Recent progress in functional genomic research in Plasmodium falciparum

Current Genomics

Volumn 11, Issue 4, 2010, Pages 279-286

  Mu, Jianbing ^a   Seydel, Karl B ^b   Bates, Adam ^a   Su, Xin Zhuan ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Comparative genomics; Genome diversity; Malaria; Microarray; Recombination; SNP

Indexed keywords

ARTICLE; DRUG SENSITIVITY; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE FUNCTION; GENE MAPPING; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; SPECIES COMPARISON; VIRULENCE;

PLASMODIUM FALCIPARUM;

EID: 77953665105     PISSN: 13892029     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920210791233081     Document Type: Article

References (107)

1. Miller, L.H.; Baruch, D.I.; Marsh, K.; Doumbo, O.K. The pathogenic basis of malaria. Nature, 2002, 415, 673-679.
2. White, NJ. Plasmodium knowlesi: the fifth human malaria parasite. Clin. Infect. Dis., 2008, 46, 172-173.
3. Pain, A.; Hertz-Fowler, C. Plasmodium genomics: latest milestone. Nat. Rev. Microbiol., 2009, 7, 180-181.
4. Aravind, L.; Iyer, L.M.; Wellems, T.E.; Miller, L.H. Plasmodium biology: genomic gleanings. Cell, 2003, 115, 771-785.
5. 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, M.; Barrell, B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, 2002, 419, 498-511.
6. Lu, F.; Jiang, H.; Ding, J.; Mu, J.; Valenzuela, J.G.; Ribeiro, J.M.; Su, X.Z. cDNA sequences reveal considerable gene prediction inaccuracy in the Plasmodium falciparum genome. BMC Genomics, 2007, 8, 255.
7. Wakaguri, H.; Suzuki, Y.; Katayama, T.; Kawashima, S.; Kibukawa, E.; Hiranuka, K.; Sasaki, M.; Sugano, S.; Watanabe, J. Full-Malaria/Parasites and Full-Arthropods: databases of full-length cDNAs of parasites and arthropods, update 2009. Nucleic Acids Res., 2009, 37(Database issue), D520-525.
8. Anderson, T.J. Mapping drug resistance genes in Plasmodium falciparum by genome-wide association. Curr. Drug Targets Infect. Disord., 2004, 4, 65-78.
9. Su, X.; Hayton, K.; Wellems, T.E. Genetic linkage and association analyses for trait mapping in Plasmodium falciparum. Nat. Rev. Genet., 2007, 8, 497-506.
10. Su, X.; Kirkman, L.A.; Fujioka, H.; Wellems, T.E. Complex polymorphisms in an approximately 330 kDa protein are linked to chloroquine-resistant P. falciparum in Southeast Asia and Africa. Cell, 1997, 91, 593-603.
11. Fidock, D.A.; Nomura, T.; Talley, A.K.; Cooper, R.A.; Dzekunov, S.M.; Ferdig, M.T.; Ursos, L.M.; Sidhu, A.B.; Naude, B.; Deitsch, K.W.; Su, X.Z.; Wootton, J.C.; Roepe, P.D.; Wellems, T.E. Mutations in the P. falciparum digestive vacuole transmembrane protein PfCRT and evidence for their role in chloroquine resistance. Mol. Cell, 2000, 6, 861-871.
12. Wellems, T.E.; Panton, L.J.; Gluzman, I.Y.; do Rosario, V.E.; Gwadz, R.W.; Walker-Jonah, A.; Krogstad, D.J. Chloroquine resistance not linked to mdr-like genes in a Plasmodium falciparum cross. Nature, 1990, 345, 253-255.
13. Peterson, D.S.; Walliker, D.; Wellems, T.E. Evidence that a point mutation in dihydrofolate reductase-thymidylate synthase confers resistance to pyrimethamine in falciparum malaria. Proc. Natl. Acad. Sci. USA, 1988, 85, 9114-9118.
14. Hayton, K.; Gaur, D.; Liu, A.; Takahashi, J.; Henschen, B.; Singh, S.; Lambert, L.; Furuya, T.; Bouttenot, R.; Doll, M.; Nawaz, F.; Mu, J.; Jiang, L.; Miller, L.H.; Wellems, T.E. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe, 2008, 4, 40-51.
15. Mu, J.; Duan, J.; Makova, K.D.; Joy, D.A.; Huynh, C.Q.; Branch, O.H.; Li, W.H.; Su, X.Z. Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature, 2002, 418, 323-326.
16. Mu, J.; Ferdig, M.T.; Feng, X.; Joy, D.A.; Duan, J.; Furuya, T.; Subramanian, G.; Aravind, L.; Cooper, R.A.; Wootton, J.C.; Xiong, M.; Su, X.Z. Multiple transporters associated with malaria parasite responses to chloroquine and quinine. Mol. Microbiol., 2003, 49, 977-989.
17. Jeffares, D.C.; Pain, A.; Berry, A.; Cox, A.V.; Stalker, J.; Ingle, C.E.; Thomas, A.; Quail, M.A.; Siebenthall, K.; Uhlemann, A.C.; Kyes, S.; Krishna, S.; Newbold, C.; Dermitzakis, E.T.; Berriman, M. Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat. Genet., 2007, 39, 120-125.
18. Volkman, S.K.; Sabeti, P.C.; DeCaprio, D.; Neafsey, D.E.; Schaffner, S.F.; Milner, D.A. Jr., Daily, J.P.; Sarr, O.; Ndiaye, D.; Ndir, O.; Mboup, S.; Duraisingh, M.T.; Lukens, A.; Derr, A.; Stange-Thomann, N.; Waggoner, S.; Onofrio, R.; Ziaugra, L.; Mauceli, E.; Gnerre, S.; Jaffe, D.B.; Zainoun, J.; Wiegand, R.C.; Birren, B.W.; Hartl, D.L.; Galagan, J.E.; Lander, E.S.; Wirth, D.F. A genome-wide map of diversity in Plasmodium falciparum. Nat. Genet., 2007, 39, 113-119.
19. Carlton, J.M.; Escalante, A.A.; Neafsey, D.; Volkman, S.K. Comparative evolutionary genomics of human malaria parasites. TrendsParasitol., 2008, 24, 545-550.
20. Kidgell, C.; Volkman, S.K.; Daily, J.; Borevitz, J.O.; Plouffe, D.; Zhou, Y.; Johnson, J.R.; Le Roch, K.; Sarr, O.; Ndir, O.; Mboup, S.; Batalov, S.; Wirth, D.F.; Winzeler, E.A. A systematic map of genetic variation in Plasmodium falciparum. PLoS Pathog., 2006, 2, e57.
21. Jiang, H.; Yi, M.; Mu, J.; Zhang, L.; Ivens, A.; Klimczak, L.J.; Huyen, Y.; Stephens, R.M.; Su, X.Z. Detection of genome-wide polymorphisms in the AT-rich Plasmodium falciparum genome using a high-density microarray. BMC Genomics, 2008, 9, 398.
22. Bozdech, Z.; Mok, S.; Hu, G.; Imwong, M.; Jaidee, A.; Russell, B.; Ginsburg, H.; Nosten, F.; Day, N.P.; White, N.J.; Carlton, J.M.; Preiser, P.R. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc. Natl. Acad. Sci. USA, 2008, 105, 16290-16295.
23. 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, J.R. 3rd, Kafatos, F.C.; Janse, C.J.; Barrell, B.; Turner, M.; Waters, A. P.; Sinden, R.E. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science, 2005, 307, 82-86.
24. Dharia, N.V.; Sidhu, A.B.; Cassera, M.B.; Westenberger, S.J.; Bopp, S.E.; Eastman, R.T.; Plouffe, D.; Batalov, S.; Park, D.J.; Volkman, S.K.; Wirth, D.F.; Zhou, Y.; Fidock, D.A.; Winzeler, E.A. Use of high-density tiling microarrays to identify mutations globally and elucidate mechanisms of drug resistance in Plasmodium falciparum. Genome Biol., 2009, 10, R21.
25. Mu, J.; Myers, R.A.; Jiang, H.; Liu, S.; Ricklefs, S.; Waisberg, M.; Chotivanich, K.; Wilairatana, P.; Krudsood, S.; White, N.J.; Udomsangpetch, R.; Cui, L.; Ho, M.; Ou, F.; Li, H.; Song, J.; Li, G.; Wang, X.; Seila, S.; Sokunthea, S.; Socheat, D.; Sturdevant, E.; Porcella, S.F.; Fairhurst, R.M.; Wellems, T.E.; Awadalla, P.; Su, X.Z. Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat. Genet., 2010, 42(3), 268-71.
26. Mu, J.; Awadalla, P.; Duan, J.; McGee, K.; Joy, D.; McVean, G.; Su, X.-Z. Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol., 2005, 3, e335.
27. Neafsey, D.E.; Schaffner, S.F.; Volkman, S.K.; Park, D.; Montgomery, P.; Milner, D.A. Jr., Lukens, A.; Rosen, D.; Daniels, R.; Houde, N.; Cortese, J.F.; Tyndall, E.; Gates, C.; Stange-Thomann, N.; Sarr, O.; Ndiaye, D.; Ndir, O.; Mboup, S.; Ferreira, M.U.; Moraes Sdo, L.; Dash, A.P.; Chitnis, C.E.; Wiegand, R.C.; Hartl, D.L.; Birren, B.W.; Lander, E.S.; Sabeti, P.C.; Wirth, D.F. Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol., 2008, 9, R171.
28. Duan, J.; Mu, J.; Thera, M.A.; Joy, D.; Kosakovsky Pond, S.L.; Diemert, D.; Long, C.; Zhou, H.; Miura, K.; Ouattara, A.; Dolo, A.; Doumbo, O.; Su, X.Z.; Miller, L. Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen 1: Implications for vaccine design. Proc. Natl.Acad. Sci. USA, 2008, 105(22), 7857-62.
29. Voight, B.F.; Kudaravalli, S.; Wen, X.; Pritchard, J.K. A map of recent positive selection in the human genome. PLoS Biol., 2006, 4, e72.
30. Sabeti, P.C.; Varilly, P.; Fry, B.; Lohmueller, J.; Hostetter, E.; Cotsapas, C.; Xie, X.; Byrne, E.H.; McCarroll, S.A.; Gaudet, R.; Schaffner, S.F.; Lander, E.S. Genome-wide detection and characterization of positive selection in human populations. Nature, 2007, 449, 913-918.
31. Hurst, L.D. Fundamental concepts in genetics: Genetics and the understanding of selection. Nat. Rev. Genet., 2009, 10(2), 83-93.
32. Wootton, J.C.; Feng, X.; Ferdig, M.T.; Cooper, R.A.; Mu, J.; Baruch, D.I.; Magill, A.J.; Su, X.Z. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature, 2002, 418, 320-323.
33. Nash, D.; Nair, S.; Mayxay, M.; Newton, P.N.; Guthmann, J.P.; Nosten, F.; Anderson, T.J. Selection strength and hitchhiking around two anti-malarial resistance genes. Proc. Biol. Sci., 2005, 272, 1153-1161.
34. Mu, J.; Awadalla, P.; Duan, J.; McGee, K.M.; Keebler, J.; Seydel, K.; McVean, G.A.; Su, X.Z. Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat. Genet., 2007, 39, 126-130.
35. Henrichsen, C.N.; Chaignat, E.; Reymond, A. Copy number variants, diseases and gene expression. Hum. Mol. Genet., 2009, 18, R1-8.
36. Anderson, T.J.; Patel, J.; Ferdig, M.T. Gene copy number and malaria biology. Trends Parasitol., 2009, 25, 336-343.
37. Price, R.N.; Uhlemann, A.C.; Brockman, A.; McGready, R.; Ashley, E.; Phaipun, L.; Patel, R.; Laing, K.; Looareesuwan, S.; White, N.J.; Nosten, F.; Krishna, S. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet, 2004, 364, 438-447.
38. Nair, S.; Miller, B.; Barends, M.; Jaidee, A.; Patel, J.; Mayxay, M.; Newton, P.; Nosten, F.; Ferdig, M.T.; Anderson, T.J. Adaptive copy number evolution in malaria parasites. PLoS Genet., 2008, 4, e1000243.
39. Yuan, J.; Johnson, R.L.; Huang, R.; Wichterman, J.; Jiang, H.; Hayton, K.; Fidock, D.A.; Wellems, T.E.; Inglese, J.; Austin, C.P.; Su, X.Z. Genetic mapping of targets mediating differential chemical phenotypes in Plasmodium falciparum. Nat. Chem. Biol., 2009, 5, 765-771.
40. Chakrabarti, K.; Pearson, M.; Grate, L.; Sterne-Weiler, T.; Deans, J.; Donohue, J.P.; Ares, M. Jr. Structural RNAs of known and unknown function identified in malaria parasites by comparative genomics and RNA analysis. RNA, 2007, 13, 1923-1939.
41. Mourier, T.; Carret, C.; Kyes, S.; Christodoulou, Z.; Gardner, P.P.; Jeffares, D.C.; Pinches, R.; Barrell, B.; Berriman, M.; Griffiths-Jones, S.; Ivens, A.; Newbold, C.; Pain, A. Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res., 2008, 18, 281-292.
42. Hertel, J.; Stadler, P. F. Hairpins in a Haystack: recognizing microRNA precursors in comparative genomics data. Bioinformatics, 2006, 22, e197-202.
43. Iyer, J.; Gruner, A.C.; Renia, L.; Snounou, G.; Preiser, P.R. Invasion of host cells by malaria parasites: a tale of two protein families. Mol. Microbiol., 2007, 65, 231-249.
44. Cowman, A.F.; Crabb, B.S. Invasion of red blood cells by malaria parasites. Cell, 2006, 124, 755-766.
45. Gaur, D.; Mayer, D.C.; Miller, L.H. Parasite ligand-host receptor interactions during invasion of erythrocytes by Plasmodium merozoites. Int. J. Parasitol., 2004, 34, 1413-1429.
46. Singh, S.; Plassmeyer, M.; Gaur, D.; Miller, L.H. Mononeme: a new secretory organelle in Plasmodium falciparum merozoites identified by localization of rhomboid-1 protease. Proc. Natl. Acad. Sci. USA, 2007, 104, 20043-20048.
47. Yeoh, S.; O'Donnell, R.A.; Koussis, K.; Dluzewski, A.R.; Ansell, K.H.; Osborne, S.A.; Hackett, F.; Withers-Martinez, C.; Mitchell, G.H.; Bannister, L.H.; Bryans, J.S.; Kettleborough, C.A.; Blackman, M.J. Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell, 2007, 131, 1072-1083.
48. Blackman, M.J. Malarial proteases and host cell egress: an 'emerging' cascade. Cell Microbiol., 2008, 10, 1925-1934.
49. 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.
50. De Silva, E.K.; Gehrke, A.R.; Olszewski, K.; Leon, I.; Chahal, J.S.; Bulyk, M.L.; Llinas, M. Specific DNA-binding by apicomplexan AP2 transcription factors. Proc. Natl. Acad. Sci. USA, 2008, 105, 8393-8398.
51. Aurrecoechea, C.; Brestelli, J.; Brunk, B.P.; Dommer, J.; Fischer, S.; Gajria, B.; Gao, X.; Gingle, A.; Grant, G.; Harb, O.S.; Heiges, M.; Innamorato, F.; Iodice, J.; Kissinger, J.C.; Kraemer, E.; Li, W.; Miller, J.A.; Nayak, V.; Pennington, C.; Pinney, D.F.; Roos, D.S.; Ross, C.; Stoeckert, C.J. Jr., Treatman, C.; Wang, H. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res., 2009, 37(Database issue), D539-543.
52. Young, J.A.; Johnson, J.R.; Benner, C.; Yan, S.F.; Chen, K.; Le Roch, K.G.; Zhou, Y.; Winzeler, E.A. In silico discovery of transcription regulatory elements in Plasmodium falciparum. BMC Genomics, 2008, 9, 70.
53. Hiller, N.L.; Bhattacharjee, S.; van Ooij, C.; Liolios, K.; Harrison, T.; Lopez-Estrano, C.; Haldar, K. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science, 2004, 306, 1934-1937.
54. Marti, M.; Good, R.T.; Rug, M.; Knuepfer, E.; Cowman, A.F. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science, 2004, 306, 1930-1933.
55. Maier, A.G.; Rug, M.; O'Neill, M.T.; Brown, M.; Chakravorty, S.; Szestak, T.; Chesson, J.; Wu, Y.; Hughes, K.; Coppel, R.L.; Newbold, C.; Beeson, J.G.; Craig, A.; Crabb, B.S.; Cowman, A.F. Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell, 2008, 134, 48-61.
56. Maier, A.G.; Cooke, B.M.; Cowman, A.F.; Tilley, L. Malaria parasite proteins that remodel the host erythrocyte. Nat. Rev. Microbiol., 2009, 7, 341-354.
57. van Ooij, C.; Tamez, P.; Bhattacharjee, S.; Hiller, N.L.; Harrison, T.; Liolios, K.; Kooij, T.; Ramesar, J.; Balu, B.; Adams, J.; Waters, P.; Janse, C.J.; Haldar, K. The malaria secretome: from algorithms to essential function in blood stage infection. PLoS Pathog., 2008, 4, e1000084.
58. de Koning-Ward, T.F.; Gilson, P.R.; Boddey, J.A.; Rug, M.; Smith, J.; Papenfuss, A.T.; Sanders, P.R.; Lundie, R.J.; Maier, A.G.; Cowman, A.F.; Crabb, B.S. A newly discovered protein export machine in malaria parasites. Nature, 2009, 459, 945-949.
59. Cui, L.; Fan, Q.; Miao, J. Histone lysine methyltransferases and demethylases in Plasmodium falciparum. Int. J. Parasitol., 2008, 38, 1083-1097.
60. Cui, L.; Miao, J.; Furuya, T.; Fan, Q.; Li, X.; Rathod, P.K.; Su, X.Z. Histone acetyltransferase inhibitor anacardic acid causes changes in global gene expression during in vitro Plasmodium falciparum development. Eukaryot. Cell, 2008, 7, 1200-1210.
61. Fan, Q.; Miao, J.; Cui, L.; Cui, L. Characterization of protein arginine methyltransferase I from Plasmodium falciparum. Biochem. J., 2009, 421(1), 107-18.
62. 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.; Winzeler, E.A. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science, 2003, 301, 1503-1508.
63. Zhou, Y.; Young, J.A.; Santrosyan, A.; Chen, K.; Yan, S.F.; Winzeler, E.A. In silico gene function prediction using ontology-based pattern identification. Bioinformatics, 2005, 21, 1237-1245.
64. Zhou, Y.; Ramachandran, V.; Kumar, K.A.; Westenberger, S.; Refour, P.; Zhou, B.; Li, F.; Young, J.A.; Chen, K.; Plouffe, D.; Henson, K.; Nussenzweig, V.; Carlton, J.; Vinetz, J.M.; Duraisingh, M.T.; Winzeler, E.A. Evidence-based annotation of the malaria parasite's genome using comparative expression profiling. PLoS ONE, 2008, 3, e1570.
65. Hu, G.; Cabrera, A.; Kono, M.; Mok, S.; Chaal, B.K.; Haase, S.; Engelberg, K.; Cheemadan, S.; Spielmann, T.; Preiser, P.R.; Gilberger, T.W.; Bozdech, Z. Transcriptional profiling of growth perturbations of the human malaria parasite Plasmodium falciparum. Nat. Biotechnol., 2010, 28, 91-98.
66. Bozdech, Z.; Llinas, M.; Pulliam, B.L.; Wong, E.D.; Zhu, J.; DeRisi, J.L. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol., 2003, 1, E5.
67. Llinas, M.; Bozdech, Z.; Wong, E.D.; Adai, A.T.; DeRisi, J.L. Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res., 2006, 34, 1166-1173.
68. Daily, J.P.; Scanfeld, D.; Pochet, N.; Le Roch, K.; Plouffe, D.; Kamal, M.; Sarr, O.; Mboup, S.; Ndir, O.; Wypij, D.; Levasseur, K.; Thomas, E.; Tamayo, P.; Dong, C.; Zhou, Y.; Lander, E.S.; Ndiaye, D.; Wirth, D.; Winzeler, E.A.; Mesirov, J.P.; Regev, A. Distinct physiological states of Plasmodium falciparum in malaria-infected patients. Nature, 2007, 450, 1091-1095.
69. Gonzales, J.M.; Patel, J.J.; Ponmee, N.; Jiang, L.; Tan, A.; Maher, S.P.; Wuchty, S.; Rathod, P.K.; Ferdig, M.T. Regulatory hotspots in the malaria parasite genome dictate transcriptional variation. PLoS Biol., 2008, 6, e238.
70. Huang, Y.; Wuchty, S.; Ferdig, M.T.; Przytycka, T.M. Graph theoretical approach to study eQTL: a case study of Plasmodium falciparum. Bioinformatics, 2009, 25, i15-20.
71. Lemieux, J.E.; Gomez-Escobar, N.; Feller, A.; Carret, C.; Amambua-Ngwa, A.; Pinches, R.; Day, F.; Kyes, S.A.; Conway, D.J.; Holmes, C.C.; Newbold, C.I. 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. USA, 2009, 106, 7559-7564.
72. Jiang, H.; Patel, J.J.; Yi, M.; Mu, J.; Ding, J.; Stephens, R.; Cooper, R.A.; Ferdig, M.T.; Su, X.Z. Genome-wide compensatory changes accompany drug- selected mutations in the Plasmodium falciparum crt gene. PLoS ONE, 2008, 3, e2484.
73. 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.
74. Gaur, D.; Furuya, T.; Mu, J.; Jiang, L.B.; Su, X.Z.; Miller, L.H. Upregulation of expression of the reticulocyte homology gene 4 in the Plasmodium falciparum clone Dd2 is associated with a switch in the erythrocyte invasion pathway. Mol. Biochem. Parasitol., 2006, 145, 205-215.
75. Eksi, S.; Haile, Y.; Furuya, T.; Ma, L.; Su, X.; Williamson, K.C. Identification of a subtelomeric gene family expressed during the asexual-sexual stage transition in Plasmodium falciparum. Mol. Biochem. Parasitol., 2005, 143, 90-99.
76. Deitsch, K. W. A mark of silence in malaria parasites. Cell Host Microbe, 2009, 5, 112-113.
77. Deitsch, K. W.; Lukehart, S.A.; Stringer, J.R. Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat. Rev. Microbiol., 2009, 7, 493-503.
78. Scherf, A.; Lopez-Rubio, J.J.; Riviere, L. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol., 2008, 62, 445-470.
79. Su, X.Z.; Heatwole, V.M.; Wertheimer, S.P.; Guinet, F.; Herrfeldt, J.A.; Peterson, D.S.; Ravetch, J.A.; Wellems, T.E. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell, 1995, 82, 89-100.
80. Chen, Q.; Fernandez, V.; Sundstrom, A.; Schlichtherle, M.; Datta, S.; Hagblom, P.; Wahlgren, M. Developmental selection of var gene expression in Plasmodium falciparum. Nature, 1998, 394, 392-395.
81. Chookajorn, T.; Dzikowski, R.; Frank, M.; Li, F.; Jiwani, A.Z.; Hartl, D.L.; Deitsch, K. W. Epigenetic memory at malaria virulence genes. Proc. Natl. Acad. Sci. USA, 2007, 704, 899-902.
82. 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, 727, 13-24.
83. 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.; Scherf, A. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell, 2005, 727, 25-36.
84. Deitsch, K.W.; Calderwood, M.S.; Wellems, T.E. Malaria. Cooperative silencing elements in var genes. Nature, 2001, 472, 875-876.
85. Gannoun-Zaki, L.; Jost, A.; Mu, J.; Deitsch, K.W.; Wellems, T.E. A silenced Plasmodium falciparum var promoter can be activated in vivo through spontaneous deletion of a silencing element in the intron. Eukaryot. Cell, 2005, 4, 490-492.
86. Lopez-Rubio, J.J.; Gontijo, A.M.; Nunes, M.C.; Issar, N.; Hernandez Rivas, 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.
87. 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.
88. 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.; Green, R.D.; Sauerwein, R.W.; Jensen, O.N.; Stunnenberg, H.G. Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA, 2009, 706, 9655-9660.
89. Chaal, B.K.; Gupta, A.P.; Wastuwidyaningtyas, B.D.; Luah, Y.H.; Bozdech, Z. Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoSPathog., 2010, 6, e1000737.
90. Florens, L.; Washburn, M.P.; Raine, J.D.; Anthony, R.M.; Grainger, M.; Haynes, J.D.; Moch, J.K.; Muster, N.; Sacci, J.B.; Tabb, D.L.; Witney, A.A.; Wolters, D.; Wu, Y.; Gardner, M.J.; Holder, A.A.; Sinden, R.E.; Yates, J.R.; Carucci, D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature, 2002, 479, 520-526.
91. Lasonder, E.; Ishihama, Y.; Andersen, J.S.; Vermunt, A.M.; Pain, A.; Sauerwein, R.W.; Eling, W.M.; Hall, N.; Waters, A.P.; Stunnenberg, H.G.; Mann, M. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature, 2002, 479, 537-542.
92. Cooper, R.A.; Carucci, D.J. Proteomic approaches to studying drug targets and resistance in Plasmodium. Curr. Drug Targets Infect. Disord., 2004, 4, 41-51.
93. Prieto, J.H.; Koncarevic, S.; Park, S.K.; Yates, J.; Becker, K. Large-Scale Differential Proteome Analysis in Plasmodium falciparum under Drug Treatment. PLoS ONE, 2008, 3, e4098.
94. Belli, S.I.; Walker, R.A.; Flowers, S.A. Global protein expression analysis in apicomplexan parasites: current status. Proteomics, 2005, 5, 918-924.
95. Lal, K.; Prieto, J.H.; Bromley, E.; Sanderson, S.J.; Yates, J.R. 3rd, Wastling, J.M.; Tomley, F.M.; Sinden, R.E. Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics, 2009, 9(5), 1142-51.
96. Tarun, A.S.; Peng, X.; Dumpit, R.F.; Ogata, Y.; Silva-Rivera, H.; Camargo, N.; Daly, T.M. Bergman, L.W.; Kappe, S.H. A combined transcriptome and proteome survey of malaria parasite liver stages. Proc. Natl. Acad. Sci. USA, 2008, 705, 305-310.
97. Lasonder, E.; Janse, C.J.; van Gemert, G.J.; Mair, G.R.; Vermunt, A.M.; Douradinha, B.G.; van Noort, V.; Huynen, M.A.; Luty, A.J.; Kroeze, H.; Khan, S.M.; Sauerwein, R.W.; Waters, A.P.; Mann, M.; Stunnenberg, H.G. Proteomic profiling of Plasmodium sporozoite maturation identifies new proteins essential for parasite development and infectivity. PLoS Pathog., 2008, 4, e1000195.
98. Khan, S.M.; Franke-Fayard, B.; Mair, G.R.; Lasonder, E.; Janse, C.J.; Mann, M.; Waters, A. P. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell, 2005, 727, 675-687.
99. 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(7), 3439-50.
100. Di Girolamo, F.; Raggi, C.; Birago, C.; Pizzi, E.; Lalle, M.; Picci, L.; Pace, T.; Bachi, A.; de Jong, J.; Janse, C.J.; Waters, A.P.; Sargiacomo, M.; Ponzi, M. Plasmodium lipid rafts contain proteins implicated in vesicular trafficking and signalling as well as members of the PIR superfamily, potentially implicated in host immune system interactions. Proteomics, 2008, 8, 2500-2513.
101. Singh, M.; Mukherjee, P.; Narayanasamy, K.; Arora, R.; Sen, S.D.; Gupta, S.; Natarajan, K.; Malhotra, P. Proteome analysis of plasmodium falciparum extracellular secretory antigens at asexual blood stages reveals a cohort of proteins with possible roles in immune modulation and signaling. Mol. Cell Proteomics, 2009, 8(9), 2102-18.
102. Olszewski, K.L.; Morrisey, J.M.; Wilinski, D.; Burns, J.M.; Vaidya, A.B.; Rabinowitz, J.D.; Llinas, M. Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe, 2009, 5, 191-199.
103. Tyagi, N.; Swapna, L.S.; Mohanty, S.; Agarwal, G.; Gowri, V.S.; Anamika, K.; Priya, M.L.; Krishnadev, O.; Srinivasan, N. Evolutionary divergence of Plasmodium falciparum: sequences, protein-protein interactions, pathways and processes. Infect. Disord. Drug Targets, 2009, 9, 257-271.
104. Bongfen, S.E.; Laroque, A.; Berghout, J.; Gros, P. Genetic and genomic analyses of host-pathogen interactions in malaria. Trends Parasitol., 2009, 25, 417-422.
105. Kafsack, B.F.; Llinas, M. Eating at the table of another: metabolomics of host-parasite interactions. Cell Host Microbe, 2010, 7, 90-99.
106. Balu, B.; Shoue, D.A.; Fraser, M.J. Jr., Adams, J.H. High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc. Natl. Acad. Sci. USA, 2005, 702, 16391-16396.
107. Janse, C.J.; Ramesar, J.; Waters, A.P. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat. Protoc., 2006, 7, 346-356.