Deconstructing Stepwise Fate Conversion of Human Fibroblasts to Neurons by MicroRNAs
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Cell-fate conversion generally requires reprogramming effectors to both introduce fate programs of the target cell type and erase the identity of starting cell population. Here, we reveal insights into the activity of microRNAs miR-9/9∗ and miR-124 (miR-9/9∗-124) as reprogramming agents that orchestrate direct conversion of human fibroblasts into motor neurons by first eradicating fibroblast identity and promoting uniform transition to a neuronal state in sequence. We identify KLF-family transcription factors as direct target genes for miR-9/9∗-124 and show their repression is critical for erasing fibroblast fate. Subsequent gain of neuronal identity requires upregulation of a small nuclear RNA, RN7SK, which induces accessibilities of chromatin regions and neuronal gene activation to push cells to a neuronal state. Our study defines deterministic components in the microRNA-mediated reprogramming cascade.
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The miRNA+TFs approach generated a highly enriched neuronal population as previously characterized by single cell and bulk RNA-seq and electrically active cells in 2D culture, showing inward and outward currents and multiple action potentials measured by whole-cell recording.
“This miRNA+TFs approach generated a highly enriched neuronal population as previously characterized by single cell and bulk RNA-seq (20, 28, 29) and electrically active cells in 2D culture, showing inward and outward currents and multiple action potentials measured by whole-cell recording (Fig. S1A).”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [29]
Split into 2 atoms — 1 confirmed, 0 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredMiR-9/9* and miR-124, when expressed in human adult fibroblasts, induce chromatin reconfiguration leading to sequential steps of fibroblast identity erasure and neuronal program activation with high efficiency reaching over 80% of conversion rate.
“MiR-9/9* and miR-124 (miR-9/9*−124), when expressed in human adult fibroblasts, induce chromatin reconfiguration leading to sequential steps of fibroblast identity erasure and neuronal program activation with high efficiency reaching over 80% of conversion rate (28, 29).”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [29]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredMiR-9/9*−124-induced neurons are primarily composed of neurons as previously characterized by single-cell RNA-seq.
“MiR-9/9*−124-induced neurons are primarily composed of neurons as previously characterized by single-cell RNA-seq (20, 29).”
From Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming (2024) · cites this paper as [29]
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Modeling late-onset Alzheimer’s disease neuropathology via direct neuronal reprogramming
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Self-citationDirect Neuronal Reprogramming: Bridging the Gap Between Basic Science and Clinical Application
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MiR-124 synergism with ELAVL3 enhances target gene expression to promote neuronal maturity
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The nerve cells in gastrointestinal cancers: from molecular mechanisms to clinical intervention
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Patient-Derived In Vitro Models of Microglial Function and Synaptic Engulfment in Schizophrenia
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MicroRNA Roles in Cell Reprogramming Mechanisms
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Serum-tolerant polymeric complex for stem-cell transfection and neural differentiation
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Probing cell identity hierarchies by fate titration and collision during direct reprogramming
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Self-citationOne Big Step to a Neuron, Two Small Steps for miRNAs
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Reprogramming cellular identity in vivo
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Parallel gene size and isoform expansion of ancient neuronal genes
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Proliferation history and transcription factor levels drive direct conversion
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Brain Repair by Cell Replacement via In Situ Neuronal Reprogramming
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Self-citationKeeping the balance: The noncoding RNA 7SK as a master regulator for neuron development and function
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Self-citationhnRNP R negatively regulates transcription by modulating the association of P‐TEFb with 7SK and BRD4
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Upregulation of circ0000381 attenuates microglial/macrophage pyroptosis after spinal cord injury
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Epigenetic Dynamics in Reprogramming to Dopaminergic Neurons for Parkinson's Disease
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Self-citationDirect Conversion of Cell Fate and Induced Endothelial Cells
Han, J., Shin, Y., & Kim, H.-S. (2021) · Circulation Journal · doi:10.1253/circj.cj-21-0703 · Cited by 5 · see citing works
Moving CNS axon growth and regeneration research into human model systems
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Cellular identity through the lens of direct lineage reprogramming
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Iyer, D. P., Moyon, L., Ringeling, F. R., Cheng, C.-Y., Wittler, L., Canzar, S., Marsico, A., & Bulut-Karslıoğlu, A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.20.572612 · Cited by 5 · see citing works
Accelerated neuronal aging in vitro ∼melting watch ∼
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Emerging directions in tauopathy research
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A cutting-edge strategy for spinal cord injury treatment: resident cellular transdifferentiation
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The effect of LARP7 on gene expression during osteogenesis
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Direct Neural Reprogramming in situ: Existing Approaches and Their Optimization
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Role and Therapeutic Potential of Non-coding RNAs in Astrocytes during Neonatal Brain InjuryPreprint
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Self-citationThree-dimensional direct neuronal reprogramming for modeling Alzheimer’s disease neuropathology
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Self-citationChurch, V. A., Krzyżosiak, A., Miao, B., Chen, S., Walker, C. K., Kwon, J., Dahiya, S. M., Wang, L., Al‐Dalahmah, O., Zhang, B., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-78010-0 · Cited by 1 · see citing works
Self-citationNotch inhibition enhances morphological reprogramming of microRNA-induced human neurons
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Self-citationSAK3 confers neuroprotection in the neurodegeneration model of X-linked Dystonia-ParkinsonismPreprint
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Self-citationIgnorance is bliss: Inhibition of proteomic stress sensing improves direct neuronal conversion
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Analysis of clinical application value of miR-1284 in type 2 diabetes mellitus
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CDKN1A protects medium spiny neurons from Huntington's disease pathology
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Canonical and isomiR products of miR-142 enhance dendritic cell reprogramming
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RNA dysregulation as a determinant of aging and neurodegenerative vulnerability
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- Authors
- Cates, K., McCoy, M. J., Kwon, J.-S., Liu, Y., Abernathy, D. G., Zhang, B., Liu, S., Gontarz, P., Kim, W. K., Chen, S., Kong, W., Ho, J. N., Burbach, K. F., Gabel, H. W., Morris, S. A., & Yoo, A. S.
- Affiliations
- Washington University in St. Louis (US)
- Corresponding author
- Yoo, Andrew S.
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2021-01
- Volume
- 28
- Issue
- 1
- Pages
- 127-140.e9
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC7796891
- OpenAlex
- W3040771723
- Cited by
- 67
- References
- 84
- Citations by year
- 2026: 10 · 2025: 9 · 2024: 15 · 2023: 13 · 2022: 10 · 2021: 10
- FWCI
- 2.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Cure Alzheimer's Fund (4DP2NS083372)
- National Institute on Aging
- National Institute of Neurological Disorders and Stroke (R01NS107488, DP2NS083372)
- Edward Mallinckrodt, Jr. Foundation
- National Institutes of Health
- Alfred P. Sloan Foundation
- Paul G. Allen Frontiers Group
- National Institute of General Medical Sciences
- Vallee Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- fibroblast-to-neuron conversion, motor neurons, miR-124, KLF transcription factors, small nuclear RNA, chromatin accessibility, neuronal identity, cell fate conversion
- MeSH terms
- Cell Differentiation, Chromatin, Fibroblasts, Humans, Transcription Factors, MicroRNAs, Cellular Reprogramming
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