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Cloning and structure of a histocompatibility class IIA gene (Lelo-DAA) in Chinese longsnout catfish (Leiocassis longirostris)

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Abstract

Here, the major histocompatibility complex (MHC) class II alpha chain gene in the Chinese longsnout catfish (Leiocassis longirostris) was characterized through cloning, sequencing, polymorphism analysis, and expression patterns in various tissues. The full-length LeloDAA cDNA comprises 1,114 bp with a 5′-UTR region of 79 bp, an open reading frame of 714 bp and a 3′-UTR of 302 bp. The deduced protein sequence shows the following important features: leader peptide, α1, α2, and CP/TM/CYT regions. Using long PCR techniques, the genomic sequence was further identified to be 2,093 bp in length, containing four exons and three introns. Three class IIA alleles were identified from four individuals. Two different alleles observed (at most) in each individual suggest the existence of a single locus of class IIA gene in the Chinese longsnout catfish genome. This locus is polymorphic and most of the amino acidic changes occurred in the α1 domain containing the peptide-binding region. Lelo-DAA mRNA expression was mainly found in the intestine, gills, spleen, head kidney and liver; minor expression was detected in the stomach, skin, heart and muscle. Our results yield insight into Chinese longsnout catfish T cell immune responses and will aid future work on the genetic status of this economically important species.

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References

  • Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    Article  CAS  PubMed  Google Scholar 

  • Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 1:179–224

    Article  Google Scholar 

  • Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Mol Evol 16:363–377

    CAS  Google Scholar 

  • Buonocore F, Randelli E, Casani D, Costantini S, Facchiano A, Scapigliati G, Stet RJM (2007) Molecular cloning, differential expression and 3D structural analysis of the MHC class IIb chain from sea bass (Dicentrarchus labrax). Fish Shellfish Immun 23:853–866

    Article  CAS  Google Scholar 

  • Chen SL, Xu MY, Hu SN, Li L (2004) Analysis of immune-relevant genes expressed in red sea bream (Chrysophrys major) spleen. Aquaculture 240(1):115–130

    Article  CAS  Google Scholar 

  • Cosson P, Bonifacino JS (1992) Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science 258:659–662

    Article  CAS  PubMed  Google Scholar 

  • Dai JH, Yin WL, Yang DS, Xiong QM (1994) Studies on mitochondrial DNA from liver of Leiocassis longirostris. J Wuhan Univ 1:115–120 (in Chinese)

    Google Scholar 

  • Dixon B, Stet RJM (2001) The relationship between major histocompatibility receptors and innate immunity in teleost fish. Dev Comp Immunol 25:683–699

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  CAS  PubMed  Google Scholar 

  • Gannagé M, Münz C (2009) Autophagy in MHC class II presentation of endogenous antigens. Curr Top Microbiol 335:123–140

    Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins M, Appel R, Bairoch A (2005) Protein identification and analysis tool on the ExPASy server. In: Walker J (ed) The Proteomics Protocols Handbook. Humana Press, Totowa, pp 571–607

    Chapter  Google Scholar 

  • Godwin UB, Flores M, Quiniou S, Wilson MR, Miller NW, Clem LW, McConnell TJ (2000) MHC class II A genes in the channel catfish (Ictalurus punctatus). Dev Comp Immunol 24:609–622

    Article  CAS  PubMed  Google Scholar 

  • Grimholt U, Getahun A, Hermsen T, Stet RJM (2005) The major histocompatibility class II alpha chain in salmonid fishes. Dev Comp Immunol 24:751–763

    Article  Google Scholar 

  • Hardee JJ, Godwin U, Benedetto R, McConnell TJ (1995) Major histocompatibility complex class II A gene polymorphism in the striped bass. Immunogenetics 41:229–238

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Nakanishi T, Kurosawa Y (1990) Isolation of carp genes encoding major histocmpatibility complex antigens. P Natl Acad Sci USA 87:6863–6867

    Article  CAS  Google Scholar 

  • Hulo N, Bairoch A, Bulliard V, Cerutti L, Cuche BA, Castro ED, Lachaize C, Langendijk-Genevaux PS, Sigrist CJA (2008) The 20 years of PROSITE. Nucleic Acids Res 36:245–249

    Article  Google Scholar 

  • Janeway CA, Travers P, Walport M, Shlomchik M (2001) Immunobiology: the immune system in health and disease. Garland Science, New York

    Google Scholar 

  • Julenius K, Mølgaard A, Gupta R, Brunak S (2005) Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15:153–164

    Article  CAS  PubMed  Google Scholar 

  • Kennedy LJ, Ryvar R, Gaskell RM, Addie DD, Willoughbym K, Carter SD, Thomson W, Ollier WER, Radford AD (2002) Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics 54:348–352

    Article  CAS  PubMed  Google Scholar 

  • Klein J (1986) Natural history of the major histocompatibility complex. Wiley, New York, vol xv, 775 p

  • Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    Article  CAS  PubMed  Google Scholar 

  • Lehman N, Decker DJ, Stewart BS (2004) Divergent patterns of variation in major histocompatibility complex class II alleles among antartic phocid pinnipeds. J Mammal 85:1215–1224

    Article  Google Scholar 

  • Luo M, Jiang LK, Liu Y, Zhan GQ, Xia SZ (2000) Comparative study on isoenzymes in Leiocassis longirostris. Chin J Appl Environ Biol 6:447–451

    CAS  Google Scholar 

  • Meager S, Potts WK (1997) A microsatellite-based MHC genotyping system for house mice (Mus domesticus). Hereditas 127:75–82

    Article  Google Scholar 

  • Milinski M (2003) The function of mate choice in sticklebacks: optimizing Mhc genetics. J Fish Biol 63:1–16

    Article  Google Scholar 

  • Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol S 37:159–186

    Article  Google Scholar 

  • Morris DJ, Adams A, Richards RH (2000) In situ hybridisation identifies the gill as a portal of entry for PKK (Phylum Myxozoa), the causative agent of proliferative kidney disease in salmonids. Parasitol Res 86:950–956

    Article  CAS  PubMed  Google Scholar 

  • Murray BW, Sültmann H, Klein J (1999) New family of Mhc class II A genes identified from cDNA sequences in the cichlid fish Aulonocara hansbaenschi. Immunogenetics 49:544–548

    Article  CAS  PubMed  Google Scholar 

  • Nielsen M, Lundegaard C, Lund O, Petersen TN (2010) CPH models-3.0 -Remote homology modeling using structure guided sequence profiles. Nucleic Acids Res 38(Web Server issue):576–581

    Article  Google Scholar 

  • Ober C, van der Ven K (1997) Immunogenetics of reproduction: an overview. Curr Top Microbiol 222:1–23

    CAS  Google Scholar 

  • Pollastri G, McLysaght A (2005) Porter: a new, accurate server for protein secondary structure prediction. Bioinformatics 21:1719–1720

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Shen T, Xu SX, Yang M, Pang SY, Yang G (2011) Molecular cloning, expression pattern, and 3D structural analysis of the MHC class IIB gene in the Chinese longsnout catfish (Leiocassis longirostris). Vet Immunol Immunop 141:33–45

    Article  CAS  Google Scholar 

  • Steinmetz M, Hood L (1983) Genes of the major histocompatibility complex in mouse and man. Science 222:727–733

    Article  CAS  PubMed  Google Scholar 

  • Sültmann H, Mayer WE, Figueroa F, O’hUigin C, Klein J (1993) Zebrafish Mhc class II α chain-encoding genes: polymorphism, expression, and function. Immunogenetics 38:408–420

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evolution Biol 16:224–232

    Article  CAS  Google Scholar 

  • Wu JM, Jiang RL, Zhang JP (1999) Artificial induced spawning of Leiocassis longirostris and change of ultrastructure of hypophysis GTH cell. J Fish China 23:248–253

    CAS  Google Scholar 

  • Xu TJ, Chen SL, Ji XS, Sha ZX (2009) Molecular cloning, genomic structure, polymorphism and expression analysis of major histocompatibility complex class IIA and IIB genes of half-smooth tongue sole (Cynoglossus semilaevis). Fish Shellfish Immun 27:192–201

    Article  CAS  Google Scholar 

  • Zhang YX, Chen SL (2006) Molecular identification, polymorphism, and expression analysis of major histocompatibility complex class IIA and B genes of turbot (Scophthalmus maximus). Mar Biotechnol 8:611–623

    Article  CAS  PubMed  Google Scholar 

  • Zhang YX, Chen SL, Liu YG, Sha ZX, Liu ZJ (2006) Major histocompatibility complex class IIB allele polymorphism and its association with resistance/susceptibility to vibrio anguillarum in Japanese flounder (Paralichthys olivaceus). Mar Biotechnol 8:600–610

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported as a China Postdoctoral Science Foundation Funded Project (2013m541726), University Science Research Project of Jiangsu Province (13kjb310019), Natural Science Foundation of Jiangsu Province for Youth (BK20140364).

Conflict of interest

We confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

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Authors and Affiliations

  1. Pathology Center and Department of Pathology, Soochow University, Suzhou, 215123, Jiangsu, China

    Tong Shen, Xiaoshun He, Meiling Lei, Jingru Wang, Xiuming Li & Jianming Li

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  1. Tong Shen
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  2. Xiaoshun He
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  3. Meiling Lei
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  4. Jingru Wang
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  5. Xiuming Li
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  6. Jianming Li
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Corresponding author

Correspondence to Jianming Li.

Additional information

Tong Shen, Xiaoshun He: Both authors contributed equally to this work.

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Supplementary material

Additional file 1: Table S1 Primers used for cloning and expression analysis of the Chinese longsnout catfish MHC class IIA gene.

Additional file 2: Table S2 MHC class IIA amino acid identity of the Chinese longsnout catfish with other vertebrates, as determined by Blast.

Supplementary material 1 (DOCX 18 kb)

Supplementary material 1 (DOCX 17 kb)

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Shen, T., He, X., Lei, M. et al. Cloning and structure of a histocompatibility class IIA gene (Lelo-DAA) in Chinese longsnout catfish (Leiocassis longirostris). Genes Genom 36, 745–753 (2014). https://doi.org/10.1007/s13258-014-0208-7

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  • DOI: https://doi.org/10.1007/s13258-014-0208-7

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