Advertisement

Plasmodium falciparum: Epigenetic Control of var Gene Regulation and Disease

  • Abhijit S. Deshmukh
  • Sandeep Srivastava
  • Suman Kumar Dhar
Part of the Subcellular Biochemistry book series (SCBI, volume 61)

Abstract

Plasmodium, one of the most important members of Apicomplexan protozoans imposes a significant economic and health impact on human populations around the world. Plasmodium parasite has complex life cycle with morphologically distinct asexual and sexual developmental stages in the human host and Anopheline mosquito vector. The parasites undergo rapid transition between morphological states and antigenic variation in order to sustain chronic infection and immune evasion in human host. To achieve all these, parasites adopt various regulatory pathways including transcriptional and posttranscriptional regulation of gene expression, translational repression and posttranslational modification of proteins. These regulatory modes help to respond to host conditions during an acute stage infection or life cycle transition of the parasite.

Keywords

Histone Modification Plasmodium Falciparum Histone Acetylation Cerebral Malaria Antigenic Variation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

Work in Dhar laboratory is funded by Swarnajayanti Fellowship (Department of Science and Technology, Govt. of India), MALSIG project (European Union), Alexander Von Humboldt Fellowship and National Biosciences award for career development awarded by Dept. of Biotechnology, Government of India. AD and SS acknowledge Council of Scientific and Industrial Research (CSIR), India for fellowships. The authors acknowledge Department of Biotechnology, Government of India for providing the Centre of Excellence in Parasitology grant.

References

  1. Aikawa M, Rabbage JR, Udeinya I, Miller LH (1983) Electron microscopy of knobs in Plasmodium falciparum infected erythrocytes. J Parasitol 69:435–437PubMedCrossRefGoogle Scholar
  2. Andrews KT, Tran TN, Lucke AJ, Kahnberg P, Le GT, Boyle GM, Gardiner DL, Skinner-Adams TS, Fairlie DP (2008) Potent antimalarial activity of histone deacetylase inhibitor analogues. Antimicrob Agents Chemother 52:1454–1461PubMedCrossRefGoogle Scholar
  3. Andrews KT, Tran TN, Wheatley NC, Fairlie DP (2009) Targeting histone deacetylase inhibitors for anti-malarial therapy. Curr Top Med Chem 9:292–308PubMedCrossRefGoogle Scholar
  4. Artavanis-Tsakonas K, Misaghi S, Comeaux CA, Catic A, Spooner E, Duraisingh MT, Ploegh HL (2006) Identification by functional proteomics of a deubiquitinating/deNeddylating enzyme in Plasmodium falciparum. Mol Microbiol 61:1187–1195PubMedCrossRefGoogle Scholar
  5. Balaji S, Babu MM, Iyer LM, Aravind L (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 33:3994–4006PubMedCrossRefGoogle Scholar
  6. Beauchamps P, Tourvieille B, Cesbron-Delauw MF, Capron A (1997) The partial sequence of the Plasmodium falciparum histone H4 gene. Res Microbiol 148:201–203PubMedCrossRefGoogle Scholar
  7. Beeson JG, Brown GV (2002) Pathogenesis of Plasmodium falciparum malaria: the roles of parasite adhesion and antigenic variation. Cell Mol Life Sci 59:258–271PubMedCrossRefGoogle Scholar
  8. Bennett BJ, Thompson J, Coppel RL (1995) Identification of Plasmodium falciparum histone 2B and histone 3 genes. Mol Biochem Parasitol 70:231–233PubMedCrossRefGoogle Scholar
  9. Berger SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12:142–148PubMedCrossRefGoogle Scholar
  10. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A (2009) An operational definition of epigenetics. Genes Dev 23:781–783PubMedCrossRefGoogle Scholar
  11. Biggs BA, Gooze L, Wycherley K, Wollish W, Southwell B et al (1991) Antigenic variation in Plasmodium falciparum. Proc Natl Acad Sci 88:9171–9174PubMedCrossRefGoogle Scholar
  12. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1:E5PubMedCrossRefGoogle Scholar
  13. Carrozza MJ, Utley RT, Workman JL, Cote J (2003) The diverse functions of histone acetyltransferase complexes. Trends Genet 19:321–329PubMedCrossRefGoogle Scholar
  14. Cary C, Lamont D, Dalton JP, Doerig C (1994) Plasmodium falciparum chromatin: nucleosomal organisation and histone-like proteins. Parasitol Res 80:255–258PubMedCrossRefGoogle Scholar
  15. Chaal BK, Gupta AP, Wastuwidyaningtyas BD, Luah YH, Bozdech Z (2010) Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog 6:e1000737PubMedCrossRefGoogle Scholar
  16. Chen Q, Fernandez V, Sundstrom A, Schlichtherle M, Datta S, Hagblom P, Wahlgren M (1998) Developmental selection of var gene expression in Plasmodium falciparum. Nature 394:392–395PubMedCrossRefGoogle Scholar
  17. Choi SW, Keyes ME, Horrocks P (2006) LC/ESI-MS demonstrates the absence of 5-methyl-2-deoxycytosine in Plasmodium falciparum genomic DNA. Mol Biochem Parasitol 150:350–352PubMedCrossRefGoogle Scholar
  18. Chung DW, Ponts N, Cervantes S, Le Roch KG (2009) Post-translational modifications in Plasmodium: more than you think! Mol Biochem Parasitol 168:123–134PubMedCrossRefGoogle Scholar
  19. Colletti SL, Myers RW, Darkin-Rattray SJ, Gurnett AM, Dulski PM, Galuska S, Allocco JJ, Ayer MB, Li C, Lim J, Crumley TM, Cannova C, Schmatz DM, Wyvratt MJ, Fisher MH, Meinke PT (2001) Broad spectrum antiprotozoal agents that inhibit histone deacetylase: structure-activity relationships of apicidin. Part 2. Bioorg Med Chem Lett 11:113–117PubMedCrossRefGoogle Scholar
  20. Cortes A, Carret C, Kaneko O, Lim BYSY, Ivens A, Holder A (2007) Epigenetic silencing of Plasmodium falciparum genes linked to erythrocyte invasion. PLoS Pathog 3:1023–1035CrossRefGoogle Scholar
  21. Cui L, Miao J (2010) Chromatin-mediated epigenetic regulation in the malaria parasite Plasmodium falciparum. Eukaryot Cell 9:1138–1149PubMedCrossRefGoogle Scholar
  22. Cui L, Miao J, Furuya T, Li X, Su X, Cui L (2007) PfGCN5 mediated histone H3 acetylation plays a key role in gene expression in Plasmodium falciparum. Eukaryot Cell 6:1219–1227PubMedCrossRefGoogle Scholar
  23. Cui L, Fan Q, Cui L, Miao J (2008a) Histone lysine methyltransferases and demethylases in Plasmodium falciparum. Int J Parasitol 38:1083–1109PubMedCrossRefGoogle Scholar
  24. Cui L, Miao J, Furuya T, Fan Q, Li X, Rathod PK, Su XZ, Cui L (2008b) Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development. Eukaryot Cell 7:1200–1210PubMedCrossRefGoogle Scholar
  25. Darkin-Rattray SJ, Gurnett AM, Myers RW, Dulski PM, Crumley TM, Allocco JJ, Cannova C, Meinke PT, Colletti SL, Bednarek MA, Singh SB, Goetz MA, Dombrowski AW, Polishook JD, Schmatz DM (1996) Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase. Proc Natl Acad Sci USA 93:13143–13147sPubMedCrossRefGoogle Scholar
  26. Deitsch KW, del Pinal A, Wellems TE (1999) Intracluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum. Mol Biochem Parasitol 101:107–116PubMedCrossRefGoogle Scholar
  27. Deitsch KW, Lukehart SA, Stringer JR (2009) Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 7:493–503PubMedCrossRefGoogle Scholar
  28. Deshmukh AS, Srivastava S, Herrmann S, Gupta A, Mitra P, Gilberger TW, Dhar SK (2012) The role of N-terminus of Plasmodium falciparum ORC1 in telomeric localization and var gene silencing. Nucleic Acids Res. Epub ahead of printGoogle Scholar
  29. DiPaolo C, Kieft R, Cross M, Sabatini R (2005) Regulation of trypanosome DNA glycosylation by a SWI2/SNF2-like protein. Mol Cell 17:441–451PubMedCrossRefGoogle Scholar
  30. Dow GS et al (2008) Antimalarial activity of phenylthiazolyl-bearing hydroxamate-based histone deacetylase inhibitors. Antimicrob Agents Chemother 52:3467–3477PubMedCrossRefGoogle Scholar
  31. Duffy MF, Brown GV, Basuki W, Krejany EO, Noviyanti R, Cowman AF, Reeder JC (2002) Transcription of multiple var genes by individual, trophozoite-stage Plasmodium falciparum cells expressing a chondroitin sulphate A binding phenotype. Mol Microbiol 43:1285–1293PubMedCrossRefGoogle Scholar
  32. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, Thompson JK, Freitas-Junior LH, Scherf A, Crabb BS, Cowman AF (2005) Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121:13–24PubMedCrossRefGoogle Scholar
  33. Fan Q, An L, Cui L (2004a) Plasmodium falciparum histone acetyltransferase, a yeast GCN5 homologue involved in chromatin remodeling. Eukaryot Cell 3:264–276PubMedCrossRefGoogle Scholar
  34. Fan Q, Li J, Kariuki M, Cui L (2004b) Characterization of PfPuf2, member of the Puf family RNA-binding proteins from the malaria parasite Plasmodium falciparum. DNA Cell Biol 23:753–760PubMedCrossRefGoogle Scholar
  35. Fan Q, Miao J, Cui L, Cui L (2009) Characterization of PRMT1 from Plasmodium falciparum. Biochem J 421:107–118PubMedCrossRefGoogle Scholar
  36. Fernandez V, Chen Q, Sundstrom A, Scherf A, Hagblom P, Wahlgren M (2002) Mosaic-like transcription of var genes in single Plasmodium falciparum parasites. Mol Biochem Parasitol 121:195–203PubMedCrossRefGoogle Scholar
  37. Figueiredo LM, Pirrit LA, Scherf A (2000) Genomic organisation and chromatin structure of Plasmodium falciparum chromosome ends. Mol Biochem Parasitol 106:169–174PubMedCrossRefGoogle Scholar
  38. Figueiredo LM, Rocha EPC, Mancio-Silva L, Prevost C, Hernandez-Verdun D, Scherf A (2005) The unusually large Plasmodium telomerase reverse-transcriptase localizes in a discrete compartment associated with the nucleolus. Nucleic Acids Res 33:1111–1122PubMedCrossRefGoogle Scholar
  39. Flueck C, Bartfai R, Volz J, Niederwieser I, Salcedo-Amaya AM et al (2009) Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 5:e1000569PubMedCrossRefGoogle Scholar
  40. Freitas-Junior LH, Hernandez-Rivas R, Ralph SA, Montiel-Condado D, Ruvalcaba-Salazar OK, Rojas-Meza AP, Mancio-Silva L, Leal-Silvestre RJ, Gontijo AM, Shorte S, Scherf A (2005) Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121:25–36PubMedCrossRefGoogle Scholar
  41. French JB, Cen Y, Sauve AA (2008) Plasmodium falciparum Sir2 is an NAD+-dependent deacetylase and an acetyllysine-dependent and acetyllysine-independent NAD+ glycohydrolase. Biochemistry 47:10227–10239PubMedCrossRefGoogle Scholar
  42. Frickel EM, Quesada V, Muething L, Gubbels MJ, Spooner E, Ploegh H, Artavanis-Tsakonas K (2007) Apicomplexan UCHL3 retains dual specificity for ubiquitin and Nedd8 throughout evolution. Cell Microbiol 9:1601–1610PubMedCrossRefGoogle Scholar
  43. Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635–638PubMedCrossRefGoogle Scholar
  44. Grant S, Easley C, Kirkpatrick P (2007) Vorinostat. Nat Rev Drug Discov 6:21–22PubMedCrossRefGoogle Scholar
  45. Grau GE, Tayler TE, Moleneux ME, Wirima JJ, Vasalli P, Homell M, Lambert PH (1989) Tumor necrosis factor and disease severity in children with P. falciparum malaria. N Engl J Med 320:1589–1591CrossRefGoogle Scholar
  46. Grau GE, Fajardo LF, Piquet PF, Allet B, Lambert PH, Vasalli P (1997) Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237:1210–1212CrossRefGoogle Scholar
  47. Gruenberg J, Allred D, Sherman IW (1983) Scanning microscope analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum infected erythrocytes. J Cell Biol 97:795–802PubMedCrossRefGoogle Scholar
  48. Ho M, Davis TME, Silamut K, Bunnang D, White NJ (1991) Rosette formation of Plasmodium falciparum infected erythrocytes from patients with acute malaria. Infect Immun 59:2135–2139PubMedGoogle Scholar
  49. Horrocks P, Wong E, Russell K, Emes RD (2009) Control of gene expression in Plasmodium falciparum – ten years on. Mol Biochem Parasitol 164:9–25PubMedCrossRefGoogle Scholar
  50. Howard RJ, Barnwell JW, Kao V (1983) Antigenic variation in Plasmodium knowlesi malaria: identification of the variant antigen on infected erythrocytes. Proc Natl Acad Sci 80:4129–4133PubMedCrossRefGoogle Scholar
  51. Issar N, Ralph SA, Mancio-Silva L, Keeling C, Scherf A (2008a) Differential subnuclear localisation of repressive and activating histone methyl modifications in P. falciparum. Microbes Infect 11:403–407PubMedCrossRefGoogle Scholar
  52. Issar N, Roux E, Mattei D, Scherf A (2008b) Identification of a novel post-translational modification in Plasmodium falciparum: protein sumoylation in different cellular compartments. Cell Microbiol 10:1999–2011PubMedCrossRefGoogle Scholar
  53. Iyer LM, Anantharaman V, Wolf MY, Aravind L (2008) Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol 38:1–31PubMedCrossRefGoogle Scholar
  54. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080PubMedCrossRefGoogle Scholar
  55. Joshi MB, Lin DT, Chiang PH, Goldman ND, Fujioka H, Aikawa M, Syin C (1999) Molecular cloning and nuclear localization of a histone deacetylase homologue in Plasmodium falciparum. Mol Biochem Parasitol 99:11–19PubMedCrossRefGoogle Scholar
  56. Jutta M, Ferryanto C, Pak P, Wabiser F, Kenangalem E, Piera KA, Fairlie DP, Tjitra E, Anstey NM, Andrews KT, Price RN (2011) Ex Vivo activity of histone deacetylase inhibitors against multidrug-resistant clinical isolates of Plasmodium falciparum and P. vivax. Antimicrob Agents Chemother 55:961–966CrossRefGoogle Scholar
  57. Kaiser K, Matuschewski K, Camargo N, Ross J, Kappe SH (2004) Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Mol Microbiol 51:1221–1232PubMedCrossRefGoogle Scholar
  58. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMedCrossRefGoogle Scholar
  59. Lanzer M, de Bruin D, Wertheimer SP, Ravetch JV (1994) Transcriptional and nucleosomal characterization of a subtelomeric gene cluster flanking a site of chromosomal rearrangements in Plasmodium falciparum. Nucleic Acids Res 22:4176–4182PubMedCrossRefGoogle Scholar
  60. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch CH, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Winzeler EA (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301:1503–1508PubMedCrossRefGoogle Scholar
  61. Lee KK, Workman JL (2007) Histone acetyltransferase complexes: one size doesn’t fit all. Nat Rev Mol Cell Biol 8:284–295PubMedCrossRefGoogle Scholar
  62. Llinas M, Bozdech Z, Wong ED, Adai AT, DeRisi JL (2006) Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res 34:1166–1173PubMedCrossRefGoogle Scholar
  63. Lopez-Rubio JJ, Gontijo AM, Nunes MC, Issar N, Hernandez Rivas R, Scherf A (2007) 5′ flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol 66:1296–1305PubMedGoogle Scholar
  64. Luger K, Mäder AW, Richmond RK, Sargen DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389:251–260PubMedCrossRefGoogle Scholar
  65. Macdonald N, Welburn JP, Noble ME, Nguyen A, Yaffe MB, Clynes D, Moggs JG, Orphanides G, Thomson S, Edmunds JW, Clayton AL, Endicott JA, Mahadevan LC (2005) Molecular basis for the recognition of phosphorylated and phosphoacetylated histone h3 by 14-3-3. Mol Cell 20:199–211PubMedCrossRefGoogle Scholar
  66. Malik M, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10:882–891PubMedCrossRefGoogle Scholar
  67. Mancio-Silva L, Rojas-Meza AP, Vargas M, Scherf A, Hernandez-Rivas R (2008) Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum. J Cell Sci 121(Pt12):2046–2053PubMedCrossRefGoogle Scholar
  68. Mancio-Silva L, Zhanga Q, Scheidig-Benatara C, Scherf A (2010) Clustering of dispersed ribosomal DNA and its role in gene regulation and chromosome-end associations in malaria parasites. Proc Natl Acad Sci USA 107:15117–15122PubMedCrossRefGoogle Scholar
  69. Martens JA, Winston F (2003) Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr Opin Genet Dev 13:136–142PubMedCrossRefGoogle Scholar
  70. Matuschewski K, Ross J, Brown SM, Kaiser K, Nussenzweig V, Kappe SH (2002) Infectivity-associated changes in the transcriptional repertoire of the malaria parasite sporozoite stage. J Biol Chem 277:41948–41953PubMedCrossRefGoogle Scholar
  71. Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CF (2003) The Tudor domain ‘Royal Family’: Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem Sci 28:69–74PubMedCrossRefGoogle Scholar
  72. Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112:725–736PubMedCrossRefGoogle Scholar
  73. Merrick CJ, Duraisingh MT (2007) Plasmodium falciparum Sir2: an unusual sirtuin with dual histone deacetylase and ADP-ribosyltransferase activity. Eukaryot Cell 6:2081–2091PubMedCrossRefGoogle Scholar
  74. Merrick CJ, Duraisingh MT (2010) Epigenetics in Plasmodium: what do we really know? Eukaryot Cell 9:1150–1158PubMedCrossRefGoogle Scholar
  75. Merrick CJ, Dzikowski R, Imamura H, Chuang J, Deitsch K, Duraisingh MT (2010) 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 40:35–43PubMedCrossRefGoogle Scholar
  76. Miao J, Fan Q, Cui L, Li J, Li J, Cui L (2006) The malaria parasite Plasmodium falciparum histones: organization, expression, and acetylation. Gene 369:53–65PubMedCrossRefGoogle Scholar
  77. Mok BW, Ribacke U, Winter G, Yip BH, Tan CS, Fernandez V, Chen Q, Nilsson P, Wahlgren M (2007) Comparative transcriptomal analysis of isogenic Plasmodium falciparum clones of distinct antigenic and adhesive phenotypes. Mol Biochem Parasitol 151:184–192PubMedCrossRefGoogle Scholar
  78. Mok BW, Ribacke U, Rasti N, Kironde F, Chen Q, Nilsson P, Wahlgren M (2008) Default pathway of var2csa switching and translational repression in Plasmodium falciparum. PLoS One 3:e1982PubMedCrossRefGoogle Scholar
  79. Perez-Toledo K, Rojas-Meza AP, Mancio-Silva L, Hernandez-Cuevas NA, Delgadillo DM et al (2009) 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 37:2596–2606PubMedCrossRefGoogle Scholar
  80. Petter M, Lee CC, Byrne TJ, Boysen KE, Volz J, Ralph SA, Cowman AF, Brown GV, Duffy MF (2011) Expression of P. falciparum var genes involves exchange of the histone variant H2A.Z at the promoter. PLoS Pathog 7:e1001292PubMedCrossRefGoogle Scholar
  81. Ponder EL, Bogyo M (2007) Ubiquitin-like modifiers and their deconjugating enzymes in medically important parasitic protozoa. Eukaryot Cell 6:1943–1952PubMedCrossRefGoogle Scholar
  82. Ponts N, Yang J, Chung DW, Prudhomme J, Girke T, Horrocks P, Le Roch KG (2008) Deciphering the ubiquitin-mediated pathway in apicomplexan parasites: a potential strategy to interfere with parasite virulence. PLoS One 3:e2386PubMedCrossRefGoogle Scholar
  83. Prusty D, Mehra P, Srivastava S, Shivange AV, Gupta A, Roy N, Dhar SK (2008) Nicotinamide inhibits Plasmodium falciparum Sir2 activity in vitro and parasite growth. FEMS Microbiol Lett 282:266–272PubMedCrossRefGoogle Scholar
  84. Przyborski JM, Bartels K, Lanzer M, Andrews KT (2003) The histone H4 gene of Plasmodium falciparum is developmentally transcribed in asexual parasites. Parasitol Res 90:387–389PubMedCrossRefGoogle Scholar
  85. Raibaud A, Brahimi K, Roth CW, Brey PT, Faust DM (2006) Differential gene expression in the ookinete stage of the malaria parasite Plasmodium berghei. Mol Biochem Parasitol 150:107–113PubMedCrossRefGoogle Scholar
  86. Ralph SA, Scheidig-Benatar C, Scherf A (2005) Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. Proc Natl Acad Sci USA 102:5414–5419PubMedCrossRefGoogle Scholar
  87. Ruthenburg AJ, Wang W, Graybosch DM, Li H, Allis CD, Patel DJ, Verdine GL (2006) Histone H3 recognition and presentation by the WDR5 module of the MLL1 complex. Nat Struct Mol Biol 13:704–712PubMedCrossRefGoogle Scholar
  88. Sacci JB, Ribeiro JM Jr, Huang F, Alam U, Russell JA, Blair PL, Witney A, Carucci DJ, Azad AF, Aguiar JC (2005) Transcriptional analysis of in vivo Plasmodium yoelii liver stage gene expression. Mol Biochem Parasitol 142:177–183PubMedCrossRefGoogle Scholar
  89. Salanti A, Staalsoe T, Lavstsen T, Atr J, Mpk S et al (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49:179–191PubMedCrossRefGoogle Scholar
  90. Sautel CF, Cannella D, Bastien O, Kieffer S, Aldebert D, Garin J, Tardieux I, Belrhali H, Hakimi MA (2007) SET8-mediated methylations of histone H4 lysine 20 mark silent heterochromatic domains in apicomplexan genomes. Mol Cell Biol 27:5711–5724PubMedCrossRefGoogle Scholar
  91. Scherf A, Hernandez-Rivas H, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M (1998) Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 17:5418–5426PubMedCrossRefGoogle Scholar
  92. Scholander C, Carlson J, Kremsenr PG, Wahlgren M (1998) Extensive immunoglobulin binding of Plasmodium falciparum-infected erythrocytes in a group of children with moderate anemia. Infect Immun 66:361–363PubMedGoogle Scholar
  93. Shi Y, Whetstine JR (2007) Dynamic regulation of histone lysine methylation by demethylases. Mol Cell 25:1–14PubMedCrossRefGoogle Scholar
  94. Shiio Y, Eisenman RN (2003) Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci USA 100:13225–13230PubMedCrossRefGoogle Scholar
  95. Silvestrini F, Bozdech Z, Lanfrancotti A, Di Giulio E, Bultrini E, Picci L, Derisi JL, Pizzi E, Alano P (2005) Genome-wide identification of genes upregulated at the onset of gametocytogenesis in Plasmodium falciparum. Mol Biochem Parasitol 143:100–110PubMedCrossRefGoogle Scholar
  96. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101–110PubMedCrossRefGoogle Scholar
  97. Sullivan WJ Jr (2003) Histone H3 and H3.3 variants in the protozoan pathogens of Plasmodium falciparum and Toxoplasma gondii. DNA Seq 14:227–231PubMedCrossRefGoogle Scholar
  98. Tarun AS, Peng X, Dumpit RF, Ogata Y, Silva-Rivera H, Camargo N, Daly TM, Bergman LW, Kappe SH (2008) A combined transcriptome and proteome survey of malaria parasite liver stages. Proc Natl Acad Sci USA 105:305–310PubMedCrossRefGoogle Scholar
  99. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ (2007) How chromatin-binding modules interpret histone modifications: lesson from professional pocket pickers. Nat Struct Mol Biol 14:1025–1040PubMedCrossRefGoogle Scholar
  100. Templeton TJ, Iyer LM, Anantharaman V, Enomoto S, Abrahante JE, Subramanian GM, Hoffman SL, Abrahamsen MS, Aravind L (2004) Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res 14:1686–1695PubMedCrossRefGoogle Scholar
  101. Tonkin CJ, Carret CK, Duraisingh MT, Voss TS, Ralph RA, Hommel M, Duffy MF, Silva LM, Scherf A, Ivens A, Speed TP, Beeson JG, Cowman AF (2009) Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 7:e84PubMedCrossRefGoogle Scholar
  102. Trelle MB, Salcedo-Amaya AM, Cohen AM, Stunnenberg HG, Jensen ON (2009) Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum. J Proteome Res 8:3439–3450PubMedCrossRefGoogle Scholar
  103. Voss TS, Kaestli M, Vogel D, Bopp S, Beck HP (2003) Identification of nuclear proteins that differentially interact with Plasmodium falciparum var gene promoters. Mol Microbiol 48:1593–1607PubMedCrossRefGoogle Scholar
  104. Voss TS, Healer J, Marty AJ, Duffy MF, Thompson JK, Beeson JG, Reeder JC, Crabb BS, Cowman AF (2006) A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439:1004–1008PubMedGoogle Scholar
  105. Voss TS, Tonkin CJ, Marty AJ, Thompson JK, Healer J, Crabb BS, Cowman AF (2007) Alterations in local chromatin environment are involved in silencing and activation of subtelomeric var genes in Plasmodium falciparum. Mol Microbiol 66:139–150PubMedCrossRefGoogle Scholar
  106. Waddington CH (1942) The epigenotype. Endeavour 1:18–20Google Scholar
  107. Weake VM, Workman JL (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29:653–663PubMedCrossRefGoogle Scholar
  108. Westenberger SJ, Cui L, Dharia N, Winzeler E, Cui L (2009) Genome-wide nucleosome mapping of Plasmodium falciparum reveals histone-rich coding and histone-poor intergenic regions and chromatin remodeling of core and subtelomeric genes. BMC Genomics 10:610PubMedCrossRefGoogle Scholar
  109. Xu WS, Parmigiani RB, Marks PA (2007) Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26:5541–5552PubMedCrossRefGoogle Scholar
  110. Yang XJ, Seto E (2007) HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 26:5310–5318PubMedCrossRefGoogle Scholar
  111. Yuda M, Iwanaga S, Shigenobu S, Mair GR, Janse CJ, Waters AP, Kato T, Kaneko I (2009) Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol 71:1402–1414PubMedCrossRefGoogle Scholar
  112. Zeng L, Zhou MM (2002) Bromodomain: an acetyl-lysine binding domain. FEBS Lett 513:124–128PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Abhijit S. Deshmukh
    • 1
  • Sandeep Srivastava
    • 1
  • Suman Kumar Dhar
    • 1
  1. 1.Special Centre for Molecular MedicineJawaharlal Nehru UniversityNew DelhiIndia

Personalised recommendations