Generation of serotonin neurons from human pluripotent stem cells.
- Authors
- Lu, Jianfeng; Zhong, Xuefei; Liu, Huisheng; Hao, Ling; Huang, Cindy Tzu-Ling; Sherafat, Mohammad Amin; Jones, Jeffrey; Ayala, Melvin; Li, Lingjun; Zhang, Su-Chun
- Year
- 2016
- Journal
- Nature biotechnology
- PMID
- 26655496
- DOI
- 10.1038/nbt.3435
- PMCID
- PMC4711820
Serotonin neurons located in the raphe nucleus of the hindbrain have crucial roles in regulating brain functions and have been implicated in various psychiatric disorders. Yet functional human serotonin neurons are not available for in vitro studies. Through manipulation of the WNT pathway, we demonstrate efficient differentiation of human pluripotent stem cells (hPSCs) to cells resembling central serotonin neurons, primarily those located in the rhombomeric segments 2-3 of the rostral raphe, which participate in high-order brain functions. The serotonin neurons express a series of molecules essential for serotonergic development, including tryptophan hydroxylase 2, exhibit typical electrophysiological properties and release serotonin in an activity-dependent manner. When treated with the FDA-approved drugs tramadol and escitalopram oxalate, they release or uptake serotonin in a dose- and time-dependent manner, suggesting the utility of these cells for the evaluation of drug candidates.
Specification of rostral hindbrain progenitors. (a) Schematic representation of human central serotonergic neuron generation process. (b) Regional markers along the anterior-posterior neuroaxis (A–P axis). (c) RT-PCR of regional neural markers along the A–P axis when cells were treated with different concentrations of CHIR99021 (n = 2). (d) Cells stained for typical regional markers when treated with different concentrations of CHIR99021. (e) Quantification of positively stained cells in d (n = 3). Data are represented as mean ± s.e.m. Scale bar, 50 µm. Ho, Hoechst staining; HFB, human fetal brain samples; CHIR, CHIR99021.
LLM interpretation
This figure illustrates the specification of rostral hindbrain progenitors using varying concentrations of CHIR99021. It includes a schematic of the neuron generation process (a), a map of regional markers along the A-P axis (b), and RT-PCR results (c) showing marker expression changes based on CHIR concentration. Immunofluorescence images (d) and corresponding quantification (e) demonstrate a shift from forebrain/midbrain markers (e.g., FOXG1, OTX2) to hindbrain markers (e.g., HOXB1, HOXB4, HOXA2) as CHIR99021 concentration increases from 0 to 3.0 $\mu$M.
Specification of ventral hindbrain progenitors. (a) Regional markers along the dorsal-ventral neuroaxis (D–V axis). (b) Q-PCR of regional markers along the D–V axis when cells were treated with different concentrations of SHH (n = 3). Data are represented as mean ± s.e.m. (c) Cells stained with typical regional markers when treated with different concentrations of SHH. (d) Quantification of positively stained cells in c (n = 3). Data are represented as mean ± s.e.m. (e–g) Cells stained for Ki67, NESTIN, SOX2, GATA2, SOX1 and GATA3 when treated with 1,000 ng/ml SHH. (h) FACS image of NKX2.2-expressing cells when treated with 1,000 ng/ml SHH. (i) Quantification of positively stained cells in f, g, k, l and m (n = 3). Data are represented as mean ± s.e.m. (j–m) Cells stained for NKX2.2, NKX6.1, OLIG2, PHOX2B, MASH1 and FOXA2 when treated with 1,000 ng/ml SHH. (n) Cells stained for PHOX2B, FOXA2 and TPH2, either untreated or treated with FGF4 in week 3 of differentiation. (o) Quantification of positively stained cells in n (n = 3). Data are represented as mean ± s.e.m. *P < 0.05, Student’s t-test. Scale bars, 50 µm. Ho, Hoechst staining.
LLM interpretation
This figure consists of a schematic diagram (a), multiple bar charts (b, d, i, o), immunofluorescence microscopy images (c, e–g, j–m, n), and a FACS histogram (h) analyzing ventral hindbrain progenitor specification. The data show that increasing concentrations of SHH (0, 100, 1,000 ng/ml) shift marker expression from dorsal (PAX3/7) to ventral (NKX6.1, NKX2.2) identities, as evidenced by Q-PCR and cell quantification. Additionally, FGF4 treatment increases the percentage of PHOX2B, FOXA2, and TPH2 positive cells, with statistical significance indicated by asterisks (*P < 0.05).
Generation of central serotonin neurons. (a) Cells stained for Tuj1, GFAP and Ki67 after 4 weeks of neuronal differentiation. (b) Quantification of positively stained cells in a (n = 3). Data are represented as mean ± s.e.m. (c) Cells stained for serotonin, TH and GABA after 4 weeks of neuronal differentiation. (d) Quantification of positively stained cells in c (n = 3). Data are represented as mean ± s.e.m. (e, f) Cells co-stained for Tuj1 and serotonin, TPH2, GATA3, GATA2, GATA3, AADC and VMAT2 after 4 weeks of neuronal differentiation. In e, arrowhead indicates VMAT2− cell, arrow indicates VMAT2+ cell; in f, arrowhead indicates AADC− cell, arrows indicate AADC+ cells, and asterisk marks Hoechst-stained nucleus. (g) Q-PCR of central serotonergic neuron markers FEV, LMX1B, TPH2 and SERT during neuronal differentiation (n = 3). Data are represented as mean ± s.e.m. (h) Western blot of central serotonin neuron markers FEV and SERT during neuronal differentiation. Scale bars, 50 µm. Ho, Hoechst staining; HFB, human fetal brain samples; ESC, human embryonic stem cells; D0, day 0; D7, day 7; D14, day 14. Full-length blots can be found in Supplementray Figure 5.
LLM interpretation
This figure demonstrates the generation of central serotonin neurons through a combination of microscopy, quantification, and molecular analysis. Panels (a, c, e, f) show immunofluorescence staining for neuronal (Tuj1), glial (GFAP), proliferative (Ki67), and serotonergic markers (Serotonin, TPH2, GATA3, GATA2, AADC, VMAT2), with corresponding bar charts in (b, d) quantifying positive cells across three cell lines (H9, GM14, GM15). Panel (g) uses bar charts to show the relative expression of serotonergic markers (FEV, LMX1B, TPH2, SERT) increasing from ESC to D7, and panel (h) provides a Western blot confirming the protein expression of FEV and SERT from D0 to D14.
Functional properties of the central serotonin neurons. (a) Representative hPSC-derived serotonergic neuron (stained with serotonin and injected with streptavidin-FITC) used for the electrophysiological assays. (b) Neurons displayed low rate of spontaneous action potential spiking with a subthreshold oscillatory potential (−30 mV). (c) Neurons displayed large action potential (AP) and after hyperpolarization (AHP), and long AHP duration. (d) Serotonin release from the neurons during neuronal maturation. Samples from hESCs (H9) (n = 4). (e) K+-induced serotonin release from the serotonin neurons (n = 3). *P < 0.05, Student’s t-test. N.D., not detectable. (f) Serotonin release in the presence of different dosages of tramadol (n = 3). (g) Serotonin release in the presence of different dosages of escitalopram oxalate (EO) (n = 3). (h, i) Time-dependent serotonin release of hESC H9-derived (h) or iPSC GM15-derived (i) central serotonergic neurons after being treated with 100 µM of tramadol, 100 µM of EO or the same quantity of DMSO (n = 3). Tramadol vs. DMSO: *P < 0.05; EO vs. DMSO: #P < 0.05; two-way analysis of variance. Data are represented as mean ± s.e.m. H9: human ESCs; GM14, GM15: human iPSCs. Scale bar, 50 µm.
LLM interpretation
This figure presents the functional characterization of hPSC-derived serotonergic neurons through multiple modalities. Panels (a-c) show a microscopy image of a serotonin-positive neuron and electrophysiological traces demonstrating spontaneous spiking and action potential (AP) properties. Panels (d-g) use line and bar graphs to show serotonin release increasing over maturation time, in response to high $\text{K}^+$, and dose-dependently with tramadol and escitalopram oxalate (EO). Panels (h-i) show time-dependent serotonin release in H9 and GM15 neurons treated with tramadol or EO compared to DMSO, with statistical significance indicated by * ($P < 0.05$) and # ($P < 0.05$).
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In this knowledge base
| Title | Year | PMID |
|---|---|---|
| Genetics of Alcohol Use Disorder: A Role for Induced Pluripotent Stem Cells? | 2018 | 29897633 |
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