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Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes

The evolution of amniotes has involved major molecular innovations in the epidermis. In particular, distinct structural proteins that undergo covalent cross-linking during cornification of keratinocytes facilitate the formation of mechanically resilient superficial cell layers and help to limit wate...

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Autores principales: Strasser, Bettina, Mlitz, Veronika, Hermann, Marcela, Rice, Robert H., Eigenheer, Richard A., Alibardi, Lorenzo, Tschachler, Erwin, Eckhart, Leopold
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4245816/
https://www.ncbi.nlm.nih.gov/pubmed/25169930
http://dx.doi.org/10.1093/molbev/msu251
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author Strasser, Bettina
Mlitz, Veronika
Hermann, Marcela
Rice, Robert H.
Eigenheer, Richard A.
Alibardi, Lorenzo
Tschachler, Erwin
Eckhart, Leopold
author_facet Strasser, Bettina
Mlitz, Veronika
Hermann, Marcela
Rice, Robert H.
Eigenheer, Richard A.
Alibardi, Lorenzo
Tschachler, Erwin
Eckhart, Leopold
author_sort Strasser, Bettina
collection PubMed
description The evolution of amniotes has involved major molecular innovations in the epidermis. In particular, distinct structural proteins that undergo covalent cross-linking during cornification of keratinocytes facilitate the formation of mechanically resilient superficial cell layers and help to limit water loss to the environment. Special modes of cornification generate amniote-specific skin appendages such as claws, feathers, and hair. In mammals, many protein substrates of cornification are encoded by a cluster of genes, termed the epidermal differentiation complex (EDC). To provide a basis for hypotheses about the evolution of cornification proteins, we screened for homologs of the EDC in non-mammalian vertebrates. By comparative genomics, de novo gene prediction and gene expression analyses, we show that, in contrast to fish and amphibians, the chicken and the green anole lizard have EDC homologs comprising genes that are specifically expressed in the epidermis and in skin appendages. Our data suggest that an important component of the cornified protein envelope of mammalian keratinocytes, that is, loricrin, has originated in a common ancestor of modern amniotes, perhaps during the acquisition of a fully terrestrial lifestyle. Moreover, we provide evidence that the sauropsid-specific beta-keratins have evolved as a subclass of EDC genes. Based on the comprehensive characterization of the arrangement, exon–intron structures and conserved sequence elements of EDC genes, we propose new scenarios for the evolutionary origin of epidermal barrier proteins via fusion of neighboring S100A and peptidoglycan recognition protein genes, subsequent loss of exons and highly divergent sequence evolution.
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spelling pubmed-42458162014-12-01 Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes Strasser, Bettina Mlitz, Veronika Hermann, Marcela Rice, Robert H. Eigenheer, Richard A. Alibardi, Lorenzo Tschachler, Erwin Eckhart, Leopold Mol Biol Evol Discoveries The evolution of amniotes has involved major molecular innovations in the epidermis. In particular, distinct structural proteins that undergo covalent cross-linking during cornification of keratinocytes facilitate the formation of mechanically resilient superficial cell layers and help to limit water loss to the environment. Special modes of cornification generate amniote-specific skin appendages such as claws, feathers, and hair. In mammals, many protein substrates of cornification are encoded by a cluster of genes, termed the epidermal differentiation complex (EDC). To provide a basis for hypotheses about the evolution of cornification proteins, we screened for homologs of the EDC in non-mammalian vertebrates. By comparative genomics, de novo gene prediction and gene expression analyses, we show that, in contrast to fish and amphibians, the chicken and the green anole lizard have EDC homologs comprising genes that are specifically expressed in the epidermis and in skin appendages. Our data suggest that an important component of the cornified protein envelope of mammalian keratinocytes, that is, loricrin, has originated in a common ancestor of modern amniotes, perhaps during the acquisition of a fully terrestrial lifestyle. Moreover, we provide evidence that the sauropsid-specific beta-keratins have evolved as a subclass of EDC genes. Based on the comprehensive characterization of the arrangement, exon–intron structures and conserved sequence elements of EDC genes, we propose new scenarios for the evolutionary origin of epidermal barrier proteins via fusion of neighboring S100A and peptidoglycan recognition protein genes, subsequent loss of exons and highly divergent sequence evolution. Oxford University Press 2014-12 2014-08-27 /pmc/articles/PMC4245816/ /pubmed/25169930 http://dx.doi.org/10.1093/molbev/msu251 Text en © The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Strasser, Bettina
Mlitz, Veronika
Hermann, Marcela
Rice, Robert H.
Eigenheer, Richard A.
Alibardi, Lorenzo
Tschachler, Erwin
Eckhart, Leopold
Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes
title Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes
title_full Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes
title_fullStr Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes
title_full_unstemmed Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes
title_short Evolutionary Origin and Diversification of Epidermal Barrier Proteins in Amniotes
title_sort evolutionary origin and diversification of epidermal barrier proteins in amniotes
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4245816/
https://www.ncbi.nlm.nih.gov/pubmed/25169930
http://dx.doi.org/10.1093/molbev/msu251
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