Non-molting glossy/shroud encodes a short-chain dehydrogenase/reductase that functions in the 'Black Box' of the ecdysteroid biosynthesis pathway

Development

Volumn 137, Issue 12, 2010, Pages 1991-1999

  Niwa, Ryusuke ^a   Namiki, Toshiki ^b   Ito, Katsuhiko ^c   Shimada Niwa, Yuko ^a   Kiuchi, Makoto ^b   Kawaoka, Shinpei ^c   Kayukawa, Takumi ^b   Banno, Yutaka ^d   Fujimoto, Yoshinori ^e   Shigenobu, Shuji ^f   Kobayashi, Satoru ^f   Shimada, Toru ^c   Katsuma, Susumu ^c   Shinoda, Tetsuro ^b  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^f OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

Author keywords

Black box; Bombyx mori; Drosophila melanogaster; Ecdysone; Halloween mutant; Prothoracic gland; Short chain dehydrogenase reductase

Indexed keywords

7 DEHYDROCHOLESTEROL; CHOLESTEROL; ECDYSONE; ECDYSTEROID; HORMONE PRECURSOR; MUTANT PROTEIN; NON MOLTING GLOSSY PROTEIN; OXIDOREDUCTASE; SHROUD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; FEMALE; GENE FUNCTION; GENE ISOLATION; GENE LOCUS; GENE OVEREXPRESSION; GENETIC CODE; HORMONE DEFICIENCY; HORMONE SYNTHESIS; LETHALITY; LOSS OF FUNCTION MUTATION; MALE; MOLECULAR CLONING; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PHENOTYPE; PRIORITY JOURNAL; SILKWORM; STEROIDOGENESIS;

ANIMALS; BOMBYX; DEHYDROCHOLESTEROLS; DROSOPHILA MELANOGASTER; ECDYSONE; ECDYSTEROIDS; MOLTING; OXIDOREDUCTASES;

BOMBYX MORI; DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 77953052425     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.045641     Document Type: Article

References (50)

1. Blais, C., Dauphin-Villemant, C., Kovganko, N., Girault, J. P., Descoins, C., Jr and Lafont, R. (1996). Evidence for the involvement of 3-oxo-delta4 intermediates in ecdysteroid biosynthesis. Biochem. J. 320, 413-419. (Pubitemid 26417760)
2. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
3. Chávez, V. M., Marques, G., Delbecque, J. P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J. E. and O'Connor, M. B. (2000). The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development 127, 4115-4126.
4. Dauphin-Villemant, C., Bocking, D., Blais, C., Toullec, J. Y. and Lafont, R. (1997). Involvement of a 3beta-hydroxysteroid dehydrogenase activity in ecdysteroid biosynthesis. Mol. Cell. Endocrinol. 128, 139-149.
5. Ghanim, M. and White, K. P. (2006). Genotyping method to screen individual Drosophila embryos prior to RNA extraction. BioTechniques 41, 414-418.
6. Giesen, K., Lammel, U., Langehans, D., Krukkert, K., Bunse, I. and Klämbt, C. (2003). Regulation of glial cell number and differentiation by ecdysone and Fos signaling. Mech. Dev. 120, 401-413.
7. Gilbert, L. I. and Warren, J. T. (2005). A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Vitam. Horm. 73, 31-57.
8. Gilbert, L. I., Rybczynski, R. and Warren, J. T. (2002). Control and biochemical nature of the ecdysteroidogenic pathway. Annu. Rev. Entomol. 47, 883-916.
9. Hudson, S. G. and Goldstein, E. S. (2008). The gene structure of the Drosophila melanogaster proto-oncogene, kayak, and its nested gene, fos-intronic gene. Gene 420, 76-81.
10. Ito, K., Kidokoro, K., Sezutsu, H., Nohata, J., Yamamoto, K., Kobayashi, I., Uchino, K., Kalyebi, A., Eguchi, R., Hara, W. et al. (2008). Deletion of a gene encoding an amino acid transporter in the midgut membrane causes resistance to a Bombyx parvo-like virus. Proc. Natl. Acad. Sci. USA 105, 7523-7527.
11. Ito, K., Katsuma, S., Yamamoto, K., Kadono-Okuda, K., Mita, K. and Shimada, T. (2009). A 25 bp-long insertional mutation in the BmVarp gene causes the waxy translucent skin of the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 39, 287-293.
12. Jürgens, G., Wieschaus, E., Nüsslein-Volhard, C. and Kluding, H. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster II. Zygotic loci on the 3rd chromosome. Roux's Arch. Dev. Biol. 193, 283-295.
13. Kallberg, Y., Oppermann, U., Jörnvall, H. and Persson, B. (2002). Short-chain dehydrogenase/reductases (SDRs): Coenzyme-based functional assignments in completed genomes. Eur. J. Biochem. 269, 4409-4417.
14. Kavanagh, K. L., Jornvall, H., Persson, B. and Oppermann, U. (2008). Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell. Mol. Life Sci. 65, 3895-3906.
15. Kennerdell, J. R. and Carthew, R. W. (2000). Heritable gene silencing in Drosophila using double-stranded RNA. Nat. Biotechnol. 18, 896-898.
16. Kiguchi, K. and Agui, N. (1981). Ecdysteroid levels and developmental events during larval moulting in the silkworm, Bombyx mori. J. Insect Physiol. 27, 805-812.
17. Kiguchi, K., Agui, N., Kawasaki, H. and Kobayashi, H. (1985). Developmental timetable for the last larval and pharate pupal stages in the silkworm, Bombyx mori, with special reference to the correlation between the developmental events and haemolymph ecdysteroid levels. Bull. Sericul. Exp. Stn. 30, 83-100.
18. Lafont, R., Dauphin-Villemant, C., Warren, J. T. and Rees, H. (2005). Ecdysteroid chemistry and biochemistry. In Comprehensive Molecular Insect Science, vol. 3 (ed. L. I. Gilbert, K. Iatrou and S. Gill), pp. 125-195. Oxford: Elsevier.
19. Maróy, P., Kaufmann, G. and Dübendorfer, A. (1988). Embryonic ecdysteroids of Drosophila melanogaster. J. Insect Physiol. 34, 633-637.
20. McBrayer, Z., Ono, H., Shimell, M., Parvy, J. P., Beckstead, R. B., Warren, J. T., Thummel, C. S., Dauphin-Villemant, C., Gilbert, L. I. and O'Connor, M. B. (2007). Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev. Cell 13, 857-871.
21. Mirth, C. K. and Riddiford, L. M. (2007). Size assessment and growth control: how adult size is determined in insects. BioEssays 29, 344-355.
22. Mita, K., Kasahara, M., Sasaki, S., Nagayasu, Y., Yamada, T., Kanamori, H., Namiki, N., Kitagawa, M., Yamashita, H., Yasukochi, Y. et al. (2004). The genome sequence of silkworm, Bombyx mori. DNA Res. 11, 27-35.
23. Nagata, M., Tsuchida, K., Shimizu, K. and Yoshitake, N. (1987). Physiological aspects of nm-g mutant: An ecdysteroid-deficient mutant of the silkworm, Bombyx mori. J. Insect Physiol. 33, 723-727.
24. Namiki, T., Niwa, R., Sakudoh, T., Shirai, K., Takeuchi, H. and Kataoka, H. (2005). Cytochrome P450 CYP307A1/Spook: a regulator for ecdysone synthesis in insects. Biochem. Biophys. Res. Comm. 337, 367-374.
25. Niwa, R., Matsuda, T., Yoshiyama, T., Namiki, T., Mita, K., Fujimoto, Y. and Kataoka, H. (2004). CYP306A1, a cytochrome P450 enzyme, is essential for ecdysteroid biosynthesis in the prothoracic glands of Bombyx and Drosophila. J. Biol. Chem. 279, 35942-35949.
26. Niwa, R., Sakudoh, T., Namiki, T., Saida, K., Fujimoto, Y. and Kataoka, H. (2005). The ecdysteroidogenic P450 Cyp302a1/disembodied from the silkworm, Bombyx mori, is transcriptionally regulated by prothoracicotropic hormone. Insect Mol. Biol. 14, 563-571.
27. Ono, H., Rewitz, K. F., Shinoda, T., Itoyama, K., Petryk, A., Rybczynski, R., Jarcho, M., Warren, J. T., Marques, G., Shimell, M. J. et al. (2006). Spook and Spookier code for stage-specific components of the ecdysone biosynthetic pathway in Diptera. Dev. Biol. 298, 555-570.
28. Petryk, A., Warren, J. T., Marques, G., Jarcho, M. P., Gilbert, L. I., Kahler, J., Parvy, J. P., Li, Y., Dauphin-Villemant, C. and O'Connor, M. B. (2003). Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc. Natl. Acad. Sci. USA 100, 13773-13778.
29. Rewitz, K. F. and Gilbert, L. I. (2008). Daphnia Halloween genes that encode cytochrome P450s mediating the synthesis of the arthropod molting hormone: evolutionary implications. BMC Evol. Biol. 8, 60.
30. Rewitz, K. F., Larsen, M. R., Lobner-Olesen, A., Rybczynski, R., O'Connor, M. B. and Gilbert, L. I. (2009). A phosphoproteomics approach to elucidate neuropeptide signal transduction controlling insect metamorphosis. Insect Biochem. Mol. Biol. 39, 475-483.
31. Riddiford, L. M. (1993). Hormones and Drosophila development. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 899-939. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
32. Shinoda, T. and Itoyama, K. (2003). Juvenile hormone acid methyltransferase: A key regulatory enzyme for insect metamorphosis. Proc. Natl. Acad. Sci. USA 100, 11986-11991.
33. Spindler, K. D., Honl, C., Tremmel, C., Braun, S., Ruff, H. and Spindler-Barth, M. (2009). Ecdysteroid hormone action. Cell. Mol. Life Sci. 66, 3837-3850.
34. Sullivan, A. A. and Thummel, C. S. (2003). Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. Mol. Endocrinol. 17, 2125-2137.
35. Takeda, S., Kiuchi, M. and Ueda, S. (1986). Preparation of anti-20-hydroxyecdysone serum and its application for radioimmunoassay of ecdysteroids in silkworm hemolymph. Bull. Sericul. Exp. Stn. 30, 361-374.
36. Takeuchi, H., Chen, J. H., O'Reilly, D. R., Rees, H. H. and Turner, P. C. (2000). Regulation of ecdysteroid signalling: molecular cloning, characterization and expression of 3-dehydroecdysone 3alpha-reductase, a novel eukaryotic member of the short-chain dehydrogenases/reductases superfamily from the cotton leafworm, Spodoptera littoralis. Biochem. J. 349, 239-245.
37. Tanaka, Y. (1998). Induction of larval ecdysis by ecdysone in the non-molting glossy (nm-g) mutant larvae of Bombyx mori. J. Seric. Sci. Jpn. 67, 109-115.
38. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
39. Thummel, C. S. (2001). Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev. Cell 1, 453-465.
40. Timmons, L., Becker, J., Barthmaier, P., Fyrberg, C., Shearn, A. and Fyrberg, E. (1997). Green fluorescent protein/β-galactosidase double reporters for visualizing Drosophila gene expression patterns. Dev. Genet. 20, 338-347.
41. Warren, J. T. and Hetru, C. (1990). Ecdysone biosynthesis-pathways, enzymes, and the early steps problem. Invertebr. Reprod. Dev. 18, 91-99.
42. Warren, J. T., Petryk, A., Marques, G., Jarcho, M., Parvy, J. P., Dauphin-Villemant, C., O'Connor, M. B. and Gilbert, L. I. (2002). Molecular and biochemical characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 99, 11043-11048.
43. Warren, J. T., Petryk, A., Marques, G., Parvy, J. P., Shinoda, T., Itoyama, K., Kobayashi, J., Jarcho, M., Li, Y., O'Connor, M. B. et al. (2004). Phantom encodes the 25-hydroxylase of Drosophila melanogaster and Bombyx mori: a P450 enzyme critical in ecdysone biosynthesis. Insect Biochem. Mol. Biol. 34, 991-1010.
44. Warren, J. T., O'Connor, M. B. and Gilbert, L. I. (2009). Studies on the black box: Incorporation of 3-oxo-7-dehydrocholesterol into ecdysteroid by Drosophila melanogaster and Manduca sexta. Insect Biochem. Mol. Biol. 39, 677-687.
45. Wu, X., Lukacik, P., Kavanagh, K. L. and Oppermann, U. (2007). SDR-type human hydroxysteroid dehydrogenases involved in steroid hormone activation. Mol. Cell. Endocrinol. 265-266, 71-76.
46. Xia, Q. Y., Wang, J., Zhou, Z. Y., Li, R. Q., Fan, W., Cheng, D. J., Cheng, T. C., Qin, J. J., Duan, J., Xu, H. F. et al. (2008). The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem. Mol. Biol. 38, 1036-1045.
47. Yamamoto, K., Narukawa, J., Kadono-Okuda, K., Nohata, J., Sasanuma, M., Suetsugu, Y., Banno, Y., Fujii, H., Goldsmith, M. R. and Mita, K. (2006). Construction of a single nucleotide polymorphism linkage map for the silkworm, Bombyx mori, based on bacterial artificial chromosome end sequences. Genetics 173, 151-161.
48. Yamamoto, K., Nohata, J., Kadono-Okuda, K., Narukawa, J., Sasanuma, M., Sasanuma, S., Minami, H., Shimomura, M., Suetsugu, Y., Banno, Y. et al. (2008). A BAC-based integrated linkage map of the silkworm Bombyx mori. Genome Biol. 9, R21.
49. Yoshiyama, T., Namiki, T., Mita, K., Kataoka, H. and Niwa, R. (2006). Neverland is an evolutionally conserved Rieske-domain protein that is essential for ecdysone synthesis and insect growth. Development 133, 2565-2574.
50. Zeitlinger, J., Kockel, L., Peverali, F. A., Jackson, D. B., Mlodzik, M. and Bohmann, D. (1997). Defective dorsal closure and loss of epidermal decapentaplegic expression in Drosophila fos mutants. EMBO J. 16, 7393-7401.