Influence of RNA secondary structure on the pre-mRNA splicing process

Molecular and Cellular Biology

Volumn 24, Issue 24, 2004, Pages 10505-10514

  Buratti, Emanuele ^a   Baralle, Francisco E ^a,b  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b NONE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA PRECURSOR; RNA; RNA BINDING PROTEIN; RNA SPLICING FACTOR; UNCLASSIFIED DRUG;

ENHANCER REGION; EXON; HUMAN; IN VIVO STUDY; INTRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA SECONDARY STRUCTURE; RNA SPLICING; RNA STRUCTURE; SHORT SURVEY; SILENCER ELEMENT;

ANIMALS; BASE SEQUENCE; EXONS; HUMANS; INTRONS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; RNA; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; RNA, MESSENGER; RNA, SMALL NUCLEAR; SPLICEOSOMES; TRANSCRIPTION, GENETIC;

EID: 10044274340     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.24.10505-10514.2004     Document Type: Short Survey

References (110)

1. Adams, M. D., D. Z. Rudner, and D. C. Rio. 1996. Biochemistry and regulation of pre-mRNA splicing. Curr. Opin. Cell Biol. 8:331-339.
2. Antson, A. A. 2000. Single-stranded-RNA binding proteins. Curr. Opin. Struct. Biol. 10:87-94.
3. Balvay, L., D. Libri, and M. Y. Fiszman. 1993. Pre-mRNA secondary structure and the regulation of splicing. Bioessays 15:165-169.
4. Baraniak, A. P., E. L. Lasda, E. J. Wagner, and M. A. Garcia-Blanco. 2003. A stem structure in fibroblast growth factor receptor 2 transcripts mediates cell-type-specific splicing by approximating intronic control elements. Mol. Cell. Biol. 23:9327-9337.
5. Black, D. L. 1991. Does steric interference between splice sites block the splicing of a short c-src neuron-specific exon in non-neuronal cells? Genes Dev. 5:389-402.
6. Blanchette, M., and B. Chabot. 1997. A highly stable duplex structure sequesters the 5′ splice site region of hnRNP A1 alternative exon 7B. RNA 3:405-419.
7. Blanchette, M., and B. Chabot. 1999. Modulation of exon skipping by high-affinity hnRNP A1-binding sites and by intron elements that repress splice site utilization. EMBO J. 18:1939-1952.
8. Blencowe, B. J. 2000. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 25:106-110.
9. Brion, P., and E. Westhof. 1997. Hierarchy and dynamics of RNA folding. Annu. Rev. Biophys. Biomol. Struct. 26:113-137.
10. Buckanovich, R. J., and R. B. Darnell. 1997. The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol. Cell. Biol. 17:3194-3201.
11. Buratti, E., A. Brindisi, F. Pagani, and F. E. Baralle. 2004. Nuclear factor TDP-43 binds to the polymorphic TG repeats in CFTR intron 8 and causes skipping of exon 9: a functional link with disease penetrance. Am. J. Hum. Genet. 74:1322-1325.
12. Buratti, E., T. Dork, E. Zuccato, F. Pagani, M. Romano, and F. E. Baralle. 2001. Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 20:1774-1784.
13. Buratti, E., A. F. Muro, M. Giombi, D. Gherbassi, A. Iaconcig, and F. E. Baralle. 2004. RNA folding affects the recruitment of SR proteins by mouse and human polypurinic enhancer elements in the fibronectin EDA exon. Mol. Cell. Biol. 24:1387-1400.
14. Burge, C. B., T. Tuschl, and P. A. Sharp. 1999. Splicing of precursors to mRNAs by the spliceosome. Cold Spring Laboratory Harbor Press, Cold Spring Harbor, N.Y.
15. Cabello-Villegas, J., K. E. Giles, A. M. Soto, P. Yu, A. Mougin, K. L. Beemon, and Y. X. Wang. 2004. Solution structure of the pseudo-5′ splice site of a retroviral splicing suppressor. RNA 10:1388-1398.
16. Caceres, J. F., and A. R. Kornblihtt. 2002. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 18:186-193.
17. Carlson, C. B., O. M. Stephens, and P. A. Beal. 2003. Recognition of double-stranded RNA by proteins and small molecules. Biopolymers 70: 86-102.
18. Cartegni, L., S. L. Chew, and A. R. Krainer. 2002. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 3:285-298.
19. Cartegni, L., and A. R. Krainer. 2002. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 30:377-384.
20. Chabot, B., M. Blanchette, I. Lapierre, and H. La Branche. 1997. An intron element modulating 5′ splice site selection in the hnRNP A1 pre-mRNA interacts with hnRNP A1. Mol. Cell. Biol. 17:1776-1786.
21. Charpentier, B., and M. Rosbash. 1996. Intramolecular structure in yeast introns aids the early steps of in vitro spliceosome assembly. RNA 2:509-522.
22. Chebli, K., R. Gattoni, P. Schmitt, G. Hildwein, and J. Stevenin. 1989. The 216-nucleotide intron of the E1A pre-mRNA contains a hairpin structure that permits utilization of unusually distant branch acceptors. Mol. Cell. Biol. 9:4852-4861.
23. Chen, Y., and W. Stephan. 2003. Compensatory evolution of a precursor messenger RNA secondary structure in the Drosophila melanogaster Adh gene. Proc. Natl. Acad. Sci. USA 100:11499-11504.
24. Chou, M. Y., J. G. Underwood, J. Nikolic, M. H. Luu, and D. L. Black. 2000. Multisite RNA binding and release of polypyrimidine tract binding protein during the regulation of c-src neural-specific splicing. Mol. Cell 5:949-957.
25. Clouet d'Orval, B., Y. d'Aubenton Carafa, P. Sirand-Pugnet, M. Gallego, E. Brody, and J. Marie. 1991. RNA secondary structure repression of a muscle-specific exon in HeLa cell nuclear extracts. Science 252:1823-1828.
26. Coleman, T. P., and J. R. Roesser. 1998. RNA secondary structure: an important cis-element in rat calcitonin/CGRP pre-messenger RNA splicing. Biochemistry 37:15941-15950.
27. Conn, G. L., and D. E. Draper. 1998. RNA structure. Curr. Opin. Struct. Biol. 8:278-285.
28. Cote, J., and B. Chabot. 1997. Natural base-pairing interactions between 5′ splice site and branch site sequences affect mammalian 5′ splice site selection. RNA 3:1248-1261.
29. Cramer, P., J. F. Caceres, D. Cazalla, S. Kadener, A. F. Muro, F. E. Baralle, and A. R. Kornblihtt. 1999. Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Mol. Cell 4:251-258.
30. Cusack, S. 1999. RNA-protein complexes. Curr. Opin. Struct. Biol. 9:66-73.
31. Damgaard, C. K., T. O. Tange, and J. Kjems. 2002. hnRNP A1 controls HIV-1 mRNA splicing through cooperative binding to intron and exon splicing silencers in the context of a conserved secondary structure. RNA 8:1401-1415.
32. Del Gatto, F., A. Plet, M. C. Gesnel, C. Fort, and R. Breathnach. 1997. Multiple interdependent sequence elements control splicing of a fibroblast growth factor receptor 2 alternative exon. Mol. Cell. Biol. 17:5106-5116.
33. Deshler, J. O., and J. J. Rossi. 1991. Unexpected point mutations activate cryptic 3′ splice sites by perturbing a natural secondary structure within a yeast intron. Genes Dev. 5:1252-1263.
34. Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
35. D'Souza, I., P. Poorkaj, M. Hong, D. Nochlin, V. M. Lee, T. D. Bird, and G. D. Schellenberg. 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.
36. Eperon, L. P., I. R. Graham, A. D. Griffiths, and I. C. Eperon. 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.
37. Estes, P. A., N. E. Cooke, and S. A. Liebhaber. 1992. A native RNA secondary structure controls alternative splice-site selection and generates two human growth hormone isoforms. J. Biol. Chem. 267:14902-14908.
38. Faustino, N. A., and T. A. Cooper. 2003. Pre-mRNA splicing and human disease. Genes Dev. 17:419-437.
39. Fontana, W., D. A. Konings, P. F. Stadler, and P. Schuster. 1993. Statistics of RNA secondary structures. Biopolymers 33:1389-1404.
40. Garcia-Blanco, M. A., A. P. Baraniak, and E. L. Lasda. 2004. Alternative splicing in disease and therapy. Nat. Biotechnol. 22:535-546.
41. Gattoni, R., P. Schmitt, and J. Stevenin. 1988. In vitro splicing of adenovirus E1A transcripts: characterization of novel reactions and of multiple branch points abnormally far from the 3′ splice site. Nucleic Acids Res. 16:2389-2409.
42. Goguel, V., and M. Rosbash. 1993. Splice site choice and splicing efficiency are positively influenced by pre-mRNA intramolecular base pairing in yeast. Cell 72:893-901.
43. Goguel, V., Y. Wang, and M. Rosbash. 1993. Short artificial hairpins sequester splicing signals and inhibit yeast pre-mRNA splicing. Mol. Cell. Biol. 13:6841-6848.
44. Graveley, B. R., K. J. Hertel, and T. Maniatis. 1998. A systematic analysis of the factors that determine the strength of pre-mRNA splicing enhancers. EMBO J. 17:6747-6756.
45. Green, M. R. 1991. Biochemical mechanisms of constitutive and regulated pre-mRNA splicing. Annu. Rev. Cell Biol. 7:559-599.
46. Grover, A., H. Houlden, M. Baker, J. Adamson, J. Lewis, G. Prihar, S. Pickering-Brown, K. Duff, and M. Hutton. 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.
47. Halfter, H., and D. Gallwitz. 1988. Impairment of yeast pre-mRNA splicing by potential secondary structure-forming sequences near the conserved branchpoint sequence. Nucleic Acids Res. 16:10413-10423.
48. Hefferon, T. W., J. D. Groman, C. E. Yurk, and G. R. Cutting. 2004. A variable dinucleotide repeat in the CFTR gene contributes to phenotype diversity by forming RNA secondary structures that alter splicing. Proc. Natl. Acad. Sci. USA 101:3504-3509.
49. Hennig, E. E., A. H. Conney, and S. J. Wei. 1995. Characterization of hprt splicing mutations induced by the ultimate carcinogenic metabolite of benzo[a]pyrene in Chinese hamster V-79 cells. Cancer Res. 55:1550-1558.
50. Hoffmeyer, S., P. Nurnberg, H. Ritter, R. Fahsold, W. Leistner, D. Kaufmann, and W. Krone. 1998. Nearby stop codons in exons of the neurofibromatosis type 1 gene are disparate splice effectors. Am. J. Hum. Genet. 62:269-277.
51. Hofmann, Y., C. L. Lorson, S. Stamm, E. J. Androphy, and B. Wirth. 2000. Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc. Natl. Acad. Sci. USA 97:9618-9623.
52. Jacquenet, S., D. Ropers, P. S. Bilodeau, L. Damier, A. Mougin, C. M. Stoltzfus, and C. Branlant. 2001. Conserved stem-loop structures in the HIV-1 RNA region containing the A3 3′ splice site and its cis-regulatory element: possible involvement in RNA splicing. Nucleic Acids Res. 29:464-478.
53. Jiang, Z., J. Cote, J. M. Kwon, A. M. Goate, and J. Y. Wu. 2000. Aberrant splicing of tau pre-mRNA caused by intronic mutations associated with the inherited dementia frontotemporal dementia with parkinsonism linked to chromosome 17. Mol. Cell. Biol. 20:4036-4048.
54. Jurica, M. S., and M. J. Moore. 2003. Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell 12:5-14.
55. Kadener, S., J. P. Fededa, M. Rosbash, and A. R. Kornblihtt. 2002. Regulation of alternative splicing by a transcriptional enhancer through RNA pol II elongation. Proc. Natl. Acad. Sci. USA 99:8185-8190.
56. Kashima, T., and J. L. Manley. 2003. A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy. Nat. Genet. 34:460-463.
57. Katz, L., and C. B. Burge. 2003. Widespread selection for local RNA secondary structure in coding regions of bacterial genes. Genome Res. 13:2042-2051.
58. Kaufmann, D., W. Leistner, P. Kruse, O. Kenner, S. Hoffmeyer, C. Hein, W. Vogel, L. Messiaen, and B. Bartelt. 2002. Aberrant splicing in several human tumors in the tumor suppressor genes neurofibromatosis type 1, neurofibromatosis type 2, and tuberous sclerosis 2. Cancer Res. 62:1503-1509.
59. Kent, O. A., A. Reayi, L. Foong, K. A. Chilibeck, and A. M. MacMillan. 2003. Structuring of the 3′ splice site by U2AF65. J. Biol. Chem. 278:50572-50577.
60. Klaff, P., D. Riesner, and G. Steger. 1996. RNA structure and the regulation of gene expression. Plant Mol. Biol. 32:89-106.
61. Knudsen, B., and J. Hein. 1999. RNA secondary structure prediction using stochastic context-free grammars and evolutionary history. Bioinformatics 15:446-454.
62. Krainer, A. R. 1997. Eukaryotic mRNA processing. Oxford University Press Inc., New York, N.Y.
63. Lamond, A. I. 1993. The spliceosome. Bioessays 15:595-603.
64. Libri, D., A. Piseri, and M. Y. Fiszman. 1991. Tissue-specific splicing in vivo of the beta-tropomyosin gene: dependence on an RNA secondary structure. Science 252:1842-1845.
65. Libri, D., F. Stutz, T. McCarthy, and M. Rosbash. 1995. RNA structural patterns and splicing: molecular basis for an RNA-based enhancer. RNA 1:425-436.
66. Liu, H. X., G. J. Goodall, R. Kole, and W. Filipowicz. 1995. Effects of secondary structure on pre-mRNA splicing: hairpins sequestering the 5′ but not the 3′ splice site inhibit intron processing in Nicotiana plumbaginifolia. EMBO J. 14:377-388.
67. Loeb, D. D., A. A. Mack, and R. Tian. 2002. A secondary structure that contains the 5′ and 3′ splice sites suppresses splicing of duck hepatitis B virus pregenomic RNA. J. Virol. 76:10195-10202.
68. Lopez De Silanes, I., M. Zhan, A. Lal, X. Yang, and M. Gorospe. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101:2987-2992.
69. Maniatis, T., and R. Reed. 2002. An extensive network of coupling among gene expression machines. Nature 416:499-506.
70. Maniatis, T., and B. Tasic. 2002. Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418:236-243.
71. Matsuo, M., H. Nishio, Y. Kitoh, U. Francke, and H. Nakamura. 1992. Partial deletion of a dystrophin gene leads to exon skipping and to loss of an intra-exon hairpin structure from the predicted mRNA precursor. Biochem. Biophys. Res. Commun. 182:495-500.
72. Miriami, E., H. Margalit, and R. Sperling. 2003. Conserved sequence elements associated with exon skipping. Nucleic Acids Res. 31:1974-1983.
73. Mistry, N., W. Harrington, E. Lasda, E. J. Wagner, and M. A. Garcia-Blanco. 2003. Of urchins and men: evolution of an alternative splicing unit in fibroblast growth factor receptor genes. RNA 9:209-217.
74. Miyaso, H., M. Okumura, S. Kondo, S. Higashide, H. Miyajima, and K. Imaizumi. 2003. An intronic splicing enhancer element in survival motor neuron (SMN) pre-mRNA. J. Biol. Chem. 278:15825-15831.
75. Muh, S. J., R. H. Hovhannisyan, and R. P. Carstens. 2002. A non-sequence-specific double-stranded RNA structural element regulates splicing of two mutually exclusive exons of fibroblast growth factor receptor 2 (FGFR2). J. Biol. Chem. 277:50143-50154.
76. Munroe, S. H. 1984. Secondary structure of splice sites in adenovirus mRNA precursors. Nucleic Acids Res. 12:8437-8456.
77. Muro, A. F., M. Caputi, R. Pariyarath, F. Pagani, E. Buratti, and F. E. Baralle. 1999. Regulation of fibronectin EDA exon alternative splicing: possible role of RNA secondary structure for enhancer display. Mol. Cell. Biol. 19:2657-2671.
78. Nagel, R. J., A. M. Lancaster, and A. M. Zahler. 1998. Specific binding of an exonic splicing enhancer by the pre-mRNA splicing factor SRp55. RNA 4:11-23.
79. Nasim, F. U., S. Hutchison, M. Cordeau, and B. Chabot. 2002. High-affinity hnRNP A1 binding sites and duplex-forming inverted repeats have similar effects on 5′ splice site selection in support of a common looping out and repression mechanism. RNA 8:1078-1089.
80. Newman, A. 1987. Specific accessory sequences in Saccharomyces cerevisiae introns control assembly of pre-mRNAs into spliceosomes. EMBO J. 6:3833-3839.
81. Nilsen, T. W. 2003. The spliceosome: the most complex macromolecular machine in the cell? Bioessays 25:1147-1149.
82. Nissim-Rafinia, M., and B. Kerem. 2002. Splicing regulation as a potential genetic modifier. Trends Genet. 18:123-127.
83. Pagani, F., and F. E. Baralle. 2004. Genomic variants in exons and introns: identifying the splicing spoilers. Nat. Rev. Genet. 5:389-395.
84. Patterson, D. J., K. Yasuhara, and W. L. Ruzzo. 2002. Pre-mRNA secondary structure prediction aids splice site prediction. Pac. Symp. Biocomput. 7:223-234.
85. Perez-Canadillas, J. M., and G. Varani. 2001. Recent advances in RNA-protein recognition. Curr. Opin. Struct. Biol. 11:53-58.
86. Proudfoot, N. J., A. Furger, and M. J. Dye. 2002. Integrating mRNA processing with transcription. Cell 108:501-512.
87. Seffens, W., and D. Digby. 1999. mRNAs have greater negative folding free energies than shuffled or codon choice randomized sequences. Nucleic Acids Res. 27:1578-1584.
88. Shen, L. X., J. P. Basilion, and V. P. Stanton, Jr. 1999. Single-nucleotide polymorphisms can cause different structural folds of mRNA. Proc. Natl. Acad. Sci. USA 96:7871-7876.
89. Shi, H., B. E. Hoffman, and J. T. Lis. 1997. A specific RNA hairpin loop structure binds the RNA recognition motifs of the Drosophila SR protein B52. Mol. Cell. Biol. 17:2649-2657.
90. Singh, N. N., E. J. Androphy, and R. N. Singh. 2004. An extended inhibitory context causes skipping of exon 7 of SMN2 in spinal muscular atrophy. Biochem. Biophys. Res. Commun. 315:381-388.
91. Sirand-Pugnet, P., P. Durosay, B. C. Clouet d'Orval, E. Brody, and J. Marie. 1995. beta-tropomyosin pre-mRNA folding around a muscle-specific exon interferes with several steps of spliceosome assembly. J. Mol. Biol. 251:591-602.
92. Smith, C. W., and J. Valcarcel. 2000. Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem. Sci. 25:381-388.
93. Sobczak, K., M. De Mezer, G. Michlewski, J. Krol, and W. J. Krzyzosiak. 2003. RNA structure of trinucleotide repeats associated with human neurological diseases. Nucleic Acids Res. 31:5469-5482.
94. Solnick, D. 1985. Alternative splicing caused by RNA secondary structure. Cell 43:667-676.
95. Solnick, D., and S. I. Lee. 1987. Amount of RNA secondary structure required to induce an alternative splice. Mol. Cell. Biol. 7:3194-3198.
96. Stamm, S. 2002. Signals and their transduction pathways regulating alternative splicing: a new dimension of the human genome. Hum Mol. Genet. 11:2409-2416.
97. Stamm, S., J. Zhu, K. Nakai, P. Stoilov, O. Stoss, and M. Q. Zhang. 2000. An alternative-exon database and its statistical analysis. DNA Cell Biol. 19:739-756.
98. Tu, M., W. Tong, R. Perkins, and C. R. Valentine. 2000. Predicted changes in pre-mRNA secondary structure vary in their association with exon skipping for mutations in exons 2, 4, and 8 of the Hprt gene and exon 51 of the fibrillin gene. Mutat. Res. 432:15-32.
99. Vandenbroucke, I., T. Callens, A. De Paepe, and L. Messiaen. 2002. Complex splicing pattern generates great diversity in human NF1 transcripts. BMC Genomics 3:13.
100. Varani, L., M. Hasegawa, M. G. Spillantini, M. J. Smith, J. R. Murrell, B. Ghetti, A. Klug, M. Goedert, and G. Varani. 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.
101. Varani, L., M. G. Spillantini, M. Goedert, and G. Varani. 2000. Structural basis for recognition of the RNA major groove in the tau exon 10 splicing regulatory element by aminoglycoside antibiotics. Nucleic Acids Res. 28: 710-719.
102. Vilardell, J., and J. R. Warner. 1994. Regulation of splicing at an intermediate step in the formation of the spliceosome. Genes Dev. 8:211-220.
103. Wagner, E. J., and M. A. Garcia-Blanco. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21:3281-3288.
104. Wang, H. Y., I. F. Wang, J. Bose, and C. K. Shen. 2004. Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics 83:130-139.
105. Watakabe, A., K. Inoue, H. Sakamoto, and Y. Shimura. 1989. A secondary structure at the 3′ splice site affects the in vitro splicing reaction of mouse immunoglobulin mu chain pre-mRNAs. Nucleic Acids Res. 17:8159-8169.
106. Wimmer, K., M. Eckart, P. F. Stadler, H. Rehder, and C. Fonatsch. 2000. Three different premature stop codons lead to skipping of exon 7 in neurofibromatosis type I patients. Hum. Mutat. 16:90-91.
107. Workman, C., and A. Krogh. 1999. No evidence that mRNAs have lower folding free energies than random sequences with the same dinucleotide distribution. Nucleic Acids Res. 27:4816-4822.
108. Yasuda, M., J. Takamatsu, I. D'Souza, R. A. Crowther, T. Kawamata, M. Hasegawa, H. Hasegawa, M. G. Spillantini, S. Tanimukai, P. Poorkaj, L. Varani, G. Varani, T. Iwatsubo, M. Goedert, D. G. Schellenberg, and C. Tanaka. 2000. A novel mutation at position +12 in the intron following exon 10 of the tau gene in familial frontotemporal dementia (FTD-Kumamoto). Ann. Neurol. 47:422-429.
109. Zhou, Z., L. J. Licklider, S. P. Gygi, and R. Reed. 2002. Comprehensive proteomic analysis of the human spliceosome. Nature 419:182-185.
110. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.