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Review: The Role of Neural Crest Cells in the Endocrine System

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Abstract

The neural crest is a pluripotent population of cells that arises at the junction of the neural tube and the dorsal ectoderm. These highly migratory cells form diverse derivatives including neurons and glia of the sensory, sympathetic, and enteric nervous systems, melanocytes, and the bones, cartilage, and connective tissues of the face. The neural crest has long been associated with the endocrine system, although not always correctly. According to current understanding, neural crest cells give rise to the chromaffin cells of the adrenal medulla, chief cells of the extra-adrenal paraganglia, and thyroid C cells. The endocrine tumors that correspond to these cell types are pheochromocytomas, extra-adrenal paragangliomas, and medullary thyroid carcinomas. Although controversies concerning embryological origin appear to have mostly been resolved, questions persist concerning the pathobiology of each tumor type and its basis in neural crest embryology. Here we present a brief history of the work on neural crest development, both in general and in application to the endocrine system. In particular, we present findings related to the plasticity and pluripotency of neural crest cells as well as a discussion of several different neural crest tumors in the endocrine system.

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References

  1. Zito G, et al. In vitro identification and characterization of CD133(pos) cancer stem-like cells in anaplastic thyroid carcinoma cell lines. PLoS ONE 3(10):e3544, 2008. doi:10.1371/journal.pone.0003544.

    PubMed  Google Scholar 

  2. Sieber-Blum M, et al. Characterization of epidermal neural crest stem cell (EPI-NCSC) grafts in the lesioned spinal cord. Mol Cell Neurosci 32(1–2):67–81, 2006. doi:10.1016/j.mcn.2006.02.003.

    PubMed  CAS  Google Scholar 

  3. Song YS, et al. Human neural crest stem cells transplanted in rat penile corpus cavernosum to repair erectile dysfunction. BJU Int 102(2):220–4, 2008. discussion 224. doi:10.1111/j.1464-410X.2008.07469.x.

    PubMed  CAS  Google Scholar 

  4. Basch ML, Bronner-Fraser M, Garcia-Castro MI. Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441(7090):218–22, 2006. doi:10.1038/nature04684.

    PubMed  CAS  Google Scholar 

  5. Anderson DJ. Molecular control of cell fate in the neural crest: the sympathoadrenal lineage. Annu Rev Neurosci 16:129–58, 1993. doi:10.1146/annurev.ne.16.030193.001021.

    PubMed  CAS  Google Scholar 

  6. Unsicker K. The chromaffin cell: paradigm in cell, developmental and growth factor biology. J Anat 183(Pt 2):207–21, 1993.

    PubMed  CAS  Google Scholar 

  7. Baker CV, Bronner-Fraser M. The origins of the neural crest. Part I: embryonic induction. Mech Dev 69(1–2):3–11, 1997. doi:10.1016/S0925-4773(97)00132-9.

    PubMed  CAS  Google Scholar 

  8. Le Douarin NM, Kalcheim C, Crest TN. The neural crest. Cambridge, UK: Cambridge University Press; 1999.

    Google Scholar 

  9. Hall BK. The neural crest in development and evolution. New York: Springer; 1999. p. 314.

    Google Scholar 

  10. Le Douarin NM, Teillet MA. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev Biol 41(1):162–84, 1974. doi:10.1016/0012-1606(74)90291-7.

    PubMed  Google Scholar 

  11. Le Douarin N, Fontaine J, Le Lievre C. New studies on the neural crest origin of the avian ultimobranchial glandular cells—interspecific combinations and cytochemical characterization of C cells based on the uptake of biogenic amine precursors. Histochemistry 38(4):297–305, 1974. doi:10.1007/BF00496718.

    PubMed  Google Scholar 

  12. Pearse AG. The cytochemistry of the thyroid C cells and their relationship to calcitonin. Proc R Soc Lond B Biol Sci 164(996):478–87, 1966.

    PubMed  CAS  Google Scholar 

  13. Bussolati G, Pearse AG. Immunofluorescent localization of calcitonin in the ‘C’ cells of pig and dog thyroid. J Endocrinol 37(2):205–9, 1967. doi:10.1677/joe.0.0370205.

    PubMed  CAS  Google Scholar 

  14. Polak JM, et al. Immunocytochemical confirmation of the neural crest origin of avian calcitonin-producing cells. Histochemistry 40(3):209–14, 1974. doi:10.1007/BF00501955.

    PubMed  CAS  Google Scholar 

  15. Gans C, Northcutt RG. Neural crest and the origin of vertebrates: a new head. Science 220(4594):268–73, 1983. doi:10.1126/science.220.4594.268.

    PubMed  CAS  Google Scholar 

  16. Kuratani S. Evolutionary developmental studies of cyclostomes and the origin of the vertebrate neck. Dev Growth Differ 50(Suppl 1):S189–94, 2008.

    PubMed  Google Scholar 

  17. Meulemans D, Bronner-Fraser M. Central role of gene cooption in neural crest evolution. J Exp Zoolog B Mol Dev Evol 304(4):298–303, 2005. doi:10.1002/jez.b.21047.

    PubMed  Google Scholar 

  18. Sauka-Spengler T, Bronner-Fraser M. Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr Opin Genet Dev 16(4):360–6, 2006. doi:10.1016/j.gde.2006.06.006.

    PubMed  CAS  Google Scholar 

  19. Sauka-Spengler T, et al. Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell 13(3):405–20, 2007. doi:10.1016/j.devcel.2007.08.005.

    PubMed  CAS  Google Scholar 

  20. Sauka-Spengler T, Bronner-Fraser M. A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9(7):557–68, 2008. doi:10.1038/nrm2428.

    PubMed  CAS  Google Scholar 

  21. Clark K, et al. Evidence for the neural crest origin of turtle plastron bones. Genesis. 2001;31(3):111–17. doi:10.1002/gene.10012.

    PubMed  CAS  Google Scholar 

  22. Cebra-Thomas JA, et al. Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Evol Dev 9(3):267–77, 2007.

    PubMed  CAS  Google Scholar 

  23. Gilbert SF, et al. Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol Dev 3(2):47–58, 2001. doi:10.1046/j.1525-142x.2001.003002047.x.

    PubMed  CAS  Google Scholar 

  24. Sanchez-Martin M, et al. SLUG (SNAI2) deletions in patients with Waardenburg disease. Hum Mol Genet 11(25):3231–6, 2002. doi:10.1093/hmg/11.25.3231.

    PubMed  CAS  Google Scholar 

  25. Smith SH, Murray RG, Hall M. The surface structure of Leptotrichia buccalis. Can J Microbiol 40(2):90–8, 1994.

    PubMed  CAS  Google Scholar 

  26. Freitas R, et al. Developmental origin of shark electrosensory organs. Evol Dev 8(1):74–80, 2006. doi:10.1111/j.1525-142X.2006.05076.x.

    PubMed  Google Scholar 

  27. Cano A, et al. The transcription factor snail controls epithelial–mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2(2):76–83, 2000. doi:10.1038/35000025.

    PubMed  CAS  Google Scholar 

  28. Graveson AC, Smith MM, Hall BK. Neural crest potential for tooth development in a urodele amphibian: developmental and evolutionary significance. Dev Biol 188(1):34–42, 1997. doi:10.1006/dbio.1997.8563.

    PubMed  CAS  Google Scholar 

  29. Lumsden AG. Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103(Suppl):155–69, 1988.

    PubMed  Google Scholar 

  30. Smith MM, Hall BK. Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev Camb Philos Soc 65(3):277–373, 1990. doi:10.1111/j.1469-185X.1990.tb01427.x.

    PubMed  CAS  Google Scholar 

  31. Noden DM. Cell movements and control of patterned tissue assembly during craniofacial development. J Craniofac Genet Dev Biol 11(4):192–213, 1991.

    PubMed  CAS  Google Scholar 

  32. Couly GF, Coltey PM, Le Douarin NM. The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114(1):1–15, 1992.

    PubMed  CAS  Google Scholar 

  33. Couly GF, Coltey PM, Le Douarin NM. The triple origin of skull in higher vertebrates: a study in quail–chick chimeras. Development 117(2):409–29, 1993.

    PubMed  CAS  Google Scholar 

  34. Heanue TA, Pachnis V. Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8(6):466–79, 2007. doi:10.1038/nrn2137.

    PubMed  CAS  Google Scholar 

  35. Le Lievre CS, Le Douarin NM. Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morphol 34(1):125–54, 1975.

    PubMed  Google Scholar 

  36. Jiang X, et al. Normal fate and altered function of the cardiac neural crest cell lineage in retinoic acid receptor mutant embryos. Mech Dev 117(1–2):115–22, 2002. doi:10.1016/S0925-4773(02)00206-X.

    PubMed  CAS  Google Scholar 

  37. Ito K, Sieber-Blum M. In vitro clonal analysis of quail cardiac neural crest development. Dev Biol 148(1):95–106, 1991. doi:10.1016/0012-1606(91)90320-3.

    PubMed  CAS  Google Scholar 

  38. His W. Die erste Entwicklung des Hühnchens im Ei: Untersuchungen über die erste Anlage des Wirbelthierleibes; 1868.

  39. Hörstadius S. The neural crest: its properties and derivatives in the light of experimental research. London: Oxford University Press; 1950.

    Google Scholar 

  40. Landacre FL. The fate of the neural crest in the head of urodeles. J Comp Neurol 33:1–44, 1921. doi:10.1002/cne.900330102.

    Google Scholar 

  41. Chibon P. Nuclear labelling by tritiated thymidine of neural crest derivatives in the amphibian urodele Pleurodeles waltlii Michah. J Embryol Exp Morphol 18(3):343–58, 1967.

    PubMed  CAS  Google Scholar 

  42. Weston JA. A radioautographic analysis of the migration and localization of trunk neural crest cells in the chick. Dev Biol 6:279–310, 1963. doi:10.1016/0012-1606(63)90016-2.

    PubMed  CAS  Google Scholar 

  43. Pearse AG. The cytochemistry and ultrastructure of polypeptide hormone-producing cells of the APUD series and the embryologic, physiologic and pathologic implications of the concept. J Histochem Cytochem 17(5):303–13, 1969.

    PubMed  CAS  Google Scholar 

  44. Fontaine J, Le Douarin NM. Analysis of endoderm formation in the avian blastoderm by the use of quail-chick chimaeras. The problem of the neurectodermal origin of the cells of the APUD series. J Embryol Exp Morphol 41:209–22, 1977.

    PubMed  CAS  Google Scholar 

  45. Andrew A, Kramer B, Rawdon BB. The origin of gut and pancreatic neuroendocrine (APUD) cells–the last word? J Pathol 186(2):117–18, 1998. doi:10.1002/(SICI)1096-9896(1998100)186:2<117::AID-PATH152>3.0.CO;2-J.

    PubMed  CAS  Google Scholar 

  46. Gross JB, Hanken J. Review of fate-mapping studies of osteogenic cranial neural crest in vertebrates. Dev Biol 317(2):389–400, 2008. doi:10.1016/j.ydbio.2008.02.046.

    PubMed  CAS  Google Scholar 

  47. Rollhauser-ter Horst J. Artificial neural crest formation in amphibia. Anat Embryol (Berl) 157(1):113–20, 1979. doi:10.1007/BF00315644.

    CAS  Google Scholar 

  48. Rollhauser-ter Horst J. Neural crest replaced by gastrula ectoderm in amphibia. Effect on neurulation, CNS, gills and limbs. Anat Embryol (Berl) 160(2):203–11, 1980. doi:10.1007/BF00301861.

    CAS  Google Scholar 

  49. Moury JD, Jacobson AG. Neural fold formation at newly created boundaries between neural plate and epidermis in the axolotl. Dev Biol 133(1):44–57, 1989. doi:10.1016/0012-1606(89)90295-9.

    PubMed  CAS  Google Scholar 

  50. Moury JD, Jacobson AG. The origins of neural crest cells in the axolotl. Dev Biol 141(2):243–53, 1990. doi:10.1016/0012-1606(90)90380-2.

    PubMed  CAS  Google Scholar 

  51. Selleck MA, Bronner-Fraser M. Origins of the avian neural crest: the role of neural plate–epidermal interactions. Development 121(2):525–38, 1995.

    PubMed  CAS  Google Scholar 

  52. Dickinson ME, et al. Dorsalization of the neural tube by the non-neural ectoderm. Development 121(7):2099–106, 1995.

    PubMed  CAS  Google Scholar 

  53. Gammill LS, Bronner-Fraser M. Genomic analysis of neural crest induction. Development 129(24):5731–41, 2002. doi:10.1242/dev.00175.

    PubMed  CAS  Google Scholar 

  54. Adams MS, Gammill LS, Bronner-Fraser M. Discovery of transcription factors and other candidate regulators of neural crest development. Dev Dyn 237(4):1021–33, 2008. doi:10.1002/dvdy.21513.

    PubMed  CAS  Google Scholar 

  55. Mancilla A, Mayor R. Neural crest formation in Xenopus laevis: mechanisms of Xslug induction. Dev Biol 177(2):580–9, 1996. doi:10.1006/dbio.1996.0187.

    PubMed  CAS  Google Scholar 

  56. Bronner-Fraser M, Fraser SE. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335(6186):161–4, 1988. doi:10.1038/335161a0.

    PubMed  CAS  Google Scholar 

  57. Funahashi J, et al. Role of Pax-5 in the regulation of a mid-hindbrain organizer's activity. Dev Growth Differ 41(1):59–72, 1999. doi:10.1046/j.1440-169x.1999.00401.x.

    PubMed  CAS  Google Scholar 

  58. Nakamura H, Watanabe Y, Funahashi J. Misexpression of genes in brain vesicles by in ovo electroporation. Dev Growth Differ 42(3):199–201, 2000. doi:10.1046/j.1440-169x.2000.00501.x.

    PubMed  CAS  Google Scholar 

  59. Katahira T, Nakamura H. Gene silencing in chick embryos with a vector-based small interfering RNA system. Dev Growth Differ 45(4):361–7, 2003. doi:10.1046/j.1440-169X.2003.00705.x.

    PubMed  CAS  Google Scholar 

  60. Sauka-Spengler T, Barembaum M. Gain- and loss-of-function approaches in the chick embryo. Methods Cell Biol 87:237–56, 2008. doi:10.1016/S0091-679X(08)00212-4.

    PubMed  CAS  Google Scholar 

  61. Tucker RP, Erickson CA. Morphology and behavior of quail neural crest cells in artificial three-dimensional extracellular matrices. Dev Biol 104(2):390–405, 1984. doi:10.1016/0012-1606(84)90094-0.

    PubMed  CAS  Google Scholar 

  62. Erickson CA, Loring JF, Lester SM. Migratory pathways of HNK-1-immunoreactive neural crest cells in the rat embryo. Dev Biol 134(1):112–18, 1989. doi:10.1016/0012-1606(89)90082-1.

    PubMed  CAS  Google Scholar 

  63. Chou DK, Schachner M, Jungalwala FB. HNK-1 sulfotransferase null mice express glucuronyl glycoconjugates and show normal cerebellar granule neuron migration in vivo and in vitro. J Neurochem 82(5):1239–51, 2002. doi:10.1046/j.1471-4159.2002.01066.x.

    PubMed  CAS  Google Scholar 

  64. 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 Embryol Exp Morphol 90:437–55, 1985.

    PubMed  CAS  Google Scholar 

  65. Bronner-Fraser M. Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev Biol 115(1):44–55, 1986. doi:10.1016/0012-1606(86)90226-5.

    PubMed  CAS  Google Scholar 

  66. Sadaghiani B, Vielkind JR. Distribution and migration pathways of HNK-1-immunoreactive neural crest cells in teleost fish embryos. Development 110(1):197–209, 1990.

    PubMed  CAS  Google Scholar 

  67. Jeffery WR, Strickler AG, Yamamoto Y. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431(7009):696–9, 2004. doi:10.1038/nature02975.

    PubMed  CAS  Google Scholar 

  68. Hou L. Effects of local tissue environment on the differentiation of neural crest cells in turtle, with special reference to understanding the spatial distribution of pigment cells. Pigment Cell Res 12(2):81–8, 1999. doi:10.1111/j.1600-0749.1999.tb00747.x.

    PubMed  CAS  Google Scholar 

  69. Sieber-Blum M, Cohen AM. Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of noncrest cells. Dev Biol 80(1):96–106, 1980. doi:10.1016/0012-1606(80)90501-1.

    PubMed  CAS  Google Scholar 

  70. Bronner-Fraser M, Sieber-Blum M, Cohen AM. Clonal analysis of the avian neural crest: migration and maturation of mixed neural crest clones injected into host chicken embryos. J Comp Neurol 193(2):423–34, 1980. doi:10.1002/cne.901930209.

    PubMed  CAS  Google Scholar 

  71. Bronner-Fraser M, Fraser S. Developmental potential of avian trunk neural crest cells in situ. Neuron 3(6):755–66, 1989. doi:10.1016/0896-6273(89)90244-4.

    PubMed  CAS  Google Scholar 

  72. Sieber-Blum M. Commitment of neural crest cells to the sensory neuron lineage. Science 243(4898):1608–11, 1989. doi:10.1126/science.2564699.

    PubMed  CAS  Google Scholar 

  73. Stemple DL, Anderson DJ. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71(6):973–85, 1992. doi:10.1016/0092-8674(92)90393-Q.

    PubMed  CAS  Google Scholar 

  74. Morrison SJ, et al. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96(5):737–49, 1999. doi:10.1016/S0092-8674(00)80583-8.

    PubMed  CAS  Google Scholar 

  75. Baroffio A, Dupin E, Le Douarin NM. Clone-forming ability and differentiation potential of migratory neural crest cells. Proc Natl Acad Sci USA 85(14):5325–9, 1988. doi:10.1073/pnas.85.14.5325.

    PubMed  CAS  Google Scholar 

  76. Baroffio A, Dupin E, Le Douarin NM. Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 112(1):301–5, 1991.

    PubMed  CAS  Google Scholar 

  77. Le Douarin NM, et al. Neural crest cell plasticity and its limits. Development 131(19):4637–50, 2004. doi:10.1242/dev.01350.

    PubMed  Google Scholar 

  78. Youn YH, et al. Neural crest stem cell and cardiac endothelium defects in the TrkC null mouse. Mol Cell Neurosci 24(1):160–70, 2003. doi:10.1016/S1044-7431(03)00125-8.

    PubMed  CAS  Google Scholar 

  79. Trentin A, et al. Self-renewal capacity is a widespread property of various types of neural crest precursor cells. Proc Natl Acad Sci USA 101(13):4495–500, 2004. doi:10.1073/pnas.0400629101.

    PubMed  CAS  Google Scholar 

  80. Lee G, et al. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 25(12):1468–75, 2007. doi:10.1038/nbt1365.

    PubMed  CAS  Google Scholar 

  81. Sieber-Blum M, et al. Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn 231(2):258–69, 2004. doi:10.1002/dvdy.20129.

    PubMed  CAS  Google Scholar 

  82. Duff RS, et al. In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail embryo. Dev Biol 147(2):451–9, 1991. doi:10.1016/0012-1606(91)90303-K.

    PubMed  CAS  Google Scholar 

  83. Sieber-Blum M, Hu Y. Epidermal neural crest stem cells (EPI-NCSC) and pluripotency. Stem Cell Rev 4(4):256–60, 2008. doi:10.1007/s12015-008-9042-0.

    PubMed  Google Scholar 

  84. Ito K, Sieber-Blum M. Pluripotent and developmentally restricted neural-crest-derived cells in posterior visceral arches. Dev Biol 156(1):191–200, 1993. doi:10.1006/dbio.1993.1069.

    PubMed  CAS  Google Scholar 

  85. Kruger GM, et al. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35(4):657–69, 2002. doi:10.1016/S0896-6273(02)00827-9.

    PubMed  CAS  Google Scholar 

  86. Richardson MK, Sieber-Blum M. Pluripotent neural crest cells in the developing skin of the quail embryo. Dev Biol 157(2):348–58, 1993. doi:10.1006/dbio.1993.1140.

    PubMed  CAS  Google Scholar 

  87. Nagoshi N, et al. Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad. Cell Stem Cell 2(4):392–403, 2008. doi:10.1016/j.stem.2008.03.005.

    PubMed  CAS  Google Scholar 

  88. Hu YF, Zhang ZJ, Sieber-Blum M. An epidermal neural crest stem cell (EPI-NCSC) molecular signature. Stem Cells 24(12):2692–702, 2006. doi:10.1634/stemcells.2006-0233.

    PubMed  CAS  Google Scholar 

  89. Rosai J. Basomelanocytic tumors: another nail in the neural crest coffin? In American Society of Dermatopathology Annual Meeting. 2009.

  90. Tischler AS. Pheochromocytoma and extra-adrenal paraganglioma: updates. Arch Pathol Lab Med 132(8):1272–84, 2008.

    PubMed  Google Scholar 

  91. Eisenhofer G, et al. Distinct gene expression profiles in norepinephrine- and epinephrine-producing hereditary and sporadic pheochromocytomas: activation of hypoxia-driven angiogenic pathways in von Hippel-Lindau syndrome. Endocr Relat Cancer 11(4):897–911, 2004. doi:10.1677/erc.1.00838.

    PubMed  CAS  Google Scholar 

  92. Wong DL. Why is the adrenal adrenergic? Endocr Pathol 14(1):25–36, 2003. doi:10.1385/EP:14:1:25.

    PubMed  CAS  Google Scholar 

  93. Huynh TT, et al. Transcriptional regulation of phenylethanolamine N-methyltransferase in pheochromocytomas from patients with von Hippel-Lindau syndrome and multiple endocrine neoplasia type 2. Ann N Y Acad Sci 1073:241–52, 2006. doi:10.1196/annals.1353.026.

    PubMed  CAS  Google Scholar 

  94. Unsicker K, et al. The chromaffin cell and its development. Neurochem Res 30(6–7):921–5, 2005. doi:10.1007/s11064-005-6966-5.

    PubMed  CAS  Google Scholar 

  95. Bryant J, et al. Pheochromocytoma: the expanding genetic differential diagnosis. J Natl Cancer Inst 95(16):1196–204, 2003.

    Article  PubMed  CAS  Google Scholar 

  96. Maher ER, Eng C. The pressure rises: update on the genetics of phaeochromocytoma. Hum Mol Genet 11(20):2347–54, 2002. doi:10.1093/hmg/11.20.2347.

    PubMed  CAS  Google Scholar 

  97. Eisenhofer G, et al. Malignant pheochromocytoma: current status and initiatives for future progress. Endocr Relat Cancer 11(3):423–36, 2004. doi:10.1677/erc.1.00829.

    PubMed  CAS  Google Scholar 

  98. Lloyd RV, et al. Immunohistochemical localization of epinephrine, norepinephrine, catecholamine-synthesizing enzymes, and chromogranin in neuroendocrine cells and tumors. Am J Pathol 125(1):45–54, 1986.

    PubMed  CAS  Google Scholar 

  99. Tischler AS, Kimura N, McNicol AM. Pathology of pheochromocytoma and extra-adrenal paraganglioma. Ann N Y Acad Sci 1073:557–70, 2006. doi:10.1196/annals.1353.059.

    PubMed  Google Scholar 

  100. Lee S, et al. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 8(2):155–67, 2005. doi:10.1016/j.ccr.2005.06.015.

    PubMed  Google Scholar 

  101. Jacks T, et al. Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat Genet 7(3):353–61, 1994. doi:10.1038/ng0794-353.

    PubMed  CAS  Google Scholar 

  102. Tischler AS, et al. Characterization of pheochromocytomas in a mouse strain with a targeted disruptive mutation of the neurofibromatosis gene Nf1. Endocr Pathol 6(4):323–35, 1995. doi:10.1007/BF02738732.

    PubMed  Google Scholar 

  103. Powers JF, et al. Pheochromocytomas in Nf1 knockout mice express a neural progenitor gene expression profile. Neuroscience 147(4):928–37, 2007. doi:10.1016/j.neuroscience.2007.05.008.

    PubMed  CAS  Google Scholar 

  104. Reilly KM, Van Dyke T. It takes a (dysfunctional) village to raise a tumor. Cell 135(3):408–10, 2008. doi:10.1016/j.cell.2008.10.009.

    PubMed  CAS  Google Scholar 

  105. Couto SS, Cardiff RD. The genomic revolution and endocrine pathology. Endocr Pathol 19(3):139–47, 2008. doi:10.1007/s12022-008-9042-2.

    PubMed  Google Scholar 

  106. Joseph NM, et al. The loss of Nf1 transiently promotes self-renewal but not tumorigenesis by neural crest stem cells. Cancer Cell 13(2):129–40, 2008. doi:10.1016/j.ccr.2008.01.003.

    PubMed  CAS  Google Scholar 

  107. Nakamura E, Kaelin WG Jr. Recent insights into the molecular pathogenesis of pheochromocytoma and paraganglioma. Endocr Pathol 17(2):97–106, 2006. doi:10.1385/EP:17:2:97.

    PubMed  CAS  Google Scholar 

  108. Hilfer SR. Cellular interactions in the genesis and maintenance of thyroid characteristics. In: Fleischmajer R, Billingham RE, editors. Epithelial–mesenchymal interactions. Baltimore: Williams and Wilkins Co.; 1968.

    Google Scholar 

  109. Pearse AG, Carvalheira AF. Cytochemical evidence for an ultimobranchial origin of rodent thyroid C cells. Nature 214(5091):929–30, 1967. doi:10.1038/214929a0.

    PubMed  CAS  Google Scholar 

  110. Fontaine J. Multistep migration of calcitonin cell precursors during ontogeny of the mouse pharynx. Gen Comp Endocrinol 37(1):81–92, 1979. doi:10.1016/0016-6480(79)90049-2.

    PubMed  CAS  Google Scholar 

  111. Biddinger PW, Ray M. Distribution of C cells in the normal and diseased thyroid gland. Pathol Annu 28(Pt 1):205–29, 1993.

    PubMed  Google Scholar 

  112. Manley NR, Capecchi MR. Hox group 3 paralogs regulate the development and migration of the thymus, thyroid, and parathyroid glands. Dev Biol 195(1):1–15, 1998. doi:10.1006/dbio.1997.8827.

    PubMed  CAS  Google Scholar 

  113. Di Lauro R, De Felice M. Thyroid gland: anatomy and development. In: DeGroot L, Jameson J, editors. Endocrinology. Philadelphia: Saunders; 2001.

    Google Scholar 

  114. Moseley JM, et al. The ultimobranchial origin of calcitonin. Lancet 1(7534):108–10, 1968. doi:10.1016/S0140-6736(68)92720-7.

    PubMed  CAS  Google Scholar 

  115. Pearse AG, Polak JM. Cytochemical evidence for the neural crest origin of mammalian ultimobranchial C cells. Histochemie 27(2):96–102, 1971. doi:10.1007/BF00284951.

    PubMed  CAS  Google Scholar 

  116. Williams ED, Toyn CE, Harach HR. The ultimobranchial gland and congenital thyroid abnormalities in man. J Pathol 159(2):135–41, 1989. doi:10.1002/path.1711590208.

    PubMed  CAS  Google Scholar 

  117. Williams ED. Diarrhoea and thyroid carcinoma. Proc R Soc Med 59(7):602–3, 1966.

    PubMed  CAS  Google Scholar 

  118. Williams ED. Histogenesis of medullary carcinoma of the thyroid. J Clin Pathol 19(2):114–18, 1966. doi:10.1136/jcp. 19.2.114.

    PubMed  CAS  Google Scholar 

  119. Al-Rawi M, Wheeler MH. Medullary thyroid carcinoma—update and present management controversies. Ann R Coll Surg Engl 88(5):433–8, 2006. doi:10.1308/003588406X117043.

    PubMed  Google Scholar 

  120. Agoff SN, et al. Thyroid transcription factor-1 is expressed in extrapulmonary small cell carcinomas but not in other extrapulmonary neuroendocrine tumors. Mod Pathol 13(3):238–42, 2000. doi:10.1038/modpathol.3880044.

    PubMed  CAS  Google Scholar 

  121. Pueblitz S, Weinberg AG, Albores-Saavedra J. Thyroid C cells in the DiGeorge anomaly: a quantitative study. Pediatr Pathol 13(4):463–73, 1993. doi:10.3109/15513819309048236.

    PubMed  CAS  Google Scholar 

  122. Kalhor N, Zander DS, Liu J. TTF-1 and p63 for distinguishing pulmonary small-cell carcinoma from poorly differentiated squamous cell carcinoma in previously pap-stained cytologic material. Mod Pathol 19(8):1117–23, 2006.

    PubMed  CAS  Google Scholar 

  123. Prok AL, Prayson RA. Thyroid transcription factor-1 staining is useful in identifying brain metastases of pulmonary origin. Ann Diagn Pathol 10(2):67–71, 2006. doi:10.1016/j.anndiagpath.2005.07.013.

    PubMed  Google Scholar 

  124. Al-Zahrani IH. The value of immunohistochemical expression of TTF-1, CK7 and CK20 in the diagnosis of primary and secondary lung carcinomas. Saudi Med J 29(7):957–61, 2008.

    PubMed  Google Scholar 

  125. Su YC, Hsu YC, Chai CY. Role of TTF-1, CK20, and CK7 immunohistochemistry for diagnosis of primary and secondary lung adenocarcinoma. Kaohsiung J Med Sci 22(1):14–19, 2006.

    PubMed  Google Scholar 

  126. Lin X, et al. Diagnostic value of CDX-2 and TTF-1 expressions in separating metastatic neuroendocrine neoplasms of unknown origin. Appl Immunohistochem Mol Morphol 15(4):407–14, 2007. doi:10.1097/01.pai.0000210416.53493.0f.

    PubMed  CAS  Google Scholar 

  127. Tsao SC, et al. Use of caveolin-1, thyroid transcription factor-1, and cytokeratins 7 and 20 in discriminating between primary and secondary pulmonary adenocarcinoma from breast or colonic origin. Kaohsiung J Med Sci 23(7):325–31, 2007.

    Article  PubMed  Google Scholar 

  128. Guazzi S, et al. Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity. EMBO J 9(11):3631–9, 1990.

    PubMed  CAS  Google Scholar 

  129. Mizuno K, Gonzalez FJ, Kimura S. Thyroid-specific enhancer-binding protein (T/EBP): cDNA cloning, functional characterization, and structural identity with thyroid transcription factor TTF-1. Mol Cell Biol 11(10):4927–33, 1991.

    PubMed  CAS  Google Scholar 

  130. Kikkawa F, Gonzalez FJ, Kimura S. Characterization of a thyroid-specific enhancer located 5.5 kilobase pairs upstream of the human thyroid peroxidase gene. Mol Cell Biol 10(12):6216–24, 1990.

    PubMed  CAS  Google Scholar 

  131. Kimura S, et al. The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10(1):60–9, 1996. doi:10.1101/gad.10.1.60.

    PubMed  CAS  Google Scholar 

  132. De Felice M, et al. A mouse model for hereditary thyroid dysgenesis and cleft palate. Nat Genet 19(4):395–8, 1998. doi:10.1038/1289.

    PubMed  Google Scholar 

  133. Mansouri A, Chowdhury K, Gruss P. Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet 19(1):87–90, 1998. doi:10.1038/ng0598-87.

    PubMed  CAS  Google Scholar 

  134. Damante G, Tell G, Di Lauro R. A unique combination of transcription factors controls differentiation of thyroid cells. Prog Nucleic Acid Res Mol Biol 66:307–56, 2001. doi:10.1016/S0079-6603(00)66033-6.

    PubMed  CAS  Google Scholar 

  135. De Felice M, Di Lauro R. Thyroid development and its disorders: genetics and molecular mechanisms. Endocr Rev 25(5):722–46, 2004. doi:10.1210/er.2003-0028.

    PubMed  Google Scholar 

  136. Lazzaro D, et al. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113(4):1093–104, 1991.

    PubMed  CAS  Google Scholar 

  137. Meunier D, Aubin J, Jeannotte L. Perturbed thyroid morphology and transient hypothyroidism symptoms in Hoxa5 mutant mice. Dev Dyn 227(3):367–78, 2003. doi:10.1002/dvdy.10325.

    PubMed  CAS  Google Scholar 

  138. Kusakabe T, Hoshi N, Kimura S. Origin of the ultimobranchial body cyst: T/ebp/Nkx2.1 expression is required for development and fusion of the ultimobranchial body to the thyroid. Dev Dyn 235(5):1300–9, 2006. doi:10.1002/dvdy.20655.

    PubMed  CAS  Google Scholar 

  139. Huntly BJ, Gilliland DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat Rev Cancer 5(4):311–21, 2005. doi:10.1038/nrc1592.

    PubMed  CAS  Google Scholar 

  140. Wang JC, Dick JE. Cancer stem cells: lessons from leukemia. Trends Cell Biol 15(9):494–501, 2005. doi:10.1016/j.tcb.2005.07.004.

    PubMed  CAS  Google Scholar 

  141. Song LL, Miele L. Cancer stem cells—an old idea that's new again: implications for the diagnosis and treatment of breast cancer. Expert Opin Biol Ther 7(4):431–8, 2007. doi:10.1517/14712598.7.4.431.

    PubMed  CAS  Google Scholar 

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  1. California Institute of Technology, Pasadena, CA, USA

    Meghan Sara Adams & Marianne Bronner-Fraser

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Adams, M.S., Bronner-Fraser, M. Review: The Role of Neural Crest Cells in the Endocrine System. Endocr Pathol 20, 92–100 (2009). https://doi.org/10.1007/s12022-009-9070-6

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