1887

Chapter 5 : The Transcriptome of the Malaria Parasite

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

The Transcriptome of the Malaria Parasite , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817558/9781555813307_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555817558/9781555813307_Chap05-2.gif

Abstract:

This chapter explains how such data, when combined, can give a comprehensive overview of the transcriptome of the malaria parasite throughout its life cycle. These data are expected to lead to the identification of key -specific regulatory targets, a fundamental step for the development of new antimalarials. Gene expression throughout the cell cycle is usually regulated by complex interactions between DNA regulatory motifs and transcription factors that bind to these motifs, as well as regulation by distinct chromatin structures. Parasite isolates possess a high degree of diversity within their genes because of duplications, deletions, or recombination events that provide the parasite with a huge repertoire of antigenic determinants. Before the complete release of the genome sequence, several genomic efforts were accomplished to investigate the transcriptome of the malaria parasite. The first large-scale expression study of was accomplished with a DNA microarray platform constructed using a nuclease-generated genomic library. With the completion of the genome, two transcriptional analyses covering the entire genome were published. Both techniques allow effective and complete genome design. The 70-mer oligonucleotide array study was confined to a high-resolution analysis of the erythrocytic cell cycle. Gene expression in parasitic protozoa has shown itself to be unique when it comes to mechanisms of regulation. For instance, and other members of the Trypanosomatidae have polycistronic transcription with maturation of their mRNA by transplicing events.

Citation: Le Roch K, Winzeler E. 2005. The Transcriptome of the Malaria Parasite , p 68-84. In Sherman I (ed), Molecular Approaches to Malaria. ASM Press, Washington, DC. doi: 10.1128/9781555817558.ch5

Key Concept Ranking

Gene Expression and Regulation
0.6753685
Transcription Start Site
0.5762161
Bacteria and Archaea
0.51806
DNA Synthesis
0.45915133
Fatty Acid Biosynthesis
0.43443614
0.6753685
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555817558.chap5
1. Agabian, N. 1990. Trans splicing of nuclear premRNAs. Cell 61: 1157 1160.
2. Beetham, J. K.,, J. E. Donelsin,, and R. R. Dahlin. 2003. Surface glycoprotein PSA (GP46) expression during short- and long-term culture of Leishmania chagasi. Mol. Biochem. Parasitol. 131: 109 117.
3. Beetham, J. K.,, K. S. Myung,, J. J. McCoy,, M. E. Wilson,, and J. E. Donelson. 1997. Glycoprotein 46 mRNA abundance is post-transcriptionally regulated during development of Leishmania chagasi promastigotes to an infectious form. J. Biol. Chem. 272: 17360 17366.
4. Bennett, B. J.,, J. Thompson,, and R. L. Coppel. 1995. Identification of Plasmodium falciparum histone 2B and histone 3 genes. Mol. Biochem.Parasitol. 70: 231 233.
5. Bischoff, E.,, M. Guillotte,, O. Mercereau-Puijalon,, and S. Bonnefoy. 2000. A member of the Plasmodium falciparum Pf60 multigene family codes for a nuclear protein expressed by readthrough of an internal stop codon. Mol. Microbiol. 35: 1005 1016.
6. Blumenthal, T.,, D. Evans,, C. D. Link,, A. Guffanti,, D. Lawson,, J. Thierry-Mieg,, D. Thierry-Mieg,, W. L. Chiu,, K. Duke,, M. Kiraly,, and S. K. Kim. 2002. A global analysis of Caenorhabditis elegans operons. Nature 417: 851 854.
7. Bozdech, Z.,, M. Llinas,, B. L. Pulliam,, E. D. Wong,, J. Zhu,, and J. L. DeRisi. 2003a. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5.
8. Bozdech, Z.,, J. Zhu,, M. P. Joachimiak,, F. E. Cohen,, B. Pulliam,, and J. L. DeRisi. 2003b. Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biol. 4: R9.
9. Breitling, R.,, A. Amtmann,, and P. Herzyk. 2004a. Graph-based Iterative Group Analysis enhances microarray interpretation. BMC Bioinformatics 5: 100.
10. Breitling, R.,, A. Amtmann,, and P. Herzyk. 2004b. Iterative Group Analysis (iGA): a simple tool to enhance sensitivity and facilitate interpretation of microarray experiments. BMC Bioinformatics 5: 34.
11. Burchmore, R. J.,, and S. M. Landfear. 1998. Differential regulation of multiple glucose transporter genes in Leishmania mexicana. J. Biol. Chem. 273: 29118 29126.
12. Cary, C.,, D. Lamont,, J. P. Dalton,, and C. Doerig. 1994. Plasmodium falciparum chromatin:nucleosomal organisation and histone-like proteins. Parasitol. Res. 80: 255 258.
13. Chen, Q.,, V. Fernandez,, A. Sundstrom,, M. Schlichtherle,, S. Datta,, P. Hagblom,, and M. Wahlgren. 1998. Developmental selection of var gene expression in Plasmodium falciparum. Nature 394: 392 395.
14. Cheng, Q.,, N. Cloonan,, K. Fischer,, J. Thompson,, G. Waine,, M. Lanzer,, and A. Saul. 1998. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol. 97: 161 176.
15. Coulson, R. M.,, N. Hall,, and C. A. Ouzounis. 2004. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res. 14: 1548 1554.
16. Crabb, B. S.,, and A. F. Cowman. 1996. Characterization of promoters and stable transfection by homologous and nonhomologous recombination in Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 93: 7289 7294.
17. Crabb, B. S.,, T. Triglia,, J. G. Waterkeyn,, and A. F. Cowman. 1997. Stable transgene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 90: 131 144.
18. Creedon, K. A.,, D. C. Kaslow,, P. K. Rathod,, and T. E. Wellems. 1992. Identification of a Plasmodium falciparum histone 2A gene. Mol. Biochem. Parasitol. 54: 113 115.
19. Cui, L.,, Q. Fan,, and J. Li. 2002. The malaria parasite Plasmodium falciparum encodes members of the Puf RNA-binding protein family with conserved RNA binding activity. Nucleic Acids Res. 30: 4607 4617.
20. Daily, J. P.,, K. G. Le Roch,, O. Sarr,, D. Ndiaye,, A. Lukens,, Y. Zhou,, O. Ndir,, S. Mboup,, A. Sultan,, E. A. Winzeler,, and D. F. Wirth. 2005. In vivo transcriptome of Plasmodium falciparum reveals overexpression of transcripts that encode surface proteins. J. Infect. Dis. 191: 1196 1203.
21. Darkin-Rattray, S. J.,, A. M. Gurnett,, R. W. Myers,, P. M. Dulski,, T. M. Crumley,, J. J. Allocco,, C. Cannova,, P. T. Meinke,, S. L. Colletti,, M. A. Bednarek,, S. B. Singh,, M. A. Goetz,, A. W. Dombrowski,, J. D. Polishook,, and D. M. Schmatz. 1996. Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase. Proc. Natl.Acad. Sci. USA 93: 13143 13147.
22. Dechering, K. J.,, A. M. Kaan,, W. Mbacham,, D. F. Wirth,, W. Eling,, R. N. Konings,, and H. G. Stunnenberg. 1999. Isolation and functional characterization of two distinct sexual-stage-specific promoters of the human malaria parasite Plasmodium falciparum. Mol. Cell. Biol. 19: 967 978.
23. Dechering, K. J.,, J. Thompson,, H. J. Dodemont,, W. Eling,, and R. N. Konings. 1997. Developmentally regulated expression of pfs16, a marker for sexual differentiation of the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 89: 235 244.
24. Deitsch, K. W.,, M. S. Calderwood,, and T. E. Wellems. 2001. Malaria. Cooperative silencing elements in var genes. Nature 412: 875 876.
25. Deitsch, K.W.,, A. del Pinal,, and T. E. Wellems. 1999. Intra-cluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum. Mol. Biochem. Parasitol. 101: 107 116.
26. Doerig, C. 2004. Protein kinases as targets for anti-parasitic chemotherapy. Biochim. Biophys.Acta 1697: 155 168.
27. Eisen, M. B.,, and P. O. Brown. 1999. DNA arrays for analysis of gene expression. Methods Enzymol. 303: 179 205.
28. Evans, W. E.,, and R. K. Guy. 2004. Gene expression as a drug discovery tool. Nat. Genet. 36: 214 215.
29. Fang, J.,, and T. F. McCutchan. 2002. Thermoregulation in a parasite's life cycle. Nature 418: 742.
30. Fernandez, V.,, M. Hommel,, Q. Chen,, P. Hagblom,, and M. Wahlgren. 1999. Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J. Exp. Med. 190: 1393 1404.
31. Florens, L.,, X. Liu,, Y. Wang,, S. Yang,, O. Schwartz,, M. Peglar,, D. J. Carucci,, J. R. Yates III,, and Y. Wub. 2004. Proteomics approach reveals novel proteins on the surface of malaria-infected erythrocytes. Mol. Biochem. Parasitol. 135: 1 11.
32. Florens, L.,, M. P. Washburn,, J. D. Raine,, R. M. Anthony,, M. Grainger,, J. D. Haynes,, J. K. Moch,, N. Muster,, J. B. Sacci,, D. L. Tabb,, A. A. Witney,, D. Wolters,, Y. Wu,, M. J. Gardner,, A. A. Holder,, R. E. Sinden,, J. R. Yates,, and D. J. Carucci. 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520 526.
33. Foth, B. J.,, and G. I. McFadden. 2003. The apicoplast: a plastid in Plasmodium falciparum and other Apicomplexan parasites. Int.Rev.Cytol. 224: 57 110.
34. Foth, B. J.,, S. A. Ralph,, C. J. Tonkin,, N. S. Struck,, M. Fraunholz,, D. S. Roos,, A. F. Cowman,, and G. I. McFadden. 2003. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705 708.
35. Ganesan, K.,, L. Jiang,, J. White,, and P. K. Rathod. 2003. Rigidity of the plasmodium transcriptome revealed by a lethal antifolate. Presented at the Molecular Parasitology Meeting, Woods Hole, Mass.
36. Gardner, J. P.,, R. A. Pinches,, D. J. Roberts,, and C. I. Newbold. 1996. Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc. Natl.Acad. Sci. USA 93: 3503 3508.
37. Gardner, M. J.,, N. Hall,, E. Fung,, O. White,, M. Berriman,, R. W. Hyman,, J. M. Carlton,, A. Pain,, K. E. Nelson,, S. Bowman,, I. T. Paulsen,, K. James,, J. A. Eisen,, K. Rutherford,, S. L. Salzberg,, A. Craig,, S. Kyes,, M. S. Chan,, V. Nene,, S. J. Shallom,, B. Suh,, J. Peterson,, S. Angiuoli,, M. Pertea,, J. Allen,, J. Selengut,, D. Haft,, M. W. Mather,, A. B. Vaidya,, D. M. Martin,, A. H. Fairlamb,, M. J. Fraunholz,, D. S. Roos,, S. A. Ralph,, G. I. McFadden,, L. M. Cummings,, G. M. Subramanian,, C. Mungall,, J. C. Venter,, D. J. Carucci,, S. L. Hoffman,, C. Newbold,, R. W. Davis,, C. M. Fraser,, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498 511.
38. Gatton, M. L.,, J. M. Peters,, E. V. Fowler,, and Q. Cheng. 2003. Switching rates of Plasmodium falciparum var genes: faster than we thought? Trends Parasitol. 19: 202 208.
39. Goonewardene, R.,, J. Daily,, D. Kaslow,, T. J. Sullivan,, P. Duffy,, R. Carter,, K. Mendis,, and D. Wirth. 1993. Transfection of the malaria parasite and expression of firefly luciferase. Proc. Natl. Acad. Sci. USA 90: 5234 5236.
40. Gunasekera, A. M.,, S. Patankar,, J. Schug,, G. Eisen,, J. Kissinger,, D. Roos,, and D. F. Wirth. 2004. Widespread distribution of antisense transcripts in the Plasmodium falciparum genome. Mol. Biochem. Parasitol. 136: 35 42.
41. Gunther, E. C.,, D. J. Stone,, R. W. Gerwien,, P. Bento,, and M. P. Heyes. 2003. Prediction of clinical drug efficacy by classification of drug-induced genomic expression profiles in vitro. Proc. Natl.Acad. Sci. USA 100: 9608 9613.
42. Hatzixanthis, K.,, M. Mollapour,, I. Seymour,, B. E. Bauer,, G. Krapf,, C. Schuller,, K. Kuchler,, and P. W. Piper. 2003. Moderately lipophilic carboxylate compounds are the selective inducers of the Saccharomyces cerevisiae Pdr12p ATP-binding cassette transporter. Yeast 20: 575 585.
43. Hayward, R. E.,, J. L. Derisi,, S. Alfadhli,, D. C. Kaslow,, P. O. Brown,, and P. K. Rathod. 2000. Shotgun DNA microarrays and stage-specific gene expression in Plasmodium falciparum malaria. Mol. Microbiol. 35: 6 14.
44. Horrocks, P.,, K. Dechering,, and M. Lanzer. 1998. Control of gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 95: 171 181.
45. Horrocks, P.,, M. Jackson,, S. Cheesman,, J. H. White,, and B. J. Kilbey. 1996. Stage specific expression of proliferating cell nuclear antigen and DNA polymerase delta from Plasmodium falciparum. Mol. Biochem. Parasitol. 79: 177 182.
46. Horrocks, P.,, and B. J. Kilbey. 1996. Physical and functional mapping of the transcriptional start sites of Plasmodium falciparum proliferating cell nuclear antigen. Mol. Biochem. Parasitol. 82: 207 215.
47. Horrocks, P.,, and M. Lanzer. 1999. Differences in nucleosome organization over episomally located plasmids coincide with aberrant promoter activity in P. falciparum. Parasitol. Int. 48: 55 61.
48. Inselburg, J.,, and H. S. Banyal. 1984. Synthesis of DNA during the asexual cycle of Plasmodium falciparum in culture. Mol. Biochem. Parasitol. 10: 79 87.
49. Ji, D. D.,, and D. E. Arnot. 1997. A Plasmodium falciparum homologue of the ATPase subunit of a multi-protein complex involved in chromatin remodelling for transcription. Mol. Biochem. Parasitol. 88: 151 162.
50. Kappe, S. H.,, M. J. Gardner,, S. M. Brown,, J. Ross,, K. Matuschewski,, J. M. Ribeiro,, J. H. Adams,, J. Quackenbush,, J. Cho,, D. J. Carucci,, S. L. Hoffman,, and V. Nussenzweig. 2001. Exploring the transcriptome of the malaria sporozoite stage. Proc. Natl.Acad. Sci. USA 98: 9895 9900.
51. Kidgell, C.,, J. Borevitz,, D. Plouffe,, S. Volkman,, J. Johnson,, K. Le Roch,, D. Wirth,, Y. Zhou,, S. Batalov,, and E. Winzeler. Genome-wide analysis of Plasmodium falciparum strains reveals novel polymorphic proteins under selection and identifies genetic heterogeneity within the parasite genome. Submitted for publication.
52. Kuwabara, P. E.,, and A. Coulson. 2000. RNAi—prospects for a general technique for determining gene function. Parasitol.Today 16: 347 349.
53. Kyes, S.,, Z. Christodoulou,, R. Pinches,, and C. Newbold. 2002. Stage-specific merozoite surface protein 2 antisense transcripts in Plasmodium falciparum. Mol. Biochem. Parasitol. 123: 79 83.
54. Kyes, S.,, R. Pinches,, and C. Newbold. 2000. A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol. Biochem. Parasitol. 105: 311 315.
55. Kyes, S. A.,, J. A. Rowe,, N. Kriek,, and C. I. Newbold. 1999. Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc. Natl.Acad. Sci. USA 96: 9333 9338.
56. Labo, P.,, G. Grant,, and D. Ross. 2004. Integrating functional genomics data sets: Plasmodium falciparum gene expression. Presented at the Molecular Parasitology Meeting, Woods Hole, Mass.
57. Lambermon, M. H.,, Y. Fu,, D. A. Wieczorek Kirk,, M. Dupasquier,, W. Filipowicz,, and Z. J. Lorkovic. 2002. UBA1 and UBA2, two proteins that interact with UBP1, a multifunctional effector of pre-mRNA maturation in plants. Mol. Cell. Biol. 22: 4346 4357.
58. Lanzer, M.,, S. P. Wertheimer,, D. de Bruin,, and J. V. Ravetch. 1993. Plasmodium: control of gene expression in malaria parasites. Exp. Parasitol. 77: 121 128.
59. Lanzer, M.,, S. P. Wertheimer,, D. de Bruin,, and J. V. Ravetch. 1994. Chromatin structure determines the sites of chromosome breakages in Plasmodium falciparum. Nucleic Acids Res. 22: 3099 3103.
60. Lasonder, E.,, Y. Ishihama,, J. S. Andersen,, A. M. Vermunt,, A. Pain,, R. W. Sauerwein,, W. M. Eling,, N. Hall,, A. P. Waters,, H. G. Stunnenberg,, and M. Mann. 2002. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419: 537 542.
61. Le Roch, K.,, J. Johnson,, Z. Zhou,, K. Henson,, Y. Yates,, H. Vial,, and E. Winzeler. Functional genomics of the antimalarial choline analogue T4 on Plasmodium falciparum reveal potential therapeutic targets. Unpublished data.
62. Le Roch, K.G.,, J. R. Johnson,, L. Florens,, Y. Zhou,, A. Santrosyan,, M. Grainger,, S. F. Yan,, K. C. Williamson,, A. A. Holder,, D. J. Carucci,, J. R. Yates III,, and E. A. Winzeler. 2004. Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res. 14: 2308 2318.
63. Le Roch, K. G.,, Y. Zhou,, S. Batalov,, and E. A. Winzeler. 2002. Monitoring the chromosome 2 intraerythrocytic transcriptome of Plasmodium falciparum using oligonucleotide arrays. Am. J.Trop. Med. Hyg. 67: 233 243.
64. Le Roch, K.G.,, Y. Zhou,, P. L. Blair,, M. Grainger,, J. K. Moch,, J. D. Haynes,, P. De La Vega,, A. A. Holder,, S. Batalov,, D. J. Carucci,, and E. A. Winzeler. 2003. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503 1508.
65. Lee, S. G.,, J. U. Hur,, and Y. S. Kim. 2004. A graph-theoretic modeling on GO space for biological interpretation of gene clusters. Bioinformatics 20: 381 388.
66. Levitt, A.,, F. O. Dimayuga,, and V. R. Ruvolo. 1993. Analysis of malarial transcripts using cDNA directed polymerase chain reaction. J. Parasitol. 79: 653 662.
67. Martinez-Calvillo, S.,, S. Yan,, D. Nguyen,, M. Fox,, K. Stuart,, and P. J. Myler. 2003. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol. Cell 11: 1291 1299.
68. McRobert, L.,, and G. A. McConkey. 2002. RNA interference (RNAi) inhibits growth of Plasmodium falciparum. Mol. Biochem. Parasitol. 119: 273 278.
69. Militello, K. T.,, M. Dodge,, L. Bethke,, and D. F. Wirth. 2004. Identification of regulatory elements in the Plasmodium falciparum genome. Mol. Biochem. Parasitol. 134: 75 88.
70. Munasinghe, A.,, S. Patankar,, B. P. Cook,, S. L. Madden,, R. K. Martin,, D. E. Kyle,, A. Shoaibi,, L. M. Cummings,, and D. F. Wirth. 2001. Serial analysis of gene expression (SAGE) in Plasmodium falciparum: application of the technique to A-T rich genomes. Mol. Biochem. Parasitol. 113: 23 34.
71. Painter, H. J.,, J. A. Morrisey,, J. Stumhofer,, and A. B. Vaidya. 2004. Early response to antimalaria drug treatment examined by whole genome transcription profiling. Presented at the Molecular Parasitology Meeting, Woods Hole, Mass.
72. Patankar, S.,, A. Munasinghe,, A. Shoaibi,, L. M. Cummings,, and D. F. Wirth. 2001. 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 12: 3114 3125.
73. Porter, M. E. 2001. The DNA polymerase delta promoter from Plasmodium falciparum contains an unusually long 5′ untranslated region and intrinsic DNA curvature. Mol. Biochem. Parasitol. 114: 249 255.
74. Ralph, S. A.,, B. J. Foth,, N. Hall,, and G. I. Mc-Fadden. 2004. Evolutionary pressures on apicoplast transit peptides. Mol. Biol. Evol. 21: 2183 2194.
75. Rehkopf, D. H.,, D. E. Gillespie,, M. I. Harrell,, and J. E. Feagin. 2000. Transcriptional mapping and RNA processing of the Plasmodium falciparum mitochondrial mRNAs. Mol. Biochem. Parasitol. 105: 91 103.
76. Reinoso-Martin, C.,, C. Schuller,, M. Schuetzer-Muehlbauer,, and K. Kuchler. 2003. The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryot. Cell 2: 1200 1210.
77. Robinson, K. A.,, and S. M. Beverley. 2003. Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. Mol. Biochem. Parasitol. 128: 217 228.
78. Rosenow, C.,, R. M. Saxena,, M. Durst,, and T. R. Gingeras. 2001. Prokaryotic RNA preparation methods useful for high density array analysis: comparison of two approaches. Nucleic Acids Res. 29: E112.
79. Rosenthal, P. J. 2002. Hydrolysis of erythrocyte proteins by proteases of malaria parasites. Curr. Opin. Hematol. 9: 140 145.
80. Rosenthal, P. J.,, P. S. Sijwali,, A. Singh,, and B. R. Shenai. 2002. Cysteine proteases of malaria parasites: targets for chemotherapy. Curr. Pharm. Des. 8: 1659 1672.
81. Scherf, A.,, R. Hernandez-Rivas,, P. Buffet,, E. Bottius,, C. Benatar,, B. Pouvelle,, J. Gysin,, and M. Lanzer. 1998. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J. 17: 5418 5426.
82. Schuller, C.,, Y. M. Mamnun,, M. Mollapour,, G. Krapf,, M. Schuster,, B. E. Bauer,, P. W. Piper,, and K. Kuchler. 2004. Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Mol. Biol. Cell 15: 706 720.
83. Sibley, L. D. 2004. Intracellular parasite invasion strategies. Science 304: 248 253.
84. Soto, M.,, L. Quijada,, R. Larreta,, S. Iborra,, C. Alonso,, and J. M. Requena. 2003. Leishmania infantum possesses a complex family of histone H2A genes: structural characterization and analysis of expression. Parasitology 127: 95 105.
85. Struhl, K. 1996. Chromatin structure and RNA polymerase II connection: implications for transcription. Cell 84: 179 182.
86. Su, X. Z.,, V. M. Heatwole,, S. P. Wertheimer,, F. Guinet,, J. A. Herrfeldt,, D. S. Peterson,, J. A. Ravetch,, and T. E. Wellems. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89 100.
87. Toronen, P. 2004. Selection of informative clusters from hierarchical cluster tree with gene classes. BMC Bioinformatics 5: 32.
88. Velculescu, V. E.,, L. Zhang,, B. Vogelstein,, and K. W. Kinzler. 1995. Serial analysis of gene expression. Science 270: 484 487.
89. Vervenne, R. A.,, R. W. Dirks,, J. Ramesar,, A. P. Waters,, and C. J. Janse. 1994. Differential expression in blood stages of the gene coding for the 21-kilo-dalton surface protein of ookinetes of Plasmodium berghei as detected by RNA in situ hybridisation. Mol. Biochem. Parasitol. 68: 259 266.
90. Vial, H. J.,, P. Eldin,, A. G. Tielens,, and J. J. van Hellemond. 2003. Phospholipids in parasitic protozoa. Mol. Biochem. Parasitol. 126: 143 154.
91. Volkman, S. K.,, D. L. Hartl,, D. F. Wirth,, K. M. Nielsen,, M. Choi,, S. Batalov,, Y. Zhou,, D. Plouffe,, K. G. Le Roch,, R. Abagyan,, and E. A. Winzeler. 2002. Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 298: 216 218.
92. Voss, T. S.,, J. K. Thompson,, J. Waterkeyn,, I. Felger,, N. Weiss,, A. F. Cowman,, and H. P. Beck. 2000. Genomic distribution and functional characterisation of two distinct and conserved Plasmodium falciparum var gene 5′ flanking sequences. Mol. Biochem. Parasitol. 107: 103 115.
93. Waters, A. P. 2003. Parasitology. Guilty until proven otherwise. Science 301: 1487 1488.
94. Waters, A. P.,, C. Syin,, and T. F. McCutchan. 1989. Developmental regulation of stage-specific ribosome populations in Plasmodium. Nature 342: 438 440.
95. Waters, A. P.,, W. White,, and T. F. McCutchan. 1995. The structure of the large subunit rRNA expressed in blood stages of Plasmodium falciparum. Mol. Biochem. Parasitol. 72: 227 237.
96. Wengelnik, K.,, V. Vidal,, M. L. Ancelin,, A. M. Cathiard,, J. L. Morgat,, C. H. Kocken,, M. Calas,, S. Herrera,, A. W. Thomas,, and H. J. Vial. 2002. A class of potent antimalarials and their specific accumulation in infected erythrocytes. Science 295: 1311 1314.
97. Wu, Y.,, C. D. Sifri,, H. H. Lei,, X. Z. Su,, and T. E. Wellems. 1995. Transfection of Plasmodium falciparum within human red blood cells. Proc. Natl. Acad. Sci. USA 92: 973 977.
98. Wu, Y.,, X. Wang,, X. Liu,, and Y. Wang. 2003. Datamining approaches reveal hidden families of proteases in the genome of malaria parasite. Genome Res. 13: 601 616.
99. Young, J.,, Q. Fivelman,, P. Blair,, K. Chen,, K. Le Roch,, F. Yan,, D. Baker,, D. Carucci,, Y. Zhou,, and E. Winzeler. Elucidation of Plasmodium falciparum gene function using ontology-based pattern identification. Submitted for publication.
100. Zhou, Y.,, and R. Abagyan. 2002. Match-only intesity oligonucleotide array analysis. BMC Bioinformatics 3: 3.
101. Zhou, Y.,, and R. Abagyan. 2003. Algorithms for high-density oligonucleotide array. Curr. Opin. Drug Discov. Devel. 6: 339 345.
102. Zhou, Y.,, J. A. Young,, A. Santrosyan,, K. Chen,, F. S. Yan,, and E. A. Winzeler. 2004. In silico gene function prediction using ontology-based pattern identification. Bioinformatics 21: 1237 1245.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error