The Salmonid MHC Class I: More Ancient Loci Uncovered

Overview

Journal Immunogenetics

Specialties Allergy & Immunology
Genetics

Date 2006 Jun 24

PMID 16794819

Citations 19

Authors

Kristina M Miller

Shaorong Li

Tobi J Ming

Karia H Kaukinen

Angela D Schulze

Affiliations

Soon will be listed here.

Abstract

An unprecedented level of sequence diversity has been maintained in the salmonid major histocompatibility complex (MHC) class I UBA gene, with between lineage AA sequence identities as low as 34%. The derivation of deep allelic lineages may have occurred through interlocus exon shuffling or convergence of ancient loci with the UBA locus, but until recently, no such ancient loci were uncovered. Herein, we document the existence of eight additional MHC class I loci in salmon (UCA, UDA, UEA, UFA, UGA, UHA, ULA, and ZE), six of which share exon 2 and 3 lineages with UBA, and three of which have not been described elsewhere. Half of the UBA exon 2 lineages and all UBA exon 3 lineages are shared with other loci. Two loci, UGA and UEA, share only a single exon lineage with UBA, likely generated through exon shuffling. Based on sequence homologies, we hypothesize that most exchanges and duplications occurred before or during tetraploidization (50 to 100 Ma). Novel loci that share no relationship with other salmonid loci are also identified (UHA and ZE). Each locus is evaluated for its potential to function as a class Ia gene based on gene expression, conserved residues and polymorphism. UBA is the only locus that can indisputably be classified as a class Ia gene, although three of the eight loci (ZE, UCA, and ULA) conform in three out of four measures. We hypothesize that these additional loci are in varying states of degradation to class Ib genes.

Citing Articles

MHC class I evolution; from Northern pike to salmonids.

Grimholt U, Lukacs M BMC Ecol Evol. 2021; 21(1):3.

PMID: 33514321 PMC: 7853315. DOI: 10.1186/s12862-020-01736-y.

Major Histocompatibility Complex (MHC) Genes and Disease Resistance in Fish.

Yamaguchi T, Dijkstra J Cells. 2019; 8(4).

PMID: 31027287 PMC: 6523485. DOI: 10.3390/cells8040378.

Major histocompatibility complex (MHC) fragment numbers alone - in Atlantic cod and in general - do not represent functional variability.

Dijkstra J, Grimholt U F1000Res. 2018; 7:963.

PMID: 30135730 PMC: 6081975. DOI: 10.12688/f1000research.15386.2.

Small-scale intraspecific patterns of adaptive immunogenetic polymorphisms and neutral variation in Lake Superior lake trout.

Baillie S, Hemstock R, Muir A, Krueger C, Bentzen P Immunogenetics. 2017; 70(1):53-66.

PMID: 28547520 DOI: 10.1007/s00251-017-0996-4.

EGAR, A Food Protein-Derived Tetrapeptide, Reduces Seizure Activity in Pentylenetetrazole-Induced Epilepsy Models Through α-Amino-3-Hydroxy-5-Methyl-4-Isoxazole Propionate Receptors.

Cai S, Ling C, Lu J, Duan S, Wang Y, Zhu H Neurotherapeutics. 2016; 14(1):212-226.

PMID: 27783277 PMC: 5233631. DOI: 10.1007/s13311-016-0489-4.

References

Stet R, Kruiswijk C, Dixon B . Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol. 2004; 23(5-6):441-71. DOI: 10.1615/critrevimmunol.v23.i56.50. View

Phillips R, Zimmerman A, Noakes M, Palti Y, Morasch M, Eiben L . Physical and genetic mapping of the rainbow trout major histocompatibility regions: evidence for duplication of the class I region. Immunogenetics. 2003; 55(8):561-9. DOI: 10.1007/s00251-003-0615-4. View

Shiina T, Dijkstra J, Shimizu S, Watanabe A, Yanagiya K, Kiryu I . Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics. 2005; 56(12):878-93. DOI: 10.1007/s00251-004-0755-1. View

Aoyagi K, Dijkstra J, Xia C, Denda I, Ototake M, Hashimoto K . Classical MHC class I genes composed of highly divergent sequence lineages share a single locus in rainbow trout (Oncorhynchus mykiss). J Immunol. 2001; 168(1):260-73. DOI: 10.4049/jimmunol.168.1.260. View

Kaufman J, Salomonsen J, Flajnik M . Evolutionary conservation of MHC class I and class II molecules--different yet the same. Semin Immunol. 1994; 6(6):411-24. DOI: 10.1006/smim.1994.1050. View

Kiryu I, Dijkstra J, Sarder R, Fujiwara A, Yoshiura Y, Ototake M . New MHC class Ia domain lineages in rainbow trout (Oncorhynchus mykiss) which are shared with other fish species. Fish Shellfish Immunol. 2004; 18(3):243-54. DOI: 10.1016/j.fsi.2004.07.007. View

Shum B, Rajalingam R, Magor K, Azumi K, Carr W, Dixon B . A divergent non-classical class I gene conserved in salmonids. Immunogenetics. 1999; 49(6):479-90. DOI: 10.1007/s002510050524. View

Bjorkman P, Saper M, Samraoui B, Bennett W, Strominger J, Wiley D . The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature. 1987; 329(6139):512-8. DOI: 10.1038/329512a0. View

Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D . The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1998; 25(24):4876-82. PMC: 147148. DOI: 10.1093/nar/25.24.4876. View

10.

Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset 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(4):210-9. DOI: 10.1007/s00251-003-0567-8. View

11.

Shum B, Guethlein L, Flodin L, Adkison M, Hedrick R, Nehring R . Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol. 2001; 166(5):3297-308. DOI: 10.4049/jimmunol.166.5.3297. View

12.

Persson A, Stet R, Pilstrom L . Characterization of MHC class I and beta(2)-microglobulin sequences in Atlantic cod reveals an unusually high number of expressed class I genes. Immunogenetics. 1999; 50(1-2):49-59. DOI: 10.1007/s002510050685. View

13.

Myers R, Fischer S, LERMAN L, Maniatis T . Nearly all single base substitutions in DNA fragments joined to a GC-clamp can be detected by denaturing gradient gel electrophoresis. Nucleic Acids Res. 1985; 13(9):3131-45. PMC: 341225. DOI: 10.1093/nar/13.9.3131. View

14.

Bjorkman P, Parham P . Structure, function, and diversity of class I major histocompatibility complex molecules. Annu Rev Biochem. 1990; 59:253-88. DOI: 10.1146/annurev.bi.59.070190.001345. View

15.

Saper M, Bjorkman P, Wiley D . Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J Mol Biol. 1991; 219(2):277-319. DOI: 10.1016/0022-2836(91)90567-p. View

16.

Young W, Wheeler P, Fields R, Thorgaard G . DNA fingerprinting confirms isogenicity of androgenetically derived rainbow trout lines. J Hered. 1996; 87(1):77-80. DOI: 10.1093/oxfordjournals.jhered.a022960. View

17.

Miller K, Kaukinen K, Schulze A . Expansion and contraction of major histocompatibility complex genes: a teleostean example. Immunogenetics. 2002; 53(10-11):941-63. DOI: 10.1007/s00251-001-0398-4. View

18.

Miller K, Kaukinen K, Beacham T, Withler R . Geographic heterogeneity in natural selection on an MHC locus in sockeye salmon. Genetica. 2002; 111(1-3):237-57. DOI: 10.1023/a:1013716020351. View

19.

Consuegra S, Megens H, Schaschl H, Leon K, Stet R, Jordan W . Rapid evolution of the MH class I locus results in different allelic compositions in recently diverged populations of Atlantic salmon. Mol Biol Evol. 2005; 22(4):1095-106. DOI: 10.1093/molbev/msi096. View

20.

Klein J . Of HLA, tryps, and selection: an essay on coevolution of MHC and parasites. Hum Immunol. 1991; 30(4):247-58. DOI: 10.1016/0198-8859(91)90003-r. View