The bHLH transcription factor hand2 is essential for noradrenergic differentiation of sympathetic neurons

Development

Volumn 133, Issue 20, 2006, Pages 4015-4024

  Lucas, Marsha E ^a   Müller, Frank ^b,c   Rüdiger, Roland ^b   Henion, Paul D ^a   Rohrer, Hermann ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Dopamine hydroxylase; Gata2; Hand2; Phox2b; Tyrosine hydroxylase; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN; DOPAMINE BETA MONOOXYGENASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR HAND2; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL AGGREGATION; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE OVEREXPRESSION; IN SITU HYBRIDIZATION; LOCUS CERULEUS; MARKER GENE; NERVE CELL DIFFERENTIATION; NERVE FUNCTION; NONHUMAN; NORADRENERGIC NERVE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; SYMPATHETIC GANGLION; ZEBRA FISH;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; GANGLIA, SYMPATHETIC; GATA2 TRANSCRIPTION FACTOR; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; NEURONS; NOREPINEPHRINE; TRANSCRIPTION FACTOR AP-2; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 33751036180     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02574     Document Type: Article

References (60)

1. Adachi, M. and 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. Alexander, J., Stainier, D. Y. and Yelon, D. (1998). Sreening mosaic F1 females for mutations affecting zebrafish heart induction and patterning. Dev. Genet. 22, 288-299.
3. Allende, M. L. and Weinberg, E. S. (1994). The expression pattern of two zebrafish achaete-scute Homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev. Biol. 166, 509-530.
4. An, M., Luo, R. and Henion, P. D. (2002). Differentiation and maturation of zebrafish dorsal root and sympathetic ganglion neurons. J. Comp. Neurol. 446, 267-275.
5. Barallo-Gimeno, A., Holzschuh, J., Driever, W. and Knapik, E. W. (2004). Neural crest survival and differentiation in zebrafish depends on mont blanc/tfap2a gene function. Development 131, 1463-1477.
6. Bixby, S., Kruger, G. M., Mosher, J. T., Joseph, N. M. and Morrison, S. J. (2002). Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 35, 643-656.
7. Bruneau, B. G., Bao, Z.-Z., Tanaka, M., Schott, J.-J., Izumo, S., Cepko, C. L., Seidman, J. G. and Seidman, C. E. (2000). Cardiac expression of the ventricle-specific homeobox gene lrx4 is modulated by Nkx2-5 and dHand. Dev. Biol. 217, 266-277.
8. Coppola, E., Pattyn, A., Guthrie, S. C., Goridis, C. and Studer, M. (2005). Reciprocal gene replacements reveal unique functions for Phox2 paralogous homeobox genes during neural differentiation. EMBO J. 24, 4392-4403.
9. Dai, Y. S., Cserjesi, P., Markham, B. E. and Molkentin, J. D. (2002). The transcription factors GATA4 and dHAND physically interact to synergistically activate cardiac gene expression through a p300-dependent mechanism. J. Biol. Chem. 277, 24390-24398.
10. Dai, Y.-S., Hao, J., Bonin, C., Morikawa, Y. and Cserjesi, P. (2004). JAB1 enhances HAND2 transcriptional activity by regulating HAND2 DNA binding. J. Neurosci. Res. 76, 613-622.
11. Duff, R. S., Langtimm, C. J., Richardson, M. K. and Sieber-Blum, M. (1991). In vitro clonal analysis of progenitor cell patterns in dorsal root and sympathetic ganglia of the quail. Dev. Biol. 147, 451-459.
12. Firulli, A. B. (2003). A HANDful of questions: the molecular biology of the heart and neural crest derivatives (HAND)-subclass of basic helix-loop-helix transcription factors. Gene 312, 27-40.
13. Goridis, C. and Rohrer, H. (2002). Specification of catecholaminergic and serotonergic neurons. Nat. Rev. Neurosci. 3, 531-541.
14. Greco, D., Zellmer, E., Zhang, Z. and Lewis, E. (1995). Transcription factor AP-2 regulates expression of the dopamine beta-hydoxylase gene. J. Neurochem. 65, 510-516.
15. Guillemot, F., Lo, L.-C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993). Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476.
16. Guo, S., Wilson, S. W., Cooke, S., Chitnis, A. B., Driever, W. and Rosenthal, A. (1999). Mutations in the zebrafish unmask shared regulatory pathways controlling the development of catecholaminergic neurons. Dev. Biol. 208, 473-487.
17. Hirsch, M. R., Tiveron, M. C., Guillemot, F, Brunet, J. F. and Goridis, C. (1998). Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125, 599-608.
18. Holzschuh, J., Ryu, S., Aberger, F. and Driever, W. (2001). Dopamine transporter expression distinguishes dopaminergic neurons from other catecholaminergic neurons in the developing zebrafish embryo. Mech. Dev. 101, 237-243.
19. Holzschuh, J., Barrallo-Gimeno, A., Ettl, A. K., Durr, K., Knapik, E. W. and Driever, W. (2003). Noradrenergic neurons in zebrafish hindbrain are induced by retinoic acid and require tfap2a for expression of the neurotransmitter phenotype. Development 130, 5741-5754.
20. Howard, M. J. (2005). Mechanisms and perspectives on differentiation of autonomic neurons. Dev. Biol. 277, 271-286.
21. Howard, M. J. and Cserjesi, P. (1996). Chicken eHand and dHand influence neural crest cell differentiation. Soc. Neurosci. Abstr. 22, 21.2.
22. Howard, M., Foster, D. N. and Cserjesi, P. (1999). Expression of Hand gene products may be sufficient for the differentiation of avian neural crest-derived cells into catecholaminergic neurons in culture. Dev. Biol. 215, 62-77.
23. Howard, M. J., Stanke, M., Schneider, C., Wu, X and Rohrer, H. (2000). The transcription factor dHAND is a downstream effector of BMPs in sympathetic neuron specification. Development 127, 4073-4081.
24. Kim, C. H., Ueshima, E., Muraoka, O., Tanaka, H., Yeo, S. Y., Huh, T. L. and Mikki, N. (1996). Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci. Lett. 216, 109-112.
25. Kim, H.-S., Seo, H., Yang, C., Brunet, J.-F. and Kim, K.-S. (1998). Noradrenergic-specific transcription of the dopamine b-hydroxylase gene requires synergy of multiple cis-acting elements including at least two Phox2a-binding sites. J. Neurosci. 18, 8247-8260.
26. Kim, H.-S., Hong, S. J., LeDoux, M. S. and Kim, K.-S. (2001). Regulation of the tyrosine hydroxylase and dopamine β-hydroxylase genes by the transcription factor AP-2. J. Neurochem. 76, 280-294.
27. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
28. Knight, R. D., Nair, S., Nelson, S. S., Afshar, A., Javidan, Y., Geisler, R., Rauch, G.-D. and Schilling, T. F. (2003). lockjaw encodes a zebrafish tfap2a required for early neural crest development. Development 130, 5755-5768.
29. Lee, V. M., Bronner-Fraser, M. and Baker, C. V. H. (2005). Restricted response of mesencephalic neural crest to sympathetic differentiation signals to the trunk. Dev. Biol. 278, 175-192.
30. Le Lièvre, C. S., Schweizer, G. G., Ziller, C. M. and LeDouarin, N. M. (1980). Restrictions of developmental capabilities in neural crest cell derivatives as tested by in vivo transplantation experiments. Dev. Biol. 77, 362-378.
31. Lim K.-C., Lakshmanan, G., Crawford, S. E., Gu, Y., Grosveld, F. and Engel, J. D. (2000). Gata3 loss leads to embryonic lethality due to noradrenaline deficiency of the sympathetic nervous system. Nat. Genet. 25, 209-212.
32. Lo, L. C., Tiveron, M. C. and 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.
33. Lo, L. C., Morin, X., Brunet, J. F. and Anderson, D. J. (1999). Specification of neurotransmitter identity by Phox2 proteins in neural crest stem cells. Neuron 22, 693-705.
34. McFadden, D. G., McAnally, J., Richardson, J. A., Charité, J. and Olson, E. N. (2002). Misexpression of dHAND induces ectopic digits in the developing limb bud in the absence of direct DNA binding. Development 129, 3077-3088.
35. Morin, X, Cremer, H., Hirsch, M. R., Kapur, R. P., Goridis, C. and Brunet, J. F. (1997). Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 18, 411-423.
36. Müller, F. and Rohrer, H. (2002). Molecular control of ciliary neuron development: BMPs and downstream transcriptional control in the parasympathetic lineage. Development 129, 5707-5717.
37. O'Brien, E. K., d'Alencon, C., Bonde, G., Li, W., Schoenebeck, J., Allende, M. L., Gelb, B. D., Yelon, D., Eisen, J. S. and Cornell, R. A. (2004). Transcription factor Ap-2α is necessary for development of embryonic melanophores, autonomic neurons and pharyngeal skeleton in zebrafish. Dev. Biol. 265, 246-261.
38. Pattyn, A., Morin, X., Cremer, H., Goridis, C. and Brunet, J. F. (1997). Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124, 4065-4075.
39. Pattyn, A., Morin, X., Cremer, H., Goridis, C. and 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.
40. Pattyn, A., Hirsch, M. R., Goridis, C. and Brunet, J. F. (2000a). Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development 127, 1349-1358.
41. Pattyn, A., Goridis, C. and Brunet, J. F. (2000b). Specification of the central noradrenergic phenotype by the homeobox gene Phox2b. Mol. Cell. Neurosci. 15, 235-243.
42. Raible, D. W. and Eisen, J. S. (1994). Restriction of neural crest cell fate in the trunk of the embryonic zebrafish. Development 120, 495-503.
43. Reissmann, E., Ernsberger, U., Francis-West, P. H., Rueger, D., Brickell, P. M. and 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.
44. Rohrer, H. (2003). The role of bone morphogenetic proteins in sympathetic neuron development. Drug News Perspect. 16, 589-596.
45. Rychlik, J. L., Gerbasi, V. and Lewis, E. J. (2003). The interaction between dHand and Arix at the dopamine b-hydroxylase promotor region is independent of direct dHand binding to DNA. J. Biol. Chem. 278, 49652-49660.
46. Schneider, C., Wicht, H., Enderich, J., Wegner, M. and Rohrer, H. (1999). Bone morphogenetic proteins are required in vivo for the generation of sympathetic neurons. Neuron 24, 861-870.
47. Srivastava, D. (1999). HAND proteins: Molecular mediators of cardiac development and congenital disease. Trends Cardiovasc. Med. 9, 11-18.
48. Srivastava, D., Cserjesi, P. and Olson, E. N. (1995). A subclass of bHLH proteins required for cardiac morphogenesis. Science 270, 1995-1999.
49. Stanke, M., Junghans, D., Geissen, M., Goridis, C., Ernsberger, U. and Rohrer, H. (1999). The Phox2 homeodomain proteins are sufficient to promote the development of sympathetic neurons. Development 126, 4087-4094.
50. Stanke, M., Stubbusch, J. and Rohrer, H. (2004). Interaction of Mash1 and Phox2b in sympathetic neuron development. Mol. Cell. Neurosci. 25, 374-382.
51. Stewart, R. A., Look, A. T., Kanki, J. P. and Henion, P. D. (2004). Development of the peripheral sympathetic nervous system in zebrafish. Methods Cell Biol, 76, 236-258.
52. Swanson, D. J., Zellmer, E. and Lewis, E. J. (1997). The homeodomain protein arix interacts synergistically with cyclic AMP to regulate expression of neurotransmitter biosynthetic genes. J. Biol. Chem. 272, 27382-27392.
53. Thisse, C., Thise, B., Schilling, T. F. and Postlethwait, J. H. (1993). Structure of the zebrafish snail 1 gene and ist expression in wild-type, spade tail, and no-tail mutant embryos. Development 119, 1203-1215.
54. Tsarovina, K., Pattyn, A., Stubbusch, J., Müller, F., Van der Wees, J., Schneider, C., Brunet J.-F. and Rohrer, H. (2004). Essential role of Gata transcription factors in sympathetic neuron development. Development 131, 4775-4786.
55. Wu, X. and Howard, M. J. (2002). Transcripts encoding HAND genes are differentially expressed and regulated by BMP4 and GDNF in developing avian gut. Gene Expr. 10, 279-293.
56. Xu, H. M., Firulli, A. B., Zhang, X. T. and Howard, M. J. (2003). HAND2 synergistically enhances transcription of dopamine-b-hydroxylase in the presence of Phox2a. Dev. Biol. 262, 183-193.
57. Yamagishi, H., Garg, V., Matsuoka, R., Thomas, T. and Srivastava, D. (1999). A molecular pathway revealing a genetic basis for human cardiac and craniofacial defects. Science 283, 1158-1161.
58. Yang, C., Kim, H.-S., Seo, H. and Kim, K.-S. (1998). Identification and characterization of potential cis-regulatory elements governing transcriptional activation of the rat tyrosine hydroxylase gene. J. Neurochem. 71, 1358-1368.
59. Yelon, D., Ticho, B., Halpern, M. E., Ruvinsky, I., Ho, R. K., Silver, L. M. and Stainier, D. Y. R. (2000). The bHLH transcription factor Hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127, 2573-2582.
60. Zellmer, E., Zhang, Z., Greco, D., Rhodes, J., Cassel, S. and Lewis, E. J. (1995). A homeodomain protein selectively expressed in noradrenergic tissue regulates transcription of neurotransmitter biosynthetic genes. J. Neurosci. 15, 8109-8120.