Nuclear repositioning precedes promoter accessibility and is linked to the switching frequency of a plasmodium falciparum invasion gene

Cell Host and Microbe

Volumn 12, Issue 6, 2012, Pages 739-750

  Coleman, Bradley I ^a   Ribacke, Ulf ^a   Manary, Micah ^b   Bei, Amy K ^a   Winzeler, Elizabeth A ^b   Wirth, Dyann F ^a   Duraisingh, Manoj T ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE INVASION LIGAND PFRH4; LIGAND; UNCLASSIFIED DRUG;

ARTICLE; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENE SWITCHING; HETEROCHROMATIN; NONHUMAN; PARASITE VIRULENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

ANTIGENIC VARIATION; CELL NUCLEUS; CHROMATIN; MEMBRANE PROTEINS; PLASMODIUM FALCIPARUM; PROMOTER REGIONS, GENETIC; PROTOZOAN PROTEINS; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

PLASMODIUM FALCIPARUM; PROKARYOTA;

EID: 84870991630     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2012.11.004     Document Type: Article

References (53)

1. K.T. Andrews, T.N. Tran, A.J. Lucke, P. Kahnberg, G.T. Le, G.M. Boyle, D.L. Gardiner, T.S. Skinner-Adams, and D.P. Fairlie Potent antimalarial activity of histone deacetylase inhibitor analogues Antimicrob. Agents Chemother. 52 2008 1454 1461
2. K.T. Andrews, A.P. Gupta, T.N. Tran, D.P. Fairlie, G.N. Gobert, and Z. Bozdech Comparative gene expression profiling of P. falciparum malaria parasites exposed to three different histone deacetylase inhibitors PLoS ONE 7 2012 e31847 10.1371/journal.pone.0031847
3. L.A. Banaszynski, L.-C. Chen, L.A. Maynard-Smith, A.G.L. Ooi, and T.J. Wandless A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules Cell 126 2006 995 1004
4. J. Baum, A.G. Maier, R.T. Good, K.M. Simpson, and A.F. Cowman Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions PLoS Pathog. 1 2005 e37 10.1371/journal.ppat.0010037
5. A.K. Bei, C.D. Membi, J.C. Rayner, M. Mubi, B. Ngasala, A.A. Sultan, Z. Premji, and M.T. Duraisingh Variant merozoite protein expression is associated with erythrocyte invasion phenotypes in Plasmodium falciparum isolates from Tanzania Mol. Biochem. Parasitol. 153 2007 66 71
6. A.K. Bei, T.M. Desimone, A.S. Badiane, A.D. Ahouidi, T. Dieye, D. Ndiaye, O. Sarr, O. Ndir, S. Mboup, and M.T. Duraisingh A flow cytometry-based assay for measuring invasion of red blood cells by Plasmodium falciparum Am. J. Hematol. 85 2010 234 237
7. K.J. Brolin, U. Ribacke, S. Nilsson, J. Ankarklev, K. Moll, M. Wahlgren, and Q. Chen Simultaneous transcription of duplicated var2csa gene copies in individual Plasmodium falciparum parasites Genome Biol. 10 2009 R117
8. T.L. Campbell, E.K. De Silva, K.L. Olszewski, O. Elemento, and M. Llinás Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite PLoS Pathog. 6 2010 e1001165 10.1371/journal.ppat.1001165
9. T. Chookajorn, R. Dzikowski, M. Frank, F. Li, A.Z. Jiwani, D.L. Hartl, and K.W. Deitsch Epigenetic memory at malaria virulence genes Proc. Natl. Acad. Sci. USA 104 2007 899 902
10. K. Chotivanich, R. Udomsangpetch, J.A. Simpson, P. Newton, S. Pukrittayakamee, S. Looareesuwan, and N.J. White Parasite multiplication potential and the severity of Falciparum malaria J. Infect. Dis. 181 2000 1206 1209
11. C.A. Comeaux, B.I. Coleman, A.K. Bei, N. Whitehurst, and M.T. Duraisingh Functional analysis of epigenetic regulation of tandem RhopH1/clag genes reveals a role in Plasmodium falciparum growth Mol. Microbiol. 80 2011 378 390
12. C. Crosnier, L.Y. Bustamante, S.J. Bartholdson, A.K. Bei, M. Theron, M. Uchikawa, S. Mboup, O. Ndir, D.P. Kwiatkowski, and M.T. Duraisingh Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum Nature 480 2011 534 537
13. K.W. Deitsch, S.A. Lukehart, and J.R. Stringer Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens Nat. Rev. Microbiol. 7 2009 493 503
14. E.K. De Silva, A.R. Gehrke, K. Olszewski, I. León, J.S. Chahal, M.L. Bulyk, and M. Llinás Specific DNA-binding by apicomplexan AP2 transcription factors Proc. Natl. Acad. Sci. USA 105 2008 8393 8398
15. S.A. Dolan, L.H. Miller, and T.E. Wellems Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum J. Clin. Invest. 86 1990 618 624
16. M.F. Duffy, T.J. Byrne, S.R. Elliott, D.W. Wilson, S.J. Rogerson, J.G. Beeson, R. Noviyanti, and G.V. Brown Broad analysis reveals a consistent pattern of var gene transcription in Plasmodium falciparum repeatedly selected for a defined adhesion phenotype Mol. Microbiol. 56 2005 774 788
17. M.T. Duraisingh, T. Triglia, S.A. Ralph, J.C. Rayner, J.W. Barnwell, G.I. McFadden, and A.F. Cowman Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes EMBO J. 22 2003 1047 1057
18. M.T. Duraisingh, T.S. Voss, A.J. Marty, M.F. Duffy, R.T. Good, J.K. Thompson, L.H. Freitas-Junior, A. Scherf, B.S. Crabb, and A.F. Cowman Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum Cell 121 2005 13 24
19. R. Dzikowski, F. Li, B. Amulic, A. Eisberg, M. Frank, S. Patel, T.E. Wellems, and K.W. Deitsch Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites EMBO Rep. 8 2007 959 965
20. Y. Fastman, R. Noble, M. Recker, and R. Dzikowski Erasing the epigenetic memory and beginning to switch - the onset of antigenic switching of var genes in Plasmodium falciparum PLoS ONE 7 2012 e34168 10.1371/journal.pone.0034168
21. Z. Fehér, S.L. Schlagman, Z. Miner, and S. Hattman In vivo methylation of yeast DNA by prokaryotic DNA methyltransferases Gene 74 1988 193 195
22. C. Flueck, R. Bartfai, J. Volz, I. Niederwieser, A.M. Salcedo-Amaya, B.T.F. Alako, F. Ehlgen, S.A. Ralph, A.F. Cowman, and Z. Bozdech Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors PLoS Pathog. 5 2009 e1000569 10.1371/journal.ppat.1000569
23. C. Flueck, R. Bartfai, I. Niederwieser, K. Witmer, B.T. Alako, S. Moes, Z. Bozdech, P. Jenoe, H.G. Stunnenberg, and T.S. Voss A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology PLoS Pathog. 6 2010 e1000784 10.1371/journal.ppat.1000784
24. L.H. Freitas-Junior, E. Bottius, L.A. Pirrit, K.W. Deitsch, C. Scheidig, F. Guinet, U. Nehrbass, T.E. Wellems, and A. Scherf Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum Nature 407 2000 1018 1022
25. L.H. Freitas-Junior, R. Hernandez-Rivas, S.A. Ralph, D. Montiel-Condado, O.K. Ruvalcaba-Salazar, A.P. Rojas-Meza, L. Mâncio-Silva, R.J. Leal-Silvestre, A.M. Gontijo, S. Shorte, and A. Scherf Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites Cell 121 2005 25 36
26. D. Gaur, S. Singh, S. Singh, L. Jiang, A. Diouf, and L.H. Miller Recombinant Plasmodium falciparum reticulocyte homology protein 4 binds to erythrocytes and blocks invasion Proc. Natl. Acad. Sci. USA 104 2007 17789 17794
27. S.M. Görisch, M. Wachsmuth, K.F. Tóth, P. Lichter, and K. Rippe Histone acetylation increases chromatin accessibility J. Cell Sci. 118 2005 5825 5834
28. D.E. Gottschling Telomere-proximal DNA in Saccharomyces cerevisiae is refractory to methyltransferase activity in vivo Proc. Natl. Acad. Sci. USA 89 1992 4062 4065
29. S. Hattman DNA-[adenine] methylation in lower eukaryotes Biochemistry (Mosc.) 70 2005 550 558
30. C.A. Howitt, D. Wilinski, M. Llinás, T.J. Templeton, R. Dzikowski, and K.W. Deitsch Clonally variant gene families in Plasmodium falciparum share a common activation factor Mol. Microbiol. 73 2009 1171 1185
31. L. Jiang, M.J. López-Barragán, H. Jiang, J. Mu, D. Gaur, K. Zhao, G. Felsenfeld, and L.H. Miller Epigenetic control of the variable expression of a Plasmodium falciparum receptor protein for erythrocyte invasion Proc. Natl. Acad. Sci. USA 107 2010 2224 2229
32. D. Landeira, and M. Navarro Nuclear repositioning of the VSG promoter during developmental silencing in Trypanosoma brucei J. Cell Biol. 176 2007 133 139
33. K.G. Le Roch, 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 Discovery of gene function by expression profiling of the malaria parasite life cycle Science 301 2003 1503 1508
34. J.-J. Lopez-Rubio, L. Mancio-Silva, and A. Scherf Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites Cell Host Microbe 5 2009 179 190
35. S. Nery, A.-M. Deans, M. Mosobo, K. Marsh, J.A. Rowe, and D.J. Conway Expression of Plasmodium falciparum genes involved in erythrocyte invasion varies among isolates cultured directly from patients Mol. Biochem. Parasitol. 149 2006 208 215
36. L.J. Nkrumah, R.A. Muhle, P.A. Moura, P. Ghosh, G.F. Hatfull, W.R. Jacobs Jr., and D.A. Fidock Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase Nat. Methods 3 2006 615 621
37. K. Pérez-Toledo, A.P. Rojas-Meza, L. Mancio-Silva, N.A. Hernández-Cuevas, D.M. Delgadillo, M. Vargas, S. Martínez- Calvillo, A. Scherf, and R. Hernandez-Rivas Plasmodium falciparum heterochromatin protein 1 binds to tri-methylated histone 3 lysine 9 and is linked to mutually exclusive expression of var genes Nucleic Acids Res. 37 2009 2596 2606
38. K.E.M. Persson, F.J. McCallum, L. Reiling, N.A. Lister, J. Stubbs, A.F. Cowman, K. Marsh, and J.G. Beeson Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies J. Clin. Invest. 118 2008 342 351
39. M. Petter, C.C. Lee, T.J. Byrne, K.E. Boysen, J. Volz, S.A. Ralph, A.F. Cowman, G.V. Brown, and M.F. Duffy Expression of P. falciparum var genes involves exchange of the histone variant H2A.Z at the promoter PLoS Pathog. 7 2011 e1001292 10.1371/journal.ppat.1001292
40. S.A. Ralph, C. Scheidig-Benatar, and A. Scherf Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations Proc. Natl. Acad. Sci. USA 102 2005 5414 5419
41. A. Scherf, R. Hernandez-Rivas, P. Buffet, E. Bottius, C. Benatar, B. Pouvelle, J. Gysin, and M. Lanzer Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum EMBO J. 17 1998 5418 5426
42. J. Singh, and A.J. Klar Active genes in budding yeast display enhanced in vivo accessibility to foreign DNA methylases: a novel in vivo probe for chromatin structure of yeast Genes Dev. 6 1992 186 196
43. S.C. Soubes, T.E. Wellems, and L.H. Miller Plasmodium falciparum: a high proportion of parasites from a population of the Dd2 strain are able to invade erythrocytes by an alternative pathway Exp. Parasitol. 86 1997 79 83
44. J. Stubbs, K.M. Simpson, T. Triglia, D. Plouffe, C.J. Tonkin, M.T. Duraisingh, A.G. Maier, E.A. Winzeler, and A.F. Cowman Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes Science 309 2005 1384 1387
45. W.H. Tham, D.W. Wilson, S. Lopaticki, C.Q. Schmidt, P.B. Tetteh-Quarcoo, P.N. Barlow, D. Richard, J.E. Corbin, J.G. Beeson, and A.F. Cowman Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand Proc. Natl. Acad. Sci. USA 107 2010 17327 17332
46. W. Trager, and J.B. Jensen Human malaria parasites in continuous culture Science 193 1976 673 675
47. T. Triglia, M.T. Duraisingh, R.T. Good, and A.F. Cowman Reticulocyte-binding protein homologue 1 is required for sialic acid-dependent invasion into human erythrocytes by Plasmodium falciparum Mol. Microbiol. 55 2005 162 174
48. J.C. Volz, R. Bártfai, M. Petter, C. Langer, G.A. Josling, T. Tsuboi, F. Schwach, J. Baum, J.C. Rayner, and H.G. Stunnenberg PfSET10, a Plasmodium falciparum methyltransferase, maintains the active var gene in a poised state during parasite division Cell Host Microbe 11 2012 7 18
49. T.S. Voss, J. Healer, A.J. Marty, M.F. Duffy, J.K. Thompson, J.G. Beeson, J.C. Reeder, B.S. Crabb, and A.F. Cowman A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria Nature 439 2006 1004 1008
50. A. Weiner, N. Dahan-Pasternak, E. Shimoni, V. Shinder, P. von Huth, M. Elbaum, and R. Dzikowski 3D nuclear architecture reveals coupled cell cycle dynamics of chromatin and nuclear pores in the malaria parasite Plasmodium falciparum Cell. Microbiol. 13 2011 967 977
51. D.R. Wines, P.B. Talbert, D.V. Clark, and S. Henikoff Introduction of a DNA methyltransferase into Drosophila to probe chromatin structure in vivo Chromosoma 104 1996 332 340
52. K. Zhang, and P.K. Rathod Divergent regulation of dihydrofolate reductase between malaria parasite and human host Science 296 2002 545 547
53. Q. Zhang, Y. Huang, Y. Zhang, X. Fang, A. Claes, M. Duchateau, A. Namane, J.J. Lopez-Rubio, W. Pan, and A. Scherf A critical role of perinuclear filamentous actin in spatial repositioning and mutually exclusive expression of virulence genes in malaria parasites Cell Host Microbe 10 2011 451 463