Extracellular Vesicles from Parasitic Helminths Contain Specific Excretory/Secretory Proteins and Are Internalized in Intestinal Host Cells

被引:272
作者
Marcilla, Antonio [1 ]
Trelis, Maria [1 ]
Cortes, Alba [1 ]
Sotillo, Javier [1 ]
Cantalapiedra, Fernando [1 ]
Teresa Minguez, Maria [2 ]
Luz Valero, Maria [2 ,3 ]
Sanchez del Pino, Manuel Mateo [4 ]
Munoz-Antoli, Carla [1 ]
Toledo, Rafael [1 ]
Bernal, Dolores [4 ]
机构
[1] Univ Valencia, Area Parasitol, Dept Biol Celular & Parasitol, Valencia, Spain
[2] Univ Valencia, Serv Cent Soporte Invest Expt SCSIE, Valencia, Spain
[3] Ctr Invest Principe Felipe, Serv Prote, Valencia, Spain
[4] Univ Valencia, Dept Bioquim & Biol Mol, Valencia, Spain
关键词
ECHINOSTOMA-FRIEDI TREMATODA; FASCIOLA-HEPATICA; LEUCINE AMINOPEPTIDASE; SECRETORY PRODUCTS; MOLECULAR-CLONING; EXOSOMES; IDENTIFICATION; INFECTIONS; CAPRONI; ENOLASE;
D O I
10.1371/journal.pone.0045974
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The study of host-parasite interactions has increased considerably in the last decades, with many studies focusing on the identification of parasite molecules (i.e. surface or excretory/secretory proteins (ESP)) as potential targets for new specific treatments and/or diagnostic tools. In parallel, in the last few years there have been significant advances in the field of extracellular vesicles research. Among these vesicles, exosomes of endocytic origin, with a characteristic size ranging from 30-100 nm, carry several atypical secreted proteins in different organisms, including parasitic protozoa. Here, we present experimental evidence for the existence of exosome-like vesicles in parasitic helminths, specifically the trematodes Echinostoma caproni and Fasciola hepatica. These microvesicles are actively released by the parasites and are taken up by host cells. Trematode extracellular vesicles contain most of the proteins previously identified as components of ESP, as confirmed by proteomic, immunogold labeling and electron microscopy studies. In addition to parasitic proteins, we also identify host proteins in these structures. The existence of extracellular vesicles explains the secretion of atypical proteins in trematodes, and the demonstration of their uptake by host cells suggests an important role for these structures in host-parasite communication, as described for other infectious agents.
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页数:9
相关论文
共 52 条
[1]   Fasciola hepatica leucine aminopeptidase, a promising candidate for vaccination against ruminant fasciolosis [J].
Acosta, Daniel ;
Cancela, Martin ;
Piacenza, Lucia ;
Roche, Leda ;
Carmona, Carlos ;
Tort, Jose F. .
MOLECULAR AND BIOCHEMICAL PARASITOLOGY, 2008, 158 (01) :52-64
[2]   ECHINOSTOMA-CAPRONI IN MICE - SHEDDING OF ANTIGENS FROM THE SURFACE OF AN INTESTINAL TREMATODE [J].
ANDRESEN, K ;
SIMONSEN, PE ;
ANDERSEN, BJ ;
BIRCHANDERSEN, A .
INTERNATIONAL JOURNAL FOR PARASITOLOGY, 1989, 19 (01) :111-118
[3]   Identification of proteins in excretory/secretory extracts of Echinostoma friedi (Trematoda) from chronic and acute infections [J].
Bernal, D ;
Carpena, I ;
Espert, AM ;
De la Rubia, JE ;
Esteban, JG ;
Toledo, R ;
Marcilla, A .
PROTEOMICS, 2006, 6 (09) :2835-2843
[4]   Identification of enolase as a plasminogen-binding protein in excretory-secretory products of Fasciola hepatica [J].
Bernal, D ;
de la Rubia, JE ;
Carrasco-Abad, AM ;
Toledo, R ;
Mas-Coma, S ;
Marcilla, A .
FEBS LETTERS, 2004, 563 (1-3) :203-206
[5]  
Bobrie A, 2011, TRAFFIC
[6]  
Clayton C, 2010, ADV EXP MED BIOL, V702, P39, DOI 10.1007/978-1-4419-7841-7_4
[7]   Cell biology - The ins and outs of exosomes [J].
Couzin, J .
SCIENCE, 2005, 308 (5730) :1862-1863
[8]   Helminth vaccines: from mining genomic information for vaccine targets to systems used for protein expression [J].
Dalton, JP ;
Brindley, PJ ;
Knox, DP ;
Brady, CP ;
Hotez, PJ ;
Donnelly, S ;
O'Neill, SM ;
Mulcahy, G ;
Loukas, A .
INTERNATIONAL JOURNAL FOR PARASITOLOGY, 2003, 33 (5-6) :621-640
[9]   Cloning and characterization of a plasminogen-binding surface-associated enolase from Schistosoma bovis [J].
de la Torre-Escudero, Eduardo ;
Manzano-Roman, Raul ;
Perez-Sanchez, Ricardo ;
Siles-Lucas, Mar ;
Oleaga, Ana .
VETERINARY PARASITOLOGY, 2010, 173 (1-2) :76-84
[10]   Nanovesicles from Malassezia sympodialis and Host Exosomes Induce Cytokine Responses - Novel Mechanisms for Host-Microbe Interactions in Atopic Eczema [J].
Gehrmann, Ulf ;
Qazi, Khaleda Rahman ;
Johansson, Catharina ;
Hultenby, Kjell ;
Karlsson, Maria ;
Lundeberg, Lena ;
Gabrielsson, Susanne ;
Scheynius, Annika .
PLOS ONE, 2011, 6 (07)