A subpellicular microtubule dynein transport machinery regulates ookinete morphogenesis for mosquito transmission of Plasmodium yoelii.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
04 Oct 2024
04 Oct 2024
Historique:
received:
28
06
2024
accepted:
25
09
2024
medline:
5
10
2024
pubmed:
5
10
2024
entrez:
4
10
2024
Statut:
epublish
Résumé
The cortical cytoskeleton of subpellicular microtubules (SPMTs) supports the Plasmodium ookinete morphogenesis during mosquito transmission of malaria. SPMTs are hypothesized to function as the cytoskeletal tracks in motor-driven cargo transport for apical organelle and structure assembly in ookinetes. However, the SPMT-based transport motor has not been identified in the Plasmodium. The cytoplasmic dynein is the motor moving towards the minus end of microtubules (MTs) and likely be responsible for cargo transport to the apical part in ookinetes. Here we screen 7 putative dynein heavy chain (DHC) proteins in the P. yoelii and identify DHC3 showing peripheral localization in ookinetes. DHC3 is localized at SPMTs throughout ookinete morphogenesis. We also identify five other dynein subunits localizing at SPMTs. DHC3 disruption impairs ookinete development, shape, and gliding, leading to failure in mosquito infection of Plasmodium. The DHC3-deficient ookinetes display defective formation or localization of apical organelles and structures. Rab11A and Rab11B interact with DHC3 at SPMTs in a DHC3-dependent manner, likely functioning as the receptors for the cargoes driven by SPMT-dynein. Disturbing Rab11A or Rab11B phenocopies DHC3 deficiency in ookinete morphogenesis. Our study reveals an SPMT-based dynein motor driving the transport of Rab11A- and Rab11B-labeled cargoes in the ookinete morphogenesis of Plasmodium.
Identifiants
pubmed: 39366980
doi: 10.1038/s41467-024-52970-7
pii: 10.1038/s41467-024-52970-7
doi:
Substances chimiques
Dyneins
EC 3.6.4.2
Protozoan Proteins
0
rab GTP-Binding Proteins
EC 3.6.5.2
rab11 protein
EC 3.6.1.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8590Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32170427
Informations de copyright
© 2024. The Author(s).
Références
World Health Organization. World Malaria Report 2020 (World Health Organization, Geneva, Switzerland, 2020).
Bennink, S., Kiesow, M. J. & Pradel, G. The development of malaria parasites in the mosquito midgut. Cell Microbiol. 18, 905–918 (2016).
pubmed: 27111866
pmcid: 5089571
doi: 10.1111/cmi.12604
Guttery, D. S., Roques, M., Holder, A. A. & Tewari, R. Commit and transmit: molecular players in plasmodium sexual development and zygote differentiation. Trends Parasitol. 31, 676–685 (2015).
pubmed: 26440790
doi: 10.1016/j.pt.2015.08.002
Wang, X., Qian, P., Cui, H., Yao, L. & Yuan, J. A protein palmitoylation cascade regulates microtubule cytoskeleton integrity in Plasmodium. EMBO J. 39, e104168 (2020).
pubmed: 32395856
pmcid: 7327484
doi: 10.15252/embj.2019104168
Aly, A. S., Vaughan, A. M. & Kappe, S. H. Malaria parasite development in the mosquito and infection of the mammalian host. Annu. Rev. Microbiol. 63, 195–221 (2009).
pubmed: 19575563
pmcid: 2841446
doi: 10.1146/annurev.micro.091208.073403
Kono, M., Prusty, D., Parkinson, J. & Gilberger, T. W. The apicomplexan inner membrane complex. Front. Biosci. 18, 982–992 (2013).
Morrissette, N. S. & Sibley, L. D. Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev. 66, 21–38 (2002).
pubmed: 11875126
pmcid: 120781
doi: 10.1128/MMBR.66.1.21-38.2002
Bertiaux, E. et al. Expansion microscopy provides new insights into the cytoskeleton of malaria parasites including the conservation of a conoid. PLoS Biol. 19, e3001020 (2021).
pubmed: 33705377
pmcid: 7951857
doi: 10.1371/journal.pbio.3001020
Spreng, B. et al. Microtubule number and length determine cellular shape and function in Plasmodium. EMBO J. 38, e100984 (2019).
pubmed: 31368598
pmcid: 6669926
doi: 10.15252/embj.2018100984
Harding, C. R. & Frischknecht, F. The riveting cellular structures of apicomplexan parasites. Trends Parasitol. 36, 979–991 (2020).
pubmed: 33011071
doi: 10.1016/j.pt.2020.09.001
Ferreira, J. L. et al. Variable microtubule architecture in the malaria parasite. Nat. Commun. 14, 1216 (2023).
pubmed: 36869034
pmcid: 9984467
doi: 10.1038/s41467-023-36627-5
Fowler, R. E., Fookes, R. E., Lavin, F., Bannister, L. H. & Mitchell, G. H. Microtubules in Plasmodium falciparum merozoites and their importance for invasion of erythrocytes. Parasitology 117, 425–433 (1998).
pubmed: 9836307
doi: 10.1017/S003118209800328X
Qian, P. et al. Apical anchorage and stabilization of subpellicular microtubules by apical polar ring ensures Plasmodium ookinete infection in mosquito. Nat. Commun. 13, 7465 (2022).
pubmed: 36463257
pmcid: 9719560
doi: 10.1038/s41467-022-35270-w
Raibaud, A. et al. Cryofracture electron microscopy of the ookinete pellicle of Plasmodium gallinaceum reveals the existence of novel pores in the alveolar membranes. J. Struct. Biol. 135, 47–57 (2001).
pubmed: 11562165
doi: 10.1006/jsbi.2001.4396
Canning, E. U. & Sinden, R. E. The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67, 29–40 (1973).
pubmed: 4579580
doi: 10.1017/S0031182000046266
Cyrklaff, M. et al. Cryoelectron tomography reveals periodic material at the inner side of subpellicular microtubules in apicomplexan parasites. J. Exp. Med. 204, 1281–1287 (2007).
pubmed: 17562819
pmcid: 2118598
doi: 10.1084/jem.20062405
Frenal, K. & Soldati-Favre, D. Role of the parasite and host cytoskeleton in apicomplexa parasitism. Cell Host Microbe 5, 602–611 (2009).
pubmed: 19527887
doi: 10.1016/j.chom.2009.05.013
Francia, M. E. & Striepen, B. Cell division in apicomplexan parasites. Nat. Rev. Microbiol. 12, 125–136 (2014).
pubmed: 24384598
doi: 10.1038/nrmicro3184
Sibley, L. D. Intracellular parasite invasion strategies. Science 304, 248–253 (2004).
pubmed: 15073368
doi: 10.1126/science.1094717
Blackman, M. J. & Bannister, L. H. Apical organelles of Apicomplexa: biology and isolation by subcellular fractionation. Mol. Biochem. Parasitol. 117, 11–25 (2001).
pubmed: 11551628
doi: 10.1016/S0166-6851(01)00328-0
Sweeney, H. L. & Holzbaur, E. L. F. Motor proteins. Cold Spring Harb. Perspect. Biol. https://doi.org/10.1101/cshperspect.a021931 (2018).
Downing, K. H. & Nogales, E. Tubulin and microtubule structure. Curr. Opin. Cell Biol. 10, 16–22 (1998).
pubmed: 9484591
doi: 10.1016/S0955-0674(98)80082-3
Nogales, E., Whittaker, M., Milligan, R. A. & Downing, K. H. High-resolution model of the microtubule. Cell 96, 79–88 (1999).
pubmed: 9989499
doi: 10.1016/S0092-8674(00)80961-7
Hirokawa, N., Noda, Y., Tanaka, Y. & Niwa, S. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682–696 (2009).
pubmed: 19773780
doi: 10.1038/nrm2774
Reck-Peterson, S. L., Redwine, W. B., Vale, R. D. & Carter, A. P. The cytoplasmic dynein transport machinery and its many cargoes. Nat. Rev. Mol. Cell Biol. 19, 382–398 (2018).
pubmed: 29662141
pmcid: 6457270
doi: 10.1038/s41580-018-0004-3
Schroer, T. A., Steuer, E. R. & Sheetz, M. P. Cytoplasmic dynein is a minus end-directed motor for membranous organelles. Cell 56, 937–946 (1989).
pubmed: 2522353
doi: 10.1016/0092-8674(89)90627-2
Viswanadha, R., Sale, W. S. & Porter, M. E. Ciliary motility: regulation of axonemal dynein motors. Cold Spring Harb. Perspect. Biol. 9, a018325 (2017).
pubmed: 28765157
pmcid: 5538414
doi: 10.1101/cshperspect.a018325
Hook, P. & Vallee, R. B. The dynein family at a glance. J. Cell Sci. 119, 4369–4371 (2006).
pubmed: 17074830
doi: 10.1242/jcs.03176
Zhang, C. et al. CRISPR/Cas9 mediated sequential editing of genes critical for ookinete motility in Plasmodium yoelii. Mol. Biochem. Parasitol. 212, 1–8 (2017).
pubmed: 28034675
doi: 10.1016/j.molbiopara.2016.12.010
Zhang, C. et al. Efficient editing of malaria parasite genome using the CRISPR/Cas9 system. mBio 5, e01414-14 (2014).
pubmed: 24987097
pmcid: 4161241
doi: 10.1128/mBio.01414-14
Yusuf, N. A. et al. The plasmodium class XIV myosin, MyoB, has a distinct subcellular location in invasive and motile stages of the malaria parasite and an unusual light chain. J. Biol. Chem. 290, 12147–12164 (2015).
pubmed: 25802338
pmcid: 4424349
doi: 10.1074/jbc.M115.637694
Wall, R. J. et al. SAS6-like protein in Plasmodium indicates that conoid-associated apical complex proteins persist in invasive stages within the mosquito vector. Sci. Rep. 6, 28604 (2016).
pubmed: 27339728
pmcid: 4919640
doi: 10.1038/srep28604
Gao, H. et al. ISP1-anchored polarization of GCbeta/CDC50A complex initiates malaria ookinete gliding motility. Curr. Biol. 28, 2763–2776.e6 (2018).
pubmed: 30146157
doi: 10.1016/j.cub.2018.06.069
Dessens, J. T. et al. CTRP is essential for mosquito infection by malaria ookinetes. EMBO J. 18, 6221–6227 (1999).
pubmed: 10562534
pmcid: 1171685
doi: 10.1093/emboj/18.22.6221
Tsai, Y. L., Hayward, R. E., Langer, R. C., Fidock, D. A. & Vinetz, J. M. Disruption of Plasmodium falciparum chitinase markedly impairs parasite invasion of mosquito midgut. Infect. Immun. 69, 4048–4054 (2001).
pubmed: 11349075
pmcid: 98468
doi: 10.1128/IAI.69.6.4048-4054.2001
Dessens, J. T. et al. Knockout of the rodent malaria parasite chitinase pbCHT1 reduces infectivity to mosquitoes. Infect. Immun. 69, 4041–4047 (2001).
pubmed: 11349074
pmcid: 98467
doi: 10.1128/IAI.69.6.4041-4047.2001
Alam, M. S. Proximity ligation assay (PLA). Curr. Protoc. Immunol. 123, e58–e58 (2018).
pubmed: 30238640
pmcid: 6205916
doi: 10.1002/cpim.58
Wang, X. et al. Cryo-EM structure of cortical microtubules from human parasite Toxoplasma gondii identifies their microtubule inner proteins. Nat. Commun. 12, 3065 (2021).
pubmed: 34031406
pmcid: 8144581
doi: 10.1038/s41467-021-23351-1
Long, S., Anthony, B., Drewry, L. L. & Sibley, L. D. A conserved ankyrin repeat-containing protein regulates conoid stability, motility and cell invasion in Toxoplasma gondii. Nat. Commun. 8, 2236 (2017).
pubmed: 29269729
pmcid: 5740107
doi: 10.1038/s41467-017-02341-2
Gee, M. A., Heuser, J. E. & Vallee, R. B. An extended microtubule-binding structure within the dynein motor domain. Nature 390, 636–639 (1997).
pubmed: 9403697
doi: 10.1038/37663
Carter, A. P. et al. Structure and functional role of dynein’s microtubule-binding domain. Science 322, 1691–1695 (2008).
pubmed: 19074350
pmcid: 2663340
doi: 10.1126/science.1164424
Pfister, K. K. et al. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet. 2, e1 (2006).
pubmed: 16440056
pmcid: 1331979
doi: 10.1371/journal.pgen.0020001
Stenmark, H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513–525 (2009).
pubmed: 19603039
doi: 10.1038/nrm2728
Bhuin, T. & Roy, J. K. Rab proteins: the key regulators of intracellular vesicle transport. Exp. Cell Res. 328, 1–19 (2014).
pubmed: 25088255
doi: 10.1016/j.yexcr.2014.07.027
Patil, H. et al. Zygote morphogenesis but not the establishment of cell polarity in Plasmodium berghei is controlled by the small GTPase, RAB11A. PLoS Pathog. 16, e1008091 (2020).
pubmed: 32463831
pmcid: 7255598
doi: 10.1371/journal.ppat.1008091
Otto, T. D. et al. A comprehensive evaluation of rodent malaria parasite genomes and gene expression. BMC Biol. 12, 86 (2014).
pubmed: 25359557
pmcid: 4242472
doi: 10.1186/s12915-014-0086-0
Reddy, J. M., Raut, N. G. R., Seifert, J. L. & Hynds, D. L. Regulation of small GTPase prenylation in the nervous system. Mol. Neurobiol. 57, 2220–2231 (2020).
pubmed: 31989383
doi: 10.1007/s12035-020-01870-0
Khandelwal, P. et al. Rab11a-dependent exocytosis of discoidal/fusiform vesicles in bladder umbrella cells. Proc. Natl Acad. Sci. USA 105, 15773–15778 (2008).
pubmed: 18843107
pmcid: 2572972
doi: 10.1073/pnas.0805636105
Stone, R., Hayashi, T., Bajimaya, S., Hodges, E. & Takimoto, T. Critical role of Rab11a-mediated recycling endosomes in the assembly of type I parainfluenza viruses. Virology 487, 11–18 (2016).
pubmed: 26484934
doi: 10.1016/j.virol.2015.10.008
Agop-Nersesian, C. et al. Rab11A-controlled assembly of the inner membrane complex is required for completion of apicomplexan cytokinesis. PLoS Pathog. 5, e1000270 (2009).
pubmed: 19165333
pmcid: 2622761
doi: 10.1371/journal.ppat.1000270
Venugopal, K. et al. Rab11A regulates dense granule transport and secretion during Toxoplasma gondii invasion of host cells and parasite replication. PLoS Pathog. 16, e1008106 (2020).
pubmed: 32463830
pmcid: 7255593
doi: 10.1371/journal.ppat.1008106
Allan, V. J. Cytoplasmic dynein. Biochem. Soc. Trans. 39, 1169–1178 (2011).
pubmed: 21936784
doi: 10.1042/BST0391169
Ferreira, J. L. et al. The dynamic roles of the inner membrane complex in the multiple stages of the malaria parasite. Front. Cell Infect. Microbiol. 10, 611801 (2020).
pubmed: 33489940
doi: 10.3389/fcimb.2020.611801
Arnot, D. E., Ronander, E. & Bengtsson, D. C. The progression of the intra-erythrocytic cell cycle of Plasmodium falciparum and the role of the centriolar plaques in asynchronous mitotic division during schizogony. Int. J. Parasitol. 41, 71–80 (2011).
pubmed: 20816844
doi: 10.1016/j.ijpara.2010.07.012
Mayer, D. C. G. Protein dorting in Plasmodium falciparum. Life https://doi.org/10.3390/life11090937 (2021).
Zeeshan, M. et al. Plasmodium kinesin-8X associates with mitotic spindles and is essential for oocyst development during parasite proliferation and transmission. PLoS Pathog. 15, e1008048 (2019).
pubmed: 31600347
pmcid: 6786531
doi: 10.1371/journal.ppat.1008048
Zeeshan, M. et al. Genome-wide functional analysis reveals key roles for kinesins in the mammalian and mosquito stages of the malaria parasite life cycle. PLoS Biol. 20, e3001704 (2022).
pubmed: 35900985
pmcid: 9333250
doi: 10.1371/journal.pbio.3001704
Kjos, I., Vestre, K., Guadagno, N. A., Borg Distefano, M. & Progida, C. Rab and Arf proteins at the crossroad between membrane transport and cytoskeleton dynamics. Biochim. Biophys. Acta Mol. Cell Res. 1865, 1397–1409 (2018).
pubmed: 30021127
doi: 10.1016/j.bbamcr.2018.07.009
McKenney, R. J., Huynh, W., Tanenbaum, M. E., Bhabha, G. & Vale, R. D. Activation of cytoplasmic dynein motility by dynactin-cargo adapter complexes. Science 345, 337–341 (2014).
pubmed: 25035494
pmcid: 4224444
doi: 10.1126/science.1254198
Wilson, G. M. et al. The FIP3-Rab11 protein complex regulates recycling endosome targeting to the cleavage furrow during late cytokinesis. Mol. Biol. Cell 16, 849–860 (2005).
pubmed: 15601896
pmcid: 545916
doi: 10.1091/mbc.e04-10-0927
Liu, C. Y. et al. Generation of Plasmodium yoelii malaria parasite for conditional degradation of proteins. Mol. Biochem. Parasitol. https://doi.org/10.1016/j.molbiopara.2020.111346 (2021).
Carter, V., Cable, H. C., Underhill, B. A., Williams, J. & Hurd, H. Isolation of Plasmodium berghei ookinetes in culture using Nycodenz density gradient columns and magnetic isolation. Malar. J. 2, 35 (2003).
pubmed: 14613512
pmcid: 293433
doi: 10.1186/1475-2875-2-35
Philip, N., Vaikkinen, H. J., Tetley, L. & Waters, A. P. A unique Kelch domain phosphatase in Plasmodium regulates ookinete morphology, motility and invasion. PLoS ONE 7, e44617 (2012).
pubmed: 22957089
pmcid: 3434153
doi: 10.1371/journal.pone.0044617
Meijering, E., Dzyubachyk, O. & Smal, I. Methods for cell and particle tracking. Methods Enzymol. 504, 183–200 (2012).
pubmed: 22264535
doi: 10.1016/B978-0-12-391857-4.00009-4
Orfano, A. S. et al. Species-specific escape of Plasmodium sporozoites from oocysts of avian, rodent, and human malarial parasites. Malar. J. 15, 394 (2016).
pubmed: 27480269
pmcid: 4969971
doi: 10.1186/s12936-016-1451-y
Aurrecoechea, C. et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 37, D539–D543 (2009).
pubmed: 18957442
doi: 10.1093/nar/gkn814
Peng, D. & Tarleton, R. EuPaGDT: a web tool tailored to design CRISPR guide RNAs for eukaryotic pathogens. Micro Genom. 1, e000033 (2015).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019