A dual-targeted aminoacyl-tRNA synthetase in Plasmodium falciparum charges cytosolic and apicoplast tRNACys

Biochemical Journal

Volumn 458, Issue 3, 2014, Pages 513-523

  Pham, James S ^a   Sakaguchi, Reiko ^b   Yeoh, Lee M ^a,c   De Silva, Nilushi S ^a,d   Mcfadden, Geoffrey I ^c   Hou, Ya Ming ^b   Ralph, Stuart A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d Department of Medicine   (United States)

Author keywords

Alternative splicing; Aminoacyl tRNA synthetase; Aminoacylation; Apicomplexa; Apicoplast; Dual targeted; Plasmodium; Toxoplasma gondii; Trafficking; tRNA

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; CYSTEINE TRANSFER RNA; CYSTEINYL TRANSFER RNA SYNTHETASE; ISOENZYME; TRANSFER RNA; UNCLASSIFIED DRUG;

APICOMPLEXA; APICOPLAST; ARTICLE; CELL NUCLEUS; CELL ORGANELLE; CONTROLLED STUDY; CYTOSOL; ENDOSYMBIONT; EUKARYOTE; GENOME; NONHUMAN; PLASMODIUM FALCIPARUM; PLASTID; PRIORITY JOURNAL; PROTEIN TRANSPORT; RNA TRANSLATION; TOXOPLASMA GONDII;

ALTERNATIVE SPLICING; AMINO ACYL-TRNA SYNTHETASES; APICOPLASTS; CYTOSOL; ESCHERICHIA COLI PROTEINS; GREEN FLUORESCENT PROTEINS; ISOENZYMES; KINETICS; MUTATION; PLASMODIUM FALCIPARUM; PROTEIN TRANSPORT; TEMPERATURE; TOXOPLASMA;

EID: 84896861333     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131451     Document Type: Article

References (73)

1. Ambrogelly, A., Ahel, I., Polycarpo, C., Bunjun-Srihari, S., Krett, B., Jacquin-Becker, C., Ruan, B., Kohrer, C., Stathopoulos, C., RajBhandary, U. L. and Soll, D. (2002) Methanocaldococcus jannaschii prolyl-tRNA synthetase charges tRNA(Pro) with cysteine. J. Biol. Chem. 277, 34749-34754
2. Ibba, M. and Soll, D. (2001) The renaissance of aminoacyl-tRNA synthesis. EMBO Rep. 2, 382-387 (Pubitemid 32509952)
3. Hauenstein, S., Zhang, C.-M., Hou, Y.-M. and Perona, J. J. (2004) Shape-selective RNA recognition by cysteinyl-tRNA synthetase. Nat. Struct. Mol. Biol. 11, 1134-1141 (Pubitemid 39453344)
4. Zhang, C.-M., Christian, T., Newberry, K. J., Perona, J. J. and Hou, Y.-M. (2003) Zinc-mediated amino acid discrimination in cysteinyl-tRNA synthetase. J. Mol. Biol. 327, 911-917 (Pubitemid 36363700)
5. Ibba, M., Hong, K. W., Sherman, J. M., Sever, S. and Soll, D. (1996) Interactions between tRNA identity nucleotides and their recognition sites in glutaminyl-tRNA synthetase determine the cognate amino acid affinity of the enzyme. Proc. Natl. Acad. Sci. U.S.A. 93, 6953-6958 (Pubitemid 26243481)
6. Jeannin, G., Burkard, G. and Weil, J. H. (1976) Aminoacylation of Phaseolus vulgaris cytoplasmic, chloroplastic and mitochondrial tRNAsPro and tRNAsLys by homologous and heterologous enzymes. Biochim. Biophys. Acta 442, 24-31
7. Duchene, A.-M., Giritch, A., Hoffmann, B., Cognat, V., Lancelin, D., Peeters, N. M., Zaepfel, M., Marechal-Drouard, L. and Small, I. D. (2005) Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana . Proc. Natl. Acad. Sci. U.S.A. 102, 16484-16489 (Pubitemid 41688940)
8. Small, I., Wintz, H., Akashi, K. and Mireau, H. (1998) Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol. Biol. 38, 265-277 (Pubitemid 28403777)
9. Rettig, J., Wang, Y., Schneider, A. and Ochsenreiter, T. (2012) Dual targeting of isoleucyl-tRNA synthetase in Trypanosoma brucei is mediated through alternative trans-splicing. Nucleic Acids Res. 40, 1299-1306
10. Rinehart, J., Krett, B., Rubio, M. A., Alfonzo, J. D. and Soll, D. (2005) Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev. 19, 583-592 (Pubitemid 40314990)
11. Dias, J., Octobre, G., Kobbi, L., Comisso, M., Flisiak, S. and Mirande, M. (2012) Activation of human mitochondrial lysyl-tRNA synthetase upon maturation of its premitochondrial precursor. Biochemistry 51, 909-916
12. Morgante, C. V., Rodrigues, R. A., Marbach, P. A., Borgonovi, C. M., Moura, D. S. and Silva-Filho, M. C. (2009) Conservation of dual-targeted proteins in Arabidopsis and rice points to a similar pattern of gene-family evolution. Mol. Genet. Genomics 281, 525-538
13. McFadden, G. I., Reith, M. E., Munholland, J. and Lang-Unnasch, N. (1996) Plastid in human parasites. Nature 381, 482-482
14. Bhatt, T. K., Kapil, C., Khan, S., Jairajpuri, M. A., Sharma, V., Santoni, D., Silvestrini, F., Pizzi, E. and Sharma, A. (2009) A genomic glimpse of aminoacyl-tRNA synthetases in malaria parasite Plasmodium falciparum. BMC Genomics 10, 644
15. Jackson, K. E., Habib, S., Frugier, M., Hoen, R., Khan, S., Pham, J. S., Ribas de Pouplana, L., Royo, M., Santos, M. A., Sharma, A. and Ralph, S. A. (2011) Protein translation in Plasmodium parasites. Trends Parasitol. 27, 467-476
16. Waller, R. F., Reed, M. B., Cowman, A. F. and McFadden, G. I. (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19, 1794-1802 (Pubitemid 30204391)
17. Motorin, Y. and Waller, J. P. (1998) Purification and properties of cysteinyl-tRNA synthetase from rabbit liver. Biochimie 80, 579-590 (Pubitemid 29151437)
18. Jackson, K. E., Pham, J. S., Kwek, M., De Silva, N. S., Allen, S. M., Goodman, C. D., McFadden, G. I., de Pouplana, L. R. and Ralph, S. A. (2012) Dual targeting of aminoacyl-tRNA synthetases to the apicoplast and cytosol in Plasmodium falciparum. Int. J. Parasitol. 42, 177-186
19. Khan, S., Sharma, A., Jamwal, A., Sharma, V., Pole, A. K. and Thakur, K. K. (2011) Uneven spread of cis- and trans-editing aminoacyl-tRNA synthetase domains within translational compartments of P. falciparum. Sci. Rep. 1, 188
20. Pino, P., Aeby, E., Foth, B. J., Sheiner, L., Soldati, T., Schneider, A. and Soldati-Favre, D. (2010) Mitochondrial translation in absence of local tRNA aminoacylation and methionyl tRNAMet formylation in Apicomplexa. Mol. Microbiol. 76, 706-718
21. Istvan, E. S., Dharia, N. V., Bopp, S. E., Gluzman, I., Winzeler, E. A. and Goldberg, D. E. (2011) Validation of isoleucine utilization targets in Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 108, 1627-1632
22. Ishiyama, A., Iwatsuki, M., Namatame, M., Nishihara-Tsukashima, A., Sunazuka, T., Takahashi, Y., Omura, S. and Otoguro, K. (2011) Borrelidin, a potent antimalarial: stage-specific inhibition profile of synchronized cultures of Plasmodium falciparum. J. Antibiot. (Tokyo) 64, 381-384
23. Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S. et al. (2009) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 37, D539-D543
24. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (Pubitemid 27359211)
25. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. and Sayers, E. W. (2011) GenBank. Nucleic Acids Res. 39, D32-D37
26. Chen, F., Mackey, A. J., Stoeckert, Jr, C. J. and Roos, D. S. (2006) OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res. 34, D363-D368
27. Petersen, T. N., Brunak, S., von Heijne, G. and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
28. Zuegge, J., Ralph, S., Schmuker, M., McFadden, G. I. and Schneider, G. (2001) Deciphering apicoplast targeting signals: feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 280, 19-26 (Pubitemid 34014880)
29. Foth, B., Ralph, S., Tonkin, C., Struck, N., Fraunholz, M., Roos, D., Cowman, A. and McFadden, G. (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299, 705-708 (Pubitemid 36159484)
30. Felsenstein, K. M. and Lewis-Higgins, L. (1993) Processing of the β-amyloid precursor protein carrying the familial, Dutch-type, and a novel recombinant C-terminal mutation. Neurosci. Lett. 152, 185-189 (Pubitemid 23149344)
31. Neron, B., Menager, H., Maufrais, C., Joly, N., Maupetit, J., Letort, S., Carrere, S., Tuffery, P. and Letondal, C. (2009) Mobyle: a new full web bioinformatics framework. Bioinformatics 25, 3005-3011
32. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321
33. Kyes, S., Pinches, R. and Newbold, C. (2000) A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol. Biochem. Parasitol. 105, 311-315 (Pubitemid 30067771)
34. Boddey, J. A., Moritz, R. L., Simpson, R. J. and Cowman, A. F. (2009) Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic 10, 285-299
35. Triglia, T., Tham, W. H., Hodder, A. and Cowman, A. F. (2009) Reticulocyte binding protein homologues are key adhesins during erythrocyte invasion by Plasmodium falciparum. Cell. Microbiol. 11, 1671-1687
36. Trager, W. and Jensen, J. (1976) Human malaria parasites in continuous culture. Science 193, 673-675
37. Duraisingh, M. T., Triglia, T. and Cowman, A. F. (2002) Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. Int. J. Parasitol. 32, 81-89 (Pubitemid 34131595)
38. Striepen, B. and Soldati, D. (2007) Genetic manipulation of Toxoplasma gondii. In Toxoplasma gondii: The Model Apicomplexan. Perspective and Methods (Weiss, L. D. and Kim, K., eds), pp. 391-418, Elsevier, Amsterdam
39. Huynh, M. H. and Carruthers, V. B. (2009) Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot. Cell 8, 530-539
40. Donald, R. G. and Roos, D. S. (1993) Stable molecular transformation of Toxoplasma gondii: a selectable dihydrofolate reductase-thymidylate synthase marker based on drug-resistance mutations in malaria. Proc. Natl. Acad. Sci. U.S.A. 90, 11703-11707 (Pubitemid 24008707)
41. Ehlgen, F., Pham, J. S., de Koning-Ward, T., Cowman, A. F. and Ralph, S. A. (2012) Investigation of the Plasmodium falciparum food vacuole through inducible expression of the chloroquine resistance transporter (PfCRT). PLoS ONE 7, e38781
42. Tonkin, C., van Dooren, G., Spurck, T., Struck, N., Good, R., Handman, E., Cowman, A. and McFadden, G. (2004) Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol. Biochem. Parasitol. 137, 13-21
43. Bohman, K. and Isaksson, L. A. (1979) Temperature-sensitive mutants in cysteinyl-tRNA ligase of E. coli K-12. Mol. Gen. Genet. 176, 53-55 (Pubitemid 10197125)
44. Hou, Y. M., Westhof, E. and Giege, R. (1993) An unusual RNA tertiary interaction has a role for the specific aminoacylation of a transfer RNA. Proc. Natl. Acad. Sci. U.S.A. 90, 6776-6780 (Pubitemid 23207296)
45. Fechter, P., Rudinger, J., Giege, R. and Theobald-Dietrich, A. (1998) Ribozyme processed tRNA transcripts with unfriendly internal promoter for T7 RNA polymerase: production and activity. FEBS Lett. 436, 99-103 (Pubitemid 28454614)
46. Gardner, M., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R., Carlton, J., Pain, A., Nelson, K., Bowman, S. et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511
47. Eriani, G., Dirheimer, G. and Gangloff, J. (1991) Cysteinyl-tRNA synthetase: determination of the last E. coli aminoacyl-tRNA synthetase primary structure. Nucleic Acids Res. 19, 265-269 (Pubitemid 21896968)
48. Davidson, E., Caffarella, J., Vitseva, O., Hou, Y. M. and King, M. P. (2001) Isolation of two cDNAs encoding functional human cytoplasmic cysteinyl-tRNA synthetase. Biol. Chem. 382, 399-406 (Pubitemid 32372483)
49. Liu, C., Gamper, H., Shtivelband, S., Hauenstein, S., Perona, J. J. and Hou, Y.-M. (2007) Kinetic quality control of anticodon recognition by a eukaryotic aminoacyl-tRNA synthetase. J. Mol. Biol. 367, 1063-1078 (Pubitemid 46386072)
50. Abrahamsen, M. S., Templeton, T. J., Enomoto, S., Abrahante, J. E., Zhu, G., Lancto, C. A., Deng, M., Liu, C., Widmer, G., Tzipori, S. et al. (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304, 441-445 (Pubitemid 38495940)
51. Cavalier-Smith, T. (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46, 347-366
52. Waller, R. F., Keeling, P. J., Donald, R. G., Striepen, B., Handman, E., Lang-Unnasch, N., Cowman, A. F., Besra, G. S., Roos, D. S. and McFadden, G. I. (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 95, 12352-12357 (Pubitemid 28483769)
53. 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. and Stunnenberg, H. G. (2010) H2A.Z demarcates intergenic regions of the Plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3. PLoS Pathog. 6, e1001223
54. Esseiva, A. C., Naguleswaran, A., Hemphill, A. and Schneider, A. (2004) Mitochondrial tRNA Import in Toxoplasma gondii. J. Biol. Chem. 279, 42363-42368 (Pubitemid 39372117)
55. Nair, S. C., Brooks, C. F., Goodman, C. D., Strurm, A., McFadden, G. I., Sundriyal, S., Anglin, J. L., Song, Y., Moreno, S. N. J. and Striepen, B. (2011) Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J. Exp. Med. 208, 1547-1559
56. Agrawal, S., van Dooren, G. G., Beatty, W. L. and Striepen, B. (2009) Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins. J. Biol. Chem. 284, 33683-33691
57. Ponpuak, M., Klemba, M., Park, M., Gluzman, I. Y., Lamppa, G. K. and Goldberg, D. E. (2007) A role for falcilysin in transit peptide degradation in the Plasmodium falciparum apicoplast. Mol. Microbiol. 63, 314-334 (Pubitemid 46058922)
58. Kehr, S., Sturm, N., Rahlfs, S., Przyborski, J. M. and Becker, K. (2010) Compartmentation of redox metabolism in malaria parasites. PLoS Pathog. 6, e1001242
59. Ruan, B., Nakano, H., Tanaka, M., Mills, J. A., DeVito, J. A., Min, B., Low, K. B., Battista, J. R. and Soll, D. (2004) Cysteinyl-tRNA(Cys) formation in Methanocaldococcus jannaschii: the mechanism is still unknown. J. Bacteriol. 186, 8-14 (Pubitemid 38020280)
60. Lee, C. P., Mandal, N., Dyson, M. R. and RajBhandary, U. L. (1993) The discriminator base influences tRNA structure at the end of the acceptor stem and possibly its interaction with proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 7149-7152 (Pubitemid 23222406)
61. Hou, Y. M. and Schimmel, P. (1992) Novel transfer RNAs that are active in Escherichia coli. Biochemistry 31, 4157-4160
62. Christian, T., Lipman, R. S., Evilia, C. and Hou, Y. M. (2000) Alternative design of a tRNA core for aminoacylation. J. Mol. Biol. 303, 503-514
63. Liu, C., Gamper, H., Liu, H., Cooperman, B. S. and Hou, Y. M. (2011) Potential for interdependent development of tRNA determinants for aminoacylation and ribosome decoding. Nat. Commun. 2, 329
64. Hou, Y. M., Lipman, R. S. and Zarutskie, J. A. (1998) A tRNA circularization assay: evidence for the variation of the conformation of the CCA end. RNA 4, 733-738 (Pubitemid 28317822)
65. Hou, Y. M. and Schimmel, P. (1989) Evidence that a major determinant for the identity of a transfer RNA is conserved in evolution. Biochemistry 28, 6800-6804
66. Gershon, P. D. and Howells, R. E. (1986) Mitochondrial protein synthesis in Plasmodium falciparum. Mol. Biochem. Parasitol. 18, 37-43 (Pubitemid 16169346)
67. Chaubey, S., Kumar, A., Singh, D. and Habib, S. (2005) The apicoplast of Plasmodium falciparum is translationally active. Mol. Microbiol. 56, 81-89 (Pubitemid 40461489)
68. Keller, T. L., Zocco, D., Sundrud, M. S., Hendrick, M., Edenius, M., Yum, J., Kim, Y. J., Lee, H. K., Cortese, J. F., Wirth, D. F. et al. (2012) Halofuginone and other febrifugine derivatives inhibit prolyl-tRNA synthetase. Nat. Chem. Biol. 8, 311-317
69. Hoepfner, D., McNamara, C. W., Lim, C. S., Studer, C., Riedl, R., Aust, T., McCormack, S. L., Plouffe, D. M., Meister, S., Schuierer, S. et al. (2012) Selective and specific inhibition of the Plasmodium falciparum lysyl-tRNA synthetase by the fungal secondary metabolite cladosporin. Cell Host Microbe 11, 654-663
70. Hoen, R., Novoa, E. M., Lopez, A., Camacho, N., Cubells, L., Vieira, P., Santos, M., Marin-Garcia, P., Bautista, J. M., Cortes, A. et al. (2013) Selective inhibition of an apicoplastic aminoacyl-tRNA synthetase from Plasmodium falciparum. ChemBioChem 14, 499-509
71. Otoguro, K., Ui, H., Ishiyama, A., Kobayashi, M., Togashi, H., Takahashi, Y., Masuma, R., Tanaka, H., Tomoda, H., Yamada, H. and Omura, S. (2003) 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) 56, 727-729 (Pubitemid 37081107)
72. Pfefferkorn, E. R. and Borotz, S. E. (1994) Comparison of mutants of Toxoplasma gondii selected for resistance to azithromycin, spiramycin, or clindamycin. Antimicrob. Agents Chemother. 38, 31-37 (Pubitemid 24018153)
73. Fichera, M. E., Bhopale, M. K. and Roos, D. S. (1995) In vitro assays elucidate peculiar kinetics of clindamycin action against Toxoplasma gondii. Antimicrob. Agents Chemother. 39, 1530-1537