Persistent expression of BMP-4 in embryonic chick adrenal cortical cells and its role in chromaffin cell development

Neural Development

Volumn 3, Issue 1, 2008, Pages

  Huber, Katrin ^a   Franke, Aylin ^a   Brühl, Barbara ^a   Krispin, Shlomi ^c   Ernsberger, Uwe ^a   Schober, Andreas ^a   Halbach, Oliver Von Bohlen Und ^a   Rohrer, Hermann ^b   Kalcheim, Chaya ^c   Unsicker, Klaus ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c HEBREW UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; STEROIDOGENIC FACTOR 1; TYROSINE 3 MONOOXYGENASE;

ADRENAL GLAND; ANIMAL; ARTICLE; CELL PROLIFERATION; CHICK EMBRYO; CHO CELL; CHROMAFFIN CELL; CRICETULUS; CYTOLOGY; ELECTRON MICROSCOPY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; NERVE CELL; PREGNANCY; PRENATAL DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYMPATHETIC GANGLION; TISSUE CULTURE TECHNIQUE; ULTRASTRUCTURE;

ADRENAL GLANDS; ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; CELL PROLIFERATION; CHICK EMBRYO; CHO CELLS; CHROMAFFIN CELLS; CRICETINAE; CRICETULUS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GANGLIA, SYMPATHETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICROSCOPY, ELECTRON; NEURONS; PREGNANCY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEROIDOGENIC FACTOR 1; TISSUE CULTURE TECHNIQUES; TYROSINE 3-MONOOXYGENASE;

EID: 56049113492     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-3-28     Document Type: Article

References (51)

1. NM Le Douarin C Kalcheim, The Neural Crest Cambridge: Cambridge University Press 2 1999
2. The chromaffin cell: paradigm in cell, developmental and growth factor biology. K Unsicker, J Anat 1993 183 207 221 8300412
3. Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. E Reissmann U Ernsberger PH Francis-West D Rueger PM Brickell H Rohrer, Development 1996 122 2079 2088 8681789
4. Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. C Schneider H Wicht J Enderich M Wegner H Rohrer, Neuron 1999 24 861 870 10.1016/S0896-6273(00)81033-8 10624949
5. Alternative neural crest cell fates are instructively promoted by TGF beta superfamily members. NM Shah AK Groves DJ Anderson, Cell 1996 85 331 343 10.1016/S0092-8674(00)81112-5 8616889
6. Specification of catecholaminergic and serotonergic neurons. C Goridis H Rohrer, Nat Rev Neurosci 2002 7 531 541 10.1038/nrn871
7. Changes in competence determine the timing of two sequential glucocorticoid effects on sympathoadrenal progenitors. AM Michelsohn DJ Anderson, Neuron 1992 8 589 604 10.1016/0896-6273(92)90285-L 1347997
8. RE Coupland, The Natural History of the Chromaffin Cells London and Colchester: Spottiswoode, Ballanntyne and Co. Ltd 1995
9. The development and maturation of adrenal medullary chromaffin cells of the rat in vivo: a descriptive and quantitative study. RE Coupland A Tomlinson, Int J Dev Neurosci 1989 7 419 438 10.1016/0736-5748(89)90003-8 2816482
10. Molecular markers of sympathoadrenal cells. K Langley NJ Grant, Cell Tissue Res 1999 298 185 206 10.1007/PL00008810 10550645
11. Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: Impairment by glucocorticoids. K Unsicker B Krisch J Otten H Thoenen, Proc Natl Acad Sci USA 1978 75 3498 3502 28526 10.1073/pnas.75.7.3498
12. A bipotential neuroendocrine precursor whose choice of cell fate is determined by NGF and glucocorticoids. DJ Anderson R Axel, Cell 1986 47 1079 1090 10.1016/0092-8674(86)90823-8 2877748
13. Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors and chromaffin cell plasticity. AJ Doupe SC Landis PH Patterson, J Neurosci 1985 5 2119 2142 4020432
14. The determination of the adrenal medullary cell fate during embryogenesis. K Seidl K Unsicker, Dev Biol 1989 136 481 490 10.1016/0012-1606(89)90273-X 2573552
15. Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. S Finotto K Krieglstein A Schober F Deimling K Lindner B Brühl K Beier J Metz JE Garcia-Arraras JL Roig-Lopez P Monaghan W Schmid TJ Cole C Kellendonk F Tronche G Schütz K Unsicker, Development 1999 126 2935 2944 10357937
16. Reduction of endogenous TGF-beta increases proliferation of developing adrenal chromaffin cells in vivo. SE Combs K Krieglstein K Unsicker, J Neurosci Res 2000 59 379 383 10.1002/(SICI)1097-4547(20000201)59:3<379::AID- JNR12>3.0.CO;2-5 10679774
17. Bone: formation by autoinduction. MR Urist, Science 1965 150 893 899 10.1126/science.150.3698.893 5319761
18. Recombinant human bone morphogenetic protein induces bone formation. EA Wang V Rosen JS D'Alessandro M Bauduy P Cordes T Harada DI Israel RM Hewick KM Kerns P LaPan DP Luxenberg D McQuaid IK Moutsatsos J Nove JM Wozney, Proc Natl Acad Sci USA 1990 87 2220 2224 2315314 10.1073/pnas.87.6.2220
19. The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF beta superfamily. DM Kingsley AE Bland JM Grubber PC Marker LB Russell NG Copeland NA Jenkins, Cell 1992 71 399 410 10.1016/0092-8674(92)90510-J 1339316
20. Bone morphogenetic protein signalling and vertebrate nervous system development. A Liu LA Niswander, Nat Rev Neurosci 2005 6 945 954 10.1038/nrn1805 16340955
21. Expression of a constitutively active type I BMP receptor using a retroviral vector promotes the development of adrenergic cells in neural crest cultures. JE Varley CE McPherson H Zou L Niswander GD Maxwell, Dev Biol 1998 196 1 107 118 10.1006/dbio.1998.8853 9527884
22. BMP growth factors and Phox2 transcription factors can induce synaptotagmin I and neurexin I during sympathetic neuron development. H Patzke E Reissmann M Stanke JL Bixby U Ernsberger, Mech Dev 2001 108 149 159 10.1016/S0925-4773(01)00503-2 11578868
23. A series of normal stages in the development of the chick embryo. V Hamburger HL Hamilton, J Exp Zool 1951 88 49 92
24. Neural induction by the secreted polypeptide noggin. TM Lamb AK Knecht WC Smith SE Stachel AN Economides N Stahl GD Yancopolous RM Harland, Science 1993 262 713 718 10.1126/science.8235591 8235591
25. 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. U Ernsberger H Patzke JP Tissier-Seta T Reh C Goridis H Rohrer, Mech Dev 1995 52 125 136 10.1016/0925-4773(95)00396-I 7577670
26. The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. M Stanke D Junghans M Geissen C Goridis U Ernsberger H Rohrer, Development 1999 126 4087 4094 10457017
27. Identification of gene products expressed in the developing chick visual system: characterization of a middle-molecular-weight neurofilament cDNA. D Zopf I Hermans-Borgmeyer ED Gundelfinger H Betz, Genes Dev 1987 1 699 708 10.1101/gad.1.7.699 3123320
28. Bone morphogenetic proteins and a signalling pathway that controls patterning in the developing chick limb. PH Francis MK Richardson PM Brickell C Tickle, Development 1994 120 209 218 8119128
29. The developmental expression of choline acetyltransferase (ChAT) and the neuropeptide VIP in chick sympathetic neurons: evidence for different regulatory events in cholinergic differentiation. U Ernsberger H Patzke H Rohrer, Mech Dev 1997 68 115 126 10.1016/S0925-4773(97)00135-4 9431809
30. Antagonistic roles of full-length N cadherin and its soluble BMP cleavage product in neural crest delamination. I Shoval A Ludwig C Kalcheim, Development 2007 134 491 501 10.1242/dev.02742 17185320
31. A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation. X Luo Y Ikeda KL Parker, Cell 1994 77 481 490 10.1016/0092-8674(94)90211-9 8187173
32. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. F Guillemot LC Lo JE Johnson A Auerbach DJ Anderson AL Joyner, Cell 1993 75 463 476 10.1016/0092-8674(93)90381-Y 8221886
33. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. A Pattyn X Morin H Cremer C Goridis JF Brunet, Nature 1999 399 366 370 10.1038/20700 10360575
34. The sympathoadrenal cell lineage: specification, diversification, and new perspectives. K Huber, Dev Biol 2006 298 335 343 10.1016/j.ydbio.2006.07.010 16928368
35. The chromaffin cell and its development. K Unsicker K Huber G Schütz C Kalcheim, Neurochem Res 2005 30 921 925 10.1007/s11064-005-6966-5 16187226
36. Controlling TGF-beta signalling. J Massagué YG Chen, Genes Dev 2000 14 627 644 10733523
37. The Spemann organizer signal Noggin binds and inactivates bone morphogenetic protein 4. LB Zimmerman JM De Jesús-Escobar RM Harland, Cell 1996 86 599 606 10.1016/S0092-8674(00)80133-6 8752214
38. Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen. U Ernsberger L Esposito S Partimo K Huber A Franke JL Bixby C Kalcheim K Unsicker, Cell Tissue Res 2005 319 1 13 10.1007/s00441-004-0996-1 15565470
39. Lack of an adrenal cortex in Sf1 mutant mice is compatible with the generation and differentiation of chromaffin cells. P Gut K Huber J Lohr B Bruhl S Oberle M Treier U Ernsberger C Kalcheim K Unsicker, Development 2005 132 4611 4619 10.1242/dev.02052 16176945
40. ER Kande JH Schartz TM Jessel, Principles of Neural Science New York: McGraw-Hill 4 2000
41. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. TJ Cole JA Blendy AP Monaghan K Krieglstein W Schmid A Aguzzi G Fantuzzi E Hummler K Unsicker G Schütz, Genes Dev 1995 13 1608 1621 10.1101/gad.9.13.1608
42. Glia induce dendritic growth in cultured sympathetic neurons by modulating the balance between bone morphogenetic proteins (BMPs) and BMP antagonists. PJ Lein HN Beck V Chandrasekaran PJ Gallagher HL Chen Y Lin X Guo PL Kaplan H Tiedge D Higgins, J Neurosci 2002 22 10377 10387 12451137
43. Evidence for an evolutionary conserved role of bone morphogenetic protein growth factors and phox2 transcription factors during noradrenergic differentiation of sympathetic neurons. Induction of a putative synexpression group of neurotransmitter-synthesizing enzymes. U Ernsberger, Eur J Biochem 2000 267 6976 6981 10.1046/j.1432-1327.2000.01827.x 11106406
44. Mechanisms and perspectives on differentiation of autonomic neurons. MJ Howard, Dev Biol 2005 277 271 286 10.1016/j.ydbio.2004.09.034 15617674
45. The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. MJ Howard M Stanke C Schneider X Wu H Rohrer, Development 2000 127 4073 4081 10952904
46. Essential role of Gata transcription factors in sympathetic neuron development. K Tsarovina A Pattyn J Stubbusch F Müller J van der Wees C Schneider JF Brunet H Rohrer, Development 2004 131 4775 4786 10.1242/dev.01370 15329349
47. Development of chick paravertebral sympathetic ganglia. I. Fine structure and correlative histofluorescence of catecholaminergic cells. L Luckenbill-Edds C van Horn, J Comp Neurol 1980 191 65 76 10.1002/cne.901910104 7400392
48. Differentiation of embryonic chick sympathetic neurons in vivo: ultrastructure, and quantitative determinations of catecholamines and somatostatin. S Ross A Fischer K Unsicker, Cell Tissue Res 1990 260 147 159 10.1007/BF00297500 1971197
49. Development of chromaffin cells depends on MASH1 function. K Huber B Bruhl F Guillemot EN Olson U Ernsberger K Unsicker, Development 2002 129 4729 4738 12361965
50. The role of Phox2B in chromaffin cell development. K Huber N Karch U Ernsberger C Goridis Unsicker, Dev Biol 2005 279 501 508 10.1016/j.ydbio.2005. 01.007 15733675
51. Insm1 (IA-1) is a crucial component of the transcriptional network that controls differentiation of the sympatho-adrenal lineage. H Wildner MS Gierl M Strehle P Pla C Birchmeier, Development 2008 135 473 481 10.1242/dev.011783 18094025