Mitochondrial RNA processing in trypanosomes

Research in Microbiology

Volumn 162, Issue 7, 2011, Pages 655-663

  Aphasizhev, Ruslan ^a   Aphasizheva, Inna ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mitochondria; Polyadenylation; RNA editing; Translation; Trypanosoma

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL RNA; PENTATRICOPEPTIDE REPEAT PROTEIN; PEPTIDE DERIVATIVE; RNA EDITING TUTASE 1; UNCLASSIFIED DRUG;

ADENYLATION; ARTICLE; BIOGENESIS; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; RNA PROCESSING; RNA STABILITY; TRYPANOSOMA;

PROTOZOAN PROTEINS; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, PROTOZOAN; TRYPANOSOMA;

TRYPANOSOMA;

EID: 79960890415     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2011.04.015     Document Type: Article

References (78)

1. Acestor N., Panigrahi A.K., Carnes J., Zikova A., Stuart K.D. The MRB1 complex functions in kinetoplastid RNA processing. RNA 2009, 15:277-286.
2. Adler B.K., Harris M.E., Bertrand K.I., Hajduk S.L. Modification of Trypanosoma brucei mitochondrial rRNA by posttranscriptional 3′ polyuridine tail formation. Mol. Cell. Biol. 1991, 11:5878-5884.
3. Alfonzo J.D., Soll D. Mitochondrial tRNA import - the challenge to understand has just begun. Biol. Chem. 2009, 390:717-722.
4. Alfonzo J.D., Thiemann O.H., Simpson L. Purification and characterization of MAR1-A mitochondrial associated ribonuclease from Leishmania tarentolae. J. Biol. Chem. 1998, 273:30003-30011.
5. Aphasizhev R. RNA uridylyltransferases. Cell. Mol. Life Sci. 2005, 62:2194-2203.
6. Aphasizhev R., Aphasizheva I. Terminal RNA uridylyltransferases of trypanosomes. Biochim. Biophys. Acta 2008, 1779:270-280.
7. Aphasizhev, R., Aphasizheva, I. Uridine insertion/deletion mRNA editing in trypanosomes: a playground for non-templated information transfer. Wiley Interdiscip. Rev. RNA, in press. doi:10.1002/wrna.82.
8. Aphasizhev R., Aphasizheva I., Nelson R.E., Gao G., Simpson A.M., Kang X., Falick A.M., Sbicego S., Simpson L. Isolation of a U-insertion/deletion editing complex from Leishmania tarentolae mitochondria. EMBO J. 2003, 22:913-924.
9. Aphasizhev R., Aphasizheva I., Simpson L. A tale of two TUTases. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:10617-10622.
10. Aphasizhev R., Aphasizheva I., Simpson L. Multiple terminal uridylyltransferases of trypanosomes. FEBS Lett. 2004, 572:15-18.
11. Aphasizhev R., Sbicego S., Peris M., Jang S.H., Aphasizheva I., Simpson A.M., Rivlin A., Simpson L. Trypanosome mitochondrial 3′ terminal uridylyl transferase (TUTase): the key enzyme in U-insertion/deletion RNA editing. Cell 2002, 108:637-648.
12. Aphasizhev R., Simpson L. Isolation and characterization of a U-specific 3′-5′ exonuclease from mitochondria of Leishmania tarentolae. J. Biol. Chem. 2001, 276:21280-21284.
13. Aphasizheva I., Aphasizhev R. RET1-catalyzed uridylylation shapes the mitochondrial transcriptome in Trypanosoma brucei. Mol. Cell. Biol. 2010, 30:1555-1567.
14. Aphasizheva I., Maslov D., Wang X., Huang L., Aphasizhev R. Pentatricopeptide repeat proteins stimulate mRNA adenylation/uridylation to activate mitochondrial translation in trypanosomes. Mol. Cell 2011, 42:106-117.
15. Aphasizheva I., Ringpis G.E., Weng J., Gershon P.D., Lathrop R.H., Aphasizhev R. Novel TUTase associates with an editosome-like complex in mitochondria of Trypanosoma brucei. RNA 2009, 15:1322-1337.
16. Bakalara N., Simpson A.M., Simpson L. The Leishmania kinetoplast-mitochondrion contains terminal uridylyltransferase and RNA ligase activities. J. Biol. Chem. 1989, 264:18679-18686.
17. Bhat G.J., Myler P.J., Stuart K. The two ATPase 6 mRNAs of Leishmania tarentolae differ at their 3′ ends. Mol. Biochem. Parasitol. 1991, 48:139-150.
18. Bhat G.J., Souza A.E., Feagin J.E., Stuart K. Transcript-specific developmental regulation of polyadenylation in Trypanosoma brucei mitochondria. Mol. Biochem. Parasitol. 1992, 52:231-240.
19. Blom D., Burg J., Breek C.K., Speijer D., Muijsers A.O., Benne R. 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. 2001, 29:2950-2962.
20. Blum B., Bakalara N., Simpson L. A model for RNA editing in kinetoplastid mitochondria: "Guide" RNA molecules transcribed from maxicircle DNA provide the edited information. Cell 1990, 60:189-198.
21. Blum B., Simpson L. Guide RNAs in kinetoplastid mitochondria have a nonencoded 3′ oligo-(U) tail involved in recognition of the pre-edited region. Cell 1990, 62:391-397.
22. Brown S.V., Hosking P., Li J., Williams N. ATP synthase is responsible for maintaining mitochondrial membrane potential in bloodstream form Trypanosoma brucei. Eukaryot. Cell 2006, 5:45-53.
23. Clement S.L., Koslowsky D.J. Unusual organization of a developmentally regulated mitochondrial RNA polymerase (TBMTRNAP) gene in Trypanosoma brucei. Gene 2001, 272:209-218.
24. Clement S.L., Mingler M.K., Koslowsky D.J. An intragenic guide RNA location suggests a complex mechanism for mitochondrial gene expression in Trypanosoma brucei. Eukaryot. Cell 2004, 3:862-869.
25. Delannoy E., Stanley W.A., Bond C.S., Small I.D. Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem. Soc. Trans. 2007, 35:1643-1647.
26. El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., Caler E., Renauld H., et al. Comparative genomics of trypanosomatid parasitic protozoa. Science 2005, 309:404-409.
27. Etheridge R.D., Aphasizheva I., Gershon P.D., Aphasizhev R. 3′ adenylation determines mRNA abundance and monitors completion of RNA editing in T. brucei mitochondria. EMBO J. 2008, 27:1596-1608.
28. Etheridge R.D., Clemens D.M., Aphasizhev R. Identification and characterization of nuclear non-canonical poly(A) polymerases from Trypanosoma brucei. Mol. Biochem. Parasitol. 2009, 164:66-73.
29. Feagin J., Jasmer D., Stuart K. Developmentally regulated addition of nucleotides within apocytochrome b transcripts in Trypanosoma brucei. Cell 1987, 49:337-345.
30. Grams J., McManus M.T., Hajduk S.L. Processing of polycistronic guide RNAs is associated with RNA editing complexes in Trypanosoma brucei. EMBO J. 2000, 19:5525-5532.
31. Grams J., Morris J.C., Drew M.E., Wang Z., Englund P.T., Hajduk S.L. A trypanosome mitochondrial RNA polymerase is required for transcription and replication. J. Biol. Chem. 2002, 277:16952-16959.
32. Gray M.W., Lukes J., Archibald J.M., Keeling P.J., Doolittle W.F. Cell biology. Irremediable complexity?. Science 2010, 330:920-921.
33. Hajduk S., Ochsenreiter T. RNA editing in kinetoplastids. RNA Biol. 2010, 7:229-236.
34. Hashimi H., Cicova Z., Novotna L., Wen Y.Z., Lukes J. Kinetoplastid guide RNA biogenesis is dependent on subunits of the mitochondrial RNA binding complex 1 and mitochondrial RNA polymerase. RNA 2009, 15:588-599.
35. Hayman M.L., Read L.K. Trypanosoma brucei RBP16 is a mitochondrial Y-box family protein with guide RNA binding activity. J. Biol. Chem. 1999, 274:12067-12074.
36. Hernandez A., Madina B.R., Ro K., Wohlschlegel J.A., Willard B., Kinter M.T., Cruz-Reyes J. REH2 RNA helicase in kinetoplastid mitochondria: ribonucleoprotein complexes and essential motifs for unwinding and guide RNA (gRNA) binding. J. Biol. Chem. 2010, 285:1220-1228.
37. Hong M., Simpson L. Genomic organization of Trypanosoma brucei kinetoplast DNA minicircles. Protist 2003, 154:265-279.
38. Jasmer D., Stuart K. Sequence organization in African trypanosome minicircles is defined by 18 base pair inverted repeats. Mol. Biochem. Parasitol. 1986, 18:321-332.
39. Kao C.Y., Read L.K. Opposing effects of polyadenylation on the stability of edited and unedited mitochondrial RNAs in Trypanosoma brucei. Mol. Cell. Biol. 2005, 25:1634-1644.
40. Kao C.Y., Read L.K. Targeted depletion of a mitochondrial nucleotidyltransferase suggests the presence of multiple enzymes that polymerize mRNA 3′ tails in Trypanosoma brucei mitochondria. Mol. Biochem. Parasitol. 2007, 154:158-169.
41. Koslowsky D.J., Yahampath G. Mitochondrial mRNA 3′ cleavage polyadenylation and RNA editing in Trypanosoma brucei are independent events. Mol. Biochem. Parasitol. 1997, 90:81-94.
42. Lange H., Sement F.M., Canaday J., Gagliardi D. Polyadenylation-assisted RNA degradation processes in plants. Trends Plant Sci. 2009, 14:497-504.
43. Liu B., Liu Y., Motyka S.A., Agbo E.E., Englund P.T. Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol. 2005, 21:363-369.
44. Madej M.J., Alfonzo J.D., Huttenhofer A. Small ncRNA transcriptome analysis from kinetoplast mitochondria of Leishmania tarentolae. Nucleic Acids Res. 2007, 35:1544-1554.
45. Madej M.J., Niemann M., Huttenhofer A., Goringer H.U. Identification of novel guide RNAs from the mitochondria of Trypanosoma brucei. RNA Biol. 2008, 5:84-91.
46. Maslov D.A., Simpson L. The polarity of editing within a multiple gRNA-mediated domain is due to formation of anchors for upstream gRNAs by downstream editing. Cell 1992, 70:459-467.
47. Mattiacio J.L., Read L.K. Roles for TbDSS-1 in RNA surveillance and decay of maturation by-products from the 12S rRNA locus. Nucleic Acids Res. 2008, 36:319-329.
48. Michelotti E.F., Harris M.E., Adler B., Torri A.F., Hajduk S.L. Trypanosoma brucei mitochondrial ribosomal RNA synthesis, processing and developmentally regulated expression. Mol. Biochem. Parasitol. 1992, 54:31-42.
49. Militello K.T., Read L.K. Coordination of kRNA editing and polyadenylation in Trypanosoma brucei mitochondria: complete editing is not required for long poly(A) tract addition. Nucleic Acids Res. 1999, 27:1377-1385.
50. Militello K.T., Read L.K. UTP-dependent and -independent pathways of mRNA turnover in Trypanosoma brucei mitochondria. Mol. Cell. Biol. 2000, 20:2308-2316.
51. Ochsenreiter T., Cipriano M., Hajduk S.L. KISS: the kinetoplastid RNA editing sequence search tool. RNA 2007, 13:1-4.
52. Panigrahi A.K., Schnaufer A., Ernst N.L., Wang B., Carmean N., Salavati R., Stuart K. Identification of novel components of Trypanosoma brucei editosomes. RNA 2003, 9:484-492.
53. Panigrahi A.K., Zikova A., Dalley R.A., Acestor N., Ogata Y., Anupama A., Myler P.J., Stuart K.D. Mitochondrial complexes in Trypanosoma brucei: a novel complex and a unique oxidoreductase complex. Mol. Cell. Proteomics 2007, 7:534-545.
54. Pelletier M., Miller M.M., Read L.K. RNA-binding properties of the mitochondrial Y-box protein RBP16. Nucleic Acids Res. 2000, 28:1266-1275.
55. Pfalz J., Bayraktar O.A., Prikryl J., Barkan A. Site-specific binding of a PPR protein defines and stabilizes 5′ and 3′ mRNA termini in chloroplasts. EMBO J. 2009, 28:2042-2052.
56. Pollard V.W., Rohrer S.P., Michelotti E.F., Hancock K., Hajduk S.L. Organization of minicircle genes for guide RNAs in Trypanosoma brucei. Cell 1990, 63:783-790.
57. Prikryl J., Rojas M., Schuster G., Barkan A. Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl. Acad. Sci. U.S.A. 2010, 108:415-420.
58. Pusnik M., Small I., Read L.K., Fabbro T., Schneider A. Pentatricopeptide repeat proteins in Trypanosoma brucei function in mitochondrial ribosomes. Mol. Cell. Biol. 2007, 27:6876-6888.
59. Read L.K., Stankey K.A., Fish W.R., Muthiani A.M., Stuart K. Developmental regulation of RNA editing and polyadenylation in four life cycle stages of Trypanosoma congolense. Mol. Biochem. Parasitol. 1994, 68:297-306.
60. Ryan C.M., Kao C.Y., Sleve D.A., Read L.K. Biphasic decay of guide RNAs in Trypanosoma brucei. Mol. Biochem. Parasitol. 2006, 146:68-77.
61. Ryan C.M., Militello K.T., Read L.K. Polyadenylation regulates the stability of Trypanosoma brucei mitochondrial RNAs. J. Biol. Chem. 2003, 278:32753-32762.
62. Ryan C.M., Read L.K. UTP-dependent turnover of Trypanosoma brucei mitochondrial mRNA requires UTP polymerization and involves the RET1 TUTase. RNA 2005, 11:763-773.
63. Salavati R., Panigrahi A.K., Stuart K.D. Mitochondrial ribonuclease P activity of Trypanosoma brucei. Mol. Biochem. Parasitol. 2001, 115:109-117.
64. Schmitz-Linneweber C., Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 2008, 13:663-670.
65. Schnaufer A., Panigrahi A.K., Panicucci B., Igo R.P., Salavati R., Stuart K. An RNA ligase essential for RNA editing and survival of the bloodstream form of Trypanosoma brucei. Science 2001, 291:2159-2161.
66. Schnaufer A., Clark-Walker G.D., Steinberg A.G., Stuart K. The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J. 2005, 24:4029-4040.
67. Sloof P., De Haan A., Eier W., Van Iersel M., Boel E., Van Steeg H., Benne R. The nucleotide sequence of the variable region in Trypanosoma brucei completes the sequence analysis of the maxicircle component of mitochondrial kinetoplast DNA. Mol. Biochem. Parasitol. 1992, 56:289-300.
68. Small I.D., Peeters N. The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 2000, 25:46-47.
69. Stagno J., Aphasizheva I., Aphasizhev R., Luecke H. Dual role of the RNA substrate in selectivity and catalysis by terminal uridylyl transferases. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:14634-14639.
70. Stagno J., Aphasizheva I., Bruystens J., Luecke H., Aphasizhev R. Structure of the mitochondrial editosome-like complex associated TUTase 1 reveals divergent mechanisms of UTP selection and domain organization. J. Mol. Biol. 2010, 399:464-475.
71. Stagno J., Aphasizheva I., Rosengarth A., Luecke H., Aphasizhev R. UTP-bound and Apo structures of a minimal RNA uridylyltransferase. J. Mol. Biol. 2007, 366:882-899.
72. Stern D.B., Goldschmidt-Clermont M., Hanson M.R. Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 2010, 61:125-155.
73. Stuart K., Brun R., Croft S., Fairlamb A., Gurtler R.E., McKerrow J., Reed S., Tarleton R. Kinetoplastids: related protozoan pathogens, different diseases. J. Clin. Invest. 2008, 118:1301-1310.
74. Van Hellemond J.J., Opperdoes F.R., Tielens A.G. The extraordinary mitochondrion and unusual citric acid cycle in Trypanosoma brucei. Biochem. Soc. Trans. 2005, 33:967-971.
75. Vanhamme L., Perez-Morga D., Marchal C., Speijer D., Lambert L., Geuskens M., Alexandre S., Ismaïli N., Göringer U., Benne R., Pays E. Trypanosoma brucei TBRGG1, a mitochondrial oligo(U)-binding protein that co-localizes with an in vitro RNA editing activity. J. Biol. Chem. 1998, 273:21825-21833.
76. Wang Z., Morris J.C., Drew M.E., Englund P.T. Inhibition of Trypanosoma brucei gene expression by RNA interference using an integratable vector with opposing T7 promoters. J. Biol. Chem. 2000, 275:40174-40179.
77. Weng J., Aphasizheva I., Etheridge R.D., Huang L., Wang X., Falick A.M., Aphasizhev R. Guide RNA-binding complex from mitochondria of trypanosomatids. Mol. Cell. 2008, 32:198-209.
78. Zikova A., Panigrahi A.K., Dalley R.A., Acestor N., Anupama A., Ogata Y., Myler P.J., Stuart K. Trypanosoma brucei mitochondrial ribosomes: affinity purification and component identification by mass spectrometry. Mol. Cell. Proteomics 2008, 7:1286-1296.