Slit neuronal secretion coordinates optic lobe morphogenesis in Drosophila

Caipo, Lorena; González-Ramírez, M. Constanza; Guzmán-Palma, Pablo; Contreras, Esteban G.; Palominos, Tomás; Fuenzalida‐Uribe, Nicolás; Hassan, Bassem A.; Campusano, Jorge M.; Sierralta, Jimena

doi:10.1016/j.ydbio.2019.10.004

Cited by 11 publications

(20 citation statements)

References 66 publications

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“…However, the work presented in this paper demonstrates that Slit-FL and Slit-N have dramatically different activities in vivo. The key to these findings was the identification of Tok as the Slit protease, allowing in vivo genetic manipulation of Slit fragments to uncover the independent biological function of Slit-N. Our results complement the few studies in which Slit-FL and Slit-N were observed to have distinct activities (Gohrig et al, 2014;Nguyen Ba-Charvet et al, 2001;Wang et al, 1999) as well as those which attributed activities to a specific Slit fragment (Wright et al, 2012;Ducuing et al, 2020;Caipo et al, 2020;). As Slit cleavage and Tok family proteases are evolutionarily conserved (Brose et al, 1999;Hopkins et al, 2007), it seems highly likely that processing of Slits by BMP-1/Tolloid family proteases will diversify the biological output of Slit signaling in many different systems.…”

Section: Discussionsupporting

confidence: 68%

“…Slit-N was previously suspected to be the only biologically active fragment of Slit, because it includes the Robo binding site and most Slit functions are Robo-dependent . However, significant evidence in multiple systems suggests that Slit-FL, Slit-N, and Slit-C are all necessary for normal development (Battye et al, 2001;Chen et al, 2001;Morlot et al, 2007;Coleman et al, 2010;Delloye-Bourgeois et al, 2015;Svensson et al, 2016;Caipo et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…This latter work provides a molecular explanation for how Slit-FL and Slit-N could have different signaling outputs, via alternative receptor complexes, and establishes longitudinal axon guidance as a biological readout for Slit-N functions, independent of Slit-FL-mediated midline repulsion. Additionally, Slit-N and Slit-FL are incapable of substituting for one another in fly muscle development and optic lobe formation Caipo et al, 2020). No functions for Slit-C have been yet identified in…”

Section: Introductionmentioning

confidence: 99%

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Proteolytic cleavage of Slit by the Tolkin protease converts an axon repulsion cue to an axon growth cue in vivo

et al. 2020

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Slit is a secreted protein that has a canonical function of repelling growing axons from the CNS midline. The full-length Slit (Slit-FL) is cleaved into Slit-N and Slit-C fragments, which have potentially distinct functions via different receptors. Here we report that the BMP-1/Tolloid family metalloprotease, Tolkin (Tok), is responsible for Slit proteolysis in vivo and in vitro. In tok mutants lacking Slit cleavage, midline repulsion of axons occurs normally, confirming that Slit-FL is sufficient to repel axons. However, longitudinal axon guidance is highly disrupted in tok mutants and can be rescued by midline expression of Slit-N, suggesting that Slit is the primary substrate for Tok in the embryonic CNS. Transgenic restoration of Slit-N or Slit-C does repel axons in Slit-null animals. Slit-FL and Slit-N are both biologically active cues with distinct axon guidance functions in vivo. Slit signaling is used in diverse biological processes, thus differentiating between Slit-FL and Slit fragments will be essential for evaluating Slit function in broader contexts.

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Section: Discussionsupporting

confidence: 68%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Proteolytic cleavage of Slit by the Tolkin protease converts an axon repulsion cue to an axon growth cue in vivo

et al. 2020

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“…One way in which glial cells prevent neuropil mixing is by secreting Slit, which is also secreted by medulla neurons. Gliaexpressed Slit prevents Robo-expressing IPC neurons from mixing with the lamina precursor cells in the OPC; mutants in these genes cause lobula complex neurons born from the IPC (C or T neurons) to inappropriately invade the developing larval lamina and bisect the lamina and medulla neuropils (118,119).…”

Section: Optic Lobe Organization: a Primermentioning

confidence: 99%

Neural specification, targeting, and circuit formation during visual system assembly

Malin

Desplan

2021

Proc. Natl. Acad. Sci. U.S.A.

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Like other sensory systems, the visual system is topographically organized: Its sensory neurons, the photoreceptors, and their targets maintain point-to-point correspondence in physical space, forming a retinotopic map. The iterative wiring of circuits in the visual system conveniently facilitates the study of its development. Over the past few decades, experiments in Drosophila have shed light on the principles that guide the specification and connectivity of visual system neurons. In this review, we describe the main findings unearthed by the study of the Drosophila visual system and compare them with similar events in mammals. We focus on how temporal and spatial patterning generates diverse cell types, how guidance molecules distribute the axons and dendrites of neurons within the correct target regions, how vertebrates and invertebrates generate their retinotopic map, and the molecules and mechanisms required for neuronal migration. We suggest that basic principles used to wire the fly visual system are broadly applicable to other systems and highlight its importance as a model to study nervous system development.

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“…The distal neurons present at the edges of the lobula cortex invade the lamina in slit and robo loss of function conditions (Tayler et al, 2004). Furthermore, cell-specific loss of function experiments demonstrated that Slit expression in glial cells present at the interfaces between lamina and lobula plate, and that of lamina and medulla are required for the optic lobe segregation (Caipo et al, 2020, Suzuki et al, 2018, Tayler et al, 2004. Additionally to glial expression, Slit secretion by neurons from the medulla is essential for cell segregation in this region of the brain (Caipo et al, 2020).…”

Section: B) Cell Segregation In the Development Of The Optic Lobementioning

confidence: 99%

Cell segregation and boundary formation during nervous system development

González-Ramírez¹,

Guzmán-Palma²

2021

Int. J. Dev. Biol.

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The development of multicellular organisms involves three main events: differentiation, growth, and morphogenesis. These processes need to be coordinated for a correct developmental program to work. Mechanisms of cell segregation and the formation of boundaries during development play essential roles in this coordination, allowing the generation and maintenance of distinct regions in an organism. These mechanisms are also at work in the nervous system. The process of regionalization involves first the patterning of the developing organism through gradients and the expression of transcription factors in specific regions. Once different tissues have been induced, segregation mechanisms may operate to avoid cell mixing between different compartments. Three mechanisms have been proposed to achieve segregation: (1) differential affinity, which mainly involves the expression of distinct pools of adhesion molecules such as members of the cadherin superfamily; (2) contact inhibition, which is largely mediated by Eph-ephrin signaling; and (3) cortical tension, which involves the actomyosin cytoskeleton. In many instances, these mechanisms collaborate in cell segregation. In the last three decades, there have been several advances in our understanding of how cell segregation and boundaries participate in the development of the nervous system. Interestingly as in other aspects of development, the molecular players are remarkably similar between vertebrates and invertebrates. Here we summarize the main concepts of cell segregation and boundary formation, focusing on the nervous system and highlighting the similarities between vertebrate and invertebrate model organisms.

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Slit neuronal secretion coordinates optic lobe morphogenesis in Drosophila

Cited by 11 publications

References 66 publications

Proteolytic cleavage of Slit by the Tolkin protease converts an axon repulsion cue to an axon growth cue in vivo

Proteolytic cleavage of Slit by the Tolkin protease converts an axon repulsion cue to an axon growth cue in vivo

Neural specification, targeting, and circuit formation during visual system assembly

Cell segregation and boundary formation during nervous system development

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