Advertisement

Origin of Adrenal Chromaffin Cells from the Neural Crest

Chapter
  • 22 Downloads
Part of the Medical Intelligence Unit book series (MIU.LANDES)

Abstract

Adrenal chromaffin cells, or pheochromocytes, are one of the most experimentally accessible and extensively studied derivatives of the neural crest. Histological techniques based on catecholamine biochemistry allowed early researchers to identify the precursors for adrenal chromaffin cells as they migrate from the primary sympathetic chains into the adrenal primordia. Subsequent production of antisera that recognize catecholamine-synthesizing enzymes allowed further characterization of precursor migration patterns and chromaffin cell differentiation. Recently, identification of numerous molecular markers of neuronal differentiation and transcriptional regulation has led to the development of a model for the sympathoadrenal lineage and responsiveness of these cells to particular environmental cues. I will first describe the migration patterns of the neural crest-derived precursors for adrenal chromaffin cells in avian and mammalian embryos. I will then review the expression of catecholamine-synthesizing enzymes, neuronal markers and transcription factors in the sympathoadrenal lineage, and relate these patterns of differentiation to environmental cues encountered by pheochromocytes.

Keywords

Neural Crest Chromaffin Cell Multiple Endocrine Neoplasia Type Neural Crest Cell Sympathetic Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Weston JA. The migration and differentiation of neural crest cells. Adv Morphogen 1970; 8: 41–114.Google Scholar
  2. 2.
    LeDouarin NM. The neural crest. Cambridge: Cambridge University Press, 1982.Google Scholar
  3. 3.
    Rickmann M, Fawcett JW, Keynes RJ. The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Exp Morphol Embryol 1985; 90: 437–55.Google Scholar
  4. 4.
    Bronner-Fraser M. Analysis of the early stages of trunk neural crest migration in avian embryos using the monoclonal antibody HNK-1. Dev Biol 1986; 115: 44–55.PubMedCrossRefGoogle Scholar
  5. 5.
    Loring J, Erickson C. Neural crest cell migration pathways in the chick embryo. Dev Biol 1987; 121: 230–6.CrossRefGoogle Scholar
  6. 6.
    Teillet MA, Kalcheim C, LeDouarin NM. Formation of the dorsal root ganglion in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. Dev Biol 1987; 120: 329–47.PubMedCrossRefGoogle Scholar
  7. 7.
    Lallier T, Bronner-Fraser M. A spatial and temporal analysis of dorsal root and sympathetic ganglion formation in the avian embryo. Dev Biol 1988; 127: 99–112.PubMedCrossRefGoogle Scholar
  8. 8.
    Kalcheim C, Teillet MA. Consequences of somite manipulation on the pattern of dorsal root ganglion development. Development 1989; 106: 85–93.PubMedGoogle Scholar
  9. 9.
    Goldstein RS, Kalcheim C. Normal segmentation and size of the primary sympathetic ganglia depend upon the alternation of rostrocaudal properties of the somites. Development 1991; 112: 327–34.PubMedGoogle Scholar
  10. 10.
    Tosney KW, Dehnbostel DB, Erickson CA. Neural crest cells prefer the myotome’s basal lamina over the sclerotome as a substratum. Dev Biol 1994; 163: 389–406.PubMedCrossRefGoogle Scholar
  11. 11.
    Erickson CA, Duong TD, Tosney KW. Descriptive and experimental analysis of the dispersion of neural crest cells along the dorsolateral path and their entry into ectoderm in the chick embryo. Dev Biol 1992; 151: 251–72.PubMedCrossRefGoogle Scholar
  12. 12.
    Weston JA. Sequential segregation and fate of developmentally restricted intermediate cell populations in the neural crest lineage. Curr Topics Dev Biol 1991; 23: 133–53.CrossRefGoogle Scholar
  13. 13.
    Vogel KS, Weston JA. A subpopulation of cultured avian neural crest cells has transient neurogenic potential. Neuron 1988; 1: 569–77.PubMedCrossRefGoogle Scholar
  14. 14.
    Artinger KB, Bronner-Fraser M. Partial restriction in the developmental potential of late emigrating avian neural crest cells. Dev Biol 1992; 149: 149–57.PubMedCrossRefGoogle Scholar
  15. 15.
    Raible DW, Eisen JS. Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 1994; 120: 495–503.PubMedGoogle Scholar
  16. 16.
    Serbedzija GN, Bronner-Fraser M, Fraser SE. Developmental potential of trunk neural crest cells in the mouse. Development 1994; 120: 1709–18.PubMedGoogle Scholar
  17. 17.
    Erickson CA, Goins TL. Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes. Development 1995; 121: 915–24.PubMedGoogle Scholar
  18. 18.
    Rau AS, Johnston PH. Observations on the development of the sympathetic system and suprarenal bodies in the sparrow. Proc Zool Soc London 1923; 3: 741–68.Google Scholar
  19. 19.
    Willier BH. A study of the origin and differentiation of the suprarenal gland in the chick embryo by chorio-allantoic grafting. Physiol Zool 1930; 3: 201–25.Google Scholar
  20. 20.
    Pankratz DS. The development of the suprarenal gland in the albino rat. Anat Rec 1931; 49: 31–9.CrossRefGoogle Scholar
  21. 21.
    Hammond WS, Yntema CL. Depletions in the thoraco-lumbar sympathetic system following removal of neural crest in the chick. J Comp Neurol 1947; 86: 237–65.PubMedCrossRefGoogle Scholar
  22. 22.
    Weston JA. A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Dev Biol 1963; 6: 279–310.PubMedCrossRefGoogle Scholar
  23. 23.
    LeDouarin NM, Teillet MA. Localisation, par la methode des greffes interspecifiques, du territoire neural dont derivent les cellules adrenales surrenaliennes chez l’embryon d’Oiseau. CR Acad Sci 1971; 272: 481–4.Google Scholar
  24. 24.
    Teillet MA, LeDouarin NM. Determination par la methode des greffes heterospecifiques d’ebauches neurales de Caille sur l’embryon de polet, du niveau du nevraxe dont derivent les cellules medullosurrenaliennes. Arch Anat Microsc Morphol Exp 1974; 63: 51–62.PubMedGoogle Scholar
  25. 25.
    Anderson DJ, Axel R. A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 1986; 47: 1079–90.PubMedCrossRefGoogle Scholar
  26. 26.
    Falck B. Observations on the possibilities of the cellular localization of monoamines by a fluorescence method. Acta Physiol Scand 1962; Suppl 197.Google Scholar
  27. 27.
    Enemar A, Falck B, Hakanson R. Observations on the appearance of norepinephrine in the sympathetic nervous system of the chick embryo. Dev Biol 1965; 11: 268–83.PubMedCrossRefGoogle Scholar
  28. 28.
    Kirby ML, Gilmore SA. A correlative histofluorescence and light microscopic study of the formation of the sympathetic trunks in chick embryos. Anat Rec 1976; 186: 437–50.PubMedCrossRefGoogle Scholar
  29. 29.
    Allan IJ, Newgreen DF. Catecholamine accumulation in neural crest cells and the primary sympathetic chain. Amer J Anat 1977; 149: 413–21.PubMedCrossRefGoogle Scholar
  30. 30.
    Fernholm M. On the development of the sympathetic chain and adrenal medulla in the mouse. Z Anat Entwicldungsgesch 1971; 133: 305–17.CrossRefGoogle Scholar
  31. 31.
    Polak JM, Rost FWD, Pearse AGE. Fluorogenic amine tracing of neural crest derivatives forming the adrenal medulla Gen Comp Endocrinol 1971; 16: 132–6.Google Scholar
  32. 32.
    Teitelman G, Baker H, Joh TH et al. Appearance of catecholamine-synthesizing enzymes during development of the rat sympathetic nervous system: Possible role of tissue environment. Proc Natl Acad Sci USA 1979; 76: 509–13.PubMedCrossRefGoogle Scholar
  33. 33.
    Cochard P, Goldstein M, Black IB. Ontogenic appearance and disappearance of tyrosine hydroxylase and catecholamines in the rat embryo. Proc Nad Acad Sci USA 1978; 75: 2986–90.CrossRefGoogle Scholar
  34. 34.
    Cochard P, Goldstein M, Black IB. Initial development of the noradrenergic phenotype in autonomic neuroblasts of the rat embryo in vivo. Dev Biol 1979; 71: 100–14.PubMedCrossRefGoogle Scholar
  35. 35.
    Rothman TP, Gershon MD, Holtzer H. The relationship of cell division to the acquisition of adrenergic characteristics by develop- ing sympathetic ganglion cell precursors. Dey Biol 1978; 65: 322–41.CrossRefGoogle Scholar
  36. 36.
    Henion PD, Landis SC. Asynchronous appearance and topographic segregation of neuropeptide-containing cells in the developing rat adrenal medulla. J Neurosci 1990; 10: 2886–96.Google Scholar
  37. 37.
    Vogel KS, Weston JA. The sympathoadrenal lineage in avian embryos 1. Adrenal chromaffin cells lose neuronal traits during embryogenesis. Dev Biol 1990; 139: 1–12.PubMedCrossRefGoogle Scholar
  38. 38.
    Groves AK, George KM, Tissier-Seta JP et al. Differential regulation of transcription factor gene expression and phenotypic markers in developing sympathetic neurons. Development 1995; 121: 887–901.PubMedGoogle Scholar
  39. 39.
    Bohn MC, Goldstein M, Black IB. Role of glucocorticoids in expression of the adrenergic phenotype in rat embryonic adrenal gland. Dev Biol 1981; 82: 1–10.PubMedCrossRefGoogle Scholar
  40. 40.
    Bohn MC, Goldstein M, Black IB. Expression of phenylethanolamine N-methyltransferase in rat sympathetic ganglia and extra-adrenal chromaffin tissue. Dev Biol 1982; 89: 299–308.PubMedCrossRefGoogle Scholar
  41. 41.
    Verhofstad AAJ, Hokfelt T, Goldstein M et al. Appearance of tyrosine hydroxylase, aromatic amino-acid decarboxylase, dopamine B-hrdroxylase and phenylethanolamine N-methyltransferase during the ontogenesis of the adrenal medulla: An immunohistochemical study in the rat. Cell Tissue Res 1979; 200: 1–13.PubMedCrossRefGoogle Scholar
  42. 42.
    Ehrlich ME, Evinger M, Regunathan S et al. Mammalian adrenal chromaffin cells coexpress the epinephrine-synthesizing enzyme and neuronal properties in vivo and in vitro. Dev Biol 1994; 163: 480–90.PubMedCrossRefGoogle Scholar
  43. 43.
    Cochard P, Paulin D. Initial expression of neurofilaments and vimentin in the central and peripheral nervous system of the mouse embryo in vivo. J Neurosci 1984; 4: 2080–94.PubMedGoogle Scholar
  44. 44.
    Stein R, Mori N, Matthews K. The NGF-inducible SCG-10 mRNA encodes a novel membrane-bound protein present in growth cones and abundant in developing neurons. Neuron 1988; 1: 463–76.PubMedCrossRefGoogle Scholar
  45. 45.
    Anderson DJ, Axel R. Molecular probes for the development and plasticity of neural crest derivatives. Cell 1985; 42: 649–62.PubMedCrossRefGoogle Scholar
  46. 46.
    Anderson DJ, Carnahan JF, Michelson A et al. Antibody markers identify a common progenitor to sympathetic neurons and chromaffin cells in vivo and reveal the timing of commitment to neuronal differentiation in the sympathoadrenal lineage. J Neurosci 1991; 11: 3507–19.PubMedGoogle Scholar
  47. 47.
    Schultzberg M, Lundberg JM, Hokfelt T et al. Enkephalin-like immunoreactivity in gland cells and nerve terminals of the adrenal medulla. Neurosci 1978; 3: 1169–86.CrossRefGoogle Scholar
  48. 48.
    Bohn MC, Kessler JA, Golightly L et al. Appearance of enkephalin-immunoreactivity in rat adrenal medulla following treatment with nicotinic antagonists or reserpine. Cell Tissue Res 1983; 231: 469–79.PubMedCrossRefGoogle Scholar
  49. 49.
    deQuidt ME, Emson PC. Neuropeptide Y in the adrenal gland: characterization, distribution and drug effects. Neurosci 1986; 19: 1011–22.CrossRefGoogle Scholar
  50. 50.
    Livett BG, Day R, Elde RP et al. Co-storage of enkephalins and adrenaline in the bovine adrenal medulla. Neurosci 1982; 7: 1323–32.CrossRefGoogle Scholar
  51. 51.
    Carnahan JF, Patterson PH. The generation of monoclonal antibodies that bind preferentially to adrenal chromaffin cells and the cells of embryonic sympathetic ganglia. J Neurosci 1991; 11: 3493–506.PubMedGoogle Scholar
  52. 52.
    Carnahan JF, Patterson PH. Isolation of the progenitor cells of the sympathoadrenal lineage from embryonic sympathetic ganglia with the SA monoclonal antibodies. J Neurosci 1991; 11: 3520–30.PubMedGoogle Scholar
  53. 53.
    Johnson JE, Birren SJ, Anderson DJ. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 1990; 346: 858–61.PubMedCrossRefGoogle Scholar
  54. 54.
    Lo LC, Johnson JE, Wuenschell CW et al. Mammalian achaetescute homolog-1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 1991; 5: 1524–37.PubMedCrossRefGoogle Scholar
  55. 55.
    Guillemot F, Lo LC, Johnson JE et al. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 1993; 75: 463–76.PubMedCrossRefGoogle Scholar
  56. 56.
    Valarche I, Tissier-Seta JP, Hirsch MR et al. The mouse homeodomain protein Phox2 regulates Ncam promoter activity in concert with Cux/CDP and is a putative determinant of neurotransmitter phenotype. Development 1993; 119: 881–96.PubMedGoogle Scholar
  57. 57.
    Unsicker K, Krisch B, Otten U et al. Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc Natl Acad Sci USA 1978; 75: 3498–3502.PubMedCrossRefGoogle Scholar
  58. 58.
    Aloe L, Levi-Montalcini R. Nerve growth factor-induced transformation of immature chromaffin cells in vivo into sympathetic neurons: effect of antiserum to nerve growth factor. Proc Natl Acad Sci USA 1979; 76: 1246–50.PubMedCrossRefGoogle Scholar
  59. 59.
    Doupe AJ, Landis SC, Patterson PH. Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J Neurosci 1985; 5: 2119–42.PubMedGoogle Scholar
  60. 60.
    Cohen AM. Factors directing the expression of sympathetic nerve traits in cells of neural crest origin. J Exp Zool 1972; 179: 167–82.PubMedCrossRefGoogle Scholar
  61. 61.
    Norr SC. In vitro analysis of sympathetic neuron differentiation from chick neural crest cells. Dev Biol 1973; 34: 16–38.PubMedCrossRefGoogle Scholar
  62. 62.
    Howard MJ, Bronner-Fraser M. The influence of neural tube-derived factors on differentiation of neural crest cells in vitro 1. Histochemical study on the appearance of adrenergic cells. J Neurosci 1985; 5: 3302–9.PubMedGoogle Scholar
  63. 63.
    Teillet MA, LeDouarin NM. Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev Biol 1983; 98: 192–211.PubMedCrossRefGoogle Scholar
  64. 64.
    Stern CD, Artinger KB, Bronner-Fraser M. Tissue interactions affecting the migration and differentiation of neural crest cells in the chick embryo. Development 1991; 113: 207–16.PubMedGoogle Scholar
  65. 65.
    Maxwell GD, Forbes ME. Exogenous basement membrane-like matrix stimulates adrenergic development in avian neural crest cultures. Development 1987; 101: 767–76.PubMedGoogle Scholar
  66. 66.
    Sieber-Blum M, Sieber F, Yamada KM. Cellular fibronectin promotes adrenergic differentiation of quail neural crest cells in vitro. Exp Cell Res 1981; 133: 285–95.PubMedCrossRefGoogle Scholar
  67. 67.
    Loring J, Glimelius B, Weston JA. Extracellular matrix materials influence quail neural crest cell differentiation in vitro. Dev Biol 1982; 90: 165–74.PubMedCrossRefGoogle Scholar
  68. 68.
    Newgreen DF, Thiery JP. Fibronectin in early avian embryos: synthesis and distribution along the migration pathways of neural crest cells. Cell Tissue Res 1980; 211: 269–91.PubMedCrossRefGoogle Scholar
  69. 69.
    Rogers SL, Gegick PJ, Alexander SM et al. Transforming growth factor-B alters differentiation in cultures of avian neural crest-derived cells: Effects on cell morphology, proliferation, fibronectin expression, and melanogenesis. Dev Biol 1992; 151: 192–203.PubMedCrossRefGoogle Scholar
  70. 70.
    Howard MJ, Gershon MD. Role of growth factors in catecholaminergic expression by neural crest cells: in vitro effects of transforming growth factor beta-1. Dev Dynamics 1993; 196: 1–10.CrossRefGoogle Scholar
  71. 71.
    Maxwell GD, Forbes ME. Stimulation of adrenergic development in neural crest cultures by a reconstituted basement membrane-like matrix is inhibited by agents that elevate cAMP. J Neurosci Res 1990; 25: 172–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Smith J, Fauquet M. Glucocorticoids stimulate adrenergic differentiation in cultures of migrating and premigratory neural crest. J Neurosci 1984; 4: 2160–72.PubMedGoogle Scholar
  73. 73.
    Unsicker K, Millar TJ, Muller TH et al. Embryonic rat adrenal glands in organ culture: Effects of dexamethasone, nerve growth fator and its antibodies on pheochromoblast differentiation. Cell tissue Res 1985; 241: 207–17.PubMedCrossRefGoogle Scholar
  74. 74.
    Vogel KS, Weston JA. The sympathoadrenal lineage in avian embryos II. Effects of glucocorticoids on cultured neural crest cells. Dev Biol 1990; 139: 13–23.PubMedCrossRefGoogle Scholar
  75. 75.
    Ross ME, Evinger MJ, Hyman SE et al. Identification of a functional glucocorticoid response element in the phenylethanolamine N-methyltransferase promoter using fusion genes introduced into chromaffin cells in primary culture. J Neurosci 1990; 10: 520–30.PubMedGoogle Scholar
  76. 76.
    Seidl K, Unsicker K. The determination of the adrenal medullary cell fate during embryogenesis. Dev Biol 1989; 136: 481–90.PubMedCrossRefGoogle Scholar
  77. 77.
    Margolis FL, Roffi J, Jost A. Norepinephrine methylation in fetal rat adrenals. Science 1966; 154: 275–6.PubMedCrossRefGoogle Scholar
  78. 78.
    Wurtman RJ, Axelrod J. Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. J Biol Chem 1970; 241: 2301–5.Google Scholar
  79. 79.
    Ciaranello RD, Jacobowitz D, Axelrod J. Effect of dexamethasone on phenylethanolamine N-methyltransferase in chromaffin tissue of the neonatal rat. J Neurochem 1973; 20: 799–805.PubMedCrossRefGoogle Scholar
  80. 80.
    Teitelman G, Joh TH, Park DH et al. Expression of the adrenergic phenotype in cultured fetal adrenal medullary cells: Role of extrinsic and intrinsic factors. Dev Biol 1982; 89: 450–9.PubMedCrossRefGoogle Scholar
  81. 81.
    Grothe C, Hofmann HD, Verhofstad AAJ et al. Nerve growth factor and dexamethasone specify catecholaminergic phenotype of cultured rat chromaffin cells: Dependence on developmental stage. Dev Brain Res 1985; 21: 125–32.CrossRefGoogle Scholar
  82. 82.
    Michelson AM, Anderson DJ. Changes in competence determine the timing of two sequential glucocorticoid effects on sympathoadrenal progenitors. Neuron 1992; 8: 589–604.CrossRefGoogle Scholar
  83. 83.
    Lillien LE, Claude P. Nerve growth factor is a mitogen for cultured chromaffin cells. Nature 1985; 317: 632–4.PubMedCrossRefGoogle Scholar
  84. 84.
    Naujoks KW, Korsching S, Rohrer H et al. Nerve growth factor-mediated induction of tyrosine hydroxylase and of neurite outgrowth in cultures of bovine adrenal chromaffin cells: dependence on developmental stage. Dev Biol 1982; 92: 365–79.PubMedCrossRefGoogle Scholar
  85. 85.
    Tischler AS, Riseberg JC, Hardenbrook MA et al. Nerve growth factor is a potent inducer of proliferation and neuronal differentiation for adult rat chromaffin cells in vitro. J Neurosci 1993; 13: 1533–42.PubMedGoogle Scholar
  86. 86.
    Stemple DL, Mahanthappa NK, Anderson DJ. Basic FGF induces neuronal differentiation, cell division, and NGF dependence in chromaffin cells: A sequence of events in sympathetic development. Neuron 1988; 1: 517–25.PubMedCrossRefGoogle Scholar
  87. 87.
    Frodin M, Gammeltoft S. Insulin-like growth factors act synergistically with basic fibroblast growth factor and nerve growth factor to promote chromaffin cell proliferation. Proc Natl Acad Sci USA 1994; 91: 1771–5.PubMedCrossRefGoogle Scholar
  88. 88.
    Claude P, Parada IM, Gordon KA et al. Acidic fibroblast growth factor stimulates adrenal chromaffin cells to proliferate and to extend neurites, but is not a long-term survival factor. Neuron 1988; 1: 783–90.PubMedCrossRefGoogle Scholar
  89. 89.
    Anderson DJ. Molecular control of cell fate in the neural crest: the sympathoadrenal lineage. Ann Rev Neurosci 1993; 16: 129–58.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1996

Authors and Affiliations

There are no affiliations available

Personalised recommendations