Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens

Abstract Several lines of evidence indirectly suggest that antigenic stimulation through the B‐cell receptor (BCR) supports chronic lymphocytic leukemia (CLL) development. In addition to self‐antigens, a number of microbial antigens have been proposed to contribute to the selection of the immunoglob...

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Main Authors: Nereida Jiménez de Oya, Marco De Giovanni, Jessica Fioravanti, Rudolf Übelhart, Pietro Di Lucia, Amleto Fiocchi, Stefano Iacovelli, Dimitar G Efremov, Federico Caligaris‐Cappio, Hassan Jumaa, Paolo Ghia, Luca G Guidotti, Matteo Iannacone
Format: Article
Language:English
Published: Springer Nature 2017-09-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201707732
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author Nereida Jiménez de Oya
Marco De Giovanni
Jessica Fioravanti
Rudolf Übelhart
Pietro Di Lucia
Amleto Fiocchi
Stefano Iacovelli
Dimitar G Efremov
Federico Caligaris‐Cappio
Hassan Jumaa
Paolo Ghia
Luca G Guidotti
Matteo Iannacone
author_facet Nereida Jiménez de Oya
Marco De Giovanni
Jessica Fioravanti
Rudolf Übelhart
Pietro Di Lucia
Amleto Fiocchi
Stefano Iacovelli
Dimitar G Efremov
Federico Caligaris‐Cappio
Hassan Jumaa
Paolo Ghia
Luca G Guidotti
Matteo Iannacone
author_sort Nereida Jiménez de Oya
collection DOAJ
description Abstract Several lines of evidence indirectly suggest that antigenic stimulation through the B‐cell receptor (BCR) supports chronic lymphocytic leukemia (CLL) development. In addition to self‐antigens, a number of microbial antigens have been proposed to contribute to the selection of the immunoglobulins expressed in CLL. How pathogen‐specific BCRs drive CLL development remains, however, largely unexplored. Here, we utilized mouse models of CLL pathogenesis to equip B cells with virus‐specific BCRs and study the effect of antigen recognition on leukemia growth. Our results show that BCR engagement is absolutely required for CLL development. Unexpectedly, however, neither acute nor chronic exposure to virus‐derived antigens influenced leukemia progression. Rather, CLL clones preferentially selected light chains that, when paired with virus‐specific heavy chains, conferred B cells the ability to recognize a broad range of autoantigens. Taken together, our results suggest that pathogens may drive CLL pathogenesis by selecting and expanding pathogen‐specific B cells that cross‐react with one or more self‐antigens.
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publishDate 2017-09-01
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spelling doaj-art-bd9fe90f9288488ea8972d0c1f258c6d2025-08-20T03:46:21ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842017-09-019111482149010.15252/emmm.201707732Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigensNereida Jiménez de Oya0Marco De Giovanni1Jessica Fioravanti2Rudolf Übelhart3Pietro Di Lucia4Amleto Fiocchi5Stefano Iacovelli6Dimitar G Efremov7Federico Caligaris‐Cappio8Hassan Jumaa9Paolo Ghia10Luca G Guidotti11Matteo Iannacone12Division of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteDivision of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteDivision of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteInstitute of Immunology, University Hospital UlmDivision of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteDivision of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteMolecular Hematology Unit, International Centre for Genetic Engineering & BiotechnologyMolecular Hematology Unit, International Centre for Genetic Engineering & BiotechnologyDivision of Experimental Oncology, IRCCS San Raffaele Scientific InstituteInstitute of Immunology, University Hospital UlmVita‐Salute San Raffaele UniversityDivision of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteDivision of Immunology, Transplantation and Infectious Diseases, IRCCS San Raffaele Scientific InstituteAbstract Several lines of evidence indirectly suggest that antigenic stimulation through the B‐cell receptor (BCR) supports chronic lymphocytic leukemia (CLL) development. In addition to self‐antigens, a number of microbial antigens have been proposed to contribute to the selection of the immunoglobulins expressed in CLL. How pathogen‐specific BCRs drive CLL development remains, however, largely unexplored. Here, we utilized mouse models of CLL pathogenesis to equip B cells with virus‐specific BCRs and study the effect of antigen recognition on leukemia growth. Our results show that BCR engagement is absolutely required for CLL development. Unexpectedly, however, neither acute nor chronic exposure to virus‐derived antigens influenced leukemia progression. Rather, CLL clones preferentially selected light chains that, when paired with virus‐specific heavy chains, conferred B cells the ability to recognize a broad range of autoantigens. Taken together, our results suggest that pathogens may drive CLL pathogenesis by selecting and expanding pathogen‐specific B cells that cross‐react with one or more self‐antigens.https://doi.org/10.15252/emmm.201707732autoantigensB‐cell receptorchronic lymphocytic leukemiainfectionlight chains
spellingShingle Nereida Jiménez de Oya
Marco De Giovanni
Jessica Fioravanti
Rudolf Übelhart
Pietro Di Lucia
Amleto Fiocchi
Stefano Iacovelli
Dimitar G Efremov
Federico Caligaris‐Cappio
Hassan Jumaa
Paolo Ghia
Luca G Guidotti
Matteo Iannacone
Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens
EMBO Molecular Medicine
autoantigens
B‐cell receptor
chronic lymphocytic leukemia
infection
light chains
title Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens
title_full Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens
title_fullStr Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens
title_full_unstemmed Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens
title_short Pathogen‐specific B‐cell receptors drive chronic lymphocytic leukemia by light‐chain‐dependent cross‐reaction with autoantigens
title_sort pathogen specific b cell receptors drive chronic lymphocytic leukemia by light chain dependent cross reaction with autoantigens
topic autoantigens
B‐cell receptor
chronic lymphocytic leukemia
infection
light chains
url https://doi.org/10.15252/emmm.201707732
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