Phantom encodes the 25-hydroxylase of Drosophila melanogaster and Bombyx mori: A P450 enzyme critical in ecdysone biosynthesis

Insect Biochemistry and Molecular Biology

Volumn 34, Issue 9, 2004, Pages 991-1010

  Warren, James T ^a   Petryk, Anna ^a,b   Marqués, Guillermo ^c   Parvy, Jean Philippe ^d   Shinoda, Tetsuro ^e   Itoyama, Kyo ^f   Kobayashi, Jun ^g   Jarcho, Michael ^b   Li, Yutai ^a   O'Connor, Michael B ^c   Dauphin Villemant, Chantal ^d   Gilbert, Lawrence I ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d SORBONNE UNIVERSITÉ   (France)

^e NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^f Akita Agric Experiment Station   (Japan)

^g YAMAGUCHI UNIVERSITY   (Japan)

Author keywords

20 hydroxyecdysone; Microsomal CYP enzyme; Prothoracic gland; Ring gland; Steroid molting hormone

Indexed keywords

BOMBYX; BOMBYX MORI; DROSOPHILA MELANOGASTER; HEXAPODA; INSECTA; MELANOGASTER;

EID: 19944373719     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2004.06.009     Document Type: Article

References (62)

1. Adams, M.D., Celniker, S., Holt, R., Evans, C., Gocayne, J., Amanatides, P., Scherer, S., Li, P., Hoskins, R., Galle, R., et al., 2000. The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
2. Baker, K.D., Warren, J.T., Thummel, C., Gilbert, L.I., Mangelsdorf, J., 2000. Transcriptional activation of the Drosophila ecdysone receptor by insect and plant ecdysteroids. Insect Biochem. Mol. Biol. 30, 1037-1043.
3. Bhanot, P., Brink, M., Samos, C., Hsieh, J., Wang, Y., Macke, J., Andrew, D., Nathans, J., Nusse, R., 1996. A new member of the frizzled family from Drosophila functions as a Wingless receptor. Nature (London) 382, 225-230.
4. Bialecki, M., Shilton, A., Fichtenberg, C., Segraves, W., Thummel, C., 2002. Loss of the ecdysteroid-inducible E75A orphan nuclear receptor uncouples molting from metamorphosis in Drosophila. Dev. Cell 3, 209-220.
5. Bollenbacher, W., Faux, A.F., Galbraith, N., Gilbert, L.I., Horn, D.H.S., Wilkie, J.S., 1979. In vitro metabolism of possible ecdysone precursors by prothoracic glands of the tobacco hornworm, Manduca sexta. Steroids 34, 509-526.
6. Bownes, M., Shirras, A., Blair, M., Collins, J., Coulson, A., 1988. Evidence that insect embryogenesis is regulated by ecdysteroids released from yolk proteins. Proc. Natl. Acad. Sci. USA 85, 1554-1557.
7. Brown, G.D., 1998. The biosynthesis of steroids and triterpenoids. Nat. Prod. Rep. 15, 653-696.
8. Brown, N., Kafatos, F., 1988. Functional cDNA libraries from Drosophila embryos. J. Mol. Biol. 203, 425-437.
9. Chang, E.S., Kaufman, W.R., 2004. Endocrinology of Crustacea and Chelicerata. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford. In press.
10. Charles, J.-P., Shinoda, T., Chinzel, Y., 1999. Characterization and DNA-binding properties of GRF, a novel monomeric binding orphan receptor related to GCNF and βFTZ-F1. Eur. J. Biochem. 266, 181-190.
11. Chávez, V.M., Marqués, G., Delbecque, J.P., Kobayashi, K., Hollingsworth, M., Burr, J., Natzle, J., O'Connor, M., 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.
12. Campos-Ortega, J., Hartenstein, V., 1985. The embryonic development of Drosophila melanogaster. Springer, Tokyo Berlin Heidelberg New York.
13. Dai, J.-D., Gilbert, L.I., 1991. Metamorphosis of the corpus allatum and degeneration of the prothoracic glands during the larval-pupal-adult transformation of Drosophila melanogaster: a cytophysiological analysis of the ring gland. Dev. Biol. 144, 309-326.
14. Dauphin-Villemant, C., Böcking, D., Tom, M., Maïbèche, M., Lafont, R., 1999. Cloning of a novel cytochrome P-450 (CYP4C15) differentially expressed in the steroidogenic glands of an arthropod. Biochem. Biophys. Res. Commun. 264, 413-418.
15. Deak, P., Zavorszky, P., Maroy, P., 1988. Moulting hormone regulates its receptor level in Drosophila melanogaster. Insect Biochem. 18, 847-852.
16. Delbecque, J.-P., Weidner, K., Hoffman, K.H., 1990. Alternative sites for ecdysteroid production in insects. Invertebr. Reprod. Dev. 18, 29-42.
17. Feyereisen, R., 2004. Insect cytochrome P450. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 4. Elsevier, Oxford. In press.
18. Gilbert, L.I., 2004. Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Mol. Cell. Endocrinol. 215, 1-10.
19. Gilbert, L.I., Song, Q., Rybczynski, R., 1997. Control of ecdysteroidogenesis: activation and inhibition of prothoracic gland activity. Invertebr. Neurosci. 3, 205-216.
20. Gilbert, L.I., Rybczynski, R., Warren, J.T., 2002. Control and biochemical nature of the ecdysteroidogenic pathway. Annu. Rev. Entomol. 47, 883-916.
21. Grau, V., Gutzeit, H., 1990. Asymmetrically distributed ecdysteroid-related antigens in follicles and young embryos of Drosophila melanogaster. Roux's Arch. Dev. Biol. 198, 295-302.
22. Grieneisen, M., Warren, J.T., Sakurai, S., Gilbert, L.I., 1991. A putative route to ecdysteroids: metabolism of cholesterol in vitro by mildly disrupted prothoracic glands of Manduca sexta. Insect Biochem. 21, 41-51.
23. Grieneisen, M., Warren, J.T., Gilbert, L.I., 1993. Early steps in ecdysteroid biosynthesis: evidence for the involvement of cytochrome P-450 enzymes. Insect Biochem. 23, 13-23.
24. Haerry, T.E., O'Connor, M.B., 2002. Isolation of Drosophila activin and follistatin cDNAs using novel MACH amplification protocols. Gene 291, 85-93.
25. Han, K., 1996. An efficient DDAB-mediated transfection of Drosophila S2 cells. Nucleic Acids Res. 24, 4362-4363.
26. Henrich, V., 2004. The ecdysteroid receptor. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford. In press.
27. Honkakoski, P., Negishi, M., 2000. Regulation of cytochrome P450 (CYP) genes by nuclear receptors. Biochem. J. 347, 321-337.
28. Horn, D.H.S., 1971. The ecdysones. In: Jacobson, M., Crosby, D.G. (Eds.), Naturally Occurring Insecticides. Marcel Dekker, New York, pp. 333-459.
29. Hummel, T., Schimmelpfeng, K., Klambt, C., 1999. Commissure formation in the embryonic CNS of Drosophila. Dev. Biol. 209, 381-398.
30. Jürgens, G., Wieschaus, E., Nüsslein-Volhard, C., Kluding, H., 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II Zygotic loci on the third chromosome. Roux's Arch. Dev. Biol. 193, 283-295.
31. Kappler, C., Kabbouh, M., Hétru, C., Durst, F., Hoffmann, J.A., 1988. Characterization of the three hydroxylases involved in the final steps of biosynthesis of the steroid hormone ecdysone in Locusta migratoria (Insecta, Orthoptera). Steroid Biochem. 31, 891-898.
32. Kiguchi, K., Agui, N., 1981. Ecdysteroid levels and developmental events during larval moulting in the silkworm, Bombyx mori. J. Insect Physiol. 27, 805-812.
33. Kiguchi, K., Agui, N., Kawasaki, H., Kobayashi, H., 1985. Developmental time-table 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. Rep. Sericult. Exp. Stn. 30, 83-100.
34. Kiriishi, S., Rountree, D.B., Sakurai, S., Gilbert, L.I., 1990. Prothoracic gland synthesis of 3-dehydroecdysone and its hemolymph 3β-reductase mediated conversion to ecdysone in representative insects. Experientia 46, 716-721.
35. Kozlova, T., Thummel, C., 2003. Essential roles for ecdysone signaling during Drosophila mid-embryonic development. Science 301, 1911-1914.
36. Kraminsky, G., Clark, W., Estelle, M., Gietz, R., Sage, B., O'Connor, J., Hodgetts, R., 1980. Induction of translatable mRNA for dopa decarboxylase in Drosophila: an early response to ecdysterone. Proc. Natl. Acad. Sci. USA 77, 4175-4179.
37. Lafont, R., Dauphin-Villemant, C., Warren, J.T., Rees, H., 2004. Ecdysteroid chemistry and biochemistry. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford. In press.
38. Lala, D., Syka, P., Lazarchik, S., Mangelsdorf, D., Parker, K., Heyman, R., 1997. Activation of the orphan nuclear receptor steroidogenic factor 1 by oxysterols. Proc. Natl. Acad. Sci. USA 94, 4895-4900.
39. Maroy, P., Koczka, K., Fekete, E., Vargha, J., 1980. Molting hormone titer of D. melanogaster larvae. Dros. Inf. Serv. 55, 98-99.
40. Maroy, P., Kauffmann, G., Dübendorfer, A., 1988. Embryonic ecdysteroids of Drosophila melanogaster. J. Insect Physiol. 34, 633-637.
41. Meister, M.F., Dimarcq, J.-L., Kappler, C., Hétru, C., Lagueux, M., Lanot, R., Luu, B., Hoffmann, J.A., 1985. Conversion of a labelled ecdysone precursor, 2,22,25-trideoxyecdysone, by embryonic and larval tissues of Locusta migratoria. Mol. Cell. Endocrinol. 41, 27-44.
42. Meister, M.F., Brandtner, H., Koolman, J., Hoffmann, J., 1987. Conversion of a radiolabeled putative ecdysone precursor, 2,22,25-trideoxyecdysone (5β-ketodiol) in larvae and pupae of Calliphora vicina. Int. J. Invertebr. Reprod. Dev. 12, 13-28.
43. Nusslein-Volhard, C., Wieschaus, E., Kluding, H., 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux's Arch. Dev. Biol. 183, 267-282.
44. Petryk, A., Warren, J.T., Marqués, G., Jarcho, M.P., Gilbert, L.I., Parvy, J.-P., Dauphin-Villemant, C., O'Connor, M.B., 2003. Shade: 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.
45. Raikhel, A.S., Belles, X., Brown, M.R., 2004. Hormonal control of reproductive processes. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford. In press.
46. Redfern, C.P.F., 1984. Evidence for the presence of makisterone A in Drosophila larvae and the secretion of 20-deoxymakisterone A by the ring gland. Proc. Natl. Acad. Sci. USA 81, 5643-5647.
47. Ross, J., Shimmi, O., Vilmos, P., Petryk, A., Kim, H., Gaudenz, K., Hermanson, S., Ekker, S., O'Connor, M., Marsh, J., 2001. Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410, 479-483.
48. Rybczynski, R., in press. The prothoracicotropic hormone. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford.
49. Sakurai, S., in press. Feedback regulation. In: Gilbert, L.I., Iatrou, K., Gill, S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford.
50. Sakurai, S., Warren, J.T., Gilbert, L.I., 1989. Mediation of ecdysone synthesis in Manduca sexta by a hemolymph enzyme. Arch. Insect Biochem. Physiol. 10, 179-197.
51. Schwartz, L.M., Truman, J.W., 1983. Hormonal control of rates of metamorphic development in the tobacco hornworm, Manduca sexta. Dev. Biol. 99, 103-114.
52. Shinoda, T., Itoyama, K., 2003. Juvenile hormone acid methyltransferase: a key regulatory enzyme for insect metamorphosis. Proc. Natl. Acad. Sci. USA 100, 11986-11991.
53. Sullivan, A.A., Thummel, C.S., 2003. Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. Mol. Endocrinol. 17, 2125-2137.
54. Tsruya, R., Schlesinger, A., Reich, A., Gabay, L., Sapir, A., Shilo, B.-Z., 2002. Intracellular trafficking by Star regulates cleavage of the Drosophila EGF receptor ligand Spitz. Genes Dev. 16, 222-234.
55. Warren, J.T., Gilbert, L.I., 1986. Ecdysone metabolism and distribution during the pupal-adult development of Manduca sexta. Insect Biochem. 16, 65-82.
56. Warren, J.T., Gilbert, L.I., 1988. Radioimmunoassay of ecdysteroids. In: Gilbert, L.I., Miller, T.A. (Eds.), Immunological Techniques In Insect Biology. Springer-Verlag, Berlin, pp. 181-214.
57. Warren, J.T., Gilbert, L.I., 1996. Metabolism in vitro of cholesterol and 25-hydroxycholesterol by the larval prothoracic glands of Manduca sexta. Insect Biochem. Mol. Biol. 26, 917-929.
58. Warren, J.T., Sakurai, S., Rountree, D., Gilbert, L.I., Lee, S.-S., Nakanishi, K., 1988. Regulation of the ecdysteroid titer of Manduca sexta: reappraisal of the role of the prothoracic glands. Proc. Natl. Acad. Sci. USA 85, 958-962.
59. Warren, J.T., Dai, J., Gilbert, L.I., 1999. Can the insect nervous system synthesize ecdysteroids? Insect Biochem. Mol. Biol. 29, 571-579.
60. Warren, J.T., Wismar, J., Subrahmanyam, B., Gilbert, L.I., 2001. Woe (without children) gene control of ecdysone biosynthesis in Drosophila melanogaster. Mol. Cell. Endocrinol. 181, 1-14.
61. Warren, J.T., Petryk, A., Marqués, G., Jarcho, M., Parvy, J.-P., Dauphin-Villemant, C., O'Connor, M.B., 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.
62. Wieschaus, E., Nüsslein-Volhard, C., Jürgens, G., 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. III Zygotic loci on the X-chromosome and fourth chromosome. Roux's Arch. Dev. Biol. 193, 296-307.