Sympathoadrenal neural crest cells: The known, unknown and forgotten?

Development Growth and Differentiation

Volumn 57, Issue 2, 2015, Pages 146-157

  Lumb, Rachael ^a,b   Schwarz, Quenten ^a  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Autonomic nervous system; Blood vessel; Migration; Neural crest; Sympathodrenal

Indexed keywords

ADRENAL MEDULLA; AUTONOMIC NERVOUS SYSTEM; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELLS BY BODY ANATOMY; CHROMAFFIN CELL; GANGLION; HUMAN; MOLECULAR MECHANICS; MORPHOGENESIS; MOUSE MODEL; NEURAL CREST CELL; NONHUMAN; REVIEW; SENSORY GANGLION; SIGNAL TRANSDUCTION; STEM CELL; SYMPATHETIC GANGLION; SYMPATHETIC TRUNK; TISSUE INTERACTION; ANIMAL; CELL MOTION; CHROMAFFIN SYSTEM; CYTOLOGY; EMBRYOLOGY; METABOLISM; MOUSE; NEURAL CREST; NEURAL STEM CELL; PHYSIOLOGY;

ANIMALS; CELL MOVEMENT; GANGLIA, SYMPATHETIC; HUMANS; MICE; NEURAL CREST; NEURAL STEM CELLS; PARA-AORTIC BODIES;

EID: 84923625570     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12189     Document Type: Review

References (72)

1. Adameyko, I., Lallemend, F., Aquino, J. B., Pereira, J. A., Topilko, P., Muller, T., Fritz, N., Beljajeva, A., Mochii, M., Liste, I., Usoskin, D., Suter, U., Birchmeier, C. & Ernfors, P. 2009. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139, 366-379.
2. Baroffio, A., Dupin, E. & Le Douarin, N. M. 1988. Clone-forming ability and differentiation potential of migratory neural crest cells. Proc. Natl Acad. Sci. USA 85, 5325-5329.
3. Belmadani, A., Tran, P. B., Ren, D., Assimacopoulos, S., Grove, E. A. & Miller, R. J. 2005. The chemokine stromal cell-derived factor-1 regulates the migration of sensory neuron progenitors. J. Neurosci. 25, 3995-4003.
4. Britsch, S., Goerich, D. E., Riethmacher, D., Peirano, R. I., Rossner, M., Nave, K.-A., Birchmeier, C. & Wegner, M. 1998. The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 12, 1825-1836.
5. Britsch, S., Li, L., Kirchhoff, S., Theuring, F., Brinkmann, V., Birchmeier, C. & Riethmacher, D. 2001. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 15, 66-78.
6. Brodeur, G. M. 2003. Neuroblastoma: biological insights into a clinical enigma. Nat. Rev. Cancer 3, 203-216.
7. Bronner-Fraser, M. & Fraser, S. E. 1988. Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335, 161-164.
8. Bronner-Fraser, M. & Fraser, S. 1989. Developmental potential of avian trunk neural crest cells in situ. Neuron 3, 755-766.
9. Bronner-Fraser, M., Sieber-Blum, M. & Cohen, A. M. 1980. Clonal analysis of the avian neural crest: migration and maturation of mixed neural crest clones injected into host chicken embryos. J. Comp. Neurol. 193, 423-434.
10. Burridge, K. & Fath, K. 1989. Focal contacts: transmembrane links between the extracellular matrix and the cytoskeleton. BioEssays 10, 104-108.
11. Cohen, A. M. & Konigsberg, I. R. 1975. A clonal approach to the problem of neural crest determination. Dev. Biol. 46, 262-280.
12. Cordero, D. R., Brugmann, S., Chu, Y., Bajpai, R., Jame, M. & Helms, J. A. 2010. Cranial neural crest cells on the move: their roles in craniofacial development. Am. J. Med. Genet. A 155A, 270-279.
13. Dyachuk, V., Furlan, A., Shahidi, M. K., Giovenco, M., Kaukua, N., Konstantinidou, C., Pachnis, V., Memic, F., Marklund, U., Muller, T., Birchmeier, C. & Fried, K. P. 2014. Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science 345, 82-87.
14. Enomoto, H., Crawford, P. A., Gorodinsky, A., Heuckeroth, R. O., Johnson, E. M. Jr & Milbrandt, J. 2001. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128, 3963-3974.
15. Erickson, C. A. & Goins, T. L. 1995. Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes. Development 121, 915-924.
16. Erickson, C. A., Duong, T. D. & Tosney, K. W. 1992. 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. 151, 251-272.
17. Ernsberger, U., Esposito, L., Partimo, S., Huber, K., Franke, A., Bixby, J., Kalcheim, C. & Unsicker, K. 2005. Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen. Cell Tissue Res. 319, 1-13.
18. Espinosa-Medina, I., Outin, E., Picard, C. A., Chettouh, Z., Dymecki, S., Consalez, G. G., Coppola, E. & Brunet, J. F. 2014. Neurodevelopment. Parasympathetic ganglia derive from Schwann cell precursors. Science 345, 87-90.
19. Fitch, S.R., Kimber, G.M., Wilson, N.K., Parker, A., Mirshekar-Syahkal, B., Göttgens, B., Medvinsky, A., Dzierzak, E. & Ottersbach, K. 2012. Signaling from the sympathetic nervous system regulates hematopoietic stem cell emergence during embryogenesis. Cell Stem Cell 11, 554-566.
20. Gammill, L. S., Gonzalez, C., Gu, C. & Bronner-Fraser, M. 2006. Guidance of trunk neural crest migration requires neuropilin 2/semaphorin 3F signaling. Development 133, 99-106.
21. George, L., Chaverra, M., Todd, V., Lansford, R. & Lefcort, F. 2007. Nociceptive sensory neurons derive from contralaterally migrating, fate-restricted neural crest cells. Nat. Neurosci. 10, 1287-1293.
22. Gut, P., Huber, K., Lohr, J., Bruhl, B., Oberle, S., Treier, M., Ernsberger, U., Kalcheim, C. & Unsicker, K. 2005. Lack of an adrenal cortex in Sf1 mutant mice is compatible with the generation and differentiation of chromaffin cells. Development 132, 4611-4619.
23. Harris, M. L., Hall, R. & Erickson, C. A. 2008. Directing pathfinding along the dorsolateral path - the role of EDNRB2 and EphB2 in overcoming inhibition. Development 135, 4113-4122.
24. Henion, P. D. & Weston, J. A. 1997. Timing and pattern of cell fate restrictions in the neural crest lineage. Development 124, 4351-4359.
25. Hong, S. J., Lardaro, T., Oh, M. S., Huh, Y., Ding, Y., Kang, U. J., Kirfel, J., Buettner, R. & Kim, K. S. 2008. Regulation of the noradrenaline neurotransmitter phenotype by the transcription factor AP-2beta. J. Biol. Chem. 283, 16860-16867.
26. Huber, K., Kalcheim, C. & Unsicker, K. 2009. The development of the chromaffin cell lineage from the neural crest. Auton Neurosci 151.
27. Ieda, M., Kanazawa, H., Kimura, K., Hattori, F., Ieda, Y., Taniguchi, M., Lee, J.-K., Matsumura, K., Tomita, Y., Miyoshi, S., Shimoda, K., Makino, S., Sano, M., Kodama, I., Ogawa, S. & Fukuda, K. 2007. Sema3a maintains normal heart rhythm through sympathetic innervation patterning. Nat. Med. 13, 604-612.
28. Jia, L., Cheng, L. & Raper, J. 2005. Slit/Robo signaling is necessary to confine early neural crest cells to the ventral migratory pathway in the trunk. Dev. Biol. 282, 411-421.
29. Kantorovich, V. & Pacak, K. 2010. Pheochromocytoma and paraganglioma. Prog. Brain Res. 182, 343-373.
30. Kasemeier-Kulesa, J. C., McLennan, R., Romine, M. H., Kulesa, P. M. & Lefcort, F. 2010. CXCR4 controls ventral migration of sympathetic precursor cells. J. Neurosci. 30, 13078-13088.
31. Kirby, M. L., McKenzie, J. W. & Weidman, T. A. 1980. Developing innervation of the chick heart: A histofluorescence and light microscopic study of sympathetic innervation. Anat. Rec. 196, 333-340.
32. Krispin, S., Nitzan, E., Kassem, Y. & Kalcheim, C. 2010. Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 137, 585-595.
33. Le Douarin, N. & Kalcheim, C. 1999. The Neural Crest, 2nd edn. Cambridge University Press, Cambridge.
34. Le Douarin, N. M., Creuzet, S., Couly, G. & Dupin, E. 2004. Neural crest cell plasticity and its limits. Development 131, 4637-4650.
35. Leke, R. J., Nasah, B. T. & Mtango, F. D. 1988. Introduction of high risk pregnancy care in rural Cameroon: health service research approach. J Obstet Gynaecol East Cent Africa. May;7(7):7-10.
36. Lim, K.-C., Lakshmanan, G., Crawford, S. E., Gu, Y., Grosveld, F. & Douglas Engel, J. 2000. Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat. Genet. 25, 209-212.
37. Lumb, R., Wiszniak, S., Kabbara, S., Scherer, M., Harvey, N. & Schwarz, Q. 2014. Neuropilins define distinct populations of neural crest cells. Neural Development 9: 24.
38. Ma, Q., Kintner, C. & Anderson, D. J. 1996. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87, 43-52.
39. Ma, Q., Kintner, C. & Anderson, D. J. 2012. NRP1 and NRP2 cooperate to regulate gangliogenesis, axon guidance and target innervation in the sympathetic nervous system. Dev. Biol. 369, 277-285.
40. Matsui, Y., Zsebo, K. M. & Hogan, B. L. 1990. Embryonic expression of a haematopoietic growth factor encoded by the Sl locus and the ligand for c-kit. Nature 347, 667-669.
41. McKinney, M. C., Fukatsu, K., Morrison, J., McLennan, R., Bronner, M. E. & Kulesa, P. M. 2013. Evidence for dynamic rearrangements but lack of fate or position restrictions in premigratory avian trunk neural crest. Development 140, 820-830.
42. Morikawa, Y., Zehir, A., Maska, E., Deng, C., Schneider, M. D., Mishina, Y. & Cserjesi, P. 2009. BMP signaling regulates sympathetic nervous system development through Smad4-dependent and -independent pathways. Development 136, 3575-3584.
43. Narkiewicz, K. & Somers, V. K. 1997. The sympathetic nervous system and obstructive sleep apnea: implications for hypertension. J. Hypertens. 15, 1613-1619.
44. Nitzan, E., Pfaltzgraff, E. R., Labosky, P. A. & Kalcheim, C. 2013. Neural crest and Schwann cell progenitor-derived melanocytes are two spatially segregated populations similarly regulated by Foxd3. Proc. Natl Acad. Sci. USA 110, 12709-12714.
45. Pandolfi, P. P., Roth, M. E., Karis, A., Leonard, M. W., Dzierzak, E., Grosveld, F. G., Engel, J. D. & Lindenbaum, M. H. 1995. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet. 11, 40-44.
46. Perez, S. E., Rebelo, S. & Anderson, D. J. 1999. Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126, 1715-1728.
47. Reedy, M. V., Faraco, C. D. & Erickson, C. A. 1998. Specification and migration of melanoblasts at the vagal level and in hyperpigmented Silkie chickens. Dev. Dyn. 213, 476-485.
48. Reiprich, S., Stolt, C. C., Schreiner, S., Parlato, R. & Wegner, M. 2008. SoxE proteins are differentially required in mouse Adrenal gland development. Mol. Biol. Cell 19, 1575-1586.
49. Roffers-Agarwal, J. & Gammill, L. S. 2009. Neuropilin receptors guide distinct phases of sensory and motor neuronal segmentation. Development 136, 1879-1888.
50. Roosen, A., Schober, A., Strelau, J., Bottner, M., Faulhaber, J., Bendner, G., McIlwrath, S. L., Seller, H., Ehmke, H., Lewin, G. R. & Unsicker, K. 2001. Lack of neurotrophin-4 causes selective structural and chemical deficits in sympathetic ganglia and their preganglionic innervation. J. Neurosci. 21, 3073-3084.
51. Ruhrberg, C. & Schwarz, Q. 2010. In the beginning: Generating neural crest cell diversity. Cell Adh. Migr. 4, 622-630.
52. Saito, D., Takase, Y., Murai, H. & Takahashi, Y. 2012. The dorsal aorta initiates a molecular cascade that instructs sympatho-adrenal specification. Science 336, 1578-1581.
53. Schmidt, M., Huber, L., Majdazari, A., Schutz, G., Williams, T. & Rohrer, H. 2011. The transcription factors AP-2beta and AP-2alpha are required for survival of sympathetic progenitors and differentiated sympathetic neurons. Dev. Biol. 355, 89-100.
54. Schneider, C., Wicht, H., Enderich, J., Wegner, M. & Rohrer, H. 1999. Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron 24, 861-870.
55. Schober, A., Parlato, R., Huber, K., Kinscherf, R., Hartleben, B., Huber, T. B., Schütz, G. & Unsicker, K. 2013. Cell loss and autophagy in the extra-adrenal chromaffin organ of Zuckerkandl are regulated by glucocorticoid signalling. J. Neuroendocrinol. 25, 34-47.
56. Schwarz, Q., Maden, C. H., Davidson, K. & Ruhrberg, C. 2009a. Neuropilin-mediated neural crest cell guidance is essential to organise sensory neurons into segmented dorsal root ganglia. Development 136, 1785-1789.
57. Schwarz, Q., Maden, C. H., Vieira, J. M. & Ruhrberg, C. 2009b. Neuropilin 1 signaling guides neural crest cells to coordinate pathway choice with cell specification. Proc. Natl Acad. Sci. USA 106, 6164-6169.
58. Serbedzija, G. N., Bronner-Fraser, M. & Fraser, S. E. 1989. A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. Development 106, 809-816.
59. Serbedzija, G. N., Fraser, S. E. & Bronner-Fraser, M. 1990. Pathways of trunk neural crest cell migration in the mouse embryo as revealed by vital dye labelling. Development 108, 605-612.
60. Shtukmaster, S., Schier, M. C., Huber, K., Krispin, S., Kalcheim, C. & Unsicker, K. 2013. Sympathetic neurons and chromaffin cells share a common progenitor in the neural crest in vivo. Neural Dev. 8, 12.
61. Sieber-Blum, M. & Cohen, A. M. 1980. Clonal analysis of quail neural crest cells: they are pluripotent and differentiate in vitro in the absence of noncrest cells. Dev. Biol. 80, 96-106.
62. Sommer, L., Ma, Q. & Anderson, D. J. 1996. Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell heterogeneity in the developing CNS and PNS. Mol. Cell Neurosci. 8, 221-241.
63. Stubbusch, J., Narasimhan, P., Huber, K., Unsicker, K., Rohrer, H. & Ernsberger, U. 2013. Synaptic protein and pan-neuronal gene expression and their regulation by Dicer-dependent mechanisms differ between neurons and neuroendocrine cells. Neural Dev. 8, 1-15.
64. Thomas, S. A., Matsumoto, A. M. & Palmiter, R. D. 1995. Noradrenaline is essential for mouse fetal development. Nature 374, 643-646.
65. Unsicker, K., Huber, K., Schober, A. & Kalcheim, C. 2013. Resolved and open issues in chromaffin cell development. Mech Dev 130: 324-9.
66. Wehrle-Haller, B. & Weston, J. A. 1995. Soluble and cell-bound forms of steel factor activity play distinct roles in melanocyte precursor dispersal and survival on the lateral neural crest migration pathway. Development 121, 731-742.
67. Wehrle-Haller, B., Meller, M. & Weston, J. A. 2001. Analysis of melanocyte precursors in Nf1 mutants reveals that MGF/KIT signaling promotes directed cell migration independent of its function in cell survival. Dev. Biol. 232, 471-483.
68. Weston, J. A. & Butler, S. L. 1966. Temporal factors affecting localization of neural crest cells in tbe chicken embryo. Dev. Biol. 14, 246-266.
69. Wilson, Y. M., Richards, K. L., Ford-Perriss, M. L., Panthier, J. J. & Murphy, M. 2004. Neural crest cell lineage segregation in the mouse neural tube. Development 131, 6153-6162.
70. Wiszniak, S., Kabbara, S., Lumb, R., Scherer, M., Secker, G., Harvey, N., Kumar, S. & Schwarz, Q. 2013. The ubiquitin ligase Nedd4 regulates craniofacial development by promoting cranial neural crest cell survival and stem-cell like properties. Dev Biol 383: 186-200.
71. Wilson, Y. M., Richards, K. L., Ford-Perriss, M. L., Panthier, J. J. & Murphy, M. 1995. Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374, 640-643.
72. Zirlinger, M., Lo, L., McMahon, J., McMahon, A. P. & Anderson, D. J. 2002. 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 99, 8084-8089.