Browse > Article
http://dx.doi.org/10.5656/KSAE.2022.01.1.059

Insect Juvenile Hormone Antagonists as Eco-friendly Insecticides  

Choi, Jae Young (Research Institute for Agriculture and Life Sciences, Seoul National University)
Je, Yeon Ho (Research Institute for Agriculture and Life Sciences, Seoul National University)
Publication Information
Korean journal of applied entomology / v.61, no.1, 2022 , pp. 101-108 More about this Journal
Abstract
Because of their specificity to target insects and relatively low toxicity to non-target organisms, insect growth regulators (IGRs) have been regarded as attractive alternatives to chemical insecticides. Commercially available IGRs are classified into juvenile hormone agonists (JHAs), ecdysone agonists (EAs), and chitin synthesis inhibitors (CSIs) according to their mode of action. Recently, JH-mediated interaction of methoprene-tolerant (Met), which is JH receptor, and its binding partners have been replicated in vitro using yeast cells transformed with the Met and FISC/CYC genes of A. aegypti. Using this in vitro yeast two-hybrid β-galactosidase assay, juvenile hormone antagonists (JHANs) have been identified from various sources including chemical libraries, plants, and microorganisms. As juvenile hormone (JH) is an insect specific hormone and regulates development, reproduction, diapause and other physiological processes, JHANs fatally disrupt the endocrine signals, which result in abnormal development and larval death. These results suggested that JHANs could be efficiently applied as IGR insecticides with a broad insecticidal spectrum. This review discuses JH signaling pathway mediated by Met and future prospects of JHANs as environmentally benign IGR insecticides.
Keywords
Insect growth regulator; Juvenile hormone; Receptor complex; Juvenile hormone antagonist;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Alzogaray, R.A., Zerba, E.N., 2017. Rhodnius prolixus intoxicated. J. Insect Physiol. 97, 93-113.   DOI
2 Azambuja, P.d., Garcia, E.S., 1991. Effects of proallatotoxins (precocenes) on the development and reproduction of k: some data. Memorias do Instituto Oswaldo Cruz. 86, 113-115.   DOI
3 Bowers, W., Fales, H., Thompson, M., Uebel, E., 1966. Juvenile hormone: identification of an active compound from balsam fir. Science 154, 1020-1021.   DOI
4 Schooneveld, H., 1979. Precocene-induced necrosis and haemocytemediated breakdown of corpora allata in nymphs of the locust Locusta migratoria. Cell Tissue Res. 203, 25-33.   DOI
5 Bernardo, T.J., Dubrovsky, E.B., 2012a. 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, 7821-7833.   DOI
6 Banerjee, S., Kalena, G., Banerji, A., Singh, A., 2008. New synthetic precocenoids as potential insect control agents. J. Environ. Biol 29, 951-957.
7 Baumann, A., Fujiwara, Y., Wilson, T.G., 2010b. Evolutionary divergence of the paralogs Methoprene tolerant (Met) and germ cell expressed (gce) within the genus Drosophila. J. Insect Physiol. 56, 1445-1455.   DOI
8 Bergot, B., Baker, F., Cerf, D., Jamieson, G., Schooley, D., 1981. Qualitative and quantitative aspects of juvenile hormone titers in developing embryos of several insect species: discovery of a new JH-like substance extracted from eggs of Manduca sexta. Juvenile Hormone Biochemistry 15, 33-45.
9 Bowers, W.S., 2012. Insect hormones and antihormones in plants, in: Rosenthal, G.A., Berenbaum, M.R. (Eds.), Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp. 431-456.
10 Li, M., Mead, E.A., Zhu, J., 2011. Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc. Natl. Acad. Sci. U. S. A. 108, 638-643.   DOI
11 Shin, S.W., Zou, Z., Saha, T.T., Raikhel, A.S., 2012. bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proc. Natl. Acad. Sci. U. S. A. 109, 16576-16581.   DOI
12 Slama, K., 2016. Pharmacology of insect juvenile hormones. Comprehensive Insect Physiol. Biochem. Phramacol. 11, 357-394.
13 Slama, K., Williams, C.M., 1966. 'Paper factor'as an inhibitor of the embryonic development of the European bug, Pyrrhocoris apterus. Nature 210, 329-330.   DOI
14 Wigglesworth, V.B., 1936. Memoirs: The function of the corpus allatum in the growth and reproduction of Rhodnius prolixus (Hemiptera). J. Cell Sci. 2, 91-121.   DOI
15 Pedigo, L.P., Rice, M.E., Krell, R.K., 2021. Entomology and pest management. Waveland Press. Illinois.
16 Masner, P., Angst, M., Dorn, S., 1987. Fenoxycarb, an insect growth regulator with juvenile hormone activity: A candidate for Heliothis virescens (F.) control on cotton. Pestic. Sci. 18, 89-94.   DOI
17 Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P., Hens, L., 2016. Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front. Public Health 4, 148.
18 Okazawa, T., Bakote'e, B., Suzuki, H., Kawada, H., Kere, N., 1991. Field evaluation of an insect growth regulator, pyriproxyfen, against Anopheles punctulatus on north Guadalcanal, Solomon Islands. J. Am. Mosq. Control Assoc. 7, 604-607.
19 Pener, M.P., Dhadialla, T.S., 2012. An overview of insect growth disruptors; applied aspects. Adv. Insect Physiol. 43, 1-162.   DOI
20 Riddiford, L.M., 2008. Juvenile hormone action: a 2007 perspective. J. Insect Physiol. 54, 895-901.   DOI
21 Roller, H., 1967. The structure of the juvenile hormone. Angew. Chem. Int. Ed. Engl. 6, 179-180.   DOI
22 Schneiderman, H.A., 1972. Insect hormones and insect control, in: Menn, J.J., Beroza, M. (Eds.), Insect juvenile hormones. Academic Press, New York and London, pp. 3-27.
23 Schneiderman, H.A., Gilbert, L.I., Weinstein, M.J., 1960. Juvenile hormone activity in micro-organisms and plants. Nature 188, 1041-1042.   DOI
24 Williams, C.M., Moorhead, L.V., Pulis, J.F., 1959. Juvenile hormone in thymus, human placenta and other mammalian organs. Nature 183, 405-405.   DOI
25 Bennett, G., Reid, B., 1995. Insect growth regulators, in: Rust, M.K., Owens, J.M., Reierson, D.A. (Eds.), Understanding and controlling the German cockroach. Oxford University Press, New York, pp. 267-286.
26 Konopova, B., Jindra, M., 2007. Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. U. S. A. 104, 10488-10493.   DOI
27 Park, D.H., Choi, J.Y., Lee, S.-H., Kim, J.H., Park, M.G., Kim, J.Y., Wang, M., Kim, H.J., Je, Y.H., 2020. Mosquito larvicidal activities of farnesol and farnesyl acetate via regulation of juvenile hormone receptor complex formation in Aedes mosquito. J. Asia-Pac. Entomol. 23, 689-693.   DOI
28 Williams, C.M., 1956. The juvenile hormone of insects. Nature 178, 212-213.   DOI
29 Williams, C.M., 1967. Third-generation pesticides. Sci. Am. 217, 13-17.   DOI
30 Wilson, T.G., Fabian, J., 1986. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118, 190-201.   DOI
31 Woo, R.M., Park, M.G., Choi, J.Y., Park, D.H., Kim, J.Y., Wang, M., Kim, H.J., Woo, S.D., Kim, J.S., Je, Y.H., 2020. Insecticidal and insect growth regulatory activities of secondary metabolites from entomopathogenic fungi, Lecanicillium attenuatum. J. Appl. Entomol. 144, 655-663.   DOI
32 Zhang, Z., Xu, J., Sheng, Z., Sui, Y., Palli, S.R., 2011. Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J. Biol. Chem. 286, 8437-8447.   DOI
33 Schmialek, P., 1961. Die Identifizierung zweier im Tenebriokot und in Hefe vorkommender Substanzen mit Juvenilhormonwirkung. Zeitschrift fur Naturforschung B 16, 461-464.   DOI
34 Hefti, M.H., Francoijs, K.J., de Vries, S.C., Dixon, R., Vervoort, J., 2004. The PAS fold: A redefinition of the PAS domain based upon structural prediction. Eur. J. Biochem. 271, 1198-1208.   DOI
35 Lee, S.-H., Ha, K.B., Park, D.H., Fang, Y., Kim, J.H., Park, M.G., Woo, R.M., Kim, W.J., Park, I.-K., Choi, J.Y., Je, Y.H., 2018a. Plant-derived compounds regulate formation of the insect juvenile hormone receptor complex. Pest. Biochem. Physiol. 150, 27-32.   DOI
36 Letellier, C., Haubruge, E., Gaspar, C., 1995. Biological activity of fenoxycarb against Sitophilus zeamais Motsch.(Coleoptera: Curculionidae). J. Stored Prod. Res. 31, 37-42.   DOI
37 Meyer, A.S., Schneiderman, H.A., Hanzmann, E., Ko, J.H., 1968. The two juvenile hormones from the Cecropia silk moth. Proc. Natl. Acad. Sci. U. S. A. 60, 853-860.   DOI
38 Raikhel, A., Brown, M., Belles, X., 2005. 3.9 Hormonal control of reproductive processes. Comprehens Mol. Insect Sci. 3, 433-491.   DOI
39 Schooley, D., Baker, F., Tsai, L., Miller, C., Jamieson, G., 1984. Juvenile hormones O, I, and II exist only in Lepidoptera, in: Hoffmann, J., Porchet, M. (Eds.), Biosynthesis, metabolism and mode of action of invertebrate hormones. Springer-Verlag, pp. 373-383.
40 Silva, J.J.d., Mendes, J., 2007. Susceptibility of Aedes aegypti (L) to the insect growth regulators diflubenzuron and methoprene in Uberlandia, State of Minas Gerais. Rev. Soc. Bras. Med. Trop. 40, 612-616.   DOI
41 Henrick, C.A., Staal, G.B., Siddall, J.B., 1973. Alkyl 3, 7, 11-trimethyl-2, 4-dodecadienoates, a new class of potent insect growth regulators with juvenile hormone activity. J. Agric. Food Chem. 21, 354-359.   DOI
42 Boyer, S., Zhang, H., Lemperiere, G., 2012. A review of control methods and resistance mechanisms in stored-product insects. Bull. Entomol. Res. 102, 213-229.   DOI
43 Cantrell, C.L., Dayan, F.E., Duke, S.O., 2012. Natural products as sources for new pesticides. J. Nat. Prod. 75, 1231-1242.   DOI
44 Kaneko, Y., Furuta, K., Kuwano, E., Hiruma, K., 2011. An antijuvenile hormone agent, ethyl 4-(2-benzylhexyloxy) benzoate, inhibits juvenile hormone synthesis through the suppression of the transcription of juvenile hormone biosynthetic enzymes in the corpora allata in Bombyx mori. Insect Biochem. Mol. Biol. 41, 788-794.   DOI
45 Bowers, W.S., Ohta, T., Cleere, J.S., Marsella, P.A., 1976. Discovery of insect anti-juvenile hormones in plants? 2U. Science 193, 542-547.   DOI
46 Charles, J.-P., Iwema, T., Epa, V.C., Takaki, K., Rynes, J., Jindra, M., 2011. Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc. Natl. Acad. Sci. U. S. A. 108, 21128-21133.   DOI
47 Godlewski, J., Wang, S., Wilson, T.G., 2006. Interaction of bHLHPAS proteins involved in juvenile hormone reception in Drosophila. Biochem. Biophys. Res. Commun. 342, 1305-1311.   DOI
48 Hartfelder, K., Emlen, D., 2012. Endocrine control of insect polyphenism, in: Gilbert, L.I. (Ed.), Insect endocrinology. Elsevier, pp. 464-522.
49 Kotaki, T., Shinada, T., Kaihara, K., Ohfune, Y., Numata, H., 2009. Structure determination of a new juvenile hormonefrom a heteropteran insect. Org. Lett. 11, 5234-5237.   DOI
50 Abdou, M.A., He, Q., Wen, D., Zyaan, O., Wang, J., Xu, J., Baumann, A.A., Joseph, J., Wilson, T.G., Li, S., 2011. Drosophila Met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem. Mol. Biol. 41, 938-945.   DOI
51 Lee, S.-H., Lim, H.N., Choi, J.Y., Park, D.H., Ahn, B.H., Fang, Y., Kim, J.H., Park, M.G., Woo, R.M., Lee, B.R., Kim, W.J., Ko, Y.K., Lee, I.Y., Je, Y.H., 2018b. Mosquitocidal activity of penfluridol as juvenile hormone antagonist. J. Asia-Pac. Entomol. 21, 130-133.   DOI
52 Lee, S.-H., Oh, H.-W., Fang, Y., An, S.-B., Park, D.-S., Song, H.-H., Oh, S.-R., Kim, S.-Y., Kim, S., Kim, N., Raikhel, A.S., Je, Y.H., Shin, S.W., 2015. Identification of plant compounds that disrupt the insect juvenile hormone receptor complex. Proc. Natl. Acad. Sci. U. S. A. 112, 1733-1738.   DOI
53 Hartfelder, K., 2005. Endocrine control of insect polyphenism. Comprehensive Molecular Insect Science 3, 651-703.   DOI
54 Dennehy, T.J., Degain, B.A., Harpold, V.S., Zaborac, M., Morin, S., Fabrick, J.A., Nichols, R.L., Brown, J.K., Byrne, F.J., Li, X., 2010. Extraordinary resistance to insecticides reveals exotic O biotype of Bemisia tabaci in the New World. J. Econ. Entomol. 103, 2174-2186.   DOI
55 Furuta, K., Ashibe, K., Shirahashi, H., Fujita, N., Yamashita, H., Yamada, N., Kuwano, E., 2007. Synthesis and anti-juvenile hormone activity of ethyl 4-(2-benzylalkyloxy) benzoates and their enantiomers. J. Pestic. Sci. 32, 99-105.   DOI
56 Greb-Markiewicz, B., Orlowski, M., Dobrucki, J., Ozyhar, A., 2011. Sequences that direct subcellular traffic of the Drosophila metho prene-tolerant protein (MET) are located predominantly in the PAS domains. Mol. Cell. Endocrinol. 345, 16-26.   DOI
57 He, Q., Wen, D., Jia, Q., Cui, C., Wang, J., Palli, S.R., Li, S., 2014. Heat shock protein 83(Hsp83) facilitates methoprene-tolerant (Met) nuclear import to modulate juvenile hormone signaling. J. Biol. Chem. 289, 27874-27885.   DOI
58 Kim, J.H., Choi, J.Y., Park, D.H., Park, D.-J., Park, M.G., Kim, S.Y., Ju, Y.J., Kim, J.Y., Wang, M., Kim, C.-J., Je, Y.H., 2020. Isolation and characterization of the insect growth regulatory substances from actinomycetes. Comp. Biochem. Physiol. CToxicol. Pharmacol. 228, 108651.   DOI
59 Hill, C.A., Kafatos, F.C., Stansfield, S.K., Collins, F.H., 2005. Arthropod-borne diseases: vector control in the genomics era. Nat. Rev. Microbiol. 3, 262-268.   DOI
60 Judy, K.J., Schooley, D.A., Dunham, L.L., Hall, M., Bergot, B.J., Siddall, J.B., 1973. Isolation, structure, and absolute configuration of a new natural insect juvenile hormone from Manduca sexta. Proc. Natl. Acad. Sci. U. S. A. 70, 1509-1513.   DOI
61 Koehler, P.G., Patterson, R.S., 1991. Incorporation of pyriproxyfen in a German cockroach (Dictyoptera: Blattellidae) management program. J. Econ. Entomol. 84, 917-921.   DOI
62 Kotaki, T., 1996. Evidence for a new juvenile hormone in a stink bug, Plautia stali. J. Insect Physiol. 42, 279-286.   DOI
63 Baumann, A., Barry, J., Wang, S., Fujiwara, Y., Wilson, T.G., 2010a. Paralogous genes involved in juvenile hormone action in Drosophila melanogaster. Genetics 185, 1327-1336.   DOI
64 Bernardo, T.J., Dubrovsky, E.B., 2012b. Molecular mechanisms of transcription activation by juvenile hormone: a critical role for bHLH-PAS and nuclear receptor proteins. Insects 3, 324-338.   DOI
65 Slama, K., Williams, C.M., 1965. Juvenile hormone activity for the bug Pyrrhocoris apterus. Proc. Natl. Acad. Sci. U. S. A. 54, 411-414.   DOI
66 Ashok, M., Turner, C., Wilson, T.G., 1998. Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc. Natl. Acad. Sci. 95, 2761-2766.   DOI
67 Banks, W., Lofgren, C., 1991. Effectiveness of the insect growth regulator pyriproxyfen against the red imported fire ant (Hymenoptera: Formicidae). J. Entomol. Sci. 26, 331-338.   DOI
68 Stall, G., 1986. Anti juvenile hormone agents. Annu. Rev. Entomol. 31, 391-429.   DOI