Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome

Genes and Development

Volumn 21, Issue 18, 2007, Pages 2312-2325

  Tanaka, Naoko ^a   Aronova, Anna ^a   Schwer, Beate ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

DEAH box helicase; Ntr1; Pre mRNA splicing; Prp43; Spliceosome

Indexed keywords

ADENOSINE TRIPHOSPHATE; HELICASE; MUTANT PROTEIN; PROTEIN; PROTEIN NTR1; PROTEIN PRP43; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVITY; INTRON; MISSENSE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SPLICEOSOME;

AMINO ACID SEQUENCE; DEAD-BOX RNA HELICASES; ENZYME ACTIVATION; INTRONS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA SPLICING; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPLICEOSOMES;

EID: 34548842257     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1580507     Document Type: Article

References (47)

1. Ansari, A. and Schwer, B. 1995. SLU7 and a novel activity, SSF1, act during the PRP16-dependent step of yeast pre-mRNA splicing. EMBO J. 14: 4001-4009.
2. Aravind, L. and Koonin, E.V. 1999. G-patch: A new conserved domain in eukaryotic RNA-processing proteins and type D retroviral polyproteins. Trends Biochem. Sci. 24: 342-344.
3. Arenas, J.E. and Abelson, J.N. 1997. Prp43: An RNA helicase-like factor involved in spliceosome disassembly. Proc. Natl. Acad. Sci. 94: 11798-11802.
4. Behzadnia, N., Golas, M.M., Hartmuth, K., Sander, B., Kastner, B., Deckert, J., Dube, P., Will, C.L., 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. Boon, K.L., Auchynnikava, T., Edwalds-Gilbert, G., Barrass, J.D., Droop, A.P., Dez, C., and Beggs, J.D. 2006. Yeast ntr1/ spp382 mediates prp43 function in postspliceosomes. Mol. Cell. Biol. 26: 6016-6023.
6. Burge, C.B., Tuschl, T.H., and Sharp, P.A. 1999. Splicing of precursors to mRNAs by the spliceosomes. In RNA world II (eds. R.F. Gesteland et al.), pp. 525-560. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
7. Burgess, S., Couto, J.R., and Guthrie, C. 1990. A putative ATP binding protein influences the fidelity of branchpoint recognition in yeast splicing. Cell 60: 705-717.
8. Campodonico, E. and Schwer, B. 2002. ATP-dependent remodeling of the spliceosome: Intragenic suppressors of release-defective mutants of Saccharomyces cerevisiae Prp22. Genetics 160: 407-415.
9. Chen, J.H. and Lin, R.J. 1990. The yeast PRP2 protein, a putative RNA-dependent ATPase, shares extensive sequence homology with two other pre-mRNA splicing factors. Nucleic Acids Res. 18: 6447.
10. Combs, D.J., Nagel, R.J., Ares Jr., M., and Stevens, S.W. 2006. Prp43p is a DEAH-box spliceosome disassembly factor essential for ribosome biogenesis. Mol. Cell. Biol. 26: 523-534.
11. Company, M., Arenas, J., and Abelson, J. 1991. Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes. Nature 349: 487-493.
12. Edwalds-Gilbert, G., Kim, D.H., Silverman, E., and Lin, R.J. 2004. Definition of a spliceosome interaction domain in yeast Prp2 ATPase. RNA 10: 210-220.
13. Gavin, A.C., Bosche, M., Krause, R., Grandi, P., Marziuch, M., Bauer, A., Schultz, J., Rick, J.M., Michon, A.M., Cruciat, C.M., et al. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141-147.
14. Hazbun, T.R., Malmstrom, L., Anderson, S., Graczyk, G.J., Fox, B., Riffle, M., Sardin, B.A., Aranda, J.D., McDonald, W.H., Chiu, C.H., et al. 2003. Assigning function to yeast proteins by integration of technologies. Mol. Cell 12: 1353-1365.
15. Howe, A.Y., Chase, R., Taremi, S.S., Risano, C., Beyer, B., Malcolm, B., and Lau, J.Y. 1999. A novel recombinant single-chain hepatitis C virus NS3-NS4A protein with improved helicase activity. Protein Sci. 8: 1332-1341.
16. James, S.A., Turner, W., and Schwer, B. 2002. How Slu7 and Prp18 cooperate in the second step of yeast pre-mRNA splicing. RNA 8: 1068-1077.
17. Jankowsky, E. and Bowers, H. 2006. Remodeling of ribonucleo-protein complexes with DExH/D RNA helicases. Nucleic Acids Res. 34: 4181-4188.
18. Jankowsky, E., Gross, C.H., Shuman, S., and Pyle, A.M. 2000. The DExH protein NPH-II is a processive and directional motor for unwinding RNA. Nature 403: 447-451.
19. Jurica, M.S. and Moore, M.J. 2003. Pre-mRNA splicing: Awash in a sea of proteins. Mol. Cell 12: 5-14.
20. Kim, S.H., Smith, J., Claude, A., and Lin, R.J. 1992. The purified yeast pre-mRNA splicing factor PRP2 is an RNA-dependent NTPase. EMBO J. 11: 2319-2326.
21. Krogan, N.J., Cagney, G., Yu, H., Zhong, G., Guo, X., Iqnatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A.B., et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
22. Lebaron, S., Froment, C., Fromont-Racine, M., Rain, J.C., Monsarrat, B., Caizergues-Ferrer, M., and Henry, Y. 2005. The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol. Cell Biol. 25: 9269-9282.
23. Leeds, N.B., Small, E.C., Hiley, S.L., Hughes, T.R., and Staley, J.P. 2006. The splicing factor Prp43p, a DEAH box ATPase, functions in ribosome biogenesis. Mol. Cell Biol. 26: 513-522.
24. Martin, A., Schneider, S., and Schwer, B. 2002. Prp43 is an essential RNA-dependent ATPase required for release of lariatintron from the spliceosome. J. Biol. Chem. 277: 17743-17750.
25. Noble, C.G. and Song, H. 2007. MLN51 stimulates the RNA-helicase activity of eIF4AIII. PLoS ONE. 3: e303. doi: 10.1371/journal.pone. 0000303.
26. Oberer, M., Marintchev, A., and Wagner, G. 2005. Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes & Dev. 19: 2212-2223.
27. Pandit, S., Lynn, B., and Rymond, B.C. 2006. Inhibition of a spliceosome turnover pathway suppresses splicing defects. Proc. Natl. Acad. Sci. 103: 13700-13705.
28. Pang, P.S., Jankowsky, E., Planet, P.J., and Pyle, A.M. 2002. The hepatitis C viral NS3 protein is a processive DNA helicase with cofactor enhanced RNA unwinding. EMBO J. 21: 1168-1176.
29. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M., and Séraphin, B. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17: 1030-1032.
30. Rogers Jr., G.W., Richter, N.J., Lima, W.F., and Merrick, W.C. 2001. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J. Biol. Chem. 276: 30914-30922.
31. Roy, J., Kim, K., Maddock, J.R., Anthony, J.G., and Woolford Jr., J.L. 1995. The final stages of spliceosome maturation require Spp2p that can interact with the DEAH box protein Prp2p and promote step 1 of splicing. RNA 1: 375-390.
32. Ruskin, B. and Green, M. 1985. An RNA processing activity that debranches RNA lariats. Science 229: 135-140.
33. Schneider, S., Campodonico, E., and Schwer, B. 2004. Motifs IV and V in the DEAH box splicing factor Prp22 are important for RNA unwinding, and helicase-defective Prp22 mutants are suppressed by Prp8. J. Biol. Chem. 279: 8617-8626.
34. Schwer, B. and Meszaros, T. 2000. RNA helicase dynamics in pre-mRNA splicing. EMBO J. 19: 6582-6591.
35. Shuman, S. 1992. Vaccinia virus RNA helicase: An essential enzyme related to the DE-H family of RNA-dependent NTPases. Proc. Natl. Acad. Sci. 89: 10935-10939.
36. Silverman, E., Edwalds-Gilbert, G., and Lin, R.J. 2003. DExD/ H-box proteins and their partners: Helping RNA helicases unwind. Gene 312: 1-16.
37. Silverman, E.J., Maeda, A., Wei, J., Smith, P., Beggs, J.D., and Lin, R.J. 2004. Interaction between a G-patch protein and a spliceosomal DEXD/H-box ATPase that is critical for splicing. Mol. Cell. Biol. 24: 10101-10110.
38. Small, E.C., Leggett, S.R., Winans, A.A., and Staley, J.P. 2006. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol. Cell 23: 389-399.
39. Staley, J.P. and Guthrie, C. 1998. Mechanical devices of the spliceosome: Motors, clocks, springs, and things. Cell 92: 315-326.
40. Sugimoto, N., Nakano, S., Katoh, M., Matsumura, A., Nakamuta, H., Ohmichi, T., Yoneyama, M., and Sasaki, M. 1995. Thermodynamic parameters to predict stability of RNA/ DNA hybrid duplexes. Biochemistry 34: 11211-11216.
41. Tanaka, N. and Schwer, B. 2005. Characterization of the NTPase, RNA-binding, and RNA helicase activities of the DEAH-box splicing factor Prp22. Biochemistry 44: 9795-9803.
42. Tanaka, N. and Schwer, B. 2006. Mutations in PRP43 that uncouple RNA-dependent NTPase activity and pre-mRNA splicing function. Biochemistry 45: 6510-6521.
43. Tanner, N.K. and Linder, P. 2001. DExD/H box RNA helicases: From generic motors to specific dissociation functions. Mol. Cell 8: 251-262.
44. Tsai, R.T., Fu, R.H., Yeh, F.L., Tseng, C.K., Lin, Y.C., Huang, Y.H., and Cheng, S.C. 2005. Spliceosome disassembly catalyzed by Prp43 and its associated components Ntr1 and Ntr2. Genes & Dev. 19: 2991-3003.
45. Valadkhan, S. 2005. snRNAs as the catalysts of pre-mRNA splicing. Curr. Opin. Chem. Biol. 9: 603-608.
46. Will, C.L. and Lührmann, R. 2006. Spliceosome structure and function. In The RNA world (ed. R.F. Gesteland, T.R. Cech, and J.F. Atkins), pp. 369-400. Cold Spring Harbor Press, Cold Spring Harbor, NY.
47. Xie, J., Beickman, K., Otte, E., and Rymond, B.C. 1998. Progression through the spliceosome cycle requires Prp38p function for U4/U6 snRNA dissociation. EMBO J. 17: 2938-2946.