Multi-disciplinary methods to define RNA-protein interactions and regulatory networks

Current Opinion in Genetics and Development

Volumn 23, Issue 1, 2013, Pages 20-28

  Ascano, Manuel ^a   Gerstberger, Stefanie ^a   Tuschl, Thomas ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; FRAGILE X MENTAL RETARDATION PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HUR PROTEIN; LONG UNTRANSLATED RNA; MESSENGER RNA; MUSASHI 1 PROTEIN; PROTEIN LIN28A; PROTEIN LIN28B; RIBONUCLEASE; RIBONUCLEOPROTEIN; RNA; RNA BINDING PROTEIN; SERINE ARGININE RICH PROTEIN; SMALL NUCLEAR RNA; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 3; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; BINDING SITE; COMPLEX FORMATION; DNA LIBRARY; GENE REGULATORY NETWORK; GENE TARGETING; HUMAN; IMMUNOPRECIPITATION; MALIGNANT NEOPLASTIC DISEASE; MASS SPECTROMETRY; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CROSS LINKING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN RNA BINDING; REVIEW; RNA PROCESSING; RNA SEQUENCE; RNA STABILITY; RNA TRANSLATION; STRUCTURE ACTIVITY RELATION;

GENE EXPRESSION PROFILING; GENE LIBRARY; GENE REGULATORY NETWORKS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84877926794     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2013.01.003     Document Type: Review

References (58)

1. König J., Zarnack K., Rot G., Curk T., Kayikci M., Zupan B., Turner D.J., Luscombe N.M., Ule J. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 2010, 17:909-915.
2. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., Chi S.W., Clark T.A., Schweitzer A.C., Blume J.E., Wang X., et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
3. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.-C., Munschauer M., et al. Transcriptome-wide Identification of RNA-binding protein and MicroRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
4. Wang Z., Kayikci M., Briese M., Zarnack K., Luscombe N.M., Rot G., Zupan B., Curk T., Ule J. iCLIP predicts the dual splicing effects of TIA-RNA interactions. PLoS Biol 2010, 8:e1000530.
5. Granneman S., Kudla G., Petfalski E., Tollervey D. Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proc Natl Acad Sci USA 2009, 106:9613-9618.
6. Ascano M., Hafner M., Cekan P., Gerstberger S., Tuschl T. Identification of RNA-protein interaction networks using PAR-CLIP. WIREs RNA 2012, 3:159-177.
7. Morris A.R., Mukherjee N., Keene J.D. Systematic analysis of posttranscriptional gene expression. Wiley Interdiscip Rev Syst Biol Med 2010, 2:162-180.
8. Zhao J., Ohsumi T.K., Kung J.T., Ogawa Y., Grau D.J., Sarma K., Song J.-J., Kingston R.E., Borowsky M., Lee J.T. Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell 2010, 40:939-953.
9. Mukherjee N., Corcoran D.L., Nusbaum J.D., Reid D.W., Georgiev S., Hafner M., Ascano M., Tuschl T., Ohler U., Keene J.D. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples Pre-mRNA processing and mRNA stability. Mol Cell 2011, 43:327-339.
10. Ascano M., Mukherjee N., Bandaru P., Miller J.B., Nusbaum J.D., Corcoran D.L., Langlois C., Munschauer M., Dewell S., Hafner M., et al. FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature 2012, 492:382-386.
11. Abdelmohsen K., Gorospe M. Posttranscriptional regulation of cancer traits by HuR. WIREs RNA 2010, 1:214-229.
12. Garcia-Blanco M.A., Jamison S.F., Sharp P.A. Identification and purification of a 62,000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev 1989, 3:1874-1886.
13. Patton J.G., Mayer S.A., Tempst P., Nadal-Ginard B. Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev 1991, 5:1237-1251.
14. Dreyfuss G., Choi Y.D., Adam S.A. Characterization of heterogeneous nuclear RNA-protein complexes in vivo with monoclonal antibodies. Mol Cell Biol 1984, 4:1104-1114.
15. Sharma S. Isolation of a sequence-specific RNA binding protein, polypyrimidine tract binding protein, using RNA affinity chromatography. Methods Mol Biol 2008, 488:1-8.
16. Steen H., Jensen O.N. Analysis of protein-nucleic acid interactions by photochemical cross-linking and mass spectrometry. Mass Spectrom Rev 2002, 21:163-182.
17. Williams K.R., Konigsberg W.H. Identification of amino acid residues at interface of protein-nucleic acid complexes by photochemical cross-linking. Methods Enzymol 1991, 208:516-539.
18. Urlaub H., Hartmuth K., Kostka S., Grelle G., Luhrmann R. A general approach for identification of RNA-protein cross-linking sites within native human spliceosomal small nuclear ribonucleoproteins (snRNPs). Analysis of RNA-protein contacts in native U1 and U4/U6.U5 snRNPs. J Biol Chem 2000, 275:41458-41468.
19. Butter F., Scheibe M., Mörl M., Mann M. Unbiased RNA-protein interaction screen by quantitative proteomics. Proc Natl Acad Sci USA 2009, 106:10626-10631.
20. Scheibe M., Butter F., Hafner M., Tuschl T., Mann M. Quantitative mass spectrometry and PAR-CLIP to identify RNA-protein interactions. Nucleic Acids Res 2012, 40:9897-9902.
21. Bardwell V.J., Wickens M. Purification of RNA and RNA-protein complexes by an R17 coat protein affinity method. Nucleic Acids Res 1990, 18:6587-6594.
22. Zhou Z., Reed R. Purification of functional RNA-protein complexes using MS2-MBP. Curr Protoc Mol Biol 2003, 3. Chapter 27:Unit 27.
23. Windbichler N., Schroeder R. Isolation of specific RNA-binding proteins using the streptomycin-binding RNA aptamer. Nat Protoc 2006, 1:637-640.
24. Walker S.C., Scott F.H., Srisawat C., Engelke D.R. RNA affinity tags for the rapid purification and investigation of RNAs and RNA-protein complexes. Methods Mol Biol 2008, 488:23-40.
25. Tsai B.P., Wang X., Huang L., Waterman M.L. Quantitative profiling of in vivo-assembled RNA-protein complexes using a novel integrated proteomic approach. Mol Cell Proteomics 2011, 10. M110.007385.
26. Tyagi S. Imaging intracellular RNA distribution and dynamics in living cells. Nat Methods 2009, 6:331-338.
27. Bertrand E., Chartrand P., Schaefer M., Shenoy S.M., Singer R.H., Long R.M. Localization of ASH1 mRNA particles in living yeast. Mol Cell 1998, 2:437-445.
28. Castello A., Fischer B., Eichelbaum K., Horos R., Beckmann B.M., Strein C., Davey N.E., Humphreys D.T., Preiss T., Steinmetz L.M., et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149:1393-1406.
29. Baltz A.G., Munschauer M., Schwanhausser B., Vasile A., Murakawa Y., Schueler M., Youngs N., Penfold-Brown D., Drew K., Milek M., et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 2012, 46:674-690.
30. Kiledjian M., Dreyfuss G. Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J 1992, 11:2655-2664.
31. Gerber A.P., Luschnig S., Krasnow M.A., Brown P.O., Herschlag D. Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci USA 2006, 103:4487-4492.
32. White E.K., Moore-Jarrett T., Ruley H.E. PUM2, a novel murine puf protein, and its consensus RNA-binding site. RNA 2001, 7:1855-1866.
33. Wang X., Zamore P.D., Hall T.M. Crystal structure of a Pumilio homology domain. Mol Cell 2001, 7:855-865.
34. Wang X., McLachlan J., Zamore P.D., Hall T.M. Modular recognition of RNA by a human pumilio-homology domain. Cell 2002, 110:501-512.
35. Buckanovich R.J., Darnell R.B. The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol Cell Biol 1997, 17:3194-3201.
36. Lewis H.A., Chen H., Edo C., Buckanovich R.J., Yang Y.Y., Musunuru K., Zhong R., Darnell R.B., Burley S.K. Crystal structures of Nova-1 and Nova-2 K-homology RNA-binding domains. Cell 1999, 7:191-203.
37. Jensen K.B., Musunuru K., Lewis H.A., Burley S.K., Darnell R.B. The tetranucleotide UCAY directs the specific recognition of RNA by the Nova K-homology 3 domain. Proc Natl Acad Sci USA 2000, 97:5740-5745.
38. Teplova M., Malinina L., Darnell J.C., Song J., Lu M., Abagyan R., Musunuru K., Teplov A., Burley S.K., Darnell R.B., et al. Protein-RNA and protein-protein recognition by dual KH1/2 domains of the neuronal splicing factor Nova-1. Cell 2011, 19:930-944.
39. Valverde R., Pozdnyakova I., Kajander T., Venkatraman J., Regan L. Fragile X mental retardation syndrome: structure of the KH1-KH2 domains of fragile X mental retardation protein. Structure 2007, 15:1090-1098.
40. Darnell J.C., Fraser C.E., Mostovetsky O., Stefani G., Jones T.A., Eddy S.R., Darnell R.B. Kissing complex RNAs mediate interaction between the Fragile-X mental retardation protein KH2 domain and brain polyribosomes. Genes Dev 2005, 19:903-918.
41. Jonson L., Vikesaa J., Krogh A., Nielsen L.K., Hansen T.V., Borup R., Johnsen A.H., Christiansen J., Nielsen F.C. Molecular composition of IMP1 ribonucleoprotein granules. Mol Cell Proteomics 2007, 6:798-811.
42. Chao J.A., Patskovsky Y., Patel V., Levy M., Almo S.C., Singer R.H. ZBP1 recognition of β-actin zipcode induces RNA looping. Genes Dev 2010, 24:148-158.
43. Patel V.L., Mitra S., Harris R., Buxbaum A.R., Lionnet T., Brenowitz M., Girvin M., Levy M., Almo S.C., Singer R.H., et al. Spatial arrangement of an RNA zipcode identifies mRNAs under post-transcriptional control. Genes Dev 2012, 26:43-53.
44. Bell J.L., Wächter K., Mühleck B., Pazaitis N., Köhn M., Lederer M., Huttelmaier S. Insulin-like growth factor 2 mRNA-binding proteins (IGF2BPs): post-transcriptional drivers of cancer progression?. Cell Mol Life Sci 2012, 10.1007/s00018-012-1186-z.
45. Zhang R., So B.R., Li P., Yong J., Glisovic T., Wan L., Dreyfuss G. Structure of a key intermediate of the SMN complex reveals Gemin2's crucial function in snRNP assembly. Cell 2011, 146:384-395.
46. Singh R., Valcárcel J. Building specificity with nonspecific RNA-binding proteins. Nat Struct Mol Biol 2005, 12:645-653.
47. Ingolia N.T., Ghaemmaghami S., Newman J.R., Weissman J.S. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science (New York, NY) 2009, 324:218-223.
48. Arava Y., Wang Y., Storey J.D., Liu C.L., Brown P.O., Herschlag D. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2003, 100:3889-3894.
49. Ingolia N.T., Lareau L.F., Weissman J.S. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 2011, 147:789-802.
50. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840.
51. Sandberg R., Neilson J.R., Sarma A., Sharp P.A., Burge C.B. Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. Science 2008, 320:1643-1647.
52. Mayr C., Bartel D.P. Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 2009, 138:673-684.
53. Berg M.G., Singh L.N., Younis I., Liu Q., Pinto A.M., Kaida D., Zhang Z., Cho S., Sherrill-Mix S., Wan L., et al. U1 snRNP determines mRNA length and regulates isoform expression. Cell 2012, 150:53-64.
54. Jan C.H., Friedman R.C., Ruby J.G., Bartel D.P. Formation, regulation and evolution of Caenorhabditis elegans 3'UTRs. Nature 2011, 469:97-101.
55. Thornton J.E., Gregory R.I. How does Lin28 let-7 control development and disease?. Trends Cell Biol 2012, 22:474-482.
56. Vo D.T., Subramaniam D., Remke M., Burton T.L., Uren P.J., Gelfond J.A., de Sousa Abreu R., Burns S.C., Qiao M., Suresh U., et al. The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis. Am J Pathol 2012, 181:1762-1772.
57. Kharas M.G., Lengner C.J., Al-Shahrour F., Bullinger L., Ball B., Zaidi S., Morgan K., Tam W., Paktinat M., Okabe R., et al. Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nat Med 2010, 16:903-908.
58. Ito T., Kwon H.Y., Zimdahl B., Congdon K.L., Blum J., Lento W.E., Zhao C., Lagoo A., Gerrard G., Foroni L., et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 2010, 466:765-768.