An essential role of KREPB4 in RNA editing and structural integrity of the editosome in Trypanosoma brucei

RNA

Volumn 13, Issue 5, 2007, Pages 737-744

  Babbarwal, Vinod Kumar ^a,c   Fleck, Michele ^a   Ernst, Nancy Lewis ^a   Schnaufer, Achim ^a   Stuart, Kenneth ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Caterpillar Logistics Services India Pvt Ltd   (India)

Author keywords

Editosome; Endonuclease; RNA editing; RNase III; Trypanosoma brucei; Trypanosomatids

Indexed keywords

ENDONUCLEASE; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN; PROTEIN EDITOSOME; PROTEIN KREPB4; PROTEIN RBP16; PROTOZOAL PROTEIN; RIBONUCLEASE; RNA; RNA LIGASE; UNCLASSIFIED DRUG; URIDINE PHOSPHATE;

ARTICLE; CATALYSIS; CELL LYSATE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE INSERTION; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; RNA EDITING; RNA INTERFERENCE; RNA PROCESSING; RNA STRUCTURE; TRYPANOSOMA BRUCEI;

ANIMALS; CELL PROLIFERATION; ENDONUCLEASES; MACROMOLECULAR SUBSTANCES; PROTOZOAN PROTEINS; RIBONUCLEASE III; RNA EDITING; RNA, PROTOZOAN; RNA-BINDING PROTEINS; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 34247340565     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.327707     Document Type: Article

References (51)

1. Aphasizhev, R., Sbicego, S., Peris, M., Jang, S.H., Aphasizheva, I., Simpson, A.M., Rivlin, A., and Simpson, L. 2002. Trypanosome mitochondrial 3′-terminal uridylyl transferase (TUTase): The key enzyme in U-insertion/deletion RNA editing. Cell 108: 637-648.
2. Aphasizhev, R., Aphasizheva, I., Nelson, R.E., Gao, G., Simpson, A.M., Kang, X., Falick, A.M., Sbicego, S., and Simpson, L. 2003a. Isolation of a U-insertion/deletion editing complex from Leishmania tarentolae mitochondria. EMBO J. 22: 913-924.
3. Aphasizhev, R., Aphasizheva, I., Nelson, R.E., and Simpson, L. 2003b. A 100-kD complex of two RNA-binding proteins from mitochondria of Leishmania tarentolae catalyzes RNA annealing and interacts with several RNA editing components. RNA 9: 62-76.
4. Aphasizhev, R., Aphasizheva, I., and Simpson, L. 2003c. A tale of two TUTases. Proc. Natl. Acad. Sci. 100: 10617-10622.
5. Brecht, M., Niemann, M., Schlüter, E., Müller, U.F., Stuart, K., and Göringer, H.U. 2005. TbMP42, a protein component of the RNA editing complex in African trypanosomes has endo-exoribonuclease activity. Mol. Cell 17: 621-630.
6. Carnes, J., Trotter, J.R., Ernst, N.L., Steinberg, A.G., and Stuart, K. 2005. An essential RNase III insertion editing endonuclease in Trypanosoma brucei. Proc. Natl. Acad. Sci. 102: 16614-16619.
7. Cruz-Reyes, J., Zhelonkina, A., Rusché, L., and Sollner-Webb, B. 2001. Trypanosome RNA editing: Simple guide RNA features enhance U deletion 100-fold. Mol. Cell. Biol. 21: 884-892.
8. Deng, J., Ernst, N.L., Turley, S., Stuart, K.D., and Hol, W.G.J. 2005. Structural basis for UTP specificity of RNA Editing TUTases from Trypanosoma brucei. EMBO J. 24: 4007-4017.
9. Drozdz, M., Palazzo, S.S., Salavati, R., O'Rear, J., Clayton, C., and Stuart, K. 2002. TbMP81 is required for RNA editing in Trypanosoma brucei. EMBO J. 21: 1791-1799.
10. Ernst, N.L., Panicucci, B., Igo Jr., R.P., Panigrahi, A.K., Salavati, R., and Stuart, K. 2003. TbMP57 is a 3′-terminal uridylyl transferase (TUTase) of the Trypanosoma brucei editosome. Mol. Cell 11: 1525-1536.
11. Gan, J., Tropea, J.E., Austin, B.P., Court, D.L., Waugh, D.S., and Ji, X. 2006. Structural insight into the mechanism of double-stranded RNA processing by ribonuclease III. Cell 124: 355-366.
12. Gao, G. and Simpson, L. 2003. Is the Trypanosoma brucei REL1 RNA ligase specific for U-deletion RNA editing, and is the REL2 RNA ligase specific for U-insertion editing? J. Biol. Chem. 278: 27570-27574.
13. Hayman, M.L. and Read, L.K. 1999. Trypanosoma brucei RBP16 is a mitochondrial Y-box family protein with guide RNA binding activity. J. Biol. Chem. 274: 12067-12074.
14. Huang, C.E., Cruz-Reyes, J., Zhelonkina, A.G., O'Hearn, S., Wirtz, E., and Sollner-Webb, B. 2001. Roles for ligases in the RNA editing complex of Trypanosoma brucei: Band IV is needed for U-deletion and RNA repair. EMBO J. 20: 4694-4703.
15. Huang, C.E., O'Hearn, S.F., and Sollner-Webb, B. 2002. Assembly and function of the RNA editing complex in Trypanosoma brucei requires band III protein. Mol. Cell. Biol. 22: 3194-3203.
16. Igo Jr., R.P., Palazzo, S.S., Burgess, M.L.K., Panigrahi, A.K., and Stuart, K. 2000. Uridylate addition and RNA ligation contribute to the specificity of kinteoplastid insertion RNA editing. Mol. Cell. Biol. 20: 8447-8457.
17. Igo Jr., R.P., Weston, D.S., Ernst, N.L., Panigrahi, A.K., Salavati, R., and Stuart, K. 2002. Role of uridylate-specific exoribonuclease activity in Trypanosoma brucei RNA editing. Eukaryot. Cell 1: 112-118.
18. Kang, X., Rogers, K., Gao, G., Falick, A.M., Zhou, S., and Simpson, L. 2005. Reconstitution of uridine-deletion precleaved RNA editing with two recombinant enzymes. Proc. Natl. Acad. Sci. 102: 1017-1022.
19. Kang, X., Gao, G., Rogers, K., Falick, A.M., Zhou, S., and Simpson, L. 2006. Reconstitution of full-round uridine-deletion RNA editing with three recombinant proteins. Proc. Natl. Acad. Sci. 103: 13944-13949.
20. Madison-Antenucci, S. and Hajduk, S. 2001. RNA editing-associated protein 1 is an RNA binding protein with specificity for preedited mRNA. Mol. Cell 7: 879-886.
21. Madison-Antenucci, S., Grams, J., and Hajduk, S.L. 2002. Editing machines: The complexities of trypanosome RNA editing. Cell 108: 435-438.
22. McManus, M.T., Shimamura, M., Grams, J., and Hajduk, S.L. 2001. Identification of candidate mitochondrial RNA editing ligases from Trypanosoma brucei. RNA 7: 167-175.
23. Müller, U.F. and Göringer, H.U. 2002. Mechanism of the gBP21-mediated RNA/RNA annealing reaction: Matchmaking and charge reduction. Nucleic Acids Res. 30: 447-455.
24. O'Hearn, S., Huang, C.E., Hemann, M., Zhelonkina, A., and Sollner-Webb, B. 2003. Trypanosoma brucei RNA editing complex: Band II is structurally critical and maintains band V ligase, which is nonessential. Mol. Cell. Biol. 23: 7909-7919.
25. Palazzo, S.S., Panigrahi, A.K., Igo Jr., R.P., Salavati, R., and Stuart, K. 2003. Kinetoplastid RNA editing ligases: Complex association, characterization, and substrate requirements. Mol. Biochem. Parasitol. 127: 161-167.
26. Panigrahi, A.K., Gygi, S., Ernst, N., Igo Jr., R.P., Palazzo, S.S., Schnaufer, A., Weston, D., Carmean, N., Salavati, R., Aebersold, R., et al. 2001a. Association of two novel proteins, TbMP52 and TbMP48, with the Trypanosoma brucei RNA editing complex. Mol. Cell. Biol. 21: 380-389.
27. Panigrahi, A.K., Schnaufer, A., Carmean, N., Igo Jr., R.P., Gygi, S.P., Ernst, N.L., Palazzo, S.S., Weston, D.S., Aebersold, R., Salavati, R., et al. 2001b. Four related proteins of the Trypanosoma brucei RNA editing complex. Mol. Cell. Biol. 21: 6833-6840.
28. Panigrahi, A.K., Allen, T.E., Haynes, P.A., Gygi, S.P., and Stuart, K. 2003a. Mass spectrometric analysis of the editosome and other multiprotein complexes in Trypanosoma brucei. J. Am. Soc. Mass Spectrom. 14: 728-735.
29. Panigrahi, A.K., Schnaufer, A., Ernst, N.L., Wang, B., Carmean, N., Salavati, R., and Stuart, K. 2003b. Identification of novel components of Trypanosoma brucei editosomes. RNA 9: 484-492.
30. Panigrahi, A.K., Ernst, N.L., Domingo, G.J., Fleck, M., Salavati, R., and Stuart, K.D. 2006. Compositionally and functionally distinct editosomes in Trypanosoma brucei. RNA 12: 1038-1049.
31. Pelletier, M. and Read, L.K. 2003. RBP16 is a multifunctional gene regulatory protein involved in editing and stabilization of specific mitochondrial mRNAs in Trypanosoma brucei. RNA 9: 457-468.
32. Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
33. Ramakers, C., Ruijter, J.M., Deprez, R.H.L., and Moorman, A.F.M. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339: 62-66.
34. Rusche, L.N., Cruz-Reyes, J., Piller, K.J., and Sollner-Webb, B. 1997. Purification of a functional enzymatic editing complex from Trypanosoma brucei mitochondria. EMBO J. 16: 4069-4081.
35. Rusché, L.N., Huang, C.E., Piller, K.J., Hemann, M., Wirtz, E., and Sollner-Webb, B. 2001. The two RNA ligases of the Trypanosoma brucei RNA editing complex: Cloning the essential band IV gene and identifying the band V gene. Mol. Cell. Biol. 21: 979-989.
36. Sabatini, R. and Hajduk, S.L. 1995. RNA ligase and its involvement in guide RNA/mRNA chimera formation. Evidence for a cleavageligation mechanism of Trypanosoma brucei mRNA editing. J. Biol. Chem. 270: 7233-7240.
37. Salavati, R., Ernst, N.L., O'Rear, J., Gilliam, T., Tarun Jr., S., and Stuart, K. 2006. KREPA4, an RNA binding protein essential for editosome integrity and survival of Trypanosoma brucei. RNA 12: 819-831.
38. Schnaufer, A., Panigrahi, A.K., Panicucci, B., Igo Jr., R.P., Salavati, R., and Stuart, K. 2001. An RNA ligase essential for RNA editing and survival of the bloodstream form of Trypanosoma brucei. Science 291: 2159-2162.
39. Schnaufer, A., Ernst, N., O'Rear, J., Salavati, R., and Stuart, K. 2003. Separate insertion and deletion subcomplexes of the Trypanosoma brucei RNA editing complex. Mol. Cell 12: 307-319.
40. Schumacher, M.A., Karamooz, E., Zikova, A., Trantirek, L., and Lukes, J. 2006. Crystal structures of Trypanosoma brucei MRP1/MRP2 guide-RNA-binding complex reveals RNA matchmaking mechanism. Cell 126: 701-711.
41. Simpson, L., Aphasizhev, R., Gao, G., and Kang, X. 2004. Mitochondrial proteins and complexes in Leishmania and Trypanosoma involved in U-insertion/deletion RNA editing. RNA 10: 159-170.
42. Stuart, K., Allen, T.E., Heidmann, S., and Seiwert, S.D. 1997. RNA editing in kinetoplastid protozoa. Microbiol. Mol. Biol. Rev. 61: 105-120.
43. Stuart, K.D., Panigrahi, A.K., Schnaufer, A., Drozdz, M., Clayton, C., and Salavati, R. 2002. Composition of the editing complex of Trypanosoma brucei. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357: 71-79.
44. Stuart, K.D., Schnaufer, A., Ernst, N.L., and Panigrahi, A.K. 2005. Complex management: RNA editing in trypanosomes. Trends Biochem. Sci. 30: 97-105.
45. Trotter, J.R., Ernst, N.L., Carnes, J., Panicucci, B., and Stuart, K. 2005. A deletion site editing endonuclease in Trypanosoma brucei. Mol. Cell 20: 403-412.
46. Vanhamme, L., Perez-Morga, D., Marchal, C., Speijer, D., Lambert, L., Geuskens, M., Alexandre, S., Ismaïli, N., Göringer, U., Benne, R., et al. 1998. Trypanosoma brucei TBRGG1, a mitochondrial oligo(u)-binding protein that colocalizes with an in vitro RNA editing activity. J. Biol. Chem. 273: 21825-21833.
47. Vondruskova, E., Van den Burg, J., Zikova, A., Ernst, N.L., Stuart, K., Benne, R., and Lukes, J. 2005. RNA interference analyses suggest a transcript-specific regulatory role for mitochondrial RNA-binding proteins MRP1 and MRP2 in RNA editing and other RNA processing in Trypanosoma brucei. J. Biol. Chem. 280: 2429-2438.
48. Wang, Z., Morris, J.C., Drew, M.E., and Englund, P.T. 2000. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275: 40174-40179.
49. Wang, B., Ernst, N.L., Palazzo, S.S., Panigrahi, A.K., Salavati, R., and Stuart, K. 2003. TbMP44 is essential for RNA editing and structural integrity of the editosome in Trypanosoma brucei. Eukaryot. Cell 2: 578-587.
50. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A.M. 1999. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99: 89-101.
51. Worthey, E.A., Schnaufer, A., Mian, I.S., Stuart, K., and Salavati, R. 2003. Comparative analysis of editosome proteins in trypanosomatids. Nucleic Acids Res. 31: 6392-6408.