Abstract
The olfactory system represents a perfect model to study the interactions between the central and peripheral nervous systems in order to establish a neural circuit during early embryonic development. In addition, another important feature of this system is the capability to integrate new cells generated in two neurogenic zones: the olfactory epithelium in the periphery and the wall of the lateral ventricles in the CNS, both during development and adulthood. In all these processes the combination and sequence of specific molecular signals plays a critical role in the wiring of the olfactory axons, as well as the precise location of the incoming cell populations to the olfactory bulb. The purpose of this review is to summarize recent insights into the cellular and molecular events that dictate cell settling position and axonal trajectories from their origin in the olfactory placode to the formation of synapses in the olfactory bulb to ensure rapid and reliable transmission of olfactory information from the nose to the brain.
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Polak E. T., Trotier D., Baliguand E., Odor similarities in structurally related odorants, Chem. Sens. Flav., 1978, 3, 369–380
Døving K. B., Trotier D., Structure and function of the vomeronasal organ, J. Exp. Biol., 1998, 201, 2913–2925
Dulac C., Torello A. T., Molecular dandection of pheromone signals in mammals, from genes to behaviour, Nat. Rev. Neurosci., 2003, 4, 551–562
Meredith M., Graziadei P. P., Graziadei G. A., Rashotti M. E., Smith J. C., Olfactory function after bulbectomy, Science, 1983, 222, 1254–1255
Spehr M., Spehr J., Ukhanov K., Kelliher K. R., Leinders-Zufall T., Zufall F., Parallel processing of social signals by the mammalian main and accessory olfactory systems, Cell. Mol. Life Sci., 2006, 63, 1476–1484
Trinh K., Storm D. R., Vomeronasal organ dandects odorants in absence of signaling through main olfactory epithelium, Nat. Neurosci., 2003, 6, 519–525
Lin D. M., Wang F., Lowe G., Gold G. H., Axel R., Ngai J. et al., Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity, Neuron, 2000, 26, 69–80
Golgi C., Sulla fine struttura dei bulbi olfattori, Rivista Sperimentale di Freniatria e di Medicina Legale, Regio-Emilia, 1875
Cajal S. R., Origen y terminación de las fibras nerviosas olfatorias, Gac. San. Barcelona, 1890
Cajal S. R., La textura del sistema nervioso del hombre y los vertebrados, Moya, Madrid, 1904
Chess A., Simon I., Cedar H., Axel R., Allelic inactivation regulates olfactory receptor gene expression, Cell, 1994, 78, 823–834
Malnic B., Hirono J., Sato T., Buck L. B., Combinatorial receptor codes for odors, Cell, 1999, 96, 713–723
Buck L., Axel R., A novel multigene family may encode odorant receptors: a molecular basis for odor recognition, Cell, 1991, 65, 175–187
Zhang X., Firestein S., The olfactory receptor gene superfamily of the mouse, Nat. Neurosci., 2002, 5, 124–133
Godfrey P. A., Malnic B., Buck L. B., The mouse olfactory receptor gene family, Proc. Natl. Acad. Sci. U S A, 2004, 101, 2156–2161
Malnic B., Godfrey P. A., Buck L. B., The human olfactory receptor gene family, Proc. Natl. Acad. Sci. U S A, 2004, 101, 2584–2589
Ressler K. J., Sullivan S. L., Buck L. B., A zonal organization of odorant receptor gene expression in the olfactory epithelium, Cell, 1993, 73, 597–609
Vassar R., Ngai J., Axel R., Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium, Cell, 1993, 74, 309–318
Ressler K. J., Sullivan S. L., Buck L. B., Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb, Cell, 1994, 79, 1245–1255
Vassar R., Chao S. K., Sitcheran R., Nuñez J. M., Vosshall L. B., Axel R., Topographic organization of sensory projections to the olfactory bulb, Cell, 1994, 79, 981–991
Mombaerts P., Wang F., Dulac C., Chao S. K., Nemes A., Mendelsohn M. et al., Visualizing an olfactory sensory map, Cell, 1996, 87, 675–686
Wang F., Nemes A., Mendelsohn M., Axel R., Odorant receptors govern the formation of a precise topographic map, Cell, 1998, 93, 47–60
Miller A. M., Maurer L. R., Zou D. J., Firestein S., Greer C. A., Axon fasciculation in the develo** olfactory nerve, Neural Dev., 2010, 5, 20
Valverde F., Studies on the Piriform Lobe, Harvard University Press, 1965
Price J. L., A study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex, J. Comp. Neurol., 1973, 150, 87–108
Devor M., Fiber trajectories of olfactory bulb efferents in the hamster, J. Comp. Neurol., 1976, 166, 31–48
Schwob J. E., Price J. L., The development of lamination of afferent fibers to the olfactory cortex in rats, with additional observations in the adult, J. Comp. Neurol., 1984, 223, 203–222
López-Mascaraque L., De Carlos J. A., Valverde F., Early onset of the rat olfactory bulb projections, Neuroscience, 1996, 70, 255–266
Walz A., Omura M., Mombaerts P., Development and topography of the lateral olfactory tract in the mouse, imaging by genetically encoded and injected fluorescent markers, J. Neurobiol., 2006, 66, 835–846
Inaki K., Nishimura S., Nakashiba T., Itohara S., Yoshihara Y., Laminar organization of the develo** lateral olfactory tract revealed by differential expression of cell recognition molecules, J. Comp. Neurol., 2004, 479, 243–256
Yamatani H., Sato Y., Fujisawa H., Hirata T., Chronotopic organization of the olfactory bulb axons in the lateral olfactory tract, J. Comp. Neurol., 2004, 475, 247–260
Altman J., 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., 1969, 137, 433–457
Graziadei G. A., Graziadei P. P., Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy, J. Neurocytol., 1979, 8, 197–213
Mombaerts P., Axonal wiring in the mouse olfactory system, Annu. Rev. Cell. Dev. Biol., 2006, 22, 713–737
Luskin M. B., Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone, Neuron, 1993, 11, 173–189
Lois C., Alvarez-Buylla A., Long-distance neuronal migration in the adult mammalian brain, Science, 1994, 264, 1145–1148
Doetsch F., Caillé I., Lim D. A., García-Verdugo J. M., Alvarez-Buylla A., Subventricular zone astrocytes are neural stem cells in the adult mammalian brain, Cell, 1999, 97, 703–716
Suzuki S. O., Goldman J. E., Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways, a dynamic study of glial and neuronal progenitor migration, J. Neurosci., 2003, 23, 4240–4250
Alvarez-Buylla A., Kohwi M., Nguyen T. M., Merkle F. T., The heterogeneity of adult stem cells and the emerging complexity of their niche, Cold Spring Harb. Symp. Quant. Biol., 2008, 73, 357–365
García-Moreno F., López-Mascaraque L., De Carlos J. A., Early telencephalic migration topographically converging in the olfactory cortex, Cereb. Cortex, 2008, 18, 1239–1252
Ninkovic J., Mori T., Götz M., Distinct modes of neuron addition in adult mouse neurogenesis, J. Neurosci., 2007, 27, 10906–10911
Brill M. S., Ninkovic J., Winpenny E., Hodge R. D., Ozen I., Yang R. et al., Adult generation of glutamatergic olfactory bulb interneurons, Nat. Neurosci., 2009, 12, 1524–1533
Doucette J. R. The glial cells in the nerve fiber layer of the rat olfactory bulb, Anat. Rec., 1984, 210, 385–391
Valverde F., Santacana M., Heredia M., Formation of an olfactory glomerulus, morphological aspects of development and organization, Neuroscience, 1992, 49, 255–275
Farbman A. I., Squinto L. M., Early development of olfactory receptor cell axons, Brain Res., 1985, 351, 205–213
Marin-Padilla M., Amieva M. R., Early neurogenesis of the mouse olfactory nerve, Golgi and electron microscopic studies, J. Comp. Neurol., 1989, 288, 339–352
De Carlos J. A., López-Mascaraque L., Valverde F., The telencephalic vesicles are innervated by olfactory placode-derived cells, a possible mechanism to induce neocortical development, Neuroscience, 1995, 68, 1167–1178
Fornaro M., Geuna S., Fasolo A., Giacobini-Robecchi M. G., Evidence of very early neuronal migration from the olfactory placode of the chick embryo, Neuroscience, 2001, 107, 191–197
Hinds J. W., Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of ori-gin of neurons and neuroglia, J. Comp. Neurol., 1968, 134, 287–304
Bayer S. A., 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb, Exp. Brain Res., 1983, 50, 329–340
Jiménez D., García C., de Castro F., Chédotal A., Sotelo C., De Carlos J. A. et al., Evidence for intrinsic development of olfactory structures in Pax-6 mutant mice, J. Comp. Neurol., 2000, 428, 511–526
Blanchart A., De Carlos J. A., López-Mascaraque L., Time frame of mitral cell development in the mice olfactory bulb, J. Comp. Neurol., 2006, 496, 529–543
Santacana M., Heredia M., Valverde F., Development of the main efferent cells of the olfactory bulb and of the bulbar component of the anterior commissure, Brain Res. Dev. Brain Res., 1992, 65, 75–83
Gong Q., Shipley M. T., Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb, Neuron, 1995, 14, 91–101
López-Mascaraque L., García C., Valverde F., de Carlos J. A., Central olfactory structures in Pax-6 mutant mice, Ann. N Y Acad. Sci., 1998, 855, 83–94
López-Mascaraque L., de Castro F., The olfactory bulb as an independent developmental domain, Cell Death Differ., 2002, 9, 1279–1286
Doucette R., Development of the nerve fiber layer in the olfactory bulb of mouse embryos, J. Comp. Neurol., 1989, 285, 514–527
Pellier V., Astic L., Oestreicher A. B., Saucier D., B-50/GAP-43 expression by the olfactory receptor cells and the neurons migrating from the olfactory placode in embryonic rats, Brain Res. Dev. Brain Res., 1994, 80, 63–72
Honma S., Kawano M., Hayashi S., Kawano H., Hisano S., Expression and immunohistochemical localization of vesicular glutamate transporter 2 in the migratory pathway from the rat olfactory placode, Eur. J. Neurosci., 2004, 20, 923–936
Miller A. M., Treloar H. B., Greer C. A., Composition of the migratory mass during development of the olfactory nerve, J. Comp. Neurol., 2010, 518, 4825–4841
Blanchart A., Martín-López E., De Carlos J. A., López-Mascaraque L., Peripheral contributions to olfactory bulb cell populations (migrations towards the olfactory bulb), Glia, 2011, 59, 278–292
Murdoch B., Roskams A. J., A novel embryonic nestin-expressing radial glia-like progenitor gives rise to zonally restricted olfactory and vomeronasal neurons, J. Neurosci., 2008, 28, 4271–4282
Blanchart A., Romaguera M., García-Verdugo J. M., De Carlos J. A., López-Mascaraque L., Synaptogenesis in the mouse olfactory bulb during glomerulus development, Eur. J. Neurosci., 2008, 27, 2838–2846
Blanes T., Sobre algunos puntos dudoses de la estructura del bulbo olfatorio, Rev. Trimest. Microgr., 1898, 3, 99–127
Valverde F., López-Mascaraque L., Neuroglial arrangements in the olfactory glomeruli of the hedgehog, J. Comp. Neurol., 1991, 307, 658–674
Goodman M. N., Silver J., Jacobberger J. W., Establishment and neurite outgrowth properties of neonatal and adult rat olfactory bulb glial cell lines, Brain Res., 1993, 619, 199–213
Tisay K. T., Key B., The extracellular matrix modulates olfactory neurite outgrowth on ensheathing cells, J. Neurosci., 1999, 19, 9890–9899
Kafitz K. W., Greer C. A., Olfactory ensheathing cells promote neurite extension from embryonic olfactory receptor cells in vitro, Glia, 1999, 25, 99–110
Lipson A. C., Widenfalk J., Lindqvist E., Ebendal T., Olson L., Neurotrophic properties of olfactory ensheathing glia, Exp., Neurol., 2003, 180, 167–171
Chung R. S., Woodhouse A., Fung S., Dickson T. C., West A. K., Vickers J. C. et al., Olfactory ensheathing cells promote neurite sprouting of injured axons in vitro by direct cellular contact and secretion of soluble factors, Cell. Mol. Life Sci., 2004, 61, 1238–1245
Leaver S. G., Harvey A. R., Plant G. W., Adult olfactory ensheathing glia promote the long-distance growth of adult retinal ganglion cell neurites in vitro, Glia, 2006, 53, 467–476
Deumens R., Koopmans G. C., Honig W. M., Hamers F. P., Maquet V., Jérôme R., et al., Olfactory ensheathing cells, olfactory nerve fibroblasts and biomatrices to promote long-distance axon regrowth and functional recovery in the dorsally hemisected adult rat spinal cord, Exp. Neurol., 2006, 200, 89–103
Au E., Richter M. W., Vincent A. J., Tetzlaff W., Aebersold R., Sage E. H. et al., SPARC from olfactory ensheathing cells stimulates Schwann cells to promote neurite outgrowth and enhances spinal cord repair, J. Neurosci., 2007, 27, 7208–7221
Runyan S. A., Phelps P. E., Mouse olfactory ensheathing glia enhance axon outgrowth on a myelin substrate in vitro, Exp. Neurol., 2009, 216, 95–104
Pellitteri R., Spatuzza M., Russo A., Zaccheo D., Stanzani S., Olfactory ensheathing cells represent an optimal substrate for hippocampal neurons, an in vitro study, Int. J. Dev., Neurosci., 2009, 27, 453–458
Wang Y. Z., Molotkov A., Song L., Li Y., Pleasure D. E., Zhou C. J., Activation of the Wnt/beta-catenin signaling reporter in develo** mouse olfactory nerve layer marks a specialized subgroup of olfactory ensheathing cells, Dev. Dynam., 2008, 237, 3157–3168
Zaghetto A. A., Paina S., Mantero S., Platonov N., Peretto P., Bovetti S. et al., Activation of the Wnt-beta catenin pathway in a cell population on the surface of the forebrain is essential for the establishment of olfactory axon connections, J. Neurosci., 2007, 27, 9757–9768
Liu K. L., Chuah M. I., Lee K. K., Soluble factors from the olfactory bulb attract olfactory Schwann cells, J. Neurosci., 1995, 15, 990–1000
López-Mascaraque L., García C., Blanchart A., De Carlos J. A., Olfactory epithelium influences the orientation of mitral cell dendrites during development, Dev. Dynam., 2005, 232, 325–335
Jefferis G. S., Vyas R. M., Berdnik D., Ramaekers A., Stocker R. F., Tanaka N. K. et al. Developmental origin of wiring specificity in the olfactory system of Drosophila, Development, 2004, 131, 117–130
Graziadei P. P., Monti-Graziadei A. G., The influence of the olfactory placode on the development of the telencephalon in Xenopus laevis, Neuroscience, 1992, 46, 617–629
LaMantia A. S., Bhasin N., Rhodes K., Heemskerk J., Mesenchymal/epithelial induction mediates olfactory pathway formation, Neuron, 2000, 28, 411–425
Anchan R. M., Drake D. P., Haines C. F., Gerwe E. A., LaMantia A. S., Disruption of local retinoid-mediated gene expression accompanies abnormal development in the mammalian olfactory pathway, J. Comp. Neurol., 1997, 379, 171–184
Mizrahi A., Katz L. C., Dendritic stability in the adult olfactory bulb, Nat. Neurosci., 2003, 6, 1201–1207
Kossel A. H., Williams C. V., Schweizer M., Kater S. B., Afferent innervation influences the development of dendritic branches and spines via both activity-dependent and non-activity-dependent mechanisms, J. Neurosci., 1997, 17, 6314–6324
Acebes A., Ferrús A., Cellular and molecular features of axon collaterals and dendrites, Trends Neurosci., 2000, 23, 557–565
Cline, H. T., Dendritic arbor development and synaptogenesis, Curr. Opin. Neurobiol., 2001, 11, 118–126
Wong R. O., Ghosh A., Activity-dependent regulation of dendritic growth and patterning, Nat. Rev. Neurosci., 2002, 3, 803–812
Yuan Q., Knöpfel T., Olfactory nerve stimulation-induced calcium signaling in the mitral cell distal dendritic tuft, J. Neurophysiol., 2006, 95, 2417–2426
Zhou Z., **ong W., Masurkar A. V., Chen W. R., Shepherd G. M., Dendritic calcium plateau potentials modulate input-output properties of juxtaglomerular cells in the rat olfactory bulb, J. Neurophysiol., 2006, 96, 2354–2363
Hinds J. W., Ruffett T. L., Mitral cell development in the mouse olfactory bulb, reorientation of the perikaryon and maturation of the axon initial segment, J. Comp. Neurol., 1973, 151, 281–306
Chen H., He Z., Bagri A., Tessier-Lavigne M., Semaphorin-neuropilin interactions underlying sympathetic axon responses to class III semaphorins, Neuron, 1998, 21, 1283–1290
Zou Y., Stoeckli E., Chen H., Tessier-Lavigne M., Squeezing axons out of the gray matter, a role for slit and semaphorin proteins from midline and ventral spinal cord, Cell, 2000, 102, 363–375
Giger R. J., Cloutier J. F., Sahay A., Prinjha R. K., Levengood D. V., Moore S. E. et al., Neuropilin-2 is required in vivo for selective axon guidance responses to secreted semaphorins, Neuron, 2000, 25, 29–41
Kobayashi H., Koppel A. M., Luo Y., Raper J. A., A role for collapsin-1 in olfactory and cranial sensory axon guidance, J. Neurosci., 1997, 17, 8339–8352
Schwarting G. A., Kostek C., Ahmad N., Dibble C., Pays L., Puschel A. W., Semaphorin 3A is required for guidance of olfactory axons in mice, J. Neurosci., 2000, 20, 7691–7697
Takeuchi H., Inokuchi K., Aoki M., Suto F., Tsuboi A., Matsuda I. et al., Sequential arrival and graded secretion of Sema 3F by olfactory neuron axons specify map topography at the bulb, Cell, 2010, 141, 1056–1067
Walz A., Rodriguez I., Mombaerts P., Aberrant sensory innervation of the olfactory bulb in neuropilin-2 mutant mice, J. Neurosci., 2002, 22, 4025–4035
Renzi M. J., Wexler T. L., Raper J. A., Olfactory sensory axons expressing a dominant-negative semaphorin receptor enter the CNS early and overshoot their target, Neuron, 2000, 28, 437–447
Giger R. J., Urquhart E. R., Gillespie S. K., Levengood D. V., Ginty D. D., Kolodkin A. L., Neuropilin-2 is a receptor for semaphorin IV, insight into the structural basis of receptor function and specificity, Neuron, 1998, 21, 1079–1092
De Castro F., Wiring olfaction: the cellular and molecular mechanisms that guide the development of synaptic connections from the nose to the cortex, Front. Neurosci., 2009, doi: 10. 3389/neuro. 22. 004. 2009.
Chen H., Chédotal A., He Z., Goodman C. S., Tessier-Lavigne M., Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorinsSema E and Sema IV but not Sema III, Neuron, 1997, 19, 547–559
Chen H., Bagri A., Zupicich J. A., Zou Y., Stoeckli E., Pleasure S. J., et al., Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections, 2000, Neuron, 25, 43–56
Kiani C., Chen L., Wu Y. J., Yee A. J., Yang B. B., Structure and function of aggrecan, Cell Res., 2002, 12, 19–32
Seidenbecher C. I., Richter K., Rauch U., Fässler R., Garner C. C., Gundelfinger E. D., Brevican, a chondroitin sulfate proteoglycan of rat brain, occurs as secreted and cell surface glycosylphosphatidylinositolanchored isoforms, J. Biol. Chem., 1995, 270, 27, 206–212
Pyka M., Wetzel C., Aguado A., Geissler M., Hatt H., Faissner A., Chondroitin sulfate proteoglycans regulate astrocyte-dependent synaptogenesis and modulate synaptic activity in primary embryonic hippocampal neurons, Eur. J. Neurosci., 2011, 33, 2187–2202
Yamada H., Fredette B., Shitara K., Hagihara K., Miura R., Ranscht B. et al., The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons, J. Neurosci., 1997, 17, 7784–7795
Turner N., Mason P. J., Brown R., Fox M., Povey S., Rees A. et al., Molecular cloning of the human Goodpasture antigen demonstrates it to be the alpha 3 chain of type IV collagen, J. Clin. Invest., 1992, 89, 592–601
Abrahamson D. R., Isom K., Roach E., Stroganova L., Zelenchuk A., Miner J. H. et al., Laminin compensation in collagen alpha3(IV) knockout (Alport) glomeruli contributes to permeability defects, J. Am. Soc. Nephrol., 2007, 18, 2465–2472
Tanaka M., Asada M., Higashi A. Y., Nakamura J., Oguchi A., Tomita M. et al., Loss of the BMP antagonist USAG-1 ameliorates disease in a mouse model of the progressive hereditary kidney disease Alport syndrome, J. Clin. Invest., 2010, 120, 768–777
Demyanenko G. P., Riday T. T., Tran T. S., Dalal J., Darnell E. P., Brennaman L. H., et al., NrCAM deletion causes topographic mistargeting of thalamocortical axons to the visual cortex and disrupts visual acuity, J. Neurosci., 2011, 31, 1545–1558
De Carlos J. A., López-Mascaraque L., Valverde F., Early olfactory fiber projections and cell migration into the rat telencephalon, Int. J. Dev. Neurosci., 1996, 14, 853–866
Bailey M., Puche A. C., Shipley M. T., Development of the olfactory bulb, evidence for glia-neuron interactions in glomerular formation, J. Comp. Neurol., 1999, 415, 423–448
Treloar H. B., Purcell A. L., Greer C. A., Glomerular formation in the develo** rat olfactory bulb, J. Comp. Neurol., 1999, 413, 289–304
Treloar H. B, Uboha U., Jeromin A., Greer C. A., Expression of the neuronal calcium sensor protein NCS-1 in the develo** mouse olfactory pathways, J. Comp. Neurol., 2005, 482, 201–216
Aiga M., Levinson J. N., Bamji S. X., N-cadherin and neuroligins cooperate to regulate synapse formation in hippocampal cultures, J. Biol. Chem., 2011, 286, 851–858
Lee H., Dean C., Isacoff E., Alternative splicing of neuroligin regulates the rate of presynaptic differentiation, J. Neurosci., 2010, 30, 11435–11446
Ahn K., Shelton C. C., Tian Y., Zhang X., Gilchrist M. L., Sisodia S. S., et al., Activation and intrinsic gamma-secretase activity of presenilin 1, Proc. Natl. Acad. Sci. U S A, 2010, 107, 21435–21440
Gadadhar A., Marr R., Lazarov O., Presenilin-1 regulates neural progenitor cell differentiation in the adult brain, J. Neurosci., 2011, 31, 2615–2623
Tran P. B., Banisadr G., Ren D., Chenn A., Miller R. J., Chemokine receptor expression by neural progenitor cells in neurogenic regions of mouse brain, J. Comp. Neurol., 2007, 500, 1007–1033
Skuljec J., Sun H., Pul R., Bénardais K., Ragancokova D., Moharregh-Khiabani D. et al., CCL5 induces a pro-inflammatory profile in microglia in vitro, Cell Immunol., 2011, 270, 164–171
Bolitho C., Hahn M. A., Baxter R. C., Marsh D. J., The chemokine CXCL1 induces proliferation in epithelial ovarian cancer cells by transactivation of the epidermal growth factor receptor, Endocr. Relat. Cancer, 2010, 17, 929–940
Pineau I., Sun L., Bastien D., Lacroix S., Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/MyD88-dependent fashion, Brain Behav. Immun., 2010, 24, 540–553
Krathwohl M. D., Kaiser J. L., Chemokines promote quiescence and survival of human neural progenitor cells, Stem Cells, 2004, 22, 109–118
Ni H. T., Hu S., Sheng W. S., Olson J. M., Cheeran M. C., Chan A. S. et al., High-level expression of functional chemokine receptor CXCR4 on human neural precursor cells, Brain Res. Dev. Brain Res., 2004, 152, 159–169
Tran P. B., Ren D., Miller R. J., The HIV-1 coat protein gp120 regulates CXCR4-mediated signaling in neural progenitor cells, J. Neuroimmunol., 2005, 160, 68–76
Ceci M. L., López-Mascaraque L., De Carlos J. A., The influence of the environment on Cajal-Retzius cell migration, Cereb. Cortex, 2010, 20, 2348–2360
Fearon E. R., Cho K. R., Nigro J. M., Kern S. E., Simons J. W., Ruppert J. M. et al., Identification of a chromosome 18q gene that is altered in colorectal cancers. Science, 1990, 247, 49–56
Keino-Masu K., Masu M., Hinck L., Leonardo E. D., Chan S. S., Culotti J. G. et al. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor, Cell, 1996, 87, 175–185
Chan S. S., Zheng H., Su M. W., Wilk R., Killeen M. T., Hedgecock E. M. et al., UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues, Cell, 1996, 87, 187–195
Fazeli A., Dickinson S. L., Hermiston M. L., Tighe R. V., Steen R. G., Small C. G. et al., Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene, Nature, 1997, 386, 796–804
Stein E., Tessier-Lavigne M., Hierarchical organization of guidance receptors, silencing of netrin attraction by slit through a Robo/DCC receptor complex, Science, 2001, 291, 1928–1938
Mehlen P., Rabizadeh S., Snipas S. J., Assa-Munt N., Salvesen G. S., Bredesen D. E., The DCC gene product induces apoptosis by a mechanism requiring receptor proteolysis, Nature, 1998, 395, 801–804
Shi M., Zheng M. H., Liu Z. R., Hu Z. L., Huang Y., Chen J. Y. et al., DCC is specifically required for the survival of retinal ganglion and displaced amacrine cells in the develo** mouse retina, Dev. Biol., 2010, 348, 87–96
Pellier V., Saucier D., Oestreicher A. B., Astic L., Ultrastructural and cytochemical identification of apoptotic cell death accompanying development of the fetal rat olfactory nerve layer, Anat. Embryol., 1996, 194, 99–109
Beltaifa S., Webster M. J., Ligons D. L., Fatula R. J., Herman M. M., Kleinman J. E. et al., Discordant changes in cortical TrkC mRNA and protein during the human lifespan, Eur. J. Neurosci., 2005, 21, 2433–2444
Nikoletopoulou V., Lickert H., Frade J. M., Rencurel C., Giallonardo P., Zhang L. et al., Neurotrophin receptors TrkA and TrkC cause neuronal death whereas TrkB does not, Nature, 2010, 467, 59–63
Irie A., Yates E. A., Turnbull J. E., Holt C. E., Specific heparan sulfate structures involved in retinal axon targeting, Development, 2002, 129, 61–70
Inatani M., Irie F., Plump A. S., Tessier-Lavigne M., Yamaguchi Y., Mammalian brain morphogenesis and midline axon guidance require heparan sulphate, Science, 2003, 302, 1044–1046
Johnson K. G., Ghose A., Epstein E., Lincecum J., O’Connor M. B., Van Vactor D., Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance, Curr. Biol., 2004, 14, 499–504
Steigemann P., Molitor A., Fellert S., Jäckle H., Vorbrüggen G., Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signalling, Curr. Biol., 2004, 14, 225–230
Ivins J. K., Litwack E. D., Kumbasar A., Stipp C. S., Lander A. D., Cerebroglycan, a developmentally regulated cell-surface heparansulfate proteoglycan, is expressed on develo** axons and growth cones, Dev. Biol., 1997, 184, 320–332
Alahari S. K., Lee J. W., Juliano R. L., Nischarin, a novel protein that interacts with the integrin alpha5 subunit and inhibits cell migration, J. Cell. Biol., 2000, 151, 1141–1154
Alahari S. K., Nasrallah H., A membrane proximal region of the integrin alpha5 subunit is important for its interaction with nischarin, Biochem. J., 2004, 377, 449–457
Cho J. H., Lépine M., Andrews W., Parnavelas J., Cloutier J. F., Requirement for Slit-1 and Robo-2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb, J. Neurosci., 2007, 27, 9094–9104
Nguyen-Ba-Charvet K. T., Di Meglio T., Fouquet C., Chédotal A., Robos and slits control the pathfinding and targeting of mouse olfactory sensory axons, J. Neurosci., 2008, 28, 4244–4249
Prince J. E., Cho J. H., Dumontier E., Andrews W., Cutforth T., Tessier-Lavigne M. et al., Robo-2 controls the segregation of a portion of basal vomeronasal sensory neuron axons to the posterior region of the accessory olfactory bulb, J. Neurosci, 2009, 29, 14211–14222
Patel K., Nash J. A., Itoh A., Liu Z., Sundaresan V., Pini A., Slit proteins are not dominant chemorepellents for olfactory tract and spinal motor axons, Development, 2001, 128, 5031–5037
Dugan J. P., Stratton A., Riley H. P., Farmer W. T., Mastick G. S., Midbrain dopaminergic axons are guided longitudinally through the diencephalon by Slit/Robo signals, Mol. Cell. Neurosci., 2011, 46, 347–356
Indulekha C. L., Divya T. S., Divya M. S., Sanalkumar R., Rasheed V. A., Dhanesh S. B. et al., Hes-1 regulates the excitatory fate of neural progenitors through modulation of Tlx3 (HOX11L2) expression, Cell. Mol. Life Sci., 2011, in press, DOI 10. 1007/s00018-011-0765-8
Kondo T., Matsuoka A. J., Shimomura A., Koehler K. R., Chan R. J., Miller J. M., et al., Wnt signaling promotes neuronal differentiation from mesenchymal stem cells through activation of Tlx 3, Stem Cells, 2011, 29, 836–846
Wang Y. Z., Molotkov A., Song L., Li Y., Pleasure D. E., Zhou C. J., Activation of the Wnt/beta-catenin signalling reporter in develo** mouse olfactory nerve layer marks a specialized subgroup of olfactory ensheating cells, Dev. Dynam., 2008, 237, 157–168
Corotto F. S., Henegar J. A., Maruniak J. A., Neurogenesis persists in the subependymal layer of the adult mouse brain, Neurosci. Lett., 1993, 149, 111–114
Yoon S. O., Lois C., Alvirez M., Alvarez-Buylla A., Falck-Pedersen E., Chao M. V., Adenovirus-mediated gene delivery into neuronal precursors of the adult mouse brain, Proc. Natl. Acad. Sci. U S A, 1996, 93, 11974–11979
Batista-Brito R., Close J., Machold R., Fishell G., The distinct temporal origins of olfactory bulb interneuron subtypes, J. Neurosci., 2008, 28, 3966–3975
Popp S., Andersen J. S., Maurel P., Margolis R. U., Localization of aggrecan and versican in the develo** rat central nervous system, Dev. Dynam., 2003, 227, 143–149
Adams N. C., Tomoda T., Cooper M., Dietz G., Hatten M. E., Mice that lack astrotactin have slowed neuronal migration, Development, 2002, 129, 965–972
Samson M., Labbe O., Mollereau C., Vassart G., Parmentier M., Molecular cloning and functional expression of a new human CCchemokine receptor gene”, Biochemistry, 1996, 35, 3362–3367
Wu Q, Maniatis T., A striking organization of a large family of human neural cadherin-like cell adhesion genes, Cell, 1999, 97, 779–790
Anisowicz A., Bardwell L., Sager R., Constitutive overexpression of a growth-regulated gene in transformed Chinese hamster and human cells, Proc. Natl. Acad. Sci. U S A, 1987, 84, 7188–7192
Bagri A., Gurney T., He X., Zou Y. R., Littman D. R., Tessier-Lavigne M. et al., The chemokine SDF 1 regulates migration of dentate granule cells, Development, 2002, 129, 4249–4260
Tissir F., Wang C. E., Goffinet A. M., Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development, Brain Res. Dev. Brain Res., 2004, 149, 63–71
Lieberam I., Agalliu D., Nagasawa T., Ericson J., Jessell T. M., A Cxcl 12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons, Neuron, 2005, 47, 667–679
Belmadani A., Tran P. B., Ren D., Assimacopoulos S., Grove E. A., Miller R. J., The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors, J. Neurosci., 2005, 25, 3995–4003
Martín-López E., Blanchart A., De Carlos J. A., López-Mascaraque L., Dab1 (disable homolog-1) reelin adaptor protein is overexpressed in the olfactory bulb at early postnatal stages. PLoS One, 2011, 6, e26673
Mehlen P., Bredesen D. E., The dependence receptor hypothesis, Apoptosis, 2004, 9, 37–49
Fischman K., Edman J. C., Shackleford G. M., Turner J. A., Rutter W. J., Nir U., A murine fer testis-specific transcript (ferT) encodes a truncated Fer protein, Mol. Cell Biol., 1990, 10, 146–153
Craig A. W., Greer P. A., Fer kinase is required for sustained p38 kinase activation and maximal chemotaxis of activated mast cells, Mol. Cell. Biol., 2002, 22, 6363–6367
Herndon M. E., Stipp C. S., Lander A. D., Interactions of neural glycosaminoglycans and proteoglycans with protein ligands, assessment of selectivity, heterogeneity and the participation of core proteins in binding, Glycobiology, 1999, 9, 143–155
Chuang P. T., McMahon A. P., Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein, Nature, 1999, 397, 617–621
Semple B. D., Kossmann T., Morganti-Kossmann M. C., Role of chemokines in CNS health and pathology, a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks, J. Cereb. Blood Flow Metab., 2010, 30, 459–473
Deng Q., Andersson E., Hedlund E., Alekseenko Z., Coppola E., Panman L., et al., Specific and integrated roles of Lmx 1a, Lmx1b and Phox2a in ventral midbrain development, Development, 2011, 138, 3399–3408
Li H. P., Oohira A., Ogawa M., Kawamura K., Kawano H., Aberrant trajectory of thalamocortical axons associated with abnormal localization of neurocan immunoreactivity in the cerebral neocortex of reeler mutant mice, Eur. J. Neurosci., 2005, 22, 2689–2696
Pollard J. D., Armati P. J., CIDP — the relevance of recent advances in Schwann cell/axonal neurobiology, J. Peripher. Nerv. Syst., 2011, 16, 15–23
Cariboni A., Davidson K., Rakic S., Maggi R., Parnavelas J. G., Ruhrberg C., Defective gonadotropin-releasing hormone neuron migration in mice lacking SEMA3A signalling through NRP1 and NRP2: implications for the aetiology of hypogonadotropic hypogonadism, Hum. Mol. Genet., 2011, 20, 336–344
McIntyre J. C., Titlow W. B., McClintock T. S., Axon growth and guidance genes identify nascent, immature, and mature olfactory sensory neurons, J. Neurosci. Res., 2010, 88, 3243–3256
Barallobre M. J., Pascual M., Del Río J. A., Soriano E., The netrin family of guidance factors: emphasis on netrin-1 signalling, Brain Res. Brain Res. Rev., 2005, 49, 22–47
Hakanen J., Duprat S., Salminen M., Netrin1 is required for neural and glial precursor migrations into the olfactory bulb, Dev. Biol., 2011, 355, 101–114
Imamura F., Greer C. A., Dendritic branching of olfactory bulb mitral and tufted cells, regulation by TrkB, PLoS One, 2009, 4, e6729
Hasegawa R., Takami S., Nishiyama F., Immunoelectron microscopic analysis of the distribution of tyrosine kinase receptor B in olfactory axons, Anat. Sci. Int., 2008, 83, 186–194
Levy J. B., Canoll P. D., Silvennoinen O., Barnea G., Morse B., Honegger A. M. et al., The cloning of a receptor-type protein tyrosine phosphatase expressed in the central nervous system, J. Biol. Chem., 1993, 268, 10573–10581
Ulbricht U., Eckerich C., Fillbrandt R., Westphal M., Lamszus K., RNA interference targeting protein tyrosine phosphatase zeta/receptortype protein tyrosine phosphatase beta suppresses glioblastoma growth in vitro and in vivo, J. Neurochem., 2006, 98, 1497–1506
Hivert B., Liu Z., Chuang C. Y., Doherty P., Sundaresan V., Robo1 and Robo2 are homophilic binding molecules that promote axonal growth, Mol. Cell. Neurosci., 2002, 21, 534–545
Walz A., Feinstein P., Khan M., Mombaerts P., Axonal wiring of guanylate cyclase-D-expressing olfactory neurons is dependent on neuropilin 2 and semaphorin 3F, Development, 2007, 134, 4063–4072
Cloutier J. F., Sahay A., Chang E. C., Tessier-Lavigne M., Dulac C., Kolodkin A. L. et al., Differential requirements for semaphorin 3F and Slit-1 in axonal targeting, fasciculation, and segregation of olfactory sensory neuron projections, J. Neurosci., 2004, 24, 9087–9096
Tsim T. Y., Wong E. Y., Leung M. S., Wong C. C., Expression of axon guidance molecules and their related genes during development and sexual differentiation of the olfactory bulb in rats, Neuroscience, 2004, 123, 951–965
Nguyen-Ba-Charvet K. T., Brose K., Marillat V., Kidd T., Goodman C. S., Tessier-Lavigne M. et al., Slit 2-mediated chemorepulsion and collapse of develo** forebrain axons, Neuron, 1999, 22, 1–20
Scherberich A., Tucker R. P., Samandari E., Brown-Luedi M., Martin D., Chiquet-Ehrismann R., Murine tenascin-W, a novel mammalian tenascin expressed in kidney and at sites of bone and smooth muscle development, J. Cell. Sci., 2004, 117, 571–581
Kim D., Ackerman S. L., The UNC5C netrin receptor regulates dorsal guidance of mouse hindbrain axons, J. Neurosci., 2011, 31, 2167–2179
Cariboni A., Rakic S., Liapi A., Maggi R., Goffinet A., Parnavelas J. G., Reelin provides an inhibitory signal in the migration of gonadotropinreleasing hormone neurons, Development, 2005, 132, 4709–4718
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Blanchart, A., López-Mascaraque, L. From the periphery to the brain: Wiring the olfactory system. Translat.Neurosci. 2, 293–309 (2011). https://doi.org/10.2478/s13380-011-0038-x
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DOI: https://doi.org/10.2478/s13380-011-0038-x