Ycf93 (orf105), a small apicoplast-encoded membrane protein in the relict plastid of the malaria parasite Plasmodium falciparum that is conserved in Apicomplexa

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Goodman, Christopher D ^a   McFadden, Geoffrey I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINONIN; CELL MEMBRANE PROTEIN; UNCLASSIFIED DRUG; YCF93 PROTEIN; MEMBRANE PROTEIN; PROTOZOAL PROTEIN;

APICOMPLEXA; APICOPLAST; ARTICLE; ASEXUAL REPRODUCTION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE PRODUCT; GENETIC CODE; GENOME; IMMUNOFLUORESCENCE; MICROBIAL GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLASMODIUM FALCIPARUM; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; WESTERN BLOTTING; YCF93 GENE; AMINO ACID SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; PLASTID; PROTEIN DEGRADATION; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; APICOMPLEXA; APICOPLASTS; CONSERVED SEQUENCE; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PLASTIDS; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY;

EID: 84899431930     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091178     Document Type: Article

References (59)

1. Tan KR, Magill AJ, Parise ME, Arguin PM, Centers for Disease C, et al. (2011) Doxycycline for malaria chemoprophylaxis and treatment: report from the CDC expert meeting on malaria chemoprophylaxis. Am J Trop Med Hyg 84: 517-531.
2. Krishna S, Staines HM (2012) Non-Antifolate Antibiotics: Clindamycin, Doxycycline, Azithromycin and Fosmidomycin. In: Staines HM, Krisha S, editors. Treatment and Prevention of Malaria: Antimalarial Drug Chemistry, Action and Use: Springer. pp. 141-156.
3. Goodman CD, Su V, McFadden GI (2007) The effects of anti-bacterials on the malaria parasite Plasmodium falciparum. Mol Biochem Parasitol 152: 181-191.
4. Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 107: 10949-10954.
5. McFadden GI, Waller RF (1997) Plastids in parasites of humans. BioEssays 19: 1033-1040. (Pubitemid 27510364)
6. Okamoto N, McFadden GI (2008) The mother of all parasites. Future Microbiol 3: 391-395.
7. Fichera ME, Roos DS (1997) A plastid organelle as a drug target in apicomplexan parasites. Nature 390: 407-409. (Pubitemid 28027322)
8. Wilson RJM, Denny PW, Preiser PR, Rangachari K, Roberts K, et al. (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum . J Mol Biol 261: 155-172. (Pubitemid 26275799)
9. El Bakkouri M, Pow A, Mulichak A, Cheung KL, Artz JD, et al. (2010) The Clp chaperones and proteases of the human malaria parasite Plasmodium falciparum. J Mol Biol 404: 456-477.
10. Preiser P, Williamson DH, Wilson RJ (1995) tRNA genes transcribed from the plastid-like DNA of Plasmodium falciparum. Nucl Acids Res 23: 4329-4336.
11. Hallick RB, Bairoch A (1994) Proposals for the Naming of Chloroplast Genes. III. Nomenclature for Open Reading Frames Encoded in Chloroplast Genomes. Plant Mol Biol Reporter 12: S29-S30.
12. Waller RF, Cowman AF, Reed MB, McFadden GI (2000) Protein trafficking to the plastid in Plasmodium falciparum is via the secretory pathway. EMBO J 19: 1794-1802. (Pubitemid 30204391)
13. Bordier C (1981) Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 256: 1604-1607.
14. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, et al. (2004) Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216. (Pubitemid 39490083)
15. Zhang YJ, Tian HF, Wen JF (2009) The evolution of YidC/Oxa/Alb3 family in the three domains of life: a phylogenomic analysis. BMC Evol Biol 9: 137.
16. van Dooren GG, Marti M, Tonkin CJ, Stimmler LM, Cowman AF, et al. (2005) Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol 57: 405-419. (Pubitemid 40979342)
17. Drew DR, Sanders PR, Crabb BS (2005) Plasmodium falciparum merozoite surface protein 8 is a ring-stage membrane protein that localizes to the parasitophorous vacuole of infected erythrocytes. Infect Immun 73: 3912-3922. (Pubitemid 40923129)
18. Triglia T, Healer J, Caruana SR, Hodder AN, Anders RF, et al. (2000) Apical membrane antigen 1 plays a central role in erythrocyte invasion by Plasmodium species. Mol Microbiol 38: 706-718.
19. Kato Y, Sakamoto W (2013) Plastid protein degradation during leaf development and senescence: Role of proteases and chaperones. Advances in Photosynthesis and Respiration 36: 453-477.
20. van Dooren GG, Su V, D'Ombrain MC, McFadden GI (2002) Processing of an apicoplast leader sequence in Plasmodium falciparum and the identification of a putative leader cleavage enzyme. J Biol Chem 277: 23612-23619. (Pubitemid 34952198)
21. Ponpuak M, Klemba M, Park M, Gluzman IY, Lamppa GK, et al. (2007) A role for falcilysin in transit peptide degradation in the Plasmodium falciparum apicoplast. Mol Microbiol 63: 314-334. (Pubitemid 46058922)
22. Rathore S, Sinha D, Asad M, Bottcher T, Afrin F, et al. (2010) A cyanobacterial serine protease of Plasmodium falciparum is targeted to the apicoplast and plays an important role in its growth and development. Mol Microbiol 77: 873-890.
23. Lin W, Chan M, Sim TS (2009) Atypical caseinolytic protease homolog from Plasmodium falciparum possesses unusual substrate preference and a functional nuclear localization signal. Parasitol Res 105: 1715-1722.
24. Giglione C, Meinnel T (2001) Organellar peptide deformylases: universality of the N-terminal methionine cleavage mechanism. Trends Plant Sci 6: 566-572. (Pubitemid 34004078)
25. Giglione C, Vallon O, Meinnel T (2003) Control of protein life-span by Nterminal methionine excision. Embo J 22: 13-23. (Pubitemid 36091265)
26. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
27. Tonkin CJ, Van Dooren GG, Spurck TP, Struck NS, Good RT, et al. (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. (Pubitemid 38987938)
28. Giglione C, Pierre M, Meinnel T (2000) Peptide deformylase as a target for new generation, broad spectrum antimicrobial agents. Mol Microbiol 36: 1197-1205. (Pubitemid 30449958)
29. Giglione C, Meinnel T (2002) The situation on antimicrobial agents and chemotherapy in 2002: Highlights of the 42nd ICAAC. Expert Opin Ther Targets 6: 691-697. (Pubitemid 36054580)
30. Madison V, Duca J, Bennett F, Bohanon S, Cooper A, et al. (2002) Binding affinities and geometries of various metal ligands in peptide deformylase inhibitors. Biophys Chem 101-102: 239-247. (Pubitemid 35462050)
31. Clements JM, Beckett RP, Brown A, Catlin G, Lobell M, et al. (2001) Antibiotic activity and characterization of BB-3497, a novel peptide deformylase inhibitor. Antimicrob Agents Chemother 45: 563-570. (Pubitemid 32105294)
32. Molteni V, He X, Nabakka J, Yang K, Kreusch A, et al. (2004) Identification of novel potent bicyclic peptide deformylase inhibitors. Bioorg Med Chem Lett 14: 1477-1481. (Pubitemid 38299432)
33. Wiesner J, Sanderbrand S, Altincicek B, Beck E, Jomaa H (2001) Seeking new targets for antiparasitic agents. Trends Parasitol 17: 7-8.
34. Bracchi-Ricard V, Nguyen KT, Zhou Y, Rajagopalan PTR, Chakrabarti D, et al. (2001) Characterization of an eukaryotic peptide deformylase from Plasmodium falciparum. Archives of Biochemistry and Biophysics 396: 162-170. (Pubitemid 34073173)
35. Dahl EL, Rosenthal PJ (2007) Multiple antibiotics exert delayed effects against the Plasmodium falciparum apicoplast. Antimicrob Agents Chemother 51: 3485-3490. (Pubitemid 47519333)
36. Dahl EL, Rosenthal PJ (2008) Apicoplast translation, transcription and genome replication: targets for antimalarial antibiotics. Trends Parasitol 24: 279-284.
37. Dahl EL, Shock JL, Shenai BR, Gut J, DeRisi JL, et al. (2006) Tetracyclines specifically target the apicoplast of the malaria parasite Plasmodium falciparum. Antimicrob Agents Chemother 50: 3124-3131. (Pubitemid 44396421)
38. Nair SC, Brooks CF, Goodman CD, Strurm A, McFadden GI, et al. (2011) Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J Exp Med 208: 1547-1559.
39. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, et al. (1999) Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285: 1573-1576. (Pubitemid 29420582)
40. Yeh E, DeRisi J (2011) Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum . PLoS Biology 9: e1001138.
41. Wellner D, Panneerselvam C, Horecker BL (1990) Sequencing of peptides and proteins with blocked N-terminal amino acids: N-acetylserine or N-acetylthreonine. Proc Natl Acad Sci U S A 87: 1947-1949.
42. Arisue N, Hashimoto T, Mitsui H, Palacpac NM, Kaneko A, et al. (2012) The Plasmodium apicoplast genome: conserved structure and close relationship of P. ovale to rodent malaria parasites. Mol Biol Evol 29: 2095-2099.
43. Sato S, Sesay AK, Holder AA (2013) The unique structure of the apicoplast genome of the rodent malaria parasite Plasmodium chabaudi chabaudi. PLoS One 8: e61778.
44. Imura T, Sato S, Sato Y, Sakamoto D, Isobe T, et al. (2013) The apicoplast genome of Leucocytozoon caulleryi, a pathogenic apicomplexan parasite of the chicken. Parasitol Res published online 04 December 2013 DOI 10.1007/s00436-013-3712-9.
45. Cai X, Fuller AL, McDougald LR, Zhu G (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321: 39-46. (Pubitemid 37421393)
46. Köhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, et al. (1997) A plastid of probable green algal origin in apicomplexan parasites. Science 275: 1485-1488.
47. Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, et al. (2007) Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 3: 1401-1413. (Pubitemid 350085605)
48. Lau AO, McElwain TF, Brayton KA, Knowles DP, Roalson EH (2009) Babesia bovis: a comprehensive phylogenetic analysis of plastid-encoded genes supports green algal origin of apicoplasts. Exp Parasitol 123: 236-243.
49. Gardner MJ, Bishop R, Shah T, de Villiers EP, Carlton JM, et al. (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309: 134-137. (Pubitemid 40934992)
50. Obornik M, Modry D, Lukes M, Cernotikova-Stribrna E, Cihlar J, et al. (2012) Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist 163: 306-323.
51. Moore RB, Obornik M, Janouskovec J, Chrudimsky T, Vancova M, et al. (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451: 959-963. (Pubitemid 351301735)
52. Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
53. Smilkstein M, Sriwilaijaroen N, Kelly JX, Wilairat P, Riscoe M (2004) Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob Agents Chemother 48: 1803-1806. (Pubitemid 38544392)
54. Mullin KA, Lim L, Ralph SA, Spurck TP, Handman E, et al. (2006) Membrane transporters in the relict plastid of malaria parasites. Proc Natl Acad Sci U S A 103: 9572-9577. (Pubitemid 43955866)
55. Kalanon M, Tonkin CJ, McFadden GI (2009) Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell 8: 1146-1154.
56. Boyle MJ, Richards JS, Gilson PR, Chai W, Beeson JG (2010) Interactions with heparin-like molecules during erythrocyte invasion by Plasmodium falciparum merozoites. Blood 115: 4559-4568.
57. Kumar N, Koski G, Harada M, Aikawa M, Zheng H (1991) Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Mol Biochem Parasitol 48: 47-58.
58. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. (Pubitemid 350162903)
59. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580. (Pubitemid 33032862)