Transcriptional variation in the malaria parasite Plasmodium falciparum

Genome Research

Volumn 22, Issue 5, 2012, Pages 925-938

  Rovira Graells, Núria ^a,b   Gupta, Archna P ^c   Planet, Evarist ^a   Crowley, Valerie M ^a   Mok, Sachel ^c   De Pouplana, Lluís Ribas ^a,d   Preiser, Peter R ^c   Bozdech, Zbynek ^c   Cortés, Alfred ^a,b,d  

^a INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL LINE; CLONAL VARIATION; CONTROLLED STUDY; EPIGENETICS; ERYTHROCYTE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HEAT SHOCK; HETEROCHROMATIN; HOST PARASITE INTERACTION; IMMUNE EVASION; LIPID METABOLISM; MULTIGENE FAMILY; NATURAL SELECTION; NONHUMAN; PARASITE SURVIVAL; PHENOTYPIC VARIATION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN FOLDING;

ADAPTATION, PHYSIOLOGICAL; CULTURE TECHNIQUES; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENES, PROTOZOAN; HEAT-SHOCK RESPONSE; HETEROCHROMATIN; PLASMODIUM FALCIPARUM; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; TROPHOZOITES;

PLASMODIUM FALCIPARUM;

EID: 84859888831     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.129692.111     Document Type: Article

References (69)

1. Anders RF, Brown GV, Edwards A. 1983. Characterization of an S antigen synthesized by several isolates of Plasmodium falciparum. Proc Natl Acad Sci 80: 6652-6656. (Pubitemid 14240153)
2. 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: 3994-4006. (Pubitemid 41487260)
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Statist Soc 57: 289-300.
4. Bethke LL, Zilversmit M, Nielsen K, Daily J, Volkman SK, Ndiaye D, Lozovsky ER, Hartl DL, Wirth DF. 2006. Duplication, gene conversion, and genetic diversity in the species-specific acyl-CoA synthetase gene family of Plasmodium falciparum. Mol Biochem Parasitol 150: 10-24. (Pubitemid 44332573)
5. Bischoff E, Vaquero C. 2010. In silico and biological survey of transcription-associated proteins implicated in the transcriptional machinery during the erythrocytic development of Plasmodium falciparum. BMC Genomics 11: 34. doi: 10.1186/1471-2164-11-34.
6. 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: E5. doi: 10.1371/journal.pbio.0000005.
7. Burkot TR, Williams JL, Schneider I. 1984. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg 78: 339-341.
8. Campbell TL, De Silva EK, Olszewski KL, Elemento O, Llinas M. 2010. Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite. PLoS Pathog 6: e1001165. doi: 10.1371/journal.ppat.1001165.
9. Chookajorn T, Dzikowski R, Frank M, Li F, Jiwani AZ, Hartl DL, Deitsch KW. 2007. Epigenetic memory at malaria virulence genes. Proc Natl Acad Sci 104: 899-902. (Pubitemid 46154708)
10. Comeaux CA, Coleman BI, Bei AK, Whitehurst N, Duraisingh MT. 2011. Functional analysis of epigenetic regulation of tandem RhopH1/clag genes reveals a role in Plasmodium falciparum growth. Mol Microbiol 80: 378-390.
11. Cortés A. 2005. A chimeric Plasmodium falciparum Pfnbp2b/Pfnbp2a gene originated during asexual growth. Int J Parasitol 35: 125-130. (Pubitemid 40248706)
12. Cortés A. 2008. Switching Plasmodium falciparum genes on and off for erythrocyte invasion. Trends Parasitol 24: 517-524.
13. Cortés A, Benet A, Cooke BM, Barnwell JW, Reeder JC. 2004. Ability of Plasmodium falciparum to invade Southeast Asian ovalocytes varies between parasite lines. Blood 104: 2961-2966. (Pubitemid 39434988)
14. Cortés A, Carret C, Kaneko O, Yim Lim BY, Ivens A, Holder AA. 2007. Epigenetic silencing of Plasmodium falciparum genes linked to erythrocyte invasion. PLoS Pathog 3: e107. doi: 10.1371/journal.ppat.0030107.
15. Coulson RM, Hall N, Ouzounis CA. 2004. Comparative genomics of transcriptional control in the human malaria parasite Plasmodium falciparum. Genome Res 14: 1548-1554. (Pubitemid 39193405)
16. Crowley VM, Rovira-Graells N, de Pouplana LR, Cortés A. 2011. Heterochromatin formation in bistable chromatin domains controls the epigenetic repression of clonally variant Plasmodium falciparum genes linked to erythrocyte invasion. Mol Microbiol 80: 391-406.
17. Daily JP, Scanfeld D, Pochet N, Le Roch K, Plouffe D, Kamal M, Sarr O, Mboup S, Ndir O, Wypij D, et al. 2007. Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature 450: 1091-1095. (Pubitemid 350273605)
18. Dodd IB, Micheelsen MA, Sneppen K, Thon G. 2007. Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129: 813-822. (Pubitemid 46802381)
19. Eksi S, Haile Y, Furuya T, Ma L, Su X, Williamson KC. 2005. Identification of a subtelomeric gene family expressed during the asexual-sexual stage transition in Plasmodium falciparum. Mol Biochem Parasitol 143: 90-99. (Pubitemid 41039035)
20. Flueck C, Bartfai R, Volz J, Niederwieser I, Salcedo-Amaya AM, Alako BT, Ehlgen F, Ralph SA, Cowman AF, Bozdech Z, et al. 2009. Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 5: e1000569. doi: 10.1371/journal.ppat. 1000569.
21. Functional Genomics Workshop Group. 2007. Mechanisms of gene regulation in Plasmodium. Am J Trop Med Hyg 77: 201-208.
22. Ganesan K, Ponmee N, Jiang L, Fowble JW, White J, Kamchonwongpaisan S, Yuthavong Y, Wilairat P, Rathod PK. 2008. A genetically hard-wired metabolic transcriptome in Plasmodium falciparum fails to mount protective responses to lethal antifolates. PLoS Pathog 4: e1000214. doi: 10.1371/journal.ppat.1000214.
23. Gomez-Escobar N, Amambua-Ngwa A, Walther M, Okebe J, Ebonyi A, Conway DJ. 2010. Erythrocyte invasion and merozoite ligand gene expression in severe andmild Plasmodium falciparum malaria. J Infect Dis 201: 444-452.
24. Gonzales JM, Patel JJ, PonmeeN, Jiang L, Tan A, Maher SP, Wuchty S, Rathod PK, Ferdig MT. 2008. Regulatory hotspots in the malaria parasite genome dictate transcriptional variation. PLoS Biol 6: e238. doi: 10.1371/journal.pbio. 0060238.
25. Grewal SI, Jia S. 2007. Heterochromatin revisited. Nat Rev Genet 8: 35-46. (Pubitemid 46006048)
26. Gunasekera AM, Myrick A, Le Roch K, Winzeler E, Wirth DF. 2007. Plasmodium falciparum: Genome wide perturbations in transcript profiles among mixed stage cultures after chloroquine treatment. Exp Parasitol 117: 87-92. (Pubitemid 47102295)
27. Hayton K, Gaur D, Liu A, Takahashi J, Henschen B, Singh S, Lambert L, Furuya T, Bouttenot R, Doll M, et al. 2008. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4: 40-51. (Pubitemid 351958114)
28. Hu G, Llinas M, Li J, Preiser PR, Bozdech Z. 2007. Selection of long oligonucleotides for gene expression microarrays using weighted ranksum strategy. BMC Bioinformatics 8: 350. doi: 10.1186/1471-2105-8-350.
29. Hu G, Cabrera A, Kono M, Mok S, Chaal BK, Haase S, Engelberg K, Cheemadan S, Spielmann T, Preiser PR, et al. 2010. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat Biotechnol 28: 91-98.
30. Jeffares DC, Pain A, Berry A, Cox AV, Stalker J, Ingle CE, Thomas A, Quail MA, Siebenthall K, Uhlemann AC, et al. 2007. Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet 39: 120-125. (Pubitemid 46026511)
31. Jiang L, Lopez-Barragan MJ, Jiang H, Mu J, Gaur D, Zhao K, Felsenfeld G, Miller LH. 2010. Epigenetic control of the variable expression of a Plasmodium falciparum receptor protein for erythrocyte invasion. Proc Natl Acad Sci 107: 2224-2229.
32. Kussell E, Leibler S. 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078. (Pubitemid 41362330)
33. Lavazec C, Sanyal S, Templeton TJ. 2007. Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodiumfalciparum. Mol Microbiol 64: 1621-1634. (Pubitemid 46889912)
34. Lemieux JE, Gomez-Escobar N, Feller A, Carret C, Amambua-Ngwa A, Pinches R, Day F, Kyes SA, Conway DJ, Holmes CC, et al. 2009. Statistical estimation of cell-cycle progression and lineage commitment in Plasmodium falciparum reveals a homogeneous pattern of transcription in ex vivo culture. Proc Natl Acad Sci 106: 7559-7564.
35. Le Roch KG, Johnson JR, Ahiboh H, Chung DW, Prudhomme J, Plouffe D, Henson K, Zhou Y, Witola W, Yates JR, et al. 2008. A systematic approach to understand themechanism of action of the bisthiazolium compound T4 on the human malaria parasite, Plasmodium falciparum. BMC Genomics 9: 513. doi: 10.1186/1471-2164-9-513.
36. 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: 1166-1173.
37. Lopez-Rubio JJ, Gontijo AM, Nunes MC, Issar N, Hernandez Rivas R, Scherf A. 2007. 59 flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol 66: 1296-1305. (Pubitemid 350179681)
38. Lopez-Rubio JJ, Mancio-Silva L, Scherf A. 2009. Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites. Cell Host Microbe 5: 179-190.
39. Mackinnon MJ, Marsh K. 2010. The selection landscape of malaria parasites. Science 328: 866-871.
40. Mackinnon MJ, Li J, Mok S, Kortok MM, Marsh K, Preiser PR, Bozdech Z. 2009. Comparative transcriptional and genomic analysis of Plasmodium falciparum field isolates. PLoS Pathog 5: e1000644. doi: 10.1371/journal.ppat.1000644.
41. Merrick CJ, Duraisingh MT. 2010. Epigenetics in Plasmodium: what do we really know? Eukaryot Cell 9: 1150-1158.
42. 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: 184-192. (Pubitemid 46054214)
43. Mu J, Awadalla P, Duan J, McGee KM, Keebler J, Seydel K, McVean GA, Su XZ. 2007. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet 39: 126-130. (Pubitemid 46026512)
44. Mu J, Myers RA, Jiang H, Liu S, Ricklefs S, Waisberg M, Chotivanich K, Wilairatana P, Krudsood S, White NJ, et al. 2010. Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat Genet 42: 268-271.
45. Natalang O, Bischoff E, Deplaine G, Proux C, Dillies MA, Sismeiro O, Guigon G, Bonnefoy S, Patarapotikul J, Mercereau-Puijalon O, et al. 2008. Dynamic RNA profiling in Plasmodium falciparum synchronized blood stages exposed to lethal doses of artesunate. BMC Genomics 9: 388. doi: 10.1186/1471-2164-9- 388.
46. Ndonwi M, Burlingame OO, Miller AS, Tollefsen DM, Broze GJ Jr, Goldberg DE. 2011. Inhibition of antithrombin by Plasmodium falciparum histidine-rich protein II. Blood 117: 6347-6354.
47. Nguitragool W, Bokhari AA, Pillai AD, Rayavara K, Sharma P, Turpin B, Aravind L, Desai SA. 2011. Malaria parasite clag3 genes determine channel-mediated nutrient uptake by infected red blood cells. Cell 145: 665-677.
48. Nunes MC, Goldring JP, Doerig C, Scherf A. 2007. A novel protein kinase family in Plasmodium falciparum is differentially transcribed and secreted to various cellular compartments of the host cell. Mol Microbiol 63: 391-403. (Pubitemid 46058927)
49. Oakley MS, Kumar S, Anantharaman V, Zheng H, Mahajan B, Haynes JD, Moch JK, Fairhurst R, McCutchan TF, Aravind L. 2007. Molecular factors and biochemical pathways induced by febrile temperature in intraerythrocytic Plasmodium falciparum parasites. Infect Immun 75: 2012-2025. (Pubitemid 46559471)
50. Ochola LI, Tetteh KK, Stewart LB, Riitho V, Marsh K, Conway DJ. 2010. Allele frequency-based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol Biol Evol 27: 2344-2351.
51. Petter M, Haeggstrom M, Khattab A, Fernandez V, Klinkert MQ, Wahlgren M. 2007. Variant proteins of the Plasmodium falciparum RIFIN family show distinct subcellular localization and developmental expression patterns. Mol Biochem Parasitol 156: 51-61. (Pubitemid 47348143)
52. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat Biotechnol 29: 24-26.
53. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. 2006. TM4 microarray software suite. Methods Enzymol 411: 134-193.
54. Salcedo-Amaya AM, van Driel MA, Alako BT, Trelle MB, van den Elzen AM, Cohen AM, Janssen-Megens EM, van de Vegte-Bolmer M, Selzer RR, Iniguez AL, et al. 2009. Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum. Proc Natl Acad Sci 106: 9655-9660.
55. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, Speed TP, Cowman AF. 2006. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 7: R12. doi: 10.1186/gb-2006-7-2-r12.
56. Scherf A, Lopez-Rubio JJ, Riviere L. 2008. Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62: 445-470.
57. Spielmann T, Fergusen DJ, Beck HP. 2003. etramps, a new Plasmodium falciparum gene family coding for developmentally regulated and highly charged membrane proteins located at the parasite-host cell interface. Mol Biol Cell 14: 1529-1544. (Pubitemid 36547420)
58. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci 102: 15545-15550. (Pubitemid 41528093)
59. Tamez PA, Bhattacharjee S, van Ooij C, Hiller NL, Llinas M, Balu B, Adams JH, Haldar K. 2008. An erythrocyte vesicle protein exported by the malaria parasite promotes tubovesicular lipid import from the host cell surface. PLoS Pathog 4: e1000118. doi: 10.1371/journal.ppat.1000118.
60. Tellez M, Matesanz F, Alcina A. 2003. The C-terminal domain of the Plasmodium falciparum acyl-CoA synthetases PfACS1 and PfACS3 functions as ligand for ankyrin. Mol Biochem Parasitol 129: 191-198. (Pubitemid 36794571)
61. Templeton TJ. 2009. The varieties of gene amplification, diversification and hypervariability in the human malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 166: 109-116.
62. Templeton TJ, Kaslow DC. 1999. Identification of additional members define a Plasmodium falciparum gene superfamily which includes Pfs48/45 and Pfs230. Mol Biochem Parasitol 101: 223-227. (Pubitemid 29257855)
63. Trojer P, Reinberg D. 2007. Facultative heterochromatin: is there a distinctive molecular signature? Mol Cell 28: 1-13. (Pubitemid 47531977)
64. Van Tyne D, Park DJ, Schaffner SF, Neafsey DE, Angelino E, Cortese JF, Barnes KG, Rosen DM, Lukens AK, Daniels RF, et al. 2011. Identification and functional validation of the novel antimalarial resistance locus PF10-0355 in Plasmodium falciparum. PLoS Genet 7: e1001383. doi: 10.1371/journal.pgen. 1001383.
65. Veening JW, Smits WK, Kuipers OP. 2008. Bistability, epigenetics, and bethedging in bacteria. Annu Rev Microbiol 62: 193-210.
66. Volkman SK, Sabeti PC, DeCaprio D, Neafsey DE, Schaffner SF, Milner DA Jr, Daily JP, Sarr O, Ndiaye D, Ndir O, et al. 2007. A genome-wide map of diversity in Plasmodium falciparum. Nat Genet 39: 113-119. (Pubitemid 46026510)
67. Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, London WT, Corcoran LM, Burkot TR, Carter R. 1987. Genetic analysis of the human malaria parasite Plasmodium falciparum. Science 236: 1661-1666. (Pubitemid 17091020)
68. Winter G, Kawai S, Haeggstrom M, Kaneko O, von Euler A, Kawazu S, Palm D, Fernandez V, Wahlgren M. 2005. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med 201: 1853-1863. (Pubitemid 41002903)
69. Young JA, Johnson JR, Benner C, Yan SF, Chen K, Le Roch KG, Zhou Y, Winzeler EA. 2008. In silico discovery of transcription regulatory elements in Plasmodium falciparum. BMC Genomics 9: 70. doi: 10.1186/1471-2164-9-70.