Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9

Summary: MCM8 and MCM9 are newly proposed cancer predisposition genes, linked to polyposis and early-onset cancer, in addition to their previously established association with hypogonadism. Given the uncertain range of phenotypic manifestations and unclear cancer risk estimates, this study aimed to...

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Main Authors: Noah C. Helderman, Ting Yang, Claire Palles, Diantha Terlouw, Hailiang Mei, Ruben H.P. Vorderman, Davy Cats, Marcos Díaz-Gay, Marjolijn C.J. Jongmans, Ashwin Ramdien, Irma van de Beek, Thomas F. Eleveld, Andrew Green, Frederik J. Hes, Marry M. van den Heuvel-Eibrink, Annelore Van Der Kelen, Sabine Kliesch, Roland P. Kuiper, Inge M.M. Lakeman, Lisa E.E.L.O. Lashley, Leendert H.J. Looijenga, Manon S. Oud, Johanna Steingröver, Yardena Tenenbaum-Rakover, Carli M. Tops, Frank Tüttelmann, Richarda M. de Voer, Dineke Westra, Margot J. Wyrwoll, Mariano Golubicki, Marina Antelo, Laia Bonjoch, Mariona Terradas, Laura Valle, Ludmil B. Alexandrov, Hans Morreau, Tom van Wezel, Sergi Castellví-Bel, Yael Goldberg, Maartje Nielsen
Format: Article
Language:English
Published: Elsevier 2025-10-01
Series:HGG Advances
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666247725000831
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author Noah C. Helderman
Ting Yang
Claire Palles
Diantha Terlouw
Hailiang Mei
Ruben H.P. Vorderman
Davy Cats
Marcos Díaz-Gay
Marjolijn C.J. Jongmans
Ashwin Ramdien
Irma van de Beek
Thomas F. Eleveld
Andrew Green
Frederik J. Hes
Marry M. van den Heuvel-Eibrink
Annelore Van Der Kelen
Sabine Kliesch
Roland P. Kuiper
Inge M.M. Lakeman
Lisa E.E.L.O. Lashley
Leendert H.J. Looijenga
Manon S. Oud
Johanna Steingröver
Yardena Tenenbaum-Rakover
Carli M. Tops
Frank Tüttelmann
Richarda M. de Voer
Dineke Westra
Margot J. Wyrwoll
Mariano Golubicki
Marina Antelo
Laia Bonjoch
Mariona Terradas
Laura Valle
Ludmil B. Alexandrov
Hans Morreau
Tom van Wezel
Sergi Castellví-Bel
Yael Goldberg
Maartje Nielsen
author_facet Noah C. Helderman
Ting Yang
Claire Palles
Diantha Terlouw
Hailiang Mei
Ruben H.P. Vorderman
Davy Cats
Marcos Díaz-Gay
Marjolijn C.J. Jongmans
Ashwin Ramdien
Irma van de Beek
Thomas F. Eleveld
Andrew Green
Frederik J. Hes
Marry M. van den Heuvel-Eibrink
Annelore Van Der Kelen
Sabine Kliesch
Roland P. Kuiper
Inge M.M. Lakeman
Lisa E.E.L.O. Lashley
Leendert H.J. Looijenga
Manon S. Oud
Johanna Steingröver
Yardena Tenenbaum-Rakover
Carli M. Tops
Frank Tüttelmann
Richarda M. de Voer
Dineke Westra
Margot J. Wyrwoll
Mariano Golubicki
Marina Antelo
Laia Bonjoch
Mariona Terradas
Laura Valle
Ludmil B. Alexandrov
Hans Morreau
Tom van Wezel
Sergi Castellví-Bel
Yael Goldberg
Maartje Nielsen
author_sort Noah C. Helderman
collection DOAJ
description Summary: MCM8 and MCM9 are newly proposed cancer predisposition genes, linked to polyposis and early-onset cancer, in addition to their previously established association with hypogonadism. Given the uncertain range of phenotypic manifestations and unclear cancer risk estimates, this study aimed to delineate the molecular and clinical characteristics of biallelic germline MCM8/MCM9 variant carriers. We found significant enrichment of biallelic MCM9 variants in individuals with colonic polyps (odds ratio [OR] 6.51, 95% confidence interval [CI] 1.24–34.11, p = 0.03), rectal polyps (OR 8.40, 95% CI 1.28–55.35, p = 0.03), and gastric cancer (OR 27.03, 95% CI 2.93–248.5; p = 0.004) in data from the 100000 Genomes Project, compared to controls. No similar enrichment was found for biallelic MCM8 variants or in the 200000 UK Biobank. Likewise, in our case series, which included 26 MCM8 and 28 MCM9 variant carriers, we documented polyposis, gastric cancer, and early-onset colorectal cancer (CRC) in MCM9 carriers but not in MCM8 carriers. Moreover, our case series indicates that beyond hypogonadism, biallelic MCM8 and MCM9 variants are associated with early-onset germ cell tumors (occurring before age 15). Tumors from MCM8/MCM9 variant carriers predominantly displayed clock-like mutational processes, without evidence of DNA repair deficiency-associated signatures. Collectively, our data indicate that biallelic MCM9 variants are associated with polyposis, gastric cancer, and early-onset CRC, while both biallelic MCM8 and MCM9 variants are linked to hypogonadism and the early development of germ cell tumors. These findings underscore the importance of including MCM8/MCM9 in diagnostic gene panels for certain clinical contexts and suggest that biallelic carriers may benefit from cancer surveillance.
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spelling doaj-art-3d2ca6dd8e7b422cba827f54cd1930152025-08-20T04:00:55ZengElsevierHGG Advances2666-24772025-10-016410048010.1016/j.xhgg.2025.100480Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9Noah C. Helderman0Ting Yang1Claire Palles2Diantha Terlouw3Hailiang Mei4Ruben H.P. Vorderman5Davy Cats6Marcos Díaz-Gay7Marjolijn C.J. Jongmans8Ashwin Ramdien9Irma van de Beek10Thomas F. Eleveld11Andrew Green12Frederik J. Hes13Marry M. van den Heuvel-Eibrink14Annelore Van Der Kelen15Sabine Kliesch16Roland P. Kuiper17Inge M.M. Lakeman18Lisa E.E.L.O. Lashley19Leendert H.J. Looijenga20Manon S. Oud21Johanna Steingröver22Yardena Tenenbaum-Rakover23Carli M. Tops24Frank Tüttelmann25Richarda M. de Voer26Dineke Westra27Margot J. Wyrwoll28Mariano Golubicki29Marina Antelo30Laia Bonjoch31Mariona Terradas32Laura Valle33Ludmil B. Alexandrov34Hans Morreau35Tom van Wezel36Sergi Castellví-Bel37Yael Goldberg38Maartje Nielsen39Department of Clinical Genetics, Leiden University Medical Center, Leiden, the NetherlandsDepartment of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093, USA; Department of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, La Jolla, CA 92037, USAInstitute of Cancer and Genomic Sciences, University of Birmingham, Birmingham, UKDepartment of Pathology, Leiden University Medical Center, Leiden, the NetherlandsSequencing Analysis Support Core, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, the NetherlandsSequencing Analysis Support Core, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, the NetherlandsSequencing Analysis Support Core, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, the NetherlandsDepartment of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093, USA; Department of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, La Jolla, CA 92037, USA; Digital Genomics Group, Structural Biology Program, Spanish National Cancer Research Center (CNIO), 28029 Madrid, SpainPrincess Maxima Center for Pediatric Oncology, Utrecht, the Netherlands; Department of Genetics, University Medical Center Utrecht, University of Utrecht, Utrecht, the NetherlandsDepartment of Clinical Genetics, Leiden University Medical Center, Leiden, the NetherlandsDepartment of Clinical Genetics, The Netherlands Cancer Institute, Amsterdam, the NetherlandsPrincess Maxima Center for Pediatric Oncology, Utrecht, the NetherlandsDepartment of Clinical Genetics, Children’s Health Ireland (CHI) at Crumlin, Dublin, IrelandVrije Universiteit Brussel (VUB), Universitair Ziekenhuis Brussel (UZ Brussel), Clinical Sciences, Research Group Genetics, Reproduction, and Development, Centre for Medical Genetics, Brussels, BelgiumPrincess Maxima Center for Pediatric Oncology, Utrecht, the Netherlands; Division of Childhealth, University Medical Center Utrecht, Utrecht, the NetherlandsVrije Universiteit Brussel (VUB), Universitair Ziekenhuis Brussel (UZ Brussel), Clinical Sciences, Research Group Genetics, Reproduction, and Development, Centre for Medical Genetics, Brussels, BelgiumCentre of Reproductive Medicine and Andrology, Department of Clinical and Surgical Andrology, University Hospital Münster, Münster, GermanyPrincess Maxima Center for Pediatric Oncology, Utrecht, the NetherlandsDepartment of Clinical Genetics, Leiden University Medical Center, Leiden, the NetherlandsDepartment of Obstetrics and Gynecology, Leiden University Medical Center, Leiden, the NetherlandsPrincess Maxima Center for Pediatric Oncology, Utrecht, the Netherlands; Department of Pathology, University Medical Center Utrecht, Utrecht, the NetherlandsDepartment of Human Genetics, Donders Institute for Brain, Cognition, and Behaviour, Radboud University Medical Center, Nijmegen, the NetherlandsCentre of Medical Genetics, Institute of Reproductive Genetics, University and University Hospital of Münster, Münster, GermanyPediatric Endocrinology, Clalit Health Services, Afula, Israel; The Ruth and Bruce Rappaport Faculty of Medicine, Technion, Haifa, IsraelDepartment of Clinical Genetics, Leiden University Medical Center, Leiden, the NetherlandsCentre of Medical Genetics, Institute of Reproductive Genetics, University and University Hospital of Münster, Münster, GermanyDepartment of Human Genetics, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Nijmegen, the NetherlandsDepartment of Human Genetics, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Nijmegen, the NetherlandsCentre for Regenerative Medicine, Institute for Stem Cell Research, School of Biological Sciences, University of Edinburgh, Edinburgh, UKOncology Section and Molecular Biology Laboratory, Hospital of Gastroenterology “Dr. C.B. Udaondo”, Buenos Aires, ArgentinaOncology Section and Molecular Biology Laboratory, Hospital of Gastroenterology “Dr. C.B. Udaondo”, Buenos Aires, ArgentinaGastroenterology, Fundació de Recerca Clínic Barcelona-Institut d’Investigacions Biomèdiques August Pi I Sunyer (FRCB-IDIBAPS), CIBEREHD, Universitat de Barcelona, Clínic Barcelona, Barcelona, SpainHereditary Cancer Program, Catalan Institute of Oncology, Oncobell Program, IDIBELL, CIBERONC, Hospitalet de Llobregat, Barcelona, SpainHereditary Cancer Program, Catalan Institute of Oncology, Oncobell Program, IDIBELL, CIBERONC, Hospitalet de Llobregat, Barcelona, SpainDepartment of Cellular and Molecular Medicine, University of California, San Diego, La Jolla, CA 92093, USA; Department of Bioengineering, University of California, San Diego, La Jolla, CA 92093, USA; Moores Cancer Center, University of California, San Diego, La Jolla, CA 92037, USADepartment of Pathology, Leiden University Medical Center, Leiden, the NetherlandsDepartment of Pathology, Leiden University Medical Center, Leiden, the NetherlandsGastroenterology, Fundació de Recerca Clínic Barcelona-Institut d’Investigacions Biomèdiques August Pi I Sunyer (FRCB-IDIBAPS), CIBEREHD, Universitat de Barcelona, Clínic Barcelona, Barcelona, SpainRaphael Recanati Genetic Institute, Rabin Medical Center-Beilinson Hospital, Petah Tikva, IsraelDepartment of Clinical Genetics, Leiden University Medical Center, Leiden, the Netherlands; Corresponding authorSummary: MCM8 and MCM9 are newly proposed cancer predisposition genes, linked to polyposis and early-onset cancer, in addition to their previously established association with hypogonadism. Given the uncertain range of phenotypic manifestations and unclear cancer risk estimates, this study aimed to delineate the molecular and clinical characteristics of biallelic germline MCM8/MCM9 variant carriers. We found significant enrichment of biallelic MCM9 variants in individuals with colonic polyps (odds ratio [OR] 6.51, 95% confidence interval [CI] 1.24–34.11, p = 0.03), rectal polyps (OR 8.40, 95% CI 1.28–55.35, p = 0.03), and gastric cancer (OR 27.03, 95% CI 2.93–248.5; p = 0.004) in data from the 100000 Genomes Project, compared to controls. No similar enrichment was found for biallelic MCM8 variants or in the 200000 UK Biobank. Likewise, in our case series, which included 26 MCM8 and 28 MCM9 variant carriers, we documented polyposis, gastric cancer, and early-onset colorectal cancer (CRC) in MCM9 carriers but not in MCM8 carriers. Moreover, our case series indicates that beyond hypogonadism, biallelic MCM8 and MCM9 variants are associated with early-onset germ cell tumors (occurring before age 15). Tumors from MCM8/MCM9 variant carriers predominantly displayed clock-like mutational processes, without evidence of DNA repair deficiency-associated signatures. Collectively, our data indicate that biallelic MCM9 variants are associated with polyposis, gastric cancer, and early-onset CRC, while both biallelic MCM8 and MCM9 variants are linked to hypogonadism and the early development of germ cell tumors. These findings underscore the importance of including MCM8/MCM9 in diagnostic gene panels for certain clinical contexts and suggest that biallelic carriers may benefit from cancer surveillance.http://www.sciencedirect.com/science/article/pii/S2666247725000831MCM8MCM9Polyposisadenomatous polypsinheritable tumor syndromeearly-onset colorectal cancer
spellingShingle Noah C. Helderman
Ting Yang
Claire Palles
Diantha Terlouw
Hailiang Mei
Ruben H.P. Vorderman
Davy Cats
Marcos Díaz-Gay
Marjolijn C.J. Jongmans
Ashwin Ramdien
Irma van de Beek
Thomas F. Eleveld
Andrew Green
Frederik J. Hes
Marry M. van den Heuvel-Eibrink
Annelore Van Der Kelen
Sabine Kliesch
Roland P. Kuiper
Inge M.M. Lakeman
Lisa E.E.L.O. Lashley
Leendert H.J. Looijenga
Manon S. Oud
Johanna Steingröver
Yardena Tenenbaum-Rakover
Carli M. Tops
Frank Tüttelmann
Richarda M. de Voer
Dineke Westra
Margot J. Wyrwoll
Mariano Golubicki
Marina Antelo
Laia Bonjoch
Mariona Terradas
Laura Valle
Ludmil B. Alexandrov
Hans Morreau
Tom van Wezel
Sergi Castellví-Bel
Yael Goldberg
Maartje Nielsen
Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9
HGG Advances
MCM8
MCM9
Polyposis
adenomatous polyps
inheritable tumor syndrome
early-onset colorectal cancer
title Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9
title_full Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9
title_fullStr Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9
title_full_unstemmed Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9
title_short Clinical syndromes linked to biallelic germline variants in MCM8 and MCM9
title_sort clinical syndromes linked to biallelic germline variants in mcm8 and mcm9
topic MCM8
MCM9
Polyposis
adenomatous polyps
inheritable tumor syndrome
early-onset colorectal cancer
url http://www.sciencedirect.com/science/article/pii/S2666247725000831
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