Genome-Wide Identification of the Target Genes of AP2-O, a AP2-Family Transcription Factor

1. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, et al. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307 : 82–86. 15637271

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. 16040597

3. De Silva EK, Gehrke AR, Olszewski K, Leon I, Chahal JS, et al. (2008) Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci U S A 105 : 8393–8398. doi: 10.1073/pnas.0801993105 18541913

4. Reece-Hoyes JS, Deplancke B, Shingles J, Grove CA, Hope IA, et al. (2005) A compendium of Caenorhabditis elegans regulatory transcription factors: a resource for mapping transcription regulatory networks. Genome Biol 6: R110. 16420670

5. Adryan B, Teichmann SA (2006) FlyTF: a systematic review of site-specific transcription factors in the fruit fly Drosophila melanogaster. Bioinformatics 22 : 1532–1533. 16613907

6. Hughes TR, de Boer CG (2013) Mapping yeast transcriptional networks. Genetics 195 : 9–36. doi: 10.1534/genetics.113.153262 24018767

7. Yuda M, Iwanaga S, Shigenobu S, Mair GR, Janse CJ, et al. (2009) Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol 71 : 1402–1414. doi: 10.1111/j.1365-2958.2009.06609.x 19220746

8. Yuda M, Iwanaga S, Shigenobu S, Kato T, Kaneko I (2010) Transcription factor AP2-Sp and its target genes in malarial sporozoites. Mol Microbiol 75 : 854–863. doi: 10.1111/j.1365-2958.2009.07005.x 20025671

9. Kafsack BF, Rovira-Graells N, Clark TG, Bancells C, Crowley VM, et al. (2014) A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 507 : 248–252. doi: 10.1038/nature12920 24572369

10. Sinha A, Hughes KR, Modrzynska KK, Otto TD, Pfander C, et al. (2014) A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium. Nature 507 : 253–257. doi: 10.1038/nature12970 24572359

11. Iwanaga S, Kaneko I, Kato T, Yuda M (2012) Identification of an AP2-family protein that is critical for malaria liver stage development. PLoS One 7: e47557. doi: 10.1371/journal.pone.0047557 23144823

12. Cheng C, Min R, Gerstein M (2011) TIP: a probabilistic method for identifying transcription factor target genes from ChIP-seq binding profiles. Bioinformatics 27 : 3221–3227. doi: 10.1093/bioinformatics/btr552 22039215

13. Wu S, Wang J, Zhao W, Pounds S, Cheng C (2010) ChIP-PaM: an algorithm to identify protein-DNA interaction using ChIP-Seq data. Theor Biol Med Model 7 : 18. doi: 10.1186/1742-4682-7-18 20525272

14. Feng J, Liu T, Qin B, Zhang Y, Liu XS (2012) Identifying ChIP-seq enrichment using MACS. Nat Protocols 7 : 1728–1740. doi: 10.1038/nprot.2012.101 22936215

15. Mair GR, Braks JA, Garver LS, Wiegant JC, Hall N, et al. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313 : 667–669. 16888139

16. Lal K, Prieto JH, Bromley E, Sanderson SJ, Yates JR 3rd, et al. (2009) Characterisation of Plasmodium invasive organelles; an ookinete microneme proteome. Proteomics 9 : 1142–1151. doi: 10.1002/pmic.200800404 19206106

17. Patra KP, Johnson JR, Cantin GT, Yates JR 3rd, Vinetz JM (2008) Proteomic analysis of zygote and ookinete stages of the avian malaria parasite Plasmodium gallinaceum delineates the homologous proteomes of the lethal human malaria parasite Plasmodium falciparum. Proteomics 8 : 2492–2499. doi: 10.1002/pmic.200700727 18563747

18. Hall N, Carlton J (2005) Comparative genomics of malaria parasites. Curr Opin Genet Dev 15 : 609–613. 16182520

19. Ecker A, Bushell ES, Tewari R, Sinden RE (2008) Reverse genetics screen identifies six proteins important for malaria development in the mosquito. Mol Microbiol 70 : 209–220. doi: 10.1111/j.1365-2958.2008.06407.x 18761621

20. Gilk SD, Raviv Y, Hu K, Murray JM, Beckers CJ, et al. (2006) Identification of PhIL1, a novel cytoskeletal protein of the Toxoplasma gondii pellicle, through photosensitized labeling with 5-[125I]iodonaphthalene-1-azide. Eukaryot Cell 5 : 1622–1634. 17030994

21. Barkhuff WD, Gilk SD, Whitmarsh R, Tilley LD, Hunter C, et al. (2011) Targeted disruption of TgPhIL1 in Toxoplasma gondii results in altered parasite morphology and fitness. PLoS One 6: e23977. doi: 10.1371/journal.pone.0023977 21901148

22. Khater EI, Sinden RE, Dessens JT (2004) A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol 167 : 425–432. 15533999

23. Tremp AZ, Khater EI, Dessens JT (2008) IMC1b is a putative membrane skeleton protein involved in cell shape, mechanical strength, motility, and infectivity of malaria ookinetes. J Biol Chem 283 : 27604–27611. doi: 10.1074/jbc.M801302200 18650444

24. Tran JQ, Li C, Chyan A, Chung L, Morrissette NS (2012) SPM1 stabilizes subpellicular microtubules in Toxoplasma gondii. Eukaryot Cell 11 : 206–216. doi: 10.1128/EC.05161-11 22021240

25. Beck JR, Rodriguez-Fernandez IA, Cruz de Leon J, Huynh MH, Carruthers VB, et al. (2010) A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating parasite division. PLoS Pathog 6: e1001094. doi: 10.1371/journal.ppat.1001094 20844581

26. Poulin B, Patzewitz EM, Brady D, Silvie O, Wright MH, et al. (2013) Unique apicomplexan IMC sub-compartment proteins are early markers for apical polarity in the malaria parasite. Biol Open 2 : 1160–1170. doi: 10.1242/bio.20136163 24244852

27. Frenal K, Polonais V, Marq JB, Stratmann R, Limenitakis J, et al. (2010) Functional dissection of the apicomplexan glideosome molecular architecture. Cell Host Microbe 8 : 343–357. doi: 10.1016/j.chom.2010.09.002 20951968

28. Bullen HE, Tonkin CJ, O'Donnell RA, Tham WH, Papenfuss AT, et al. (2009) A novel family of Apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. J Biol Chem 284 : 25353–25363. doi: 10.1074/jbc.M109.036772 19561073

29. Tremp AZ, Dessens JT (2011) Malaria IMC1 membrane skeleton proteins operate autonomously and participate in motility independently of cell shape. J Biol Chem 286 : 5383–5391. doi: 10.1074/jbc.M110.187195 21098480

30. Kaiser K, Camargo N, Coppens I, Morrisey JM, Vaidya AB, et al. (2004) A member of a conserved Plasmodium protein family with membrane-attack complex/perforin (MACPF)-like domains localizes to the micronemes of sporozoites. Mol Biochem Parasitol 133 : 15–26. 14668008

31. Yuda M, Sawai T, Chinzei Y (1999) Structure and expression of an adhesive protein-like molecule of mosquito invasive-stage malarial parasite. J Exp Med 189 : 1947–1952. 10377190

32. Dessens JT, Siden-Kiamos I, Mendoza J, Mahairaki V, Khater E, et al. (2003) SOAP, a novel malaria ookinete protein involved in mosquito midgut invasion and oocyst development. Mol Microbiol 49 : 319–329. 12828632

33. Yuda M, Yano K, Tsuboi T, Torii M, Chinzei Y (2001) von Willebrand Factor A domain-related protein, a novel microneme protein of the malaria ookinete highly conserved throughout Plasmodium parasites. Mol Biochem Parasitol 116 : 65–72. 11463467

34. Hinds L, Green JL, Knuepfer E, Grainger M, Holder AA (2009) Novel putative glycosylphosphatidylinositol-anchored micronemal antigen of Plasmodium falciparum that binds to erythrocytes. Eukaryot Cell 8 : 1869–1879. doi: 10.1128/EC.00218-09 19820120

35. Kadota K, Ishino T, Matsuyama T, Chinzei Y, Yuda M (2004) Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci U S A 101 : 16310–16315. 15520375

36. Huber M, Cabib E, Miller LH (1991) Malaria parasite chitinase and penetration of the mosquito peritrophic membrane. Proc Natl Acad Sci U S A 88 : 2807–2810. 2011589

37. Kariu T, Ishino T, Yano K, Chinzei Y, Yuda M (2006) CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol 59 : 1369–1379. 16468982

38. Deligianni E, Morgan RN, Bertuccini L, Wirth CC, de Monerri NC, et al. (2013) A perforin-like protein mediates disruption of the erythrocyte membrane during egress of Plasmodium berghei male gametocytes. Cell Microbiol 15 : 1438–1455. doi: 10.1111/cmi.12131 23461714

39. Ishino T, Chinzei Y, Yuda M (2005) A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol 7 : 199–208. 15659064

40. Ecker A, Pinto SB, Baker KW, Kafatos FC, Sinden RE (2007) Plasmodium berghei: Plasmodium perforin-like protein 5 is required for mosquito midgut invasion in Anopheles stephensi. Exp Parasitol 116 : 504–508. 17367780

41. Kondos SC, Hatfaludi T, Voskoboinik I, Trapani JA, Law RH, et al. (2010) The structure and function of mammalian membrane-attack complex/perforin-like proteins. Tissue Antigens 76 : 341–351. doi: 10.1111/j.1399-0039.2010.01566.x 20860583

42. Marois E (2011) The multifaceted mosquito anti-Plasmodium response. Curr Opin Microbiol 14 : 429–435. doi: 10.1016/j.mib.2011.07.016 21802348

43. Molina-Cruz A, DeJong RJ, Charles B, Gupta L, Kumar S, et al. (2008) Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J Biol Chem 283 : 3217–3223. 18065421

44. Jortzik E, Becker K (2012) Thioredoxin and glutathione systems in Plasmodium falciparum. Int J Med Microbiol 302 : 187–194. doi: 10.1016/j.ijmm.2012.07.007 22939033

45. Vega-Rodriguez J, Franke-Fayard B, Dinglasan RR, Janse CJ, Pastrana-Mena R, et al. (2009) The glutathione biosynthetic pathway of Plasmodium is essential for mosquito transmission. PLoS Pathog 5: e1000302. doi: 10.1371/journal.ppat.1000302 19229315

46. Pastrana-Mena R, Dinglasan RR, Franke-Fayard B, Vega-Rodriguez J, Fuentes-Caraballo M, et al. (2010) Glutathione reductase-null malaria parasites have normal blood stage growth but arrest during development in the mosquito. J Biol Chem 285 : 27045–27056. doi: 10.1074/jbc.M110.122275 20573956

47. Srinivasan P, Fujioka H, Jacobs-Lorena M (2008) PbCap380, a novel oocyst capsule protein, is essential for malaria parasite survival in the mosquito. Cell Microbiol 10 : 1304–1312. doi: 10.1111/j.1462-5822.2008.01127.x 18248630

48. Zhang M, Fennell C, Ranford-Cartwright L, Sakthivel R, Gueirard P, et al. (2010) The Plasmodium eukaryotic initiation factor-2alpha kinase IK2 controls the latency of sporozoites in the mosquito salivary glands. J Exp Med 207 : 1465–1474. doi: 10.1084/jem.20091975 20584882

49. Ning J, Otto TD, Pfander C, Schwach F, Brochet M, et al. (2013) Comparative genomics in Chlamydomonas and Plasmodium identifies an ancient nuclear envelope protein family essential for sexual reproduction in protists, fungi, plants, and vertebrates. Genes Dev 27 : 1198–1215. doi: 10.1101/gad.212746.112 23699412

50. Bushell ES, Ecker A, Schlegelmilch T, Goulding D, Dougan G, et al. (2009) Paternal effect of the nuclear formin-like protein MISFIT on Plasmodium development in the mosquito vector. PLoS Pathog 5: e1000539. doi: 10.1371/journal.ppat.1000539 19662167

51. Ishino T, Orito Y, Chinzei Y, Yuda M (2006) A calcium-dependent protein kinase regulates Plasmodium ookinete access to the midgut epithelial cell. Mol Microbiol 59 : 1175–1184. 16430692

52. Tewari R, Straschil U, Bateman A, Bohme U, Cherevach I, et al. (2010) The systematic functional analysis of Plasmodium protein kinases identifies essential regulators of mosquito transmission. Cell Host Microbe 8 : 377–387. doi: 10.1016/j.chom.2010.09.006 20951971

53. Sebastian S, Brochet M, Collins MO, Schwach F, Jones ML, et al. (2012) A Plasmodium calcium-dependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe 12 : 9–19. doi: 10.1016/j.chom.2012.05.014 22817984

54. Segal E, Shapira M, Regev A, Pe'er D, Botstein D, et al. (2003) Module networks: identifying regulatory modules and their condition-specific regulators from gene expression data. Nat Genet 34 : 166–176. 12740579

55. 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 : 1–31. 17949725

56. Thorvaldsdottir H, Robinson JT, Mesirov JP (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14 : 178–192. doi: 10.1093/bib/bbs017 22517427

57. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137. doi: 10.1186/gb-2008-9-9-r137 18798982

58. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14 : 1188–1190. 15173120

59. Orosz F (2009) Apicortin, a unique protein, with a putative cytoskeletal role, shared only by apicomplexan parasites and the placozoan Trichoplax adhaerens. Infect Genet Evol 9 : 1275–1286. doi: 10.1016/j.meegid.2009.09.001 19778640

60. Peris L, Thery M, Faure J, Saoudi Y, Lafanechere L, et al. (2006) Tubulin tyrosination is a major factor affecting the recruitment of CAP-Gly proteins at microtubule plus ends. J Cell Biol 174 : 839–849. 16954346

61. Montagna GN, Buscaglia CA, Munter S, Goosmann C, Frischknecht F, et al. (2012) Critical role for heat shock protein 20 (HSP20) in migration of malarial sporozoites. J Biol Chem 287 : 2410–2422. doi: 10.1074/jbc.M111.302109 22139844