Characterization of a nuclear transport factor 2-like domain-containing protein in Plasmodium berghei.

Export NTF2-like protein Noncanonical Plasmodium mRNA

Journal

Malaria journal
ISSN: 1475-2875
Titre abrégé: Malar J
Pays: England
ID NLM: 101139802

Informations de publication

Date de publication:
09 Jan 2024
Historique:
received: 17 05 2023
accepted: 03 01 2024
medline: 10 1 2024
pubmed: 10 1 2024
entrez: 9 1 2024
Statut: epublish

Résumé

Plasmodium lacks an mRNA export receptor ortholog, such as yeast Mex67. Yeast Mex67 contains a nuclear transport factor 2 (NTF2)-like domain, suggesting that NTF2-like domain-containing proteins might be associated with mRNA export in Plasmodium. In this study, the relationship between mRNA export and an NTF2-like domain-containing protein, PBANKA_1019700, was investigated using the ANKA strain of rodent malaria parasite Plasmodium berghei. The deletion mutant Δ1019700 was generated by introducing gene-targeting vectors into the P. berghei ANKA genome, and parasite growth and virulence were examined. To investigate whether PBANKA_1019700 is involved in mRNA export, live-cell fluorescence imaging and immunoprecipitation coupled to mass spectrometry (IP-MS) were performed using transgenic parasites expressing fusion proteins (1019700::mCherry). Deletion of PBANKA_1019700 affected the sexual phase but not the asexual phase of malaria parasites. Live-cell fluorescence imaging showed that PBANKA_1019700 localizes to the cytoplasm. Moreover, IP-MS analysis of 1019700::mCherry indicated that PBANKA_1019700 interacts with ubiquitin-related proteins but not nuclear proteins. PBANKA_1019700 is a noncanonical NTF2-like superfamily protein.

Sections du résumé

BACKGROUND BACKGROUND
Plasmodium lacks an mRNA export receptor ortholog, such as yeast Mex67. Yeast Mex67 contains a nuclear transport factor 2 (NTF2)-like domain, suggesting that NTF2-like domain-containing proteins might be associated with mRNA export in Plasmodium. In this study, the relationship between mRNA export and an NTF2-like domain-containing protein, PBANKA_1019700, was investigated using the ANKA strain of rodent malaria parasite Plasmodium berghei.
METHODS METHODS
The deletion mutant Δ1019700 was generated by introducing gene-targeting vectors into the P. berghei ANKA genome, and parasite growth and virulence were examined. To investigate whether PBANKA_1019700 is involved in mRNA export, live-cell fluorescence imaging and immunoprecipitation coupled to mass spectrometry (IP-MS) were performed using transgenic parasites expressing fusion proteins (1019700::mCherry).
RESULTS RESULTS
Deletion of PBANKA_1019700 affected the sexual phase but not the asexual phase of malaria parasites. Live-cell fluorescence imaging showed that PBANKA_1019700 localizes to the cytoplasm. Moreover, IP-MS analysis of 1019700::mCherry indicated that PBANKA_1019700 interacts with ubiquitin-related proteins but not nuclear proteins.
CONCLUSIONS CONCLUSIONS
PBANKA_1019700 is a noncanonical NTF2-like superfamily protein.

Identifiants

DOI: 10.1186/s12936-024-04839-9 PMID: 38195464
pubmed: 38195464
doi: 10.1186/s12936-024-04839-9
pii: 10.1186/s12936-024-04839-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

13

Informations de copyright

© 2024. The Author(s).

Références

Hackmann A, Wu H, Schneider UM, Meyer K, Jung K, Krebber H. Quality control of spliced mRNAs requires the shuttling SR proteins Gbp2 and Hrb1. Nat Commun. 2014;5:3123.
doi: 10.1038/ncomms4123 pubmed: 24452287
Katahira J. Nuclear export of messenger RNA. Genes (Basel). 2015;6:163–84.
doi: 10.3390/genes6020163 pubmed: 25836925
Zander G, Krebber H. Quick or quality? How mRNA escapes nuclear quality control during stress. RNA Biol. 2017;14:1642–8.
doi: 10.1080/15476286.2017.1345835 pubmed: 28708448 pmcid: 5731798
Xie Y, Ren Y. Mechanisms of nuclear mRNA export: a structural perspective. Traffic. 2019;20:829–40.
doi: 10.1111/tra.12691 pubmed: 31513326 pmcid: 7074880
Wickramasinghe VO, Laskey RA. Control of mammalian gene expression by selective mRNA export. Nat Rev Mol Cell Biol. 2015;16:431–42.
doi: 10.1038/nrm4010 pubmed: 26081607
Burki F, Roger AJ, Brown MW, Simpson AGB. The new tree of eukaryotes. Trends Ecol Evol. 2020;35:43–55.
doi: 10.1016/j.tree.2019.08.008 pubmed: 31606140
Niikura M, Fukutomi T, Mitobe J, Kobayashi F. Roles and cellular localization of GBP2 and NAB2 during the blood stage of malaria parasites. Front Cell Infect Microbiol. 2021;11:737457.
doi: 10.3389/fcimb.2021.737457 pubmed: 34604117 pmcid: 8479154
Tuteja R, Mehta J. A genomic glance at the components of the mRNA export machinery in Plasmodium falciparum. Commun Integr Biol. 2010;3:318–26.
doi: 10.4161/cib.3.4.11886 pubmed: 20798816 pmcid: 2928308
Avila AR, Cabezas-Cruz A, Gissot M. mRNA export in the apicomplexan parasite Toxoplasma gondii: emerging divergent components of a crucial pathway. Parasit Vectors. 2018;11:62.
doi: 10.1186/s13071-018-2648-4 pubmed: 29370868 pmcid: 5785795
Kubina J, Geldreich A, Gales JP, Baumberger N, Bouton C, Ryabova LA, et al. Nuclear export of plant pararetrovirus mRNAs involves the TREX complex, two viral proteins and the highly structured 5′ leader region. Nucleic Acids Res. 2021;49:8900–22.
doi: 10.1093/nar/gkab653 pubmed: 34370034 pmcid: 8421220
Aibara S, Valkov E, Lamers M, Stewart M. Domain organization within the nuclear export factor Mex67:Mtr2 generates an extended mRNA binding surface. Nucleic Acids Res. 2015;43:1927–36.
doi: 10.1093/nar/gkv030 pubmed: 25618852 pmcid: 4330389
Dostalova A, Kaser S, Cristodero M, Schimanski B. The nuclear mRNA export receptor Mex67-Mtr2 of Trypanosoma brucei contains a unique and essential zinc finger motif. Mol Microbiol. 2013;88:728–39.
doi: 10.1111/mmi.12217 pubmed: 23560737
Frankel MB, Knoll LJ. The ins and outs of nuclear trafficking: unusual aspects in apicomplexan parasites. DNA Cell Biol. 2009;28:277–84.
doi: 10.1089/dna.2009.0853 pubmed: 19348590 pmcid: 2903460
Niikura M, Komatsuya K, Inoue SI, Matsuda R, Asahi H, Inaoka DK, et al. Suppression of experimental cerebral malaria by disruption of malate:quinone oxidoreductase. Malar J. 2017;16:247.
doi: 10.1186/s12936-017-1898-5 pubmed: 28606087 pmcid: 5469008
Niikura M, Inoue SI, Mineo S, Asahi H, Kobayashi F. IFNGR1 signaling is associated with adverse pregnancy outcomes during infection with malaria parasites. PLoS ONE. 2017;12:e0185392.
doi: 10.1371/journal.pone.0185392 pubmed: 29117241 pmcid: 5678718
Ecker A, Moon R, Sinden RE, Billker O. Generation of gene targeting constructs for Plasmodium berghei by a PCR-based method amenable to high throughput applications. Mol Biochem Parasitol. 2006;145:265–8.
doi: 10.1016/j.molbiopara.2005.10.006 pubmed: 16290088
Niikura M, Fukutomi T, Fukui K, Inoue SI, Asahi H, Kobayashi F. G-strand binding protein 2 is involved in asexual and sexual development of Plasmodium berghei. Parasitol Int. 2020;76:102059.
doi: 10.1016/j.parint.2020.102059 pubmed: 31958569
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. 2015;11:e1004905.
doi: 10.1371/journal.ppat.1004905 pubmed: 26018192 pmcid: 4446032
Niikura M, Inoue S, Mineo S, Yamada Y, Kaneko I, Iwanaga S, et al. Experimental cerebral malaria is suppressed by disruption of nucleoside transporter 1 but not purine nucleoside phosphorylase. Biochem Biophys Res Commun. 2013;432:504–8.
doi: 10.1016/j.bbrc.2013.02.004 pubmed: 23402751
Wang G, Wu WW, Zhang Z, Masilamani S, Shen RF. Decoy methods for assessing false positives and false discovery rates in shotgun proteomics. Anal Chem. 2009;81:146–59.
doi: 10.1021/ac801664q pubmed: 19061407 pmcid: 2653784
Käll L, Canterbury JD, Weston J, Noble WS, MacCoss MJ. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods. 2007;4:923–5.
doi: 10.1038/nmeth1113 pubmed: 17952086
De Niz M, Ullrich AK, Heiber A, Blancke Soares A, Pick C, Lyck R, et al. The machinery underlying malaria parasite virulence is conserved between rodent and human malaria parasites. Nat Commun. 2016;7:11659.
doi: 10.1038/ncomms11659 pubmed: 27225796 pmcid: 4894950
Schwede A, Manful T, Jha BA, Helbig C, Bercovich N, Stewart M, et al. The role of deadenylation in the degradation of unstable mRNAs in trypanosomes. Nucleic Acids Res. 2009;37:5511–28.
doi: 10.1093/nar/gkp571 pubmed: 19596809 pmcid: 2760810
Serpeloni M, Vidal NM, Goldenberg S, Avila AR, Hoffmann FG. Comparative genomics of proteins involved in RNA nucleocytoplasmic export. BMC Evol Biol. 2011;11:7.
doi: 10.1186/1471-2148-11-7 pubmed: 21223572 pmcid: 3032688
Ambekar SV, Beck JR, Mair GR. TurboID identification of evolutionarily divergent components of the nuclear pore complex in the malaria model Plasmodium berghei. mBio. 2022;13:e0181522.
doi: 10.1128/mbio.01815-22 pubmed: 36040030
Vuksanovic N, Zhu X, Serrano DA, Siitonen V, Metsa-Ketela M, Melancon CE III, et al. Structural characterization of three noncanonical NTF2-like superfamily proteins: implications for polyketide biosynthesis. Acta Crystallogr F Struct Biol Commun. 2020;76:372–83.
doi: 10.1107/S2053230X20009814 pubmed: 32744249 pmcid: 7397469

Auteurs

Mamoru Niikura (M)

Department of Infectious Diseases, Kyorin University School of Medicine, Tokyo, Japan. mniikura@ks.kyorin-u.ac.jp.

Toshiyuki Fukutomi (T)

Department of Pharmacology and Toxicology, Kyorin University School of Medicine, Tokyo, Japan.

Jiro Mitobe (J)

Department of Infectious Diseases, Kyorin University School of Medicine, Tokyo, Japan.

Fumie Kobayashi (F)

Department of Environmental Science, School of Life and Environmental Science, Azabu University, Kanagawa, 252-5201, Japan.

Classifications MeSH