HnRNP L and HnRNP A1 Induce Extended U1 snRNA Interactions with an Exon to Repress Spliceosome Assembly

Molecular Cell

Volumn 49, Issue 5, 2013, Pages 972-982

  Chiou, Ni Ting ^a   Shankarling, Ganesh ^a   Lynch, Kristen W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CATALYSIS; EXON; GENE CONTROL; HUMAN; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA SEQUENCE; RNA SPLICING; SPLICEOSOME;

ALTERNATIVE SPLICING; ANTIGENS, CD45; BASE SEQUENCE; BINDING SITES; EXONS; HEK293 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN L; HUMANS; RNA INTERFERENCE; RNA SPLICING; RNA, MESSENGER; RNA, SMALL NUCLEAR; SPLICEOSOMES;

EID: 84876820281     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.12.025     Document Type: Article

References (34)

1. Abad X., Vera M., Jung S.P., Oswald E., Romero I., Amin V., Fortes P., Gunderson S.I. Requirements for gene silencing mediated by U1 snRNA binding to a target sequence. Nucleic Acids Res. 2008, 36:2338-2352.
2. Freund M., Hicks M.J., Konermann C., Otte M., Hertel K.J., Schaal H. Extended base pair complementarity between U1 snRNA and the 5' splice site does not inhibit splicing in higher eukaryotes, but rather increases 5' splice site recognition. Nucleic Acids Res. 2005, 33:5112-5119.
3. Hermiston M.L., Xu Z., Majeti R., Weiss A. Reciprocal regulation of lymphocyte activation by tyrosine kinases and phosphatases. J. Clin. Invest. 2002, 109:9-14.
4. House A.E., Lynch K.W. An exonic splicing silencer represses spliceosome assembly after ATP-dependent exon recognition. Nat. Struct. Mol. Biol. 2006, 13:937-944.
5. Huelga S.C., Vu A.Q., Arnold J.D., Liang T.Y., Liu P.P., Yan B.Y., Donohue J.P., Shiue L., Hoon S., Brenner S., et al. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Reports 2012, 1:167-178.
6. Jurica M.S., Licklider L.J., Gygi S.R., Grigorieff N., Moore M.J. Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA 2002, 8:426-439.
7. Kaida D., Berg M.G., Younis I., Kasim M., Singh L.N., Wan L., Dreyfuss G. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 2010, 468:664-668.
8. Konarska M.M., Vilardell J., Query C.C. Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol. Cell 2006, 21:543-553.
9. Konforti B.B., Konarska M.M. U4/U5/U6 snRNP recognizes the 5' splice site in the absence of U2 snRNP. Genes Dev. 1994, 8:1962-1973.
10. Kumar A., Wilson S.H. Studies of the strand-annealing activity of mammalian hnRNP complex protein A1. Biochemistry 1990, 29:10717-10722.
11. Labourier E., Adams M.D., Rio D.C. Modulation of P-element pre-mRNA splicing by a direct interaction between PSI and U1 snRNP 70K protein. Mol. Cell 2001, 8:363-373.
12. Lynch K.W., Weiss A. A CD45 polymorphism associated with multiple sclerosis disrupts an exonic splicing silencer. J. Biol. Chem. 2001, 276:24341-24347.
13. Maroney P.A., Romfo C.M., Nilsen T.W. Functional recognition of 5' splice site by U4/U6.U5 tri-snRNP defines a novel ATP-dependent step in early spliceosome assembly. Mol. Cell 2000, 6:317-328.
14. Martinez-Contreras R., Cloutier P., Shkreta L., Fisette J.-F., Revil T., Chabot B. hnRNP proteins and splicing control. Adv. Exp. Med. Biol. 2007, 623:123-147.
15. Melton A.A., Jackson J., Wang J., Lynch K.W. Combinatorial control of signal-induced exon repression by hnRNP L and PSF. Mol. Cell. Biol. 2007, 27:6972-6984.
16. Motta-Mena L.B., Heyd F., Lynch K.W. Context-dependent regulatory mechanism of the splicing factor hnRNP L. Mol. Cell 2010, 37:223-234.
17. Motta-Mena L.B., Smith S.A., Mallory M.J., Jackson J., Wang J., Lynch K.W. A disease-associated polymorphism alters splicing of the human CD45 phosphatase gene by disrupting combinatorial repression by heterogeneous nuclear ribonucleoproteins (hnRNPs). J. Biol. Chem. 2011, 286:20043-20053.
18. Nilsen T.W., Graveley B.R. Expansion of the eukaryotic proteome by alternative splicing. Nature 2010, 463:457-463.
19. Pomeranz Krummel D.A., Oubridge C., Leung A.K., Li J., Nagai K. Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 2009, 458:475-480.
20. Pontius B.W., Berg P. Renaturation of complementary DNA strands mediated by purified mammalian heterogeneous nuclear ribonucleoprotein A1 protein: implications for a mechanism for rapid molecular assembly. Proc. Natl. Acad. Sci. USA 1990, 87:8403-8407.
21. Portman D.S., Dreyfuss G. RNA annealing activities in HeLa nuclei. EMBO J. 1994, 13:213-221.
22. Rothrock C., Cannon B., Hahm B., Lynch K.W. A conserved signal-responsive sequence mediates activation-induced alternative splicing of CD45. Mol. Cell 2003, 12:1317-1324.
23. Rothrock C.R., House A.E., Lynch K.W. HnRNP L represses exon splicing via a regulated exonic splicing silencer. EMBO J. 2005, 24:2792-2802.
24. Roybal G.A., Jurica M.S. Spliceostatin A inhibits spliceosome assembly subsequent to prespliceosome formation. Nucleic Acids Res. 2010, 38:6664-6672.
25. Schneider M., Hsiao H.H., Will C.L., Giet R., Urlaub H., Lührmann R. Human PRP4 kinase is required for stable tri-snRNP association during spliceosomal B complex formation. Nat. Struct. Mol. Biol. 2010, 17:216-221.
26. Schneider M., Will C.L., Anokhina M., Tazi J., Urlaub H., Lührmann R. Exon definition complexes contain the tri-snRNP and can be directly converted into B-like precatalytic splicing complexes. Mol. Cell 2010, 38:223-235.
27. Sharma S., Falick A.M., Black D.L. Polypyrimidine tract binding protein blocks the 5' splice site-dependent assembly of U2AF and the prespliceosomal E complex. Mol. Cell 2005, 19:485-496.
28. Sharma S., Maris C., Allain F.H., Black D.L. U1 snRNA directly interacts with polypyrimidine tract-binding protein during splicing repression. Mol. Cell 2011, 41:579-588.
29. Smith D.J., Query C.C., Konarska M.M. " Nought may endure but mutability" : spliceosome dynamics and the regulation of splicing. Mol. Cell 2008, 30:657-666.
30. Staley J.P., Guthrie C. An RNA switch at the 5' splice site requires ATP and the DEAD box protein Prp28p. Mol. Cell 1999, 3:55-64.
31. Tong A., Nguyen J., Lynch K.W. Differential expression of CD45 isoforms is controlled by the combined activity of basal and inducible splicing-regulatory elements in each of the variable exons. J. Biol. Chem. 2005, 280:38297-38304.
32. Wahl M.C., Will C.L., Lührmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009, 136:701-718.
33. Yu Y., Maroney P.A., Denker J.A., Zhang X.H., Dybkov O., Lührmann R., Jankowsky E., Chasin L.A., Nilsen T.W. Dynamic regulation of alternative splicing by silencers that modulate 5' splice site competition. Cell 2008, 135:1224-1236.
34. Zhou Z., Sim J., Griffith J., Reed R. Purification and electron microscopic visualization of functional human spliceosomes. Proc. Natl. Acad. Sci. USA 2002, 99:12203-12207.