Uridine insertion/deletion RNA editing in trypanosome mitochondria - A review

Gene

Volumn 240, Issue 2, 1999, Pages 247-260

  Estévez, Antonio M ^a   Simpson, Larry ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Cell Devmtl Biol Med M   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Kinetoplast DNA; L. tarentolae; Mitochondria; RNA editing; T. brucei

Indexed keywords

MITOCHONDRIAL DNA; RNA;

FRAMESHIFT MUTATION; GENE DELETION; GENE INSERTION; LEISHMANIA; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; REVIEW; RNA EDITING; STOP CODON; TRANSCRIPTION REGULATION; TRYPANOSOMA BRUCEI;

ANIMALS; BASE SEQUENCE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PROTOZOAN PROTEINS; RNA EDITING; RNA, GUIDE; RNA, PROTOZOAN; SEQUENCE DELETION; TRYPANOSOMATINA; URIDINE;

PROTOZOA; TRYPANOSOMA; TRYPANOSOMA BRUCEI;

EID: 0037922159     PISSN: 03781119     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-1119(99)00437-0     Document Type: Review

References (102)

1. Abraham J., Feagin J., Stuart K. Characterization of cytochrome c oxidase III transcripts that are edited only in the 3′ region. Cell. 55:1988;267-272.
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. 11:1991;5878-5884.
3. Alfonzo J.D., Thiemann O., Simpson L. The mechanism of U insertion/deletion RNA editing in kinetoplastid mitochondria. Nucleic Acids Res. 25:1997;3751-3759.
4. Alfonzo J.D., Thiemann O.H., Simpson L. Purification and characterization of MAR1 - A mitochondrial associated ribonuclease from Leishmania tarentolae. J. Biol. Chem. 273:1998;30003-30011.
5. Allen T.E., Heidmann S., Reed R., Myler P.J., Göringer H.U., Stuart K.D. Association of guide RNA binding protein gBP21 with active RNA editing complexes in Trypanosoma brucei. Mol. Cell. Biol. 18:1998;6014-6022.
6. Bakalara N., Simpson A.M., Simpson L. The Leishmania kinetoplast-mitochondrion contains terminal uridylyltransferase and RNA ligase activities. J. Biol. Chem. 264:1989;18679-18686.
7. Benne R., Van den Burg J., Brakenhoff J., Sloof P., Van Boom J., Tromp M. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 46:1986;819-826.
8. Bhat G.J., Koslowsky D.J., Feagin J.E., Smiley B.L., Stuart K. An extensively edited mitochondrial transcript in kinetoplastids encodes a protein homologous to ATPase subunit 6. Cell. 61:1990;885-894.
9. Bhat G.J., Souza A.E., Feagin J.E., Stuart K. Transcript-specific developmental regulation of polyadenylation in Trypanosoma brucei mitochondria. Mol. Biochem. Parasitol. 52:1992;231-240.
10. Blanc V., Aphasizhev R., Alfonzo J.D., Simpson L. The mitochondrial RNA ligase from Leishmania tarentolae can join RNA molecules bridged by a complementary RNA. J. Biol. Chem. 274:1999;24289-24296.
11. Blom D., De Haan A., Van den Berg M., Sloof P., Jirku M., Lukes J., Benne R. RNA editing in the free-living bodonid Bodo saltans. Nucleic Acids Res. 26:1998;1205-1213.
12. 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. 60:1990;189-198.
13. 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. 62:1990;391-397.
14. Blum B., Sturm N.R., Simpson A.M., Simpson L. Chimeric gRNA-mRNA molecules with oligo(U) tails covalently linked at sites of RNA editing suggest that U addition occurs by transesterification. Cell. 65:1991;543-550.
15. Bringaud F., Stripecke R., Frech G.C., Freedland S., Turck C., Byrne E.M., Simpson L. Mitochondrial glutamate dehydrogenase from Leishmania tarentolae is a guide RNA-binding protein. Mol. Cell. Biol. 17:1997;3915-3923.
16. Brown L.M., Burbach B.J., McKenzie B.A., Connell G.J. A cis-acting A-U sequence element induces kinetoplastid U-insertions. J. Biol. Chem. 274:1999;6295-6304.
17. Burgess M.L.K., Heidmann S., Stuart K. Kinetoplastid RNA editing does not require the terminal 3′ hydroxyl of guide RNA, but modifications to the guide RNA terminus can inhibit in vitro U insertion. RNA Publ. RNA Soc. 5:1999;883-892.
18. Byrne E., Bringaud F., Simpson L. RNA-protein interactions in the ribonucleoprotein T-complexes in a mitochondrial extract from Leishmania tarentolae. Mol. Biochem. Parasitol. 72:1995;65-76.
19. Byrne E.M., Connell G.J., Simpson L. Guide RNA-directed uridine insertion RNA editing in vitro. EMBO J. 15:1996;6758-6765.
20. Cech T.R. RNA editing: World's smallest introns. Cell. 64:1991;667-669.
21. Clayton C. Developmental regulation of nuclear gene expression in Trypanosoma brucei. Prog. Nucleic Acid Res. Mol. Biol. 43:1992;37-66.
22. Connell G.J., Byrne E.M., Simpson L. Guide RNA-independent and guide RNA-dependent uridine insertion into cytochrome b mRNA in a mitochondrial extract from Leishmania tarentolae. J. Biol. Chem. 272:1997;4212-4218.
23. Corell R.A., Myler P., Stuart K. Trypanosoma brucei mitochondrial CR4 gene encodes an extensively edited mRNA with completely edited sequence only in bloodstream forms. Mol. Biochem. Parasitol. 64:1994;65-74.
24. 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., Stuart K.D. Complexes from Trypanosoma brucei that exhibit deletion editing and other editing-associated properties. Mol. Cell. Biol. 16:1996;1410-1418.
25. Cruz-Reyes J., Sollner-Webb B. Trypanosome U-deletional RNA editing involves guide RNA-directed endonuclease cleavage, terminal U exonuclease, and RNA ligase activities. Proc. Natl. Acad. Sci. USA. 93:1996;8901-8906.
26. Cruz-Reyes J., Rusche L., Piller K.J., Sollner-Webb B. T. brucei RNA editing: adenosine nucleotides inversely affect U-deletion and U-insertion reactions at mRNA cleavage. Mol. Cell. 1:1998;401-409.
27. Das A., Peterson G.C., Kanner S.B., Frevert U., Parsons M. A major tyrosine-phosphorylated protein of Trypanosoma brucei is a nucleolar RNA-binding protein. J. Biol. Chem. 271:1996;15675-15681.
28. Decker C.J., Sollner-Webb B. RNA editing involves indiscriminate U changes throughout precisely defined editing domains. Cell. 61:1990;1001-1011.
29. Estévez A.M., Kierzenbaum F., Wirtz E., Bringaud F., Grunstein J., Simpson L. Knockout of the glutamate dehydrogenase gene in bloodstream Trypanosoma brucei in culture has no effect on editing of mitochondrial mRNAs. Mol. Biochem. Parasitol. 100:1999;5-17.
30. Feagin J., Stuart K. Differential expression of mitochondrial genes between the life cycle stages of Trypanosoma brucei. Proc. Natl. Acad. Sci. USA. 82:1985;3380-3384.
31. Feagin J., Stuart K. Developmental aspects of uridine addition within mitochondrial transcripts of Trypanosoma brucei. Mol. Cell Biol. 8:1988;1259-1265.
32. Feagin J.E., Abraham J., Stuart K. Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell. 53:1988;413-422.
33. Feagin J.E., Shaw J.M., Simpson L., Stuart K. Creation of AUG initiation codons by addition of uridines within cytochrome b transcripts of kinetoplastids. Proc. Natl. Acad. Sci. USA. 85:1988;539-543.
34. Fernandes A.P., Nelson K., Beverley S.M. Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: Perspectives on the age and origins of parasitism. Proc. Natl. Acad. Sci. USA. 90:1993;11608-11612.
35. Frech G.C., Bakalara N., Simpson L., Simpson A.M. In vitro RNA editing-like activity in a mitochondrial extract from Leishmania tarentolae. EMBO J. 14:1995;178-187.
36. Graham S.V. Mechanisms of stage-regulated gene expression in Kinetoplastida. Parasitol. Today. 11:1995;217-223.
37. Harris M., Decker C., Sollner-Webb B., Hajduk S. Specific cleavage of pre-edited mRNAs in trypanosome mitochondrial extracts. Mol. Cell. Biol. 12:1992;2591-2598.
38. Hayman M.L., Read L.K. Trypanosoma brucei RBP16 is a mitochondrial Y-box family protein with guide RNA binding activity. J. Biol. Chem. 274:1999;12067-12074.
39. Hentze M.W. Enzymes as RNA-binding proteins: a role for (di)nucleotide- binding domains? Trends. Biochem. Sci. 19:1994;101-103.
40. Hotz H.R., Biebinger S., Flaspohler J., Clayton C. PARP gene expression: control at many levels. Mol. Biochem. Parasitol. 91:1998;131-143.
41. Kable M.L., Seiwert S.D., Heidmann S., Stuart K. RNA editing: a mechanism for gRNA-specified uridylate insertion into precursor mRNA. Science. 273:1996;1189-1195.
42. Kapushoc S.T., Simpson L. In vitro uridine insertion RNA editing mediated by cis-acting guide RNAs. RNA. 5:1999;656-669.
43. Koller J., Muller U.F., Schmid B., Missel A., Kruft V., Stuart K., Göringer H.U. Trypanosoma brucei gBP21. An arginine-rich mitochondrial protein that binds to guide RNA with high affinity. J. Biol. Chem. 272:1997;3749-3757.
44. Koslowsky D.J., Bhat G.J., Perrollaz A.L., Feagin J.E., Stuart K. The MURF3 gene of T. brucei contains multiple domains of extensive editing and is homologous to a subunit of NADH dehydrogenase. Cell. 62:1990;901-911.
45. Koslowsky D.J., Bhat G.J., Read L.K., Stuart K. Cycles of progressive realignment of gRNA with mRNA in RNA editing. Cell. 67:1991;537-546.
46. Koslowsky D.J., Riley G.R., Feagin J.E., Stuart K. Guide RNAs for transcripts with developmentally regulated RNA editing are present in both life cycle stages of Trypanosoma brucei. Mol. Cell. Biol. 12:1992;2043-2049.
47. Koslowsky D.J., Yahampath G. Mitochondrial mRNA 3′ cleavage polyadenylation and RNA editing in Trypanosoma brucei are independent events. Mol. Biochem. Parasitol. 90:1997;81-94.
48. Lambert L., Muller U.F., Souza A.E., Göringer H.U. The involvement of gRNA-binding protein gBP21 in RNA editing-an in vitro and in vivo analysis. Nucleic Acids Res. 27:1999;1429-1436.
49. Landweber L.F. The evolution of RNA editing in kinetoplastid protozoa. BioSystems. 28:1992;41-45.
50. Leegwater P., Speijer D., Benne R. Identification by UV cross-linking of oligo(U)-binding proteins in mitochondria of the insect trypanosomatid Crithidia fasciculata. Eur. J. Biochem. 227:1995;780-786.
51. Leung S.S., Koslowsky D.J. Mapping contacts between gRNA and mRNA in trypanosome RNA editing. Nucleic Acids Res. 27:1999;778-787.
52. McConville M.J., Turco S.J., Ferguson M.A., Sacks D.L. Developmental modification of lipophosphoglycan during the differentiation of Leishmania major promastigotes to an infectious stage. EMBO J. 11:1992;3593-3600.
53. Madison-Antenucci S., Sabatini R.S., Pollard V.W., Hajduk S.L. Kinetoplastid RNA-editing-associated protein 1 (REAP-1): a novel editing complex protein with repetitive domains. EMBO J. 17:1998;6368-6376.
54. 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. 70:1992;459-467.
55. Maslov D.A., Sturm N.R., Niner B.M., Gruszynski E.S., Peris M., Simpson L. An intergenic G-rich region in Leishmania tarentolae kinetoplast maxicircle DNA is a pan-edited cryptogene encoding ribosomal protein S12. Mol. Cell. Biol. 12:1992;56-67.
56. Maslov D.A., Hollar L., Haghighat P., Nawathean P. Demonstration of mRNA editing and localization of guide RNA genes in kinetoplast-mitochondria of the plant trypanosomatid Phytomonas serpens. Mol. Biochem. Parasitol. 93:1998;225-236.
57. Maslov D.A., Nawathean P., Scheel J. Partial kinetoplast-mitochondrial gene organization and expression in the respiratory deficient plant trypanosomatid Phytomonas serpens. Mol. Biochem. Parasitol. 99:1999;207-221.
58. Michelotti E., Hajduk S. Developmental regulation of trypanosome mitochondrial DNA gene expression. J. Biol. Chem. 262:1987;927-932.
59. 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. 54:1992;31-42.
60. 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. 27:1999;1377-1385.
61. Missel A., Göringer H.U. Trypanosoma brucei mitochondria contain RNA helicase activity. Nucleic Acids Res. 22:1994;4050-4056.
62. Missel A., Souza A.E., Norskau G., Göringer H.U. Disruption of a gene encoding a novel mitochondrial DEAD-box protein in Trypanosoma brucei affects edited mRNAs. Mol. Cell Biol. 17:1997;4895-4903.
63. 0-ATPase. Eur. J. Biochem. 209:1992;207-216.
64. Opperdoes F.R., Baudhuin P., Coppens I., De Roe C., Edwards S.W., Weijers P.J., Misset O. Purification, morphometric analysis, and characterization of the glycosomes (microbodies) of the protozoan hemoflagellate Trypanosoma brucei. J. Cell Biol. 98:1984;1178-1184.
65. Paulin J. Conformation of a single mitochondrion in the trypomastigote stage of Trypanosoma cruzi. J. Parasitol. 69:1983;242-244.
66. Paulin J.J. The chondriome of selected trypanosomatids. A three-dimensional study based on serial thick sections and high voltage electron microscopy. J. Cell Biol. 66:1975;404-413.
67. Paulin J.J. Crithidia fasciculata: reconstruction of the mitochondrion based on serial thick sections and high-voltage electron microscopy. Exp. Parasitol. 41:1977;283-289.
68. Pays E., Vanhamme L., Berberof M. Genetic controls for the expression of surface antigens in African trypanosomes. Annu. Rev. Microbiol. 48:1994;25-52.
69. Peris M., Frech G.C., Simpson A.M., Bringaud F., Byrne E., Bakker A., Simpson L. Characterization of two classes of ribonucleoprotein complexes possibly involved in RNA editing from Leishmania tarentolae mitochondria. EMBO J. 13:1994;1664-1672.
70. Peris M., Simpson A.M., Grunstein J., Liliental J.E., Frech G.C., Simpson L. Native gel analysis of ribonucleoprotein complexes from a Leishmania tarentolae mitochondrial extract. Mol. Biochem. Parasitol. 85:1997;9-24.
71. Piller K.J., Rusche L.N., Cruz-Reyes J., Sollner-Webb B. Resolution of the RNA editing gRNA-directed endonuclease from two other endonucleases of Trypanosoma brucei mitochondria. RNA. 3:1997;279-290.
72. Pollard V.W., Harris M.E., Hajduk S.L. Native mRNA editing complexes from Trypanosoma brucei mitochondria. EMBO J. 11:1992;4429-4438.
73. Priest J.W., Hajduk S.L. Developmental regulation of mitochondrial biogenesis in Trypanosoma brucei. J. Bioenerg. Biomembr. 26:1994;179-192.
74. Read L.K., Myler P.J., Stuart K. Extensive editing of both processed and preprocessed maxicircle CR6 transcripts in Trypanosoma brucei. J. Biol. Chem. 267:1992;1123-1128.
75. Read L.K., Göringer H.U., Stuart K. Assembly of mitochondrial ribonucleoprotein complexes involves specific guide RNA (gRNA)-binding proteins and gRNA domains but does not require preedited mRNA. Mol. Cell. Biol. 14:1994;2629-2639.
76. 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. 68:1994;297-306.
77. Riley G.R., Myler P.J., Stuart K. Quantitation of RNA editing substrates, products and potential intermediates: implications for developmental regulation. Nucleic. Acids. Res. 23:1995;708-712.
78. Rusche L.N., Cruz-Reyes J., Piller K.J., Sollner-Webb B. Purification of a functional enzymatic editing complex from Trypanosoma brucei mitochondria. EMBO J. 16:1997;4069-4081.
79. Sabatini R., Hajduk S.L. RNA ligase and its involvement in guide RNA/mRNA chimera formation. J. Biol. Chem. 270:1995;7233-7240.
80. Sachs A., Wahle E. Poly(A) tail metabolism and function in eucaryotes. J. Biol. Chem. 268:1993;22955-22958.
81. Schmid B., Riley G.R., Stuart K., Göringer H.U. The secondary structure of guide RNA molecules from Trypanosoma brucei. Nucleic Acids Res. 23:1995;3093-3102.
82. Seiwert S.D., Stuart K. RNA editing: transfer of genetic information from gRNA to precursor mRNA in vitro. Science. 266:1994;114-117.
83. Seiwert S.D., Heidmann S., Stuart K. Direct visualization of uridylate deletion in vitro suggests a mechanism for kinetoplastid RNA editing. Cell. 84:1996;831-841.
84. Shapiro T.A., Englund P.T. The structure and replication of kinetoplast DNA. Annu. Rev. Microbiol. 49:1995;117-143.
85. Shaw J., Feagin J.E., Stuart K., Simpson L. Editing of mitochondrial mRNAs by uridine addition and deletion generates conserved amino acid sequences and AUG initiation codons. Cell. 53:1988;401-411.
86. Shaw J., Campbell D., Simpson L. Internal frameshifts within the mitochondrial genes for cytochrome oxidase subunit II and maxicircle unidentified reading frame 3 in Leishmania tarentolae are corrected by RNA editing: Evidence for translation of the edited cytochrome oxidase subunit II mRNA. Proc. Natl. Acad. Sci. 86:1989;6220-6224.
87. Simpson A.M., Bakalara N., Simpson L. A ribonuclease activity is activated by heparin or by digestion with proteinase K in mitochondrial extracts of Leishmania tarentolae. J. Biol. Chem. 267:1992;6782-6788.
88. Simpson L. The mitochondrial genome of kinetoplastid protozoa: Genomic organization, transcription, replication and evolution. Ann. Rev. Microbiol. 41:1987;363-382.
89. Simpson L., Neckelmann N., de la Cruz V., Simpson A., Feagin J., Jasmer D., Stuart K. Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence. J. Biol. Chem. 262:1987;6182-6196.
90. Simpson L., Shaw J. RNA editing and the mitochondrial cryptogenes of kinetoplastid protozoa. Cell. 57:1989;355-366.
91. Simpson L., Maslov D.A. RNA editing and the evolution of parasites. Science. 264:1994;1870-1871.
92. Simpson L., Maslov D.A. Ancient origin of RNA editing in kinetoplastid protozoa. Curr. Opin. Genet. Dev. 4:1994;887-894.
93. Simpson L., Kretzer F. 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. 87:1997;71-78.
94. Stuart K., Gelvin S. Kinetoplast DNA of normal and mutant Trypanosoma brucei. Am. J. Trop. Med. Hyg. 29:(Suppl. 1075-1081):1982.
95. Sturm N.R., Simpson L. Kinetoplast DNA minicircles encode guide RNAs for editing of cytochrome oxidase subunit III mRNA. Cell. 61:1990;879-884.
96. Sturm N.R., Simpson L. Partially edited mRNAs for cytochrome b and subunit III of cytochrome oxidase from Leishmania tarentolae mitochondria: RNA editing intermediates. Cell. 61:1990;871-878.
97. Thiemann O.H., Maslov D.A., Simpson L. Disruption of RNA editing in Leishmania tarentolae by the loss of minicircle-encoded guide RNA genes. EMBO J. 13:1994;5689-5700.
98. Thomas J.H. Thinking about genetic redundancy. Trends Genet. 9:1993;395-399.
99. Vanhamme L., Pays E. Control of gene expression in trypanosomes. Microbiol. Rev. 59:1995;223-240.
100. 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. 273:1998;21825-21833.
101. Wirtz E., Clayton C. Inducible gene expression in trypanosomes mediated by a prokaryotic repressor. Science. 268:1995;1179-1183.
102. Wirtz E., Leal S., Ochatt C., Cross G.A. A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol. Biochem. Parasitol. 99:1999;89-101.