Sequence polymorphism of two major histocompatibility (MH) class II B genes and their association with Vibrio anguillarum infection in half-smooth tongue sole (Cynoglossus semilaevis)

Chunmei Li; Quanqi Zhang; Yan Yu; Shuo Li; Qiwang Zhong; Yeying Sun; Zhigang Wang; Jie Qi; Jieming Zhai; Xubo Wang

doi:10.1007/s00343-011-0278-1

Your Location：

Home >

Browse articles >

Sequence polymorphism of two major histocompatibility (MH) class II B genes and their association with Vibrio anguillarum infection in half-smooth tongue sole (Cynoglossus semilaevis)

Updated：2023-05-16

- Sequence polymorphism of two major histocompatibility (MH) class II B genes and their association with Vibrio anguillarum infection in half-smooth tongue sole (Cynoglossus semilaevis)
- Journal of Oceanology and Limnology Vol. 29, Issue 6, Pages: 1275-1286(2011)
- Affiliations：
  
  1. Key Laboratory of Marine Genetics and Breeding of Ministry of Education Ocean University of China
  2. Laizhou Ming Bo Aquatic Co. Ltd.
- Author bio：
- Funds：
- DOI：10.1007/s00343-011-0278-1
  CLC：
- Online First：25 October 2011，
  
  Published：2011
- Accepted：
Scan QR Code
Li, C., Zhang, Q., Yu, Y. et al. Sequence polymorphism of two major histocompatibility (MH) class II B genes and their association with Vibrio anguillarum infection in half-smooth tongue sole (Cynoglossus semilaevis)., Chin. J. Ocean. Limnol. 29, 1275–1286 (2011). https://doi.org/10.1007/s00343-011-0278-1
DOI：

Li, C., Zhang, Q., Yu, Y. et al. Sequence polymorphism of two major histocompatibility (MH) class II B genes and their association with Vibrio anguillarum infection in half-smooth tongue sole (Cynoglossus semilaevis)., Chin. J. Ocean. Limnol. 29, 1275–1286 (2011). https://doi.org/10.1007/s00343-011-0278-1 DOI：

摘要

Abstract

Major histocompatibility complex (MHC) class II B molecules play an important role in the adaptive immune response in fish. Previous study has reported that two highly polymorphic class II B genes

Cyse-DAB and Cyse-DBB exist in half-smooth tongue sole (Cynoglossus semilaevis). In this study

the polymorphism within exon 2 of the class II B genes following bacterial challenge was evaluated. Two hundred C. semilaevis individuals were injected intraperitoneally with Vibrio anguillarum. Muscle tissue from the first 20 dead and 20 of the survivors was collected for genotyping. Sixty alleles from the 40 individuals were isolated

of which 32 belonged to Cyse-DAB and 28 belonged to Cyse-DBB. The rate of d N (non-synonymous substitution) was higher than that of d S (synonymous substitution) in the PBRs (peptide binding residues) of both class II B genes. Conversely

the rate of d S was higher than d N in the non-PBRs and the complete exon 2 sequence. Thus

the results suggest that positive selection has occurred in the PBRs and purifying selection in the non-PBRs and exon 2. Thirteen class II B alleles were used to study the association between alleles and resistance to infection. Though not significant

alleles Cyse-DAB*0601

Cyse-DAB*0706

and Cyse-DBB*0101

Cyse-DBB*1301 were only found in surviving individuals and may represent alleles that have resistance against V. anguillarum infection. Alleles Cyse-DAB*0701 and Cyse-DAB*1301 were significantly more prevalent in dead individuals than in surviving ones and may represent alleles that are associated with increased susceptibility to V. anguillarum infection.

关键词

Keywords

references

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

Brown J H, Jardetzky T S, Gorga J C, Stern L J, Urban R G, Strominger J L, Wiley D C. 1993. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature, 364: 33–39.

Buonocore F, Randelli E, Casani D, Costantini S, Facchiano A, Scapigliati G, Stet R J M. 2007. Molecular cloning, differential expression and 3D structural analysis of the MHC class-II beta chain from sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol., 23: 853–866.

Consuegra S, Garcia de Leaniz C. 2008 MHC-mediated mate choice increases parasite resistance in salmon. Proc. R. Soc. B., 275: 1 397–1 403.

Croisetière S, Tarte P D, Bernatchez L, Belhumeur P. 2008. Identification of MHC class IIβ resistance/susceptibility alleles to Aeromonas salmonicida in brook charr (Salvelinus fontinalis). Mol. Immunol., 45: 3 107–3 116.

Davies C J, Andersson L, Ellis S A, Hensen E J, Lewin H A, Mikko S, Muggli-Cockett N E, van der Poel J J, Russell G C. 1997. Nomenclature for factors of the BoLA system, 1996: report of the ISAG BoLA Nomenclature Committee. Animal Genetics, 28: 159–168.

Ding S, Zhang Z, Du J, Wang J, Zeng H, Wang Y, Chen X. 2009. The cloning and polymorphism of MHC class II B gene from Epinephelus akaara. Acta Oceanologica Sinica, 31: 129–138.

Dionne M, Miller K M, Dodson J J, Bernatchez L. 2009. MHC standing genetic variation and pathogen resistance in wild Atlantic salmon. Philos. Trans. R. Soc Lond B: Biol. Sci., 364: 1 555–1 565.

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

Evans M L, Neff B D. 2009. Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha). Mol. Ecol., 18: 4 716–4 729.

Flajnik M F, Kasahara M. 2001. Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity, 15: 351–362.

Hedrick P W. 2002. Pathogen resistance and genetic variation at MHC loci. Evolution, 56: 1 902–1 908.

Hughes A L, Nei M. 1989. Nucleotide substitution atmajor histocompatibility complex class II loci: evidence for overdominant selection. Proc. Natl. Acad. Sci. U. S. A., 86: 958–962.

Jeffery K J, Bangham C R. 2000. Do infectious diseases drive MHC diversity? Micorbes Infect., 2: 1 355–1 341.

Kekäläinen J, Vallunen J A, Primmer C R, Rättyä J, Taskinen J. 2009. Signals of major histocompatibility complex overdominance in a wild salmonid population. Proc. Biol. Sci., 276: 3 133–3 140.

Klein J, Figueroa F. 1986. Evolution of the major histocompatibility complex. Crit. Rev. Immunol., 6: 295–386.

Klein D, Ono H, O’hUigin C, Vincek V, Goldschmidt T, Klein J. 1993. Extensive MHC variability in cichlid fishes of Lake Malawi. Nature, 364: 330.

König R. 2002. Interactions between MHC molecules and co-receptors of the TCR. Curr. Opin. Immunol., 14: 75–83.

Kruiswijk C P, Hermsen T, van Heerwaarden J, Dixon B, Savelkoul H F J, Stet R J M. 2005. Major histocompatibility genes in the Lake Tana African large barb species flock: evidence for complete partitioning of class II B, but not class I, genes among different species. Immunogenetics, 56: 894–908.

Li C, Yu Y, Sun Y, Li S, Zhong Q, Wang X, Wang Z, Qi J, Zhang Q. 2010. Isolation, polymorphism and expression study of two distinct major histocompatibility complex class II B genes from half-smooth tongue sole (Cynoglossus semilaevis). Int. J. Immunogenet., 37: 185–197.

Lohm J, Grahn M, Langefors A, Anderson Ø, Storset A, von Schantz T. 2002. Experimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection. Proc. Biol. Sci., 269: 2 029–2 033.

Matthews B, Harmon L J, M’Gonigle L, Marchinko K B, Schaschl H. 2010. Sympatric and allopatric divergence of MHC genes in threespine stickleback. PLoS One, 5: e10948.

Nei M, Gojobori T. 1986. Simple methods for estimating the number of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol., 3: 418–426.

Nikolich-Žugich J, Fremont D H, Miley M J, Messaoudi I. 2004. The role of mhc polymorphism in anti-microbial resistance. Microbes Infect., 6: 501–512.

Niu H, Chang J, Ma S, Wang L. 2007. The biology and cultural ecology of Cynoglossus semilaevis Günther. Fish. Sci., 26: 425–426.

Ono H, Klein D, Vincek V, Figueroa F, O’Huigin C. 1992. Major histocompatibility complex class II genes of zebrafish. Proc. Natl. Acad. Sci. U. S. A., 89: 11 886–11 890.

Ono H, O’hUigin C, Tichy H, Klein J. 1993. Major histocompatibility complex variation in two species of cichlid fishes from Lake Malawi. Mol. Biol. Evol., 10: 1 060–1 072.

Ottová E, Šimkova A, Martin J F, de Bellocp J G, Gelnar M, Allienne J F, Morand S. 2005. Evolution and trans-species polymorphism of MHC class IIβ genes in cyprinid fish. Fish Shellfish Immunol., 18: 199–222.

Rakus K Ł, Wiegertjes G F, Adamek M, Bekh V, Stet R J M, Irnazarow I. 2008. Application of PCR-RF-SSCP to study major histocompatibitity class II B polymorphism in common carp (Cyprinus carpio L.). Fish Shellfish Immunol., 24: 734–744.

Rakus K Ł, Wiegertjes G F, Jurecka P, Walker P D, Pilarczyk A, Irnazarow I. 2009. Major histocompatibility (MH) class II B gene polymorphism influences disease resistance of common carp (Cyprinus carpio L.). Aquaculture, 288: 44–50.

Rice W R. 1989. Analysis tables of statistical tests. Evolution, 43: 223–225.

Ristow S S, Grabowski L D, Thompson S M, Warr G W, Kaattari S L, de Avila J M, Thorgaard G H. 1999. Coding sequences of the MHC b chain of homozygous rainbow trout (Oncorhynchus mykiss). Dev. Comp. Immunol., 23: 51–60.

Rothbard J B, Gefter M L. 1991. Interactions between immunogenic peptides and MHC proteins. Annu. Rev. Immunol., 9: 527–565.

Rozas J, Rozas R. 1997. DnaSP version 2.0: a novel software package for extensive molecular population genetic analysis. Comput. Appl. Biosci., 13: 307–311.

Stet R J, de Vries B, Mudde K, Hermsen T, van Heerwaarden J, Shum B P, Grimholt U. 2002. Unique haplotypes of co-segregating major histocompatibility class II A and class II B alleles in Atlantic salmon (Salmo salar) give rise to diverse class II genotypes. Immunogenetics, 54: 320–331.

Summers K, Roney K E, da Silva J, Capraro G, Cuthbertson B J, Kazianis S, Rosenthal G G, Ryan M J, McConnell T J. 2009. Divergent patterns of selection on the DAB and DXB MHC class II loci in Xiphophorus fishes. Genetica, 135: 379–390.

Takahata N, Nei M. 1990. Allelic genealogy under overdominant and frequency dependent selection and polymorphism of major histocompatibility complex loci. Genetics, 124: 967–978.

Trowsdale J, Parham P. 2004. Mini-review: defence strategies and immunity-related genes. Eur. J. Immunol., 34: 7–17.

Wang Y, Han Y, Chen J, Zhang X. 2007. Isolation of Photobacterium damselae subsp. piscicida from diseased tongue sole (Cynoglossus semilaevis Gunther) in China. Acta Microbiol. Sin., 47: 763–768.

Wedekind C, Walker M, Portmann J, Cenni B, Müller R, Binz T. 2004. MHC-linked susceptibility to a bacterial infection, but no MHC-linked cryptic female choice in whitefish. J. Evol. Biol., 17: 11–18.

Wegner K M, Kalbe M, Milinski M, Reusch T B. 2008. Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype. BMC Evol. Biol., 8: 124.

Xu T, Chen S, Ji X, Tian Y. 2008. MHC polymorphism and disease resistance to Vibrio anguillarum in 12 selective Japanese flounder (Paralichthys olivaceus) families. Fish Shellfish Immunol., 25: 213–221.

Yang Z, Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol., 19: 908–917.

Yu Y, Zhong Q, Li C, Jiang L, Yan F, Wang Z, Zhang Q. 2009a. Isolation and characterization of Toll-like receptor 9 in half-smooth tongue sole Cynoglossus semilaevis. Fish Shellfish Immunol., 26: 492–499.

Yu Y, Zhong Q, Zhang Q, Wang Z, Li C, Yan F, Jiang L. 2009b. Full-length sequence and expression analysis of a myeloid differentiation factor 88 (MyD88) in half-smooth tongue sole Cynoglossus semilaevis. Int. J. Immunogenet., 36: 173–182.

Zhang Y, Chen S. 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.

Zhang Y, Chen S, Liu Y, Sha Z, Liu Z. 2006. Major histocompatibility complex class II B allele polymorphism and its association with resistance/susceptibility to Vibrio anguillarum in Japanese flounder (Paralichthys olivaceus). Mar. Biotechnol., 8: 600–610.

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

AVibrio anguillarum strain associated with skin ulcer on cultured flounder,Paralichthys olivaceus

Properties of proteolytic toxin ofVibrio anguilolarum from diseased flounder

Distribution of bacteria injected in body of giant black shrimp,Penaeus monodon

Construction and characterization of a fosmid library for pathogenic bacterium Vibrio anguillarum

Identification and characterization of the Vibrio anguillarum prtV gene encoding a new metalloprotease

Related Author

Zhang Pei-jun

Xu Yong-li

Tan Xun-gang

Mo Zhao-lan

Zhang Pei-jun

Chen Shi-yong

Mo Zhao-lan

Karin vande Braak

Related Institution

Experimental Marine Biology Laboratory Institute of Oceanology Chinese Academy of Sciences

Experimental Biology Laboratory Institute of Oceanology Chinese Academy of Sciences

South China Sea Fisheries Research Institute

Ocean University of China

Institute of Oceanology Chinese Academy of Sciences

Address：Editorial Office of JOL, 88 Haijun Rd. Qingdao, 266000, China
Tel：+86-532-82898754 Email：jol@qdio.ac.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰