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Conservation of Different Mechanisms of Hox Cluster Regulation Within Chordates

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Conservation of Different Mechanisms of Hox Cluster Regulation Within Chordates Conservation of different mechanisms of Hox cluster regulation within chordates Carlos Herrera Úbeda Aquesta tesi doctoral està subjecta a la llicència Reconeixement- NoComercial – CompartirIgual 4.0. Espanya de Creative Commons. Esta tesis doctoral está sujeta a la licencia Reconocimiento - NoComercial – CompartirIgual 4.0. España de Creative Commons. This doctoral thesis is licensed under the Creative Commons Attribution-NonCommercial- ShareAlike 4.0. Spain License. PHD THESIS 2019 CONSERVATION OF DIFFERENT MECHANISMS OF HOX CLUSTER REGULATION WITHIN CHORDATES CARLOS HERRERA ÚBEDA PHD THESIS 2019 CARLOS HERRERA ÚBEDA Departamento de Genética, Microbiología y Estadística Programa de Doctorado de Genetica 2019 Tesis Doctoral presentada por Carlos Herrera Úbeda bajo el título Conservation of different mechanisms of Hox cluster regulation within chordates para optar al titulo de doctor por la Universitat de Barcelona Firmado, el doctorando Firmado, el Director, responsable asimismo de la tutela de la tesis Jordi Garcia Fernàndez Barcelona, 27 de Septiembre de 2019 We are LEGIONX David Haller Summary 1 Acknowledgements 3 Introduction 9 1. Evolution and development 9 1.1. Dawn of the Evo-Devo 9 1.2. Changes vs Conservation 9 1.3. Amphioxus 10 Overview 10 Development 12 Functional genomics 13 1.4. Xenopus tropicalis 14 1.5. Hox Cluster 15 1.6. ParaHox Cluster 17 2. Long non-coding RNAs 19 2.1. Overview of lncRNAs 19 History 19 Origin and characteristics of lncRNAs 21 Evolution of lncRNAs 22 Classification 23 Challenges 24 2.2. Hotairm1 (HOX antisense intergenic RNA myeloid 1) 25 Overview 25 Mechanism of Hotairm1 26 Objectives 33 Results 37 Article RI 39 Article RII 67 Article RIII 83 Discussion 137 1. Expanding the tools for understanding Evolution 137 2. Conserved lincRNAs within Chordata 138 2.1. lncRNA fraction in amphioxus 138 2.2. Novelty of the LincOFinder pipeline 138 2.3. Origins of Hotairm1 140 2.4. Conservation on the expression between frog and lancelet Hotairm1 141 2.5. Conservation of the mechanism of function between frog and human Hotairm1 143 2.6. Conservation of Hotairm1 across Chordata 144 3. Conserved regulation of Hox Cluster in Chordata 146 3.1. Analysis of Pdx and Cdx knockouts during development 146 3.2. Gut-enrichment in both datasets 147 3.3. Conservation of the anterior and middle Hox cluster regulation via Cdx 148 Conclusions 153 Annexes 157 Article AI 157 Article AII 173 Summary In this thesis we have covered the importance of finding underlying conservation events to better understand the regulatory mechanisms of important development orchestrators like the Hox cluster. As an example of these non-evident conservation, we have shown two cases, as described below. The first case studied, after developing a software able to detect homologous long noncoding RNAs by means of microsynteny analyses, is the conservation of Hotairm1 in Chordata. For assessing the homology of this lncRNA, first we had to identify the lncRNA fraction within the B. lanceolatum transcriptome. With a reliable lincRNA dataset, we used our pipeline, LincOFinder, to identify orthologs between human and amphioxus through microsynteny. After the identification of Hotairm1 as one of the lincRNAs with conserved microsynteny, we used Xenopus as a proxy to analyse the homologies in the expression and the function. We had to proceed this way due to the difficulties associated with the inhibition of genes in B. lanceolatum, and the unavailability of expression patterns for Hotairm1 in the bibliography. After we successfully characterised Hotairm1 expression in amphioxus and Xenopus, we injected morpholino oligonucleotides to target and inhibit the splicing of Hotairm1 to promote an isoform imbalance. Through the phenotype obtained and the performing of qPCRs, we were able to deduct the mechanism of Hotairm1 and successfully relate this mechanism with the one described in human cells. With all the data obtained we were able to strongly suggest that the amphioxus Hotairm1 is homologous to the Xenopus and human Hotairm1, thus being conserved in most of the lineages within chordates. The second case studied was the conservation of the regulation of the Hox cluster mediated by Cdx. When analysing the B. floridae knockouts of Cdx and Pdx obtained using the TALEN technique, we found a severe phenotype of the developing larvae in Cdx-/- and a mild phenotype in Pdx-/-. The Cdx-/- phenotype consisted in the disruption of posterior gut development, as well as an underdevelopment of the postanal tail, coupled with a non-opening anus. When looking at changes in the expression of the Hox cluster in this Cdx-/- embryos, we found collinear misregulation of the expressed Hox genes, with the most anterior Hox cluster genes upregulated, and the most posterior ones downregulated. This is very similar to findings seen in triple morpholino knockdowns of the Cdx genes in Xenopus, indicating that in both, Xenopus and amphioxus, Cdx is regulating the Hox cluster through a homologous mechanism. 1 Acknowledgements Bueno, llego el mejor momento de escribir la tesis, el de dar las gracias. Siempre me gusta leer los agradecimientos de las tesis que ojeo, porque es como mirar una foto hecha de palabras del momento en el que se escribió. Así que espero sacar a todo el que pueda en mi foto, y si alguien que esperaba salir no se encuentra, será porque se me ha quedado el cerebro frito. Voy a seguir un orden tan organizado como yo, así que será totalmente aleatorio. Eso si, empezare por mi familia. En general ya sabéis que os quiero, y que sin vosotros no habría podido hacer la tesis bliblablu, pero hay cosas que son dignas de reseñar. Como por ejemplo tus visitas brother, que aun siendo yo el peor organizador de planes del mundo sigues haciendo de tanto en tanto y que me encantan. También las tuyas sister (y Edu) que, aunque menos habituales, siempre acaban incluyendo un room escape, o un laser tag, o un apartamento con extrañas habitaciones en Badalona… lo típico. También me gustaría agradecer aquí las discusiones (de lo que sea) que tengo contigo mamá, que me obligan a estar siempre rápido de mente, y que cuando me aburra en el larguiiiisimo viaje de 15 minutos de vuelta a casa, estés en el teléfono. A ti papá te debo mi pasión por los videojuegos, por los ordenadores y por la tecnología en general, pero mas que por todo eso (que no es poco) quiero darte las gracias por enseñarme que prácticamente todo tiene arreglo si le dedicas el tiempo y la energía suficiente y que desmontar algo es la mejor manera de aprender como funciona. Lo dicho, os quiero, incluida a ti Blanca (no prima, tu vas luego) que aunque aun no has nacido y tardaras bastante en poder leer esto quiero que sepas que tu tío pensaba mucho en ti durante su tesis. Blanca (ahora si primi), gracias por tu sonrisa y por encontrarte conmigo en Mallorca; Pablo, gracias por tu humor negro, siempre consigues hacerme reir. Al resto de mi familia, sois demasiados para poneros a todos, pero sabéis que os quiero y que me encanta veros cuando voy de visita. Pondría mas cosas, pero no es plan de hacer unos agradecimientos mas largos que la Introducción no? Ahora toca el turno a la gente del lab. Bea, tu primero. Gracias por haberme enseñado desde que entre en el lab a hacer las cosas bien. No solo en ciencia, sino en la vida en general. Mother of volumes, sexadora de amphioxus, la que no deja que el laboratorio arda, gracias por todo. Kike, gracias por… esto… tu… un dia me hiciste un café! XD obviamente es broma gil, gracias por todas las discusiones que hemos tenido, sobre moral, economía, política y sobretodo ciencia y por las veces que me pones contra las cuerdas (dialécticamente, aquel pulso lo gane yo). Solo por haber aguantado todas las canciones que he hecho con la palabra “Kika”, te has ganado un rinconcito de cielo. Ari ari adnaaaaa!! Te toca. El lab esh un lugar mash aburrido deshde que te fuishte… Graciash por las cancionesh de frozen, las nochesh eshcribiendo el master y no she, por ti, en general ashin a lo loco. Aina, para tu els agraïments seran en català. Ets la persona que mes m’ha fet voler parlar-lo bé. Gracies per el “sexi com tu”, per acollir-me en Cambridge i per la connexion mental absoluta. Et trobo a faltar moltíssim i a més ja ningú li demana a Kika si es feliç. Coral, obviamente gracias por peluquerias Coral, y bueno por Coral Industries en general. Y por los masajes! El próximo me lo das en Ámsterdam no? Vero, ahora que me acerco al final de la tesis puedo decir que esto si que es la gloria. Miquel, a ti gracias por toda la cencia y las conversaciones del brujo (y sus cartas). Eudi, shaval, para ti me faltan palabras. Gracias por confiar en mi para tus proyectos, ya sean cienteficos o científicos. Esto se acaba, y no se me ocurre mejor persona junto a quien acabarlo. Mi compañero de las antípodas, let’s finish this! Al resto de gente del lab, ya sean del pasado (Maria, Demi, Nidia, Roser, Sara, Nieves, Sisco, Jose, Sheila, Jordi, Elena italiana, etc) o del presente (la otra Maria, Dani y Susana) gracias por haber compartido esto conmigo y no haberme estrangulado en el proceso. Kike no era el único que tenia que aguantar las Kika melodías. O frozen. O el hielo seco. El chiste de las patatas, etc, etc, ya me entendéis. Hacer la tesis aquí ha sido genial en gran parte por todos vosotros, asi que lo dicho, gracias. De los otros labs, las moscas, esos bichos tan majos, gracias a José por seguirme el ritmo silbando entre otras cosas, y a Qi por dejarse adoptar.
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