Transcriptome Dynamics of Developing Photoreceptors in Three‐Dimensional Retina Cultures Recapitulates Temporal Sequence of Human Cone and Rod Differentiation Revealing Cell Surface Markers and Gene Networks

The derivation of three‐dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of c...

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Published inStem cells (Dayton, Ohio) Vol. 33; no. 12; pp. 3504 - 3518
Main Authors Kaewkhaw, Rossukon, Kaya, Koray Dogan, Brooks, Matthew, Homma, Kohei, Zou, Jizhong, Chaitankar, Vijender, Rao, Mahendra, Swaroop, Anand
Format Journal Article
LanguageEnglish
Published England Oxford University Press 01.12.2015
John Wiley and Sons Inc
Subjects
Antigens, Differentiation - biosynthesis
Cell Differentiation
Cell Line
Eye Proteins - biosynthesis
Gene expression
Global gene profiling
Human Embryonic Stem Cells - cytology
Human Embryonic Stem Cells - metabolism
Human rod and cone photoreceptors
Humans
Next generation sequencing
Photoreception
Photoreceptors
Retina
Retinal Cone Photoreceptor Cells - cytology
Retinal Cone Photoreceptor Cells - metabolism
Retinal Rod Photoreceptor Cells - cytology
Retinal Rod Photoreceptor Cells - metabolism
Stem cells
Three‐dimensional organoid culture
Transcriptome
Translational and Clinical Research
Retina
Three-dimensional organoid culture
Global gene profiling
Next generation sequencing
Human rod and cone photoreceptors
Stem cells
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Abstract The derivation of three‐dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone‐rod homeobox (CRX), an established marker of postmitotic photoreceptor precursors. The CRXp‐GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self‐organizing 3D retina‐like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S‐opsin and no rhodopsin or L/M‐opsin is present. The transcriptome profile, by RNA‐seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures. Stem Cells 2015;33:3504–3518
AbstractList The derivation of three-dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone-rod homeobox (CRX), an established marker of postmitotic photoreceptor precursors. The CRXp-GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self-organizing 3D retina-like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S-opsin and no rhodopsin or L/M-opsin is present. The transcriptome profile, by RNA-seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures.The derivation of three-dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone-rod homeobox (CRX), an established marker of postmitotic photoreceptor precursors. The CRXp-GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self-organizing 3D retina-like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S-opsin and no rhodopsin or L/M-opsin is present. The transcriptome profile, by RNA-seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures.
The derivation of three-dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone-rod homeobox (CRX), an established marker of postmitotic photoreceptor precursors. The CRXp-GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self-organizing 3D retina-like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S-opsin and no rhodopsin or L/M-opsin is present. The transcriptome profile, by RNA-seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures.
The derivation of three-dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone-rod homeobox (CRX), an established marker of postmitotic photoreceptor precursors. The CRXp-GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self-organizing 3D retina-like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S-opsin and no rhodopsin or L/M-opsin is present. The transcriptome profile, by RNA-seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures. Stem Cells  2015;33:3504–3518
The derivation of three-dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone-rod homeobox (CRX), an established marker of postmitotic photoreceptor precursors. The CRXp-GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self-organizing 3D retina-like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S-opsin and no rhodopsin or L/M-opsin is present. The transcriptome profile, by RNA-seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures. Stem Cells 2015;33:3504-3518
The derivation of three‐dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have generated a H9 human embryonic stem cell subclone that carries a green fluorescent protein (GFP) reporter under the control of the promoter of cone‐rod homeobox ( CRX ), an established marker of postmitotic photoreceptor precursors. The CRXp ‐GFP reporter replicates endogenous CRX expression in vitro when the H9 subclone is induced to form self‐organizing 3D retina‐like tissue. At day 37, CRX+ photoreceptors appear in the basal or middle part of neural retina and migrate to apical side by day 67. Temporal and spatial patterns of retinal cell type markers recapitulate the predicted sequence of development. Cone gene expression is concomitant with CRX, whereas rod differentiation factor neural retina leucine zipper protein (NRL) is first observed at day 67. At day 90, robust expression of NRL and its target nuclear receptor NR2E3 is evident in many CRX+ cells, while minimal S‐opsin and no rhodopsin or L/M‐opsin is present. The transcriptome profile, by RNA‐seq, of developing human photoreceptors is remarkably concordant with mRNA and immunohistochemistry data available for human fetal retina although many targets of CRX, including phototransduction genes, exhibit a significant delay in expression. We report on temporal changes in gene signatures, including expression of cell surface markers and transcription factors; these expression changes should assist in isolation of photoreceptors at distinct stages of differentiation and in delineating coexpression networks. Our studies establish the first global expression database of developing human photoreceptors, providing a reference map for functional studies in retinal cultures. S tem C ells 2015;33:3504–3518
Author Chaitankar, Vijender
Homma, Kohei
Kaya, Koray Dogan
Rao, Mahendra
Kaewkhaw, Rossukon
Brooks, Matthew
Zou, Jizhong
Swaroop, Anand
AuthorAffiliation 3 Center for Regenerative Medicine National Institutes of Health Bethesda Maryland USA
5 Department of Physiology Nippon Medical School Tokyo Japan
1 Neurobiology‐Neurodegeneration & Repair Laboratory, National Eye Institute National Institutes of Health Bethesda Maryland USA
2 Research Center, Faculty of Medicine Ramathibodi Hospital Mahidol University Bangkok Thailand
4 iPSC Core, Center for Molecular Medicine National Heart, Lung, and Blood Institute Bethesda Maryland USA
6 The New York Stem Cell Foundation Research Institute New York NY 10023
AuthorAffiliation_xml – name: 5 Department of Physiology Nippon Medical School Tokyo Japan
– name: 4 iPSC Core, Center for Molecular Medicine National Heart, Lung, and Blood Institute Bethesda Maryland USA
– name: 3 Center for Regenerative Medicine National Institutes of Health Bethesda Maryland USA
– name: 2 Research Center, Faculty of Medicine Ramathibodi Hospital Mahidol University Bangkok Thailand
– name: 1 Neurobiology‐Neurodegeneration & Repair Laboratory, National Eye Institute National Institutes of Health Bethesda Maryland USA
– name: 6 The New York Stem Cell Foundation Research Institute New York NY 10023
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  givenname: Rossukon
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  fullname: Kaya, Koray Dogan
  organization: National Institutes of Health
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  givenname: Matthew
  surname: Brooks
  fullname: Brooks, Matthew
  organization: National Institutes of Health
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/26235913$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2015 This article is a U.S. Government work and is in the public domain in the USA. STEM CELLS published by Wiley Periodicals, Inc. on behalf of AlphaMed Press AlphaMed Press
2015 This article is a U.S. Government work and is in the public domain in the USA. STEM CELLS published by Wiley Periodicals, Inc. on behalf of AlphaMed Press AlphaMed Press.
2015 AlphaMed Press
Copyright_xml – notice: 2015 This article is a U.S. Government work and is in the public domain in the USA. STEM CELLS published by Wiley Periodicals, Inc. on behalf of AlphaMed Press AlphaMed Press
– notice: 2015 This article is a U.S. Government work and is in the public domain in the USA. STEM CELLS published by Wiley Periodicals, Inc. on behalf of AlphaMed Press AlphaMed Press.
– notice: 2015 AlphaMed Press
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Issue 12
Keywords Retina
Three-dimensional organoid culture
Global gene profiling
Next generation sequencing
Human rod and cone photoreceptors
Stem cells
Language English
License Attribution-NonCommercial
http://creativecommons.org/licenses/by-nc/4.0
2015 This article is a U.S. Government work and is in the public domain in the USA. STEM CELLS published by Wiley Periodicals, Inc. on behalf of AlphaMed Press AlphaMed Press.
This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
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Notes This article was published online on 14 August 2015. An error was subsequently identified. This notice is included in the online and print versions to indicate that both have been corrected 4 September 2015.
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OpenAccessLink https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fstem.2122
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PublicationTitle Stem cells (Dayton, Ohio)
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Snippet The derivation of three‐dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have...
The derivation of three-dimensional (3D) stratified neural retina from pluripotent stem cells has permitted investigations of human photoreceptors. We have...
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SubjectTerms Antigens, Differentiation - biosynthesis
Cell Differentiation
Cell Line
Eye Proteins - biosynthesis
Gene expression
Global gene profiling
Human Embryonic Stem Cells - cytology
Human Embryonic Stem Cells - metabolism
Human rod and cone photoreceptors
Humans
Next generation sequencing
Photoreception
Photoreceptors
Retina
Retinal Cone Photoreceptor Cells - cytology
Retinal Cone Photoreceptor Cells - metabolism
Retinal Rod Photoreceptor Cells - cytology
Retinal Rod Photoreceptor Cells - metabolism
Stem cells
Three‐dimensional organoid culture
Transcriptome
Translational and Clinical Research
Title Transcriptome Dynamics of Developing Photoreceptors in Three‐Dimensional Retina Cultures Recapitulates Temporal Sequence of Human Cone and Rod Differentiation Revealing Cell Surface Markers and Gene Networks
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fstem.2122
https://www.ncbi.nlm.nih.gov/pubmed/26235913
https://www.proquest.com/docview/1755482308
https://www.proquest.com/docview/1760856735
https://www.proquest.com/docview/1780522456
https://pubmed.ncbi.nlm.nih.gov/PMC4713319
Volume 33
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