Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Transcriptional regulation of chicken leukocyte cell-derived chemotaxin 2 in response to toll-like receptor 3 stimulation

  • Lee, Seokhyun (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) ;
  • Lee, Ra Ham (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) ;
  • Kim, Sung-Jo (Department of Biotechnology, Hoseo University) ;
  • Lee, Hak-Kyo (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) ;
  • Na, Chong-Sam (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University) ;
  • Song, Ki-Duk (Department of Animal Biotechnology, College of Agricultural and Life Sciences, Jeonbuk National University)
  • Received : 2019.03.07
  • Accepted : 2019.06.20
  • Published : 2019.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: Leukocyte cell-derived chemotaxin 2 (LECT2) is associated with several physiological processes including inflammation, tumorigenesis, and natural killer T cell generation. Chicken LECT2 (chLECT2) gene was originally identified as one of the differentially expressed genes in chicken kidney tissue, where the chickens were fed with different calcium doses. In this study, the molecular characteristics and gene expression of chLECT2 were analyzed under the stimulation of toll-like receptor 3 (TLR3) ligand to understand the involvement of chLECT2 expression in chicken metabolic disorders. Methods: Amino acid sequence of LECT2 proteins from various species including fowl, fish, and mammal were retrieved from the Ensembl database and subjected to Insilco analyses. In addition, the time- and dose-dependent expression of chLECT2 was examined in DF-1 cells which were stimulated with polyinosinic:polycytidylic acid (poly [I:C]), a TLR3 ligand. Further, to explore the transcription factors required for the transcription of chLECT2, DF-1 cells were treated with poly (I:C) in the presence or absence of the nuclear factor ${\kappa}B$ ($NF{\kappa}B$) and activated protein 1 (AP-1) inhibitors. Results: The amino acid sequence prediction of chLECT2 protein revealed that along with duck LECT2 (duLECT2), it has unique signal peptide different from other vertebrate orthologs, and only chLECT2 and duLECT2 have an additional 157 and 161 amino acids on their carboxyl terminus, respectively. Phylogenetic analysis suggested that chLECT2 is evolved from a common ancestor along with the actinopterygii hence, more closely related than to the mammals. Our quantitative polymerase chain reaction results showed that, the expression of chLECT2 was up-regulated significantly in DF-1 cells under the stimulation of poly (I:C) (p<0.05). However, in the presence of $NF{\kappa}B$ or AP-1 inhibitors, the expression of chLECT2 is suppressed suggesting that both $NF{\kappa}B$ and AP-1 transcription factors are required for the induction of chLECT2 expression. Conclusion: The present results suggest that chLECT2 gene might be a target gene of TLR3 signaling. For the future, the expression pattern or molecular mechanism of chLECT2 under stimulation of other innate immune receptors shall be studied. The protein function of chLECT2 will be more clearly understood if further investigation about the mechanism of LECT2 in TLR pathways is conducted.

Keywords

References

  1. Yamagoe S, Mizuno S, Suzuki K. Molecular cloning of human and bovine LECT2 having a neutrophil chemotactic activity and its specific expression in the liver. Biochim Biophys Acta 1998;1396:105-13. https://doi.org/10.1016/S0167-4781(97)00181-4
  2. Okumura A, Suzuki T, Dohmae N, et al. Identification and assignment of three disulfide bonds in mammalian leukocyte cell-derived chemotaxin 2 by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Biosci Trends 2009;3:139-43.
  3. Sato Y, Watanabe H, Kameyama H, et al. Changes in serum LECT 2 levels during the early period of liver regeneration after adult living related donor liver transplantation. Transplant Proc 2004;36:2357-8. https://doi.org/10.1016/j.transproceed.2004.07.006
  4. Ong HT, Tan PK, Wang SM, Hian Low DT, Ooi LL, Hui KM. The tumor suppressor function of LECT2 in human hepatocellular carcinoma makes it a potential therapeutic target. Cancer Gene Ther 2011;18:399-406. https://doi.org/10.1038/cgt.2011.5
  5. Anson M, Crain-Denoyelle AM, Baud V, et al. Oncogenic beta-catenin triggers an inflammatory response that determines the aggressiveness of hepatocellular carcinoma in mice. J Clin Invest 2012;122:586-99. https://doi.org/10.1172/JCI43937
  6. Okumura A, Saito T, Otani I, et al. Suppressive role of leukocyte cell-derived chemotaxin 2 in mouse anti-type II collagen antibody-induced arthritis. Arthritis Rheum 2008;58:413-21. https://doi.org/10.1002/art.23215
  7. Dang MH, Kato H, Ueshiba H, et al. Possible role of LECT2 as an intrinsic regulatory factor in SEA-induced toxicity in d-galactosamine-sensitized mice. Clin Immunol 2010;137:311-21. https://doi.org/10.1016/j.clim.2010.08.002
  8. Saito T, Okumura A, Watanabe H, et al. Increase in hepatic NKT cells in leukocyte cell-derived chemotaxin 2-deficient mice contributes to severe concanavalin A-induced hepatitis. J Immunol 2004;173:579-85. https://doi.org/10.4049/jimmunol.173.1.579
  9. Ando K, Kato H, Kotani T, Ozaki M, Arimura Y, Yagi J. Plasma leukocyte cell-derived chemotaxin 2 is associated with the severity of systemic inflammation in patients with sepsis. Microbiol Immunol 2012;56:708-18. https://doi.org/10.1111/j.1348-0421.2012.00488.x
  10. Ovejero C, Cavard C, Perianin A, et al. Identification of the leukocyte cell-derived chemotaxin 2 as a direct target gene of beta-catenin in the liver. Hepatology 2004;40:167-76. https://doi.org/10.1002/hep.20286
  11. Lu XJ, Chen J, Yu CH, et al. LECT2 protects mice against bacterial sepsis by activating macrophages via the CD209a receptor. J Exp Med 2013;210:5-13. https://doi.org/10.1084/jem.20121466
  12. Yoo HJ, Hwang SY, Choi JH, et al. Association of leukocyte cell-derived chemotaxin 2 (LECT2) with NAFLD, metabolic syndrome, and atherosclerosis. PLoS One 2017;12:e0174717. https://doi.org/10.1371/journal.pone.0174717
  13. Bischoff KM, Pishko EJ, Genovese KJ, et al. Chicken mim-1 protein, P33, is a heterophil chemotactic factor present in Salmonella enteritidis immune lymphokine. J Food Prot 2001;64:1503-9. https://doi.org/10.4315/0362-028x-64.10.1503
  14. Sekelova Z, Stepanova H, Polansky O, et al. Differential protein expression in chicken macrophages and heterophils in vivo following infection with Salmonella Enteritidis. Vet Res 2017;48:35. https://doi.org/10.1186/s13567-017-0439-0
  15. Sekelova Z, Polansky O, Stepanova H, et al. Different roles of CD4, CD8 and gammadelta T-lymphocytes in naive and vaccinated chickens during Salmonella Enteritidis infection. Proteomics 2017;17:1700073. https://doi.org/10.1002/pmic.201700073
  16. Xu Q, Chen Y, Tong YY, et al. Identification and expression analysis of the leukocyte cell-derived chemotaxin-2 (LECT2) gene in duck (Anas platyrhynchos). Gene 2014;533:280-5. https://doi.org/10.1016/j.gene.2013.09.047
  17. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010;11:373-84. https://doi.org/10.1038/ni.1863
  18. Kogut MH, Genovese KJ, He H. Flagellin and lipopolysaccharide stimulate the MEK-ERK signaling pathway in chicken heterophils through differential activation of the small GTPases, Ras and Rap1. Mol Immunol 2007;44:1729-36. https://doi.org/10.1016/j.molimm.2006.07.292
  19. Kogut MH, Genovese KJ, He H, Kaiser P. Flagellin and lipopolysaccharide up-regulation of IL-6 and CXCLi2 gene expression in chicken heterophils is mediated by ERK1/2-dependent activation of AP-1 and NF-kappaB signaling pathways. Innate Immun 2008;14:213-22. https://doi.org/10.1177/1753425908094416
  20. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870-4. https://doi.org/10.1093/molbev/msw054
  21. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  22. Park W, Rengaraj D, Kil DY, Kim H, Lee HK, Song KD. RNAseq analysis of the kidneys of broiler chickens fed diets containing different concentrations of calcium. Sci Rep 2017;7:11740. https://doi.org/10.1038/s41598-017-11379-7
  23. Lan F, Misu H, Chikamoto K, et al. LECT2 functions as a hepatokine that links obesity to skeletal muscle insulin resistance. Diabetes 2014;63:1649-64. https://doi.org/10.2337/db13-0728
  24. Hwang HJ, Jung TW, Hong HC, et al. LECT2 induces atherosclerotic inflammatory reaction via CD209 receptor-mediated JNK phosphorylation in human endothelial cells. Metabolism 2015;64:1175-82. https://doi.org/10.1016/j.metabol.2015.06.001
  25. Bornelov S, Seroussi E, Yosefi S, et al. Comparative omics and feeding manipulations in chicken indicate a shift of the endocrine role of visceral fat towards reproduction. BMC Genomics 2018;19:295. https://doi.org/10.1186/s12864-018-4675-0
  26. Kamimura T, Isobe N, Yoshimura Y. Effects of inhibitors of transcription factors, nuclear factor-kappaB and activator protein 1, on the expression of proinflammatory cytokines and chemokines induced by stimulation with Toll-like receptor ligands in hen vaginal cells. Poult Sci 2017;96:723-30. https://doi.org/10.3382/ps/pew366
  27. Lin B, Chen S, Cao Z, et al. Acute phase response in zebrafish upon Aeromonas salmonicida and Staphylococcus aureus infection: striking similarities and obvious differences with mammals. Mol Immunol 2007;44:295-301. https://doi.org/10.1016/j.molimm.2006.03.001
  28. Li MY, Chen J, Shi YH. Molecular cloning of leucocyte cellderived chemotaxin-2 gene in croceine croaker (Pseudosciaena crocea). Fish Shellfish Immunol 2008;24:252-6. https://doi.org/10.1016/j.fsi.2007.09.003
  29. Fu GH, Bai ZY, Xia JH, et al. Characterization of the LECT2 gene and its associations with resistance to the big belly disease in Asian seabass. Fish Shellfish Immunol 2014;37:131-8. https://doi.org/10.1016/j.fsi.2014.01.019
  30. Wang Z, Lu J, Li C, Li Q, Pang Y. Characterization of the LECT2 gene and its protective effects against microbial infection via large lymphocytes in Lampetra japonica. Dev Comp Immunol 2018;79:75-85. https://doi.org/10.1016/j.dci.2017.09.018
  31. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 2006;80:5059-64. https://doi.org/10.1128/JVI.80.10.5059-5064.2006
  32. Okahira S, Nishikawa F, Nishikawa S, Akazawa T, Seya T, Matsumoto M. Interferon-beta induction through toll-like receptor 3 depends on double-stranded RNA structure. DNA Cell Biol 2005;24:614-23. https://doi.org/10.1089/dna.2005.24.614
  33. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001;413:732-8. https://doi.org/10.1038/35099560

Cited by

  1. Expression of Chicken Leukocyte Cell-Derived Chemotaxin 2 in the Embryonic Bursa of Fabricius vol.20, pp.1, 2019, https://doi.org/10.3923/ijps.2021.43.47
  2. LECT2 Protects Nile Tilapia (Oreochromis niloticus) Against Streptococcus agalatiae Infection vol.12, 2021, https://doi.org/10.3389/fimmu.2021.667781