Integrative analysis revealed the molecular mechanism underlying RBM10-mediated splicing regulation

EMBO Molecular Medicine

Volumn 5, Issue 9, 2013, Pages 1431-1442

  Wang, Yongbo ^a   Gogol Döring, Andreas ^a   Hu, Hao ^b   Fröhler, Sebastian ^a   Ma, Yunxia ^c   Jens, Marvin ^a   Maaskola, Jonas ^a   Murakawa, Yasuhiro ^a   Quedenau, Claudia ^a   Landthaler, Markus ^a   Kalscheuer, Vera ^b   Wieczorek, Dagmar ^d   Wang, Yang ^e   Hu, Yuhui ^a   Chen, Wei ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c Taiyuan Central Hospital   (China)

^d UNIVERSITY HOSPITAL ESSEN   (Germany)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative splicing; Mechanistic model; RBM10

Indexed keywords

RNA BINDING PROTEIN; RNA BINDING PROTEIN 10; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; CONGENITAL MALFORMATION; CONTROLLED STUDY; CROSS LINKING; EMBRYO; EXON SKIPPING; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN RNA BINDING; SPLICING DEFECT; TALIPES EQUINOVARUS ATRIAL SEPTAL DEFECT ROBIN SEQUENCE AND PERSISTENT LEFT SUPERIOR VENA CAVA SYNDROME;

ALTERNATIVE SPLICING; MECHANISTIC MODEL; RBM10;

ALTERNATIVE SPLICING; CLUBFOOT; GENE EXPRESSION REGULATION; HEART DEFECTS, CONGENITAL; HUMANS; PIERRE ROBIN SYNDROME; RNA-BINDING PROTEINS;

EID: 84883379498     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201302663     Document Type: Article

References (51)

1. Agafonov DE, Deckert J, Wolf E, Odenwälder P, Bessonov S, Will CL, Urlaub H, Lührmann R (2011) Semiquantitative proteomic analysis of the human spliceosome via a novel two-dimensional gel electrophoresis method. Mol Cell Biol 31: 2667-2682
2. Anders G, Mackowiak SD, Jens M, Maaskola J, Kuntzagk A, Rajewsky N, Landthaler M, Dieterich C (2012) doRiNA: a database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res 40: D180-D186
3. Barash Y, Calarco JA, Gao W, Pan Q, Wang X, Shai O, Blencowe BJ, Frey BJ (2010) Deciphering the splicing code. Nature 465: 53-59
4. Behzadnia N, Golas MM, Hartmuth K, Sander B, Kastner B, Deckert J, Dube P, Will CL, Urlaub H, Stark H, et al (2007) Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J 26: 1737-1748
5. Bessonov S, Anokhina M, Will CL, Urlaub H, Luhrmann R (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature 452: 846-850
6. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Ann Rev Biochem 72: 291-336
7. Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126: 37-47
8. Bonnal S, Martínez C, Förch P, Bachi A, Wilm M, Valcárcel J (2008) RBM5/Luca-15/H37 regulates Fas alternative splice site pairing after exon definition. Mol Cell 32: 81-95
9. Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92
10. Chen M, Manley JL (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat Rev Mol Cell Biol 10: 741-754
11. Cooper TA, Wan L, Dreyfuss G (2009) RNA and disease. Cell 136: 777-793
12. Garcia-Blanco MA, Baraniak AP, Lasda EL (2004) Alternative splicing in disease and therapy. Nat Biotechnol 22: 535-546
13. Glisovic T, Bachorik JL, Yong J, Dreyfuss G (2008) RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 582: 1977-1986
14. Gripp KW, Hopkins E, Johnston JJ, Krause C, Dobyns WB, Biesecker LG (2011) Long-term survival in TARP syndrome and confirmation of RBM10 as the disease-causing gene. Am J Med Genet A 155: 2516-2520
15. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp A-C, Munschauer M, et al (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141
16. Heckman KL, Pease LR (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924-932
17. Hegele A, Kamburov A, Grossmann A, Sourlis C, Wowro S, Weimann M, Will Cindy L, Pena V, Lührmann R, Stelzl U (2012) Dynamic protein-protein interaction wiring of the human spliceosome. Mol Cell 45: 567-580
18. Huang DW, Sherman BT, Lempicki RA (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
19. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13
20. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, Cho J, Suh J, Capelletti M, Sivachenko A, et al (2012) Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 150: 1107-1120
21. Johnston JJ, Teer JK, Cherukuri PF, Hansen NF, Loftus SK, Chong K, Mullikin JC, Biesecker LG (2010) Massively parallel sequencing of exons on the X chromosome identifies RBM10 as the gene that causes a syndromic form of cleft palate. Am J Hum Genet 86: 743-748
22. Keene JD (2007) RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 8: 533-543
23. Landthaler M, Gaidatzis D, Rothballer A, Chen PY, Soll SJ, Dinic L, Ojo T, Hafner M, Zavolan M, Tuschl T (2008) Molecular characterization of human Argonaute-containing ribonucleoprotein complexes and their bound target mRNAs. RNA 14: 2580-2596
24. Lebedeva S, Jens M, Theil K, Schwanhäusser B, Selbach M, Landthaler M, Rajewsky N (2011) Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 43: 340-352
25. Licatalosi DD, Yano M, Fak JJ, Mele A, Grabinski SE, Zhang C, Darnell RB (2012) Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev 26: 1626-1642
26. Makarov EM, Owen N, Bottrill A, Makarova OV (2011) Functional mammalian spliceosomal complex E contains SMN complex proteins in addition to U1 and U2 snRNPs. Nucleic Acids Res 40: 2639-2652
27. Maniatis T, Tasic B (2002) Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418: 236-243
28. Maydan G, Noyman I, Har-Zahav A, Neriah ZB, Pasmanik-Chor M, Yeheskel A, Albin-Kaplanski A, Maya I, Magal N, Birk E, et al (2011) Multiple congenital anomalies-hypotonia-seizures syndrome is caused by a mutation in PIGN. J Med Genet 48: 383-389
29. McMillin MJ, Below JE, Shively KM, Beck AE, Gildersleeve HI, Pinner J, Gogola GR, Hecht JT, Grange DK, Harris DJ, et al (2013) Mutations in ECEL1 cause distal arthrogryposis type 5D. Am J Hum Genet 92: 150-156
30. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628
31. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano M, Tuschl T, Ohler U, Keene JD (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 43: 327-339
32. Najm J, Horn D, Wimplinger I, Golden JA, Chizhikov VV, Sudi J, Christian SL, Ullmann R, Kuechler A, Haas CA, et al (2008) Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum. Nat Genet 40: 1065-1067
33. Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463: 457-463
34. Padgett RA (2012) New connections between splicing and human disease. Trends Genet: TIG 28: 147-154
35. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415
36. Polymenidou M, Lagier-Tourenne C, Hutt KR, Huelga SC, Moran J, Liang TY, Ling S-C, Sun E, Wancewicz E, Mazur C, et al (2011) Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 14: 459-468
37. Rappsilber J, Ryder U, Lamond AI, Mann M (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12: 1231-1245
38. Sayer JA, Otto EA, O'Toole JF, Nurnberg G, Kennedy MA, Becker C, Hennies HC, Helou J, Attanasio M, Fausett BV, et al (2006) The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4. Nat Genet 38: 674-681
39. Sutherland LC, Rintala-Maki ND, White RD, Morin CD (2005) RNA binding motif (RBM) proteins: a novel family of apoptosis modulators? J Cell Biochem 94: 5-24
40. Ule J, Stefani G, Mele A, Ruggiu M, Wang X, Taneri B, Gaasterland T, Blencowe BJ, Darnell RB (2006) An RNA map predicting Nova-dependent splicing regulation. Nature 444: 580-586
41. Wang TE, Cody NA, Jog S, Biancolella M, Wang TT, Treacy DJ, Luo S, Schroth GP, Housman DE, Reddy S et al (2012) Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 150: 710-724
42. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476
43. Wang G-S, Cooper TA (2007) Splicing in disease: disruption of the splicing code and the decoding machinery. Nat Rev Genet 8: 749-761
44. Wang Y, Cheong C-G, Tanaka Hall TM, Wang Z (2009) Engineering splicing factors with designed specificities. Nat Methods 6: 825-830
45. Wang Y, Xiao X, Zhang J, Choudhury R, Robertson A, Li K, Ma M, Burge CB, Wang Z (2013) A complex network of factors with overlapping affinities represses splicing through intronic elements. Nat Struct Mol Biol 20: 36-45
46. Waterham HR, Koster J, van Roermund CWT, Mooyer PAW, Wanders RJA, Leonard JV (2007) A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 356: 1736-1741
47. Weiss J, Axelrod L, Whitcomb RW, Harris PE, Crowley WF, Jameson JL (1992) Hypogonadism caused by a single amino acid substitution in the β subunit of luteinizing hormone. N Engl J Med 326: 179-183
48. Witten JT, Ule J (2011) Understanding splicing regulation through RNA splicing maps. Trends Genet 27: 89-97
49. Xue Y, Zhou Y, Wu T, Zhu T, Ji X, Kwon Y-S, Zhang C, Yeo G, Black DL, Sun H, et al (2009) Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol Cell 36: 996-1006
50. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu X-D, Gage FH (2009) An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 16: 130-137
51. Yoshida K, Sanada M, Shiraishi Y, Nowak D, Nagata Y, Yamamoto R, Sato Y, Sato-Otsubo A, Kon A, Nagasaki M, et al (2011) Frequent pathway mutations of splicing machinery in myelodysplasia. Nature 478: 64-69