Impairment of Human Dopaminergic Neurons at Different Developmental Stages by Perfluoro-Octanoic Acid (PFOA) and Differential Human Brain Areas Accumulation of Perfluoroalkyl Chemicals
Open accessAbstract
Perfluoroalkyl substances (PFASs) are synthetic chemicals widely used in industrial and consumer products. The environmental spreading of PFASs raises concerns for their impact on human health. In particular, the bioaccumulation in humans due to environmental exposure has been reported also in total brain samples and PFAS exposure has been associated with neurodevelopmental disorders. In this study we aimed to investigate the specific PFAS bioaccumulation in different brain areas. Our data reported major accumulation in the brainstem region, which is richly populated by dopaminergic neurons (DNs), in brain autopsy samples from people resident in a PFAS-polluted area of Italy. Since DNs are the main source of dopamine (DA) in the mammalian central nervous system (CNS), we evaluated the possible functional consequences of perfluoro-octanoic acid (PFOA) exposure in a human model of DNs obtained by differentiation of human induced pluripotent stem cells (hiPSCs). Particularly, we analyzed the specific effect of the exposure to PFOA for 24 h, at the concentration of 10 ng/ml, at 3 different steps of dopaminergic differentiation: the neuronal commitment phase (DP1), the neuronal precursor phase (DP2) and the mature dopaminergic differentiation phase (DP3). Interestingly, compared to untreated cells, exposure to PFOA was associated with a reduced expression of Tyrosine Hydroxylase (TH) and Neurofilament Heavy (NFH), both markers of dopaminergic maturation at DP2 phase. In addition, cells at DP3 phase exposed to PFOA showed a severe reduction in the expression of the Dopamine Transporter (DAT), functionally involved in pre-synaptic dopamine reuptake. In this proof-of-concept study we show a significant impact of PFOA exposure, mainly on the most sensitive stage of neural dopaminergic differentiation, prompting the way for further investigations more directly relevant to risk assessment of these chemicals.
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Both rodent and human brain studies reported brain-region-specific accumulation of PFAS, with increased exposure in the hypothalamus and decreased exposure in the cortex.
“both studies reported brain-region-specific accumulation, demonstrating increased exposure in the hypothalamus and decreased exposure in the cortex (Austin et al., 2003; Di Nisio et al., 2022).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Di Nisio et al., 2022
Section 3.1 and the Discussion report region-specific PFAS accumulation in human brains, with particularly high concentrations in the hypothalamus. Table 1 shows a lower concentration in the frontal lobe than in the hypothalamus, but the paper does not establish decreased exposure across the cortex as a whole. Its Introduction mentions rodent brain-region accumulation but does not give the claimed directional comparison for rodents. (LLM, conf=0.82)
Experimental — accuracy not yet measuredStudies in a rodent model and human brain samples showed a similar pattern of brain distribution for PFOS, PFHxS, and PFHxA as was seen in polar bears.
“Studies in a rodent model and human brain samples showed a similar pattern of distribution in the brain for PFOS, perfluorohexanesulfonic acid (PFHxS), and perfluorohexanoic acid (PFHxA) as was seen in the polar bears.”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Di Nisio et al., 2022
Section 3.1 reports regional accumulation of PFHxS and PFHxA in human brain samples, and the Introduction cites animal studies of PFOS accumulation in specific brain areas. But Section 3.1 says PFOS was detectable only in blood, not in the human brain samples. The paper does not establish that the three chemicals had a similar brain-distribution pattern across rodents, humans, and polar bears. (LLM, conf=0.84)
Experimental — accuracy not yet measuredDisruptions in Ca2+ homeostasis and its signaling pathways likely contribute to other PFAS-associated changes in neurophysiology, including alterations in neuron structure, signaling, and neuronal cell death.
“Disruptions in Ca2+ homeostasis and its signaling pathways likely contribute to other PFAS associated changes in neurophysiology, including alterations in neuron structure, signaling, and even neuronal cell death”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Di Nisio et al., 2022
The Results (section 3.3; page unavailable) report that PFOA exposure reduced markers of neuronal differentiation and dopaminergic function. The Discussion (section 4; page unavailable) also describes PFAS-associated neuronal cell death. Neither passage links these effects to disrupted Ca2+ homeostasis or Ca2+ signaling, so the claim’s proposed mechanism is unsupported by this paper. (LLM, conf=0.87)
Experimental — accuracy not yet measuredDi Nisio et al. (2022) analyzed PFOA, PFHxS, and PFHxA concentrations across brain regions in 5 deceased human male subjects and found the greatest concentrations in the hypothalamus across all compounds (206.93 ± 78.23 ng/g).
“Similarly, Di Nisio et al. (2022) analyzed PFOA, PFHxS, and PFHxA concentrations across brain regions in 5 deceased human male subjects and found the greatest concentrations in the hypothalamus across all compounds (206.93 ± 78.23 ng/g).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Di Nisio et al., 2022
In Di Nisio et al. (2022), the lowest overall PFAS concentrations were found in the thalamus (19.75 ± 6.73 ng/g), midbrain (24.01 ± 6.65 ng/g), and frontal lobe (29.58 ± 10.73 ng/g).
“the lowest overall PFAS concentrations were found in the thalamus (19.75 ± 6.73 ng/g), midbrain (24.01 ± 6.65 ng/g), and frontal lobe (29.58 ± 10.73 ng/g).”
From A Critical Review and Meta-Analysis of Impacts of Per- and Polyfluorinated Substances on the Brain and Behavior (2022) · cites this paper as Di Nisio et al., 2022
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- Authors
- Di Nisio, A., Pannella, M., Vogiatzis, S., Sut, S., Dall'Acqua, S., Rocca, M. S., Antonini, A., Porzionato, A., De Caro, R., Bortolozzi, M., Toni, L. D., & Foresta, C.
- Affiliations
- University of Padua (IT)
- Corresponding author
- Toni, Luca De
- ORCID
- Venue
- Environment International
- Publisher
- Elsevier BV
- Published
- 2022-01
- Volume
- 158
- Pages
- 106982
- ISSN
- 0160-4120 (ISSN-L)
- OpenAlex
- W3213236989
- Cited by
- 103
- References
- 64
- Citations by year
- 2026: 26 · 2025: 30 · 2024: 22 · 2023: 15 · 2022: 10
- FWCI
- 4.43
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Environment International (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Padua Research Archive (University of Padova) (submittedVersion, cc-by)
- Funders
- Università degli Studi di Padova
- Topics
- Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmaceutical Science › Fluorine in Organic Chemistry
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- perfluorinated compounds, dopaminergic neurons, dopaminergic differentiation, human induced pluripotent stem cells, brainstem, PFAS bioaccumulation, tyrosine hydroxylase, neurofilament heavy chain, dopamine transporter, neurodevelopmental disorders, PFAS exposure, neurotoxicity
- MeSH terms
- Animals, Brain, Caprylates, Fluorocarbons, Humans, Alkanesulfonic Acids, Induced Pluripotent Stem Cells, Dopaminergic Neurons
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