Beyond Axon Guidance: Roles of Slit-Robo Signaling in Neocortical Formation

Overview

Journal Front Cell Dev Biol

Specialty Cell Biology

Date 2021 Jan 11

PMID 33425915

Citations 33

Authors

Yuko Gonda

Takashi Namba

Carina Hanashima

Affiliations

Soon will be listed here.

Abstract

The formation of the neocortex relies on intracellular and extracellular signaling molecules that are involved in the sequential steps of corticogenesis, ranging from the proliferation and differentiation of neural progenitor cells to the migration and dendrite formation of neocortical neurons. Abnormalities in these steps lead to disruption of the cortical structure and circuit, and underly various neurodevelopmental diseases, including dyslexia and autism spectrum disorder (ASD). In this review, we focus on the axon guidance signaling Slit-Robo, and address the multifaceted roles of Slit-Robo signaling in neocortical development. Recent studies have clarified the roles of Slit-Robo signaling not only in axon guidance but also in progenitor cell proliferation and migration, and the maturation of neocortical neurons. We further discuss the etiology of neurodevelopmental diseases, which are caused by defects in Slit-Robo signaling during neocortical formation.

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References

Roberts B . Neuronal Migration Disorders. Radiol Technol. 2018; 89(3):279-295. View

Tong M, Jun T, Nie Y, Hao J, Fan D . The Role of the Slit/Robo Signaling Pathway. J Cancer. 2019; 10(12):2694-2705. PMC: 6584916. DOI: 10.7150/jca.31877. View

Rakic P . Evolution of the neocortex: a perspective from developmental biology. Nat Rev Neurosci. 2009; 10(10):724-35. PMC: 2913577. DOI: 10.1038/nrn2719. View

Zhu Y, Li H, Zhou L, Wu J, Rao Y . Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex. Neuron. 1999; 23(3):473-85. DOI: 10.1016/s0896-6273(00)80801-6. View

Haubensak W, Attardo A, Denk W, Huttner W . Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci U S A. 2004; 101(9):3196-201. PMC: 365766. DOI: 10.1073/pnas.0308600100. View

La Fata G, Gartner A, Dominguez-Iturza N, Dresselaers T, Dawitz J, Poorthuis R . FMRP regulates multipolar to bipolar transition affecting neuronal migration and cortical circuitry. Nat Neurosci. 2014; 17(12):1693-700. DOI: 10.1038/nn.3870. View

Petros T, Bultje R, Ross M, Fishell G, Anderson S . Apical versus Basal Neurogenesis Directs Cortical Interneuron Subclass Fate. Cell Rep. 2015; 13(6):1090-1095. PMC: 4704102. DOI: 10.1016/j.celrep.2015.09.079. View

Holmes G, Negus K, Burridge L, Raman S, Algar E, Yamada T . Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis. Mech Dev. 1999; 79(1-2):57-72. DOI: 10.1016/s0925-4773(98)00174-9. View

Rhee J, Buchan T, Zukerberg L, Lilien J, Balsamo J . Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol. 2007; 9(8):883-92. DOI: 10.1038/ncb1614. View

10.

Koschutzke L, Bertram J, Hartmann B, Bartsch D, Lotze M, von Bohlen Und Halbach O . SrGAP3 knockout mice display enlarged lateral ventricles and specific cilia disturbances of ependymal cells in the third ventricle. Cell Tissue Res. 2015; 361(2):645-50. DOI: 10.1007/s00441-015-2224-6. View

11.

Blockus H, Chedotal A . Slit-Robo signaling. Development. 2016; 143(17):3037-44. DOI: 10.1242/dev.132829. View

12.

Reynolds A, Daniel J, McCrea P, Wheelock M, Wu J, Zhang Z . Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol Cell Biol. 1994; 14(12):8333-42. PMC: 359372. DOI: 10.1128/mcb.14.12.8333-8342.1994. View

13.

Noctor S, Flint A, Weissman T, Dammerman R, Kriegstein A . Neurons derived from radial glial cells establish radial units in neocortex. Nature. 2001; 409(6821):714-20. DOI: 10.1038/35055553. View

14.

Whitford K, Marillat V, Stein E, Goodman C, Tessier-Lavigne M, Chedotal A . Regulation of cortical dendrite development by Slit-Robo interactions. Neuron. 2002; 33(1):47-61. DOI: 10.1016/s0896-6273(01)00566-9. View

15.

Brose K, Bland K, Wang K, Arnott D, Henzel W, Goodman C . Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell. 1999; 96(6):795-806. DOI: 10.1016/s0092-8674(00)80590-5. View

16.

Cardenas A, Borrell V . Molecular and cellular evolution of corticogenesis in amniotes. Cell Mol Life Sci. 2019; 77(8):1435-1460. PMC: 11104948. DOI: 10.1007/s00018-019-03315-x. View

17.

Peterson R, Pennington B . Developmental dyslexia. Lancet. 2012; 379(9830):1997-2007. PMC: 3465717. DOI: 10.1016/S0140-6736(12)60198-6. View

18.

Sekine K, Kawauchi T, Kubo K, Honda T, Herz J, Hattori M . Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of integrin α5β1. Neuron. 2012; 76(2):353-69. PMC: 3479437. DOI: 10.1016/j.neuron.2012.07.020. View

19.

Marin O, YARON A, Bagri A, Tessier-Lavigne M, Rubenstein J . Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science. 2001; 293(5531):872-5. DOI: 10.1126/science.1061891. View

20.

Gaiano N, Nye J, Fishell G . Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron. 2000; 26(2):395-404. DOI: 10.1016/s0896-6273(00)81172-1. View