Genome-wide screening reveals the genetic basis of mammalian embryonic eye development

Author:

Chee Justine M.,Lanoue Louise,Clary Dave,Higgins Kendall,Bower Lynette,Flenniken Ann,Guo Ruolin,Adams David J.,Bosch Fatima,Braun Robert E.,Brown Steve D. M.,Chin H.-J. Genie,Dickinson Mary E.,Hsu Chih-Wei,Dobbie Michael,Gao Xiang,Galande Sanjeev,Grobler Anne,Heaney Jason D.,Herault Yann,de Angelis Martin Hrabe,Mammano Fabio,Nutter Lauryl M. J.,Parkinson Helen,Qin Chuan,Shiroishi Toshi,Sedlacek Radislav,Seong J-K,Xu Ying,Ackert-Bicknell Cheryl,Adams Douglas,Adoum Anne-Tounsia,Aguilar-Pimentel Juan A.,Akoma Uchechukwu,Ali-Hadji Dalila,Amarie Oana V.,André Philippe,Auburtin Aurelie,Bam’Hamed Chaouki,Beckers Johannes,Beig Joachim,Berberovic Zorana,Bezginov Alexandr,Birling Marie-Christine,Boroviak Katharina,Bottomley Joanna,Bürger Antje,Busch Dirk H.,Butterfield Natalie C.,Cacheiro Pilar,Calzada-Wack Julia,Cambridge Emma L.,Camilleri Susan,Champy Marie-France,Cater Heather,Charles Philippe,Chesler Elissa J.,Cho Yi-Li,Christiansen Audrey E.,Cipriani Valentina,Cockle Nicola,Codner Gemma,Creighton Amie,Cruz Maribelle,Curry Katharine F.,D’Souza Abigail,Danisment Ozge,Delbarre Daniel,Dewhurst Hannah F.,Doe Brendan,Dorr Alex,Giesert Florian,Duddy Graham,Duffin Kyle,El Amri Amal,Elrick Hillary,Eskandarian Mohammad,Fray Martin,Frost Anthony,Fuchs Helmut,Gailus-Durner Valerie,Gampe Karen K.,Ganguly Milan,Gannon David,Garrett Lillian,Gertsenstein Marina,Gleeson Diane,Goodwin Leslie,Graw Jochen,Grimsrud Kristin,Haselimashhadi Hamed,Hobson Liane,Hörlein Andreas,Hölter Sabine M.,Hong Seung-Hyun,Horner Neil,Trainor Amanda G.,Huang Ziyue,Kane Coleen,Katsman Yulia,Keith Lance C.,Kelsey Lois,Kenyon Janet,King Ruairidh,Keskivali-Bond Piia,Kirton Andrea,Klein-Rodewald Tanja,Klopstock Thomas,Komla-Ebri Davide,Konopka Tomasz,Kühn Ralf,Kussy Fiona,Lafont David,Lan Qing,Lanza Denise G.,Laurin Valerie,Le Marchand Elise,Leblanc Sophie,Leitch Victoria D.,Lelliott Chris,Lengger Christoph,Lintott Lauri,Logan John G.,Lorenzo Isabel,Mallon Ann-Marie,Mannan Naila S.,Marschall Susan,McElwee Melissa L.,Mckay Matthew,McLaren-Jones Robbie S. B.,Mason Jeremy,Meehan Terrence F.,Miller David,Moore Michayla,Munoz-Fuentes Violeta,Murray Stephen A.,Nguyen-Bresinsky Dong,Oritz Oskar,Pandis Panos,Parlog Alexandru,Patel Amit,Pavlovic Guillaume,Pereira Monica,Peterson Kevin,Philip Vivek,Pollard Andrea S.,Prochazka Jan,Qu Dawei,Ramirez Ayexa,Rangarajan Sean,Rasmussen Tara L.,Rathkolb Birgit,Relac Mike,Roberton Kyle,Roper Willson,Rousseau Stéphane,Rowe David W.,Rozman Jan,Ryan Jennifer,Ryder Edward J.,Santos Luis,Sanz-Moreno Adrián,Schick Joel,Seavey Zachary,Seavitt John R.,Seisenberger Claudia,Selloum Mohammed,Shang Xueyuan,Shin Dong-Guk,Simon Michelle,Sleep Gillian,Smedley Damian,Sorg Tania,Sparkes Penny C.,Spielmann Nadine,Steinkamp Ralph,Stewart Michelle,Stoeger Claudia,Straiton Ewan,Svenson Karen L.,Swash Holly,Teboul Lydia,Tondat Sandra,Treise Irina,Tudor Catherine,Urban Rachel,Vancollie Valerie E.,Vasseur Laurent,Vukobradovic Igor,Wardle-Jones Hannah,Warren Jonathan,Wattenhofer-Donze Marie,Wells Sara E.,White Jacqueline K.,Wiegand Jean-Paul,Willett Amelia,Witmeyer Catherine,Wolf Eckhard,Wong Leeyean,Wood Joshua,Wurst Wolfgang,Xu Catherine,Zimprich Annemarie,Brooks Brian,McKerlie Colin,Lloyd K. C. Kent,Westerberg Henrik,Moshiri Ala,

Abstract

AbstractBackgroundMicrophthalmia, anophthalmia, and coloboma (MAC) spectrum disease encompasses a group of eye malformations which play a role in childhood visual impairment. Although the predominant cause of eye malformations is known to be heritable in nature, with 80% of cases displaying loss-of-function mutations in the ocular developmental genes OTX2 or SOX2, the genetic abnormalities underlying the remaining cases of MAC are incompletely understood. This study intended to identify the novel genes and pathways required for early eye development. Additionally, pathways involved in eye formation during embryogenesis are also incompletely understood. This study aims to identify the novel genes and pathways required for early eye development through systematic forward screening of the mammalian genome.ResultsQuery of the International Mouse Phenotyping Consortium (IMPC) database (data release 17.0, August 01, 2022) identified 74 unique knockout lines (genes) with genetically associated eye defects in mouse embryos. The vast majority of eye abnormalities were small or absent eyes, findings most relevant to MAC spectrum disease in humans. A literature search showed that 27 of the 74 lines had previously published knockout mouse models, of which only 15 had ocular defects identified in the original publications. These 12 previously published gene knockouts with no reported ocular abnormalities and the 47 unpublished knockouts with ocular abnormalities identified by the IMPC represent 59 genes not previously associated with early eye development in mice. Of these 59, we identified 19 genes with a reported human eye phenotype. Overall, mining of the IMPC data yielded 40 previously unimplicated genes linked to mammalian eye development. Bioinformatic analysis showed that several of the IMPC genes colocalized to several protein anabolic and pluripotency pathways in early eye development. Of note, our analysis suggests that the serine-glycine pathway producing glycine, a mitochondrial one-carbon donator to folate one-carbon metabolism (FOCM), is essential for eye formation.ConclusionsUsing genome-wide phenotype screening of single-gene knockout mouse lines, STRING analysis, and bioinformatic methods, this study identified genes heretofore unassociated with MAC phenotypes providing models to research novel molecular and cellular mechanisms involved in eye development. These findings have the potential to hasten the diagnosis and treatment of this congenital blinding disease.

Funder

Genome Canada

National Institutes of Health

Publisher

Springer Science and Business Media LLC

Subject

Cell Biology,Developmental Biology,Plant Science,General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,Physiology,Ecology, Evolution, Behavior and Systematics,Structural Biology,Biotechnology

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