Interleukin-17 producing cells in swine induced by microbiota during the early postnatal period - a brief research report
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
37799720
PubMed Central
PMC10548118
DOI
10.3389/fimmu.2023.1214444
Knihovny.cz E-zdroje
- Klíčová slova
- T cells, germ-free, interleukin-17, postnatal, swine,
- MeSH
- interleukin-17 * metabolismus MeSH
- mikrobiota * MeSH
- prasata MeSH
- receptory antigenů T-buněk gama-delta metabolismus MeSH
- T-lymfocyty - podskupiny MeSH
- výzkumná zpráva MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- interleukin-17 * MeSH
- receptory antigenů T-buněk gama-delta MeSH
Interleukin-17A (IL-17) is a pro-inflammatory cytokine involved in the immune response to many pathogens playing also a role in certain chronic and autoimmune diseases. The presented study focused on the early postnatal development of IL-17 producing cells in swine. In agreement with previous studies, αβ T-helper (CD3+CD4+) and γδ T (CD3+TCRγδ+) cells were found to be the major producers of IL-17. In newborn conventional piglets, αβ T-helper cells positive for IL-17 were almost undetectable, but their frequency increased markedly with age in all issues examined, i.e., blood, spleen, and mesenteric lymph nodes (MLN). Additional analyses of CD8 and CD27 expression showed that the main αβ T-helper producers of IL-17 has CD8+CD27- phenotype in all tissues. IL-17 positive CD8+CD27+ αβ T-helper subpopulation was found only in blood and spleen. The production of IL17 in CD8-CD27+ αβ T-helper cells was always minor. In contrast, γδ T cells positive for IL-17 did not show a similar age-dependent increase in blood and spleen, whereas they increased in MLN. Because of the age-dependent increase in conventional animals, we included a comparison with germ-free piglets to show that the increase in IL-17 positive cells was clearly depended on the presence of the microbiota as the production in germ-free animals was negligible without any age-dependent increase.
Department of Infectious Diseases and Preventive Medicine Veterinary Research Institute Brno Czechia
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Moseley TA, Haudenschild DR, Rose L, Reddi AH. Interleukin-17 family and IL-17 receptors. Cytokine Growth Factor Rev (2003) 14:155–74. doi: 10.1016/S1359-6101(03)00002-9 PubMed DOI
Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, et al. . Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol (2005) 6:1123–32. doi: 10.1038/NI1254 PubMed DOI
Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, et al. . A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol (2005) 6:1133–41. doi: 10.1038/NI1261 PubMed DOI PMC
Roark CL, Simonian PL, Fontenot AP, Born WK, O’Brien RL. gammadelta T cells: an important source of IL-17. Curr Opin Immunol (2008) 20:353–7. doi: 10.1016/J.COI.2008.03.006 PubMed DOI PMC
Pandya AD, Al-Jaderi Z, Høglund RA, Holmøy T, Harbo HF, Norgauer J, et al. . Identification of human NK17/NK1 cells. PloS One (2011) 6(10):e26780. doi: 10.1371/JOURNAL.PONE.0026780 PubMed DOI PMC
Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov II, et al. . Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med (2009) 206:35–41. doi: 10.1084/JEM.20072713 PubMed DOI PMC
Godinez I, Raffatellu M, Chu H, Paixão TA, Haneda T, Santos RL, et al. . Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect Immun (2009) 77:387–98. doi: 10.1128/IAI.00933-08 PubMed DOI PMC
Siegemund S, Schütze N, Schulz S, Wolk K, Nasilowska K, Straubinger RK, et al. . Differential IL-23 requirement for IL-22 and IL-17A production during innate immunity against Salmonella enterica serovar Enteritidis. Int Immunol (2009) 21:555–65. doi: 10.1093/INTIMM/DXP025 PubMed DOI
Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, Luger D, et al. . Cutting edge: NKT cells constitutively express IL-23 receptor and RORgammat and rapidly produce IL-17 upon receptor ligation in an IL-6-independent fashion. J Immunol (2008) 180:5167–71. doi: 10.4049/JIMMUNOL.180.8.5167 PubMed DOI PMC
Katoh S, Kitazawa H, Shimosato T, Tohno M, Kawai Y, Saito T. Cloning and characterization of Swine interleukin-17, preferentially expressed in the intestines. J Interferon Cytokine Res (2004) 24:553–9. doi: 10.1089/JIR.2004.24.553 PubMed DOI
Pilon C, Levast B, Meurens F, Le Vern Y, Kerboeuf D, Salmon H, et al. . CD40 engagement strongly induces CD25 expression on porcine dendritic cells and polarizes the T cell immune response toward Th1. Mol Immunol (2009) 46:437–47. doi: 10.1016/J.MOLIMM.2008.10.014 PubMed DOI
Kiros TG, van Kessel J, Babiuk LA, Gerdts V. Induction, regulation and physiological role of IL-17 secreting helper T-cells isolated from PBMC, thymus, and lung lymphocytes of young pigs. Vet Immunol Immunopathol (2011) 144:448–54. doi: 10.1016/J.VETIMM.2011.08.021 PubMed DOI
Stepanova H, Mensikova M, Chlebova K, Faldyna M. CD4+ and γδTCR+ T lymphocytes are sources of interleukin-17 in swine. Cytokine (2012) 58:152–7. doi: 10.1016/J.CYTO.2012.01.004 PubMed DOI
Manirarora JN, Walker KE, Patil V, Renukaradhya GJ, LaBresh J, Sullivan Y, et al. . Development and characterization of new monoclonal antibodies against porcine interleukin-17A and interferon-gamma. Front Immunol (2022) 13:786396/FULL. doi: 10.3389/FIMMU.2022.786396/FULL PubMed DOI PMC
Sassu EL, Ladinig A, Talker SC, Stadler M, Knecht C, Stein H, et al. . Frequency of Th17 cells correlates with the presence of lung lesions in pigs chronically infected with Actinobacillus pleuropneumoniae. Vet Res (2017) 48:1–16. doi: 10.1186/S13567-017-0411-Z PubMed DOI PMC
Sedlak C, Patzl M, Saalmüller A, Gerner W. CD2 and CD8α define porcine γδ T cells with distinct cytokine production profiles. Dev Comp Immunol (2014) 45:97–106. doi: 10.1016/J.DCI.2014.02.008 PubMed DOI
Karalyan Z, Voskanyan H, Ter-Pogossyan Z, Saroyan D, Karalova E. IL-23/IL-17/G-CSF pathway is associated with granulocyte recruitment to the lung during African swine fever. Vet Immunol Immunopathol (2016) 179:58–62. doi: 10.1016/J.VETIMM.2016.08.005 PubMed DOI
Li C, Yang P, Sun Y, Li T, Wang C, Wang Z, et al. . IL-17 response mediates acute lung injury induced by the 2009 pandemic influenza A (H1N1) virus. Cell Res (2012) 22:528–38. doi: 10.1038/CR.2011.165 PubMed DOI PMC
Luo Y, Van Nguyen U, de la Fe Rodriguez PY, Devriendt B, Cox E. F4+ ETEC infection and oral immunization with F4 fimbriae elicits an IL-17-dominated immune response. Vet Res (2015) 46. doi: 10.1186/S13567-015-0264-2 PubMed DOI PMC
Sato T, Okamura T, Kojima-Shibata C, Kadowaki H, Suzuki E, Uenishi H, et al. . Correlated response of peripheral blood cytokines with selection for reduced mycoplasma pneumonia of swine lesions in Landrace pigs. Anim Sci J (2016) 87:477–83. doi: 10.1111/ASJ.12462 PubMed DOI
He X, Song X, Cao H, Zhou Q, Zhang J, Yue H, et al. . Glaesserella parasuis induces IL-17 production might through PKC-ERK/MAPK and IκB/NF-κB signaling pathways. Vet Microbiol (2022) 273. doi: 10.1016/J.VETMIC.2022.109521 PubMed DOI
Liu X, Walton SF, Murray HC, King M, Kelly A, Holt DC, et al. . Crusted scabies is associated with increased IL-17 secretion by skin T cells. Parasite Immunol (2014) 36:594–604. doi: 10.1111/PIM.12129 PubMed DOI
Mounsey KE, Murray HC, Bielefeldt-Ohmann H, Pasay C, Holt DC, Currie BJ, et al. . Prospective study in a porcine model of sarcoptes scabiei indicates the association of Th2 and Th17 pathways with the clinical severity of scabies. PloS Negl Trop Dis (2015) 9(3):e0003498. doi: 10.1371/JOURNAL.PNTD.0003498 PubMed DOI PMC
Magiri RB, Lai K, Chaffey AM, Wilson HL, Berry WE, Szafron ML, et al. . Response of immune response genes to adjuvants poly [di(sodium carboxylatoethylphenoxy)phosphazene] (PCEP), CpG oligodeoxynucleotide and emulsigen at intradermal injection site in pigs. Vet Immunol Immunopathol (2016) 175:57–63. doi: 10.1016/J.VETIMM.2016.05.003 PubMed DOI
Levast B, de Monte M, Chevaleyre C, Melo S, Berri M, Mangin F, et al. . Ultra-early weaning in piglets results in low serum IgA concentration and IL17 mRNA expression. Vet Immunol Immunopathol (2010) 137:261–8. doi: 10.1016/J.VETIMM.2010.06.004 PubMed DOI
Butler JE, Šinkora M. The isolator piglet: a model for studying the development of adaptive immunity. Immunol Res (2007) 39:33–51. doi: 10.1007/S12026-007-0062-7 PubMed DOI
Štěpánová K, Šinkora M. The expression of CD25, CD11b, SWC1, SWC7, MHC-II, and family of CD45 molecules can be used to characterize different stages of γδ T lymphocytes in pigs. Dev Comp Immunol (2012) 36:728–40. doi: 10.1016/J.DCI.2011.11.003 PubMed DOI
Stepanova K, Sinkora M. Porcine γδ T Lymphocytes Can Be Categorized into Two Functionally and Developmentally Distinct Subsets according to Expression of CD2 and Level of TCR. J Immunol (2013) 190:2111–20. doi: 10.4049/jimmunol.1202890 PubMed DOI
Šinkora M, Butler JE. The ontogeny of the porcine immune system. Dev Comp Immunol (2009) 33:273–83. doi: 10.1016/J.DCI.2008.07.011 PubMed DOI PMC
Potockova H, Sinkorova J, Karova K, Sinkora M. The distribution of lymphoid cells in the small intestine of germ-free and conventional piglets. Dev Comp Immunol (2015) 51:99–107. doi: 10.1016/J.DCI.2015.02.014 PubMed DOI
Hlavová K, Štěpánová H, Št’astný K, Levá L, Hodkovicová N, Vícenová M, et al. . Minimal concentrations of deoxynivalenol reduce cytokine production in individual lymphocyte populations in pigs. Toxins (Basel) (2020) 12(3):190. doi: 10.3390/TOXINS12030190 PubMed DOI PMC
Brevi A, Cogrossi LL, Grazia G, Masciovecchio D, Impellizzieri D, Lacanfora L, et al. . Much more than IL-17A: cytokines of the IL-17 family between microbiota and cancer. Front Immunol (2020) 11:565470. doi: 10.3389/FIMMU.2020.565470 PubMed DOI PMC
Stepanova H, Samankova P, Leva L, Sinkora J, Faldyna M. Early postnatal development of the immune system in piglets: the redistribution of T lymphocyte subsets. Cell Immunol (2007) 249:73–9. doi: 10.1016/J.CELLIMM.2007.11.007 PubMed DOI
Muro R, Takayanagi H, Nitta T. T cell receptor signaling for γδT cell development. Inflammation Regener (2019) 39:6. doi: 10.1186/S41232-019-0095-Z PubMed DOI PMC
Ivanov II, Frutos R de L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, et al. . Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe (2008) 4:337–49. doi: 10.1016/J.CHOM.2008.09.009 PubMed DOI PMC
Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, et al. . ATP drives lamina propria T(H)17 cell differentiation. Nature (2008) 455:808–12. doi: 10.1038/NATURE07240 PubMed DOI
Wilson S, Norton P, Haverson K, Leigh J, Bailey M. Development of the palatine tonsil in conventional and germ-free piglets. Dev Comp Immunol (2005) 29:977–87. doi: 10.1016/J.DCI.2005.03.008 PubMed DOI
Šinkora M, Šinkora J, Řeháková Z, Šplíchal I, Yang H, Parkhouse RME, et al. . Prenatal ontogeny of lymphocyte subpopulations in pigs. Immunology (1998) 95:595–603. doi: 10.1046/J.1365-2567.1998.00641.X PubMed DOI PMC
Reutner K, Leitner J, Müllebner A, Ladinig A, Essler SE, Duvigneau JC, et al. . CD27 expression discriminates porcine T helper cells with functionally distinct properties. Vet Res (2013) 44(1):18. doi: 10.1186/1297-9716-44-18 PubMed DOI PMC
Šinkora M, Šinkora J, Reháková Z, Butler JE. Early ontogeny of thymocytes in pigs: sequential colonization of the thymus by T cell progenitors. J Immunol (2000) 165:1832–9. doi: 10.4049/JIMMUNOL.165.4.1832 PubMed DOI
Sinkora M, Butler JE, Holtmeier W, Sinkorova J. Lymphocyte development in fetal piglets: Facts and surprises. Vet Immunol Immunopathol (2005) 108:177–84. doi: 10.1016/J.VETIMM.2005.08.013 PubMed DOI
Šinkora M, Šinkorová J, Cimburek Z, Holtmeier W. Two groups of porcine TCRγδ+ Thymocytes behave and diverge differently. J Immunol (2007) 178:711–9. doi: 10.4049/jimmunol.178.2.711 PubMed DOI
Shibata K, Yamada H, Nakamura R, Sun X, Itsumi M, Yoshikai Y. Identification of CD25+ gamma delta T cells as fetal thymus-derived naturally occurring IL-17 producers. J Immunol (2008) 181:5940–7. doi: 10.4049/JIMMUNOL.181.9.5940 PubMed DOI
Cai Y, Shen X, Ding C, Qi C, Li K, Li X, et al. . Pivotal role of dermal IL-17-producing γδ T cells in skin inflammation. Immunity (2011) 35:596–610. doi: 10.1016/J.IMMUNI.2011.08.001 PubMed DOI PMC
Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KHG. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity (2009) 31:331–41. doi: 10.1016/J.IMMUNI.2009.08.001 PubMed DOI
Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity (2009) 31:321–30. doi: 10.1016/J.IMMUNI.2009.06.020 PubMed DOI
Sutton CE, Mielke LA, Mills KHG. IL-17-producing γδ T cells and innate lymphoid cells. Eur J Immunol (2012) 42:2221–31. doi: 10.1002/EJI.201242569 PubMed DOI
Wen K, Li G, Zhang W, Azevedo MSP, Saif LJ, Liu F, et al. . Development of γδ T cell subset responses in gnotobiotic pigs infected with human rotaviruses and colonized with probiotic lactobacilli. Vet Immunol Immunopathol (2011) 141:267–75. doi: 10.1016/J.VETIMM.2011.03.016 PubMed DOI PMC