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Semaphorin-3A and its receptor neuropilin-1 are predominantly expressed in endothelial cells along the rostral migratory stream of young and adult mice

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Abstract

In the adult brain, neuroblasts originating in the subventricular zone migrate through the rostral migratory stream to the olfactory bulb. While migrating, neuroblasts undergo progressive differentiation until reaching their final locations and fates. Because molecules involved in migration may also exert differentiating effects on young neurons, the identification of factors that support migration could also shed light on the processes of adult neuroblast differentiation. This is the case for members of the family of semaphorins and of its cognate receptors, the neuropilins. Here, we have evaluated the presence of semaphorin-3A and of its receptor neuropilin-1 along the rostral migratory stream in young and adult mice by using immunocytochemical, histochemical, and in situ hybridization techniques. Our morphological studies show that semaphorin-3A and neuropilin-1 are both mainly expressed on endothelial cells along the rostral migratory stream during postnatal development. Our results suggest that endothelial cells constitute the primary source and target of semaphorin-3A along the rostral migratory stream. Moreover, the present work outlines the potential role of blood vessels on neuroblast migration in the postnatal rostral migratory stream.

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References

  • Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433–457

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in the adult subventricular zone. J Neurosci 2:629–634

    Google Scholar 

  • Bagnard D, Lohrum M, Uziel D, Püschel AW, Bolz J (1998) Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections. Development 125:5043–5053

    PubMed  CAS  Google Scholar 

  • Bagnard D, Vaillant C, Khuth ST, Dufay N, Lohrum M, Püschel AW, Belin MF, Bolz J, Thomasset NJ (2001) Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J Neurosci 21:3332–3341

    PubMed  CAS  Google Scholar 

  • Balenci L, Saoudi Y, Grunwald D, Deloulme JC, Bouron A, Bernards A, Baudier J (2007) IAGAP1 regulates adult neural progenitors in vivo and vascular endothelial growth factor-triggered neural progenitor migration in vitro. J Neurosci 27:4716–4724

    Article  PubMed  CAS  Google Scholar 

  • Bovetti S, Hsieh YC, Bovolin P, Perroteau I, Kazunori T, Puche AC (2007) Blood vessels form a scaffold for neuroblast migration in the adult ofactoty bulb. J Neurosci 27:5976–5980

    Article  PubMed  CAS  Google Scholar 

  • Coskun V, Luskin MB (2002) Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J Neurosci Res 69:795–802

    Article  PubMed  CAS  Google Scholar 

  • Fenstermaker V, Chen Y, Ghosh A, Yuste R (2004) Regulation of dendritic length and branching by semaphorin 3A. J Neurobiol 58:403–412

    Article  PubMed  CAS  Google Scholar 

  • Fujita H, Zhang B, Sato K, Tanaka J, Sakanaka M (2001) Expressions of neuropilin-1, neuropilin-2 and semaphoring 3A mRNA in the rat brain after middle cerebral artery occlusion. Brain Res 914:1–14

    Article  PubMed  CAS  Google Scholar 

  • Fukushima N, Yokouchi K, Kawagishi K, Moriizumi T (2002) Differential neurogenesis and gliogenesis by local and migrating neural stem cells in the olfactory bulb. Neurosci Res 44:467–473

    Article  PubMed  CAS  Google Scholar 

  • Gage FH (2002) Neurogenesis in the adult brain. J Neurosci 22:612–613

    PubMed  CAS  Google Scholar 

  • Giger RJ, Pasterkamp RJ, Heijnen S, Holtmaat AJ, Verhaagen J (1998) Anatomical distribution of the chemorepellent semaphorin III/collapsin-1 in the adult rat and human brain: predominant expression in structures of the olfactory-hippocampal pathway and the motor system. J Neurosci Res 52:27–42

    Article  PubMed  CAS  Google Scholar 

  • Gonthier B, Nasarre C, Roth L, Perraut M, Thomasset N, Roussel G, Aunis D, Bagnard D (2006) Functional interaction between matrix metalloproteinase-3 and semaphoring-3C during cortical axonal growth and guidance. Cereb Cortex 17:1712–1721

    Article  PubMed  Google Scholar 

  • Hu H, Rutishauser U (1996) A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16:933–940

    Article  PubMed  CAS  Google Scholar 

  • Jankovski A, Sotelo C (1996) Subventricular zone-olfactory bulb migratory pathway in the adult mouse: cellular composition and specificity as determined by heterochonic and heterotopic transplantation. J Comp Neurol 371:376–396

    Article  PubMed  CAS  Google Scholar 

  • Kolodkin AL, Matthes DJ, Goodman CG (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75:1389–1399

    Article  PubMed  CAS  Google Scholar 

  • Lois C, Alvarez-Buylla A (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90:2074–2077

    Article  PubMed  CAS  Google Scholar 

  • Luskin MB (1998) Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J Neurobiol 36:221–233

    Article  PubMed  CAS  Google Scholar 

  • Mendoza-Torreblanca JG, Martínez-Martínez E, Tapia-Rodríguez M, Ramírez-Hernández R, Gutiérrez-Ospina G (2008) The rostral migratory stream is a neurogenic niche that predominantly engenders periglomerular cells: in vivo evidence in the adult rat brain. Neurosci Res 60:289–299

    Article  PubMed  Google Scholar 

  • Miao HQ, Soker S, Feiner L, Alonso JL, Raper JA, Klagsbrun M (1999) Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J Cell Biol 146:233–242

    PubMed  CAS  Google Scholar 

  • Murase S, Horwitz AF (2002) Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J Neurosci 22:3568–3579

    PubMed  CAS  Google Scholar 

  • Narazaki M, Tosato G (2006) Ligand-induced internalization selects use of common receptor neuropilin-1 by VEGF165 and semaphorin3A. Blood 107:3892–3901

    Article  PubMed  CAS  Google Scholar 

  • Ohab JJ, Fleming S, Blesch A, Carmichael ST (2006) A neurovascular niche for neurogenesis after stroke. J Neurosci 26:13007–13016

    Article  PubMed  CAS  Google Scholar 

  • Osborne NJ, Begbie J, Chilton JK, Schmidt H, Eickhold BJ (2005) Semaphorin/neuropilin signaling influences the positioning of migratory neural crest cells within the hindbrain region of the chick. Dev Dyn 232:939–949

    Article  PubMed  CAS  Google Scholar 

  • Palmer TD, Willhoite AR, Gage FH (2000) Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494

    Article  PubMed  CAS  Google Scholar 

  • Pascual M, Pozas E, Soriano E (2005) Role of class 3 semaphorins in the development and maturation of the septohippocampal pathway. Hippocampus 15:184–202

    Article  PubMed  CAS  Google Scholar 

  • Peretto P, Giachino C, Aimar P, Fasolo A, Bonfanti L (2005) Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 487:407–427

    Article  PubMed  Google Scholar 

  • Püschel AW, Adams RH, Betz H (1995) Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron 14:941–948

    Article  PubMed  Google Scholar 

  • Riddle DR, Gutierrez G, Zheng D, White LE, Richards A, Purves D (1993) Differential metabolic and electrical activity in the somatic sensory cortex of juvenile and adult rats. J Neurosci 13:4193–4213

    PubMed  CAS  Google Scholar 

  • Schwarz Q, Gu C, Fujisawa H, Sabelko K, Gertsenstein M, Nagy A, Taniguchi M, Kolodkin AL, Ginty DD, Shima DT, Ruhrberg C (2004) Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve. Genes Dev 18:2822–2834

    Article  PubMed  CAS  Google Scholar 

  • Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M, Tessier-Lavigne M, Taniguchi M, Puschel AW, Bussolino F (2003) Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 424:391–397

    Article  PubMed  CAS  Google Scholar 

  • Shen Q, Goderie SK, Jin L, Karant N, Sun Y, Abramova N, Vincent P, Pumiglia K, Sally T (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340

    Article  PubMed  CAS  Google Scholar 

  • Skaliora I, Singer W, Betz H, Püschel AW (1998) Differential patterns of semaphorin expression in the developing rat brain. Eur J Neurosci 10:1215–1229

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Zhang ZG, Zhang RL, Gregg SR, Hozeska-Solgot A, LeTornneau Y, Wang Y, Chopp M (2006) Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 26:5996–6003

    Article  PubMed  CAS  Google Scholar 

  • Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A (1999) Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2:461–466

    Article  PubMed  CAS  Google Scholar 

  • Yamashita T, Ninomiya M, Hernández-Acosta P, García-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K (2006) Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26:6627–6636

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Mujtaba T, Venkatraman G, Wu YY, Rao MS, Luskin MB (2000) Region-specific differentiation of neural tube-derived neuronal restricted progenitor cells after heterotopic transplantation. Proc Natl Acad Sci USA 97:13366–13371

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Luis R. Hernández for his valuable participation at the beginning of this work, to Dr. Román Vidal-Tamayo for critical review of the manuscript, and to Patricia Padilla Cortés for administrative support and technical assistance.

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Authors and Affiliations

  1. Departamento de Biología Celular y Fisiología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, México City, D.F., 04510, México

    Esperanza Meléndez-Herrera, Dannia Colín-Castelán & Gabriel Gutiérrez-Ospina

  2. Departamento de Neurobiología del Desarrollo, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, México

    Alfredo Varela-Echavarría

  3. Grupo de Investigación de Células Troncales, IMPULSA 02, Universidad Nacional Autónoma de México, México City, D.F., 04510, Mexico

    Esperanza Meléndez-Herrera, Alfredo Varela-Echavarría & Gabriel Gutiérrez-Ospina

Authors
  1. Esperanza Meléndez-Herrera
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  2. Dannia Colín-Castelán
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  3. Alfredo Varela-Echavarría
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  4. Gabriel Gutiérrez-Ospina
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Corresponding authors

Correspondence to Esperanza Meléndez-Herrera or Gabriel Gutiérrez-Ospina.

Additional information

This work was supported by grants from Dirección General de Asuntos del Personal Académico (PAPIIT No. IN210105) and from IMPULSA 02, Universidad Nacional Autónoma de México. Additional funding was provided by grants from Consejo Nacional de Ciencia y Tecnología (CONACYT No. P45872-M). Esperanza Meléndez-Herrera is a postdoctoral fellow receiving support from DGAPA-UNAM.

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Fig. S1. (Supplementary Material)

Specificity of the hybridization probe and the antibodies used in this work. Photomicrographs illustrating parasaggital sections of the mouse hippocampal formation stained for sema-3A mRNA (a) and protein (b), and npn-1 receptor protein (c). Subgranular (sg) and subpyramidal (sp) cell layers of the dentate gyrus (DG) express and transduce the mRNAs that encode both proteins (Pascual et al. 2005). The corresponding negative controls are shown (d–f). Scale bar = 100 μm. (GIF 286 KB)

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Meléndez-Herrera, E., Colín-Castelán, D., Varela-Echavarría, A. et al. Semaphorin-3A and its receptor neuropilin-1 are predominantly expressed in endothelial cells along the rostral migratory stream of young and adult mice. Cell Tissue Res 333, 175–184 (2008). https://doi.org/10.1007/s00441-008-0643-3

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  • DOI: https://doi.org/10.1007/s00441-008-0643-3

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