Epigenetic memory takes center stage in the survival strategy of malaria parasites

Current Opinion in Microbiology

Volumn 20, Issue , 2014, Pages 88-95

  Voss, Till S ^a,b   Bozdech, Zbynek ^c   Bártfai, Richárd ^d  

^a SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE;

ANTIGENIC VARIATION; EPIGENETICS; ERYTHROCYTE; GENE EXPRESSION; GENETIC REGULATION; HISTONE MODIFICATION; MALARIA; NONHUMAN; NUTRIENT UPTAKE; PARASITE SURVIVAL; PARASITE TRANSMISSION; PLASMODIUM; PLASMODIUM FALCIPARUM; REVIEW; SEX DIFFERENTIATION; SEX TRANSFORMATION; ADAPTATION; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; CELL SURVIVAL; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; PLASMODIUM FALCIPARUM;

EID: 84902526618     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2014.05.007     Document Type: Review

References (68)

1. Kyes S., Horrocks P., Newbold C. Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 2001, 55:673-707.
2. Berger S.L., Kouzarides T., Shiekhattar R., Shilatifard A. An operational definition of epigenetics. Genes Dev 2009, 23:781-783.
3. Bannister A.J., Kouzarides T. Regulation of chromatin by histone modifications. Cell Res 2011, 21:381-395.
4. Miao J., Fan Q., Cui L., Li J., Li J., Cui L. The malaria parasite Plasmodium falciparum histones: organization, expression, and acetylation. Gene 2006, 369:53-65.
5. Trelle M.B., Salcedo-Amaya A.M., Cohen A.M., Stunnenberg H.G., Jensen O.N. Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum. J Proteome Res 2009, 8:3439-3450.
6. Miao J., Lawrence M., Jeffers V., Zhao F., Parker D., Ge Y., Sullivan W.J., Cui L. Extensive lysine acetylation occurs in evolutionarily conserved metabolic pathways and parasite-specific functions during Plasmodium falciparum intraerythrocytic development. Mol Microbiol 2013, 89:660-675.
7. Dastidar E.G., Dzeyk K., Krijgsveld J., Malmquist N.A., Doerig C., Scherf A., Lopez-Rubio J.J. Comprehensive histone phosphorylation analysis and identification of Pf14-3-3 protein as a histone H3 phosphorylation reader in malaria parasites. PLoS ONE 2013, 8:e53179.
8. Hoeijmakers W.A., Stunnenberg H.G., Bartfai R. Placing the Plasmodium falciparum epigenome on the map. Trends Parasitol 2012, 28:486-495.
9. Salcedo-Amaya A.M., van Driel M.A., Alako B.T., Trelle M.B., van den Elzen A.M., Cohen A.M., Janssen-Megens E.M., van de Vegte-Bolmer M., Selzer R.R., Iniguez A.L., et al. Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum. Proc Natl Acad Sci U S A 2009, 106:9655-9660.
10. Gupta A.P., Chin W.H., Zhu L., Mok S., Luah Y.H., Lim E.H., Bozdech Z. Dynamic epigenetic regulation of gene expression during the life cycle of malaria parasite Plasmodium falciparum. PLoS Pathog 2013, 9:e1003170.
11. Hoeijmakers W.A., Salcedo-Amaya A.M., Smits A.H., Francoijs K.J., Treeck M., Gilberger T.W., Stunnenberg H.G., Bartfai R. H2A.Z/H2B.Z double-variant nucleosomes inhabit the AT-rich promoter regions of the Plasmodium falciparum genome. Mol Microbiol 2013, 87:1061-1073.
12. Petter M., Selvarajah S.A., Lee C.C., Chin W.H., Gupta A.P., Bozdech Z., Brown G.V., Duffy M.F. H2A.Z. and H2B.Z double-variant nucleosomes define intergenic regions and dynamically occupy var gene promoters in the malaria parasite Plasmodium falciparum. Mol Microbiol 2013, 87:1167-1182.
13. Bartfai R., Hoeijmakers W.A., Salcedo-Amaya A.M., Smits A.H., Janssen-Megens E., Kaan A., Treeck M., Gilberger T.W., Francoijs K.J., Stunnenberg H.G. H2A.Z demarcates intergenic regions of the plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3. PLoS Pathog 2010, 6:e1001223.
14. Flueck C., Bartfai R., Volz J., Niederwieser I., Salcedo-Amaya A.M., Alako B.T., Ehlgen F., Ralph S.A., Cowman A.F., Bozdech Z., et al. Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 2009, 5:e1000569.
15. Lopez-Rubio J.J., Mancio-Silva L., Scherf A. Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites. Cell Host Microbe 2009, 5:179-190.
16. Rovira-Graells N., Gupta A.P., Planet E., Crowley V.M., Mok S., Ribas de P.L., Preiser P.R., Bozdech Z., Cortes A. Transcriptional variation in the malaria parasite Plasmodium falciparum. Genome Res 2012, 22:925-938.
17. Ponts N., Fu L., Harris E.Y., Zhang J., Chung D.W., Cervantes M.C., Prudhomme J., Atanasova-Penichon V., Zehraoui E., Bunnik E.M., et al. Genome-wide mapping of DNA methylation in the human malaria parasite Plasmodium falciparum. Cell Host Microbe 2013, 14:696-706.
18. Scherf A., Lopez-Rubio J.J., Riviere L. Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 2008, 62:445-470.
19. Pasternak N.D., Dzikowski R. PfEMP1: an antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum. Int J Biochem Cell Biol 2009, 41:1463-1466.
20. Lopez-Rubio J.J., Gontijo A.M., Nunes M.C., Issar N., Hernandez R.R., Scherf A. 5' flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol 2007, 66:1296-1305.
21. Perez-Toledo K., Rojas-Meza A.P., Mancio-Silva L., Hernandez-Cuevas N.A., Delgadillo D.M., Vargas M., Martinez-Calvillo S., Scherf A., Hernandez-Rivas R. 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 2009, 37:2596-2606.
22. 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., et al. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 2005, 121:25-36.
23. 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., Cowman A.F. Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 2005, 121:13-24.
24. Tonkin C.J., Carret C.K., Duraisingh M.T., Voss T.S., Ralph S.A., Hommel M., Duffy M.F., Silva L.M., Scherf A., Ivens A., et al. Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 2009, 7:e84.
25. Merrick C.J., Dzikowski R., Imamura H., Chuang J., Deitsch K., Duraisingh M.T. The effect of Plasmodium falciparum Sir2a histone deacetylase on clonal and longitudinal variation in expression of the var family of virulence genes. Int J Parasitol 2010, 40:35-43.
26. Volz J., Carvalho T.G., Ralph S.A., Gilson P., Thompson J., Tonkin C.J., Langer C., Crabb B.S., Cowman A.F. Potential epigenetic regulatory proteins localise to distinct nuclear sub-compartments in Plasmodium falciparum. Int J Parasitol 2010, 40:109-121.
27. Jiang L., Mu J., Zhang Q., Ni T., Srinivasan P., Rayavara K., Yang W., Turner L., Lavstsen T., Theander T.G., et al. PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 2013, 499:223-227.
28. Ukaegbu U.E., Kishore S.P., Kwiatkowski D.L., Pandarinath C., Dahan-Pasternak N., Dzikowski R., Deitsch K.W. Recruitment of PfSET2 by RNA polymerase II to variant antigen encoding loci contributes to antigenic variation in P. falciparum. PLoS Pathog 2014, 10:e1003854.
29. Marty A.J., Thompson J.K., Duffy M.F., Voss T.S., Cowman A.F., Crabb B.S. Evidence that Plasmodium falciparum chromosome end clusters are cross-linked by protein and are the sites of both virulence gene silencing and activation. Mol Microbiol 2006, 62:72-83.
30. Voss T.S., Healer J., Marty A.J., Duffy M.F., Thompson J.K., Beeson J.G., Reeder J.C., Crabb B.S., Cowman A.F. A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 2006, 439:1004-1008.
31. Ralph S.A., Scheidig-Benatar C., Scherf A. Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. Proc Natl Acad Sci U S A 2005, 102:5414-5419.
32. Dzikowski R., Li F., Amulic B., Eisberg A., Frank M., Patel S., Wellems T.E., Deitsch K.W. Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep 2007, 8:959-965.
33. Zhang Q., Huang Y., Zhang Y., Fang X., Claes A., Duchateau M., Namane A., Lopez-Rubio J.J., Pan W., Scherf A. A critical role of perinuclear filamentous actin in spatial repositioning and mutually exclusive expression of virulence genes in malaria parasites. Cell Host Microbe 2011, 10:451-463.
34. Swamy L., Amulic B., Deitsch K.W. Plasmodium falciparum var gene silencing is determined by cis DNA elements that form stable and heritable interactions. Eukaryot Cell 2011, 10:530-539.
35. Dzikowski R., Frank M., Deitsch K. Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. PLoS Pathog 2006, 2:e22.
36. Frank M., Dzikowski R., Costantini D., Amulic B., Berdougo E., Deitsch K. Strict pairing of var promoters and introns is required for var gene silencing in the malaria parasite Plasmodium falciparum. J Biol Chem 2006, 281:9942-9952.
37. Calderwood M.S., Gannoun-Zaki L., Wellems T.E., Deitsch K.W. 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 2003, 278:34125-34132.
38. Deitsch K.W., Calderwood M.S., Wellems T.E. Malaria. Cooperative silencing elements in var genes. Nature 2001, 412:875-876.
39. Brancucci N.M., Witmer K., Schmid C.D., Flueck C., Voss T.S. Identification of a cis-acting DNA-protein interaction implicated in singular var gene choice in Plasmodium falciparum. Cell Microbiol 2012, 14:1836-1848.
40. Avraham I., Schreier J., Dzikowski R. Insulator-like pairing elements regulate silencing and mutually exclusive expression in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 2012, 109:E3678-E3686.
41. Flueck C., Bartfai R., Niederwieser I., Witmer K., Alako B.T., Moes S., Bozdech Z., Jenoe P., Stunnenberg H.G., Voss T.S. A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology. PLoS Pathog 2010, 6:e1000784.
42. Voss T.S., Tonkin C.J., Marty A.J., Thompson J.K., Healer J., Crabb B.S., Cowman A.F. Alterations in local chromatin environment are involved in silencing and activation of subtelomeric var genes in Plasmodium falciparum. Mol Microbiol 2007, 66:139-150.
43. Voss T.S., Kaestli M., Vogel D., Bopp S., Beck H.P. Identification of nuclear proteins that interact differentially with Plasmodium falciparum var gene promoters. Mol Microbiol 2003, 48:1593-1607.
44. Volz J.C., Bartfai R., Petter M., Langer C., Josling G.A., Tsuboi T., Schwach F., Baum J., Rayner J.C., Stunnenberg H.G., et al. PfSET10, a Plasmodium falciparum methyltransferase, maintains the active var gene in a poised state during parasite division. Cell Host Microbe 2012, 11:7-18.
45. Desai S.A. Ion and nutrient uptake by malaria parasite-infected erythrocytes. Cell Microbiol 2012, 14:1003-1009.
46. Desai S.A. Targeting ion channels of Plasmodium falciparum -infected human erythrocytes for antimalarial development. Curr Drug Targets Infect Disord 2004, 4:79-86.
47. Nguitragool W., Bokhari A.A., Pillai A.D., Rayavara K., Sharma P., Turpin B., Aravind L., Desai S.A. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 2011, 145:665-677.
48. Pillai A.D., Nguitragool W., Lyko B., Dolinta K., Butler M.M., Nguyen S.T., Peet N.P., Bowlin T.L., Desai S.A. Solute restriction reveals an essential role for clag3-associated channels in malaria parasite nutrient acquisition. Mol Pharmacol 2012, 82:1104-1114.
49. Cortes A., Carret C., Kaneko O., Yim Lim B.Y., Ivens A., Holder A.A. Epigenetic silencing of Plasmodium falciparum genes linked to erythrocyte invasion. PLoS Pathog 2007, 3:e107.
50. Crowley V.M., Rovira-Graells N., de Pouplana L.R., Cortes A. Heterochromatin formation in bistable chromatin domains controls the epigenetic repression of clonally variant Plasmodium falciparum genes linked to erythrocyte invasion. Mol Microbiol 2011, 80:391-406.
51. Comeaux C.A., Coleman B.I., Bei A.K., Whitehurst N., Duraisingh M.T. Functional analysis of epigenetic regulation of tandem RhopH1/clag genes reveals a role in Plasmodium falciparum growth. Mol Microbiol 2011, 80:378-390.
52. Mira-Martinez S., Rovira-Graells N., Crowley V.M., Altenhofen L.M., Llinas M., Cortes A. Epigenetic switches in clag3 genes mediate blasticidin S resistance in malaria parasites. Cell Microbiol 2013, 15:1913-1923.
53. Sharma P., Wollenberg K., Sellers M., Zainabadi K., Galinsky K., Moss E., Nguitragool W., Neafsey D., Desai S.A. An epigenetic antimalarial resistance mechanism involving parasite genes linked to nutrient uptake. J Biol Chem 2013, 288:19429-19440.
54. Balaji S., Babu M.M., Iyer L.M., 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 Res 2005, 33:3994-4006.
55. Kafsack B.F., Rovira-Graells N., Clark T.G., Bancells C., Crowley V.M., Campino S.G., Williams A.E., Drought L.G., Kwiatkowski D.P., Baker D.A., et al. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 2014, 507:248-252.
56. Sinha A., Hughes K.R., Modrzynska K.K., Otto T.D., Pfander C., Dickens N.J., Religa A.A., Bushell E., Graham A.L., Cameron R., et al. A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 2014, 507:253-257.
57. Jiang L., Lopez-Barragan M.J., Jiang H., Mu J., Gaur D., Zhao K., Felsenfeld G., Miller L.H. Epigenetic control of the variable expression of a Plasmodium falciparum receptor protein for erythrocyte invasion. Proc Natl Acad Sci U S A 2010, 107:2224-2229.
58. Coleman B.I., Ribacke U., Manary M., Bei A.K., Winzeler E.A., Wirth D.F., Duraisingh M.T. Nuclear repositioning precedes promoter accessibility and is linked to the switching frequency of a Plasmodium falciparum invasion gene. Cell Host Microbe 2012, 12:739-750.
59. Scherf A., Hernandez-Rivas R., Buffet P., Bottius E., Benatar C., Pouvelle B., Gysin J., Lanzer M. Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 1998, 17:5418-5426.
60. Stubbs J., Simpson K.M., Triglia T., Plouffe D., Tonkin C.J., Duraisingh M.T., Maier A.G., Winzeler E.A., Cowman A.F. Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 2005, 309:1384-1387.
61. Mantel P.Y., Hoang A.N., Goldowitz I., Potashnikova D., Hamza B., Vorobjev I., Ghiran I., Toner M., Irimia D., Ivanov A.R., et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 2013, 13:521-534.
62. Regev-Rudzki N., Wilson D.W., Carvalho T.G., Sisquella X., Coleman B.M., Rug M., Bursac D., Angrisano F., Gee M., Hill A.F., et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 2013, 153:1120-1133.
63. Morahan B., Garcia-Bustos J. Kinase signalling in Plasmodium sexual stages and interventions to stop malaria transmission. Mol Biochem Parasitol 2014, 193:23-32.
64. Baum J., Papenfuss A.T., Mair G.R., Janse C.J., Vlachou D., Waters A.P., Cowman A.F., Crabb B.S., de Koning-Ward T.F. Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res 2009, 37:3788-3798.
65. Castel S.E., Martienssen R.A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 2013, 14:100-112.
66. Spence P.J., Jarra W., Levy P., Reid A.J., Chappell L., Brugat T., Sanders M., Berriman M., Langhorne J. Vector transmission regulates immune control of Plasmodium virulence. Nature 2013, 498:228-231.
67. Broadbent K.M., Park D., Wolf A.R., Van T.D., Sims J.S., Ribacke U., Volkman S., Duraisingh M., Wirth D., Sabeti P.C., et al. A global transcriptional analysis of Plasmodium falciparum malaria reveals a novel family of telomere-associated lncRNAs. Genome Biol 2011, 12:R56.
68. Epp C., Li F., Howitt C.A., Chookajorn T., Deitsch K.W. Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum. RNA 2009, 15:116-127.