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Axon growth and guidance genes identify nascent, immature, and mature olfactory sensory neurons
dc.contributor.authorMcIntyre, Jeremy C.en_US
dc.contributor.authorTitlow, William B.en_US
dc.contributor.authorMcClintock, Timothy S.en_US
dc.date.accessioned2014-05-21T18:02:49Z
dc.date.available2014-05-21T18:02:49Z
dc.date.issued2010-11-15en_US
dc.identifier.citationMcIntyre, Jeremy C.; Titlow, William B.; McClintock, Timothy S. (2010). "Axon growth and guidance genes identify nascent, immature, and mature olfactory sensory neurons." Journal of Neuroscience Research 88(15): 3243-3256. <http://hdl.handle.net/2027.42/106698>en_US
dc.identifier.issn0360-4012en_US
dc.identifier.issn1097-4547en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/106698
dc.description.abstractNeurogenesis of projection neurons requires that axons be initiated, extended, and connected. Differences in the expression of axon growth and guidance genes must drive these events, but comprehensively characterizing these differences in a single neuronal type has not been accomplished. Guided by a catalog of gene expression in olfactory sensory neurons (OSNs), in situ hybridization and immunohistochemistry revealed that Cxcr4 and Dbn1 , two axon initiation genes, marked the developmental transition from basal progenitor cells to immature OSNs in the olfactory epithelium. The CXCR4 immunoreactivity of these nascent OSNs overlapped partially with markers of proliferation of basal progenitor cells and partially with immunoreactivity for GAP43, the canonical marker of immature OSNs. Intracellular guidance cue signaling transcripts Ablim1, Crmp1, Dypsl2, Dpysl3, Dpysl5, Gap43, Marcskl1, and Stmn1–4 were specific to, or much more abundant in, the immature OSN layer. Receptors that mediate axonal inhibition or repulsion tended to be expressed in both immature and mature OSNs ( Plxna1, Plxna4, Nrp2, Efna5 ) or specifically in mature OSNs ( Plxna3, Unc5b, Efna3, Epha5, Epha7 ), although some were specific to immature OSNs ( Plxnb1, Plxnb2, Plxdc2, Nrp1 ). Cell adhesion molecules were expressed either by both immature and mature OSNs ( Dscam, Ncam1, Ncam2, Nrxn1 ) or solely by immature OSNs ( Chl1, Nfasc1, Dscaml1 ). Given the loss of intracellular signaling protein expression, the continued expression of guidance cue receptors in mature OSNs is consistent with a change in the role of these receptors, perhaps to sending signals back to the cell body and nucleus. © 2010 Wiley‐Liss, Inc.en_US
dc.publisherWiley Subscription Services, Inc., A Wiley Companyen_US
dc.subject.otherAxonogenesisen_US
dc.subject.otherCell Adhesionen_US
dc.subject.otherNeurogenesisen_US
dc.subject.otherGrowth Coneen_US
dc.subject.otherNeural Developmenten_US
dc.titleAxon growth and guidance genes identify nascent, immature, and mature olfactory sensory neuronsen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelPsychologyen_US
dc.subject.hlbsecondlevelPublic Healthen_US
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biologyen_US
dc.subject.hlbsecondlevelNeurosciencesen_US
dc.subject.hlbtoplevelSocial Sciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Pharmacology, University of Michigan, 1150 W. Medical Center Drive, Ann Arbor, MI 48109‐5632en_US
dc.contributor.affiliationotherDepartment of Physiology, University of Kentucky, Lexington, Kentuckyen_US
dc.identifier.pmid20882566en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/106698/1/22497_ftp.pdf
dc.identifier.doi10.1002/jnr.22497en_US
dc.identifier.sourceJournal of Neuroscience Researchen_US
dc.identifier.citedreferenceSkene JH, Willard M. 1981a. Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J Cell Biol 89: 96 – 103.en_US
dc.identifier.citedreferenceSchwob JE. 2002. Neural regeneration and the peripheral olfactory system. Anat Rec 269: 33 – 49.en_US
dc.identifier.citedreferenceSerizawa S, Miyamichi K, Takeuchi H, Yamagishi Y, Suzuki M, Sakano H. 2006. A neuronal identity code for the odorant receptor‐specific and activity‐dependent axon sorting. Cell 127: 1057 – 1069.en_US
dc.identifier.citedreferenceShay EL, Greer CA, Treloar HB. 2008. Dynamic expression patterns of ECM molecules in the developing mouse olfactory pathway. Dev Dyn 237: 1837 – 1850.en_US
dc.identifier.citedreferenceShelly M, Lim BK, Cancedda L, Heilshorn SC, Gao H, Poo MM. 2010. Local and long‐range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 327: 547 – 552.en_US
dc.identifier.citedreferenceShetty RS, Bose SC, Nickell MD, McIntyre JC, Hardin DH, Harris AM, McClintock TS. 2005. Transcriptional changes during neuronal death and replacement in the olfactory epithelium. Mol Cell Neurosci 30: 583 – 600.en_US
dc.identifier.citedreferenceShirao T, Kojima N, Obata K. 1992. Cloning of drebrin A and induction of neurite‐like processes in drebrin‐transfected cells. Neuroreport 3: 109 – 112.en_US
dc.identifier.citedreferenceSkene JH, Willard M. 1981b. Characteristics of growth‐associated polypeptides in regenerating toad retinal ganglion cell axons. J Neurosci 1: 419 – 426.en_US
dc.identifier.citedreferenceSmith DS, Skene JH. 1997. A transcription‐dependent switch controls competence of adult neurons for distinct modes of axon growth. J Neurosci 17: 646 – 658.en_US
dc.identifier.citedreferenceSobel A. 1991. Stathmin: a relay phosphoprotein for multiple signal transduction? Trends Biochem Sci 16: 301 – 305.en_US
dc.identifier.citedreferenceSong HJ, Ming GL, Poo MM. 1997. cAMP‐induced switching in turning direction of nerve growth cones. Nature 388: 275 – 279.en_US
dc.identifier.citedreferenceSoucy ER, Albeanu DF, Fantana AL, Murthy VN, Meister M. 2009. Precision and diversity in an odor map on the olfactory bulb. Nat Neurosci 12: 210 – 220.en_US
dc.identifier.citedreferenceStrotmann J, Conzelmann S, Beck A, Feinstein P, Breer H, Mombaerts P. 2000. Local permutations in the glomerular array of the mouse olfactory bulb. J Neurosci 20: 6927 – 6938.en_US
dc.identifier.citedreferenceTessier‐Lavigne M, Goodman CS. 1996. The molecular biology of axon guidance. Science 274: 1123 – 1133.en_US
dc.identifier.citedreferenceToba Y, Tiong JD, Ma Q, Way S. 2008. CXCR4/SDF‐1 system modulates development of GnRH neurons and the olfactory system. Dev Neurobiol 68: 487 – 503.en_US
dc.identifier.citedreferenceToda M, Shirao T, Uyemura K. 1999. Suppression of an actin‐binding protein, drebrin, by antisense transfection attenuates neurite outgrowth in neuroblastoma B104 cells. Brain Res Dev Brain Res 114: 193 – 200.en_US
dc.identifier.citedreferenceTreloar H, Tomasiewicz H, Magnuson T, Key B. 1997. The central pathway of primary olfactory axons is abnormal in mice lacking the N‐CAM‐180 isoform. J Neurobiol 32: 643 – 658.en_US
dc.identifier.citedreferenceVassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79: 981 – 991.en_US
dc.identifier.citedreferenceWalz A, Rodriguez I, Mombaerts P. 2002. Aberrant sensory innervation of the olfactory bulb in neuropilins‐2 mutant mice. J Neurosci 22: 4025 – 4035.en_US
dc.identifier.citedreferenceWalz A, Mombaerts P, Greer CA, Treloar HB. 2006. Disrupted compartmental organization of axons and dendrites with olfactory glomeruli of mice deficient in the olfactory cells adhesion molecule, OCAM. Mol Cell Neurosci 32: 1 – 14.en_US
dc.identifier.citedreferenceWhitesides JG 3rd, LaMantia AS. 1996. Differential adhesion and the initial assembly of the mammalian olfactory nerve. J Comp Neurol 373: 240 – 254.en_US
dc.identifier.citedreferenceWilliams EO, Xiao Y, Sickles HM, Shafer P, Yona G, Yang JY, Lin DM. 2007. Novel subdomains of the mouse olfactory bulb defined by molecular heterogeneity in the nascent external plexiform and glomerular layers. BMC Dev Biol 7: 48.en_US
dc.identifier.citedreferenceYoshihara Y, Kawasaki M, Tamada A, Fujita H, Hayashi H, Kagamiyama H, Mori K. 1997. OCAM: a new member of the neural cell adhesion molecule family related to zone‐to‐zone projection of olfactory and vomeronasal axons. J Neurosci 17: 5830 – 5842.en_US
dc.identifier.citedreferenceYu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA. 2004. Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42: 553 – 566.en_US
dc.identifier.citedreferenceYu TT, McIntyre JC, Bose SC, Hardin D, Owen MC, McClintock TS. 2005. Differentially expressed transcripts from phenotypically identified olfactory sensory neurons. J Comp Neurol 483: 251 – 262.en_US
dc.identifier.citedreferenceZheng C, Feinstein P, Bozza T, Rodriguez I, Mombaerts P. 2000. Peripheral olfactory projections are differentially affected in mice deficient in a cyclic nucleotide gated channel subunit. Neuron 26: 81 – 91.en_US
dc.identifier.citedreferenceZimmer C, Tiveron M‐C, Bodmer R, Cremer H. 2004. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 14: 1408 – 1419.en_US
dc.identifier.citedreferenceZou D‐J, Chesler AT, Le Pichon CE, Kuznetsov A, Pei X, Hwang El, Firestein S. 2007. Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J Neurosci 27: 6675 – 6683.en_US
dc.identifier.citedreferenceAbercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94: 239 – 247.en_US
dc.identifier.citedreferenceAkins MR, Greer CA. 2006. Axon behavior in the olfactory nerve reflects the involvement of catenin‐cadherin mediated adhesion. J Comp Neurol 499: 979 – 989.en_US
dc.identifier.citedreferenceAndrews GL, Tanglao S, Farmer WT, Morin S, Brotman S, Berberoglu MA, Price H, Fernandez GC, Mastick GS, Charron F, Kidd T. 2008. Dscam guides embryonic axons by Netrin‐dependent and ‐independent functions. Development 135: 3839 – 3848.en_US
dc.identifier.citedreferenceAstic L, Pellier‐Monnin V, Saucier D, Charrier C, Mehlen P. 2002. Expression of netrin‐1 and netrin‐1 receptor, DCC, in the rat olfactory nerve pathway during development and axonal regeneration. Neuroscience 109: 643 – 656.en_US
dc.identifier.citedreferenceAu WW, Treloar HB, Greer CA. 2002. Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446: 68 – 80.en_US
dc.identifier.citedreferenceBaldassa S, Gnesutta N, Fascio U, Sturani E, Zippel R. 2007. SCLIP, a microtubule‐destabilizing factor, interacts with RasGRF1 and inhibits its ability to promote Rac activation and neurite outgrowth. J Biol Chem 282: 2333 – 2345.en_US
dc.identifier.citedreferenceBarrientos T, Frank D, Kuwahara K, Bezprozvannaya S, Pipes GC, Bassel‐Duby R, Richardson JA, Katus HA, Olson EN, Frey N. 2007. Two novel members of the ABLIM protein family, ABLIM‐2 and ‐3, associate with STARS and directly bind F‐actin. J Biol Chem 282: 8393 – 8403.en_US
dc.identifier.citedreferenceBelluscio L, Gold GH, Nemes A, Axel R. 1998. Mice deficient in Golf are anosmic. Neuron 20: 69 – 81.en_US
dc.identifier.citedreferenceBlackmore M, Letourneau PC. 2006. Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J Neurobiol 66: 348 – 360.en_US
dc.identifier.citedreferenceBong YS, Lee HS, Carim‐Todd L, Mood K, Nishanian TG, Tessarollo L, Daar IO. 2007. ephrinB1 signals from the cell surface to the nucleus by recruitment of STAT3. Proc Natl Acad Sci U S A 104: 17305 – 17310.en_US
dc.identifier.citedreferenceCai D, Shen Y, De Bellard M, Tang S, Filbin MT. 1999. Prior exposure to neurotrophins blocks inhibition of axonal regeneration by MAG and myelin via a cAMP‐dependent mechanism. Neuron 22: 89 – 101.en_US
dc.identifier.citedreferenceCamoletto P, Colesanti A, Ozon S, Sobel A, Fasolo A. 2001. Expression of stathmin and SCG10 proteins in the olfactory neurogenesis during development and after lesion in the adulthood. Brain Res Bull 54: 19 – 28.en_US
dc.identifier.citedreferenceCao L, Dhilla A, Mukai J, Blazeski R, Lodovichi C, Mason CA, Gogos JA. 2007. Genetic modulation of BDNF signaling affects the outcome of axonal competition in vivo. Curr Biol 17: 911 – 921.en_US
dc.identifier.citedreferenceChalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA. 2003. A chemokine, SDF‐1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23: 1360 – 1371.en_US
dc.identifier.citedreferenceChalasani SH, Sabol A, Xu H, Gyda MA, Rasband K, Granato M, Chien CB, Raper JA. 2007. Stromal cell‐derived factor‐1 antagonizes slit/robo signaling in vivo. J Neurosci 27: 973 – 980.en_US
dc.identifier.citedreferenceChesler AT, Zou D‐J, Le Pichon CE, Peterlin ZA, Matthews GA, Pei X, Miller MC, Firestein S. 2007. A G protein/cAMP signal cascade is required for axonal convergence into olfactory glomeruli. Proc Natl Acad Sci U S A 104: 1039 – 1044.en_US
dc.identifier.citedreferenceCho JH, Lepine M, Andrews W, Parnavelas J, Cloutier JF. 2007. Requirement for Slit‐1 and Robo‐2 in zonal segregation of olfactory sensory neuron axons in the main olfactory bulb. J Neurosci 27: 9094 – 9204.en_US
dc.identifier.citedreferenceCloutier J‐F, Ginger RJ, Koentges G, Dulac C, Kolodkin AL, Ginty DD. 2002. Neuropilin‐2 mediates axonal fasciculation, zonal segregation but not axonal convergence, of primary accessory olfactory neurons. Neuron 33: 877 – 892.en_US
dc.identifier.citedreferenceCloutier JF, Sahay A, Chang EC, Tessier‐Lavigne M, Dulac C, Kolodkin AL, Ginty DD. 2004. Differential requirements for semaphorin 3F and Slit‐1 in axonal targeting, fasciculation, and segregation of olfactory sensory neurons. J Neurosci 24: 9087 – 9096.en_US
dc.identifier.citedreferenceCol JA, Matsuo T, Storm DR, Rodriguez I. 2007. Adenylyl cyclase‐dependent axonal targeting in the olfactory system. Development 134: 2481 – 2489.en_US
dc.identifier.citedreferenceCostanzo RM 1985. Neural regeneration and functional reconnection following olfactory nerve transection in hamster. Brain Res 361: 258 – 266.en_US
dc.identifier.citedreferenceCutforth T, Moring L, Mendelsohn M, Nemes A, Shah NM, Kim MM, Frisen J, Axel R. 2003. Axonal Ephrin‐As and odorant receptors: coordinate determination of the olfactory sensory map. Cell 114: 311 – 322.en_US
dc.identifier.citedreferenceDoucette R. 1989. Development of the nerve fiber layer in the olfactory bulb of mouse embryos. J Comp Neurol 285: 514 – 527.en_US
dc.identifier.citedreferenceDoucette R. 1990. Glial influences on axonal growth in the primary olfactory system. Glia 3: 433 – 449.en_US
dc.identifier.citedreferenceDudanova I, Tabuchi K, Rohlmann A, Sudhof TC, Missler M. 2007. Deletion of α‐neuroexins does not cause a major impairment of axonal pathfinding or synapse formation. J Comp Neurol 502: 261 – 274.en_US
dc.identifier.citedreferenceFeinstein P, Mombaerts P. 2004. A contextual model for axonal sorting into glomeruli in the mouse olfactory system. Cell 117: 817 – 831.en_US
dc.identifier.citedreferenceFeinstein P, Bozza T, Rodriquez I, Vassalli A, Mombaerts P. 2004. Axon guidance of mouse olfactory sensory neurons by odorant receptors and the β2 adrenergic receptor. Cell 117: 833 – 846.en_US
dc.identifier.citedreferenceGeraldo S, Khanzada UK, Parsons M, Chilton JK, Gordon‐Weeks PR. 2008. Targeting of the F‐actin‐binding protein drebrin by the microtubule plus‐tip protein EB3 is required for neuritogenesis. Nat Cell Biol 10: 1181 – 1189.en_US
dc.identifier.citedreferenceGitai Z, Yu TW, Lundquist EA, Tessier‐Lavigne M, Bargmann CI. 2003. The netrin receptor UNC‐40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC‐115/AbLIM. Neuron 37: 53 – 65.en_US
dc.identifier.citedreferenceGong Q, Shipley MT. 1996. Expression of extracellular matrix molecules and cell surface molecules in the olfactory nerve pathway during early development. J Comp Neurol 366: 1 – 14.en_US
dc.identifier.citedreferenceGrenningloh G, Soehrman S, Bondallaz P, Ruchti E, Cadas H. 2004. Role of the microtubule destabilizing proteins SCG10 and stathmin in neuronal growth. J Neurobiol 58: 60 – 69.en_US
dc.identifier.citedreferenceHasegawa S, Hamada S, Kumode Y, Esumi S, Katori S, Fukuda E, Uchiyama Y, Hirabayashi T, Mombaerts P, Yagi T. 2008. The protocadherin‐alpha family is involved in axonal coalescence of olfactory sensory neurons into glomeruli of the olfactory bulb in mouse. Mol Cell Neurosci 38: 66 – 79.en_US
dc.identifier.citedreferenceHolm S. 1979. A simple sequentially rejective multiple test procedure. Scand J Statist 6: 65 – 70.en_US
dc.identifier.citedreferenceImai T, Sakano H. 2008. Odorant receptor‐mediated signaling in the mouse. Curr Opin Neurobiol 18: 251 – 260.en_US
dc.identifier.citedreferenceImai T, Suzuki M, Sakano H. 2006. Odorant receptor‐derived cAMP signals direct axonal targeting. Science 314: 657 – 661.en_US
dc.identifier.citedreferenceIshikawa R, Hayashi K, Shirao T, Xue Y, Takagi T, Sasaki Y, Kohama K. 1994. Drebrin, a development‐associated brain protein from rat embryo, causes the dissociation of tropomyosin from actin filaments. J Biol Chem 269: 29928 – 29933.en_US
dc.identifier.citedreferenceKaneko‐Goto T, Yoshihara S, Miyazaki H, Yoshihara Y. 2008. BIG‐2 mediates olfactory axon convergence to target glomeruli. Neuron 57: 834 – 846.en_US
dc.identifier.citedreferenceKee N, Sivalingam S, Boonstra R, Wojtowicz JM. 2002. The utility of Ki‐67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115: 97 – 105.en_US
dc.identifier.citedreferenceKim H, Greer CA. 2000. The emergence of compartmental organization in olfactory bulb glomeruli during postnatal development. J Comp Neurol 422: 297 – 311.en_US
dc.identifier.citedreferenceKlenoff JR, Greer CA. 1998. Postnatal development of olfactory receptor cell axonal arbors. J Comp Neurol 390: 256 – 267.en_US
dc.identifier.citedreferenceKobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, Mori K, Sakano H. 2007. Innate versus learned odour processing in the mouse olfactory bulb. Nature 450: 503 – 508.en_US
dc.identifier.citedreferenceLi D, Field PM, Raisman G. 1995. Failure of axon regeneration in postnatal rat entorhinohippocampal slice coculture is due to maturation of the axon, not that of the pathway or target. Eur J Neurosci 7: 1164 – 1171.en_US
dc.identifier.citedreferenceLieberam I, Agalliu D, Nagasawa T, Ericson J, Jessell TM. 2005. A Cxcl12‐CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47: 667 – 679.en_US
dc.identifier.citedreferenceLin D, Wang F, Lowe G, Gold GH, Axel R, Ngai J, Brunet L. 2000. Formation of precise connections in the olfactory bulb occurs in absence of odorant‐evoked neuronal activity. Neuron 26: 69 – 80.en_US
dc.identifier.citedreferenceLundquist EA, Herman RK, Shaw JE, Bargmann CI. 1998. UNC‐115, a conserved protein with predicted LIM and actin‐binding domains, mediates axon guidance in C. elegans. Neuron 21: 385 – 392.en_US
dc.identifier.citedreferenceLy A, Nikolaev A, Suresh G, Zheng Y, Tessier‐Lavigne M, Stein E. 2008. DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin‐1. Cell 133: 1241 – 1254.en_US
dc.identifier.citedreferenceMombaerts P. 2006. Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22: 713 – 737.en_US
dc.identifier.citedreferenceMombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87: 675 – 686.en_US
dc.identifier.citedreferenceMontag‐Sallaz M, Schachner M, Montag D. 2002. Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Mol Cell Biol 22: 7967 – 7981.en_US
dc.identifier.citedreferenceMonti Graziadei GA. 1983. Experimental studies on the olfactory marker protein. III. The olfactory marker protein in the olfactory neuroepithelium lacking connections with the forebrain. Brain Res 262: 303 – 308.en_US
dc.identifier.citedreferenceMonti Graziadei GA, Graziadei PP. 1979. Neurogenesis and neuron regeneration in the olfactory system of mammals. II. Degeneration and reconstitution of the olfactory sensory neurons after axotomy. J Neurocytol 8: 197 – 213.en_US
dc.identifier.citedreferenceMorii H, Shiraishi‐Yamaguchi Y, Mori N. 2006. SCG10, a microtubule destabilizing factor, stimulates the neurite outgrowth by modulating microtubule dynamics in rat hippocampal primary cultured neurons. J Neurobiol 66: 1101 – 1114.en_US
dc.identifier.citedreferenceMiyasaka N, Knaut H, Yoshihara Y. 2007. Cxcl12/Cxcr4 chemokine signaling is required for placode assembly and sensory axon pathfinding in the zebrafish olfactory system. Development 134: 2459 – 2468.en_US
dc.identifier.citedreferenceNishiumi F, Komiya T, Ikenishi K. 2005. The mode and molecular mechanisms of the migration of presumptive PGC in the endoderm cell mass of Xenopus embryos. Dev Growth Differ 47: 37 – 48.en_US
dc.identifier.citedreferenceNorlin EM, Alenius M, Gussing F, Hägglund M, Vedin V, Bohm S. 2001. Evidence for gradients of gene expression correlating with zonal topography of the olfactory sensory map. Mol Cell Neurosci 18: 283 – 295.en_US
dc.identifier.citedreferenceOzon S, Maucuer A, Sobel A. 1997. The stathmin family—molecular and biological characterization of novel mammalian proteins expressed in the nervous system. Eur J Biochem 248: 794 – 806.en_US
dc.identifier.citedreferenceOzon S, Mestikawy SE, Sobel A. 1999. Differential, regional, and cellular expression of the stathmin family transcripts in the adult rat brain. J Neurosci Res 56: 553 – 564.en_US
dc.identifier.citedreferencePellier‐Monnin V, Astic L, Bichet S, Riederer BM, Grenningloh G. 2001. Expression of SCG10 and stathmin proteins in the rat olfactory system during development and axonal regeneration. J Comp Neurol 433: 239 – 254.en_US
dc.identifier.citedreferencePinching AJ, Powell TPS. 1971. The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9: 347 – 377.en_US
dc.identifier.citedreferencePoulain FE, Sobel A. 2007. The “SCG10‐Like Protein” SCLIP is a novel regulator of axonal branching in hippocampal neurons, unlike SCG10. Mol Cell Neurosci 34: 137 – 146.en_US
dc.identifier.citedreferenceRessler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79: 1245 – 1255.en_US
dc.identifier.citedreferenceRhee J, Buchan T, Zukerberg L, Lillien J, Balsamo J. 2007. Cables links Robo‐bound Abl kinase to N‐cadherin‐bound beta‐catenin to mediate Slit‐induced modulation of adhesion and transcription. Nat Cell Biol 9: 883 – 892.en_US
dc.identifier.citedreferenceRoof DJ, Hayes A, Adamian M, Chishti AH, Li T. 1997. Molecular characterization of abLIM, a novel actin‐binding and double zinc finger protein. J Cell Biol 138: 575 – 588.en_US
dc.identifier.citedreferenceRoyet JP, Souchier C, Jourdan F, Ploye H. 1988. Mophometric study of the glomerular population in the mouse olfactory bulb: numerical density and size distribution along the rostrocaudal axis. J Comp Neurol 270: 559 – 568.en_US
dc.identifier.citedreferenceSammeta N, Yu TT, Bose SC, McClintock TS. 2007. Mouse olfactory sensory neurons express 10,000 genes. J Comp Neurol 502: 1138 – 1156.en_US
dc.identifier.citedreferenceSchaefer ML, Finger TE, Restrepo D. 2001. Variability of position of the P2 glomerulus within a map of the mouse olfactory bulb. J Comp Neurol 436: 351 – 362.en_US
dc.identifier.citedreferenceSchwarting GA, Kostek C, Ahmad N, Dibble C, Pays L, Puschel AW. 2000. Semaphorin 3A is required for guidance of olfactory axons in mice. J Neurosci 20: 7691 – 7697.en_US
dc.identifier.citedreferenceSchwarting GA, Raitcheva D, Crandall JE, Burkardt C, Puschel AW. 2004. Semaphorin 3A mediated axon guidance regulates convergence and targeting of P2 odorant receptor axons. Eur J Neurosci 19: 1800 – 1810.en_US
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