RNA binding proteins in the regulation of heart development

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 11, 2013, Pages 2467-2478

  Blech Hermoni, Yotam ^a,b   Ladd, Andrea N ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Development; Heart; Morphogenesis; Regulation; RNA binding protein; RNA processing

Indexed keywords

DYSTROGLYCAN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MICRORNA; NEUROTROPHIN 3; RNA BINDING PROTEIN; ROUNDABOUT RECEPTOR; SERINE ARGININE RICH PROTEIN;

ALTERNATIVE RNA SPLICING; ATRIOVENTRICULAR CANAL; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL VIABILITY; CONGENITAL HEART MALFORMATION; CONGESTIVE CARDIOMYOPATHY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; ENDOCARDIAL CUSHION; GENE EXPRESSION; HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE CELL; HUMAN; MATURATION; MORPHOGENESIS; MUSCLE FIBRIL; MUSCLE FUNCTION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIMITIVE STREAK; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TISSUE REPAIR; ANIMAL; CELL LINEAGE; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEART; METABOLISM;

ANIMALS; CARDIOVASCULAR DISEASES; CELL LINEAGE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HUMANS; MORPHOGENESIS; RNA-BINDING PROTEINS;

EID: 84883514228     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.08.008     Document Type: Review

References (189)

1. Y. Adereth, V. Dammai, N. Kose, R. Li, and T. Hsu RNA-dependent integrin alpha3 protein localization regulated by the Muscleblind-like protein MLP1 Nature Cell Biology 7 2005 1240 1247
2. E.G. Ames, M.J. Lawson, A.J. Mackey, and J.W. Holmes Sequencing of mRNA identifies re-expression of fetal splice variants in cardiac hypertrophy Journal of Molecular and Cellular Cardiology 62C 2013 99 107
3. J. Amiel, L. de Pontual, and A. Henrion-Caude miRNA, development and disease Advances in Genetics 80 2012 1 36
4. S. Anant, J. Henderson, D. Mukhopadhyay, N. Navaratnam, S. Kennedy, and J. Min Novel role for RNA-binding protein CUGBP2 in mammalian RNA editing Journal of Biological Chemistry 276 2001 47338 47351
5. H.M. Arthur, and S.D. Bamforth TGFbeta signaling and congenital heart disease: insights from mouse studies Birth Defects Research Part A Clinical and Molecular Teratology 91 2011 423 434
6. G. Ast How did alternative splicing evolve Nature Review Genetics 5 2004 773 782 (Pubitemid 39336361)
7. E.H. Baehrecke who encodes a KH RNA binding protein that functions in muscle development Development 124 1997 1323 1332 (Pubitemid 27190105)
8. N.L. Barbosa-Morais, M. Carmo-Fonseca, and S. Aparicio Systematic genome-wide annotation of spliceosomal proteins reveals differential gene family expansion Genome Research 16 2006 66 77 (Pubitemid 43048935)
9. N.S. Belaguli, W. Zhou, T.H. Trinh, M.W. Majesky, and R.J. Schwartz Dominant negative murine serum response factor: alternative splicing within the activation domain inhibits transactivation of serum response factor binding targets Molecular and Cellular Biology 19 1999 4582 4591 (Pubitemid 29289496)
10. D.S. Berger, and A.N. Ladd Repression of nuclear CELF activity can rescue CELF-regulated alternative splicing defects in skeletal muscle models of myotonic dystrophy PLoS Currents 4 2012 RRN1305
11. C.S. Bland, E.T. Wang, A. Vu, M.P. David, J.C. Castle, and J.M. Johnson Global regulation of alternative splicing during myogenic differentiation Nucleic Acids Research 38 2010 7651 7664
12. Y. Blech-Hermoni, S.J. Stillwagon, and A.N. Ladd Diversity and conservation of CELF1 and CELF2 RNA and protein expression patterns during embryonic development Developmental Dynamics 242 2013 767 777
13. R. Bodmer The gene tinman is required for specification of the heart and visceral muscles in Drosophila Development 118 1993 719 729 (Pubitemid 23232780)
14. P.L. Boutz, P. Stoilov, Q. Li, C.H. Lin, G. Chawla, and K. Ostrow A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons Genes & Development 21 2007 1636 1652 (Pubitemid 47026368)
15. T. Brand Heart development: molecular insights into cardiac specification and early morphogenesis Developmental Biology 258 2003 1 19 (Pubitemid 36637027)
16. R. Brandenberger, H. Wei, S. Zhang, S. Lei, J. Murage, and G.J. Fisk Transcriptome characterization elucidates signaling networks that control human ES cell growth and differentiation Nature Biotechnology 22 2004 707 716 (Pubitemid 38702827)
17. K.M. Brauch, M.L. Karst, K.J. Herron, M. de Andrade, P.A. Pellikka, and R.J. Rodeheffer Mutations in ribonucleic acid binding protein gene cause familial dilated cardiomyopathy Journal of the American College of Cardiology 54 2009 930 941
18. M. Brudno, M. Gelfand, S. Spengler, M. Zorn, I. Dubchak, and J. Conboy Computational analysis of candidate intron regulatory elements for tissue-specific alternative pre-mRNA splicing Nucleic Acids Research 29 2001 2338 2348 (Pubitemid 32514936)
19. C. Burd, and G. Dreyfuss Conserved structures and diversity of functions of RNA-binding proteins Science 265 1994 615 621 (Pubitemid 24268271)
20. E. Chapnik, V. Sasson, R. Blelloch, and E. Hornstein Dgcr8 controls neural crest cells survival in cardiovascular development Developmental Biology 362 2012 50 56
21. N. Charlet-B, R. Savkur, G. Singh, A. Philips, E. Grice, and T. Cooper Loss of the muscle-specific chloride channel in type I myotonic dystrophy lead to misregulated alternative splicing Molecular Cell 10 2002 45 53 (Pubitemid 34879148)
22. A.L. Chateigner-Boutin, and I. Small Organellar RNA editing Wiley Interdisciplinary Reviews RNA 2 2011 493 506
23. H.W. Chen, S.L. Yu, W.J. Chen, P.C. Yang, C.T. Chien, and H.Y. Chou Dynamic changes of gene expression profiles during postnatal development of the heart in mice Heart 90 2004 927 934
24. J. Chen, and D.Z. Wang MicroRNAs in cardiovascular development Journal of Molecular and Cellular Cardiology 52 2012 949 957
25. N. Cloonan, A.R. Forrest, G. Kolle, B.B. Gardiner, G.J. Faulkner, and M.K. Brown Stem cell transcriptome profiling via massive-scale mRNA sequencing Nature Methods 5 2008 613 619 (Pubitemid 351911866)
26. T.A. Cooper Use of minigene systems to dissect alternative splicing elements Methods 37 2005 331 340 (Pubitemid 41682503)
27. D. Das, T.A. Clark, A. Schweitzer, M. Yamamoto, H. Marr, and J. Arribere A correlation with exon expression approach to identify cis-regulatory elements for tissue-specific alternative splicing Nucleic Acids Research 35 2007 4845 4857 (Pubitemid 47250354)
28. B. De Craene, and G. Berx Regulatory networks defining EMT during cancer initiation and progression Nature Reviews Cancer 13 2013 97 110
29. D.M. DeLaughter, L. Saint-Jean, H.S. Baldwin, and J.V. Barnett What chick and mouse models have taught us about the role of the endocardium in congenital heart disease Birth Defects Research Part A Clinical and Molecular Teratology 91 2011 511 525
30. J-H. Ding, X. Xu, D. Yang, P-H. Chu, N. Dalton, and Z. Ye Dilated cardiomyopathy caused by tissue-specific ablation of SC35 in heart EMBO Journal 23 2004 885 896 (Pubitemid 38418755)
31. K.A. Dittmar, P. Jiang, J.W. Park, K. Amirikian, J. Wan, and S. Shen Genome-wide determination of a broad ESRP-regulated posttranscriptional network by high-throughput sequencing Molecular and Cellular Biology 32 2012 1468 1482
32. S.L. Dunwoodie Combinatorial signaling in the heart orchestrates cardiac induction, lineage specification and chamber formation Seminars in Cell & Developmental Biology 18 2007 54 66 (Pubitemid 46330846)
33. B. Engels, S. van't Padje, L. Blonden, L.A. Severijnen, B.A. Oostra, and R. Willemsen Characterization of Fxr1 in Danio rerio; a simple vertebrate model to study costamere development Journal of Experimental Biology 207 2004 3329 3338 (Pubitemid 39348335)
34. C. Fan, Q. Chen, and Q.K. Wang Functional role of transcriptional factor TBX5 in pre-mRNA splicing and Holt-Oram syndrome via association with SC35 The Journal of Biological Chemistry 284 2009 25653 25663
35. M. Fardaei, M. Rogers, H. Thorpe, K. Larkin, M. Hamshere, and P. Harper Three proteins, MBNL, MBLL and MBXL, co-localize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells Human Molecular Genetics 11 2002 805 814 (Pubitemid 34428648)
36. Y. Feng, M.T. Valley, J. Lazar, A.L. Yang, R.T. Bronson, and S. Firestein SRp38 regulates alternative splicing and is required for Ca(2+) handling in the embryonic heart Developmental Cell 16 2009 528 538
37. J.M. Fernandes, J.R. Kinghorn, and I.A. Johnston Characterization of two paralogous muscleblind-like genes from the tiger pufferfish (Takifugu rubripes) Comparative Biochemistry and Physiology Part B, Biochemistry & Molecular Biology 146 2007 180 186 (Pubitemid 46201917)
38. I. Fetka, A. Radeghieri, and T. Bouwmeester Expression of the RNA recognition motif-containing protein SEB-4 during Xenopus embryonic development Mechanisms of Development 94 2000 283 286 (Pubitemid 30332417)
39. T.L. Gallagher, J.A. Arribere, P.A. Geurts, C.R. Exner, K.L. McDonald, and K.K. Dill Rbfox-regulated alternative splicing is critical for zebrafish cardiac and skeletal muscle functions Developmental Biology 359 2011 251 261
40. F.B. Gao, and J.P. Taylor RNA-binding proteins in neurological disease Brain Research 1462 2012 1 2
41. V. Garg, C. Yamagishi, T. Hu, I.S. Kathiriya, H. Yamagishi, and D. Srivastava Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development Developmental Biology 235 2001 62 73 (Pubitemid 32612560)
42. D.P. Gates, L.A. Coonrod, and J.A. Berglund Autoregulated splicing of muscleblind-like 1 (MBNL1) Pre-mRNA The Journal of Biological Chemistry 286 2011 34224 34233
43. W.V. Gerber, S.A. Vokes, N.R. Zearfoss, and P.A. Krieg A role for the RNA-binding protein, hermes, in the regulation of heart development Developmental Biology 247 2002 116 126 (Pubitemid 34681169)
44. W.V. Gerber, T.A. Yatskievych, P.B. Antin, K.M. Correia, R.A. Conlon, and P.A. Krieg The RNA-binding protein gene, hermes, is expressed at high levels in the developing heart Mechanisms of Development 80 1999 77 86 (Pubitemid 29067591)
45. N.D. Glaser, Y.O. Lukyanenko, Y. Wang, G.M. Wilson, and T.B. Rogers JNK activation decreases PP2A regulatory subunit B56alpha expression and mRNA stability and increases AUF1 expression in cardiomyocytes American Journal of Physiology Heart and Circulatory Physiology 291 2006 H1183 H1192
46. T. Glisovic, J.L. Bachorik, J. Yong, and G. Dreyfuss RNA-binding proteins and post-transcriptional gene regulation FEBS Letters 582 2008 1977 1986
47. E.S. Goers, J. Purcell, R.B. Voelker, D.P. Gates, and J.A. Berglund MBNL1 binds GC motifs embedded in pyrimidines to regulate alternative splicing Nucleic Acids Research 38 2010 2467 2484
48. A. Gouble, and D. Morello Synchronous and regulated expression of two AU-binding proteins, AUF1 and HuR, throughout murine development Oncogene 19 2000 5377 5384
49. K.W. Gripp, E. Hopkins, J.J. Johnston, C. Krause, W.B. Dobyns, and L.G. Biesecker Long-term survival in TARP syndrome and confirmation of RBM10 as the disease-causing gene American Journal of Medical Genetics Part A 155A 2011 2516 2520
50. W. Guo, S. Schafer, M.L. Greaser, M.H. Radke, M. Liss, and T. Govindarajan RBM20, a gene for hereditary cardiomyopathy, regulates titin splicing Nature Medicine 18 2012 766 773
51. M.D. Harrell, S. Harbi, J.F. Hoffman, J. Zavadil, and W.A. Coetzee Large-scale analysis of ion channel gene expression in the mouse heart during perinatal development Physiological Genomics 28 2007 273 283 (Pubitemid 46708768)
52. R. Harvey, and N. Rosenthal Heart Development 1999 Academic Press, Inc. San Diego 530
53. T. Ho, M. Charlet-B.N. Poulos, G. Singh, M. Swanson, and T. Cooper Muscleblind proteins regulate alternative splicing The EMBO Journal 23 2004 3103 3112 (Pubitemid 39093604)
54. T.H. Ho, D. Bundman, D.L. Armstrong, and T.A. Cooper Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy Human Molecular Genetics 14 2005 1539 1547 (Pubitemid 40823462)
55. M.E. Huot, N. Bisson, L. Davidovic, R. Mazroui, Y. Labelle, and T. Moss The RNA-binding protein fragile X-related 1 regulates somite formation in Xenopus laevis Molecular Biology of the Cell 16 2005 4350 4361 (Pubitemid 41262902)
56. P. Iakova, G.L. Wang, L. Timchenko, M. Michalak, O.M. Pereira-Smith, and J.R. Smith Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate The EMBO Journal 23 2004 406 417 (Pubitemid 38294505)
57. Y. Jin, H. Suzuki, S. Maegawa, H. Endo, S. Sugano, and K. Hashimoto A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG The EMBO Journal 22 2003 905 912 (Pubitemid 36227792)
58. J.J. Johnston, J.K. Teer, P.F. Cherukuri, N.F. Hansen, S.K. Loftus, and K. Chong Massively parallel sequencing of exons on the X chromosome identifies RBM10 as the gene that causes a syndromic form of cleft palate American Journal of Human Genetics 86 2010 743 748
59. H. Jumaa, G. Wei, and P.J. Nielsen Blastocyst formation is blocked in mouse embryos lacking the splicing factor SRp20 Current Biology 9 1999 899 902 (Pubitemid 29456007)
60. M.J. Justice, and K.K. Hirschi The role of quaking in mammalian embryonic development Advances in Experimental Medicine and Biology 693 2010 82 92
61. A. Kalsotra, K. Wang, P.F. Li, and T.A. Cooper MicroRNAs coordinate an alternative splicing network during mouse postnatal heart development Genes & Development 2010
62. A. Kalsotra, X. Xiao, A.J. Ward, J.C. Castle, J.M. Johnson, and C.B. Burge A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart Proceedings of the National Academy of Sciences of the United States of America 105 2008 20333 20338
63. R.N. Kanadia, K.A. Johnstone, A. Mankodi, C. Lungu, C.A. Thornton, and D. Esson A muscleblind knockout model for myotonic dystrophy Science 302 2003 1978 1980 (Pubitemid 37523508)
64. R.N. Kanadia, J. Shin, Y. Yuan, S.G. Beattie, T.M. Wheeler, and C.A. Thornton Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy Proceedings of the National Academy of Sciences of the United States of America 103 2006 11748 11753 (Pubitemid 44182522)
65. R.N. Kanadia, C.R. Urbinati, V.J. Crusselle, D. Luo, Y.J. Lee, and J.K. Harrison Developmental expression of mouse muscleblind genes Mbnl1, Mbnl2 and Mbnl3 Gene Expression Patterns 3 2003 459 462 (Pubitemid 36950421)
66. O. Kelemen, P. Convertini, Z. Zhang, Y. Wen, M. Shen, and M. Falaleeva Function of alternative splicing Gene 514 2013 1 30
67. A. Keyte, and M.R. Hutson The neural crest in cardiac congenital anomalies Differentiation 84 2012 25 40
68. M.L. Kirby Cardiac Development 2007 Oxford University Press New York
69. S. Kishore, S. Luber, and M. Zavolan Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression Brief Functional Genomics 9 2010 391 404
70. K. Komamura, N. Iwai, K. Kokame, Y. Yasumura, J. Kim, and M. Yamagishi The role of a common TNNT2 polymorphism in cardiac hypertrophy Journal of Human Genetics 49 2004 129 133 (Pubitemid 38506726)
71. T. Kondo, T. Furuta, K. Mitsunaga, T.A. Ebersole, M. Shichiri, and J. Wu Genomic organization and expression analysis of the mouse qkI locus Mammalian Genome 10 1999 662 669 (Pubitemid 29393670)
72. J. Kong, and P. Lasko Translational control in cellular and developmental processes Nature Reviews Genetics 13 2012 383 394
73. S.W. Kong, Y.W. Hu, J.W. Ho, S. Ikeda, S. Polster, and R. John Heart failure-associated changes in RNA splicing of sarcomere genes Circulation: Cardiovascular Genetics 3 2010 138 146
74. M. Koshelev, S. Sarma, R.E. Price, X.H. Wehrens, and T.A. Cooper Heart-specific overexpression of CUGBP1 reproduces functional and molecular abnormalities of myotonic dystrophy type 1 Human Molecular Genetics 19 2010 1066 1075
75. B.P. Kruithof, S.N. Duim, A.T. Moerkamp, and M.J. Goumans TGFbeta and BMP signaling in cardiac cushion formation: lessons from mice and chicken Differentiation 84 2012 89 102
76. H. Kuroyanagi Fox-1 family of RNA-binding proteins Cellular and Molecular Life Sciences 66 2009 3895 3907
77. N.M. Kuyumcu-Martinez, G.S. Wang, and T.A. Cooper Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation Molecular Cell 28 2007 68 78 (Pubitemid 47531966)
78. A. Ladd, M. Stenberg, M. Swanson, and T. Cooper A dynamic balance between activation and repression regulates pre-mRNA alternative splicing during heart development Developmental Dynamics 233 2005 783 793 (Pubitemid 40853454)
79. A. Ladd, G. Taffet, C. Hartley, D. Kearney, and T. Cooper Cardiac-specific repression of CELF activity disrupts alternative splicing and causes cardiomyopathy Molecular and Cellular Biology 25 2005 6267 6278 (Pubitemid 40946574)
80. A.N. Ladd, T.A. Yatskievych, and P.B. Antin Regulation of avian cardiac myogenesis by activin/TGFbeta and bone morphogenetic proteins Developmental Biology 204 1998 407 419 (Pubitemid 29024488)
81. S. Lale, S. Yu, and A. Ahmed Complex congenital heart defects in association with maternal diabetes and partial deletion of the A2BP1 gene Fetal and Pediatric Pathology 30 2011 161 166
82. P. Lasko Gene regulation at the RNA layer: RNA binding proteins in intercellular signaling networks Science Signal Transduction Knowledge Environment 2003 2003 RE6
83. M.H. Lee, and T. Schedl RNA-binding proteins WormBook 2006 1 13
84. K.E. LeMasters, Y. Blech-Hermoni, S.J. Stillwagon, N.A. Vajda, and A.N. Ladd Loss of muscleblind-like 1 promotes invasive mesenchyme formation in endocardial cushions by stimulating autocrine TGFbeta3 BMC Developmental Biology 12 2012 22
85. D. Li, L. Bachinski, and R. Roberts Genomic organization and isoform-specific tissue expression of human NAPOR (CUGBP2) as a candidate gene for familial arrhythmogenic right ventricular dysplasia Genomics 74 2001 396 401
86. D. Li, A. Morales, J. Gonzalez-Quintana, N. Norton, J.D. Siegfried, and M. Hofmeyer Identification of novel mutations in RBM20 in patients with dilated cardiomyopathy Clinical and Translational Science 3 2010 90 97
87. S. Li, W. Guo, C.N. Dewey, and M.L. Greaser Rbm20 regulates titin alternative splicing as a splicing repressor Nucleic Acids Research 41 2013 2659 2672
88. X. Li, J. Wang, and J.L. Manley Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation Genes & Development 19 2005 2705 2714 (Pubitemid 41627937)
89. P. Lichtner, T. Attié-Bitach, S. Schuffenhauer, J. Henwood, P. Bouvagnet, and P. Scambler Expression and mutation analysis of Brunol3, a candidate gene for heart and thymus developmental defects associated with partial monosomy 10p Journal of Molecular Medicine 80 2002 431 442 (Pubitemid 34754209)
90. M.I. Lin, I. Das, G.M. Schwartz, P. Tsoulfas, T. Mikawa, and B.L. Hempstead Trk C receptor signaling regulates cardiac myocyte proliferation during early heart development in vivo Developmental Biology 226 2000 180 191
91. Y.F. Liu, H.Y. Liu, L.C. Tu, C.W. Lin, K.M. Hsiao, and H. Pan Zebrafish muscleblind-like genes: identification, structural features and expression Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology 151 2008 118 124
92. Z.P. Liu, O. Nakagawa, M. Nakagawa, H. Yanagisawa, R. Passier, and J.A. Richardson CHAMP, a novel cardiac-specific helicase regulated by MEF2C Developmental Biology 234 2001 497 509 (Pubitemid 32552674)
93. Z.P. Liu, and E.N. Olson Suppression of proliferation and cardiomyocyte hypertrophy by CHAMP, a cardiac-specific RNA helicase Proceedings of the National Academy of Sciences of the United States of America 99 2002 2043 2048 (Pubitemid 34169011)
94. J.Y. Lu, and R.J. Schneider Tissue distribution of AU-rich mRNA-binding proteins involved in regulation of mRNA decay The Journal of Biological Dhemistry 279 2004 12974 12979 (Pubitemid 38445873)
95. B.M. Lunde, C. Moore, and G. Varani RNA-binding proteins: modular design for efficient function Nature Reviews Molecular Cell Biology 8 2007 479 490 (Pubitemid 46809150)
96. S. Maas Gene regulation through RNA editing Discovery Medicine 10 2010 379 386
97. L.E. Machuca-Tzili, S. Buxton, A. Thorpe, C.M. Timson, P. Wigmore, and P.K. Luther Zebrafish deficient for Muscleblind-like 2 exhibit features of myotonic dystrophy Disease Models & Mechanisms 4 2011 381 392
98. W.R. MacLellan, and M.D. Schneider Genetic dissection of cardiac growth control pathways Annual Review of Physiology 62 2000 289 319 (Pubitemid 30618265)
99. A. Mallela, and K. Nishikura A-to-I editing of protein coding and noncoding RNAs Critical Reviews in Biochemistry and Molecular Biology 47 2012 493 501
100. R. Mango, S. Biocca, F. del Vecchio, F. Clementi, F. Sangiuolo, and F. Amati In vivo and in vitro studies support that a new splicing isoform of OLR1 gene is protective against acute myocardial infarction Circulation Research 97 2005 152 158 (Pubitemid 41033471)
101. T. Maniatis, and B. Tasic Alternative pre-mRNA splicing and proteome expansion in metazoans Nature 418 2002 236 243 (Pubitemid 34773783)
102. S. Maragh, R.A. Miller, S.L. Bessling, D.M. McGaughey, M.W. Wessels, and B. de Graaf Identification of RNA binding motif proteins essential for cardiovascular development BMC Developmental Biology 11 2011 62
103. A. Masuda, H.S. Andersen, T.K. Doktor, T. Okamoto, M. Ito, and B.S. Andresen CUGBP1 and MBNL1 preferentially bind to 3′ UTRs and facilitate mRNA decay Scientific Reports 2 2012 209
104. K. Masuda, B. Marasa, J.L. Martindale, M.K. Halushka, and M. Gorospe Tissue- and age-dependent expression of RNA-binding proteins that influence mRNA turnover and translation Aging 1 2009 681 698
105. A.E. McKee, E. Minet, C. Stern, S. Riahi, C.D. Stiles, and P.A. Silver A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain BMC Developmental Biology 5 2005 14
106. C. Medioni, M. Astier, M. Zmojdzian, K. Jagla, and M. Semeriva Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation The Journal of Cell Biology 182 2008 249 261
107. C. Medioni, K. Mowry, and F. Besse Principles and roles of mRNA localization in animal development Development 139 2012 3263 3276
108. E.J. Mientjes, R. Willemsen, L.L. Kirkpatrick, I.M. Nieuwenhuizen, M. Hoogeveen-Westerveld, and M. Verweij Fxr1 knockout mice show a striated muscle phenotype: implications for Fxr1p function in vivo Human Molecular Genetics 13 2004 1291 1302 (Pubitemid 38961637)
109. R.A. Miller, N. Christoforou, J. Pevsner, A.S. McCallion, and J.D. Gearhart Efficient array-based identification of novel cardiac genes through differentiation of mouse ESCs PLoS One 3 2008 e2176
110. C.M. Misquitta, T. Chen, and A.K. Grover Control of protein expression through mRNA stability in calcium signalling Cell Calcium 40 2006 329 346 (Pubitemid 44307907)
111. C.M. Misquitta, V.R. Iyer, E.S. Werstiuk, and A.K. Grover The role of 3′-untranslated region (3′-UTR) mediated mRNA stability in cardiovascular pathophysiology Molecular and Cellular Biochemistry 224 2001 53 67 (Pubitemid 32962652)
112. A.F. Moorman, and V.M. Christoffels Cardiac chamber formation: development, genes, and evolution Physiological Reviews 83 2003 1223 1267 (Pubitemid 37222272)
113. A.D. Mori, and B.G. Bruneau TBX5 mutations and congenital heart disease: Holt-Oram syndrome revealed Current Opinion in Cardiology 19 2004 211 215 (Pubitemid 38657439)
114. C.F. Mueller, A. Berger, S. Zimmer, V. Tiyerili, and G. Nickenig The heterogenous nuclear riboprotein S1-1 regulates AT1 receptor gene expression via transcriptional and posttranscriptional mechanisms Archives of Biochemistry and Biophysics 488 2009 76 82
115. T.W. Nilsen, and B.R. Graveley Expansion of the eukaryotic proteome by alternative splicing Nature 463 2010 457 463
116. R. Nir, R. Grossman, Z. Paroush, and T. Volk Phosphorylation of the Drosophila melanogaster RNA-binding protein HOW by MAPK/ERK enhances its dimerization and activity PLoS Genetics 8 2012 e1002632
117. H.J. Okano, and R.B. Darnell A hierarchy of Hu RNA binding proteins in developing and adult neurons Journal of Neuroscience 17 1997 3024 3037 (Pubitemid 27175816)
118. K. Ono, Y. Kuwabara, and J. Han MicroRNAs and cardiovascular diseases FEBS Journal 278 2011 1619 1633
119. Q. Pan, O. Shai, L.J. Lee, B.J. Frey, and B.J. Blencowe Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing Nature Genetics 40 2008 1413 1415
120. J.Y. Park, W. Li, D. Zheng, P. Zhai, Y. Zhao, and T. Matsuda Comparative analysis of mRNA isoform expression in cardiac hypertrophy and development reveals multiple post-transcriptional regulatory modules PLoS One 6 2011 e22391
121. M. Pascual, M. Vicente, L. Monferrer, and R. Artero The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing Differentiation 74 2006 65 80 (Pubitemid 43376167)
122. A. Pende, K.D. Tremmel, C.T. DeMaria, B.C. Blaxall, W.A. Minobe, and J.A. Sherman Regulation of the mRNA-binding protein AUF1 by activation of the beta-adrenergic receptor signal transduction pathway The Journal of Biological Chemistry 271 1996 8493 8501 (Pubitemid 26108689)
123. N. Perrone-Bizzozero, and F. Bolognani Role of HuD and other RNA-binding proteins in neural development and plasticity Journal of Neuroscience Research 68 2002 121 126 (Pubitemid 34275005)
124. A.D. Person, S.E. Klewer, and R.B. Runyan Cell biology of cardiac cushion development International Review of Cytology 243 2005 287 335 (Pubitemid 41557302)
125. J.K. Pickrell, A.A. Pai, Y. Gilad, and J.K. Pritchard Noisy splicing drives mRNA isoform diversity in human cells PLoS Genetics 6 2010 e1001236
126. K.L. Poon, K.T. Tan, Y.Y. Wei, C.P. Ng, A. Colman, and V. Korzh RNA-binding protein RBM24 is required for sarcomere assembly and heart contractility Cardiovascular Research 94 2012 418 427
127. C.A. Pratt, and K.L. Mowry Taking a cellular road-trip: mRNA transport and anchoring Current Opinion in Cell Biology 25 2013 99 106
128. M. Pritsker, T.T. Doniger, L.C. Kramer, S.E. Westcot, and I.R. Lemischka Diversification of stem cell molecular repertoire by alternative splicing Proceedings of the National Academy of Sciences of the United States of America 102 2005 14290 14295 (Pubitemid 41429691)
129. S.R. Qayyum, S. Webb, R.H. Anderson, F.J. Verbeek, N.A. Brown, and M.K. Richardson Septation and valvar formation in the outflow tract of the embryonic chick heart The Anatomical Record 264 2001 273 283 (Pubitemid 33035468)
130. G.D. Raffel, G.C. Chu, J.L. Jesneck, D.E. Cullen, R.T. Bronson, and O.A. Bernard Ott1 (Rbm15) is essential for placental vascular branching morphogenesis and embryonic development of the heart and spleen Molecular and Cellular Biology 29 2009 333 341
131. J. Rappsilber, U. Ryder, A.I. Lamond, and M. Mann Large-scale proteomic analysis of the human spliceosome Genome Research 12 2002 1231 1245 (Pubitemid 41264425)
132. M.M. Refaat, S.A. Lubitz, S. Makino, Z. Islam, J.M. Frangiskakis, and H. Mehdi Genetic variation in the alternative splicing regulator RBM20 is associated with dilated cardiomyopathy Heart Rhythm 9 2012 390 396
133. L.M. Reinke, Y. Xu, and C. Cheng Snail represses the splicing regulator epithelial splicing regulatory protein 1 to promote epithelial-mesenchymal transition The Journal of Biological Chemistry 287 2012 36435 36442
134. T. Revil, and L.A. Jerome-Majewska During embryogenesis, esrp1 expression is restricted to a subset of epithelial cells and is associated with splicing of a number of developmentally important genes Developmental Dynamics 242 2013 281 290
135. S. Richard, N. Torabi, G.V. Franco, G.A. Tremblay, T. Chen, and G. Vogel Ablation of the Sam68 RNA binding protein protects mice from age-related bone loss PLoS Genetics 1 2005 e74
136. J.J. Rosenthal, and P.H. Seeburg A-to-I RNA editing: effects on proteins key to neural excitability Neuron 74 2012 432 439
137. S.P. Ryder, and J.R. Williamson Specificity of the STAR/GSG domain protein Qk1: implications for the regulation of myelination RNA 10 2004 1449 1458 (Pubitemid 39122115)
138. N. Salomonis, B. Nelson, K. Vranizan, A.R. Pico, K. Hanspers, and A. Kuchinsky Alternative splicing in the differentiation of human embryonic stem cells into cardiac precursors PLoS Computational Biology 5 2009 e1000553
139. N. Salomonis, C.R. Schlieve, L. Pereira, C. Wahlquist, A. Colas, and A.C. Zambon Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation Proceedings of the National Academy of Sciences of the United States of America 107 2010 10514 10519
140. R. Savkur, A. Phillips, and T. Cooper Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy Nature Genetics 29 2001 40 47 (Pubitemid 32801806)
141. D.R. Schoenberg, and L.E. Maquat Regulation of cytoplasmic mRNA decay Nature Reviews Genetics 13 2012 246 259
142. B. Schoser, and L. Timchenko Myotonic dystrophies 1 and 2: complex diseases with complex mechanisms Current Genomics 11 2010 77 90
143. H. Seitz, and P.D. Zamore Rethinking the microprocessor Cell 125 2006 827 829 (Pubitemid 43795190)
144. I.M. Shapiro, A.W. Cheng, N.C. Flytzanis, M. Balsamo, J.S. Condeelis, and M.H. Oktay An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype PLoS Genetics 7 2011 e1002218
145. X. Shen, C. Franzini-Armstrong, J.R. Lopez, L.R. Jones, Y.M. Kobayashi, and Y. Wang Triadins modulate intracellular Ca(2+) homeostasis but are not essential for excitation-contraction coupling in skeletal muscle The Journal of Biological Chemistry 282 2007 37864 37874
146. P.J. Shepard, and K.J. Hertel The SR protein family Genome Biology 10 2009 242
147. H. Shibata, D.P. Huynh, and S.M. Pulst A novel protein with RNA-binding motifs interacts with ataxin-2 Human Molecular Genetics 9 2000 1303 1313 (Pubitemid 30312479)
148. C. Shin, Y. Feng, and J.L. Manley Dephosphorylated SRp38 acts as a splicing repressor in response to heat shock Nature 427 2004 553 558 (Pubitemid 38209114)
149. S. Siedner, M. Kruger, M. Schroeter, D. Metzler, W. Roell, and B.K. Fleischmann Developmental changes in contractility and sarcomeric proteins from the early embryonic to the adult stage in the mouse heart Journal of Physiology 548 2003 493 505 (Pubitemid 36527471)
150. H. Siomi, and G. Dreyfuss RNA-binding proteins as regulators of gene expression Current Opinion in Genetics & Development 7 1997 345 353 (Pubitemid 27292286)
151. M.C. Siomi, H. Siomi, W.H. Sauer, S. Srinivasan, R.L. Nussbaum, and G. Dreyfuss FXR1, an autosomal homolog of the fragile X mental retardation gene The EMBO Journal 14 1995 2401 2408
152. H.K. Song, S.E. Hong, T. Kim, and H. Kim do Deep RNA sequencing reveals novel cardiac transcriptomic signatures for physiological and pathological hypertrophy PLoS One 7 2012 e35552
153. C.W. Sugnet, K. Srinivasan, T.A. Clark, G. O'Brien, M.S. Cline, and H. Wang Unusual intron conservation near tissue-regulated exons found by splicing microarrays PLoS Computational Biology 2 2006 e4
154. L.C. Sutherland, N.D. Rintala-Maki, R.D. White, and C.D. Morin RNA binding motif (RBM) proteins: a novel family of apoptosis modulators Journal of Cellular Biochemistry 94 2005 5 24 (Pubitemid 41420320)
155. F. Terenzi, K.R. Brimacombe, M.S. Penn, and A.N. Ladd CELF-mediated alternative splicing is required for cardiac function during early, but not later, postnatal life Journal of Molecular and Cellular Cardiology 46 2009 395 404
156. F. Terenzi, and A.N. Ladd Conserved developmental alternative splicing of muscleblind-like (MBNL) transcripts regulates MBNL localization and activity RNA Biology 7 2010 43 55
157. N.A. Timchenko, R. Patel, P. Iakova, Z.J. Cai, L. Quan, and L.T. Timchenko Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis Journal of Biological Chemistry 279 2004 13129 13139 (Pubitemid 38445891)
158. L. Twyffels, C. Gueydan, and V. Kruys Shuttling SR proteins: more than splicing factors FEBS Journal 278 2011 3246 3255
159. T. Ueyama, H. Kasahara, T. Ishiwata, N. Yamasaki, and S. Izumo Csm, a cardiac-specific isoform of the RNA helicase Mov10l1, is regulated by Nkx2.5 in embryonic heart The Journal of Biological Chemistry 278 2003 28750 28757 (Pubitemid 36935783)
160. N.A. Vajda, K.R. Brimacombe, K.E. LeMasters, and A.N. Ladd Muscleblind-like 1 is a negative regulator of TGF-beta-dependent epithelial-mesenchymal transition of atrioventricular canal endocardial cells Developmental Dynamics 238 2009 3266 3272
161. S. Van't Padje, B. Chaudhry, L.A. Severijnen, H.C. van der Linde, E.J. Mientjes, and B.A. Oostra Reduction in fragile X related 1 protein causes cardiomyopathy and muscular dystrophy in zebrafish Journal of Experimental Biology 212 2009 2564 2570
162. J.P. Venables, E. Vignal, S. Baghdiguian, P. Fort, and J. Tazi Tissue-specific alternative splicing of Tak1 is conserved in deuterostomes Molecular Biology and Evolution 29 2012 261 269
163. F. Vitelli, M. Morishima, I. Taddei, E.A. Lindsay, and A. Baldini Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways Human Molecular Genetics 11 2002 915 922 (Pubitemid 34449779)
164. M. Wagner, and M.A. Siddiqui Signal transduction in early heart development (II): ventricular chamber specification, trabeculation, and heart valve formation Experimental Biology and Medicine 232 2007 866 880 (Pubitemid 47026792)
165. E.T. Wang, N.A. Cody, S. Jog, M. Biancolella, T.T. Wang, and D.J. Treacy Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins Cell 150 2012 710 724
166. E.T. Wang, R. Sandberg, S. Luo, I. Khrebtukova, L. Zhang, and C. Mayr Alternative isoform regulation in human tissue transcriptomes Nature 456 2008 470 476 (Pubitemid 352759009)
167. H.Y. Wang, X. Xu, J.H. Ding, J.R. Bermingham Jr., and X.D. Fu SC35 plays a role in T cell development and alternative splicing of CD45 Molecular Cell 7 2001 331 342 (Pubitemid 32206501)
168. J. Wang, Y. Takagaki, and J.L. Manley Targeted disruption of an essential vertebrate gene: ASF/SF2 is required for cell viability Genes & Development 10 1996 2588 2599 (Pubitemid 26357225)
169. Z. Wang, M. Gerstein, and M. Snyder RNA-Seq: a revolutionary tool for transcriptomics Nature Reviews Genetics 10 2009 57 63
170. A.J. Ward, M. Rimer, J.M. Killian, J.J. Dowling, and T.A. Cooper CUGBP1 overexpression in mouse skeletal muscle reproduces features of myotonic dystrophy type 1 Human Molecular Genetics 19 2010 3614 3622
171. M.B. Warf, M. Nakamori, C.M. Matthys, C.A. Thornton, and J.A. Berglund Pentamidine reverses the splicing defects associated with myotonic dystrophy Proceedings of the National Academy of Sciences of the United States of America 106 2009 18551 18556
172. C.C. Warzecha, P. Jiang, K. Amirikian, K.A. Dittmar, H. Lu, and S. Shen An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition The EMBO Journal 29 2010 3286 3300
173. C.C. Warzecha, T.K. Sato, B. Nabet, J.B. Hogenesch, and R.P. Carstens ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing Molecular Cell 33 2009 591 601
174. C.C. Warzecha, S. Shen, Y. Xing, and R.P. Carstens The epithelial splicing factors ESRP1 and ESRP2 positively and negatively regulate diverse types of alternative splicing events RNA Biology 6 2009 546 562
175. B.L. Weis, E. Schleiff, and W. Zerges Protein targeting to subcellular organelles via MRNA localization Biochimica et Biophysica Acta 1833 2013 260 273
176. T.M. Wheeler, K. Sobczak, J.D. Lueck, R.J. Osborne, X. Lin, and R.T. Dirksen Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA Science 325 2009 336 339
177. E.J. White, G. Brewer, and G.M. Wilson Post-transcriptional control of gene expression by AUF1: mechanisms, physiological targets, and regulation Biochimica et Biophysica Acta 1829 2013 680 688
178. S.A. Whitman, C. Cover, L. Yu, D.L. Nelson, D.C. Zarnescu, and C.C. Gregorio Desmoplakin and talin2 are novel mRNA targets of fragile X-related protein-1 in cardiac muscle Circulation Research 109 2011 262 271
179. H.P. Wilmore, P.J. McClive, C.A. Smith, and A.H. Sinclair Expression profile of the RNA-binding protein gene hermes during chicken embryonic development Developmental Dynamics 233 2005 1045 1051 (Pubitemid 40853482)
180. H. Wu, S. Sun, K. Tu, Y. Gao, B. Xie, and A.R. Krainer A splicing-independent function of SF2/ASF in microRNA processing Molecular Cell 38 2010 67 77
181. J.I. Wu, R.B. Reed, P.J. Grabowski, and K. Artzt Function of quaking in myelination: regulation of alternative splicing Proceedings of the National Academy of Sciences of the United States of America 99 2002 4233 4238 (Pubitemid 34285969)
182. X. Xu, D. Yang, J.H. Ding, W. Wang, P.H. Chu, and N.D. Dalton ASF/SF2-regulated CaMKIIdelta alternative splicing temporally reprograms excitation-contraction coupling in cardiac muscle Cell 120 2005 59 72 (Pubitemid 40094603)
183. X.Q. Xu, S.Y. Soo, W. Sun, and R. Zweigerdt Global expression profile of highly enriched cardiomyocytes derived from human embryonic stem cells Stem Cells 27 2009 2163 2174
184. M. Yano, Y. Hayakawa-Yano, A. Mele, and R.B. Darnell Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling Neuron 66 2010 848 858
185. T.A. Yatskievych, A.N. Ladd, and P.B. Antin Induction of cardiac myogenesis in avian pregastrula epiblast: the role of the hypoblast and activin Development 124 1997 2561 2570 (Pubitemid 27341756)
186. G.W. Yeo, X. Xu, T.Y. Liang, A.R. Muotri, C.T. Carson, and N.G. Coufal Alternative splicing events identified in human embryonic stem cells and neural progenitors PLoS Computational Biology 3 2007 1951 1967 (Pubitemid 350043410)
187. S. Zaffran, M. Astier, D. Gratecos, and M. Semeriva The held out wings (how) Drosophila gene encodes a putative RNA-binding protein involved in the control of muscular and cardiac activity Development 124 1997 2087 2098 (Pubitemid 27270276)
188. C. Zhang, Z. Zhang, J. Castle, S. Sun, J. Johnson, and A.R. Krainer Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2 Genes & Development 22 2008 2550 2563
189. Z. Zhou, and X.D. Fu Regulation of splicing by SR proteins and SR protein-specific kinases Chromosoma 122 2013 191 207