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Characterization and Functional Study on Octopus ocellatus Interleukin-17

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Abstract

Interleukin-17 (IL-17), a prototype member of IL-17 family, plays an important role in defending against extracellular pathogens as a pro-inflammatory cytokine. The function and distribution of IL-17 have been extensively studied in many vertebrates. However, few study has focused on the role of IL-17 in invertebrates, especially in mollusks. In this study, an IL-17 homolog was identified in Octopus ocellatus, which was designated as OoIL-17. The phylogenetic analysis showed that OoIL-17 is clustered well with other invertebrate IL-17, indicating it is highly similar with the IL-17 of other invertebrates. The expression of OoIL-17 gene was analyzed with qRT-PCR in a variety of healthy tissues and the hemocytes infected with Vibro anguillarum or Micrococcus luteus. The mRNA of OoIL-17 gene is constitutively expressed at different levels in all examined tissues of healthy O. ocellatus, including mantle, stomach, hemocytes, muscle, gonad, hepatopancreas, systemic heart and gill. The lowest expression was observed in mantle while the highest was observed in hepatopancreas. The expression level of OoIL-17 gene is significantly up-regulated in O. ocellatus hemocytes upon infection with V. anguillarum and M. luteus, indicating its active involvement in the host immune response against bacterial pathogens. The results laid the foundation for further understanding the innate immune mechanisms of IL-17 in O. ocellatus and mollusks.

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References

  • Aas, K., 2010. Treatment with a neutralizing anti-murine inter-leukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum, 50 (2): 650–659.

    Google Scholar 

  • Bagiolini, M., 1998. Chemokines and leukocyte traffic. Nature, 392 (6676): 565–568.

    Article  Google Scholar 

  • Bessis, N., and Boissier, M. C., 2001. Novel pro-inflammatory interleukins: potential therapeutic targets in rheumatoid arthritis. Joint Bone Spine Revue Du Rhumatisme, 68 (6): 477–481.

    Article  Google Scholar 

  • Cerenius, L., Jiravanichpaisal, P., Liu, H., and Soderhall, I., 2010. Crustacean immunity. Oxygen Transport to Tissue XXXIII, 708 (92): 239–259.

    Google Scholar 

  • Chen, S., Chinnaswamy, A., and Biswas, S. K., 2007. Cell interaction knowledgebase: An online database for innate immune cells, cytokines and chemokines. Silico Biology, 7 (6): 569–574.

    Google Scholar 

  • Fujino, S., Andoh, A., Bamba, S., Ogawa, A., Hata, K., and Araki, Y., 2003. Increased expression of interleukin 17 in inflammatory bowel disease. Gut, 52 (1): 65–70.

    Article  Google Scholar 

  • Gaffen, S. L., 2004. Biology of recently discovered cytokines: Interleukin-17-α unique inflammatory cytokine with roles in bone biology and arthritis. Arthritis Research & Therapy, 6 (6): 240.

    Article  Google Scholar 

  • Gaffen, S. L., 2009. Structure and signaling in the IL-17 receptor family. Nature Reviews Immunology, 9 (11): 556–567.

    Article  Google Scholar 

  • Gerhardt, S., Abbott, W. M., Hargreaves, D., Pauptit, R. A., Davies, R. A., and Needham, M. R., 2009. Structure of IL-17A in complex with a potent, fully human neutralizing antibody. Journal of Molecular Biology, 394: 905–921.

    Article  Google Scholar 

  • Gunimaladevi, I., Savan, R., and Sakai, M., 2006. Identification, cloning and characterization of interleukin-17 and its family from zebrafish. Fish & Shellfish Immunology, 21 (4): 393–403.

    Article  Google Scholar 

  • Hymowitz, S. G., 2014. IL-17s adopt a cystine knot fold: Structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO Journal, 20 (19): 5332–5341.

    Article  Google Scholar 

  • Iwakura, Y., Ishigame, H., Saijo, S., and Nakae, S., 2011. Functional specialization of interleukin-17 family members. Immunity, 34 (2): 149–162.

    Article  Google Scholar 

  • Kawaguchi, M., Adachi, M., Oda, N., Kokubu, F., and Huang, S. K., 2004. IL-17 cytokine family. Journal of Allergy & Clinical Immunology, 114 (6): 1265–1273.

    Article  Google Scholar 

  • Kazunori, H., Akira, A., Mitsue, S., Sanae, F., Shigeki, B., and Yoshio, A., 2002. IL-17 stimulates inflammatory responses via nf-kappab and map kinase pathways in human colonic myofibroblasts. American Journal of Physiology-Gastrointestinal and Liver Physiology, 282 (6): 10–35.

    Google Scholar 

  • Kong, P. F., Zhang, H., and Wang, L. L., 2010. AiC1qDC-1, a novel gC1q-domain-containing protein from bay scallop Argopecten irradians with fungi agglutinating activity. Developmental & Comparative Immunology, 34 (8): 837–846.

    Article  Google Scholar 

  • Kono, T., Korenaga, H., and Sakai, M., 2011. Genomics of fish IL-17 ligand and receptors: A review. Fish & Shellfish Immunology, 31 (5): 635–6431.

    Article  Google Scholar 

  • Korenaga, H., Kono, T., and Sakai, M., 2010. Isolation of seven IL-17 family genes from the Japanese pufferfish Takifugu rubripes. Fish & Shellfish Immunology, 28 (5): 809–818.

    Article  Google Scholar 

  • Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., and Sedgwick, J. D., 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. Journal of Experimental Medicine, 201 (2): 233–240.

    Article  Google Scholar 

  • Lemaitre, B., and Hoffmann, J., 2007. The host defense of Drosophila melanogaster. Annual Review of Immunology, 25 (1): 697–743.

    Article  Google Scholar 

  • Li, J., Zhang, Y., and Zhang, Y., 2014. Genomic characterization and expression analysis of five novel IL-17 genes in the Pacific oyster, Crassostrea gigas. Fish & Shellfish Immunology, 40 (2): 455–465.

    Article  Google Scholar 

  • Min, W., and Lillehoj, H. S., 2002. Isolation and characterization of chicken interleukin-17 cDNA. Journal of Interferon & Cytokine Research, 22 (11): 1123–1128.

    Article  Google Scholar 

  • Moseley, T. A., Haudenschild, D. R., and Rose, L., 2003. Interleukin-17 family and IL-17 receptors. Cytokine & Growth Factor Reviews, 14 (2): 155–174.

    Article  Google Scholar 

  • Nakae, S., Nambu, A., Sudo, K., and Iwakura, Y., 2003. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. Journal of Immunology, 171 (11): 6173–6177.

    Article  Google Scholar 

  • Pappu, R., Ramirez-Carrozzi, V., Ota, N., Ouyang, W., and Hu, Y., 2010. The IL-17 family cytokines in immunity and disease. Journal of Clinical Immunology, 30 (2): 185–195.

    Article  Google Scholar 

  • Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., and Wang, Y. H., 2005. A distinct lineage of cd4 t cells regulates tissue inflammation by producing interleukin 17. Nature Immunology, 6 (11): 1133–1141.

    Article  Google Scholar 

  • Pfeffer, S. R., and Rothman, J. E., 1987. Biosynthetic protein transport and sorting by the endoplasmic reticulum and Golgi. Annual Review of Biochemistry, 56 (1): 829–852.

    Article  Google Scholar 

  • Riollet, C., Mutuel, D., and Duonorcérutti, M., 2006. Determination and characterization of bovine interleukin-17 cDNA. Journal of Interferon and Cytokine Research, 26 (3): 141–149.

    Article  Google Scholar 

  • Roberts, S., Gueguen, Y., and Lorgeril, J. D., 2008. Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure. Developmental & Comparative Immunology, 32 (9): 1099–1104.

    Article  Google Scholar 

  • Rouvier, E., Luciani, M. F., Mattéi, M. G., Denizot, F., and Golstein, P., 1993. Ctla-8, cloned from an activated T cell, bearing au-rich messenger RNA instability sequences, and homologous to a Herpesvirus saimiri gene. Journal of Immunology, 150 (12): 5445–5456.

    Google Scholar 

  • Valenzuela, M. V., and Gallardo, E. C., 2014. Molecular cloning and expression of IRAK-4, IL-17 and I-ΰB genes in Haliotis rufescens challenged with Vibrio anguillarum. Fish & Shellfish Immunology, 36 (2): 503–509.

    Article  Google Scholar 

  • Wei, X., Xu, J., and Yang, J., 2015. Involvement of a Serpin serine protease inhibitor (OoSerpin) from mollusc Octopus ocellatus, in antibacterial response. Fish & Shellfish Immunology, 42 (1): 79–87.

    Article  Google Scholar 

  • Wei, X., Yang, J., and Yang, J., 2012. A four-domain Kunitztype proteinase inhibitor from Solen grandis is implicated in immune response. Fish & Shellfish Immunology, 33 (6): 1276–1284.

    Article  Google Scholar 

  • Witowski, J., Ksiazek, K., and Jörres, A., 2004. Interleukin-17: A mediator of inflammatory responses. Cellular & Molecular Life Sciences Cmls, 61 (5): 567–579.

    Article  Google Scholar 

  • Wu, S. Z., Huang, X. D., and Li, Q., 2013. Interleukin-17 in pearl oyster (Pinctada fucata): molecular cloning and functional characterization. Fish & Shellfish Immunology, 34 (5): 1050–1056.

    Article  Google Scholar 

  • Yao, Z., Fanslow, W. C., Seldin, M. F., Rousseau, A. M., Painter, S. L., and Comeau, M. R., 1995. Herpesvirus saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity, 187 (9): 811–821.

    Article  Google Scholar 

  • Zhang, R., Wang, M., and Xia, N., 2016. Cloning and analysis of gene expression of interleukin-17 homolog in triangle-shell pearl mussel, Hyriopsis cumingii, during pearl sac formation. Fish & Shellfish Immunology, 52: 151–156.

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the earmarked fund for the Modern Agro-Industry Technology Research System (No. CARS-49), the Natural Science Foundation of Shandong Province (No. ZR2019BC052), and the Marine and Fisheries Science and Technology Innovation Program of Shan- dong Province (No. 2017YY04).

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Correspondence to Jianmin Yang.

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Li, Z., Fan, T., Liu, X. et al. Characterization and Functional Study on Octopus ocellatus Interleukin-17. J. Ocean Univ. China 18, 1443–1450 (2019). https://doi.org/10.1007/s11802-019-4116-y

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  • DOI: https://doi.org/10.1007/s11802-019-4116-y

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