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REST suppression mediates neural conversion of adult human fibroblasts via microRNA‐dependent and ‐independent pathways

Drouin‐Ouellet, Janelle, Lau, Shong, Brattås, Per Ludvik, Rylander Ottosson, Daniella, Pircs, Karolina, Grassi, Daniela A, Collins, Lucy M, Vuono, Romina, Andersson Sjöland, Annika, Westergren‐Thorsson, Gunilla, Graff, Caroline, Minthon, Lennart, Toresson, Håkan, Barker, Roger A, Jakobsson, Johan, Parmar, Malin·2017·EMBO Molecular Medicine
DOI 10.15252/emmm.201607471PMC PMC5538296
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Figure 1 Bicistronic approach successfully reprograms fetal fibroblasts but fails to reprogram adult fibroblasts AVector maps of constructs containing the neural conversion factors ASCL1 coding for MASH1 and BRN2 as well as woodchuck hepatitis posttranscriptional element (WPRE) at different positions.BQuantitative analysis showing the difference in fluorescence intensity of ASCL1 (red bar graphs) and BRN2 (yellow bar graphs) following transduction with the different constructs.C, DRepresentative images of double‐immunofluorescent staining of ASCL1 (in green) and BRN2 (in red) (C) as well as MAP2 staining (D) showing the different expression levels of each transcription factor and the resulting neuronal conversion for each construct.EQuantification of the number of iNs converted 12 days after transduction with either Pgk.Ascl1 + Pgk.Brn2 + Pgk.Myt1L or pB.pA.FRNA‐seq analysis illustrating the fold changes in gene expression in fetal fibroblasts transduced with pB.pA as compared to untransduced cells, with genes that are significantly up‐ or down‐regulated marked as red dots.GGene ontology enrichment analysis reveals significant enrichment of neuronal genes (in bold) among the up‐regulated genes in the pB.pA‐transduced fetal fibroblasts.HRepresentative fluorescence images showing the MAP2 expression in fetal and adult fibroblasts (dermal and lung) reprogrammed with pB.pA.IFC correlation analysis and Venn diagram showing genes that are significantly changed in both adult and fetal pB.pA‐transduced cells (red) and significantly changed in fetal cells only (blue) or adult cells only (green) or not changed (black).JGene ontology enrichment analysis showing the genes associated with neurons (in bold) that are up‐regulated in the pB.pA‐transduced fetal fibroblasts but not in the adult fibroblasts transduced with pB.pA.Data information: Scale bars, 100 μm in (D), 50 μm in (H). ahDF, adult human dermal fibroblasts; ahFL, adult human lung fibroblasts; CTR, control. Data are expressed as mean ± SEM and are from biological replicates (n = 3). *P < 0.05. Exact P‐values and statistical tests used to calculate them are provided in Appendix Table S4.
Figure 1 Bicistronic approach successfully reprograms fetal fibroblasts but fails to reprogram adult fibroblasts AVector maps of constructs containing the neural conversion factors ASCL1 coding for MASH1 and BRN2 as well as woodchuck hepatitis posttranscriptional element (WPRE) at different positions.BQuantitative analysis showing the difference in fluorescence intensity of ASCL1 (red bar graphs) and BRN2 (yellow bar graphs) following transduction with the different constructs.C, DRepresentative images of double‐immunofluorescent staining of ASCL1 (in green) and BRN2 (in red) (C) as well as MAP2 staining (D) showing the different expression levels of each transcription factor and the resulting neuronal conversion for each construct.EQuantification of the number of iNs converted 12 days after transduction with either Pgk.Ascl1 + Pgk.Brn2 + Pgk.Myt1L or pB.pA.FRNA‐seq analysis illustrating the fold changes in gene expression in fetal fibroblasts transduced with pB.pA as compared to untransduced cells, with genes that are significantly up‐ or down‐regulated marked as red dots.GGene ontology enrichment analysis reveals significant enrichment of neuronal genes (in bold) among the up‐regulated genes in the pB.pA‐transduced fetal fibroblasts.HRepresentative fluorescence images showing the MAP2 expression in fetal and adult fibroblasts (dermal and lung) reprogrammed with pB.pA.IFC correlation analysis and Venn diagram showing genes that are significantly changed in both adult and fetal pB.pA‐transduced cells (red) and significantly changed in fetal cells only (blue) or adult cells only (green) or not changed (black).JGene ontology enrichment analysis showing the genes associated with neurons (in bold) that are up‐regulated in the pB.pA‐transduced fetal fibroblasts but not in the adult fibroblasts transduced with pB.pA.Data information: Scale bars, 100 μm in (D), 50 μm in (H). ahDF, adult human dermal fibroblasts; ahFL, adult human lung fibroblasts; CTR, control. Data are expressed as mean ± SEM and are from biological replicates (n = 3). *P < 0.05. Exact P‐values and statistical tests used to calculate them are provided in Appendix Table S4.CC BY · PubMed Central
Figure 2 REST knockdown promotes the pB.pA‐driven reprogramming of adult human fibroblasts qPCR analysis of REST gene expression.Representative immunofluorescence images showing a high density of MAP2+ cells in pB.pA + RESTi reprogrammed adult fibroblasts from different sources.Quantification of neuronal efficiency and purity of pB.pA + RESTi reprogrammed adult human dermal fibroblasts from five healthy donors (61–71 years).Quantification of neuronal efficiency and purity of an adult human dermal fibroblast line reprogrammed with pB.pA + RESTi at different passages.Double‐immunofluorescence stainings showing the expression of neuronal markers in iNs reprogrammed from adult fibroblasts 25 days post‐transduction with pB.pA + RESTi. In vitro patch‐clamp recordings of adult iNs depicting repetitive current‐induced action potentials indicative of mature neuronal physiology at 12–15 weeks post‐transduction.Presence of repetitive current‐induced action potentials and spontaneous postsynaptic currents in vivo 8 weeks following transplantation.Data information: Scale bars, 100 μm in (B), 25 μm in (E–G). ahDF, adult human dermal fibroblasts; ahFL, adult human lung fibroblasts; shREST, short hairpin RNA against REST. Data are expressed as mean ± SEM and are from biological replicates (n = 3–4). *P < 0.05, **P < 0.01. Exact P‐values and statistical tests used to calculate them are provided in Appendix Table S4.
Figure 2 REST knockdown promotes the pB.pA‐driven reprogramming of adult human fibroblasts qPCR analysis of REST gene expression.Representative immunofluorescence images showing a high density of MAP2+ cells in pB.pA + RESTi reprogrammed adult fibroblasts from different sources.Quantification of neuronal efficiency and purity of pB.pA + RESTi reprogrammed adult human dermal fibroblasts from five healthy donors (61–71 years).Quantification of neuronal efficiency and purity of an adult human dermal fibroblast line reprogrammed with pB.pA + RESTi at different passages.Double‐immunofluorescence stainings showing the expression of neuronal markers in iNs reprogrammed from adult fibroblasts 25 days post‐transduction with pB.pA + RESTi. In vitro patch‐clamp recordings of adult iNs depicting repetitive current‐induced action potentials indicative of mature neuronal physiology at 12–15 weeks post‐transduction.Presence of repetitive current‐induced action potentials and spontaneous postsynaptic currents in vivo 8 weeks following transplantation.Data information: Scale bars, 100 μm in (B), 25 μm in (E–G). ahDF, adult human dermal fibroblasts; ahFL, adult human lung fibroblasts; shREST, short hairpin RNA against REST. Data are expressed as mean ± SEM and are from biological replicates (n = 3–4). *P < 0.05, **P < 0.01. Exact P‐values and statistical tests used to calculate them are provided in Appendix Table S4.CC BY · PubMed Central
Figure 3 Neuronal microRNA expression partly drives neuronal reprogramming of adult fibroblasts AqPCR measurements of miR‐124 and miR‐9 in adult fibroblasts reprogrammed with pB.pA only or pB.pA + RESTi and normalized on the non‐transduced fibroblast values (yellow dashed line).BRegion‐specific microRNAs qPCR measurements in adult fibroblasts reprogrammed with pB.pA only or pB.pA + RESTi and normalized on the non‐transduced fibroblast values (yellow dashed line).CVector maps of constructs containing the transcription factors Ascl1 and Brn2 with and without miR‐9 and miR‐124, as well as the shRNA sequences against REST.DQuantification of the neuronal yield as assessed by MAP2 expression in adult fibroblasts transduced with different reprogramming vectors.E, FQuantification of the total number of cells as well as the percentage of TAU+ cells and the average fluorescence intensity in adult iNs with and without miR‐124 (E) or miR‐9 (F) knockdown.GRepresentative images of the high content screening target activation analysis showing the cells expressing mCherry (successfully transduced with the miRNA inhibition or control constructs) that have been included in the analysis of the TAU staining (white contours). Rejected nuclei are circled in yellow and valid nuclei that do not express mCherry exhibit blue contours.Data information: Scale bar, 50 μm in (G). CTR, control; KD, knockdown. Data are expressed as mean ± SEM and are from biological replicates (n = 3–4). **P < 0.01. Exact P‐values and statistical tests used to calculate them are provided in Appendix Table S4.
Figure 3 Neuronal microRNA expression partly drives neuronal reprogramming of adult fibroblasts AqPCR measurements of miR‐124 and miR‐9 in adult fibroblasts reprogrammed with pB.pA only or pB.pA + RESTi and normalized on the non‐transduced fibroblast values (yellow dashed line).BRegion‐specific microRNAs qPCR measurements in adult fibroblasts reprogrammed with pB.pA only or pB.pA + RESTi and normalized on the non‐transduced fibroblast values (yellow dashed line).CVector maps of constructs containing the transcription factors Ascl1 and Brn2 with and without miR‐9 and miR‐124, as well as the shRNA sequences against REST.DQuantification of the neuronal yield as assessed by MAP2 expression in adult fibroblasts transduced with different reprogramming vectors.E, FQuantification of the total number of cells as well as the percentage of TAU+ cells and the average fluorescence intensity in adult iNs with and without miR‐124 (E) or miR‐9 (F) knockdown.GRepresentative images of the high content screening target activation analysis showing the cells expressing mCherry (successfully transduced with the miRNA inhibition or control constructs) that have been included in the analysis of the TAU staining (white contours). Rejected nuclei are circled in yellow and valid nuclei that do not express mCherry exhibit blue contours.Data information: Scale bar, 50 μm in (G). CTR, control; KD, knockdown. Data are expressed as mean ± SEM and are from biological replicates (n = 3–4). **P < 0.01. Exact P‐values and statistical tests used to calculate them are provided in Appendix Table S4.CC BY · PubMed Central
Figure 4 Differences in gene expression between pB.pA + RESTi and pB.mir9/124.pA Graph illustrating the fold changes in gene expression in adult fibroblasts transduced with pB.pA + RESTi as compared to untransduced cells (genes that are significantly up‐ or down‐regulated marked as red dots).Graph illustrating the fold changes in gene expression in adult fibroblasts transduced with pB.mir9/124.pA as compared to untransduced cells (genes that are significantly up‐ or down‐regulated marked as red dots).FC correlation analysis showing the genes that are significantly changed in both pB.pA + RESTi‐ and pB.mir9/124.pA‐transduced cells (red) that are significantly changed in pB.mir9/124.pA‐transduced cells only (blue) or pB.pA + RESTi cells only (green) or unchanged (black).Venn diagram showing the genes that are significantly changed in both pB.pA + RESTi‐ and pB.mir9/124.pA‐transduced cells (red) that are significantly changed in pB.mir9/124.pA‐transduced cells only (blue) or pB.pA + RESTi cells only (green).
Figure 4 Differences in gene expression between pB.pA + RESTi and pB.mir9/124.pA Graph illustrating the fold changes in gene expression in adult fibroblasts transduced with pB.pA + RESTi as compared to untransduced cells (genes that are significantly up‐ or down‐regulated marked as red dots).Graph illustrating the fold changes in gene expression in adult fibroblasts transduced with pB.mir9/124.pA as compared to untransduced cells (genes that are significantly up‐ or down‐regulated marked as red dots).FC correlation analysis showing the genes that are significantly changed in both pB.pA + RESTi‐ and pB.mir9/124.pA‐transduced cells (red) that are significantly changed in pB.mir9/124.pA‐transduced cells only (blue) or pB.pA + RESTi cells only (green) or unchanged (black).Venn diagram showing the genes that are significantly changed in both pB.pA + RESTi‐ and pB.mir9/124.pA‐transduced cells (red) that are significantly changed in pB.mir9/124.pA‐transduced cells only (blue) or pB.pA + RESTi cells only (green).CC BY · PubMed Central
Figure 5 Enhanced neuronal gene up‐regulation in pB.pA + RESTi reprogrammed adult iNs Clustering of RNA‐seq samples, using euclidean distance on normalized and log‐transformed read counts.Principal component analysis showing a separation of the groups that reprogram well from those that do not on PC1 and a separation of the groups with REST knockdown on PC2.Gene ontology enrichment analysis showing significant enrichment of neuronal genes (in bold) among the genes up‐regulated in the pB.pA + RESTi‐transduced fibroblasts but not in the adult fibroblasts transduced with pB.mir9/124.pA.Gene ontology enrichment analysis showing that no genes associated with neurons are uniquely up‐regulated in the pB.mir9/124.pA‐transduced fibroblasts.
Figure 5 Enhanced neuronal gene up‐regulation in pB.pA + RESTi reprogrammed adult iNs Clustering of RNA‐seq samples, using euclidean distance on normalized and log‐transformed read counts.Principal component analysis showing a separation of the groups that reprogram well from those that do not on PC1 and a separation of the groups with REST knockdown on PC2.Gene ontology enrichment analysis showing significant enrichment of neuronal genes (in bold) among the genes up‐regulated in the pB.pA + RESTi‐transduced fibroblasts but not in the adult fibroblasts transduced with pB.mir9/124.pA.Gene ontology enrichment analysis showing that no genes associated with neurons are uniquely up‐regulated in the pB.mir9/124.pA‐transduced fibroblasts.CC BY · PubMed Central
Figure 6 All‐in‐one vector to reprogram skin fibroblasts from patients with a range of different neurodegenerative disorders Map of the single reprogramming vector containing REST shRNA sequences as well as Brn2 and Ascl1.Quantitative comparison of the total number of cells, as well as the number of MAP2+ and TAU+ cells per well using separate vectors or one single vector for pB.pA + RESTi reprogramming in four different adult dermal fibroblast lines.Fluorescence microscopy images of iNs reprogrammed using the single vector from healthy individuals as well as from patients with various neurodegenerative disorders.Quantification of the neuronal counts and purity.Fluorescence microscopy images of iNs derived from an HD patient after optimization of culture conditions.Percentage of cells displaying various number of neurites for each line.qPCR analysis of six neuronal genes in healthy individuals as well as from patients with various neurodegenerative disorders.Data information: Scale bars, 25 μm in (C), 100 μm in (E). FAD, familial Alzheimer's disease; FPD, familial Parkinson's disease; HD, Huntington's disease; SPD, sporadic Parkinson's disease. Data are expressed as mean ± SEM and are from biological replicates (n = 4).
Figure 6 All‐in‐one vector to reprogram skin fibroblasts from patients with a range of different neurodegenerative disorders Map of the single reprogramming vector containing REST shRNA sequences as well as Brn2 and Ascl1.Quantitative comparison of the total number of cells, as well as the number of MAP2+ and TAU+ cells per well using separate vectors or one single vector for pB.pA + RESTi reprogramming in four different adult dermal fibroblast lines.Fluorescence microscopy images of iNs reprogrammed using the single vector from healthy individuals as well as from patients with various neurodegenerative disorders.Quantification of the neuronal counts and purity.Fluorescence microscopy images of iNs derived from an HD patient after optimization of culture conditions.Percentage of cells displaying various number of neurites for each line.qPCR analysis of six neuronal genes in healthy individuals as well as from patients with various neurodegenerative disorders.Data information: Scale bars, 25 μm in (C), 100 μm in (E). FAD, familial Alzheimer's disease; FPD, familial Parkinson's disease; HD, Huntington's disease; SPD, sporadic Parkinson's disease. Data are expressed as mean ± SEM and are from biological replicates (n = 4).CC BY · PubMed Central

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Authors
Drouin‐Ouellet, J., Lau, S., Brattås, P. L., Rylander Ottosson, D., Pircs, K., Grassi, D. A., Collins, L. M., Vuono, R., Andersson Sjöland, A., Westergren‐Thorsson, G., Graff, C., Minthon, L., Toresson, H., Barker, R. A., Jakobsson, J., & Parmar, M.
ORCID
Venue
EMBO Molecular Medicine
Publisher
Springer Science and Business Media LLC
Published
2017-06-23
Volume
9
Issue
8
Pages
1117-1131
ISSN
  • 1757-4676
  • 1757-4684
DOI
10.15252/emmm.201607471
PMC
PMC5538296
Cited by
110
References
11
Language
en
Licence
Funders
  • New York Stem Cell Foundation
  • H2020 European Research Council (602278, 30971, FP/2007‐2013)
  • Vetenskapsrådet (521‐2012‐5624, 2016‐00873, 70862601)
  • Parkinsonfonden (874/16)
  • Canadian Institutes of Health Research (358492)
  • Lunds Universitet
  • Stiftelsen för Strategisk Forskning (FFL12‐0074)
  • National Institute for Health Research

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