Zinc finger proteins of Plasmodium falciparum.

Plasmodium epigenetic regulator gene expression malaria transcription factor zinc finger protein

Journal

Cellular microbiology
ISSN: 1462-5822
Titre abrégé: Cell Microbiol
Pays: India
ID NLM: 100883691

Informations de publication

Date de publication:
12 2021
Historique:
revised: 19 07 2021
received: 29 04 2021
accepted: 24 07 2021
pubmed: 22 8 2021
medline: 14 1 2022
entrez: 21 8 2021
Statut: ppublish

Résumé

Zinc finger proteins (ZFPs) are a large diverse family of proteins with one or more zinc finger domains in which zinc is important in stabilising the domain. ZFPs can interact with DNA, RNA, lipids or even other proteins and therefore contribute to diverse cellular processes including transcriptional regulation, ubiquitin-mediated protein degradation, mRNA decay and stability. In this review, we provide the first comprehensive classification of ZFPs of the malaria parasite Plasmodium falciparum and provide a state of knowledge on the main ZFPs in the parasite, which include the C2H2, CCCH, RING finger and the PHD finger proteins. TAKE AWAYS: The Plasmodium falciparum genome encodes 170 putative Zinc finger proteins (ZFPs). The C2H2, CCCH, RING finger and PHD finger subfamilies of ZFPs are most represented. Known ZFP functions include the regulation of mRNA metabolism and proteostasis.

Identifiants

pubmed: 34418264
doi: 10.1111/cmi.13387
doi:

Substances chimiques

Proteins 0
DNA 9007-49-2

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13387

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : NG170/1-1
Organisme : Deutsche Forschungsgemeinschaft
ID : PR905/7-1
Organisme : Deutsche Forschungsgemeinschaft
ID : PR905/20-1
Organisme : Deutscher Akademischer Austauschdienst
ID : PhD scholarship

Informations de copyright

© 2021 The Authors. Cellular Microbiology published by John Wiley & Sons Ltd.

Références

Abbehausen, C. (2019). Zinc finger domains as therapeutic targets for metal-based compounds - an update. Metallomics, 11, 15-28.
Agrawal, S., Chung, D. W., Ponts, N., van Dooren, G. G., Prudhomme, J., Brooks, C. F., … Le Roch, K. G. (2013). An apicoplast localized ubiquitylation system is required for the import of nuclear-encoded plastid proteins. PLoS Pathogens, 9, e1003426.
Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., … Harb, O. S. (2009). PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Research, 37, D539-D543.
Baumgarten, S., Bryant, J. M., Sinha, A., Reyser, T., Preiser, P. R., Dedon, P. C., & Scherf, A. (2019). Transcriptome-wide dynamics of extensive m6A mRNA methylation during plasmodium falciparum blood-stage development. Nature Microbiology, 4, 2246-2259.
Bennink, S., & Pradel, G. (2019). The molecular machinery of translational control in malaria parasites. Molecular Microbiology, 112, 1658-1673.
Bertschi, N. L., Toenhake, C. G., Zou, A., Niederwieser, I., Henderson, R., Moes, S., … Voss, T. S. (2017). Malaria parasites possess a telomere repeat-binding protein that shares ancestry with transcription factor IIIA. Nature Microbiology, 2, 17033.
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.
Borden, K. L. (2000). RING domains: Master builders of molecular scaffolds? Journal of Molecular Biology, 295, 1103-1112.
Bozdech, Z., Llinas, M., Pulliam, B. L., Wong, E. D., Zhu, J., & DeRisi, J. L. (2003). The transcriptome of the intraerythrocytic developmental cycle of plasmodium falciparum. PLoS Biology, 1, E5.
Bunnik, E. M., Batugedara, G., Saraf, A., Prudhomme, J., Florens, L., & Le Roch, K. G. (2016). The mRNA-bound proteome of the human malaria parasite plasmodium falciparum. Genome Biology, 17, 147.
Bushell, E., Gomes, A. R., Sanderson, T., Anar, B., Girling, G., Herd, C., … Billker, O. (2017). Functional profiling of a plasmodium genome reveals an abundance of essential genes. Cell, 170, 260-272.
Cassandri, M., Smirnov, A., Novelli, F., Pitolli, C., Agostini, M., Malewicz, M., … Raschellà, G. (2017). Zinc-finger proteins in health and disease. Cell Death Discovery, 3, 17071.
Chen, Y., Jirage, D., Caridha, D., Kathcart, A. K., Cortes, E. A., Dennull, R. A., … Waters, N. C. (2006). Identification of an effector protein and gain-of-function mutants that activate Pfmrk, a malarial cyclin-dependent protein kinase. Molecular and Biochemical Parasitology, 149, 48-57.
Chung, D. W., Ponts, N., Prudhomme, J., Rodrigues, E. M., & Le Roch, K. G. (2012). Characterization of the ubiquitylating components of the human malaria parasite's protein degradation pathway. PLoS ONE, 7, e43477.
Collart, M. A. (2013). The Not4 RING E3 ligase: A relevant player in Cotranslational quality control. ISRN Molecular Biology, 2013, 548359.
Coulson, R. M., Hall, N., & Ouzounis, C. A. (2004). Comparative genomics of transcriptional control in the human malaria parasite plasmodium falciparum. Genome Research, 14, 1548-1554.
Cui, L., Fan, Q., Cui, L., & Miao, J. (2008). Histone lysine methyltransferases and demethylases in plasmodium falciparum. International Journal for Parasitology, 38, 1083-1097.
Daubenberger, C. A., Diaz, D., Curcic, M., Mueller, M. S., Spielmann, T., Certa, U., … Pluschke, G. (2003). Identification and characterization of a conserved, stage-specific gene product of plasmodium falciparum recognized by parasite growth inhibitory antibodies. Infection and Immunity, 71, 2173-2181.
Deshaies, R. J., & Joazeiro, C. A. (2009). RING domain E3 ubiquitin ligases. Annual Review of Biochemistry, 78, 399-434.
Erath, J., Djuranovic, S., & Djuranovic, S. P. (2019). Adaptation of translational machinery in malaria parasites to accommodate translation of poly-adenosine stretches throughout its life cycle. Frontiers in Microbiology, 10, 2823.
Fan, Q., An, L., & Cui, L. (2004). Plasmodium falciparum histone acetyltransferase, a yeast GCN5 homologue involved in chromatin remodeling. Eukaryotic Cell, 3, 264-276.
Fesquet, D., Labbe, J. C., Derancourt, J., Capony, J. P., Galas, S., Girard, F., … Cavadore, J. C. (1993). The MO15 gene encodes the catalytic subunit of a protein kinase that activates cdc2 and other cyclin-dependent kinases (CDKs) through phosphorylation of Thr161 and its homologues. The EMBO Journal, 12, 3111-3121.
Fisher, R. P., & Morgan, D. O. (1994). A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell, 78, 713-724.
Fu, M., & Blackshear, P. J. (2017). RNA-binding proteins in immune regulation: A focus on CCCH zinc finger proteins. Nature Reviews. Immunology, 17, 130-143.
Gissot, M., Hovasse, A., Chaloin, L., Schaeffer-Reiss, C., Van, D. A., & Tomavo, S. (2017). An evolutionary conserved zinc finger protein is involved in toxoplasma gondii mRNA nuclear export. Cellular Microbiology, 19, e12644.
Gopalakrishnan, A. M., Aly, A. S. I., Aravind, L., & Kumar, N. (2017). Multifunctional involvement of a C2H2 zinc finger protein (PbZfp) in malaria transmission, histone modification, and susceptibility to DNA damage response. MBio, 8, e01298-17.
Hajikhezri, Z., Darweesh, M., Akusjarvi, G., & Punga, T. (2020). Role of CCCH-type zinc finger proteins in human adenovirus infections. Viruses, 12, 1322.
Harbut, M. B., Patel, B. A., Yeung, B. K., McNamara, C. W., Bright, A. T., Ballard, J., … Greenbaum, D. C. (2012). Targeting the ERAD pathway via inhibition of signal peptide peptidase for antiparasitic therapeutic design. Proceedings of the National Academy of Sciences of the United States of America, 109, 21486-21491.
Hoeijmakers, W. A. M., Miao, J., Schmidt, S., Toenhake, C. G., Shrestha, S., Venhuizen, J., … Bártfai, R. (2019). Epigenetic reader complexes of the human malaria parasite, plasmodium falciparum. Nucleic Acids Research, 47, 11574-11588.
Hollin, T., & Le Roch, K. G. (2020). From genes to transcripts, a tightly regulated journey in plasmodium. Frontiers in Cellular and Infection Microbiology, 10, 618454.
Jen, J., & Wang, Y. C. (2016). Zinc finger proteins in cancer progression. Journal of Biomedical Science, 23, 53.
Jiang, L., Mu, J., Zhang, Q., Ni, T., Srinivasan, P., Rayavara, K., … Miller, L. H. (2013). PfSETvs methylation of histone H3K36 represses virulence genes in plasmodium falciparum. Nature, 499, 223-227.
Jirage, D., Chen, Y., Caridha, D., O'Neil, M. T., Eyase, F., Witola, W. H., … Waters, N. C. (2010). The malarial CDK Pfmrk and its effector PfMAT1 phosphorylate DNA replication proteins and co-localize in the nucleus. Molecular and Biochemical Parasitology, 172, 9-18.
Juszkiewicz, S., Chandrasekaran, V., Lin, Z., Kraatz, S., Ramakrishnan, V., & Hegde, R. S. (2018). ZNF598 is a quality control sensor of collided ribosomes. Molecular Cell, 72, 469-481.
Kang, H. J., Jeong, S. J., Kim, K. N., Baek, I. J., Chang, M., Kang, C. M., … Yun, C.-W. (2014). A novel protein, Pho92, has a conserved YTH domain and regulates phosphate metabolism by decreasing the mRNA stability of PHO4 in Saccharomyces cerevisiae. The Biochemical Journal, 457, 391-400.
Kelly, S. M., Leung, S. W., Pak, C., Banerjee, A., Moberg, K. H., & Corbett, A. H. (2014). A conserved role for the zinc finger polyadenosine RNA binding protein, ZC3H14, in control of poly(a) tail length. RNA, 20, 681-688.
Kelly, S. M., Pabit, S. A., Kitchen, C. M., Guo, P., Marfatia, K. A., Murphy, T. J., … Berland, K. M. (2007). Recognition of polyadenosine RNA by zinc finger proteins. Proceedings of the National Academy of Sciences of the United States of America, 104, 12306-12311.
Klug, A. (2010). The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annual Review of Biochemistry, 79, 213-231.
Kralovicova, J., Knut, M., Cross, N. C., & Vorechovsky, I. (2015). Identification of U2AF(35)-dependent exons by RNA-Seq reveals a link between 3′ splice-site organization and activity of U2AF-related proteins. Nucleic Acids Research, 43, 3747-3763.
Li, Y., & Li, H. (2012). Many keys to push: Diversifying the 'readership' of plant homeodomain fingers. Acta Biochimica et Biophysica Sinica Shanghai, 44, 28-39.
Lopez-Barragan, M. J., Lemieux, J., Quinones, M., Williamson, K. C., Molina-Cruz, A., Cui, K., … Su, X.-z. (2011). Directional gene expression and antisense transcripts in sexual and asexual stages of plasmodium falciparum. BMC Genomics, 12, 587.
Lu, Q., Murakami, C., Hoshino, F., Murakami, Y., & Sakane, F. (2020). Diacylglycerol kinase δ destabilizes serotonin transporter protein through the ubiquitin-proteasome system. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1865(3), 158608. http://dx.doi.org/10.1016/j.bbalip.2019.158608
Luo, S., & Tong, L. (2014). Molecular basis for the recognition of methylated adenines in RNA by the eukaryotic YTH domain. Proceedings of the National Academy of Sciences of the United States of America, 111, 13834-13839.
Maeda, K., & Akira, S. (2017). Regulation of mRNA stability by CCCH-type zinc-finger proteins in immune cells. International Immunology, 29, 149-155.
Masoumi, K. C., Marfany, G., Wu, Y., & Massoumi, R. (2016). Putative role of SUMOylation in controlling the activity of deubiquitinating enzymes in cancer. Future Oncology, 12, 565-574.
Ngwa, C. J., Gross, M. R., Musabyimana, J. P., Pradel, G., & Deitsch, K. W. (2021). The role of the histone Methyltransferase PfSET10 in antigenic variation by malaria parasites: A cautionary tale. mSphere, 6, e01217-e01220.
Ngwa, C. J., Kiesow, M. J., Orchard, L. M., Farrukh, A., Llinás, M., & Pradel, G. (2019). The G9a histone Methyltransferase inhibitor BIX-01294 modulates gene expression during plasmodium falciparum gametocyte development and transmission. International Journal of Molecular Sciences, 20, 5087.
Ngwa, C. J., Kiesow, M. J., Papst, O., Orchard, L. M., Filarsky, M., Rosinski, A. N., … Pradel, G. (2017). Transcriptional profiling defines histone acetylation as a regulator of gene expression during human-to-mosquito transmission of the malaria parasite plasmodium falciparum. Frontiers in Cellular and Infection Microbiology, 7, 320.
Nigg, E. A. (1996). Cyclin-dependent kinase 7: At the cross-roads of transcription, DNA repair and cell cycle control? Current Opinion in Cell Biology, 8, 312-317.
Oehring, S. C., Woodcroft, B. J., Moes, S., Wetzel, J., Dietz, O., Pulfer, A., … Voss, T. S. (2012). Organellar proteomics reveals hundreds of novel nuclear proteins in the malaria parasite plasmodium falciparum. Genome Biology, 13, R108.
Panasenko, O. O., & Collart, M. A. (2011). Not4 E3 ligase contributes to proteasome assembly and functional integrity in part through Ecm29. Molecular and Cellular Biology, 31, 1610-1623.
Park, H. Y., Lee, K. C., Jang, Y. H., Kim, S. K., Thu, M. P., Lee, J. H., & Kim, J.-K. (2017). The Arabidopsis splicing factors, AtU2AF65, AtU2AF35, and AtSF1 shuttle between nuclei and cytoplasms. Plant Cell Reports, 36, 1113-1123.
Patil, D. P., Pickering, B. F., & Jaffrey, S. R. (2018). Reading m6A in the Transcriptome: m6A-binding proteins. Trends in Cell Biology, 28, 113-127.
Ponts, N., Saraf, A., Chung, D. W., Harris, A., Prudhomme, J., Washburn, M. P., … Le Roch, K. G. (2011). Unraveling the ubiquitome of the human malaria parasite. The Journal of Biological Chemistry, 286, 40320-40330.
Rasche, N., Dybkov, O., Schmitzová, J., Akyildiz, B., Fabrizio, P., & Lührmann, R. (2012). Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre. The EMBO Journal, 31(6), 1591-1604. http://dx.doi.org/10.1038/emboj.2011.502
Rawat, M., Malhotra, R., Shintre, S., Pani, S., & Karmodiya, K. (2020). Role of PfGCN5 in nutrient sensing and transcriptional regulation in plasmodium falciparum. Journal of Biosciences, 45, 11.
Reddy, B. P., Shrestha, S., Hart, K. J., Liang, X., Kemirembe, K., Cui, L., & Lindner, S. E. (2015). A bioinformatic survey of RNA-binding proteins in plasmodium. BMC Genomics, 16, 890.
Reilly Ayala, H. B., Wacker, M. A., Siwo, G., & Ferdig, M. T. (2010). Quantitative trait loci mapping reveals candidate pathways regulating cell cycle duration in plasmodium falciparum. BMC Genomics, 11, 577.
Saurin, A. J., Borden, K. L., Boddy, M. N., & Freemont, P. S. (1996). Does this have a familiar RING? Trends in Biochemical Sciences, 21, 208-214.
Schwach, F., Bushell, E., Gomes, A. R., Anar, B., Girling, G., Herd, C., … Billker, O. (2015). PlasmoGEM, a database supporting a community resource for large-scale experimental genetics in malaria parasites. Nucleic Acids Research, 43, D1176-D1182.
Shock, J. L., Fischer, K. F., & DeRisi, J. L. (2007). Whole-genome analysis of mRNA decay in plasmodium falciparum reveals a global lengthening of mRNA half-life during the intra-erythrocytic development cycle. Genome Biology, 8, R134.
Shuttleworth, J. (1995). The regulation and functions of cdk7. Progress in Cell Cycle Research, 1, 229-240.
Singh, J. K., & van Attikum, H. (2021). DNA double-strand break repair: Putting zinc fingers on the sore spot. Seminars in Cell & Developmental Biology, 113, 65-74.
Sorber, K., Dimon, M. T., & DeRisi, J. L. (2011). RNA-Seq analysis of splicing in plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts. Nucleic Acids Research, 39, 3820-3835.
Stevens, A. T., Howe, D. K., & Hunt, A. G. (2018). Characterization of mRNA polyadenylation in the apicomplexa. PLoS ONE, 13, e0203317.
Szymczyna, B. R., Bowman, J., McCracken, S., Pineda-Lucena, A., Lu, Y., Cox, B., … Blencowe, B. J. (2003). Structure and function of the PWI motif: A novel nucleic acid-binding domain that facilitates pre-mRNA processing. Genes & Development, 17, 461-475.
Torii, K. U., Stoop-Myer, C. D., Okamoto, H., Coleman, J. E., Matsui, M., & Deng, X. W. (1999). The RING finger motif of photomorphogenic repressor COP1 specifically interacts with the RING-H2 motif of a novel Arabidopsis protein. The Journal of Biological Chemistry, 274, 27674-27681.
Tuteja, R., & Mehta, J. (2010). A genomic glance at the components of the mRNA export machinery in plasmodium falciparum. Communicative & Integrative Biology, 3, 318-326.
Ukaegbu, U. E., Kishore, S. P., Kwiatkowski, D. L., Pandarinath, C., Dahan-Pasternak, N., Dzikowski, R., & Deitsch, K. W. (2014). Recruitment of PfSET2 by RNA polymerase II to variant antigen encoding loci contributes to antigenic variation in P. falciparum. PLoS Pathogens, 10, e1003854.
van Leuken, R. J., Luna-Vargas, M. P., Sixma, T. K., Wolthuis, R. M., & Medema, R. H. (2008). Usp39 is essential for mitotic spindle checkpoint integrity and controls mRNA-levels of aurora B. Cell Cycle, 7, 2710-2719.
Volz, J., Carvalho, T. G., Ralph, S. A., Gilson, P., Thompson, J., Tonkin, C. J., … Cowman, A. F. (2010). Potential epigenetic regulatory proteins localise to distinct nuclear sub-compartments in plasmodium falciparum. International Journal for Parasitology, 40, 109-121.
Voss, T. S., Bozdech, Z., & Bártfai, R. (2014). Epigenetic memory takes center stage in the survival strategy of malaria parasites. Current Opinion in Microbiology, 20, 88-95. http://dx.doi.org/10.1016/j.mib.2014.05.007
Wang, B. B., & Brendel, V. (2004). The ASRG database: Identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biology, 5, R102.
WHO World Malaria Report 2020. (2020). https://www.who.int/publications/i/item/9789240015791
Wolfe, S. A., Nekludova, L., & Pabo, C. O. (2000). DNA Recognition by Cys2His2Zinc Finger Proteins. Annual Review of Biophysics and Biomolecular Structure, 29(1), 183-212. http://dx.doi.org/10.1146/annurev.biophys.29.1.183
Yu, P., Chen, Y., Tagle, D. A., & Cai, T. (2002). PJA1, encoding a RING-H2 finger ubiquitin ligase, is a novel human X chromosome gene abundantly expressed in brain. Genomics, 79, 869-874.
Zaccara, S., & Jaffrey, S. R. (2020). A Unified Model for the Function of YTHDF Proteins in Regulating m6A-Modified mRNA. Cell, 181(7), 1582-1595. http://dx.doi.org/10.1016/j.cell.2020.05.012
Zhang, M., Wang, C., Otto, T. D., Oberstaller, J., Liao, X., Adapa, S. R., … Adams, J. H. (2018). Uncovering the essential genes of the human malaria parasite plasmodium falciparum by saturation mutagenesis. Science, 360, eaap7847.

Auteurs

Che Julius Ngwa (CJ)

Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, Aachen, Germany.

Afia Farrukh (A)

Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, Aachen, Germany.

Gabriele Pradel (G)

Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, Aachen, Germany.

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