The mRNA-bound proteome of the human malaria parasite Plasmodium falciparum

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Bunnik, Evelien M ^a   Batugedara, Gayani ^a   Saraf, Anita ^b   Prudhomme, Jacques ^a   Florens, Laurence ^b   Le Roch, Karine G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

Gene expression; Post transcriptional regulation; Protein domains; RNA binding proteins; Translation

Indexed keywords

CITH PROTEIN; DOZI PROTEIN; MESSENGER RNA; MUSASHI PROTEIN; PFALBA1 PROTEIN; PFALBA2 PROTEIN; PFALBA3 PROTEIN; PFALBA4 PROTEIN; PFCELF2 PROTEIN; PROTEOME; REGULATOR PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

APICOMPLEXAN LIFE CYCLE STAGE; ARTICLE; CONTROLLED STUDY; EUKARYOTE; GENE ONTOLOGY; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA DEGRADATION; TRANSLATION REGULATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; GENOME; HUMAN; MALARIA FALCIPARUM; PARASITOLOGY; PATHOGENICITY; PROTEIN DOMAIN; PROTEIN SYNTHESIS; RNA PROCESSING;

GENE EXPRESSION REGULATION; GENOME; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTEIN BIOSYNTHESIS; PROTEIN DOMAINS; PROTEOME; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA-BINDING PROTEINS;

EID: 84984600096     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-1014-0     Document Type: Article

References (81)

1. WHO. The World Malaria Report. 2015. http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/.
2. Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Mao S, Sam B, et al. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 2014;371:411-23.
3. Takala-Harrison S, Jacob CG, Arze C, Cummings MP, Silva JC, Dondorp AM, Fukuda MM, Hien TT, Mayxay M, Noedl H, et al. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in Southeast Asia. J Infect Dis. 2015;211:670-9.
4. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002;419:498-511.
5. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 2003;1:E5.
6. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Winzeler EA. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science. 2003;301:1503-8.
7. Young JA, Winzeler EA. Using expression information to discover new drug and vaccine targets in the malaria parasite Plasmodium falciparum. Pharmacogenomics. 2005;6:17-26.
8. Balaji S, Babu MM, Iyer LM, Aravind L. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res. 2005;33:3994-4006.
9. Bischoff E, Vaquero C. In silico and biological survey of transcription-associated proteins implicated in the transcriptional machinery during the erythrocytic development of Plasmodium falciparum. BMC Genomics. 2010;11:34.
10. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature. 2008;455:757-63.
11. Coulson RM, Hall N, Ouzounis CA. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res. 2004;14:1548-54.
12. Duffy MF, Selvarajah SA, Josling GA, Petter M. The role of chromatin in Plasmodium gene expression. Cell Microbiol. 2012;14:819-28.
13. Salcedo-Amaya AM, Hoeijmakers WA, Bartfai R, Stunnenberg HG. Malaria: could its unusual epigenome be the weak spot? Int J Biochem Cell Biol. 2010;42:781-4.
14. Bunnik EM, Chung DW, Hamilton M, Ponts N, Saraf A, Prudhomme J, Florens L, Le Roch KG. Polysome profiling reveals translational control of gene expression in the human malaria parasite Plasmodium falciparum. Genome Biol. 2013;14:R128.
15. Caro F, Ahyong V, Betegon M, DeRisi JL. Genome-wide regulatory dynamics of translation in the asexual blood stages. Elife. 2014;3:e04106.
16. Foth BJ, Zhang N, Mok S, Preiser PR, Bozdech Z. Quantitative protein expression profiling reveals extensive post-transcriptional regulation and post-translational modifications in schizont-stage malaria parasites. Genome Biol. 2008;9:R177.
17. Le Roch KG, Johnson JR, Florens L, Zhou Y, Santrosyan A, Grainger M, Yan SF, Williamson KC, Holder AA, Carucci DJ, et al. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 2004;14:2308-18.
18. Aravind L, Iyer LM, Wellems TE, Miller LH. Plasmodium biology: genomic gleanings. Cell. 2003;115:771-85.
19. Zhang M, Fennell C, Ranford-Cartwright L, Sakthivel R, Gueirard P, Meister S, Caspi A, Doerig C, Nussenzweig RS, Tuteja R, et al. The Plasmodium eukaryotic initiation factor-2alpha kinase IK2 controls the latency of sporozoites in the mosquito salivary glands. J Exp Med. 2010;207:1465-74.
20. Muller K, Matuschewski K, Silvie O. The Puf-family RNA-binding protein Puf2 controls sporozoite conversion to liver stages in the malaria parasite. PLoS One. 2011;6:e19860.
21. Gomes-Santos CS, Braks J, Prudencio M, Carret C, Gomes AR, Pain A, Feltwell T, Khan S, Waters A, Janse C, et al. Transition of Plasmodium sporozoites into liver stage-like forms is regulated by the RNA binding protein Pumilio. PLoS Pathog. 2011;7:e1002046.
22. Lindner SE, Mikolajczak SA, Vaughan AM, Moon W, Joyce BR, Sullivan Jr WJ, Kappe SH. Perturbations of Plasmodium Puf2 expression and RNA-seq of Puf2-deficient sporozoites reveal a critical role in maintaining RNA homeostasis and parasite transmissibility. Cell Microbiol. 2013;15:1266-83.
23. Guerreiro A, Deligianni E, Santos JM, Silva PA, Louis C, Pain A, Janse CJ, Franke-Fayard B, Carret CK, Siden-Kiamos I, Mair GR. Genome-wide RIP-Chip analysis of translational repressor-bound mRNAs in the Plasmodium gametocyte. Genome Biol. 2014;15:493.
24. Mair GR, Braks JA, Garver LS, Wiegant JC, Hall N, Dirks RW, Khan SM, Dimopoulos G, Janse CJ, Waters AP. Regulation of sexual development of Plasmodium by translational repression. Science. 2006;313:667-9.
25. Mair GR, Lasonder E, Garver LS, Franke-Fayard BM, Carret CK, Wiegant JC, Dirks RW, Dimopoulos G, Janse CJ, Waters AP. Universal features of post-transcriptional gene regulation are critical for Plasmodium zygote development. PLoS Pathog. 2010;6:e1000767.
26. Miao J, Fan Q, Parker D, Li X, Li J, Cui L. Puf mediates translation repression of transmission-blocking vaccine candidates in malaria parasites. PLoS Pathog. 2013;9:e1003268.
27. Balu B, Maher SP, Pance A, Chauhan C, Naumov AV, Andrews RM, Ellis PD, Khan SM, Lin JW, Janse CJ, et al. CCR4-associated factor 1 coordinates the expression of Plasmodium falciparum egress and invasion proteins. Eukaryot Cell. 2011;10:1257-63.
28. Vembar SS, Macpherson CR, Sismeiro O, Coppee JY, Scherf A. The PfAlba1 RNA-binding protein is an important regulator of translational timing in Plasmodium falciparum blood stages. Genome Biol. 2015;16:212.
29. Eshar S, Altenhofen L, Rabner A, Ross P, Fastman Y, Mandel-Gutfreund Y, Karni R, Llinas M, Dzikowski R. PfSR1 controls alternative splicing and steady-state RNA levels in Plasmodium falciparum through preferential recognition of specific RNA motifs. Mol Microbiol. 2015;96:1283-97.
30. Reddy BP, Shrestha S, Hart KJ, Liang X, Kemirembe K, Cui L, Lindner SE. A bioinformatic survey of RNA-binding proteins in Plasmodium. BMC Genomics. 2015;16:890.
31. Gerstberger S, Hafner M, Tuschl T. A census of human RNA-binding proteins. Nat Rev Genet. 2014;15:829-45.
32. Mitchell SF, Parker R. Principles and properties of eukaryotic mRNPs. Mol Cell. 2014;54:547-58.
33. He W, Parker R. Functions of Lsm proteins in mRNA degradation and splicing. Curr Opin Cell Biol. 2000;12:346-50.
34. Lopez-Barragan MJ, Lemieux J, Quinones M, Williamson KC, Molina-Cruz A, Cui K, Barillas-Mury C, Zhao K, Su XZ. Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics. 2011;12:587.
35. Wongsombat C, Aroonsri A, Kamchonwongpaisan S, Morgan HP, Walkinshaw MD, Yuthavong Y, Shaw PJ. Molecular characterization of Plasmodium falciparum Bruno/CELF RNA binding proteins. Mol Biochem Parasitol. 2014;198:1-10.
36. Braun L, Cannella D, Ortet P, Barakat M, Sautel CF, Kieffer S, Garin J, Bastien O, Voinnet O, Hakimi MA. A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog. 2010;6:e1000920.
37. Wang J, Liu X, Jia B, Lu H, Peng S, Piao X, Hou N, Cai P, Yin J, Jiang N, Chen Q. A comparative study of small RNAs in Toxoplasma gondii of distinct genotypes. Parasit Vectors. 2012;5:186.
38. Kolev NG, Tschudi C, Ullu E. RNA interference in protozoan parasites: achievements and challenges. Eukaryot Cell. 2011;10:1156-63.
39. Lee I, Hong W. RAP - a putative RNA-binding domain. Trends Biochem Sci. 2004;29:567-70.
40. Mitchell SF, Jain S, She M, Parker R. Global analysis of yeast mRNPs. Nat Struct Mol Biol. 2013;20:127-33.
41. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM, et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell. 2012;149:1393-406.
42. Baltz AG, Munschauer M, Schwanhausser B, Vasile A, Murakawa Y, Schueler M, Youngs N, Penfold-Brown D, Drew K, Milek M, et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell. 2012;46:674-90.
43. Matia-Gonzalez AM, Laing EE, Gerber AP. Conserved mRNA-binding proteomes in eukaryotic organisms. Nat Struct Mol Biol. 2015;22:1027-33.
44. Beckmann BM, Horos R, Fischer B, Castello A, Eichelbaum K, Alleaume AM, Schwarzl T, Curk T, Foehr S, Huber W, et al. The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs. Nat Commun. 2015;6:10127.
45. Wessels HH, Imami K, Baltz AG, Kolinksi M, Beldovskaya A, Selbach M, Small S, Ohler U, Landthaler M. The mRNA-bound proteome of the early fly embryo. Genome Res. 2016. doi: 10.1101/gr.200386.115.
46. Oehring SC, Woodcroft BJ, Moes S, Wetzel J, Dietz O, Pulfer A, et al. Organellar proteomics reveals hundreds of novel nuclear proteins in the malaria parasite Plasmodium falciparum. Genome Biol. 2012;13:R108.
47. Tarique M, Ahmad M, Ansari A, Tuteja R. Plasmodium falciparum DOZI, an RNA helicase interacts with eIF4E. Gene. 2013;522:46-59.
48. Wong W, Bai XC, Brown A, Fernandez IS, Hanssen E, Condron M, Tan YH, Baum J, Scheres SH. Cryo-EM structure of the Plasmodium falciparum 80S ribosome bound to the anti-protozoan drug emetine. Elife. 2014;3:e03080.
49. Sun M, Li W, Blomqvist K, Das S, Hashem Y, Dvorin JD, Frank J. Dynamical features of the Plasmodium falciparum ribosome during translation. Nucleic Acids Res. 2015;43:10515-24.
50. De Gaudenzi JG, Noe G, Campo VA, Frasch AC, Cassola A. Gene expression regulation in trypanosomatids. Essays Biochem. 2011;51:31-46.
51. Queiroz R, Benz C, Fellenberg K, Hoheisel JD, Clayton C. Transcriptome analysis of differentiating trypanosomes reveals the existence of multiple post-transcriptional regulons. BMC Genomics. 2009;10:495.
52. Ouellette M, Papadopoulou B. Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J Biol. 2009;8:100.
53. Kramer S, Carrington M. Trans-acting proteins regulating mRNA maturation, stability and translation in trypanosomatids. Trends Parasitol. 2011;27:23-30.
54. Simone LE, Keene JD. Mechanisms coordinating ELAV/Hu mRNA regulons. Curr Opin Genet Dev. 2013;23:35-43.
55. Balu B, Singh N, Maher SP, Adams JH. A genetic screen for attenuated growth identifies genes crucial for intraerythrocytic development of Plasmodium falciparum. PLoS One. 2010;5:e13282.
56. Baragana B, Hallyburton I, Lee MC, Norcross NR, Grimaldi R, Otto TD, Proto WR, Blagborough AM, Meister S, Wirjanata G, et al. A novel multiple-stage antimalarial agent that inhibits protein synthesis. Nature. 2015;522:315-20.
57. Friedersdorf MB, Keene JD. Advancing the functional utility of PAR-CLIP by quantifying background binding to mRNAs and lncRNAs. Genome Biol. 2014;15:R2.
58. Van Nostrand EL, Pratt GA, Shishkin AA, Gelboin-Burkhart C, Fang MY, Sundararaman B, Blue SM, Nguyen TB, Surka C, Elkins K, et al. Robust transcriptome-wide discovery of RNA-binding protein binding sites with enhanced CLIP (eCLIP). Nat Methods. 2016;13:508-14.
59. Date SV, Stoeckert Jr CJ. Computational modeling of the Plasmodium falciparum interactome reveals protein function on a genome-wide scale. Genome Res. 2006;16:542-9.
60. Chene A, Vembar SS, Riviere L, Lopez-Rubio JJ, Claes A, Siegel TN, Sakamoto H, Scheidig-Benatar C, Hernandez-Rivas R, Scherf A. PfAlbas constitute a new eukaryotic DNA/RNA-binding protein family in malaria parasites. Nucleic Acids Res. 2012;40:3066-77.
61. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell. 2009;36:932-41.
62. Decker CJ, Parker R. P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol. 2012;4:a012286.
63. Anderson P, Kedersha N. RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol. 2009;10:430-6.
64. Miller JE, Reese JC. Ccr4-Not complex: the control freak of eukaryotic cells. Crit Rev Biochem Mol Biol. 2012;47:315-33.
65. Preissler S, Reuther J, Koch M, Scior A, Bruderek M, Frickey T, Deuerling E. Not4-dependent translational repression is important for cellular protein homeostasis in yeast. EMBO J. 2015;34:1905-24.
66. Engel SR, Dietrich FS, Fisk DG, Binkley G, Balakrishnan R, Costanzo MC, Dwight SS, Hitz BC, Karra K, Nash RS, et al. The reference genome sequence of Saccharomyces cerevisiae: then and now. G3 (Bethesda). 2014;4:389-98.
67. Cunningham F, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. Ensembl 2015. Nucleic Acids Res. 2015;43:D662-9.
68. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42:D222-30.
69. Eddy SR. Profile hidden Markov models. Bioinformatics. 1998;14:755-63.
70. R Code Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2014. https://www.r-project.org/.
71. Fang H, Gough J. A domain-centric solution to functional genomics via dcGO Predictor. BMC Bioinformatics. 2013;14 Suppl 3:S9.
72. Trager W, Jensen JB. Human malaria parasites in continuous culture. Science. 1976;193:673-5.
73. Lambros C, Vanderberg JP. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol. 1979;65:418-20.
74. Lacsina JR, LaMonte G, Nicchitta CV, Chi JT. Polysome profiling of the malaria parasite Plasmodium falciparum. Mol Biochem Parasitol. 2011;179:42-6.
75. McDonald WH, Ohi R, Miyamoto DT, Mitchison TJ, Yates JR. Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LCMS/MS, 2-phase MudPIT, and 3-phase MudPIT. Internat J Mass Spectrometry. 2002;219:245-51.
76. Florens L, Washburn MP. Proteomic analysis by multidimensional protein identification technology. Methods Mol Biol. 2006;328:159-75.
77. Eng JK, McCormack AL, Yates JR. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom. 1994;5:976-89.
78. Tabb DL, McDonald WH, Yates 3rd JR. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res. 2002;1:21-6.
79. Zhang Y, Wen Z, Washburn MP, Florens L. Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal Chem. 2010;82:2272-81.
80. Choi H, Fermin D, Nesvizhskii AI. Significance analysis of spectral count data in label-free shotgun proteomics. Mol Cell Proteomics. 2008;7:2373-85.
81. Alexa A, Rahnenfuhrer J. topGO: enrichment analysis for gene ontology. R package version 2.6.0. 2010. http://www.bioconductor.org/packages/release/bioc/html/topGO.html.