Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Increased Innate Lymphoid Cell 3 and IL-17 Production in Mouse Lamina Propria Stimulated with Giardia lamblia

  • Lee, Hye-Yeon (Department of Environmental Medical Biology and Institute of Tropical Medicine, Brain Korea 21 PLUS Project for Medical Science, Yonsei University College of Medicine) ;
  • Park, Eun-Ah (Department of Environmental Medical Biology and Institute of Tropical Medicine, Brain Korea 21 PLUS Project for Medical Science, Yonsei University College of Medicine) ;
  • Lee, Kyung-Jo (Department of Life Science, Sogang University) ;
  • Lee, Kyu-Ho (Department of Life Science, Sogang University) ;
  • Park, Soon-Jung (Department of Environmental Medical Biology and Institute of Tropical Medicine, Brain Korea 21 PLUS Project for Medical Science, Yonsei University College of Medicine)
  • Received : 2019.03.26
  • Accepted : 2019.05.23
  • Published : 2019.06.30
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Abstract

Innate lymphoid cells (ILCs) are key players during an immune response at the mucosal surfaces, such as lung, skin, and gastrointestinal tract. Giardia lamblia is an extracellular protozoan pathogen that inhabits the human small intestine. In this study, ILCs prepared from the lamina propria of mouse small intestine were incubated with G. lamblia trophozoites. Transcriptional changes in G. lamblia-exposed ILCs resulted in identification of activation of several immune pathways. Secretion of interleukin (IL)-17A, IL-17F, $IL-1{\beta}$, and interferon-${\gamma}$ was increased, whereas levels of IL-13, IL-5, and IL-22, was maintained or reduced upon exposure to G. lamblia. Goup 3 ILC (ILC3) was found to be dominant amongst the ILCs, and increased significantly upon co-cultivation with G. lamblia trophozoites. Oral inoculation of G. lamblia trophozoites into mice resulted in their presence in the small intestine, of which, the highest number of parasites was detected at the 5 days-post infection. Increased ILC3 was observed amongst the ILC population at the 5 days-post infection. These findings indicate that ILC3 from the lamina propria secretes IL-17 in response to G. lamblia, leading to the intestinal pathology observed in giardiasis.

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References

  1. Kraft MR, Klotz C, Bucker R, Schulzke JD, Aebischer T. Giardia's epithelial cell interaction in vitro: mimicking asymptomatic infection? Front Cell Infect Microbiol 2017; 7: 421. https://doi.org/10.3389/fcimb.2017.00421
  2. Fink MY, Singer SM. The intersection of immune responses, microbiota, and pathogenesis in giardiasis. Trends Parasitol 2017; 33: 901-913. https://doi.org/10.1016/j.pt.2017.08.001
  3. Eckmann L. Mucosal defense against Giardia. Parasite Immunol 2003 25: 259-270. https://doi.org/10.1046/j.1365-3024.2003.00634.x
  4. Eckmann L, Laurent F, Langford TD, Hetsko ML, Smith JR, Kagnoff MF, Gillin FD. Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J Immunol 2000; 1643: 1478-1487.
  5. Stadelmann B, Merino MC, Persson L, Svard SG. Arginine consumption by the intestinal parasite Giardia intestinalis reduces proliferation of intestinal epithelial cells. PLoS One 2012; 79: e45325.
  6. Zhou P, Li E, Zhu N, Robertson J, Nash T, Singer SM. Role of interleukin-6 in the control of acute and chronic Giardia lamblia infections in mice. Infect Immun 2003; 71: 1566-1568. https://doi.org/10.1128/IAI.71.3.1566-1568.2003
  7. Solaymani-Mohammadi S, Singer SM. Host immunity and pathogen strain contribute to intestinal disaccharidase impairment following gut infection. J Immunol 2011; 187: 3769-3775. https://doi.org/10.4049/jimmunol.1100606
  8. Grit GH, Van Coppernolle S, Devriendt B, Geurden T, Dreesen L, Hope J, Vercruysse J, Cox E, Geldhof P, Claerebout E. Evaluation of cellular and humoral systemic immune response against Giardia duodenalis infection in cattle. Vet Parasitol 2014; 202: 145-155. https://doi.org/10.1016/j.vetpar.2014.03.012
  9. Saghaug CS, Sornes S, Peirasmaki D, Svard S, Langeland N, Hanevik K. Human memory CD4+ T-cell immune responses against Giardia lamblia. Clin. Vaccine Immunol 2015; 23: 11-18. https://doi.org/10.1128/CVI.00419-15
  10. Dreesen L, De Bosscher K, Grit G, Staels B, Lubberts E, Bauge E, Bauge E, Geldhof P. Giardia muris infection in mice is associated with a protective interleukin 17A response and induction of peroxisome proliferator-activated receptor alpha. Infect Immun 2014; 82: 3333-3340. https://doi.org/10.1128/IAI.01536-14
  11. Paerewijck O, Maertens B, Dreesen L, Van Meulder F, Peelaers I, Ratman D, Li RW, Lubberts E, De Bosscher K, Geldhof P. Interleukin-17 receptor A (IL-17RA) as a central regulator of the protective immune response against Giardia. Sci Rep 2017; 7: 8520. https://doi.org/10.1038/s41598-017-08590-x
  12. Eberl G, Colonna M, Di Santo JP, McKenzie AN. Innate lymphoid cells: a new paradigm in immunology. Science 2015; 348: aaa6566. https://doi.org/10.1126/science.aaa6566
  13. Keister DB. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 1983; 77: 487-488. https://doi.org/10.1016/0035-9203(83)90120-7
  14. Moro K, Ealey KN, Kabata H, Koyasu S. Isolation and analysis of group 2 innate lymphoid cells in mice. Nat Protoc 2015; 10: 792-806. https://doi.org/10.1038/nprot.2015.047
  15. Buzzelli JN, Chalinor HV, Pavlic DI, Sutton P, Menheniott TR, Giraud AS, Judd LM. IL33 Is a Stomach Alarmin That Initiates a Skewed Th2 Response to Injury and Infection. Cell Mol Gastroenterol Hepatol 2015; 1: 203-221. https://doi.org/10.1016/j.jcmgh.2014.12.003
  16. De Obaldia ME, Bhandoola A. Transcriptional regulation of innate and adaptive lymphocyte lineages. Annu Rev Immunol 2015; 33: 607-642. https://doi.org/10.1146/annurev-immunol-032414-112032
  17. Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie AN, Mebius RE, Powrie F, Vivier E. Innate lymphoid cells--a proposal for uniform nomenclature. Nat Rev Immunol 2013; 13: 145-149. https://doi.org/10.1038/nri3365
  18. Singer SM. Control of giardiasis by interleukin-17 in humans and mice--are the questions all answered? Clin Vaccine Immunol 2015; 23: 2-5. https://doi.org/10.1128/CVI.00648-15
  19. Bando JK, Colonna M. Innate lymphoid cell function in the context of adaptive immunity. Nat Immunol 2016; 17: 783-789. https://doi.org/10.1038/ni.3484
  20. Robinette ML, Fuchs A, Cortez VS, Lee JS, Wang Y, Durum SK, Gilfillan S, Colonna M. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat Immunol 2015; 16: 306-317. https://doi.org/10.1038/ni.3094
  21. Drake LY, Kita H. Group 2 innate lymphoid cells in the lung. Adv Immunol 2014; 124: 1-16. https://doi.org/10.1016/B978-0-12-800147-9.00001-7
  22. Hepworth MR, Monticelli LA, Fung TC, Ziegler CG, Grunberg S, Sinha R, Mantegazza AR, Ma HL, Crawford A, Angelosanto JM, Wherry EJ, Koni PA, Bushman FD, Elson CO, Eberl G, Artis D, Sonnenberg GF. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 2013; 498: 113-117. https://doi.org/10.1038/nature12240
  23. Melo-Gonzalez F, Hepworth MR. Functional and phenotypic heterogeneity of group 3 innate lymphoid cells. Immunology 2017; 150: 265-275. https://doi.org/10.1111/imm.12697
  24. Licona-Limon P, Kim LK, Palm NW, Flavell RA. TH2, allergy and group 2 innate lymphoid cells. Nat Immunol 2013; 14: 536-542. https://doi.org/10.1038/ni.2617
  25. von Burg N, Chappaz S, Baerenwaldt A, Horvath E, Bose Dasgupta S, Ashok D, Pieters J, Tacchini-Cottier F, Rolink A, Acha-Orbea H, Finke D. Activated group 3 innate lymphoid cells promote T-cell-mediated immune responses. Proc Natl Acad Sci USA 2014; 111: 12835-12840. https://doi.org/10.1073/pnas.1406908111
  26. Kruglov AA, Grivennikov SI, Kuprash DV, Winsauer C, Prepens S, Seleznik GM, Eberl G, Littman DR, Heikenwalder M, Tumanov AV, Nedospasov SA. Nonredundant function of soluble $LT{\alpha}3$ produced by innate lymphoid cells in intestinal homeostasis. Science 2013; 342: 113-119. https://doi.org/10.1126/science.342.6154.11-c

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