Zebrafish diencephalic A11-related dopaminergic neurons share a conserved transcriptional network with neuroendocrine cell lineages

Development

Volumn 136, Issue 6, 2009, Pages 1007-1017

  Löhr, Heiko ^a   Ryu, Soojin ^a,b   Driever, Wolfgang ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

arnt2; Diencephalon; Dopaminergic neurons; Hypothalamus; Neural differentiation; Neurosecretory cells; otp; sim1

Indexed keywords

ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR 2; CARRIER PROTEIN; CELL PROTEIN; HOMEODOMAIN PROTEIN; HYPOXIA INDUCIBLE FACTOR 1BETA; NEUROHORMONE; SINGLE MINDED 1 PROTEIN; TRANSCRIPTION FACTOR ORTHOPEDIA; UNCLASSIFIED DRUG; ARNT2 PROTEIN, ZEBRAFISH; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DOPAMINE; REPRESSOR PROTEIN; SIM1 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LINEAGE; CELL SPECIFICITY; CONTROLLED STUDY; DIENCEPHALON; DOPAMINERGIC NERVE CELL; EMBRYO; GENE OVEREXPRESSION; GENE REGULATORY NETWORK; GENETIC CONSERVATION; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; NERVE CELL DIFFERENTIATION; NEUROSECRETORY CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ZEBRA FISH; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; NERVE CELL; NUCLEOTIDE SEQUENCE; PRENATAL DEVELOPMENT; SECRETION;

DANIO RERIO; VERTEBRATA;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; DIENCEPHALON; DOPAMINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUTATION; NEUROENDOCRINE CELLS; NEURONS; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 66149116429     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.033878     Document Type: Article

References (62)

1. Acampora, D., Postiglione, M., Avantaggiato, V., Di Bonito, M., Vaccarino, F., Michaud, J. and Simeone, A. (1999). Progressive impairment of developing neuroendocrine cell lineages in the hypothalamus of mice lacking the Orthopedia gene. Genes Dev. 13, 2787-2800.
2. Acampora, D., Postiglione, M. P., Avantaggiato, V., Di Bonito, M. and Simeone, A. (2000). The role of Otx and Otp genes in brain development. Int. J. Dev. Biol. 44, 669-677.
3. Andreasen, E. A., Spitsbergen, J. M., Tanguay, R. L., Stegeman, J. J., Heideman, W. and Peterson, R. E. (2002). Tissue-specific expression of AHR2, ARNT2, and CYP1A in zebrafish embryos and larvae: effects of developmental stage and 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. Toxicol. Sci. 68, 403-419.
4. Bjorklund, A. and Skagerberg, G. (1979). Evidence for a major spinal cord projection from the diencephalic A11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing. Brain Res. 177, 170-175.
5. Björklund, A. and Dunnett, S. B. (2007). Dopamine neuron systems in the brain: an update. Trends Neurosci. 30, 194-202.
6. Blechman, J., Borodovsky, N., Eisenberg, M., Nabel-Rosen, H., Grimm, J. and Levkowitz, G. (2007). Specification of hypothalamic neurons by dual regulation of the homeodomain protein Orthopedia. Development 134, 4417-4426.
7. Chandrasekar, G., Lauter, G. and Hauptmann, G. (2007). Distribution of corticotropin-releasing hormone in the developing zebrafish brain. J. Comp. Neurol. 505, 337-351.
8. Clemens, S., Rye, D. and Hochman, S. (2006). Restless legs syndrome: revisiting the dopamine hypothesis from the spinal cord perspective. Neurology 67, 125-130.
9. Crews, S. T. and Fan, C. M. (1999). Remembrance of things PAS: regulation of development by bHLH-PAS proteins. Curr. Opin. Genet. Dev. 9, 580-587.
10. Del Giacco, L., Sordino, P., Pistocchi, A., Andreakis, N., Tarallo, R., Di Benedetto, B. and Cotelli, F. (2006). Differential regulation of the zebrafish orthopedia1 gene during fate determination of diencephalic neurons. BMC Dev. Biol. 6, 50.
11. Devos, N., Deflorian, G., Biemar, F., Bortolussi, M., Martial, J. A., Peers, B. and Argenton, F. (2002). Differential expression of two somatostatin genes during zebrafish embryonic development. Mech. Dev. 115, 133-137.
12. Diaz, M. L., Becerra, M., Manso, M. J. and Anadon, R. (2002). Distribution of thyrotropin-releasing hormone (TRH) immunoreactivity in the brain of the zebrafish (Danio rerio). J. Comp. Neurol. 450, 45-60.
13. Eaton, J. and Glasgow, E. (2006). The zebrafish bHLH PAS transcriptional regulator, single-minded 1 (sim1), is required for isotocin cell development. Dev. Dyn. 235, 2071-2082.
14. Eaton, J. and Glasgow, E. (2007). Zebrafish orthopedia (otp) is required for isotocin cell development. Dev. Genes Evol. 217, 149-158.
15. Eaton, J., Holmqvist, B. and Glasgow, E. (2008). Ontogeny of vasotocin-expressing cells in zebrafish: selective requirement for the transcriptional regulators orthopedia and single-minded 1 in the preoptic area. Dev. Dyn. 237, 995-1005.
16. Ema, M., Morita, M., Ikawa, S., Tanaka, M., Matsuda, Y., Gotoh, O., Saijoh, Y., Fujii, H., Hamada, H., Kikuchi, Y. et al. (1996). Two new members of the murine Sim gene family are transcriptional repressors and show different expression patterns during mouse embryogenesis. Mol. Cell. Biol. 16, 5865-5875.
17. Erbel-Sieler, C., Dudley, C., Zhou, Y., Wu, X., Estill, S. J., Han, T., Diaz-Arrastia, R., Brunskill, E. W., Potter, S. S. and McKnight, S. L. (2004). Behavioral and regulatory abnormalities in mice deficient in the NPAS1 and NPAS3 transcription factors. Proc. Natl. Acad. Sci. USA 101, 13648-13653.
18. Fan, C. M., Kuwana, E., Bulfone, A., Fletcher, C. F., Copeland, N. G., Jenkins, N. A., Crews, S., Martinez, S., Puelles, L., Rubenstein, J. L. et al. (1996). Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down syndrome. Mol. Cell Neurosci. 7, 1-16.
19. Filippi, A., Durr, K., Ryu, S., Willaredt, M., Holzschuh, J. and Driever, W. (2007). Expression and function of nr4a2, lmx1b, and pitx3 in zebrafish dopaminergic and noradrenergic neuronal development. BMC Dev. Biol. 7, 135.
20. Fuxe, K., Agnati, L. F., Kalia, M., Goldstein, M., Anderson, K. and Harfstrand, A. (1985). Dopaminergic systems in the brain and pituitary. In The Dopaminergic System: Basic and Clinical Aspects of Neuroscience (ed. B. Halasz, K. Fuxe, L. F. Agnati, M. Kalia, M. Goldstein, K. Anderson and A. Harfstrand). Berlin: Springer-Verlag.
21. Geisler, R., Rauch, G., Geiger-Rudolph, S., Albrecht, A., Van Bebber, F., Berger, A., Busch-Nentwich, E., Dahm, R., Dekens, M. P., Dooley, C. et al. (2007). Large-scale mapping of mutations affecting zebrafish development. BMC Genomics 8, 11.
22. Golling, G., Amsterdam, A., Sun, Z., Antonelli, M., Maldonado, E., Chen, W., Burgess, S., Haldi, M., Artzt, K., Farrington, S. et al. (2002). Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat. Genet. 31, 135-140.
23. Gu, Y. Z., Hogenesch, J. B. and Bradfield, C. A. (2000). The PAS superfamily: sensors of environmental and developmental signals. Annu. Rev. Pharmacol. Toxicol. 40, 519-561.
24. Hallbeck, M. and Blomqvist, A. (1999). Spinal cord-projecting vasopressinergic neurons in the rat paraventricular hypothalamus. J. Comp. Neurol. 411, 201-211.
25. 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.
26. Hosoya, T., Oda, Y., Takahashi, S., Morita, M., Kawauchi, S., Ema, M., Yamamoto, M. and Fujii-Kuriyama, Y. (2001). Defective development of secretory neurones in the hypothalamus of Arnt2-knockout mice. Genes Cells 6, 361-374.
27. Jain, S., Dolwick, K. M., Schmidt, J. V. and Bradfield, C. A. (1994). Potent transactivation domains of the Ah receptor and the Ah receptor nuclear translocator map to their carboxyl termini. J. Biol. Chem. 269, 31518-31524.
28. Jeong, J. Y., Einhorn, Z., Mercurio, S., Lee, S., Lau, B., Mione, M., Wilson, S. W. and Guo, S. (2006). Neurogenin1 is a determinant of zebrafish basal forebrain dopaminergic neurons and is regulated by the conserved zinc finger protein Tof/Fezl. Proc. Natl. Acad. Sci. USA 103, 5143-5148.
29. Kaslin, J. and Panula, P. (2001). Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J. Comp. Neurol. 440, 342-377.
30. Keith, B., Adelman, D. M. and Simon, M. C. (2001). Targeted mutation of the murine arylhydrocarbon receptor nuclear translocator 2 (Arnt2) gene reveals partial redundancy with Arnt. Proc. Natl. Acad. Sci. USA 98, 6692-6697.
31. Kerman, I. (2008). Organization of brain somatomotor-sympathetic circuits. Exp. Brain Res. 187, 1-16.
32. Kewley, R. (2004). The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int. J. Biochem. Cell Biol. 36, 189-204.
33. Kim, C. H., Bae, Y. K., Yamanaka, Y., Yamashita, S., Shimizu, T., Fujii, R., Park, H. C., Yeo, S. Y., Huh, T. L., Hibi, M. et al. (1997). Overexpression of neurogenin induces ectopic expression of HuC in zebrafish. Neurosci. Lett. 239, 113-116.
34. Knapik, E. W., Goodman, A., Ekker, M., Chevrette, M., Delgado, J., Neuhauss, S., Shimoda, N., Driever, W., Fishman, M. C. and Jacob, H. J. (1998). A microsatellite genetic linkage map for zebrafish (Danio rerio). Nat. Genet. 18, 338-343.
35. Krisch, B. (1981). Somatostatin-immunoreactive fiber projections into the brain stem and the spinal cord of the rat. Cell Tissue Res. 217, 531-552.
36. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C. B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
37. Langheinrich, U., Hennen, E., Stott, G. and Vacun, G. (2002). Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr. Biol. 12, 2023-2028.
38. Marin, F., Herrero, M. T., Vyas, S. and Puelles, L. (2005). Ontogeny of tyrosine hydroxylase mRNA expression in mid- and forebrain: neuromeric pattern and novel positive regions. Dev. Dyn. 234, 709-717.
39. McLean, D. L. and Fetcho, J. R. (2004). Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish. J. Comp. Neurol. 480, 38-56.
40. Michaud, J. L. (2001). The developmental program of the hypothalamus and its disorders. Clin. Genet. 60, 255-263.
41. Michaud, J., Rosenquist, T., May, N. and Fan, C. (1998). Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. Genes Dev. 12, 3264-3275.
42. Michaud, J., Derossi, C., May, N., Holdener, B. and Fan, C. (2000). ARNT2 acts as the dimerization partner of SIM1 for the development of the hypothalamus. Mech. Dev. 90, 253-261.
43. Nakai, S., Kawano, H., Yudate, T., Nishi, M., Kuno, J., Nagata, A., Jishage, K., Hamada, H., Fujii, H., Kawamura, K. et al. (1995). The POU domain transcription factor Brn-2 is required for the determination of specific neuronal lineages in the hypothalamus of the mouse. Genes Dev. 9, 3109-3121.
44. Prakash, N. and Wurst, W. (2006). Development of dopaminergic neurons in the mammalian brain. Cell Mol. Life Sci. 63, 187-206.
45. Puelles, L. and Verney, C. (1998). Early neuromeric distribution of tyrosine-hydroxylase -immunoreactive neurons in human embryos. J. Comp. Neurol. 394, 283-308.
46. Rink, E. and Wullimann, M. F. (2002). Development of the catecholaminergic system in the early zebrafish brain: an immunohistochemical study. Brain Res. Dev. Brain Res. 137, 89-100.
47. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A. and Ekker, S. C. (2007). p53 activation by knockdown technologies. PLoS Genet. 3, e78.
48. Rose, J. D. and Moore, F. L. (2002). Behavioral neuroendocrinology of vasotocin and vasopressin and the sensorimotor processing hypothesis. Front. Neuroendocrinol. 23, 317-341.
49. Ryu, S., Holzschuh, J., Mahler, J. and Driever, W. (2006). Genetic analysis of dopaminergic system development in zebrafish. J. Neural. Transm. 70, 61-66.
50. Ryu, S., Mahler, J., Acampora, D., Holzschuh, J., Erhardt, S., Omodei, D., Simeone, A. and Driever, W. (2007). Orthopedia homeodomain protein is essential for diencephalic dopaminergic neuron development. Curr. Biol. 17, 873-880.
51. Sawchenko, P. E. (1987). Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus. Brain Res. 437, 253-263.
52. Schonemann, M. D., Ryan, A. K., McEvilly, R. J., O'Connell, S. M., Arias, C. A., Kalla, K. A., Li, P., Sawchenko, P. E. and Rosenfeld, M. G. (1995). Development and survival of the endocrine hypothalamus and posterior pituitary gland requires the neuronal POU domain factor Brn-2. Genes Dev. 9, 3122-3135.
53. Sesack, S. R. and Carr, D. B. (2002). Selective prefrontal cortex inputs to dopamine cells: implications for schizophrenia. Physiol. Behav. 77, 513-517.
54. Sharp, Z. D. and Morgan, W. W. (1996). Brain POU-er. BioEssays 18, 347-350.
55. Smeets, W. J. and Gonzalez, A. (2000). Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res. Brain Res. Rev. 33, 308-379.
56. Takada, M., Li, Z. K. and Hattori, T. (1988). Single thalamic dopaminergic neurons project to both the neocortex and spinal cord. Brain Res. 455, 346-352.
57. Tanguay, R. L., Andreasen, E., Heideman, W. and Peterson, R. E. (2000). Identification and expression of alternatively spliced aryl hydrocarbon nuclear translocator 2 (ARNT2) cDNAs from zebrafish with distinct functions. Biochim. Biophys. Acta 1494, 117-128.
58. Taylor, B. L. and Zhulin, I. B. (1999). PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63, 479-506.
59. Teh, C. H., Loh, C., Lam, K. K., Loo, J., Yan, T. and Lim, T. (2007). Neuronal PAS domain protein 1 regulates tyrosine hydroxylase level in dopaminergic neurons. J. Neurosci. Res. 85, 1762-1773.
60. Treier, M. and Rosenfeld, M. G. (1996). The hypothalamic-pituitary axis: co-development of two organs. Curr. Opin. Cell Biol. 8, 833-843.
61. Wang, W. and Lufkin, T. (2000). The murine Otp homeobox gene plays an essential role in the specification of neuronal cell lineages in the developing hypothalamus. Dev. Biol. 227, 432-449.
62. Westerfield, M. (2000). The Zebrafish Book: A Guide For The Laboratory Use Of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.