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 cart...
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ftoslouniv:oai:www.duo.uio.no:10852/98435 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 http://hdl.handle.net/10852/98435 https://doi.org/10.1186/s12915-022-01489-8 eng eng BMC Biology. 2022 Dec 27;20(1):293 http://hdl.handle.net/10852/98435 2103839 https://doi.org/10.1186/s12915-022-01489-8 The Author(s) Attribution 4.0 International http://creativecommons.org/licenses/by/4.0/ CC-BY Journal article Tidsskriftartikkel Peer reviewed PublishedVersion 2022 ftoslouniv https://doi.org/10.1186/s12915-022-01489-8 2023-02-01T23:36:24Z 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 ... Article in Journal/Newspaper atlantic cod Universitet i Oslo: Digitale utgivelser ved UiO (DUO) BMC Biology 20 1 |
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Open Polar |
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Universitet i Oslo: Digitale utgivelser ved UiO (DUO) |
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ftoslouniv |
language |
English |
description |
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 ... |
format |
Article in Journal/Newspaper |
author |
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 |
spellingShingle |
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 |
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 |
publishDate |
2022 |
url |
http://hdl.handle.net/10852/98435 https://doi.org/10.1186/s12915-022-01489-8 |
genre |
atlantic cod |
genre_facet |
atlantic cod |
op_relation |
BMC Biology. 2022 Dec 27;20(1):293 http://hdl.handle.net/10852/98435 2103839 https://doi.org/10.1186/s12915-022-01489-8 |
op_rights |
The Author(s) Attribution 4.0 International http://creativecommons.org/licenses/by/4.0/ |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1186/s12915-022-01489-8 |
container_title |
BMC Biology |
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20 |
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1 |
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1766357848117215232 |