Sympathetic neurons and chromaffin cells share a common progenitor in the neural crest in vivo

Neural Development

Klaus Unsicker¹  Chaya Kalcheim²  Shlomo Krispin²  Katrin Huber¹  Marie Catherine Schier³  Stella Shtukmaster¹ 

[1] Department of Molecular Embryology, Institute of Anatomy and Cell Biology University of Freiburg, Albertstr. 17, Freiburg D-79104, Germany;Department of Medical Neurobiology, IMRIC and ELSC-Hebrew University of Jerusalem, Hadassah Medical School, POB 12272, Jerusalem 9112102, Israel;Clinical Cooperation Unit Pediatric Oncology, German Cancer Research Center (DKFZ), Heidelberg D-69120, Germany

关键词: Sympathoadrenal progenitors;    Sympathetic neurons;    Single cell electroporation;    Neural crest;    Chromaffin cells;    Chicken embryo;   

Others  :  804541
DOI  :  10.1186/1749-8104-8-12

 received in 2012-12-17, accepted in 2013-05-17,  发布年份 2013

【 摘 要 】

Background

The neural crest (NC) is a transient embryonic structure unique to vertebrates, which generates peripheral sensory and autonomic neurons, glia, neuroendocrine chromaffin and thyroid C-cells, melanocytes, and mesenchymal derivatives such as parts of the skull, heart, and meninges. The sympathoadrenal (SA) cell lineage is one major sub-lineage of the NC that gives rise to sympathetic neurons, chromaffin cells, and the intermediate small intensely fluorescent (SIF) cells. A key question is when during NC ontogeny do multipotent progenitors segregate into the different NC-derived lineages. Recent evidence suggested that sympathetic, sensory, and melanocyte progenitors delaminate from the thoracic neural tube (NT) in successive, largely non-overlapping waves and that at least certain NC progenitors are already fate-restricted within the NT. Whether sympathetic neurons and chromaffin cells, suggested by cell culture studies to share a common progenitor, are also fate segregated in ovo prior to emigration, is not known.

Results

We have conducted single cell electroporations of a GFP-encoding plasmid into the dorsal midline of E2 chick NTs at the adrenomedullary level of the NC. Analysis of their derivatives, performed at E6, revealed that in most cases, labelled progeny was detected in both sympathetic ganglia and adrenal glands, where cells co-expressed characteristic marker combinations.

Conclusions

Our results show that sympathetic neurons and adrenal chromaffin cells share a common progenitor in the NT. Together with previous findings we suggest that phenotypic diversification of these sublineages is likely to occur after delamination from the NT and prior to target encounter.

【 授权许可】

   
2013 Shtukmaster et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]LeDouarin NM, Kalcheim C: The Neural Crest. Cambridge: Cambridge University Press; 1999.
• [2]Huber K, Kalcheim C, Unsicker K: The development of the chromaffin cell lineage from the neural crest. Auton Neurosci 2009, 151(1):10-16.
• [3]Langley K, Grant NJ: Molecular markers of sympathoadrenal cells. Cell Tissue Res 1999, 298(2):185-206.
• [4]Unsicker K: The chromaffin cell: paradigm in cell, developmental and growth factor biology. J Anat 1993, 183(Pt 2):207-221.
• [5]Unsicker K, Huber K, Schütz G, Kalcheim C: The chromaffin cell and its development. Neurochem Res 2005, 30(6–7):921-925.
• [6]Unsicker K, Huber K, Schober A, Kalcheim C: Resolved and open issues in chromaffin cell development. Mech Dev 2013, 130:324-329.
• [7]Krispin S, Nitzan E, Kalcheim C: The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 2010, 70(12):796-812.
• [8]Serbedzija GN, Bronner-Fraser M, Fraser SE: A vital dye analysis of the timing and pathways of avian trunk neural crest cell migration. Development 1989, 106(4):809-816.
• [9]Reissmann E, Ernsberger U, Francis-West PH, Rueger D, Brickell PM, Rohrer H: Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development 1996, 122(7):2079-2088.
• [10]Schneider C, Wicht H, Enderich J, Wegner M, Rohrer H: Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron 1999, 24(4):861-870.
• [11]Ernsberger U, Patzke H, Tissier-Seta J-P, Reh T, Goridis C, Rohrer H: 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 1995, 52(1):125-136.
• [12]Guillemot F, Lo LC, Johnson JE, Auerbach A, Anderson DJ, Joyner AL: Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 1993, 75(3):463-476.
• [13]Ernsberger U, Reissmann E, Mason I, Rohrer H: The expression of dopamine beta-hydroxylase, tyrosine hydroxylase, and Phox2 transcription factors in sympathetic neurons: evidence for common regulation during noradrenergic induction and diverging regulation later in development. Mech Dev 2000, 92(2):169-177.
• [14]Howard MJ, Stanke M, Schneider C, Wu X, Rohrer H: The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 2000, 127(18):4073-4081.
• [15]Lucas ME, Muller F, Rudiger R, Henion PD, Rohrer H: The bHLH transcription factor hand2 is essential for noradrenergic differentiation of sympathetic neurons. Development 2006, 133:4015-4024.
• [16]Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF: Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 1997, 124:4065-4075.
• [17]Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF: The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 1999, 399:366-370.
• [18]Tsarovina K, Pattyn A, Stubbusch J, Müller F, Wees J, Schneider C, Brunet JF: Essential role of Gata transcription factors in sympathetic neuron development. Development 2004, 131(19):4775-4786.
• [19]Wildner H, Gierl MS, Strehle M, Pla P, Birchmeier C: Insm1 (IA-1) is a crucial component of the transcriptional network that controls differentiation of the sympatho-adrenal lineage. Development 2008, 135(3):473-481.
• [20]Huber K: The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev Biol 2006, 298(2):335-343.
• [21]Rohrer H: Transcriptional control of differentiation and neurogenesis in autonomic ganglia. Eur J Neurosci 2011, 34(10):1563-1573.
• [22]Anderson DJ, Axel R: A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. Cell 1986, 47(6):1079-1090.
• [23]Michelsohn AM, Anderson DJ: Changes in competence determine the timing of two sequential glucocorticoid effects on sympathoadrenal progenitors. Neuron 1992, 8(3):589-604.
• [24]Unsicker K, Krisch B, Otten U, Thoenen H: Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc Natl Acad Sci U S A 1978, 75(7):3498-3502.
• [25]Anderson DJ: Cell fate determination in the peripheral nervous system: the sympathoadrenal progenitor. J Neurobiol 1993, 24(2):185-198.
• [26]Finotto S, Krieglstein K, Schober A, Deimling F, Lindner K, Brühl B, Beier K, Metz J, Garcia-Arraras JE, Roig-Lopez JL, Monaghan P, Schmid W, Cole TJ, Kellendonk C, Tronche F, Schütz G, Unsicker K: 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 1999, 126(13):2935-2944.
• [27]Gut P, Huber K, Lohr J, Brühl B, Oberle S, Treier M, Ernsberger U, Kalcheim C, Unsicker K: Lack of an adrenal cortex in Sf1 mutant mice is compatible with the generation and differentiation of chromaffin cells. Development 2005, 132(20):4611-4619.
• [28]Ernsberger U, Esposito L, Partimo S, Huber K, Franke A, Bixby JL, Kalcheim C, Unsicker K: Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen. Cell Tissue Res 2005, 319(1):1-13.
• [29]Krispin S, Nitzan E, Kassem Y, Kalcheim C: Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 2010, 137:585-595.
• [30]LeDouarin NM, Creuzet S, Couly G, Dupin E: Neural crest cell plasticity and its limits. Development 2004, 131(19):4637-4650.
• [31]Huber K, Franke A, Brühl B, Krispin S, Ernsberger U, Schober A, Von Bohlen Und Halbach O, Rohrer H, Kalcheim C, Unsicker K: Persistent expression of BMP-4 in embryonic chick adrenal cortical cells and its role in chromaffin cell development. Neural Dev 2008, 3:28. BioMed Central Full Text
• [32]Unsicker K: Fine structure and innervation of the avian adrenal gland. I Fine structure of adrenal chromaffin cells and ganglion cells. Z Zellforsch Mikrosk Anat 1973, 145:389-416.
• [33]Unsicker K, Habura-Flüh O, Zwarg J: Different types of small granule containing cells and neurons in the guinea pig adrenal medulla. Cell Tissue Res 1978, 189(1):109-130.
• [34]Vogel KS, Weston JA: The sympathoadrenal lineage in avian embryos. I. Adrenal chromaffin cells lose neuronal traits during embryogenesis. Dev Biol 1990, 139(1):1-12.
• [35]Wakamatsu Y, Maynard TM, Weston JA: Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development 2000, 127(13):2811-2821.
• [36]Anderson DJ: Genes, lineages and the neural crest: a speculative review. Philos Trans R Soc Lond B Biol Sc 2000, 355(1399):953-964.
• [37]Dorsky RI, Moon RT, Raible DW: Environmental signals and cell fate specification in premigratory neural crest. Bioessays 2000, 22(8):708-716.
• [38]Harris ML, Erickson CA: Lineage specification in neural crest cell path finding. Dev Dyn 2007, 236(1):1-19.
• [39]Hass K, Sin WC, Javaherian A, Li Z, Cline HT: Single-cell electroporation for gene transfer in vivo. Neuron 2001, 29:583-591.
• [40]Brown CY, Eom DS, Amarnath S, Agarwala S: A simple technique for early in vivo electroporation of E1 chick embryos. Dev Dyn 2012, 241(3):545-552.
• [41]Hamburger V, Hamilton HL: A series of normal stages in the development of the chick embryo 1951. Dev Dyn 1992, 195(4):231-272.
• [42]Ben-Yair R, Kalcheim C: Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 2005, 132(4):689-701.
• [43]Momose T, Tonegawa A, Takeuchi J, Ogawa H, Umesono K, Yasuda K: Efficient targeting of gene expression in chick embryos by microelectroporation. Dev Growth Differ 1999, 41:335-344.
• [44]Zopf D, Hermans-Borgmeyer I, Gundelfinger ED, Betz H: Identification of gene products expressed in the developing chick visual system: characterization of a middle-molecular-weight neurofilament cDNA. Genes Dev 1987, 1(7):699-708.