Loss of MBNL leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease

Molecular Cell

Volumn 56, Issue 2, 2014, Pages 311-322

  Batra, Ranjan ^a   Charizanis, Konstantinos ^a   Manchanda, Mini ^a   Mohan, Apoorva ^a   Li, Moyi ^a   Finn, Dustin J ^a   Goodwin, Marianne ^a   Zhang, Chaolin ^b   Sobczak, Krzysztof ^c,d   Thornton, Charles A ^c   Swanson, Maurice S ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ELAVL1 PROTEIN; HISTONE DEACETYLASE 5; LUCIFERASE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MUSCLEBLIND LIKE PROTEIN; MUSCLEBLIND LIKE PROTEIN 1; MUSCLEBLIND LIKE PROTEIN 2; MUSCLEBLIND LIKE PROTEIN 3; PROTEIN; RNA; SMALL INTERFERING RNA; SOMATOMEDIN C; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CARRIER PROTEIN; DNA BINDING PROTEIN; MBNL1 PROTEIN, MOUSE; MBNL2 PROTEIN, MOUSE; MBNL3 PROTEIN, MOUSE; MICROSATELLITE DNA; PROTEIN BINDING; RNA BINDING PROTEIN; RNA PRECURSOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELL FRACTIONATION; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYO; GENETIC TRANSFECTION; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MOUSE; MUSCLE DEVELOPMENT; MYOTONIC DYSTROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYADENYLATION; POSTNATAL DEVELOPMENT; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; UBIQUITINATION; 3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; RNA INTERFERENCE; RNA PROCESSING; SKELETAL MUSCLE;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; ANIMALS; BINDING SITES; CARRIER PROTEINS; CELLS, CULTURED; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICROSATELLITE REPEATS; MUSCLE, SKELETAL; MYOTONIC DYSTROPHY; POLYADENYLATION; PROTEIN BINDING; RNA INTERFERENCE; RNA PRECURSORS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

EID: 84922319971     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.08.027     Document Type: Article

References (41)

1. Arnold, E.S., Ling, S.C., Huelga, S.C., Lagier-Tourenne, C., Polymenidou, M., Ditsworth, D., Kordasiewicz, H.B., McAlonis-Downes, M., Platoshyn, O., Parone, P.A., et al. (2013). ALS-linked TDP-43 mutations produce aberrant RNA splicing and adult-onset motor neuron disease without aggregation or loss of nuclear TDP-43. Proc. Natl. Acad. Sci. USA 110, E736-E745.
2. Berg, M.G., Singh, L.N., Younis, I., Liu, Q., Pinto, A.M., Kaida, D., Zhang, Z., Cho, S., Sherrill-Mix, S., Wan, L., and Dreyfuss, G. (2012). U1 snRNP determines mRNA length and regulates isoform expression. Cell 150, 53-64.
3. Chamberlain, C.M., and Ranum, L.P. (2012). Mouse model of muscleblind-like 1 overexpression: skeletal muscle effects and therapeutic promise. Hum. Mol. Genet. 21, 4645-4654.
4. Charizanis, K., Lee, K.Y., Batra, R., Goodwin, M., Zhang, C., Yuan, Y., Shiue, L., Cline, M., Scotti, M.M., Xia, G., et al. (2012). Muscleblind-like 2-mediated alternative splicing in the developing brain and dysregulation in myotonic dystrophy. Neuron 75, 437-450.
5. Cohen, T.J., Waddell, D.S., Barrientos, T., Lu, Z., Feng, G., Cox, G.A., Bodine, S.C., and Yao, T.P. (2007). The histone deacetylase HDAC4 connects neural activity to muscle transcriptional reprogramming. J. Biol. Chem. 282, 33752-33759.
6. Danckwardt, S., Hentze, M.W., and Kulozik, A.E. (2008). 30'end mRNA processing: molecular mechanisms and implications for health and disease. EMBO J. 27, 482-498.
7. de Klerk, E., Venema, A., Anvar, S.Y., Goeman, J.J., Hu, O., Trollet, C., Dickson, G., den Dunnen, J.T., van der Maarel, S.M., Raz, V., and T'Hoen, P.A. (2012). Poly(A) binding protein nuclear 1 levels affect alternative polyadenylation. Nucleic Acids Res. 40, 9089-9101.
8. Derti, A., Garrett-Engele, P., Macisaac, K.D., Stevens, R.C., Sriram, S., Chen, R., Rohl, C.A., Johnson, J.M., and Babak, T. (2012). A quantitative atlas of polyadenylation in five mammals. Genome Res. 22, 1173-1183.
9. Di Giammartino, D.C., Nishida, K., and Manley, J.L. (2011). Mechanisms and consequences of alternative polyadenylation. Mol. Cell 43, 853-866.
10. Du, H., Cline, M.S., Osborne, R.J., Tuttle, D.L., Clark, T.A., Donohue, J.P., Hall, M.P., Shiue, L., Swanson, M.S., Thornton, C.A., and Ares, M., Jr. (2010). Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat. Struct. Mol. Biol. 17, 187-193.
11. Elkon, R., Ugalde, A.P., and Agami, R. (2013). Alternative cleavage and polyadenylation: extent, regulation and function. Nat. Rev. Genet. 14, 496-506.
12. Han, H., Irimia, M., Ross, P.J., Sung, H.K., Alipanahi, B., David, L., Golipour, A., Gabut, M., Michael, I.P., Nachman, E.N., et al. (2013). MBNL proteins repress ES-cell-specific alternative splicing and reprogramming. Nature 498, 241-245.
13. Ho, T.H., Charlet-B, N., Poulos, M.G., Singh, G., Swanson, M.S., and Cooper, T.A. (2004). Muscleblind proteins regulate alternative splicing. EMBO J. 23, 3103-3112.
14. Jenal, M., Elkon, R., Loayza-Puch, F., van Haaften, G., Kühn, U., Menzies, F.M., Oude Vrielink, J.A., Bos, A.J., Drost, J., Rooijers, K., et al. (2012). The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites. Cell 149, 538-553.
15. Jensen, K.B., and Darnell, R.B. (2008). CLIP: crosslinking and immunoprecipitation of in vivo RNA targets of RNA-binding proteins. Methods Mol. Biol. 488, 85-98.
16. Ji, Z., Lee, J.Y., Pan, Z., Jiang, B., and Tian, B. (2009). Progressive lengthening of 3' untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc. Natl. Acad. Sci. USA 106, 7028-7033.
17. Kaida, D., Berg, M.G., Younis, I., Kasim, M., Singh, L.N., Wan, L., and Dreyfuss, G. (2010). U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468, 664-668.
18. Kanadia, R.N., Johnstone, K.A., Mankodi, A., Lungu, C., Thornton, C.A., Esson, D., Timmers, A.M., Hauswirth, W.W., and Swanson, M.S. (2003). A muscleblind knockout model for myotonic dystrophy. Science 302, 1978-
19. Kornblihtt, A.R., Schor, I.E., Alló, M., Dujardin, G., Petrillo, E., and Muñoz, M.J. (2013). Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14, 153-165.
20. Laplante, M., and Sabatini, D.M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293.
21. Lee, K.Y., Li, M., Manchanda, M., Batra, R., Charizanis, K., Mohan, A., Warren, S.A., Chamberlain, C.M., Finn, D., Hong, H., et al. (2013). Compound loss of muscleblind-like function in myotonic dystrophy. EMBO Mol Med 5, 1887-1900.
22. Licatalosi, D.D., Mele, A., Fak, J.J., Ule, J., Kayikci, M., Chi, S.W., Clark, T.A., Schweitzer, A.C., Blume, J.E., Wang, X., et al. (2008). HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456, 464-469.
23. Lin, X., Miller, J.W., Mankodi, A., Kanadia, R.N., Yuan, Y., Moxley, R.T., Swanson, M.S., and Thornton, C.A. (2006). Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum. Mol. Genet. 15, 2087-2097.
24. Mankodi, A., Logigian, E., Callahan, L., McClain, C., White, R., Henderson, D., Krym, M., and Thornton, C.A. (2000). Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 289, 1769-1773.
25. Martianov, I., Ramadass, A., Serra Barros, A., Chow, N., and Akoulitchev, A. (2007). Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445, 666-670.
26. Mayr, C., and Bartel, D.P. (2009). Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-684.
27. Moresi, V., Williams, A.H., Meadows, E., Flynn, J.M., Potthoff, M.J., McAnally, J., Shelton, J.M., Backs, J., Klein, W.H., Richardson, J.A., et al. (2010). Myogenin and class II HDACs control neurogenic muscle atrophy by inducing E3 ubiquitin ligases. Cell 143, 35-45.
28. Naipauer, J., Gattelli, A., Degese, M.S., Slomiansky, V., Wertheimer, E., LaMarre, J., Castilla, L., Abba, M., Kordon, E.C., and Coso, O.A. (2013). The use of alternative polyadenylation sites renders integrin b1 (Itgb1) mRNA isoforms with differential stability during mammary gland development. Biochem. J. 454, 345-357.
29. Nakamori, M., Sobczak, K., Puwanant, A., Welle, S., Eichinger, K., Pandya, S., Dekdebrun, J., Heatwole, C.R., McDermott, M.P., Chen, T., et al. (2013). Splicing biomarkers of disease severity in myotonic dystrophy. Ann. Neurol. 74, 862-872.
30. Pascual, M., Vicente, M., Monferrer, L., and Artero, R. (2006). The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation 74, 65-80.
31. Poulos, M.G., Batra, R., Charizanis, K., and Swanson, M.S. (2011). Developments in RNA splicing and disease. Cold Spring Harb. Perspect. Biol. 3, a000778.
32. Poulos, M.G., Batra, R., Li, M., Yuan, Y., Zhang, C., Darnell, R.B., and Swanson, M.S. (2013). Progressive impairment of muscle regeneration in muscleblind-like 3 isoform knockout mice. Hum. Mol. Genet. 22, 3547-3558.
33. Rau, F., Freyermuth, F., Fugier, C., Villemin, J.P., Fischer, M.C., Jost, B., Dembele, D., Gourdon, G., Nicole, A., Duboc, D., et al. (2011). Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat. Struct. Mol. Biol. 18, 840-845.
34. Singh, R.K., and Cooper, T.A. (2012). Pre-mRNA splicing in disease and therapeutics. Trends Mol. Med. 18, 472-482.
35. Tang, H., Macpherson, P., Marvin, M., Meadows, E., Klein, W.H., Yang, X.J., and Goldman, D. (2009). A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression. Mol. Biol. Cell 20, 1120-1131.
36. Tian, B., and Manley, J.L. (2013). Alternative cleavage and polyadenylation: the long and short of it. Trends Biochem. Sci. 38, 312-320.
37. Wang, E.T., Cody, N.A., Jog, S., Biancolella, M., Wang, T.T., Treacy, D.J., Luo, S., Schroth, G.P., Housman, D.E., Reddy, S., et al. (2012). Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 150, 710-724.
38. Wu, J., Anczuków, O., Krainer, A.R., Zhang, M.Q., and Zhang, C. (2013). OLego: fast and sensitive mapping of spliced mRNA-Seq reads using small seeds. Nucleic Acids Res. 41, 5149-5163.
39. Yao, C., Biesinger, J., Wan, J., Weng, L., Xing, Y., Xie, X., and Shi, Y. (2012). Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc. Natl. Acad. Sci. USA 109, 18773-18778.
40. Zhang, C., and Darnell, R.B. (2011). Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat. Biotechnol. 29, 607-614.
41. Zhang, Z., Pinto, A.M., Wan, L., Wang, W., Berg, M.G., Oliva, I., Singh, L.N., Dengler, C., Wei, Z., and Dreyfuss, G. (2013). Dysregulation of synaptogenesis genes antecedes motor neuron pathology in spinal muscular atrophy. Proc. Natl. Acad. Sci. USA 110, 19348-19353.