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Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family

The evolutionary mode of a multi-gene family can change over time, depending on the functional differentiation and local genomic environment of family members. In this study, we demonstrate such a change in the melanoma antigen (MAGE) gene family on the mammalian X chromosome. The MAGE gene family i...

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Autores principales: Katsura, Yukako, Satta, Yoko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3112145/
https://www.ncbi.nlm.nih.gov/pubmed/21695252
http://dx.doi.org/10.1371/journal.pone.0020365
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author Katsura, Yukako
Satta, Yoko
author_facet Katsura, Yukako
Satta, Yoko
author_sort Katsura, Yukako
collection PubMed
description The evolutionary mode of a multi-gene family can change over time, depending on the functional differentiation and local genomic environment of family members. In this study, we demonstrate such a change in the melanoma antigen (MAGE) gene family on the mammalian X chromosome. The MAGE gene family is composed of ten subfamilies that can be categorized into two types. Type I genes are of relatively recent origin, and they encode epitopes for human leukocyte antigen (HLA) in cancer cells. Type II genes are relatively ancient and some of their products are known to be involved in apoptosis or cell proliferation. The evolutionary history of the MAGE gene family can be divided into four phases. In phase I, a single-copy state of an ancestral gene and the evolutionarily conserved mode had lasted until the emergence of eutherian mammals. In phase II, eight subfamily ancestors, with the exception for MAGE-C and MAGE-D subfamilies, were formed via retrotransposition independently. This would coincide with a transposition burst of LINE elements at the eutherian radiation. However, MAGE-C was generated by gene duplication of MAGE-A. Phase III is characterized by extensive gene duplication within each subfamily and in particular the formation of palindromes in the MAGE-A subfamily, which occurred in an ancestor of the Catarrhini. Phase IV is characterized by the decay of a palindrome in most Catarrhini, with the exception of humans. Although the palindrome is truncated by frequent deletions in apes and Old World monkeys, it is retained in humans. Here, we argue that this human-specific retention stems from negative selection acting on MAGE-A genes encoding epitopes of cancer cells, which preserves their ability to bind to highly divergent HLA molecules. These findings are interpreted with consideration of the biological factors shaping recent human MAGE-A genes.
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spelling pubmed-31121452011-06-21 Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family Katsura, Yukako Satta, Yoko PLoS One Research Article The evolutionary mode of a multi-gene family can change over time, depending on the functional differentiation and local genomic environment of family members. In this study, we demonstrate such a change in the melanoma antigen (MAGE) gene family on the mammalian X chromosome. The MAGE gene family is composed of ten subfamilies that can be categorized into two types. Type I genes are of relatively recent origin, and they encode epitopes for human leukocyte antigen (HLA) in cancer cells. Type II genes are relatively ancient and some of their products are known to be involved in apoptosis or cell proliferation. The evolutionary history of the MAGE gene family can be divided into four phases. In phase I, a single-copy state of an ancestral gene and the evolutionarily conserved mode had lasted until the emergence of eutherian mammals. In phase II, eight subfamily ancestors, with the exception for MAGE-C and MAGE-D subfamilies, were formed via retrotransposition independently. This would coincide with a transposition burst of LINE elements at the eutherian radiation. However, MAGE-C was generated by gene duplication of MAGE-A. Phase III is characterized by extensive gene duplication within each subfamily and in particular the formation of palindromes in the MAGE-A subfamily, which occurred in an ancestor of the Catarrhini. Phase IV is characterized by the decay of a palindrome in most Catarrhini, with the exception of humans. Although the palindrome is truncated by frequent deletions in apes and Old World monkeys, it is retained in humans. Here, we argue that this human-specific retention stems from negative selection acting on MAGE-A genes encoding epitopes of cancer cells, which preserves their ability to bind to highly divergent HLA molecules. These findings are interpreted with consideration of the biological factors shaping recent human MAGE-A genes. Public Library of Science 2011-06-10 /pmc/articles/PMC3112145/ /pubmed/21695252 http://dx.doi.org/10.1371/journal.pone.0020365 Text en Katsura, Satta. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Katsura, Yukako
Satta, Yoko
Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family
title Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family
title_full Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family
title_fullStr Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family
title_full_unstemmed Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family
title_short Evolutionary History of the Cancer Immunity Antigen MAGE Gene Family
title_sort evolutionary history of the cancer immunity antigen mage gene family
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3112145/
https://www.ncbi.nlm.nih.gov/pubmed/21695252
http://dx.doi.org/10.1371/journal.pone.0020365
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