Advances in research on parasite proteomics of extracellular vesicles

doi:10.12140/j.issn.1000-7423.2021.04.017

Abstract

Abstract:

Extracellular vesicles are lipid-bilayer vesicles containing proteins, nucleic acids and lipids, secreted by a variety of cells, and are important mediators involving in intercellular interactions. Parasites use extracellular vesicles to secrete proteins during invasion, survival and reproduction, thereby regulating the host immune response to benefit parasitism. This review summarizes the recent research progress on extracellular vesicle proteomics of parasitic helminths and protozoan, in order to provide clues for characterizing the mechanisms of host-parasite interplay.

Key words: Parasite, Extracellular vesicles, Proteomics, Interaction mechanism

CLC Number:

XU Feng-yan, YANG Yong, GAO Xin, LIU Xiao-lei, WANG Yang, LIU Ming-yuan, ZHANG Yuan-yuan, BAI Xue. Advances in research on parasite proteomics of extracellular vesicles[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2021, 39(4): 526-532.

References 56

[1]	Ma L, Li Y, Peng JY, et al. Discovery of the migrasome, an organelle mediating release of cytoplasmic contents during cell migration[J]. Cell Res, 2015, 25(1):24-38.
[2]	Xie F, Zhou X, Fang M, et al. Extracellular vesicles in cancer immune microenvironment and cancer immunotherapy[J]. Adv Sci, 2019, 6(24):1901779. doi: 10.1002/advs.v6.24
[3]	Ofir-Birin Y, Regev-Rudzki N. Extracellular vesicles in parasite survival[J]. Science, 2019, 363(6429):817-818. doi: 10.1126/science.aau4666 pmid: 30792291
[4]	Schwartz C, Fallon PG. Schistosoma ‘eggs-iting’ the host: granuloma formation and egg excretion[J]. Front Immunol, 2018, 9:2492. doi: 10.3389/fimmu.2018.02492
[5]	Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes[J]. Science, 2020, 367(6478):eaau6977. doi: 10.1126/science.aau6977
[6]	Lawrence E, John S, Peter Q, et al. Exosomes[M]. 2020: 179-198.
[7]	Liu L, Yang Y, Gao X, et al. Preliminary prevention effect of Trichinella spiralis extracellular vesicles on TNBS-induced experimental colitis in mice[J]. Prog Vet Med, 2020, 41(5):67-73. (in Chinese)
	(刘蕾, 杨勇, 高欣, 等. 旋毛虫细胞外囊泡对TNBS诱导的小鼠实验性结肠炎的初步干预作用[J]. 动物医学进展, 2020, 41(5):67-73.)
[8]	Nawaz M, Malik MI, Hameed M, et al. Research progress on the composition and function of parasite-derived exosomes[J]. Acta Trop, 2019, 196:30-36. doi: 10.1016/j.actatropica.2019.05.004
[9]	Shen H, Liu CY, Zhao YM. Extracellular vesicles of parasites: research development and prospect[J]. Chin J Parasitol Parasit Dis, 2018, 36(4):413-417. (in Chinese)
	(沈辉, 刘春英, 赵玉敏. 寄生虫细胞外囊泡的研究现状及展望[J]. 中国寄生虫学与寄生虫病杂志, 2018, 36(4):413-417.)
[10]	Huang L, Ye CL, Sheng Y, et al. Advances in research on parasite exosomal miRNA[J]. J Pathog Biol, 2019, 14(9):1115-1118. (in Chinese)
	(黄琳, 叶昌林, 生燕, 等. 外泌体miRNA在寄生虫中的进展[J]. 中国病原生物学杂志, 2019, 14(9):1115-1118.)
[11]	Whitehead B, Boysen AT, Mardahl M, et al. Unique glycan and lipid composition of helminth-derived extracellular vesicles may reveal novel roles in host-parasite interactions[J]. Int J Parasitol, 2020, 50(9):647-654. doi: S0020-7519(20)30120-X pmid: 32526222
[12]	Andrade G, Bertsch DJ, Gazzinelli A, et al. Decline in infection-related morbidities following drug-mediated reductions in the intensity of Schistosoma infection: a systematic review and meta-analysis[J]. PLoS Negl Trop Dis, 2017, 11(2):e0005372. doi: 10.1371/journal.pntd.0005372
[13]	Sun CS, Hu W, Wang TP. Advances in research on schistosome-host interactions mediated by extracellular vesicles[J]. Chin J Parasitol Parasit Dis, 2020, 38(3):378-382. (in Chinese)
	(孙成松, 胡薇, 汪天平. 胞外囊泡介导血吸虫与宿主相互作用的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2020, 38(3):378-382.)
[14]	Sotillo J, Pearson M, Potriquet J, et al. Extracellular vesicles secreted by Schistosoma mansoni contain protein vaccine candidates[J]. Int J Parasitol, 2016, 46(1):1-5. doi: 10.1016/j.ijpara.2015.09.002 pmid: 26460238
[15]	Gómez-Arreaza A, Acosta H, Quiñones W, et al. Extracellular functions of glycolytic enzymes of parasites: unpredicted use of ancient proteins[J]. Mol Biochem Parasitol, 2014, 193(2):75-81. doi: 10.1016/j.molbiopara.2014.02.005
[16]	Caraballo L, Coronado S. Parasite allergens[J]. Mol Immunol, 2018, 100:113-119. doi: S0161-5890(18)30093-2 pmid: 29588070
[17]	Rinaldi G, Morales ME, Alrefaei YN, et al. RNA interference targeting leucine aminopeptidase blocks hatching of Schistosoma mansoni eggs[J]. Mol Biochem Parasitol, 2009, 167(2):118-126. doi: 10.1016/j.molbiopara.2009.05.002
[18]	Kifle DW, Pearson MS, Becker L, et al. Proteomic analysis of two populations of Schistosoma mansoni-derived extracellular vesicles: 15 k pellet and 120 k pellet vesicles[J]. Mol Biochem Parasitol, 2020, 236:111264. doi: 10.1016/j.molbiopara.2020.111264
[19]	Bexkens ML, van Gestel RA, van Breukelen B, et al. Schistosoma mansoni infection affects the proteome and lipidome of circulating extracellular vesicles in the host[J]. Mol Biochem Parasitol, 2020, 238:111296. doi: 10.1016/j.molbiopara.2020.111296
[20]	Nowacki FC, Swain MT, Klychnikov OI, et al. Protein and small non-coding RNA-enriched extracellular vesicles are released by the pathogenic blood fluke Schistosoma mansoni[J]. J Extracell Vesicles, 2015, 4:28665. doi: 10.3402/jev.v4.28665 pmid: 26443722
[21]	Arbelaiz A, Azkargorta M, Krawczyk M, et al. Serum extracellular vesicles contain protein biomarkers for primary sclerosing cholangitis and cholangiocarcinoma[J]. Hepatology, 2017, 66(4):1125-1143. doi: 10.1002/hep.29291 pmid: 28555885
[22]	Corral-Ruiz GM, Sánchez-Torres LE. Fasciola hepatica-derived molecules as potential immunomodulators[J]. Acta Trop, 2020, 210:105548. doi: S0001-706X(20)30014-0 pmid: 32505597
[23]	de la Torre-Escudero E, Gerlach JQ, Bennett APS, et al. Surface molecules of extracellular vesicles secreted by the helminth pathogen Fasciola hepatica direct their internalisation by host cells[J]. PLoS Negl Trop Dis, 2019, 13(1):e0007087. doi: 10.1371/journal.pntd.0007087
[24]	Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes[J]. Curr Opin Cell Biol, 2014, 29:116-125. doi: 10.1016/j.ceb.2014.05.004
[25]	Chaiyadet S, Sotillo J, Smout M, et al. Carcinogenic liver fluke secretes extracellular vesicles that promote cholangiocytes to adopt a tumorigenic phenotype[J]. J Infect Dis, 2015, 212(10):1636-1645. doi: 10.1093/infdis/jiv291 pmid: 25985904
[26]	Alvarez Rojas CA, Kronenberg PA, Aitbaev S, et al. Genetic diversity of Echinococcus multilocularis and Echinococcus granulosus sensu lato in Kyrgyzstan: the A2 haplotype of E. multilocularis is the predominant variant infecting humans[J]. PLoS Negl Trop Dis, 2020, 14(5):e0008242. doi: 10.1371/journal.pntd.0008242
[27]	Nicolao MC, Rodriguez Rodrigues C, Cumino AC. Extracellular vesicles from Echinococcus granulosus larval stage: isolation, characterization and uptake by dendritic cells[J]. PLoS Negl Trop Dis, 2019, 13(1):e0007032. doi: 10.1371/journal.pntd.0007032
[28]	Zhou X, Wang W, Cui F, et al. Extracellular vesicles derived from Echinococcus granulosus hydatid cyst fluid from patients: isolation, characterization and evaluation of immunomodulatory functions on T cells[J]. Int J Parasitol, 2019, 49(13/14):1029-1037. doi: 10.1016/j.ijpara.2019.08.003
[29]	Siles-Lucas M, Sánchez-Ovejero C, González-Sánchez M, et al. Isolation and characterization of exosomes derived from fertile sheep hydatid cysts[J]. Vet Parasitol, 2017, 236:22-33. doi: S0304-4017(17)30032-8 pmid: 28288760
[30]	Arias-Hernández D, García-Jiménez S, Domínguez-Roldan R, et al. Effects of Taenia pisiformis infection and obesity on clinical parameters, organometry and fat distribution in male rabbits[J]. Pathogens, 2020, 9(11):861. doi: 10.3390/pathogens9110861
[31]	Wang LQ, Liu TL, Liang PH, et al. Characterization of exosome-like vesicles derived from Taenia pisiformis cysticercus and their immunoregulatory role on macrophages[J]. Parasites Vectors, 2020, 13(1):318. doi: 10.1186/s13071-020-04186-z
[32]	Sadaow L, Sanpool O, Phosuk I, et al. Molecular identification of Ascaris lumbricoides and Ascaris suum recovered from humans and pigs in Thailand, Lao PDR, and Myanmar[J]. Parasitol Res, 2018, 117(8):2427-2436. doi: 10.1007/s00436-018-5931-6
[33]	Hansen EP, Fromm B, Andersen SD, et al. Exploration of extracellular vesicles from Ascaris suum provides evidence of parasite-host cross talk[J]. J Extracell Vesicles, 2019, 8(1):1578116. doi: 10.1080/20013078.2019.1578116 pmid: 30815237
[34]	Kalra H, Simpson RJ, Ji H, et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation[J]. PLoS Biol, 2012, 10(12):e1001450. doi: 10.1371/journal.pbio.1001450
[35]	Gordon CA, Jones MK, McManus DP. The history of bancroftian lymphatic filariasis in Australasia and Oceania: is there a threat of re-occurrence in mainland Australia?[J]. Trop Med Infect Dis, 2018, 3(2):E58.
[36]	Harischandra H, Yuan W, Loghry HJ, et al. Profiling extracellular vesicle release by the filarial nematode Brugia malayi reveals sex-specific differences in cargo and a sensitivity to ivermectin[J]. PLoS Neglected Trop Dis, 2018, 12(4):e0006438. doi: 10.1371/journal.pntd.0006438
[37]	Sánchez-Valdéz FJ, Padilla A, Wang W, et al. Spontaneous dormancy protects Trypanosoma cruzi during extended drug exposure[J]. Elife, 2018, 7:e34039. doi: 10.7554/eLife.34039
[38]	Cronemberger-Andrade A, Xander P, Soares RP, et al. Trypanosoma cruzi-infected human macrophages shed proinflammatory extracellular vesicles that enhance host-cell invasion via toll-like receptor 2[J]. Front Cell Infect Microbiol, 2020, 10:99. doi: 10.3389/fcimb.2020.00099
[39]	Urményi TP, Silva R, Rondinelli E. The heat shock proteins of Trypanosoma cruzi[J]. Subcell Biochem, 2014, 74:119-135. doi: 10.1007/978-94-007-7305-9_5 pmid: 24264243
[40]	Kengne-Ouafo JA, Sutherland CJ, Binka FN, et al. Immune responses to the sexual stages of Plasmodium falciparum parasites[J]. Front Immunol, 2019, 10:136. doi: 10.3389/fimmu.2019.00136 pmid: 30804940
[41]	Demarta-Gatsi C, Rivkin A, Di Bartolo V, 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[J]. Cell Microbiol, 2019, 21(7):e13021.
[42]	Nandan D, Yi TL, Lopez M, et al. Leishmania EF-1α activates the src homology 2 domain containing tyrosine phosphatase SHP-1 leading to macrophage deactivation[J]. J Biol Chem, 2002, 277(51):50190-50197. pmid: 12384497
[43]	Toda H, Diaz-Varela M, Segui-Barber J, et al. Plasma-derived extracellular vesicles from Plasmodium vivax patients signal spleen fibroblasts via NF-kB facilitating parasite cytoadherence[J]. Nat Commun, 2020, 11:2761. doi: 10.1038/s41467-020-16337-y
[44]	Díaz-Varela M, de Menezes-Neto A, Perez-Zsolt D, et al. Proteomics study of human cord blood reticulocyte-derived exosomes[J]. Sci Rep, 2018, 8(1):14046. doi: 10.1038/s41598-018-32386-2 pmid: 30232403
[45]	Bernabeu M, Lopez FJ, Ferrer M, et al. Functional analysis of Plasmodium vivax VIR proteins reveals different subcellular localizations and cytoadherence to the ICAM-1 endothelial receptor[J]. Cell Microbiol, 2012, 14(3):386-400. doi: 10.1111/j.1462-5822.2011.01726.x pmid: 22103402
[46]	Medina G, Leyán P, da Silva CV, et al. Intra-amoebic localization of Arcobacter butzleri as an endocytobiont of Acanthamoeba castellanii[J]. Arch Microbiol, 2019, 201(10):1447-1452. doi: 10.1007/s00203-019-01699-9 pmid: 31302710
[47]	Lin WC, Tsai CY, Huang JM, et al. Quantitative proteomic analysis and functional characterization of Acanthamoeba castellanii exosome-like vesicles[J]. Parasit Vectors, 2019, 12(1):467. doi: 10.1186/s13071-019-3725-z
[48]	Gonçalves DS, Ferreira MDS, Liedke SC, et al. Extracellular vesicles and vesicle-free secretome of the protozoa Acanthamoeba castellanii under homeostasis and nutritional stress and their damaging potential to host cells[J]. Virulence, 2018, 9(1):818-836. doi: 10.1080/21505594.2018.1451184 pmid: 29560793
[49]	Zhang Y, Lai BS, Juhas M, et al. Toxoplasma gondii secretory proteins and their role in invasion and pathogenesis[J]. Microbiol Res, 2019, 227:126293. doi: S0944-5013(19)30471-9 pmid: 31421715
[50]	Wowk PF, Zardo ML, Miot HT, et al. Proteomic profiling of extracellular vesicles secreted from Toxoplasma gondii[J]. Proteomics, 2017, 17(15/16):1600477. doi: 10.1002/pmic.v17.15-16
[51]	Li PJ, Zuo SQ, Duan YJ, et al. Advances in research on exosomes of Toxoplasma spp.[J]. Chin J Parasitol Parasit Dis, 2020, 38(5):653-658. (in Chinese)
	(李朋举, 左素琼, 段玉娟, 等. 弓形虫外泌体研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2020, 38(5):653-658.)
[52]	Ramírez-Flores CJ, Cruz-Mirón R, Mondragón-Castelán ME, et al. Proteomic and structural characterization of self-assembled vesicles from excretion/secretion products of Toxoplasma gondii[J]. J Proteomics, 2019, 208:103490. doi: S1874-3919(19)30262-3 pmid: 31434009
[53]	Leroux LP, Dasanayake D, Rommereim LM, et al. Secreted Toxoplasma gondii molecules interfere with expression of MHC-II in interferon gamma-activated macrophages[J]. Int J Parasitol, 2015, 45(5):319-332. doi: 10.1016/j.ijpara.2015.01.003
[54]	Rezaei F, Sarvi S, Sharif M, et al. A systematic review of Toxoplasma gondii antigens to find the best vaccine candidates for immunization[J]. Microb Pathog, 2019, 126:172-184. doi: 10.1016/j.micpath.2018.11.003
[55]	Calero-Bernal R, Horcajo P, Hernández M, et al. Absence of Neospora caninum DNA in human clinical samples, Spain[J]. Emerg Infect Dis, 2019, 25(6):1226-1227. doi: 10.3201/eid2506.181431 pmid: 31107232
[56]	Li S, Gong P, Tai L, et al. Extracellular vesicles secreted by Neospora caninum are recognized by Toll-Like receptor 2 and modulate host cell innate immunity through the MAPK signaling pathway[J]. Front Immunol, 2018, 9:1633. doi: 10.3389/fimmu.2018.01633