Advances in research on schistosome-host interactions mediated by extracellular vesicles

doi:10.12140/j.issn.1000-7423.2020.03.019

Abstract

Abstract:

Extracellular vesicles are lipid-bilayer vesicles that are released by cells into the extracellular space. They contain bioactive molecules such as proteins, lipids, DNA and RNA, and can transfer effector molecules via binding to receptors of target cells or by direct fusing to, thus exerting biological function. Extracellular vesicles as a new type of intercellular signal transduction mechanism, play a critical role in regulating interaction between schistosome and host. This review underlines the researches advance on extracellular vesicles in regard to the classification, origin, structure and functions, and the role to mediate the parasite-host interactions upon secreted from schistosomes at different developmental stages, thus providing new ideas for researches on the prevention and control of schistosomiasis.

Key words: Schistosome, Extracellular vesicle, Host, Interaction mechanism

CLC Number:

R383.2+4

SUN Cheng-song, HU Wei, WANG Tian-ping. Advances in research on schistosome-host interactions mediated by extracellular vesicles[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2020, 38(3): 378-382.

Figures/Tables 1

References 45

[1]	Podolska M, Nadolna K. Acetylcholinesterase secreted by Anisakis simplex larvae (Nematoda : Anisakidae) parasitizing herring, Clupea harengus: an inverse relationship of enzyme activity in the host-parasite system[J]. Parasitol Res, 2014,113(6):2231-2238.
[2]	Yang X, Liu J, Yue Y, et al. Cloning, expression and characterisation of a type Ⅱ cystatin from Schistosoma japonicum, which could regulate macrophage activation[J]. Parasitol Res, 2014,113(11):3985-3992.
[3]	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.
[4]	Wang J, Zhao F, Yu CX, et al. Identification of proteins inducing short-lived antibody responses from excreted/secretory products of Schistosoma japonicum adult worms by immunoproteomic analysis[J]. J Proteomics, 2013,87:53-67.
[5]	Cao XD, Fu ZQ, Zhang M, et al. Excretory/secretory proteome of 14-day schistosomula, Schistosoma japonicum[J]. J Proteomics, 2016,130:221-230.
[6]	Dvo?ák J, Fajtová P, Ulrychová L, et al. Excretion/secretion products from Schistosoma mansoni adults, eggs and schistosomula have unique peptidase specificity profiles[J]. Biochimie, 2016,122:99-109.
[7]	Szempruch AJ, Sykes SE, Kieft R, et al. Extracellular vesicles from Trypanosoma brucei mediate virulence factor transfer and cause host Anemia[J]. Cell, 2016,164(1/2):246-257.
[8]	Regev-Rudzki N, Wilson DW, Carvalho TG, et al. Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles[J]. Cell, 2013,153(5):1120-1133.
[9]	Ghosh J, Bose M, Roy S, et al. Leishmania donovani targets Dicer1 to downregulate miR-122, lower serum cholesterol, and facilitate murine liver infection[J]. Cell Host Microbe, 2013,13(3):277-288.
[10]	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.
[11]	Buck AH, Coakley G, Simbari F, et al. Erratum: Exosomes secreted by nematode parasites transfer small RNAs to mammalian cells and modulate innate immunity[J]. Nat Commun, 2015,6:8772.
[12]	Guenat D, Hermetet F, Prétet JL, et al. Exosomes and other extracellular vesicles in HPV transmission and carcinogenesis[J]. Viruses, 2017,9(8):E211.
[13]	Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends[J]. J Cell Biol, 2013,200(4):373-383.
[14]	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.
[15]	Bobrie A, Colombo M, Raposo G, et al. Exosome secretion: molecular mechanisms and roles in immune responses[J]. Traffic, 2011,12(12):1659-1668.
[16]	Simons M, Raposo G. Exosomes: vesicular carriers for intercellular communication[J]. Curr Opin Cell Biol, 2009,21(4):575-581.
[17]	Hauser P, Wang S, Didenko VV. Apoptotic bodies: selective detection in extracellular vesicles[J]. Methods Mol Biol, 2017,1554:193-200.
[18]	Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines[J]. J Extracell Vesicles, 2018,7(1):1535750.
[19]	Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes)[J]. J Biol Chem, 1987,262(19):9412-9420.
[20]	Keller S, Sanderson MP, Stoeck A, et al. Exosomes: from biogenesis and secretion to biological function[J]. Immunol Lett, 2006,107(2):102-108.
[21]	Skog J, Würdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers[J]. Nat Cell Biol, 2008,10(12):1470-1476.
[22]	Cestari I, Ansa-Addo E, Deolindo P, et al. Trypanosoma cruzi immune evasion mediated by host cell-derived microvesicles[J]. J Immunol, 2012,188(4):1942-1952.
[23]	Théry C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids[J]. Curr Protoc Cell Biol, 2006, Chapter(3): Unit 3. 22.
[24]	Anderson HC. Vesicles associated with calcification in the matrix of epiphyseal cartilage[J]. J Cell Biol, 1969,41(1):59-72.
[25]	Harding CV, Heuser JE, Stahl PD. Exosomes: looking back three decades and into the future[J]. J Cell Biol, 2013,200(4):367-371.
[26]	Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes[J]. J Cell Biol, 1983,97(2):329-339.
[27]	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.
[28]	Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles[J]. J Exp Med, 1996,183(3):1161-1172.
[29]	Deng ZB, Zhuang XY, Ju SW, et al. Exosome-like nanoparticles from intestinal mucosal cells carry prostaglandin E2 and suppress activation of liver NKT cells[J]. J Immunol, 2013,190(7):3579-3589.
[30]	Montecalvo A, Larregina AT, Shufesky WJ, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes[J]. Blood, 2012,119(3):756-766.
[31]	Chen G, Huang AC, Zhang W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response[J]. Nature, 2018,560(7718):382-386.
[32]	Aswad H, Forterre A, Wiklander OP, et al. Exosomes participate in the alteration of muscle homeostasis during lipid-induced insulin resistance in mice[J]. Diabetologia, 2014,57(10):2155-2164.
[33]	Atay S, Banskota S, Crow J, et al. Oncogenic KIT-containing exosomes increase gastrointestinal stromal tumor cell invasion[J]. Proc Natl Acad Sci USA, 2014,111(2):711-716.
[34]	Fong MY, Zhou WY, Liu L, et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis[J]. Nat Cell Biol, 2015,17(2):183-194.
[35]	Zocco D, Ferruzzi P, Cappello F, et al. Extracellular vesicles as shuttles of tumor biomarkers and anti-tumor drugs[J]. Front Oncol, 2014,4:267.
[36]	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.
[37]	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.
[38]	Zhu LH, Liu JT, Dao JW, et al. Molecular characterization of S. japonicum exosome-like vesicles reveals their regulatory roles in parasite-host interactions[J]. Sci Rep, 2016,6:25885.
[39]	Liu JT, Zhu LH, Wang JB, et al. Schistosoma japonicum extracellular vesicle miRNA cargo regulates host macrophage functions facilitating parasitism[J]. PLoS Pathog, 2019,15(6):e1007817.
[40]	Wang LF, Li ZT, Shen J, et al. Exosome-like vesicles derived by Schistosoma japonicum adult worms mediates M1 type immune-activity of macrophage[J]. Parasitol Res, 2015,114(5):1865-1873.
[41]	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.
[42]	Zhu SL, Wang S, Lin Y, et al. Release of extracellular vesicles containing small RNAs from the eggs of Schistosoma japonicum[J]. Parasit Vectors, 2016,9(1):574.
[43]	Chen YJ, Giri BR, Li X, et al. Preliminary evaluation of the diagnostic potential of Schistosoma japonicum extracellular vesicle proteins for schistosomiasis japonica[J]. Acta Trop, 2020,201:105184.
[44]	Meningher T, Lerman G, Regev-Rudzki N, et al. Schistosomal MicroRNAs isolated from extracellular vesicles in sera of infected patients: a new tool for diagnosis and follow-up of human schistosomiasis[J]. J Infect Dis, 2017,215(3):378-386.
[45]	Lv S, Xu J, Cao CL, et al. China fighting against schistosomiasis for 70 years: progress and experience[J]. Chin J Parasitol Parasit Dis, 2019,37(5):514-519. (in Chinese)
[45]	( 吕山, 吕山, 曹淳力, 等. 我国血吸虫病防治70年历程与经验[J]. 中国寄生虫学与寄生虫病杂志, 2019,37(5):514-519.)

EVs类型	外泌体	微囊泡	凋亡小体
尺寸	30~100 nm	100~1 000 nm	1~5 μm
形态	杯状	形态多样	形态多样
离心力	100 000~200 000 g	10 000~20 000 g	< 10 000 g
蛋白标志物	CD63、 CD9、 CD81、肿瘤特异性糖蛋白（tumor-specific glycoprotein 101,Tsg101）、 ALG-2相互作用蛋白X（ALG-2-interacting protein X,Alix）	蛋白质、非编码 RNA、 mRNA	组蛋白
主要组分	蛋白质、非编码 RNA、 mRNA	蛋白质、非编码RNA、 mRNA	蛋白质、非编码RNA、 mRNA、 DNA
产生机制	细胞内多泡体直接与胞质膜融合以胞吐形式释放	细胞质膜向外以脱落或出芽形式产生	细胞程序性死亡或凋亡过程中形成