CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES >
Advances in research on exosomes of Toxoplasma spp.
Received date: 2020-02-22
Online published: 2020-11-12
Supported by
National Natural Science Foundation of China(81702025);Science and Technology Project of Henan Province(182102310220);Doctoral Research Fund of Xinxiang Medical University(XYBSKYZZ201504)
Exosomes are a type of extracellular vesicles secreted by a variety of cells, and contain many active components such as proteins, lipids, and nucleic acids. Studies have shown that a majority of parasites can secrete exosomes, which play important roles in mediating communications between parasites and host cells, regulating host immune responses, as well as transmitting pathogenic factors, drug resistance-associated genes and differentiation factors. In addition, exosome-based therapies and vaccine development are still under the way. In this paper, we summarize the biological characteristics and functions of exosomes secreted by Toxoplasma spp., and discuss their application potentials.
Key words: Toxoplasma; Exosome; Immunomodulation; Application
Peng-ju LI , Su-qiong ZUO , Yu-juan DUAN , Hao-ran LI , Zhen-chao ZHANG , Xiang-rui LI , Shuai WANG . Advances in research on exosomes of Toxoplasma spp.[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2020 , 38(5) : 653 -657 . DOI: 10.12140/j.issn.1000-7423.2020.05.020
| [1] | Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor[J]. Cell, 1983,33(3):967-978. |
| [2] | Johnstone RM, Adam M, Hammond JR, et al. Vesicle folmation during reticulocyte maturationasosiciation of playsma membrane activities with released vesicles (exosomes)[J]. J Biol Chem, 1987,262(19):9412-9420. |
| [3] | Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes[J]. Science, 2020, 367(367):eaau6977. |
| [4] | Johnstone RM, Mathew A, Mason AB, et al. Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins[J]. J Cell Physiol, 1991,147(1):27-36. |
| [5] | Valadi H, Ekstr?m K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells[J]. Nat Cell Biol, 2007,9(6):654-659. |
| [6] | Xu ZK, Li W, Wang YJ. The roles and applications of exosomes in the host defense against Mycobacterium tuberculosis infection[J]. Chin J Animal Vet Sci, 2018,49(9):1803-1809. (in Chinese) |
| [6] | ( 徐兆坤, 李武, 王玉炯. 外泌体在机体抗结核分枝杆菌感染中的作用及其应用[J]. 畜牧兽医学报, 2018,49(9):1803-1809.) |
| [7] | Cazzoli R, Buttitta F, Di Nicola M, et al. microRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer[J]. J Thorac Oncol, 2013,8(9):1156-1162. |
| [8] | Kruger S, Elmageed ZYA, Hawke DH, et al. Molecular characterization of exosome-like vesicles from breast cancer cells[J]. BMC Cancer, 2014,14(1):1-10. |
| [9] | Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake[J]. Cell Mol Neurobiol, 2016,36(3):301-312. |
| [10] | Schorey JS, Cheng Y, Singh PP, et al. Exosomes and other extracellular vesicles in host-pathogen interactions[J]. EMBO Rep, 2015,16(1):24-43. |
| [11] | Coakley G, Buck AH, Maizels RM. Host parasite communications-messages from helminths for the immune system: parasite communication and cell-cell interactions[J]. Mol Biochem Parasitol, 2016,208(1):33-40. |
| [12] | Wowk PF, Zardo ML, Miot HT, et al. Proteomic profiling of extracellular vesicles secreted from Toxoplasma gondii[J]. Proteomics, 2017,17:1600477. |
| [13] | Nilsson J, Skog J, Nordstrand A, et al. Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer[J]. Br J Cancer, 2009,100(10):1603-1607. |
| [14] | Bell BM, Kirk ID, Hiltbrunner S, et al. Designer exosomes as next-generation cancer immunotherapy[J]. Nanomedicine, 2016,12(1):163-169. |
| [15] | Kim MS, Haney MJ, Zhao YL, et al. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells[J]. Nanomedicine, 2016,12(3):655-664. |
| [16] | Kissinger P. Trichomonas vaginalis: a review of epidemiologic, clinical and treatment issues[J]. BMC Infect Dis, 2015,15(1):1-8. |
| [17] | Twu O, de Miguel N, Lustig G, et al. Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host∶ parasite interactions[J]. PLoS Pathog, 2013,9(7):e1003482. |
| [18] | 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. |
| [19] | Coakley G, Maizels RM, Buck AH. Exosomes and other extracellular vesicles: the new communicators in parasite infections[J]. Trends Parasitol, 2015,31(10):477-489. |
| [20] | Nantakomol D, Dondorp AM, Krudsood S, et al. Circulating red cell-derived microparticles in human malaria[J]. J Infect Dis, 2011,203(5):700-706. |
| [21] | Torrecilhas AC, Schumacher RI, Alves MJM, et al. Vesicles as carriers of virulence factors in parasitic protozoan diseases[J]. Microbes Infect, 2012,14(15):1465-1474. |
| [22] | Record M, Carayon K, Poirot M, et al. Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies[J]. Biochim Biophys Acta, 2014,1841(1):108-120. |
| [23] | Marcilla A, Martin-Jaular L, Trelis M, et al. Extracellular vesicles in parasitic diseases[J]. J Extracell Vesicles, 2014,3(1):25040. |
| [24] | El-Assaad F, Wheway J, Hunt NH, et al. Production, fate and pathogenicity of plasma microparticles in murine cerebral malaria[J]. PLoS Pathog, 2014,10(3):e1003839. |
| [25] | Singh B, Daneshvar C. Human infections and detection of Plasmodium knowlesi[J]. Clin Microbiol Rev, 2013,26(2):165-184. |
| [26] | Cronemberger AA, Arag?o FL, de Araujo CF, et al. Extracellular vesicles from Leishmania-infected macrophages confer an anti-infection cytokine-production profile to naive macrophages[J]. PLoS Negl Trop Dis, 2014,8(9):e3161. |
| [27] | Silverman JM, Chan SK, Robinson DP, et al. Proteomic analysis of the secretome of Leishmania donovani[J]. Genome Biol, 2008,9(2):1-21. |
| [28] | da Silveira JF, Abrahamsohn PA, Colli W. Plasma membrane vesicles isolated from epimastigote forms of Trypanosoma cruzi[J]. Biochim Biophys Acta, 1979,550(2):222-232. |
| [29] | Garcia MR, Cura RF, Cabrera CF, et al. Extracellular vesicles shed by Trypanosoma cruzi are linked to small RNA pathways, life cycle regulation, and susceptibility to infection of mammalian cells[J]. Parasitol Res, 2014,113(1):285-304. |
| [30] | Liégeois S, Benedetto A, Garnier JM, et al. The V0-ATPase mediates apical secretion of exosomes containing hedgehog-related proteins in Caenorhabditis elegans[J]. J Cell Biol, 2006,173(6):949-961. |
| [31] | Aline F, Bout D, Amigorena S, et al. Toxoplasma gondii antigen-pulsed-dendritic cell-derived exosomes induce a protective immune response against T. gondii infection[J]. Infect Immun, 2004,72(7):4127-4137. |
| [32] | Ramírez CJ, Cruz MR, Mondragón ME, et al. Proteomic and structural characterization of self-assembled vesicles from excretion/secretion products of Toxoplasma gondii[J]. J Proteom, 2019,208:103490. |
| [33] | Silva VO, Maia MM, Torrecilhas AC, et al. Extracellular vesicles isolated from Toxoplasma gondii induce host immune response[J]. Parasite Immunol, 2018,40(9):e12571. |
| [34] | Pope SM, L?sser C. Toxoplasma gondii infection of fibroblasts causes the production of exosome-like vesicles containing a unique array of mRNA and miRNA transcripts compared to serum starvation[J]. J Extracell Vesicles, 2013,2(1):22484. |
| [35] | Kim MJ, Jung BK, Cho J, et al. Exosomes secreted by Toxoplasma gondii-infected L6 cells: their effects on host cell proliferation and cell cycle changes[J]. Korean J Parasitol, 2016,54(2):147-154. |
| [36] | Li DL, Zou WH, Deng SQ, et al. Analysis of the differential exosomal miRNAs of DC2.4 dendritic cells induced by Toxoplasma gondii infection[J]. Int J Mol Sci, 2019,20(21):5506. |
| [37] | Zhang M, Zhang CG, Ding W. Exosome in cancer diagnosis and treatment[J]. Prog Physiol Sci, 2014,45(5):372-378. (in Chinese) |
| [37] | ( 张敏, 张晨光, 丁卫. 外泌体及其在肿瘤诊疗中的意义[J]. 生理科学进展, 2014,45(5):372-378.) |
| [38] | Villarroya BC, Baixauli F, Gutiérrez VC, et al. Sorting it out: Regulation of exosome loading[J]. Semin Cancer Biol, 2014,28:3-13. |
| [39] | Jewett TJ, Sibley LD. The Toxoplasma proteins MIC2 and M2AP form a hexameric complex necessary for intracellular survival[J]. J Biol Chem, 2004,279(10):9362-9369. |
| [40] | Garcia RN, Lebrun M, Fourmaux MN, et al. The microneme protein MIC3 of Toxoplasma gondii is a secretory adhesin that binds to both the surface of the host cells and the surface of the parasite[J]. Cell Microbiol, 2000,2(4):353-364. |
| [41] | Brecht S, Carruthers VB, Ferguson DJ, et al. The Toxoplasma micronemal protein MIC4 is an adhesin composed of six conserved apple domains[J]. J Biol Chem, 2001,276(6):4119-4127. |
| [42] | Reiss M, Viebig N, Brecht S, et al. Identification and characterization of an escorter for two secretory adhesins in Toxoplasma gondii[J]. J Cell Biol, 2001,152(3):563-578. |
| [43] | Clough B, Frickel EM. The Toxoplasma parasitophorous vacuole: an evolving host-parasite frontier[J]. Trends Parasitol, 2017,33(6):473-488. |
| [44] | Besteiro S, Dubremetz JF, Lebrun M. The moving junction of apicomplexan parasites: a key structure for invasion[J]. Cell Microbiol, 2011,13(6):797-805. |
| [45] | Alexander DL, Mital J, Ward GE, et al. Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles[J]. PLoS Pathog, 2005,1(2):e17. |
| [46] | Mordue DG, Desai N, Dustin ML, et al. Invasion by Toxoplasma gondii establishes a moving junction that selectively excludes host cell plasma membrane proteins on the basis of their membrane anchoring[J]. J Exp Med, 1999,190(12):1783-1792. |
| [47] | Théry C, Duban L, Segura E, et al. Indirect activation of na?ve CD4 + T cells by dendritic cell-derived exosomes [J]. Nat Immunol, 2002,3(12):1156-1162. |
| [48] | Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function[J]. Nat Rev Immunol, 2002,2(8):569-579. |
| [49] | Bhatnagar S, Shinagawa K, Castellino FJ, et al. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo[J]. Blood, 2007,110(9):3234-3244. |
| [50] | Li YW, Liu Y, Xiu FM, et al. Characterization of exosomes derived from Toxoplasma gondii and their functions in modulating immune responses[J]. Int J Nanomed, 2018,13:467-477. |
| [51] | Li YW, Xiu FM, Mou ZZ, et al. Exosomes derived from Toxoplasma gondii stimulate an inflammatory response through JNK signaling pathway[J]. Nanomed Lond Engl, 2018,13(10):1157-1168. |
| [52] | Ni AX, Ma H, Chen JL. Research progress of parasite-derived exosomes[J]. Chin J Animal Vet Sci, 2019,50(5):909-917. (in Chinese) |
| [52] | ( 倪爱心, 麻慧, 陈继兰. 寄生虫来源的外泌体研究进展[J]. 畜牧兽医学报, 2019,50(5):909-917.) |
| [53] | Li YW, Zhou HY. Moving towards improved vaccines for Toxoplasma gondii[J]. Expert Opin Biol Ther, 2018,18(3):273-280. |
| [54] | Beauvillain C, Ruiz S, Guiton R, et al. A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice[J]. Microbes Infect, 2007,9(14/15):1614-1622. |
| [55] | Beauvillain C, Juste MO, Dion S, et al. Exosomes are an effective vaccine against congenital toxoplasmosis in mice[J]. Vaccine, 2009,27(11):1750-1757. |
| [56] | Colineau L, Clos J, Moon KM, et al. Leishmania donovani chaperonin 10 regulates parasite internalization and intracellular survival in human macrophages[J]. Med Microbiol Immunol, 2017,206(3):235-257. |
| [57] | Zhu LH, Zhao JP, Wang JB, et al. MicroRNAs are involved in the regulation of ovary development in the pathogenic blood fluke Schistosoma japonicum[J]. PLoS Pathog, 2016,12(2):e1005423. |
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