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Exploring the Structural and Functional Dynamics of the X-Inactivation Centre Locus During Development Rafael Galupa

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Exploring the Structural and Functional Dynamics of the X-Inactivation Centre Locus During Development Rafael Galupa Exploring the structural and functional dynamics of the X-inactivation centre locus during development Rafael Galupa To cite this version: Rafael Galupa. Exploring the structural and functional dynamics of the X-inactivation centre lo- cus during development. Genetics. Université Paris Saclay (COmUE), 2017. English. NNT : 2017SACLS305. tel-02724642 HAL Id: tel-02724642 https://tel.archives-ouvertes.fr/tel-02724642 Submitted on 2 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. NNT : 2017SACLS305 THESE DE DOCTORAT DE L’UNIVERSITE PARIS-SACLAY PREPAREE A L’UNIVERSITE PARIS-SUD ECOLE DOCTORALE N° 577 Structure et Dynamique des Systèmes Vivants (SDSV) Spécialité de doctorat : Sciences de la vie et de la santé Par Rafael MARTINS GALUPA Exploring the structural and functional dynamics of the X-inactivation centre locus during development Thèse présentée et soutenue à l’Institut Curie, Paris, le 19 septembre 2017 : Composition du Jury : Pr. Pierre CAPY Professeur à l’Université Paris-Sud Président Dr. Angela TADDEI Directrice de Recherche CNRS à l’Institut Curie Rapportrice Pr. Reiner VEITIA Professeur à l’Université Paris Diderot Rapporteur Pr. Carolyn J. BROWN Professeure à l’Université de la Colombie-Britannique Examinatrice Pr. Denis DUBOULE Professeur à l’École Polytechnique Fédérale de Lausanne Examinateur Pr. Edith HEARD Professeure au Collège de France Directrice de thèse Ad astra per aspera Luca’s prayer while we were doing 3C together, following the ‘old’ protocol. 3 4 (…) Em cada célula do homem estão inscritas A cor dos olhos e a argúcia do olhar O desenho dos ossos e o contorno da boca Por isso te olhas ao espelho: E no espelho te buscas para te reconhecer Porém em cada célula desde o início Foi inscrito o signo veemente da tua liberdade Pois foste criado e tens de ser real Por isso não percas nunca teu fervor mais austero Tua exigência de ti e por entre Espelhos deformantes e desastres e desvios Nem um momento só podes perder A linha musical do encantamento Que é teu sol tua luz teu alimento Sophia de Mello Breyner Andresen in O Búzio de Cós e outros poemas 5 6 In the maturing germ cells of the fire wasp Pyrrhocoris, Hermann Henking noted a deeply staining chromatin body which persisted throughout most of the first meiotic division. At anaphase of the second meiotic division there was a small “chromatin element” (which Henking designated “X”) which, unlike the other chromosomes, did not appear to be double. This body went to one of the poles without dividing, lagging behind the other chromosomes, and led to the production of daughter cells with eleven and twelve chromosomes, respectively. Similar observations were subsequently made by other workers, but it was not until 1903 that the extra “chromatin element” was identified as a sex chromosome. "Henking, Hermann" Complete Dictionary of Scientific Biography Encyclopedia.com (July 9, 2017) 7 8 TABLE OF CONTENTS RÉSUMÉ (in French) ----------------------------------------------------------------------- 11 SUMMARY --------------------------------------------------------------------------------- 13 ACKNOWLEDGEMENTS --------------------------------------------------------------------- 15 INTRODUCTION ------------------------------------------------------------------------- 17 Prologue: the paradigm of the X-inactivation centre ------------------------------------ 19 Review 1: X-chromosome inactivation: new insights into cis and trans regulation (review published in Current Opinion in Genetics & Development, 2015) -------------- 29 Review 2: Chromatin architecture and gene regulation during X-chromosome inactivation (review in preparation for Annual Review of Genetics, 2018) -------------- 31 Review 3: From promoters and enhancers to TADs and regulatory landscapes across development, disease and evolution (unpublished review) ----------------------------- 51 RESULTS ---------------------------------------------------------------------------------- 71 Article 1: Predictive polymer modelling reveals coupled fluctuations in chromosome conformation and transcription (published in Cell, 2014) ------------------------------- 77 Article 2: Evidence for cross-TAD communication during X-inactivation via the noncoding Linx locus (manuscript in preparation) -------------------------------------- 79 Article 3: Genetic dissection of TAD organisation and function at the X-inactivation centre (manuscript in preparation) ------------------------------------------------------- 81 Methods for Article 2 and Article 3 ------------------------------------------------------ 83 DISCUSSION & PERSPECTIVES ------------------------------------------------------- 87 REFERENCES ----------------------------------------------------------------------------- 97 APPENDICES --------------------------------------------------------------------------- 123 Supplementary Results ------------------------------------------------------------------ 125 Article 4: Xist-dependent imprinted X inactivation and the early developmental consequences of its failure (published in Nat Struct Mol Biol, 2017) ------------------ 127 9 10 RÉSUMÉ Exploration de la dynamique fonctionnelle de l’architecture du locus Xic lors du développement La régulation de l’expression génique chez les mammifères dépend de l’organisation tridimensionnelle des chromosomes, en particulier à l’échelle des communications entre les séquences régulatrices et leurs promoteurs cibles. Ainsi, les chromosomes sont organisés en une nouvelle architecture consistant en domaines d’interactions topologiques (TADs, acronyme anglais). Mon projet de thèse avait pour but de caractériser les mécanismes moléculaires impliqués dans cette architecture et leurs importances au cours du développement embryonnaire, pour un locus bien particulier, le Xic (acronyme anglais pour X-inactivation centre). Le Xic contient les éléments régulateurs nécessaires pour initier l’inactivation du chromosome X (ICX), un phénomène épigénétique spécifique du développement des mammifères femelles, rendant l’un des deux chromosomes X inactif du point de vue transcriptionnelle. L’ICX permet d’égaliser l’expression des gènes liés au X entre les sexes chez les mammifères. Le Xic est organisé au moins en deux TADs mais une partie du locus reste encore non identifiée. Je présente ici une analyse fonctionnelle approfondie des différents éléments régulateurs au sein du Xic, comprenant des enhancers, des gènes d’ARNs non codants et des éléments structurels. Après avoir créé une série d’allèles mutés chez la souris et les cellules souches embryonnaires murines, j’ai caractérisé l’impact de ces réarrangements génomiques sur le paysage structurel et transcriptionnel du Xic. J’ai identifié des nouveaux acteurs dans la régulation de ce locus, en particulier des séquences régulatrices conservées chez les mammifères placentaires et des éléments structurels importants pour la formation d’une frontière entre les deux TADs du Xic, importante pour leur séparation et régulation. Je décris aussi la découverte de communication entre ces TADs, ce qui constitue un mécanisme inédit de régulation génique pendant le développement. Ce travail contribue à un nouveau niveau de compréhension des lois qui régissent l’organisation des TADs dans le contexte de la régulation génique chez les mammifères. 11 LONG RÉSUMÉ Exploration de la dynamique fonctionnelle de l’architecture du locus Xic lors du développement INTRODUCTION Chez les génomes des mammifères, la communication en cis entre les promoteurs des gènes et leurs séquences régulatrices, comme les éléments distales et proximales dits « enhancers », est essentielle pour une mise en place correcte des patrons d’expression génique au cours du développement embryonnaire (Long et al, 2016). Il est très probable que ces évènements régulateurs soient aidés par des interactions physiques entre les gènes et les enhancers. Ces interactions se passeraient par des repliements des chromosomes de l’ordre de 100kb-1Mb. À cette échelle, les chromosomes sont organisés dans des domaines d’interactions topologiques (TADs, acronyme anglais) (Dixon et al, 2012 ; Nora et al, 2012). De nombreuses études supportent l’idée que les TADs fournissent une base structurelle pour les paysages régulateurs des gènes, non seulement en permettant que promoteurs et enhancers s’associent plus fréquemment même sur de grandes distances génomiques , mais aussi en prévenant des interactions ectopiques et délétères. Un exemple classique d’un paysage régulateur important au cours du développement embryonnaire est celui du gène Xist, qui produit le large ARN non-codant (lncRNA, acronyme anglais) impliqué dans l’inactivation du chromosome X (ICX) chez les mammifères placentaires (pour revue, Galupa and Heard, 2015). L’ICX est un phénomène épigénétique spécifique du développement des mammifères femelles, qui rend l’un des deux chromosomes X inactif du point de vue transcriptionel, permettant d’égaliser l’expression des gènes liés à l’X entre les sexes. Les cellules souches embryonnaires murines (mESC, acronyme anglais)
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