Fate-restricted retinal progenitor cells adopt a molecular profile and spatial position distinct from multipotent progenitor cells

During development, multipotent retinal progenitor cells generate a large number of unique cell types. Recent evidence suggests that there are fate-restricted progenitor cell states in addition to multipotent ones. Here we report a transcriptomic analysis of fate- restricted progenitor cells biased...

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Published in:	Developmental biology Vol. 443; no. 1; pp. 35 - 49
Main Authors:	Buenaventura, Diego F., Ghinia-Tegla, Miruna G., Emerson, Mark M.
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 01-11-2018
Subjects:	Animals Cell Differentiation - physiology Cell Lineage - genetics Chick Embryo Cone photoreceptor Gene Expression Regulation, Developmental - genetics Genes, erbA - genetics Homeodomain Proteins - genetics LIM-Homeodomain Proteins - genetics Mice PAX6 Transcription Factor - genetics Restricted progenitor Retina - cytology Retina - embryology Retinal Cone Photoreceptor Cells - metabolism Retinal Cone Photoreceptor Cells - physiology Stem Cells - physiology Transcription Factors - genetics Transcriptome Transcriptome - genetics Restricted progenitor Transcriptome Cone photoreceptor
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Abstract	During development, multipotent retinal progenitor cells generate a large number of unique cell types. Recent evidence suggests that there are fate-restricted progenitor cell states in addition to multipotent ones. Here we report a transcriptomic analysis of fate- restricted progenitor cells biased to produce cone photoreceptors and horizontal cells, marked by the THRB cis-regulatory element ThrbCRM1. Comparison to a control population enriched in multipotent progenitor cells identified several genes considered to be pan-progenitor, such as VSX2, LHX2, and PAX6, as downregulated in these fate- restricted retinal progenitor cells. This differential regulation occurs in chick and in a different restricted progenitor population in mouse suggesting that this is a conserved feature of progenitor dynamics during retinal development. S-phase labeling also revealed that nuclear positions of restricted progenitor populations occupy distinct spatial niches within the developing chick retina. Using a conserved regulatory element proximal to the VSX2 gene, a potential negative feedback mechanism from specific transcription factors enriched in cone/horizontal cell progenitor cells was identified. This study identifies conserved molecular and cellular changes that occur during the generation of fate restricted retinal progenitor cells from multipotent retinal progenitor cells. •Transcriptome of retinal progenitors restricted to cone and horizontal cell fates.•Progenitor cell genes are regulated differently in specific progenitor populations.•The nuclei of different progenitor populations occupy unique spatial locations.•Gene regulatory networks in restricted progenitor cells repress multipotent programs.
AbstractList	During development, multipotent retinal progenitor cells generate a large number of unique cell types. Recent evidence suggests that there are fate-restricted progenitor cell states in addition to multipotent ones. Here we report a transcriptomic analysis of fate- restricted progenitor cells biased to produce cone photoreceptors and horizontal cells, marked by the THRB cis-regulatory element ThrbCRM1. Comparison to a control population enriched in multipotent progenitor cells identified several genes considered to be pan-progenitor, such as VSX2, LHX2, and PAX6, as downregulated in these fate- restricted retinal progenitor cells. This differential regulation occurs in chick and in a different restricted progenitor population in mouse suggesting that this is a conserved feature of progenitor dynamics during retinal development. S-phase labeling also revealed that nuclear positions of restricted progenitor populations occupy distinct spatial niches within the developing chick retina. Using a conserved regulatory element proximal to the VSX2 gene, a potential negative feedback mechanism from specific transcription factors enriched in cone/horizontal cell progenitor cells was identified. This study identifies conserved molecular and cellular changes that occur during the generation of fate restricted retinal progenitor cells from multipotent retinal progenitor cells. During development, multipotent retinal progenitor cells generate a large number of unique cell types. Recent evidence suggests that there are fate-restricted progenitor cell states in addition to multipotent ones. Here we report a transcriptomic analysis of fate- restricted progenitor cells biased to produce cone photoreceptors and horizontal cells, marked by the THRB cis-regulatory element ThrbCRM1. Comparison to a control population enriched in multipotent progenitor cells identified several genes considered to be pan-progenitor, such as VSX2, LHX2, and PAX6, as downregulated in these fate- restricted retinal progenitor cells. This differential regulation occurs in chick and in a different restricted progenitor population in mouse suggesting that this is a conserved feature of progenitor dynamics during retinal development. S-phase labeling also revealed that nuclear positions of restricted progenitor populations occupy distinct spatial niches within the developing chick retina. Using a conserved regulatory element proximal to the VSX2 gene, a potential negative feedback mechanism from specific transcription factors enriched in cone/horizontal cell progenitor cells was identified. This study identifies conserved molecular and cellular changes that occur during the generation of fate restricted retinal progenitor cells from multipotent retinal progenitor cells. •Transcriptome of retinal progenitors restricted to cone and horizontal cell fates.•Progenitor cell genes are regulated differently in specific progenitor populations.•The nuclei of different progenitor populations occupy unique spatial locations.•Gene regulatory networks in restricted progenitor cells repress multipotent programs.
Author	Emerson, Mark M. Ghinia-Tegla, Miruna G. Buenaventura, Diego F.
AuthorAffiliation	1 Department of Biology, The City College of New York, City University of New York, New York, NY, 10031 2 Biology Ph.D. Program, Graduate Center, City University of New York, New York, NY, 10031
AuthorAffiliation_xml	– name: 1 Department of Biology, The City College of New York, City University of New York, New York, NY, 10031 – name: 2 Biology Ph.D. Program, Graduate Center, City University of New York, New York, NY, 10031
Author_xml	– sequence: 1 givenname: Diego F. surname: Buenaventura fullname: Buenaventura, Diego F. organization: Department of Biology, The City College of New York, City University of New York, New York, NY 10031, United States – sequence: 2 givenname: Miruna G. surname: Ghinia-Tegla fullname: Ghinia-Tegla, Miruna G. organization: Department of Biology, The City College of New York, City University of New York, New York, NY 10031, United States – sequence: 3 givenname: Mark M. surname: Emerson fullname: Emerson, Mark M. email: memerson@ccny.cuny.edu organization: Department of Biology, The City College of New York, City University of New York, New York, NY 10031, United States
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Keywords	Restricted progenitor Transcriptome Cone photoreceptor
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Snippet	During development, multipotent retinal progenitor cells generate a large number of unique cell types. Recent evidence suggests that there are fate-restricted...
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SubjectTerms	Animals Cell Differentiation - physiology Cell Lineage - genetics Chick Embryo Cone photoreceptor Gene Expression Regulation, Developmental - genetics Genes, erbA - genetics Homeodomain Proteins - genetics LIM-Homeodomain Proteins - genetics Mice PAX6 Transcription Factor - genetics Restricted progenitor Retina - cytology Retina - embryology Retinal Cone Photoreceptor Cells - metabolism Retinal Cone Photoreceptor Cells - physiology Stem Cells - physiology Transcription Factors - genetics Transcriptome Transcriptome - genetics
Title	Fate-restricted retinal progenitor cells adopt a molecular profile and spatial position distinct from multipotent progenitor cells
URI	https://dx.doi.org/10.1016/j.ydbio.2018.06.023 https://www.ncbi.nlm.nih.gov/pubmed/30145104 https://search.proquest.com/docview/2094410213 https://pubmed.ncbi.nlm.nih.gov/PMC6441625
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