An exome-wide study of renal operational tolerance
BackgroundRenal operational tolerance is a rare and beneficial state of prolonged renal allograft function in the absence of immunosuppression. The underlying mechanisms are unknown. We hypothesized that tolerance might be driven by inherited protein coding genetic variants with large effect, at lea...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Medicine |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmed.2022.976248/full |
| _version_ | 1827920857276612608 |
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| author | Annick Massart Annick Massart Annick Massart Richard Danger Catharina Olsen Catharina Olsen Catharina Olsen Mary J. Emond Ondrej Viklicky Valérie Jacquemin Valérie Jacquemin Julie Soblet Julie Soblet Julie Soblet Sarah Duerinckx Sarah Duerinckx Didier Croes Didier Croes Didier Croes Didier Croes Camille Perazzolo Petra Hruba Dorien Daneels Dorien Daneels Dorien Daneels Ben Caljon Ben Caljon Mehmet Sukru Sever Julio Pascual Julio Pascual Marius Miglinas the Renal Tolerance Investigators Isabelle Pirson Lidia Ghisdal Guillaume Smits Guillaume Smits Magali Giral Magali Giral Magali Giral Daniel Abramowicz Marc Abramowicz Marc Abramowicz Marc Abramowicz Sophie Brouard Sophie Brouard Sophie Brouard Maria Aguilar Rodríguez Friederike Bachmann Rajendra Bahadur Shahi Frederike Bemelman Luboslav Bena Luigi Biancone Laura Braun Klemens Budde Alejandro Camargo-Salamanca Katia Clemente Hulya Colak Adrian Covic Jacques Degreve Philippe Gatault François Glowacki Karine Hadaya Marc Hazzan Bénédicte Janbon Christophe Legendre Umberto Maggiore Marius Miglinas Anja Mühlfeld Maarten Naesens Christian Noël Rainer Oberbauer Evangeline Pillebout Gian Benedetto Piredda Francesco Pisani Ana Ramírez Puga Tomas Reischig Francisco González-Roncero Søren Schwartz Sørensen Daniel Seron Micas Nurhan Seyahi Dimitrie Siriopol Goce Spasovski Jean-François Subra Erik Teugels Serhan Tuǧlular Sonia Van Dooren Catheline Vilain Florence Villemain Xavier Warling Bruno Watschinger Laurent Weekers |
| author_facet | Annick Massart Annick Massart Annick Massart Richard Danger Catharina Olsen Catharina Olsen Catharina Olsen Mary J. Emond Ondrej Viklicky Valérie Jacquemin Valérie Jacquemin Julie Soblet Julie Soblet Julie Soblet Sarah Duerinckx Sarah Duerinckx Didier Croes Didier Croes Didier Croes Didier Croes Camille Perazzolo Petra Hruba Dorien Daneels Dorien Daneels Dorien Daneels Ben Caljon Ben Caljon Mehmet Sukru Sever Julio Pascual Julio Pascual Marius Miglinas the Renal Tolerance Investigators Isabelle Pirson Lidia Ghisdal Guillaume Smits Guillaume Smits Magali Giral Magali Giral Magali Giral Daniel Abramowicz Marc Abramowicz Marc Abramowicz Marc Abramowicz Sophie Brouard Sophie Brouard Sophie Brouard Maria Aguilar Rodríguez Friederike Bachmann Rajendra Bahadur Shahi Frederike Bemelman Luboslav Bena Luigi Biancone Laura Braun Klemens Budde Alejandro Camargo-Salamanca Katia Clemente Hulya Colak Adrian Covic Jacques Degreve Philippe Gatault François Glowacki Karine Hadaya Marc Hazzan Bénédicte Janbon Christophe Legendre Umberto Maggiore Marius Miglinas Anja Mühlfeld Maarten Naesens Christian Noël Rainer Oberbauer Evangeline Pillebout Gian Benedetto Piredda Francesco Pisani Ana Ramírez Puga Tomas Reischig Francisco González-Roncero Søren Schwartz Sørensen Daniel Seron Micas Nurhan Seyahi Dimitrie Siriopol Goce Spasovski Jean-François Subra Erik Teugels Serhan Tuǧlular Sonia Van Dooren Catheline Vilain Florence Villemain Xavier Warling Bruno Watschinger Laurent Weekers |
| author_sort | Annick Massart |
| collection | DOAJ |
| description | BackgroundRenal operational tolerance is a rare and beneficial state of prolonged renal allograft function in the absence of immunosuppression. The underlying mechanisms are unknown. We hypothesized that tolerance might be driven by inherited protein coding genetic variants with large effect, at least in some patients.MethodsWe set up a European survey of over 218,000 renal transplant recipients and collected DNAs from 40 transplant recipients who maintained good allograft function without immunosuppression for at least 1 year. We performed an exome-wide association study comparing the distribution of moderate to high impact variants in 36 tolerant patients, selected for genetic homogeneity using principal component analysis, and 192 controls, using an optimal sequence-kernel association test adjusted for small samples.ResultsWe identified rare variants of HOMER2 (3/36, FDR 0.0387), IQCH (5/36, FDR 0.0362), and LCN2 (3/36, FDR 0.102) in 10 tolerant patients vs. 0 controls. One patient carried a variant in both HOMER2 and LCN2. Furthermore, the three genes showed an identical variant in two patients each. The three genes are expressed at the primary cilium, a key structure in immune responses.ConclusionRare protein coding variants are associated with operational tolerance in a sizable portion of patients. Our findings have important implications for a better understanding of immune tolerance in transplantation and other fields of medicine.ClinicalTrials.gov, identifier: NCT05124444. |
| first_indexed | 2024-03-13T04:18:48Z |
| format | Article |
| id | doaj.art-728d19d9593f48acbfe88073eed48e31 |
| institution | Directory Open Access Journal |
| issn | 2296-858X |
| language | English |
| last_indexed | 2024-03-13T04:18:48Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Medicine |
| spelling | doaj.art-728d19d9593f48acbfe88073eed48e312023-06-20T16:06:32ZengFrontiers Media S.A.Frontiers in Medicine2296-858X2023-05-01910.3389/fmed.2022.976248976248An exome-wide study of renal operational toleranceAnnick Massart0Annick Massart1Annick Massart2Richard Danger3Catharina Olsen4Catharina Olsen5Catharina Olsen6Mary J. Emond7Ondrej Viklicky8Valérie Jacquemin9Valérie Jacquemin10Julie Soblet11Julie Soblet12Julie Soblet13Sarah Duerinckx14Sarah Duerinckx15Didier Croes16Didier Croes17Didier Croes18Didier Croes19Camille Perazzolo20Petra Hruba21Dorien Daneels22Dorien Daneels23Dorien Daneels24Ben Caljon25Ben Caljon26Mehmet Sukru Sever27Julio Pascual28Julio Pascual29Marius Miglinas30the Renal Tolerance InvestigatorsIsabelle Pirson31Lidia Ghisdal32Guillaume Smits33Guillaume Smits34Magali Giral35Magali Giral36Magali Giral37Daniel Abramowicz38Marc Abramowicz39Marc Abramowicz40Marc Abramowicz41Sophie Brouard42Sophie Brouard43Sophie Brouard44Maria Aguilar RodríguezFriederike BachmannRajendra Bahadur ShahiFrederike BemelmanLuboslav BenaLuigi BianconeLaura BraunKlemens BuddeAlejandro Camargo-SalamancaKatia ClementeHulya ColakAdrian CovicJacques DegrevePhilippe GataultFrançois GlowackiKarine HadayaMarc HazzanBénédicte JanbonChristophe LegendreUmberto MaggioreMarius MiglinasAnja MühlfeldMaarten NaesensChristian NoëlRainer OberbauerEvangeline PilleboutGian Benedetto PireddaFrancesco PisaniAna Ramírez PugaTomas ReischigFrancisco González-RonceroSøren Schwartz SørensenDaniel Seron MicasNurhan SeyahiDimitrie SiriopolGoce SpasovskiJean-François SubraErik TeugelsSerhan TuǧlularSonia Van DoorenCatheline VilainFlorence VillemainXavier WarlingBruno WatschingerLaurent WeekersHuman Genetics Unit, Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM), Université Libre de Bruxelles (ULB), Brussels, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumDepartment of Nephrology, Antwerp University Hospital and Laboratory of Experimental Medicine, University of Antwerp, Antwerp, BelgiumCHU Nantes, Nantes Université, INSERM, Center for Research in Transplantation and Translational Immunology, CR2TI, UMR 1064, ITUN, Nantes, FranceInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumBrussels Interuniversity Genomics High Throughput Core (BRIGHTcore), VUB-ULB, Brussels, BelgiumCenter for Medical Genetics, Reproduction and Genetics, Reproduction Genetics and Regenerative Medicine, Vrije Universiteit Brussel, UZ Brussel, Brussels, BelgiumDepartment of Biostatistics, University of Washington, Seattle, WA, United StatesTransplant Laboratory, Institute for Clinical and Experimental Medicine, Prague, CzechiaHuman Genetics Unit, Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM), Université Libre de Bruxelles (ULB), Brussels, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumDepartment of Genetics, Hôpital Erasme, ULB Center of Human Genetics, Université Libre de Bruxelles, Brussels, Belgium0Department of Genetics, Hôpital Universitaire des Enfants Reine Fabiola, ULB Center of Human Genetics, Université Libre de Bruxelles, Brussels, BelgiumHuman Genetics Unit, Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM), Université Libre de Bruxelles (ULB), Brussels, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumBrussels Interuniversity Genomics High Throughput Core (BRIGHTcore), VUB-ULB, Brussels, BelgiumCenter for Medical Genetics, Reproduction and Genetics, Reproduction Genetics and Regenerative Medicine, Vrije Universiteit Brussel, UZ Brussel, Brussels, Belgium1Center for Human Genetics, Clinique Universitaires Saint Luc, Brussels, BelgiumHuman Genetics Unit, Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM), Université Libre de Bruxelles (ULB), Brussels, BelgiumTransplant Laboratory, Institute for Clinical and Experimental Medicine, Prague, CzechiaInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumBrussels Interuniversity Genomics High Throughput Core (BRIGHTcore), VUB-ULB, Brussels, BelgiumCenter for Medical Genetics, Reproduction and Genetics, Reproduction Genetics and Regenerative Medicine, Vrije Universiteit Brussel, UZ Brussel, Brussels, BelgiumBrussels Interuniversity Genomics High Throughput Core (BRIGHTcore), VUB-ULB, Brussels, BelgiumCenter for Medical Genetics, Reproduction and Genetics, Reproduction Genetics and Regenerative Medicine, Vrije Universiteit Brussel, UZ Brussel, Brussels, Belgium2Istanbul Tip Fakültesi, Istanbul School of Medicine, Internal Medicine, Nephrology, Istanbul, Türkiye3Department of Nephrology, Hospital del Mar, Institute Mar for Medical Research, Barcelona, Spain4Department of Nephrology, Hospital Universitario 12 de Octubre, Madrid, Spain5Nephrology Center, Santaros Klinikos, Medical Faculty, Vilnius University, Vilnius, LithuaniaHuman Genetics Unit, Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM), Université Libre de Bruxelles (ULB), Brussels, Belgium6Department of Nephrology, Hospital Centre EpiCURA, Baudour, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, BelgiumDepartment of Genetics, Hôpital Erasme, ULB Center of Human Genetics, Université Libre de Bruxelles, Brussels, BelgiumCHU Nantes, Nantes Université, INSERM, Center for Research in Transplantation and Translational Immunology, CR2TI, UMR 1064, ITUN, Nantes, France7CHU Nantes, Centre d'Investigation Clinique en Biothérapie, Centre de Ressources Biologiques (CRB), Nantes, France8LabEx IGO “Immunotherapy, Graft, Oncology”, Nantes, FranceDepartment of Nephrology, Antwerp University Hospital and Laboratory of Experimental Medicine, University of Antwerp, Antwerp, BelgiumHuman Genetics Unit, Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM), Université Libre de Bruxelles (ULB), Brussels, BelgiumInteruniversity Institute of Bioinformatics in Brussels (IB2), Université Libre de Bruxelles - Vrije Universiteit Brussel (ULB-VUB), Brussels, Belgium9Department of Genetic Medicine and Development, Faculty of Medicine, Université de Geneve, Geneva, SwitzerlandCHU Nantes, Nantes Université, INSERM, Center for Research in Transplantation and Translational Immunology, CR2TI, UMR 1064, ITUN, Nantes, France7CHU Nantes, Centre d'Investigation Clinique en Biothérapie, Centre de Ressources Biologiques (CRB), Nantes, France8LabEx IGO “Immunotherapy, Graft, Oncology”, Nantes, FranceBackgroundRenal operational tolerance is a rare and beneficial state of prolonged renal allograft function in the absence of immunosuppression. The underlying mechanisms are unknown. We hypothesized that tolerance might be driven by inherited protein coding genetic variants with large effect, at least in some patients.MethodsWe set up a European survey of over 218,000 renal transplant recipients and collected DNAs from 40 transplant recipients who maintained good allograft function without immunosuppression for at least 1 year. We performed an exome-wide association study comparing the distribution of moderate to high impact variants in 36 tolerant patients, selected for genetic homogeneity using principal component analysis, and 192 controls, using an optimal sequence-kernel association test adjusted for small samples.ResultsWe identified rare variants of HOMER2 (3/36, FDR 0.0387), IQCH (5/36, FDR 0.0362), and LCN2 (3/36, FDR 0.102) in 10 tolerant patients vs. 0 controls. One patient carried a variant in both HOMER2 and LCN2. Furthermore, the three genes showed an identical variant in two patients each. The three genes are expressed at the primary cilium, a key structure in immune responses.ConclusionRare protein coding variants are associated with operational tolerance in a sizable portion of patients. Our findings have important implications for a better understanding of immune tolerance in transplantation and other fields of medicine.ClinicalTrials.gov, identifier: NCT05124444.https://www.frontiersin.org/articles/10.3389/fmed.2022.976248/fullexome sequencingrenal transplantationoperational toleranceNGALLCN2Homer2 |
| spellingShingle | Annick Massart Annick Massart Annick Massart Richard Danger Catharina Olsen Catharina Olsen Catharina Olsen Mary J. Emond Ondrej Viklicky Valérie Jacquemin Valérie Jacquemin Julie Soblet Julie Soblet Julie Soblet Sarah Duerinckx Sarah Duerinckx Didier Croes Didier Croes Didier Croes Didier Croes Camille Perazzolo Petra Hruba Dorien Daneels Dorien Daneels Dorien Daneels Ben Caljon Ben Caljon Mehmet Sukru Sever Julio Pascual Julio Pascual Marius Miglinas the Renal Tolerance Investigators Isabelle Pirson Lidia Ghisdal Guillaume Smits Guillaume Smits Magali Giral Magali Giral Magali Giral Daniel Abramowicz Marc Abramowicz Marc Abramowicz Marc Abramowicz Sophie Brouard Sophie Brouard Sophie Brouard Maria Aguilar Rodríguez Friederike Bachmann Rajendra Bahadur Shahi Frederike Bemelman Luboslav Bena Luigi Biancone Laura Braun Klemens Budde Alejandro Camargo-Salamanca Katia Clemente Hulya Colak Adrian Covic Jacques Degreve Philippe Gatault François Glowacki Karine Hadaya Marc Hazzan Bénédicte Janbon Christophe Legendre Umberto Maggiore Marius Miglinas Anja Mühlfeld Maarten Naesens Christian Noël Rainer Oberbauer Evangeline Pillebout Gian Benedetto Piredda Francesco Pisani Ana Ramírez Puga Tomas Reischig Francisco González-Roncero Søren Schwartz Sørensen Daniel Seron Micas Nurhan Seyahi Dimitrie Siriopol Goce Spasovski Jean-François Subra Erik Teugels Serhan Tuǧlular Sonia Van Dooren Catheline Vilain Florence Villemain Xavier Warling Bruno Watschinger Laurent Weekers An exome-wide study of renal operational tolerance Frontiers in Medicine exome sequencing renal transplantation operational tolerance NGAL LCN2 Homer2 |
| title | An exome-wide study of renal operational tolerance |
| title_full | An exome-wide study of renal operational tolerance |
| title_fullStr | An exome-wide study of renal operational tolerance |
| title_full_unstemmed | An exome-wide study of renal operational tolerance |
| title_short | An exome-wide study of renal operational tolerance |
| title_sort | exome wide study of renal operational tolerance |
| topic | exome sequencing renal transplantation operational tolerance NGAL LCN2 Homer2 |
| url | https://www.frontiersin.org/articles/10.3389/fmed.2022.976248/full |
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florencevillemain exomewidestudyofrenaloperationaltolerance AT xavierwarling exomewidestudyofrenaloperationaltolerance AT brunowatschinger exomewidestudyofrenaloperationaltolerance AT laurentweekers exomewidestudyofrenaloperationaltolerance |