Plasma-derived extracellular vesicles from Plasmodium vivax patients signal spleen fibroblasts via NF-kB facilitating parasite cytoadherence.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
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

2761

Références

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

Auteurs

Haruka Toda (H)

ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, 08036, Spain.

Miriam Diaz-Varela (M)

ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, 08036, Spain.

Joan Segui-Barber (J)

ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, 08036, Spain.

Wanlapa Roobsoong (W)

Mahidol Vivax Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, 10400, Thailand.

Barbara Baro (B)

Fundaçao de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, Amazonas, 69040-000, Brazil.
ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, Spain.

Susana Garcia-Silva (S)

Microenvironment and Metastasis Laboratory, Department of Molecular Oncology, Spanish National Cancer Research Center (CNIO), Madrid, 28029, Spain.

Alicia Galiano (A)

Àrea de Parasitologia, Departament de Farmàcia i Tecnologia Farmacèutica i Parasitologia, Universitat de València, Burjassot, Valencia, 46100, Spain.

Melisa Gualdrón-López (M)

Germans Trias i Pujol Health Science Research Institute (IGTP), Badalona, 08916, Spain.

Anne C G Almeida (ACG)

Fundaçao de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, Amazonas, 69040-000, Brazil.
Universidade do Estado do Amazonas (UEA), Manaus, Amazonas, 69020-070, Brazil.

Marcelo A M Brito (MAM)

Fundaçao de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, Amazonas, 69040-000, Brazil.
Universidade do Estado do Amazonas (UEA), Manaus, Amazonas, 69020-070, Brazil.

Gisely Cardoso de Melo (GC)

Fundaçao de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, Amazonas, 69040-000, Brazil.
Universidade do Estado do Amazonas (UEA), Manaus, Amazonas, 69020-070, Brazil.

Iris Aparici-Herraiz (I)

ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, 08036, Spain.

Carlos Castro-Cavadía (C)

Grupo de Salud y Comunidad Cesar Uribe Piedrahíta, Universidad de Antioquia, Medellín, Colombia.

Wuelton Marcelo Monteiro (WM)

Fundaçao de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, Amazonas, 69040-000, Brazil.
Universidade do Estado do Amazonas (UEA), Manaus, Amazonas, 69020-070, Brazil.

Eva Borràs (E)

Proteomics Unit, Centre de Regulació Genòmica (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, 08003, Spain.
Universitat Pompeu Fabra (UPF), Barcelona, 08002, Spain.

Eduard Sabidó (E)

Proteomics Unit, Centre de Regulació Genòmica (CRG), Barcelona Institute of Science and Technology (BIST), Barcelona, 08003, Spain.
Universitat Pompeu Fabra (UPF), Barcelona, 08002, Spain.

Igor C Almeida (IC)

Border Biomedical Research Center, Department of Biological Sciences, College of Science, University of Texas El Paso, El Paso, TX, 79902, USA.

Jakub Chojnacki (J)

AIDS Research Institute IrsiCaixa, Badalona, 08916, Spain.

Javier Martinez-Picado (J)

Germans Trias i Pujol Health Science Research Institute (IGTP), Badalona, 08916, Spain.
AIDS Research Institute IrsiCaixa, Badalona, 08916, Spain.
University of Vic-Central University of Catalonia, Vic, 08500, Spain.
Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, 08010, Spain.

Maria Calvo (M)

Unitat de Microscopia Òptica Avançada, Facultat de Medicina, Centres Científics i Tecnològics, Universitat de Barcelona, Barcelona, 08028, Spain.

Pilar Armengol (P)

Germans Trias i Pujol Health Science Research Institute (IGTP), Badalona, 08916, Spain.

Jaime Carmona-Fonseca (J)

Grupo de Salud y Comunidad Cesar Uribe Piedrahíta, Universidad de Antioquia, Medellín, Colombia.

Maria Fernanda Yasnot (MF)

Grupo de Investigaciones Microbiológicas y Biomédicas de Córdoba-GIMBIC, Universidad de Córdoba, Monteria, 230001, Colombia.

Ricardo Lauzurica (R)

Nephrology Service, Germans Trias i Pujol University Hospital, Badalona, 08916, Spain.

Antonio Marcilla (A)

Àrea de Parasitologia, Departament de Farmàcia i Tecnologia Farmacèutica i Parasitologia, Universitat de València, Burjassot, Valencia, 46100, Spain.

Hector Peinado (H)

Microenvironment and Metastasis Laboratory, Department of Molecular Oncology, Spanish National Cancer Research Center (CNIO), Madrid, 28029, Spain.

Mary R Galinski (MR)

Emory Vaccine Center, Yerkes National Primate Research Center, School of Medicine, Division of Infectious Diseases, Emory University, Atlanta, GA, 30329, USA.

Marcus V G Lacerda (MVG)

Fundaçao de Medicina Tropical Dr. Heitor Vieira Dourado (FMT-HVD), Manaus, Amazonas, 69040-000, Brazil.
Instituto Leônidas & Maria Deane (ILMD), Fiocruz, Manaus, Amazonas, 69057-070, Brazil.

Jetsumon Sattabongkot (J)

Mahidol Vivax Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, 10400, Thailand.

Carmen Fernandez-Becerra (C)

ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, 08036, Spain. carmen.fernandez@isglobal.org.
Germans Trias i Pujol Health Science Research Institute (IGTP), Badalona, 08916, Spain. carmen.fernandez@isglobal.org.

Hernando A Del Portillo (HA)

ISGlobal, Hospital Clínic - Universitat de Barcelona, Barcelona, 08036, Spain. hernandoa.delportillo@isglobal.org.
Germans Trias i Pujol Health Science Research Institute (IGTP), Badalona, 08916, Spain. hernandoa.delportillo@isglobal.org.
Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, 08010, Spain. hernandoa.delportillo@isglobal.org.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH