UG repeats/TDP-43 interactions near 5′ splice sites exert unpredictable effects on splicing modulation

Journal of Molecular Biology

Volumn 415, Issue 1, 2012, Pages 46-60

  Passoni, Monica ^a   De Conti, Laura ^a   Baralle, Marco ^a   Buratti, Emanuele ^a  

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

Author keywords

BRCA1; ETF1; pre mRNA splicing; RNA; RXRG

Indexed keywords

BRCA1 PROTEIN; RETINOID X RECEPTOR GAMMA; TAR DNA BINDING PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; EXON; HUMAN; HUMAN CELL; MUTANT; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN BINDING; REGULATORY SEQUENCE; RNA SPLICING; WILD TYPE;

EID: 84855261305     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.11.003     Document Type: Article

References (83)

1. Lagier-Tourenne, C., Polymenidou, M. & Cleveland, D. W. (2010). TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 19, R46-R64.
2. Geser, F., Martinez-Lage, M., Kwong, L. K., Lee, V. M. & Trojanowski, J. Q. (2009). Amyotrophic lateral sclerosis, frontotemporal dementia and beyond: the TDP-43 diseases. J. Neurol. 256, 1205-1214.
3. Neumann, M., Sampathu, D. M., Kwong, L. K., Truax, A. C., Micsenyi, M. C., Chou, T. T. et al. (2006). Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314, 130-133. (Pubitemid 44547757)
4. Krecic, A. M. & Swanson, M. S. (1999). hnRNP complexes: composition, structure, and function. Curr. Opin. Cell Biol. 11, 363-371. (Pubitemid 29273808)
5. Martinez-Contreras, R., Cloutier, P., Shkreta, L., Fisette, J. F., Revil, T. & Chabot, B. (2007). hnRNP proteins and splicing control. Adv. Exp. Med. Biol. 623, 123-147.
6. He, Y. & Smith, R. (2009). Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B. Cell. Mol. Life Sci. 66, 1239-1256.
7. Prasanth, K. V., Prasanth, S. G., Xuan, Z., Hearn, S., Freier, S. M., Bennett, C. F. et al. (2005). Regulating gene expression through RNA nuclear retention. Cell, 123, 249-263. (Pubitemid 41457215)
8. Dreyfuss, G., Kim, V. N. & Kataoka, N. (2002). Messenger-RNA-binding proteins and the messages they carry. Nat. Rev., Mol. Cell Biol. 3, 195-205.
9. Ou, S. H., Wu, F., Harrich, D., Garcia-Martinez, L. F. & Gaynor, R. B. (1995). Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol. 69, 3584-3596.
10. Lalmansingh, A. S., Urekar, C. J. & Reddi, P. P. (2011). TDP-43 is a transcriptional repressor: the testis-specific mouse acrv1 gene is a TDP-43 target in vivo. J. Biol. Chem. 286, 10970-10982.
11. Fiesel, F. C., Voigt, A., Weber, S. S., Van den Haute, C., Waldenmaier, A., Gorner, K. et al. (2010). Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J. 29, 209-221.
12. Volkening, K., Leystra-Lantz, C., Yang, W., Jaffee, H. & Strong, M. J. (2009). Tar DNA binding protein of 43 kDa (TDP-43), 14-3-3 proteins and copper/zinc superoxide dismutase (SOD1) interact to modulate NFL mRNA stability. Implications for altered RNA processing in amyotrophic lateral sclerosis (ALS). Brain Res. 1305, 168-182.
13. Kim, S. H., Shanware, N. P., Bowler, M. J. & Tibbetts, R. S. (2010). Amyotrophic lateral sclerosis-associated proteins TDP-43 and FUS/TLS function in a common biochemical complex to co-regulate HDAC6 mRNA. J. Biol. Chem. 285, 34097-34105.
14. Buratti, E., De Conti, L., Stuani, C., Romano, M., Baralle, M. & Baralle, F. (2010). Nuclear factor TDP-43 can affect selected microRNA levels. FEBS J. 277, 2268-2281.
15. Buratti, E., Dork, T., Zuccato, E., Pagani, F., Romano, M. & Baralle, F. E. (2001). Nuclear factor TDP-43 and SR proteins promote in vitro and in vivo CFTR exon 9 skipping. EMBO J. 20, 1774-1784. (Pubitemid 32299413)
16. Bose, J. K., Wang, I. F., Hung, L., Tarn, W. Y. & Shen, C. K. (2008). TDP-43 overexpression enhances exon 7 inclusion during the survival of motor neuron premRNA splicing. J. Biol. Chem. 283, 28852-28859.
17. Mercado, P. A., Ayala, Y. M., Romano, M., Buratti, E.& Baralle, F. E. (2005). Depletion of TDP 43 overrides the need for exonic and intronic splicing enhancers in the human apoA-II gene. Nucleic Acids Res. 33, 6000-6010. (Pubitemid 41742619)
18. Dreumont, N., Hardy, S., Behm-Ansmant, I., Kister, L., Branlant, C., Stevenin, J. & Bourgeois, C. F. (2010). Antagonistic factors control the unproductive splicing of SC35 terminal intron. Nucleic Acids Res. 38, 1353-1366.
19. Wang, I. F., Wu, L. S., Chang, H. Y. & Shen, C. K. (2008). TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 105, 797-806.
20. Polymenidou, M., Lagier-Tourenne, C., Hutt, K. R., Huelga, S. C., Moran, J., Liang, T. Y. et al. (2011). Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat. Neurosci. 14, 459-468.
21. Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M. et al. (2011). Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci. 14, 452-458.
22. Sephton, C. F., Cenik, C., Kucukural, A., Dammer, E. B., Cenik, B., Han, Y. et al. (2011). Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J. Biol. Chem. 286, 1204-1215.
23. Xiao, S., Sanelli, T., Dib, S., Sheps, D., Findlater, J., Bilbao, J. et al. (2011). RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol. Cell. Neurosci. 47, 167-180.
24. Kishore, S., Khanna, A., Zhang, Z., Hui, J., Balwierz, P. J., Stefan, M. et al. (2010). The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum. Mol. Genet. 19, 1153-1164.
25. Rabin, S. J., Kim, J. M., Baughn, M., Libby, R. T., Kim, Y. J., Fan, Y. et al. (2010). Sporadic ALS has compartment-specific aberrant exon splicing and altered cell-matrix adhesion biology. Hum. Mol. Genet. 19, 313-328.
26. Ayala, Y. M., Misteli, T. & Baralle, F. E. (2008). TDP-43 regulates retinoblastoma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc. Natl Acad. Sci. USA, 105, 3785-3789. (Pubitemid 351723476)
27. Igaz, L. M., Kwong, L. K., Lee, E. B., Chen-Plotkin, A., Swanson, E., Unger, T. et al. (2011). Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest. 121, 726-738.
28. Chiang, P. M., Ling, J., Jeong, Y. H., Price, D. L., Aja, S. M. & Wong, P. C. (2010). Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Proc. Natl Acad. Sci. USA, 107, 16320-16324.
29. Shan, X., Chiang, P. M., Price, D. L. & Wong, P. C. (2010). Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc. Natl Acad. Sci. USA, 107, 16325-16330.
30. Elden, A. C., Kim, H. J., Hart, M. P., Chen-Plotkin, A. S., Johnson, B. S., Fang, X. et al. (2010). Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature, 466, 1069-1075.
31. Kuo, P. H., Doudeva, L. G., Wang, Y. T., Shen, C. K. & Yuan, H. S. (2009). Structural insights into TDP-43 in nucleic-acid binding and domain interactions. Nucleic Acids Res. 37, 1799-1808.
32. Shiina, Y., Arima, K., Tabunoki, H. & Satoh, J. (2010). TDP-43 dimerizes in human cells in culture. Cell. Mol. Neurobiol. 30, 641-652.
33. Buratti, E. & Baralle, F. E. (2001). Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J. Biol. Chem. 276, 36337-36343.
34. Ayala, Y. M., Pantano, S., D'Ambrogio, A., Buratti, E., Brindisi, A., Marchetti, C. et al. (2005). Human, Drosophila, and C. elegans TDP43: nucleic acid binding properties and splicing regulatory function. J. Mol. Biol. 348, 575-588. (Pubitemid 40515670)
35. Ayala, Y. M., De Conti, L., Avendano-Vazquez, S. E., Dhir, A., Romano, M., D'Ambrogio, A. et al. (2011). TDP-43 regulates its mRNA levels through a negative feedback loop. EMBO J. 30, 277-288.
36. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J. et al. (2001). Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
37. Bayele, H. K., Peyssonnaux, C., Giatromanolaki, A., Arrais-Silva, W. W., Mohamed, H. S., Collins, H. et al. (2007). HIF-1 regulates heritable variation and allele expression phenotypes of the macrophage immune response gene SLC11A1 from a Z-DNA-forming microsatellite. Blood, 110, 3039-3048. (Pubitemid 350006959)
38. Hough, C., Cameron, C. L., Notley, C. R., Brown, C., O'Brien, L., Keightley, A. M. et al. (2008). Influence of a GT repeat element on shear stress responsiveness of the VWF gene promoter. J. Thromb. Haemost. 6, 1183-1190. (Pubitemid 351859129)
39. Gao, P. S., Heller, N. M., Walker, W., Chen, C. H., Moller, M., Plunkett, B. et al. (2004). Variation in dinucleotide (GT) repeat sequence in the first exon of the STAT6 gene is associated with atopic asthma and differentially regulates the promoter activity in vitro. J. Med. Genet. 41, 535-539. (Pubitemid 38932114)
40. Nolan, L. S., Jagutpal, S. S., Cadge, B. A., Woo, P. & Dawson, S. J. (2007). Identification and functional analysis of common sequence variants in the DFNA15 gene, Brn-3c. Gene, 400, 89-97. (Pubitemid 47284736)
41. Gonzalez, A. A., Carvajal, C. A., Riquelme, E., Krall, P. M., Munoz, C. R., Mosso, L. M. et al. (2007). A polymorphic GT short tandem repeat affecting beta-ENaC mRNA expression is associated with low renin essential hypertension. Am. J. Hypertens. 20, 800-806. (Pubitemid 46936177)
42. Gau, B. H., Chen, T. M., Shih, Y. H. & Sun, H. S. (2011). FUBP3 interacts with FGF9 3′ microsatellite and positively regulates FGF9 translation. Nucleic Acids Res. 39, 3582-3593.
43. Omi, K., Ohashi, J., Patarapotikul, J., Hananantachai, H., Naka, I., Looareesuwan, S. & Tokunaga, K. (2003). CD36 polymorphism is associated with protection from cerebral malaria. Am. J. Hum. Genet. 72, 364-374. (Pubitemid 36194245)
44. 2+ exchanger intron 2 activates splicing. Eur. J. Biochem. 268, 1076-1083.
45. Kornblihtt, A. R. (2005). Promoter usage and alternative splicing. Curr. Opin. Cell Biol. 17, 262-268.
46. Buratti, E. & Baralle, F. E. (2004). Influence of RNA secondary structure on the pre-mRNA splicing process. Mol. Cell. Biol. 24, 10505-10514. (Pubitemid 39603113)
47. McManus, C. J. & Graveley, B. R. (2011). RNA structure and the mechanisms of alternative splicing. Curr. Opin. Genet. Dev. 21, 373-379.
48. Han, J., Xiong, J., Wang, D. & Fu, X. D. (2011). PremRNA splicing: where and when in the nucleus. Trends Cell Biol. 21, 336-343.
49. Luco, R. F., Allo, M., Schor, I. E., Kornblihtt, A. R. & Misteli, T. (2011). Epigenetics in alternative premRNA splicing. Cell, 144, 16-26.
50. Hnilicova, J. & Stanek, D. (2011). Where splicing joins chromatin. Nucleus, 2, 182-188.
51. Blaustein, M., Pelisch, F. & Srebrow, A. (2007). Signals, pathways and splicing regulation. Int. J. Biochem. Cell Biol. 39, 2031-2048. (Pubitemid 47376826)
52. Wang, Z., Rolish, M. E., Yeo, G., Tung, V., Mawson, M. & Burge, C. B. (2004). Systematic identification and analysis of exonic splicing silencers. Cell, 119, 831-845. (Pubitemid 40017689)
53. Zhang, X. H. & Chasin, L. A. (2004). Computational definition of sequence motifs governing constitutive exon splicing. Genes Dev. 18, 1241-1250. (Pubitemid 38720592)
54. Buratti, E., Chivers, M., Kralovicova, J., Romano, M., Baralle, M., Krainer, A. R. & Vorechovsky, I. (2007). Aberrant 5′ splice sites in human disease genes: mutation pattern, nucleotide structure and comparison of computational tools that predict their utilization. Nucleic Acids Res. 35, 4250-4263. (Pubitemid 47260233)
55. Roca, X., Sachidanandam, R. & Krainer, A. R. (2005). Determinants of the inherent strength of human 5′splice sites. RNA, 11, 683-698. (Pubitemid 40594335)
56. Buratti, E., Brindisi, A., Pagani, F. & Baralle, F. E. (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. (Pubitemid 38669335)
57. Gayther, S. A., Russell, P., Harrington, P., Antoniou, A. C., Easton, D. F. & Ponder, B. A. (1999). The contribution of germline BRCA1 and BRCA2 mutations to familial ovarian cancer: no evidence for other ovarian cancer-susceptibility genes. Am. J. Hum. Genet. 65, 1021-1029. (Pubitemid 30462958)
58. Claes, K., Poppe, B., Machackova, E., Coene, I., Foretova, L., De Paepe, A. & Messiaen, L. (2003). Differentiating pathogenic mutations from polymorphic alterations in the splice sites of BRCA1 and BRCA2. Genes Chromosomes Cancer, 37, 314-320. (Pubitemid 36667570)
59. Buratti, E., Brindisi, A., Giombi, M., Tisminetzky, S., Ayala, Y. M. & Baralle, F. E. (2005). TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through itsC-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J. Biol. Chem. 280, 37572-37584. (Pubitemid 41642366)
60. Dujardin, G., Buratti, E., Charlet-Berguerand, N., Martins de Araujo, M., Mbopda, A., Le Jossic-Corcos, C. et al. (2010). CELF proteins regulate CFTR premRNA splicing: essential role of the divergent domain of ETR-3. Nucleic Acids Res. 38, 7273-7285.
61. Ash, P. E., Zhang, Y. J., Roberts, C. M., Saldi, T., Hutter, H., Buratti, E. et al. (2010). Neurotoxic effects of TDP-43 overexpression in C. elegans. Hum. Mol. Genet. 19, 3206-3218.
62. D'Ambrogio, A., Buratti, E., Stuani, C., Guarnaccia, C., Romano, M., Ayala, Y. M. & Baralle, F. E. (2009). Functional mapping of the interaction between TDP-43 and hnRNP A2 in vivo. Nucleic Acids Res. 37, 4116-4126.
63. Hung, L. H., Heiner, M., Hui, J., Schreiner, S., Benes, V. & Bindereif, A. (2008). Diverse roles of hnRNP L in mammalian mRNA processing: a combined microarray and RNAi analysis. RNA, 14, 284-296. (Pubitemid 351171589)
64. Heiner, M., Hui, J., Schreiner, S., Hung, L. H. & Bindereif, A. (2010). HnRNP L-mediated regulation of mammalian alternative splicing by interference with splice site recognition. RNA Biol. 7, 56-64.
65. Hui, J., Hung, L. H., Heiner, M., Schreiner, S., Neumuller, N., Reither, G. et al. (2005). Intronic CA-repeat and CA-rich elements: a new class of regulators of mammalian alternative splicing. EMBO J. 24, 1988-1998. (Pubitemid 40896170)
66. Cheli, Y. & Kunicki, T. J. (2006). hnRNP L regulates differences in expression of mouse integrin α2β1. Blood, 107, 4391-4398. (Pubitemid 43801365)
67. Stamm,S., Riethoven, J. J.,LeTexier,V.,Gopalakrishnan, C., Kumanduri, V., Tang, Y. et al. (2006). ASD: a bioinformatics resource on alternative splicing. Nucleic Acids Res. 34, D46-D55.
68. Thanaraj, T. A., Stamm, S., Clark, F., Riethoven, J. J., Le Texier, V. & Muilu, J. (2004). ASD: the Alternative Splicing Database. Nucleic Acids Res. 32, D64-D69. (Pubitemid 38081606)
69. Disset, A., Michot, C., Harris, A., Buratti, E., Claustres, M. & Tuffery-Giraud, S. (2005). A T3 allele in the CFTR gene exacerbates exon 9 skipping in vas deferens and epididymal cell lines and is associated with Congenital Bilateral Absence of Vas Deferens (CBAVD). Hum. Mutat. 25, 72-81. (Pubitemid 40075916)
70. Huang, C., Xia, P. Y. & Zhou, H. (2010). Sustained expression of TDP-43 and FUS in motor neurons in rodent's lifetime. Int. J. Biol. Sci. 6, 396-406.
71. Alkalaeva, E. Z., Pisarev, A. V., Frolova, L. Y., Kisselev, L. L. & Pestova, T. V. (2006). In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell, 125, 1125-1136. (Pubitemid 43866201)
72. Szanto, A., Narkar, V., Shen, Q., Uray, I. P., Davies, P. J. &Nagy, L. (2004). Retinoid X receptors: X-ploring their (patho)physiological functions. Cell Death Differ. 11, S126-S143. (Pubitemid 40163969)
73. Baralle, D. & Baralle, M. (2005). Splicing in action: assessing disease causing sequence changes. J. Med. Genet. 42, 737-748. (Pubitemid 41475248)
74. Cramer, P., Caceres, J. F., Cazalla, D., Kadener, S., Muro, A. F., Baralle, F. E. & Kornblihtt, A. R. (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. (Pubitemid 29456893)
75. Kornblihtt, A. R. (2007). Coupling transcription and alternative splicing. Adv. Exp. Med. Biol. 623, 175-189.
76. Oesterreich, F. C., Bieberstein, N.&Neugebauer, K. M. (2011). Pause locally, splice globally. Trends Cell Biol. 21, 328-335.
77. Buratti, E., Baralle, M. & Baralle, F. E. (2006). Defective splicing, disease and therapy: searching for master checkpoints in exon definition. Nucleic Acids Res. 34, 3494-3510.
78. Hertel, K. J. (2008). Combinatorial control of exon recognition. J. Biol. Chem. 283, 1211-1215.
79. Matlin, A. J., Clark, F. & Smith, C. W. (2005). Understanding alternative splicing: towards a cellular code. Nat. Rev., Mol. Cell Biol. 6, 386-398. (Pubitemid 40637856)
80. Baralle, M., Baralle, D., De Conti, L., Mattocks, C., Whittaker, J., Knezevich, A. et al. (2003). Identification of a mutation that perturbs NF1, a gene splicing using genomic DNA samples and a minigene assay. J. Med. Genet. 40, 220-222. (Pubitemid 36315397)
81. Deirdre, A., Scadden, J. & Smith, C. W. (1995). Interactions between the terminal bases of mammalian introns are retained in inosine-containing premRNAs. EMBO J. 14, 3236-3246.
82. Reese, M. G., Eeckman, F. H., Kulp, D. & Haussler, D. (1997). Improved splice site detection in Genie. J. Comput. Biol. 4, 311-323. (Pubitemid 27355870)
83. Buratti, E., Baralle, M., De Conti, L., Baralle, D., Romano, M., Ayala, Y. M. & Baralle, F. E. (2004). hnRNP H binding at the 5′ splice site correlates with the pathological effect of two intronic mutations in the NF-1 and TSHβ genes. Nucleic Acids Res. 32, 4224-4236. (Pubitemid 39232295)