In silico discovery of transcription regulatory elements in Plasmodium falciparum

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Young, Jason A ^a   Johnson, Jeffery R ^a   Benner, Chris ^b,c   Yan, S Frank ^d   Chen, Kaisheng ^d   Le Roch, Karine G ^e   Zhou, Yingyao ^d   Winzeler, Elizabeth A ^a,d  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; HEAT SHOCK PROTEIN;

ANTIGENIC VARIATION; ARTICLE; CELL INVASION; COMPUTER MODEL; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; GEL MOBILITY SHIFT ASSAY; GENE CLUSTER; GENE ENRICHMENT MOTIF SEARCHING ANALYSIS; GENE EXPRESSION; GENETIC ALGORITHM; GEOMETRY; LIFE CYCLE; MICROARRAY ANALYSIS; NONHUMAN; PLASMODIUM FALCIPARUM; PROMOTER REGION; PROTEIN SYNTHESIS; REPORTER GENE; SCORING SYSTEM; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEXUAL DEVELOPMENT; TRANSCRIPTION REGULATION; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; DNA REPLICATION; ERYTHROCYTE; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INTRON; METABOLISM; METHODOLOGY; MULTIGENE FAMILY; PARASITOLOGY; PATHOGENICITY; REGULATORY SEQUENCE; SPOROZOITE;

EUKARYOTA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

ALGORITHMS; ANIMALS; ANTIGENIC VARIATION; COMPUTATIONAL BIOLOGY; DNA REPLICATION; ERYTHROCYTES; GENOME, PROTOZOAN; HUMANS; INTRONS; MODELS, GENETIC; MULTIGENE FAMILY; PLASMODIUM FALCIPARUM; PROTEIN BIOSYNTHESIS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SEXUAL DEVELOPMENT; SPOROZOITES;

EID: 41049114729     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-70     Document Type: Article

References (69)

1. Gardner MJ Hall N Fung E White O Berriman M Hyman RW Carlton JM Pain A Nelson KE Bowman S Paulsen IT James K Eisen JA Rutherford K Salzberg SL Craig A Kyes S Chan MS Nene V Shallom SJ Suh B Peterson J Angiuoli S Pertea M Allen J Selengut J Haft D Mather MW Vaidya AB Martin DM Fairlamb AH Fraunholz MJ Roos DS Ralph SA McFadden GI Cummings LM Subramanian GM Mungall C Venter JC Carucci DJ Hoffman SL Newbold C Davis RW Fraser CM Barrell B Genome sequence of the human malaria parasite Plasmodium falciparum Nature 2002, 419(6906):498-511. 10.1038/ nature01097 12368864
2. Carlton JM Angiuoli SV Suh BB Kooij TW Pertea M Silva JC Ermolaeva MD Allen JE Selengut JD Koo HL Peterson JD Pop M Kosack DS Shumway MF Bidwell SL Shallom SJ van Aken SE Riedmuller SB Feldblyum TV Cho JK Quackenbush J Sedegah M Shoaibi A Cummings LM Florens L Yates JR Raine JD Sinden RE Harris MA Cunningham DA Preiser PR Bergman LW Vaidya AB van Lin LH Janse CJ Waters AP Smith HO White OR Salzberg SL Venter JC Fraser CM Hoffman SL Gardner MJ Carucci DJ Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii Nature 2002, 419(6906):512-519. 10.1038/nature01099 12368865
3. Hall N Karras M Raine JD Carlton JM Kooij TW Berriman M Florens L Janssen CS Pain A Christophides GK James K Rutherford K Harris B Harris D Churcher C Quail MA Ormond D Doggett J Trueman HE Mendoza J Bidwell SL Rajandream MA Carucci DJ Yates JR 3rd Kafatos FC Janse CJ Barrell B Turner CM Waters AP Sinden RE A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses Science 2005, 307(5706):82-86. 10.1126/science.1103717 15637271
4. Horrocks P Kilbey BJ Physical and functional mapping of the transcriptional start sites of Plasmodium falciparum proliferating cell nuclear antigen Mol Biochem Parasitol 1996, 82(2):207-215. 10.1016/ 0166-6851(96)02737-5 8946386
5. Crabb BS Cowman AF Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum Proc Natl Acad Sci U S A 1996, 93(14):7289-7294. 38976 8692985 10.1073/ pnas.93.14.7289
6. Su XZ Wellems TE Sequence, transcript characterization and polymorphisms of a Plasmodium falciparum gene belonging to the heat-shock protein (HSP) 90 family Gene 1994, 151(1-2):225-230. 10.1016/ 0378-1119(94)90661-0 7828879
7. Horrocks P Lanzer M Mutational analysis identifies a five base pair cis-acting sequence essential for GBP130 promoter activity in Plasmodium falciparum Mol Biochem Parasitol 1999, 99(1):77-87. 10.1016/ S0166-6851(98)00182-0 10215026
8. Voss TS Kaestli M Vogel D Bopp S Beck HP Identification of nuclear proteins that interact differentially with Plasmodium falciparum var gene promoters Mol Microbiol 2003, 48(6):1593-1607. 10.1046/ j.1365-2958.2003.03528.x 12791141
9. Militello KT Dodge M Bethke L Wirth DF Identification of regulatory elements in the Plasmodium falciparum genome Mol Biochem Parasitol 2004, 134(1):75-88. 10.1016/j.molbiopara.2003.11.004 14747145
10. Osta M Gannoun-Zaki L Bonnefoy S Roy C Vial HJ A 24 bp cis-acting element essential for the transcriptional activity of Plasmodium falciparum CDP-diacylglycerol synthase gene promoter Mol Biochem Parasitol 2002, 121(1):87-98. 10.1016/S0166-6851(02)00029-4 11985865
11. Pace T Olivieri A Sanchez M Albanesi V Picci L Kiamos IS Janse CJ Waters AP Pizzi E Ponzi M Set regulation in asexual and sexual Plasmodium parasites reveals a novel mechanism of stage-specific expression Mol Microbiol 2006, 60(4):870-882. 10.1111/j.1365-2958.2006.05141.x 16677299
12. Tham WH Payne PD Brown GV Rogerson SJ Identification of basic transcriptional elements required for rif gene transcription Int J Parasitol 2007, 37(6):605-615. 10.1016/j.ijpara.2006.11.006 17196595
13. 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(1):E5. 176545 12929205 10.1371/journal.pbio.0000005
14. 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(5639):1503-1508. 10.1126/science.1087025 12893887
15. Callebaut I Prat K Meurice E Mornon JP Tomavo S Prediction of the general transcription factors associated with RNA polymerase II in Plasmodium falciparum: Conserved features and differences relative to other eukaryotes BMC Genomics 2005, 6:100. 1199594 16042788 10.1186/ 1471-2164-6-100
16. Patankar S Munasinghe A Shoaibi A Cummings LM Wirth DF Serial analysis of gene expression in Plasmodium falciparum reveals the global expression profile of erythrocytic stages and the presence of anti-sense transcripts in the malarial parasite Mol Biol Cell 2001, 12(10):3114-3125. 60160 11598196
17. Munasinghe A Patankar S Cook BP Madden SL Martin RK Kyle DE Shoaibi A Cummings LM Wirth DF Serial analysis of gene expression (SAGE) in Plasmodium falciparum: Application of the technique to A-T rich genomes Mol Biochem Parasitol 2001, 113(1):23-34. 10.1016/S0166-6851(00)00378-9 11254951
18. Militello KT Patel V Chessler AD Fisher JK Kasper JM Gunasekera A Wirth DF RNA polymerase II synthesizes antisense RNA in Plasmodium falciparum Rna 2005, 11(4):365-370. 1370726 15703443 10.1261/rna.7940705
19. Gunasekera AM Patankar S Schug J Eisen G Kissinger J Roos D Wirth DF Widespread distribution of antisense transcripts in the Plasmodium falciparum genome Mol Biochem Parasitol 2004, 136(1):35-42. 10.1016/ j.molbiopara.2004.02.007 15138065
20. 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(5787):667-669. 1609190 16888139 10.1126/science.1125129
21. Florens L Washburn MP Raine JD Anthony RM Grainger M Haynes JD Moch JK Muster N Sacci JB Tabb DL Witney AA Wolters D Wu Y Gardner MJ Holder AA Sinden RE Yates JR Carucci DJ A proteomic view of the Plasmodium falciparum life cycle Nature 2002, 419(6906):520-526. 10.1038/ nature01107 12368866
22. Le Roch KG Johnson JR Florens L Zhou Y Santrosyan A Grainger M Yan SF Williamson KC Holder AA Carucci DJ Yates JR 3rd Winzeler EA Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle Genome Res 2004, 14(11):2308-2318. 525690 15520293 10.1101/gr.2523904
23. Chookajorn T Dzikowski R Frank M Li F Jiwani AZ Hartl DL Deitsch KW Epigenetic memory at malaria virulence genes Proc Natl Acad Sci U S A 2007, 104(3):899-902. 1764221 17209011 10.1073/pnas.0609084103
24. Bailey TLE C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers Proc Int Conf Intell Syst Mol Biol 1994, 2:28-36. 7584402
25. Hughes JD Estep PW Tavazoie S Church GM Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae J Mol Biol 2000, 296(5):1205-1214. 10.1006/jmbi.2000.3519 10698627
26. Liu XS Brutlag DL Liu JS An algorithm for finding protein-DNA binding sites with applications to chromatin-immunoprecipitation microarray experiments Nat Biotechnol 2002, 20(8):835-839. 12101404
27. Pavesi G Mauri G Pesole G An algorithm for finding signals of unknown length in DNA sequences Bioinformatics 2001, 17 Suppl 1:S207-14. 11473011
28. D'Haeseleer P How does DNA sequence motif discovery work? Nat Biotechnol 2006, 24(8):959-961. 10.1038/nbt0806-959 16900144
29. Harbison CT Gordon DB Lee TI Rinaldi NJ Macisaac KD Danford TW Hannett NM Tagne JB Reynolds DB Yoo J Jennings EG Zeitlinger J Pokholok DK Kellis M Rolfe PA Takusagawa KT Lander ES Gifford DK Fraenkel E Young RA Transcriptional regulatory code of a eukaryotic genome Nature 2004, 431(7004):99-104. 10.1038/nature02800 15343339
30. Zhou Y Young JA Santrosyan A Chen K Yan SF Winzeler EA In silico gene function prediction using ontology-based pattern identification Bioinformatics 2005, 21(7):1237-1245. 10.1093/bioinformatics/bti111 15531612
31. Ashburner M Ball CA Blake JA Botstein D Butler H Cherry JM Davis AP Dolinski K Dwight SS Eppig JT Harris MA Hill DP Issel-Tarver L Kasarskis A Lewis S Matese JC Richardson JE Ringwald M Rubin GM Sherlock G Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium Nat Genet 2000, 25(1):25-29. 10.1038/75556 10802651
32. Young JA Fivelman QL Blair PL de la Vega P Le Roch KG Zhou Y Carucci DJ Baker DA Winzeler EA The Plasmodium falciparum sexual development transcriptome: A microarray analysis using ontology-based pattern identification Mol Biochem Parasitol 2005, 143(1):67-79. 10.1016/ j.molbiopara.2005.05.007 16005087
33. GEMS: P. falciparum Analysis Homepage http://carrier.gnf.org/ publications/motif/
34. GEMS: P. falciparum Intron Analysis Results http://carrier.gnf.org/ publications/motif/Intron
35. Chow CS Wirth DF Linker scanning mutagenesis of the Plasmodium gallinaceum sexual stage specific gene pgs28 reveals a novel downstream cis-control element Mol Biochem Parasitol 2003, 129(2):199-208. 10.1016/ S0166-6851(03)00101-4 12850264
36. Khan SM Franke-Fayard B Mair GR Lasonder E Janse CJ Mann M Waters AP Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology Cell 2005, 121(5):675-687. 10.1016/ j.cell.2005.03.027 15935755
37. Planta RJ Goncalves PM Mager WH Global regulators of ribosome biosynthesis in yeast Biochem Cell Biol 1995, 73(11-12):825-834. 8721998
38. Cowman AF Crabb BS Invasion of red blood cells by malaria parasites Cell 2006, 124(4):755-766. 10.1016/j.cell.2006.02.006 16497586
39. Bradley PJ Ward C Cheng SJ Alexander DL Coller S Coombs GH Dunn JD Ferguson DJ Sanderson SJ Wastling JM Boothroyd JC Proteomic analysis of rhoptry organelles reveals many novel constituents for host-parasite interactions in Toxoplasma gondii J Biol Chem 2005, 280(40):34245-34258. 10.1074/jbc.M504158200 16002398
40. Flick K Chen Q var genes, PfEMP1 and the human host Mol Biochem Parasitol 2004, 134(1):3-9. 10.1016/j.molbiopara.2003.09.010 14747137
41. Kurtz S Shore D RAP1 protein activates and silences transcription of mating-type genes in yeast Genes Dev 1991, 5(4):616-628. 10.1101/ gad.5.4.616 2010087
42. Sussel L Shore D Separation of transcriptional activation and silencing functions of the RAP1-encoded repressor/activator protein 1: Isolation of viable mutants affecting both silencing and telomere length Proc Natl Acad Sci U S A 1991, 88(17):7749-7753. 52380 1881914 10.1073/ pnas.88.17.7749
43. Bro C Regenberg B Lagniel G Labarre J Montero-Lomeli M Nielsen J Transcriptional, proteomic, and metabolic responses to lithium in galactose-grown yeast cells J Biol Chem 2003, 278(34):32141-32149. 10.1074/jbc.M304478200 12791685
44. Cinato E Peleraux A Silve S Galiegue S Dhers C Picard C Jbilo O Loison G Casellas P A DNA microarray-based approach to elucidate the effects of the immunosuppressant SR31747A on gene expression in Saccharomyces cerevisiae Gene Expr 2002, 10(5-6):213-230. 12450214
45. Zakrzewska A Boorsma A Brul S Hellingwerf KJ Klis FM Transcriptional response of Saccharomyces cerevisiae to the plasma membrane-perturbing compound chitosan Eukaryot Cell 2005, 4(4):703-715. 1087819 15821130 10.1128/EC.4.4.703-715.2005
46. GEMS: P. falciparum Heat Shock Analysis Results http://carrier.gnf.org/ publications/motif/HeatShock2k/MAP/
47. Voss TS Thompson JK Waterkeyn J Felger I Weiss N Cowman AF Beck HP Genomic distribution and functional characterisation of two distinct and conserved Plasmodium falciparum var gene 5′ flanking sequences Mol Biochem Parasitol 2000, 107(1):103-115. 10.1016/S0166-6851(00)00176-6 10717306
48. Nussenzweig RS Zavala F A malaria vaccine based on a sporozoite antigen N Engl J Med 1997, 336(2):128-130. 10.1056/NEJM199701093360210 8988893
49. Ginsburg H Malaria Parasite Metabolic Pathways http://sites.huji.ac.il/ malaria/
50. Waller RF McFadden GI The apicoplast: A review of the derived plastid of apicomplexan parasites Curr Issues Mol Biol 2005, 7(1):57-79. 15580780
51. McGuire AM Hughes JD Church GM Conservation of DNA regulatory motifs and discovery of new motifs in microbial genomes Genome Res 2000, 10(6):744-757. 10.1101/gr.10.6.744 10854408
52. Martinez MJ Smith AD Li B Zhang MQ Harrod KS Computational prediction of novel components of lung transcriptional networks Bioinformatics 2007, 23(1):21-29. 10.1093/bioinformatics/btl531 17050569
53. van Noort V Huynen MA Combinatorial gene regulation in Plasmodium falciparum Trends Genet 2006, 22(2):73-78. 10.1016/j.tig.2005.12.002 16380193
54. Lu F Jiang H Ding J Mu J Valenzuela JG Ribeiro JM Su XZ cDNA sequences reveal considerable gene prediction inaccuracy in the Plasmodium falciparum genome BMC Genomics 2007, 8(1):255. 1978503 17662120 10.1186/ 1471-2164-8-255
55. Sinha S Tompa M Discovery of novel transcription factor binding sites by statistical overrepresentation Nucleic Acids Res 2002, 30(24):5549-5560. 140044 12490723 10.1093/nar/gkf669
56. Trager W Jensen JB Human malaria parasites in continuous culture Science 1976, 193(4254):673-675. 10.1126/science.781840 781840
57. Le Roch KG Zhou Y Batalov S Winzeler EA Monitoring the chromosome 2 intraerythrocytic transcriptome of Plasmodium falciparum using oligonucleotide arrays Am J Trop Med Hyg 2002, 67(3):233-243. 12408661
58. Zhou Y Abagyan R Match-only integral distribution (MOID) algorithm for high-density oligonucleotide array analysis BMC Bioinformatics 2002, 3:3. 65509 11835687 10.1186/1471-2105-3-3
59. Barrera L Benner C Tao YC Winzeler E Zhou Y Leveraging two-way probe-level block design for identifying differential gene expression with high-density oligonucleotide arrays BMC Bioinformatics 2004, 5:42. 411067 15099405 10.1186/1471-2105-5-42
60. Bahl A Brunk B Crabtree J Fraunholz MJ Gajria B Grant GR Ginsburg H Gupta D Kissinger JC Labo P Li L Mailman MD Milgram AJ Pearson DS Roos DS Schug J Stoeckert CJ Jr. Whetzel P PlasmoDB: The Plasmodium genome resource. A database integrating experimental and computational data Nucleic Acids Res 2003, 31(1):212-215. 165528 12519984 10.1093/nar/gkg081
61. Beer MA Tavazoie S Predicting gene expression from sequence Cell 2004, 117(2):185-198. 10.1016/S0092-8674(04)00304-6 15084257
62. Willett P Barnard JM Downs GM Chemical similarity searching J Chem Inf Comp Sci 1998, 38:983-996.
63. Tompa M Li N Bailey TL Church GM De Moor B Eskin E Favorov AV Frith MC Fu Y Kent WJ Makeev VJ Mironov AA Noble WS Pavesi G Pesole G Regnier M Simonis N Sinha S Thijs G van Helden J Vandenbogaert M Weng Z Workman C Ye C Zhu Z Assessing computational tools for the discovery of transcription factor binding sites Nat Biotechnol 2005, 23(1):137-144. 10.1038/nbt1053 15637633
64. MDScan http://motif.stanford.edu/distributions/mdscan
65. RepeatMasker http://www.repeatmasker.org
66. Militello KT Wirth DF A new reporter gene for transient transfection of Plasmodium falciparum Parasitol Res 2003, 89(2):154-157. 10.1007/ s00436-002-0721-5 12489017
67. Lambros C Vanderberg JP Synchronization of Plasmodium falciparum erythrocytic stages in culture J Parasitol 1979, 65(3):418-420. 10.2307/ 3280287 383936
68. Deitsch K Driskill C Wellems T Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes Nucleic Acids Res 2001, 29(3):850-853. 30384 11160909 10.1093/nar/ 29.3.850
69. Wu Y Sifri CD Lei HH Su XZ Wellems TE Transfection of Plasmodium falciparum within human red blood cells Proc Natl Acad Sci U S A 1995, 92(4):973-977. 42619 7862676 10.1073/pnas.92.4.973