Genetic landscape of a large cohort of Primary Ovarian Insufficiency: New genes and pathways and implications for personalized medicine.

Meiosis/DNA repair genes Mitophagy NF-KB Personalized medicine Post - translational regulation Primary ovarian insufficiency

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Oct 2022
Historique:
received: 09 02 2022
revised: 17 08 2022
accepted: 19 08 2022
pubmed: 14 9 2022
medline: 19 10 2022
entrez: 13 9 2022
Statut: ppublish

Résumé

Primary Ovarian Insufficiency (POI), a public health problem, affects 1-3.7% of women under 40 yielding infertility and a shorter lifespan. Most causes are unknown. Recently, genetic causes were identified, mostly in single families. We studied an unprecedented large cohort of POI to unravel its molecular pathophysiology. 375 patients with 70 families were studied using targeted (88 genes) or whole exome sequencing with pathogenic/likely-pathogenic variant selection. Mitomycin-induced chromosome breakages were studied in patients' lymphocytes if necessary. A high-yield of 29.3% supports a clinical genetic diagnosis of POI. In addition, we found strong evidence of pathogenicity for nine genes not previously related to a Mendelian phenotype or POI: ELAVL2, NLRP11, CENPE, SPATA33, CCDC150, CCDC185, including DNA repair genes: C17orf53(HROB), HELQ, SWI5 yielding high chromosomal fragility. We confirmed the causal role of BRCA2, FANCM, BNC1, ERCC6, MSH4, BMPR1A, BMPR1B, BMPR2, ESR2, CAV1, SPIDR, RCBTB1 and ATG7 previously reported in isolated patients/families. In 8.5% of cases, POI is the only symptom of a multi-organ genetic disease. New pathways were identified: NF-kB, post-translational regulation, and mitophagy (mitochondrial autophagy), providing future therapeutic targets. Three new genes have been shown to affect the age of natural menopause supporting a genetic link. We have developed high-performance genetic diagnostic of POI, dissecting the molecular pathogenesis of POI and enabling personalized medicine to i) prevent/cure comorbidities for tumour/cancer susceptibility genes that could affect life-expectancy (37.4% of cases), or for genetically-revealed syndromic POI (8.5% of cases), ii) predict residual ovarian reserve (60.5% of cases). Genetic diagnosis could help to identify patients who may benefit from the promising in vitro activation-IVA technique in the near future, greatly improving its success in treating infertility. Université Paris Saclay, Agence Nationale de Biomédecine.

Sections du résumé

BACKGROUND BACKGROUND
Primary Ovarian Insufficiency (POI), a public health problem, affects 1-3.7% of women under 40 yielding infertility and a shorter lifespan. Most causes are unknown. Recently, genetic causes were identified, mostly in single families. We studied an unprecedented large cohort of POI to unravel its molecular pathophysiology.
METHODS METHODS
375 patients with 70 families were studied using targeted (88 genes) or whole exome sequencing with pathogenic/likely-pathogenic variant selection. Mitomycin-induced chromosome breakages were studied in patients' lymphocytes if necessary.
FINDINGS RESULTS
A high-yield of 29.3% supports a clinical genetic diagnosis of POI. In addition, we found strong evidence of pathogenicity for nine genes not previously related to a Mendelian phenotype or POI: ELAVL2, NLRP11, CENPE, SPATA33, CCDC150, CCDC185, including DNA repair genes: C17orf53(HROB), HELQ, SWI5 yielding high chromosomal fragility. We confirmed the causal role of BRCA2, FANCM, BNC1, ERCC6, MSH4, BMPR1A, BMPR1B, BMPR2, ESR2, CAV1, SPIDR, RCBTB1 and ATG7 previously reported in isolated patients/families. In 8.5% of cases, POI is the only symptom of a multi-organ genetic disease. New pathways were identified: NF-kB, post-translational regulation, and mitophagy (mitochondrial autophagy), providing future therapeutic targets. Three new genes have been shown to affect the age of natural menopause supporting a genetic link.
INTERPRETATION CONCLUSIONS
We have developed high-performance genetic diagnostic of POI, dissecting the molecular pathogenesis of POI and enabling personalized medicine to i) prevent/cure comorbidities for tumour/cancer susceptibility genes that could affect life-expectancy (37.4% of cases), or for genetically-revealed syndromic POI (8.5% of cases), ii) predict residual ovarian reserve (60.5% of cases). Genetic diagnosis could help to identify patients who may benefit from the promising in vitro activation-IVA technique in the near future, greatly improving its success in treating infertility.
FUNDING BACKGROUND
Université Paris Saclay, Agence Nationale de Biomédecine.

Identifiants

pubmed: 36099812
pii: S2352-3964(22)00428-5
doi: 10.1016/j.ebiom.2022.104246
pmc: PMC9475279
pii:
doi:

Substances chimiques

Mitomycins 0
NF-kappa B 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104246

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no conflict of interest.

Auteurs

Abdelkader Heddar (A)

Université Paris Saclay, Faculté de Médecine. Unité de Génétique Moléculaire des Maladies Métaboliques et de la Reproduction, Hôpital Bicêtre, Assistance Publique-Hôpitaux de Paris, AP-HP, Hôpitaux Universitaires Paris-Saclay, Le Kremlin-Bicêtre, France; UMR-S 1193, INSERM, Université Paris Saclay, Faculté de Médecine, Hôpital Paul Brousse, Villejuif, France.

Cagri Ogur (C)

Igenomix Turkey, İstanbul, Turkey; Institute of Science, Department of Bioengineering Yildiz Technical University, İstanbul, Turkey.

Sabrina Da Costa (S)

Service d'Endocrinologie Pédiatrique, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, CNR pathologies gynécologiques rares, 75015, Paris, France.

Inès Braham (I)

Service d'Endocrinologie et de Médicine de la Reproduction, Hôpital Universitaire de Nice, 06200, Nice, France.

Line Billaud-Rist (L)

Service d'Endocrinologie, Assistance Publique-Hôpitaux de Paris, Hôpital Cochin/Port-Royal, 75005, Paris, France.

Necati Findikli (N)

Bahçeci Umut IVF Centre, Altunizade, İstanbul, Turkey; Faculty of Engineering and Architecture, Department of Biomedical Engineering, Beykent University, İstanbul, Turkey.

Claire Beneteau (C)

Service de Génétique Médicale, Centre Hospitalier Universitaire Nantes, 44000, Nantes, France.

Rachel Reynaud (R)

Aix Marseille Université, Assistance-Publique des Hôpitaux de Marseille (AP-HM), Service de Pédiatrie multidisciplinaire Hôpital de la Timone Enfants, 13385, Marseille Cedex 05, France.

Khaled Mahmoud (K)

Centre FERTILLIA de Médecine de la Reproduction- Clinique la ROSE, Tunis, Tunisie.

Stéphanie Legrand (S)

Centre de Fertilité - Clinique de l'Atlantique La Rochelle, 17000, La Rochelle, France.

Maud Marchand (M)

Service d'Endocrinologie Pédiatrique, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, CNR pathologies gynécologiques rares, 75015, Paris, France.

Isabelle Cedrin-Durnerin (I)

Service de Médecine de la Reproduction et Préservation de la Fertilité, hôpital Jean-Verdier, Assistance Publique-Hôpitaux de Paris, 93143 Bondy, France.

Adèle Cantalloube (A)

Service de Gynécologie et d'Obstétrique, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris, AP-HP. Faculté de Médecine Pierre et Marie Curie. Université de la Sorbonne, Paris, France.

Maeliss Peigne (M)

Service de Médecine de la Reproduction et Préservation de la Fertilité, hôpital Jean-Verdier, Assistance Publique-Hôpitaux de Paris, 93143 Bondy, France.

Marion Bretault (M)

Service d'Endocrinologie, Hôpital Ambroise Paré, Assistance Publique-Hôpitaux de Paris, 92100, Boulogne Billancourt, France.

Benedicte Dagher-Hayeck (B)

Service de Médecine de la Reproduction et Préservation de la Fertilité, hôpital Jean-Verdier, Assistance Publique-Hôpitaux de Paris, 93143 Bondy, France.

Sandrine Perol (S)

Unité de gynécologie médicale, APHP, Hôpital Port-Royal Cochin, 27 Rue du Faubourg Saint-Jacques, Paris 75014, France.

Celine Droumaguet (C)

Service de Médecine Interne, Hôpital Henri-Mondor, Assistance Publique-Hôpitaux de Paris, 94000 Créteil, France.

Sabri Cavkaytar (S)

Bahçeci Umut IVF Centre, Altunizade, İstanbul, Turkey; Üsküdar University, Faculty of Medicine, Department of Obstetrics and Gynecology, İstanbul, Turkey.

Carole Nicolas-Bonne (C)

Service de Gynécologie et d'Obstétrique, Centre Hospitalier Alpes Léman, 74130, Contamine-Sur-Arve, France.

Hanen Elloumi (H)

Centre FERTILLIA de Médecine de la Reproduction- Clinique la ROSE, Tunis, Tunisie.

Mohamed Khrouf (M)

Centre FERTILLIA de Médecine de la Reproduction- Clinique la ROSE, Tunis, Tunisie.

Charlotte Rougier-LeMasle (C)

Service d'Endocrinologie et de Médicine de la Reproduction, Hôpital Universitaire de Nice, 06200, Nice, France.

Melanie Fradin (M)

Service de Génétique Clinique, Centre Hospitalier Universitaire de Rennes, Hôpital Sud, Univ Rennes, CNRS IGDR UMR 6290, Centre de référence Anomalies du développement CLAD-Ouest, ERN ITHACA, 35203, Rennes, France; Service de Génétique Médicale, Centre Hospitalier de Saint Brieuc, 22000, Saint-Brieuc, France.

Elsa Le Boette (E)

Service de Génétique Médicale, Centre Hospitalier de Saint Brieuc, 22000, Saint-Brieuc, France.

Perrine Luigi (P)

Service d'Endocrinologie-Diabétologie, Centre Hospitalier Antibes Juan Les Pins, 06600, Antibes, France.

Anne-Marie Guerrot (AM)

Normandie Univ, UNIROUEN, Inserm U1245, CHU Rouen, Department of Genetics and reference center for developmental disorders, FHU G4 Génomique, F-76000 Rouen, France.

Emmanuelle Ginglinger (E)

Service de Génétique, Centre Hospitalier de Mulhouse, 68100, Mulhouse, France.

Amandine Zampa (A)

Service de Génétique, Centre Hospitalier de Mulhouse, 68100, Mulhouse, France.

Anais Fauconnier (A)

Service d'Endocrinologie, Diabète et Maladies Métaboliques, Centre Hospitalier Universitaire de Saint-Etienne, 42270, Saint-Priest-en-Jarez, France.

Nathalie Auger (N)

Service de génétique des tumeurs. Institut Gustave Roussy, 94805, Villejuif, France.

Françoise Paris (F)

Département de Pédiatrie, Unité d'Endocrinologie-Gynécologie Pédiatrique, Hôpital A.-de-Villeneuve, Centre Hospitalier Universitaire Montpellier et Université Montpellier, 34090, Montpellier, France; Constitutif Sud, Centre de Référence Maladies Rares du Développement Génital, Hôpital Lapeyronie, Centre Hospitalier Universitaire Montpellier, Université de Montpellier, 34090 Montpellier, France; INSERM 1203, Développement Embryonnaire Fertilité Environnement, Université de Montpellier, 34090, Montpellier, France.

Elise Brischoux-Boucher (E)

Centre de Génétique Humaine, Université de Franche-Comté, Centre Hospitalier Universitaire de Besançon, 25000, Besançon, France.

Christelle Cabrol (C)

Centre de Génétique Humaine, Université de Franche-Comté, Centre Hospitalier Universitaire de Besançon, 25000, Besançon, France.

Aurore Brun (A)

Service de Génétique, Centre Hospitalier Universitaire de Poitiers, Université de Poitiers, 86021, Poitiers, France.

Laura Guyon (L)

Service de Génétique Médicale, Centre Hospitalier Universitaire Nantes, 44000, Nantes, France.

Melanie Berard (M)

Service de Génétique Clinique, Centre Hospitalier Régional Universitaire de Nancy, F-54000, Nancy, France.

Axelle Riviere (A)

Service de Génétique Clinique, Centre Hospitalier Régional Universitaire de Nancy, F-54000, Nancy, France.

Nicolas Gruchy (N)

Normandy University, UNICAEN, Caen University Hospital, Department of Genetics, EA 7450 BioTARGen, FHU G4 Genomics, Caen, France.

Sylvie Odent (S)

Service de Génétique Clinique, Centre Hospitalier Universitaire de Rennes, Hôpital Sud, Univ Rennes, CNRS IGDR UMR 6290, Centre de référence Anomalies du développement CLAD-Ouest, ERN ITHACA, 35203, Rennes, France.

Brigitte Gilbert-Dussardier (B)

Service de Génétique, Centre Hospitalier Universitaire de Poitiers, Université de Poitiers, 86021, Poitiers, France.

Bertrand Isidor (B)

Service de Génétique Médicale, Centre Hospitalier Universitaire Nantes, 44000, Nantes, France.

Juliette Piard (J)

Centre de Génétique Humaine, Université de Franche-Comté, Centre Hospitalier Universitaire de Besançon, 25000, Besançon, France.

Laetitia Lambert (L)

Service de Génétique Clinique, Centre Hospitalier Régional Universitaire de Nancy, F-54000, Nancy, France.

Samir Hamamah (S)

INSERM 1203, Développement Embryonnaire Fertilité Environnement, Université de Montpellier, 34090, Montpellier, France; Centre Hospitalier Universitaire de Montpellier, Département de Biologie de la Reproduction, Biologie de la Reproduction/DPI et CECOS, Université de Montpellier, Montpellier, France.

Anne Marie Guedj (AM)

Service d'Endocrinologie et de Maladies Métaboliques, Centre Hospitalier Universitaire Nîmes, Université de Montpellier, 30029, Nîmes, France.

Aude Brac de la Perriere (A)

Fédération d'Endocrinologie, Centre de Référence des Maladies Rares du Développement Génital, Groupement Hospitalier Est, Hôpital Louis Pradel, 69002, Lyon, France.

Hervé Fernandez (H)

Service de Gynecologie et d'Obstétrique, Assistance Publique-Hôpitaux de Paris, Hôpital Bicêtre, Faculté de médicine, Université Paris-Saclay, 94270 Le Kremlin Bicêtre, France; UVSQ, Inserm, CESP, Université Paris-Saclay, 94807 Villejuif, France.

Marie-Laure Raffin-Sanson (ML)

Service d'Endocrinologie, Hôpital Ambroise Paré, Assistance Publique-Hôpitaux de Paris, 92100, Boulogne Billancourt, France.

Michel Polak (M)

Service d'Endocrinologie Pédiatrique, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris, CNR pathologies gynécologiques rares, 75015, Paris, France.

Hélène Letur (H)

Service de Gynécologie Obstétrique et Médecine de la Reproduction, Hôpital Foch, 40 rue Worth 92 150 Suresnes, France; Service de Médecine de la Reproduction et Préservation de la Fertilité, Polyclinique de Navarre, 8, boulevard Hauterive, 64000 Pau, France.

Sylvie Epelboin (S)

Service de Gynécologie et d'Obstétrique, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris, AP-HP. Faculté de Médecine Pierre et Marie Curie. Université de la Sorbonne, Paris, France.

Genevieve Plu-Bureau (G)

Unité de gynécologie médicale, APHP, Hôpital Port-Royal Cochin, 27 Rue du Faubourg Saint-Jacques, Paris 75014, France.

Sławomir Wołczyński (S)

Department of Reproduction and Gynecological Endocrinology, Medical University of Bialystok, Bialystok, Poland.

Sylvie Hieronimus (S)

Service d'Endocrinologie et de Médicine de la Reproduction, Hôpital Universitaire de Nice, 06200, Nice, France.

Kristiina Aittomaki (K)

Department of Clinical Genetics, Helsinki University Hospital, University of Helsinki, Helsinki, Finland.

Sophie Catteau-Jonard (S)

Service de gynécologie médicale, orthogénie et sexologie, Centre Hospitalier Universitaire de Lille, Université de Lille, 59000 Lille, France.

Micheline Misrahi (M)

Université Paris Saclay, Faculté de Médecine. Unité de Génétique Moléculaire des Maladies Métaboliques et de la Reproduction, Hôpital Bicêtre, Assistance Publique-Hôpitaux de Paris, AP-HP, Hôpitaux Universitaires Paris-Saclay, Le Kremlin-Bicêtre, France; UMR-S 1193, INSERM, Université Paris Saclay, Faculté de Médecine, Hôpital Paul Brousse, Villejuif, France. Electronic address: micheline.misrahi@aphp.fr.

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