Expression of netrin-1 and netrin-1 receptor, DCC, in the rat olfactory nerve pathway during development and axonal regeneration
Section snippets
Animals
Wistar SPF (IFFA-Credo, France) rat embryos from the 13th to the 19th day of gestation (day of conception=E1) and rats aged 1, 6, 15, 30 and 50 post-natal days (day of birth=P1) were used in this study. Animals were housed in polypropylene cages, kept in a 12–12-h light–dark cycle and provided with food and water ad libitum.
Surgical procedures
Thirty-day-old male rats were anesthetized with Equithesin (3 mg/kg, i.p.). Animals were placed in a stereotaxic apparatus and the frontal bones over the olfactory bulbs
Developmental regulation of DCC expression
The two monoclonal antisera used to determine the expression of DCC in the developing olfactory system gave very similar patterns of immunoreactivity. Since a weaker labelling intensity was generally observed with AF5 antibody generated against the extracellular domain of the protein, we therefore reported results obtained with the antibody directed against the intracellular domain of DCC.
Netrin-1 and DCC expressions in the developing olfactory pathway
One of the netrin-1 receptors, DCC, is known to be expressed on various projecting populations of axons during early stages of the neural development (Keino-Masu et al., 1996, Deiner et al., 1997, De la Torre et al., 1997, Shu et al., 2000, Anderson et al., 2000). In agreement with these studies, our results demonstrate that DCC protein is dynamically regulated on the axon populations emerging from the olfactory epithelium and the vomeronasal epithelium during embryogenesis and early post-natal
Conclusion
The present study provides a detailed analysis of the spatio-temporal expression patterns of both netrin-1 and DCC proteins in the developing rat olfactory system. It has been shown that the association of netrin-1 expression along DCC-expressing olfactory axons is restricted to the initial period of olfactory nerve pathfinding, which suggests that netrin-1 may play a role in the directed outgrowth of the nascent olfactory axons toward the telencephalon. The idea that this function should be
Acknowledgements
This study was supported by the Centre National de la Recherche Scientifique (UMR 5020, UMR 5534), the Ligue contre le cancer (P.M.), the ARC (5931, P.M.) and the University of Lyon (BQR).
References (64)
- et al.
DCC plays a role in navigation of forebrain axons across the ventral midbrain commissure in embryonic Xenopus
Dev. Biol.
(2000) - et al.
Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium
Exp. Neurol.
(1992) - et al.
Conservation and divergence of axon guidance mechanisms
Curr. Opin. Neurobiol.
(1999) - et al.
cDCC (chicken homologue to a gene deleted in colorectal carcinoma) is an epithelial adhesion molecule expressed in the basal cells and involved in epithelial–mesenchymal interaction
Dev. Biol.
(1994) - et al.
The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons
Cell
(1995) - et al.
Neurogenesis persists in the subependymal layer of the adult mouse brain
Neurosci. Lett.
(1993) - et al.
DCC and netrins
Curr. Opin. Cell Biol.
(1998) - et al.
Netrin-1 and DCC mediate axon guidance locally at the optic disc: Loss of function leads to optic nerve hypoplasia
Neuron
(1997) - et al.
Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC
Neuron
(1997) - et al.
The expression patterns of guidance receptors, DCC and neogenin, are spatially and temporally distinct throughout mouse embryogenesis
Dev. Biol.
(1997)
Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb
Neuron
Netrins evoke mixed reactions in motile cells
Trends Genet.
Differential development of binding sites of two lectins in the vomeronasal axons of the rat accessory olfactory bulb
Dev. Brain Res.
UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans
Neuron
Deleted in colorectal cancer (DCC) encodes a netrin receptor
Cell
Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord
Cell
Netrin and netrin receptor expression in the embryonic mammalian nervous system suggests roles in retinal, striatal, nigral, and cerebellar development
Mol. Cell. Neurosci.
Early onset of the rat olfactory bulb projections
Neuroscience
Netrin-1 and peripheral nerve regeneration in the adult rat
Exp. Neurol.
Ontogenesis of the axonal circuitry associated with the olfactory system of the rat embryo
Neurosci. Lett.
A proposed relationship between increases in the number of olfactory receptor neurons, convergence ratio and sensitivity in the developing rat
Dev. Brain Res.
B-50/GAP-43 expression by the olfactory receptor cells and the neurons migrating from the olfactory placode in embryonic rats
Dev. Brain Res.
Lesion-induced regulation of netrin receptors and modification of netrin-1 expression in the retina of fish and grafted rats
Mol. Cell. Neurosci.
Divergent properties of mouse netrins
Mech. Dev.
Transient pattern of exuberant projections of olfactory axons during development in the rat
Dev. Brain Res.
The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6
Cell
Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system
Cell
Guidance of circumferentially growing axons by netrin-dependent and -independent floor plate chemotropism in the vertebrate brain
Neuron
Signal transduction underlying growth cone guidance by diffusible factors
Curr. Opin. Neurobiol.
Identification and expression of mouse netrin-4
Mech. Dev.
Development of the olfactory bulb: Evidence for glia–neuron interactions in glomerular formation
J. Comp. Neurol.
Netrin-1 promotes thalamic axon growth and is required for proper development of the thalamocortical projection
J. Neurosci.
Cited by (50)
Netrin-1 in the developing enteric nervous system and colorectal cancer
2012, Trends in Molecular MedicineIgSF8: A developmentally and functionally regulated cell adhesion molecule in olfactory sensory neuron axons and synapses
2012, Molecular and Cellular NeuroscienceCitation Excerpt :For example, OSNs express the cell adhesion molecules NCAM and N-cadherin which are important for olfactory pathway formation (Akins and Greer, 2006; Treloar et al., 1997). Similarly, they express many cell surface receptors which are members of the Ig superfamily, such as DCC, Neuropilin-1, DSCAM and Robos1-2 (Agarwala et al., 2001; Astic et al., 2002; Cho et al., 2007; Nagao et al., 2000). Structurally, IgSF8 possesses a short signal sequence at the N terminus, four Ig-like domains, 3 putative N-glycosylation sites, a transmembrane domain and a short intracellular region (Yamada et al., 2006; Zhang et al., 2003) (Fig. 2A).
Temporally distinct expression of vesicular glutamate transporters 1 and 2 during embryonic development of the rat olfactory system
2011, Neuroscience ResearchCitation Excerpt :In the OB neurogenesis, the interneurons are derived from the subpallium in embryonic ages (Wichterle et al., 1999) and from neuronal stem cells residing in the subventricular zone in adulthood (Brill et al., 2009). Early in olfactory system development, olfactory receptor neurons generate in the olfactory placode, project to the prospective OB of telencephalon while forming olfactory and vomeronasal nerves, and make contact with the projection neurons (Pellier et al., 1994; LaMantia et al., 2000; Astic et al., 2002; Ikeda et al., 2007). In contrast, although a recent in vivo cell tracing study (Nomura and Osumi, 2004) using green fluorescent protein has supported previous data that mitral cell progenitors originate from the rostral dorsal telencephalon (Bulfone et al., 1998; Puelles et al., 2000), much is still unknown about the development of projection neurons.
Molecular development of the extrinsic sensory innervation of the gastrointestinal tract
2011, Autonomic Neuroscience: Basic and ClinicalCitation Excerpt :After first finding the bowel during development, vagal sensory axons must then be guided to their correct locations in the gut wall. Netrins have been identified as important axon guidance molecules in the CNS, where they act through both attractive (Astic et al., 2002; Serafini et al., 1996) and repellent (Colamarino and Tessier-Lavigne, 1995) mechanisms. Like many signaling molecules, netrins occur in the gut as well as in the brain (Gershon and Ratcliffe, 2004; Young et al., 2004).
Expression of DCC in differentiating ameloblasts from developing tooth germs in rats
2009, Archives of Oral BiologyCitation Excerpt :However, about the role of DCC in tooth development is unclear. It was reported that DCC functions as an axonal chemoattractant during axon guidance24 and as an antagonistic effector on the lar-tp (leukocyte-common antigen-related tyrosine phosphatase) function25 in the nervous system. Recently, we reported the existence of lar-tp in molar tooth development.26
Mechanisms of Axon Guidance in the Developing Nervous System
2005, Current Topics in Developmental BiologyCitation Excerpt :DCC has also been found in the embryonic rodent olfactory bulb, on the granule cells, and on pioneer axons from output neurons (Gad et al., 1997; Shu et al., 2000). A detailed analysis of the spatio‐temporal expression patterns of both Netrin‐1 and DCC proteins in the developing rat olfactory system showed that the association of Netrin‐1 expression near DCC‐expressing olfactory axons is restricted to the initial period of olfactory nerve pathfinding, which suggests that Netrin‐1 may play a role in the directed outgrowth of the nascent olfactory axons toward the telencephalon (Astic et al., 2002). Another member of the netrin family, Netrin‐4, is localized within the lateral olfactory tract and may be involved in promoting neurite elongation (Koch et al., 2000).
- 1
These authors contributed equally to this work.