CELFish ways to modulate mRNA decay

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 6-7, 2013, Pages 695-707

  Vlasova St Louis, Irina ^a   Dickson, Alexa M ^b   Bohjanen, Paul R ^a   Wilusz, Carol J ^b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

CELF (CUGBP ELAV Like Family) protein; Deadenylation; ELAV; GU rich element; MRNA decay; Myotonic dystrophy

Indexed keywords

CHEMOKINE RECEPTOR CCR4; CUGBP ELAV LIKE FAMILY 1 PROTEIN; CUGBP ELAV LIKE FAMILY 2 PROTEIN; CUGBP ELAV LIKE FAMILY 3 PROTEIN; CUGBP ELAV LIKE FAMILY 4 PROTEIN; CUGBP ELAV LIKE FAMILY 5 PROTEIN; CUGBP ELAV LIKE FAMILY 6 PROTEIN; CUGBP ELAV LIKE FAMILY PROTEIN; MESSENGER RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; CELL FUNCTION; DROSOPHILA; GENE EXPRESSION; GENE SEQUENCE; HUMAN; MESSENGER RNA DECAY; MYOTONIC DYSTROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN RNA BINDING; PROTEIN STRUCTURE; REVIEW; RNA DEGRADATION; RNA METABOLISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ALTERNATIVE SPLICING; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-DELTA; DROSOPHILA; EXORIBONUCLEASES; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA PRECURSORS; RNA STABILITY; RNA, MESSENGER;

EID: 84877818604     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.01.001     Document Type: Review

References (176)

1. Antic D., Keene J.D. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation, and posttranscriptional gene expression. Am. J. Hum. Genet. 1997, 61:273-278.
2. Srikantan S., Gorospe M. HuR function in disease. Front. Biosci. 2012, 17:189-205.
3. Timchenko L.T., Timchenko N.A., Caskey C.T., Roberts R. Novel proteins with binding specificity for DNA CTG repeats and RNA CUG repeats: implications for myotonic dystrophy. Hum. Mol. Genet. 1996, 5:115-121.
4. Timchenko L.T., Miller J.W., Timchenko N.A., DeVore D.R., Datar K.V., Lin L., Roberts R., Caskey C.T., Swanson M.S. Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res. 1996, 24:4407-4414.
5. Brook J.D., McCurrach M.E., Harley H.G., Buckler A.J., Church D., Aburatani H., Hunter K., Stanton V.P., Thirion J.P., Hudson T., et al. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3' end of a transcript encoding a protein kinase family member. Cell 1992, 69:385.
6. Sicot G., Gourdon G., Gomes-Pereira M. Myotonic dystrophy, when simple repeats reveal complex pathogenic entities: new findings and future challenges. Hum. Mol. Genet. 2011, 20:R116-R123.
7. Kim-Ha J., Kerr K., Macdonald P.M. Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell 1995, 81:403-412.
8. Paillard L., Omilli F., Legagneux V., Bassez T., Maniey D., Osborne H.B. EDEN and EDEN-BP, a cis element and an associated factor that mediate sequence-specific mRNA deadenylation in Xenopus embryos. EMBO J. 1998, 17:278-287.
9. Ladd A.N., Charlet N., Cooper T.A. The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol. Cell. Biol. 2001, 21:1285-1296.
10. Wagnon J.L., Mahaffey C.L., Sun W., Yang Y., Chao H.T., Frankel W.N. Etiology of a genetically complex seizure disorder in Celf4 mutant mice. Genes Brain Behav. 2011, 10:765-777.
11. Ladd A.N., Nguyen N.H., Malhotra K., Cooper T.A. CELF6, a member of the CELF family of RNA-binding proteins, regulates muscle-specific splicing enhancer-dependent alternative splicing. J. Biol. Chem. 2004, 279:17756-17764.
12. Han J., Cooper T.A. Identification of CELF splicing activation and repression domains in vivo. Nucleic Acids Res. 2005, 33:2769-2780.
13. Tsuda K., Kuwasako K., Takahashi M., Someya T., Inoue M., Terada T., Kobayashi N., Shirouzu M., Kigawa T., Tanaka A., Sugano S., Guntert P., Muto Y., Yokoyama S. Structural basis for the sequence-specific RNA-recognition mechanism of human CUG-BP1 RRM3. Nucleic Acids Res. 2009, 37:5151-5166.
14. Edwards J., Malaurie E., Kondrashov A., Long J., de Moor C.H., Searle M.S., Emsley J. Sequence determinants for the tandem recognition of UGU and CUG rich RNA elements by the two N-terminal RRMs of CELF1. Nucleic Acids Res. 2011, 39:8638-8650.
15. Teplova M., Song J., Gaw H.Y., Teplov A., Patel D.J. Structural insights into RNA recognition by the alternate-splicing regulator CUG-binding protein 1. Structure 2010, 18:1364-1377.
16. Ladd A.N., Cooper T.A. Multiple domains control the subcellular localization and activity of ETR-3, a regulator of nuclear and cytoplasmic RNA processing events. J. Cell Sci. 2004, 117:3519-3529.
17. Gallo J.M., Spickett C. The role of CELF proteins in neurological disorders. RNA Biol. 2010, 7:474-479.
18. Vlasova I.A., Bohjanen P.R. Posttranscriptional regulation of gene networks by GU-rich elements and CELF proteins. RNA Biol. 2008, 5:201-207.
19. Dasgupta T., Ladd A.N. The importance of CELF control: molecular and biological roles of the CUG-BP, Elav-like family of RNA-binding proteins. Wiley Interdiscip. Rev. RNA 2012, 3:104-121.
20. Ladd A.N. CUG-BP, Elav-like family (CELF)-mediated alternative splicing regulation in the brain during health and disease. Mol. Cell. Neurosci. 2012, http://www.ncbi.nlm.nih.gov/pubmed/23247071.
21. Takahashi N., Sasagawa N., Suzuki K., Ishiura S. The CUG-binding protein binds specifically to UG dinucleotide repeats in a yeast three-hybrid system. Biochem. Biophys. Res. Commun. 2000, 277:518-523.
22. Faustino N.A., Cooper T.A. Identification of putative new splicing targets for ETR-3 using sequences identified by systematic evolution of ligands by exponential enrichment. Mol. Cell. Biol. 2005, 25:879-887.
23. Marquis J., Paillard L., Audic Y., Cosson B., Danos O., Le Bec C., Osborne H.B. CUG-BP1/CELF1 requires UGU-rich sequences for high-affinity binding. Biochem. J. 2006, 400:291-301.
24. Mori D., Sasagawa N., Kino Y., Ishiura S. Quantitative analysis of CUG-BP1 binding to RNA repeats. J. Biochem. 2008, 143:377-383.
25. Vlasova I.A., Tahoe N.M., Fan D., Larsson O., Rattenbacher B., Sternjohn J.R., Vasdewani J., Karypis G., Reilly C.S., Bitterman P.B., Bohjanen P.R. Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol. Cell 2008, 29:263-270.
26. Lee J.E., Lee J.Y., Wilusz J., Tian B., Wilusz C.J. Systematic analysis of cis-elements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells. PLoS One 2010, 5:e11201.
27. Rattenbacher B., Beisang D., Wiesner D.L., Jeschke J.C., von Hohenberg M., St Louis-Vlasova I.A., Bohjanen P.R. Analysis of CUGBP1 targets identifies GU-repeat sequences that mediate rapid mRNA decay. Mol. Cell. Biol. 2010, 30:3970-3980.
28. Beisang D., Rattenbacher B., Vlasova-St Louis I.A., Bohjanen P.R. Regulation of CUG-binding protein 1 (CUGBP1) binding to target transcripts upon T cell activation. J. Biol. Chem. 2012, 287:950-960.
29. Graindorge A., Le Tonqueze O., Thuret R., Pollet N., Osborne H.B., Audic Y. Identification of CUG-BP1/EDEN-BP target mRNAs in Xenopus tropicalis. Nucleic Acids Res. 2008, 36:1861-1870.
30. Daughters R.S., Tuttle D.L., Gao W., Ikeda Y., Moseley M.L., Ebner T.J., Swanson M.S., Ranum L.P. RNA gain-of-function in spinocerebellar ataxia type 8. PLoS Genet. 2009, 5:e1000600.
31. Masuda A., Andersen H.S., Doktor T.K., Okamoto T., Ito M., Andresen B.S., Ohno K. CUGBP1 and MBNL1 preferentially bind to 3' UTRs and facilitate mRNA decay. Sci. Rep. 2012, 2:209.
32. Bonnet-Corven S., Audic Y., Omilli F., Osborne H.B. An analysis of the sequence requirements of EDEN-BP for specific RNA binding. Nucleic Acids Res. 2002, 30:4667-4674.
33. Delaunay J., Le Mee G., Ezzeddine N., Labesse G., Terzian C., Capri M., Ait-Ahmed O. The Drosophila Bruno paralogue Bru-3 specifically binds the EDEN translational repression element. Nucleic Acids Res. 2004, 32:3070-3082.
34. Suzuki H., Jin Y., Otani H., Yasuda K., Inoue K. Regulation of alternative splicing of alpha-actinin transcript by Bruno-like proteins. Genes Cells 2002, 7:133-141.
35. Wagnon J.L., Briese M., Sun W., Mahaffey C.L., Curk T., Rot G., Ule J., Frankel W.N. CELF4 regulates translation and local abundance of a vast set of mRNAs, including genes associated with regulation of synaptic function. PLoS Genet. 2012, 8:e1003067.
36. Bae E.J., Kim S.G. Enhanced CCAAT/enhancer-binding protein beta-liver-enriched inhibitory protein production by Oltipraz, which accompanies CUG repeat-binding protein-1 (CUGBP1) RNA-binding protein activation, leads to inhibition of preadipocyte differentiation. Mol. Pharmacol. 2005, 68:660-669.
37. Timchenko N.A., Welm A.L., Lu X., Timchenko L.T. CUG repeat binding protein (CUGBP1) interacts with the 5' region of C/EBPbeta mRNA and regulates translation of C/EBPbeta isoforms. Nucleic Acids Res. 1999, 27:4517-4525.
38. Miyazaki Y., Adachi H., Katsuno M., Minamiyama M., Jiang Y.M., Huang Z., Doi H., Matsumoto S., Kondo N., Iida M., Tohnai G., Tanaka F., Muramatsu S., Sobue G. Viral delivery of miR-196a ameliorates the SBMA phenotype via the silencing of CELF2. Nat. Med. 2012, 18:1136-1141.
39. Zhang L., Lee J.E., Wilusz J., Wilusz C.J. The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for Myotonic Dystrophy. J. Biol. Chem. 2008, 283:22457-22463.
40. Mukhopadhyay D., Houchen C.W., Kennedy S., Dieckgraefe B.K., Anant S. Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol. Cell 2003, 11:113-126.
41. Dembowski J.A., Grabowski P.J. The CUGBP2 splicing factor regulates an ensemble of branchpoints from perimeter binding sites with implications for autoregulation. PLoS Genet. 2009, 5:e1000595.
42. Fox J.T., Stover P.J. Mechanism of the internal ribosome entry site-mediated translation of serine hydroxymethyltransferase 1. J. Biol. Chem. 2009, 284:31085-31096.
43. Horb L.D., Horb M.E. BrunoL1 regulates endoderm proliferation through translational enhancement of cyclin A2 mRNA. Dev. Biol. 2010, 345:156-169.
44. Iakova P., Wang G.L., Timchenko L., Michalak M., Pereira-Smith O.M., Smith J.R., Timchenko N.A. Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate. EMBO J. 2004, 23:406-417.
45. Zheng Y., Miskimins W.K. CUG-binding protein represses translation of p27Kip1 mRNA through its internal ribosomal entry site. RNA Biol. 2011, 8:365-371.
46. Timchenko N.A., Wang G.L., Timchenko L.T. RNA CUG-binding protein 1 increases translation of 20-kDa isoform of CCAAT/enhancer-binding protein beta by interacting with the alpha and beta subunits of eukaryotic initiation translation factor 2. J. Biol. Chem. 2005, 280:20549-20557.
47. Sofola O.A., Jin P., Qin Y., Duan R., Liu H., de Haro M., Nelson D.L., Botas J. RNA-binding proteins hnRNP A2/B1 and CUGBP1 suppress fragile X CGG premutation repeat-induced neurodegeneration in a Drosophila model of FXTAS. Neuron 2007, 55:565-571.
48. Snee M., Benz D., Jen J., Macdonald P.M. Two distinct domains of Bruno bind specifically to the oskar mRNA. RNA Biol. 2008, 5:1-9.
49. Lyon A.M., Reveal B.S., Macdonald P.M., Hoffman D.W. Bruno protein contains an expanded RNA recognition motif. Biochemistry (Mosc) 2009, 48:12202-12212.
50. Kim H.H., Gorospe M. GU-rich RNA: expanding CUGBP1 function, broadening mRNA turnover. Mol. Cell 2008, 29:151-152.
51. Peng S.S., Chen C.Y., Shyu A.B. Functional characterization of a non-AUUUA AU-rich element from the c-jun proto-oncogene mRNA: evidence for a novel class of AU-rich elements. Mol. Cell. Biol. 1996, 16:1490-1499.
52. Halees A.S., Hitti E., Al-Saif M., Mahmoud L., Vlasova-St Louis I.A., Beisang D.J., Bohjanen P.R., Khabar K. Global assessment of GU-rich regulatory content and function in the human transcriptome. RNA Biol. 2011, 8:681-691.
53. Barreau C., Paillard L., Mereau A., Osborne H.B. Mammalian CELF/Bruno-like RNA-binding proteins: molecular characteristics and biological functions. Biochimie 2006, 88:515-525.
54. Moraes K.C., Wilusz C.J., Wilusz J. CUG-BP binds to RNA substrates and recruits PARN deadenylase. RNA 2006, 12:1084-1091.
55. Paillard L., Legagneux V., Maniey D., Osborne H.B. c-Jun ARE targets mRNA deadenylation by an EDEN-BP (embryo deadenylation element-binding protein)-dependent pathway. J. Biol. Chem. 2002, 277:3232-3235.
56. Lee J.E., Lee J.Y., Trembly J., Wilusz J., Tian B., Wilusz C.J. The PARN deadenylase targets a discrete Set of mRNAs for decay and regulates cell motility in mouse myoblasts. PLoS Genet. 2012, 8:e1002901.
57. Walker M.R., Brown S.L., Riehl T.E., Stenson W.F., Stappenbeck T.S. Growth factor regulation of prostaglandin-endoperoxide synthase 2 (Ptgs2) expression in colonic mesenchymal stem cells. J. Biol. Chem. 2010, 285:5026-5039.
58. Gareau C., Fournier M.J., Filion C., Coudert L., Martel D., Labelle Y., Mazroui R. p21(WAF1/CIP1) upregulation through the stress granule-associated protein CUGBP1 confers resistance to bortezomib-mediated apoptosis. PLoS One 2011, 6:e20254.
59. Mukhopadhyay D., Jung J., Murmu N., Houchen C.W., Dieckgraefe B.K., Anant S. CUGBP2 plays a critical role in apoptosis of breast cancer cells in response to genotoxic injury. Ann. N. Y. Acad. Sci. 2003, 1010:504-509.
60. Murmu N., Jung J., Mukhopadhyay D., Houchen C.W., Riehl T.E., Stenson W.F., Morrison A.R., Arumugam T., Dieckgraefe B.K., Anant S. Dynamic antagonism between RNA-binding protein CUGBP2 and cyclooxygenase-2-mediated prostaglandin E2 in radiation damage. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13873-13878.
61. Natarajan G., Ramalingam S., Ramachandran I., May R., Queimado L., Houchen C.W., Anant S. CUGBP2 downregulation by prostaglandin E2 protects colon cancer cells from radiation-induced mitotic catastrophe. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G1235-G1244.
62. Subramaniam D., Ramalingam S., Linehan D.C., Dieckgraefe B.K., Postier R.G., Houchen C.W., Jensen R.A., Anant S. RNA binding protein CUGBP2/CELF2 mediates curcumin-induced mitotic catastrophe of pancreatic cancer cells. PLoS One 2011, 6:e16958.
63. Snee M.J., Harrison D., Yan N., Macdonald P.M. A late phase of Oskar accumulation is crucial for posterior patterning of the Drosophila embryo, and is blocked by ectopic expression of Bruno. Differentiation 2007, 75:246-255.
64. Reveal B., Garcia C., Ellington A., Macdonald P.M. Multiple RNA binding domains of Bruno confer recognition of diverse binding sites for translational repression. RNA Biol. 2011, 8:1047-1060.
65. Wilhelm J.E., Hilton M., Amos Q., Henzel W.J. Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz. J. Cell Biol. 2003, 163:1197-1204.
66. Nakamura A., Sato K., Hanyu-Nakamura K. Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 2004, 6:69-78.
67. Igreja C., Izaurralde E. CUP promotes deadenylation and inhibits decapping of mRNA targets. Genes Dev. 2011, 25:1955-1967.
68. Gao M., Wilusz C.J., Peltz S.W., Wilusz J. A novel mRNA-decapping activity in HeLa cytoplasmic extracts is regulated by AU-rich elements. EMBO J. 2001, 20:1134-1143.
69. Dehlin E., Wormington M., Korner C.G., Wahle E. Cap-dependent deadenylation of mRNA. EMBO J. 2000, 19:1079-1086.
70. Kalsotra A., Xiao X., Ward A.J., Castle J.C., Johnson J.M., Burge C.B., Cooper T.A. A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20333-20338.
71. Bland C.S., Wang E.T., Vu A., David M.P., Castle J.C., Johnson J.M., Burge C.B., Cooper T.A. Global regulation of alternative splicing during myogenic differentiation. Nucleic Acids Res. 2010, 38:7651-7664.
72. Kalsotra A., Wang K., Li P.F., Cooper T.A. MicroRNAs coordinate an alternative splicing network during mouse postnatal heart development. Genes Dev. 2010, 24:653-658.
73. Zhang X., Wang X., Zhu H., Zhu C., Wang Y., Pu W.T., Jegga A.G., Fan G.C. Synergistic effects of the GATA-4-mediated miR-144/451 cluster in protection against simulated ischemia/reperfusion-induced cardiomyocyte death. J. Mol. Cell. Cardiol. 2010, 49:841-850.
74. Cui Y.H., Xiao L., Rao J.N., Zou T., Liu L., Chen Y., Turner D.J., Gorospe M., Wang J.Y. miR-503 represses CUG-binding protein 1 translation by recruiting CUGBP1 mRNA to processing bodies. Mol. Biol. Cell 2012, 23:151-162.
75. Karagiannides I., Thomou T., Tchkonia T., Pirtskhalava T., Kypreos K.E., Cartwright A., Dalagiorgou G., Lash T.L., Farmer S.R., Timchenko N.A., Kirkland J.L. Increased CUG triplet repeat-binding protein-1 predisposes to impaired adipogenesis with aging. J. Biol. Chem. 2006, 281:23025-23033.
76. Salisbury E., Sakai K., Schoser B., Huichalaf C., Schneider-Gold C., Nguyen H., Wang G.L., Albrecht J.H., Timchenko L.T. Ectopic expression of cyclin D3 corrects differentiation of DM1 myoblasts through activation of RNA CUG-binding protein, CUGBP1. Exp. Cell Res. 2008, 314:2266-2278.
77. Huichalaf C., Sakai K., Jin B., Jones K., Wang G.L., Schoser B., Schneider-Gold C., Sarkar P., Pereira-Smith O.M., Timchenko N., Timchenko L. Expansion of CUG RNA repeats causes stress and inhibition of translation in myotonic dystrophy 1 (DM1) cells. FASEB J. 2010, 24:3706-3719.
78. Xu K., Kitchen C.M., Shu H.K., Murphy T.J. Platelet-derived growth factor-induced stabilization of cyclooxygenase 2 mRNA in rat smooth muscle cells requires the c-Src family of protein-tyrosine kinases. J. Biol. Chem. 2007, 282:32699-32709.
79. Roberts R., Timchenko N.A., Miller J.W., Reddy S., Caskey C.T., Swanson M.S., Timchenko L.T. Altered phosphorylation and intracellular distribution of a (CUG)n triplet repeat RNA-binding protein in patients with myotonic dystrophy and in myotonin protein kinase knockout mice. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13221-13226.
80. Kuyumcu-Martinez N.M., Wang G.S., Cooper T.A. Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation. Mol. Cell 2007, 28:68-78.
81. Wang G.S., Kuyumcu-Martinez M.N., Sarma S., Mathur N., Wehrens X.H., Cooper T.A. PKC inhibition ameliorates the cardiac phenotype in a mouse model of myotonic dystrophy type 1. J. Clin. Invest. 2009, 119:3797-3806.
82. Orengo J.P., Chambon P., Metzger D., Mosier D.R., Snipes G.J., Cooper T.A. Expanded CTG repeats within the DMPK 3' UTR causes severe skeletal muscle wasting in an inducible mouse model for myotonic dystrophy. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2646-2651.
83. Detivaud L., Pascreau G., Karaiskou A., Osborne H.B., Kubiak J.Z. Regulation of EDEN-dependent deadenylation of Aurora A/Eg2-derived mRNA via phosphorylation and dephosphorylation in Xenopus laevis egg extracts. J. Cell Sci. 2003, 116:2697-2705.
84. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
85. Gnad F., Gunawardena J., Mann M. PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Res. 2011, 39:D253-D260.
86. Brook M., McCracken L., Reddington J.P., Lu Z.L., Morrice N.A., Gray N.K. The multifunctional poly(A)-binding protein (PABP) 1 is subject to extensive dynamic post-translational modification, which molecular modelling suggests plays an important role in co-ordinating its activities. Biochem. J. 2012, 441:803-812.
87. Linero F.N., Thomas M.G., Boccaccio G.L., Scolaro L.A. Junin virus infection impairs stress-granule formation in Vero cells treated with arsenite via inhibition of eIF2alpha phosphorylation. J. Gen. Virol. 2011, 92:2889-2899.
88. Kedersha N.L., Gupta M., Li W., Miller I., Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J. Cell Biol. 1999, 147:1431-1442.
89. Balagopal V., Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 2009, 21:403-408.
90. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., Dember L.M., Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 2004, 15:5383-5398.
91. Fujimura K., Kano F., Murata M. Dual localization of the RNA binding protein CUGBP-1 to stress granule and perinucleolar compartment. Exp. Cell Res. 2008, 314:543-553.
92. Timchenko N.A., Iakova P., Cai Z.J., Smith J.R., Timchenko L.T. Molecular basis for impaired muscle differentiation in myotonic dystrophy. Mol. Cell. Biol. 2001, 21:6927-6938.
93. Chekulaeva M., Hentze M.W., Ephrussi A. Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles. Cell 2006, 124:521-533.
94. Pollock C., Daily K., Nguyen V.T., Wang C., Lewandowska M.A., Bensaude O., Huang S. Characterization of MRP RNA-protein interactions within the perinucleolar compartment. Mol. Biol. Cell 2011, 22:858-867.
95. Corbeil-Girard L.P., Klein A.F., Sasseville A.M., Lavoie H., Dicaire M.J., Saint-Denis A., Page M., Duranceau A., Codere F., Bouchard J.P., Karpati G., Rouleau G.A., Massie B., Langelier Y., Brais B. PABPN1 overexpression leads to upregulation of genes encoding nuclear proteins that are sequestered in oculopharyngeal muscular dystrophy nuclear inclusions. Neurobiol. Dis. 2005, 18:551-567.
96. Ramalingam S., Natarajan G., Schafer C., Subramaniam D., May R., Ramachandran I., Queimado L., Houchen C.W., Anant S. Novel intestinal splice variants of RNA-binding protein CUGBP2: isoform-specific effects on mitotic catastrophe. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G971-G981.
97. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 2009, 36:932-941.
98. Cammas A., Lewis S.M., Vagner S., Holcik M. Post-transcriptional control of gene expression through subcellular relocalization of mRNA binding proteins. Biochem. Pharmacol. 2008, 76:1395-1403.
99. Subramaniam D., Natarajan G., Ramalingam S., Ramachandran I., May R., Queimado L., Houchen C.W., Anant S. Translation inhibition during cell cycle arrest and apoptosis: Mcl-1 is a novel target for RNA binding protein CUGBP2. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G1025-G1032.
100. Pruitt K.D., Tatusova T., Brown G.R., Maglott D.R. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res. 2012, 40:D130-D135.
101. Suzuki H., Takeuchi M., Sugiyama A., Alam A.K., Vu L.T., Sekiyama Y., Dam H.C., Ohki S.Y., Tsukahara T. Alternative splicing produces structural and functional changes in CUGBP2. BMC Biochem. 2012, 13:6.
102. Cosson B., Gautier-Courteille C., Maniey D., Ait-Ahmed O., Lesimple M., Osborne H.B., Paillard L. Oligomerization of EDEN-BP is required for specific mRNA deadenylation and binding. Biol. Cell. 2006, 98:653-665.
103. Charlet B.N., Logan P., Singh G., Cooper T.A. Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol. Cell 2002, 9:649-658.
104. Ladd A.N., Taffet G., Hartley C., Kearney D.L., Cooper T.A. Cardiac tissue-specific repression of CELF activity disrupts alternative splicing and causes cardiomyopathy. Mol. Cell. Biol. 2005, 25:6267-6278.
105. Berger D.S., Moyer M., Kliment G.M., van Lunteren E., Ladd A.N. Expression of a dominant negative CELF protein in vivo leads to altered muscle organization, fiber size, and subtype. PLoS One 2011, 6:e19274.
106. Miller J.W., Urbinati C.R., Teng-Umnuay P., Stenberg M.G., Byrne B.J., Thornton C.A., Swanson M.S. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J. 2000, 19:4439-4448.
107. Pascual M., Vicente M., Monferrer L., Artero R. The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation 2006, 74:65-80.
108. Kino Y., Mori D., Oma Y., Takeshita Y., Sasagawa N., Ishiura S. Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum. Mol. Genet. 2004, 13:495-507.
109. 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., Lecuyer E., Burge C.B. Transcriptome-wide Regulation of Pre-mRNA Splicing and mRNA Localization by Muscleblind Proteins. Cell 2012, 150:710-724.
110. Cho S.J., Zhang J., Chen X. RNPC1 modulates the RNA-binding activity of, and cooperates with, HuR to regulate p21 mRNA stability. Nucleic Acids Res. 2010, 38:2256-2267.
111. van der Giessen K., Di-Marco S., Clair E., Gallouzi I.E. RNAi-mediated HuR depletion leads to the inhibition of muscle cell differentiation. J. Biol. Chem. 2003, 278:47119-47128.
112. Miyamoto S., Hidaka K., Jin D., Morisaki T. RNA-binding proteins Rbm38 and Rbm24 regulate myogenic differentiation via p21-dependent and -independent regulatory pathways. Genes Cells 2009, 14:1241-1252.
113. Timchenko N.A., Patel R., Iakova P., Cai Z.J., Quan L., Timchenko L.T. Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis. J. Biol. Chem. 2004, 279:13129-13139.
114. Sureban S.M., Murmu N., Rodriguez P., May R., Maheshwari R., Dieckgraefe B.K., Houchen C.W., Anant S. Functional antagonism between RNA binding proteins HuR and CUGBP2 determines the fate of COX-2 mRNA translation. Gastroenterology 2007, 132:1055-1065.
115. Xiao S., Sanelli T., Dib S., Sheps D., Findlater J., Bilbao J., Keith J., Zinman L., Rogaeva E., Robertson J. RNA targets of TDP-43 identified by UV-CLIP are deregulated in ALS. Mol. Cell. Neurosci. 2011, 47:167-180.
116. Dujardin G., Buratti E., Charlet-Berguerand N., Martins de Araujo M., Mbopda A., Le Jossic-Corcos C., Pagani F., Ferec C., Corcos L. CELF proteins regulate CFTR pre-mRNA splicing: essential role of the divergent domain of ETR-3. Nucleic Acids Res. 2010, 38:7273-7285.
117. Srikantan S., Tominaga K., Gorospe M. Functional interplay between RNA-binding protein HuR and microRNAs. Curr. Protein Pept. Sci. 2012, 13:372-379.
118. Leveille N., Elkon R., Davalos V., Manoharan V., Hollingworth D., Oude Vrielink J., le Sage C., Melo C.A., Horlings H.M., Wesseling J., Ule J., Esteller M., Ramos A., Agami R. Selective inhibition of microRNA accessibility by RBM38 is required for p53 activity. Nat. Commun. 2011, 2:513.
119. Jacobsen A., Wen J., Marks D.S., Krogh A. Signatures of RNA binding proteins globally coupled to effective microRNA target sites. Genome Res. 2010, 20:1010-1019.
120. Hwang-Verslues W.W., Chang P.H., Wei P.C., Yang C.Y., Huang C.K., Kuo W.H., Shew J.Y., Chang K.J., Lee E.Y., Lee W.H. miR-495 is upregulated by E12/E47 in breast cancer stem cells, and promotes oncogenesis and hypoxia resistance via downregulation of E-cadherin and REDD1. Oncogene 2011, 30:2463-2474.
121. Li Z., Cao Y., Jie Z., Liu Y., Li Y., Li J., Zhu G., Liu Z., Tu Y., Peng G., Lee D.W., Park S.S. miR-495 and miR-551a inhibit the migration and invasion of human gastric cancer cells by directly interacting with PRL-3. Cancer Lett. 2012, 323:41-47.
122. Eisenberg I., Eran A., Nishino I., Moggio M., Lamperti C., Amato A.A., Lidov H.G., Kang P.B., North K.N., Mitrani-Rosenbaum S., Flanigan K.M., Neely L.A., Whitney D., Beggs A.H., Kohane I.S., Kunkel L.M. Distinctive patterns of microRNA expression in primary muscular disorders. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17016-17021.
123. Kawahara Y., Mieda-Sato A. TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3347-3352.
124. Trabucchi M., Briata P., Garcia-Mayoral M., Haase A.D., Filipowicz W., Ramos A., Gherzi R., Rosenfeld M.G. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009, 459:1010-1014.
125. Perbellini R., Greco S., Sarra-Ferraris G., Cardani R., Capogrossi M.C., Meola G., Martelli F. Dysregulation and cellular mislocalization of specific miRNAs in myotonic dystrophy type 1. Neuromuscul. Disord. 2011, 21:81-88.
126. Gambardella S., Rinaldi F., Lepore S.M., Viola A., Loro E., Angelini C., Vergani L., Novelli G., Botta A. Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J. Transl. Med. 2010, 8:48.
127. Rau F., Freyermuth F., Fugier C., Villemin J.P., Fischer M.C., Jost B., Dembele D., Gourdon G., Nicole A., Duboc D., Wahbi K., Day J.W., Fujimura H., Takahashi M.P., Auboeuf D., Dreumont N., Furling D., Charlet-Berguerand N. Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat. Struct. Mol. Biol. 2011, 18:840-845.
128. Schoser B., Timchenko L. Myotonic dystrophies 1 and 2: complex diseases with complex mechanisms. Curr. Genomics 2010, 11:77-90.
129. Ward A.J., Rimer M., Killian J.M., Dowling J.J., Cooper T.A. CUGBP1 overexpression in mouse skeletal muscle reproduces features of myotonic dystrophy type 1. Hum. Mol. Genet. 2010, 19:3614-3622.
130. Koshelev M., Sarma S., Price R.E., Wehrens X.H., Cooper T.A. Heart-specific overexpression of CUGBP1 reproduces functional and molecular abnormalities of myotonic dystrophy type 1. Hum. Mol. Genet. 2010, 19:1066-1075.
131. Yu Z., Wang A.M., Robins D.M., Lieberman A.P. Altered RNA splicing contributes to skeletal muscle pathology in Kennedy disease knock-in mice. Dis. Models Mech. 2009, 2:500-507.
132. Cibois M., Boulanger G., Audic Y., Paillard L., Gautier-Courteille C. Inactivation of the Celf1 Gene that Encodes an RNA-Binding Protein Delays the First Wave of Spermatogenesis in Mice. PLoS One 2012, 7:e46337.
133. Kress C., Gautier-Courteille C., Osborne H.B., Babinet C., Paillard L. Inactivation of CUG-BP1/CELF1 causes growth, viability, and spermatogenesis defects in mice. Mol. Cell. Biol. 2007, 27:1146-1157.
134. Ho T.H., Bundman D., Armstrong D.L., Cooper T.A. Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy. Hum. Mol. Genet. 2005, 14:1539-1547.
135. Wang G.S., Kearney D.L., De Biasi M., Taffet G., Cooper T.A. Elevation of RNA-binding protein CUGBP1 is an early event in an inducible heart-specific mouse model of myotonic dystrophy. J. Clin. Invest. 2007, 117:2802-2811.
136. Orengo J.P., Ward A.J., Cooper T.A. Alternative splicing dysregulation secondary to skeletal muscle regeneration. Ann. Neurol. 2011, 69:681-690.
137. Wheeler T.M., Lueck J.D., Swanson M.S., Dirksen R.T., Thornton C.A. Correction of ClC-1 splicing eliminates chloride channelopathy and myotonia in mouse models of myotonic dystrophy. J. Clin. Invest. 2007, 117:3952-3957.
138. Osborne R.J., Lin X., Welle S., Sobczak K., O'Rourke J.R., Swanson M.S., Thornton C.A. Transcriptional and post-transcriptional impact of toxic RNA in myotonic dystrophy. Hum. Mol. Genet. 2009, 18:1471-1481.
139. Ranum L.P., Cooper T.A. RNA-mediated neuromuscular disorders. Annu. Rev. Neurosci. 2006, 29:259-277.
140. Meola G. Myotonic dystrophies as a brain disorder. Neurol. Sci. 2010, 31:863-864.
141. Romeo V. Myotonic Dystrophy Type 1 or Steinert's disease. Adv. Exp. Med. Biol. 2012, 724:239-257.
142. Di Costanzo A., Santoro L., de Cristofaro M., Manganelli F., Di Salle F., Tedeschi G. Familial aggregation of white matter lesions in myotonic dystrophy type 1. Neuromuscul. Disord. 2008, 18:299-305.
143. Leroy O., Wang J., Maurage C.A., Parent M., Cooper T., Buee L., Sergeant N., Andreadis A., Caillet-Boudin M.L. Brain-specific change in alternative splicing of Tau exon 6 in myotonic dystrophy type 1. Biochim. Biophys. Acta 2006, 1762:460-467.
144. Lee G., Leugers C.J. Tau and tauopathies. Prog. Mol. Biol. Transl. Sci. 2012, 107:263-293.
145. Marteyn A., Maury Y., Gauthier M.M., Lecuyer C., Vernet R., Denis J.A., Pietu G., Peschanski M., Martinat C. Mutant human embryonic stem cells reveal neurite and synapse formation defects in type 1 myotonic dystrophy. Cell Stem Cell 2011, 8:434-444.
146. Anderson K.N., Baban D., Oliver P.L., Potter A., Davies K.E. Expression profiling in spinal muscular atrophy reveals an RNA binding protein deficit. Neuromuscul. Disord. 2004, 14:711-722.
147. Halgren C., Bache I., Bak M., Myatt M.W., Anderson C.M., Brondum-Nielsen K., Tommerup N. Haploinsufficiency of CELF4 at 18q12.2 is associated with developmental and behavioral disorders, seizures, eye manifestations, and obesity. Eur. J. Hum. Genet. 2012, 20:1315-1319.
148. Yang Y., Mahaffey C.L., Berube N., Maddatu T.P., Cox G.A., Frankel W.N. Complex seizure disorder caused by Brunol4 deficiency in mice. PLoS Genet. 2007, 3:e124.
149. King O.D., Gitler A.D., Shorter J. The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res. 2012, 1462:61-80.
150. Colby D.W., Prusiner S.B. Prions. Cold Spring Harb. Perspect. Biol. 2011, 3:a006833.
151. Lee E.B., Lee V.M., Trojanowski J.Q. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat. Rev. Neurosci. 2012, 13:38-50.
152. Udan M., Baloh R.H. Implications of the prion-related Q/N domains in TDP-43 and FUS. Prion 2011, 5:1-5.
153. Chang E.T., Donahue J.M., Xiao L., Cui Y., Rao J.N., Turner D.J., Twaddell W.S., Wang J.Y., Battafarano R.J. The RNA-binding protein CUG-BP1 increases survivin expression in oesophageal cancer cells through enhanced mRNA stability. Biochem. J. 2012, 446:113-123.
154. Rodriguez F.J., Giannini C., Asmann Y.W., Sharma M.K., Perry A., Tibbetts K.M., Jenkins R.B., Scheithauer B.W., Anant S., Jenkins S., Eberhart C.G., Sarkaria J.N., Gutmann D.H. Gene expression profiling of NF-1-associated and sporadic pilocytic astrocytoma identifies aldehyde dehydrogenase 1 family member L1 (ALDH1L1) as an underexpressed candidate biomarker in aggressive subtypes. J. Neuropathol. Exp. Neurol. 2008, 67:1194-1204.
155. Geh J.L., Moss A.L. Multiple pilomatrixomata and myotonic dystrophy: a familial association. Br. J. Plast. Surg. 1999, 52:143-145.
156. Gadalla S.M., Lund M., Pfeiffer R.M., Gortz S., Mueller C.M., Moxley R.T., Kristinsson S.Y., Bjorkholm M., Shebl F.M., Hilbert J.E., Landgren O., Wohlfahrt J., Melbye M., Greene M.H. Cancer risk among patients with myotonic muscular dystrophy. JAMA 2011, 306:2480-2486.
157. Win A.K., Perattur P.G., Pulido J.S., Pulido C.M., Lindor N.M. Increased cancer risks in myotonic dystrophy. Mayo Clin. Proc. 2012, 87:130-135.
158. Mueller C.M., Hilbert J.E., Martens W., Thornton C.A., Moxley R.T., Greene M.H. Hypothesis: neoplasms in myotonic dystrophy. Cancer Causes Control 2009, 20:2009-2020.
159. Wang G.L., Salisbury E., Shi X., Timchenko L., Medrano E.E., Timchenko N.A. HDAC1 promotes liver proliferation in young mice via interactions with C/EBPbeta. J. Biol. Chem. 2008, 283:26179-26187.
160. Arnal-Estape A., Tarragona M., Morales M., Guiu M., Nadal C., Massague J., Gomis R.R. HER2 silences tumor suppression in breast cancer cells by switching expression of C/EBPss isoforms. Cancer Res. 2010, 70:9927-9936.
161. Guerzoni C., Bardini M., Mariani S.A., Ferrari-Amorotti G., Neviani P., Panno M.L., Zhang Y., Martinez R., Perrotti D., Calabretta B. Inducible activation of CEBPB, a gene negatively regulated by BCR/ABL, inhibits proliferation and promotes differentiation of BCR/ABL-expressing cells. Blood 2006, 107:4080-4089.
162. Raghavan A., Ogilvie R.L., Reilly C., Abelson M.L., Raghavan S., Vasdewani J., Krathwohl M., Bohjanen P.R. Genome-wide analysis of mRNA decay in resting and activated primary human T lymphocytes. Nucleic Acids Res. 2002, 30:5529-5538.
163. Vlasova-St Louis I., Bohjanen P.R. Coordinate regulation of mRNA decay networks by GU-rich elements and CELF1. Curr. Opin. Genet. Dev. 2011, 21:444-451.
164. Nguyen-Chi M., Morello D. RNA-binding proteins, RNA granules, and gametes: is unity strength?. Reproduction 2011, 142:803-817.
165. Dev A., Nayernia K., Meins M., Adham I., Lacone F., Engel W. Mice deficient for RNA-binding protein brunol1 show reduction of spermatogenesis but are fertile. Mol. Reprod. Dev. 2007, 74:1456-1464.
166. Gautier-Courteille C., Le Clainche C., Barreau C., Audic Y., Graindorge A., Maniey D., Osborne H.B., Paillard L. EDEN-BP-dependent post-transcriptional regulation of gene expression in Xenopus somitic segmentation. Development 2004, 131:6107-6117.
167. Cibois M., Gautier-Courteille C., Vallee A., Paillard L. A strategy to analyze the phenotypic consequences of inhibiting the association of an RNA-binding protein with a specific RNA. RNA 2010, 16:10-15.
168. Matsui T., Sasaki A., Akazawa N., Otani H., Bessho Y. Celf1 regulation of dmrt2a is required for somite symmetry and left-right patterning during zebrafish development. Development 2012, 139:3553-3560.
169. Milne C.A., Hodgkin J. ETR-1, a homologue of a protein linked to myotonic dystrophy, is essential for muscle development in Caenorhabditis elegans. Curr. Biol. 1999, 9:1243-1246.
170. Loria P.M., Duke A., Rand J.B., Hobert O. Two neuronal, nuclear-localized RNA binding proteins involved in synaptic transmission. Curr. Biol. 2003, 13:1317-1323.
171. Yan N., Macdonald P.M. Genetic interactions of Drosophila melanogaster arrest reveal roles for translational repressor Bruno in accumulation of Gurken and activity of Delta. Genetics 2004, 168:1433-1442.
172. Malone J.H., Oliver B. Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol. 2011, 9:34.
173. Tani H., Akimitsu N. Genome-wide technology for determining RNA stability in mammalian cells: Historical perspective and recent advantages based on modified nucleotide labeling. RNA Biol. 2012, 9.
174. Adeli K. Translational control mechanisms in metabolic regulation: critical role of RNA binding proteins, microRNAs, and cytoplasmic RNA granules. Am. J. Physiol. Endocrinol. Metab. 2011, 301:E1051-E1064.
175. Scheu S., Stetson D.B., Reinhardt R.L., Leber J.H., Mohrs M., Locksley R.M. Activation of the integrated stress response during T helper cell differentiation. Nat. Immunol. 2006, 7:644-651.
176. Lin J.C., Tarn W.Y. RNA-binding motif protein 4 translocates to cytoplasmic granules and suppresses translation via argonaute2 during muscle cell differentiation. J. Biol. Chem. 2009, 284:34658-34665.