Patterns of gene-specific and total transcriptional activity during the Plasmodium falciparum intraerythrocytic developmental cycle

Eukaryotic Cell

Volumn 8, Issue 3, 2009, Pages 327-338

  Sims, Jennifer S ^a,b   Militello, Kevin T ^c   Sims, Peter A ^d   Patel, Vishal P ^a,b   Kasper, Jacob M ^a   Wirth, Dyann F ^a,b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL PROTEIN;

ANIMAL; ARTICLE; ERYTHROCYTE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PLASMODIUM FALCIPARUM;

ANIMALS; ERYTHROCYTES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; TRANSCRIPTION, GENETIC;

PLASMODIUM FALCIPARUM;

EID: 61949478255     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00340-08     Document Type: Article

References (75)

1. Akhtar, A., G. Faye, and D. L. Bentley. 1996. Distinct activated and nonactivated RNA polymerase II complexes in yeast. EMBO J. 15:4654-4664.
2. Balaji, S., M. M. Babu, L. M. Iyer, and L. Aravind. 2005. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Res. 33:3994-4006.
3. Bozdech, Z., M. Llinas, B. L. Pulliam, E. D. Wong, J. Zhu, and J. L. DeRisi. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:E5.
4. Bzik, D. J. 1991. The structure and role of RNA polymerases in Plasmodium. Parasitol. Today 7:211-214.
5. Callebaut, I., K. Prat, E. Meurice, J. P. Mornon, and S. Tomavo. 2005. Prediction of the general transcription factors associated with RNA polymerase II in Plasmodium falciparum: conserved features and differences relative to other eukaryotes. BMC Genomics 6:100.
6. Chen, Y., D. Jirage, D. Caridha, A. K. Kathcart, E. A. Cortes, R. A. Dennull, J. A. Geyer, S. T. Prigge, and N. C. Waters. 2006. Identification of an effector protein and gain-of-function mutants that activate Pfmrk, a malarial cyclin-dependent protein kinase. Mol. Biochem. Parasitol. 149:48-57.
7. Coleman, B. I., and M. T. Duraisingh. 2008. Transcriptional control and gene silencing in Plasmodium falciparum. Cell. Microbiol. 10:1935-1946.
8. 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.
9. Daily, J. P., D. Scanfeld, N. Pochet, K. Le Roch, D. Plouffe, M. Kamal, O. Sarr, S. Mboup, O. Ndir, D. Wypij, K. Levasseur, E. Thomas, P. Tamayo, C. Dong, Y. Zhou, E. S. Lander, D. Ndiaye, D. Wirth, E. A. Winzeler, J. P. Mesirov, and A. Regev. 2007. Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature 450:1091-1095.
10. Deans, J. A., A. W. Thomas, P. M. Inge, and S. Cohen. 1983. Stage-specific protein synthesis by asexual blood stage parasites of Plasmodium falciparum. Mol. Biochem. Parasitol. 8:45-51.
11. Deitsch, K., M. Duraisingh, R. Dzikowski, A. Gunasekera, S. Khan, K. Le Roch, M. Llinas, G. Mair, V. McGovern, D. Roos, J. Shock, J. Sims, R. Wiegand, and E. Winzeler. 2007. Mechanisms of gene regulation in Plasmodium. Am. J. Trop. Med. Hyg. 77:201-208.
12. De Silva, E. K., A. R. Gehrke, K. Olszewski, I. Leon, J. S. Chahal, M. L. Bulyk, and M. Llinas. 2008. Specific DNA-binding by apicomplexan AP2 transcription factors. Proc. Natl. Acad. Sci. USA 105:8393-8398.
13. Desjardins, R. E., C. J. Canfield, J. D. Haynes, and J. D. Chulay. 1979. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob. Agents Chemother. 16:710-718.
14. Dieckmann, A., and A. Jung. 1986. Stage-specific sensitivity of Plasmodium falciparum to antifolates. Z. Parasitenkd. 72:591-594.
15. 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.
16. Garcia-Martinez, J., A. Aranda, and J. E. Perez-Ortin. 2004. Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol. Cell 15:303-313.
17. 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.
18. Gissot, M., S. Briquet, P. Refour, C. Boschet, and C. Vaquero. 2005. PfMyb1, a Plasmodium falciparum transcription factor, is required for intra-erythrocytic growth and controls key genes for cell cycle regulation. J. Mol. Biol. 346:29-42.
19. Gritzmacher, C. A., and R. T. Reese. 1984. Protein and nucleic acid synthesis during synchronized growth of Plasmodium falciparum. J. Bacteriol. 160:1165-1167.
20. Gunasekera, A. M., A. Myrick, K. T. Militello, J. S. Sims, C. K. Dong, T. Gierahn, K. Le Roch, E. Winzeler, and D. F. Wirth. 2007. Regulatory motifs uncovered among gene expression clusters in Plasmodium falciparum. Mol. Biochem. Parasitol. 153:19-30.
21. 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.
22. Gupta, S. K., S. Schulman, and J. P. Vanderberg. 1985. Stage-dependent toxicity of N-acetyl-glucosamine to Plasmodium falciparum. J. Protozool. 32:91-95.
23. Hakimi, M. A., and K. W. Deitsch. 2007. Epigenetics in Apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation. Curr. Opin. Microbiol. 10:357-362.
24. Hall, N., M. Karras, J. D. Raine, J. M. Carlton, T. W. Kooij, M. Berriman, L. Florens, C. S. Janssen, A. Pain, G. K. Christophides, K. James, K. Rutherford, B. Harris, D. Harris, C. Churcher, M. A. Quail, D. Ormond, J. Doggett, H. E. Trueman, J. Mendoza, S. L. Bidwell, M. A. Rajandream, D. J. Carucci, J. R. Yates III, F. C. Kafatos, C. J. Janse, B. Barrell, C. M. Turner, A. P. Waters, and R. E. Sinden. 2005. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307:82-86.
25. Hirayoshi, K., and J. T. Lis. 1999. Nuclear run-on assays: assessing transcription by measuring density of engaged RNA polymerases. Methods Enzymol. 304:351-362.
26. 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.
27. Horrocks, P., and M. Lanzer. 1999. Mutational analysis identifies a five base pair cis-acting sequence essential for GBP130 promoter activity in Plasmodium falciparum. Mol. Biochem. Parasitol. 99:77-87.
28. Kuersten, S., and E. B. Goodwin. 2003. The power of the 3′ UTR: translational control and development. Nat. Rev. Genet. 4:626-637.
29. 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.
30. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:418-420.
31. Lanzer, M., D. de Bruin, and J. V. Ravetch. 1992. A sequence element associated with the Plasmodium falciparum KAHRP gene is the site of developmentally regulated protein-DNA interactions. Nucleic Acids Res. 20:3051-3056.
32. Lanzer, M., D. de Bruin, and J. V. Ravetch. 1992. Transcription mapping of a 100 kb locus of Plasmodium falciparum identifies an intergenic region in which transcription terminates and reinitiates. EMBO J. 11:1949-1955.
33. 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.
34. 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.
35. Lindell, T. J., F. Weinberg, P. W. Morris, R. G. Roeder, and W. J. Rutter. 1970. Specific inhibition of nuclear RNA polymerase II by alpha-amanitin. Science 170:447-449.
36. Lis, J. T. 2007. Imaging Drosophila gene activation and polymerase pausing in vivo. Nature 450:198-202.
37. Llinas, M., Z. Bozdech, E. D. Wong, A. T. Adai, and J. L. DeRisi. 2006. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 34:1166-1173.
38. Lopez-Estrano, C., A. M. Gopalakrishnan, J. P. Semblat, M. R. Fergus, D. Mazier, and K. Haldar. 2007. An enhancer-like region regulates hrp3 promoter stage-specific gene expression in the human malaria parasite Plasmodium falciparum. Biochim. Biophys. Acta 1769:506-513.
39. Lopez-Rubio, J. J., L. Riviere, and A. Scherf. 2007. Shared epigenetic mechanisms control virulence factors in protozoan parasites. Curr. Opin. Microbiol. 10:560-568.
40. Loyevsky, M., F. Mompoint, E. Yikilmaz, S. F. Altschul, T. Madden, J. C. Wootton, J. Kurantsin-Mills, O. O. Kassim, V. R. Gordeuk, and T. A. Rouault. 2003. Expression of a recombinant IRP-like Plasmodium falciparum protein that specifically binds putative plasmodial IREs. Mol. Biochem. Parasitol. 126:231-238.
41. Mair, G. R., J. A. Braks, L. S. Garver, J. C. Wiegant, N. Hall, R. W. Dirks, S. M. Khan, G. Dimopoulos, C. J. Janse, and A. P. Waters. 2006. Regulation of sexual development of Plasmodium by translational repression. Science 313:667-669.
42. Reference deleted.
43. Martin, R. E., R. I. Henry, J. L. Abbey, J. D. Clements, and K. Kirk. 2005. The "permeome" of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 6:R26.
44. 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.
45. Militello, K. T., V. Patel, A. D. Chessler, J. K. Fisher, J. M. Kasper, A. Gunasekera, and D. F. Wirth. 2005. RNA polymerase II synthesizes antisense RNA in Plasmodium falciparum. RNA 11:365-370.
46. Militello, K. T., P. Refour, C. A. Comeaux, and M. T. Duraisingh. 2008. Antisense RNA and RNAi in protozoan parasites: working hard or hardly working? Mol. Biochem. Parasitol. 157:117-126.
47. Myrick, A., A. Munasinghe, S. Patankar, and D. F. Wirth. 2003. Mapping of the Plasmodium falciparum multidrug resistance gene 5′-upstream region, and evidence of induction of transcript levels by antimalarial drugs in chloroquine sensitive parasites. Mol. Microbiol. 49:671-683.
48. Newlands, S., L. K. Levitt, C. S. Robinson, A. B. Karpf, V. R. Hodgson, R. P. Wade, and E. C. Hardeman. 1998. Transcription occurs in pulses in muscle fibers. Genes Dev. 12:2748-2758.
49. Newport, J., and M. Kirschner. 1982. A major developmental transition in early Xenopus embryos. II. Control of the onset of transcription. Cell 30:687-696.
50. Osta, M., L. Gannoun-Zaki, S. Bonnefoy, C. Roy, and H. J. Vial. 2002. A 24 bp cis-acting element essential for the transcriptional activity of Plasmodium falciparum CDP-diacylglycerol synthase gene promoter. Mol. Biochem. Parasitol. 121:87-98.
51. 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.
52. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
53. 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.
54. Robson, K. J., and M. W. Jennings. 1991. The structure of the calmodulin gene of Plasmodium falciparum. Mol. Biochem. Parasitol. 46:19-34.
55. Ruvalcaba-Salazar, O. K., M. del Carmen Ramirez-Estudillo, D. Montiel-Condado, F. Recillas-Targa, M. Vargas, and R. Hernandez-Rivas. 2005. Recombinant and native Plasmodium falciparum TATA-binding-protein binds to a specific TATA box element in promoter regions. Mol. Biochem. Parasitol. 140:183-196.
56. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. Schaner, C. E., and W. G. Kelly. 24 January 2006. Germline chromatin. In The C. elegans Research Community, WormBook. doi:10.1895/wormbook.1.73.1.
58. Schieck, E., J. M. Pfahler, C. P. Sanchez, and M. Lanzer. 2007. Nuclear run-on analysis of var gene expression in Plasmodium falciparum. Mol. Biochem. Parasitol. 153:207-212.
59. Shock, J. L., K. F. Fischer, and J. L. DeRisi. 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.
60. Silamut, K., and N. J. White. 1993. Relation of the stage of parasite development in the peripheral blood to prognosis in severe falciparum malaria. Trans. R. Soc. Trop. Med. Hyg. 87:436-443.
61. Skinner, T. S., L. S. Manning, W. A. Johnston, and T. M. Davis. 1996. In vitro stage-specific sensitivity of Plasmodium falciparum to quinine and artemisinin drugs. Int. J. Parasitol. 26:519-525.
62. Sunil, S., V. S. Chauhan, and P. Malhotra. 2008. Distinct and stage specific nuclear factors regulate the expression of falcipains, Plasmodium falciparum cysteine proteases. BMC Mol. Biol. 9:47.
63. Trager, W., and J. B. Jensen. 1976. Human malaria parasites in continuous culture. Science 193:673-675.
64. Ullu, E., C. Tschudi, and T. Chakraborty. 2004. RNA interference in protozoan parasites. Cell. Microbiol. 6:509-519.
65. van Noort, V., and M. A. Huynen. 2006. Combinatorial gene regulation in Plasmodium falciparum. Trends Genet. 22:73-78.
66. Vernot-Hernandez, J. P., and H. G. Heidrich. 1984. Time-course of synthesis, transport and incorporation of a protein identified in purified membranes of host erythrocytes infected with a knob-forming strain of Plasmodium falciparum. Mol. Biochem. Parasitol. 12:337-350.
67. Volkman, S. K., P. C. Sabeti, D. DeCaprio, D. E. Neafsey, S. F. Schaffner, D. A. Milner, Jr., J. P. Daily, O. Sarr, D. Ndiaye, O. Ndir, S. Mboup, M. T. Duraisingh, A. Lukens, A. Derr, N. Stange-Thomann, S. Waggoner, R. Onofrio, L. Ziaugra, E. Mauceli, S. Gnerre, D. B. Jaffe, J. Zainoun, R. C. Wiegand, B. W. Birren, D. L. Hartl, J. E. Galagan, E. S. Lander, and D. F. Wirth. 2007. A genome-wide map of diversity in Plasmodium falciparum. Nat. Genet. 39:113-119.
68. Walker, A. K., P. R. Boag, and T. K. Blackwell. 2007. Transcription reactivation steps stimulated by oocyte maturation in C. elegans. Dev. Biol. 304:382-393.
69. Waters, A. P., C. Syin, and T. F. McCutchan. 1989. Developmental regulation of stage-specific ribosome populations in Plasmodium. Nature 342:438-440.
70. Wechselberger, M., B. Wielgat, and G. Kahl. 1979. Rhythmic changes in transcriptional activity during the development of potato tubers. Planta 147:199-204.
71. Weil, P. A., and S. P. Blatti. 1975. Partial purification and properties of calf thymus deoxyribonucleic acid dependent RNA polymerase III. Biochemistry 14:1636-1642.
72. Wu, J., D. H. Sieglaff, J. Gervin, and X. S. Xie. 2008. Discovering regulatory motifs in the Plasmodium genome using comparative genomics. Bioinformatics 24:1843-1849.
73. Yeh, I., T. Hanekamp, S. Tsoka, P. D. Karp, and R. B. Altman. 2004. Computational analysis of Plasmodium falciparum metabolism: organizing genomic information to facilitate drug discovery. Genome Res. 14:917-924.
74. Yonaha, M., T. Chibazakura, S. Kitajima, and Y. Yasukochi. 1995. Cell cycle-dependent regulation of RNA polymerase II basal transcription activity. Nucleic Acids Res. 23:4050-4054.
75. Young, J. A., J. R. Johnson, C. Benner, S. F. Yan, K. Chen, K. G. Le Roch, Y. Zhou, and E. A. Winzeler. 2008. In silico discovery of transcription regulatory elements in Plasmodium falciparum. BMC Genomics 9:70.