A novel Plasmodium falciparum SR protein is an alternative splicing factor required for the parasites' proliferation in human erythrocytes

Nucleic Acids Research

Volumn 40, Issue 19, 2012, Pages 9903-9916

  Eshar, Shiri ^a   Allemand, Eric ^b   Sebag, Ariel ^c   Glaser, Fabian ^d   Muchardt, Christian ^b   Mandel Gutfreund, Yael ^d   Karni, Rotem ^c   Dzikowski, Ron ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b INSTITUT PASTEUR   (France)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN PFSR1; PROTEIN SRSF1; SERINE ARGININE RICH PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL MATURATION; CELL NUCLEUS; ERYTHROCYTE; GENE; GENE ACTIVITY; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MAMMAL; NONHUMAN; PARASITE VIRULENCE; PFSR1 GENE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM;

ALTERNATIVE SPLICING; CELL LINE; ERYTHROCYTES; HUMANS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PROTEINS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RNA PRECURSORS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EUKARYOTA; MAMMALIA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

EID: 84868144335     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks735     Document Type: Article

References (47)

1. WHO. (2010) World Malaria Report (2010).
2. Bozdech, Z., Llinas, M., Pulliam, B.L., Wong, E.D., Zhu, J.C. and Derisi, J.L. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PloS Biol., 1, 85-100.
3. 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.
4. Keren, H., Lev-Maor, G. and Ast, G. (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet., 11, 345-355.
5. Knapp, B., Nau, U., Hundt, E. and Kupper, 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)
6. 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)
7. Singh, N., Preiser, P., Renia, L., Balu, B., Barnwell, J., Blair, P., Jarra, W., Voza, T., Landau, I. and Adams, J.H. (2004) Conservation and developmental control of alternative splicing in maebl among malaria parasites. J. Mol. Biol., 343, 589-599. (Pubitemid 39311607)
8. Fonager, J., Cunningham, D., Jarra, W., Koernig, S., Henneman, A.A., Langhorne, J. and Preiser, P. (2007) Transcription and alternative splicing in the yir multigene family of the malaria parasite Plasmodium y. yoelii: identification of motifs suggesting epigenetic and post-transcriptional control of RNA expression. Mol. Biochem. Parasitol., 156, 1-11. (Pubitemid 47348137)
9. Iriko, H., Jin, L., Kaneko, O., Takeo, S., Han, E.T., Tachibana, M., Otsuki, H., Torii, M. and Tsuboi, T. (2009) A small-scale systematic analysis of alternative splicing in Plasmodium falciparum. Parasitol. Int., 58, 196-199.
10. Otto, T.D., Wilinski, D., Assefa, S., Keane, T.M., Sarry, L.R., Bohme, 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.
11. Sorber, K., Dimon, M.T. and DeRisi, J.L. (2011) RNA-Seq analysis of splicing in Plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts. Nucleic Acids Res., 39, 3820-3835.
12. Shepard, P.J. and Hertel, K.J. (2009) The SR protein family. Genome Biol., 10, 242.
13. Long, J.C. and Caceres, J.F. (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem J, 417, 15-27.
14. Chen, M. and Manley, J.L. (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell Biol., 10, 741-754.
15. Black, D.L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem., 72, 291-336. (Pubitemid 36930448)
16. Ast, G. (2004) How did alternative splicing evolve? Nat. Rev. Genet., 5, 773-782. (Pubitemid 39336361)
17. Portal, D., Espinosa, J.M., Lobo, G.S., Kadener, S., Pereira, C.A., De La Mata, M., Tang, Z., Lin, R.J., Kornblihtt, A.R., Baralle, F.E. et al. (2003) An early ancestor in the evolution of splicing: a Trypanosoma cruzi serine-arginine-rich protein (TcSR) is functional in cis-splicing. Mol. Biochem. Parasitol., 127, 37-46. (Pubitemid 36263231)
18. Dixit, A., Singh, P.K., Sharma, G.P., Malhotra, P. and Sharma, P. (2010) PfSRPK1, a novel splicing-related kinase from Plasmodium falciparum. J. Biol. Chem., 285, 38315-38323.
19. Caceres, J.F., Stamm, S., Helfman, D.M. and Krainer, A.R. (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science, 265, 1706-1709. (Pubitemid 24314901)
20. Boucher, L., Ouzounis, C.A., Enright, A.J. and Blencowe, B.J. (2001) A genome-wide survey of RS domain proteins. RNA, 7, 1693-1701. (Pubitemid 34042284)
21. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797. (Pubitemid 38832724)
22. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol., 4, 406-425.
23. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28, 2731-2739.
24. Aley, S.B., Sherwood, J.A. and Howard, R.J. (1984) Knob-positive and knob-negative Plasmodium falciparum differ in expression of a strain-specific malarial antigen on the surface of infected erythrocytes. J. Exp. Med. 160, 1585-1590. (Pubitemid 15220785)
25. Calderwood, M.S., Gannoun-Zaki, L., Wellems, T.E. and Deitsch, K.W. (2003) Plasmodium falciparum var genes are regulated by two regions with separate promoters, one upstream of the coding region and a second within the intron. J. Biol. Chem., 278, 34125-34132. (Pubitemid 37553253)
26. Durocher, Y., Perret, S. and Kamen, A. (2002) High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. Nucleic Acids Res., 30, E9.
27. Sinha, R., Allemand, E., Zhang, Z., Karni, R., Myers, M.P. and Krainer, A.R. (2010) Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF. Mol. Cell Biol., 30, 2762-2774.
28. Epp, C., Raskolnikov, D. and Deitsch, K.W. (2008) A regulatable transgene expression system for cultured Plasmodium falciparum parasites. Malar. J., 7, 86.
29. Deitsch, K.W., Driskill, C.L. and Wellems, T.E. (2001) Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res., 29, 850-853. (Pubitemid 32124398)
30. Dzikowski, R. and Deitsch, K.W. (2008) Active transcription is required for maintenance of epigenetic memory in the malaria parasite Plasmodium falciparum. J. Mol. Biol, 382, 288-297.
31. Dzikowski, R., Frank, M. and Deitsch, K. (2006) Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. PLoS Pathog., 2, e22.
32. Kyes, S., Pinches, R. and Newbold, C. (2000) A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol. Biochem. Parasitol., 105, 311-315. (Pubitemid 30067771)
33. Krainer, A.R., Conway, G.C. and Kozak, D. (1990) The essential pre-mRNA splicing factor SF2 influences 5' splice site selection by activating proximal sites. Cell, 62, 35-42.
34. Krainer, A.R., Conway, G.C. and Kozak, D. (1990) Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev., 4, 1158-1171.
35. Agarwal, S., Kern, S., Halbert, J., Przyborski, J.M., Baumeister, S., Dandekar, T., Doerig, C. and Pradel, G. (2011) Two nucleus-localized CDK-like kinases with crucial roles for malaria parasite erythrocytic replication are involved in phosphorylation of splicing factor. J. Cell. Biochem., 112, 1295-1310.
36. Zhang, Z. and Krainer, A.R. (2004) Involvement of SR proteins in mRNA surveillance. Mol. Cell, 16, 597-607. (Pubitemid 39531882)
37. Caceres, J.F., Misteli, T., Screaton, G.R., Spector, D.L. and Krainer, A.R. (1997) Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell. Biol., 138, 225-238. (Pubitemid 27323527)
38. Allemand, E., Gattoni, R., Bourbon, H.M., Stevenin, J., Caceres, J.F., Soret, J. and Tazi, J. (2001) Distinctive features of Drosophila alternative splicing factor RS domain: implication for specific phosphorylation, shuttling, and splicing activation. Mol. Cell Biol., 21, 1345-1359. (Pubitemid 32114982)
39. Karni, R., de Stanchina, E., Lowe, S.W., Sinha, R., Mu, D. and Krainer, A.R. (2007) The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat. Struct. Mol. Biol., 14, 185-193. (Pubitemid 46355578)
40. Caceres, J.F. and Krainer, A.R. (1993) Functional analysis of pre-mRNA splicing factor SF2/ASF structural domains. EMBO J., 12, 4715-4726. (Pubitemid 23330277)
41. Sanford, J.R., Ellis, J.D., Cazalla, D. and Caceres, J.F. (2005) Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc. Natl Acad. Sci. USA, 102, 15042-15047. (Pubitemid 41513331)
42. Anczukow, O., Rosenberg, A.Z., Akerman, M., Das, S., Zhan, L., Karni, R., Muthuswamy, S.K. and Krainer, A.R. (2012) The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation. Nat. Struct. Mol. Biol., 19, 220-228.
43. Lopez-Barragan, M.J., Lemieux, J., Quinones, M., Williamson, K.C., Molina-Cruz, A., Cui, K., Barillas-Mury, C., Zhao, K. and Su, X.Z. (2011) Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics, 12, 587.
44. Caceres, J.F., Screaton, G.R. and Krainer, A.R. (1998) A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev., 12, 55-66. (Pubitemid 28083658)
45. Huang, Y. and Steitz, J.A. (2005) SRprises along a messenger's journey. Mol. Cell, 17, 613-615. (Pubitemid 40320911)
46. Li, X. and Manley, J.L. (2005) New talents for an old acquaintance: the SR protein splicing factor ASF/SF2 functions in the maintenance of genome stability. Cell Cycle, 4, 1706-1708. (Pubitemid 41827307)
47. Li, X., Wang, J. and Manley, J.L. (2005) Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation. Genes Dev., 19, 2705-2714. (Pubitemid 41627937)