弓形虫外泌体研究进展

doi:10.12140/j.issn.1000-7423.2020.05.020

中国寄生虫学与寄生虫病杂志 ›› 2020, Vol. 38 ›› Issue (5): 653-657.doi: 10.12140/j.issn.1000-7423.2020.05.020

弓形虫外泌体研究进展

李朋举¹(), 左素琼¹, 段玉娟¹, 李浩然¹^,², 张振超¹^,², 李祥瑞¹^,²^,³, 王帅¹^,²^,^*()

1 新乡医学院基础医学院,新乡 453003
2 新乡医学院新乡市病原生物学重点实验室,新乡 453003
3 南京农业大学动物医学院,南京 210095

收稿日期:2020-02-22 出版日期:2020-10-30 发布日期:2020-11-12
通讯作者: 王帅
作者简介:李朋举（1997-）,男,本科生,从事弓形虫研究。E-mail:a1251632651@qq.com
基金资助:
国家自然科学基金项目(81702025);河南省科技攻关计划项目(182102310220);新乡医学院博士科研启动基金(XYBSKYZZ201504)

Advances in research on exosomes of Toxoplasma spp.

LI Peng-ju¹(), ZUO Su-qiong¹, DUAN Yu-juan¹, LI Hao-ran¹^,², ZHANG Zhen-chao¹^,², LI Xiang-rui¹^,²^,³, WANG Shuai¹^,²^,^*()

1 School of Basic Medical Sciences, Xinxiang Medical University, Xinxiang 453003, China
2 Xinxiang Key Laboratory of Pathogenic Biology, Xinxiang Medical University, Xinxiang 453003, China
3 College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, China

Received:2020-02-22 Online:2020-10-30 Published:2020-11-12
Contact: WANG Shuai
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)

摘要/Abstract

摘要：

外泌体是一种由多种细胞分泌的细胞外囊泡,包含蛋白质、脂质、核酸等多种活性成分。研究表明,多数寄生虫也能分泌外泌体,其在介导虫体-宿主细胞间信息交流、调节宿主免疫反应、传递致病因子、药物抗性基因和分化因子等方面扮演着重要的角色。此外,基于外泌体进行的治疗和疫苗研制方兴未艾。本文主要对弓形虫外泌体的生物学特征和功能进行总结,并对其应用前景进行阐述。

关键词: 弓形虫, 外泌体, 免疫调节, 应用

Abstract:

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

中图分类号:

R382.5

李朋举, 左素琼, 段玉娟, 李浩然, 张振超, 李祥瑞, 王帅. 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): 653-657.

LI Peng-ju, ZUO Su-qiong, DUAN Yu-juan, LI Hao-ran, ZHANG Zhen-chao, LI Xiang-rui, WANG Shuai. Advances in research on exosomes of Toxoplasma spp.[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2020, 38(5): 653-657.

参考文献 57

[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. doi: 10.1016/0092-8674(83)90040-5 pmid: 6307529
[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. pmid: 3597417
[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. doi: 10.1002/jcp.1041470105 pmid: 2037622
[5]	Valadi H, Ekström 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. doi: 10.1038/ncb1596 pmid: 17486113
[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)
	( 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. doi: 10.1097/JTO.0b013e318299ac32 pmid: 23945385
[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. doi: 10.1186/1471-2407-14-1
[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. doi: 10.1007/s10571-016-0366-z pmid: 27053351
[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. doi: 10.15252/embr.201439363 pmid: 25488940
[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. doi: 10.1016/j.molbiopara.2016.06.003 pmid: 27297184
[12]	Wowk PF, Zardo ML, Miot HT, et al. Proteomic profiling of extracellular vesicles secreted from Toxoplasma gondii[J]. Proteomics, 2017,17:1600477. doi: 10.1002/pmic.v17.15-16
[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. doi: 10.1038/sj.bjc.6605058 pmid: 19401683
[14]	Bell BM, Kirk ID, Hiltbrunner S, et al. Designer exosomes as next-generation cancer immunotherapy[J]. Nanomedicine, 2016,12(1):163-169. doi: 10.1016/j.nano.2015.09.011 pmid: 26500074
[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. doi: 10.1016/j.nano.2015.10.012 pmid: 26586551
[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. doi: 10.1371/journal.ppat.1003482 pmid: 23853596
[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. doi: 10.1016/j.ijpara.2015.09.002 pmid: 26460238
[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. doi: 10.1016/j.pt.2015.06.009 pmid: 26433251
[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. doi: 10.1093/infdis/jiq104 pmid: 21282195
[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. doi: 10.1016/j.micinf.2012.07.008 pmid: 22892602
[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. doi: 10.1016/s0005-2736(97)00174-0 pmid: 9459589
[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. doi: 10.1371/journal.ppat.1003839 pmid: 24651155
[25]	Singh B, Daneshvar C. Human infections and detection of Plasmodium knowlesi[J]. Clin Microbiol Rev, 2013,26(2):165-184. doi: 10.1128/CMR.00079-12 pmid: 23554413
[26]	Cronemberger AA, Aragão 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. doi: 10.1371/journal.pntd.0003161 pmid: 25232947
[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. doi: 10.1016/0005-2736(79)90209-8 pmid: 365244
[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. doi: 10.1007/s00436-013-3655-1 pmid: 24241124
[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. pmid: 16785323
[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. doi: 10.1128/IAI.72.7.4127-4137.2004 pmid: 15213158
[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. doi: 10.1111/pim.12571 pmid: 29974519
[34]	Pope SM, Lässer 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. doi: 10.3347/kjp.2016.54.2.147 pmid: 27180572
[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)
	( 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. pmid: 24769058
[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. doi: 10.1074/jbc.M312590200 pmid: 14670959
[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. pmid: 11207591
[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. doi: 10.1074/jbc.M008294200 pmid: 11053441
[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. doi: 10.1083/jcb.152.3.563 pmid: 11157983
[43]	Clough B, Frickel EM. The Toxoplasma parasitophorous vacuole: an evolving host-parasite frontier[J]. Trends Parasitol, 2017,33(6):473-488. doi: 10.1016/j.pt.2017.02.007 pmid: 28330745
[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. doi: 10.1111/j.1462-5822.2011.01597.x pmid: 21535344
[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. doi: 10.1371/journal.ppat.0010017 pmid: 16244709
[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. doi: 10.1084/jem.190.12.1783 pmid: 10601353
[47]	Théry C, Duban L, Segura E, et al. Indirect activation of naïve CD4 + T cells by dendritic cell-derived exosomes [J]. Nat Immunol, 2002,3(12):1156-1162. doi: 10.1038/ni854 pmid: 12426563
[48]	Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function[J]. Nat Rev Immunol, 2002,2(8):569-579. doi: 10.1038/nri855 pmid: 12154376
[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. doi: 10.1182/blood-2007-03-079152 pmid: 17666571
[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)
	( 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. doi: 10.1080/14712598.2018.1413086 pmid: 29216783
[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. doi: 10.1016/j.vaccine.2009.01.022 pmid: 19186199
[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. doi: 10.1007/s00430-017-0500-7 pmid: 28283754
[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. doi: 10.1371/journal.ppat.1005423 pmid: 26871705

弓形虫外泌体研究进展

Advances in research on exosomes of Toxoplasma spp.

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