AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway

Abstract Activation‐induced deaminase (AID) initiates secondary antibody diversification in germinal center B cells, giving rise to higher affinity antibodies through somatic hypermutation (SHM) or to isotype‐switched antibodies through class switch recombination (CSR). SHM and CSR are triggered by...

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Main Authors: Arantxa Pérez‐García, Pablo Pérez‐Durán, Thomas Wossning, Isora V Sernandez, Sonia M Mur, Marta Cañamero, Francisco X Real, Almudena R Ramiro
Format: Article
Language:English
Published: Springer Nature 2015-08-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201505348
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author Arantxa Pérez‐García
Pablo Pérez‐Durán
Thomas Wossning
Isora V Sernandez
Sonia M Mur
Marta Cañamero
Francisco X Real
Almudena R Ramiro
author_facet Arantxa Pérez‐García
Pablo Pérez‐Durán
Thomas Wossning
Isora V Sernandez
Sonia M Mur
Marta Cañamero
Francisco X Real
Almudena R Ramiro
author_sort Arantxa Pérez‐García
collection DOAJ
description Abstract Activation‐induced deaminase (AID) initiates secondary antibody diversification in germinal center B cells, giving rise to higher affinity antibodies through somatic hypermutation (SHM) or to isotype‐switched antibodies through class switch recombination (CSR). SHM and CSR are triggered by AID‐mediated deamination of cytosines in immunoglobulin genes. Importantly, AID activity in B cells is not restricted to Ig loci and can promote mutations and pro‐lymphomagenic translocations, establishing a direct oncogenic mechanism for germinal center‐derived neoplasias. AID is also expressed in response to inflammatory cues in epithelial cells, raising the possibility that AID mutagenic activity might drive carcinoma development. We directly tested this hypothesis by generating conditional knock‐in mouse models for AID overexpression in colon and pancreas epithelium. AID overexpression alone was not sufficient to promote epithelial cell neoplasia in these tissues, in spite of displaying mutagenic and genotoxic activity. Instead, we found that heterologous AID expression in pancreas promotes the expression of NKG2D ligands, the recruitment of CD8+ T cells, and the induction of epithelial cell death. Our results indicate that AID oncogenic potential in epithelial cells can be neutralized by immunosurveillance protective mechanisms.
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spelling doaj-art-f845f41e876b414eaa2cf320fdb7f77d2025-08-20T03:46:16ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842015-08-017101327133610.15252/emmm.201505348AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathwayArantxa Pérez‐García0Pablo Pérez‐Durán1Thomas Wossning2Isora V Sernandez3Sonia M Mur4Marta Cañamero5Francisco X Real6Almudena R Ramiro7B Cell Biology Lab, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)B Cell Biology Lab, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)B Cell Biology Lab, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)B Cell Biology Lab, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)B Cell Biology Lab, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)Roche Diagnostics GmbHEpithelial Carcinogenesis Group, Spanish National Cancer Research Centre (CNIO)B Cell Biology Lab, Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC)Abstract Activation‐induced deaminase (AID) initiates secondary antibody diversification in germinal center B cells, giving rise to higher affinity antibodies through somatic hypermutation (SHM) or to isotype‐switched antibodies through class switch recombination (CSR). SHM and CSR are triggered by AID‐mediated deamination of cytosines in immunoglobulin genes. Importantly, AID activity in B cells is not restricted to Ig loci and can promote mutations and pro‐lymphomagenic translocations, establishing a direct oncogenic mechanism for germinal center‐derived neoplasias. AID is also expressed in response to inflammatory cues in epithelial cells, raising the possibility that AID mutagenic activity might drive carcinoma development. We directly tested this hypothesis by generating conditional knock‐in mouse models for AID overexpression in colon and pancreas epithelium. AID overexpression alone was not sufficient to promote epithelial cell neoplasia in these tissues, in spite of displaying mutagenic and genotoxic activity. Instead, we found that heterologous AID expression in pancreas promotes the expression of NKG2D ligands, the recruitment of CD8+ T cells, and the induction of epithelial cell death. Our results indicate that AID oncogenic potential in epithelial cells can be neutralized by immunosurveillance protective mechanisms.https://doi.org/10.15252/emmm.201505348activation‐induced deaminasecancerepitheliumNKG2Dpancreas
spellingShingle Arantxa Pérez‐García
Pablo Pérez‐Durán
Thomas Wossning
Isora V Sernandez
Sonia M Mur
Marta Cañamero
Francisco X Real
Almudena R Ramiro
AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway
EMBO Molecular Medicine
activation‐induced deaminase
cancer
epithelium
NKG2D
pancreas
title AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway
title_full AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway
title_fullStr AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway
title_full_unstemmed AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway
title_short AID‐expressing epithelium is protected from oncogenic transformation by an NKG2D surveillance pathway
title_sort aid expressing epithelium is protected from oncogenic transformation by an nkg2d surveillance pathway
topic activation‐induced deaminase
cancer
epithelium
NKG2D
pancreas
url https://doi.org/10.15252/emmm.201505348
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