The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity
From fly to man, the Wingless (Wg)/Wnt signaling molecule is essential for both the stability and plasticity of the nervous system. The Drosophila neuromuscular junction (NMJ) has proven to be a useful system for deciphering the role of Wg in directing activity-dependent synaptic plasticity (ADSP),...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-04-01
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| Series: | Frontiers in Synaptic Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnsyn.2024.1322771/full |
| _version_ | 1797226489773555712 |
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| author | Carihann Dominicci-Cotto Carihann Dominicci-Cotto Mariam Vazquez Mariam Vazquez Bruno Marie Bruno Marie Bruno Marie |
| author_facet | Carihann Dominicci-Cotto Carihann Dominicci-Cotto Mariam Vazquez Mariam Vazquez Bruno Marie Bruno Marie Bruno Marie |
| author_sort | Carihann Dominicci-Cotto |
| collection | DOAJ |
| description | From fly to man, the Wingless (Wg)/Wnt signaling molecule is essential for both the stability and plasticity of the nervous system. The Drosophila neuromuscular junction (NMJ) has proven to be a useful system for deciphering the role of Wg in directing activity-dependent synaptic plasticity (ADSP), which, in the motoneuron, has been shown to be dependent on both the canonical and the noncanonical calcium Wg pathways. Here we show that the noncanonical planar cell polarity (PCP) pathway is an essential component of the Wg signaling system controlling plasticity at the motoneuron synapse. We present evidence that disturbing the PCP pathway leads to a perturbation in ADSP. We first show that a PCP-specific allele of disheveled (dsh) affects the de novo synaptic structures produced during ADSP. We then show that the Rho GTPases downstream of Dsh in the PCP pathway are also involved in regulating the morphological changes that take place after repeated stimulation. Finally, we show that Jun kinase is essential for this phenomenon, whereas we found no indication of the involvement of the transcription factor complex AP1 (Jun/Fos). This work shows the involvement of the neuronal PCP signaling pathway in supporting ADSP. Because we find that AP1 mutants can perform ADSP adequately, we hypothesize that, upon Wg activation, the Rho GTPases and Jun kinase are involved locally at the synapse, in instructing cytoskeletal dynamics responsible for the appearance of the morphological changes occurring during ADSP. |
| first_indexed | 2024-04-24T14:25:44Z |
| format | Article |
| id | doaj.art-6e6f2414b6104e71ba1bd9c456765ca4 |
| institution | Directory Open Access Journal |
| issn | 1663-3563 |
| language | English |
| last_indexed | 2024-04-24T14:25:44Z |
| publishDate | 2024-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Synaptic Neuroscience |
| spelling | doaj.art-6e6f2414b6104e71ba1bd9c456765ca42024-04-03T04:52:13ZengFrontiers Media S.A.Frontiers in Synaptic Neuroscience1663-35632024-04-011610.3389/fnsyn.2024.13227711322771The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticityCarihann Dominicci-Cotto0Carihann Dominicci-Cotto1Mariam Vazquez2Mariam Vazquez3Bruno Marie4Bruno Marie5Bruno Marie6Department of Anatomy and Neurobiology, Medical Sciences Campus, University of Puerto Rico, San Juan, PR, United StatesInstitute of Neurobiology, Medical Sciences Campus, University of Puerto Rico, San Juan, PR, United StatesInstitute of Neurobiology, Medical Sciences Campus, University of Puerto Rico, San Juan, PR, United StatesMolecular Sciences Research Center, University of Puerto Rico, San Juan, PR, United StatesDepartment of Anatomy and Neurobiology, Medical Sciences Campus, University of Puerto Rico, San Juan, PR, United StatesInstitute of Neurobiology, Medical Sciences Campus, University of Puerto Rico, San Juan, PR, United StatesMolecular Sciences Research Center, University of Puerto Rico, San Juan, PR, United StatesFrom fly to man, the Wingless (Wg)/Wnt signaling molecule is essential for both the stability and plasticity of the nervous system. The Drosophila neuromuscular junction (NMJ) has proven to be a useful system for deciphering the role of Wg in directing activity-dependent synaptic plasticity (ADSP), which, in the motoneuron, has been shown to be dependent on both the canonical and the noncanonical calcium Wg pathways. Here we show that the noncanonical planar cell polarity (PCP) pathway is an essential component of the Wg signaling system controlling plasticity at the motoneuron synapse. We present evidence that disturbing the PCP pathway leads to a perturbation in ADSP. We first show that a PCP-specific allele of disheveled (dsh) affects the de novo synaptic structures produced during ADSP. We then show that the Rho GTPases downstream of Dsh in the PCP pathway are also involved in regulating the morphological changes that take place after repeated stimulation. Finally, we show that Jun kinase is essential for this phenomenon, whereas we found no indication of the involvement of the transcription factor complex AP1 (Jun/Fos). This work shows the involvement of the neuronal PCP signaling pathway in supporting ADSP. Because we find that AP1 mutants can perform ADSP adequately, we hypothesize that, upon Wg activation, the Rho GTPases and Jun kinase are involved locally at the synapse, in instructing cytoskeletal dynamics responsible for the appearance of the morphological changes occurring during ADSP.https://www.frontiersin.org/articles/10.3389/fnsyn.2024.1322771/fullNMJdisheveledRho1Rac1Cdc42Jun kinase |
| spellingShingle | Carihann Dominicci-Cotto Carihann Dominicci-Cotto Mariam Vazquez Mariam Vazquez Bruno Marie Bruno Marie Bruno Marie The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity Frontiers in Synaptic Neuroscience NMJ disheveled Rho1 Rac1 Cdc42 Jun kinase |
| title | The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity |
| title_full | The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity |
| title_fullStr | The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity |
| title_full_unstemmed | The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity |
| title_short | The Wingless planar cell polarity pathway is essential for optimal activity-dependent synaptic plasticity |
| title_sort | wingless planar cell polarity pathway is essential for optimal activity dependent synaptic plasticity |
| topic | NMJ disheveled Rho1 Rac1 Cdc42 Jun kinase |
| url | https://www.frontiersin.org/articles/10.3389/fnsyn.2024.1322771/full |
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