Antagonistic Action of Siah2 and Pard3/JamC to Promote Germinal Zone Exit of Differentiated Cerebellar Granule Neurons by Modulating Ntn1 Signaling Via Dcc

Overview

Journal Res Sq

Date 2024 Oct 14

PMID 39399669

Authors

Christophe Laumonnerie

Maleelo Shamambo

Daniel R Stabley

Tommy L Lewis Jr

Niraj Trivedi

Danielle Howell

David J Solecki

Affiliations

Soon will be listed here.

Abstract

Exiting a germinal zone (GZ) initiates a cascade of events that promote neuronal maturation and circuit assembly. Developing neurons and their progenitors must interpret various niche signals-such as morphogens, guidance molecules, extracellular matrix components, and adhesive cues-to navigate this region. How differentiating neurons integrate and adapt to multiple cell-extrinsic niche cues with their cell-intrinsic machinery in exiting a GZ is unknown. We establish cooperation between cell polarity-regulated adhesion and Netrin-1 (Ntn-1) signaling comprises a coincidence detection circuit repelling maturing neurons from their GZ. In this circuit, the Partitioning defective 3 (Pard3) polarity protein and Junctional adhesion molecule-C (JamC) adhesion protein promote, while the Seven in absentia 2 (Siah2) ubiquitin ligase inhibits, Deleted in colorectal cancer (Dcc) receptor surface recruitment to gate differentiation linked repulsion to GZ Ntn-1. These results demonstrate cell polarity as a central integrator of adhesive- and guidance cues cooperating to spur GZ exit.

References

Hatten M . Central nervous system neuronal migration. Annu Rev Neurosci. 1999; 22:511-39. DOI: 10.1146/annurev.neuro.22.1.511. View

Miesenbock G, De Angelis D, Rothman J . Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature. 1998; 394(6689):192-5. DOI: 10.1038/28190. View

Kullmann J, Trivedi N, Howell D, Laumonnerie C, Nguyen V, Banerjee S . Oxygen Tension and the VHL-Hif1α Pathway Determine Onset of Neuronal Polarization and Cerebellar Germinal Zone Exit. Neuron. 2020; 106(4):607-623.e5. PMC: 7244394. DOI: 10.1016/j.neuron.2020.02.025. View

Poliak S, Morales D, Croteau L, Krawchuk D, Palmesino E, Morton S . Synergistic integration of Netrin and ephrin axon guidance signals by spinal motor neurons. Elife. 2015; 4. PMC: 4764565. DOI: 10.7554/eLife.10841. View

Ong T, Trivedi N, Wakefield R, Frase S, Solecki D . Siah2 integrates mitogenic and extracellular matrix signals linking neuronal progenitor ciliogenesis with germinal zone occupancy. Nat Commun. 2020; 11(1):5312. PMC: 7576183. DOI: 10.1038/s41467-020-19063-7. View

van den Berghe V, Stappers E, Vandesande B, Dimidschstein J, Kroes R, Francis A . Directed migration of cortical interneurons depends on the cell-autonomous action of Sip1. Neuron. 2013; 77(1):70-82. DOI: 10.1016/j.neuron.2012.11.009. View

Ackerman S, Kozak L, Przyborski S, Rund L, Boyer B, Knowles B . The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature. 1997; 386(6627):838-42. DOI: 10.1038/386838a0. View

Ebnet K, Suzuki A, Horikoshi Y, Hirose T, Meyer Zu Brickwedde M, Ohno S . The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J. 2001; 20(14):3738-48. PMC: 125258. DOI: 10.1093/emboj/20.14.3738. View

Xu K, Wu Z, Renier N, Antipenko A, Tzvetkova-Robev D, Xu Y . Neural migration. Structures of netrin-1 bound to two receptors provide insight into its axon guidance mechanism. Science. 2014; 344(6189):1275-9. PMC: 4369087. DOI: 10.1126/science.1255149. View

10.

Hu G, Zhang S, Vidal M, BAER J, Xu T, Fearon E . Mammalian homologs of seven in absentia regulate DCC via the ubiquitin-proteasome pathway. Genes Dev. 1997; 11(20):2701-14. PMC: 316613. DOI: 10.1101/gad.11.20.2701. View

11.

Plooster M, Menon S, Winkle C, Urbina F, Monkiewicz C, Phend K . TRIM9-dependent ubiquitination of DCC constrains kinase signaling, exocytosis, and axon branching. Mol Biol Cell. 2017; 28(18):2374-2385. PMC: 5576901. DOI: 10.1091/mbc.E16-08-0594. View

12.

Adler C, Fetter R, Bargmann C . UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci. 2006; 9(4):511-8. PMC: 2613020. DOI: 10.1038/nn1666. View

13.

Alcantara S, Ruiz M, de Castro F, Soriano E, Sotelo C . Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development. 2000; 127(7):1359-72. DOI: 10.1242/dev.127.7.1359. View

14.

Famulski J, Trivedi N, Howell D, Yang Y, Tong Y, Gilbertson R . Siah regulation of Pard3A controls neuronal cell adhesion during germinal zone exit. Science. 2010; 330(6012):1834-8. PMC: 3065828. DOI: 10.1126/science.1198480. View

15.

Yung A, Nishitani A, Goodrich L . Phenotypic analysis of mice completely lacking netrin 1. Development. 2015; 142(21):3686-91. PMC: 4647218. DOI: 10.1242/dev.128942. View

16.

Dominici C, Moreno-Bravo J, Puiggros S, Rappeneau Q, Rama N, Vieugue P . Floor-plate-derived netrin-1 is dispensable for commissural axon guidance. Nature. 2017; 545(7654):350-354. PMC: 5438598. DOI: 10.1038/nature22331. View

17.

Palmesino E, Rousso D, Kao T, Klar A, Laufer E, Uemura O . Foxp1 and lhx1 coordinate motor neuron migration with axon trajectory choice by gating Reelin signalling. PLoS Biol. 2010; 8(8):e1000446. PMC: 2919418. DOI: 10.1371/journal.pbio.1000446. View

18.

House C, Frew I, Huang H, Wiche G, Traficante N, Nice E . A binding motif for Siah ubiquitin ligase. Proc Natl Acad Sci U S A. 2003; 100(6):3101-6. PMC: 152253. DOI: 10.1073/pnas.0534783100. View

19.

Akkermans O, Delloye-Bourgeois C, Peregrina C, Carrasquero-Ordaz M, Kokolaki M, Berbeira-Santana M . GPC3-Unc5 receptor complex structure and role in cell migration. Cell. 2022; 185(21):3931-3949.e26. PMC: 9596381. DOI: 10.1016/j.cell.2022.09.025. View

20.

Matsumoto H, Nagashima M . Netrin-1 elevates the level and induces cluster formation of its receptor DCC at the surface of cortical axon shafts in an exocytosis-dependent manner. Neurosci Res. 2010; 67(2):99-107. DOI: 10.1016/j.neures.2010.02.004. View