Skip to main content
Log in

Cloning and expression analysis of two pro-inflammatory cytokines, IL-1β and its receptor, IL-1R2, in the Asian swamp eel Monopterus albus

  • Genomics. Transcriptomics
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

Interleukin-1β (IL-1β) is the prototypic pro-inflammatory cytokine, whose functions are mediated through interaction with its receptors (IL-1R1 and IL-1R2). Herein, we cloned the full-length cDNA and genomic DNA of IL-1β and IL-1R2 in the Asian swamp eel (Monopterus albus). The eel IL-1β cDNA encodes a putative polypeptide of 246 amino acids. The protein sequence includes a typical IL-1 family signature, but lacked an interleukin-converting enzyme cleavage site. The genomic DNA of eel IL-1β was 2520 bp and comprised five exons and four introns. The eel IL-1R2 cDNA encoded a putative propeptide of 423 amino acid residues, comprising a signal peptide, a transmembrane region and two Ig-like domains in the extracellular region. Similar to other vertebrates, the genomic DNA of the eel IL-1R2 has nine exons and eight introns. Real-time PCR analysis indicated that IL-1β and IL-1R2 were constitutively expressed in all tissues, especially in the liver and immune-related organs. After infection with Aeromonas hydrophila, the transcript levels of IL-1β and IL-1R2 were induced in the head kidney and spleen, reaching their highest levels at 6 h post injection. In vitro, IL-1β and IL-1R2 mRNA levels were also upregulated rapidly at 1h post infection with A. hydrophila. Furthermore, acanthocephalan Pallisentis (Neosentis) celatus could induce the expression of both genes in the head kidney and intestine. In infected intestines, the transcript levels of IL-1β and IL-1R2 were increased by 21.4-fold and 20.8-fold, respectively, relative to the control. The present study indicated that IL-1β and IL-1R2 play an important role in inflammation and host defense, especially in the antiacanthocephalan response.

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.

Similar content being viewed by others

References

  1. Singh V., Mani I., Chaudhary D.K., Somvanshi P. 2011. Molecular detection and cloning of thermostable hemolysin gene from Aeromonas hydrophila. Mol. Biol. (Moscow). 45, 551–560.

    Article  CAS  Google Scholar 

  2. Wang X.W., Deng D.H., Gong L.J., Chen X.L., Yang L.S. 2008. Method of prevention and cure for common illness in the Asian swamp eel. Fishery Guide To Be Rich. 22, 56.

    Google Scholar 

  3. Saksirisampant W., Thanomsub B.W. 2012. Positivity and intensity of Gnathostoma spinigerum infective larvae in farmed and wild-caught swamp eels in Thailand. Korean J. Parasitol. 50, 113–118.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cole R.A., Choudhury A., Nico L.G., Griffin K.M. 2014. Gnathostoma spinigerum in live Asian swamp eels (Monopterus spp.) from food markets and wild populations, United States. Emerg. Infect. Dis. 20, 634–642.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Song R., Li W.X., Zou H., Wang G.T. 2013. Seasonal dynamics and frequency distribution of the endoparasites Pallisentis (Neosentis) celatus and Eustrongylides sp. in the rice field eel Monopterus albus. Acta Hydrobiol. Sinica. 37, 1044–1050.

    Google Scholar 

  6. Ou T., Zhu R.L., Chen Z.Y., Zhang Q.Y. 2013. Isolation and identification of a lethal rhabdovirus from farmed rice field eels Monopterus albus. Dis. Aquat. Organ. 106, 197–206.

    Article  CAS  PubMed  Google Scholar 

  7. Danilko K.V., Korytyna G.F., Akhmadishina L.Z., Yanbaeva D.G. 2007. Association of polymorphisms of cytokine genes (IL1B, IL1RN, TNFA, LTA, IL6, IL8, and IL10) with chronic obstructive pulmonary disease. Mol. Biol. (Moscow). 41, 22–31.

    Article  CAS  Google Scholar 

  8. McMahan C.J., Slack J.L., Mosley B., Cosman D., Lupton S.D., Brunton L.L., Grubin C.E., Wignall J.M., Jenkins N.A., Brannan C.I. 1991. A novel IL-1 receptor, cloned from B cells by mammalian expression, is expressed in many cell types. EMBO. J. 10, 2821–2832.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Moltó A., Olivé A. 2010. Anti-IL-1 molecules: New comers and new indications. Joint Bone Spine. 77, 102–107.

    Article  PubMed  Google Scholar 

  10. Yang X., Wang S.N., Du L.Y., Yang K., Wang X.Y., Zhang A.Y., Zhou H. 2013. Molecular and functional characterization of IL-1 receptor type 2 in grass carp: A potent inhibitor of IL-1β signaling in head kidney leukocytes. Dev. Comp. Immunol. 41, 738–745.

    Article  CAS  PubMed  Google Scholar 

  11. Husain M., Bird S., van Zwieten R., Secombes C.J., Wang T.H. 2012. Cloning of the IL-1β3 gene and IL-1β4 pseudogene in salmonids uncovers a second type of IL-1b gene in teleost fish. Dev. Comp. Immunol. 38, 431–446.

    Article  CAS  PubMed  Google Scholar 

  12. Xu Q.Q., Chang M.X., Sun R.H., Xiao F.S., Nie P. 2010. The first non-mammalian CXCR5 in a teleost fish: Molecular cloning and expression analysis in grass carp (Ctenopharyngodon idella). BMC Immunol. 11, 25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Xu Q.Q., Li R.G., Monte M., Jiang Y.S., Nie P., Holland J.W., Secombes C.J., Wang T.H. 2014. Sequence and expression analysis of rainbow trout CXCR2, CXCR3a and CXCR3b aids interpretation of lineagespecific conversion, loss and expansion of these receptors during vertebrate evolution. Dev. Comp. Immunol. 45, 201–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Secombes C.J., Wang T.H., Bird S. 2011. The interleukins of fish. Dev. Comp. Immunol. 35, 1336–1345.

    Article  CAS  PubMed  Google Scholar 

  15. Liu Q.Y., Yan X.S. 2008. Method of prevention and cure for common illness in the Asian swamp eel. Fishery Guide to be Rich. 24, 64.

    Google Scholar 

  16. Bird S., Zou J., Wang T., Munday B., Cunningham C., Secombes C.J. 2002. Evolution of interleukin-1β. Cytokine Growth Factor Rev. 13, 483–502.

    Article  CAS  PubMed  Google Scholar 

  17. Buonocore F., Prugnoli D., Falasca C., Secombes C.J., Scapigliati G. 2003. Peculiar gene organisation and incomplete splicing of sea bass (Dicentrarchus labrax L.) interleukin-1β. Cytokine. 21, 257–264.

    Article  CAS  PubMed  Google Scholar 

  18. Lee D.S., Hong S.H., Lee H.J., Jun L.J., Chung J.K., Kim K.H., Jeong H.D. 2006. Molecular cDNA cloning and analysis of the organization and expression of the IL-1β gene in the Nile tilapia, Oreochromis niloticus. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 143, 307–314.

    Article  Google Scholar 

  19. Pelegrin P., Garcia-Castillo J., Mulero V., Meseguer J. 2001. Interleukin-1β isolated from a marine fish reveals up-regulated expression in macrophages following activation with lipopolysaccharide and lymphokines. Cytokine. 16, 67–72.

    Article  CAS  PubMed  Google Scholar 

  20. Fan Y.D., Li S., Qi J., Zeng L.B., Zhong Q.W., Zhang Q.Q. 2010. Cloning and characterization of type II interleukin-1 receptor cDNA from Japanese flounder (Paralichthys olivaceus). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 157, 59–65.

    Article  PubMed  Google Scholar 

  21. Kuno K., Okamoto S., Hirose K., Murakami S., Matsushima K. 1993. Structure and function of the intracellular portion of the mouse interleukin 1 receptor (type I). Determining the essential region for transducing signals to activate the interleukin 8 gene. J. Biol. Chem. 268, 13210–13218.

    Google Scholar 

  22. Kononova T.E., Urazova O.I., Novitskii V.V., Churina E.G. 2013. Regulation of antibacterial (antitubercular) immunity mediated by T-helper type-17 lymphocytes. Mol. Biol. (Moscow). 47, 769–775.

    Article  CAS  Google Scholar 

  23. Amaia S.V., Martin S.A.M., O’Dea P.G., Smith T.J. 2000. Cloning and characterization of the rainbow trout (Oncorhynchus mykiss) type II interleukin-1 receptor cDNA. Eur. J. Biochem. 267, 7031–7037.

    Article  Google Scholar 

  24. López-Castejón G., Sepulcre M.P., Roca F.J., Castellana B., Planas J.V., Meseguer J., Mulero V. 2007. The type II interleukin-1 receptor (IL-1RII) of the bony fish gilthead seabream Sparus aurata is strongly induced after infection and tightly regulated at transcriptional and post-transcriptional levels. Mol. Immunol. 44, 2772–2780.

    Article  PubMed  Google Scholar 

  25. Morrison R.N., Young N.D., Nowak B.F. 2012. Description of an Atlantic salmon (Salmo salar L.) type II interleukin-1 receptor cDNA and analysis of interleukin-1 receptor expression in amoebic gill disease affected fish. Fish Shellfish Immunol. 32, 1185–1190.

    Article  CAS  PubMed  Google Scholar 

  26. Li X., Qin J. 2005. Modulation of Toll-interleukin 1 receptor mediated signaling. J. Mol. Med. 83, 258–266.

    Article  CAS  PubMed  Google Scholar 

  27. Jiang S., Zhang D., Li J., Liu Z. 2008. Molecular characterization, recombinant expression and bioactivity analysis of the interleukin-1 beta from the yellowfin sea bream, Acanthopagrus latus (Houttuyn). Fish Shellfish Immunol. 24, 323–336.

    Article  CAS  PubMed  Google Scholar 

  28. Yan Y., Zhong Q.W., Li C.M., Jiang L.M., Sun Y.Y., Wang X.B., Wang Z.G., Zhang Q.Q. 2012. Molecular cloning and characterization of interleukin-1β in halfsmooth tongue sole Cynoglossus semilaevis. Vet. Immunol. Immunop. 146, 270–276.

    Article  Google Scholar 

  29. Tsutsui S., Iwamoto T., Nakamura O., Watanabe T. 2007. LPS induces gene expression of interleukin-1beta in conger eel (Conger myriaster) macrophages: First cytokine sequence within Anguilliformes. Fish Shellfish Immunol. 23, 911–916.

    Article  CAS  PubMed  Google Scholar 

  30. Wang Y.P., Wang Q., Baoprasertkul P., Peatman E., Liu Z.J. 2006. Genomic organization, gene duplication, and expression analysis of interleukin-1β in channel catfish (Ictalurus punctatus). Mol. Immunol. 43, 1653–1664.

    Article  CAS  PubMed  Google Scholar 

  31. Shintani F., Nakaki T., Kanba S., Kato R. Asai M. 1995. Role of interleukin-1 in stress responses. A putative neurotransmitter. Mol. Neurobiol. 10, 47–71.

    Article  CAS  PubMed  Google Scholar 

  32. Wang B.Y., Mao X.Z. 1999. Immune role of liver. Foreign Med. Sci.: Immunol. 22, 158–161.

    Google Scholar 

  33. Corripio-Miyar Y., Bird S., Tsamopoulos K., Secombes C.J. 2007. Cloning and expression analysis of two pro-inflammatory cytokines, IL-1β and IL-8, in haddock (Melanogrammus aeglefinus). Mol. Immunol. 44, 1361–1373.

    Article  CAS  PubMed  Google Scholar 

  34. Zou J., Holland J., Pleguezuelos O., Cunningham C., Secombes C.J. 2000. Factors influencing the expression of interleukin-1 beta in cultured rainbow trout (Oncorhynchus mykiss) leucocytes. Dev. Comp. Immunol. 24, 575–582.

    Article  CAS  PubMed  Google Scholar 

  35. Dinarello C.A. 1998. Interleukin-1, interleukin-1 receptors and interleukin-1 receptor antagonist. Int. Rev. Immunol. 16, 457–499.

    Article  CAS  PubMed  Google Scholar 

  36. Lu D.Q., Bei J.X., Feng L.N., Zhang Y., Liu X.C., Wang L., Chen J.L., Lin H.R. 2008. Interleukin-1β gene in orange-spotted grouper, Epinephelus coioides: Molecular cloning, expression, biological activities and signal transduction. Mol. Immunol. 45, 857–867.

    Article  CAS  PubMed  Google Scholar 

  37. Lindenstrøm T., Buchmann K., Secombes C.J. 2003. Gyrodactylus derjavini infection elicits IL-1beta expression in rainbow trout skin. Fish Shellfish Immunol. 15, 107–115.

    Article  PubMed  Google Scholar 

  38. Sigh J., Lindenstrøm T., Buchmann K. 2004. Expression of pro-inflammatory cytokines in rainbow trout (Oncorhynchus mykiss) during an infection with Ichthyophthirius multifiliis. Fish Shellfish Immunol. 17, 75–86.

    Article  CAS  PubMed  Google Scholar 

  39. Saeij J.P., de Vries B.J., Wiegertjes G.F. 2003. The immune response of carp to Trypanoplasma borreli: Kinetics of immune gene expression and polyclonal lymphocyte activation. Dev. Comp. Immunol. 27, 859–874.

    Article  CAS  PubMed  Google Scholar 

  40. Bridle A.R., Morrison R.N., Cupit Cunningham P.M., Nowak B.F. 2006. Quantitation of immune response gene expression and cellular localisation of interleukin-1b mRNA in Atlantic salmon, Salmo salar L., affected by amoebic gill disease (AGD). Vet. Immunol. Immunop. 114, 121–134.

    Article  CAS  Google Scholar 

  41. Akira S., Takeda K. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499–511.

    Article  CAS  PubMed  Google Scholar 

  42. Didierlaurent A., Brissoni B., Velin D., Aebi N., Tardivel A., Käslin E., Sirard J.C., Angelov G., Tschopp J., Burns K. 2006. Tollip regulates proinflammatory responses to interleukin-1 and lipopolysaccharide. Mol. Cell Biol. 26, 735–742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Bristulf J., Bartfai T. 1995. Interleukin-1 beta and tumour necrosis factor-alpha stimulate the mRNA expression of interleukin-1 receptors in mouse anterior pituitary AtT-20 cells. Neurosci. Lett. 187, 53–56.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. Q. Yang.

Additional information

Published in Russian in Molekulyarnaya Biologiya, 2016, Vol. 50, No. 5, pp. 760–774.

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Q.Q., Xu, P., Zhou, J.W. et al. Cloning and expression analysis of two pro-inflammatory cytokines, IL-1β and its receptor, IL-1R2, in the Asian swamp eel Monopterus albus . Mol Biol 50, 671–683 (2016). https://doi.org/10.1134/S0026893316030122

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893316030122

Keywords

Navigation