Semaphorin 3F Is a Bifunctional Guidance Cue for Dopaminergic Axons and Controls Their Fasciculation, Channeling, Rostral Growth, and Intracortical Targeting
Open accessAbstract
Dopaminergic neurons in the mesodiencephalon (mdDA neurons) make precise synaptic connections with targets in the forebrain via the mesostriatal, mesolimbic, and mesoprefrontal pathways. Because of the functional importance of these remarkably complex ascending axon pathways and their implication in human disease, the mechanisms underlying the development of these connections are of considerable interest. Despite extensive in vitro studies, the molecular determinants that ensure the perfect formation of these pathways in vivo remain mostly unknown. Here, we determine the embryonic origin and ontogeny of the mouse mesoprefrontal pathway and use these data to reveal an unexpected requirement for semaphorin 3F (Sema3F) and its receptor neuropilin-2 (Npn-2) during mdDA pathway development using tissue culture approaches and analysis of sema3F−/−,npn-2−/−, and npn-2−/−;TH-Cre mice. We show that Sema3F is a bifunctional guidance cue for mdDA axons, some of which have the remarkable ability to regulate their responsiveness to Sema3F as they develop. During early developmental stages, Sema3F chemorepulsion controls previously uncharacterized aspects of mdDA pathway development through both Npn-2-dependent (axon fasciculation and channeling) and Npn-2-independent (rostral growth) mechanisms. Later on, chemoattraction mediated by Sema3F and Npn-2 is required to orient mdDA axon projections in the cortical plate of the medial prefrontal cortex. This latter finding demonstrates that regulation of axon orientation in the target field occurs by chemoattractive mechanisms, and this is likely to also apply to other neural systems. In all, this study provides a framework for additional dissection of the molecular basis of mdDA pathway development and disease.
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A subset of the medial part of the ventral tegmental area (VTA) starts to project to prefrontal subdomains around E15/E16 in rodent and week 10-13 in human.
“A subset of the medial part of the ventral tegmental area (VTA) starts to project to prefrontal subdomains around E15/E16 (rodent) and week 10–13 in human [155–158].”
From Development of prefrontal cortex (2022) · cites this paper as [156]
In “Development of mesoprefrontal mdDA axon projections in the mouse” (page unavailable), the paper traces axons from the rostral medial VTA to the medial prefrontal cortex and reports subplate innervation around E16. It does not give a human onset at weeks 10–13; its mention of human PFC concerns a previously reported waiting period, not that timing. (LLM, conf=0.88)
Experimental — accuracy not yet measuredSemaphorin3F orchestrates the fasciculation, rostral growth and targeting of dopaminergic projections within the various mPFC subdomains.
“while Semaphorin3F is orchestrating their fasciculation, rostral growth and targeting within the various mPFC subdomains [156].”
From Development of prefrontal cortex (2022) · cites this paper as [156]
The Figure 7 and Figure 8 legends report defasciculation and impaired rostral growth of dopaminergic axons in sema3F-deficient mice. The section on aberrant intracortical targeting reports disrupted axon targeting within the mPFC, but it describes cortical zones and axon distribution rather than targeting across distinct mPFC subdomains. (LLM, conf=0.82)
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Mest/Peg1 Is Essential for the Development and Maintenance of a SNc Neuronal Subset
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Establishing functionally segregated dopaminergic circuits
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Tcf4 Is Involved in Subset Specification of Mesodiencephalic Dopaminergic Neurons
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MicroRNA-338 modulates cortical neuronal placement and polarity
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Self-citationView Point: Semaphorin-3E: An Emerging Modulator of Natural Killer Cell Functions?
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Polymethacryloyl-L-Phenylalanine [PMAPA]-Based Monolithic Column for Capillary Electrochromatography
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Transplantation in the nonhuman primate MPTP model of Parkinson's disease: update and perspectives
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Dynamic Insights into Dopamine Axon Growth in Adolescence and its Implications for Psychiatric Risk
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Circular RNAs regulate neuron size and migration of midbrain dopamine neurons during development
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Fibroblast Growth Factor: Promising Target for Schizophrenia
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Tgfbr2 in Dental Pulp Cells Guides Neurite Outgrowth in Developing Teeth
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Functions of Neuropilins in Wiring the Nervous System and Their Role in Neurological Disorders
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Grealish, S. (2012) · Lund University Publications (Lund University)
- Authors
- Kolk, S. M., Gunput, R.-A. F., Tran, T. S., van den Heuvel, D. M. A., Prasad, A. A., Hellemons, A. J. C. G. M., Adolfs, Y., Ginty, D. D., Kolodkin, A. L., Burbach, J. P. H., Smidt, M. P., & Pasterkamp, R. J.
- Affiliations
- University Medical Center Utrecht (NL)
- Utrecht University (NL)
- Howard Hughes Medical Institute (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-10-07
- Volume
- 29
- Issue
- 40
- Pages
- 12542-12557
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3097132
- OpenAlex
- W2142820387
- Cited by
- 114
- References
- 77
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 5 · 2023: 6 · 2022: 4 · 2021: 8 · 2020: 7 · 2019: 8 · 2018: 3 · 2017: 13 · 2016: 2 · 2015: 8 · 2014: 6 · 2013: 11 · 2012: 12
- FWCI
- 3.74
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- Howard Hughes Medical Institute
- National Alliance for Research on Schizophrenia and Depression
- Parkinsonfonden
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Keywords
- SEMA3F, neuropilin-2, axon fasciculation, chemoattraction, chemorepulsion, axon targeting, medial prefrontal cortex, axon orientation, dopaminergic neuron development
- MeSH terms
- Animals, Axons, Diencephalon, Dopamine, Immunohistochemistry, Membrane Proteins, Mice, Inbred C57BL, Mice, Mutant Strains, Nerve Tissue Proteins, Neurons, Neurites, Prosencephalon, Body Patterning, Protein Transport, Neuropilin-2, Tissue Culture Techniques, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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