Resistance to a Malignant Lymphoma in Chickens Is Mapped to Subregion of Major Histocompatibility (
            <i>B</i>
            ) Complex

Briles, W. E.; Briles, R. W.; Taffs, RE; Stone, Howard A.

doi:10.1126/science.6823560

Cited by 155 publications

(93 citation statements)

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“…Antigen presenting molecules encoded by different BF2 alleles bind quite different classes of peptides (7-10) and thereby likely selectively influence adaptive immune responses to antigen, but the gene or genes that provide MHC-linked resistance to virally induced tumors in chickens are not known. Recently, the crossover breakpoint in the recombinant haplotype originally used to map MD resistance to the MHC-B subregion marked by BF2 was localized, which revealed that 27 genes lie within the region between the crossover breakpoint and the BF2 locus (4,11). Thus, it is now evident that many genes are candidates for providing the long noted MHC-B haplotype-linked resistance to MD.…”

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confidence: 99%

“…In the chicken, the MHC-B region has an exceptionally strong role in genetic resistance to Marek's disease (MD) caused by gallid herpesvirus-2 (GaHV-2) and to Rous sarcoma virus (RSV)-induced tumors (1,2). Resistance to these diseases maps to the MHC-B subregion marked by a highly expressed classical MHC class I gene (3)(4)(5)(6). It has been suggested that strong MHC-B disease associations are apparent as the result of alleles at this single locus for classical class I antigen presentation, BF2, contributing to immune responses either independently or in concert with closely-linked transporter associated with antigenprocessing (TAP) genes (6,7).…”

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BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

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Wang

Taylor

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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Pathogen selection is postulated to drive MHC allelic diversity at loci for antigen presentation. However, readily apparent MHC infectious disease associations are rare in most species. The strong link between MHC- B haplotype and the occurrence of virally induced tumors in the chicken provides a means for defining the relationship between pathogen selection and MHC polymorphism. Here, we verified a significant difference in resistance to gallid herpesvirus-2 (GaHV-2)-induced lymphomas (Marek's disease) conferred by two closely-related recombinant MHC- B haplotypes. We mapped the crossover breakpoints that distinguish these haplotypes to the highly polymorphic BG1 locus. BG1 encodes an Ig-superfamily type I transmembrane receptor-like protein that contains an immunoreceptor tyrosine-based inhibition motif (ITIM), which undergoes phosphorylation and is recognized by Src homology 2 domain-containing protein tyrosine phosphatase (SHP-2). The recombinant haplotypes are identical, except for differences within the BG1 3′-untranslated region (3′-UTR). The 3′-UTR of the BG1 allele associated with increased lymphoma contains a 225-bp insert of retroviral origin and showed greater inhibition of luciferase reporter gene translation compared to the other allele. These findings suggest that BG1 could affect the outcome of GaHV-2 infection through modulation of the lymphoid cell responsiveness to infection, a condition that is critical for GaHV-2 replication and in which the MHC- B haplotype has been previously implicated. This work provides a mechanism by which MHC- B region genetics contributes to the incidence of GaHV-2-induced malignant lymphoma in the chicken and invites consideration of the possibility that similar mechanisms might affect the incidence of lymphomas associated with other oncogenic viral infections.

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BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

Goto

Wang

Taylor

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…However, background genes (including non-immune system genes) appear to have an important role in MHC-dependent parasite resistance where a particular MHC haplotype may be associated with either resistance or susceptibility to a given pathogen depending on the genetic background of the host (Apanius et al 1997;Medina & North 1998). Hence, it is still a contentious issue to what extent the results from inbred laboratory strains can be extrapolated to outbred populations (Apanius et al 1997), where evidence is solely based on correlative data with no control for effects of non-MHC genes (Briles et al 1983;Hill et al 1991;Thursz et al 1997;Paterson et al 1998;Carrington et al 1999;Langefors et al 2001).…”

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Experimental evidence for major histocompatibility complex–allele–specific resistance to a bacterial infection

Lohm

Grahn

Langefors

et al. 2002

Proc. R. Soc. Lond. B

134

114

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The extreme polymorphism found at some major histocompatibility complex (MHC) loci is believed to be maintained by balancing selection caused by infectious pathogens. Experimental support for this is inconclusive. We have studied the interaction between certain MHC alleles and the bacterium Aeromonas salmonicida, which causes the severe disease furunculosis, in Atlantic salmon (Salmo salar L.). We designed full-sibling broods consisting of combinations of homozygote and heterozygote genotypes with respect to resistance or susceptibility alleles. The juveniles were experimentally infected with A. salmonicida and their individual survival was monitored. By comparing full siblings carrying different MHC genotypes the effects on survival due to other segregating genes were minimized. We show that a pathogen has the potential to cause very intense selection pressure on particular MHC alleles; the relative fitness difference between individuals carrying different MHC alleles was as high as 0.5. A co-dominant pattern of disease resistance/susceptibility was found, indicative of qualitative difference in the immune response between individuals carrying the high-and low-resistance alleles. Rather unexpectedly, survival was not higher among heterozygous individuals as compared with homozygous ones.

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“…T cells recognize and bind the Mhc-foreign antigen complex, thereby initiating a chain of events to stimulate the adaptive immune response to fight infection. It is now well appreciated that Mhc polymorphism plays a central role in resistance to infectious and autoimmune disease in birds and mammals (Briles et al 1983;Kaufman and Wallny 1996;Hill 1999). Soon after the proximate molecular functions of Mhc genes were elucidated, it was also recognized that, by nature of their role in self-nonself recognition and high polymorphism, Mhc genes could play a role in kin recognition and mate choice (Yamazaki et al 1976).…”

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An Mhc Component to Kin Recognition and Mate Choice in Birds: Predictions, Progress, and Prospects

Zelano

Edwards

2002

The American Naturalist

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The major histocompatibility complex (Mhc) has been identified as a locus influencing disease resistance, mate choice, and kin recognition in mammals and fish. However, it is unclear whether the mechanisms by which Mhc genes influence behavior in mammals are applicable to other nonmammalian vertebrates such as birds. We review the biology of Mhc genes with particular reference to their relevance to avian mating and social systems. New genomics approaches recently have been applied to the Mhcs of chickens, quail, and several icons of avian behavioral ecology, including red-winged blackbirds (Agelaius phoeniceus) and house finches (Carpodacus mexicanus). The predominance of concerted evolution at avian Mhc loci makes such methods attractive for providing access to this complicated multigene family. Although some biological processes influenced by Mhc in mammals are physiologically implausible for birds, Mhc could influence cues that form well-known bases for mate choice in birds by influencing the health and vigor of individuals. The tight associations of Mhc variation and disease resistance in chickens raise hope that finding associations of Mhc genes, disease, and mate choice in natural populations of birds will be as fruitful as in mammalian systems.

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Resistance to a Malignant Lymphoma in Chickens Is Mapped to Subregion of Major Histocompatibility ( B ) Complex

Cited by 155 publications

References 15 publications

BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken

Experimental evidence for major histocompatibility complex–allele–specific resistance to a bacterial infection

An Mhc Component to Kin Recognition and Mate Choice in Birds: Predictions, Progress, and Prospects

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