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

Volumn 9, Issue 1, 2003, Pages 62-76

  Aphasizhev, Ruslan ^a   Aphasizheva, Inna ^a   Nelson, Robert E ^a   Simpson, Larry ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

RNA annealing; RNA binding proteins; RNA editing; Trypanosomes

Indexed keywords

BACTERIAL PROTEIN; COMPLEMENTARY RNA; MESSENGER RNA; NUCLEOTIDE DERIVATIVE; PROTEIN GBP21; PROTEIN GBP25; PROTEIN GBP27; PROTEIN GBP29; PROTEIN LTP26; PROTEIN LTP28; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN; RNA; RNA BINDING PROTEIN; THIOURIDINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; CRITHIDIA FASCICULATA; CROSS LINKING; GENE EXPRESSION; GENETIC TRANSFECTION; LEISHMANIA TARENTOLAE; MITOCHONDRION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEIN RNA BINDING; PROTEIN STABILITY; RNA ANALYSIS; RNA EDITING; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATALYSIS; LEISHMANIA; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PRECIPITIN TESTS; RNA EDITING; RNA, PROTOZOAN; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TWO-HYBRID SYSTEM TECHNIQUES;

BACTERIA (MICROORGANISMS); CRITHIDIA FASCICULATA; LEISHMANIA TARENTOLAE; PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0037276124     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.2134303     Document Type: Article

References (40)

1. Allen, T.E., Heidmann, S., Reed, R., Myler, P.J., Goringer, H.U., and Stuart, K.D. 1998. Association of guide RNA binding protein gBP21 with active RNA editing complexes in Trypanosoma brucei. Mol. Cell. Biol. 18: 6014-6022.
2. Aphasizhev, R. and Simpson, L. 2001. Isolation and characterization of a U-specific 3′-5′ exonuclease from mitochondria of Leishmania tarentolae. J. Biol. Chem. 276: 21280-21284.
3. 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.
4. Blom, D., Burg, J., Breek, C.K., Speijer, D., Muijsers, A.O., and Benne, R. 2001. Cloning and characterization of two guide RNA-binding proteins from mitochondria of Crithidia fasciculata: gBP27, a novel protein, and gBP29, the orthologue of Trypanosoma brucei gBP21. Nucleic Acids Res. 29: 2950-2962.
5. 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.
6. Braly, P., Simpson, L., and Kretzer, F. 1974. Isolation of kinetoplast-mitochondrial complexes from Leishmania tarentolae. J. Protozool. 21: 782-790.
7. Bringaud, F., Peris, M., Zen, K.H., and Simpson, L. 1995. Characterization of two nuclear-encoded protein components of mitochondrial ribonucleoprotein complexes from Leishmania tarentolae. Mol. Biochem. Parasitol. 71: 65-79.
8. Bringaud, F., Stripecke, R., Frech, G.C., Freedland, S., Turck, C., Byrne, E.M., and Simpson, L. 1997. Mitochondrial glutamate dehydrogenase from Leishmania tarentolae is a guide RNA-binding protein. Mol. Cell. Biol. 17: 3915-3923.
9. Byrne, E.M., Connell, G.J., and Simpson, L. 1996. Guide RNA-directed uridine insertion RNA editing in vitro. EMBO J. 15, 6758-6765.
10. Chien, C.T., Bartel, P.L., Sternglanz, R., and Fields, S. 1991. The two-hybrid system: A method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. 88: 9578-9582.
11. Corell, R.A., Read, L.K., Riley, G.R., Nellissery, J.K., Allen, T.E., Kable, M.L., Wachal, M.D., Seiwert, S.D., Myler, P.J., and Stuart, K.D. 1996. Complexes from Trypanosoma brucei that exhibit deletion editing and other editing-associated properties. Mol. Cell. Biol. 16: 1410-1418.
12. 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.
13. Estévez, A.M., Kierszenbaum, F., Wirtz, E., Bringaud, F., Grunstein, J., and Simpson, L. 1999. Knockout of the glutamate dehydrogenase gene in bloodstream Trypanosoma brucei in culture has no effect on editing of mitochondrial mRNAs. Mol. Biochem. Parasitol. 100: 5-17.
14. Favre, A., Moreno, G., Blondel, M.O., Kliber, J., Vinzens, F., and Salet, C. 1986. 4-Thiouridine photosensitized RNA-protein crosslinking in mammalian cells. Biochem. Biophys. Res. Commun. 141: 847-854.
15. 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.
16. 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.
17. Igo, 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.
18. Kapushoc, S.T. and Simpson, L. 1999. In vitro uridine insertion RNA editing mediated by cis-acting guide RNAs. RNA 5: 656-669.
19. Kim, C.H. and Abelson, J. 1996. Site-specific crosslinks of yeast U6 snRNA to the pre-mRNA near the 5′ splice site. RNA 2: 995-1010.
20. Koller, J., Muller, U.F., Schmid, B., Missel, A., Kruft, V., Stuart, K., and Goringer, H.U. 1997. Trypanosoma brucei gBP21. An arginine-rich mitochondrial protein that binds to guide RNA with high affinity. J. Biol. Chem. 272: 3749-3757.
21. Köller, J., Nörskau, G., Paul, A.S., Stuart, K., and Goringer, H.U. 1994. Different Trypanosoma brucei guide RNA molecules associate with an identical complement of mitochondrial proteins in vitro. Nucleic Acids Res. 22: 1988-1995.
22. Lambert, L., Muller, U.F., Souza, A.E., and Goringer, H.U. 1999. The involvement of gRNA-binding protein gBP21 in RNA editing-an in vitro and in vivo analysis. Nucleic Acids Res. 27: 1429-1436.
23. LeBowitz, J.H., Coburn, C.M., McMahon-Pratt, D., and Beverley, S.M. 1990. Development of a stable Leishmania expression vector and application to the study of parasite surface antigen genes. Proc. Natl. Acad. Sci. 87: 9736-9740.
24. Leegwater, P., Speijer, D., Benne, R. 1995. Identification by UV cross-linking of oligo (U)-binding proteins in mitochondria of the insect trypanosomatid Crithidia fasciculata. Eur. J. Biochem. 227: 780-786.
25. 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.
26. 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.
27. Muller, U.F., Lambert, L., and Goringer, H.U. 2001. Annealing of RNA editing substrates facilitated by guide RNA-binding protein gBP21. EMBO J. 20:1394-1404.
28. Panigrahi, A.K., Gygi, S.P., Ernst, N.L., Igo, R.P., Palazzo, S.S., Schnaufer, A., Weston, D.S., Carmean, N., Salavati, R., Aebersold, R., et al. 2001. Association of two novel proteins, TbMP52 and TbMP48, with the Trypanosoma brucei RNA editing complex. Mol. Cell. Biol. 21: 380-389.
29. Pelletier, M., Miller, M.M., and Read, L.K. 2000. RNA-binding properties of the mitochondrial Y-box protein RBP16. Nucleic Acids Res. 28: 1266-1275.
30. Peris, M., Frech, G.C., Simpson, A.M., Bringaud, F., Byrne, E., Bakker, A., and Simpson, L. 1994. Characterization of two classes of ribonucleoprotein complexes possibly involved in RNA editing from Leishmania tarentolae mitochondria. EMBO J. 13: 1664-1672.
31. Peris, M., Simpson, A.M., Grunstein, J., Liliental, J.E., Frech, G.C., and Simpson, L. 1997. Native gel analysis of ribonucleoprotein complexes from a Leishmania tarentolae mitochondrial extract. Mol. Biochem. Parasitol. 85: 9-24.
32. Pollard, V.W., Harris, M.E., Hajduk, S.L. 1992. Native mRNA editing complexes from Trypanosoma brucei mitochondria. EMBO J. 11: 4429-4438.
33. Portman, D.S. and Dreyfuss, G. 1994. RNA annealing activities in HeLa nuclei. EMBO J. 13: 213-221.
34. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado-Nilsson, E., Wilm, M., and Seraphin, B. 2001. The tandem affinity purification (TAP) method: A general procedure of protein complex purification. Methods 24: 218-229.
35. 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.
36. Sabatini, R. and Hajduk, S.L. 1995. RNA ligase and its involvement in guide RNA/mRNA chimera formation. J. Biol. Chem. 270: 7233-7240.
37. Schnaufer, A., Panigrahi, A.K., Panicucci, B., Igo, 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: 2159-2161.
38. Seiwert, S.D., Heidmann, S., and Stuart, K. 1996. Direct visualization of uridylate deletion in vitro suggests a mechanism for kinetoplastid RNA editing. Cell 84: 831-841.
39. Simpson, L. and Kretzer, F. 1997. The mitochondrion in dividing Leishmania tarentolae cells is symmetric and becomes a single asymmetric tubule in non-dividing cells due to division of the kinetoplast portion. Mol. Biochem. Parasitol. 87: 71-78.
40. 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 co-localizes with an in vitro RNA editing activity. J. Biol. Chem. 273: 21825-21833.