The KREPA3 zinc finger motifs and OB-fold domain are essential for RNA editing and survival of Trypanosoma brucei

Molecular and Cellular Biology

Volumn 28, Issue 22, 2008, Pages 6939-6953

  Guo, Xuemin ^a   Ernst, Nancy Lewis ^a   Stuart, Kenneth D ^a,b  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN KREPA3; UNCLASSIFIED DRUG; URACIL; ZINC FINGER PROTEIN;

ARTICLE; BACTERIAL SURVIVAL; CONTROLLED STUDY; GENE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; RNA EDITING; RNA INTERFERENCE; TRYPANOSOMA BRUCEI;

ANIMALS; DNA MUTATIONAL ANALYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; RIBONUCLEOPROTEINS; RNA EDITING; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI; ZINC FINGERS;

TRYPANOSOMA BRUCEI;

EID: 55849153500     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01115-08     Document Type: Article

References (62)

1. Agrawal, V., and K. V. Kishan. 2003. OB-fold: growing bigger with functional consistency. Curr. Protein Pept. Sci. 4:195-206.
2. Aphasizhev, R., I. Aphasizheva, R. E. Nelson, and L. Simpson. 2003. 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.
3. Aphasizhev, R., I. Aphasizheva, and L. Simpson. 2003. A tale of two TUTases. Proc. Natl. Acad. Sci. USA 100:10617-10622.
4. Babbarwal, V. K., M. Fleck, N. L. Ernst, A. Schnaufer, and K. D. Stuart. 2007. An essential role of KREPB4 in RNA editing and structural integrity of the editosome in Trypanosoma brucei. RNA 13:737-744.
5. Besteiro, S., M. P. Barrett, L. Riviere, and F. Bringaud. 2005. Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol. 21:185-191.
6. Blum, B., N. Bakalara, and L. Simpson. 1990. A model for RNA editing in kinetoplastid mitochondria: "guide" RNA molecules transcribed from maxicircle DNA provide the edited information. Cell 60:189-198.
7. Brayer, K. J., and D. J. Segal. 2008. Keep your fingers off my DNA: protein-protein interactions mediated by C2H2 zinc finger domains. Cell Biochem. Biophys. 50:111-131.
8. Brecht, M., M. Niemann, E. Schlüter, U. F. Müller, K. Stuart, and H. U. Göringer. 2005. TbMP42, a protein component of the RNA editing complex in African trypanosomes has endo-exoribonuclease activity. Mol. Cell 17: 621-630.
9. Carnes, J., and K. Stuart. 2007. Working together: the RNA editing machinery in Trypanosoma brucei, p. 143-164. In H. U. Göringer (ed.), RNA editing, vol. 20. Springer Verlag, Heidelberg, Germany.
10. Carnes, J., J. R. Trotter, N. L. Ernst, A. G. Steinberg, and K. Stuart. 2005. An essential RNase III insertion editing endonuclease in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA 102:16614-16619.
11. Carnes, J., J. R. Trotter, A. Peltan, M. Fleck, and K. Stuart. 2008. RNA editing in Trypanosoma brucei requires three different editosomes. Mol. Cell. Biol. 28:122-130.
12. Cruz-Reyes, J., and B. Sollner-Webb. 1996. Trypanosome U-deletional RNA editing involves guide RNA-directed endonuclease cleavage, terminal U exonuclease, and RNA ligase activities. Proc. Natl. Acad. Sci. USA 93:8901-8906.
13. Cruz-Reyes, J., A. Zhelonkina, L. Rusché, and B. Sollner-Webb. 2001. Trypanosome RNA editing: simple guide RNA features enhance U deletion 100-fold. Mol. Cell. Biol. 21:884-892.
14. Drozdz, M., S. S. Palazzo, R. Salavati, J. O'Rear, C. Clayton, and K. Stuart. 2002. TbMP81 is required for RNA editing in Trypanosoma brucei. EMBO J. 21:1791-1799.
15. Ernst, N. L., B. Panicucci, R. P. Igo, Jr., A. K. Panigrahi, R. Salavati, and K. Stuart. 2003. TbMP57 is a 3′ terminal uridylyl transferase (TUTase) of the Trypanosoma brucei editosome. Mol. Cell 11:1525-1536.
16. Gao, G., and L. Simpson. 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.
17. Hannaert, V., F. Bringaud, F. R. Opperdoes, and P. A. Michels. 2003. Evolution of energy metabolism and its compartmentation in Kinetoplastida. Kinetoplastid Biol. Dis. 2:11-40.
18. Harris, M. E., D. R. Moore, and S. L. Hajduk. 1990. Addition of uridines to edited RNAs in trypanosome mitochondria occurs independently of transcription. J. Biol. Chem. 265:11368-11376.
19. Huang, C. E., S. F. O'Hearn, and B. Sollner-Webb. 2002. Assembly and function of the RNA editing complex in Trypanosoma brucei requires band III protein. Mol. Cell. Biol. 22:3194-3203.
20. Igo, R. P., Jr., S. S. Palazzo, M. L. K. Burgess, A. K. Panigrahi, and K. Stuart. 2000. Uridylate addition and RNA ligation contribute to the specificity of kinteoplastid insertion RNA editing. Mol. Cell. Biol. 20:8447-8457.
21. Igo, R. P., Jr., D. S. Weston, N. L. Ernst, A. K. Panigrahi, R. Salavati, and K. Stuart. 2002. Role of uridylate-specific exoribonuclease activity in Trypanosoma brucei RNA editing. Eukaryot. Cell 1:112-118.
22. Iuchi, S. 2001. Three classes of C2H2 zinc finger proteins. Cell Mol. Life Sci. 58:625-635.
23. Jensen, B. C., C. T. Kifer, D. L. Brekken, A. C. Randall, Q. Wang, B. L. Drees, and M. Parsons. 2006. Characterization of protein kinase CK2 from Trypanosoma brucei. Mol. Biochem. Parasitol. 151:28-40.
24. Kable, M. L., S. D. Seiwert, S. Heidmann, and K. Stuart. 1996. RNA editing: a mechanism for gRNA-specified uridylate insertion into precursor mRNA. Science 273:1189-1195.
25. Kang, X., A. M. Falick, R. E. Nelson, G. Gao, K. Rogers, R. Aphasizhev, and L. Simpson. 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.
26. Kang, X., G. Gao, K. Rogers, A. M. Falick, S. Zhou, and L. Simpson. 2006. Reconstitution of full-round uridine-deletion RNA editing with three recombinant proteins. Proc. Natl. Acad. Sci. USA 103:13944- 13949.
27. Kang, X., K. Rogers, G. Gao, A. M. Falick, S. Zhou, and L. Simpson. 2005. Reconstitution of uridine-deletion precleaved RNA editing with two recombinant enzymes. Proc. Natl. Acad. Sci. USA 102:1017-1022.
28. Law, J. A., C. E. Huang, S. F. O'Hearn, and B. Sollner-Webb. 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.
29. Law, J. A., S. O'Hearn, and B. Sollner-Webb. 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.
30. Law, J. A., S. F. O'Hearn, and B. Sollner-Webb. 2008. 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. 14:1187-1200.
31. Lu, D., M. A. Searles, and A. Klug. 2003. Crystal structure of a zinc-finger-RNA complex reveals two modes of molecular recognition. Nature 426:96-100.
32. Madison-Antenucci, S., J. Grams, and S. L. Hajduk. 2002. Editing machines: the complexities of trypanosome RNA editing. Cell 108:435-438.
33. Miller, M. M., K. Halbig, J. Cruz-Reyes, and L. K. Read. 2006. RBP16 stimulates trypanosome RNA editing in vitro at an early step in the editing reaction. RNA 12:1292-1303.
34. Muller, U. F., L. Lambert, and H. U. Goringer. 2001. Annealing of RNA editing substrates facilitated by guide RNA-binding protein gBP21. EMBO J. 20:1394-1404.
35. Murzin, A. G. 1993. OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J. 12:861-867.
36. Niemann, M., M. Brecht, E. Schluter, K. Weitzel, M. Zacharias, and H. U. Goringer. 2008. TbMP42 is a structure-sensitive ribonuclease that likely follows a metal ion catalysis mechanism. Nucleic Acids Res. 36:4465-4473.
37. O'Hearn, S., C. E. Huang, M. Hemann, A. Zhelonkina, and B. Sollner-Webb. 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.
38. Panigrahi, A. K., N. L. Ernst, G. J. Domingo, M. Fleck, R. Salavati, and K. D. Stuart. 2006. Compositionally and functionally distinct editosomes in Trypanosoma brucei. RNA 12:1038-1049.
39. Panigrahi, A. K., A. Schnaufer, N. Carmean, R. P. Igo, Jr., S. P. Gygi, N. L. Ernst, S. S. Palazzo, D. S. Weston, R. Aebersold, R. Salavati, and K. D. Stuart. 2001. Four related proteins of the Trypanosoma brucei RNA editing complex. Mol. Cell. Biol. 21:6833-6840.
40. Panigrahi, A. K., A. Schnaufer, N. L. Ernst, B. Wang, N. Carmean, R. Salavati, and K. Stuart. 2003. Identification of novel components of Trypanosoma brucei editosomes. RNA 9:484-492.
41. Parker, H. L., T. Hill, K. Alexander, N. B. Murphy, W. R. Fish, and M. Parsons. 1995. Three genes and two isozymes: gene conversion and the compartmentalization and expression of the phosphoglycerate kinases of Trypanosoma (Nannomonas) congolense. Mol. Biochem. Parasitol. 69:269-279.
42. Pelletier, M., and L. K. Read. 2003. RBP16 is a multifunctional gene regulatory protein involved in editing and stabilization of specific mitochondrial mRNAs in Trypanosoma brucei. RNA 9:457-468.
43. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
44. Ramakers, C., J. M. Ruijter, R. H. L. Deprez, and A. F. M. Moorman. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339:62-66.
45. Rogers, K., G. Gao, and L. Simpson. 2007. Uridylate-specific 3′-5′ exoribonucleases involved in uridylate-deletion RNA editing in trypanosomatid mitochondria. J. Biol. Chem. 282:29073-29080.
46. Salavati, R., N. L. Ernst, J. O'Rear, T. Gilliam, S. Tarun, Jr., and K. Stuart. 2006. KREPA4, an RNA binding protein essential for editosome integrity and survival of Trypanosoma brucei. RNA 12:819-831.
47. Schnaufer, A., N. Ernst, J. O'Rear, R. Salavati, and K. Stuart. 2003. Separate insertion and deletion sub-complexes of the Trypanosoma brucei RNA editing complex. Mol. Cell 12:307-319.
48. Schnaufer, A., A. K. Panigrahi, B. Panicucci, R. P. Igo, Jr., R. Salavati, and K. Stuart. 2001. An RNA ligase essential for RNA editing and survival of the bloodstream form of Trypanosoma brucei. Science 291:2159-2162.
49. Seiwert, S. D., S. Heidmann, and K. Stuart. 1996. Direct visualization of uridylate deletion in vitro suggests a mechanism for kinetoplastid RNA editing. Cell 84:831-841.
50. Simpson, L., R. Aphasizhev, G. Gao, and X. Kang. 2004. Mitochondrial proteins and complexes in Leishmania and Trypanosoma involved in U-insertion/deletion RNA editing. RNA. 10:159-170.
51. Stefl, R., L. Skrisovska, and F. H. Allain. 2005. RNA sequence- and shape-dependent recognition by proteins in the ribonucleoprotein particle. EMBO Rep. 6:33-38.
52. Stuart, K., T. E. Allen, S. Heidmann, and S. D. Seiwert. 1997. RNA editing in kinetoplastid protozoa. Microbiol. Mol. Biol. Rev. 61:105-120.
53. Stuart, K. D., A. Schnaufer, N. L. Ernst, and A. K. Panigrahi. 2005. Complex management: RNA editing in trypanosomes. Trends Biochem. Sci. 30:97-105.
54. Tarun, S. Z., Jr., A. Schnaufer, N. L. Ernst, R. Proff, J. Deng, W. Hol, and K. Stuart. 2008. KREPA6 is an RNA binding protein essential for editosome integrity and survival of Trypanosoma brucei. RNA 14:347-358.
55. Theobald, D. L., R. M. Mitton-Fry, and D. S. Wuttke. 2003. Nucleic acid recognition by OB-fold proteins. Annu. Rev. Biophys. Biomol. Struct. 32: 115-133.
56. Trotter, J. R., N. L. Ernst, J. Carnes, B. Panicucci, and K. Stuart. 2005. A deletion site editing endonuclease in Trypanosoma brucei. Mol. Cell 20:403-412.
57. Vanhamme, L., D. Perez-Morga, C. Marchal, D. Speijer, L. Lambert, M. Geuskens, S. Alexandre, N. Ismaïli, U. Göringer, R. Benne, and E. Pays. 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.
58. Wang, B., N. L. Ernst, S. S. Palazzo, A. K. Panigrahi, R. Salavati, and K. Stuart. 2003. TbMP44 is essential for RNA editing and structural integrity of the editosome in Trypanosoma brucei. Eukaryot. Cell 2:578-587.
59. Wang, Z., J. C. Morris, M. E. Drew, and P. T. Englund. 2000. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 275:40174-40179.
60. Wirtz, E., S. Leal, C. Ochatt, and G. A. M. Cross. 1999. A tightly regulated inducible expression system for conditional gene knockouts and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:89-101.
61. Wolfe, S. A., L. Nekludova, and C. O. Pabo. 2000. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 29:183-212.
62. Worthey, E. A., A. Schnaufer, I. S. Mian, K. Stuart, and R. Salavati. 2003. Comparative analysis of editosome proteins in trypanosomatids. Nucleic Acids Res. 31:6392-6408.