Skip to main content
SpringerLink
Log in

Specification of Sensory Neuron Cell Fate from the Neural Crest

  • Chapter
Neural Crest Induction and Differentiation

Part of the book series: Advances in Experimental Medicine and Biology ((volume 589))

Abstract

How distinct cell fates are generated from initially homogeneous cell populations is a driving question in developmental biology. The neural crest is one such cell population that is capable of producing an incredible array of derivatives.1 Cells as different in function and form as the pigment cells in the skin or the neurons and glia of the peripheral nervous system are all derived from neural crest. How do these cells choose to migrate along distinct routes, populate defined regions of the embryo and differentiate into specific cell types?

This chapter focuses on the development of one particular neural crest derivative, sensory neurons, as a model for studying these questions of cell fate specification. In the head, sensory neurons reside in the trigeminal and epibranchial ganglia, while in the trunk they form the spinal or dorsal root ganglia (DRG). The development of the DRG will be the main focus of this review. The neurons and glia of the DRG derive from trunk neural crest cells that coalesce at the lateral edge of the spinal cord (Fig. 1). These neural crest cells migrate along the same routes as neural crest cells that populate the autonomic sympathetic ganglia located along the dorsal aorta. Somehow DRG precursors must make the decision to stop and adopt a sensory fate adjacent to the spinal cord rather than continuing on to become part of the autonomic ganglia. Moreover, once the DRG precursors aggregate in their final positions there are still a number of fate choices to be made. The mature DRG is composed of many neurons with different morphologies and distinct biochemical properties as well as glial cells that support these neurons.2

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Le Douarin N, Kalcheim C. The neural crest. Cambridge (UK): Cambridge University Press, 1999.

    Google Scholar 

  2. Scott S. Sensory neurons: Diversity, development and pasticity. New York: Oxford University Press, 1992.

    Google Scholar 

  3. Kuntzer T, Antoine JC, Steck AJ. Clinical features and pathophysiological basis of sensory neuronopathies (ganglionopathies). Muscle Nerve 2004;30(3):255–268.

    Article  PubMed  Google Scholar 

  4. Toth C, Brussee V, Cheng C et al. Diabetes mellitus and the sensory neuron. J Neuropathol Exp Neurol 2004;63(6):561–573.

    PubMed  CAS  Google Scholar 

  5. Hunt SP, Mantyh PW. The molecular dynamics of pain control. Nat Rev Neurosci 2001;2(2):83–91.

    Article  PubMed  CAS  Google Scholar 

  6. Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature 2001;413(6852):203–210.

    Article  PubMed  CAS  Google Scholar 

  7. His W. Untersuchungen uber die erste Anlage des Wirbeltierliebes. Die erste Entwicklung des Huhnchens im Ei. Liepzig: F.C.W. Vogel, 1868.

    Google Scholar 

  8. Horstadius S. The neural crest. London: Oxford University Press, 1950.

    Google Scholar 

  9. Weston JA. The migration and differentiation of neural crest cells. Adv Morphog 1970;8:41–114.

    PubMed  CAS  Google Scholar 

  10. Hamburger V. Experimental analysis of the dual origin of the trigeminal ganglion in the chick embryo. J Exp Zool 1961;148:91–117.

    Article  PubMed  CAS  Google Scholar 

  11. Johnston MC. A radioautographic study of the migration and fate of cranial neural crest cells in the chick embryo. Anat Rec 1966;156(2):143–155.

    Article  PubMed  CAS  Google Scholar 

  12. Noden DM. The control of avian cephalic neural crest cytodifferentiation. II. Neural tissues. Dev Biol 1978;67(2):313–329.

    Article  PubMed  CAS  Google Scholar 

  13. D’AmicoMartel A, Noden DM. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat 1983;166(4):445–468.

    Article  CAS  Google Scholar 

  14. Maro GS, Vermeren M, Voiculescu O et al. Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat Neurosci 2004;7(9):930–938.

    Article  PubMed  CAS  Google Scholar 

  15. Loring JF, Barker DL, Erickson CA. Migration and differentiation of neural crest and ventral neural tube cells in vitro: Implications for in vitro and in vivo studies of the neural crest. J Neurosci 1988;8(3):1001–1015.

    PubMed  CAS  Google Scholar 

  16. Sohal GS, Bockman DE, Ali MM et al. DiI labeling and homeobox gene islet-1 expression reveal the contribution of ventral neural tube cells to the formation of the avian trigeminal ganglion. Int J Dev Neurosci 1996;14(4):419–427.

    Article  PubMed  CAS  Google Scholar 

  17. Dickinson DP, Machnicki M, Ali MM et al. Ventrally emigrating neural tube (VENT) cells: A second neural tube-derived cell population. J Anat 2004;205(2):79–98.

    Article  PubMed  Google Scholar 

  18. Price J. An immunohistochemical and quantitative examination of dorsal root ganglion neuronal subpopulations. J Neurosci 1985;5(8):2051–2059.

    PubMed  CAS  Google Scholar 

  19. Wright DE, Snider WD. Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J Comp Neurol 1995;351(3):329–338.

    Article  PubMed  CAS  Google Scholar 

  20. Djouhri L, Lawson SN. Abeta-fiber nociceptive primary afferent neurons: A review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 2004;46(2):131–145.

    Article  PubMed  Google Scholar 

  21. Lawson SN, Harper AA, Harper EI et al. A monoclonal antibody against neurofilament protein specifically labels a subpopulation of rat sensory neurones. J Comp Neurol 1984;228(2):263–272.

    Article  PubMed  CAS  Google Scholar 

  22. Goldstein ME, House SB, Gainer H. NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J Neurosci Res 1991;30(1):92–104.

    Article  PubMed  CAS  Google Scholar 

  23. Amaya F, Decosterd I, Samad TA et al. Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2. Mol Cell Neurosci 2000;15(4):331–342.

    Article  PubMed  CAS  Google Scholar 

  24. New HV, Mudge AW. Distribution and ontogeny of SP, CGRP, SOM, and VIP in chick sensory and sympathetic ganglia. Dev Biol 1986;116(2):337–346.

    Article  PubMed  CAS  Google Scholar 

  25. Lawson SN. Neuropeptides in morphologically and functionally identified primary afferent neurons in dorsal root ganglia: Substance P, CGRP and somatostatin. Prog Brain Res 1995;104:161–173.

    Article  PubMed  CAS  Google Scholar 

  26. Greffrath W, Binzen U, Schwarz ST et al. Coexpression of heat sensitive vanilloid receptor subtypes in rat dorsal root ganglion neurons. Neuroreport 2003;14(17):2251–2255.

    Article  PubMed  CAS  Google Scholar 

  27. Lewinter RD, Skinner K, Julius D et al. Immunoreactive TRPV-2 (VRL-1), a capsaicin receptor homolog, in the spinal cord of the rat. J Comp Neurol 2004;470(4):400–408.

    Article  PubMed  CAS  Google Scholar 

  28. Tamura S, Morikawa Y, Senba E. TRPV2, a capsaicin receptor homologue, is expressed predominantly in the neurotrophin-3-dependent subpopulation of primary sensory neurons. Neuroscience 2005;130(1):223–228.

    Article  PubMed  CAS  Google Scholar 

  29. Petruska JC, Cooper BY, Gu JG et al. Distribution of P2X1, P2X2, and P2X3 receptor subunits in rat primary afferents: Relation to population markers and specific cell types. J Chem Neuroanat 2000;20(2):141–162.

    Article  PubMed  CAS  Google Scholar 

  30. Kobayashi K, Fukuoka T, Yamanaka H et al. Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J Comp Neurol 2005;481(4):377–390.

    Article  PubMed  CAS  Google Scholar 

  31. Dong X, Han S, Zylka MJ et al. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell 2001;106(5):619–632.

    Article  PubMed  CAS  Google Scholar 

  32. Bender E, Buist A, Jurzak M et al. Characterization of an orphan G protein-coupled receptor localized in the dorsal root ganglia reveals adenine as a signaling molecule. Proc Natl Acad Sci USA 2002;99(13):8573–8578.

    Article  PubMed  CAS  Google Scholar 

  33. Lembo PM, Grazzini E, Groblewski T et al. Proenkephalin A gene products activate a new family of sensory neuron—specific GPCRs. Nat Neurosci 2002;5(3):201–209.

    Article  PubMed  CAS  Google Scholar 

  34. Zylka MJ, Rice FL, Anderson DJ. Topographically distinct epidermal nociceptive circuits revealed by axonal tracers targeted to Mrgprd. Neuron 2005;45(1):17–25.

    Article  PubMed  CAS  Google Scholar 

  35. Hamburger V, Levi-Montalcini R. Proliferation, differentiation and degeneration in the spinal ganglia of teh chick embryo under normal and experimental conditions. J Exp Zool 1949;11:457–502.

    Article  Google Scholar 

  36. Mu X, Silos-Santiago I, Carroll SL et al. Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J Neurosci 1993;13(9):4029–4041.

    PubMed  CAS  Google Scholar 

  37. Kashiba H, Ueda Y, Senba E. Coexprcssion of prcprotachykinin-A, alpha-calcitonin gene-related peptide, somatostatin, and neurotrophin receptor family messenger RNAs in rat dorsal root ganglion neurons. Neuroscience 1996;70(1):179–189.

    Article  PubMed  CAS  Google Scholar 

  38. McMahon SB, Armanini MP, Ling LH et al. Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 1994;12(5):1161–1171.

    Article  PubMed  CAS  Google Scholar 

  39. Henion PD, Garner AS, Large TH et al. trkC-mediated NT-3 signaling is required for the early development of a subpopulation of neurogenic neural crest cells. Dev Biol 1995;172(2):602–613.

    Article  PubMed  CAS  Google Scholar 

  40. Rifkin JT, Todd VJ, Anderson LW et al. Dynamic expression of neurotrophin receptors during sensory neuron genesis and differentiation. Dev Biol 2000;227(2):465–480.

    Article  PubMed  CAS  Google Scholar 

  41. Klein R, Silos-Santiago I, Smeyne RJ et al. Disruption of the neurotrophin-3 receptor gene trkC eliminates la muscle afferents and results in abnormal movements. Nature 1994;368(6468):249–251.

    Article  PubMed  CAS  Google Scholar 

  42. Tessarollo L, Vogel KS, Palko ME et al. Targeted mutation in the neurotrophin-3 gene results in loss of muscle sensory neurons. Proc Natl Acad Sci USA 1994;91(25):11844–11848.

    Article  PubMed  CAS  Google Scholar 

  43. Farinas I, Jones KR, Backus C et al. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 1994;369(6482):658–661.

    Article  PubMed  CAS  Google Scholar 

  44. Ernfors P, Lee KF, Kucera J et al. Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 1994;77(4):503–512.

    Article  PubMed  CAS  Google Scholar 

  45. Minichiello L, Piehl F, Vazquez E et al. Differential effects of combined trk receptor mutations on dorsal root ganglion and inner ear sensory neurons. Development 1995;121(12):4067–4075.

    PubMed  CAS  Google Scholar 

  46. Crowley C, Spencer SD, Nishimura MC et al. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 1994;76(6):1001–1011.

    Article  PubMed  CAS  Google Scholar 

  47. Smeyne RJ, Klein R, Schnapp A et al. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 1994;368(6468):246–249.

    Article  PubMed  CAS  Google Scholar 

  48. Silos-Santiago I, Molliver DC, Ozaki S et al. NonTrkA-expressing small DRG neurons are lost in TrkA deficient mice. J Neurosci 1995;15(9):5929–5942.

    PubMed  CAS  Google Scholar 

  49. Deckwerth TL, Elliott JL, Knudson CM et al. BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 1996;17(3):401–411.

    Article  PubMed  CAS  Google Scholar 

  50. Lentz SI, Knudson CM, Korsmeyer SJ et al. Neurotrophins support the development of diverse sensory axon morphologies. J Neurosci 1999;19(3):1038–1048.

    PubMed  CAS  Google Scholar 

  51. Patel TD, Jackman A, Rice FL et al. Development of sensory neurons in the absence of NGF/TrkA signaling in vivo. Neuron 2000;25(2):345–357.

    Article  PubMed  CAS  Google Scholar 

  52. Patel TD, Kramer I, Kucera J et al. Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents. Neuron 2003;38(3):403–416.

    Article  PubMed  CAS  Google Scholar 

  53. Genc B, Ozdinler PH, Mendoza AE et al. A chemoattractant role for NT-3 in proprioceptive axon guidance. PLoS Biol 2004;2(12):e403.

    Article  PubMed  CAS  Google Scholar 

  54. Bronner-Fraser M, Fraser S. Developmental potential of avian trunk neural crest cells in situ. Neuron 1989;3(6):755–766.

    Article  PubMed  CAS  Google Scholar 

  55. Frank E, Sanes JR. Lineage of neurons and glia in chick dorsal root ganglia: Analysis in vivo with a recombinant retrovirus. Development 1991;111(4):895–908.

    PubMed  CAS  Google Scholar 

  56. Duff RS, Langtimm CJ, Richardson MK et al. In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail embryo. Dev Biol 1991;147(2):451–459.

    Article  PubMed  CAS  Google Scholar 

  57. Hagedorn L, Suter U, Sommer L. P0 and PMP22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-beta family factors. Development 1999;126(17):3781–3794.

    PubMed  CAS  Google Scholar 

  58. Ziller C, Fauquet M, Kalcheim C et al. Cell lineages in peripheral nervous system ontogeny: Medium-induced modulation of neuronal phenotypic expression in neural crest cell cultures. Dev Biol 1987;120(1):101–111.

    Article  PubMed  CAS  Google Scholar 

  59. Sieber-Blum M. Commitment of neural crest cells to the sensory neuron lineage. Science 1989;243(4898):1608–1611.

    Article  PubMed  CAS  Google Scholar 

  60. Matsumoto SG. Neuronal differentiation in cultures of murine neural crest. II. Development of capsaicin-sensitive neurons. Brain Res Dev Brain Res 1994;83(1):17–27.

    Article  PubMed  CAS  Google Scholar 

  61. Greenwood AL, Turner EE, Anderson DJ. Identification of dividing, determined sensory neuron precursors in the mammalian neural crest. Development 1999;126(16):3545–3559.

    PubMed  CAS  Google Scholar 

  62. Carr VM, Simpson Jr SB. Proliferative and degenerative events in the early development of chick dorsal root ganglia. I. Normal development. J Comp Neurol 1978;182(4):727–739.

    Article  PubMed  CAS  Google Scholar 

  63. Lawson SN, Biscoe TJ. Development of mouse dorsal root ganglia: An autoradiographic and quantitative study. J Neurocytol 1979;8(3):265–274.

    Article  PubMed  CAS  Google Scholar 

  64. Kitao Y, Robertson B, Kudo M et al. Neurogenesis of subpopulations of rat lumbar dorsal root ganglion neurons including neurons projecting to the dorsal column nuclei. J Comp Neurol 1996;371(2):249–257.

    Article  PubMed  CAS  Google Scholar 

  65. Ma Q, Fode C, Guillemot F et al. Neurogenin1 and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev 1999;13(13):1717–1728.

    PubMed  CAS  Google Scholar 

  66. Ma Q, Chen Z, del Barco Barrantes I et al. Neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 1998;20(3):469–482.

    Article  PubMed  CAS  Google Scholar 

  67. Fode C, Gradwohl G, Morin X et al. The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 1998;20(3):483–494.

    Article  PubMed  CAS  Google Scholar 

  68. Andermann P, Ungos J, Raible DW. Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev Biol 2002;251(1):45–58.

    Article  PubMed  CAS  Google Scholar 

  69. Ma Q, Kintner C, Anderson DJ. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 1996;87(1):43–52.

    Article  PubMed  CAS  Google Scholar 

  70. Blader P, Fischer N, Gradwohl G et al. The activity of neurogenin1 is controlled by local cues in the zebrafish embryo. Development 1997;124(22):4557–4569.

    PubMed  CAS  Google Scholar 

  71. Perez SE, Rebelo S, Anderson DJ. Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 1999;126(8):1715–1728.

    PubMed  CAS  Google Scholar 

  72. Shah NM, Groves AK, Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 1996;85(3):331–343.

    Article  PubMed  CAS  Google Scholar 

  73. Lo L, Dormand E, Greenwood A et al. Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 2002;129(7):1553–1567.

    PubMed  CAS  Google Scholar 

  74. Parras CM, Schuurmans C, Scardigli R et al. Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev 2002;16(3):324–338.

    Article  PubMed  CAS  Google Scholar 

  75. Fedtsova NG, Turner EE. Brn-3.0 expression identifies early post-mitotic CNS neurons and sensory neural precursors. Mech Dev 1995;53(3):291–304.

    Article  PubMed  CAS  Google Scholar 

  76. McEvilly RJ, Erkman L, Luo L et al. Requirement for Brn-3.0 in differentiation and survival of sensory and motor neurons. Nature 1996;384(6609):574–577.

    Article  PubMed  CAS  Google Scholar 

  77. Xiang M, Gan L, Zhou L et al. Targeted deletion of the mouse POU domain gene Brn-3a causes selective loss of neurons in the brainstem and trigeminal ganglion, uncoordinated limb movement, and impaired suckling. Proc Natl Acad Sci USA 1996;93(21):11950–11955.

    Article  PubMed  CAS  Google Scholar 

  78. Huang EJ, Zang K, Schmidt A et al. POU domain factor Brn-3a controls the differentiation and survival of trigeminal neurons by regulating Trk receptor expression. Development 1999;126(13):2869–2882.

    PubMed  CAS  Google Scholar 

  79. Eng SR, Gratwick K, Rhee JM et al. Defects in sensory axon growth precede neuronal death in Brn3a-deficient mice. J Neurosci 2001;21(2):541–549.

    PubMed  CAS  Google Scholar 

  80. Eng SR, Lanier J, Fedtsova N et al. Coordinated regulation of gene expression by Brn3a in developing sensory ganglia. Development 2004;131(16):3859–3870.

    Article  PubMed  CAS  Google Scholar 

  81. Coffman JA. Runx transcription factors and the developmental balance between cell proliferation and differentiation. Cell Biol Int 2003;27(4):315–324.

    Article  PubMed  CAS  Google Scholar 

  82. Levanon D, Brenner O, Negreanu V et al. Spatial and temporal expression pattern of Runx3 (Aml2) and Runx1 (Aml1) indicates nonredundant functions during mouse embryogenesis. Mech Dev 2001;109(2):413–417.

    Article  PubMed  CAS  Google Scholar 

  83. Inoue K, Ozaki S, Ito K et al. Runx3 is essential for the target-specific axon pathfinding of trkc-expressing dorsal root ganglion neurons. Blood Cells Mol Dis 2003;30(2):157–160.

    Article  PubMed  CAS  Google Scholar 

  84. Okuda T, van Deursen J, Hiebert SW et al. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 1996;84(2):321–330.

    Article  PubMed  CAS  Google Scholar 

  85. Bangsow C, Rubins N, Glusman G et al. The RUNX3 gene—sequence, structure and regulated expression. Gene 2001;279(2):221–232.

    Article  PubMed  CAS  Google Scholar 

  86. Levanon D, Bettoun D, Harris-Cerruti C et al. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 2002;21(13):3454–3463.

    Article  PubMed  CAS  Google Scholar 

  87. Ma L, Merenmies J, Parada LF. Molecular characterization of the TrkA/NGF receptor minimal enhancer reveals regulation by multiple cis elements to drive embryonic neuron expression. Development 2000;127(17):3777–3788.

    PubMed  CAS  Google Scholar 

  88. Ma L, Lei L, Eng SR et al. Brn3a regulation of TrkA/NGF receptor expression in developing sensory neurons. Development 2003;130(15):3525–3534.

    Article  PubMed  CAS  Google Scholar 

  89. Lei L, Ma L, Nef S et al. mKlf7, a potential transcriptional regulator of TrkA nerve growth factor receptor expression in sensory and sympathetic neurons. Development 2001;128(7):1147–1158.

    PubMed  CAS  Google Scholar 

  90. Wiggins AK, Wei G, Doxakis E et al. Interaction of Brn3a and HIPK2 mediates transcriptional repression of sensory neuron survival. J Cell Biol 2004;167(2):257–267.

    Article  PubMed  CAS  Google Scholar 

  91. Smaldone S, Laub F, Else C et al. Identification of MoKA, a novel F-box protein that modulates Kruppel-like transcription factor 7 activity. Mol Cell Biol 2004;24(3):1058–1069.

    Article  PubMed  CAS  Google Scholar 

  92. Chen HH, Hippenmeyer S, Arber S et al. Development of the monosynaptic stretch reflex circuit. Curr Opin Neurobiol 2003;13(1):96–102.

    Article  PubMed  CAS  Google Scholar 

  93. Lin JH, Saito T, Anderson DJ et al. Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell 1998;95(3):393–407.

    Article  PubMed  CAS  Google Scholar 

  94. Arber S, Ladle DR, Lin JH et al. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 2000;101(5):485–498.

    Article  PubMed  CAS  Google Scholar 

  95. Livet J, Sigrist M, Stroebel S et al. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 2002;35(5):877–892.

    Article  PubMed  CAS  Google Scholar 

  96. Hari L, Brault V, Kleber M et al. Lineage-specific requirements of beta-catenin in neural crest development. J Cell Biol 2002;159(5):867–880.

    Article  PubMed  CAS  Google Scholar 

  97. Lee HY, Kleber M, Hari L et al. Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells. Science 2004;303(5660):1020–1023.

    Article  PubMed  CAS  Google Scholar 

  98. Dorsky RI, Moon RT, Raible DW. Control of neural crest cell fate by the Wnt signalling pathway. Nature 1998;396(6709):370–373.

    Article  PubMed  CAS  Google Scholar 

  99. Jin EJ, Erickson CA, Takada S et al. Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev Biol 2001;233(1):22–37.

    Article  PubMed  CAS  Google Scholar 

  100. Lewis JL, Bonner J, Modrell M et al. Reiterated Wnt signaling during zebrafish neural crest development. Development 2004;131(6):1299–1308.

    Article  PubMed  CAS  Google Scholar 

  101. Burstyn-Cohen T, Stanleigh J, Sela-Donenfeld D et al. Canonical Wnt activity regulates trunk neural crest delamination linking BMP/noggin signaling with G1/S transition. Development 2004;131(21):5327–5339.

    Article  PubMed  CAS  Google Scholar 

  102. Wakamatsu Y, Maynard TM, Weston JA. Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 2000;127(13):2811–2821.

    PubMed  CAS  Google Scholar 

  103. Morrison SJ, Perez SE, Qiao Z et al. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 2000;101(5):499–510.

    Article  PubMed  CAS  Google Scholar 

  104. Kubu CJ, Orimoto K, Morrison SJ et al. Developmental changes in Notch1 and numb expression mediated by local cell-cell interactions underlie progressively increasing delta sensitivity in neural crest stem cells. Dev Biol 2002;244(1):199–214.

    Article  PubMed  CAS  Google Scholar 

  105. Zilian O, Saner C, Hagedorn L et al. Multiple roles of mouse Numb in tuning developmental cell fates. Curr Biol 2001;11(7):494–501.

    Article  PubMed  CAS  Google Scholar 

  106. Cornell RA, Eisen JS. Delta/Notch signaling promotes formation of zebrafish neural crest by repressing Neurogenin 1 function. Development 2002;129(11):2639–2648.

    PubMed  CAS  Google Scholar 

  107. Glavic A, Silva F, Aybar MJ et al. Interplay between Notch signaling and the homeoprotein Xirol is required for neural crest induction in Xenopus embryos. Development 2004;131(2):347–359.

    Article  PubMed  CAS  Google Scholar 

  108. Huang EJ, Li H, Tang AA et al. Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization. Genes Dev 2005;19(1):138–151.

    Article  PubMed  CAS  Google Scholar 

  109. Ungos JM, Karlstrom RO, Raible DW. Hedgehog signaling is directly required for the development of zebrafish dorsal root ganglia neurons. Development 2003;130(22):5351–5362.

    Article  PubMed  CAS  Google Scholar 

  110. Ota M, Ito K. Induction of neurogenin-1 expression by sonic hedgehog: Its role in development of trigeminal sensory neurons. Dev Dyn 2003;227(4):544–551.

    Article  PubMed  CAS  Google Scholar 

  111. Fedtsova N, Perris R, Turner EE. Sonic hedgehog regulates the position of the trigeminal ganglia. Dev Biol 2003;261(2):456–469.

    Article  PubMed  CAS  Google Scholar 

  112. Ahlgren SC, Bronner-Fraser M. Inhibition of sonic hedgehog signaling in vivo results in craniofacial neural crest cell death. Curr Biol 1999;9(22):1304–1314.

    Article  PubMed  CAS  Google Scholar 

  113. Jeong J, Mao J, Tenzen T et al. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 2004;18(8):937–951.

    Article  PubMed  CAS  Google Scholar 

  114. Fu M, Lui VC, Sham MH et al. Sonic hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut. J Cell Biol 2004;166(5):673–684.

    Article  PubMed  CAS  Google Scholar 

  115. Zirlinger M, Lo L, McMahon J et al. Transient expression of the bHLH factor neurogenin-2 marks a subpopulation of neural crest cells biased for a sensory but not a neuronal fate. Proc Natl Acad Sci USA 2002;99(12):8084–8089.

    Article  PubMed  CAS  Google Scholar 

  116. Luo R, Gao J, Wehrle-Haller B et al. Molecular identification of distinct neurogenic and melanogenic neural crest sublineages. Development 2003;130(2):321–330.

    Article  PubMed  CAS  Google Scholar 

  117. White PM, Morrison SJ, Orimoto K et al. Neural crest stem cells undergo cell-intrinsic developmental changes in sensitivity to instructive differentiation signals. Neuron 2001;29(1):57–71.

    Article  PubMed  CAS  Google Scholar 

  118. Bixby S, Kruger GM, Mosher JT et al. Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 2002;35(4):643–656.

    Article  PubMed  CAS  Google Scholar 

  119. Kruger GM, Mosher JT, Bixby S et al. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 2002;35(4):657–669.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Structure, University of Washington, Seattle, Washington, USA

    David W. Raible & Josette M. Ungos

Authors
  1. David W. Raible
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Josette M. Ungos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David W. Raible .

Editor information

Editors and Affiliations

  1. Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Jean-Pierre Saint-Jeannet Ph.D.

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Raible, D.W., Ungos, J.M. (2006). Specification of Sensory Neuron Cell Fate from the Neural Crest. In: Saint-Jeannet, JP. (eds) Neural Crest Induction and Differentiation. Advances in Experimental Medicine and Biology, vol 589. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-46954-6_10

Download citation

Publish with us

Policies and ethics

Search

Navigation