Dominant variants in major spliceosome U4 and U5 small nuclear RNA genes cause neurodevelopmental disorders through splicing disruption

Caroline Nava*, Benjamin Cogne, Amandine Santini, Elsa Leitão, François Lecoquierre, Yuyang Chen, Sarah L. Stenton, Thomas Besnard, Solveig Heide, Sarah Baer, Abhilasha Jakhar, Sonja Neuser, Boris Keren, Anne Faudet, Sylvie Forlani, Marie Faoucher, Kevin Uguen, Konrad Platzer, Alexandra Afenjar, Jean Luc AlessandriStephanie Andres, Chloé Angelini, Bernard Aral, Benoit Arveiler, Tania Attie-Bitach, Marion Aubert Mucca, Guillaume Banneau, Tahsin Stefan Barakat, Giulia Barcia, Stéphanie Baulac, Claire Beneteau, Fouzia Benkerdou, Virginie Bernard, Stéphane Bézieau, Dominique Bonneau, Marie Noelle Bonnet-Dupeyron, Simon Boussion, Odile Boute, Elise Brischoux-Boucher, Samantha J. Bryen, Julien Buratti, Tiffany Busa, Almuth Caliebe, Yline Capri, Kévin Cassinari, Roseline Caumes, Camille Cenni, Pascal Chambon, Perrine Charles, John Christodoulou, Cindy Colson, Solène Conrad, Auriane Cospain, Juliette Coursimault, Thomas Courtin, Madeline Couse, Charles Coutton, Isabelle Creveaux, Alissa M. D’Gama, Benjamin Dauriat, Jean Madeleine de Sainte Agathe, Giulia Del Gobbo, Andrée Delahaye-Duriez, Julian Delanne, Anne Sophie Denommé-Pichon, Anne Dieux-Coeslier, Laura Do Souto Ferreira, Martine Doco-Fenzy, Stephan Drukewitz, Véronique Duboc, Christèle Dubourg, Yannis Duffourd, David Dyment, Salima El Chehadeh, Monique Elmaleh, Laurence Faivre, Samuel Fennelly, Hanna Fischer, Mélanie Fradin, Camille Galludec Vaillant, Benjamin Ganne, Jamal Ghoumid, Himanshu Goel, Zeynep Gokce-Samar, Alice Goldenberg, Romain Gonfreville Robert, Svetlana Gorokhova, Louise Goujon, Victoria Granier, Mathilde Gras, John M. Greally, Bianca Greiten, Paul Gueguen, Anne Marie Guerrot, Saurav Guha, Anne Guimier, Tobias B. Haack, Hamza Hadj Abdallah, Yosra Halleb, Radu Harbuz, Madeleine Harris, Julia Hentschel, Bénédicte Héron, Marc Phillip Hitz, A. Micheil Innes, Vincent Jadas, Louis Januel, Nolwenn Jean-Marçais, Vaidehi Jobanputra, Florence Jobic, Ludmila Jornea, Céline Jost, Sophie Julia, Frank J. Kaiser, Daniel Kaschta, Sabine Kaya, Petra Ketteler, Bochra Khadija, Fabian Kilpert, Cordula Knopp, Florian Kraft, Ilona Krey, Marilyn Lackmy, Fanny Laffargue, Laetitia Lambert, Ryan Lamont, Vincent Laugel, Steven Laurie, Julie L. Lauzon, Louis Lebreton, Marine Lebrun, Marine Legendre, Eric Leguern, Daphné Lehalle, Elodie Lejeune, Gaetan Lesca, Marion Lesieur-Sebellin, Jonathan Levy, Agnès Linglart, Stanislas Lyonnet, Kevin Lüthy, Alan S. Ma, Corinne Mach, Jean Louis Mandel, Lamisse Mansour-Hendili, Julien Marcadier, Victor Marin, Henri Margot, Valentine Marquet, Angèle May, Johannes A. Mayr, Catherine Meridda, Vincent Michaud, Caroline Michot, Gwenael Nadeau, Sophie Naudion, Laetitia Nguyen, Mathilde Nizon, Frédérique Nowak, Sylvie Odent, Valerie Olin, Ikeoluwa A. Osei-Owusu, Matthew Osmond, Katrin Õunap, Laurent Pasquier, Sandrine Passemard, Melissa Pauly, Olivier Patat, Marine Pensec, Laurence Perrin-Sabourin, Florence Petit, Christophe Philippe, Marc Planes, Annapurna Poduri, Céline Poirsier, Antoine Pouzet, Bradley Prince, Clément Prouteau, Aurora Pujol, Caroline Racine, Mélanie Rama, Francis Ramond, Kara Ranguin, Margaux Raway, André Reis, Mathilde Renaud, Nicole Revencu, Anne Claire Richard, Lucile Riera-Navarro, Rocio Rius, Diana Rodriguez, Agustí Rodriguez-Palmero, Sophie Rondeau, Annika Roser-Unruh, Christelle Rougeot Jung, Hana Safraou, Véronique Satre, Pascale Saugier-Veber, Clément Sauvestre, Elise Schaefer, Wanqing Shao, Ina Schanze, Jan Ulrich Schlump, Agatha Schlüter Martin, Caroline Schluth-Bolard, Sarah Schuhmann, Christopher Schröder, Monisha Sebastin, Sabine Sigaudy, Malte Spielmann, Marta Spodenkiewicz, Laura St Clair, Julie Steffann, Radka Stoeva, Harald Surowy, Mark A. Tarnopolsky, Calina Todosi, Annick Toutain, Frédéric Tran Mau-Them, Astrid Unterlauft, Julien Van-Gils, Clémence Vanlerberghe, Georgia Vasileiou, Gabriella Vera, André Verdel, Alain Verloes, Yoann Vial, Cédric Vignal, Marie Vincent, Catherine Vincent-Delorme, Aline Vincent-Devulder, Antonio Vitobello, Sacha Weber, Marjolaine Willems, Khaoula Zaafrane-Khachnaoui, Pia Zacher, Lena Zeltner, Alban Ziegler, Wojciech P. Galej, Hélène Dollfus, Christel Thauvin, Kym M. Boycott, Pierre Marijon, Alban Lermine, Valérie Malan, Marlène Rio, Alma Kuechler, Bertrand Isidor, Séverine Drunat, Thomas Smol, Nicolas Chatron, Amélie Piton, Gael Nicolas, Matias Wagner, Rami Abou Jamra, Delphine Héron, Cyril Mignot, Pierre Blanc, Anne O’Donnell-Luria, Nicola Whiffin, Camille Charbonnier, Clément Charenton, Julien Thevenon, Christel Depienne*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

3 Citations (Scopus)
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Abstract

The major spliceosome contains five small nuclear RNAs (snRNAs; U1, U2, U4, U5 and U6) essential for splicing. Variants in RNU4-2, encoding U4, cause a neurodevelopmental disorder called ReNU syndrome. We investigated de novo variants in 50 snRNA-encoding genes in a French cohort of 23,649 individuals with rare disorders and gathered additional cases through international collaborations. Altogether, we identified 145 previously unreported probands with (likely) pathogenic variants in RNU4-2 and 21 individuals with de novo and/or recurrent variants in RNU5B-1 and RNU5A-1, encoding U5. Pathogenic variants typically arose de novo on the maternal allele and cluster in regions critical for splicing. RNU4-2 variants mainly localize to two structures, the stem III and T-loop/quasi-pseudoknot, which position the U6 ACAGAGA box for 5′ splice site recognition and associate with different phenotypic severity. RNU4-2 variants result in specific defects in alternative 5′ splice site usage and methylation patterns (episignatures) that correlate with variant location and clinical severity. This study establishes RNU5B-1 as a neurodevelopmental disorder gene, suggests RNU5A-1 as a strong candidate and highlights the role of de novo variants in snRNAs.

Original languageEnglish
Pages (from-to)1374-1388
Number of pages15
JournalNature Genetics
Volume57
Issue number6
DOIs
Publication statusPublished - Jun 2025

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