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Neural Crest and Olfactory System: New Prospective

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Abstract

Sensory neurons in vertebrates are derived from two embryonic transient cell sources: neural crest (NC) and ectodermal placodes. The placodes are thickenings of ectodermal tissue that are responsible for the formation of cranial ganglia as well as complex sensory organs that include the lens, inner ear, and olfactory epithelium. The NC cells have been indicated to arise at the edges of the neural plate/dorsal neural tube, from both the neural plate and the epidermis in response to reciprocal interactions Moury and Jacobson (Dev Biol 141:243–253, 1990). NC cells migrate throughout the organism and give rise to a multitude of cell types that include melanocytes, cartilage and connective tissue of the head, components of the cranial nerves, the dorsal root ganglia, and Schwann cells. The embryonic definition of these two transient populations and their relative contribution to the formation of sensory organs has been investigated and debated for several decades (Basch and Bronner-Fraser, Adv Exp Med Biol 589:24–31, 2006; Basch et al., Nature 441:218–222, 2006) review (Baker and Bronner-Fraser, Dev Biol 232:1–61, 2001). Historically, all placodes have been described as exclusively derived from non-neural ectodermal progenitors. Recent genetic fate-mapping studies suggested a NC contribution to the olfactory placodes (OP) as well as the otic (auditory) placodes in rodents (Murdoch and Roskams, J Neurosci Off J Soc Neurosci 28:4271–4282, 2008; Murdoch et al., J Neurosci 30:9523–9532, 2010; Forni et al., J Neurosci Off J Soc Neurosci 31:6915–6927, 2011b; Freyer et al., Development 138:5403–5414, 2011; Katoh et al., Mol Brain 4:34, 2011). This review analyzes and discusses some recent developmental studies on the OP, placodal derivatives, and olfactory system.

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References

  1. Bhattacharyya S, Bailey AP, Bronner-Fraser M, Streit A (2004) Segregation of lens and olfactory precursors from a common territory: cell sorting and reciprocity of Dlx5 and Pax6 expression. Dev Biol 271:403–414

    Article  PubMed  CAS  Google Scholar 

  2. Kozlowski DJ, Murakami T, Ho RK, Weinberg ES (1997) Regional cell movement and tissue patterning in the zebrafish embryo revealed by fate mapping with caged fluorescein. Biochem Cell Biol 75:551–562

    Article  PubMed  CAS  Google Scholar 

  3. Verwoerd CD, van Oostrom CG (1979) Cephalic neural crest and placodes. Adv Anat Embryol Cell Biol 58:1–75

    Article  PubMed  CAS  Google Scholar 

  4. Couly GF, Le Douarin NM (1985) Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110:422–439

    Article  PubMed  CAS  Google Scholar 

  5. Schlosser G (2008) Do vertebrate neural crest and cranial placodes have a common evolutionary origin? Bioessays 30:659–672

    Article  PubMed  CAS  Google Scholar 

  6. Streit A (2002) Extensive cell movements accompany formation of the otic placode. Dev Biol 249:237–254

    Article  PubMed  CAS  Google Scholar 

  7. Whitlock KE, Westerfield M (2000) The olfactory placodes of the zebrafish form by convergence of cellular fields at the edge of the neural plate. Development 127:3645–3653

    PubMed  CAS  Google Scholar 

  8. Forni PE, Taylor-Burds C, Melvin VS, Williams T, Wray S (2011) Neural crest and ectodermal cells intermix in the nasal placode to give rise to GnRH-1 neurons, sensory neurons, and olfactory ensheathing cells. J Neurosci Off J Soc Neurosci 31:6915–6927

    Article  CAS  Google Scholar 

  9. Freyer L, Aggarwal V, Morrow BE (2011) Dual embryonic origin of the mammalian otic vesicle forming the inner ear. Development 138:5403–5414

    Article  PubMed  CAS  Google Scholar 

  10. Katoh H, Shibata S, Fukuda K, Sato M, Satoh E, Nagoshi N, Minematsu T, Matsuzaki Y, Akazawa C, Toyama Y, Nakamura M, Okano H (2011) The dual origin of the peripheral olfactory system: placode and neural crest. Mol Brain 4:34

    Article  PubMed  CAS  Google Scholar 

  11. Murdoch B, DelConte C, Garcia-Castro MI (2010) Embryonic Pax7-expressing progenitors contribute multiple cell types to the postnatal olfactory epithelium. J Neurosci 30:9523–9532

    PubMed  CAS  Google Scholar 

  12. Barraud P, Seferiadis AA, Tyson LD, Zwart MF, Szabo-Rogers HL, Ruhrberg C, Liu KJ, Baker CV (2010) Neural crest origin of olfactory ensheathing glia. Proc Natl Acad Sci U S A 107:21040–21045

    Article  PubMed  CAS  Google Scholar 

  13. Sabado V, Barraud P, Baker CV, Streit A (2011) Specification of GnRH-1 neurons by antagonistic FGF and retinoic acid signaling. Dev Biol 362:254–262

    Article  PubMed  CAS  Google Scholar 

  14. Cuschieri A, Bannister LH (1975) The development of the olfactory mucosa in the mouse: light microscopy. J Anat 119:277–286

    PubMed  CAS  Google Scholar 

  15. Graham A, Blentic A, Duque S, Begbie J (2007) Delamination of cells from neurogenic placodes does not involve an epithelial-to-mesenchymal transition. Development 134:4141–4145

    Article  PubMed  CAS  Google Scholar 

  16. Bedford EA (1904) The early history of the olfactory nerve in swine. J Comp Neurol 14:390–410

    Article  Google Scholar 

  17. Schwanzel-Fukuda M, Pfaff DW (1989) Origin of luteinizing hormone-releasing hormone neurons. Nature 338:161–164

    Article  PubMed  CAS  Google Scholar 

  18. Wray S, Key S, Qualls R, Fueshko SM (1994) A subset of peripherin positive olfactory axons delineates the luteinizing hormone releasing hormone neuronal migratory pathway in developing mouse. Dev Biol 166:349–354

    Article  PubMed  CAS  Google Scholar 

  19. Doucette R (1990) Glial influences on axonal growth in the primary olfactory system. Glia 3:433–449

    Article  PubMed  CAS  Google Scholar 

  20. Fornaro M, Geuna S (2001) Confocal imaging of HuC/D RNA-binding proteins in adult rat primary sensory neurons. Ann Anat 183:471–473

    Article  PubMed  CAS  Google Scholar 

  21. Fornaro M, Geuna S, Fasolo A, Giacobini-Robecchi MG (2003) HuC/D confocal imaging points to olfactory migratory cells as the first cell population that expresses a post-mitotic neuronal phenotype in the chick embryo. Neuroscience 122:123–128

    Article  PubMed  CAS  Google Scholar 

  22. Miller AM, Treloar HB, Greer CA (2010) Composition of the migratory mass during development of the olfactory nerve. J Comp Neurol 518:4825–4841

    Article  PubMed  Google Scholar 

  23. Schwarting GA, Gridley T, Henion TR (2007) Notch1 expression and ligand interactions in progenitor cells of the mouse olfactory epithelium. J Mol Histol 38:543–553

    Article  PubMed  CAS  Google Scholar 

  24. Tarozzo G, Peretto P, Fasolo A (1995) Cell migration from the olfactory placode and the ontogeny of the neuroendocrine compartments. Zoolog Sci 12:367–383

    Article  PubMed  CAS  Google Scholar 

  25. Valverde F, Heredia M, Santacana M (1993) Characterization of neuronal cell varieties migrating from the olfactory epithelium during prenatal development in the rat. Immunocytochemical study using antibodies against olfactory marker protein (OMP) and luteinizing hormone-releasing hormone (LH-RH). Brain Res Dev Brain Res 71:209–220

    Article  PubMed  CAS  Google Scholar 

  26. Whitlock KE, Westerfield M (1998) A transient population of neurons pioneers the olfactory pathway in the zebrafish. J Neurosci 18:8919–8927

    PubMed  CAS  Google Scholar 

  27. Wray S, Grant P, Gainer H (1989) Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc Natl Acad Sci U S A 86:8132–8136

    Article  PubMed  CAS  Google Scholar 

  28. Farbman AI, Squinto LM (1985) Early development of olfactory receptor cell axons. Brain Res 351:205–213

    PubMed  CAS  Google Scholar 

  29. Conzelmann S, Levai O, Breer H, Strotmann J (2002) Extraepithelial cells expressing distinct olfactory receptors are associated with axons of sensory cells with the same receptor type. Cell Tissue Res 307:293–301

    Article  PubMed  CAS  Google Scholar 

  30. Schwarzenbacher K, Fleischer J, Breer H, Conzelmann S (2004) Expression of olfactory receptors in the cribriform mesenchyme during prenatal development. Gene Expr Patterns 4:543–552

    Article  PubMed  CAS  Google Scholar 

  31. Hilal EM, Chen JH, Silverman AJ (1996) Joint migration of gonadotropin-releasing hormone (GnRH) and neuropeptide Y (NPY) neurons from olfactory placode to central nervous system. J Neurobiol 31:487–502

    Article  PubMed  CAS  Google Scholar 

  32. Wray S (2010) From nose to brain: development of gonadotrophin-releasing hormone-1 neurones. J Neuroendocrinol 22:743–753

    Article  PubMed  CAS  Google Scholar 

  33. Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N (2005) Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19:1028–1033

    Article  PubMed  CAS  Google Scholar 

  34. Murdoch B, Roskams AJ (2007) Olfactory epithelium progenitors: insights from transgenic mice and in vitro biology. J Mol Histol 38:581–599

    Article  PubMed  CAS  Google Scholar 

  35. Hegedus B, Dasgupta B, Shin JE, Emnett RJ, Hart-Mahon EK, Elghazi L, Bernal-Mizrachi E, Gutmann DH (2007) Neurofibromatosis-1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Ras-dependent mechanisms. Cell Stem Cell 1:443–457

    Article  PubMed  CAS  Google Scholar 

  36. Graziadei PP, Monti-Graziadei AG (1992) The influence of the olfactory placode on the development of the telencephalon in Xenopus laevis. Neuroscience 46:617–629

    Article  PubMed  CAS  Google Scholar 

  37. Ramon-Cueto A, Avila J (1998) Olfactory ensheathing glia: properties and function. Brain Res Bull 46:175–187

    Article  PubMed  CAS  Google Scholar 

  38. Stout RP, Graziadei PP (1980) Influence of the olfactory placode on the development of the brain in Xenopus laevis (Daudin). I. Axonal growth and connections of the transplanted olfactory placode. Neuroscience 5:2175–2186

    Article  PubMed  CAS  Google Scholar 

  39. Watanabe Y, Inoue K, Okuyama-Yamamoto A, Nakai N, Nakatani J, Nibu K, Sato N, Iiboshi Y, Yusa K, Kondoh G, Takeda J, Terashima T, Takumi T (2009) Fezf1 is required for penetration of the basal lamina by olfactory axons to promote olfactory development. J Comp Neurol 515:565–584

    Article  PubMed  CAS  Google Scholar 

  40. Smart IH (1971) Location and orientation of mitotic figures in the developing mouse olfactory epithelium. J Anat 109:243–251

    PubMed  CAS  Google Scholar 

  41. Cuschieri A, Bannister LH (1975) The development of the olfactory mucosa in the mouse: electron microscopy. J Anat 119:471–498

    PubMed  CAS  Google Scholar 

  42. Forni PE, Fornaro M, Guenette S, Wray S (2011) A role for FE65 in controlling GnRH-1 neurogenesis. J Neurosci 31:480–491

    Article  PubMed  CAS  Google Scholar 

  43. Tucker ES, Lehtinen MK, Maynard T, Zirlinger M, Dulac C, Rawson N, Pevny L, Lamantia AS (2010) Proliferative and transcriptional identity of distinct classes of neural precursors in the mammalian olfactory epithelium. Development 137:2471–2481

    Article  PubMed  CAS  Google Scholar 

  44. Maier E, Gunhaga L (2009) Dynamic expression of neurogenic markers in the developing chick olfactory epithelium. Dev Dyn 238:1617–1625

    Article  PubMed  CAS  Google Scholar 

  45. Berghard A, Hagglund AC, Bohm S, Carlsson L (2012) Lhx2-dependent specification of olfactory sensory neurons is required for successful integration of olfactory, vomeronasal, and GnRH neurons. Faseb J. doi:10.1096/fj.12-206193

  46. Wray S, Nieburgs A, Elkabes S (1989) Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode. Brain Res Dev Brain Res 46:309–318

    Article  PubMed  CAS  Google Scholar 

  47. Wray S (2002) Development of gonadotropin-releasing hormone-1 neurons. Front Neuroendocrinol 23:292–316

    Article  PubMed  CAS  Google Scholar 

  48. el Amraoui A, Dubois PM (1993) Experimental evidence for an early commitment of gonadotropin-releasing hormone neurons, with special regard to their origin from the ectoderm of nasal cavity presumptive territory. Neuroendocrinology 57:991–1002

    Article  PubMed  Google Scholar 

  49. Metz H, Wray S (2010) Use of mutant mouse lines to investigate origin of gonadotropin-releasing hormone-1 neurons: lineage independent of the adenohypophysis. Endocrinology 151:766–773

    Article  PubMed  CAS  Google Scholar 

  50. Whitlock KE, Wolf CD, Boyce ML (2003) Gonadotropin-releasing hormone (GnRH) cells arise from cranial neural crest and adenohypophyseal regions of the neural plate in the zebrafish, Danio rerio. Dev Biol 257:140–152

    Article  PubMed  CAS  Google Scholar 

  51. Kramer PR, Guerrero G, Krishnamurthy R, Mitchell PJ, Wray S (2000) Ectopic expression of luteinizing hormone-releasing hormone and peripherin in the respiratory epithelium of mice lacking transcription factor AP-2alpha. Mech Dev 94:79–94

    Article  PubMed  CAS  Google Scholar 

  52. Boehm U, Zou Z, Buck LB (2005) Feedback loops link odor and pheromone signaling with reproduction. Cell 123:683–695

    Article  PubMed  CAS  Google Scholar 

  53. Jasoni CL, Porteous RW, Herbison AE (2009) Anatomical location of mature GnRH neurons corresponds with their birthdate in the developing mouse. Dev Dyn 238:524–531

    Article  PubMed  Google Scholar 

  54. Onuma TA, Ding Y, Abraham E, Zohar Y, Ando H, Duan C (2011) Regulation of temporal and spatial organization of newborn GnRH neurons by IGF signaling in zebrafish. J Neurosci Off J Soc Neurosci 31:11814–11824

    Article  CAS  Google Scholar 

  55. Kallmann FJBS (1944) The genetic aspects of primary eunuchoidism. J Ment Defic 48:203–236

    Google Scholar 

  56. Chan YM, Broder-Fingert S, Seminara SB (2009) Reproductive functions of kisspeptin and Gpr54 across the life cycle of mice and men. Peptides 30:42–48

    Article  PubMed  CAS  Google Scholar 

  57. Trarbach EB, Teles MG, Costa EM, Abreu AP, Garmes HM, Guerra G Jr, Baptista MT, de Castro M, Mendonca BB, Latronico AC (2010) Screening of autosomal gene deletions in patients with hypogonadotropic hypogonadism using multiplex ligation-dependent probe amplification: detection of a hemizygosis for the fibroblast growth factor receptor 1. Clin Endocrinol (Oxf) 72:371–376

    Article  CAS  Google Scholar 

  58. Albuisson J, Pecheux C, Carel JC, Lacombe D, Leheup B, Lapuzina P, Bouchard P, Legius E, Matthijs G, Wasniewska M, Delpech M, Young J, Hardelin JP, Dode C (2005) Kallmann syndrome: 14 novel mutations in KAL1 and FGFR1 (KAL2). Hum Mutat 25:98–99

    Article  PubMed  CAS  Google Scholar 

  59. Bailleul-Forestier I, Gros C, Zenaty D, Bennaceur S, Leger J, de Roux N (2010) Dental agenesis in Kallmann syndrome individuals with FGFR1 mutations. Int J Paediatr Dent 20:305–312

    Article  PubMed  Google Scholar 

  60. Jaffe MJ, Currie J, Schwankhaus JD, Sherins RJ (1987) Ophthalmic midline dysgenesis in Kallmann syndrome. Ophthalmic Paediatr Genet 8:171–174

    Article  PubMed  CAS  Google Scholar 

  61. Ribeiro RS, Vieira TC, Abucham J (2007) Reversible Kallmann syndrome: report of the first case with a KAL1 mutation and literature review. Eur J Endocrinol 156:285–290

    Article  PubMed  CAS  Google Scholar 

  62. Ueno H, Yamaguchi H, Katakami H, Matsukura S (2004) A case of Kallmann syndrome associated with Dandy–Walker malformation. Exp Clin Endocrinol Diabetes 112:62–67

    Article  PubMed  CAS  Google Scholar 

  63. Villanueva C, de Roux N (2010) FGFR1 mutations in Kallmann syndrome. Front Horm Res 39:51–61

    Article  PubMed  CAS  Google Scholar 

  64. Zenaty D, Bretones P, Lambe C, Guemas I, David M, Leger J, de Roux N (2006) Paediatric phenotype of Kallmann syndrome due to mutations of fibroblast growth factor receptor 1 (FGFR1). Mol Cell Endocrinol 254–255:78–83

    Article  PubMed  CAS  Google Scholar 

  65. Zhang Y, McMahon R, Charles SJ, Green JS, Moore AT, Barton DE, Yates JR (1993) Genetic mapping of the Kallmann syndrome and X linked ocular albinism gene loci. J Med Genet 30:923–925

    Article  PubMed  CAS  Google Scholar 

  66. Bergman JE, Janssen N, Hoefsloot LH, Jongmans MC, Hofstra RM, van Ravenswaaij-Arts CM (2011) CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J Med Genet 48:334–342

    Article  PubMed  CAS  Google Scholar 

  67. Jongmans MC, van Ravenswaaij-Arts CM, Pitteloud N, Ogata T, Sato N, Claahsen-van der Grinten HL, van der Donk K, Seminara S, Bergman JE, Brunner HG, Crowley WF Jr, Hoefsloot LH (2009) CHD7 mutations in patients initially diagnosed with Kallmann syndrome—the clinical overlap with CHARGE syndrome. Clin Genet 75:65–71

    Article  PubMed  CAS  Google Scholar 

  68. Trarbach EB, Baptista MT, Garmes HM, Hackel C (2005) Molecular analysis of KAL-1, GnRH-R, NELF and EBF2 genes in a series of Kallmann syndrome and normosmic hypogonadotropic hypogonadism patients. J Endocrinol 187:361–368

    Article  PubMed  CAS  Google Scholar 

  69. Bianco SD, Kaiser UB (2009) The genetic and molecular basis of idiopathic hypogonadotropic hypogonadism. Nat Rev Endocrinol 5:569–576

    Article  PubMed  CAS  Google Scholar 

  70. Abzhanov A, Tabin CJ (2004) Shh and Fgf8 act synergistically to drive cartilage outgrowth during cranial development. Dev Biol 273:134–148

    Article  PubMed  CAS  Google Scholar 

  71. Bajpai R, Chen DA, Rada-Iglesias A, Zhang J, Xiong Y, Helms J, Chang CP, Zhao Y, Swigut T, Wysocka J (2010) CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463:958–962

    Article  PubMed  CAS  Google Scholar 

  72. Creuzet S, Schuler B, Couly G, Le Douarin NM (2004) Reciprocal relationships between Fgf8 and neural crest cells in facial and forebrain development. Proc Natl Acad Sci U S A 101:4843–4847

    Article  PubMed  CAS  Google Scholar 

  73. Falardeau J et al (2008) Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest 118:2822–2831

    Article  PubMed  CAS  Google Scholar 

  74. Kawauchi S, Shou J, Santos R, Hebert JM, McConnell SK, Mason I, Calof AL (2005) Fgf8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development 132:5211–5223

    Article  PubMed  CAS  Google Scholar 

  75. Trarbach EB, Abreu AP, Silveira LF, Garmes HM, Baptista MT, Teles MG, Costa EM, Mohammadi M, Pitteloud N, Mendonca BB, Latronico AC (2010) Nonsense mutations in FGF8 gene causing different degrees of human gonadotropin-releasing deficiency. J Clin Endocrinol Metab 95:3491–3496

    Article  PubMed  CAS  Google Scholar 

  76. Balmer CW, LaMantia AS (2005) Noses and neurons: induction, morphogenesis, and neuronal differentiation in the peripheral olfactory pathway. Dev Dyn 234:464–481

    Article  PubMed  CAS  Google Scholar 

  77. LaMantia AS, Bhasin N, Rhodes K, Heemskerk J (2000) Mesenchymal/epithelial induction mediates olfactory pathway formation. Neuron 28:411–425

    Article  PubMed  CAS  Google Scholar 

  78. Graziadei PP, Monti Graziadei GA (1985) Neurogenesis and plasticity of the olfactory sensory neurons. Ann N Y Acad Sci 457:127–142

    Article  PubMed  CAS  Google Scholar 

  79. Kawauchi S, Beites CL, Crocker CE, Wu HH, Bonnin A, Murray R, Calof AL (2004) Molecular signals regulating proliferation of stem and progenitor cells in mouse olfactory epithelium. Dev Neurosci 26:166–180

    Article  PubMed  CAS  Google Scholar 

  80. Carr VM, Farbman AI (1992) Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol 115:55–59

    Article  PubMed  CAS  Google Scholar 

  81. Hinds JW, Hinds PL, McNelly NA (1984) An autoradiographic study of the mouse olfactory epithelium: evidence for long-lived receptors. Anat Rec 210:375–383

    Article  PubMed  CAS  Google Scholar 

  82. Huard JM, Schwob JE (1995) Cell cycle of globose basal cells in rat olfactory epithelium. Dev Dyn 203:17–26

    Article  PubMed  CAS  Google Scholar 

  83. Newman MP, Feron F, Mackay-Sim A (2000) Growth factor regulation of neurogenesis in adult olfactory epithelium. Neuroscience 99:343–350

    Article  PubMed  CAS  Google Scholar 

  84. Carter LA, MacDonald JL, Roskams AJ (2004) Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J Neurosci 24:5670–5683

    Article  PubMed  CAS  Google Scholar 

  85. Guo Z, Packard A, Krolewski RC, Harris MT, Manglapus GL, Schwob JE (2010) Expression of Pax6 and Sox2 in adult olfactory epithelium. J Comp Neurol 518:4395–4418

    Article  PubMed  Google Scholar 

  86. Farbman AI, Buchholz JA (1996) Transforming growth factor-alpha and other growth factors stimulate cell division in olfactory epithelium in vitro. J Neurobiol 30:267–280

    Article  PubMed  CAS  Google Scholar 

  87. Feron F, Bianco J, Ferguson I, Mackay-Sim A (2008) Neurotrophin expression in the adult olfactory epithelium. Brain Res 1196:13–21

    Article  PubMed  CAS  Google Scholar 

  88. Leung CT, Coulombe PA, Reed RR (2007) Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci 10:720–726

    Article  PubMed  CAS  Google Scholar 

  89. Beites CL, Kawauchi S, Crocker CE, Calof AL (2005) Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp Cell Res 306:309–316

    Article  PubMed  CAS  Google Scholar 

  90. Cau E, Gradwohl G, Casarosa S, Kageyama R, Guillemot F (2000) Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development 127:2323–2332

    PubMed  CAS  Google Scholar 

  91. Guillemot F, Lo LC, Johnson JE, Auerbach A, Anderson DJ, Joyner AL (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75:463–476

    Article  PubMed  CAS  Google Scholar 

  92. Delorme B, Nivet E, Gaillard J, Haupl T, Ringe J, Deveze A, Magnan J, Sohier J, Khrestchatisky M, Roman FS, Charbord P, Sensebe L, Layrolle P, Feron F (2010) The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev 19:853–866

    Article  PubMed  CAS  Google Scholar 

  93. Doyle KL, Kazda A, Hort Y, McKay SM, Oleskevich S (2007) Differentiation of adult mouse olfactory precursor cells into hair cells in vitro. Stem Cells 25:621–627

    Article  PubMed  CAS  Google Scholar 

  94. Murrell W, Feron F, Wetzig A, Cameron N, Splatt K, Bellette B, Bianco J, Perry C, Lee G, Mackay-Sim A (2005) Multipotent stem cells from adult olfactory mucosa. Dev Dyn 233:496–515

    Article  PubMed  Google Scholar 

  95. Nivet E, Vignes M, Girard SD, Pierrisnard C, Baril N, Deveze A, Magnan J, Lante F, Khrestchatisky M, Feron F, Roman FS (2011) Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. J Clin Invest 121:2808–2820

    Article  PubMed  CAS  Google Scholar 

  96. Tome M, Lindsay SL, Riddell JS, Barnett SC (2009) Identification of nonepithelial multipotent cells in the embryonic olfactory mucosa. Stem Cells 27:2196–2208

    Article  PubMed  CAS  Google Scholar 

  97. Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabe-Heider F, Biernaskie J, Junek A, Kobayashi NR, Toma JG, Kaplan DR, Labosky PA, Rafuse V, Hui CC, Miller FD (2004) A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6:1082–1093

    Article  PubMed  CAS  Google Scholar 

  98. Blentic A, Tandon P, Payton S, Walshe J, Carney T, Kelsh RN, Mason I, Graham A (2008) The emergence of ectomesenchyme. Dev Dyn 237:592–601

    Article  PubMed  Google Scholar 

  99. Breau MA, Pietri T, Stemmler MP, Thiery JP, Weston JA (2008) A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc Natl Acad Sci U S A 105:7750–7755

    Article  PubMed  CAS  Google Scholar 

  100. Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429

    PubMed  CAS  Google Scholar 

  101. Fernandes KJ, Toma JG, Miller FD (2008) Multipotent skin-derived precursors: adult neural crest-related precursors with therapeutic potential. Philos Trans R Soc B Biol Sci 363:185–198

    Article  CAS  Google Scholar 

  102. Girard SD, Deveze A, Nivet E, Gepner B, Roman FS, Feron F (2011) Isolating nasal olfactory stem cells from rodents or humans. J Vis Exp 54:2762

    Google Scholar 

  103. Franklin RJ, Gilson JM, Franceschini IA, Barnett SC (1996) Schwann cell-like myelination following transplantation of an olfactory bulb-ensheathing cell line into areas of demyelination in the adult CNS. Glia 17:217–224

    Article  PubMed  CAS  Google Scholar 

  104. Ramon-Cueto A (2000) Olfactory ensheathing glia transplantation into the injured spinal cord. Prog Brain Res 128:265–272

    Article  PubMed  CAS  Google Scholar 

  105. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, Wegner M (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15:66–78

    Article  PubMed  CAS  Google Scholar 

  106. Astic L, Pellier-Monnin V, Godinot F (1998) Spatio-temporal patterns of ensheathing cell differentiation in the rat olfactory system during development. Neuroscience 84:295–307

    Article  PubMed  CAS  Google Scholar 

  107. Chehrehasa F, Ekberg JA, Lineburg K, Amaya D, Mackay-Sim A, St John JA (2012) Two phases of replacement replenish the olfactory ensheathing cell population after injury in postnatal mice. Glia 60:322–332

    Article  PubMed  Google Scholar 

  108. Honore A, Le Corre S, Derambure C, Normand R, Duclos C, Boyer O, Marie JP, Guerout N (2012) Isolation, characterization, and genetic profiling of subpopulations of olfactory ensheathing cells from the olfactory bulb. Glia 60:404–413

    Article  PubMed  Google Scholar 

  109. Kueh JL, Raisman G, Li Y, Stevens R, Li D (2011) Comparison of bulbar and mucosal olfactory ensheathing cells using FACS and simultaneous antigenic bivariate cell cycle analysis. Glia 59:1658–1671

    Article  PubMed  Google Scholar 

  110. Paviot A, Guerout N, Bon-Mardion N, Duclos C, Jean L, Boyer O, Marie JP (2011) Efficiency of laryngeal motor nerve repair is greater with bulbar than with mucosal olfactory ensheathing cells. Neurobiol Dis 41:688–694

    Article  PubMed  Google Scholar 

  111. Richter MW, Fletcher PA, Liu J, Tetzlaff W, Roskams AJ (2005) Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J Neurosci 25:10700–10711

    Article  PubMed  CAS  Google Scholar 

  112. Barnett SC (2004) Olfactory ensheathing cells: unique glial cell types? J Neurotrauma 21:375–382

    Article  PubMed  Google Scholar 

  113. Lakatos A, Franklin RJ, Barnett SC (2000) Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 32:214–225

    Article  PubMed  CAS  Google Scholar 

  114. Li BC, Xu C, Zhang JY, Li Y, Duan ZX (2012) Differing Schwann cells and olfactory ensheathing cells behaviors, from interacting with astrocyte, produce similar improvements in contused rat spinal cord’s motor function. J Mol Neurosci doi:10.1007/s12031-012-9740-6

  115. Vincent AJ, Taylor JM, Choi-Lundberg DL, West AK, Chuah MI (2005) Genetic expression profile of olfactory ensheathing cells is distinct from that of Schwann cells and astrocytes. Glia 51:132–147

    Article  PubMed  Google Scholar 

  116. Boyd JG, Jahed A, McDonald TG, Krol KM, Van Eyk JE, Doucette R, Kawaja MD (2006) Proteomic evaluation reveals that olfactory ensheathing cells but not Schwann cells express calponin. Glia 53:434–440

    Article  PubMed  Google Scholar 

  117. Franssen EH, De Bree FM, Essing AH, Ramon-Cueto A, Verhaagen J (2008) Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia 56:1285–1298

    Article  PubMed  Google Scholar 

  118. Norgren RB Jr, Ratner N, Brackenbury R (1992) Development of olfactory nerve glia defined by a monoclonal antibody specific for Schwann cells. Dev Dyn 194:231–238

    Article  PubMed  Google Scholar 

  119. Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB (2002) Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. J Neurosci 22:6670–6681

    PubMed  CAS  Google Scholar 

  120. Thompson RJ, Roberts B, Alexander CL, Williams SK, Barnett SC (2000) Comparison of neuregulin-1 expression in olfactory ensheathing cells, Schwann cells and astrocytes. J Neurosci Res 61:172–185

    Article  PubMed  CAS  Google Scholar 

  121. Gasser C (1956) Olfactory nerve fibres. J Gen Physiol 39:483–496

    Article  Google Scholar 

  122. Mendoza AS, Breipohl W, Miragall F (1982) Cell migration from the chick olfactory placode: a light and electron microscopic study. J Embryol Exp Morphol 69:47–59

    PubMed  CAS  Google Scholar 

  123. Doucette R (1991) PNS-CNS transitional zone of the first cranial nerve. J Comp Neurol 312:451–466

    Article  PubMed  CAS  Google Scholar 

  124. Chuah MI, Au C (1991) Olfactory Schwann cells are derived from precursor cells in the olfactory epithelium. J Neurosci Res 29:172–180

    Article  PubMed  CAS  Google Scholar 

  125. Calof AL, Guevara JL (1993) Cell lines derived from retrovirus mediated oncogene transduction into olfactory epithelium cultures. Neuroprotocols Companion Meth Neurosci 3:222–231

    Google Scholar 

  126. Mumm JS, Shou J, Calof AL (1996) Colony-forming progenitors from mouse olfactory epithelium: evidence for feedback regulation of neuron production. Proc Natl Acad Sci U S A 93:11167–11172

    Article  PubMed  CAS  Google Scholar 

  127. Whitlock KE (2004) A new model for olfactory placode development. Brain Behav Evol 64:126–140

    Article  PubMed  Google Scholar 

  128. Basch ML, Bronner-Fraser M, Garcia-Castro MI (2006) Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441:218–222

    Article  PubMed  CAS  Google Scholar 

  129. D’Amico-Martel A, Noden DM (1983) Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat 166:445–468

    Article  PubMed  Google Scholar 

  130. Collazo A, Fraser SE, Mabee PM (1994) A dual embryonic origin for vertebrate mechanoreceptors. Science 264:426–430

    Article  PubMed  CAS  Google Scholar 

  131. Echelard Y, Vassileva G, McMahon AP (1994) Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120:2213–2224

    PubMed  CAS  Google Scholar 

  132. Hebert JM, McConnell SK (2000) Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev Biol 222:296–306

    Article  PubMed  CAS  Google Scholar 

  133. Keilhoff G, Goihl A, Langnase K, Fansa H, Wolf G (2006) Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells. Eur J Cell Biol 85:11–24

    Article  PubMed  CAS  Google Scholar 

  134. Brand G (2006) Olfactory/trigeminal interactions in nasal chemoreception. Neurosci Biobehav Rev 30:908–917

    Article  PubMed  Google Scholar 

  135. Finger TE, Bottger B (1993) Peripheral peptidergic fibers of the trigeminal nerve in the olfactory bulb of the rat. J Comp Neurol 334:117–124

    Article  PubMed  CAS  Google Scholar 

  136. Schaefer ML, Bottger B, Silver WL, Finger TE (2002) Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J Comp Neurol 444:221–226

    Article  PubMed  Google Scholar 

  137. Silver WL, Finger TE (2009) The anatomical and electrophysiological basis of peripheral nasal trigeminal chemoreception. Ann N Y Acad Sci 1170:202–205

    Article  PubMed  Google Scholar 

  138. Stone H, Rebert CS (1970) Observations on trigeminal olfactory interactions. Brain Res 21:138–142

    Article  PubMed  CAS  Google Scholar 

  139. Rawson NE, Lischka FW, Yee KK, Peters AZ, Tucker ES, Meechan DW, Zirlinger M, Maynard TM, Burd GB, Dulac C, Pevny L, LaMantia AS (2010) Specific mesenchymal/epithelial induction of olfactory receptor, vomeronasal, and gonadotropin-releasing hormone (GnRH) neurons. Dev Dyn 239:1723–1738

    Article  PubMed  CAS  Google Scholar 

  140. Carmona-Fontaine C, Acuna G, Ellwanger K, Niehrs C, Mayor R (2007) Neural crests are actively precluded from the anterior neural fold by a novel inhibitory mechanism dependent on Dickkopf1 secreted by the prechordal mesoderm. Dev Biol 309:208–221

    Article  PubMed  CAS  Google Scholar 

  141. Monsoro-Burq AH, Fletcher RB, Harland RM (2003) Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals. Development 130:3111–3124

    Article  PubMed  CAS  Google Scholar 

  142. Villanueva S, Glavic A, Ruiz P, Mayor R (2002) Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction. Dev Biol 241:289–301

    Article  PubMed  CAS  Google Scholar 

  143. Wu J, Yang J, Klein PS (2005) Neural crest induction by the canonical Wnt pathway can be dissociated from anterior–posterior neural patterning in Xenopus. Dev Biol 279:220–232

    Article  PubMed  CAS  Google Scholar 

  144. Brun RB (1985) Neural fold and neural crest movement in the Mexican salamander Ambystoma mexicanum. J Exp Zool 234:57–61

    Article  PubMed  CAS  Google Scholar 

  145. Au E, Roskams AJ (2003) Olfactory ensheathing cells of the lamina propria in vivo and in vitro. Glia 41:224–236

    Article  PubMed  Google Scholar 

  146. Northcutt RG, Gans C (1983) The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q Rev Biol 58:1–28

    Article  PubMed  CAS  Google Scholar 

  147. Williams MS (2005) Speculations on the pathogenesis of CHARGE syndrome. Am J Med Genet A 133A:318–325

    Article  PubMed  Google Scholar 

  148. Begbie J, Graham A (2001) Integration between the epibranchial placodes and the hindbrain. Science 294:595–598

    Article  PubMed  CAS  Google Scholar 

  149. Shiau CE, Lwigale PY, Das RM, Wilson SA, Bronner-Fraser M (2008) Robo2-Slit1 dependent cell-cell interactions mediate assembly of the trigeminal ganglion. Nat Neurosci 11:269–276

    Article  PubMed  CAS  Google Scholar 

  150. Fernandes KJ, Toma JG, Miller FD (2008) Multipotent skin-derived precursors: adult neural crest-related precursors with therapeutic potential. Philos Trans R Soc Lond B Biol Sci 363:185–198

    Article  PubMed  CAS  Google Scholar 

  151. Roisen FJ, Klueber KM, Lu CL, Hatcher LM, Dozier A, Shields CB, Maguire S (2001) Adult human olfactory stem cells. Brain Res 890:11–22

    Article  PubMed  CAS  Google Scholar 

  152. Keyvan-Fouladi N, Raisman G, Li Y (2003) Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J Neurosci 23:9428–9434

    PubMed  CAS  Google Scholar 

  153. Li Y, Field PM, Raisman G (1998) Regeneration of adult rat corticospinal axons induced by transplanted olfactory ensheathing cells. J Neurosci 18:10514–10524

    PubMed  CAS  Google Scholar 

  154. Ramon-Cueto A, Nieto-Sampedro M (1994) Regeneration into the spinal cord of transected dorsal root axons is promoted by ensheathing glia transplants. Exp Neurol 127:232–244

    Article  PubMed  CAS  Google Scholar 

  155. Binder E, Rukavina M, Hassani H, Weber M, Nakatani H, Reiff T, Parras C, Taylor V, Rohrer H (2011) Peripheral nervous system progenitors can be reprogrammed to produce myelinating oligodendrocytes and repair brain lesions. J Neurosci Off J Soc Neurosci 31:6379–6391

    Article  CAS  Google Scholar 

  156. Dupin E, Calloni GW, Le Douarin NM (2010) The cephalic neural crest of amniote vertebrates is composed of a large majority of precursors endowed with neural, melanocytic, chondrogenic and osteogenic potentialities. Cell Cycle 9:238–249

    Article  PubMed  CAS  Google Scholar 

  157. Dupin E, Calloni G, Real C, Goncalves-Trentin A, Le Douarin NM (2007) Neural crest progenitors and stem cells. C R Biol 330:521–529

    Article  PubMed  CAS  Google Scholar 

  158. Nagoshi N, Shibata S, Kubota Y, Nakamura M, Nagai Y, Satoh E, Morikawa S, Okada Y, Mabuchi Y, Katoh H, Okada S, Fukuda K, Suda T, Matsuzaki Y, Toyama Y, Okano H (2008) Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2:392–403

    Article  PubMed  CAS  Google Scholar 

  159. Real C, Glavieux-Pardanaud C, Vaigot P, Le-Douarin N, Dupin E (2005) The instability of the neural crest phenotypes: Schwann cells can differentiate into myofibroblasts. Int J Dev Biol 49:151–159

    Article  PubMed  CAS  Google Scholar 

  160. Widera D, Heimann P, Zander C, Imielski Y, Heidbreder M, Heilemann M, Kaltschmidt C, Kaltschmidt B (2011) Schwann cells can be reprogrammed to multipotency by culture. Stem Cells Dev 20:2053–2064

    Article  PubMed  CAS  Google Scholar 

  161. Yang J, Lou Q, Huang R, Shen L, Chen Z (2008) Dorsal root ganglion neurons induce transdifferentiation of mesenchymal stem cells along a Schwann cell lineage. Neurosci Lett 445:246–251

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Dr. David H. Gutmann (Washington University School of Medicine, St Louis, MO, USA) for sharing the BLBPCreIRESLacZ mouse line.

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Correspondence to Susan Wray.

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This work was supported by the Intramural Research Program of the National Institutes of Health, National Institute of Neurological Disorders and Stroke.

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Forni, P.E., Wray, S. Neural Crest and Olfactory System: New Prospective. Mol Neurobiol 46, 349–360 (2012). https://doi.org/10.1007/s12035-012-8286-5

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