MHC polymorphism and disease resistance to vibrio anguillarum in 8 families of half-smooth tongue sole (Cynoglossus semilaevis)

BMC Genetics

Jing-feng Yang¹  Yang Liu¹  Yan-hong Liu²  Song-lin Chen¹  Min Du² 

[1] Key Lab for Sustainable Utilization of Marine Fisheries Resources, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 266071, Qingdao, China;Honghe University, Mengzi, Yunnan Province,661100, China

关键词: resistance;    susceptibility;    MHC IIB;    polymorphism;    Vibrio anguillarum;    Cynoglossus semilaevis;   

Others  :  1122610
DOI  :  10.1186/1471-2156-12-78

 received in 2011-02-28, accepted in 2011-09-02,  发布年份 2011

【 摘 要 】

Background

Genes in the major histocompatibility complex (MHC) have a critical role in both the innate and adaptive immune responses because of their involvement in presenting foreign peptides to T cells. However, the nature has remained largely unknown.

Results

We examined the genetic variation in MHC class IIB in half-smooth tongue sole (Cynoglossus semilaevis) after challenge with vibrio anguillarum. Two thousand and four hundred fry from 12 half-smooth tongue sole families were challenged with Vibrio anguillarum. To determine any association between alleles and resistance or susceptibility to V. anguillarum, 160 individuals from four high-resistance (HR, < 40.55% mortality) families and four low-resistance (LR, > 73.27% mortality) families were selected for MHC IIB exon2 gene sequence analysis. The MHC IIB exon2 genes of tongue sole displayed a high level of polymorphism and were discovered at least four loci. Meanwhile, the d_N/d_S [the ratio of non-synonymous (d_N) substitutions to synonymous (d_S) substitutions] in the peptide-binding region (PBR) was higher than that in the non-peptide-binding region (non-PBR). Eighty-eight alleles were discovered among 160 individuals, and 13 out of 88 alleles were used to analyze the distribution pattern between the resistant and susceptible families. Certain alleles presented in HR and LR with a different frequency, while other alleles were discovered in only the HR or LR families, not both. Five alleles, Cyse-DBB*6501, Cyse-DBB*4002, Cyse-DBB*6102, Cyse-DBB*5601 and Cyse-DBB*2801, were found to be associated with susceptibility to V. anguillarum with a frequency of 1.25%, 1.25%, 1.25%, 1.25% and 2.5% in the HR families, and 35%, 33.75%, 27.5%, 16.25%, 15% in the LR families (p < 0.01, 0.01, 0.01, 0.01, 0.01), respectively. Four alleles, Cyse-DBB*3301, Cyse-DBB*4701, Cyse-DBB*6801 and Cyse-DBB*5901, were found to be associated with resistance to V. anguillarum, with a frequency of 13.75%, 11.25%, 11.25%, 8.75% in the HR families and 1.25%, 1.25%, 1.25%, 1.25% and 1.25% in the LR families (p < 0.01, 0.05, 0.05 and p = 0.064), respectively.

Conclusions

Elucidation of the role of MHC II B genes in half-smooth tongue sole should prove to be helpful to the in-depth development of marker-assisted selective breeding in half-smooth tongue sole.

【 授权许可】

   
2011 Du et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Nikolich-Žugich J, Fremont DH, Miley MJ, Messaoudi I: The role of mhc polymorphism in anti-microbial resistance. Microbes and Infection 2004, 6:501-512.
• [2]Edwards SW, Hedrick PW: Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 1998, 13:305-311.
• [3]Srisapoome P, Ohira T, Hirono I, Aoki T: Cloning, characterization and expression of cDNA containing major histocompatibility complex classI, IIa and IIb genes of Japanese flounder. Paralichthys olivaceus. Fish Sci 2004, 70:264-276.
• [4]Rothbard JB, Gefter ML: Interactions between immunogenetic peptides and Mhc proteins. Annu Rev Immunol 1991, 9:527-565.
• [5]Kjøglum S, Larsen S, Grimholt U, Bakke HG: How specic MHC classI andclass II combinations affect disease resistance against infectious salmon anaemia in Atlantic salmon(Salmo salar). Fish Shellfish Immunol 2006, 21:431-441.
• [6]Hansen JD, Strassburger JC, Thorgaard GH, Young WP, DuPasquier L: Expression, linkage and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 1999, 163:774-786.
• [7]Graser R, O'hUigin C, Vincek V, Meyer A, Klein J: Trans-specie polymorphism of class II Mhc loci in danio fishes. Immunogenetics 1996, 44:36-48.
• [8]Sato A, Figueroa F, Murray BW, Malaga-Trillo E, Zaleska-Rutczynska Z, Sultmann H: Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 2000, 51:108-116.
• [9]Hashimoto K, Nakanishi T, Kurosawa Y: Isolation of carp genes encoding major histocompatibility complex antigens. Proc Natl Acad Sci USA 1990, 87:6863-6867.
• [10]Chen SL, Xu MY, Hu SN: Analysis of immune relevant genes expressed in red sea bream (Chrysophrys major). spleen Aquaculture 2004, 240:115-130.
• [11]Sato A, Figueroa F, O'Hugin C: Identification of major histocompatibility complex genes in the guppy,Poercilia reticulate. J Immunogenetics 1995, 43:38-49.
• [12]Rodrigues PNS: Expression of major histocompatibility complex genes in carp (Cyprinus carpio L.). Dutch: Elsevier Science Ltd. and Academic Press Ltd; 1996:1-27.
• [13]Reně JM: Inference of structure and function of fish major histocompatibility complex (MHC), molecules from expressed genes. Fish&Shellfish Immunology 1996, 6:305-318.
• [14]Godwin UB, Flores M, Quiniou S: MHC class II A gene in the channel catfish(Ictalurus punctatus). Dev Comp Immunol 2000, 24(6/7):609-622.
• [15]Grimholt U, Larsen S, Nordmo R, Midtlying P, Kjoeglum S, Storest A: MHC polymorphism and disease resistance in Atlantic salmon(Salmo salar);facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 2003, 55:210-219.
• [16]Shum BP, Azumi K, Zhang S: Unexpected beta microglobulin sequence diversity in individual rainbow trout. Proceedings of the National Academy of Sciences USA 1996, 93:2779-2784.
• [17]Klein D, Ono H, O'hUighin C: Extensive MHC variability in cichlid fishes of Lake Malawi. Nature 1993, 6:330-334.
• [18]Dorschner MO, Duris T, Bront CR: High levels of MHC class II allelic diversity in lake trout from lake superior. J Heredity 2000, 91:359-363.
• [19]Grimholt U, Olsaker I, Lindstrm DV: A study of variability in the MHC class II beta I and class I alpha2 domain exons of Atlantic salmon, Salmo salar L. Anim genet 1994, 25:147-153.
• [20]Ono H, O'hUigin C, Tichy H: Major histocompatibility complex variation in two sepecies of cichlid fishes from Lake malawi. Mol Biol Evol 1993, 10:1060-1072.
• [21]Figueroa F, Mayer WE, Sultmann H: Mhc class IIB gene evolution in East African cichlid fishes. Immunogenetics 2000, 51:556-575.
• [22]Chen SL, Zhang YX, Xu MY: Molecular polymorphism and expression analysis of MHC class IIB gene from red sea bream (Chrysophrys major). Developmental and Comparative Immunology 2006, 30:407-418.
• [23]Prapansak S, Tsuyoshi O, Ikuo H: Cloning, characterization and expression of cDNA containing major histocompatibility complex classI, IIa and IIb genes of Japanese flounder Paralichthys olivaceus. Fisheries Science 2004, 70(2):264-276.
• [24]Hardee JJ, Godwin U, Benedetto R: Major histocompatibility complex classA gene polymorphism in the striped bass. Immunogenetics 1995, 41:229-238.
• [25]Walker RB, McConnell TJ, Walker RA: Polymorphism of the Mhc Mosa class IIb chain encoding gene in the striped bass (Morone saxatilis). Dev Comp Immunol 1994, 18(4):325-342.
• [26]Kasahara M, Vazquez M, Sato KEC: Evolution of the major histocompatibility complex: isolation of class II cDNA clones from the cartilaginous fish. Proc Natl Acad Sci USA 1990, 89:6688-6692.
• [27]Kasahara MEC, Mckinney MF, Flajnik : The evolution origion of the major histocompatibility complex:polymorphism of class II cDNA clones from the cartilaginous fish. Eur J Immunol 1993, 23:2160-2165.
• [28]Zhang YX, Chen SL: Molecular identification, polymorphism and expression analysis of major histocompatibility complex class II A and B genes of turbot (Scophthalmus maximus). Mar Biotechnol 2006, 8:611-623.
• [29]Sültmann H, Mayer WE, Mayer : Zebrafish MHC class IIα chain encoding genes:polymorphism, expression, and function. Immunogenetics 1993, 38:408-420.
• [30]Briles WE, Briles RW, Taffs RE, Stone HA: Resistance to a malignant lymphoma in chicken is mapped to subregion of major histocompatibility (B) complex. Science 1983, 219:977-979.
• [31]Paterson S, Wilson K, Pemberton JM: Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population. Proc Natl Acad Sci USA 1998, 95:3714-3719.
• [32]Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA: Common West African HLA antigens associated with protection from severe malaria. Nature 1991, 352:595-600.
• [33]Flores-Villanueva PO, Hendel H, Caillat-Zucman S, Rappaport J, Burgos-Tiburcio A, Bertin-Maghit S: Associations of MHC ancestral haplotypes with resistance/susceptibility to AIDS disease development. J Immunology 2003, 170:1925-1929.
• [34]Gjedrem T, Salte R, Gjoen HM: Genetic variation in susceptibility of Atlantic salmon to furunculosis. Aquaculture 1991, 97:1-6.
• [35]Lohm J, Grahn M, Langefors A, Andersen O, Storset A, von Schantz T: Experimental evidence for major histocompatity complex-allele-specific resistance to a bacterial infection. Proc Biol Sci 2002, 269:2029-2033.
• [36]Wynne JW, Cook MT, Nowak BF, Elliott NG: Major histocompatibility polymorphism associated with resistance towards amoebic gill disease in Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 2007, 22:707-717.
• [37]Glover KA, Grimholt U, Bakke HG, Nilsen F, Storset A, Skaala : Major histocompatibility complex (MHC) variation and susceptibility to the sea louse Lepeophtheirus salmonis in Atlantic salmon Salmo salar. Dis Aquat Organ 2007, 76:57-65.
• [38]Xu TJ, Chen SL, Ji XS, Tian YS: MHC polymorphism and disease resistance to Vibrio anguillarum in 12 selective Japanese flounder (Paralichthys olivaceus) families. Fish & Shellfish Immunology 2008, 25(3):213-221.
• [39]Chen SL, Tian YS, Yang JF, Shao CW, Ji XS, Zhai JM, Liao XL, Zhuang ZM, Su PZ, Xu JY, Sha ZX, Wu PF, Wang N: Artificial Gynogenesis and Sex Determination in Half-Smooth Tongue Sole (Cynoglossus semilaevis). Mar Biotechnol 2009, 11:243-251.
• [40]Xu Tj, Chen SL, Ji XS, Sha ZX: 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 Immunology 2009, 27(2):192-201.
• [41]Liu YG, Bao BL, Liu LX, Wang L, Lin H: Isolation and characterization of polymorphic microsatellite loci from RAPD product in half-smooth tongue sole(Cynoglossus semilaevis) and a test of cross-species amplification. Molecular Ecology Resources 2008, 8:202-204.
• [42]Tang XQ, Zhou L, Zhan WB: Isolation and Characterization of Pathogenic Listonella anguillarum of Diseased Half-Smooth Tongue Sole (Cynoglossus semilaevis Günther). J Ocean Univ Chin 2008, 7(3):343-351.
• [43]Zhang YX, Chen SL, Liu YG, Sha ZX, Liu ZJ: Major histocompatibilibility complex IIB allele polymorphism and its association with resistance/susceptibility to Vibrio anguillarum in Japanese Flounder (Paralichthys olivaceus). Mar Biotechnol 2006, 8:600-610.
• [44]Chen SL, Du M, Yang JF, Hu QM, Xu Y, Zhai JM: Development and characterization for growth rate and disease resistance of families in half-smooth tongue sole (Cynoglossus semilaevis). Journal of Fisheries of China 2010, 23(12):1789-1794.
• [45]Lei JL: Marine Fish Culture Theory and Techniques [M]. China Agriculture Press; 2004.
• [46]Chen SL, Li J, Deng SP, Tian YS, Wang QY, Zhuang ZM, Sha ZX, Xu JY: Isolation of Female-Specific AFLP Markers and MolecularIdentification of Genetic Sex in Half-Smooth Tongue Sole(Cynoglossus semilaevis). Marine Biotechnology 2007, 9:173-280.
• [47]Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986, 3:418-426.
• [48]Librado P, Rozas J: DnaSP v5:A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
• [49]Rice WR: Analysis tables of statistical tests. Evolution 1989, 43:223-225.
• [50]Davies CJ, Andersson L, Ellis SA, Hensen EJ, Lewin HA, Mikko S: Nomenclature for factors of the BoLA system, report of the ISAG BoLA Nomenclature Committee. Anim Genet 1997, 28:159-168.
• [51]Xu RF, Chen GH, Xu H, Qiang BZ, Li CC: Characterization of genetic polymorphism of novel MHCB-LBIIalleles in Chinese indigenous chickens. J Genet Genomics 2007, 34(2):109-118.
• [52]Xu RF, Li K, Chen GH, Qiang YZ, Zhang YB, Lin L: Genetic variation within exon 2 of the MHC B-LB II gene inTibetan chicken. Acta Genet Sin 2005, 32(11):1136-1146.
• [53]Li MH, Li K, Kantanen J, Feng Z, Fan B, Zhao SH: Allelic variations in exon2 of caprine MHC class II DRB3 gene in Chinese indigenous goats. Small Rumin Res 2006, 66:236-243.
• [54]Langefors Å, Lohm J, Grahn M, Andersen Ø, Schantz T: Association between major histocompatibility complex class II B alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond B 2000, 268:479-485.
• [55]Kim TJ, Parker KM, Hedrick PW: Major Histocompatibility Complex Differentiation in Sacramento River Chinook Salmon. Genetics 1999, 151:1115-1122.
• [56]Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG: Strominger JL. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 1993, 364:33-39.
• [57]Ottová E, Simkova A, Martin JF, Bellocq JG, Gelnar M, Allienne JF: Evolution and trans-species polymorphism Of MHC class IIb genes in cyprinid fish. Fish & Shellfish Immunol 2005, 18:199-222.
• [58]Hughes AL, Nei M: Nucleotide substitution at major histocompatibility complex class II loci:evidence for over-dominant selection. Proc Natl Acad Sci USA 1989, 86:958-962.
• [59]Stet RJM, Vries B, Mudde K, Hermsen T, Heerwaarden J, Shum BP: 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 2002, 54:320-331.
• [60]Doherty PC, Zinkernagel RM: Enhanced immunological surveillance in mice heterozygous at the H-2gene complex. Nature 1975, 256:50-52.
• [61]Takahata N, Nei M: Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 1990, 124:967-978.
• [62]Slade RW, McCallum HI: Overdominant vs frequency-dependent selection at MHC loci. Genetics 1992, 132:861-862.
• [63]Parham P, Ohta T: Population biology of antigen presentation by MHC class I molecules. Science 1996, 272:67-74.
• [64]Langefors Å, Lohm J, Grahn M, Andersen O, von Schantz T: Association between Mhc class II B alleles and resistance to Aeromonas salmonicida in Atlantic salmon. Proc R Soc Lond B 2001, 268:479-485.
• [65]Bacon LD: Influence of the major histocompatibility complex on disease resistance and productivity. Poultry Science 1987, 66:802-811.
• [66]Miller KM, Winton JR, Schulze AD, Purcell MK, Ming TJ: Major histocompatibility complex loci are associated with susceptibility of Atlantic salmon to infectious hematopoietic necrosis virus. Environ Biol Fishes 2004, 69:307-316.
• [67]Bengtsson BO, Thomson G: Measuring the strength of associations between HLA antigens and diseases. Tissue Antigens 1981, 18:356-363.
• [68]Kjøglum S, Grimholt U, Larsen S: Non-MHC genetic and tank effects influence disease challenge tests in Atlantic salmon (Salmo salar). Aquaculture 2005, 250:102-109.
• [69]Hedrick P, Kim T: Genetics of complex polymorphisms: parasites and maintenance of MHC variation. Edited by Singh R, Krimbas C. Genetics, Evolution & Society. Harvard University Press: Cambridge; 1998.