A Knockout Screen of ApiAP2 Genes Reveals Networks of Interacting Transcriptional Regulators Controlling the Plasmodium Life Cycle

Cell Host and Microbe

Volumn 21, Issue 1, 2017, Pages 11-22

  Modrzynska, Katarzyna ^a,b   Pfander, Claudia ^a   Chappell, Lia ^a   Yu, Lu ^a   Suarez, Catherine ^a,c   Dundas, Kirsten ^a   Gomes, Ana Rita ^a   Goulding, David ^a   Rayner, Julian C ^a   Choudhary, Jyoti ^a   Billker, Oliver ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

ap2 l; ap2 o; ap2 o2; ap2 o3; ap2 o4; ap2 sp; ap2 sp2; ap2 sp3; Apetala 2; oocyst

Indexed keywords

AP2 O PROTEIN; AP2 SP PROTEIN; APIAP2 PROTEIN; CIS ACTING ELEMENT; DNA BINDING PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APICOMPLEXA; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; FEMALE; GAMETOCYTE; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT GENE; MIDGUT; MOSQUITO; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYST; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; PROMOTER REGION; SPOROGENESIS; SPOROZOITE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; ANOPHELES; CYTOLOGY; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; MALARIA; PARASITOLOGY; PHYSIOLOGY; PROTEIN DOMAIN; TRANSMISSION;

ANIMALS; ANOPHELES; APICOMPLEXA; DNA-BINDING PROTEINS; FEMALE; GENE KNOCKOUT TECHNIQUES; LIFE CYCLE STAGES; MALARIA; MICE; OOCYSTS; PLASMODIUM BERGHEI; PROTEIN DOMAINS; PROTOZOAN PROTEINS;

EID: 85009872695     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.12.003     Document Type: Article

References (48)

1. Aly, A.S.I., Matuschewski, K., A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J. Exp. Med. 202 (2005), 225–230.
2. Ay, F., Bunnik, E.M., Varoquaux, N., Vert, J.-P., Noble, W.S., Le Roch, K.G., Multiple dimensions of epigenetic gene regulation in the malaria parasite Plasmodium falciparum: gene regulation via histone modifications, nucleosome positioning and nuclear architecture in P. falciparum. BioEssays 37 (2015), 182–194.
3. Bailey, T.L., DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27 (2011), 1653–1659.
4. 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. 33 (2005), 3994–4006.
5. Campbell, T.L., De Silva, E.K., Olszewski, K.L., Elemento, O., Llinás, M., Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite. PLoS Pathog., 6, 2010, e1001165.
6. Caro, F., Ahyong, V., Betegon, M., DeRisi, J.L., Genome-wide regulatory dynamics of translation in the Plasmodium falciparum asexual blood stages. eLife, 3, 2014, e04106.
7. De Silva, E.K., Gehrke, A.R., Olszewski, K., León, I., Chahal, J.S., Bulyk, M.L., Llinás, M., Specific DNA-binding by apicomplexan AP2 transcription factors. Proc. Natl. Acad. Sci. USA 105 (2008), 8393–8398.
8. Dessens, J.T., Mendoza, J., Claudianos, C., Vinetz, J.M., Khater, E., Hassard, S., Ranawaka, G.R., Sinden, R.E., Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect. Immun. 69 (2001), 4041–4047.
9. Elemento, O., Slonim, N., Tavazoie, S., A universal framework for regulatory element discovery across all genomes and data types. Mol. Cell 28 (2007), 337–350.
10. Flueck, C., Bartfai, R., Niederwieser, I., Witmer, K., Alako, B.T.F., 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., 6, 2010, e1000784.
11. Foth, B.J., Zhang, N., Chaal, B.K., Sze, S.K., Preiser, P.R., Bozdech, Z., Quantitative time-course profiling of parasite and host cell proteins in the human malaria parasite Plasmodium falciparum. Mol. Cell. Proteomics, 10, 2011, 006411.
12. Franke-Fayard, B., Djokovic, D., Dooren, M.W., Ramesar, J., Waters, A.P., Falade, M.O., Kranendonk, M., Martinelli, A., Cravo, P., Janse, C.J., Simple and sensitive antimalarial drug screening in vitro and in vivo using transgenic luciferase expressing Plasmodium berghei parasites. Int. J. Parasitol. 38 (2008), 1651–1662.
13. Gerstein, M.B., Kundaje, A., Hariharan, M., Landt, S.G., Yan, K.-K., Cheng, C., Mu, X.J., Khurana, E., Rozowsky, J., Alexander, R., et al. Architecture of the human regulatory network derived from ENCODE data. Nature 489 (2012), 91–100.
14. Gomes, A.R., Bushell, E., Schwach, F., Girling, G., Anar, B., Quail, M.A., Herd, C., Pfander, C., Modrzynska, K., Rayner, J.C., Billker, O., A genome-scale vector resource enables high-throughput reverse genetic screening in a malaria parasite. Cell Host Microbe 17 (2015), 404–413.
15. Iwanaga, S., Kaneko, I., Kato, T., Yuda, M., Identification of an AP2-family protein that is critical for malaria liver stage development. PLoS ONE, 7, 2012, e47557.
16. Janse, C.J., Franke-Fayard, B., Waters, A.P., Selection by flow-sorting of genetically transformed, GFP-expressing blood stages of the rodent malaria parasite, Plasmodium berghei. Nat. Protoc. 1 (2006), 614–623.
17. 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. 1 (2006), 346–356.
18. Kafsack, B.F.C., 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 507 (2014), 248–252.
19. Kaneko, I., Iwanaga, S., Kato, T., Kobayashi, I., Yuda, M., Genome-Wide Identification of the Target Genes of AP2-O, a Plasmodium AP2-Family Transcription Factor. PLoS Pathog., 11, 2015, e1004905.
20. 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 121 (2005), 675–687.
21. Laurentino, E.C., Taylor, S., Mair, G.R., Lasonder, E., Bartfai, R., Stunnenberg, H.G., Kroeze, H., Ramesar, J., Franke-Fayard, B., Khan, S.M., et al. Experimentally controlled downregulation of the histone chaperone FACT in Plasmodium berghei reveals that it is critical to male gamete fertility. Cell. Microbiol. 13 (2011), 1956–1974.
22. Levo, M., Segal, E., In pursuit of design principles of regulatory sequences. Nat. Rev. Genet. 15 (2014), 453–468.
23. Licausi, F., Ohme-Takagi, M., Perata, P., APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol. 199 (2013), 639–649.
24. López-Barragán, M.J., Lemieux, J., Quiñones, M., Williamson, K.C., Molina-Cruz, A., Cui, K., Barillas-Mury, C., Zhao, K., Su, X.Z., Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics, 12, 2011, 587.
25. Mair, G.R., Braks, J.A.M., Garver, L.S., Wiegant, J.C.A.G., Hall, N., Dirks, R.W., Khan, S.M., Dimopoulos, G., Janse, C.J., Waters, A.P., Regulation of sexual development of Plasmodium by translational repression. Science 313 (2006), 667–669.
26. Moon, R.W., Taylor, C.J., Bex, C., Schepers, R., Goulding, D., Janse, C.J., Waters, A.P., Baker, D.A., Billker, O., A cyclic GMP signalling module that regulates gliding motility in a malaria parasite. PLoS Pathog., 5, 2009, e1000599.
27. Oberstaller, J., Pumpalova, Y., Schieler, A., Llinás, M., Kissinger, J.C., The Cryptosporidium parvum ApiAP2 gene family: insights into the evolution of apicomplexan AP2 regulatory systems. Nucleic Acids Res. 42 (2014), 8271–8284.
28. Orito, Y., Ishino, T., Iwanaga, S., Kaneko, I., Kato, T., Menard, R., Chinzei, Y., Yuda, M., Liver-specific protein 2: a Plasmodium protein exported to the hepatocyte cytoplasm and required for merozoite formation. Mol. Microbiol. 87 (2013), 66–79.
29. Otto, T.D., Wilinski, D., Assefa, S., Keane, T.M., Sarry, L.R., Böhme, U., Lemieux, J., Barrell, B., Pain, A., Berriman, M., et al. New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol. Microbiol. 76 (2010), 12–24.
30. Otto, T.D., Böhme, U., Jackson, A.P., Hunt, M., Franke-Fayard, B., Hoeijmakers, W.A., Religa, A.A., Robertson, L., Sanders, M., Ogun, S.A., et al. A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol., 12, 2014, 86.
31. Paul, R.E., Coulson, T.N., Raibaud, A., Brey, P.T., Sex determination in malaria parasites. Science 287 (2000), 128–131.
32. Pfander, C., Anar, B., Schwach, F., Otto, T.D., Brochet, M., Volkmann, K., Quail, M.A., Pain, A., Rosen, B., Skarnes, W., et al. A scalable pipeline for highly effective genetic modification of a malaria parasite. Nat. Methods 8 (2011), 1078–1082.
33. Philip, N., Waters, A.P., Conditional Degradation of Plasmodium Calcineurin Reveals Functions in Parasite Colonization of both Host and Vector. Cell Host Microbe 18 (2015), 122–131.
34. Pino, P., Sebastian, S., Kim, E.A., Bush, E., Brochet, M., Volkmann, K., Kozlowski, E., Llinás, M., Billker, O., Soldati-Favre, D., A tetracycline-repressible transactivator system to study essential genes in malaria parasites. Cell Host Microbe 12 (2012), 824–834.
35. Sebastian, S., Brochet, M., Collins, M.O., Schwach, F., Jones, M.L., Goulding, D., Rayner, J.C., Choudhary, J.S., Billker, O., A Plasmodium calcium-dependent protein kinase controls zygote development and transmission by translationally activating repressed mRNAs. Cell Host Microbe 12 (2012), 9–19.
36. Shock, J.L., Fischer, K.F., DeRisi, J.L., Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biol., 8, 2007, R134.
37. 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 507 (2014), 253–257.
38. Stampfel, G., Kazmar, T., Frank, O., Wienerroither, S., Reiter, F., Stark, A., Transcriptional regulators form diverse groups with context-dependent regulatory functions. Nature 528 (2015), 147–151.
39. Sturm, A., Mollard, V., Cozijnsen, A., Goodman, C.D., McFadden, G.I., Mitochondrial ATP synthase is dispensable in blood-stage Plasmodium berghei rodent malaria but essential in the mosquito phase. Proc. Natl. Acad. Sci. USA 112 (2015), 10216–10223.
40. Tao, D., Ubaida-Mohien, C., Mathias, D.K., King, J.G., Pastrana-Mena, R., Tripathi, A., Goldowitz, I., Graham, D.R., Moss, E., Marti, M., Dinglasan, R.R., Sex-partitioning of the Plasmodium falciparum stage V gametocyte proteome provides insight into falciparum-specific cell biology. Mol. Cell. Proteomics 13 (2014), 2705–2724.
41. Tarun, A.S., Peng, X., Dumpit, R.F., Ogata, Y., Silva-Rivera, H., Camargo, N., Daly, T.M., Bergman, L.W., Kappe, S.H.I., A combined transcriptome and proteome survey of malaria parasite liver stages. Proc. Natl. Acad. Sci. USA 105 (2008), 305–310.
42. Turturice, B.A., Lamm, M.A., Tasch, J.J., Zalewski, A., Kooistra, R., Schroeter, E.H., Sharma, S., Kawazu, S., Kanzok, S.M., Expression of cytosolic peroxiredoxins in Plasmodium berghei ookinetes is regulated by environmental factors in the mosquito bloodmeal. PLoS Pathog., 9, 2013, e1003136.
43. 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, 9, 2008, 70.
44. Yu, M., Kumar, T.R.S., Nkrumah, L.J., Coppi, A., Retzlaff, S., Li, C.D., Kelly, B.J., Moura, P.A., Lakshmanan, V., Freundlich, J.S., et al. The fatty acid biosynthesis enzyme FabI plays a key role in the development of liver-stage malarial parasites. Cell Host Microbe 4 (2008), 567–578.
45. Yuda, M., Iwanaga, S., Shigenobu, S., Mair, G.R., Janse, C.J., Waters, A.P., Kato, T., Kaneko, I., Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol. Microbiol. 71 (2009), 1402–1414.
46. Yuda, M., Iwanaga, S., Shigenobu, S., Kato, T., Kaneko, I., Transcription factor AP2-Sp and its target genes in malarial sporozoites. Mol. Microbiol. 75 (2010), 854–863.
47. Yuda, M., Iwanaga, S., Kaneko, I., Kato, T., Global transcriptional repression: An initial and essential step for Plasmodium sexual development. Proc. Natl. Acad. Sci. USA 112 (2015), 12824–12829.
48. Zhou, Y., Ramachandran, V., Kumar, K.A., Westenberger, S., Refour, P., Zhou, B., Li, F., Young, J.A., Chen, K., Plouffe, D., et al. Evidence-based annotation of the malaria parasite's genome using comparative expression profiling. PLoS ONE, 3, 2008, e1570.