Plasmodium falciparum: Preinitiation complex occupancy of active and inactive promoters during erythrocytic stage

Experimental Parasitology

Volumn 121, Issue 1, 2009, Pages 46-54

  Gopalakrishnan, Anusha M ^a   Nyindodo, Lilian A ^a   Ross Fergus, M ^a   López Estraño, Carlos ^a  

^a UNIVERSITY OF MEMPHIS   (United States)

Author keywords

Gene expression; Plasmodium; Promoter; Regulation; Stage specificity; Transcription

Indexed keywords

HISTONE H3; HISTONE H4; PREINITIATION COMPLEX; PROTEIN; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR IIE; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; ERYTHROCYTE; GENE CONTROL; GENETIC TRANSCRIPTION; LIFE CYCLE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ACETYLATION; ANIMALS; ANTIBODIES, PROTOZOAN; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; ERYTHROCYTES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; HUMANS; MEROZOITE SURFACE PROTEIN 1; PLASMODIUM FALCIPARUM; PROMOTER REGIONS, GENETIC; PROTOZOAN PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TATA-BOX BINDING PROTEIN; TRANSCRIPTION FACTORS, TFII;

EUKARYOTA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

EID: 57049103382     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2008.09.016     Document Type: Article

References (67)

1. Akompong T., Kadekoppala M., Harrison T., Oksman A., Goldberg D.E., Fujioka H., Samuel B.U., Sullivan D., and Haldar K. Trans expression of a Plasmodium falciparum histidine rich protein II (HRPII) reveals sorting of soluble proteins in the periphery of the host erythrocyte and disrupts transport to the malarial food vacuole. Journal of Biological Chemistry 277 (2002) 28923-28933
2. Albright S.R., and Tjian R. TAFs revisited: more data reveal new twists and confirm old ideas. Gene 242 (2000) 1-13
3. Andrau J.C., van de Pasch L., Lijnzaad P., Bijma T., Koerkamp M.G., van de Peppel J., Werner M., and Holstege F.C. Genome-wide location of the coactivator mediator: Binding without activation and transient Cdk8 interaction on DNA. Molecular Cell 22 (2006) 179-192
4. Apone L.M., Virbasius C.A., Holstege F.C., Wang J., Young R.A., and Green M.R. Broad, but not universal, transcriptional requirement for yTAFII17, a histone H3-like TAFII present in TFIID and SAGA. Molecular Cell 2 (1998) 653-661
5. Balaji S., Babu M.M., Iyer L.M., and Aravind L. Discovery of the principal specific transcription factors of Apicomplexa and their implication for the evolution of the AP2-integrase DNA binding domains. Nucleic Acids Research 33 (2005) 3994-4006
6. Ben Mamoun C., Gluzman I.Y., Hott C., MacMillan S.K., Amarakone A.S., Anderson D.L., Carlton J.M., Dame J.B., Chakrabarti D., Martin R.K., Brownstein B.H., and Goldberg D.E. Co-ordinated programme of gene expression during asexual intraerythrocytic development of the human malaria parasite Plasmodium falciparum revealed by microarray analysis. Molecular Microbiology 39 (2001) 26-36
7. Blisnick T., Morales Betoulle M.E., Barale J.C., Uzureau P., Berry L., Desroses S., Fujioka H., Mattei D., and Braun Breton C. Pfsbp1, a Maurer's cleft Plasmodium falciparum protein, is associated with the erythrocyte skeleton. Molecular and Biochemical Parasitology 111 (2000) 107-121
8. Bonnefoy S., Attal G., Langsley G., Tekaia F., and Mercereau-Puijalon O. Molecular characterization of the heat shock protein 90 gene of the human malaria parasite Plasmodium falciparum. Molecular and Biochemical Parasitology 67 (1994) 157-170
9. Boschet C., Gissot M., Briquet S., Hamid Z., Claudel-Renard C., and Vaquero C. Characterization of PfMyb1 transcription factor during erythrocytic development of 3D7 and F12 Plasmodium falciparum clones. Molecular and Biochemical Parasitology 138 (2004) 159-163
10. Bozdech Z., Llinas M., Pulliam B.L., Wong E.D., Zhu J., and DeRisi J.L. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. Public Library of Science Biology 1 (2003) E5
11. Bushnell D.A., Cramer P., and Kornberg R.D. Structural basis of transcription: alpha-amanitin-RNA polymerase II cocrystal at 2.8 A resolution. The Proceedings of the National Academy of Sciences USA 99 (2002) 1218-1222
12. Callebaut I., Prat K., Meurice E., Mornon J.P., and Tomavo S. Prediction of the general transcription factors associated with RNA polymerase II in Plasmodium falciparum: conserved features and differences relative to other eukaryotes. Biomed Central Genomics 6 (2005) 100
13. Coulson R.M., Hall N., and Ouzounis C.A. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Research 14 (2004) 1548-1554
14. Cui L., Miao J., Furuya T., Li X., Su X.Z., and Cui L. PfGCN5-mediated histone H3 acetylation plays a key role in gene expression in Plasmodium falciparum. Eukaryotic Cell 6 (2007) 1219-1227
15. Dechering K.J., Kaan A.M., Mbacham W., Wirth D.F., Eling W., Konings R.N., and Stunnenberg H.G. Isolation and functional characterization of two distinct sexual-stage specific promoters of the human malaria parasite Plasmodium falciparum. Molecular and Cellular Biology 19 (1999) 967-978
16. Deitsch K., Duraisingh M., Dzikowski R., Gunasekera A., Khan S., Le Roch K., Llinas M., Mair G., McGovern V., Roos D., Shock J., Sims J., Wiegand R., and Winzeler E. Mechanisms of gene regulation in Plasmodium. American Journal of Tropical Medicine and Hygiene 77 (2007) 201-208
17. Deitsch K.W., Calderwood M.S., and Wellems T.E. Malaria. Cooperative silencing elements in var genes. Nature 412 (2001) 875-876
18. Duraisingh M.T., Voss T.S., Marty A.J., Duffy M.F., Good R.T., Thompson J.K., Freitas-Junior L.H., Scherf A., Crabb B.S., and Cowman A.F. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121 (2005) 13-24
19. Freitas-Junior L.H., Hernandez-Rivas R., Ralph S.A., Montiel-Condado D., Ruvalcaba-Salazar O.K., Rojas-Meza A.P., Mancio-Silva L., Leal-Silvestre R.J., Gontijo A.M., Shorte S., and Scherf A. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121 (2005) 25-36
20. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., Paulsen I.T., James K., Eisen J.A., Rutherford K., Salzberg S.L., Craig A., Kyes S., Chan M.S., Nene V., Shallom S.J., Suh B., Peterson J., Angiuoli S., Pertea M., Allen J., Selengut J., Haft D., Mather M.W., Vaidya A.B., Martin D.M., Fairlamb A.H., Fraunholz M.J., Roos D.S., Ralph S.A., McFadden G.I., Cummings L.M., Subramanian G.M., Mungall C., Venter J.C., Carucci D.J., Hoffman S.L., Newbold C., Davis R.W., Fraser C.M., and Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419 (2002) 498-511
21. Gissot M., Briquet S., Refour P., Boschet C., and Vaquero C. PfMyb1, a Plasmodium falciparum transcription factor, is required for intra-erythrocytic growth and controls key genes for cell cycle regulation. Journal of Molecular Biology 346 (2005) 29-42
22. Green M.R. TBP-associated factors (TAFIIs): multiple, selective transcriptional mediators in common complexes. Trends in Biochemical Sciences 25 (2000) 59-63
23. Guenther M.G., Levine S.S., Boyer L.A., Jaenisch R., and Young R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130 (2007) 77-88
24. Hahn S. The role of TAFs in RNA polymerase II transcription. Cell 95 (1998) 579-582
25. Hall N., Karras M., Raine J.D., Carlton J.M., Kooij T.W., Berriman M., Florens L., Janssen C.S., Pain A., Christophides G.K., James K., Rutherford K., Harris B., Harris D., Churcher C., Quail M.A., Ormond D., Doggett J., Trueman H.E., Mendoza J., Bidwell S.L., Rajandream M.A., Carucci D.J., Yates III J.R., Kafatos F.C., Janse C.J., Barrell B., Turner C.M., Waters A.P., and Sinden R.E. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307 (2005) 82-86
26. Hayward R.E., Derisi J.L., Alfadhli S., Kaslow D.C., Brown P.O., and Rathod P.K. Shotgun DNA microarrays and stage specific gene expression in Plasmodium falciparum malaria. Molecular Microbiology 35 (2000) 6-14
27. Holstege F.C., Jennings E.G., Wyrick J.J., Lee T.I., Hengartner C.J., Green M.R., Golub T.R., Lander E.S., and Young R.A. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95 (1998) 717-728
28. Horrocks P., Dechering K., and Lanzer M. Control of gene expression in Plasmodium falciparum. Molecular and Biochemical Parasitology 95 (1998) 171-181
29. Hughes K., Wand M., Foulston L., Young R., Harley K., Terry S., Ersfeld K., and Rudenko G. A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO Journal 26 (2007) 2400-2410
30. Ito T., Chiba T., Ozawa R., Yoshida M., Hattori M., and Sakaki Y. A comprehensive two-hybrid analysis to explore the yeast protein interactome. The Proceedings of the National Academy of Sciences USA 98 (2001) 4569-4574
31. Jacob S.T., Sajdel E.M., and Munro H.N. Specific action of alpha-amanitin on mammalian RNA polymerase protein. Nature 225 (1970) 60-62
32. Kaneko O., Yim Lim B.Y., Iriko H., Ling I.T., Otsuki H., Grainger M., Tsuboi T., Adams J.H., Mattei D., Holder A.A., and Torii M. Apical expression of three RhopH1/Clag proteins as components of the Plasmodium falciparum RhopH complex. Molecular and Biochemical Parasitology 143 (2005) 20-28
33. Kornberg R.D. Eukaryotic transcriptional control. Trends in Cell Biology 9 (1999) M46-49
34. Kornberg R.D. Mediator and the mechanism of transcriptional activation. Trends in Biochemical Sciences 30 (2005) 235-239
35. Kornberg R.D., and Lorch Y. Chromatin-modifying and -remodeling complexes. Current Opinion in Genetics & Development 9 (1999) 148-151
36. Kuras L., and Struhl K. Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature 399 (1999) 609-613
37. Kutner S., Breuer W.V., Ginsburg H., Aley S.B., and Cabantchik Z.I. Characterization of permeation pathways in the plasma membrane of human erythrocytes infected with early stages of Plasmodium falciparum: association with parasite development. Journal of Cell Physiology 125 (1985) 521-527
38. Kyes S., Christodoulou Z., Pinches R., Kriek N., Horrocks P., and Newbold C. Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II-mediated transcription initiation. Molecular Microbiology 63 (2007) 1237-1247
39. 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., and Winzeler E.A. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301 (2003) 1503-1508
40. Lopez-Estraño C., Gopalakrishnan A.M., Semblat J.P., Fergus M.R., Mazier D., and Haldar K. An enhancer-like region regulates hrp3 promoter stage specific gene expression in the human malaria parasite Plasmodium falciparum. Biochimica et Biophysica Acta 1769 (2007) 506-513
41. Lopez-Estraño C., Semblat J.P., Gopalakrishnan A.M., Turner L., Mazier D., and Haldar K. Plasmodium falciparum: hrp3 promoter region is associated with stage specificity and episomal recombination. Experimental Parasitology 116 (2007) 327-333
42. Lopez-Rubio J.J., Gontijo A.M., Nunes M.C., Issar N., Hernandez Rivas R., and Scherf A. 5' flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Molecular Microbiology 66 (2007) 1296-1305
43. Lorch Y., Beve J., Gustafsson C.M., Myers L.C., and Kornberg R.D. Mediator-nucleosome interaction. Molecular Cell 6 (2000) 197-201
44. Mair G.R., Braks J.A., Garver L.S., Wiegant J.C., Hall N., Dirks R.W., Khan S.M., Dimopoulos G., Janse C.J., and Waters A.P. Regulation of sexual development of Plasmodium by translational repression. Science 313 (2006) 667-669
45. McAndrew M.B., Read M., Sims P.F., and Hyde J.E. Characterisation of the gene encoding an unusually divergent TATA-binding protein (TBP) from the extremely A+T-rich human malaria parasite Plasmodium falciparum. Gene 124 (1993) 165-171
46. Michel B., Komarnitsky P., and Buratowski S. Histone-like TAFs are essential for transcription in vivo. Molecular Cell 2 (1998) 663-673
47. Militello K.T., Dodge M., Bethke L., and Wirth D.F. Identification of regulatory elements in the Plasmodium falciparum genome. Molecular and Biochemical Parasitology 134 (2004) 75-88
48. Moqtaderi Z., Keaveney M., and Struhl K. The histone H3-like TAF is broadly required for transcription in yeast. Molecular Cell 2 (1998) 675-682
49. Munasinghe A., Patankar S., Cook B.P., Madden S.L., Martin R.K., Kyle D.E., Shoaibi A., Cummings L.M., and Wirth D.F. Serial analysis of gene expression (SAGE) in Plasmodium falciparum: application of the technique to A-T rich genomes. Molecular and Biochemical Parasitology 113 (2001) 23-34
50. Myler P.J. Transcritional analysis of the major merozoite surface antigen precursor (GP195) gene of Plasmodium falciparum. In: Agabian N., and Cerami A. (Eds). Parasites Molecular Biology, Drugs and Vaccine design (1990), Wiley-Liss Inc., New York 123-137
51. O'Sullivan J.M., Tan-Wong S.M., Morillon A., Lee B., Coles J., Mellor J., and Proudfoot N.J. Gene loops juxtapose promoters and terminators in yeast. Nature Genetics 36 (2004) 1014-1018
52. Ohkuma Y., Sumimoto H., Horikoshi M., and Roeder R.G. Factors involved in specific transcription by mammalian RNA polymerase II: purification and characterization of general transcription factor TFIIE. The Proceedings of the National Academy of Sciences USA 87 (1990) 9163-9167
53. Orfa Rojas M., and Wasserman M. Stage specific expression of the calmodulin gene in Plasmodium falciparum. The Journal of Biochemistry (Tokyo) 118 (1995) 1118-1123
54. Orphanides G., Lagrange T., and Reinberg D. The general transcription factors of RNA polymerase II. Genes & Development 10 (1996) 2657-2683
55. Patankar S., Munasinghe A., Shoaibi A., Cummings L.M., and Wirth D.F. 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. Molecular Biology of the Cell 12 (2001) 3114-3125
56. Radonjic M., Andrau J.C., Lijnzaad P., Kemmeren P., Kockelkorn T.T., van Leenen D., van Berkum N.L., and Holstege F.C. Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. Cerevisiae stationary phase exit. Molecular Cell 18 (2005) 171-183
57. Rock E.P., Marsh K., Saul A.J., Wellems T.E., Taylor D.W., Maloy W.L., and Howard R.J. Comparative analysis of the Plasmodium falciparum histidine rich proteins HRP-I, HRP-II and HRP-III in malaria parasites of diverse origin. Parasitology 95 (1987) 209-227 (pt 2)
58. Roeder R.G. Nuclear RNA polymerases: role of general initiation factors and cofactors in eukaryotic transcription. Methods in Enzymology 273 (1996) 165-171
59. Roh T.Y., Wei G., Farrell C.M., and Zhao K. Genome-wide prediction of conserved and nonconserved enhancers by histone acetylation patterns. Genome Research 17 (2007) 74-81
60. Ruiz i Altaba A., Ozaki L.S., Gwadz R.W., and Godson G.N. Organization and expression of the Plasmodium knowlesi circumsporozoite antigen gene. Molecular and Biochemical Parasitology 23 (1987) 233-245
61. Ruvalcaba-Salazar O.K., Ramirez-Estudillo M., Montiel-Condado D., Recillas-Targa F., Vargas M., and Hernandez-Rivas R. Recombinant and native Plasmodium falciparum TATA-binding-protein binds to a specific TATA box element in promoter regions. Molecular and Biochemical Parasitology 140 (2005) 183-196
62. Sawadogo M., Van Dyke M.W., Gregor P.D., and Roeder R.G. Multiple forms of the human gene specific transcription factor USF I. Complete purification and identification of USF from HeLa cell nuclei. Journal of Biological Chemistry 263 (1988) 11985-11993
63. Struhl K. Yeast transcriptional regulatory mechanisms. Annual Review of Genetics 29 (1995) 651-674
64. Trager W., and Jensen J.B. Human malaria in continuous culture. Science 193 (1976) 673-675
65. Van Dyke M.W., Roeder R.G., and Sawadogo M. Physical analysis of transcription preinitiation complex assembly on a class II gene promoter. Science 241 (1988) 1335-1338
66. Wellems T.E., and Howard R.J. Homologous genes include two distinct histidine rich proteins in a cloned isolate of Plasmodium falciparum. The Proceedings of the National Academy of Sciences USA 83 (1986) 6065-6069
67. Zhu X., Wiren M., Sinha I., Rasmussen N.N., Linder T., Holmberg S., Ekwall K., and Gustafsson C.M. Genome-wide occupancy profile of mediator and the Srb8-11 module reveals interactions with coding regions. Molecular Cell 22 (2006) 169-178