Plasma-derived extracellular vesicles from Plasmodium vivax patients signal spleen fibroblasts via NF-kB facilitating parasite cytoadherence.
Animals
Cell Adhesion
Cell-Derived Microparticles
Disease Models, Animal
Extracellular Vesicles
/ metabolism
Fibroblasts
/ metabolism
Host-Parasite Interactions
/ physiology
Humans
Intercellular Adhesion Molecule-1
/ metabolism
Malaria, Vivax
/ parasitology
Male
Mice
Mice, Inbred C57BL
Microvessels
/ parasitology
NF-kappa B
/ metabolism
Plasma
Plasmodium vivax
/ physiology
Proteomics
Reticulocytes
/ metabolism
Spleen
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
02 06 2020
02 06 2020
Historique:
received:
30
06
2019
accepted:
25
04
2020
entrez:
4
6
2020
pubmed:
4
6
2020
medline:
25
8
2020
Statut:
epublish
Résumé
Plasmodium vivax is the most widely distributed human malaria parasite. Previous studies have shown that circulating microparticles during P. vivax acute attacks are indirectly associated with severity. Extracellular vesicles (EVs) are therefore major components of circulating plasma holding insights into pathological processes. Here, we demonstrate that plasma-derived EVs from Plasmodium vivax patients (PvEVs) are preferentially uptaken by human spleen fibroblasts (hSFs) as compared to the uptake of EVs from healthy individuals. Moreover, this uptake induces specific upregulation of ICAM-1 associated with the translocation of NF-kB to the nucleus. After this uptake, P. vivax-infected reticulocytes obtained from patients show specific adhesion properties to hSFs, reversed by inhibiting NF-kB translocation to the nucleus. Together, these data provide physiological EV-based insights into the mechanisms of human malaria pathology and support the existence of P. vivax-adherent parasite subpopulations in the microvasculature of the human spleen.
Identifiants
pubmed: 32487994
doi: 10.1038/s41467-020-16337-y
pii: 10.1038/s41467-020-16337-y
pmc: PMC7265481
doi:
Substances chimiques
ICAM1 protein, human
0
NF-kappa B
0
Intercellular Adhesion Molecule-1
126547-89-5
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2761Références
Yanez-Mo, M. et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles 4, 27066 (2015).
pubmed: 25979354
doi: 10.3402/jev.v4.27066
Marcilla, A. et al. Extracellular vesicles in parasitic diseases. J. Extracell. Vesicles 3, 25040 (2014).
pubmed: 25536932
doi: 10.3402/jev.v3.25040
Nantakomol, D. et al. Circulating red cell-derived microparticles in human malaria. J. Infect. Dis. 203, 700–706 (2011).
pubmed: 21282195
pmcid: 3072726
doi: 10.1093/infdis/jiq104
Regev-Rudzki, N. et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153, 1120–1133 (2013).
pubmed: 23683579
doi: 10.1016/j.cell.2013.04.029
Mantel, P. Y. et al. Malaria-infected erythrocyte-derived microvesicles mediate cellular communication within the parasite population and with the host immune system. Cell Host Microbe 13, 521–534 (2013).
pubmed: 23684304
pmcid: 3687518
doi: 10.1016/j.chom.2013.04.009
Sisquella, X. et al. Malaria parasite DNA-harbouring vesicles activate cytosolic immune sensors. Nat. Commun. 8, 1985 (2017).
pubmed: 29215015
pmcid: 5719353
doi: 10.1038/s41467-017-02083-1
Mantel, P. Y. et al. Infected erythrocyte-derived extracellular vesicles alter vascular function via regulatory Ago2-miRNA complexes in malaria. Nat. Commun. 7, 12727 (2016).
pubmed: 27721445
pmcid: 5062468
doi: 10.1038/ncomms12727
Demarta-Gatsi, C. et al. Histamine releasing factor and elongation factor 1 alpha secreted via malaria parasites extracellular vesicles promote immune evasion by inhibiting specific T cell responses. Cell. Microbiol. 21, e13021 (2019).
pubmed: 30835870
doi: 10.1111/cmi.13021
Martin-Jaular, L., Nakayasu, E. S., Ferrer, M., Almeida, I. C. & Del Portillo, H. A. Exosomes from Plasmodium yoelii-infected reticulocytes protect mice from lethal infections. PLoS ONE 6, e26588 (2011).
pubmed: 22046311
pmcid: 3202549
doi: 10.1371/journal.pone.0026588
Miller, L. H., Baruch, D. I., Marsh, K. & Doumbo, O. K. The pathogenic basis of malaria. Nature 415, 673–679 (2002).
pubmed: 11832955
doi: 10.1038/415673a
Tripathi, A. K., Sullivan, D. J. & Stins, M. F. Plasmodium falciparum-infected erythrocytes increase intercellular adhesion molecule 1 expression on brain endothelium through NF-kappaB. Infect. Immun. 74, 3262–3270 (2006).
pubmed: 16714553
pmcid: 1479273
doi: 10.1128/IAI.01625-05
Trager, W. & Jensen, J. B. Human malaria parasites in continuous culture. Science 193, 673–675 (1976).
pubmed: 781840
doi: 10.1126/science.781840
Noulin, F., Borlon, C., Van Den Abbeele, J., D’Alessandro, U. & Erhart, A. 1912–2012: a century of research on Plasmodium vivax in vitro culture. Trends Parasitol. 29, 286–294 (2013).
pubmed: 23623759
doi: 10.1016/j.pt.2013.03.012
Carvalho, B. O. et al. On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J. Infect. Dis. 202, 638–647 (2010).
pubmed: 20617923
doi: 10.1086/654815
Chotivanich, K. et al. Plasmodium vivax adherence to placental glycosaminoglycans. PLoS ONE 7, e34509 (2012).
pubmed: 22529919
pmcid: 3328474
doi: 10.1371/journal.pone.0034509
De las Salas, B. et al. Adherence to human lung microvascular endothelial cells (HMVEC-L) of Plasmodium vivax isolates from Colombia. Malar. J. 12, 347 (2013).
doi: 10.1186/1475-2875-12-347
del Portillo, H. A. et al. A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 410, 839–842 (2001).
pubmed: 11298455
doi: 10.1038/35071118
Bernabeu, M. et al. Functional analysis of Plasmodium vivax VIR proteins reveals different subcellular localizations and cytoadherence to the ICAM-1 endothelial receptor. Cell. Microbiol. 14, 386–400 (2012).
pubmed: 22103402
doi: 10.1111/j.1462-5822.2011.01726.x
Martin-Jaular, L. et al. Strain-specific spleen remodelling in Plasmodium yoelii infections in Balb/c mice facilitates adherence and spleen macrophage-clearance escape. Cell. Microbiol. 13, 109–122 (2011).
pubmed: 20923452
pmcid: 3228402
doi: 10.1111/j.1462-5822.2010.01523.x
Machado Siqueira, A. et al. Spleen rupture in a case of untreated Plasmodium vivax infection. PLoS Negl. Trop. Dis. 6, e1934 (2012).
pubmed: 23272256
pmcid: 3521714
doi: 10.1371/journal.pntd.0001934
Peterson, M. S. et al. Plasmodium vivax parasite load is associated with histopathology in Saimiri boliviensis with findings comparable to P. vivax pathogenesis in humans. Open Forum Infect. Dis. 6, ofz021 (2019).
pubmed: 30937329
pmcid: 6436601
doi: 10.1093/ofid/ofz021
Fernandez-Becerra, C. et al. Plasmodium vivax and the importance of the subtelomeric multigene vir superfamily. Trends Parasitol. 25, 44–51 (2009).
pubmed: 19036639
doi: 10.1016/j.pt.2008.09.012
Fonseca, L. L., Joyner, C. J., Ma, H. C., Galinski, M. R. & Voit, E. O. A model of Plasmodium vivax concealment based on Plasmodium cynomolgi infections in Macaca mulatta. Malar. J. 16, 375 (2017).
pubmed: 28923058
pmcid: 5608162
doi: 10.1186/s12936-017-2008-4
Baird, J. K. Evidence and implications of mortality associated with acute Plasmodium vivax malaria. Clin. Microbiol Rev. 26, 36–57 (2013).
pubmed: 23297258
pmcid: 3553673
doi: 10.1128/CMR.00074-12
de Menezes-Neto, A. et al. Size-exclusion chromatography as a stand-alone methodology identifies novel markers in mass spectrometry analyses of plasma-derived vesicles from healthy individuals. J. Extracell. Vesicles 4, 27378 (2015).
pubmed: 26154623
doi: 10.3402/jev.v4.27378
Gualdron-Lopez, M. et al. Characterization of Plasmodium vivax proteins in plasma-derived exosomes from malaria-infected liver-chimeric humanized mice. Front. Microbiol. 9, 1271 (2018).
pubmed: 29988527
pmcid: 6026661
doi: 10.3389/fmicb.2018.01271
Diaz-Varela, M. et al. Proteomics study of human cord blood reticulocyte-derived exosomes. Sci. Rep. 8, 14046 (2018).
pubmed: 30232403
pmcid: 6145868
doi: 10.1038/s41598-018-32386-2
Jiang, J., Barnwell, J. W., Meyer, E. V. & Galinski, M. R. Plasmodium vivax merozoite surface protein-3 (PvMSP3): expression of an 11 member multigene family in blood-stage parasites. PLoS ONE 8, e63888 (2013).
pubmed: 23717506
pmcid: 3662707
doi: 10.1371/journal.pone.0063888
Akinyi, S. et al. A 95 kDa protein of Plasmodium vivax and P. cynomolgi visualized by three-dimensional tomography in the caveola-vesicle complexes (Schuffner’s dots) of infected erythrocytes is a member of the PHIST family. Mol. Microbiol. 84, 816–831 (2012).
pubmed: 22537295
pmcid: 3359410
doi: 10.1111/j.1365-2958.2012.08060.x
Valencia, J. et al. Characterization of human fibroblastic reticular cells as potential immunotherapeutic tools. Cytotherapy 19, 640–653 (2017).
pubmed: 28262465
doi: 10.1016/j.jcyt.2017.01.010
Karunaweera, N. D., Wijesekera, S. K., Wanasekera, D., Mendis, K. N. & Carter, R. The paroxysm of Plasmodium vivax malaria. Trends Parasitol. 19, 188–193 (2003).
pubmed: 12689650
doi: 10.1016/S1471-4922(03)00036-9
Jeppesen, D. K. et al. Reassessment of exosome composition. Cell 177, e418 (2019).
doi: 10.1016/j.cell.2019.02.029
Kowal, J. et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl Acad. Sci. USA 113, E968–E977 (2016).
pubmed: 26858453
doi: 10.1073/pnas.1521230113
Campos, F. M. et al. Augmented plasma microparticles during acute Plasmodium vivax infection. Malar. J. 9, 327 (2010).
pubmed: 21080932
pmcid: 2998527
doi: 10.1186/1475-2875-9-327
Wiklander, O. P. et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J. Extracell. Vesicles 4, 26316 (2015).
pubmed: 25899407
doi: 10.3402/jev.v4.26316
Krotoski, W. A. Discovery of the hypnozoite and a new theory of malarial relapse. Trans. R. Soc. Trop. Med Hyg. 79, 1–11 (1985).
pubmed: 3922096
doi: 10.1016/0035-9203(85)90221-4
Martin-Jaular, L. et al. Spleen-dependent immune protection elicited by CpG adjuvanted reticulocyte-derived exosomes from malaria infection is associated with changes in T cell subsets’ distribution. Front Cell Dev. Biol. 4, 131 (2016).
pubmed: 27900319
pmcid: 5110551
doi: 10.3389/fcell.2016.00131
Delicou, S. Extramedullary haemopoiesis in hemoglobinopathies. J. Hematol.Transfus. 5, 1066 (2017).
Baro, B. et al. Plasmodium vivax gametocytes in the bone marrow of an acute malaria patient and changes in the erythroid miRNA profile. PLoS Negl. Trop. Dis. 11, e0005365 (2017).
pubmed: 28384192
pmcid: 5383020
doi: 10.1371/journal.pntd.0005365
Wickramasinghe, S. N., Looareesuwan, S., Nagachinta, B. & White, N. J. Dyserythropoiesis and ineffective erythropoiesis in Plasmodium vivax malaria. Br. J. Haematol. 72, 91–99 (1989).
pubmed: 2660903
doi: 10.1111/j.1365-2141.1989.tb07658.x
Obaldia, N. III, et al. Bone marrow is a major parasite reservoir in Plasmodium vivax infection. MBio 9, e00625-18 (2018).
pubmed: 29739900
pmcid: 5941073
doi: 10.1128/mBio.00625-18
Lee, R. S., Waters, A. P. & Brewer, J. M. A cryptic cycle in haematopoietic niches promotes initiation of malaria transmission and evasion of chemotherapy. Nat. Commun. 9, 1689 (2018).
pubmed: 29703959
pmcid: 5924373
doi: 10.1038/s41467-018-04108-9
Thery, C., Amigorena, S., Raposo, G. & Clayton, A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. 30, 3.22.1–3.22.29 (2006).
doi: 10.1002/0471143030.cb0322s30
Pathan, M. et al. Vesiclepedia 2019: a compendium of RNA, proteins, lipids and metabolites in extracellular vesicles. Nucleic Acids Res. 47, D516–D519 (2019).
pubmed: 30395310
doi: 10.1093/nar/gky1029
Pathan, M. et al. FunRich: an open access standalone functional enrichment and interaction network analysis tool. Proteomics 15, 2597–2601 (2015).
pubmed: 25921073
doi: 10.1002/pmic.201400515
Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009).
pubmed: 19131956
doi: 10.1038/nprot.2008.211
Borrello, M. A. & Phipps, R. P. Differential Thy-1 expression by splenic fibroblasts defines functionally distinct subsets. Cell Immunol. 173, 198–206 (1996).
pubmed: 8912877
doi: 10.1006/cimm.1996.0268
Roobsoong, W. et al. Improvement of culture conditions for long-term in vitro culture of Plasmodium vivax. Malar. J. 14, 297 (2015).
pubmed: 26243280
pmcid: 4524445
doi: 10.1186/s12936-015-0815-z
Perez-Riverol, Y. et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
pubmed: 30395289
pmcid: 30395289
doi: 10.1093/nar/gky1106