Abstract
Gymnophalloides seoi worms were rapidly expelled from C57BL/6 mice within days 3–6 post-infection probably due to operation of mucosal innate immunity. To understand better the mucosal immunity related to worm expulsion from the host, we isolated exosomes of G. seoi metacercariae and investigated their role in induction of mRNA and protein expression of several Toll-like receptors and mucin-related factors in vitro. G. seoi-secreted exosomes were collected using differential ultracentrifugation, and cellular internalization of the exosomes into HT-29 intestinal epithelial cells was visualized by confocal microscopy. The expression of TLR2 and MUC2 in HT-29 cells was up-regulated in stimulation with the exosomes. We suggest that G. seoi-secreted exosomes offer a new point of view in the mechanism of worm expulsion from the host through enhancement of TLR2 and MUC2 expression.
References
Abe T, Sugaya H, Ishida K, Khan WI, Tasdemir I, Yoshimura K (1993) Intestinal protection against Strongyloides ratti and mastocytosis induced by administration of interleukin-3 in mice. Immunology 80:116–121
Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10:131–144
Abreu MT, Arnold ET, Thomas LS, Gonsky R, Zhou Y, Hu B, Arditi M (2002) TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 277:20431–20437
Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511
Allen A, Hutton DA, Pearson JP (1998) The MUC2 gene product: a human intestinal mucin. Int J Biochem Cell Biol 30:797–801
Beaver PC, Jung RC, Cupp EW (1984) Clinical parasitology, 9th edn. Lea & Febiger, Philadelphia
Chai JY, Choi MH, Yu JR, Lee SH (2003) Gymnophalloides seoi: a new human intestinal trematode. Trends Parasitol 19:109–112
Coakley G, Maizels RM, Buck AH (2015) Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol 31:477–489
Deolindo P, Evans-Osses I, Ramirez MI (2013) Microvesicles and exosomes as vehicles between protozoan and host cell communication. Biochem Soc Trans 41:252–257
Guk SM, Lee JH, Kim HJ, Kim WH, Shin EH, Chai JY (2009) CD4+ T-cell-dependent goblet cell proliferation and expulsion of Gymnophalloides seoi from the intestine of C57BL/6 mice. J Parasitol 95:581–590
Lee KD, Guk SM, Chai JY (2010) Toll-like receptor 2 and Muc2 expression on human intestinal epithelial cells by Gymnophalloides seoi adult antigen. J Parasitol 96:58–66
Lee SH, Chai JY (2001) A review of Gymnophalloides seoi (Digenea: Gymnophallidae) and human infections in the Republic of Korea. Korean J Parasitol 39:85–118
Lee SH, Chai JY, Lee HJ, Hong ST, Yu JR, Sohn WM, Kho WG, Choi MH, Lim YJ (1994) High prevalence of Gymnophalloides seoi infection in a village on a southwestern island of the Republic of Korea. Am J Trop Med Hyg 51:281–285
Lee SH, Park SK, Seo M, Guk SM, Choi MH, Chai JY (1997) Susceptibility of various species of animals and strains of mice to Gymnophalloides seoi infection and the effects of immunosuppression in C3H/HeN mice. J Parasitol 83:883–886
Marcilla A, Trelis M, Cortés A, Sotillo J, Cantalapiedra F, Minguez MT, Valero ML, Sánchez del Pino MM, Muñoz-Antoli C, Toledo R, Bernal D (2012) Extracellular vesicles from parasitic helminths contain specific excretory/secretory proteins and are internalized in intestinal host cells. PLoS One 7:e45974
Moncada DM, Kammanadiminti SJ, Chadee K (2003) Mucin and toll-like receptors in host defense against intestinal parasites. Trends Parasitol 19:305–311
Perez-Hernandez J, Forner MJ, Pinto C, Chaves FJ, Cortes R, Redon J (2015) Increased urinary exosomal microRNAs in patients with systemic lupus erythematosus. PLoS One 10:e0138618
Riaz F, Cheng G (2017) Exosome-like vesicles of helminths: implication of pathogenesis and vaccine development. Ann Transl Med 5:175
Rose MC, Voynow JA (2006) Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 86:245–278
Schorey JS, Cheng Y, Singh PP, Smith VL (2015) Exosomes and other extracellular vesicles in host-pathogen interactions. EMBO Rep 16:24–43
Seo M, Guk SM, Han ET, Chai JY (2003) Role of intestinal goblet cells in the expulsion of Gymnophalloides seoi from mice. J Parasitol 89:1080–1082
Sheng YH, Hasnain SZ, Png CW, McGuckin MA, Lindén SK (2012) Techniques for assessment of interactions of mucins with microbes and parasites in vitro and in vivo. Methods Mol Biol 842:297–312
Theodoropoulos G, Hicks SJ, Corfield AP, Miller BG, Carrington SD (2001) The role of mucins in host-parasite interactions: part II - helminth parasites. Trends Parasitol 17:130–135
Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581–593
Trelis M, Galiano A, Bolado A, Toledo R, Marcilla A, Bernal D (2016) Subcutaneous injection of exosomes reduces symptom severity and mortality induced by Echinostoma caproni infection in BALB/c mice. Int J Parasitol 46:799–808
Venugopal PG, Nutman TB, Semnani RT (2009) Activation and regulation of toll-like receptors (TLRs) by helminth parasites. Immunol Res 43:252–263
Wang L, Li Z, Shen J, Liu Z, Liang J, Wu X, Sun X, Wu Z (2015) Exosome-like vesicles derived by Schistosoma japonicum adult worms mediates M1 type immune- activity of macrophage. Parasitol Res 114:1865–1873
Funding
This study was funded by project no. 2011-0024699 from National Research Foundation of Korea (NRFK).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All animal experiments were approved by the Committee on the Ethics of Animal Experiments at Seoul National University (permit no. SNU-121010-4-1).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Xing-Quan Zhu
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Song, H., Jung, BK., Cho, J. et al. Worm expulsion of Gymnophalloides seoi from C57BL/6 mice: role of metacercarial exosomes in upregulating TLR2 and MUC2 expression in intestinal tissues. Parasitol Res 117, 3309–3314 (2018). https://doi.org/10.1007/s00436-018-6002-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-6002-8