RNA-Seq analysis of splicing in Plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts

Nucleic Acids Research

Volumn 39, Issue 9, 2011, Pages 3820-3835

  Sorber, Katherine ^a   Dimon, Michelle T ^a,b   Derisi, Joseph L ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GENE FUNCTION; INTRON; NONHUMAN; OPEN READING FRAME; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; RNA BINDING; RNA SEQUENCE; RNA SPLICING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SPLICEOSOME; UNTRANSLATED REGION;

ALGORITHMS; ALTERNATIVE SPLICING; GENOME, PROTOZOAN; INTRONS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RNA SPLICE SITES; RNA, ANTISENSE; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA;

PLASMODIUM FALCIPARUM;

EID: 79956001876     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq1223     Document Type: Article

References (66)

1. Bozdech, Z., Llinás, M., Pulliam, B.L., Wong, E.D., Zhu, J. and DeRisi, J.L. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol., 1, e5.
2. Le Roch, K.G., Zhou, Y., Blair, P.L., Grainger, M., Moch, J.K., Haynes, J.D., De la Vega, P., Holder, A.A., Batalov, S., Carucci, D.J. et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science, 301, 1503-1508. (Pubitemid 37128535)
3. Silvestrini, F., Bozdech, Z., Lanfrancotti, A., Di Giulio, E., Bultrini, E., Picci, L., Derisi, J.L., Pizzi, E. and Alano, P. (2005) Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol. Biochem. Parasitol., 143, 100-110. (Pubitemid 41043169)
4. Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J.M., Pain, A., Nelson, K.E., Bowman, S. et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, 419, 498-511.
5. Burtis, K.C. (1993) The regulation of sex determination and sexually dimorphic differentiation in Drosophila. Curr. Opin. Cell Biol., 5, 1006-1014. (Pubitemid 23340508)
6. Madsen, J. and Stoltzfus, C.M. (2006) A suboptimal 50 splice site downstream of HIV-1 splice site A1 is required for unspliced viral mRNA accumulation and efficient virus replication. Retrovirology, 3, 10.
7. Chakrabarti, K., Pearson, M., Grate, L., Sterne-Weiler, T., Deans, J., Donohue, J.P. and Ares, M. (2007) Structural RNAs of known and unknown function identified in malaria parasites by comparative genomics and RNA analysis. RNA, 13, 1923-1939. (Pubitemid 350005218)
8. Upadhyay, R., Bawankar, P., Malhotra, D. and Patankar, S. (2005) A screen for conserved sequences with biased base composition identifies noncoding RNAs in the A-T rich genome of Plasmodium falciparum. Mol. Biochem. Parasitol., 144, 149-158. (Pubitemid 41572221)
9. Shankar, J., Pradhan, A. and Tuteja, R. (2008) Isolation and characterization of Plasmodium falciparum UAP56 homolog: Evidence for the coupling of RNA binding and splicing activity by site-directed mutations. Arch. Biochem. Biophys., 478, 143-153.
10. Lamond, A.I. (1993) The spliceosome. Bioessays, 15, 595-603.
11. Burset, M., Seledtsov, I.A. and Solovyev, V.V. (2000) Analysis of canonical and non-canonical splice sites in mammalian genomes. Nucleic Acids Res., 28, 4364-4375.
12. Lu, F., Jiang, H., Ding, J., Mu, J., Valenzuela, J., Ribeiro, J. and Su, X. (2007) cDNA sequences reveal considerable gene prediction inaccuracy in the Plasmodium falciparum genome. BMC Genomics, 8, 255.
13. Li, L., Brunk, B.P., Kissinger, J.C., Pape, D., Tang, K., Cole, R.H., Martin, J., Wylie, T., Dante, M., Fogarty, S.J. et al. (2003) Gene discovery in the apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Res., 13, 443-454. (Pubitemid 36395402)
14. Otto, T.D., Wilinski, D., Assefa, S., Keane, T.M., Sarry, L.R., Böhme, U., Lemieux, J., Barrell, B., Pain, A., Berriman, M. et al. (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol. Microbiol., 76, 12-24.
15. Bracchi-Ricard, V., Barik, S., Delvecchio, C., Doerig, C., Chakrabarti, R. and Chakrabarti, D. (2000) PfPK6, a novel cyclin-dependent kinase/mitogen-activated protein kinase-related protein kinase from Plasmodium falciparum. Biochem. J., 347, 255-263. (Pubitemid 30199065)
16. Muhia, D.K., Swales, C.A., Eckstein-Ludwig, U., Saran, S., Polley, S.D., Kelly, J.M., Schaap, P., Krishna, S. and Baker, D.A. (2003) Multiple splice variants encode a novel adenylyl cyclase of possible plastid origin expressed in the sexual stage of the malaria parasite Plasmodium falciparum. J. Biol. Chem., 278, 22014-22022. (Pubitemid 36792610)
17. Saenz, F.E., Balu, B., Smith, J., Mendonca, S.R. and Adams, J.H. (2008) The transmembrane isoform of Plasmodium falciparum MAEBL is essential for the invasion of Anopheles salivary glands. PLoS ONE, 3, e2287.
18. Wentzinger, L., Bopp, S., Tenor, H., Klar, J., Brun, R., Beck, H.P. and Seebeck, T. (2008) Cyclic nucleotide-specific phosphodiesterases of Plasmodium falciparum: PfPDE[alpha], a non-essential cGMP-specific PDE that is an integral membrane protein. Inter. J. Parasitol., 38, 1625-1637.
19. Iriko, H., Jin, L., Kaneko, O., Takeo, S., Han, E., Tachibana, M., Otsuki, H., Torii, M. and Tsuboi, T. (2009) A small-scale systematic analysis of alternative splicing in Plasmodium falciparum. Parasitology Inter., 58, 196-199.
20. Knapp, B., Nau, U., Hundt, E. and Küpper, H.A. (1991) Demonstration of alternative splicing of a pre-mRNA expressed in the blood stage form of Plasmodium falciparum. J. Biol. Chem., 266, 7148-7154. (Pubitemid 21906345)
21. Liu, Q., Mackey, A.J., Roos, D.S. and Pereira, F.C.N. (2008) Evigan: a hidden variable model for integrating gene evidence for eukaryotic gene prediction. Bioinformatics, 24, 597-605. (Pubitemid 351321202)
22. Jen, C., Michalopoulos, I., Westhead, D. and Meyer, P. (2005) Natural antisense transcripts with coding capacity in Arabidopsis may have a regulatory role that is not linked to double-stranded RNA degradation. Genome Biol., 6, R51.
23. RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group) and the FANTOM Consortium. Katayama, S., Tomaru, Y., Kasukawa, T., Waki, K., Nakanishi, M., Nakamura, M., Nishida, H., Yap, C.C., Suzuki, M. et al. (2005) Antisense transcription in the mammalian transcriptome. Science, 309, 1564-1566.
24. Faghihi, M.A. and Wahlestedt, C. (2009) Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell Biol., 10, 637-643.
25. Militello, K.T., Patel, V., Chessler, A., Fisher, J.K., Kasper, J.M., Gunasekera, A. and Wirth, D.F. (2005) RNA polymerase II synthesizes antisense RNA in Plasmodium falciparum. RNA, 11, 365-370. (Pubitemid 40397170)
26. Raabe, C.A., Sanchez, C.P., Randau, G., Robeck, T., Skryabin, B.V., Chinni, S.V., Kube, M., Reinhardt, R., Ng, G.H., Manickam, R. et al. (2010) A global view of the nonprotein-coding transcriptome in Plasmodium falciparum. Nucleic Acids Res., 38, 608-617.
27. Sorber, K., Chiu, C., Webster, D., Dimon, M., Ruby, J.G., Hekele, A. and 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.
28. Dimon, M., Sorber, K. and DeRisi, J.L. (2010) HMMSplicer: a tool for efficient and sensitive discovery of known and novel splice junctions in RNA-Seq data. PLoS ONE, 5, e13875.
29. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
30. The Plasmodium Genome Database Collective. (2001) PlasmoDB: an integrative database of the Plasmodium falciparum genome. Tools for accessing and analyzing finished and unfinished sequence data. Nucleic Acids Res., 29, 66-69.
31. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
32. Kent, W.J. (2002) BLAT-The BLAST-Like Alignment Tool. Genome Res., 12, 656-664.
33. Moreno-Hagelsieb, G. and Latimer, K. (2008) Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics, 24, 319-324. (Pubitemid 351189006)
34. Kaufer, N.F. and Potashkin, J. (2000) Analysis of the splicing machinery in fission yeast: a comparison with budding yeast and mammals. Nucleic Acids Res., 28, 3003-3010. (Pubitemid 30624088)
35. Stevens, S.W., Barta, I., Ge, H.Y., Moore, R.E., Young, M.K., Lee, T.D. and Abelson, J. (2001) Biochemical and genetic analyses of the U5, U6, and U4/U6 x U5 small nuclear ribonucleoproteins from Saccharomyces cerevisiae. RNA, 7, 1543-1553. (Pubitemid 33078930)
36. Bessonov, S., Anokhina, M., Will, C.L., Urlaub, H. and Luhrmann, R. (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature, 452, 846-850. (Pubitemid 351550864)
37. Lardelli, R.M., Thompson, J.X., Yates, J.R. and Stevens, S.W. (2010) Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing. RNA, 16, 516-528.
38. Edwalds-Gilbert, G., Kim, D., Silverman, E. and Lin, R. (2004) Definition of a spliceosome interaction domain in yeast Prp2 ATPase. RNA, 10, 210-220. (Pubitemid 38129826)
39. Barash, Y., Calarco, J.A., Gao, W., Pan, Q., Wang, X., Shai, O., Blencowe, B.J. and Frey, B.J. (2010) Deciphering the splicing code. Nature, 465, 53-59.
40. Venables, J.P., Koh, C., Froehlich, U., Lapointe, E., Couture, S., Inkel, L., Bramard, A., Paquet, E.R., Watier, V., Durand, M. et al. (2008) Multiple and specific mRNA processing targets for the major human hnRNP proteins. Mol. Cell. Biol., 28, 6033-6043.
41. Long, J. and Caceres, J. (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem. J., 417, 15.
42. Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Birney, E., Biswas, M., Bucher, P., Cerutti, L., Corpet, F., Croning, M.D.R. et al. (2001) The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res., 29, 37-40. (Pubitemid 32054401)
43. Watanabe, J., Wakaguri, H., Sasaki, M., Suzuki, Y. and Sugano, S. (2007) Comparasite: a database for comparative study of transcriptomes of parasites defined by full-length cDNAs. Nucleic Acids Res., 35, D431-D438. (Pubitemid 46056246)
44. Florent, I., Porcel, B., Guillaume, E., Da Silva, C., Artiguenave, F., Marechal, E., Brehelin, L., Gascuel, O., Charneau, S., Wincker, P. et al. (2009) A Plasmodium falciparum FcB1-schizont-EST collection providing clues to schizont specific gene structure and polymorphism. BMC Genomics, 10, 235.
45. Crooks, G.E., Hon, G., Chandonia, J. and Brenner, S.E. (2004) WebLogo: A sequence logo generator. Genome Res., 14, 1188-1190. (Pubitemid 38811555)
46. D'haeseleer, P. (2006) What are DNA sequence motifs? Nat. Biotech., 24, 423-425.
47. Clark, F. and Thanaraj, T.A. (2002) Categorization and characterization of transcript-confirmed constitutively and alternatively spliced introns and exons from human. Hum. Mol. Genet., 11, 451-464. (Pubitemid 34213619)
48. Tarn, W. and Steitz, J.A. (1996) A novel spliceosome containing U11, U12 and U5 snRNPs excises a minor class (AT-AC) intron in vitro. Cell, 84, 801-811. (Pubitemid 26094209)
49. Sidrauski, C., Cox, J.S. and Walter, P. (1996) tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell, 87, 405-413. (Pubitemid 26374315)
50. Eckert, K.A. and Kunkel, T.A. (1991) DNA polymerase fidelity and the polymerase chain reaction. PCR Methods Appl., 1, 17-24.
51. Cocquet, J., Chong, A., Zhang, G. and Veitia, R.A. (2006) Reverse transcriptase template switching and false alternative transcripts. Genomics, 88, 127-131. (Pubitemid 44183763)
52. Shinde, D., Lai, Y., Sun, F. and Arnheim, N. (2003) Taq DNA polymerase slippage mutation rates measured by PCR and quasi-likelihood analysis: (CA/GT)n and (A/T)n microsatellites. Nucleic Acids Res., 31, 974-980. (Pubitemid 36240435)
53. Will, C.L., Schneider, C., Hossbach, M., Urlaub, H., Rauhut, R., Elbashir, S., Tuschl, T. and Luhrmann, R. (2004) The human 18S U11/U12 snRNP contains a set of novel proteins not found in the U2-dependent spliceosome. RNA, 10, 929-941. (Pubitemid 38669766)
54. Lopez, M.D., Alm Rosenblad, M. and Samuelsson, T. (2008) Computational screen for spliceosomal RNA genes aids in defining the phylogenetic distribution of major and minor spliceosomal components. Nucleic Acids Res., 36, 3001-3010. (Pubitemid 351737192)
55. Sun, S., Zhang, Z., Sinha, R., Karni, R. and Krainer, A.R. (2010) SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat. Struct. Mol. Biol., 17, 306-312.
56. Conti, E. and Izaurralde, E. (2005) Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species. Curr. Opin. Cell Biol., 17, 316-325. (Pubitemid 40719923)
57. Engebrecht, J.A., Voelkel-Meiman, K. and Roeder, G.S. (1991) Meiosis-specific RNA splicing in yeast. Cell, 66, 1257-1268. (Pubitemid 121001414)
58. Wilhelm, B.T., Marguerat, S., Watt, S., Schubert, F., Wood, V., Goodhead, I., Penkett, C.J., Rogers, J. and Bahler, J. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature, 453, 1239-1243. (Pubitemid 351913597)
59. Zhang, Y., Liu, X.S., Liu, Q. and Wei, L. (2006) Genome-wide in silico identification and analysis of cis natural antisense transcripts (cis-NATs) in ten species. Nucleic Acids Res., 34, 3465-3475.
60. Gunasekera, A.M., Patankar, S., Schug, J., Eisen, G., Kissinger, J., Roos, D. and Wirth, D.F. (2004) Widespread distribution of antisense transcripts in the Plasmodium falciparum genome. Mol. Biochem. Parasitol., 136, 35-42. (Pubitemid 38597118)
61. Sun, M., Hurst, L.D., Carmichael, G.G. and Chen, J. (2005) Evidence for a preferential targeting of 30-UTRs by cis-encoded natural antisense transcripts. Nucleic Acids Res., 33, 5533-5543. (Pubitemid 41548819)
62. Shock, J.L., Fischer, K.F. and DeRisi, J.L. (2007) Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol., 8, R134.
63. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
64. Fouser, L.A. and Friesen, J.D. (1986) Mutations in a yeast intron demonstrate the importance of specific conserved nucleotides for the two stages of nuclear mRNA splicing. Cell, 45, 81-93. (Pubitemid 16046629)
65. Kim, E., Magen, A. and Ast, G. (2006) Different levels of alternative splicing among eukaryotes. Nucleic Acids Res., 35, 125-131.
66. Stein, L.D., Mungall, C., Shu, S., Caudy, M., Mangone, M., Day, A., Nickerson, E., Stajich, J.E., Harris, T.W., Arva, A. et al. (2002) The Generic Genome Browser: a Building Block for a Model Organism System Database. Genome Res., 12, 1599-1610. (Pubitemid 35175099)