Abstract
Major histocompatibility complex (MHC) class II molecules play an important role in the immune response of vertebrates. In this paper, full-length MHC IIA cDNA was isolated from swamp eel (Monopterus albus) by rapid amplification of cDNA ends PCR. The genomic structure, molecular polymorphism, tissue distribution, and immune response of the MHC IIA gene to bacterial challenge were investigated. The full-length cDNA (GenBank accession No.: KC616308) is 1,509 bp in length including an 83 bp-long 5′ untranslated region (UTR) and a 709 bp-long 3′ UTR, which encoded a 238 amino acids protein. In the 2,339 bp-long MHC IIA genomic DNA, four exons and three introns were identified. Sequence comparison exhibited that the deduced amino acid sequence shared 27.1–66.3% identity with those of other species. Seven alleles were identified from five healthy individuals. Number of alleles per individual diversified from two to five. Five different 5′ UTR sequences and two different 3′ UTR sequences from one individual may infer the existence of five loci at least. Real-time quantitative PCR demonstrated that swamp eel MHC IIA transcripts were ubiquitously expressed in ten tissues, but the expression level was distinctly different. Significant changes were observed in liver, spleen, kidney and intestine after challenged with pathogenic bacteria Aeromonas hydrophilia.
Key words: swamp eel, Monopterus albus, MHC IIA, gene cloning and expression
Abbreviations
- MHC
major histocompatibility complex
- RACE
rapid amplification of cDNA ends
- UTR
untranslated region
References
- Banat GR, Tkalcic S, Dzielawa JA, Jackwood MW, Saggese MD, Yates L, Kopulos R, Briles WE, Collisson EW. Association of the chicken MHC B haplotypes with resistance to avian coronavirus. Dev. Comp. Immunol. 2013;39:430–437. doi: 10.1016/j.dci.2012.10.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Briles WE, Briles RW, Taffs RE, Stone HA. Resistance to a malignant lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex. Science. 1983;219:977–979. doi: 10.1126/science.6823560. [DOI] [PubMed] [Google Scholar]
- Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. Three-dimensional structure of the human class II histocompatibility antigen HLADR1. Nature. 1993;364:33–39. doi: 10.1038/364033a0. [DOI] [PubMed] [Google Scholar]
- Chen HQ, Lu CP. Study on pathogen of bacterial hemorrhagic septicemia of rice eel (Monopterus albus) Chinese Journal of Zoonoses. 1991;7:21–23. [Google Scholar]
- Chen SL, Zhang YX, Xu MY, Ji XS, Yu GC, Dong CF. Molecular polymorphism and expression analysis of MHC class II B gene from red sea bream (Chrysophrys major) Dev. Comp. Immunol. 2006;30:407–418. doi: 10.1016/j.dci.2005.06.001. [DOI] [PubMed] [Google Scholar]
- Cosson P, Bonifacino JS. Role of transmembrane domain interactions in the assembly of class II MHC molecules. Science. 1992;258:659–662. doi: 10.1126/science.1329208. [DOI] [PubMed] [Google Scholar]
- Croisetiere S, Tarte PD, Bernatchez L, Belthumeur P. Identification of MHC class II β resistance/susceptibility alleles to Aernmonas salmonicida in brook charr (Salvelinus fontinalis) Mol. Immunol. 2008;45:3107–3116. doi: 10.1016/j.molimm.2008.03.007. [DOI] [PubMed] [Google Scholar]
- Du M, Chen SL, Liu YH, Liu Y, Yang JF. MHC polymorphism and disease resistance to Vibrio anguillarum in 8 families of half-smooth tongue sole (Cynoglossus semilaevis) BMC Genetics. 2011;12:78. doi: 10.1186/1471-2156-12-78. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans JJ, Klesius PH, Pasnik DJ, Bohnsack JF. Human Streptococcus agalactiae isolate in Nile tilapia (Oreochromis niloticus) Emerg. Infect. Dis. 2009;15:774–776. doi: 10.3201/eid1505.080222. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Godwin UB, Antao A, Wilson MR, Chinchar VG, Miller NW, Clem LW, McConnell TJ. MHC class II B genes in the channel catfish (Ictalurus punctatus) Dev. Comp. Immunol. 1997;21:13–23. doi: 10.1016/S0145-305X(97)00003-7. [DOI] [PubMed] [Google Scholar]
- Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset A, Saeb S, Stet RJM. 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. doi: 10.1007/s00251-003-0567-8. [DOI] [PubMed] [Google Scholar]
- Hashimoto K, Nakanishi T, Kurosawa Y. Isolation of carp genes encoding major histocompatibility complex antigens. Proc. Natl. Acad. Sci. USA. 1990;87:6863–6867. doi: 10.1073/pnas.87.17.6863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill AVS, Allsopp CEM, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Berwster D, Mcmichael AJ, Greenwood BM. Comman West African HLA antigens associated with protection from severe malaria. Nature. 1991;352:595–600. doi: 10.1038/352595a0. [DOI] [PubMed] [Google Scholar]
- Hu M, Wang N, Pan ZH, Lu CP. Identity and virulence properties of Aeromonas isolates from diseased fish, healthy controls and water environment in China. Lett. Appl. Microbiol. 2012;55:224–233. doi: 10.1111/j.1472-765X.2012.03281.x. [DOI] [PubMed] [Google Scholar]
- Kennedy L, Ryvar R, Gaskell R, Addie D, Willoughby K, Carter S, Thomson W, Ollier W, Radford A. Sequence analysis of MHC DRB alleles in domestic cats from the United Kingdom. Immunogenetics. 2002;54:348–352. doi: 10.1007/s00251-002-0465-5. [DOI] [PubMed] [Google Scholar]
- Kjoeglum S, Larsen S, Bakke HG, Grimholt U. How specific MHC class I and class II combinations affect disease resistance against infectious salmon anaemia in Atlantic salmon (Salmo salar) Fish Shellfish Immunol. 2006;21:431–441. doi: 10.1016/j.fsi.2006.02.001. [DOI] [PubMed] [Google Scholar]
- Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI. Nomenclature for themajor histocompatibility complexes of different species, a proposal. Immunogenetics. 1990;31:217–219. doi: 10.1007/BF00204890. [DOI] [PubMed] [Google Scholar]
- Koppang EO, Dannevig BH, Lie O, Ronningen K, Press CM. Expression of MHC class I and II mRNA in a macrophage-like cell line (SHK-1) derived from Atlantic salmon, Salmo salar, head kidney. Fish Shellfish Immunol. 1999;9:473–489. doi: 10.1006/fsim.1999.0213. [DOI] [Google Scholar]
- Li HJ, Jiang LX, Han JB, Su H, Yang Q, He CB. Major histocompatibility complex class IIA and IIB genes of the spotted halibut Verasper variegatus, genomic structure, molecular polymorphism, and expression analysis. Fish Physiol. Biochem. 2011;37:167–180. doi: 10.1007/s10695-011-9476-1. [DOI] [PubMed] [Google Scholar]
- Málaga-Trillo E, Zaleska-Rutczynska Z, McAndrew B, Vincek V, Figueroa F, Sültmann H, Klein J. Linkage relationships and haplotype polymorphism among cichlid MHC class II B loci. Genetics. 1998;149:1527–1537. doi: 10.1093/genetics/149.3.1527. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Medina E, North RJ. Resistance ranking of some common inbred mouse strains to Mycobacterium tuberbulosis and relationship to major histocompatibility complex haplotype and Nramp1 genotype. Immunology. 1998;93:270–274. doi: 10.1046/j.1365-2567.1998.00419.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nikolich-Zugich J, Fremont DH, Miley MJ, Messaoudi I. The role of MHC polymorphism in anti-microbial resistance. Microbes Infection. 2004;6:501–512. doi: 10.1016/j.micinf.2004.01.006. [DOI] [PubMed] [Google Scholar]
- Pang J, Gao F, Lu M, Ye X, Zhu H, Ke X. Major histocompatibility complex class IIA and IIB genes of Nile tilapia Oreochromis niloticus, genomic structure, molecular polymorphism and expression patterns. Fish Shellfish Immunol. 2013;34:486–496. doi: 10.1016/j.fsi.2012.11.048. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1073/pnas.95.7.3714. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Piertney SB, Oliver MK. The evolutionary ecology of the major histocompatibility complex. Heredity. 2006;96:7–21. doi: 10.1038/sj.hdy.6800724. [DOI] [PubMed] [Google Scholar]
- Rakus KL, Wiegertjes GF, Jurecka P, Walker PD, Pilarczyk A, Irnazarow I. Major histocompatibility (MH) class II B gene polymorphism influences disease resistance of common carp (Cyprinus carpio L. Aquaculture. 2009;288:44–50. doi: 10.1016/j.aquaculture.2008.11.016. [DOI] [Google Scholar]
- Ristow SS, Grabowski LD, Thompson SM, Warr GW, Kaattari SL, de Avila JM, Thorgaard GH. Coding sequences of the MHC II β chain of homozygous rainbow trout (Oncorhynchus mykiss) Dev. Comp. Immunol. 1999;23:51–60. doi: 10.1016/S0145-305X(98)00039-1. [DOI] [PubMed] [Google Scholar]
- Rodrigues PN, Hermsen TT, Rombout JH, Egberts E, Stet RJ. Detection of MHC class II transcripts in lymphoid tissues of the common carp (Cyprinus carpio L.) Dev. Comp. Immunol. 1995;19:483–496. doi: 10.1016/0145-305X(95)00033-P. [DOI] [PubMed] [Google Scholar]
- Rothbard J, Gefter M. Interactions between immunogenetic peptides and MHC proteins. Annu. Rev. Immunol. 1991;9:527–565. doi: 10.1146/annurev.iy.09.040191.002523. [DOI] [PubMed] [Google Scholar]
- Saitou N, Nei M. The neighbor-joining method, a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987;4:406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
- Sato A, Figueroa F, Murray BW, Malaga-Trillo E, Zaleska-Rutczynska Z, Sultmann H, Toyosawa S, Wedekind C, Steck N, Klein J. Nolinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics. 2000;51:108–116. doi: 10.1007/s002510050019. [DOI] [PubMed] [Google Scholar]
- Shen T, Xu S, Yang M, Pang S, Yang G. Molecular cloning, expression pattern, and 3D structural analysis of the MHC class IIB gene in the Chinese longsnout catfish (Leiocassis longirostris) Veter. Immunol. Immunopathol. 2011;141:33–45. doi: 10.1016/j.vetimm.2011.02.002. [DOI] [PubMed] [Google Scholar]
- Sommer S. The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front. Zool. 2005;2:16–34. doi: 10.1186/1742-9994-2-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Srisapoome P, Ohira T, Hirono I, Aoki T. Cloning, characterization and expression of cDNA containing major histocompatibility complex class II α and II β genes of Japanese flounder Paralichtys olivaceus. Fish. Sci. 2004;70:264–276. doi: 10.1111/j.1444-2906.2003.00800.x. [DOI] [Google Scholar]
- Sültmann H, Mayer WE, Figueroa F, O’Huigin C, Klein J. Organization of MHC class IIB genes in the zebrafish (Brachydanio rerio) Genomics. 1994;23:1–14. doi: 10.1006/geno.1994.1452. [DOI] [PubMed] [Google Scholar]
- Tamura K, Dudley J, Nei M, Kumar S. MEGA4, Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007;224:1596–1599. doi: 10.1093/molbev/msm092. [DOI] [PubMed] [Google Scholar]
- Tang J, Zhou C, Zhang ZJ, Zheng SS. Association of polymorphisms in non-classic MHC genes with susceptibility to autoimmune hepatitis. Hepatobiliary Pancreat. Dis. Int. 2012;11:125–131. doi: 10.1016/S1499-3872(12)60136-2. [DOI] [PubMed] [Google Scholar]
- 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. doi: 10.1016/j.fsi.2006.08.019. [DOI] [PubMed] [Google Scholar]
- Xu Q, Yang D, Tuo R, Wan J, Yuan H, Li P, Jiang T. Cloning and comparative expression of IRF4 and IRF10 in the Asian swamp eel (Monopterus albus) Fish Shellfish Immunol. 2013;34:1748. doi: 10.1016/j.fsi.2013.03.343. [DOI] [Google Scholar]
- 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 Shell-fish Immunol. 2009;27:192–201. doi: 10.1016/j.fsi.2009.04.009. [DOI] [PubMed] [Google Scholar]
- Xu TJ, Sun YN, Shi G, Cheng YZ, Wang RX. Characterization of the major histocompatibility complex class II genes in miiuy croaker. PLoS One. 2011;6:e23823. doi: 10.1371/journal.pone.0023823. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu SH, Ao JQ, Chen XH. Molecular characterization and expression analysis of MHC class II α and β genes in large yellow croaker (Pseudosciaena crocea) Mol. Biol. Rep. 2010;37:1295–1307. doi: 10.1007/s11033-009-9504-8. [DOI] [PubMed] [Google Scholar]
- Zhang YX, Chen SL. Molecular identification, polymorphism, and expression analysis of major histocompatibility complex class IIA and B genes of turbot (Scophthalmus maximus) Marine Biotechnol. 2006;8:611–623. doi: 10.1007/s10126-005-6174-y. [DOI] [PubMed] [Google Scholar]
- Zhang YX, Chen SL, Liu YG, Sha ZX, Liu ZJ. Major histocompatibility complex class IIB allele polymorphismand its association with resistance/susceptibility to Vibrio anguillarum in Japanese flounder (Paralichthys olivaceus) Marine Biotechnol. 2006;8:600–610. doi: 10.1007/s10126-005-6185-8. [DOI] [PubMed] [Google Scholar]
- Zhou F, Dong Z, Fu Y, Li T, Zeng Y, Ji X, Chen W, Zhang J, Wang H. Molecular cloning, genomic structure, polymorphism and expression analysis of major histocompatibility complex class II B gene of Nile tilapia (Oreochromis niloticus) Aquaculture. 2013;372-375:149–157. doi: 10.1016/j.aquaculture.2012.10.032. [DOI] [Google Scholar]
- Zhou R, Cheng H, Zhang Q, Guo Y, Richard RC, Terrence RT. SRY-related genes in the genome of the rice field eel (Monopterus albus) Genet. Sel. Evol. 2002;34:129–137. doi: 10.1186/1297-9686-34-1-129. [DOI] [PMC free article] [PubMed] [Google Scholar]
