How does juvenile hormone control insect metamorphosis and reproduction?

General and Comparative Endocrinology

Volumn 179, Issue 3, 2012, Pages 477-484

  Riddiford, Lynn M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Female receptivity; Insect metamorphosis; Insulin like peptide; Juvenile hormone; Methoprene tolerant; Vitellogenesis

Indexed keywords

HORMONE RECEPTOR; JH RECEPTOR; JUVENILE HORMONE; UNCLASSIFIED DRUG; INSECT PROTEIN;

ADULT; AEDES AEGYPTI; ANIMAL EXPERIMENT; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EPIDERMIS; EYE DEVELOPMENT; FEMALE; HORMONE ACTION; HORMONE BINDING; LEPIDOPTERA; MANDUCA SEXTA; METAMORPHOSIS; MOLTING; NONHUMAN; OPTIC LOBE; PAEDOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REPRODUCTIVE BEHAVIOR; REPRODUCTIVE DEVELOPMENT; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TRIBOLIUM CASTANEUM; VITELLOGENESIS; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; MALE; MANDUCA; METABOLISM; PHYSIOLOGY; TRIBOLIUM;

ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT PROTEINS; JUVENILE HORMONES; MALE; MANDUCA; METAMORPHOSIS, BIOLOGICAL; TRIBOLIUM; VITELLOGENESIS;

EID: 84878664805     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.06.001     Document Type: Short Survey

References (79)

1. M.A. Abdou, Q. Heb, D. Wen, O. Zyaan, J. Wang, J. Xu, A.A. Baumann, J. Joseph, T.G. Wilson, S. Li, J. Wang, Drosophila Met and Gce are partially redundant in transducing juvenile hormone action, Insect Biochem. Mol. Biol. 41 (2011) 938-945.
2. M. Arienti, C. Antony, C. Wicker-Thomas, J.-P. Delbecque, J.-M. Jallon, Ontogeny of Drosophila melanogaster female sex-appeal and cuticular hydrocarbons, Integr. Zool. 5 (2010) 272-282.
3. M. Ashburner, C. Chihara, P. Meltzer, G. Richards, Temporal control of puffing activity in polytene chromosomes, Cold Spring Harb. Symp. Quant. Biol. 38 (1974) 655-662.
4. J. Bai, Y. Uehara, D.J. Montell, Regulation of invasive cell behavior by Taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer, Cell 103 (2000) 1047-1058.
5. A. Baumann, Y. Fujiwara, T.G. Wilson, Evolutionary divergence of the paralogs Methoprene tolerant (Met) and germ cell expressed (gce) within the genus Drosophila, J. Insect Physiol. 56 (2010) 1445-1455.
6. A. Baumann, J. Barry, S. Wang, Y. Fujiwara, T.G. Wilson, Paralogous genes involved in juvenile hormone action in Drosophila melanogaster, Genetics 185 (2010) 1327-1336.
7. C. Bayer, L. von Kalm, J.W. Fristrom, Gene regulation in imaginal disc and salivary gland development during Drosophila metamorphosis, in: L.I. Gilbert, J.R. Tata, B.G. Atkinson (Eds.), Metamorphosis, Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells, Academic Press, San Diego, 1996, 321-361.
8. W.G. Bendena, J. Zhang, S.M. Burtenshaw, S.S. Tobe, Evidence for differential biosynthesis of juvenile hormone (and related) sesquiterpenoids in Drosophila melanogaster, Gen. Compar. Endocrinol. (2011) 56-61.
9. T.J. Bernardo, E.B. Dubrovsky, The Drosophila juvenile hormone receptor candidates Methoprene-tolerant (Met) and germ cell-expressed (gce) utilize a conserved LIXXL motif to bind the FTZ-F1 nuclear receptor, J. Biol. Chem. 287 (2012) 7821-7833.
10. T.J. Bernardo, E.B. Dubrovsky, Molecular mechanisms of transcription activation by juvenile hormone: a critical role for bHLH-PAS and nuclear receptor proteins, Insects 3 (2012) 324-338.
11. J. Bilen, L. Riddiford, Juvenile hormone modulates the maturation of female receptivity in Drosophila melanogaster, Abstract 646A, Drosophila Research Conference, Gen. Soc. America (2011) 267-268.
12. F. Bonneton, V. Laudet, Evolution of nuclear receptors in insects, in: L.I. Gilbert (Ed.), Insect Endocrinology, Elsevier, Amsterdam, 2012, 310-365.
13. M. Bownes, The regulation of yolk protein gene expression and vitellogenesis in higher Diptera, in: A.S. Raikhel, T.W. Sappington (Eds.), Reproductive Biology of Invertebrates, vol. 12, Part B Progress in Vitellogenesis, Science Publishers, Enfield, USA/Plymouth, UK, 2004, 95-128.
14. N. Bruey-Sedano, J. Alabouvette, M. Lestradet, L. Hong, A. Girard, E. Gervasio, B. Quennedey, J.P. Charles, The Drosophila ACP65A cuticle gene: deletion scanning analysis of cis-regulatory sequences and regulation by DHR38, Genesis 43 (2005) 17-27.
15. D.T. Champlin, J.W. Truman, Ecdysteroid control of cell proliferation during optic lobe neurogenesis in the moth, Manduca sexta, Development 125 (1998) 269-277.
16. D.T. Champlin, J.W. Truman, Ecdysteroids govern two phases of eye development during metamorphosis of the moth, Manduca sexta, Development 125 (1998) 2009-2018.
17. D.T. Champlin, S.E. Reiss, J.W. Truman, Truman, Hormonal control of ventral diaphragm myogenesis during metamorphosis of the moth, Manduca sexta, Dev. Genes Evol. 209 (1999) 265-274.
18. J.-P. Charles, T. Iwema, V.C. Epa, K. Takaki, J. Rynes, M. Jindra, Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant, Proc. Natl. Acad. Sci. USA 108 (2011) 21128-21133.
19. H.-Y. Cui, M. Lestradet, N. Bruey-Sedano, J.-P. Charles, L.M. Riddiford, Elucidation of the regulation of an adult cuticle gene Acp65A by the transcription factor Broad, Insect Mol. Biol. 18 (2009) 421-429.
20. J.-F. Ferveur, Drosophila female courtship and mating behaviors: sensory signals, genes, neural structures and evolution, Curr. Opin. Neurobiol. 20 (2010) 764-769.
21. D. Fristrom, J. Fristrom, The metamorphic development of the adult epidermis, in: M. Bate, A. Martinez-Arias (Eds.), The Development of Drosophila melanogaster, vol II, Cold Spring Harbor Laboratory Press, Plainview, New York, 1993, 843-897.
22. J. Godlewski, S. Wang, T.G. Wilson, Interaction of bHLH-PAS proteins involved in juvenile hormone reception in Drosophila, Biochem. Biophys. Res. Commun. 342 (2006) 1305-1311.
23. W.G. Goodman, M. Cusson, The juvenile hormones, in: L.I. Gilbert (Ed.), Insect Endocrinology, Elsevier, Amsterdam, 2012, 310-365.
24. S.S. Grewal, Insulin/TOR signaling in growth and homeostasis: a view from the fly world, Int. J. Biochem. Cell Biol. 41 (2009) 1006-1010.
25. K. Hartfelder, D.J. Emlen, Endocrine control of insect polyphenism, in: L.I. Gilbert (Ed.), Insect Endocrinology, Elsevier, Amsterdam, 2012, 464-522.
26. K. Hiruma, L.M. Riddiford, Developmental expression of mRNAs for epidermal and fat body proteins and hormonally regulated transcription factors in the tobacco hornworm, Manduca sexta, J. Insect Physiol. 56 (2010) 1390-1395.
27. J. Huang, L. Tian, C. Peng, M. Abdou, D. Wen, Y. Wang, S. Li, J. Wang, DPPmediated TGFbeta signaling regulates juvenile hormone biosynthesis by activating the expression of juvenile hormone acid methyltransferase, Development 138 (2011) 2283-2291.
28. M. Jindra, S.R. Palli, L.M. Riddiford, The juvenile hormone signaling pathway in insect development, Annu. Rev. Entomol. 58 (2013), http://dx.doi.org/10.1146/annurev-ento-120811-153700.
29. D. Jones, G. Jones, Farnesoid secretions of dipteran ring glands: what we do know and what we can know, Insect Biochem. Mol. Biol. 37 (2007) 771-798.
30. D. Jones, G. Jones, P. Teal, C. Hammac, L. Messmer, K. Osborne, Y.H. Belgace, J.-R. Martin, Suppressed production of methyl farnesoid hormones yields developmental defects and lethality in Drosophila larvae, Gen. Comp. Endocrin. 165 (2010) 244-254.
31. G. Jones, D. Jones, P. Teal, A. Sapa, M. Wozniak, The retinoid-X receptor ortholog, Ultraspiracle, binds with nanomolar affinity to an endogenous morphogenetic ligand, FEBS J. 273 (2006) 4983-4996.
32. G. Jones, D. Jones, X. Li, L. Tang, L. Ye, P. Teal, L. Riddiford, C. Sandifer, D. Borovsky, J-R. Martin, Activities of natural methyl farnesoids on pupariation and metamorphosis of Drosophila melanogaster, J. Insect Physiol. 56 (2010) 1456-1464.
33. G. Jones, D. Jones, F. Fang, Y. Xu, D. New, W.-H. Wu, Juvenile hormone action through a defined enhancer motif to modulate ecdysteroid-activation of natural core promoters, Comp. Biochem. Physiol. B 161 (2012) 219-225.
34. K. Kiguchi, L.M. Riddiford, The role of juvenile hormone in pupal development of the tobacco hornworm, Manduca sexta, J. Insect Physiol. 24 (1978) 673-680.
35. K. King-Jones, C.S. Thummel, Nuclear receptors -a perspective from Drosophila, Nat. Rev. Genet. 6 (2005) 311-323.
36. B. Konopova, M. Jindra, Juvenile hormone resistance gene Methoprenetolerant controls entry into metamorphosis in the beetle Tribolium castaneum, Proc. Natl. Acad. Sci. USA 104 (2007) 10488-10493.
37. B. Konopova, M. Jindra, Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis, Development 135 (2008) 559-568.
38. B. Konopova, V. Smykal, M. Jindra, Common and distinct roles of juvenile hormone signaling genes in metamorphosis of holometabolous and hemimetabolous insects, PLoS One 6 (2011) e28728.
39. T. Koyama, M.O. Syropyatova, L.M. Riddiford, Insulin/IGF signaling regulates the change in commitment in imaginal discs and primordia by overriding the effect of juvenile hormone, Dev. Biol. 324 (2008) 258-265.
40. M. Li, E.A. Mead, J. Zhu, Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression, Proc. Natl. Acad. Sci. USA 108 (2011) 638-643.
41. Y. Liu, Z. Sheng, H. Liu, D. Wen, Q. He, S. Wang, W. Shao, R.-J. Jiang, S. An, Y. Sun, W.G. Bendena, J. Wang, L.I. Gilbert, T.G. Wilson, Q. Song, S. Li, Juvenile hormone counteracts the bHLH-PAS transcription factors MET and GCE to prevent caspase-dependent programmed cell death in Drosophila, Development 136 (2009) 2015-2025.
42. J. Lozano, X. Belles, Conserved repressive function of Krüppel homolog 1 on insect metamorphosis in hemimetabolous and holometabolous species, Sci. Rep. 1 (2011): doi:10.1038/srep00163.
43. S.G.B. MacWhinnie, J.P. Allee, C.A. Nelson, L.M. Riddiford, J.W. Truman, D.T. Champlin, The role of nutrition in creation of the eye imaginal disc and initiation of metamorphosis in Manduca sexta, Dev. Biol. 285 (2005) 285-297.
44. A. Manning, Corpus allatum and sexual receptivity in female Drosophila melanogaster, Nature 211 (1966) 1321-1322.
45. C. Minakuchi, X. Zhou, L.M. Riddiford, Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster, Mech. Dev. 125 (2008) 91-105.
46. C. Minakuchi, T. Namiki, T. Shinoda, Krüppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum, Dev. Biol. 325 (2009) 341-350.
47. G.P.C. Nagaraju, Reproductive regulators in decapod crustaceans: an overview, J. Exp. Biol. 214 (2011) 3-16.
48. H.F. Nijhout, Insect Hormones, Princeton University Press, Princeton, 1995.
49. R. Parthasarathy, A. Tan, H. Bai, S.R. Palli, Transcription factor broad suppresses precocious development of adult structures during larval-pupal metamorphosis in the red flour beetle, Tribolium castaneum, Mech. Dev. 125 (2008) 299-313.
50. F. Pecasse, Y. Beck, C. Ruiz, G. Richards, Krüppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis, Dev. Biol. 221 (2000) 53-67.
51. A.S. Raikhel, M.R. Brown, X. Belles, Hormonal control of reproductive processes In: L.I. Gilbert, K. Iatrou, S.S. Gill, (Eds.), Comprehensive Insect Science vol. 3, Elsevier, Pergamon, Amsterdam 433-491
52. L.M. Riddiford, Hormonal control of insect epidermal cell commitment in vitro, Nature 259 (1976) 115-117.
53. L.M. Riddiford, Ecdysone-induced change in cellular commitment of the epidermis of the tobacco hornworm, Manduca sexta, at the initiation of metamorphosis, Gen. Comp. Endocrin. 34 (1978) 438-446.
54. L.M. Riddiford, Hormones and Drosophila development, in: M. Bate, A. Martinez-Arias (Eds.), The Development of Drosophila, Cold Spring Harbor Laboratory Press, Plainview, 1993, 899-939.
55. L.M. Riddiford, Cellular and molecular actions of juvenile hormone. I. General considerations and premetamorphic actions, Adv. Insect Physiol. 24 (1994) 213-274.
56. L.M. Riddiford, A.M. Ajami, Juvenile hormone: its assay and effects on pupae of Manduca sexta, J. Insect Physiol. 19 (1973) 749-762.
57. L.M. Riddiford, P.T. Cherbas, J.W. Truman, Ecdysone receptors and their biological actions, Vit. Horm. 60 (2001) 1-73.
58. L.M. Riddiford, K. Hiruma, X. Zhou, C.A. Nelson, Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster, Insect Biochem. Mol. Biol. 33 (2003) 1327-1338.
59. L.M. Riddiford, J.W. Truman, C.K. Mirth, Y. Shen, A role for juvenile hormone in the prepupal development of Drosophila melanogaster, Development 137 (2010) 1117-1126.
60. J.M. Ringo, Hormonal regulation of sexual behavior in insects, in: D.W. Pfaff, A.P. Arnold, A.M. Eigen, S.E. Fahrbach, R.T. Rubin (Eds.), Hormones, Brain and Behavior, vol. 3, Academic Press, Amsterdam, 2002, 93-114.
61. Z. Sheng, J. Xu, H. Bai, F. Zhu, S.R. Palli, Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum, J. Biol. Chem. 286 (2011) 41924-41936.
62. M. Soller, M. Bownes, E. Kubli, Control of oocyte maturation in sexually mature Drosophila females, Dev. Biol. 208 (1999) 337-351.
63. Y. Suzuki, J.W. Truman, L.M. Riddiford, The role of the transcription factor Broad in the development and evolution of the holometabolous insect pupa, Tribolium castaneum, Development 135 (2008) 569-577.
64. C.S. Thummel, Flies on steroids-Drosophila metamorphosis and the mechanism of steroid hormone action, Trends Genetics 12 (1996) 306-310.
65. C.-Y. Ting, C.-H. Lee, Visual circuit development in Drosophila, Curr. Opin. Neurobiol. 17 (2007) 65-72.
66. J.W. Truman, W.S. Talbot, S.E. Fahrbach, D.S. Hogness, Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development, Development 120 (1994) 219-234.
67. J.W. Truman, K. Hiruma, J.P. Allee, S.G.B. MacWhinnie, D.T. Champlin, L.M. Riddiford, Juvenile hormone is required to couple imaginal disc formation with nutrition in insects, Science 312 (2006) 1385-1388.
68. C. Wicker-Thomas, T. Chertemps, Molecular biology and genetics of hydrocarbon production, in: G.J. Blomquist, A.-G. Bagneres (Eds.), Insect Hydrocarbons: Biology, Biochemistry and Chemical Ecology, Cambridge University Press, Cambridge, 2010, 53-74.
69. V.B. Wigglesworth, The physiology of ecdysis in Rhodnius prolixus (Hemiptera). II. Factors controlling moulting and 'metamorphosis', Quart. J. Micr. Sci. 77 (1934) 191-222.
70. V.B. Wigglesworth, The function of the corpus allatum in the growth and reproduction of Rhodnius prolixus (Hemiptera), Quart. J. Micr. Sci. 79 (1936) 91-121.
71. C.M. Williams, The juvenile hormone. II. Its role in the endocrine control of molting, pupation, and adult development in the Cecropia silkworm, Biol. Bull. 121 (1961) 572-585.
72. T.G. Wilson, M. Ashok, Insecticide resistance resulting from an absence of target-site gene product, Proc. Natl. Acad. Sci. USA 95 (1998) 14040-14044.
73. T.G. Wilson, J. Fabian, A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone, Dev. Biol. 118 (1986) 190-201.
74. G.R. Wyatt, K.G. Davey, Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects, Adv. Insect Physiol. 26 (1996) 1-155.
75. Z. Zhang, J. Xu, Z. Sheng, Y. Sui, S.R. Palli, Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, Methoprene tolerant, J. Biol. Chem. 286 (2011) 8437-8447.
76. B. Zhou, K. Hiruma, T. Shinoda, L.M. Riddiford, Juvenile hormone prevents ecdysteroid-induced expression of Broad Complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta, Dev. Biol. 203 (1998) 233-244.
77. B. Zhou, L.M. Riddiford, Hormonal regulation and patterning of the Broad Complex in the epidermis and wing discs of the tobacco hornworm, Manduca sexta, Dev. Biol. 231 (2001) 125-137.
78. X. Zhou, L.M. Riddiford, Broad-Complex specifies pupal development and mediates the prevention of the pupal-adult transformation by juvenile hormone in Drosophila and Manduca, Development 129 (2002) 2259-2269.
79. J. Zhu, L. Chen, G. Sun, A.S. Raikhel, The competence factor bFtz-F1 potentiates ecdysone receptor activity via recruiting a p160/SRC coactivator, Mol. Cell. Biol. 26 (2006) 9402-9412.