A neuropeptide hormone cascade controls the precise onset of post-eclosion cuticular tanning in Drosophila melanogaster

Development

Volumn 134, Issue 24, 2007, Pages 4395-4404

  Davis, Monica M ^a   O'Keefe, Sandra L ^a   Primrose, David A ^a   Hodgetts, Ross B ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Drosophila melanogaster; Eclosion; Tanning; Tyrosine hydroxylase

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE; BURSICON; DOPAMINE; ECDYSONE; NEUROPEPTIDE; SERINE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CUTICLE; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME REGULATION; MOLTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN PIGMENTATION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; DNA PRIMERS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; INSECT HORMONES; MUTATION; NEUROPEPTIDES; RNA; SIGNAL TRANSDUCTION; TYROSINE 3-MONOOXYGENASE;

CRUSTACEA; DROSOPHILA MELANOGASTER;

EID: 38349054387     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.009902     Document Type: Article

References (48)

1. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004). Image processing with Image J. Biophotonics Int. 11, 36-42.
2. Baker, J. D. and Truman, J. W. (2002). Mutations in the Drosophila glycoprotein hormone receptor, rickets, eliminate neuropeptide-induced tanning and selectively block a stereotyped behavioral program. J. Exp. Biol. 205, 2555-2565.
3. Baker, J. D., McNabb, S. L. and Truman, J. W. (1999). The hormonal coordination of behavior and physiology at adult ecdysis in Drosophila melanogaster. J. Exp. Biol. 202, 3037-3048.
4. Bel, Y., Jacobson, K. B., Silva, F. J. and Ferre, J. (1992). Developmental and biochemical studies on the phenylalanine hydroxylation system in Drosophila melanogaster. Insect Biochem. Mol. Biol. 22, 633-638.
5. Birman, S., Morgan, B., Anzivino, M. and Hirsh, J. (1994). A novel and major isoform of tyrosine hydroxylase in Drosophila is generated by alternative RNA processing. J. Biol. Chem. 269, 26559-26567.
6. Cherbas, L., Hu, X., Zhimulev, I., Belyaeva, E. and Cherbas, P. (2003). EcR isoforms in Drosophila: testing tissue-specific requirements by targeted blockade and rescue. Development 130, 271-284.
7. Clark, A. C., del Campo, M. L. and Ewer, J. (2004). Neuroendocrine control of larval ecdysis behavior in Drosophila: complex regulation by partially redundant neuropeptides. J. Neurosci. 24, 4283-4292.
8. Curtis, A. T., Hori, M., Green, J. M., Wolfgang, W. J., Hiruma, K. and Riddiford, L. M. (1984). Ecdysteroid regulation of the onset of cuticular melanization in allatectornized and Black mutant Manduca sexta larvae. J. Insect Physiol. 30, 597-599.
9. Denman, R. B., Dolzhanskaya, N. and Sung, Y. J. (2004). Regulating a translational regulator: mechanisms cells use to control the activity of the fragile X mental retardation protein. Cell, Mol. Life Sci. 61, 1714-1728.
10. Dewey, E. M., McNabb, S. L., Ewer, J., Kuo, G. R., Takanishi, C. L., Truman, J. W. and Honegger, H. W. (2004). Identification of the gene encoding bursicon, an insect neuropeptide responsible for cuticle sclerotization and wing spreading. Curr. Biol. 14, 1208-1213.
11. Dunkley, P. R., Bobrovskaya, L., Graham, M. E., von Nagy-Felsobuki, E. I. and Dickson, P. W. (2004). Tyrosine hydroxylase phosphorylation: regulation and consequences. J. Neurochem. 91, 1025-1043,
12. Enright, A. J., John, B., Gaul, U., Tuschl, T., Sander, C. and Marks, D. S. (2003). MicroRNA targets in Drosophila. Genome Biol. 5, R1.
13. Ewer, J. and Truman, J. W. (1996). Increases in cyclic 3′,5′-guanosine monophosphate (cGMP) occur at ecdysis in an evolutionarily conserved crustacean cardioactive pepticle-immunoreactive insect neuronal network. J. Comp. Neurol. 370, 330-341.
14. Ewer, J., Gammie, S. C. and Truman, J. W. (1997). Control of insect ecdysis by a positive feedback endocrine system: roles of eclosion hormone and ecdysis triggering hormone. J. Exp. Biol. 200, 869-881.
15. Fraenkel, G. and Hsiao, C. (1962). Hormonal and nervous control of tanning in fly. Science 138, 27-29.
16. Fraenkel, G., Hsiao, C. and Seligman, M. (1966). Properties of bursicon: an insect protein hormone that controls cuticular tanning. Science 151, 91-93.
17. Friggi-Grelin, F, Iche, M. and Birman, S. (2003). Tissue-specific developmental requirements of Drosophila tyrosine hydroxylase isoforms. Genesis 35, 260-269.
18. Gammie, S. C. and Truman, J. W. (1997). Neuropeptide hierarchies and the activation of sequential motor behaviors in the hawkmoth, Manduca sexta. J. Neurosci. 17, 4389-4397.
19. Gammie, S. C. and Truman, J. W. (1999). Eclosion hormone provides a link between ecdysis-triggering hormone and crustacean cardioactive peptide in the neuroendocrine cascade that controls ecclysis behavior. J. Exp. Biol. 202, 343-352.
20. Hirsh, J. and Davidson, N. (1981). Isolation and characterization of the Dopa decarboxylase gene of Drosophila metanogaster. Mol. Cell. Biol. 1, 475-485.
21. Horodyski, F. M., Ewer, J., Riddiford, L. M. and Truman, J. W. (1993). Isolation, characterization and expression of the eclosion hormone gene of Drosophila melanogaster. Eur J. Biochem. 215, 221-228,
22. Hufton, S. E., Jennings, I. G. and Cotton, R. G. H. (1995). Structure and function of the aromatic amino acid hydroxylases. Biochem. J. 311, 353-366.
23. Kimura, K. and Truman, J. W. (1990). Postmetamorphic cell death in the nervous and muscular systems of Drosophila melanogaster. J. Neurosci. 10, 403-411
24. Kimura, K., Kodama, A., Hayasaka, Y. and Ohta, T. (2004). Activation of the cAMP/PKA signaling pathway is required for post-ecdysial cell death in wing epidermal cells of Drosophila melanogaster. Development 131, 1597-1606.
25. Kingan, T. G. and Adams, M. E. (2000). Ecdysteroids regulate secretory competence in Inka cells. J. Exp. Biol. 203, 3011-3018.
26. Kingan, I G., Cardullo, R. A. and Adams, M. E. (2001). Signal transduction in eclosion hormone-induced secretion of ecdysis-triggering hormone. J. Biol. Chem. 276, 25136-25142.
27. Kraminsky, G. P., Clark, W. C., Estelle, M. A., Gietz, R. D., Sage, B. A., O'Connor, J. D. and Hodgetts, R. B. (1980). Induction of translatable mRNA for Dopa decarboxylase in Drosophila: an early response to ecdysterone. Proc. Natl. Acad. Sci. USA 77, 4175-4179.
28. Kumer, S. C. and Vrana, K. E. (1996). Intricate regulation of tyrosine hydroxylase activity and gene expression. J. Neurochem. 67, 443-462.
29. Levitt, M., Spector, S., Sjoerdsma, A. and Udenfriend, S. (1965). Elucidation of rate-limiting step in norepinephrine biosynthesis in perfused guinea-pig heart. J. Pharmacol. Exp. Ther. 148, 1-8.
30. Livingstone, M. S. and Tempel, B. L. (1983). Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. Nature 303, 67-70.
31. Luan, H., Lemon, W. C., Peabody, N. C., Pohl, J. B., Zelensky, R K., Wang, D., Nitabach, M. N., Holmes, T. C. and White, B. H. (2006). Functional dissection of a neuronal network required for cutide tanning and wing expansion in Drosophila. J. Neurosci. 26, 573-584.
32. Lunan, K. D. and Mitchell, H. K. (1969). Metabolism of tyrosine- O-phosphate in Drosophila. Arch. Biochem. Biophys. 132, 450-456.
33. Luo, C. W., Dewey, E. M., Sudo, S., Ewer, J., Hsu, S. Y., Honegger, H. W. and Hsueh, A. J. (2005). Bursicon, the insect cuticle-hardening hormone, is a heterodimeric cystine knot protein that activates G protein-coupled receptor LGR2. Proc. Natl. Acad. Sci. USA 102, 2820-2825.
34. McNabb, S. L., Baker, J. D., Agapite, J., Steller, H., Riddiford, L. M. and Truman, J. W. (1997). Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 19, 813-823.
35. Mendive, F. M., Van Loy, T., Claeysen, S., Poels, J., Williamson, M., Hauser F., Grimmelikhuijzen, C. J. P., Vassart, G. and Broeck, J. V. (2005). Drosophila molting neurohormone bursicon is a heterodimer and the natural agonist of the orphan receptor DLGR2. Febs Lett. 579, 2171-2176.
36. Morgan, B. A., Johnson, W. A. and Hirsh, J. (1986). Regulated splicing produces different forms of Dopa decarboxylase in the central nervous system and hypoderm of Drosophila melanogaster, EMBO J. 5, 3335-3342.
37. Nagatsu, T., Levitt, M. and Udenfriend, S. (1964). Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. J. Biol. Chem. 239, 2910-2917.
38. Neckameyer, W. S. and White, K. (1993). Drosophila tyrosine hydroxylase is encoded by the pale locus. J. Neurogenet. 8, 189-199.
39. Park, J. H., Schroeder, A. J., Helfrich-Forster, C., Jackson, F. R. and Ewer, J. (2003). Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development 130, 2645-2656.
40. Park, Y., Filippov, V., Gill, S. S. and Adams, M. E. (2002). Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development 129, 493-503.
41. Riddiford, L. M. (1993). Hormones and Drosophila development. In The Development of Drosophila melanogaster. Vol. 2 (ed. M. Bates and A. M. Arias), pp. 899-939. New York: Cold Spring Harbor Laboratory Press.
42. Scholnick, S. B., Morgan, B. A. and Hirsh, J. (1983). The cloned Dopa decarboxylase gene is developmentally regulated when reintegrated into the Drosophila genome. Cell 34, 37-45.
43. Truman, J. W. (1996). Ecdysis control sheds another layer. Science 271, 40-41.
44. Vie, A., Cigna, M., Toci, R. and Birman, S. (1999). Differential regulation of Drosophila tyrosine hydroxylase isoforms by dopamine binding and cAMP-dependent phosphorylation. J. Biol. Chem. 274, 16788-16795.
45. Wilhelm, J. E. and Smibert, C. A. (2005). Mechanisms of translational regulation in Drosophila, Biol. Cell 97, 235-252.
46. Wright, T. R. (1987). The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv. Genet. 24, 127-222.
47. Wright, T. R., Bewley, G. C. and Sherald, A. F. (1976). The genetics of dopa decarboxylase in Drosophila melanogaster. II. Isolation and characterization of dopa-decarboxylase-deficient mutants and their relationship to the alpha-methyl-dopa-hypersensitive mutants. Genetics 84, 287-310.
48. Zigmond, R. E., Schwarzschild, M. A. and Rittenhouse, A. R. (1989). Acute regulation of tyrosine hydroxylase by nerve activity and by neurotransmitters via phosphorylation. Annu. Rev. Neurosci. 12, 415-461.