Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish
BACKGROUND: Antibody affinity maturation in vertebrates requires the enzyme activation-induced cytidine deaminase (AID) which initiates secondary antibody diversification by mutating the immunoglobulin loci. AID-driven antibody diversification is conserved across jawed vertebrates since bony and car...
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Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795746/ http://www.ncbi.nlm.nih.gov/pubmed/36575514 https://doi.org/10.1186/s12915-022-01489-8 |
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Research Article Ghorbani, Atefeh Khataeipour, S. Javad Solbakken, Monica H. Huebert, David N. G. Khoddami, Minasadat Eslamloo, Khalil Collins, Cassandra Hori, Tiago Jentoft, Sissel Rise, Matthew L. Larijani, Mani Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish |
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Research Article |
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BACKGROUND: Antibody affinity maturation in vertebrates requires the enzyme activation-induced cytidine deaminase (AID) which initiates secondary antibody diversification by mutating the immunoglobulin loci. AID-driven antibody diversification is conserved across jawed vertebrates since bony and cartilaginous fish. Two exceptions have recently been reported, the Pipefish and Anglerfish, in which the AID-encoding aicda gene has been lost. Both cases are associated with unusual reproductive behavior, including male pregnancy and sexual parasitism. Several cold water fish in the Atlantic cod (Gadinae) family carry an aicda gene that encodes for a full-length enzyme but lack affinity-matured antibodies and rely on antibodies of broad antigenic specificity. Hence, we examined the functionality of their AID. RESULTS: By combining genomics, transcriptomics, immune responsiveness, and functional enzymology of AID from 36 extant species, we demonstrate that AID of that Atlantic cod and related fish have extremely lethargic or no catalytic activity. Through ancestral reconstruction and functional enzymology of 71 AID enzymes, we show that this enzymatic inactivation likely took place relatively recently at the emergence of the true cod family (Gadidae) from their ancestral Gadiformes order. We show that this AID inactivation is not only concordant with the previously shown loss of key adaptive immune genes and expansion of innate and cell-based immune genes in the Gadiformes but is further reflected in the genomes of these fish in the form of loss of AID-favored sequence motifs in their immunoglobulin variable region genes. CONCLUSIONS: Recent demonstrations of the loss of the aicda gene in two fish species challenge the paradigm that AID-driven secondary antibody diversification is absolutely conserved in jawed vertebrates. These species have unusual reproductive behaviors forming an evolutionary pressure for a certain loss of immunity to avoid tissue rejection. We report here an instance of catalytic inactivation and ... |
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Text |
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Ghorbani, Atefeh Khataeipour, S. Javad Solbakken, Monica H. Huebert, David N. G. Khoddami, Minasadat Eslamloo, Khalil Collins, Cassandra Hori, Tiago Jentoft, Sissel Rise, Matthew L. Larijani, Mani |
author_facet |
Ghorbani, Atefeh Khataeipour, S. Javad Solbakken, Monica H. Huebert, David N. G. Khoddami, Minasadat Eslamloo, Khalil Collins, Cassandra Hori, Tiago Jentoft, Sissel Rise, Matthew L. Larijani, Mani |
author_sort |
Ghorbani, Atefeh |
title |
Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish |
title_short |
Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish |
title_full |
Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish |
title_fullStr |
Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish |
title_full_unstemmed |
Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish |
title_sort |
ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the gadiformes bony fish |
publisher |
BioMed Central |
publishDate |
2022 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795746/ http://www.ncbi.nlm.nih.gov/pubmed/36575514 https://doi.org/10.1186/s12915-022-01489-8 |
genre |
atlantic cod |
genre_facet |
atlantic cod |
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BMC Biol |
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795746/ http://www.ncbi.nlm.nih.gov/pubmed/36575514 http://dx.doi.org/10.1186/s12915-022-01489-8 |
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© The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
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ftpubmed:oai:pubmedcentral.nih.gov:9795746 2023-05-15T15:27:24+02:00 Ancestral reconstruction reveals catalytic inactivation of activation-induced cytidine deaminase concomitant with cold water adaption in the Gadiformes bony fish Ghorbani, Atefeh Khataeipour, S. Javad Solbakken, Monica H. Huebert, David N. G. Khoddami, Minasadat Eslamloo, Khalil Collins, Cassandra Hori, Tiago Jentoft, Sissel Rise, Matthew L. Larijani, Mani 2022-12-27 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795746/ http://www.ncbi.nlm.nih.gov/pubmed/36575514 https://doi.org/10.1186/s12915-022-01489-8 en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795746/ http://www.ncbi.nlm.nih.gov/pubmed/36575514 http://dx.doi.org/10.1186/s12915-022-01489-8 © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. CC0 PDM CC-BY BMC Biol Research Article Text 2022 ftpubmed https://doi.org/10.1186/s12915-022-01489-8 2023-01-01T01:51:05Z BACKGROUND: Antibody affinity maturation in vertebrates requires the enzyme activation-induced cytidine deaminase (AID) which initiates secondary antibody diversification by mutating the immunoglobulin loci. AID-driven antibody diversification is conserved across jawed vertebrates since bony and cartilaginous fish. Two exceptions have recently been reported, the Pipefish and Anglerfish, in which the AID-encoding aicda gene has been lost. Both cases are associated with unusual reproductive behavior, including male pregnancy and sexual parasitism. Several cold water fish in the Atlantic cod (Gadinae) family carry an aicda gene that encodes for a full-length enzyme but lack affinity-matured antibodies and rely on antibodies of broad antigenic specificity. Hence, we examined the functionality of their AID. RESULTS: By combining genomics, transcriptomics, immune responsiveness, and functional enzymology of AID from 36 extant species, we demonstrate that AID of that Atlantic cod and related fish have extremely lethargic or no catalytic activity. Through ancestral reconstruction and functional enzymology of 71 AID enzymes, we show that this enzymatic inactivation likely took place relatively recently at the emergence of the true cod family (Gadidae) from their ancestral Gadiformes order. We show that this AID inactivation is not only concordant with the previously shown loss of key adaptive immune genes and expansion of innate and cell-based immune genes in the Gadiformes but is further reflected in the genomes of these fish in the form of loss of AID-favored sequence motifs in their immunoglobulin variable region genes. CONCLUSIONS: Recent demonstrations of the loss of the aicda gene in two fish species challenge the paradigm that AID-driven secondary antibody diversification is absolutely conserved in jawed vertebrates. These species have unusual reproductive behaviors forming an evolutionary pressure for a certain loss of immunity to avoid tissue rejection. We report here an instance of catalytic inactivation and ... Text atlantic cod PubMed Central (PMC) BMC Biology 20 1 |