Skip to main content
Top
Published in: Brain Structure and Function 1/2016

01-01-2016 | Original Article

Anosmin-1 over-expression increases adult neurogenesis in the subventricular zone and neuroblast migration to the olfactory bulb

Authors: Diego García-González, Verónica Murcia-Belmonte, Pedro F. Esteban, Felipe Ortega, David Díaz, Irene Sánchez-Vera, Rafael Lebrón-Galán, Laura Escobar-Castañondo, Luis Martínez-Millán, Eduardo Weruaga, José Manuel García-Verdugo, Benedikt Berninger, Fernando de Castro

Published in: Brain Structure and Function | Issue 1/2016

Login to get access

Abstract

New subventricular zone (SVZ)-derived neuroblasts that migrate via the rostral migratory stream are continuously added to the olfactory bulb (OB) of the adult rodent brain. Anosmin-1 (A1) is an extracellular matrix protein that binds to FGF receptor 1 (FGFR1) to exert its biological effects. When mutated as in Kallmann syndrome patients, A1 is associated with severe OB morphogenesis defects leading to anosmia and hypogonadotropic hypogonadism. Here, we show that A1 over-expression in adult mice strongly increases proliferation in the SVZ, mainly with symmetrical divisions, and produces substantial morphological changes in the normal SVZ architecture, where we also report the presence of FGFR1 in almost all SVZ cells. Interestingly, for the first time we show FGFR1 expression in the basal body of primary cilia in neural progenitor cells. Additionally, we have found that A1 over-expression also enhances neuroblast motility, mainly through FGFR1 activity. Together, these changes lead to a selective increase in several GABAergic interneuron populations in different OB layers. These specific alterations in the OB would be sufficient to disrupt the normal processing of sensory information and consequently alter olfactory memory. In summary, this work shows that FGFR1-mediated A1 activity plays a crucial role in the continuous remodelling of the adult OB
Appendix
Available only for authorised users
Literature
go back to reference Álvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41(5):683–686 pii: S0896627304001114PubMedCrossRef Álvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41(5):683–686 pii: S0896627304001114PubMedCrossRef
go back to reference Anderson L, Burnstein RM, He X, Luce R, Furlong R, Foltynie T, Sykacek P, Menon DK, Caldwell MA (2007) Gene expression changes in long term expanded human neural progenitor cells passaged by chopping lead to loss of neurogenic potential in vivo. Exp Neurol 204(2):512–524. doi:10.1016/j.expneurol.2006.12.025 PubMedCrossRef Anderson L, Burnstein RM, He X, Luce R, Furlong R, Foltynie T, Sykacek P, Menon DK, Caldwell MA (2007) Gene expression changes in long term expanded human neural progenitor cells passaged by chopping lead to loss of neurogenic potential in vivo. Exp Neurol 204(2):512–524. doi:10.​1016/​j.​expneurol.​2006.​12.​025 PubMedCrossRef
go back to reference Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29(48):15245–15257. doi:10.1523/JNEUROSCI.3606-09.2009 PubMedCrossRef Breton-Provencher V, Lemasson M, Peralta MR 3rd, Saghatelyan A (2009) Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J Neurosci 29(48):15245–15257. doi:10.​1523/​JNEUROSCI.​3606-09.​2009 PubMedCrossRef
go back to reference Bribián A, Esteban PF, Clemente D, Soussi-Yanicostas N, Thomas JL, Zalc B, de Castro F (2008) A novel role for anosmin-1 in the adhesion and migration of oligodendrocyte precursors. Dev Neurobiol 68(13):1503–1516. doi:10.1002/dneu.20678 PubMedCrossRef Bribián A, Esteban PF, Clemente D, Soussi-Yanicostas N, Thomas JL, Zalc B, de Castro F (2008) A novel role for anosmin-1 in the adhesion and migration of oligodendrocyte precursors. Dev Neurobiol 68(13):1503–1516. doi:10.​1002/​dneu.​20678 PubMedCrossRef
go back to reference Briñón JG, Crespo C, Weruaga E, Martínez-Guijarro FJ, Aijón J, Alonso JR (2001) Bilateral olfactory deprivation reveals a selective noradrenergic regulatory input to the olfactory bulb. Neuroscience 102(1):1–10 pii: S0306-4522(00)00443-7PubMedCrossRef Briñón JG, Crespo C, Weruaga E, Martínez-Guijarro FJ, Aijón J, Alonso JR (2001) Bilateral olfactory deprivation reveals a selective noradrenergic regulatory input to the olfactory bulb. Neuroscience 102(1):1–10 pii: S0306-4522(00)00443-7PubMedCrossRef
go back to reference Cariboni A, Pimpinelli F, Colamarino S, Zaninetti R, Piccolella M, Rumio C, Piva F, Rugarli EI, Maggi R (2004) The product of X-linked Kallmann’s syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum Mol Genet 13(22):2781–2791. doi:10.1093/hmg/ddh309 PubMedCrossRef Cariboni A, Pimpinelli F, Colamarino S, Zaninetti R, Piccolella M, Rumio C, Piva F, Rugarli EI, Maggi R (2004) The product of X-linked Kallmann’s syndrome gene (KAL1) affects the migratory activity of gonadotropin-releasing hormone (GnRH)-producing neurons. Hum Mol Genet 13(22):2781–2791. doi:10.​1093/​hmg/​ddh309 PubMedCrossRef
go back to reference Cavalieri B (1966) Geometria degli indivisibile. Unione Tipografico-Editrice Torino, Turin Cavalieri B (1966) Geometria degli indivisibile. Unione Tipografico-Editrice Torino, Turin
go back to reference Choy CT, Kim H, Lee JY, Williams DM, Palethorpe D, Fellows G, Wright AJ, Laing K, Bridges LR, Howe FA, Kim SH (2013) Anosmin-1 contributes to brain tumor malignancy through integrin signal pathways. Endocr Relat Cancer. doi:10.1530/ERC-13-0181 PubMed Choy CT, Kim H, Lee JY, Williams DM, Palethorpe D, Fellows G, Wright AJ, Laing K, Bridges LR, Howe FA, Kim SH (2013) Anosmin-1 contributes to brain tumor malignancy through integrin signal pathways. Endocr Relat Cancer. doi:10.​1530/​ERC-13-0181 PubMed
go back to reference Clemente D, Esteban PF, Del Valle I, Bribián A, Soussi-Yanicostas N, Silva A, de Castro F (2008) Expression pattern of Anosmin-1 during pre- and postnatal rat brain development. Dev Dyn 237(9):2518–2528. doi:10.1002/dvdy.21659 PubMedCrossRef Clemente D, Esteban PF, Del Valle I, Bribián A, Soussi-Yanicostas N, Silva A, de Castro F (2008) Expression pattern of Anosmin-1 during pre- and postnatal rat brain development. Dev Dyn 237(9):2518–2528. doi:10.​1002/​dvdy.​21659 PubMedCrossRef
go back to reference De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F (2007) Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27(3):657–664. doi:10.1523/JNEUROSCI.2870-06.2007 PubMedCrossRef De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F (2007) Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27(3):657–664. doi:10.​1523/​JNEUROSCI.​2870-06.​2007 PubMedCrossRef
go back to reference de San Maestre, Juan A (1856) Teratología: falta total de los nervios olfatorios con anosmia en un individuo en quien existía una atrofia congénita de los testículos y el miembro viril. El Siglo Médico 3:211–221 de San Maestre, Juan A (1856) Teratología: falta total de los nervios olfatorios con anosmia en un individuo en quien existía una atrofia congénita de los testículos y el miembro viril. El Siglo Médico 3:211–221
go back to reference Dodé C, Levilliers J, Dupont JM, De Paepe A, Le Du N, Soussi-Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F, Pecheux C, Le Tessier D, Cruaud C, Delpech M, Speleman F, Vermeulen S, Amalfitano A, Bachelot Y, Bouchard P, Cabrol S, Carel JC, Delemarre-van de Waal H, Goulet-Salmon B, Kottler ML, Richard O, Sanchez-Franco F, Saura R, Young J, Petit C, Hardelin JP (2003) Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 33(4):463–465. doi:10.1038/ng1122 PubMedCrossRef Dodé C, Levilliers J, Dupont JM, De Paepe A, Le Du N, Soussi-Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F, Pecheux C, Le Tessier D, Cruaud C, Delpech M, Speleman F, Vermeulen S, Amalfitano A, Bachelot Y, Bouchard P, Cabrol S, Carel JC, Delemarre-van de Waal H, Goulet-Salmon B, Kottler ML, Richard O, Sanchez-Franco F, Saura R, Young J, Petit C, Hardelin JP (2003) Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 33(4):463–465. doi:10.​1038/​ng1122 PubMedCrossRef
go back to reference Doetsch F, Caille I, Lim DA, García-Verdugo JM, Álvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703–716 pii: S0092-8674(00)80783-7PubMedCrossRef Doetsch F, Caille I, Lim DA, García-Verdugo JM, Álvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97(6):703–716 pii: S0092-8674(00)80783-7PubMedCrossRef
go back to reference Doetsch F, Petreanu L, Caille I, García-Verdugo JM, Álvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36(6):1021–1034 pii: S0896627302011339PubMedCrossRef Doetsch F, Petreanu L, Caille I, García-Verdugo JM, Álvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36(6):1021–1034 pii: S0896627302011339PubMedCrossRef
go back to reference Esteban PF, Murcia-Belmonte V, García-Gonzalez D, de Castro F (2013) The cysteine-rich region and the whey acidic protein domain are essential for anosmin-1 biological functions. J Neurochem 124(5):708–720. doi:10.1111/jnc.12104 PubMedCrossRef Esteban PF, Murcia-Belmonte V, García-Gonzalez D, de Castro F (2013) The cysteine-rich region and the whey acidic protein domain are essential for anosmin-1 biological functions. J Neurochem 124(5):708–720. doi:10.​1111/​jnc.​12104 PubMedCrossRef
go back to reference Evans MJ, Fanucchi MV, Van Winkle LS, Baker GL, Murphy AE, Nishio SJ, Sannes PL, Plopper CG (2002) Fibroblast growth factor-2 during postnatal development of the tracheal basement membrane zone. Am J Physiol Lung Cell Mol Physiol 283(6):L1263–1270. doi:10.1152/ajplung.00180.2002 PubMedCrossRef Evans MJ, Fanucchi MV, Van Winkle LS, Baker GL, Murphy AE, Nishio SJ, Sannes PL, Plopper CG (2002) Fibroblast growth factor-2 during postnatal development of the tracheal basement membrane zone. Am J Physiol Lung Cell Mol Physiol 283(6):L1263–1270. doi:10.​1152/​ajplung.​00180.​2002 PubMedCrossRef
go back to reference Franco B, Guioli S, Pragliola A, Incerti B, Bardoni B, Tonlorenzi R, Carrozzo R, Maestrini E, Pieretti M, Taillon-Miller P, Brown CJ, Willard HF, Lawrence C, Graziella Persico M, Camerino G, Ballabio A (1991) A gene deleted in Kallmann’s syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353(6344):529–536. doi:10.1038/353529a0 PubMedCrossRef Franco B, Guioli S, Pragliola A, Incerti B, Bardoni B, Tonlorenzi R, Carrozzo R, Maestrini E, Pieretti M, Taillon-Miller P, Brown CJ, Willard HF, Lawrence C, Graziella Persico M, Camerino G, Ballabio A (1991) A gene deleted in Kallmann’s syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353(6344):529–536. doi:10.​1038/​353529a0 PubMedCrossRef
go back to reference García-González D, Clemente D, Coelho M, Esteban PF, Soussi-Yanicostas N, de Castro F (2010) Dynamic roles of FGF-2 and anosmin-1 in the migration of neuronal precursors from the subventricular zone during pre- and postnatal development. Exp Neurol 222(2):285–295. doi:10.1016/j.expneurol.2010.01.006 PubMedCrossRef García-González D, Clemente D, Coelho M, Esteban PF, Soussi-Yanicostas N, de Castro F (2010) Dynamic roles of FGF-2 and anosmin-1 in the migration of neuronal precursors from the subventricular zone during pre- and postnatal development. Exp Neurol 222(2):285–295. doi:10.​1016/​j.​expneurol.​2010.​01.​006 PubMedCrossRef
go back to reference González-Martínez D, Kim SH, Hu Y, Guimond S, Schofield J, Winyard P, Vannelli GB, Turnbull J, Bouloux PM (2004) Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci 24(46):10384–10392. doi:10.1523/JNEUROSCI.3400-04.2004 PubMedCrossRef González-Martínez D, Kim SH, Hu Y, Guimond S, Schofield J, Winyard P, Vannelli GB, Turnbull J, Bouloux PM (2004) Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci 24(46):10384–10392. doi:10.​1523/​JNEUROSCI.​3400-04.​2004 PubMedCrossRef
go back to reference Gritti A, Frolichsthal-Schoeller P, Galli R, Parati EA, Cova L, Pagano SF, Bjornson CR, Vescovi AL (1999) Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 19(9):3287–3297PubMed Gritti A, Frolichsthal-Schoeller P, Galli R, Parati EA, Cova L, Pagano SF, Bjornson CR, Vescovi AL (1999) Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J Neurosci 19(9):3287–3297PubMed
go back to reference Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A et al (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96(5):379–394PubMedCrossRef Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A et al (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96(5):379–394PubMedCrossRef
go back to reference Gunning P, Leavitt J, Muscat G, Ng SY, Kedes L (1987) A human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci USA 84(14):4831–4835PubMedPubMedCentralCrossRef Gunning P, Leavitt J, Muscat G, Ng SY, Kedes L (1987) A human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci USA 84(14):4831–4835PubMedPubMedCentralCrossRef
go back to reference Gutiérrez-Mecinas M, Crespo C, Blasco-Ibáñez JM, Gracia-Llanes FJ, Marqués-Marí AI, Nácher J, Varea E, Martínez-Guijarro FJ (2005) Distribution of D2 dopamine receptor in the olfactory glomeruli of the rat olfactory bulb. Eur J Neurosci 22(6):1357–1367. doi:10.1111/j.1460-9568.2005.04328.x PubMedCrossRef Gutiérrez-Mecinas M, Crespo C, Blasco-Ibáñez JM, Gracia-Llanes FJ, Marqués-Marí AI, Nácher J, Varea E, Martínez-Guijarro FJ (2005) Distribution of D2 dopamine receptor in the olfactory glomeruli of the rat olfactory bulb. Eur J Neurosci 22(6):1357–1367. doi:10.​1111/​j.​1460-9568.​2005.​04328.​x PubMedCrossRef
go back to reference Hébert JM, Lin M, Partanen J, Rossant J, McConnell SK (2003) FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development 130(6):1101–1111PubMedCrossRef Hébert JM, Lin M, Partanen J, Rossant J, McConnell SK (2003) FGF signaling through FGFR1 is required for olfactory bulb morphogenesis. Development 130(6):1101–1111PubMedCrossRef
go back to reference Hu Y, González-Martínez D, Kim SH, Bouloux PM (2004) Cross-talk of anosmin-1, the protein implicated in X-linked Kallmann’s syndrome, with heparan sulphate and urokinase-type plasminogen activator. Biochem J 384(Pt 3):495–505. doi:10.1042/BJ20041078 PubMedPubMedCentralCrossRef Hu Y, González-Martínez D, Kim SH, Bouloux PM (2004) Cross-talk of anosmin-1, the protein implicated in X-linked Kallmann’s syndrome, with heparan sulphate and urokinase-type plasminogen activator. Biochem J 384(Pt 3):495–505. doi:10.​1042/​BJ20041078 PubMedPubMedCentralCrossRef
go back to reference Kallmann F, Schoenfeld W, Barrera S (1944) The genetic aspects of primary eunuchoidism. Am J Ment Defic XLVIII:203–236 Kallmann F, Schoenfeld W, Barrera S (1944) The genetic aspects of primary eunuchoidism. Am J Ment Defic XLVIII:203–236
go back to reference Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25(9):2146–2157. doi:10.1634/stemcells.2007-0082 PubMedCrossRef Kerever A, Schnack J, Vellinga D, Ichikawa N, Moon C, Arikawa-Hirasawa E, Efird JT, Mercier F (2007) Novel extracellular matrix structures in the neural stem cell niche capture the neurogenic factor fibroblast growth factor 2 from the extracellular milieu. Stem Cells 25(9):2146–2157. doi:10.​1634/​stemcells.​2007-0082 PubMedCrossRef
go back to reference Klejbor I, Myers JM, Hausknecht K, Corso TD, Gambino AS, Morys J, Maher PA, Hard R, Richards J, Stachowiak EK, Stachowiak MK (2006) Fibroblast growth factor receptor signaling affects development and function of dopamine neurons—inhibition results in a schizophrenia-like syndrome in transgenic mice. J Neurochem 97(5):1243–1258. doi:10.1111/j.1471-4159.2006.03754.x PubMedCrossRef Klejbor I, Myers JM, Hausknecht K, Corso TD, Gambino AS, Morys J, Maher PA, Hard R, Richards J, Stachowiak EK, Stachowiak MK (2006) Fibroblast growth factor receptor signaling affects development and function of dopamine neurons—inhibition results in a schizophrenia-like syndrome in transgenic mice. J Neurochem 97(5):1243–1258. doi:10.​1111/​j.​1471-4159.​2006.​03754.​x PubMedCrossRef
go back to reference Legouis R, Hardelin JP, Levilliers J, Claverie JM, Compain S, Wunderle V, Millasseau P, Le Paslier D, Cohen D, Caterina D et al (1991) The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67(2):423–435 pii: 0092-8674(91)90193-3PubMedCrossRef Legouis R, Hardelin JP, Levilliers J, Claverie JM, Compain S, Wunderle V, Millasseau P, Le Paslier D, Cohen D, Caterina D et al (1991) The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67(2):423–435 pii: 0092-8674(91)90193-3PubMedCrossRef
go back to reference Li A, Saito M, Chuang JZ, Tseng YY, Dedesma C, Tomizawa K, Kaitsuka T, Sung CH (2011a) Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 13(4):402–411. doi:10.1038/ncb2218 PubMedPubMedCentralCrossRef Li A, Saito M, Chuang JZ, Tseng YY, Dedesma C, Tomizawa K, Kaitsuka T, Sung CH (2011a) Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 13(4):402–411. doi:10.​1038/​ncb2218 PubMedPubMedCentralCrossRef
go back to reference Liberia T, Blasco-Ibáñez JM, Nácher J, Varea E, Lanciego JL, Crespo C (2013) Two types of periglomerular cells in the olfactory bulb of the macaque monkey (Macaca fascicularis). Brain Struct Funct 218(4):873–887. doi:10.1007/s00429-012-0435-0 PubMedCrossRef Liberia T, Blasco-Ibáñez JM, Nácher J, Varea E, Lanciego JL, Crespo C (2013) Two types of periglomerular cells in the olfactory bulb of the macaque monkey (Macaca fascicularis). Brain Struct Funct 218(4):873–887. doi:10.​1007/​s00429-012-0435-0 PubMedCrossRef
go back to reference Lois C, Álvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264(5162):1145–1148PubMedCrossRef Lois C, Álvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264(5162):1145–1148PubMedCrossRef
go back to reference Lois C, García-Verdugo JM, Álvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271(5251):978–981PubMedCrossRef Lois C, García-Verdugo JM, Álvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271(5251):978–981PubMedCrossRef
go back to reference Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11(1):173–189 pii: 0896-6273(93)90281-UPubMedCrossRef Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11(1):173–189 pii: 0896-6273(93)90281-UPubMedCrossRef
go back to reference Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130(25):6361–6374. doi:10.1242/dev.00850 PubMedPubMedCentralCrossRef Macatee TL, Hammond BP, Arenkiel BR, Francis L, Frank DU, Moon AM (2003) Ablation of specific expression domains reveals discrete functions of ectoderm- and endoderm-derived FGF8 during cardiovascular and pharyngeal development. Development 130(25):6361–6374. doi:10.​1242/​dev.​00850 PubMedPubMedCentralCrossRef
go back to reference Martín C, Bueno D, Alonso MI, Moro JA, Callejo S, Parada C, Martín P, Carnicero E, Gato A (2006) FGF2 plays a key role in embryonic cerebrospinal fluid trophic properties over chick embryo neuroepithelial stem cells. Dev Biol 297(2):402–416. doi:10.1016/j.ydbio.2006.05.010 PubMedCrossRef Martín C, Bueno D, Alonso MI, Moro JA, Callejo S, Parada C, Martín P, Carnicero E, Gato A (2006) FGF2 plays a key role in embryonic cerebrospinal fluid trophic properties over chick embryo neuroepithelial stem cells. Dev Biol 297(2):402–416. doi:10.​1016/​j.​ydbio.​2006.​05.​010 PubMedCrossRef
go back to reference Merkle FT, Fuentealba LC, Sanders TA, Magno L, Kessaris N, Álvarez-Buylla A (2014) Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 17(2):207–214. doi:10.1038/nn.3610 PubMedCrossRef Merkle FT, Fuentealba LC, Sanders TA, Magno L, Kessaris N, Álvarez-Buylla A (2014) Adult neural stem cells in distinct microdomains generate previously unknown interneuron types. Nat Neurosci 17(2):207–214. doi:10.​1038/​nn.​3610 PubMedCrossRef
go back to reference Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Álvarez-Buylla A (2010a) The subventricular zone en-face: wholemount staining and ependymal flow. J Vis Exp (39). doi:10.3791/1938 Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Álvarez-Buylla A (2010a) The subventricular zone en-face: wholemount staining and ependymal flow. J Vis Exp (39). doi:10.​3791/​1938
go back to reference Mundiñano IC, Caballero MC, Ordóñez C, Hernández M, DiCaudo C, Marcilla I, Erro ME, Tuñón MT, Luquín MR (2011) Increased dopaminergic cells and protein aggregates in the olfactory bulb of patients with neurodegenerative disorders. Acta Neuropathol 122(1):61–74. doi:10.1007/s00401-011-0830-2 PubMedCrossRef Mundiñano IC, Caballero MC, Ordóñez C, Hernández M, DiCaudo C, Marcilla I, Erro ME, Tuñón MT, Luquín MR (2011) Increased dopaminergic cells and protein aggregates in the olfactory bulb of patients with neurodegenerative disorders. Acta Neuropathol 122(1):61–74. doi:10.​1007/​s00401-011-0830-2 PubMedCrossRef
go back to reference Murcia-Belmonte V, Medina-Rodríguez EM, Bribián A, de Castro F, Esteban PF (2014) ERK1/2 signaling is essential for the chemoattraction exerted by human FGF2 and human anosmin-1 on newborn rat and mouse OPCs via FGFR1. Glia. doi:10.1002/glia.22609 PubMed Murcia-Belmonte V, Medina-Rodríguez EM, Bribián A, de Castro F, Esteban PF (2014) ERK1/2 signaling is essential for the chemoattraction exerted by human FGF2 and human anosmin-1 on newborn rat and mouse OPCs via FGFR1. Glia. doi:10.​1002/​glia.​22609 PubMed
go back to reference Ortega F, Costa MR, Simon-Ebert T, Schroeder T, Gotz M, Berninger B (2011) Using an adherent cell culture of the mouse subependymal zone to study the behavior of adult neural stem cells on a single-cell level. Nat Protoc 6(12):1847–1859. doi:10.1038/nprot.2011.404 PubMedCrossRef Ortega F, Costa MR, Simon-Ebert T, Schroeder T, Gotz M, Berninger B (2011) Using an adherent cell culture of the mouse subependymal zone to study the behavior of adult neural stem cells on a single-cell level. Nat Protoc 6(12):1847–1859. doi:10.​1038/​nprot.​2011.​404 PubMedCrossRef
go back to reference Petreanu L, Álvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22(14):6106–6113 pii: 20026588 22/14/6106PubMed Petreanu L, Álvarez-Buylla A (2002) Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J Neurosci 22(14):6106–6113 pii: 20026588 22/14/6106PubMed
go back to reference Pignatelli A, Belluzzi O (2010) Neurogenesis in the adult olfactory bulb. In: Menini A (ed) The Neurobiology of Olfaction. CRC Press, Boca Raton (FL) Pignatelli A, Belluzzi O (2010) Neurogenesis in the adult olfactory bulb. In: Menini A (ed) The Neurobiology of Olfaction. CRC Press, Boca Raton (FL)
go back to reference Pujadas L, Gruart A, Bosch C, Delgado L, Teixeira CM, Rossi D, de Lecea L, Martínez A, Delgado-García JM, Soriano E (2010) Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J Neurosci 30(13):4636–4649. doi:10.1523/JNEUROSCI.5284-09.2010 PubMedCrossRef Pujadas L, Gruart A, Bosch C, Delgado L, Teixeira CM, Rossi D, de Lecea L, Martínez A, Delgado-García JM, Soriano E (2010) Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation. J Neurosci 30(13):4636–4649. doi:10.​1523/​JNEUROSCI.​5284-09.​2010 PubMedCrossRef
go back to reference Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000) Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 20(13):5012–5023 pii: 20/13/5012PubMed Raballo R, Rhee J, Lyn-Cook R, Leckman JF, Schwartz ML, Vaccarino FM (2000) Basic fibroblast growth factor (Fgf2) is necessary for cell proliferation and neurogenesis in the developing cerebral cortex. J Neurosci 20(13):5012–5023 pii: 20/13/5012PubMed
go back to reference Rugarli EI, Di Schiavi E, Hilliard MA, Arbucci S, Ghezzi C, Facciolli A, Coppola G, Ballabio A, Bazzicalupo P (2002) The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 129(5):1283–1294PubMed Rugarli EI, Di Schiavi E, Hilliard MA, Arbucci S, Ghezzi C, Facciolli A, Coppola G, Ballabio A, Bazzicalupo P (2002) The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 129(5):1283–1294PubMed
go back to reference Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12(6):669–688PubMedCrossRef Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12(6):669–688PubMedCrossRef
go back to reference Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, Parent A, Saghatelyan A (2009) Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci 29(13):4172–4188. doi:10.1523/JNEUROSCI.4956-08.2009 PubMedCrossRef Snapyan M, Lemasson M, Brill MS, Blais M, Massouh M, Ninkovic J, Gravel C, Berthod F, Gotz M, Barker PA, Parent A, Saghatelyan A (2009) Vasculature guides migrating neuronal precursors in the adult mammalian forebrain via brain-derived neurotrophic factor signaling. J Neurosci 29(13):4172–4188. doi:10.​1523/​JNEUROSCI.​4956-08.​2009 PubMedCrossRef
go back to reference Soussi-Yanicostas N, Hardelin JP, Arroyo-Jimenez MM, Ardouin O, Legouis R, Levilliers J, Traincard F, Betton JM, Cabanié L, Petit C (1996) Initial characterization of anosmin-1, a putative extracellular matrix protein synthesized by definite neuronal cell populations in the central nervous system. J Cell Sci 109:1749–1757 Soussi-Yanicostas N, Hardelin JP, Arroyo-Jimenez MM, Ardouin O, Legouis R, Levilliers J, Traincard F, Betton JM, Cabanié L, Petit C (1996) Initial characterization of anosmin-1, a putative extracellular matrix protein synthesized by definite neuronal cell populations in the central nervous system. J Cell Sci 109:1749–1757
go back to reference Soussi-Yanicostas N, de Castro F, Julliard AK, Perfettini I, Chedotal A, Petit C (2002) Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 109(2):217–228 pii: S0092867402007134PubMedCrossRef Soussi-Yanicostas N, de Castro F, Julliard AK, Perfettini I, Chedotal A, Petit C (2002) Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 109(2):217–228 pii: S0092867402007134PubMedCrossRef
go back to reference Stone DM, Grillo M, Margolis FL, Joh TH, Baker H (1991) Differential effect of functional olfactory bulb deafferentation on tyrosine hydroxylase and glutamic acid decarboxylase messenger RNA levels in rodent juxtaglomerular neurons. J Comp Neurol 311(2):223–233. doi:10.1002/cne.903110205 PubMedCrossRef Stone DM, Grillo M, Margolis FL, Joh TH, Baker H (1991) Differential effect of functional olfactory bulb deafferentation on tyrosine hydroxylase and glutamic acid decarboxylase messenger RNA levels in rodent juxtaglomerular neurons. J Comp Neurol 311(2):223–233. doi:10.​1002/​cne.​903110205 PubMedCrossRef
go back to reference Trumpp A, Depew MJ, Rubenstein JL, Bishop JM, Martin GR (1999) Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev 13(23):3136–3148PubMedPubMedCentralCrossRef Trumpp A, Depew MJ, Rubenstein JL, Bishop JM, Martin GR (1999) Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch. Genes Dev 13(23):3136–3148PubMedPubMedCentralCrossRef
go back to reference Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2(3):246–253. doi:10.1038/6350 PubMedCrossRef Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2(3):246–253. doi:10.​1038/​6350 PubMedCrossRef
go back to reference Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128(19):3759–3771PubMed Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128(19):3759–3771PubMed
go back to reference Yanicostas C, Herbomel E, Dipietromaria A, Soussi-Yanicostas N (2009) Anosmin-1a is required for fasciculation and terminal targeting of olfactory sensory neuron axons in the zebrafish olfactory system. Mol Cell Endocrinol 312(1–2):53–60. doi:10.1016/j.mce.2009.04.017 PubMedCrossRef Yanicostas C, Herbomel E, Dipietromaria A, Soussi-Yanicostas N (2009) Anosmin-1a is required for fasciculation and terminal targeting of olfactory sensory neuron axons in the zebrafish olfactory system. Mol Cell Endocrinol 312(1–2):53–60. doi:10.​1016/​j.​mce.​2009.​04.​017 PubMedCrossRef
go back to reference Zheng W, Nowakowski RS, Vaccarino FM (2004) Fibroblast growth factor 2 is required for maintaining the neural stem cell pool in the mouse brain subventricular zone. Dev Neurosci 26(2–4):181–196. doi:10.1159/000082136 PubMed Zheng W, Nowakowski RS, Vaccarino FM (2004) Fibroblast growth factor 2 is required for maintaining the neural stem cell pool in the mouse brain subventricular zone. Dev Neurosci 26(2–4):181–196. doi:10.​1159/​000082136 PubMed
Metadata
Title
Anosmin-1 over-expression increases adult neurogenesis in the subventricular zone and neuroblast migration to the olfactory bulb
Authors
Diego García-González
Verónica Murcia-Belmonte
Pedro F. Esteban
Felipe Ortega
David Díaz
Irene Sánchez-Vera
Rafael Lebrón-Galán
Laura Escobar-Castañondo
Luis Martínez-Millán
Eduardo Weruaga
José Manuel García-Verdugo
Benedikt Berninger
Fernando de Castro
Publication date
01-01-2016
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2016
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-014-0904-8

Other articles of this Issue 1/2016

Brain Structure and Function 1/2016 Go to the issue