Reduced ribosomes of the apicoplast and mitochondrion of Plasmodium spp. and predicted interactions with antibiotics

Open Biology

Volumn 4, Issue MAY, 2014, Pages

  Gupta, Ankit ^a   Shah, Priyanka ^a   Haider, Afreen ^a   Gupta, Kirti ^a   Siddiqi, Mohammad Imran ^a   Ralph, Stuart A ^b   Habib, Saman ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antibiotics; Apicomplexa; Large subunit (LSU) proteins; Organelles; Ribosomes; Small subunit (SSU) proteins

Indexed keywords

ALGAE; APICOMPLEXA; BACILLARIOPHYTA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM; PROTISTA; TOXOPLASMA;

ANTIINFECTIVE AGENT; RIBOSOME PROTEIN; RIBOSOME RNA;

APICOPLAST; CHEMICAL STRUCTURE; CLASSIFICATION; GENETICS; METABOLISM; MITOCHONDRIAL GENOME; MITOCHONDRION; PLASMODIUM; PLASTID GENOME; RIBOSOME; TOXOPLASMA;

ANTI-BACTERIAL AGENTS; APICOPLASTS; GENOME, MITOCHONDRIAL; GENOME, PLASTID; MITOCHONDRIA; MODELS, MOLECULAR; PLASMODIUM; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, RIBOSOMAL; TOXOPLASMA;

EID: 84902387843     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.140045     Document Type: Article

References (100)

1. Wilson RJM, Gardner MJ, Feagin JE, Williamson DH. 1991 Have malaria parasites three genomes? Parasitol. Today 7, 134-136. (doi:10.1016/0169-4758(91) 90276-T)
2. Gardner MJ et al. 2002 Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511. (doi:10.1038/nature01097)
3. Wilson RJ et al. 1996 Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 261, 155-172. (doi:10. 1006/jmbi.1996.0449)
4. Feagin JE, Gardner MJ, Williamson DH, Wilson RJ. 1991 The putative mitochondrial genome of Plasmodium falciparum. J. Protozool. 38, 243-245. (doi:10.1111/j.1550-7408.1991.tb04436.x)
5. Feagin JE, Werner E, Gardner MJ, Williamson DH, Wilson RJ. 1992 Homologies between the contiguous and fragmented rRNAs of the two Plasmodium falciparum extrachromosomal DNAs are limited to core sequences. Nucleic Acids Res. 20, 879-887. (doi:10.1093/nar/20.4.879)
6. Li WB, Bzik DJ, Gu HM, Tanaka M, Fox BA, Inselburg J. 1989 An enlarged largest subunit of Plasmodium falciparum RNA polymerase II defines conserved and variable RNA polymerase domains. Nucleic Acids Res. 17, 9621-9636. (doi:10.1093/nar/17. 23.9621)
7. Gardner MJ, Goldman N, Barnett P, Moore PW, Rangachari K, Strath M, Whyte A, Williamson DH, Wilson RJ. 1994 Phylogenetic analysis of the rpoB gene from the plastid-like DNA of Plasmodium falciparum. Mol. Biochem. Parasitol. 66, 221-231. (doi:10.1016/0166-6851(94)90149-X)
8. Li JN, Maga JA, Cermakian N, Cedergren R, Feagin JE. 2001 Identification and characterization of a Plasmodium falciparum RNA polymerase gene with similarity to mitochondrial RNA polymerases. Mol. Biochem. Parasitol. 113, 261-269. (doi:10.1016/S0166-6851(01)00223-7)
9. McFadden GI, Reith M, Munholland J, Lang-Unnasch N. 1996 Plastid in human parasites. Nature 381, 482. (doi:10.1038/381482a0)
10. Roy A, Cox RA, Williamson DH, Wilson RJ. 1999 Protein synthesis in the plastid of Plasmodium falciparum. Protist 150, 183-188. (doi:10.1016/S1434- 4610(99)70020-9)
11. Feagin JE, Harrell MI, Lee JC, Coe KJ, Sands BH, Cannone JJ, Tami G, Schnare MN, Gutell RR. 2012 The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum. PLoS ONE 7, e38320. (doi:10.1371/journal.pone.0038320)
12. Biswas S, Lim EE, Gupta A, Saqib U, Mir SS, Siddiqi MI, Ralph SA, Habib S. 2011 Interaction of apicoplast-encoded elongation factor (EF) EF-Tu with nuclear-encoded EF-Ts mediates translation in the Plasmodium falciparum plastid. Int. J. Parasitol. 41, 417-427. (doi:10.1016/j.ijpara.2010.11.003)
13. Gupta A, Mir SS, Jackson KE, Lim EE, Shah P, Sinha A, Siddiqi MI, Ralph SA, Habib S. 2013 Recycling factors for ribosome disassembly in the apicoplast and mitochondrion of Plasmodium falciparum. Mol. Microbiol. 88, 891-905. (doi:10.1111/mmi.12230)
14. Gupta A, Mir SS, Saqib U, Biswas S, Vaishya S, Srivastava K, Siddiqi MI, Habib S. 2013 The effect of fusidic acid on Plasmodium falciparum elongation factor G (EF-G). Mol. Biochem. Parasitol. 192, 39-48. (doi:10.1016/j.molbiopara. 2013.10.003)
15. Jackson KE et al. 2011 Protein translation in Plasmodium parasites. Trends Parasitol. 27, 467-476. (doi:10.1016/j.pt.2011.05.005)
16. Johnson RA, McFadden GI, Goodman CD. 2011 Characterization of two malaria parasite organelle translation elongation factor G proteins: the likely targets of the anti-malarial fusidic acid. PLoS ONE 6, e20633. (doi:10.1371/journal. pone.0020633)
17. Hepler PK, Huff CG, Sprinz H. 1966 The fine structure of the exoerythrocytic stages of Plasmodium fallax. J. Cell Biol. 30, 333-358. (doi:10.1083/jcb.30.2.333)
18. Lemgruber L, Kudryashev M, Dekiwadia C, Riglar DT, Baum J, Stahlberg H, Ralph SA, Frischknecht F. 2013 Cryo-electron tomography reveals four-membrane architecture of the Plasmodium apicoplast. Malar. J 12, 25. (doi:10.1186/1475- 2875-12-25)
19. Vaidya AB, Akella R, Suplick K. 1989 Sequences similar to genes for two mitochondrial proteins and portions of ribosomal RNA in tandemly arrayed 6-kilobase-pair DNA of a malarial parasite. Mol. Biochem. Parasitol. 35, 97-108. (doi:10.1016/0166-6851(89)90112-6)
20. Gardner MJ, Feagin JE, Moore DJ, Rangachari K, Williamson DH, Wilson RJ. 1993 Sequence and organization of large subunit rRNA genes from the extrachromosomal 35 kb circular DNA of the malaria parasite Plasmodium falciparum. Nucleic Acids Res. 21, 1067-1071. (doi:10.1093/nar/21.5.1067)
21. Gardner MJ, Bates PA, Ling IT, Moore DJ, McCready S, Gunasekera MBR, Wilson RJM, Williamson DH. 1988 Mitochondrial DNA of the human malarial parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 31, 11-18. (doi:10.1016/0166- 6851(88)90140-5)
22. Feagin JE, Mericle B, Werner E, Morris M. 1997 Identification of additional rRNA fragments encoded by the Plasmodium falciparum 6 kb element. Nucleic Acids Res. 25, 438-446. (doi:10.1093/nar/25.2.438)
23. Waller RF et al. 1998 Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl Acad. Sci. USA 95, 12 352-12 357. (doi:10.1073/pnas.95.21.12352)
24. Ohta N, Sato N, Kuroiwa T. 1998 Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res. 26, 5190-5198. (doi:10.1093/nar/26.22.5190)
25. Ohta N, Matsuzaki M, Misumi O, Miyagishima SY, Nozaki H, Tanaka K, Shin IT, Kohara Y, Kuroiwa T. 2003 Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 10, 67-77. (doi:10.1093/dnares/10.2.67)
26. Matsuzaki M et al. 2004 Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428, 653-657. (doi:10.1038/ nature02398)
27. Armbrust EV et al. 2004 The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79-86. (doi:10.1126/science.1101156)
28. Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR. 2007 Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol. Genet. Genomics 277, 427-439. (10.1007/s00438-006-0199-4)
29. Chen F, Mackey AJ, Stoeckert Jr CJ, Roos DS. 2006 OrthoMCL-DB: querying a comprehensive multispecies collection of ortholog groups. Nucleic Acids Res. 34, D363-D368. (doi:10.1093/nar/gkj123)
30. Denny P, Preisser P, Williamson D, Wilson I. 1998 Evidence for a single origin of the 35 kb plastid DNA in apicomplexans. Protist 149, 51-59. (doi:10. 1016/S1434-4610(98)70009-4)
31. Cai X, Fuller AL, McDougald LR, Zhu G. 2003 Apicoplast genome of the coccidian Eimeria tenella. Gene 321, 39-46. (doi:10.1016/j.gene. 2003.08.008)
32. Akanuma G, Nanamiya H, Natori Y, Yano K, Suzuki S, Omata S, Ishizuka M, Sekine Y, Kawamura F. 2012 Inactivation of ribosomal protein genes in Bacillus subtilis reveals importance of each ribosomal protein for cell proliferation and cell differentiation. J. Bacteriol. 194, 6282-6291. (10.1128/JB. 01544-12)
33. Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, Agmon I, Bartels H, Franceschi F, Yonath A. 2001 High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107, 679-688. (doi:10.1016/S0092- 8674(01)00546-3)
34. Bubunenko MG, Schmidt J, Subramanian AR. 1994 Protein substitution in chloroplast ribosome evolution: a eukaryotic cytosolic protein has replaced its organelle homologue (L23) in spinach. J. Mol. Biol. 240, 28-41. (10.1006/jmbi.1994.1415)
35. Korepanov AP, Korobeinikova AV, Shestakov SA, Garber MB, Gongadze GM. 2012 Protein L5 is crucial for in vivo assembly of the bacterial 50S ribosomal subunit central protuberance. Nucleic Acids Res. 40, 9153-9159. (doi:10.1093/nar/gks676)
36. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK. 2003 Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115, 97-108. (doi:10.1016/S0092-8674(03) 00762-1)
37. Yamaguchi K, Subramanian AR. 2000 The plastid ribosomal proteins. Identification of all the proteins in the 50S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275, 28 466-28 482. (doi:10.1074/jbc.M005012200)
38. Kubo N, Arimura S. 2010 Discovery of the rpl10 gene in diverse plant mitochondrial genomes and its probable replacement by the nuclear gene for chloroplast RPL10 in two lineages of angiosperms. DNA Res. 17, 1-9. (doi:10.1093/dnares/dsp024)
39. Koc EC, Burkhart W, Blackburn K, Moyer MB, Schlatzer DM, Moseley A, Spremulli LL. 2001 The large subunit of the mammalian mitochondrial ribosome. Analysis of the complement of ribosomal proteins present. J. Biol. Chem. 276, 43 958-43 969. (doi:10.1074/jbc.M106510200)
40. UniProt C. 2013 Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41, D43-D47. (doi:10.1093/nar/gks1068)
41. Feng S, Chen Y, Gao YG. 2013 Crystal structure of 70S ribosome with both cognate tRNAs in the E and P sites representing an authentic elongation complex. PLoS ONE 8, e58829. (doi:10.1371/journal. pone.0058829)
42. Cukras AR, Green R. 2005 Multiple effects of S13 in modulating the strength of intersubunit interactions in the ribosome during translation. J. Mol. Biol. 349, 47-59. (doi:10.1016/j.jmb.2005.03.075)
43. Ramaswamy P, Woodson SA. 2009 S16 throws a conformational switch during assembly of 30S 50 domain. Nat. Struct. Mol. Biol. 16, 438-445. (doi:10.1038/nsmb.1585)
44. Ueda M, Nishikawa T, Fujimoto M, Takanashi H, Arimura S, Tsutsumi N, Kadowaki K. 2008 Substitution of the gene for chloroplast RPS16 was assisted by generation of a dual targeting signal. Mol. Biol. Evol. 25, 1566-1575. (doi:10.1093/molbev/msn102)
45. Mushegian A. 2005 Protein content of minimal and ancestral ribosome. RNA 11, 1400-1466. (doi:10. 1261/rna.2180205)
46. Rogalski M, Ruf S, Bock R. 2006 Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Res. 34, 4537-4545. (doi:10.1093/nar/gkl634)
47. Tobin C, Mandava CS, Ehrenberg M, Andersson DI, Sanyal S. 2010 Ribosomes lacking protein S20 are defective in mRNA binding and subunit association. J. Mol. Biol. 397, 767-776. (doi:10.1016/j.jmb. 2010.02.004)
48. Morita-Yamamuro C, Tsutsui T, Tanaka A, Yamaguchi J. 2004 Knock-out of the plastid ribosomal protein S21 causes impaired photosynthesis and sugar-response during germination and seedling development in Arabidopsis thaliana. Plant Cell Physiol. 45, 781-788. (doi:10.1093/pcp/pch093)
49. Holmes KL, Culver GM. 2005 Analysis of conformational changes in 16 S rRNA during the course of 30 S subunit assembly. J. Mol. Biol. 354, 340-357. (doi:10.1016/j.jmb.2005. 09.056)
50. Kaczanowska M, Ryden-Aulin M. 2007 Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev. 71, 477-494. (doi:10. 1128/MMBR.00013-07)
51. Williamson Jr. 2005 Assembly of the 30S ribosomal subunit. Q. Rev. Biophys. 38, 397-403. (doi:10. 1017/S0033583506004264)
52. Shajani Z, Sykes MT, Williamson Jr. 2011 Assembly of bacterial ribosomes. Annu. Rev. Biochem. 80, 501-526. (doi:10.1146/annurev-biochem-062608-160432)
53. Britton RA. 2009 Role of GTPases in bacterial ribosome assembly. Annu. Rev. Microbiol. 63, 155-176. (doi:10.1146/annurev.micro.091208. 073225)
54. Vedadi M et al. 2007 Genome-scale protein expression and structural biology of Plasmodium falciparum and related Apicomplexan organisms. Mol. Biochem. Parasitol. 151, 100-110. (doi:10. 1016/j.molbiopara.2006.10.011)
55. Kumar A, Tanveer A, Biswas S, Ram EV, Gupta A, Kumar B, Habib S. 2010 Nuclear-encoded DnaJ homologue of Plasmodium falciparum interacts with replication ori of the apicoplast genome. Mol. Microbiol. 75, 942-956. (doi:10.1111/j.1365-2958. 2009.07033.x)
56. Sato S, Wilson RJ. 2005 Organelle-specific cochaperonins in apicomplexan parasites. Mol. Biochem. Parasitol. 141, 133-143. (doi:10.1016/j. molbiopara.2005.01.010)
57. Caldas T, Binet E, Bouloc P, Costa A, Desgres J, Richarme G. 2000 The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23 S ribosomal RNA methyltransferase. J. Biol. Chem. 275, 16 414-16 419. (doi:10.1074/jbc. M001854200)
58. Formenoy LJ, Cunningham PR, Nurse K, Pleij CW, Ofengand J. 1994 Methylation of the conserved A1518-A1519 in Escherichia coli 16S ribosomal RNA by the ksgA methyltransferase is influenced by methylations around the similarly conserved U1512.G1523 base pair in the 30 terminal hairpin. Biochimie 76, 1123-1128. (doi:10.1016/0300-9084(94)90040-X)
59. Gu XR, Gustafsson C, Ku J, Yu M, Santi DV. 1999 Identification of the 16S rRNA m5C967 methyltransferase from Escherichia coli. Biochemistry 38, 4053-4057. (doi:10.1021/bi982364y)
60. O'Farrell HC, Pulicherla N, Desai PM, Rife JP. 2006 Recognition of a complex substrate by the KsgA/Dim1 family of enzymes has been conserved throughout evolution. RNA 12, 725-733. (doi:10. 1261/rna.2310406)
61. Klootwijk J, van den Bos RC, Planta RJ. 1972 Secondary methylation of yeast ribosomal RNA. FEBS Lett. 27, 102-106. (doi:10.1016/0014-5793(72)80419-8)
62. Noon KR, Bruenger E, McCloskey JA. 1998 Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus. J. Bacteriol. 180, 2883-2888.
63. Steege DA, Graves MC, Spremulli LL. 1982 Euglena gracilis chloroplast small subunit rRNA. Sequence and base pairing potential of the 30 terminus, cleavage by colicin E3. J. Biol. Chem. 257, 10 430-10 439.
64. Van Buul CP, Hamersma M, Visser W, Van Knippenberg PH. 1984 Partial methylation of two adjacent adenosines in ribosomes from Euglena gracilis chloroplasts suggests evolutionary loss of an intermediate stage in the methyl-transfer reaction. Nucleic Acids Res. 12, 9205-9208. (doi:10.1093/nar/12. 23.9205)
65. Lovgren JM, Bylund GO, Srivastava MK, Lundberg LA, Persson OP, Wingsle G, Wikstrom PM. 2004 The PRC-barrel domain of the ribosome maturation protein RimM mediates binding to ribosomal protein S19 in the 30S ribosomal subunits. RNA 10, 1798-1812. (doi:10.1261/rna. 7720204)
66. Linder P, Lasko PF, Ashburner M, Leroy P, Nielsen PJ, Nishi K, Schnier J, Slonimski PP. 1989 Birth of the D-E-A-D box. Nature 337, 121-122. (doi:10. 1038/337121a0)
67. Jankowsky E, Gross CH, Shuman S, Pyle AM. 2001 Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science 291, 121-125. (doi:10.1126/science.291.5501.121)
68. Linder P. 2006 Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res. 34, 4168-4180. (doi:10.1093/nar/gkl468)
69. Mohr S, Stryker JM, Lambowitz AM. 2002 A DEADbox protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109, 769-779. (doi:10.1016/S0092-8674(02)00771-7)
70. Charollais J, Dreyfus M, Iost I. 2004 CsdA, a coldshock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res. 32, 2751-2759. (doi:10.1093/nar/gkh603)
71. Charollais J, Pflieger D, Vinh J, Dreyfus M, Iost I. 2003 The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli. Mol. Microbiol. 48, 1253-1265. (doi:10.1046/j.1365-2958.2003. 03513.x)
72. Jagessar KL, Jain C. 2010 Functional and molecular analysis of Escherichia coli strains lacking multiple DEAD-box helicases. RNA 16, 1386-1392. (doi:10. 1261/rna.2015610)
73. Jain C. 2008 The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA 14, 381-389. (doi:10. 1261/rna.800308)
74. Sharpe Elles LM, Sykes MT, Williamson JR, Uhlenbeck OC. 2009 A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit. Nucleic Acids Res. 37, 6503-6514. (doi:10.1093/nar/gkp711)
75. McConkey GA, Rogers MJ, McCutchan TF. 1997 Inhibition of Plasmodium falciparum protein synthesis. Targeting the plastid-like organelle with thiostrepton. J. Biol. Chem. 272, 2046-2049. (doi:10.1074/jbc.272.4.2046)
76. Dahl EL, Shock JL, Shenai BR, Gut J, DeRisi JL, Rosenthal PJ. 2006 Tetracyclines specifically target the apicoplast of the malaria parasite Plasmodium falciparum. Antimicrob. Agents Chemother. 50, 3124-3131. (doi:10.1128/AAC.00394-06)
77. Budimulja AS, Tapchaisri P, Wilairat P, Marzuki S. 1997 The sensitivity of Plasmodium protein synthesis to prokaryotic ribosomal inhibitors. Mol. Biochem. Parasitol. 84, 137-141. (doi:10.1016/S0166-6851(96)02781-8)
78. Camps M, Arrizabalaga G, Boothroyd J. 2002 An rRNA mutation identifies the apicoplast as the target for clindamycin in Toxoplasma gondii. Mol. Microbiol. 43, 1309-1318. (doi:10.1046/j.1365-2958.2002.02825.x)
79. Sidhu AB, Sun Q, Nkrumah LJ, Dunne MW, Sacchettini JC, Fidock DA. 2007 In vitro efficacy, resistance selection, and structural modeling studies implicate the malarial parasite apicoplast as the target of azithromycin. J. Biol. Chem. 282, 2494-2504. (doi:10.1074/jbc.M608615200)
80. Aminake MN, Schoof S, Sologub L, Leubner M, Kirschner M, Arndt HD, Pradel G. 2011 Thiostrepton and derivatives exhibit antimalarial and gametocytocidal activity by dually targeting parasite proteasome and apicoplast. Antimicrob. Agents Chemother. 55, 1338-1348. (doi:10.1128/AAC.01096-10)
81. Tarr SJ, Nisbet RE, Howe CJ. 2011 Transcript-level responses of Plasmodium falciparum to thiostrepton. Mol. Biochem. Parasitol. 179, 37-41. (doi:10.1016/j.molbiopara.2011.05.004)
82. Bulkley D, Innis CA, Blaha G, Steitz TA. 2010 Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc. Natl Acad. Sci. USA 107, 17 158-17 163. (doi:10.1073/pnas. 1008685107)
83. Schlunzen F, Harms JM, Franceschi F, Hansen HA, Bartels H, Zarivach R, Yonath A. 2003 Structural basis for the antibiotic activity of ketolides and azalides. Structure 11, 329-338. (doi:10.1016/S0969-2126(03)00022-4)
84. Xiong L, Korkhin Y, Mankin AS. 2005 Binding site of the bridged macrolides in the Escherichia coli ribosome. Antimicrob. Agents Chemother. 49, 281-288. (doi:10.1128/AAC.49.1.281-288.2005)
85. Dunkle JA, Xiong L, Mankin AS, Cate JH. 2010 Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc. Natl Acad. Sci. USA 107, 17 152-17 157. (doi:10.1073/pnas.1007988107)
86. Harms JM, Wilson DN, Schluenzen F, Connell SR, Stachelhaus T, Zaborowska Z, Spahn CM, Fucini P. 2008 Translational regulation via L11: molecular switches on the ribosome turned on and off by thiostrepton and micrococcin. Mol. Cell 30, 26-38. (doi:10.1016/j.molcel.2008.01.009)
87. Clough B, Strath M, Preiser P, Denny P, Wilson IR. 1997 Thiostrepton binds to malarial plastid rRNA. FEBS Lett. 406, 123-125. (doi:10.1016/S0014- 5793(97)00241-X)
88. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2013 GenBank. Nucleic Acids Res. 41, D36-D42. (doi:10.1093/nar/ gks1195)
89. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004 Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795. (doi:10. 1016/j.jmb.2004.05.028)
90. Kyte J, Doolittle RF. 1982 A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132. (doi:10.1016/0022-2836(82) 90515-0)
91. Aurrecoechea C et al. 2013 EuPathDB: the eukaryotic pathogen database. Nucleic Acids Res. 41, D684-D691. (doi:10.1093/nar/gks1113)
92. Podicheti R, Gollapudi R, Dong Q. 2009 WebGBrowse: a web server for GBrowse. Bioinformatics 25, 1550-1551. (doi:10.1093/bioinformatics/btp239)
93. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI. 2003 Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299, 705-708. (doi:10.1126/science.1078599)
94. Zuegge J, Ralph S, Schmuker M, McFadden GI, Schneider G. 2001 Deciphering apicoplast targeting signals-feature extraction from nuclear-encoded precursors of Plasmodium falciparum apicoplast proteins. Gene 280, 19-26. (doi:10.1016/S0378-1119(01)00776-4)
95. Bender A, van Dooren GG, Ralph SA, McFadden GI, Schneider G. 2003 Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum. Mol. Biochem. Parasitol. 132, 59-66. (doi:10.1016/j.molbiopara.2003. 07.001)
96. Claros MG, Vincens P. 1996 Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241, 779-786. (doi:10.1111/j. 1432-1033.1996.00779.x)
97. Logan-Klumpler FJ et al. 2012 GeneDB: an annotation database for pathogens. Nucleic Acids Res. 40, D98-D108. (doi:10.1093/nar/gkr1032)
98. Rother M, Rother K, Puton T, Bujnicki JM. 2011 ModeRNA: a tool for comparative modeling of RNA 3D structure. Nucleic Acids Res. 39, 4007-4022. (doi:10.1093/nar/gkq1320)
99. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A. 2007 Comparative protein structure modeling using MODELLER. Curr. Protoc. Protein Sci. 50, 2.9.1-2.9.31. (doi:10.1002/0471140864.ps0209s50)
100. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009 AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791. (doi:10.1002/jcc.21256)