Fisheries and Aquatic Sciences

한국수산과학회 (The Korean Society of Fisheries and Aquatic Science)
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Galectin-1 from redlip mullet Liza haematocheilia: identification, immune responses, and functional characterization as pattern recognition receptors (PRRs) in host immune defense system

  • Chaehyeon Lim (Department of Marine Life Sciences & Fish Vaccine Research Center, Jeju National University) ;
  • Hyukjae Kwon (Department of Marine Life Sciences & Fish Vaccine Research Center, Jeju National University) ;
  • Jehee Lee (Department of Marine Life Sciences & Fish Vaccine Research Center, Jeju National University)
  • 투고 : 2022.06.28
  • 심사 : 2022.10.19
  • 발행 : 2022.11.30
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초록

Galectins, a family of ß-galactoside-binding lectins, have emerged as soluble mediators in infected cells and pattern recognition receptors (PRRs) responsible for evoking and regulating innate immunity. The present study aimed to evaluate the role of galectin-1 in the host immune response of redlip mullet (Liza haematocheilia). We established a cDNA database for redlip mullet, and the cDNA sequence of galectin-1 (LhGal-1) was characterized. In silico analysis was performed, and the spatial and temporal expression patterns in gills and blood in response to lipopolysaccharide polyinosinic:polycytidylic acid, and Lactococcus garvieae were estimated via quantitative real-time PCR. Functional assays were conducted using recombinant protein to investigate carbohydrate binding, bacterial binding, and bacterial agglutination activity. LhGal-1 was composed of 135 amino acids. Conserved motifs (H-NPR, -N- and -W-E-R) within the carbohydrate recognition domain were found in LhGal-1. The tissue distribution revealed that the healthy stomach expressed high levels of LhGal-1. The temporal monitoring of LhGal-1 mRNA expression in the gill and blood showed its significant upregulation in response to immune challenges with different stimulants. rLhGal-1 exhibited binding activity in response to carbohydrates and bacteria. Moreover, the agglutination of rLhGal-1 against Escherichia coli was observed. Collectively, our findings suggest that LhGal-1 may function as a PRR in redlip mullet. Furthermore, LhGal-1 can be considered a significant gene to play a protective role in redlip mullet immune system.

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과제정보

This work was supported by the 2022 education, research and student guidance grant funded by Jeju National University.

참고문헌

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10. https://doi.org/10.1016/S0022-2836(05)80360-2
  2. Boulianne RP, Liu Y, Aebi M, Lu BC, Kues U. Fruiting body development in Coprinus cinereus: regulated expression of two galectins secreted by a non-classical pathway. Microbiology. 2000;146:1841-53. https://doi.org/10.1099/00221287-146-8-1841
  3. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54. https://doi.org/10.1016/0003-2697(76)90527-3
  4. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55:611-22. https://doi.org/10.1373/clinchem.2008.112797
  5. Cerliani JP, Stowell SR, Mascanfroni ID, Arthur CM, Cummings RD, Rabinovich GA. Expanding the universe of cytokines and pattern recognition receptors: galectins and glycans in innate immunity. J Clin Immunol. 2011;31:10-21. https://doi.org/10.1007/s10875-010-9494-2
  6. Chen HY, Weng IC, Hong MH, Liu FT. Galectins as bacterial sensors in the host innate response. Curr Opin Microbiol. 2014;17:75-81. https://doi.org/10.1016/j.mib.2013.11.006
  7. Chen X, Wei J, Xu M, Yang M, Li P, Wei S, et al. Molecular cloning and characterization of a galectin-1 homolog in orange-spotted grouper, Epinephelus coioides. Fish Shellfish Immunol. 2016;54:333-41. https://doi.org/10.1016/j.fsi.2016.02.036
  8. Elola MT, Chiesa ME, Alberti AF, Mordoh J, Fink NE. Galectin-1 receptors in different cell types. J Biomed Sci. 2005;12:13-29. https://doi.org/10.1007/s11373-004-8169-5
  9. Gayashani Sandamalika WM, Lee J. Quadruple domain-containing galectin from marine invertebrate disk abalone (Haliotis discus discus): molecular perspectives in early development, immune expression, and potent antiviral responses. Fish Shellfish Immunol. 2020;106:920-9. https://doi.org/10.1016/j.fsi.2020.09.017
  10. Han HJ, Lee NS, Kim MS, Jung SH. An outbreak of Lactococcus garvieae infection in cage-cultured red lip mullet Chelon haematocheilus with green liver syndrome. Fish Aquat Sci. 2015;18:333-9.
  11. Hirabayashi J, Kasai K. The family of metazoan metal-independent β-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology. 1993;3:297-304. https://doi.org/10.1093/glycob/3.4.297
  12. Kumagai Y, Takeuchi O, Akira S. Pathogen recognition by innate receptors. J Infect Chemother. 2008;14:86-92. https://doi.org/10.1007/s10156-008-0596-1
  13. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547-9. https://doi.org/10.1093/molbev/msy096
  14. Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F. Introduction to galectins. Glycoconj J. 2002;19:433-40. https://doi.org/10.1023/B:GLYC.0000014072.34840.04
  15. Letunic I, Bork P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2018;46:D493-6. https://doi.org/10.1093/nar/gkx922
  16. Liu S, Hu G, Sun C, Zhang S. Anti-viral activity of galectin-1 from flounder Paralichthys olivaceus. Fish Shellfish Immunol. 2013;34:1463-9. https://doi.org/10.1016/j.fsi.2013.03.354
  17. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  18. Liyanage DS, Omeka WKM, Godahewa GI, Lee S, Nam BH, Lee J. Membrane attack complex-associated molecules from redlip mullet (Liza haematocheila): molecular characterization and transcriptional evidence of C6, C7, C8β, and C9 in innate immunity. Fish Shellfish Immunol. 2018;81:1-9. https://doi.org/10.1016/j.fsi.2018.07.006
  19. Ministry of Maritime Affairs and Fisheries. 2020 Ministry of Oceans and Fisheries: statistical year book of maritime affairs and fisheries. Sejong: Ministry of Maritime Affairs and Fisheries; 2020.
  20. Minos G, Imsiridou A, Economidis PS. Liza haematocheilus (Pisces, Mugilidae) in the northern Aegean Sea. In: Golani D, Appelbaum-Golani B, editors. Fish invasions mediterr sea: change renewal. Sofia: Pensoft; 2009. p.313-32.
  21. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010;5:725-38. https://doi.org/10.1038/nprot.2010.5
  22. Sato S, St-Pierre C, Bhaumik P, Nieminen J. Galectins in innate immunity: dual functions of host soluble β-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol Rev. 2009;230:172-87. https://doi.org/10.1111/j.1600-065X.2009.00790.x
  23. Shi W, Xue C, Su X, Lu F. The roles of galectins in parasitic infections. Acta Trop. 2018;177:97-104. https://doi.org/10.1016/j.actatropica.2017.09.027
  24. Thulasitha WS, Umasuthan N, Whang I, Nam BH, Lee J. Antimicrobial response of galectin-1 from rock bream Oplegnathus fasciatus: molecular, transcriptional, and biological characterization. Fish Shellfish Immunol. 2016;50:66-78. https://doi.org/10.1016/j.fsi.2016.01.010
  25. Vasta GR. Galectins as pattern recognition receptors: structure, function, and evolution. In: Lambris JD, Hajishengallis G, editors. Current topics in innate immunity II. New York, NY: Springer; 2012.
  26. Vasta GR, Nita-Lazar M, Giomarelli B, Ahmed H, Du S, Cammarata M, et al. Structural and functional diversity of the lectin repertoire in teleost fish: relevance to innate and adaptive immunity. Dev Comp Immunol. 2011;35:1388-99. https://doi.org/10.1016/j.dci.2011.08.011
  27. Wang M, Wang L, Huang M, Yi Q, Guo Y, Gai Y, et al. A galectin from Eriocheir sinensis functions as pattern recognition receptor enhancing microbe agglutination and haemocytes encapsulation. Fish Shellfish Immunol. 2016;55:10-20. https://doi.org/10.1016/j.fsi.2016.04.019
  28. Wang WH, Lin CY, Chang MR, Urbina AN, Assavalapsakul W, Thitithanyanont A, et al. The role of galectins in virus infection - a systemic literature review. J Microbiol Immunol Infect. 2020;53:925-35. https://doi.org/10.1016/j.jmii.2019.09.005
  29. Wasano K, Hirakawa Y. Recombinant galectin-1 recognizes mucin and epithelial cell surface glycocalyces of gastrointestinal tract. J Histochem Cytochem. 1997;45:275-83. https://doi.org/10.1177/002215549704500212
  30. Wei X, Yang J, Liu X, Yang D, Xu J, Fang J, et al. Identification and transcriptional analysis of two types of lectins (SgCTL-1 and SgGal-1) from mollusk Solen grandis. Fish Shellfish Immunol. 2012;33:204-12. https://doi.org/10.1016/j.fsi.2012.04.012
  31. Zhu D, Fu P, Huang R, Xiong L, Wang Y, He L, et al. Molecular characterization, tissue distribution and functional analysis of galectin 1-like 2 in grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol. 2019;94:455-63. https://doi.org/10.1016/j.fsi.2019.09.041