Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of intraepithelial lymphocytes, goblet cells and immunoglobulin genes in the intestinal mucosal tissue of Pelodiscus sinensis after challenge with Aeromonas veronii bv. sobria and lipopolysaccharide

  • Original Article
  • Aquaculture
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Pelodiscus sinensis, which is a high-value commercial freshwater species, frequently suffers from infectious diseases induced by various pathogens. The mucosa has been confirmed to contribute to host protection, which is the first line of defence against invading pathogens, including bacteria. This study was conducted to evaluate the intestinal mucosal immunity of P. sinensis against Aeromonas veronii bv. sobria and lipopolysaccharide (LPS) infection. A significant increase in the number of intraepithelial lymphocytes (IEL) and goblet cells was observed from 12 h after challenge with A. veronii bv. sobria and LPS (P < 0.01), and the peak was observed at 48 h. The expression of immunoglobulin M (IgM) mRNA also increased between 12 h and 24 h and then decreased until 96 h. Across the experiment, the expression of IgM mRNA in the challenge groups was significantly higher than that in the control group, except at 48 h (P < 0.01), and then declined until 96 h. In contrast, the expression of IgD mRNA had no significant differences compared with the control group. This result showed that the IEL, goblet cells and IgM in P. sinensis were involved in the intestinal mucosal immunity against A. veronii bv. sobria and LPS infection.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Chen QS, Su ZH, Chen XW (2005) Morphological studies on cells involved in mucosal immunity of the intestine in the Chinese soft-shelled turtle. Acta Hydrobiol Sin 29:56–62

    Google Scholar 

  • Chen M, Li D, Fang J, Gu Y, Zhang L, Liu L, Zhang G (2017) Apolipoprotein mediates soft-shelled turtle systemic septicemia spherical virus (STSSSV) infection. Aquaculture 473:501–507

    Article  CAS  Google Scholar 

  • Choi J (1999) Lipopolysaccharide from Escherichia coli stimulates mucin secretion by cultured dog gallbladder epithelial cells. Hepatology 29:1352–1357

    Article  CAS  PubMed  Google Scholar 

  • Coe JE, Leong D, Portis JL, Thomas LA (1976) Immune response in the garter snake (Thamnophis ordinoides). Immunology 31:417–424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dang W, Lu HL, Gao Y, Dong LY, Zheng H, Liu YH (2015) Construction and application of subunit vaccines against Aeromonas sobria in Pelodiscus sinensis. J Hangzhou Norm Univ Nat Sci 14:191–195

    Google Scholar 

  • Dezfuli BS, Lui A, Giovinazzo G, Boldrini P, Giari L (2009) Intestinal inflammatory response of powan Coregonus lavaretus (Pisces) to the presence of acanthocephalan infections. Parasitology 136:929–937

    Article  CAS  PubMed  Google Scholar 

  • Dezfuli BS, Pironi F, Campisi M, Shinn AP, Giari L (2010) The response of intestinal mucous cells to the presence of enteric helminths: their distribution, histochemistry and fine structure. J Fish Dis 33:481–488

    Article  CAS  PubMed  Google Scholar 

  • Estensoro I, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J, Sitjà-Bobadilla A (2012) Modulation of the IgM gene expression and IgM immunoreactive cell distribution by the nutritional background in gilthead sea bream (Sparus aurata) challenged with Enteromyxum leei (Myxozoa). Fish Shellfish Immunol 33:401–410

    Article  CAS  PubMed  Google Scholar 

  • Forchielli ML, Walker WA (2005) The role of gut-associated lymphoid tissues and mucosal defense. Br J Nutr 93:S41

    Article  CAS  PubMed  Google Scholar 

  • Gambón Deza F, Sánchez Espinel C, Valdueza Beneitez J (2007) A novel IgA-like immunoglobulin in the reptile Eublepharis macularius. Dev Comp Immunol 31:596–605

    Article  CAS  Google Scholar 

  • Guy-grand D, Malassis-seris M, Briottet C, Vassallit P (1991) Cytotoxic differentiation of mouse gut thymodependent and independent intraepithelial T lymphocytes is induced locally. Correlation between functional assays, presence of perforin and granzyme transcripts, and cytoplasmic granules. J Exp Med 173:1549–1552

    Article  CAS  PubMed  Google Scholar 

  • Hädge D, Ambrosius H (1984) Evolution of low molecular weight immunoglobulins—IV. IgY-like immunoglobulins of birds, reptiles and amphibians, precursors of mammalian IgA. Mol Immunol 21:699–707

    Article  PubMed  Google Scholar 

  • Hu GZ, Li DF, Su XR, Li TW, He JJ, Wang MQ, Li H, Li Y (2010) Isolation and identification of bacteria from soft-shelled turtle (Trionyx sinensis) associated with fulminant septicaemia. J Fish Sci China 4:859–868

    Google Scholar 

  • Inagaki-Ohara K, Nishimura H, Sakai T, Lynch DH, Yoshikai Y (1997) Potential for involvement of Fas antigen/Fas ligand interaction in apoptosis of epithelial cells by intraepithelial lymphocytes in murine small intestine. Lab Invest 77:421–429

    CAS  PubMed  Google Scholar 

  • Kunisawa J, Kurashima Y, Kiyono H (2012) Gut-associated lymphoid tissues for the development of oral vaccines. Adv Drug Deliv Rev 64:523–530

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Wu H, Liu Q, Wang Q, Xiao J, Chang X, Zhang Y (2015) Profiling immune response in zebrafish intestine, skin, spleen and kidney bath-vaccinated with a live attenuated Vibrio anguillarum vaccine. Fish Shellfish Immunol 45:342–345

    Article  CAS  PubMed  Google Scholar 

  • Ma YZ, Shu MA (2000) Studies on the pathogens of disease of Aeromonas sobria in Trionyx sinensis. J Zhejiang Univ Sci 3:329–333

    Google Scholar 

  • Mashoof S, Goodroe A, Du CC, Eubanks JO, Jacobs N, Steiner JM, Tizard I, Suchodolski JS, Criscitiello MF (2013) Ancient T-independence of mucosal IgX/A: gut microbiota unaffected by larval thymectomy in Xenopus laevis. Mucosal Immunol 6:358–368

    Article  CAS  PubMed  Google Scholar 

  • Moncada DM, Kammanadiminti SJ, Chadee K (2003) Mucin and Toll-like receptors in host defense against intestinal parasites. Trends Parasitol 19:305–311

    Article  CAS  PubMed  Google Scholar 

  • Nair MG, Guild KJ, Du Y, Zaph C, Yancopoulos GD, Valenzuela DM, Murphy A, Stevens S, Karow M, Artis D (2008) Goblet cell-derived resistin-like molecule beta augments CD4+ T cell production of IFN-gamma and infection-induced intestinal inflammation. J Immunol 181:4709–4715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettinello R, Dooley H (2014) The immunoglobulins of cold-blooded vertebrates. Biomolecules 4:1045–1069

    Article  PubMed  PubMed Central  Google Scholar 

  • Portis JL, Coe JE (1975) IgM the secretory immunoglobulin of reptiles and amphibians. Nature 258:547–548

    Article  CAS  PubMed  Google Scholar 

  • Shatos MA, Ríos JD, Horikawa Y, Hodges RR, Bernardino CR, Chang EL, Dartt DA, Rubin PAD (2003) Isolation and characterization of cultured human conjunctival goblet cells. Investig Ophthalmol Vis Sci 44:2477–2486

    Article  Google Scholar 

  • Smirnova MG, Guo L, Birchall JP, Pearson JP (2003) LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cell Immunol 221:42–49

    Article  CAS  PubMed  Google Scholar 

  • Specian RD, Oliver MG (1991) Functional biology of intestinal goblet cells. Am J Physiol 260:C183–C193

    Article  CAS  PubMed  Google Scholar 

  • Strober W, Russell M, Cheroutre H, Lambrecht BN, Kelsall B (2015) Mucosal immunology. Elsevier, Cambridge

    Google Scholar 

  • Sun HX, Li L (2002) Biodegradable microspheres as an oral vaccine delivery system against Aeromonas hydrophila of soft-shelled turtles: the optimization of the cultural condition. Chin J Vet Sci 22:567–570

    CAS  Google Scholar 

  • Sun Q, Shang Y, She R, Jiang T, Wang D, Ding Y, Yin J (2013) Detection of intestinal intraepithelial lymphocytes, goblet cells and secretory IgA in the intestinal mucosa during Newcastle disease virus infection. Avian Pathol 42:541–545

    Article  CAS  PubMed  Google Scholar 

  • Taguchi T, Aicher WK, Fujihashi K, Yamamoto M, McGhee JR, Ja Bluestone, Kiyono H (1991) Novel function for intestinal intraepithelial lymphocytes Murine CD3+, gamma/delta TCR+ T cells produce IFN-gamma and IL-5. J Immunol 147:3736–3744

    CAS  PubMed  Google Scholar 

  • Taupin D, Podolsky DK (2003) Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 4:721–732

    Article  CAS  PubMed  Google Scholar 

  • Vaerman JP, Picard J, Heremans JF (1975) Structural data on chicken IgA and failure to identify the IgA of the tortoise. Adv Exp Med Biol 64:185

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Wei Z, Hu X, Wang X, Liu G, Yu J et al (2014) Extensive diversification of IgH subclass-encoding genes and IgM subclass switching in crocodilians. Sci Found Chin 4:1337

    Google Scholar 

  • Xu Z, Wang GL, Nie P (2009) IgM, IgD and IgY and their expression pattern in the Chinese soft-shelled turtle Pelodiscus sinensis. Mol Immunol 46:2124–2132

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto M, Fujihashi K, Amano M, McGhee JR, Beagley KW, Kiyono H (1994) Cytokine synthesis and apoptosis by intestinal intraepithelial lymphocytes: signaling of high density αβ T cell receptor + and γδ T cell receptor + T cells via T cell receptor-CD3 complex results in interferon-γ and interleukin-5 production, while low density T cells undergo DNA fragmentation. Eur J Immunol 6:1301–1306

    Article  Google Scholar 

  • Yang Z, Pan H, Sun H (2007) The immune response and protective efficacy of oral alginate microparticle Aeromonas sobria vaccine in soft-shelled turtles (Trionyx sinensis). Vet Immunol Immunopathol 119:299–302

    Article  CAS  PubMed  Google Scholar 

  • Zhu CH, Liu H, Yang JX, Zheng ZY, Liu XD, Lin TL (2009) Purification and analysis of soft-shell turtle iridovirus. Fujian J Agric Sci 24:132–136

    Google Scholar 

  • Zimmerman LM, Vogel LA, Bowden RM (2010) Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 213:661–671

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was partially supported by China National Critical Project for Science and Technology (Grant no. 2014ZX07101-012), Zhejiang Provincial Top Key Discipline of Bioengineering (ZS2017013) and the Program for Huzhou Agricultural Science and Technology Innovation Team (2014HN02).

Author information

Authors and Affiliations

  1. College of Animal Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou, 310058, Zhejiang, People’s Republic of China

    Jiehao Xu, Hanxiang Chen, Wanrong Zhang & Haisheng Xu

  2. College of Biological and Environmental Science, Zhejiang Wanli University, Ningbo, 315100, Zhejiang, People’s Republic of China

    Jiehao Xu

Authors
  1. Jiehao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hanxiang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wanrong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haisheng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haisheng Xu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, J., Chen, H., Zhang, W. et al. Evaluation of intraepithelial lymphocytes, goblet cells and immunoglobulin genes in the intestinal mucosal tissue of Pelodiscus sinensis after challenge with Aeromonas veronii bv. sobria and lipopolysaccharide. Fish Sci 85, 177–185 (2019). https://doi.org/10.1007/s12562-018-1262-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-018-1262-x

Keywords

Search

Navigation