNP within the spliceosome. RNA 2:213–225
   PubMedGoogle Scholar
• Seiwert, S. D., and Steitz, J. A.. 1993. Uncoupling two functions of the U1 small nuclear ribonucleoprotein particle during in vitro splicing. Mol. Cell. Biol. 13:3134–3145
   Google Scholar
• Senapathy, P., Shapiro, M. B., and Harris, N. L.. 1990. Splice junctions, branch point sites, and exons: sequence statistics, identification, and applications to genome project. Methods Enzymol. 183:252–278
   PubMed Web of Science ®Google Scholar
• Sirand-Pugnet, P., Durosay, P., Brody, E., and Marie, J.. 1995. An intronic (A/U)GGG repeat enhances the splicing of an alternative intron of the chicken beta-tropomyosin pre-mRNA. Nucleic Acids Res. 23:3501–3507
   PubMedGoogle Scholar
• Sirand-Pugnet, P., Durosay, P., Clouet, O., Brody, E., and Marie, J.. 1995. beta-Tropomyosin pre-mRNA folding around a muscle-specific exon interferes with several steps of spliceosome assembly. J. Mol. Biol. 251:591–602
   PubMedGoogle Scholar
• Solnick, D.. 1985. Alternative splicing caused by RNA secondary structure. Cell 43:667–676
   PubMed Web of Science ®Google Scholar
• Solnick, D., and Lee, S. I.. 1987. Amount of RNA secondary structure required to induce an alternative splice. Mol. Cell. Biol. 7:3194–3198
   PubMed Web of Science ®Google Scholar
• Spillantini, M. G., and Goedert, M.. 1998. Tau protein pathology in neurodegenerative diseases. Trends Neurosci. 21:428–433
   PubMed Web of Science ®Google Scholar
• Spillantini, M. G., Goedert, M., Crowther, R. A., Murrell, J. R., Farlow, M. R., and Ghetti, B.. 1997. Familial multiple system tauopathy with presenile dementia: a disease with abundant neuronal and glial tau filaments. Proc. Natl. Acad. Sci. USA 94:4113–4118
   PubMed Web of Science ®Google Scholar
• Spillantini, M. G., Murrell, J. R., Goedert, M., Farlow, M. R., Klug, A., and Ghetti, B.. 1998. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. USA 95:7737–7741
   PubMed Web of Science ®Google Scholar
• Teigelkamp, S., Newman, A. J., and Beggs, J. D.. 1995. Extensive interactions of PRP8 protein with the 5′ and 3′ splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J. 14:2602–2612
   PubMed Web of Science ®Google Scholar
• Varani, L., Hasegawa, M., Spillantini, M. G., Smith, M. J., Murrell, J. R., Ghetti, B., Klug, A., Goedert, M., and Varani, G.. 1999. Structure of tau exon 10 splicing regulatory element RNA and destabilization by mutations of frontotemporal dementia and parkinsonism linked to chromosome 17. Proc. Natl. Acad. Sci. USA 96:8229–8234
   PubMed Web of Science ®Google Scholar
• Vilardell, J., and Warner, J. R.. 1994. Regulation of splicing at an intermediate step in the formation of the spliceosome. Genes Dev. 8:211–220
   PubMed Web of Science ®Google Scholar
• Wu, J. Y., and Maniatis, T.. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75:1061–1070
   PubMed Web of Science ®Google Scholar
• Zhang, W. J., and Wu, J. Y.. 1996. Functional properties of p54, a novel SR protein active in constitutive and alternative splicing. Mol. Cell. Biol. 16:5400–5408
   PubMed Web of Science ®Google Scholar
• Zuo, P., and Manley, J. L.. 1994. The human splicing factor ASF/SF2 can specifically recognize pre-mRNA 5′ splice sites. Proc. Natl. Acad. Sci. USA 91:3363–3367
   PubMedGoogle Scholar