Abstract
The sympathetic division of the autonomic nervous system includes a variety of cells including neurons, endocrine cells and glial cells. A recent study (Furlan et al. 2017) has revised thinking about the developmental origin of these cells. It now appears that sympathetic neurons and chromaffin cells of the adrenal medulla do not have an immediate common ancestor in the form a “sympathoadrenal cell”, as has been long believed. Instead, chromaffin cells arise from Schwann cell precursors. This review integrates the new findings with the expanding body of knowledge on the signalling pathways and transcription factors that regulate the origin of cells of the sympathetic division of the autonomic nervous system.
Similar content being viewed by others
References
Adameyko I, Lallemend F, Aquino JB, Pereira JA, 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
Ahmed AM (2017) Immunohistochemical study of sustentacular cells in adrenal medulla of neonatal and adult rats using an antibody against S-100 protein. Folia Morphol (Warsz) 76:246–251
Ahonen M, Soinila S, Joh TH (1987) Pre- and postnatal development of rat retroperitoneal paraganglia. J Auton Nerv Syst 18:111–120
Ajioka I, Martins RA, Bayazitov IT, Donovan S, Johnson DA, Frase S, Cicero SA, Boyd K, Zakharenko SS, Dyer MA (2007) Differentiated horizontal interneurons clonally expand to form metastatic retinoblastoma in mice. Cell 131:378–390
Alam G, Cui H, Shi H, Yang L, Ding J, Mao L, Maltese WA, Ding HF (2009) MYCN promotes the expansion of Phox2B-positive neuronal progenitors to drive neuroblastoma development. Am J Pathol 175:856–866
Allmendinger A, Stoeckel E, Saarma M, Unsicker K, Huber K (2003) Development of adrenal chromaffin cells is largely normal in mice lacking the receptor tyrosine kinase c-ret. Mech Dev 120:299–304
Anderson DJ, Axel R (1985) Molecular probes for the development and plasticity of neural crest derivatives. Cell 42:649–662
Anderson DJ, Axel R (1986) A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 47:1079–1090
Anderson DJ, Carnahan JF, Michelsohn A, Patterson PH (1991) 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 11:3507–3519
Andres R, Forgie A, Wyatt S, Chen Q, de Sauvage FJ, Davies AM (2001) Multiple effects of artemin on sympathetic neurone generation, survival and growth. Development 128:3685–3695
Apostolova G, Dechant G (2009) Development of neurotransmitter phenotypes in sympathetic neurons. Auton Neurosci 151:30–38
Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I, Calegari F, Huttner WB (2011) Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun 2:154
Armstrong A, Ryu YK, Chieco D, Kuruvilla R (2011) Frizzled3 Is required for neurogenesis and target innervation during sympathetic nervous system development. J Neurosci 31:2371–2381
Baggiolini A, Varum S, Mateos JM, Bettosini D, John N, Bonalli M, Ziegler U, Dimou L, Clevers H, Furrer R, Sommer L (2015) Premigratory and migratory neural crest cells are multipotent in vivo. Cell Stem Cell 16:314–322
Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J (2000) The GDNF family ligands and receptors - implications for neural development. Curr Opin Neurobiol 10:103–110
Baroffio A, Dupin E, Le Douarin NM (1988) Clone-forming ability and differentiation potential of migratory neural crest cells. Proc Natl Acad Sci U S A 85:5325–5329
Birchmeier C, Nave KA (2008) Neuregulin-1, a key axonal signal that drives Schwann cell growth and differentiation. Glia 56:1491–1497
Blomen VA, Boonstra J (2007) Cell fate determination during G1 phase progression. Cell Mol Life Sci 64:3084–3104
Bocian-Sobkowska J, Wozniak W, Malendowicz LK, Ginda W (1996) Stereology of human fetal adrenal medulla. Histol Histopathol 11:389–393
Bodmer D, Levine-Wilkinson S, Richmond A, Hirsh S, Kuruvilla R (2009) Wnt5a Mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons. J Neurosci 29:7569–7581
Britsch S, Li L, Kirchhoff S, Theuring F, Brinkmann V, Birchmeier C, Riethmacher D (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
Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, Nave KA, Birchmeier C, Wegner M (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15:66–78
Bronner-Fraser M (1986) Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1. Dev Biol 115:44–55
Bronner-Fraser M, Fraser SE (1988) Cell lineage analysis reveals multipotency of some avian neural crest cells. Nature 335:161–164
Bronner-Fraser M, Fraser S (1989) Developmental potential of avian trunk neural crest cells in situ. Neuron 3:755–766
Brunet I, Gordon E, Han J, Cristofaro B, Broqueres-You D, Liu C, Bouvree K, Zhang J, del Toro R, Mathivet T, Larrivee B, Jagu J, Pibouin-Fragner L, Pardanaud L, Machado MJ, Kennedy TE, Zhuang Z, Simons M, Levy BI, Tessier-Lavigne M, Grenz A, Eltzschig H, Eichmann A (2014) Netrin-1 controls sympathetic arterial innervation. J Clin Invest 124:3230–3240
Buchmann-Moller S, Miescher I, John N, Krishnan J, Deng CX, Sommer L (2009) Multiple lineage-specific roles of Smad4 during neural crest development. Dev Biol 330:329–338
Burstyn-Cohen T, Kalcheim C (2002) Association between the cell cycle and neural crest delamination through specific regulation of G1/S transition. Dev Cell 3:383–395
Cacalano G, Farinas I, Wang LC, Hagler K, Forgie A, Moore M, Armanini M, Phillips H, Ryan AM, Reichardt LF, Hynes M, Davies A, Rosenthal A (1998) GFRalpha1 Is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21:53–62
Calder A, Roth-Albin I, Bhatia S, Pilquil C, Lee JH, Bhatia M, Levadoux-Martin M, McNicol J, Russell J, Collins T, Draper JS (2013) Lengthened G1 phase indicates differentiation status in human embryonic stem cells. Stem Cells Dev 22:279–295
Callahan T, Young HM, Anderson RB, Enomoto H, Anderson CR (2008) Development of satellite glia in mouse sympathetic ganglia: GDNF and GFR alpha 1 are not essential. Glia 56:1428–1437
Cameron-Curry P, Dulac C, Le Douarin NM (1993) Negative regulation of Schwann cell myelin protein gene expression by the dorsal root ganglionic microenvironment. Eur J Neurosci 5:594–604
Cane KN, Anderson CR (2009) Generating diversity: mechanisms regulating the differentiation of autonomic neuron phenotypes. Auton Neurosci 151:17–29
Castro DS, Martynoga B, Parras C, Ramesh V, Pacary E, Johnston C, Drechsel D, Lebel-Potter M, Garcia LG, Hunt C, Dolle D, Bithell A, Ettwiller L, Buckley N, Guillemot F (2011) A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev 25:930–945
Chan WH, Gonsalvez DG, Young HM, Southard-Smith EM, Cane KN, Anderson CR (2016a) Differences in CART expression and cell cycle behavior discriminate sympathetic neuroblast from chromaffin cell lineages in mouse sympathoadrenal cells. Dev Neurobiol 76:137–149
Chan WH, Stamp LA, Hirst CS, McKeown SJ, Anderson CR, Young HM (2016b) Development of the autonomic nervous system. Rev Cell Biol Mol Med. https://doi.org/10.1002/3527600906.mcb.201600018
Cheung M, Chaboissier MC, Mynett A, Hirst E, Schedl A, Briscoe J (2005) The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8:179–192
Chubb DP, Anderson CR (2010) The relationship of the birth date of rat sympathetic neurons to the target they innervate. Dev Dyn 239:897–904
Coppola E, Pattyn A, Guthrie SC, Goridis C, Studer M (2005) Reciprocal gene replacements reveal unique functions for Phox2 genes during neural differentiation. EMBO J 24:4392–4403
Coppola E, d’Autreaux F, Rijli FM, Brunet JF (2010) Ongoing roles of Phox2 homeodomain transcription factors during neuronal differentiation. Development 137:4211–4220
Corpening JC, Cantrell VA, Deal KK, Southard-Smith EM (2008) A Histone 2BCerulean BAC transgene identifies differential expression of Phox2b in migrating enteric neural crest derivatives and enteric glia. Dev Dyn 237:1119–1132
Coupland RE (1954) Post-natal fate of the abdominal para-aortic bodies in man. J Anat 88:455–464
Coupland R, Weakley B (1970) Electron microscopic observations on the adrenal medulla and extra adrenal chromaffin tissue of the postnatal rabbit. J Anat 106:213–231
Coupland RE, Kent C, Kent SE (1982) Normal function of extra-adrenal chromaffin tissues in the young rabbit and guinea-pig. J Endocrinol 92:433–442
Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Mirsky R, Jessen KR (1995) Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15:585–596
Doupe AJ, Landis SC, Patterson PH (1985) Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J Neurosci 5:2119–2142
Dulac C, Cameron-Curry P, Ziller C, Le Douarin NM (1988) A surface protein expressed by avian myelinating and nonmyelinating Schwann cells but not by satellite or enteric glial cells. Neuron 1:211–220
Dupin E, Le Douarin NM (2014) The neural crest, a multifaceted structure of the vertebrates. Birth Defects Res C 102:187–209
Dupin E, Calloni GW, Le Douarin NM (2010) The cephalic neural crest of amniote vertebrates is composed of a large majority of precursors endowed with neural, melanocytic, chondrogenic and osteogenic potentialities. Cell Cycle 9:238–249
Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M et al (1996) GDNF signalling through the ret receptor tyrosine kinase. Nature 381:789–793
Dyachuk V, Furlan A, Shahidi MK, Giovenco M, Kaukua N, Konstantinidou C, Pachnis V, Memic F, Marklund U, Muller T, Birchmeier C, Fried K, Ernfors P, Adameyko I (2014) Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science 345:82–87
El-Maghraby M, Lever JD (1980) Typification and differentiation of medullary cells in the developing rat adrenal. A histochemical and electron microscopic study. J Anat 131:103–120
Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM Jr, Milbrandt J (1998) GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317–324
Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM Jr, Milbrandt J (2001) RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128:3963–3974
Eränkö O (1955) Distribution of adrenaline and noradrenaline in the adrenal medulla. Nature 175:88–89
Erickson CA, Goins TL (1995) Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes. Development 121:915–924
Ernsberger U, Rohrer H (2009) Development of the autonomic nervous system: new perspectives and open questions. Auton Neurosci 151:1–2
Ernsberger U, Patzke H, Tissier-Seta JP, Reh T, Goridis C, Rohrer H (1995) The expression of tyrosine hydroxylase and the transcription factors cPhox-2 and Cash-1: evidence for distinct inductive steps in the differentiation of chick sympathetic precursor cells. Mech Dev 52:125–136
Ernsberger U, Esposito L, Partimo S, Huber K, Franke A, Bixby JL, 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
Espinosa-Medina I, Outin E, Picard CA, Chettouh Z, Dymecki S, Consalez GG, Coppola E, Brunet JF (2014) Neurodevelopment. Parasympathetic ganglia derive from Schwann cell precursors. Science 345:87–90
Finotto S, Krieglstein K, Schober A, Deimling F, Lindner K, Bruhl B, Beier K, Metz J, Garcia-Arraras JE, Roig-Lopez JL, Monaghan P, Schmid W, Cole TJ, Kellendonk C, Tronche F, Schutz G, Unsicker K (1999) Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. Development 126:2935–2944
Fortuna V, Pardanaud L, Brunet I, Ola R, Ristori E, Santoro MM, Nicoli S, Eichmann A (2015) Vascular mural cells promote noradrenergic differentiation of embryonic sympathetic neurons. Cell Rep 11:1786–1796
Frank E, Sanes JR (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development 111:895–908
Furlan A, Dyachuk V, Kastriti ME, Calvo-Enrique L, Abdo H, Hadjab S, Chontorotzea T, Akkuratova N, Usoskin D, Kamenev D, Petersen J, Sunadome K, Memic F, Marklund U, Fried K, Topilko P, Lallemend F, Kharchenko PV, Ernfors P, Adameyko I (2017) Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. Science 357. https://doi.org/10.1126/science.aal3753
Glebova NO, Ginty DD (2004) Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J Neurosci 24:743–751
Gonsalvez DG, Cane KN, Landman KA, Enomoto H, Young HM, Anderson CR (2013) Proliferation and cell cycle dynamics in the developing stellate ganglion. J Neurosci 33:5969–5979
Gonsalvez DG, Li-Yuen-Fong M, Cane KN, Stamp LA, Young HM, Anderson CR (2015) Different neural crest populations exhibit diverse proliferative behaviors. Dev Neurobiol 75:287–301
Granholm AC, Srivastava N, Mott JL, Henry S, Henry M, Westphal H, Pichel JG, Shen L, Hoffer BJ (1997) Morphological alterations in the peripheral and central nervous systems of mice lacking glial cell line-derived neurotrophic factor (GDNF): immunohistochemical studies. J Neurosci 17:1168–1178
Groves AK, George KM, Tissier-Seta JP, Engel JD, Brunet JF, Anderson DJ (1995) Differential regulation of transcription factor gene expression and phenotypic markers in developing sympathetic neurons. Development 121:887–901
Guillemot F, Joyner AL (1993) Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech Dev 42:171–185
Guin GH, Gilbert EF, Jones B (1969) Incidental neuroblastoma in infants. Am J Clin Pathol 51:126–136
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
Hagedorn L, Suter U, Sommer L (1999) P0 And PMP22 mark a multipotent neural crest-derived cell type that displays community effects in response to TGF-beta family factors. Development 126:3781–3794
Hagedorn L, Paratore C, Brugnoli G, Baert JL, Mercader N, Suter U, Sommer L (2000) The Ets domain transcription factor Erm distinguishes rat satellite glia from Schwann cells and is regulated in satellite cells by neuregulin signaling. Dev Biol 219:44–58
Hanani M (2010) Satellite glial cells in sympathetic and parasympathetic ganglia: in search of function. Brain Res Rev 64:304–327
Hansford LM, Thomas WD, Keating JM, Burkhart CA, Peaston AE, Norris MD, Haber M, Armati PJ, Weiss WA, Marshall GM (2004) Mechanisms of embryonal tumor initiation: distinct roles for MycN expression and MYCN amplification. Proc Natl Acad Sci U S A 101:12664–12669
Hendershot TJ, Liu H, Clouthier DE, Shepherd IT, Coppola E, Studer M, Firulli AB, Pittman DL, Howard MJ (2008) Conditional deletion of Hand2 reveals critical functions in neurogenesis and cell type-specific gene expression for development of neural crest-derived noradrenergic sympathetic ganglion neurons. Dev Biol 319:179–191
Henion PD, Weston JA (1997) Timing and pattern of cell fate restrictions in the neural crest lineage. Development 124:4351–4359
Hervonen A, Korkala O (1972) The effect of hypoxia on the catecholamine content of human fetal abdominal paraganglia and adrenal medulla. Acta Obstet Gynecol Scand 51:17–24
Hervonen A, Korkala O (1973) Effect of hypoxia on the fine structure of the catecholamine-storing cells of the human fetal paraganglia. Virchows Arch B 13:341–349
Hirsch MR, Tiveron MC, Guillemot F, Brunet JF, Goridis C (1998) Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125:599–608
Hjerling-Leffler J, Marmigere F, Heglind M, Cederberg A, Koltzenburg M, Enerback S, Ernfors P (2005) The boundary cap: a source of neural crest stem cells that generate multiple sensory neuron subtypes. Development 132:2623–2632
Holzmann J, Hennchen M, Rohrer H (2015) Prox1 Identifies proliferating neuroblasts and nascent neurons during neurogenesis in sympathetic ganglia. Dev Neurobiol 75:1352–1367
Hong CS, Saint-Jeannet JP (2005) Sox proteins and neural crest development. Semin Cell Dev Biol 16:694–703
Hong SJ, Huh YH, Leung A, Choi HJ, Ding Y, Kang UJ, Yoo SH, Buettner R, Kim K-S (2011) Transcription factor AP-2β regulates the neurotransmitter phenotype and maturation of chromaffin cells. Mol Cell Neurosci 46:245–251
Honma Y, Araki T, Gianino S, Bruce A, Heuckeroth R, Johnson E, Milbrandt J (2002) Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 35:267–282
Howard MJ (2005) Mechanisms and perspectives on differentiation of autonomic neurons. Dev Biol 277:271–286
Howard MJ, Stanke M, Schneider C, Wu X, Rohrer H (2000) The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 127:4073–4081
Huber K (2006) The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev Biol 298:335–343
Huber K, Brühl B, Guillemot F, Olson EN, Ernsberger U, Unsicker K (2002a) Development of chromaffin cells depends on MASH1 function. Development 129:4729–4738
Huber K, Combs S, Ernsberger U, Kalcheim C, Unsicker K (2002b) Generation of neuroendocrine chromaffin cells from sympathoadrenal progenitors: beyond the glucocorticoid hypothesis. Ann N Y Acad Sci 971:554–559
Huber K, Karch N, Ernsberger U, Goridis C, Unsicker K (2005) The role of Phox2B in chromaffin cell development. Dev Biol 279:501–508
Huber K, Kalcheim C, Unsicker K (2009) The development of the chromaffin cell lineage from the neural crest. Auton Neurosci 151:10–16
Huber K, Narasimhan P, Shtukmaster S, Pfeifer D, Evans SM, Sun Y (2013) The LIM-Homeodomain transcription factor Islet-1 is required for the development of sympathetic neurons and adrenal chromaffin cells. Dev Biol 380:286–298
Ikeda Y, Lister J, Bouton JM, Buyukpamukcu M (1981) Congenital neuroblastoma, neuroblastoma in situ, and the normal fetal development of the adrenal. J Pediatr Surg 16:636–644
Jacob C (2015) Transcriptional control of neural crest specification into peripheral glia. Glia 63:1883–1896
Jänig W (1989) Autonomic nervous system. In: Schmidt RF, Thews G (eds) Human physiology. Springer, Berlin, pp 333–370
Janoueix-Lerosey I, Lequin D, Brugieres L, Ribeiro A, de Pontual L, Combaret V, Raynal V, Puisieux A, Schleiermacher G, Pierron G, Valteau-Couanet D, Frebourg T, Michon J, Lyonnet S, Amiel J, Delattre O (2008) Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 455:967–970
Jessen KR, Mirsky R, Lloyd AC (2015) Schwann cells: development and role in nerve repair. Cold Spring Harb Perspect Biol 7:a020487
Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA, Dormand EL, Lee KF, Meijer D, Anderson DJ, Morrison SJ (2004) Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131:5599–5612
Kahane N, Kalcheim C (1998) Identification of early postmitotic cells in distinct embryonic sites and their possible roles in morphogenesis. Cell Tissue Res 294:297–307
Kameda Y (2007) Expression of glial progenitor markers p75NTR and S100 protein in the developing mouse parathyroid gland. Cell Tissue Res 327:15–23
Kameda Y (2014) Signaling molecules and transcription factors involved in the development of the sympathetic nervous system, with special emphasis on the superior cervical ganglion. Cell Tissue Res 357:527–548
Kannan CR (1986) Anatomy of the adrenal glands. In: Kannan CR (ed) Essential endocrinology: a primer for nonspecialists. Springer, New York, pp 233–234
Kasemeier-Kulesa JC, McLennan R, Romine MH, Kulesa PM, Lefcort F (2010) CXCR4 Controls ventral migration of sympathetic precursor cells. J Neurosci 30:13078–13088
Kaukua N, Shahidi MK, Konstantinidou C, Dyachuk V, Kaucka M, Furlan A, An Z, Wang L, Hultman I, Ahrlund-Richter L, Blom H, Brismar H, Lopes NA, Pachnis V, Suter U, Clevers H, Thesleff I, Sharpe P, Ernfors P, Fried K, Adameyko I (2014) Glial origin of mesenchymal stem cells in a tooth model system. Nature 513:551–554
Kawasaki T, Bekku Y, Suto F, Kitsukawa T, Taniguchi M, Nagatsu I, Nagatsu T, Itoh K, Yagi T, Fujisawa H (2002) Requirement of neuropilin 1-mediated Sema3A signals in patterning of the sympathetic nervous system. Development 129:671–680
Kelsh RN (2006) Sorting out Sox10 functions in neural crest development. BioEssays 28:788–798
Kerosuo L, Bronner-Fraser M (2012) What is bad in cancer is good in the embryo: importance of EMT in neural crest development. Semin Cell Dev Biol 23:320–332
Kim J, Lo L, Dormand E, Anderson DJ (2003) SOX10 Maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38:17–31
Kim CH, Pennisi P, Zhao H, Yakar S, Kaufman JB, Iganaki K, Shiloach J, Scherer PE, Quon MJ, LeRoith D (2006) MKR mice are resistant to the metabolic actions of both insulin and adiponectin: discordance between insulin resistance and adiponectin responsiveness. Am J Physiol Endocrinol Metab 291:E298–E305
Kos R, Reedy MV, Johnson RL, Erickson CA (2001) The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 128:1467–1479
Krispin S, Nitzan E, Kalcheim C (2010a) The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 70:796–812
Krispin S, Nitzan E, Kassem Y, Kalcheim C (2010b) Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 137:585–595
Kuhlbrodt K, Herbarth B, Sock E, Hermans-Borgmeyer I, Wegner M (1998) Sox10, A novel transcriptional modulator in glial cells. J Neurosci 18:237–250
Kurtz A, Zimmer A, Schnutgen F, Bruning G, Spener F, Muller T (1994) The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 120:2637–2649
Landis SC, Patterson PH (1981) Neural crest cell lineages. Trends Neurosci 4:172–175
Langman J, Guerrant RL, Freeman BG (1966) Behavior of neuro-epithelial cells during closure of the neural tube. J Comp Neurol 127:399–411
Lawson SN, Biscoe TJ (1979) Development of mouse dorsal root ganglia: an autoradiographic and quantitative study. J Neurocytol 8:265–274
Le Douarin NM, Kalcheim C (1999) The neural crest. Cambridge University Press, Cambridge
Le Douarin N, Teillet MA (1971) Localization, by the method of interspecific grafts of the neural area from which adrenal cells arise in the bird embryo. C R Acad Sci Hebd Seances Acad Sci D 272:481–484
Le Douarin NM, Teillet MA (1973) The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morpholog 30:31–48
Le Douarin N, Dulac C, Dupin E, Cameron-Curry P (1991) Glial cell lineages in the neural crest. Glia 4:175–184
Le Douarin NM, Calloni GW, Dupin E (2008) The stem cells of the neural crest. Cell Cycle 7:1013–1019
Levi-Montalcini R (1976) The nerve growth factor: its role in growth, differentiation and function of the sympathetic adrenergic neuron. Prog Brain Res 45:235–258
Lim J, Thiery JP (2012) Epithelial-mesenchymal transitions: insights from development. Development 139:3471–3486
Lim KC, Lakshmanan G, Crawford SE, Gu Y, Grosveld F, Engel JD (2000) Gata3 Loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat Genet 25:209–212
Lo L, Tiveron MC, Anderson DJ (1998) MASH1 Activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125:609–620
Lohr J, Gut P, Karch N, Unsicker K, Huber K (2006) Development of adrenal chromaffin cells in Sf1 heterozygous mice. Cell Tissue Res 325:437–444
Lucas ME, Muller F, Rudiger R, Henion PD, Rohrer H (2006) The bHLH transcription factor hand2 is essential for noradrenergic differentiation of sympathetic neurons. Development 133:4015–4024
Lumb R, Wiszniak S, Kabbara S, Scherer M, Harvey N, Schwarz Q (2014) Neuropilins define distinct populations of neural crest cells. Neural Dev 9:24
Luo XR, Ikeda YY, Parker KL (1994) A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual-differentiation. Cell 77:481–490
Luo R, Gao J, Wehrle-Haller B, Henion PD (2003) Molecular identification of distinct neurogenic and melanogenic neural crest sublineages. Development 130:321–330
Ma Q, Kintner C, Anderson DJ (1996) Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87:43–52
Mac Auley A, Werb Z, Mirkes PE (1993) Characterization of the unusually rapid cell cycles during rat gastrulation. Development 117:873–883
Maden CH, Gomes J, Schwarz Q, Davidson K, Tinker A, Ruhrberg C (2012) NRP1 And NRP2 cooperate to regulate gangliogenesis, axon guidance and target innervation in the sympathetic nervous system. Dev Biol 369:277–285
Makita T, Sucov HM, Gariepy CE, Yanagisawa M, Ginty DD (2008) Endothelins are vascular-derived axonal guidance cues for developing sympathetic neurons. Nature 452:759–763
Manousiouthakis E, Mendez M, Garner MC, Exertier P, Makita T (2014) Venous endothelin guides sympathetic innervation of the developing mouse heart. Nat Commun 5:3918
Maro GS, Vermeren M, Voiculescu O, Melton L, Cohen J, Charnay P, Topilko P (2004) Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat Neurosci 7:930–938
Mascorro JA, Yates RD (1971) Ultrastructural studies of the effects of reserpine on mouse abdominal sympathetic paraganglia. Anat Rec 170:269–279
Mascorro JA, Yates RD (1974) Innervation of abdominal paraganglia: an ultrastructural study. J Morphol 142:153–163
Mascorro JA, Yates RD (1977) The anatomical distribution and morphology of extraadrenal chromaffin tissue (abdominal paraganglia) in the dog. Tissue Cell 9:447–460
Mascorro JA, Breaux TF, Yates RD (1994) Morphological observations of small granule-containing (chromaffin) cells in the celiac ganglion of the guinea pig, with emphasis on cell contacts. Microsc Res Tech 29:169–176
Mayanil CS (2013) Transcriptional and epigenetic regulation of neural crest induction during neurulation. Dev Neurosci 35:361–372
McKinney MC, Fukatsu K, Morrison J, McLennan R, Bronner ME, Kulesa PM (2013) Evidence for dynamic rearrangements but lack of fate or position restrictions in premigratory avian trunk neural crest. Development 140:820–830
McNicol AM (2004) Adrenal Medulla and Paraganglia. Humana, New York, pp 227–243
McPherson CE, Varley JE, Maxwell GD (2000) Expression and regulation of type I BMP receptors during early avian sympathetic ganglion development. Dev Biol 221:220–232
Mitchell PJ, Timmons PM, Hebert JM, Rigby PW, Tjian R (1991) Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis. Genes Dev 5:105–119
Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76–79
Moriguchi T, Takako N, Hamada M, Maeda A, Fujioka Y, Kuroha T, Huber RE, Hasegawa SL, Rao A, Yamamoto M, Takahashi S, Lim KC, Engel JD (2006) Gata3 Participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation. Development 133:3871–3881
Morikawa Y, D’Autreaux F, Gershon MD, Cserjesi P (2007) Hand2 Determines the noradrenergic phenotype in the mouse sympathetic nervous system. Dev Biol 307:114–126
Morikawa Y, Zehir A, Maska E, Deng C, Schneider MD, Mishina Y, Cserjesi P (2009) BMP signaling regulates sympathetic nervous system development through Smad4-dependent and -independent pathways. Development 136:3575–3584
Moser M, Ruschoff J, Buettner R (1997) Comparative analysis of AP-2 alpha and AP-2 beta gene expression during murine embryogenesis. Dev Dyn 208:115–124
Muñoz WA, Trainor PA (2015) Neural crest cell evolution: how and when did a neural crest cell become a neural crest cell. In: Paul AT (ed) Current topics in developmental biology, vol 111. Academic, Cambridge, pp 3–26
Murphy P, Topilko P, Schneider-Maunoury S, Seitanidou T, Baron-Van Evercooren A, Charnay P (1996) The regulation of Krox-20 expression reveals important steps in the control of peripheral glial cell development. Development 122:2847–2857
Newbern JM (2015) Molecular control of the neural crest and peripheral nervous system development. In: Paul AT (ed) Current topics in developmental biology, vol 111. Academic, Cambridge, pp 201–231
Nishino J, Saunders TL, Sagane K, Morrison SJ (2010) Lgi4 Promotes the proliferation and differentiation of glial lineage cells throughout the developing peripheral nervous system. J Neurosci 30:15228–15240
Nitzan E, Pfaltzgraff ER, Labosky PA, Kalcheim C (2013) Neural crest and Schwann cell progenitor-derived melanocytes are two spatially segregated populations similarly regulated by Foxd3. Proc Natl Acad Sci U S A 110:12709–12714
Noisa P, Raivio T (2014) Neural crest cells: from developmental biology to clinical interventions. Birth Defects Res C 102:263–274
Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311–318
Nowakowski RS, Caviness VS Jr, Takahashi T, Hayes NL (2002) Population dynamics during cell proliferation and neuronogenesis in the developing murine neocortex. Results Probl Cell Differ 39:1–25
Orford KW, Scadden DT (2008) Deconstructing stem cell self-renewal: genetic insights into cell-cycle regulation. Nat Rev Genet 9:115–128
Ozkaynak E, Abello G, Jaegle M, van Berge L, Hamer D, Kegel L, Driegen S, Sagane K, Bermingham JR Jr, Meijer D (2010) Adam22 Is a major neuronal receptor for Lgi4-mediated Schwann cell signaling. J Neurosci 30:3857–3864
Pakkarato S, Chomphoo S, Kagawa Y, Owada Y, Mothong W, Iamsaard S, Sawatpanich T, Kondo H, Hipkaeo W (2015) Immunohistochemical analysis of sustentacular cells in the adrenal medulla, carotid body and sympathetic ganglion of mice using an antibody against brain-type fatty acid binding protein (B-FABP). J Anat 226:348–353
Paratore C, Goerich DE, Suter U, Wegner M, Sommer L (2001) Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128:3949–3961
Partanen M, Linnoila I, Hervonent A, Rapoport SI (1984a) The effect of aging on extra-adrenal catecholamine storing cells of the rat. Neurobiol Aging 5:105–110
Partanen M, Rapoport SI, Reis DJ, Joh TH, Stolk JM, Linnoila I, Teitelman G, Hervonen A (1984b) Catecholamine-synthesizing enzymes in paraganglia of aged Fischer-344 rats. Immunohistochemistry and fluorescence microscopy. Cell Tissue Res 238:217–220
Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF (1999) The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366–370
Pattyn A, Guillemot F, Brunet JF (2006) Delays in neuronal differentiation in Mash1/Ascl1 mutants. Dev Biol 295:67–75
Perez SE, Rebelo S, Anderson DJ (1999) Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126:1715–1728
Pfeuty B, David-Pfeuty T, Kaneko K (2008) Underlying principles of cell fate determination during G1 phase of the mammalian cell cycle. Cell Cycle 7:3246–3257
Potzner MR, Tsarovina K, Binder E, Penzo-Mendez A, Lefebvre V, Rohrer H, Wegner M, Sock E (2010) Sequential requirement of Sox4 and Sox11 during development of the sympathetic nervous system. Development 137:775–784
Raible DW, Eisen JS (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120:495–503
Raposo AA, Vasconcelos FF, Drechsel D, Marie C, Johnston C, Dolle D, Bithell A, Gillotin S, van den Berg DL, Ettwiller L, Flicek P, Crawford GE, Parras CM, Berninger B, Buckley NJ, Guillemot F, Castro DS (2015) Ascl1 Coordinately regulates gene expression and the chromatin landscape during neurogenesis. Cell Rep 10:1544–1556
Reid K, Nishikawa S, Bartlett PF, Murphy M (1995) Steel factor directs melanocyte development in vitro through selective regulation of the number of c-kit+ progenitors. Dev Biol 169:568–579
Reiff T, Tsarovina K, Majdazari A, Schmidt M, del Pino I, Rohrer H (2010) Neuroblastoma phox2b variants stimulate proliferation and dedifferentiation of immature sympathetic neurons. J Neurosci 30:905–915
Reiff T, Huber L, Kramer M, Delattre O, Janoueix-Lerosey I, Rohrer H (2011) Midkine and Alk signaling in sympathetic neuron proliferation and neuroblastoma predisposition. Development 138:4699–4708
Reissmann E, Ernsberger U, Francis-West PH, Rueger D, Brickell PM, Rohrer H (1996) Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development 122:2079–2088
Rickmann M, Fawcett JW, Keynes RJ (1985) The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol 90:437–455
Ridenour DA, McLennan R, Teddy JM, Semerad CL, Haug JS, Kulesa PM (2014) The neural crest cell cycle is related to phases of migration in the head. Development 141:1095–1103
Rodriguez H, Filippa V, Mohamed F, Dominguez S, Scardapane L (2007) Interaction between chromaffin and sustentacular cells in adrenal medulla of viscacha (Lagostomus Maximus Maximus). Anat Histol Embryol 36:182–185
Rohrer H (2011) Transcriptional control of differentiation and neurogenesis in autonomic ganglia. Eur J Neurosci 34:1563–1573
Rohrer H, Thoenen H (1987) Relationship between differentiation and terminal mitosis: chick sensory and ciliary neurons differentiate after terminal mitosis of precursor cells, whereas sympathetic neurons continue to divide after differentiation. J Neurosci 7:3739–3748
Rothman TP, Gershon MD, Holtzer H (1978) The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev Biol 65:322–341
Rubin de Celis MF, Garcia-Martin R, Wittig D, Valencia GD, Enikolopov G, Funk RH, Chavakis T, Bornstein SR, Androutsellis-Theotokis A, Ehrhart-Bornstein M (2015) Multipotent glia-like stem cells mediate stress adaptation. Stem Cells 33:2037–2051
Ruiz S, Panopoulos AD, Herrerias A, Bissig KD, Lutz M, Berggren WT, Verma IM, Izpisua Belmonte JC (2011) A high proliferation rate is required for cell reprogramming and maintenance of human embryonic stem cell identity. Curr Biol 21:45–52
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
Salomoni P, Calegari F (2010) Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 20:233–243
Santana MM, Chung KF, Vukicevic V, Rosmaninho-Salgado J, Kanczkowski W, Cortez V, Hackmann K, Bastos CA, Mota A, Schrock E, Bornstein SR, Cavadas C, Ehrhart-Bornstein M (2012) Isolation, characterization, and differentiation of progenitor cells from human adult adrenal medulla. Stem Cells Transl Med 1:783–791
Sauka-Spengler T, Bronner-Fraser M (2006) Development and evolution of the migratory neural crest: a gene regulatory perspective. Curr Opin Genet Dev 16:360–366
Saxena S, Wahl J, Huber-Lang MS, Stadel D, Braubach P, Debatin KM, Beltinger C (2013) Generation of murine sympathoadrenergic progenitor-like cells from embryonic stem cells and postnatal adrenal glands. PLoS ONE 8:e64454
Schilling TF, Kimmel CB (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120:483–494
Schmidt M, Lin S, Pape M, Ernsberger U, Stanke M, Kobayashi K, Howard MJ, Rohrer H (2009) The bHLH transcription factor Hand2 is essential for the maintenance of noradrenergic properties in differentiated sympathetic neurons. Dev Biol 329:191–200
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
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
Schober A, Parlato R, Huber K, Kinscherf R, Hartleben B, Huber TB, Schutz 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
Schwarz Q, Ruhrberg C (2010) Neuropilin, you gotta let me know: should I stay or should I go? Cell Adhes Migr 4:61–66
Schwarz Q, Maden CH, 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
Schwarz Q, Maden CH, Vieira JM, Ruhrberg C (2009b) Neuropilin 1 signaling guides neural crest cells to coordinate pathway choice with cell specification. Proc Natl Acad Sci U S A 106:6164–6169
Serbedzija GN, Bronner-Fraser M, Fraser SE (1989) A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. Development 106:809–816
Serbedzija GN, Fraser SE, 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
Shah NM, Marchionni MA, Isaacs I, Stroobant P, Anderson DJ (1994) Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77:349–360
Shah NM, Groves AK, Anderson DJ (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85:331–343
Shanklin DR, Soteloav C (1969) In situ tumors in fetuses, newborns and infants. Biol Neonat 14:286-&
Shi H, Cui H, Alam G, Gunning WT, Nestor A, Giovannucci D, Zhang M, Ding HF (2008) Nestin expression defines both glial and neuronal progenitors in postnatal sympathetic ganglia. J Comp Neurol 508:867–878
Shtukmaster S, Schier MC, 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
Shtukmaster S, Narasimhan P, El Faitwri T, Stubbusch J, Ernsberger U, Rohrer H, Unsicker K, Huber K (2016) MiR-124 is differentially expressed in derivatives of the sympathoadrenal cell lineage and promotes neurite elongation in chromaffin cells. Cell Tissue Res 365:225–232
Smith JL, Schoenwolf GC (1987) Cell cycle and neuroepithelial cell shape during bending of the chick neural plate. Anat Rec 218:196–206
Smith JL, Schoenwolf GC (1988) Role of cell-cycle in regulating neuroepithelial cell shape during bending of the chick neural plate. Cell Tissue Res 252:491–500
Sommer L, Ma Q, Anderson DJ (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
Stanke M, Junghans D, Geissen M, Goridis C, Ernsberger U, Rohrer H (1999) The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126:4087–4094
Stanke M, Stubbusch J, Rohrer H (2004) Interaction of Mash1 and Phox2b in sympathetic neuron development. Mol Cell Neurosci 25:374–382
Stemple DL, Anderson DJ (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71:973–985
Stewart HJ, Brennan A, Rahman M, Zoidl G, Mitchell PJ, Jessen KR, Mirsky R (2001) Developmental regulation and overexpression of the transcription factor AP-2, a potential regulator of the timing of Schwann cell generation. Eur J Neurosci 14:363–372
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 8:16
Stubbusch J, Narasimhan P, Hennchen M, Huber K, Unsicker K, Ernsberger U, Rohrer H (2015) Lineage and stage specific requirement for Dicer1 in sympathetic ganglia and adrenal medulla formation and maintenance. Dev Biol 400:210–223
Subramanian A, Maker VK (2006) Organs of Zuckerkandl: their surgical significance and a review of a century of literature. Am J Surg 192:224–234
Suzuki T, Kachi T (1994) Differences between adrenaline and Noradrenaline cells in cellular-association with supporting cells in the adrenal-medulla of the pig - an Immunohistochemical study. Neurosci Lett 176:217–220
Takahashi T, Nowakowski RS, Caviness VS Jr (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16:6183–6196
Takahashi T, Nowakowski RS, Caviness VS Jr (1997) The mathematics of neocortical neuronogenesis. Dev Neurosci 19:17–22
Theveneau E, Duband JL, Altabef M (2007) Ets-1 confers cranial features on neural crest delamination. PLoS ONE 2:e1142
Thomas AJ, Erickson CA (2009) FOXD3 Regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136:1849–1858
Thomas SA, Matsumoto AM, Palmiter RD (1995) Noradrenaline is essential for mouse fetal development. Nature 374:643–646
Tischler AS, Ruzicka LA, Donahue SR, DeLellis RA (1989) Chromaffin cell proliferation in the adult rat adrenal medulla. Int J Dev Neurosci 7:439–448
Tsarovina K, Pattyn A, Stubbusch J, Muller F, Van Der Wees J, Schneider C, Brunet JF, Rohrer H (2004) Essential role of Gata transcription factors in sympathetic neuron development. Development 131:4775–4786
Tsarovina K, Schellenberger J, Schneider C, Rohrer H (2008) Progenitor cell maintenance and neurogenesis in sympathetic ganglia involves notch signaling. Mol Cell Neurosci 37:20–31
Tsarovina K, Reiff T, Stubbusch J, Kurek D, Grosveld FG, Parlato R, Schutz G, Rohrer H (2010) The Gata3 transcription factor is required for the survival of embryonic and adult sympathetic neurons. J Neurosci 30:10833–10843
Uesaka T, Nagashimada M, Enomoto H (2015) Neuronal differentiation in Schwann cell lineage underlies postnatal neurogenesis in the enteric nervous system. J Neurosci 35:9879–9888
Unsicker K, Krisch B, Otten U, Thoenen H (1978) Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc Natl Acad Sci U S A 75:3498–3502
Van Dusen NJ, Vincentz JW, Firulli BA, Howard MJ, Rubart M, Firulli AB (2014) Loss of Hand2 in a population of Periostin lineage cells results in pronounced bradycardia and neonatal death. Dev Biol 388:149–158
Varley JE, Maxwell GD (1996) BMP-2 and BMP-4, but not BMP-6, increase the number of adrenergic cells which develop in quail trunk neural crest cultures. Exp Neurol 140:84–94
Varley JE, Wehby RG, Rueger DC, Maxwell GD (1995) Number of adrenergic and islet-1 immunoreactive cells is increased in avian trunk neural crest cultures in the presence of human recombinant osteogenic protein-1. Dev Dyn 203:434–447
Varley JE, McPherson CE, Zou H, Niswander L, Maxwell GD (1998) Expression of a constitutively active type I BMP receptor using a retroviral vector promotes the development of adrenergic cells in neural crest cultures. Dev Biol 196:107–118
Vega-Lopez GA, Cerrizuela S, Aybar MJ (2017) Trunk neural crest cells: formation, migration and beyond. Int J Dev Biol 61:5–15
Wang L, Mongera A, Bonanomi D, Cyganek L, Pfaff SL, Nusslein-Volhard C, Marquardt T (2014) A conserved axon type hierarchy governing peripheral nerve assembly. Development 141:1875–1883
Waring H (1936) Development of the adrenal gland of the mouse. Q J Microsc Sci 78:329–336
Wegner M, Stolt CC (2005) From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci 28:583–588
White J, Dalton S (2005) Cell cycle control of embryonic stem cells. Stem Cell Rev 1:131–138
Wildner H, Gierl MS, Strehle M, Pla P, Birchmeier C (2008) Insm1 (IA-1) is a crucial component of the transcriptional network that controls differentiation of the sympatho-adrenal lineage. Development 135:473–481
Wilson YM, Richards KL, Ford-Perriss ML, Panthier JJ, Murphy M (2004) Neural crest cell lineage segregation in the mouse neural tube. Development 131:6153–6162
Woodhoo A, Alonso MB, Droggiti A, Turmaine M, D’Antonio M, Parkinson DB, Wilton DK, Al-Shawi R, Simons P, Shen J, Guillemot F, Radtke F, Meijer D, Feltri ML, Wrabetz L, Mirsky R, Jessen KR (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 12:839–847
Wurtman RJ, Axelrod J (1966) Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. J Biol Chem 241:2301–2305
Young HM, Bergner AJ, Muller T (2003) Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1–11
Young HM, Cane KN, Anderson CR (2011) Development of the autonomic nervous system: a comparative view. Auton Neurosci 165:10–27
Zackenfels K, Oppenheim RW, Rohrer H (1995) Evidence for an important role of IGF-I and IGF-II for the early development of chick sympathetic neurons. Neuron 14:731–741
Zhou QY, Quaife CJ, Palmiter RD (1995) Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374:640–643
Zirlinger M, Lo L, McMahon J, McMahon AP, Anderson DJ (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 U S A 99:8084–8089
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Chan, W.H., Anderson, C.R. & Gonsalvez, D.G. From proliferation to target innervation: signaling molecules that direct sympathetic nervous system development. Cell Tissue Res 372, 171–193 (2018). https://doi.org/10.1007/s00441-017-2693-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-017-2693-x