Role of astroglia in Down’s syndrome revealed by patient-derived human-induced pluripotent stem cells
Open accessAbstract
Down’s syndrome (DS), caused by trisomy of human chromosome 21, is the most common genetic cause of intellectual disability. Here we use induced pluripotent stem cells (iPSCs) derived from DS patients to identify a role for astrocytes in DS pathogenesis. DS astroglia exhibit higher levels of reactive oxygen species and lower levels of synaptogenic molecules. Astrocyte-conditioned medium collected from DS astroglia causes toxicity to neurons, and fails to promote neuronal ion channel maturation and synapse formation. Transplantation studies show that DS astroglia do not promote neurogenesis of endogenous neural stem cells in vivo. We also observed abnormal gene expression profiles from DS astroglia. Finally, we show that the FDA-approved antibiotic drug, minocycline, partially corrects the pathological phenotypes of DS astroglia by specifically modulating the expression of S100B, GFAP, inducible nitric oxide synthase, and thrombospondins 1 and 2 in DS astroglia. Our studies shed light on the pathogenesis and possible treatment of DS by targeting astrocytes with a clinically available drug. Down’s syndrome is characterized by intellectual disability and other neuropathological symptoms. Here, the authors show that astroglia derived from induced pluripotent stem cells from Down’s syndrome patients impair the development of neurons, and that this can be attenuated with the drug minocycline.
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When cultured long enough to enable the generation of astrocytes, trisomy 21 induced pluripotent stem cells generate more astrocytes than control induced pluripotent stem cells, concomitant with a reduction in the generation of neurons.
“Similarly, when cultured for long enough to enable the generation of astrocytes, T21 iPSCs generate more of this cell type than control iPSCs, concomitant with a reduction in the generation of neurons79,82,96,103.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [82]
The Results (Generation and differentiation of DS patient-specific hiPSCs) report that, under spontaneous differentiation, DS iPSC-derived progenitors produced more astroglia and fewer neurons than controls. The claim omits that condition: the same section reports no significant difference between DS and control lines under directed differentiation, so culturing long enough to generate astrocytes does not by itself describe the finding. (LLM, conf=0.85)
Experimental — accuracy not yet measuredCo-culture with T21 iPSC-derived astrocytes reduces the intrinsic excitability of neurons and tends to have a consequent impact on synaptic development and transmission.
“Co-culture with T21 iPSC-derived astrocytes also reduces the intrinsic excitability of neurons and tends to have a consequent impact on synaptic development and transmission82,135,145.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [82]
The Results section, “Effects of DS astroglia on neuron synapses and ion channels” (page unavailable), reports less robust action-potential firing and no recorded synaptic activity in neurons given Down syndrome astroglial conditioned medium than in neurons given control medium. The Discussion also says that this medium fails to promote neuronal maturation and synapse formation. The experiments described used conditioned medium rather than direct co-culture, and the paper does not establish that reduced excitability caused the synaptic effects. (LLM, conf=0.85)
Experimental — accuracy not yet measuredTrisomic iPSCs show significant increase in astrocyte differentiation.
“A significant increase in astrocytes differentiated from trisomic iPSCs has been reported many times (Briggs et al., 2013; Chen et al., 2014; Hibaoui et al., 2014; Real et al., 2018; Mollo et al., 2021).”
From Neurodevelopment in Down syndrome: Concordance in humans and models (2022) · cites this paper as Chen et al., 2014
In Results (‘Confirmation of phenotypes of DS astroglia by isogenic iPSCs’; page not provided), the paper reports significantly more astroglia from trisomic than disomic cells under spontaneous differentiation. But Results (‘Generation and differentiation of DS patient-specific hiPSCs’; page not provided) reports no significant difference under directed differentiation, so the unqualified claim is broader than the finding. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn one study, directed differentiation of trisomy 21 and euploid induced pluripotent stem cells showed no significant differences in neuron production between genotypes, but spontaneous differentiation of the same cell lines produced a significantly decreased percentage of neurons in trisomic lines.
“Interestingly, in one study, when neurons were generated from T21 and euploid iPSCs through directed differentiation, no significant differences in neuron production between genotypes were detected, but when the same cell lines were allowed to spontaneously differentiate, the trisomic lines produced a significantly decreased percentage of neurons82.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [82]
Astrocytes play a role in regulating neuronal function in Down syndrome pathogenesis.
“This study identifies a role for astrocytes in regulating neuronal function in Down syndrome pathogenesis using trisomy 21 iPSC-derived neurons and astrocytes in co-cultures, drug treatment and chimeric mouse brains.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [82]
A separate study also found an increase in immunoreactivity of GFAP and the astrocytes showed a more activated morphology compared to control tissue in Down syndrome.
“A separate study also found an increase in immunoreactivity of GFAP and the astrocytes showed a more activated morphology compared to control tissue (Chen et al., 2014).”
From Neurodevelopment in Down syndrome: Concordance in humans and models (2022) · cites this paper as Chen et al., 2014
In directed differentiation, no difference in neuron production; in spontaneous differentiation, trisomic lines produced decreased percentage of neurons.
“Interestingly, in a study where age matched trisomic and euploid iPSCs underwent directed differentiation into neurons, there was no significant difference in neuron production between genotypes. However, if the same cell lines were allowed to spontaneously differentiate, the trisomic lines produced a significantly decreased percentage of neurons (Chen et al., 2014).”
From Neurodevelopment in Down syndrome: Concordance in humans and models (2022) · cites this paper as Chen et al., 2014
No difference in electrical properties between trisomic and euploid neurons.
“This finding was repeated using age-matched cell lines that again found no difference in electrical properties between trisomic and euploid neurons (Chen et al., 2014).”
From Neurodevelopment in Down syndrome: Concordance in humans and models (2022) · cites this paper as Chen et al., 2014
Trisomic neurons exhibit decreased neurite length.
“Finally in a third study using age matched iPSC lines, trisomic neurons again exhibited significantly decreased neurite length compared to control lines (Chen et al., 2014).”
From Neurodevelopment in Down syndrome: Concordance in humans and models (2022) · cites this paper as Chen et al., 2014
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Robust induction of functional astrocytes using NGN2 expression in human pluripotent stem cells
Berryer, M. H., Tegtmeyer, M., Binan, L., Valakh, V., Nathanson, A. J., Trendafilova, D., Crouse, E., Klein, J. A., Meyer, D., Pietiläinen, O. P. H., et al. (2023) · iScience · doi:10.1016/j.isci.2023.106995 · Cited by 22 · see citing works
- Authors
- Chen, C., Jiang, P., Xue, H., Peterson, S. E., Tran, H. T., McCann, A. E., Parast, M. M., Li, S., Pleasure, D. E., Laurent, L. C., Loring, J. F., Liu, Y., & Deng, W.
- Affiliations
- Tianjin Medical University General Hospital (CN)
- Shriners Hospitals for Children - Northern California (US)
- Scripps Research Institute (US)
- University of California San Diego (US)
- Brown Foundation Institute of Molecular Medicine for the Prevention of Human Diseases (US)
- Corresponding author
- Liu, Ying
- Deng, Wenbin
- ORCID
- Venue
- Nature Communications
- Published
- 2014-07-18
- Volume
- 5
- Issue
- 1
- Pages
- 4430-4430
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC4109022
- OpenAlex
- W2105352010
- Cited by
- 219
- References
- 70
- Citations by year
- 2026: 5 · 2025: 17 · 2024: 16 · 2023: 21 · 2022: 27 · 2021: 17 · 2020: 24 · 2019: 14 · 2018: 23 · 2017: 18 · 2016: 17 · 2015: 18 · 2014: 2
- FWCI
- 18.24
- Type
- journal article
- Language
- en
- Update notices
- correction (2020-02-21)
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature Communications (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, other-oa)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Multiple Sclerosis Society
- California Institute for Regenerative Medicine (RT1-01108, CL1‐00502, TR1-01250)
- Hartwell Foundation
- California Institute of Regenerative Medicine (CL1-00502)
- Shriners Hospitals for Children
- Multiple Sclerosis Society
- National Institutes of Health (R01NS061983 and R01ES015988, R01NS061983)
- University of California, Davis
- National Institute of Mental Health (R21MH087925)
- National Institute of Neurological Disorders and Stroke (R01NS061983)
- National Institute of Environmental Health Sciences (R01ES015988)
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD001259, K12HD001259)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Down syndrome and intellectual disability research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- Down syndrome, astrocytes, astroglia, patient-derived induced pluripotent stem cells, reactive oxygen species, synaptogenesis, astrocyte-conditioned medium, neurotoxicity, neurogenesis, neural stem cells, minocycline, S100B, glial fibrillary acidic protein, inducible nitric oxide synthase, thrombospondin, intellectual disability, astrocyte transplantation
- MeSH terms
- Thrombospondin 2, Animals, Astrocytes, Cell Differentiation, Cell Survival, Down Syndrome, Glial Fibrillary Acidic Protein, Humans, Mice, Inbred C57BL, Mice, Mutant Strains, Minocycline, Neurons, Case-Control Studies, Culture Media, Conditioned, Cell Transplantation, Homeodomain Proteins, Thrombospondins, Thrombospondin 1, Gene Expression Profiling, Nitric Oxide Synthase Type II, Induced Pluripotent Stem Cells, Neural Stem Cells, S100 Calcium Binding Protein beta Subunit
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