Rbm20 regulates titin alternative splicing as a splicing repressor

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2659-2672

  Li, Shijun ^a   Guo, Wei ^a   Dewey, Colin N ^b   Greaser, Marion L ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; MESSENGER RNA PRECURSOR; PROTEIN RBM20; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXON SHUFFLING; EXON SKIPPING; GENE; GENE CONTROL; GENE REPRESSION; INTRON RETENTION; MOLECULAR MECHANICS; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; RNA PROCESSING; TITIN GENE;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE; CELL NUCLEUS; EXONS; HEART; MUSCLE PROTEINS; MYOCYTES, CARDIAC; PROTEIN ISOFORMS; PROTEIN KINASES; RATS; RNA SPLICE SITES; RNA-BINDING PROTEINS;

EID: 84876353525     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1362     Document Type: Article

References (39)

1. Bang, M.L., Centner, T., Fornoff, F., Geach, A.J., Gotthardt, M., McNabb, M., Witt, C.C., Labeit, D., Gregorio, C.C., Granzier, H. et al. (2001) The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res., 89, 1065-1072.
2. Labeit, S. and Kolmerer, B. (1995) Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science, 270, 293-296.
3. Maruyama, K., Kimura, S., Yoshidomi, H., Sawada, H. and Kikuchi, M. (1984) Molecular size and shape of beta-connection, an elastic protein of striated muscle. J. Biochem., 95, 1423-1433.
4. Trinick, J., Knight, P. and Whiting, A. (1984) Purification and properties of native titin. J. Mol. Biol., 180, 331-356.
5. Wang, K., McCarter, R., Wright, J., Beverly, J. and Ramirez- Mitchell, R. (1991) Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension. Proc. Natl Acad. Sci. USA, 88, 7101-7105.
6. Fürst, D.O., Osborn, M., Nave, R. and Weber, K. (1988) The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J. Cell Biol., 106, 1563-1572.
7. Gregorio, C.C., Trombitás, K., Centner, T., Kolmerer, B., Stier, G., Kunke, K., Suzuki, K., Obermayr, F., Herrmann, B., Granzier, H. et al. (1998) The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J. Cell Biol., 143, 1013-1027.
8. Obermann, W.M., Gautel, M., Weber, K. and Fürst, D.O. (1997) Molecular structure of the sarcomeric M band: mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesin. EMBO J., 16, 211-220.
9. Greaser, M.L., Berri, M., Warren, C.M. and Mozdziak, P.E. (2002) Species variations in cDNA sequence and exon splicing patterns in the extensible I-band region of cardiac titin: relation to passive tension. J. Muscle Res. Cell Motil., 23, 473-482.
10. Funatsu, T., Higuchi, H. and Ishiwata, S. (1990) Elastic filaments in skeletal muscle revealed by selective removal of thin filaments with plasma gelsolin. J. Cell Biol., 110, 53-62.
11. Granzier, H.L. and Irving, T.C. (1995) Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J., 68, 1027-1044.
12. Horowits, R. and Podolsky, R.J. (1987) The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: evidence for the role of titin filaments. J. Cell Biol., 105, 2217-2223.
13. Tskhovrebova, L. and Trinick, J. (2003) Titin: properties and family relationships. Nat. Rev. Mol. Cell Biol., 4, 679-689.
14. Ohtsuka, H., Yajima, H., Maruyama, K. and Kimura, S. (1997) Binding of the N-terminal 63 kDa portion of connectin/titin to alpha-actinin as revealed by the yeast two-hybrid system. FEBS Lett., 401, 65-67.
15. Sorimachi, H., Freiburg, A., Kolmerer, B., Ishiura, S., Stier, G., Gregorio, C.C., Labeit, D., Linke, W.A., Suzuki, K. and Labeit, S. (1997) Tissue-specific expression and alpha-actinin binding properties of the Z-disc titin: implications for the nature of vertebrate Z-discs. J. Mol. Biol., 270, 688-695.
16. Labeit, S., Gautel, M., Lakey, A. and Trinick, J. (1992) Towards a molecular understanding of titin. EMBO J., 11, 1711-1716.
17. Kruger, M. and Linke, W. (2011) The giant protein titin: a regulatory node that integrates myocyte signaling pathways. J. Biol. Chem., 286, 9905-9912.
18. Freiburg, A., Trombitas, K., Hell, W., Cazorla, O., Fougerousse, F., Centner, T., Kolmerer, B., Witt, C., Beckmann, J.S., Gregorio, C.C. et al. (2000) Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ. Res., 86, 1114-1121.
19. Greaser, M.L., Krzesinski, P.R., Warren, C.M., Kirkpatrick, B., Campbell, K.S. and Moss, R.L. (2005) Developmental changes in rat cardiac titin/connectin: transitions in normal animals and in mutants with a delayed pattern of isoform transition. J. Muscle Res. Cell Motil., 26, 325-332.
20. Ottenheijm, C.A., Knottnerus, A.M., Buck, D., Luo, X., Greer, K., Hoying, A., Labeit, S. and Granzier, H. (2009) Tuning passive mechanics through differential splicing of titin during skeletal muscle development. Biophys. J., 97, 2277-2286.
21. Li, S., Guo, W., Schmitt, B. and Greaser, M.L. (2012) Comprehensive analysis of titin protein isoform and alternative splicing in normal and mutant rats. J. Cell Biochem., 113, 1365-1373.
22. Cazorla, O., Freiburg, A., Helmes, M., Centner, T., McNabb, M., Wu, Y., Trombitás, K., Labeit, S. and Granzier, H. (2000) Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ. Res., 86, 59-67.
23. Makarenko, I., Opitz, C.A., Leake, M.C., Neagoe, C., Kulke, M., Gwathmey, J.K., del Monte, F., Hajjar, R.J. and Linke, W.A. (2004) Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ. Res., 95, 708-716.
24. Nagueh, S.F., Shah, G., Wu, Y., Torre-Amione, G., King, N.M., Lahmers, S., Witt, C.C., Becker, K., Labeit, S. and Granzier, H.L. (2004) Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation, 110, 155-162.
25. Neagoe, C., Kulke, M., del Monte, F., Gwathmey, J.K., de Tombe, P.P., Hajjar, R.J. and Linke, W.A. (2002) Titin isoform switch in ischemic human heart disease. Circulation, 106, 1333-1341.
26. Warren, C.M., Jordan, M.C., Roos, K.P., Krzesinski, P.R. and Greaser, M.L. (2003) Titin isoform expression in normal and hypertensive myocardium. Cardiovasc. Res., 59, 86-94.
27. Williams, L., Howell, N., Pagano, D., Andreka, P., Vertesaljai, M., Pecor, T., Frenneaux, M. and Granzier, H. (2009) Titin isoform expression in aortic stenosis. Clin. Sci. (Lond), 117, 237-242.
28. Greaser, M.L., Warren, C.M., Esbona, K., Guo, W., Duan, Y., Parrish, A.M., Krzesinski, P.R., Norman, H.S., Dunning, S., Fitzsimons, D.P. et al. (2008) Mutation that dramatically alters rat titin isoform expression and cardiomyocyte passive tension. J. Mol. Cell. Cardiol., 44, 983-991.
29. Guo, W., Schafer, S., Greaser, M.L., Radk, M.H., Liss, M., Govindarajan, T., Maatz, H., Schulz, H., Li, S., Parrish, A.M. et al. (2012) RBM20, a gene for hereditary cardiomyopathy, regulates titin splicing. Nat. Med., 18, 766-773.
30. Brauch, K.M., Karst, M.L., Herron, K.J., de Andrade, M., Pellikka, P.A., Rodeheffer, R.J., Michels, V.V. and Olson, T.M. (2009) Mutations in ribonucleic acid binding protein gene cause familial dilated cardiomyopathy. J. Am. Coll. Cardiol., 54, 930-941.
31. Li, D., Morales, A., Gonzalez-Quintana, J., Norton, N., Siegfried, J.D., Hofmeyer, M. and Hershberger, R.E. (2010) Identification of novel mutations in RBM20 in patients with dilated cardiomyopathy. Clin. Transl. Sci., 3, 90-97.
32. Millat, G., Bouvagnet, P., Chevalier, P., Sebbag, L., Dulac, A., Dauphin, C., Jouk, P.S., Delrue, M.A., Thambo, J.B., Le Metayer, P. et al. (2011) Clinical and mutational spectrum in a cohort of 105 unrelated patients with dilated cardiomyopathy. Eur. J. Med. Genet., 54, 570-575.
33. Rampersaud, E., Siegfried, J.D., Norton, N., Li, D., Martin, E. and Hershberger, R.E. (2011) Rare variant mutations identified in pediatric patients with dilated cardiomyopathy. Prog. Pediatr. Cardiol., 31, 39-47.
34. Refaat, M.M., Lubitz, S.A., Makino, S., Islam, Z., Frangiskakis, J.M., Mehdi, H., Gutmann, R., Zhang, M.L., Bloom, H.L., MacRae, C.A. et al. (2012) Genetic variation in the alternative splicing regulator RBM20 is associated with dilated cardiomyopathy. Heart Rhythm, 9, 390-396.
35. Chaumeil, J., Augui, S., Chow, J.C. and Heard, E. (2008) Combined immunofluorescence, RNA fluorescent in situ hybridization, and DNA fluorescent in situ hybridization to study chromatin changes, transcriptional activity, nuclear organization, and X-chromosome inactivation. Methods Mol. Biol., 463, 297-308.
36. Selth, L.A., Gilbert, C. and Svejstrup, J.Q. (2009) RNA immunoprecipitation to determine RNA-protein associations in vivo. Cold Spring Harb. Protoc., 6, pdb.prot5234.
37. Grabowski, P.J. (2005) Splicing-active nuclear extracts from rat brain. Methods, 37, 323-330.
38. Warren, C.M., Krzesinski, P.R. and Greaser, M.L. (2003) Vertical agarose gel electrophoresis and electroblotting of highmolecular- weight proteins. Electrophoresis, 24, 1695-1702.
39. Kameyama, T., Suzuki, H. and Mayeda, A. (2012) Re-splicing of mature mRNA in cancer cells promotes activation of distant weak alternative splice sites. Nucleic Acids Res., 40, 7896-7906.