Trypanosoma brucei RNA editing protein TbMP42 (band VI) is crucial for the endonucleolytic cleavages but not the subsequent steps of U-deletion and U-insertion

RNA

Volumn 14, Issue 6, 2008, Pages 1187-1200

  Law, Julie A ^a,b   O'Hearn, Sean F ^a,c   Sollner Webb, Barbara ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

RNA editing; RNA interference; TbMP42; Trypanosome; U deletion; U insertion

Indexed keywords

ENDONUCLEASE; EXODEOXYRIBONUCLEASE III; MEMBRANE PROTEIN; PROTEIN; RNA; RNA INDUCED SILENCING COMPLEX; RNA LIGASE;

ARTICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RNA CLEAVAGE; RNA EDITING; RNA EXTRACTION; RNA INTERFERENCE; RNA RECOMBINATION; TRYPANOSOMA BRUCEI;

ANIMALS; CELL EXTRACTS; CELL LINE; ENDORIBONUCLEASES; MUTAGENESIS, INSERTIONAL; PROTOZOAN PROTEINS; RIBONUCLEOPROTEINS; RNA; RNA EDITING; RNA INTERFERENCE; SEQUENCE DELETION; TRYPANOSOMA BRUCEI BRUCEI;

TRYPANOSOMA BRUCEI;

EID: 44149103662     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.899508     Document Type: Article

References (67)

1. Alfonzo, J.D., Thiemann, O., and Simpson, L. 1997. The mechanism of U-insertion/deletion RNA editing in kinetoplastid mitochondria. Nucleic Acids Res. 25: 3751-3759. doi: 10.1093/nar/25.19.3751.
2. 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.
3. 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.
4. Aphasizhev, R., Aphasizheva, I., Nelson, R.E., and Simpson, L. 2003b. A 100-kDa 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.
5. Aphasizhev, R., Aphasizheva, I., and Simpson, L. 2003c. A tale of two TUTases. Proc. Natl. Acad. Sci. 100: 10617-10622.
6. Babbarwal, V.K., Fleck, M., Ernst, N.L., Schnaufer, A., and Stuart, K. 2007. An essential role of KREPB4 in RNA editing and structural integrity of the editosome in Trypanosoma brucei. RNA 13: 737-744.
7. Bakalara, N., Simpson, A.M., and Simpson, L. 1989. The Leishmania kinetoplast-mitochondrion contains terminal uridylyltransferase and RNA ligase activities. J. Biol. Chem. 264: 18679-18686.
8. Blum, B., Bakalara, N., and Simpson, L. 1990. A model for RNA editing in kinetoplastid mitochondria: "Guide" RNA molecules transcribed from maxicircle DNA provide the edited information. Cell 60: 189-198.
9. 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.
10. Byrne, E.M., Connell, G.J., and Simpson, L. 1996. Guide RNA-directed uridine insertion RNA editing in vitro. EMBO J. 15: 6758-6765.
11. Carnes, J., Trotter, J.R., Ernst, N.L., Steinberg, A., and Stuart, K. 2005. An essential RNase III insertion editing endonuclease in Trypanosoma brucei. Proc. Natl. Acad. Sci. 102: 16614-16619.
12. Carnes, J., Trotter, J.R., Peltan, A., Fleck, M., and Stuart, K. 2008. RNA editing in Trypanosoma brucei requires three different editosomes. Mol. Cell. Biol. 28: 122-130.
13. Cruz-Reyes, J. and Sollner-Webb, B. 1996. Trypanosome U-deletional RNA editing involves guide RNA-directed endonuclease cleavage, terminal U exonuclease, and RNA ligase activities. Proc. Natl. Acad. Sci. 93: 8901-8906.
14. Cruz-Reyes, J., Piller, K.J., Rusche, L.N., Mukherjee, M., and Sollner-Webb, B. 1998a. Unexpected electrophoretic migration of RNA with different 3′ termini causes a RNA sizing ambiguity that can be resolved using nuclease P1-generated sequencing ladders. Biochemistry 37: 6059-6064.
15. Cruz-Reyes, J., Rusche, L.N., Piller, K.J., and Sollner-Webb, B. 1998b. T. brucei RNA editing: Adenosine nucleotides inversely affect U-deletion and U-insertion reactions at mRNA cleavage. Mol. Cell 1: 401-409.
16. Cruz-Reyes, J., Rusche, L.N., and Sollner-Webb, B. 1998c. Trypanosoma brucei U insertion and U-deletion activities co-purify with an enzymatic editing complex but are differentially optimized. Nucleic Acids Res. 26: 3634-3639. doi: 10.1093/nar/26.16.3634.
17. Cruz-Reyes, J., Zhelonkina, A.G., Huang, C.E., and Sollner-Webb, B. 2002. Distinct functions of two RNA ligases in active Trypanosoma brucei RNA editing complexes. Mol. Cell. Biol. 22: 4652-4660.
18. 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.
19. 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.
20. Feagin, J.E., Abraham, J.M., and Stuart, K. 1988. Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell 53: 413-422.
21. 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.
22. Gao, G., Simpson, A.M., Kang, X., Rogers, K., Nebohacova, M., Li, F., and Simpson, L. 2005. Functional complementation of Trypanosoma brucei RNA in vitro editing with recombinant RNA ligase. Proc. Natl. Acad. Sci. 102: 4712-4717.
23. Harris, M.E., Moore, D.R., and Hajduk, S.L. 1990. Addition of uridines to edited RNAs in trypanosome mitochondria occurs independently of transcription. J. Biol. Chem. 265: 11368-11376.
24. 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.
25. 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.
26. Igo Jr., R.P., Palazzo, S.S., Burgess, M.L., Panigrahi, A.K., and Stuart, K. 2000. Uridylate addition and RNA ligation contribute to the specificity of kinetoplastid insertion RNA editing. Mol. Cell. Biol. 20: 8447-8457.
27. 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.
28. Kable, M.L., Seiwert, S.D., Heidmann, S., and Stuart, K. 1996. RNA editing: A mechanism for gRNA-specified uridylate insertion into precursor mRNA. Science 273: 1189-1195.
29. Kang, X., Falick, A.M., Nelson, R.E., Gao, G., Rogers, K., Aphasizhev, R., and Simpson, L. 2004. Disruption of the zinc finger motifs in the Leishmania tarentolae LC-4 (=TbMP63) L-complex editing protein affects the stability of the L-complex. J. Biol. Chem. 279: 3893-3899.
30. 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.
31. 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. 19: 13944-13949.
32. Law, J.A., Huang, C.E., O'Hearn, S.F., and Sollner-Webb, B. 2005. In Trypanosoma brucei RNA editing, band II enables recognition specifically at each step of the U insertion cycle. Mol. Cell. Biol. 25: 2785-2794.
33. Law, J.A., O'Hearn, S., and Sollner-Webb, B. 2007. In Trypanosoma brucei RNA editing, TbMP18 (band VII) is critical for editosome integrity and for both insertional and deletional cleavages. Mol. Cell. Biol. 27: 777-787.
34. Madison-Antenucci, S., Sabatini, R.S., Pollard, V.W., and Hajduk, S.L. 1998. Kinetoplastid RNA-editing-associated protein 1 (REAP-1): A novel editing complex protein with repetitive domains. EMBO J. 17: 6368-6376.
35. McManus, M.T., Adler, B.K., Pollard, V.W., and Hajduk, S.L. 2000. Trypanosoma brucei guide RNA poly(U) tail formation is stabilized by cognate mRNA. Mol. Cell. Biol. 20: 883-891.
36. 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.
37. Missel, A., Souza, A.E., Nörskau, G., and Göringer, H.U. 1997. Disruption of a gene encoding a novel mitochondrial DEAD-box protein in Trypanosoma brucei affects edited mRNAs. Mol. Cell. Biol. 17: 4895-4903.
38. 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. doi: 10.1093/nar/30.2.447.
39. Müller, U.F., Lambert, L., and Göringer, H.U. 2001. Annealing of RNA editing substrates facilitated by guide RNA-binding protein gBP21. EMBO J. 20: 1394-1404.
40. O'Hearn, S.F., 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.
41. Panigrahi, A.K., Gygi, S.P., Ernst, N.L., Igo Jr., R.P., Palazzo, S.S., Schnaufer, A., Weston, D.S., 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.
42. 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.
43. Panigrahi, A.K., Allen, T.E., Stuart, K., Haynes, P.A., and Gygi, S.P. 2003a. Mass spectrometric analysis of the editosome and other multiprotein complexes in Trypanosoma brucei. J. Am. Soc. Mass Spectrom. 14: 728-735.
44. 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.
45. 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.
46. 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.
47. Pollard, V.W., Harris, M.E., and Hajduk, S.L. 1992. Native mRNA editing complexes from Trypanosoma brucei mitochondria. EMBO J. 11: 4429-4438.
48. Rogers, K., Gao, G., and Simpson, L. 2007. U-specific 3′-5′ exoribonucleases involved in U-deletion RNA editing in trypanosomatid mitochondria. J. Biol. Chem. 282: 29073-29080.
49. 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.
50. Rusche, 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.
51. Sabatini, R. and Hajduk, S.L. 1995. RNA ligase and its involvement in guide RNA/mRNA chimera formation. Evidence for a cleavage-ligation mechanism of Trypanosoma brucei mRNA editing. J. Biol. Chem. 270: 7233-7240.
52. Sabatini, R.S., Adler, B.K., Madison-Antenucci, S., McManus, M.T., and Hajduk, S.L. 1998. Biochemical methods for analysis of kinetoplastid RNA editing. Methods 15: 15-26.
53. 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.
54. Schnaufer, A., Panigrahi, A.K., Panicucci, B., Igo Jr., R.P., Wirtz, E., 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.
55. Schnaufer, A., Ernst, N.L., Palazzo, S.S., 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.
56. Schumacher, M.A., Karamooz, E., Zikova, A., Trantirek, L., and Lukes, J. 2006. Crystal structures of T. brucei MRP1/MRP2 guide-RNA binding complex reveal RNA matchmaking mechanism. Cell 126: 701-711.
57. Seiwert, S.D., Heidmann, S., and Stuart, K. 1996. Direct visualization of uridylate deletion in vitro suggests a mechanism for kineto-plastid RNA editing. Cell 84: 831-841.
58. Simpson, L., Sbicego, S., and Aphasizhev, R. 2003. Uridine insertion/deletion RNA editing in trypanosome mitochondria: A complex business. RNA 9: 265-276.
59. 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.
60. Stuart, K. and Panigrahi, A.K. 2002. RNA editing: Complexity and complications. Mol. Microbiol. 45: 591-596.
61. 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.
62. 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.
63. 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.
64. 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.
65. Wirtz, E., Leal, S., Ochatt, C., and Cross, G.A. 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.
66. 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. doi: 10.1093/nar/gkg870.
67. Zhelonkina, A.G., O'Hearn, S.F., Law, J.A., Cruz-Reyes, J., Huang, C.E., Alatortsev, V.S., and Sollner-Webb, B. 2006. T. brucei RNA editing: Action of the U-insertional TUTase within a U-deletion cycle. RNA 12: 476-487.