Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management

Abstract Background BRCA1:c.5017_5019del (p.His1673del) is a founder variant relatively frequent in Northern Italy. Despite previous suggestion of pathogenicity, variant classification in public databases is still conflicting, needing additional evidence. Methods Maximum likelihood penetrance of bre...

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Main Authors: Giovanni Innella, Cristina Fortuno, Laura Caleca, Bing‐Jian Feng, Courtney Carroll, Michael T. Parsons, Sara Miccoli, Marco Montagna, Daniele Calistri, Laura Cortesi, Barbara Pasini, Siranoush Manoukian, Daniela Giachino, Laura Matricardi, Maria Cristina Foti, Valentina Zampiga, Claudia Piombino, Elena Barbieri, Francesca Vignolo Lutati, Jacopo Azzolini, Rita Danesi, Valentina Arcangeli, Sandrine M. Caputo, Nadia Boutry‐Kryza, Vincent Goussot, Susan Hiraki, Marcy Richardson, Hereditary Breast/Ovarian Cancer IOV network (HBOC IOVnet), Simona Ferrari, Paolo Radice, Amanda B. Spurdle, Daniela Turchetti
Format: Article
Language:English
Published: Wiley 2024-08-01
Series:Cancer Medicine
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Online Access:https://doi.org/10.1002/cam4.70114
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author Giovanni Innella
Cristina Fortuno
Laura Caleca
Bing‐Jian Feng
Courtney Carroll
Michael T. Parsons
Sara Miccoli
Marco Montagna
Daniele Calistri
Laura Cortesi
Barbara Pasini
Siranoush Manoukian
Daniela Giachino
Laura Matricardi
Maria Cristina Foti
Valentina Zampiga
Claudia Piombino
Elena Barbieri
Francesca Vignolo Lutati
Jacopo Azzolini
Rita Danesi
Valentina Arcangeli
Sandrine M. Caputo
Nadia Boutry‐Kryza
Vincent Goussot
Susan Hiraki
Marcy Richardson
Hereditary Breast/Ovarian Cancer IOV network (HBOC IOVnet)
Simona Ferrari
Paolo Radice
Amanda B. Spurdle
Daniela Turchetti
author_facet Giovanni Innella
Cristina Fortuno
Laura Caleca
Bing‐Jian Feng
Courtney Carroll
Michael T. Parsons
Sara Miccoli
Marco Montagna
Daniele Calistri
Laura Cortesi
Barbara Pasini
Siranoush Manoukian
Daniela Giachino
Laura Matricardi
Maria Cristina Foti
Valentina Zampiga
Claudia Piombino
Elena Barbieri
Francesca Vignolo Lutati
Jacopo Azzolini
Rita Danesi
Valentina Arcangeli
Sandrine M. Caputo
Nadia Boutry‐Kryza
Vincent Goussot
Susan Hiraki
Marcy Richardson
Hereditary Breast/Ovarian Cancer IOV network (HBOC IOVnet)
Simona Ferrari
Paolo Radice
Amanda B. Spurdle
Daniela Turchetti
author_sort Giovanni Innella
collection DOAJ
description Abstract Background BRCA1:c.5017_5019del (p.His1673del) is a founder variant relatively frequent in Northern Italy. Despite previous suggestion of pathogenicity, variant classification in public databases is still conflicting, needing additional evidence. Methods Maximum likelihood penetrance of breast/ovarian and other cancer types was estimated using full pedigree data from 53 informative Italian families. The effect of the variant on BRCA1‐ABRAXAS1 interaction was assessed using a GFP‐fragment reassembly‐based PPI assay. Results were combined with additional data from multiple sources to classify the variant according to ACMG/AMP classification rules specified for BRCA1/2. Results Variant‐carriers displayed increased risk for ovarian cancer (HR = 33.0, 95% CI = 7.0–155.0; cumulative risk at age 70 = 27.6%, 95% CI = 12.6–40.0%) but not for breast cancer (HR = 0.7, 95% CI = 0.2–2.2). An increased risk of uterine cancer (HR = 8.0, 95% CI = 1.03–61.6) emerged, warranting further evaluation. Likelihood‐ratio in favor of pathogenicity was 98898642.82 under assumption of standard BRCA1 breast and ovarian penetrance, and 104240832.84 after excluding breast cancer diagnoses (based on penetrance results). Functional analysis demonstrated that the variant abrogates the BRCA1‐ABRAXAS1 binding, supporting the PS3 code assignment within the ACMG/AMP rule‐based model. Collectively, these findings allowed to classify the variant as pathogenic. Conclusion Pathogenicity of BRCA1:c.5017_5019del(p.His1673del) has been confirmed; however, breast cancer risk in Italian families is not increased, unlike in families from other countries and in carriers of most BRCA1 pathogenic variants. The knowledge of atypical risk profiles for this and other variants will pave the way for personalized management based on specific genotype.
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spelling doaj-art-32f976e151b24f91bbf40981195926b12025-08-20T02:48:12ZengWileyCancer Medicine2045-76342024-08-011316n/an/a10.1002/cam4.70114Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical managementGiovanni Innella0Cristina Fortuno1Laura Caleca2Bing‐Jian Feng3Courtney Carroll4Michael T. Parsons5Sara Miccoli6Marco Montagna7Daniele Calistri8Laura Cortesi9Barbara Pasini10Siranoush Manoukian11Daniela Giachino12Laura Matricardi13Maria Cristina Foti14Valentina Zampiga15Claudia Piombino16Elena Barbieri17Francesca Vignolo Lutati18Jacopo Azzolini19Rita Danesi20Valentina Arcangeli21Sandrine M. Caputo22Nadia Boutry‐Kryza23Vincent Goussot24Susan Hiraki25Marcy Richardson26Hereditary Breast/Ovarian Cancer IOV network (HBOC IOVnet)Simona Ferrari27Paolo Radice28Amanda B. Spurdle29Daniela Turchetti30Department of Medical and Surgical Sciences (DIMEC) University of Bologna Bologna ItalyPopulation Health QIMR Berghofer Medical Research Institute Brisbane Queensland AustraliaUnit of Predictive Medicine: Molecular Bases of Genetic Risk, Department of Experimental Oncology Fondazione IRCCS Istituto Nazionale dei Tumori Milan ItalyUniversity of Utah Salt Lake City Utah USAUniversity of Utah Salt Lake City Utah USAPopulation Health QIMR Berghofer Medical Research Institute Brisbane Queensland AustraliaMedical Genetics Unit IRCCS Azienda Ospedaliero‐Universitaria di Bologna Bologna ItalyImmunology and Molecular Oncology Unit Veneto Institute of Oncology IOV—IRCCS Padua ItalyBiosciences Laboratory IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori” Meldola ItalyDivision of Medical Oncology, Department of Oncology and Hematology University Hospital of Modena Modena ItalyMedical Genetics Unit Città della Salute e della Scienza University Hospital Torino ItalyUnit of Medical Genetics, Department of Medical Oncology and Hematology Fondazione IRCCS Istituto Nazionale dei Tumori Milan ItalyMedical Genetic Unit San Luigi Gonzaga University Hospital Torino ItalyImmunology and Molecular Oncology Unit Veneto Institute of Oncology IOV—IRCCS Padua ItalyImmunology and Molecular Oncology Unit Veneto Institute of Oncology IOV—IRCCS Padua ItalyBiosciences Laboratory IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori” Meldola ItalyDivision of Medical Oncology, Department of Oncology and Hematology University Hospital of Modena Modena ItalyDivision of Medical Oncology, Department of Oncology and Hematology University Hospital of Modena Modena ItalyMedical Genetics Unit Città della Salute e della Scienza University Hospital Torino ItalyUnit of Medical Genetics, Department of Medical Oncology and Hematology Fondazione IRCCS Istituto Nazionale dei Tumori Milan ItalyRomagna Cancer Registry IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori” Meldola ItalyRomagna Cancer Registry IRCCS Istituto Romagnolo per lo Studio dei Tumori (IRST) “Dino Amadori” Meldola ItalyDepartment of Genetics, Institut Curie, Paris France and Paris Sciences Lettres Research University Paris FranceService de génétique Hospices Civils de Lyon Bron FranceDépartement de Biologie et Pathologie des Tumeurs Centre de Lutte Contre le Cancer Georges François Leclerc Dijon FranceGeneDx Gaithersburg Maryland USAAmbry Genetics Aliso Viejo California USAMedical Genetics Unit IRCCS Azienda Ospedaliero‐Universitaria di Bologna Bologna ItalyUnit of Predictive Medicine: Molecular Bases of Genetic Risk, Department of Experimental Oncology Fondazione IRCCS Istituto Nazionale dei Tumori Milan ItalyPopulation Health QIMR Berghofer Medical Research Institute Brisbane Queensland AustraliaDepartment of Medical and Surgical Sciences (DIMEC) University of Bologna Bologna ItalyAbstract Background BRCA1:c.5017_5019del (p.His1673del) is a founder variant relatively frequent in Northern Italy. Despite previous suggestion of pathogenicity, variant classification in public databases is still conflicting, needing additional evidence. Methods Maximum likelihood penetrance of breast/ovarian and other cancer types was estimated using full pedigree data from 53 informative Italian families. The effect of the variant on BRCA1‐ABRAXAS1 interaction was assessed using a GFP‐fragment reassembly‐based PPI assay. Results were combined with additional data from multiple sources to classify the variant according to ACMG/AMP classification rules specified for BRCA1/2. Results Variant‐carriers displayed increased risk for ovarian cancer (HR = 33.0, 95% CI = 7.0–155.0; cumulative risk at age 70 = 27.6%, 95% CI = 12.6–40.0%) but not for breast cancer (HR = 0.7, 95% CI = 0.2–2.2). An increased risk of uterine cancer (HR = 8.0, 95% CI = 1.03–61.6) emerged, warranting further evaluation. Likelihood‐ratio in favor of pathogenicity was 98898642.82 under assumption of standard BRCA1 breast and ovarian penetrance, and 104240832.84 after excluding breast cancer diagnoses (based on penetrance results). Functional analysis demonstrated that the variant abrogates the BRCA1‐ABRAXAS1 binding, supporting the PS3 code assignment within the ACMG/AMP rule‐based model. Collectively, these findings allowed to classify the variant as pathogenic. Conclusion Pathogenicity of BRCA1:c.5017_5019del(p.His1673del) has been confirmed; however, breast cancer risk in Italian families is not increased, unlike in families from other countries and in carriers of most BRCA1 pathogenic variants. The knowledge of atypical risk profiles for this and other variants will pave the way for personalized management based on specific genotype.https://doi.org/10.1002/cam4.70114BRCA1breast cancercancer riskclassificationclinical managementovarian cancer
spellingShingle Giovanni Innella
Cristina Fortuno
Laura Caleca
Bing‐Jian Feng
Courtney Carroll
Michael T. Parsons
Sara Miccoli
Marco Montagna
Daniele Calistri
Laura Cortesi
Barbara Pasini
Siranoush Manoukian
Daniela Giachino
Laura Matricardi
Maria Cristina Foti
Valentina Zampiga
Claudia Piombino
Elena Barbieri
Francesca Vignolo Lutati
Jacopo Azzolini
Rita Danesi
Valentina Arcangeli
Sandrine M. Caputo
Nadia Boutry‐Kryza
Vincent Goussot
Susan Hiraki
Marcy Richardson
Hereditary Breast/Ovarian Cancer IOV network (HBOC IOVnet)
Simona Ferrari
Paolo Radice
Amanda B. Spurdle
Daniela Turchetti
Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management
Cancer Medicine
BRCA1
breast cancer
cancer risk
classification
clinical management
ovarian cancer
title Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management
title_full Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management
title_fullStr Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management
title_full_unstemmed Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management
title_short Atypical cancer risk profile in carriers of Italian founder BRCA1 variant p.His1673del: Implications for classification and clinical management
title_sort atypical cancer risk profile in carriers of italian founder brca1 variant p his1673del implications for classification and clinical management
topic BRCA1
breast cancer
cancer risk
classification
clinical management
ovarian cancer
url https://doi.org/10.1002/cam4.70114
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