Skip to main content
Log in

Some characteristics of IL-5-producing T cells in mouse liver induced by Schistosoma japonicum infection

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Schistosome infection could cause significant liver damage in animal; Th2 cells play an important role in the progress of this disease. In our study, C57BL/6 mice were infected by Schistosoma japonicum and lymphocytes were isolated from the liver to detect some characteristics of interleukin-5 (IL-5)-producing T cells by different methods. The results revealed that S. japonicum infection could induce a large amount of IL-5 in mouse liver T cells by the means of fluorescent bead immunoassay and RT-PCR. Although, mouse liver contained many T cell subsets, such as Th cells, Tc cells, NKT cells, and γδ T cells. Fluorescence activated cell sorting results indicated that Th cells were the main source of IL-5 in the T cell population after phorbol 12-myristate 13-acetate and ionomycin stimulation. Moreover, the percentage of IL-5-producing Th cells continued to increase from 4 to 8 weeks after S. japonicum infection, which differed from the changes of IFN-γ+ Th1 cells, IL-4+ Th2 cells, and IL-17A+ Th17 cells during S. japonicum infection. Additionally, cytokines co-expression results demonstrated that 36.2 % of IL-5+ Th cells could express IL-4, and 10 % of it could produce IFN-γ or IL-17A. Collectively, these findings implied that IL-5-producing Th cells posses some properties which differ from other cytokines secreting Th cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aarvak T, Chabaud M, Miossec P, Natvig JB (1999) IL-17 is produced by some proinflammatory Th1/Th0 cells but not by Th2 cells. J Immunol 162:1246–1251

    PubMed  CAS  Google Scholar 

  • Asahi H, Stadecker MJ (2003) Analysis of egg antigens inducing hepatic lesions in schistosome infection. Parasitol Int 52:361–367

    Article  PubMed  CAS  Google Scholar 

  • Bloch EH, Wahab MF, Warren KS (1972) In vivo microscopic observations of the pathogenesis and pathophysiology of hepatosplenic schistosomiasis in the mouse liver. AmJTrop Med Hyg 21:546–557

    CAS  Google Scholar 

  • Blom KG, Qazi MR, Matos JB, Nelson BD, DePierre JW, Abedi-Valugerdi M (2009) Isolation of murine intrahepatic immune cells employing a modified procedure for mechanical disruption and functional characterization of the B, T and natural killer T cells obtained. Clin Exp Immunol 155:320–329

    Article  PubMed  CAS  Google Scholar 

  • Cheever AW, Xu YH, Sher A, Macedonia JG (1991) Analysis of egg granuloma formation in Schistosoma japonicum-infected mice treated with antibodies to interleukin-5 and gamma interferon. Infect Immun 59:4071–4074

    PubMed  CAS  Google Scholar 

  • Curry MP, Norris S, Golden-Mason L, Doherty DG, Deignan T, Collins C, Traynor O, McEntee GP, Hegarty JE, O’Farrelly C (2000) Isolation of lymphocytes from normal adult human liver suitable for phenotypic and functional characterization. J Immunol Methods 242:21–31

    Article  PubMed  CAS  Google Scholar 

  • de Jesus AR, Magalhaes A, Miranda DG, Miranda RG, Araujo MI, de Jesus AA, Silva A, Santana LB, Pearce E, Carvalho EM (2004) Association of type 2 cytokines with hepatic fibrosis in human Schistosoma mansoni infection. Infect Immun 72:3391–3397

    Article  PubMed  Google Scholar 

  • Dutra WO, Correa-Oliveira R, Dunne D, Cecchini LF, Fraga L, Roberts M, Soares-Silveira AM, Webster M, Yssel H, Gollob KJ (2002) Polarized Th2 like cells, in the absence of Th0 cells, are responsible for lymphocyte produced IL-4 in high IgE-producer schistosomiasis patients. BMC Immunol 3:8

    Article  PubMed  Google Scholar 

  • Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6:1123–1132

    Article  PubMed  CAS  Google Scholar 

  • Hemida MH, Mahmoud NS, El MM, Ammar ES, Kilany YF, El TD, El DT (2010) Interleukin (IL)-12, Il-5 and total IgE in hepatosplenic schistosomiasis with or without asthma. J Egypt Soc Parasitol 40:367–376

    PubMed  Google Scholar 

  • Ikutani M, Yanagibashi T, Ogasawara M, Tsuneyama K, Yamamoto S, Hattori Y, Kouro T, Itakura A, Nagai Y, Takaki S, Takatsu K (2012) Identification of innate IL-5-producing cells and their role in lung eosinophil regulation and antitumor immunity. J Immunol 188:703–713

    Article  PubMed  CAS  Google Scholar 

  • Jankovic D, Cheever AW, Kullberg MC, Wynn TA, Yap G, Caspar P, Lewis FA, Clynes R, Ravetch JV, Sher A (1998) CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling. J Exp Med 187:619–629

    Article  PubMed  CAS  Google Scholar 

  • Kaplan MH, Whitfield JR, Boros DL, Grusby MJ (1998) Th2 cells are required for the Schistosoma mansoni egg-induced granulomatous response. J Immunol 160:1850–1856

    PubMed  CAS  Google Scholar 

  • Lenzi HL, Romanha WS, Santos RM, Rosas A, Mota EM, Manso PP, Caputo LF, Pelajo-Machado M (2006) Four whole-istic aspects of schistosome granuloma biology: fractal arrangement, internal regulation, autopoietic component and closure. Mem Inst Oswaldo Cruz 101(Suppl 1):219–231

    Article  PubMed  Google Scholar 

  • Li YS, Sleigh AC, Ross AG, Williams GM, Tanner M, McManus DP (2000) Epidemiology of Schistosoma japonicum in China: morbidity and strategies for control in the Dongting Lake region. Int J Parasitol 30:273–281

    Article  PubMed  CAS  Google Scholar 

  • Milner T, Reilly L, Nausch N, Midzi N, Mduluza T, Maizels R, Mutapi F (2010) Circulating cytokine levels and antibody responses to human Schistosoma haematobium: IL-5 and IL-10 levels depend upon age and infection status. Parasite Immunol 32:710–721

    Article  PubMed  CAS  Google Scholar 

  • Saunders M, Taubert A, Dafa’Alla T, Zahner H (2008) Effect of chemotherapeutic treatment on cytokine (IFN-gamma, IL-2, IL-4, IL-5, IL-10) gene transcription in response to specific antigens in Brugia malayi-infected Mastomys coucha. Parasitol Res 103:1163–1176

    Article  PubMed  Google Scholar 

  • van den Biggelaar AH, Borrmann S, Kremsner P, Yazdanbakhsh M (2002) Immune responses induced by repeated treatment do not result in protective immunity to Schistosoma haematobium: interleukin (IL)-5 and IL-10 responses. J Infect Dis 186:1474–1482

    Article  PubMed  Google Scholar 

  • Vujanovic NL, Polimeno L, Azzarone A, Francavilla A, Chambers WH, Starzl TE, Herberman RB, Whiteside TL (1995) Changes of liver-resident NK cells during liver regeneration in rats. J Immunol 154:6324–6338

    PubMed  CAS  Google Scholar 

  • Wang W, Wang L, Liang YS (2012) Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitol Res 111:1871–1877

    Article  PubMed  Google Scholar 

  • Weaver CT, Hatton RD, Mangan PR, Harrington LE (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25:821–852

    Article  PubMed  CAS  Google Scholar 

  • Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, Wynn TA (2007) Immunopathology of schistosomiasis. Immunol Cell Biol 85:148–154

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi Y, Hayashi Y, Sugama Y, Miura Y, Kasahara T, Kitamura S, Torisu M, Mita S, Tominaga A, Takatsu K (1988) Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. J Exp Med 167:1737–1742

    Article  PubMed  CAS  Google Scholar 

  • Yssel H, Bensussan A (2010) Is there a novel subset of Th22 lymphocytes in the skin distinct from Th17 lymphocytes? Med Sci (Paris) 26:12–14

    Article  Google Scholar 

  • Zhang CW, Xiao SH (2012) Histopathological changes of juvenile Schistosoma japonicum harbored in mice treated orally with mefloquine at a smaller single dose. Parasitol Res 110:2281–2288

    Article  PubMed  Google Scholar 

  • Zhang Y, Chen L, Gao W, Hou X, Gu Y, Gui L, Huang D, Liu M, Ren C, Wang S, Shen J (2012) IL-17 neutralization significantly ameliorates hepatic granulomatous inflammation and liver damage in Schistosoma japonicum infected mice. Eur J Immunol 42:1523–1535

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Lukacs NW, Boros DL (1994) Cloning of TH0- and TH2-type helper lymphocytes from liver granulomas of Schistosoma mansoni-infected mice. Infect Immun 62:994–999

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Natural Science Foundation of China (30901353) and Natural Science Foundation of Hunan Province, China (11JJ3103) and Science and Technology Planning Project of Guangzhou City (2011 J22007). We thank Prof. Hu Xuchu in the Department of Parasitology at Zhongshan School of Medicine, Sun Yat-sen University who provide help in animal infection.

Conflict of interest

The authors declare no conflict of interest with this work.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Huilong Fang or Jun Huang.

Additional information

Hongyan Xie and Dianhui Chen equally contributed to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xie, H., Chen, D., Luo, X. et al. Some characteristics of IL-5-producing T cells in mouse liver induced by Schistosoma japonicum infection. Parasitol Res 112, 1945–1951 (2013). https://doi.org/10.1007/s00436-013-3350-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3350-2

Keywords

Navigation