H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type
Summary: Dendritic protrusions, mainly spines and filopodia, correlate with excitatory synapses in pyramidal neurons (PyNs), but this relationship may not apply universally. We found that ectopic H-Ras expression increased protrusions across various cortical cell types, including layer 2/3 PyNs, par...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Sprog: | English |
Udgivet: |
Elsevier
2024-08-01
|
Serier: | iScience |
Fag: | |
Online adgang: | http://www.sciencedirect.com/science/article/pii/S2589004224017607 |
_version_ | 1827151748046782464 |
---|---|
author | Sarah Krüssel Ishana Deb Seungkyu Son Gabrielle Ewall Minhyeok Chang Hey-Kyoung Lee Won Do Heo Hyung-Bae Kwon |
author_facet | Sarah Krüssel Ishana Deb Seungkyu Son Gabrielle Ewall Minhyeok Chang Hey-Kyoung Lee Won Do Heo Hyung-Bae Kwon |
author_sort | Sarah Krüssel |
collection | DOAJ |
description | Summary: Dendritic protrusions, mainly spines and filopodia, correlate with excitatory synapses in pyramidal neurons (PyNs), but this relationship may not apply universally. We found that ectopic H-Ras expression increased protrusions across various cortical cell types, including layer 2/3 PyNs, parvalbumin (PV)-, and vasoactive intestinal peptide (VIP)-positive interneurons (INs) in the primary motor cortex. The probability of detecting protrusions correlated with local H-Ras activity, indicating its role in protrusion formation. H-Ras overexpression led to high turnover rates by adding protrusions. Two-photon photolysis of glutamate induced de novo spine formation in mature H-Ras expressing neurons, suggesting H-Ras’s effect is not limited to early development. In PyNs and PV-INs, but not VIP-INs, spine neck lengths shifted to filopodia-like phenotypes. H-Ras primarily induced filopodia in PyNs and spines in PV- and VIP-INs. Increased protrusions in H-Ras-transfected PyNs lacked key excitatory synaptic proteins and did not affect miniature excitatory postsynaptic currents (mEPSCs), suggesting multifaceted roles beyond excitatory synapses. |
first_indexed | 2025-03-20T21:54:54Z |
format | Article |
id | doaj.art-e96f56152e854cfcb15ef37f1e07f081 |
institution | Directory Open Access Journal |
issn | 2589-0042 |
language | English |
last_indexed | 2025-03-20T21:54:54Z |
publishDate | 2024-08-01 |
publisher | Elsevier |
record_format | Article |
series | iScience |
spelling | doaj.art-e96f56152e854cfcb15ef37f1e07f0812024-08-10T05:26:29ZengElsevieriScience2589-00422024-08-01278110535H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell typeSarah Krüssel0Ishana Deb1Seungkyu Son2Gabrielle Ewall3Minhyeok Chang4Hey-Kyoung Lee5Won Do Heo6Hyung-Bae Kwon7Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USADepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of KoreaSolomon H. Snyder Department of Neuroscience, Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins School of Medicine, Baltimore, MD, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Zanvyl-Krieger Mind/Brain Institute, Johns Hopkins School of Medicine, Baltimore, MD, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, USADepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of KoreaSolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Corresponding authorSummary: Dendritic protrusions, mainly spines and filopodia, correlate with excitatory synapses in pyramidal neurons (PyNs), but this relationship may not apply universally. We found that ectopic H-Ras expression increased protrusions across various cortical cell types, including layer 2/3 PyNs, parvalbumin (PV)-, and vasoactive intestinal peptide (VIP)-positive interneurons (INs) in the primary motor cortex. The probability of detecting protrusions correlated with local H-Ras activity, indicating its role in protrusion formation. H-Ras overexpression led to high turnover rates by adding protrusions. Two-photon photolysis of glutamate induced de novo spine formation in mature H-Ras expressing neurons, suggesting H-Ras’s effect is not limited to early development. In PyNs and PV-INs, but not VIP-INs, spine neck lengths shifted to filopodia-like phenotypes. H-Ras primarily induced filopodia in PyNs and spines in PV- and VIP-INs. Increased protrusions in H-Ras-transfected PyNs lacked key excitatory synaptic proteins and did not affect miniature excitatory postsynaptic currents (mEPSCs), suggesting multifaceted roles beyond excitatory synapses.http://www.sciencedirect.com/science/article/pii/S2589004224017607Molecular biologyNeuroscienceCell biology |
spellingShingle | Sarah Krüssel Ishana Deb Seungkyu Son Gabrielle Ewall Minhyeok Chang Hey-Kyoung Lee Won Do Heo Hyung-Bae Kwon H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type iScience Molecular biology Neuroscience Cell biology |
title | H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type |
title_full | H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type |
title_fullStr | H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type |
title_full_unstemmed | H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type |
title_short | H-Ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type |
title_sort | h ras induces exuberant de novo dendritic protrusion growth in mature neurons regardless of cell type |
topic | Molecular biology Neuroscience Cell biology |
url | http://www.sciencedirect.com/science/article/pii/S2589004224017607 |
work_keys_str_mv | AT sarahkrussel hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT ishanadeb hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT seungkyuson hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT gabrielleewall hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT minhyeokchang hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT heykyounglee hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT wondoheo hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype AT hyungbaekwon hrasinducesexuberantdenovodendriticprotrusiongrowthinmatureneuronsregardlessofcelltype |