Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster

Insect Biochemistry and Molecular Biology

Volumn 33, Issue 12, 2003, Pages 1327-1338

  Riddiford, Lynn M ^a   Hiruma, Kiyoshi ^a   Zhou, Xiaofeng ^a   Nelson, Charles A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

20 hydroxyecdysone; Broad gene; Dopa decarboxylase; Ecdysone; Ecdysone induced transcription factors; Juvenile hormone; Metamorphosis; Molting; Prothoracicotropic hormone

Indexed keywords

DROSOPHILA MELANOGASTER; MANDUCA SEXTA; MELANOGASTER; NICOTIANA TABACUM;

EID: 0344153307     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2003.06.001     Document Type: Short Survey

References (91)

1. Andres, A.J., Fletcher, J.C., Karim, F.D., Thummel, C.S., 1993. Molecular analysis of the initiation of insect metamorphosis: A cooperative study of Drosophila ecdysone-regulated transcription. Dev. Biol. 160, 388-404.
2. Antoniewski, C., Laval, M., Dahan, A., Lepesant, J.A., 1994. The ecdysone response enhancer of the Fbp1 gene of Drosophila melanogaster is a direct target for the EcR/USP nuclear receptor. Mol. Cell. Biol. 14, 4465-4474.
3. Asahina, M., Jindra, M., Riddiford, L.M., 1997. Developmental expression of Ultraspiracle proteins in the epidermis of the tobacco hornworm, Manduca sexta, during larval life and the onset of metamorphosis. Dev. Genes Evol. 207, 381-388.
4. Bayer, C., von Kalm, L., Fristrom, J.W., 1996a. Gene regulation in imaginai disc and salivary gland development during Drosophila metamorphosis. In: Gilbert, L.I., Tata, J.R., Atkinson, E.G. (Eds.), Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. Academic Press, San Diego, pp. 321-361.
5. Bayer, C.A., Holley, B., Fristrom, J.W., 1996b. A switch in Broad-Complex zinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginai discs. Dev. Biol. 177, 1-14.
6. Bayer, C.A., von Kalm, L., Fristrom, J.W., 1997. Relationships between protein isoforms and genetic functions demonstrate functional redundancy at the Broad-Complex during Drosophila metamorphosis. Dev. Biol. 187, 267-282.
7. Bayer, C., Zhou, X., Zhou, B., Riddiford, L. M., von Kalm, L., 2003. Evolution of the Drosophila broad locus: the Manduca sexta broad Z4 isoform has biological activity in Drosophila. Dev. Genes Evol. (in press).
8. Bialecki, M., Shilton, A., Fichtenberg, C., Segraves, W.A., Thummel, C.S., 2002. Loss of the ecdysteroid-inducible E75A orphan nuclear receptor uncouples molting from metamorphosis in Drosophila. Dev. Cell 3, 209-220.
9. Bollenbacher, W.E., Smith, S.L., Goodman, W., Gilbert, L.I., 1981. Ecdysteroid titer during larval-pupal-adult development of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocrinol. 44, 302-306.
10. Brennan, C.A., Li, T.-R., Bender, M., Hsiung, F., Moses, K., 2001. Broad-complex, but not Ecdysone receptor, is required for progression of the morphogenetic furrow in the Drosophila eye. Development 128, 1-11.
11. Charles, J.P., Shinoda, T., Chinzei, 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.
12. Cherbas, L., Lee, K., Cherbas, P., 1991. Identification of ecdysone response elements by analysis of the Drosophila Eip28/29 gene. Genes Dev. 5, 120-131.
13. Dai, J., 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. Emery, I.F., Bedian, V., Guild, G.M., 1994. Differential expression of Broad-Complex transcription factors may forecast tissue-specific developmental fates during Drosophila metamorphosis. Development 120, 3275-3287.
15. Fletcher, J.C., Thummel, C.S., 1995. The ecdysone-inducible Broad-Complex and E75 early genes interact to regulate target gene transcription and Drosophila metamorphosis. Genetics 141, 1025-1035.
16. Fletcher, J.C., Burtis, K.C., Hogness, D.S., Thummel, C.S., 1995. The Drosophila E74 gene is required for metamorphosis and plays a role in the polytene chromosome puffing response to ecdysone. Development 121, 1455-1465.
17. Fraenkel, G.S., 1935. A hormone causing pupation in the blowfly Calliphora erythrocephala. Proc. Roy. Soc. London B. 118, 1-12.
18. Fristrom, D., Fristrom, J.W., 1993. The metamorphic development of the adult epidermis. In: Bate, M., Martinez-Arias, A. (Eds.), The Development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Plainview, NY, pp. 843-897.
19. Giguére, V., Tini, M., Flock, G., Ong, E., Evans, R.M., Otulakowski, G., 1994. Isoform-specific amino-terminal domains dictate DNA-binding properties of RARα, a novel member of orphan nuclear hormone receptors. Genes Dev. 8, 538-553.
20. Gilbert, L.I., Schneiderman, H.A., 1958a. The occurrence of substances with juvenile hormone activity in adrenal cortex of vertebrates. Science 128, 844.
21. Gilbert, L.I., Schneiderman, H.A., 1958b. Substances of juvenile hormone activity in Crustacea and other invertebrates. Biol. Bull. 115, 530-535.
22. Gilbert, L.I., Granger, N.A., Roe, R.M., 2000. The juvenile hormones: historical facts and speculations on future research directions. Insect Biochem. Mol. Biol. 30, 617-644.
23. Gilbert, L.I., Rybczynski, R., Warren, J.T., 2002. Control and biochemical nature of the ecdysteroidogenic pathway. Annu. Rev. Entomol. 47, 883-916.
24. Hampshire, F., Horn, D., 1966. Structure of crustecdysone, a crustacean moulting hormone. J. Chem. Soc., Chem. Commun., 37-38.
25. Harding, H.P., Lazar, M.A., 1993. The orphan receptor Rev-ErbAα activates transcription via a novel response element. Mol. Cell Biol. 13, 3113-3121.
26. Henrich, V.C., Rybczynski, R., Gilbert, L.I., 1999. Peptide hormones, steroid hormones, and puffs: mechanisms and models in insect development. Vit. Horm. 55, 73-125.
27. Hiruma, K., Riddiford, L.M., 1984. Regulation of melanization of tobacco hornworm larva in vitro. J. Exp. Zool. 230, 393-403.
28. Hiruma, K., Riddiford, L.M., 1985. Hormonal regulation of dopa decarboxylase during a larval molt. Dev. Biol. 110, 509-513.
29. Hiruma, K., Riddiford, L.M., 1990. Regulation of dopa decarboxylase gene expression in the larval epidermis of the tobacco hornworm by 20-hydroxyecdysone and juvenile hormone. Dev. Biol. 138, 214-224.
30. Hiruma, K., Riddiford, L.M., 2001. Regulation of transcription factors MHR4 and βFTZ-F1 by 20-hydroxyecdysone during a larval molt in the tobacco hornworm, Manduca sexta. Dev. Biol. 2232, 265-274.
31. Hiruma, K., Riddiford, L.M., 2003. Differential control of MHR3 promoter activity by isoforms of the ecdysone receptor and inhibitory effects of E75A and MHR3. Submitted for publication.
32. Hiruma, K., Riddiford, L.M., Hopkins, T.L., Morgan, T.D., 1985. Roles of dopa decarboxylase and phenoloxidase in the melanization of the tobacco hornworm and their control by 20-hydroxyecdysone. J. Comp. Physiol. 155B, 659-669.
33. Hiruma, K., Carter, M.S., Riddiford, L.M., 1995. Characterization of the dopa decarboxylase gene of Manduca sexta and its suppression by 20-hydroxyecdysone. Dev. Biol. 169, 195-209.
34. Hiruma, K., Böcking, D., Lafont, R., Riddiford, L.M., 1997. Action of different ecdysteroids on the regulation of mRNAs for the ecdysone receptor, MHR3, dopa decarboxylase, and a larval cuticle protein in the larval epidermis of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocrinol. 107, 84-97.
35. Hiruma, K., Shinoda, T., Malone, F., Riddiford, L.M., 1999. Juvenile hormone modulates 20-hydroxyecdysone-inducible ecdysone receptor and Ultraspiracle gene expression in the tobacco hornworm, Manduca sexta. Dev. Genes. Evol. 209, 18-30.
36. Hocks, P., Weichert, R., 1966. 20-Hydroxy-ecdyson, isoliert aus Insekten. Terahedron. Lett. 26, 2989-2993.
37. Hoffmeister, H., Grützmacher, H.F., 1966. Zur Chemie des Ecdysterons. Tetrahedron. Lett. 33, 4017-4023.
38. Hopkins, T.L., Kramer, K.J., 1992. Insect cuticle sclerotization. Ann. Rev. Entomol. 37, 273-302.
39. Horner, M.A., Chen, T., Thummel, C.S., 1995. Ecdysteroid regulation and DNA binding properties of Drosophila nuclear hormone receptor superfamily members. Dev. Biol. 168, 490-502.
40. Huber, R., Hoppe, W., 1965. Zur Chemie des Ecdysons. VII. Die Kristal- und Molekül-strukturanalyse des Insectenverpuppung Hormons Ecdyson mit der automatisierten Falt-molekülmethode. Chem. Ber. 98, 2403-2424.
41. Jindra, M., Malone, F., Hiruma, K., Riddiford, L.M., 1996. Developmental profiles and ecdysteroid regulation of the mRNAs for two ecdysone receptor isoforms in the epidermis and wings of the tobacco hornworm, Manduca sexta. Dev. Biol. 180, 258-272.
42. Jindra, M., Huang, J.-Y., Malone, F., Asahina, M., Riddiford, L.M., 1997. Identification and mRNA developmental profiles of two ultraspiracle isoforms in the epidermis and wings of Manduca sexta. Insect Mol. Biol. 6, 41-53.
43. Kageyama, Y., Masuda, S., Hirose, S., Ueda, H., 1997. Temporal regulation of the mid-prepupal gene FTZ-F1: DHR3 early late gene product is one of the plural positive regulators. Genes to Cells 2, 559-569.
44. Karim, F.D., Guild, G.M., Thummel, C.S., 1993. The Drosophila Broad-Complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development 118, 977-988.
45. Karlson, P., Hoffmeister, H., Hummel, H., Hocks, P., Spiteller, G., 1965. Zur Chemie des Ecdysons. VI. Reaktionen des Ecdysonmoleküls. Chem. Ber. 98, 2349-2402.
46. Kataoka, N.H., Isogai, A., Ishizaki, H., Suzuki, A., 1991. Prothoracicotropic hormone of the silkworm, Bombyx mori: amino acid sequence and dimeric structure. Agric. Biol. Chem. 55, 73-86.
47. Kawakami, A., Kataoka, H., Oka, T., Mizoguchi, A., Kimura-Kawakami, M., Adachi, T., Iwami, M., Nagasawa, H., Suzuki, A., Ishizaki, H., 1990. Molecular cloning of the Bombyx mori prothoracicotropic hormone. Science 247, 1333-1335.
48. King-Jones, K., Charles, J.-P., Thummel, C.S., 2003. Regulation and function of the Drosophila DHR4 orphan nuclear receptor. In: 44th Annual Drosophila Research Conference, Chicago, March, 2003, Abstract: Ecdysone Workshop.
49. Kopec, S., 1922. Studies on the necessity of the brain for the inception of insect metamorphosis. Biol. Bull. 42, 323-342.
50. Kopp, A., Duncan, I., 2002. Anteroposterior patterning in adult abdominal segments of Drosophila. Dev. Biol. 242, 15-30.
51. Lam, G.T., Jiang, C., Thummel, C.S., 1997. Coordination of larval and prepupal gene expression by the DHR3 orphan receptor during Drosophila metamorphosis. Development 124, 1757-1769.
52. Lan, Q., Wu, Z., Riddiford, L.M., 1997. Regulation of the ecdysone receptor, USP, E75 and MHR3 mRNAs by 20-hydroxyecdysone in the GV1 cell line of the tobacco hornworm, Manduca sexta. Insect Mol. Biol. 6, 3-10.
53. Lan, Q., Hiruma, K., Hu, X., Jindra, M., Riddiford, L.M., 1999. Activation of a delayed-early gene encoding MHR3 by the ecdysone receptor heterodimer EcR-B1/USP-1 but not by EcR-B1/USP-2. Mol. Cell Biol. 19, 4897-4906.
54. Langelan, R.E., Fisher, J.E., Hiruma, K., Palli, S.R., Riddiford, L.M., 2000. Patterns of MHR3 expression in the epidermis during a larval molt of the tobacco hornworm, Manduca sexta. Dev. Biol. 227, 481-494.
55. Lehmann, M., Wattler, F., Korge, G., 1997. Two new regulatory elements controlling the Drosophila Sgs-3 gene are potential ecdysone receptor and fork head binding sites. Mech. Dev. 62, 15-27.
56. Madhavan, M.M., Madhavan, K., 1980. Morphogenesis of the epidermis of the adult abdomen of Drosophila. J. Embryol. Exp. Morphol. 60, 1-31.
57. Mouillet, J.-F., Bousquet, F., Sedano, N., Alabouvette, J., Nicolaï, M., Zelus, D., Laudet, V., Delachambre, J., 1999. Cloning and characterization of new orphan nuclear receptors and their developmental profiles during Tenebrio metamorphosis. Eur. J. Biochem. 265, 972-981.
58. Mugat, B., Brodu, V., Kejzlarova-Lepesant, J., Antoniewski, C., Bayer, C.A., Fristrom, J.W., Lepesant, J.-A., 2000. Dynamic expression of Broad-Complex isoforms mediates temporal control of an ecdysteroid target gene at the onset of Drosophila metamorphosis. Dev. Biol. 227, 104-117.
59. Palli, S.R., Hiruma, K., Riddiford, L.M., 1992. An ecdysteroid-inducible Manduca gene similar to the Drosophila DHR3 gene, a member of the steroid hormone receptor superfamily. Dev. Biol. 150, 306-318.
60. Riddiford, L.M., 1976. Hormonal control of insect epidermal cell commitment in vitro. Nature 259, 115-117.
61. Riddiford, L.M., 1978. Ecdysone-induced change in cellular commitment of the epidermis of the tobacco hornworm, Manduca sexta, at the initiation of metamorphosis. Gen. Comp. Endocrinol. 34, 438-446.
62. Riddiford, L.M., 1994. Cellular and molecular actions of juvenile hormone. I. General considerations and premetamorphic actions. Adv. Insect Physiol. 24, 213-274.
63. Riddiford, L.M., 1995. Hormonal regulation of gene expression during lepidopteran development. In: Goldsmith, M.R., Wilkins, A.S. (Eds.), Molecular Model Systems in the Lepidoptera. Cambridge University Press, Cambridge, pp. 293-322.
64. Riddiford, L.M., 1996. Molecular aspects of juvenile hormone action in insect metamorphosis. In: Gilbert, L.I., Tata, J.R., Atkinson, B.G. (Eds.), Metamorphosis:Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. Academic Press, San Diego, pp. 223-251.
65. Riddiford, L.M., Ajami, A.M., 1973. Juvenile hormone: its assay and effects on pupae of Manduca sexta. J. Insect Physiol. 19, 749-762.
66. Riddiford, L.M., Ashburner, M., 1991. Effects of juvenile hormone mimics on larval development and metamorphosis of Drosophila melanogaster. Gen. Comp. Endocrinol. 82, 172-183.
67. Riddiford, L.M., Hiruma, K., Lan, Q., Zhou, B., 1999. Regulation and role of nuclear receptors during larval molting and metamorphosis of Lepidoptera. Am. Zool. 39, 736-746.
68. Riddiford, L.M., Cherbas, P., Truman, J.W., 2001. Ecdysone receptors and their biological actions. Vitam. Horm. 60, 1-73.
69. Röller, H., Dahm, K.H., Sweeley, C.C., Trost, B.M., 1967. The structure of the juvenile hormone. Angew. Chem. Int. Ed. 6, 179-180.
70. Roseland, C.R., Schneiderman, H.A., 1979. Regulation and metamorphosis of the abdominal histoblasts of Drosophila melanogaster. Wilhelm Roux's Arch. Dev. Biol. 186, 235-265.
71. Segraves, W.A., Hogness, D.S., 1990. The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes & Dev. 4, 204-219.
72. Segraves, W.A., Woldin, C., 1993, The E75 gene of Manduca sexta and comparison with its Drosophila homolog. Insect Biochem. Molec. Biol. 23, 91-97.
73. Stilwell, G.E., Nelson, C.A., Weller, J., Cui, H., Hiruma, K., Truman, J.W., Riddiford, L.M., 2003. E74 exhibits stage-specific hormonal regulation in the epidermis of the tobacco hornworm, Manduca sexta. Dev. Biol. 258, 76-90.
74. Sun, G.C., Hirose, S., Ueda, H., 1994. Intermittent expression of BmFTZ-F1, a member of the nuclear hormone receptor superfamily during development of the silkworm Bombyx mori. Dev. Biol. 162, 426-437.
75. Thummel, C.S., Chory, J., 2002. Steroid signaling in plants and insects - common themes, different pathways. Genes Dev. 16, 3113-3129.
76. Truman, J.W., Riddiford, L.M., 1999. The origins of insect metamorphosis. Nature 401, 447-452.
77. Truman, J.W., Riddiford, L.M., Safranek, L., 1974. Temporal patterns of response to ecdysone and juvenile hormone in the epidermis of the tobacco hornworm, Manduca sexta. Dev. Biol. 39, 247-262.
78. Truman, J.W., Rountree, D.B., Reiss, S.E., Schwartz, L.M., 1983. Ecdysteroids regulate the release and action of eclosion hormone in the tobacco hornworm, Manduca sexta (L). J. Insect Physiol. 29, 895-900.
79. Ueda, H., Hirose, S., 1991. Defining the sequence recognized with BmFTZ-F1, a sequence specific DNA binding factor in the silkworm, Bombyx mori, as revealed by direct sequencing of bound oligonucleotides and gel mobility shift competition analysis. Nucl. Acids Res. 19, 3689-3693.
80. Warren, J.T., Petryk, A., Marques, 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.
81. Weller, J., Sun, G.-C., Zhou, B., Lan, Q., Hiruma, K., Riddiford, L.M., 2001. Isolation and developmental expression of two nuclear receptors, MHR4 and βFTZ-F1, in the tobacco hornworm, Manduca sexta. Insect Biochem. Molec. Biol. 31, 827-837.
82. White, K.P., Hurban, P., Watanabe, T., Hogness, D.S., 1997. Coordination of Drosophila metamorphosis by two ecdysone-induced nuclear receptors. Science 276, 114-117.
83. Wigglesworth, V.B., 1934. The physiology of ecdysis in Rhodnius prolixus. II. Factors controlling moulting and metamorphosis. Q. J. Microscop. Sci. 77, 191-222.
84. Williams, C.M., 1956. The juvenile hormone of insects. Nature 178, 212-213.
85. Williams, C.M., Moorhead, L.V., Pulis, J.F., 1959. Juvenile hormone in thymus, human placenta, and other mammalian organs. Nature 183, 405.
86. Woodard, C.T., Baehrecke, E.H., Thummel, C.S., 1994. A molecular mechanism for the stage specificity of the Drosophila prepupal genetic response to ecdysone. Cell 79, 607-615.
87. Zhou, B., Riddiford, L.M., 2001. Hormonal regulation and patterning of the Broad-Complex in the epidermis and wing discs of the tobacco hornworm, Manduca sexta. Dev. Biol. 231, 125-137.
88. Zhou, B., Hiruma, K., Jindra, M., Shinoda, T., Segraves, W.A., Malone, F., Riddiford, L.M., 1998a. Regulation of the transcription factor E75 by 20-hydroxyecdysone and juvenile hormone in the epidermis of the tobacco hornworm, Manduca sexta, during larval molting and metamorphosis. Dev. Biol. 193, 127-138.
89. Zhou, B., Hiruma, K., Shinoda, T., Riddiford, L.M., 1998b. Juvenile hormone prevents ecdysteroid-induced expression of Broad-Complex RNA in the epidermis of the tobacco hornworm, Manduca sexta. Dev. Biol. 203, 233-244.
90. Zhou, X., Riddiford, L.M., 2002. Broad specifies pupal development and mediates the 'status quo' action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129, 2259-2269.
91. Zhou, X., Zhou, B., Truman, J.W., Riddiford, L.M., 2003. Overexpression of Broad: a new insight into its role in the Drosophila prothoracic glands. Submitted for publication.