New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq

Molecular Microbiology

Volumn 76, Issue 1, 2010, Pages 12-24

  Otto, Thomas D ^a   Wilinski, Daniel ^b   Assefa, Sammy ^a   Keane, Thomas M ^a   Sarry, Louis R ^b   Böhme, Ulrike ^a   Lemieux, Jacob ^c   Barrell, Bart ^a   Pain, Arnab ^a   Berriman, Matthew ^a   Newbold, Chris ^a,c   Llinás, Manuel ^b  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b PRINCETON UNIVERSITY   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RNA; TRANSCRIPTOME;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ARTICLE; DNA MICROARRAY; ERYTHROCYTE; GENE EXPRESSION; GENETIC MODEL; GENOME; HIGH THROUGHPUT SCREENING; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PSEUDOGENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; BLOOD; COMPARATIVE STUDY; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; PARASITOLOGY; PROCEDURES; RNA SPLICING; TIME;

PLASMODIUM FALCIPARUM;

BLOOD; ERYTHROCYTES; GENE EXPRESSION PROFILING; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMODIUM FALCIPARUM; PSEUDOGENES; RNA SPLICING; SEQUENCE ANALYSIS, DNA; TIME FACTORS;

EID: 77950265905     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.07026.x     Document Type: Article

References (47)

1. Arav-Boger, R. Shapiro, T.A. (2005) Molecular mechanisms of resistance in antimalarial chemotherapy: the unmet challenge. Annu Rev Pharmacol Toxicol 45 : 565 585.
2. Aravind, L., Iyer, L.M., Wellems, T.E. Miller, L.H. (2003) Plasmodium biology: genomic gleanings. Cell 115 : 771 785.
3. Bahl, A., Brunk, B., Crabtree, J., Fraunholz, M.J., Gajria, B., Grant, G.R., et al. (2003) PlasmoDB: the Plasmodium genome resource. A database integrating experimental and computational data. Nucleic Acids Res 31 : 212 215.
4. Bentley, D.R., Balasubramanian, S., Swerdlow, H.P., Smith, G.P., Milton, J., Brown, C.G., et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456 : 53 59.
5. Bloom, J.S., Khan, Z., Kruglyak, L., Singh, M. Caudy, A.A. (2009) Measuring differential gene expression by short read sequencing: quantitative comparison to 2-channel gene expression microarrays. BMC Genomics 10 : 221.
6. Bozdech, Z., Llinas, M., Pulliam, B.L., Wong, E.D., Zhu, J. DeRisi, J.L. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1 : E5.
7. Breman, J.G. (2001) The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg 64 : 1 11.
8. Carlton, J.M., Adams, J.H., Silva, J.C., Bidwell, S.L., Lorenzi, H., Caler, E., et al. (2008) Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455 : 757 763.
9. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M.C., Maeda, N., et al. (2005) The transcriptional landscape of the mammalian genome. Science 309 : 1559 1563.
10. Chakrabarti, K., Pearson, M., Grate, L., Sterne-Weiler, T., Deans, J., Donohue, J.P. Ares, M., Jr. (2007) Structural RNAs of known and unknown function identified in malaria parasites by comparative genomics and RNA analysis. RNA 13 : 1923 1939.
11. Chen, X.M., Huang, B.Q., Splinter, P.L., Cao, H., Zhu, G., McNiven, M.A. LaRusso, N.F. (2003) Cryptosporidium parvum invasion of biliary epithelia requires host cell tyrosine phosphorylation of cortactin via c-Src. Gastroenterology 125 : 216 228.
12. Daily, J.P., Scanfeld, D., Pochet, N., Le Roch, K., Plouffe, D., Kamal, M., et al. (2007) Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature 450 : 1091 1095.
13. Droege, M. Hill, B. (2008) The Genome Sequencer FLX System-longer reads, more applications, straight forward bioinformatics and more complete data sets. J Biotechnol 136 : 3 10.
14. Duret, L., Chureau, C., Samain, S., Weissenbach, J. Avner, P. (2006) The Xist RNA gene evolved in eutherians by pseudogenization of a protein-coding gene. Science 312 : 1653 1655.
15. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 : 498 511.
16. Griffiths-Jones, S. (2007) Annotating noncoding RNA genes. Annu Rev Genomics Hum Genet 8 : 279 298.
17. Haas, B.J., Salzberg, S.L., Zhu, W., Pertea, M., Allen, J.E., Orvis, J., et al. (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol 9 : R7.
18. Hu, G., Llinas, M., Li, J., Preiser, P.R. Bozdech, Z. (2007) Selection of long oligonucleotides for gene expression microarrays using weighted rank-sum strategy. BMC Bioinformatics 8 : 350.
19. Iriko, H., Jin, L., Kaneko, O., Takeo, S., Han, E.T., Tachibana, M., et al. (2009) A small-scale systematic analysis of alternative splicing in Plasmodium falciparum. Parasitol Int 58 : 196 199.
20. Lambros, C. Vanderberg, J.P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65 : 418 420.
21. Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301 : 1503 1508.
22. Lemieux, J.E., Gomez-Escobar, N., Feller, A., Carret, C., Amambua-Ngwa, A., Pinches, R., et al. (2009) Statistical estimation of cell-cycle progression and lineage commitment in Plasmodium falciparum reveals a homogeneous pattern of transcription in ex vivo culture. Proc Natl Acad Sci USA 106 : 7559 7564.
23. Li, H. Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 : 1754 1760.
24. Li, H., Ruan, J. Durbin, R. (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18 : 1851 1858.
25. Llinas, M., Bozdech, Z., Wong, E.D., Adai, A.T. DeRisi, J.L. (2006) Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res 34 : 1166 1173.
26. Lu, F., Jiang, H., Ding, J., Mu, J., Valenzuela, J.G., Ribeiro, J.M. Su, X.Z. (2007) cDNA sequences reveal considerable gene prediction inaccuracy in the Plasmodium falciparum genome. BMC Genomics 8 : 255.
27. Mishra, P.C., Kumar, A. Sharma, A. (2009) Analysis of small nucleolar RNAs reveals unique genetic features in malaria parasites. BMC Genomics 10 : 68.
28. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5 : 621 628.
29. Mourier, T., Carret, C., Kyes, S.A., Christodoulou, Z., Gardner, P.P., Jeffares, D.C., et al. (2008) Genome wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res 18 : 281 292.
30. Nagalakshmi, U., Wang, Z., Waern, K., Shou, C., Raha, D., Gerstein, M. Snyder, M. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320 : 1344 1349.
31. Ning, Z., Cox, A.J. Mullikin, J.C. (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11 : 1725 1729.
32. Ondov, B.D., Varadarajan, A., Passalacqua, K.D. Bergman, N.H. (2008) Efficient mapping of Applied Biosystems SOLiD sequence data to a reference genome for functional genomic applications. Bioinformatics 24 : 2776 2777.
33. Pain, A., Bohme, U., Berry, A.E., Mungall, K., Finn, R.D., Jackson, A.P., et al. (2008) The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 455 : 799 803.
34. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. Blencowe, B.J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40 : 1413 1415.
35. Rodriguez, A., Griffiths-Jones, S., Ashurst, J.L. Bradley, A. (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res 14 : 1902 1910.
36. Sargeant, T.J., Marti, M., Caler, E., Carlton, J.M., Simpson, K., Speed, T.P. Cowman, A.F. (2006) Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7 : R12.
37. Siau, A., Silvie, O., Franetich, J.F., Yalaoui, S., Marinach, C., Hannoun, L., et al. (2008) Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection. PLoS Pathog 4 : e1000121.
38. Sorber, K., Chiu, C., Webster, D., Dimon, M., Ruby, J.G., Hekele, A. DeRisi, J.L. (2008) The long march: a sample preparation technique that enhances contig length and coverage by high-throughput short-read sequencing. PLoS One 3 : e3495.
39. Sultan, M., Schulz, M.H., Richard, H., Magen, A., Klingenhoff, A., Scherf, M., et al. (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321 : 956 960.
40. Tarun, A.S., Peng, X., Dumpit, R.F., Ogata, Y., Silva-Rivera, H., Camargo, N., et al. (2008) A combined transcriptome and proteome survey of malaria parasite liver stages. Proc Natl Acad Sci USA 105 : 305 310.
41. Trager, W. Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science 193 : 673 675.
42. Wakaguri, H., Suzuki, Y., Katayama, T., Kawashima, S., Kibukawa, E., Hiranuka, K., et al. (2009a) Full-Malaria/Parasites and Full-Arthropods: databases of full-length cDNAs of parasites and arthropods, update 2009. Nucleic Acids Res 37 : D520 D525.
43. Wakaguri, H., Suzuki, Y., Sasaki, M., Sugano, S. Watanabe, J. (2009b) Inconsistencies of genome annotations in apicomplexan parasites revealed by 5′-end-one-pass and full-length sequences of oligo-capped cDNAs. BMC Genomics 10 : 312.
44. Wang, Z., Gerstein, M. Snyder, M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10 : 57 63.
45. Wilhelm, B.T., Marguerat, S., Watt, S., Schubert, F., Wood, V., Goodhead, I., et al. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453 : 1239 1243.
46. Young, J.A., Fivelman, Q.L., Blair, P.L., de la Vega, P., Le Roch, K.G., Zhou, Y., et al. (2005) The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol Biochem Parasitol 143 : 67 79.
47. Zavolan, M. van Nimwegen, E. (2006) The types and prevalence of alternative splice forms. Curr Opin Struct Biol 16 : 362 367.