A highly reproducible and efficient method for retinal organoid differentiation from human pluripotent stem cells

Jade Harkin, Kiersten H. Peña, Cátia Gomes, Melody Hernandez, Sailee S. Lavekar, Kaman So, Kelly Lentsch, Elyse M. Feder, Sarah Morrow, Kang Chieh Huang, Kaylee D. Tutrow, Ann Morris, Chi Zhang, Jason S. Meyer

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Human pluripotent stem cell (hPSC)-derived retinal organoids are three-dimensional cellular aggregates that differentiate and self-organize to closely mimic the spatial and temporal patterning of the developing human retina. Retinal organoid models serve as reliable tools for studying human retinogenesis, yet limitations in the efficiency and reproducibility of current retinal organoid differentiation protocols have reduced the use of these models for more high-throughput applications such as disease modeling and drug screening. To address these shortcomings, the current study aimed to standardize prior differentiation protocols to yield a highly reproducible and efficient method for generating retinal organoids. Results demonstrated that through regulation of organoid size and shape using quick reaggregation methods, retinal organoids were highly reproducible compared to more traditional methods. Additionally, the timed activation of BMP signaling within developing cells generated pure populations of retinal organoids at 100% efficiency from multiple widely used cell lines, with the default forebrain fate resulting from the inhibition of BMP signaling. Furthermore, given the ability to direct retinal or forebrain fates at complete purity, mRNA-seq analyses were then utilized to identify some of the earliest transcriptional changes that occur during the specification of these two lineages from a common progenitor. These improved methods also yielded retinal organoids with expedited differentiation timelines when compared to traditional methods. Taken together, the results of this study demonstrate the development of a highly reproducible and minimally variable method for generating retinal organoids suitable for analyzing the earliest stages of human retinal cell fate specification.

Original languageEnglish
Article numbere2317285121
JournalProceedings of the National Academy of Sciences of the United States of America
Volume121
Issue number25
DOIs
StatePublished - Jun 1 2024

Bibliographical note

Publisher Copyright:
© 2024 National Academy of Sciences. All rights reserved.

Funding

We thank Dr. Karl Wahlin for sharing the SIX6:GFP iPS cell line and Dr. Don Zack for sharing the BRN3b:tdTomato:Thy1.2 cell line. We also thank the Indiana University Center for Medical Genomics for assistance with RNA-seq analyses. Grant support was provided by the National Eye Institute (R01EY033022 and U24EY033269 to J.S.M.), the BrightFocus Foundation (G2020369 to J.S.M.), and the Gilbert Family Foundation (923016 to J.S.M.). Support for this project was also provided by the Sarah Roush Memorial Fellowship from the Indiana Alzheimer\u2019s Disease Center (C.G.), the BrightFocus Postdoctoral Fellowship (G2022003F to C.G.), a Shaffer Grant from the Glaucoma Research Foundation (C.G.), as well as a Cagiantas scholarship from the Indiana University School of Medicine (J.H.). ACKNOWLEDGMENTS. We thank Dr. Karl Wahlin for sharing the SIX6:GFP iPS cell line and Dr. Don Zack for sharing the BRN3b:tdTomato:Thy1.2 cell line. We also thank the Indiana University Center for Medical Genomics for assistance with RNA-seq analyses. Grant support was provided by the National Eye Institute (R01EY033022 and U24EY033269 to J.S.M.), the BrightFocus Foundation (G2020369 to J.S.M.), and the Gilbert Family Foundation (923016 to J.S.M.). Support for this project was also provided by the Sarah Roush Memorial Fellowship from the Indiana Alzheimer\u2019s Disease Center (C.G.), the BrightFocus Postdoctoral Fellowship (G2022003F to C.G.), a Shaffer Grant from the Glaucoma Research Foundation (C.G.), as well as a Cagiantas scholarship from the Indiana University School of Medicine (J.H.).

FundersFunder number
New England Glaucoma Research Foundation
Indiana University School of Medicine
University of Southern Indiana
Gilbert Family Foundation923016
Gilbert Family Foundation
Indiana Alzheimer’s Disease CenterG2022003F
National Eye Institute (NEI)U24EY033269, R01EY033022
National Eye Institute (NEI)
BrightFocus FoundationG2020369
BrightFocus Foundation

    Keywords

    • organoid
    • retina
    • stem cell

    ASJC Scopus subject areas

    • General

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