Dendrite tapering actuates a self-organizing signaling circuit for stochastic filopodia initiation in neurons

DC FieldValueLanguage
dc.contributor.authorMancinelli, Gloria
dc.contributor.authorLamparter, Lucas
dc.contributor.authorNosov, Georgii
dc.contributor.authorSaha, Tanumoy
dc.contributor.authorPawluchin, Anna
dc.contributor.authorKurre, Rainer
dc.contributor.authorRasch, Christiane
dc.contributor.authorEbrahimkutty, Mirsana
dc.contributor.authorKlingauf, Juergen
dc.contributor.authorGalic, Milos
dc.date.accessioned2021-12-23T16:06:55Z-
dc.date.available2021-12-23T16:06:55Z-
dc.date.issued2021
dc.identifier.issn00278424
dc.identifier.urihttps://osnascholar.ub.uni-osnabrueck.de/handle/unios/7616-
dc.description.abstractHow signaling units spontaneously arise from a noisy cellular background is not well understood. Here, we show that stochastic membrane deformations can nucleate exploratory dendritic filopodia, dynamic actin-rich structures used by neurons to sample its surroundings for compatible transcellular contacts. A theoretical analysis demonstrates that corecruitment of positive and negative curvature-sensitive proteins to deformed membranes minimizes the free energy of the system, allowing the formation of longlived curved membrane sections from stochastic membrane fluctuations. Quantitative experiments show that once recruited, curvature-sensitive proteins form a signaling circuit composed of interlinked positive and negative actin-regulatory feedback loops. As the positive but not the negative feedback loop can sense the dendrite diameter, this self-organizing circuit determines filopodia initiation frequency along tapering dendrites. Together, our findings identify a receptor-independent signaling circuit that employs random membrane deformations to simultaneously elicit and limit formation of exploratory filopodia to distal dendritic sites of developing neurons.
dc.description.sponsorshipGerman Research Foundation (DFG)German Research Foundation (DFG) [CRC1348/A06, CRC 944/P22, GA 2268/4-1]; Medical Faculty of the University of Munster [IZKF Ga3/016/21]; DFGGerman Research Foundation (DFG)European Commission [CRC1348/A02, CRC944/P5, PI 405/14-1]; We thank Lukas Funke, Anastasiia Sokolova, and Katrin Tkotz for technical support. We further thank members of the M.G., Matis, and J.K. laboratories for critical feedback and discussion. M.G. acknowledges funding from the German Research Foundation (DFG) (CRC1348/A06, CRC 944/P22, GA 2268/4-1) and the Medical Faculty of the University of M_unster (IZKF Ga3/016/21). J.K. acknowledges funding from the DFG (CRC1348/A02, CRC944/P5). The imaging facility Integrated Bioimaging Facility Osnabr_uck was funded by the DFG as a core facility (PI 405/14-1).
dc.language.isoen
dc.publisherNATL ACAD SCIENCES
dc.relation.ispartofPROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
dc.subjectACTIN DYNAMICS
dc.subjectACTIVATION
dc.subjectBAR domain
dc.subjectCDC42
dc.subjectfilopodia
dc.subjectINHIBITION
dc.subjectIRSP53
dc.subjectMECHANISMS
dc.subjectMEMBRANE
dc.subjectmembrane curvature
dc.subjectMORPHOGENESIS
dc.subjectMultidisciplinary Sciences
dc.subjectneuron
dc.subjectScience & Technology - Other Topics
dc.subjectself-organization
dc.subjectSPINES
dc.subjectSYNAPTOGENESIS
dc.titleDendrite tapering actuates a self-organizing signaling circuit for stochastic filopodia initiation in neurons
dc.typejournal article
dc.identifier.doi10.1073/pnas.2106921118j1of9
dc.identifier.isiISI:000715115300016
dc.description.volume118
dc.description.issue43
dc.contributor.orcid0000-0002-4493-2542
dc.publisher.place2101 CONSTITUTION AVE NW, WASHINGTON, DC 20418 USA
dcterms.isPartOf.abbreviationProc. Natl. Acad. Sci. U. S. A.
crisitem.author.deptFB 05 - Biologie/Chemie-
crisitem.author.deptidfb05-
crisitem.author.orcid0000-0002-6872-6567-
crisitem.author.parentorgUniversität Osnabrück-
crisitem.author.netidKuRa617-
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