Abstract
The proteasome subunit beta type 8 gene (PSMB8) encodes one of the beta subunits of the immunoproteasome responsible for the generation of peptides presented by major histocompatibility complex class I molecules. Dimorphic alleles of the PSMB8 gene, termed A and F types, based on the deduced 31st amino acid residue of the mature protein have been reported from various vertebrates. Phylogenetic analysis revealed the presence of dichotomous ancient lineages, one comprising the F-type PSMB8 of basal ray-finned fishes, and the other comprising the A-type PSMB8 of these animals and both the F- and A-type PSMB8 of Xenopus and acanthopterygians, indicating that evolutionary history of the PSMB8 dimorphism was not straightforward. We analyzed the PSMB8 gene of five reptile and one amphibian species and found both the A and F types from all six. Phylogenetic analysis indicated that the PSMB8 F type was apparently regenerated from the PSMB8 A type at least five times independently during tetrapod evolution. Genomic typing of wild individuals of geckos and newts indicated that the frequencies of the A- and F-type alleles are not highly biased in these species. Phylogenetic analysis of each exon of the reptile PSMB8 gene suggested interallelic sequence homogenization as a possible evolutionary mechanism for the apparent recurrent regeneration of PSMB8 dimorphism in tetrapods. An extremely strong balancing selection acting on PSMB8 dimorphism was implicated in an unprecedented pattern of allele evolution.
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Agarwal AK, Xing C, DeMartino GN, Mizrachi D, Hernandez MD, Sousa AB, Martinez de Villarreal L, dos Santos HG, Garg A (2010) PSMB8 encoding the β5i proteasome subunit is mutated in joint contractures, muscle atrophy, microcytic anemia, and panniculitis-induced lipodystrophy syndrome. Am J Hum Genet 87:866–872
Akiyama K, Yokota K, Kagawa S, Shimbara N, Tamura T, Akioka H, Nothwang HG, Noda C, Tanaka K, Ichihara A (1994) cDNA cloning and interferon gamma down-regulation of proteasomal subunits X and Y. Science 265:1231–1234
Arima K, Kinoshita A, Mishima H et al (2011) Proteasome assembly defect due to a proteasome subunit beta type 8 (PSMB8) mutation causes the autoinflammatory disorder, Nakajo-Nishimura syndrome. Proc Natl Acad Sci U S A 108:14914–14919
Dalloul RA, Long JA, Zimin AV et al (2010) Multiplatform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis. PLoS Biol 8:e1000475
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Fehling HJ, Swat W, Laplace C, Kühn R, Rajewsky K, Müller U, von Boehmer H (1994) MHC class I expression in mice lacking the proteasome subunit LMP-7. Science 265:1234–1237
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Früh K, Gossen M, Wang K, Bujard H, Peterson PA, Yang Y (1994) Displacement of housekeeping proteasome subunits by MHC encoded LMPs: a newly discovered mechanism for modulating the multicatalytic proteinase complex. EMBO J 13:3236–3244
Fujito NT, Nonaka M (2012) Highly divergent dimorphic alleles of the proteasome subunit beta type-8 (PSMB8) gene of the bichir Polypterus senegalus: implication for evolution of the PSMB8 gene of jawed vertebrates. Immunogenetics 64:447–453
Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386:463–471
Hillier LW, Miller W, Birney E et al (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716
Kasahara M (1997) New insights into the genomic organization and origin of the major histocompatibility complex: role of chromosomal (genome) duplication in the emergence of the adaptive immune system. Hereditas 127:59–65
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kitamura A, Maekawa Y, Uehara H et al (2011) A mutation in the immunoproteasome subunit PSMB8 causes autoinflammation and lipodystrophy in humans. J Clin Invest 121:4150–4160
Miura F, Tsukamoto K, Mehta RB, Naruse K, Magtoon W, Nonaka M (2010) Transspecies dimorphic allelic lineages of the proteasome subunit beta-type 8 gene (PSMB8) in the teleost genus Oryzias. Proc Natl Acad Sci U S A 107:21599–21604
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, Oxford
Nonaka M, Yamada-Namikawa C, Flajnik MF, Du Pasquier L (2000) Trans-species polymorphism of the major histocompatibility complex-encoded proteasome subunit LMP7 in an amphibian genus, Xenopus. Immunogenetics 51:186–192
Ohta Y, McKinney EC, Criscitiello MF, Flajnik MF (2002) Proteasome, transporter associated with antigen processing, and class I genes in the nurse shark Ginglymostoma cirratum: evidence for a stable class I region and MHC haplotype lineages. J Immunol 168:771–781
Ohta Y, Powis SJ, Lohr RL, Nonaka M, Du Pasquier L, Flajnik MF (2003) Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co-evolution among MHC class I region genes. Eur J Immunol 33:3017–3027
Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shen XX, Liang D, Wen JZ, Zhang P (2011) Multiple genome alignments facilitate development of NPCL markers: a case study of tetrapod phylogeny focusing on the position of turtles. Mol Biol Evol 28:3237–3252
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tanaka K, Kasahara M (1998) The MHC class I ligand-generating system: roles of immunoproteasomes and the interferon-gamma-inducible proteasome activator PA28. Immunol Rev 163:161–176
Tsukamoto K, Hayashi S, Matsuo MY, Nonaka MI, Kondo M, Shima A, Asakawa S, Shimizu N, Nonaka M (2005) Unprecedented intraspecific diversity of the MHC class I region of a teleost medaka, Oryzias latipes. Immunogenetics 57:420–431
Tsukamoto K, Miura F, Fujito NT, Yoshizaki G, Nonaka M (2012) Long-lived dichotomous lineages of the proteasome subunit beta type 8 (PSMB8) gene surviving more than 500 million years as alleles or paralogs. Mol Biol Evol 29:3071–3079
Unno M, Mizushima T, Morimoto Y, Tomisugi Y, Tanaka K, Yasuoka N, Tsukihara T (2002) The structure of the mammalian 20S proteasome at 2.75 A resolution. Structure 10:609–618
Warren WC, Clayton DF, Ellegren H et al (2010) The genome of a songbird. Nature 464:757–762
Acknowledgements
We thank Drs. M. Asashima and Y. Ito for supplying us with newt samples. We also thank Dr. M. Taira for supplying us with Xenopus tropicalis genomic DNA samples. This work was supported in part by a Grant-in-Aid for Scientific Research (B), MEXT, Japan (to M.N.).
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Huang, CH., Tanaka, Y., Fujito, N.T. et al. Dimorphisms of the proteasome subunit beta type 8 gene (PSMB8) of ectothermic tetrapods originated in multiple independent evolutionary events. Immunogenetics 65, 811–821 (2013). https://doi.org/10.1007/s00251-013-0729-2
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DOI: https://doi.org/10.1007/s00251-013-0729-2