Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
권호 표지
DOI QR코드

DOI QR Code

Insect Juvenile Hormone Antagonists as Eco-friendly Insecticides

친환경 살충제로서의 곤충 유충호르몬 길항제

  • 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)
  • 최재영 (서울대학교 농업생명과학연구원) ;
  • 제연호 (서울대학교 농업생명과학연구원)
  • Received : 2021.12.28
  • Accepted : 2022.02.09
  • Published : 2022.03.01
Download PDF
⟨ Previous Next ⟩

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.

곤충생장조절제(IGR)은 대상 해충에 대한 특이성이 높고 환경에 대한 독성이 상대적으로 낮다는 장점으로 유기합성 살충제를 효과적으로 대체할 수 있는 유망한 수단으로 여겨진다. 현재 시판되는 곤충생장조절제는 작용 기작에 따라 유충호르몬 작용제(JHA), 탈피호르몬 작용제(EA) 및 키틴 합성 저해제(CSI)의 세 가지로 구분된다. 최근 들어, 이집트숲모기의 Met과 FISC/CYC 유전자를 yeast two-hybrid system에 도입하여 유충호르몬에 의해 매개되는 Met과 FISC/CYC의 결합을 in vitro에서 구현하였으며, yeast two-hybrid β-galactosidase assay를 통하여 식물과 미생물 및 화합물 library로부터 다양한 유충호르몬 길항제(JHAN)가 분리되고 있다. 유충호르몬은 곤충의 발달, 생식, 휴면 등을 포함한 다양한 생리 작용을 조절하기 때문에, 유충호르몬 길항제는 대상 해충의 내분비 신호 전달을 방해하여 비정상적인 발달 및 유충 단계에서의 치사를 초래하며, 이는 유충호르몬 길항제가 넓은 기주 범위를 가진 살충제 개발에 효과적으로 이용될 수 있다는 것을 시사하였다. 따라서 본 논문에서는 유충호르몬 길항제의 작용점인 Met에 의해 매개되는 유충호르몬의 신호 전달 체계와 친환경 살충제로서의 유충호르몬 길항제의 전망에 대해 알아보고자 하였다.

Keywords

Acknowledgement

본 연구는 농촌진흥청에서 시행한 농축산물 생산현장의 안전관리 기술개발사업(PJ015927)의 연구비 지원에 의하여 수행되었음.

References

  1. 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. https://doi.org/10.1016/j.ibmb.2011.09.003
  2. Alzogaray, R.A., Zerba, E.N., 2017. Rhodnius prolixus intoxicated. J. Insect Physiol. 97, 93-113. https://doi.org/10.1016/j.jinsphys.2016.04.004
  3. 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. https://doi.org/10.1073/pnas.95.6.2761
  4. 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. https://doi.org/10.1590/S0074-02761991000600026
  5. Banerjee, S., Kalena, G., Banerji, A., Singh, A., 2008. New synthetic precocenoids as potential insect control agents. J. Environ. Biol 29, 951-957.
  6. 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. https://doi.org/10.18474/0749-8004-26.3.331
  7. 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. https://doi.org/10.1534/genetics.110.116962
  8. 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. https://doi.org/10.1016/j.jinsphys.2010.05.001
  9. 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.
  10. 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.
  11. 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. https://doi.org/10.1074/jbc.M111.327254
  12. 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. https://doi.org/10.3390/insects3010324
  13. Bowers, W., Fales, H., Thompson, M., Uebel, E., 1966. Juvenile hormone: identification of an active compound from balsam fir. Science 154, 1020-1021. https://doi.org/10.1126/science.154.3752.1020
  14. 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.
  15. 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. https://doi.org/10.1126/science.986685
  16. 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. https://doi.org/10.1017/S0007485311000654
  17. Cantrell, C.L., Dayan, F.E., Duke, S.O., 2012. Natural products as sources for new pesticides. J. Nat. Prod. 75, 1231-1242. https://doi.org/10.1021/np300024u
  18. 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. https://doi.org/10.1073/pnas.1116123109
  19. 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. https://doi.org/10.1603/EC10239
  20. 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. https://doi.org/10.1584/jpestics.G06-46
  21. 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. https://doi.org/10.1016/j.bbrc.2006.02.097
  22. 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. https://doi.org/10.1016/j.mce.2011.06.035
  23. Hartfelder, K., 2005. Endocrine control of insect polyphenism. Comprehensive Molecular Insect Science 3, 651-703. https://doi.org/10.1016/B0-44-451924-6/00045-4
  24. Hartfelder, K., Emlen, D., 2012. Endocrine control of insect polyphenism, in: Gilbert, L.I. (Ed.), Insect endocrinology. Elsevier, pp. 464-522.
  25. 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. https://doi.org/10.1074/jbc.M114.582825
  26. 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. https://doi.org/10.1111/j.1432-1033.2004.04023.x
  27. 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. https://doi.org/10.1021/jf60187a043
  28. 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. https://doi.org/10.1038/nrmicro1101
  29. 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. https://doi.org/10.1073/pnas.70.5.1509
  30. 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. https://doi.org/10.1016/j.ibmb.2011.05.009
  31. 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. https://doi.org/10.1016/j.cbpc.2019.108651
  32. Koehler, P.G., Patterson, R.S., 1991. Incorporation of pyriproxyfen in a German cockroach (Dictyoptera: Blattellidae) management program. J. Econ. Entomol. 84, 917-921. https://doi.org/10.1093/jee/84.3.917
  33. 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. https://doi.org/10.1073/pnas.0703719104
  34. Kotaki, T., 1996. Evidence for a new juvenile hormone in a stink bug, Plautia stali. J. Insect Physiol. 42, 279-286. https://doi.org/10.1016/0022-1910(95)00113-1
  35. 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. https://doi.org/10.1021/ol902161x
  36. 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. https://doi.org/10.1016/j.pestbp.2018.06.013
  37. 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. https://doi.org/10.1016/j.aspen.2017.11.009
  38. 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. https://doi.org/10.1073/pnas.1424386112
  39. Letellier, C., Haubruge, E., Gaspar, C., 1995. Biological activity of fenoxycarb against Sitophilus zeamais Motsch.(Coleoptera: Curculionidae). J. Stored Prod. Res. 31, 37-42. https://doi.org/10.1016/0022-474X(94)00033-P
  40. 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. https://doi.org/10.1073/pnas.1013914108
  41. 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. https://doi.org/10.1002/ps.2780180203
  42. 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. https://doi.org/10.1073/pnas.60.3.853
  43. 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.
  44. 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.
  45. 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. https://doi.org/10.1016/j.aspen.2020.05.006
  46. Pedigo, L.P., Rice, M.E., Krell, R.K., 2021. Entomology and pest management. Waveland Press. Illinois.
  47. Pener, M.P., Dhadialla, T.S., 2012. An overview of insect growth disruptors; applied aspects. Adv. Insect Physiol. 43, 1-162. https://doi.org/10.1016/B978-0-12-391500-9.00001-2
  48. Raikhel, A., Brown, M., Belles, X., 2005. 3.9 Hormonal control of reproductive processes. Comprehens Mol. Insect Sci. 3, 433-491. https://doi.org/10.1016/B0-44-451924-6/00040-5
  49. Riddiford, L.M., 2008. Juvenile hormone action: a 2007 perspective. J. Insect Physiol. 54, 895-901. https://doi.org/10.1016/j.jinsphys.2008.01.014
  50. Roller, H., 1967. The structure of the juvenile hormone. Angew. Chem. Int. Ed. Engl. 6, 179-180. https://doi.org/10.1002/anie.196701792
  51. Schmialek, P., 1961. Die Identifizierung zweier im Tenebriokot und in Hefe vorkommender Substanzen mit Juvenilhormonwirkung. Zeitschrift fur Naturforschung B 16, 461-464. https://doi.org/10.1515/znb-1961-0710
  52. 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.
  53. Schneiderman, H.A., Gilbert, L.I., Weinstein, M.J., 1960. Juvenile hormone activity in micro-organisms and plants. Nature 188, 1041-1042. https://doi.org/10.1038/1881041a0
  54. 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.
  55. 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. https://doi.org/10.1007/BF00234326
  56. 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. https://doi.org/10.1073/pnas.1214209109
  57. 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. https://doi.org/10.1590/S0037-86822007000600002
  58. Slama, K., 2016. Pharmacology of insect juvenile hormones. Comprehensive Insect Physiol. Biochem. Phramacol. 11, 357-394.
  59. Slama, K., Williams, C.M., 1965. Juvenile hormone activity for the bug Pyrrhocoris apterus. Proc. Natl. Acad. Sci. U. S. A. 54, 411-414. https://doi.org/10.1073/pnas.54.2.411
  60. 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. https://doi.org/10.1038/210329a0
  61. Stall, G., 1986. Anti juvenile hormone agents. Annu. Rev. Entomol. 31, 391-429. https://doi.org/10.1146/annurev.en.31.010186.002135
  62. 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. https://doi.org/10.1242/jcs.s2-79.313.91
  63. Williams, C.M., 1956. The juvenile hormone of insects. Nature 178, 212-213. https://doi.org/10.1038/178212b0
  64. Williams, C.M., 1967. Third-generation pesticides. Sci. Am. 217, 13-17. https://doi.org/10.1038/scientificamerican0767-13
  65. Williams, C.M., Moorhead, L.V., Pulis, J.F., 1959. Juvenile hormone in thymus, human placenta and other mammalian organs. Nature 183, 405-405. https://doi.org/10.1038/183405a0
  66. Wilson, T.G., Fabian, J., 1986. A Drosophila melanogaster mutant resistant to a chemical analog of juvenile hormone. Dev. Biol. 118, 190-201. https://doi.org/10.1016/0012-1606(86)90087-4
  67. 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. https://doi.org/10.1111/jen.12788
  68. 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. https://doi.org/10.1074/jbc.M110.191684