Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interaction is required for midline crossing in vertebrate spinal cord

Mambetisaeva, Elvira T.; Andrews, William; Camurri, Laura; Annan, Adelaide; Sundaresan, Vasi

doi:10.1002/dvdy.20324

Cited by 53 publications

(62 citation statements)

References 51 publications

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“…15,16 However, Robo3 does not appear to regulate Robo trafficking in the same way as Drosophila Comm, since the levels of Robo1 and Robo2 protein appear unchanged in Robo3 -/-embryos. 14 Taken together with the observation that Robo3 is likely to bind Slits, 14,17 these findings support a model in which Robo3 normally suppresses the responsiveness of pre-crossing commissural axons to midline-associated Slits. 14 More recently, two different isoforms of Robo3 were identified in both chick 18 and mouse 13 embryos.The mouse Robo3 isoforms, Robo3.1 and Robo3.2 arise from alternative splicing of robo3 pre-mRNA and are segregated to pre-and post-crossing segments of commissural axons, respectively (Fig.…”

supporting

confidence: 53%

Leaving the midline

Reeber

Kaprielian

2009

Cell Adhesion & Migration

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supporting

confidence: 53%

Leaving the midline

Reeber

Kaprielian

2009

Cell Adhesion & Migration

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“…Alternative splicing in the 5Ј coding sequence can generate two distinct receptor isoforms, A and B, which differ at their N-terminal end. Type A isoforms are longer (16-40 residues) than type B isoforms (Camurri et al, 2005; Kidd et al, 1998;Sundaresan et al, 1998;Yue et al, 2006). In the case of Robo3, alternative splicing by the retention or excision of one intron in the 3Ј coding sequence generates two isoforms that differ in their C-terminal domain, with Robo3.1 being longer than Robo3.2 (Chen et al, 2008a).…”

Section: Robo and Slit Structurementioning

confidence: 99%

“…Second, mammalian Robo3 has only been detected in the nervous system (Barber et al., 2009; Jen et al, 2004;Marillat et al, 2004;Sabatier et al, 2004). Third, its ability to bind Slits is debated (Camurri et al, 2005;Mambetisaeva et al, 2005), and there is to date no biological response associated with the direct binding of Slit to Robo3. Last, although it primarily controls axon guidance at the midline, Robo3 function is unusual when compared with the functions of the other Robos (Fig.…”

mentioning

confidence: 99%

Moving away from the midline: new developments for Slit and Robo

2010

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SummaryIn most tissues, the precise control of cell migration and cellcell interaction is of paramount importance to the development of a functional structure. Several families of secreted molecules have been implicated in regulating these aspects of development, including the Slits and their Robo receptors. These proteins have well described roles in axon guidance but by influencing cell polarity and adhesion, they participate in many developmental processes in diverse cell types. We review recent progress in understanding both the molecular mechanisms that modulate Slit/Robo expression and their functions in neural and non-neural tissue. Key words: Axon guidance, Cell migration, Cell-cell interaction IntroductionIn most organisms, the central nervous system (CNS) develops along a bilateral axis of symmetry located at the midline (Placzek and Briscoe, 2005). During development, the ventral midline or floor plate acts as an organiser through the secretion of diffusible proteins (Placzek and Briscoe, 2005;Gore et al., 2008), which control the growth of axons and dendrites and the migration of neurons across the midline. In the forebrain, glial or neuronal cells delineate the midline (see Glossary, Box 1) and also control axon guidance. For more than two decades, many developmental neurobiologists have tried to understand the mechanisms that control midline crossing in the CNS and to answer some key questions. Firstly, how are commissural axons (see Glossary, Box 1) attracted to the midline and how do their growth cones (see Glossary, Box1) receive and integrate the multiple and contrasting signals released by midline cells? Secondly, what are the molecular and signalling changes that enable commissural axons to leave the midline and often to switch to a longitudinal growth mode? All midline-derived axon guidance factors are expressed at other locations in many developing and mature tissues, where they control a wide range of biological processes.Roundabout receptors (Robo) and their Slit ligands form one of the most crucial ligand-receptor pairings among the axon guidance molecules. Robos were identified in Drosophila in a mutant screen for genes that control the midline crossing of commissural axons (Kidd et al., 1998;Seeger et al., 1993). Similarly, Slit was discovered in Drosophila as a protein secreted by midline glia (Rothberg et al., 1988;Rothberg et al., 1990). Homologues of both proteins have since been discovered in many species (for a review, see . However, the Slit/Robo couple not only functions in axon guidance but also in a variety of developmental Development 137, 1939Development 137, -1952Development 137, (2010 Commissural axons Axons with cell bodies (somata) located on one side of the central nervous system (CNS) that project axons across the midline to contact target cells on the opposite side. Growth cone A specialised bulbous enlargement at the end of growing axons that is characterised by dynamic filamentous extensions, known as filopodia. They sense the environment and respond to adhesi...

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“…A number of long-range guidance cues directing these axons ventrally toward the floorplate have been identified (Kennedy et al, 1994;Augsburger et al, 1999;Charron et al, 2003;Islam et al, 2009). Midline crossing is regulated by a shift from attraction to repulsion (Stoeckli and Landmesser, 1995;Stoeckli et al, 1997;Long et al, 2004;Sabatier et al, 2004;Mambetisaeva et al, 2005;Chen et al, 2008). Axonal repulsion is induced by the upregulation of Robo1 on the growth cone surface, which allows for the detection of Slit, a negative floorplate-derived signal (Philipp et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Semaphorin 6B acts as a receptor in post-crossing commissural axon guidance

et al. 2014

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Semaphorins are a large family of axon guidance molecules that are known primarily as ligands for plexins and neuropilins. Although class-6 semaphorins are transmembrane proteins, they have been implicated as ligands in different aspects of neural development, including neural crest cell migration, axon guidance and cerebellar development. However, the specific spatial and temporal expression of semaphorin 6B (Sema6B) in chick commissural neurons suggested a receptor role in axon guidance at the spinal cord midline. Indeed, in the absence of Sema6B, post-crossing commissural axons lacked an instructive signal directing them rostrally along the contralateral floorplate border, resulting in stalling at the exit site or even caudal turns. Truncated Sema6B lacking the intracellular domain was unable to rescue the loss-of-function phenotype, confirming a receptor function of Sema6B. In support of this, we demonstrate that Sema6B binds to floorplate-derived plexin A2 (PlxnA2) for navigation at the midline, whereas a cis-interaction between PlxnA2 and Sema6B on pre-crossing commissural axons may regulate the responsiveness of axons to floorplate-derived cues.

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Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interaction is required for midline crossing in vertebrate spinal cord

Cited by 53 publications

References 51 publications

Leaving the midline

Leaving the midline

Moving away from the midline: new developments for Slit and Robo

Semaphorin 6B acts as a receptor in post-crossing commissural axon guidance

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