Transcriptional control of differentiation and neurogenesis in autonomic ganglia

European Journal of Neuroscience

Volumn 34, Issue 10, 2011, Pages 1563-1573

  Rohrer, Hermann ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

Autonomic nervous system; Developmental neurobiology; Gene expression; Neurogenesis; Neuronal death; Sympathetic neuron

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE RECEPTOR CXCR4; OSTEOGENIC PROTEIN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR HAND2; TRANSCRIPTION FACTOR PHOX2B; UNCLASSIFIED DRUG;

ARTICLE; AUTONOMIC GANGLION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SPECIFICITY; CELL SURVIVAL; EMBRYO DEVELOPMENT; GENE REGULATORY NETWORK; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEURAL STEM CELL; NONHUMAN; PARASYMPATHETIC GANGLION; PRIORITY JOURNAL; SPINAL GANGLION; SYMPATHETIC GANGLION; SYMPATHETIC NERVE CELL; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; GANGLIA, AUTONOMIC; GANGLIA, PARASYMPATHETIC; GANGLIA, SYMPATHETIC; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; NEURAL CREST; NEUROGENESIS; NEURONS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 81855166236     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07860.x     Document Type: Article

References (147)

1. Adachi, M. & Lewis, E.J. (2002) The paired-like homeodomain protein, arix, mediates protein kinase A-stimulated dopamine b-hydroxylase gene transcription through its phosphorylation status. J. Biol. Chem., 277, 22915-22924.
2. Allan, I.J. & Newgreen, D.F. (1977) Catecholamine accumulation in neural crest cells and the primary sympathetic chain. Am. J. Anat., 149, 413-421.
3. Altman, J. (1969) Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats. J. Comp. Neurol., 136, 269-293.
4. Andres, R., Forgie, A., Wyatt, S., Chen, Q., De Sauvage, F.J. & Davies, A.M. (2001) Multiple effects of artemin on sympathetic neurone generation, survival and growth. Development, 128, 3685-3695.
5. Apostolova, G. & Dechant, G. (2009) Development of neurotransmitter phenotypes in sympathetic neurons. Auton. Neurosci., 151, 30-38.
6. Apostolova, G., Loy, B., Dorn, R. & Dechant, G. (2010) The sympathetic neurotransmitter switch depends on the nuclear matrix protein Satb2. J. Neurosci., 30, 16356-16364.
7. Armstrong, A., Ryu, Y.K., Chieco, D. & Kuruvilla, R. (2011) Frizzled3 is required for neurogenesis and target innervation during sympathetic nervous system development. J. Neurosci., 31, 2371-2381.
8. Asmus, S.E., Parsons, S. & Landis, S.C. (2000) Developmental changes in the transmitter properties of sympathetic neurons that innervate the periosteum. J. Neurosci., 20, 1495-1504.
9. Avivi, C. & Goldstein, R.S. (1999) Differential expression of islet-1 in neural crest-derived ganglia. Islet-1+ dorsal root ganglion cells are post-mitotic and islet-1+ sympathetic ganglion cells are still cycling. Dev. Brain Res., 115, 89-92.
10. Barrallo-Gimeno, A., Holzschuh, J., Driever, W. & Knapik, E.W. (2004) Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development, 131, 1463-1477.
11. Buchmann-Moller, S., Miescher, I., John, N., Krishnan, J., Deng, C.X. & Sommer, L. (2009) Multiple lineage-specific roles of Smad4 during neural crest development. Dev. Biol., 330, 329-338.
12. Burau, K., Stenull, I., Huber, K., Misawa, H., Berse, B., Unsicker, K. & Ernsberger, U. (2004) c-ret regulates cholinergic properties in mouse sympathetic neurons: evidence from mutant mice. Eur. J. Neurosci., 20, 353-362.
13. Callahan, T., Young, H.M., Anderson, R.B., Enomoto, H. & Anderson, C.R. (2008) Development of satellite glia in mouse sympathetic ganglia: GDNF and GFRalpha1 are not essential. Glia, 56, 1428-1437.
14. Cane, K.N. & Anderson, C.R. (2009) Generating diversity: mechanisms regulating the differentiation of autonomic neuron phenotypes. Auton. Neurosci., 151, 17-29.
15. Cannon, W.B. (1963) The Wisdom of the Body. Norton Library, New York.
16. Castro, D.S., Martynoga, B., Parras, C., Ramesh, V., Pacary, E., Johnston, C., Drechsel, D., Lebel-Potter, M., Garcia, L.G., 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.
17. Caviness, V.S. Jr, Takahashi, T. & Nowakowski, R.S. (1995) Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci., 18, 379-383.
18. Chen, S., Wang, Q.L., Nie, Z., Sun, H., Lennon, G., Copeland, N.G., Gilbert, D.J., Jenkins, N.A. & Zack, D.J. (1997) Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron, 19, 1017-1030.
19. Cheng, L., Arata, A., Mizuguchi, R., Qian, Y., Karunaratne, A., Gray, P.A., Arata, S., Shirasawa, S., Bouchard, M., Luo, P., Chen, C.L., Busslinger, M., Goulding, M., Onimaru, H. & Ma, Q. (2004) Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat. Neurosci., 7, 510-517.
20. Chubb, D.P. & Anderson, C.R. (2010) The relationship of the birth date of rat sympathetic neurons to the target they innervate. Dev. Dyn., 239, 897-904.
21. Coppola, E., Pattyn, A., Guthrie, S.C., Goridis, C. & Studer, M. (2005) Reciprocal gene replacements reveal unique functions for Phox2 paralogous homeobox genes during neural differentiation. EMBO J., 24, 4392-4403.
22. Coppola, E., d'Autreaux, F., Rijli, F.M. & Brunet, J.F. (2010) Ongoing roles of Phox2 homeodomain transcription factors during neuronal differentiation. Development, 137, 4211-4220.
23. Dalla Torre di Sanguinetto, S.A., Dasen, J.S. & Arber, S. (2008) Transcriptional mechanisms controlling motor neuron diversity and connectivity. Curr. Opin. Neurobiol., 18, 36-43.
24. Dehay, C. & Kennedy, H. (2007) Cell-cycle control and cortical development. Nat. Rev. Neurosci., 8, 438-450.
25. DiCicco-Bloom, E. & Black, I.B. (1988) Insulin growth factors regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Proc. Natl. Acad. Sci. USA, 85, 4066-4070.
26. DiCicco-Bloom, E., Townes-Anderson, E. & Black, I.B. (1990) Neuroblast mitosis in dissociated culture: regulation and relationship to differentiation. J. Cell Biol., 110, 2073-2086.
27. DiCicco-Bloom, E., Deutsch, P.J., Maltzman, J., Zhang, J.W., Pintar, J.E., Zheng, J., Friedman, W.F., Zhou, X.F. & Zaremba, T. (2000) Autocrine expression and ontogenetic functions of the PACAP ligand/receptor system during sympathetic development. Dev. Biol., 219, 197-213.
28. Dubreuil, V., Hirsch, M.R., Pattyn, A., Brunet, J.F. & Goridis, C. (2000) The Phox2b transcription factor coordinately regulates neuronal cell cycle exit and identity. Development, 127, 5191-5201.
29. Dziennis, S. & Habecker, B.A. (2004) Ciliary neurotrophic factor suppresses Phox2a in sympathetic neurons. Neuroreport, 15, 33-36.
30. Elshamy, W.M., Fridvall, L.K. & Ernfors, P. (1998) Growth arrest failure, G1 restriction point override, and S phase death of sensory precursor cells in the absence of neurotrophin-3. Neuron, 21, 1003-1015.
31. Enemar, A., Falck, B. & Hakanson, R. (1965) Observations on the appearance of norepinephrine in the sympathetic nervous system of the chick embryo. Dev. Biol., 11, 268-283.
32. Ernsberger, U. & Rohrer, H. (1999) Development of the cholinergic neurotransmitter phenotype in postganglionic sympathetic neurons. Cell Tissue Res., 297, 339-361.
33. Ernsberger, U., Patzke, H., Tissier-Seta, J.P., 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.
34. Fariñas, I., Yoshida, C.K., Backus, C. & Reichardt, L.F. (1996) Lack of neurotrophin-3 results in death of spinal sensory neurons and premature differentiation of their precursors. Neuron, 17, 1065-1078.
35. Farkas, L.M., Haffner, C., Giger, T., Khaitovich, P., Nowick, K., Birchmeier, C., Paabo, S. & Huttner, W.B. (2008) Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron, 60, 40-55.
36. Francis, N.J. & Landis, S.C. (1999) Cellular and molecular determinants of sympathetic neuron development. Annu. Rev. Neurosci., 22, 541-566.
37. Frank, E. & Sanes, J.R. (1991) Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus. Development, 111, 895-908.
38. George, L., Kasemeier-Kulesa, J., Nelson, B.R., Koyano-Nakagawa, N. & Lefcort, F. (2010) Patterned Assembly and Neurogenesis in the chick dorsal root ganglion. J. Comp. Neurol., 518, 405-422.
39. Glebova, N.O. & Ginty, D.D. (2005) Growth and survival signals controlling sympathetic nervous system development. Annu. Rev. Neurosci., 28, 191-222.
40. Goridis, C. & Rohrer, H. (2002) Specification of catecholaminergic and serotonergic neurons. Nat. Rev. Neurosci., 3, 531-541.
41. Götz, M. & Huttner, W.B. (2005) The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol., 6, 777-788.
42. Greco, D., Zellmer, E., Zhang, Z. & Lewis, E. (1995) Transcription factor AP-2 regulates expression of the dopamine b-hydroxylase gene. J. Neurochem., 65, 510-516.
43. Greenwood, A.L., Turner, E.E. & Anderson, D.J. (1999) Identification of dividing, determined sensory neuron precursors in the mammalian neural crest. Development, 126, 3545-3559.
44. Groves, A.K., George, K.M., Tissier-Seta, J.-P., Engel, J.D., Brunet, J.-F. & Anderson, D.J. (1995) Differential regulation of transcription factor gene expression and phenotypic markers in developing sympathetic neurons. Development, 121, 887-901.
45. Guidry, G. & Landis, S.C. (1998) Target-dependent development of the vesicular acetylcholine transporter in rodent sweat gland innervation. Dev. Biol., 199, 175-184.
46. Guillemot, F. (2007) Spatial and temporal specification of neural fates by transcription factor codes. Development, 134, 3771-3780.
47. Guillemot, F., Lo, L.-C., Johnson, J.E., Auerbach, A., Anderson, D.J. & Joyner, A.L. (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell, 75, 463-476.
48. Hatakeyama, J. & Kageyama, R. (2004) Retinal cell fate determination and bHLH factors. Semin. Cell Dev. Biol., 15, 83-89.
49. Hendershot, T.J., Liu, H., Clouthier, D.E., Shepherd, I.T., Coppola, E., Studer, M., Firulli, A.B., Pittman, D.L. & Howard, M.J. (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.
50. Henion, P.D. & Weston, J.A. (1997) Timing and pattern of cell fate restrictions in the neural crest lineage. Development, 124, 4351-4359.
51. Henion, P.D., Garner, A.S., Large, T.H. & Weston, J.A. (1995) trkC-mediated NT-3 signaling is required for the early development of a subpopulation of neurogenic neural crest cells. Dev. Biol., 172, 602-613.
52. Hippenmeyer, S., Kramer, I. & Arber, S. (2004) Control of neuronal phenotype: what targets tell the cell bodies. Trends Neurosci., 27, 482-488.
53. Hirsch, M.R., Tiveron, M.C., Guillemot, F., Brunet, J.F. & Goridis, C. (1998) Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development, 125, 599-608.
54. Hobert, O. (2008) Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc. Natl. Acad. Sci. USA, 105, 20067-20071.
55. Howard, M.J. (2005) Mechanisms and perspectives on differentiation of autonomic neurons. Dev. Biol., 277, 271-286.
56. Howard, M.J., 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.
57. Huber, K. (2006) The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev. Biol., 298, 335-343.
58. Huber, K., Kalcheim, C. & Unsicker, K. (2009) The development of the chromaffin cell lineage from the neural crest. Auton. Neurosci., 151, 10-16.
59. Jung, H., Lacombe, J., Mazzoni, E.O., Liem, K.F. Jr, Grinstein, J., Mahony, S., Mukhopadhyay, D., Gifford, D.K., Young, R.A., Anderson, K.V., Wichterle, H. & Dasen, J.S. (2010) Global control of motor neuron topography mediated by the repressive actions of a single hox gene. Neuron, 67, 781-796.
60. Kadkhodaei, B., Ito, T., Joodmardi, E., Mattsson, B., Rouillard, C., Carta, M., Muramatsu, S., Sumi-Ichinose, C., Nomura, T., Metzger, D., Chambon, P., Lindqvist, E., Larsson, N.G., Olson, L., Bjorklund, A., Ichinose, H. & Perlmann, T. (2009) Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J. Neurosci., 29, 15923-15932.
61. 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.
62. Kim, H.S., Hong, S.J., LeDoux, M.S. & Kim, K.S. (2001) Regulation of the tyrosine hydroxylase and dopamine b-hydroxylase genes by the transcription factor AP-2. J. Neurochem., 76, 280-294.
63. Kim, J., Lo, L., Dormand, E. & Anderson, D.J. (2003) SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron, 38, 17-31.
64. Kirby, M.L. & Gilmore, S.A. (1976) A correlative histofluorescence and light microscopic study of the formation of the sympathetic trunks in chick embryos. Anat. Rec., 186, 437-450.
65. Kittappa, R., Chang, W.W., Awatramani, R.B. & McKay, R.D. (2007) The foxa2 gene controls the birth and spontaneous degeneration of dopamine neurons in old age. PLoS Biol., 5, e325.
66. Knight, R.D., Nair, S., Nelson, S.S., Afshar, A., Javidan, Y., Geisler, R., Rauch, G.J. & Schilling, T.F. (2003) lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development, 130, 5755-5768.
67. Kondo, T. & Raff, M. (2000) Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development, 127, 2989-2998.
68. 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.
69. Kulesa, P.M., Lefcort, F. & Kasemeier-Kulesa, J.C. (2009) The migration of autonomic precursor cells in the embryo. Auton. Neurosci., 151, 3-9.
70. Landis, S.C. (1990) Target regulation of neurotransmitter phenotype. Trends Neurosci., 13, 344-350.
71. Landis, S.C. (1996) The development of cholinergic sympathetic neurons: a role for neuropoietic cytokines? Perspect. Dev. Neurobiol., 4, 53-63.
72. Landis, S.C. & Fredieu, J.R. (1986) Coexistence of calcitonin gene-related peptide and vasoactive intestinal peptide in cholinergic sympathetic innervation of rat sweat glands. Brain Res., 377, 177-181.
73. Le Douarin, N.M. & Kalcheim, C. (1999) The Neural Crest. Cambridge University Press, Cambridge.
74. Le Douarin, N.M., Creuzet, S., Couly, G. & Dupin, E. (2004) Neural crest cell plasticity and its limits. Development, 131, 4637-4650.
75. LeDouarin, N.M. & Smith, J. (1988) Development of the peripheral nervous system from the neural crest. Ann. Rev. Cell Biol., 4, 375-404.
76. Lee, V.M., Sechrist, J.W., Bronner-Fraser, M. & Nishi, R. (2002) Neuronal differentiation from postmitotic precursors in the ciliary ganglion. Dev. Biol., 252, 312-323.
77. Lee, V.M., Sechrist, J.W., Luetolf, S. & Bronner-Fraser, M. (2003) Both neural crest and placode contribute to the ciliary ganglion and oculomotor nerve. Dev. Biol., 263, 176-190.
78. Lee, V.M., Bronner-Fraser, M. & Baker, C.V.H. (2005) Restricted response of mesencephalic neural crest to sympathetic differentiation signals to the trunk. Dev. Biol., 278, 175-192.
79. Liu, H., Margiotta, J.F. & Howard, M.J. (2005) BMP4 supports noradrenergic differentiation by a PKA-dependent mechanism. Dev. Biol., 286, 521-536.
80. Liu, C., Maejima, T., Wyler, S.C., Casadesus, G., Herlitze, S. & Deneris, E.S. (2010) Pet-1 is required across different stages of life to regulate serotonergic function. Nat. Neurosci., 13, 1190-1198.
81. Lo, L.C., Tiveron, M.C. & Anderson, D.J. (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.
82. Lucas, M.E., Müller, F., Rüdiger, R., Henion, P.D. & Rohrer, H. (2006) The bHLH transcription factor hand2 is essential for noradrenergic differetiation of sympathetic neurons. Development, 133, 4015-4024.
83. Makita, T., Sucov, H.M., Gariepy, C.E., Yanagisawa, M. & Ginty, D.D. (2008) Endothelins are vascular-derived axonal guidance cues for developing sympathetic neurons. Nature, 452, 759-763.
84. McGraw, H.F., Nechiporuk, A. & Raible, D.W. (2008) Zebrafish dorsal root ganglia neural precursor cells adopt a glial fate in the absence of neurogenin1. J. Neurosci., 28, 12558-12569.
85. Moriguchi, T., Takako, N., Hamada, M., Maeda, A., Fujioka, Y., Kuroha, T., Huber, R.E., Hasegawa, S.L., Rao, A., Yamamoto, M., Takahashi, S., Lim, K.C. & Engel, J.D. (2006) Gata3 participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation. Development, 133, 3871-3881.
86. Morikawa, Y., D'Autreaux, F., Gershon, M.D. & Cserjesi, P. (2007) Hand2 determines the noradrenergic phenotype in the mouse sympathetic nervous system. Dev. Biol., 307, 114-126.
87. 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.
88. Müller, F. & Rohrer, H. (2002) Molecular control of ciliary neuron development: BMPs and downstream transcriptional control in the parasympathetic lineage. Development, 129, 5707-5717.
89. Mundell, N.A. & Labosky, P.A. (2011) Neural crest stem cell multipotency requires Foxd3 to maintain neural potential and repress mesenchymal fates. Development, 138, 641-652.
90. Nelson, B.R., Claes, K., Todd, V., Chaverra, M. & Lefcort, F. (2004) NELL2 promotes motor and sensory neuron differentiation and stimulates mitogenesis in DRG in vivo. Dev. Biol., 270, 322-335.
91. Paris, M., Wang, W.H., Shin, M.H., Franklin, D.S. & Andrisani, O.M. (2006) Homeodomain transcription factor Phox2a, via cyclic AMP-mediated activation, induces p27Kip1 transcription, coordinating neural progenitor cell cycle exit and differentiation. Mol. Cell. Biol., 26, 8826-8839.
92. Parlier, D., Ariza, A., Christulia, F., Genco, F., Vanhomwegen, J., Kricha, S., Souopgui, J. & Bellefroid, E.J. (2008) Xenopus zinc finger transcription factor IA1 (Insm1) expression marks anteroventral noradrenergic neuron progenitors in Xenopus embryos. Dev. Dyn., 237, 2147-2157.
93. Parras, C.M., Schuurmans, C., Scardigli, R., Kim, J., Anderson, D.J. & Guillemot, F. (2002) Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev., 16, 324-338.
94. Patel, T.D., Kramer, I., Kucera, J., Niederkofler, V., Jessell, T.M., Arber, S. & Snider, W.D. (2003) Peripheral NT3 signaling is required for ETS protein expression and central patterning of proprioceptive sensory afferents. Neuron, 38, 403-416.
95. Pattyn, A., Morin, X., Cremer, H., Goridis, C. & Brunet, J.-F. (1999) The homeobox gene Phox2b is essential for the development of all autonomic derivatives of the neural crest. Nature, 399, 366-370.
96. Pattyn, A., Guillemot, F. & Brunet, J.F. (2006) Delays in neuronal differentiation in Mash1/Ascl1 mutants. Dev. Biol., 295, 67-75.
97. Pellegrino, M.J., Parrish, D.C., Zigmond, R.E. & Habecker, B.A. (2011) Cytokines inhibit norepinephrine transporter expression by decreasing Hand2. Mol. Cell. Neurosci., 46, 671-680.
98. 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.
99. Potzner, M.R., 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.
100. Raabe, E.H., Laudenslager, M., Winter, C., Wasserman, N., Cole, K., LaQuaglia, M., Maris, D.J., Mosse, Y.P. & Maris, J.M. (2008) Prevalence and functional consequence of PHOX2B mutations in neuroblastoma. Oncogene, 27, 469-476.
101. Raible, D.W. & Eisen, J.S. (1994) Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development, 120, 495-503.
102. Raible, D.W. & Eisen, J.S. (1996) Regulative interactions in zebrafish neural crest. Development, 122, 510-507.
103. Reedy, M.V., Faraco, C.D. & Erickson, C.A. (1998) The delayed entry of thoracic neural crest cells into the dorsolateral path is a consequence of the late emigration of melanogenic neural crest cells from the neural tube. Dev. Biol., 200, 234-246.
104. 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.
105. 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.
106. Reissmann, E., Ernsberger, U., Francis-West, P.H., Rueger, D., Brickell, P.M. & Rohrer, H. (1996) Involvement of bone morphogenetic proteins-4 and-7 in the specification of the adrenergic phenotype in developing sympathetic neurons. Development, 122, 2079-2088.
107. 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.
108. Rothman, T.P., Gershon, M.D. & Holtzer, H. (1978) The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev. Biol., 65, 321-341.
109. Rothman, T.P., Specht, L.A., Gershon, M.D., Joh, T.H., Teitelman, G., Pickel, V.M. & Reis, D.J. (1980) Catecholamine biosynthetic enzymes are expressed in replicating cells of the peripheral but not the central nervous system. Proc. Natl. Acad. Sci. USA, 77, 6221-6225.
110. Schäfer, M.K.H., Schütz, B., Weihe, E. & Eiden, L.E. (1997) Target-independent cholinergic differentiation in the rat sympathetic nervous system. Proc. Natl. Acad. Sci. USA, 94, 4149-4154.
111. Schäfer, M.K.H., Eiden, L.E. & Weihe, E. (1998) Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. II. The peripheral nervous system. Neuroscience, 84, 361-376.
112. Schmidt, M., Lin, S., Pape, M., Ernsberger, U., Stanke, M., Kobayashi, K., Howard, M.J. & 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.
113. 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.
114. 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.
115. Schutz, B., von Engelhardt, J., Gordes, M., Schafer, M.K., Eiden, L.E., Monyer, H. & Weihe, E. (2008) Sweat gland innervation is pioneered by sympathetic neurons expressing a cholinergic/noradrenergic co-phenotype in the mouse. Neuroscience, 156, 310-318.
116. Schütz, B., Schäfer, M.K.H., Eiden, L.E. & Weihe, E. (1998) Vesicular amine transporter expression and isoform selection in developing brain, peripheral nervous system and gut. Brain Res. Dev. Brain Res., 106, 181-204.
117. 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.
118. Shah, N.M., Groves, A.K. & Anderson, D.J. (1996) Alternative neural crest cell fates are instructively promoted by TGFb superfamily members. Cell, 85, 331-343.
119. Shin, M.H., Mavila, N., Wang, W.H., Vega Alvarez, S., Hall, M.C. & Andrisani, O.M. (2009) Time-dependent activation of Phox2a by the cyclic AMP pathway modulates onset and duration of p27Kip1 transcription. Mol. Cell. Biol., 29, 4878-4890.
120. Shirasaki, R. & Pfaff, S.L. (2002) Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci., 25, 251-281.
121. 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.
122. Stanke, M., Stubbusch, J. & Rohrer, H. (2004) Interaction of Mash1 and Phox2b in sympathetic neuron development. Mol. Cell. Neurosci., 25, 374-382.
123. Stanke, M., Duong, C.V., Pape, M., Geissen, M., Burbach, G., Deller, T., Gascan, H., Otto, C., Parlato, R., Schütz, G. & Rohrer, H. (2006) Target-dependent specification of the neurotransmitter phenotype: cholinergic differentiation of sympathetic neurons is mediated in vivo by gp130 signaling. Development, 133, 141-150.
124. Stemple, D.L. & Anderson, D.J. (1992) Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell, 71, 973-985.
125. Stern, C.D., Artinger, K.B. & Bronner-Fraser, M. (1991) Tissue interactions affecting the migration and differentiation of neural crest cells in the chick embryo. Development, 113, 207-216.
126. Stewart, R.A., Arduini, B.L., Berghmans, S., George, R.E., Kanki, J.P., Henion, P.D. & Look, A.T. (2006) Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Dev. Biol., 292, 174-188.
127. Straub, J.A., Sholler, G.L. & Nishi, R. (2007) Embryonic sympathoblasts transiently express TrkB in vivo and proliferate in response to brain-derived neurotrophic factor in vitro. BMC dev. biol., 7, 10.
128. Takahashi, T., Nowakowski, R.S. & Caviness, V.S. Jr (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J. Neurosci., 16, 6183-6196.
129. Teillet, M.-A. & Le Douarin, N.M. (1983) Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev. Biol., 98, 192-211.
130. Tsarovina, K., Pattyn, A., Stubbusch, J., Müller, F., Van der Wees, J., Schneider, C., Brunet, J.F. & Rohrer, H. (2004) Essential role of Gata transcription factors in sympathetic neuron development. Development, 131, 4775-4786.
131. 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.
132. Tsarovina, K., Reiff, T., Stubbusch, J., Kurek, D., Grosveld, F.G., 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.
133. Tyrrell, S. & Landis, S.C. (1994a) The appearance of NPY and VIP in sympathetic neuroblasts and subsequent alterations in their expression. J. Neurosci., 14, 4529-4547.
134. Tyrrell, S. & Landis, S.C. (1994b) Disruption of target interactions prevents the development of enkephalin immunoreactivity in sympathetic neurons. J. Neurosci., 14, 5708-5721.
135. Varley, J.E. & Maxwell, G.D. (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.
136. Varley, J.E., Wehby, R.G., Rueger, D.C. & Maxwell, G.D. (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.
137. Vrieseling, E. & Arber, S. (2006) Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell, 127, 1439-1452.
138. Wakamatsu, Y., Maynard, T.M. & Weston, J.A. (2000) Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development, 127, 2811-2821.
139. Weston, J.A. & Butler, S.L. (1966) Temporal factors affecting localization of neural crest cells in the chicken embryo. Dev. Biol., 14, 246-266.
140. Wildner, H., Gierl, M.S., 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.
141. Wilson, Y.M., Richards, K.L., Ford-Perriss, M.L., Panthler, J.J. & Murphy, M. (2004) Neural crest cell lineage segregation in the mouse neural tube. Development, 131, 6153-6162.
142. Woldeyesus, M.T., Britsch, S., Riethmacher, D., Xu, L., Sonnenberg-Riethmacher, E., Abou-Rebyeh, F., Harvey, R., Caroni, P. & Birchmeier, C. (1999) Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev., 13, 2538-2548.
143. Yang, C., Kim, H.-S., Seo, H., Kim, C.-H., Brunet, J.-F. & Kim, K.-S. (1998a) Paired-like homeodomain proteins, Phox2a and Phox2b, are responsible for noradrenergic cell-specific transcription of the dopamine b-hydroxylase gene. J. Neurochem., 71, 1813-1826.
144. Yang, C., Kim, H.-S., Seo, H. & Kim, K.-S. (1998b) Identification and characterization of potential cis-regulatory elements governing transcriptional activation of the rat tyrosine hydroxylase gene. J. Neurochem., 71, 1358-1368.
145. Zackenfels, K., Oppenheim, R.W. & 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.
146. Zhang, T., Wang, H., Saunee, N.A., Breslin, M.B. & Lan, M.S. (2010) Insulinoma-associated antigen-1 zinc-finger transcription factor promotes pancreatic duct cell trans-differentiation. Endocrinology, 151, 2030-2039.
147. Zirlinger, M., Lo, L.C., 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.