{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T02:40:37Z","timestamp":1790563237978,"version":"4.1.0"},"reference-count":62,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2022,5,17]],"date-time":"2022-05-17T00:00:00Z","timestamp":1652745600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"the Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["NG170\/1-1"],"award-info":[{"award-number":["NG170\/1-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"the Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["PR905\/20-1"],"award-info":[{"award-number":["PR905\/20-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"the Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["No 731060"],"award-info":[{"award-number":["No 731060"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"name":"the German Academic Exchange Service (DAAD)","award":["NG170\/1-1"],"award-info":[{"award-number":["NG170\/1-1"]}]},{"name":"the German Academic Exchange Service (DAAD)","award":["PR905\/20-1"],"award-info":[{"award-number":["PR905\/20-1"]}]},{"name":"the German Academic Exchange Service (DAAD)","award":["No 731060"],"award-info":[{"award-number":["No 731060"]}]},{"name":"the European Union\u2019s Horizon 2020 research and innovation program","award":["NG170\/1-1"],"award-info":[{"award-number":["NG170\/1-1"]}]},{"name":"the European Union\u2019s Horizon 2020 research and innovation program","award":["PR905\/20-1"],"award-info":[{"award-number":["PR905\/20-1"]}]},{"name":"the European Union\u2019s Horizon 2020 research and innovation program","award":["No 731060"],"award-info":[{"award-number":["No 731060"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>CCCH zinc finger proteins (ZFPs) function mainly as RNA-binding proteins (RBPs) and play a central role in the mRNA metabolism. Over twenty seven CCCH-ZFPs are encoded in the genome of the human malaria parasite Plasmodium falciparum, the causative agent of malaria tropica. However, little is known about their functions. In this study, we characterize one member of the PfCCCH-ZFP named ZNF4. We show that ZNF4 is highly expressed in mature gametocytes, where it predominantly localizes to the cytoplasm. Targeted gene disruption of ZNF4 showed no significant effect in asexual blood stage replication and gametocyte development while male gametocyte exflagellation was significantly impaired, leading to reduced malaria transmission in the mosquito. Comparative transcriptomics between wildtype (WT) and the ZNF4-deficient line (ZNF4-KO) demonstrated the deregulation of about 473 genes (274 upregulated and 199 downregulated) in mature gametocytes. Most of the downregulated genes show peak expression in mature gametocyte with male enriched genes associated to the axonemal dynein complex formation, and cell projection organization is highly affected, pointing to the phenotype in male gametocyte exflagellation. Upregulated genes are associated to ATP synthesis. Our combined data therefore indicate that ZNF4 is a CCCH zinc finger protein which plays an important role in male gametocyte exflagellation through the regulation of male gametocyte-enriched genes.<\/jats:p>","DOI":"10.3390\/cells11101666","type":"journal-article","created":{"date-parts":[[2022,5,18]],"date-time":"2022-05-18T03:20:43Z","timestamp":1652844043000},"page":"1666","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["The Plasmodium falciparum CCCH Zinc Finger Protein ZNF4 Plays an Important Role in Gametocyte Exflagellation through the Regulation of Male Enriched Transcripts"],"prefix":"10.3390","volume":"11","author":[{"given":"Borja","family":"Hanhsen","sequence":"first","affiliation":[{"name":"Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Afia","family":"Farrukh","sequence":"additional","affiliation":[{"name":"Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2264-5558","authenticated-orcid":false,"given":"Gabriele","family":"Pradel","sequence":"additional","affiliation":[{"name":"Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Che Julius","family":"Ngwa","sequence":"additional","affiliation":[{"name":"Division of Cellular and Applied Infection Biology, Institute of Zoology, RWTH Aachen University, 52074 Aachen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,17]]},"reference":[{"key":"ref_1","unstructured":"(2022, January 13). World Malaria Report. Available online: https:\/\/www.who.int\/publications\/i\/item\/9789240040496."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"976827","DOI":"10.1155\/2010\/976827","article-title":"The coming-out of malaria gametocytes","volume":"2010","author":"Kuehn","year":"2010","journal-title":"J. Biomed. Biotechnol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1111\/cmi.12604","article-title":"The development of malaria parasites in the mosquito midgut","volume":"18","author":"Bennink","year":"2016","journal-title":"Cell. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1038\/nrmicro3519","article-title":"Sexual development in Plasmodium parasites: Knowing when it\u2019s time to commit","volume":"13","author":"Josling","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1038\/nature12920","article-title":"A transcriptional switch underlies commitment to sexual development in malaria parasites","volume":"507","author":"Kafsack","year":"2014","journal-title":"Nature"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1038\/nature12970","article-title":"A cascade of DNA-binding proteins for sexual commitment and development in Plasmodium","volume":"507","author":"Sinha","year":"2014","journal-title":"Nature"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"9264","DOI":"10.1093\/nar\/gkab683","article-title":"A cascade of transcriptional repression determines sexual commitment and development in Plasmodium falciparum","volume":"49","author":"Shang","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1111\/mmi.14334","article-title":"Female-specific gene regulation in malaria parasites by an AP2-family transcription factor","volume":"113","author":"Yuda","year":"2020","journal-title":"Mol. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e51660","DOI":"10.15252\/embr.202051660","article-title":"Plasmodium transcription repressor AP2-O3 regulates sex-specific identity of gene expression in female gametocytes","volume":"22","author":"Li","year":"2021","journal-title":"EMBO Rep."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Kaneko, I., Iwanaga, S., Kato, T., Kobayashi, I., and Yuda, M. (2015). Genome-Wide Identification of the Target Genes of AP2-O, a Plasmodium AP2-Family Transcription Factor. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1004905"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.chom.2016.12.003","article-title":"A Knockout Screen of ApiAP2 Genes Reveals Networks of Interacting Transcriptional Regulators Controlling the Plasmodium Life Cycle","volume":"21","author":"Modrzynska","year":"2017","journal-title":"Cell Host Microbe"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1658","DOI":"10.1111\/mmi.14388","article-title":"The molecular machinery of translational control in malaria parasites","volume":"112","author":"Bennink","year":"2019","journal-title":"Mol. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Bennink, S., von Bohl, A., Ngwa, C.J., Henschel, L., Kuehn, A., Pilch, N., Wei\u00dfbach, T., Rosinski, A.N., Scheuermayer, M., and Repnik, U. (2018). A seven-helix protein constitutes stress granules crucial for regulating translation during human-to-mosquito transmission of Plasmodium falciparum. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1007249"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Mair, G.R., Lasonder, E., Garver, L.S., Franke-Fayard, B.M.D., Carret, C.K., Wiegant, J.C.A.G., Dirks, R.W., Dimopoulos, G., Janse, C.J., and Waters, A.P. (2010). Universal Features of Post-Transcriptional Gene Regulation Are Critical for Plasmodium Zygote Development. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1000767"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1126\/science.1125129","article-title":"Regulation of sexual development of Plasmodium by translational repression","volume":"313","author":"Mair","year":"2006","journal-title":"Science"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1242\/jcs.059824","article-title":"The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum","volume":"123","author":"Miao","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_17","first-page":"3144","article-title":"The RNA-binding protein Puf1 functions in the maintenance of gametocytes in Plasmodium falciparum","volume":"129","author":"Shrestha","year":"2016","journal-title":"J. Cell Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"320","DOI":"10.3389\/fcimb.2017.00320","article-title":"Transcriptional Profiling Defines Histone Acetylation as a Regulator of Gene Expression during Human-to-Mosquito Transmission of the Malaria Parasite Plasmodium falciparum","volume":"7","author":"Ngwa","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Ngwa, C.J., Kiesow, M.J., Orchard, L.M., Farrukh, A., Llin\u00e1s, M., and Pradel, G. (2019). The g9a histone methyltransferase inhibitor BIX-01294 modulates gene expression during plasmodium falciparum gametocyte development and transmission. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20205087"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e13387","DOI":"10.1111\/cmi.13387","article-title":"Zinc finger proteins of Plasmodium falciparum","volume":"23","author":"Ngwa","year":"2021","journal-title":"Cell. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Hajikhezri, Z., Darweesh, M., Akusj\u00e4rvi, G., and Punga, T. (2020). Role of CCCH-Type Zinc Finger Proteins in Human Adenovirus Infections. Viruses, 12.","DOI":"10.3390\/v12111322"},{"key":"ref_22","first-page":"140","article-title":"Mitogens stimulate the rapid nuclear to cytosolic translocation of tristetraprolin, a potential zinc-finger transcription factor","volume":"10","author":"Taylor","year":"1996","journal-title":"Mol. Endocrinol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1104\/pp.109.145656","article-title":"The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA","volume":"152","author":"Pomeranz","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"647","DOI":"10.4161\/psb.6.5.15105","article-title":"Putative molecular mechanisms underlying tandem CCCH zinc finger protein mediated plant growth, stress, and gene expression responses","volume":"6","author":"Pomeranz","year":"2011","journal-title":"Plant Signal. Behav."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Ngwa, C.J., Scheuermayer, M., Mair, G.R., Kern, S., Br\u00fcgl, T., Wirth, C.C., Aminake, M.N., Wiesner, J., Fischer, R., and Vilcinskas, A. (2013). Changes in the transcriptome of the malaria parasite Plasmodium falciparum during the initial phase of transmission from the human to the mosquito. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-256"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1038\/294364a0","article-title":"Complete in vitro maturation of Plasmodium falciparum gametocytes","volume":"294","author":"Ifediba","year":"1981","journal-title":"Nature"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"418","DOI":"10.2307\/3280287","article-title":"Synchronization of Plasmodium falciparum erythrocytic stages in culture","volume":"65","author":"Lambros","year":"1979","journal-title":"J. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1038\/nmeth.4223","article-title":"A genetic system to study Plasmodium falciparum protein function","volume":"14","author":"Birnbaum","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Wagle, P., Nikoli\u0107, M., and Frommolt, P. (2015). QuickNGS elevates Next-Generation Sequencing data analysis to a new level of automation. BMC Genom., 16.","DOI":"10.1186\/s12864-015-1695-x"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: Ultrafast universal RNA-seq aligner","volume":"29","author":"Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1038\/nature01097","article-title":"Genome sequence of the human malaria parasite Plasmodium falciparum","volume":"419","author":"Gardner","year":"2002","journal-title":"Nature."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nbt.3122","article-title":"StringTie enables improved reconstruction of a transcriptome from RNA-seq reads","volume":"33","author":"Pertea","year":"2015","journal-title":"Nat. Biotechnol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","article-title":"featureCounts: An efficient general purpose program for assigning sequence reads to genomic features","volume":"30","author":"Liao","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2\u2212\u0394\u0394CT Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1046\/j.1365-2958.2003.03570.x","article-title":"Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria","volume":"49","author":"Salanti","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1186\/1475-2875-9-147","article-title":"Identification of a major rif transcript common to gametocytes and sporozoites of Plasmodium falciparum","volume":"9","author":"Wang","year":"2010","journal-title":"Malar. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"505","DOI":"10.4269\/ajtmh.1998.59.505","article-title":"Plasmodium falciparum: Purification of the various gametocyte developmental stages from in vitro-cultivated parasites","volume":"59","author":"Kariuki","year":"1998","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.molbiopara.2007.04.008","article-title":"Improved synchronous production of Plasmodium falciparum gametocytes in vitro","volume":"154","author":"Fivelman","year":"2007","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"D439","DOI":"10.1093\/nar\/gkab1061","article-title":"AlphaFold Protein Structure Database: Massively expanding the structural coverage of protein-sequence space with high-accuracy models","volume":"50","author":"Varadi","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","article-title":"Highly accurate protein structure prediction with AlphaFold","volume":"596","author":"Jumper","year":"2021","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Grant, C.E., and Bailey, T.L. (2021). XSTREME: Comprehensive motif analysis of biological sequence datasets. bioRxiv.","DOI":"10.1101\/2021.09.02.458722"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"L\u00f3pez-Barrag\u00e1n, M.J., Lemieux, J., Qui\u00f1ones, M., Williamson, K.C., Molina-Cruz, A., Cui, K., Barillas-Mury, C., Zhao, K., and Su, X. (2011). Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genom., 12.","DOI":"10.1186\/1471-2164-12-587"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"6087","DOI":"10.1093\/nar\/gkw536","article-title":"Integrated transcriptomic and proteomic analyses of P. falciparum gametocytes: Molecular insight into sex-specific processes and translational repression","volume":"44","author":"Lasonder","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1038\/nature12311","article-title":"A compendium of RNA-binding motifs for decoding gene regulation","volume":"499","author":"Ray","year":"2013","journal-title":"Nature."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"eaap7847","DOI":"10.1126\/science.aap7847","article-title":"Uncovering the essential genome of the human malaria parasitePlasmodium falciparum by saturationmutagenesis","volume":"360","author":"Zhang","year":"2018","journal-title":"Science"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"624945","DOI":"10.3389\/fcimb.2021.624945","article-title":"Pleiotropic Roles for the Plasmodium berghei RNA Binding Protein UIS12 in Transmission and Oocyst Maturation","volume":"11","author":"Silvie","year":"2021","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Aprea, I., Raidt, J., H\u00f6ben, I.M., Loges, N.T., N\u00f6the-Menchen, T., Pennekamp, P., Olbrich, H., Kaiser, T., Biebach, L., and T\u00fcttelmann, F. (2021). Defects in the Cytoplasmic Assembly of Axonemal Dynein Arms Cause Morphological Abnormalities and Dysmotility in Sperm Cells Leading to male Infertility. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009306"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1242\/jcs.051326","article-title":"Flagellar and ciliary beating: The proven and the possible","volume":"123","author":"Lindemann","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1093\/infdis\/jix237","article-title":"A Molecular Assay to Quantify Male and Female Plasmodium falciparum Gametocytes: Results From 2 Randomized Controlled Trials Using Primaquine for Gametocyte Clearance","volume":"216","author":"Stone","year":"2017","journal-title":"J. Infect. Dis."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e34463","DOI":"10.7554\/eLife.34463","article-title":"Predicting the likelihood and intensity of mosquito infection from sex specific plasmodium falciparum gametocyte density","volume":"7","author":"Bradley","year":"2018","journal-title":"Elife"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1038\/s41431-019-0489-z","article-title":"MNS1 variant associated with situs inversus and male infertility","volume":"28","author":"Leslie","year":"2020","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Ta-Shma, A., Hjeij, R., Perles, Z., Dougherty, G.W., Abu Zahira, I., Letteboer, S.J.F., Antony, D., Darwish, A., Mans, D.A., and Spittler, S. (2018). Homozygous loss-of-function mutations in MNS1 cause laterality defects and likely male infertility. PLoS Genet., 14.","DOI":"10.1371\/journal.pgen.1007602"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1126\/science.8178152","article-title":"Sex determination and dosage compensation: Lessons from flies and worms","volume":"264","author":"Parkhurst","year":"1994","journal-title":"Science"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2072","DOI":"10.1101\/gad.8.17.2072","article-title":"The sex-lethal amino terminus mediates cooperative interactions in RNA binding and is essential for splicing regulation","volume":"8","author":"Wang","year":"1994","journal-title":"Genes Dev."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.celrep.2015.06.008","article-title":"The Nuclear PolyA-Binding Protein Nab2p Is Essential for mRNA Production","volume":"12","author":"Schmid","year":"2015","journal-title":"Cell Rep."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"7752","DOI":"10.1074\/jbc.M110053200","article-title":"Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p","volume":"277","author":"Green","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1300","DOI":"10.1128\/MCB.01683-13","article-title":"Cytoplasmic poly(A) binding protein C4 serves a critical role in erythroid differentiation","volume":"34","author":"Kini","year":"2014","journal-title":"Mol. Cell. Biol."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Miao, J., Fan, Q., Parker, D., Li, X., Li, J., and Cui, L. (2013). Puf mediates translation repression of transmission-blocking vaccine candidates in malaria parasites. PLoS Pathog., 9.","DOI":"10.1371\/journal.ppat.1003268"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Hirai, M., Maeta, A., Mori, T., and Mita, T. (2021). Pb103 Regulates Zygote\/Ookinete Development in Plasmodium berghei via Double Zinc Finger Domains. Pathogens, 10.","DOI":"10.3390\/pathogens10121536"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1038\/nri.2016.129","article-title":"RNA-binding proteins in immune regulation: A focus on CCCH zinc finger proteins","volume":"17","author":"Fu","year":"2017","journal-title":"Nat. Rev. Immunol."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/10\/1666\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:13:46Z","timestamp":1760138026000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/10\/1666"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,17]]},"references-count":62,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["cells11101666"],"URL":"https:\/\/doi.org\/10.3390\/cells11101666","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.03.08.483571","asserted-by":"object"}]},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,17]]}}}