Growth Factors Regulating Neural Crest Cell Fate Decisions

  • Lukas Sommer

Abstract

Because of its unique ability to generate a wide variety of both neural and nonneural derivatives, the neural crest is an ideal model system to study the factors regulating cell lineage decisions in stem and progenitor cells. The use of various cell culture techniques and in vivo functional assays, including cell type-specific gene manipulation in mouse, helped to identify signaling factors involved in this process. Moreover, it became apparent that the biological functions of growth factors acting on neural crest cells depend on the context provided by the extracellular microenvironment. Thus, signaling molecules have to be viewed as parts of complex networks that change with time and location. Neural crest cells have to integrate these signals to ensure the generation of appropriate numbers of differentiating progeny. It will be important to determine how such signaling networks are established and how they elicit multiple signaling responses in neural crest cells to activate appropriate genetic programs.

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References

  1. 1.
    Le Douarin NM, Kalchcim C. The Neural Crest. Cambridge: Cambridge University Press, 1999.Google Scholar
  2. 2.
    Le Douarin NM, Creuzet S, Couly G et al. Neural crest cell plasticity and its limits. Development 2004;131:4637–4650.PubMedCrossRefGoogle Scholar
  3. 3.
    Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 1992;71:973–985.PubMedCrossRefGoogle Scholar
  4. 4.
    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-β family factors. Development 1999;126:3781–3794.PubMedGoogle Scholar
  5. 5.
    Morrison SJ, White PM, Zock C et al. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 1999;96:737–749.PubMedCrossRefGoogle Scholar
  6. 6.
    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;35:657–669.PubMedCrossRefGoogle Scholar
  7. 7.
    Sommer L. Context-dependent regulation of fate decisions in multipotent progenitor cells of the peripheral nervous system. Cell Tissue Res 2001;305:211–216.PubMedCrossRefGoogle Scholar
  8. 8.
    Trentin A, Glavieux-Pardanaud C, Le Douarin NM et al. Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci USA 2004;101:4495–4500.PubMedCrossRefGoogle Scholar
  9. 9.
    Anderson DJ, Groves A, Lo L et al. Cell lineage determination and the control of neuronal identity in the neural crest. Cold Spring Harb Symp Quant Biol 1997;62:493–504.PubMedGoogle Scholar
  10. 10.
    Taraviras S, Pachnis V. Development of the mammalian enteric nervous system. Curr Opin Genet Dev 1999;9:321–327.PubMedCrossRefGoogle Scholar
  11. 11.
    Abzhanov A, Tzahor E, Lassar AB et al. Dissimilar regulation of cell differentiation in mesencephalic (cranial) and sacral (trunk) neural crest cells in vitro. Development 2003;130:4567–4579.PubMedCrossRefGoogle Scholar
  12. 12.
    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;35:643–656.PubMedCrossRefGoogle Scholar
  13. 13.
    Shah N, Groves A, Anderson DJ. Alternative neural crest cell fates are instructively promoted by TGFβ superfamily members. Cell 1996;85:331–343.PubMedCrossRefGoogle Scholar
  14. 14.
    Reissmann E, Ernsberger U, Francis-West PH et al. Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development 1996;122:2079–2088.PubMedGoogle Scholar
  15. 15.
    Creuzet S, Couly G, Vincent C et al. Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton. Development 2002;129:4301–4313.PubMedGoogle Scholar
  16. 16.
    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;101:499–510.PubMedCrossRefGoogle Scholar
  17. 17.
    Shah NM, Marchionni MA, Isaacs I et al. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 1994;77:349–360.PubMedCrossRefGoogle Scholar
  18. 18.
    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;303:1020–1023.PubMedCrossRefGoogle Scholar
  19. 19.
    Guillemot F, Lo L-C, Johnson JE et al. Mammalian achaete-scute homolog-1 is required for the early development of olfactory and autonomic neurons. Cell 1993;75:463–476.PubMedCrossRefGoogle Scholar
  20. 20.
    Sommer L, Shah N, Rao M et al. The cellular function of MASH1 in autonomic neurogenesis. Neuron 1995;15:1245–1258.PubMedCrossRefGoogle Scholar
  21. 21.
    Leimeroth R, Lobsiger C, Lussi A et al. Membrane-bound neuregulinl type III actively promotes Schwann cell differentiation of multipotent progenitor cells. Dev Biol 2002;246:245–258.PubMedCrossRefGoogle Scholar
  22. 22.
    Hagedorn L, Paratore C, Brugnoli G et al. The Ets domain transcription factor Erm distinguishes rat satellite glia from Schwann cells and is regulated in satellite cells by neuregulin signaling. Dev Biol 2000;219:44–58.PubMedCrossRefGoogle Scholar
  23. 23.
    Kleber M, Sommer L. Wnt signaling and the regulation of stem cell function. Curr Opin Cell Biol 2004;16:681–687.PubMedCrossRefGoogle Scholar
  24. 24.
    Kim J, Lo L, Dormand E et al. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003;38:17–31.PubMedCrossRefGoogle Scholar
  25. 25.
    Paratore C, Eichenberger C, Suter U et al. Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum Mol Genet 2002;11:3075–3085.PubMedCrossRefGoogle Scholar
  26. 26.
    Sommer L, Rao M. Neural stem cells and regulation of cell number. Prog Neurobiol 2002;66:1–18.PubMedCrossRefGoogle Scholar
  27. 27.
    Shah NM, Anderson DJ. Integration of multiple instructive cues by neural crest stem cells reveals cell-intrinsic biases in relative growth factor responsiveness. Proc Natl Acad Sci USA 1997;94:11369–11374.PubMedCrossRefGoogle Scholar
  28. 28.
    Gurdon JB, Lemaire P, Kato K. Community effects and related phenomena in development. Cell 1993;75:831–834.PubMedCrossRefGoogle Scholar
  29. 29.
    Hagedorn L, Floris J, Suter U et al. Autonomic neurogenesis and apoptosis are alternative fates of progenitor cell communities induced by TGFbeta. Dev Biol 2000;228:57–72.PubMedCrossRefGoogle Scholar
  30. 30.
    Schneider C, Wicht H, Enderich J et al. Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron 1999;24:861–870.PubMedCrossRefGoogle Scholar
  31. 31.
    Garratt AN, Britsch S, Birchmeier C. Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays 2000;22:987–996.PubMedCrossRefGoogle Scholar
  32. 32.
    Furukawa T, Mukherjee S, Bao ZZ et al. rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 2000;26:383–394.PubMedCrossRefGoogle Scholar
  33. 33.
    Gaiano N, Nye JS, Fishell G. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 2000;26:395–404.PubMedCrossRefGoogle Scholar
  34. 34.
    Hitoshi S, Alexson T, Tropepe V et al. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 2002;16:846–858.PubMedCrossRefGoogle Scholar
  35. 35.
    Genoud S, Lappe-Siefke C, Goebbels S et al. Notch1 control of oligodendrocyte differentiation in the spinal cord. J Cell Biol 2002;158:709–718.PubMedCrossRefGoogle Scholar
  36. 36.
    Ahlgren SC, Bronner-Fraser M. Inhibition of sonic hedgehog signaling in vivo results in craniofacial neural crest cell death. Curr Biol 1999;9:1304–1314.PubMedCrossRefGoogle Scholar
  37. 37.
    Gu H, Marth JD, Orban PC et al. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 1994;265:103–106.PubMedCrossRefGoogle Scholar
  38. 38.
    Hari L, Brault V, Kléber M et al. Lineage-specific requirements of β-catenin in neural crest development. J Cell Biol 2002;159:867–880.PubMedCrossRefGoogle Scholar
  39. 39.
    Cadigan KM, Nusse R. Wnt signaling: A common theme in animal development. Genes Dev 1997;11:3286–3305.PubMedGoogle Scholar
  40. 40.
    Nakagawa S, Takeichi M. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 1998;125:2963–2971.PubMedGoogle Scholar
  41. 41.
    Borchers A, David R, Wedlich D. Xenopus cadherin-11 restrains cranial neural crest migration and influences neural crest specification. Development 2001;128:3049–3060.PubMedGoogle Scholar
  42. 42.
    Garcia-Castro MI, Marcelle C, Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science 2002;297:848–851.PubMedCrossRefGoogle Scholar
  43. 43.
    Ikeya M, Lee SM, Johnson JE et al. Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 1997;389:966–970.PubMedCrossRefGoogle Scholar
  44. 44.
    Jin EJ, Erickson CA, Takada S et al. Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo. Dev Biol 2001;233:22–37.PubMedCrossRefGoogle Scholar
  45. 45.
    Dorsky RI, Moon RT, Raible DW. Control of neural crest cell fate by the Wnt signalling pathway. Nature 1998;396:370–373.PubMedCrossRefGoogle Scholar
  46. 46.
    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;131:5327–5339.PubMedCrossRefGoogle Scholar
  47. 47.
    Brault V, Moore R, Kutsch S et al. Inactivation of the β-catenin gene by Wnt1-Cremediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001;128:1253–1264.PubMedGoogle Scholar
  48. 48.
    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;13:1717–1728.PubMedGoogle Scholar
  49. 49.
    Bronner-Fraser M. Development. Making sense of the sensory lineage. Science 2004;303:966–968.PubMedCrossRefGoogle Scholar
  50. 50.
    Lewis JL, Bonner J, Modrell M et al. Reiterated Wnt signaling during zebrafish neural crest development. Development 2004;131:1299–1308.PubMedCrossRefGoogle Scholar
  51. 51.
    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;18:937–951.PubMedCrossRefGoogle Scholar
  52. 52.
    Winnier GE, Hargett L, Hogan BL. The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev 1997;11:926–940.PubMedCrossRefGoogle Scholar
  53. 53.
    Iida K, Koseki H, Kakinuma H et al. Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 1997;124:4627–4638.PubMedGoogle Scholar
  54. 54.
    Wurdak H, Ittner LM, Lang KS et al. Inactivation of TGFβ signaling in neural crest stem cells leads to multiple defects reminiscent of DiGeorge syndrome. Genes Dev 2005;19:530–535PubMedCrossRefGoogle Scholar
  55. 55.
    Vitelli F, Baldini A. Generating and modifying DiGeorge syndrome-like phenotypes in model organisms: Is there a common genetic pathway? Trends Genet 2003;19:588–593.PubMedCrossRefGoogle Scholar
  56. 56.
    Kaartinen V, Dudas M, Nagy A et al. Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells. Development 2004;131:3481–3490.PubMedCrossRefGoogle Scholar
  57. 57.
    Kirby ML, Waldo KL. Neural crest and cardiovascular patterning. Circ Res 1995;77:211–215.PubMedGoogle Scholar
  58. 58.
    Ohnemus S, Kanzler B, Jerome-Majewska LA et al. Aortic arch and pharyngeal phenotype in the absence of BMP-dependent neural crest in the mouse. Mech Dev 2002;119:127–35.PubMedCrossRefGoogle Scholar
  59. 59.
    Conway SJ, Henderson DJ, Copp AJ. Pax3 is required for cardiac neural crest migration in the mouse: Evidence from the splotch (Sp2H) mutant. Development 1997;124:505–14.PubMedGoogle Scholar
  60. 60.
    Kioussi C, Briata P, Baek SH et al. Identification of a Wnt/Dvl/beta-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 2002;111:673–685.PubMedCrossRefGoogle Scholar
  61. 61.
    Guris DL, Fames J, Tara D et al. Mice lacking the homologue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syndrome. Nat Genet 2001;27:293–298.PubMedCrossRefGoogle Scholar
  62. 62.
    Loeys BL, Chen J, Neptune ER et al. A syndrome of altered cardiovascular, craniofacial, neurocognitive and skeletal development caused by mutations in TGFBR1 or TGFBR2. Nat Genet 2005;37:275–281.PubMedCrossRefGoogle Scholar
  63. 63.
    Feil R, Brocard J, Mascrez B et al. Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA 1996;93:10887–10890.PubMedCrossRefGoogle Scholar
  64. 64.
    Danielian PS, Muccino D, Rowitch DH et al. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr Biol 1998;8:1323–1326.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2006

Authors and Affiliations

  • Lukas Sommer
    • 1
  1. 1.Institute of Cell Biology, Swiss Federal Institute of TechnologyETH-HoenggerbergZürichSwitzerland

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