Dual targeting of aminoacyl-tRNA synthetases to the apicoplast and cytosol in Plasmodium falciparum

International Journal for Parasitology

Volumn 42, Issue 2, 2012, Pages 177-186

  Jackson, Katherine E ^a   Pham, James S ^a   Kwek, Michelle ^a   De Silva, Nilushi S ^a,e   Allen, Stacey M ^a   Goodman, Christopher D ^b   McFadden, Geoffrey I ^b   Ribas de Pouplana, Lluis ^c,d   Ralph, Stuart A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e New York Presbyterian Morgan Stanley Children's Hospital   (United States)

Author keywords

Aminoacyl tRNA synthetase; Apicoplast; Borrelidin; Dual targeting; Malaria; Mupirocin; Plasmodium; TRNA synthetase

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; ANTIMALARIAL AGENT; BORRELIDIN; PSEUDOMONIC ACID;

AMINO ACID; ANTIBIOTICS; DRUG DEVELOPMENT; ENZYME; GENOME; INHIBITION; MALARIA; MITOCHONDRION; MORPHOLOGY; PLASTID; RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AMINOACYLATION; ANIMAL CELL; APICOPLAST; ARTICLE; CELL DIVISION; CELL GROWTH; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENZYME LOCALIZATION; EXON; GENE TARGETING; MITOCHONDRION; NONHUMAN; OPEN READING FRAME; PLASMODIUM FALCIPARUM; PROTEIN TARGETING; RNA SEQUENCE; SEQUENCE ANALYSIS;

AMINO ACYL-TRNA SYNTHETASES; ANTIMALARIALS; CYTOSOL; FATTY ALCOHOLS; MUPIROCIN; PLASMODIUM FALCIPARUM; PLASTIDS; PROTEIN TRANSPORT;

PLASMODIUM FALCIPARUM;

EID: 84856419851     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2011.11.008     Document Type: Article

References (56)

1. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
2. Arnoys E.J., Wang J.L. Dual localization: proteins in extracellular and intracellular compartments. Acta Histochem. 2007, 109:89-110.
3. Aurrecoechea C., Brestelli J., Brunk B.P., Dommer J., Fischer S., Gajria B., Gao X., Gingle A., Grant G., Harb O.S., Heiges M., Innamorato F., Iodice J., Kissinger J.C., Kraemer E., Li W., Miller J.A., Nayak V., Pennington C., Pinney D.F., Roos D.S., Ross C., Stoeckert C.J., Treatman C., Wang H. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 2009, 37:D539-D543.
4. Bartfai R., Hoeijmakers W.A., Salcedo-Amaya A.M., Smits A.H., Janssen-Megens E., Kaan A., Treeck M., Gilberger T.W., Francoijs K.J., Stunnenberg H.G. H2A.Z demarcates intergenic regions of the Plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3. PLoS Pathog. 2010, 6:e1001223.
5. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
6. Ben-Menachem R., Tal M., Pines O. A third of the yeast mitochondrial proteome is dual localized: a question of evolution. Proteomics 2011, 11:4468-4476.
7. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., Sayers E.W. GenBank. Nucleic Acids Res. 2011, 39:D32-D37.
8. Berglund A.K., Pujol C., Duchene A.M., Glaser E. Defining the determinants for dual targeting of amino acyl-tRNA synthetases to mitochondria and chloroplasts. J. Mol. Biol. 2009, 393:803-814.
9. Bhatt T.K., Kapil C., Khan S., Jairajpuri M.A., Sharma V., Santoni D., Silvestrini F., Pizzi E., Sharma A. A genomic glimpse of aminoacyl-tRNA synthetases in malaria parasite Plasmodium falciparum. BMC Genomics 2009, 10:644.
10. Boddey J.A., Moritz R.L., Simpson R.J., Cowman A.F. Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 2009, 10:285-299.
11. Bowyer P.W., Simon G.M., Cravatt B.F., Bogyo M. Global profiling of proteolysis during rupture of Plasmodium falciparum from the host erythrocyte. Mol. Cell. Proteomics 2011, 10. M110.001636.
12. Chatton B., Walter P., Ebel J.P., Lacroute F., Fasiolo F. The yeast VAS1 gene encodes both mitochondrial and cytoplasmic valyl-tRNA synthetases. J. Biol. Chem. 1988, 263:52-57.
13. Chen F., Mackey A.J., Stoeckert C.J., Roos D.S. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res. 2006, 34:D363-D368.
14. Dahl E.L., Rosenthal P.J. Multiple antibiotics exert delayed effects against the Plasmodium falciparum apicoplast. Antimicrob. Agents Chemother. 2007, 51:3485-3490.
15. Duchene A.M., Giritch A., Hoffmann B., Cognat V., Lancelin D., Peeters N.M., Zaepfel M., Marechal-Drouard L., Small I.D. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U S A 2005, 102:16484-16489.
16. Duchene A.M., Pujol C., Marechal-Drouard L. Import of tRNAs and aminoacyl-tRNA synthetases into mitochondria. Curr. Genet. 2009, 55:1-18.
17. Duraisingh M.T., Triglia T., Cowman A.F. Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int. J. Parasitol. 2002, 32:81-89.
18. Esseiva A.C., Naguleswaran A., Hemphill A., Schneider A. Mitochondrial tRNA import in Toxoplasma gondii. J. Biol. Chem. 2004, 279:42363-42368.
19. Florens L., Washburn M.P., Raine J.D., Anthony R.M., Grainger M., Haynes J.D., Moch J.K., Muster N., Sacci J.B., Tabb D.L., Witney A.A., Wolters D., Wu Y., Gardner M.J., Holder A.A., Sinden R.E., Yates J.R., Carucci D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature 2002, 419:520-526.
20. Foth B.J., Ralph S.A., Tonkin C.J., Struck N.S., Fraunholz M., Roos D.S., Cowman A.F., McFadden G.I. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 2003, 299:705-708.
21. Fujino T., Man-Jong K., Minekura H., Suzuki H., Yamamoto T.T. Alternative translation initiation generates acyl-CoA synthetase 3 isoforms with heterogeneous amino termini. J. Biochem. 1997, 122:212-216.
22. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., Paulsen I.T., James K., Eisen J.A., Rutherford K., Salzberg S.L., Craig A., Kyes S., Chan M.S., Nene V., Shallom S.J., Suh B., Peterson J., Angiuoli S., Pertea M., Allen J., Selengut J., Haft D., Mather M.W., Vaidya A.B., Martin D.M., Fairlamb A.H., Fraunholz M.J., Roos D.S., Ralph S.A., McFadden G.I., Cummings L.M., Subramanian G.M., Mungall C., Venter J.C., Carucci D.J., Hoffman S.L., Newbold C., Davis R.W., Fraser C.M., Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
23. Goodman C.D., Su V., McFadden G.I. The effects of anti-bacterials on the malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 2007, 152:181-191.
24. Gurney R., Thomas C.M. Mupirocin: biosynthesis, special features and applications of an antibiotic from a gram-negative bacterium. Appl. Microbiol. Biotechnol. 2011, 90:11-21.
25. Ibba M., Soll D. Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 2000, 69:617-650.
26. Ishiyama A., Iwatsuki M., Namatame M., Nishihara-Tsukashima A., Sunazuka T., Takahashi Y., Omura S., Otoguro K. Borrelidin, a potent antimalarial: stage-specific inhibition profile of synchronized cultures of Plasmodium falciparum. J. Antibiot. (Tokyo) 2011, 64:381-384.
27. Istvan E.S., Dharia N.V., Bopp S.E., Gluzman I., Winzeler E.A., Goldberg D.E. Validation of isoleucine utilization targets in Plasmodium falciparum. Proc. Natl. Acad. Sci. U S A 2011, 108:1627-1632.
28. Jackson K.E., Habib S., Frugier M., Hoen R., Khan S., Pham J.S., Pouplana L.R., Royo M., Santos M.A., Sharma A., Ralph S.A. Protein translation in Plasmodium parasites. Trends Parasitol. 2011, 27:467-476.
29. Kehr S., Sturm N., Rahlfs S., Przyborski J.M., Becker K. Compartmentation of redox metabolism in malaria parasites. PLoS Pathog. 2010, 6:e1001242.
30. Lambros C., Vanderberg J.P. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 1979, 65:418-420.
31. Lareau L.F., Green R.E., Bhatnagar R.S., Brenner S.E. The evolving roles of alternative splicing. Curr. Opin. Struct. Biol. 2004, 14:273-282.
32. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
33. Lasonder E., Janse C.J., van Gemert G.J., Mair G.R., Vermunt A.M.W., Douradinha B.G., van Noort V., Huynen M.A., Luty A.J.F., Kroeze H., Khan S.M., Sauerwein R.W., Waters A.P., Mann M., Stunnenberg H.G. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog 2008, 4:e1000195.
34. Liu C., Gamper H., Liu H., Cooperman B.S., Hou Y.M. Potential for interdependent development of tRNA determinants for aminoacylation and ribosome decoding. Nat. Commun. 2011, 2:329.
35. Nass G., Poralla K. Genetics of borrelidin resistant mutants of Saccharomyces cerivisiae and properties of their threonyl-tRNA-synthetase. Mol. Gen. Genet. 1976, 147:39-43.
36. Natsoulis G., Hilger F., Fink G.R. The HTS1 gene encodes both the cytoplasmic and mitochondrial histidine tRNA synthetases of S. cerevisiae. Cell 1986, 46:235-243.
37. Ochsner U.A., Sun X., Jarvis T., Critchley I., Janjic N. Aminoacyl-tRNA synthetases: essential and still promising targets for new anti-infective agents. Expert Opin. Investig. Drugs 2007, 16:573-593.
38. Otoguro K., Ui H., Ishiyama A., Kobayashi M., Togashi H., Takahashi Y., Masuma R., Tanaka H., Tomoda H., Yamada H., Omura S. In vitro and in vivo antimalarial activities of a non-glycosidic 18-membered macrolide antibiotic, borrelidin, against drug-resistant strains of Plasmodia. J. Antibiot. (Tokyo) 2003, 56:727-729.
39. Otto T.D., Wilinski D., Assefa S., Keane T.M., Sarry L.R., Bohme U., Lemieux J., Barrell B., Pain A., Berriman M., Newbold C., Llinas M. New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol. Microbiol. 2010, 76:12-24.
40. Peeters N., Small I. Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 2001, 1541:54-63.
41. Pino P., Aeby E., Foth B.J., Sheiner L., Soldati T., Schneider A., Soldati-Favre D. Mitochondrial translation in absence of local tRNA aminoacylation and methionyl tRNA Met formylation in Apicomplexa. Mol. Microbiol. 2009, 76:706-718.
42. Preiser P., Williamson D.H., Wilson R.J.M. TRNA genes transcribed from the plastid-like DNA of Plasmodium falciparum. Nucleic Acids Res. 1995, 23:4329-4336.
43. Rettig, J., Wang, Y., Schneider, A., Ochsenreiter, T., in press. Dual targeting of isoleucyl-tRNA synthetase in Trypanosoma brucei is mediated through alternative trans-splicing. Nucleic Acids Res. doi:10.1093/nar/gkr794.
44. Singh N., Preiser P., Renia L., Balu B., Barnwell J., Blair P., Jarra W., Voza T., Landau I., Adams J.H. Conservation and developmental control of alternative splicing in maebl among malaria parasites. J. Mol. Biol. 2004, 343:589-599.
45. Smilkstein M., Sriwilaijaroen N., Kelly J.X., Wilairat P., Riscoe M. Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob. Agents Chemother. 2004, 48:1803-1806.
46. Soldati T., Schafer B.W., Perriard J.C. Alternative ribosomal initiation gives rise to chicken brain-type creatine kinase isoproteins with heterogeneous amino termini. J. Biol. Chem. 1990, 265:4498-4506.
47. Souciet G., Menand B., Ovesna J., Cosset A., Dietrich A., Wintz H. Characterization of two bifunctional Arabdopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs. Eur. J. Biochem. 1999, 266:848-854.
48. Takao M., Aburatani H., Kobayashi K., Yasui A. Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res. 1998, 26:2917-2922.
49. Tonkin C.J., van Dooren G.G., Spurck T.P., Struck N.S., Good R.T., Handman E., Cowman A.F., McFadden G.I. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol. Biochem. Parasitol. 2004, 137:13-21.
50. Trager W., Jensen J. Human malaria parasites in continuous culture. Science 1976, 193:673-675.
51. Triglia T., Chen L., Lopaticki S., Dekiwadia C., Riglar D.T., Hodder A.N., Ralph S.A., Baum J., Cowman A.F. Plasmodium falciparum merozoite invasion is inhibited by antibodies that target the PfRh2a and b binding domains. PLoS Pathog. 2011, 7:e1002075.
52. van Dooren G.G., Marti M., Tonkin C.J., Stimmler L.M., Cowman A.F., McFadden G.I. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol. Microbiol. 2005, 57:405-419.
53. Ward A., Campoli-Richards D.M. Mupirocin: a review of its antibacterial activity, pharmacokinetic properties and therapeutic use. Drugs 1986, 32:425-444.
54. Wilson R.J.M., Denny P.W., Preiser P.R., Rangachari K., Roberts K., Roy A., Whyte A., Strath M., Moore D.J., Moore P.W., Williamson D.H. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 1996, 261:155-172.
55. Yeh E., DeRisi J.L. Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol. 2011, 9:e1001138.
56. Zuegge J., Ralph S., Schmuker M., McFadden G.I., Schneider G. Deciphering apicoplast targeting signals - feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 2001, 280:19-26.