Transcription-inducing activity of natural and synthetic juvenile hormone agonists through the Drosophila Methoprene-tolerant protein.
Drosophila melanogaster
Methoprene-tolerant
Taiman
juvenile hormone agonists
luciferase reporter assay
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Jul 2020
Jul 2020
Historique:
received:
14
11
2019
revised:
15
01
2020
accepted:
30
01
2020
pubmed:
1
2
2020
medline:
7
8
2020
entrez:
1
2
2020
Statut:
ppublish
Résumé
Juvenile hormones (JHs) are a class of sesquiterpenoids that play a pivotal role in insect growth and reproduction. Synthetic JH agonists (JHAs), including pyriproxyfen, have been widely used as insecticides to control agricultural pests and disease vectors. The antimetamorphic action of JHAs is mediated by their intracellular receptor, the heterodimer of Methoprene-tolerant (Met) and Taiman (Tai) proteins. Although a range of bioassay systems has been developed to detect the activity of JHAs, each of these systems has its own drawback(s), such as poor reproducibility, the use of radioactive ligands or the effect of endogenous JH-signaling factors. To address these issues, we constructed a new luciferase reporter assay for JHAs in mammalian HEK293T cells transiently transfected with the Drosophila Met and Tai genes. This reporter system gave highly reproducible results and showed nanomolar sensitivity to natural JHs. We then applied this reporter system to a structure-activity relationship (SAR) analysis of 14 natural and synthetic JHAs, leading to identification of the ligand structural factors important for the transcription-inducing activity. Because this reporter system is not affected by the signaling cascade downstream of the JH receptors, it is suitable for evaluating the intrinsic activity of JHAs. The SAR results obtained in this study therefore provide invaluable information on the rational design of novel JHA insecticides.
Sections du résumé
BACKGROUND
BACKGROUND
Juvenile hormones (JHs) are a class of sesquiterpenoids that play a pivotal role in insect growth and reproduction. Synthetic JH agonists (JHAs), including pyriproxyfen, have been widely used as insecticides to control agricultural pests and disease vectors. The antimetamorphic action of JHAs is mediated by their intracellular receptor, the heterodimer of Methoprene-tolerant (Met) and Taiman (Tai) proteins. Although a range of bioassay systems has been developed to detect the activity of JHAs, each of these systems has its own drawback(s), such as poor reproducibility, the use of radioactive ligands or the effect of endogenous JH-signaling factors.
RESULTS
RESULTS
To address these issues, we constructed a new luciferase reporter assay for JHAs in mammalian HEK293T cells transiently transfected with the Drosophila Met and Tai genes. This reporter system gave highly reproducible results and showed nanomolar sensitivity to natural JHs. We then applied this reporter system to a structure-activity relationship (SAR) analysis of 14 natural and synthetic JHAs, leading to identification of the ligand structural factors important for the transcription-inducing activity.
CONCLUSION
CONCLUSIONS
Because this reporter system is not affected by the signaling cascade downstream of the JH receptors, it is suitable for evaluating the intrinsic activity of JHAs. The SAR results obtained in this study therefore provide invaluable information on the rational design of novel JHA insecticides.
Substances chimiques
Drosophila Proteins
0
Methoprene
8B830OJ2UX
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2316-2323Subventions
Organisme : Japan Society for the Promotion of Science
ID : JP16K07625
Organisme : Japan Society for the Promotion of Science
ID : JP17J01486
Organisme : Japan Society for the Promotion of Science
ID : JP19K06051
Informations de copyright
© 2020 Society of Chemical Industry.
Références
Riddiford LM, Cellular and molecular actions of juvenile hormone I. general considerations and Premetamorphic actions. Adv Insect Physiol 24:213-274 (1994).
Wyatt GR and Davey KG, Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Adv Insect Physiol 26:1-155 (1996).
Goodman WG and Cusson M, The juvenile hormones, in Insect Endocrinology, ed. by, ed. by Gilbert LI. Elsevier, Amsterdam, pp. 310-365 (2012).
Röller H, Dahm KH, Sweely CC and Trost BM, The structure of the juvenile hormone. Angew Chem Int Ed Engl 6:179-180 (1967).
Meyer AS, Schneiderman HA, Hanzmann E and Ko JH, The two juvenile hormones from the Cecropia silk moth. Proc Natl Acad Sci 60:853-860 (1968).
Judy KJ, Schooley DA, Dunham LL, Hall MS, Bergot BJ and Siddall JB, Isolation, structure, and absolute configuration of a new natural insect juvenile hormone from Manduca sexta. Proc Natl Acad Sci 70:1509-1513 (1973).
Bergot BJ, Jamieson GC, Ratcliff MA and Schooley DA, JH Zero: new naturally occurring insect juvenile hormone from developing embryos of the tobacco hornworm. Science 210:336-338 (1980).
Wen D, Rivera-Perez C, Abdou M, Jia Q, He Q, Liu X et al., Methyl Farnesoate plays a dual role in regulating Drosophila metamorphosis. PLoS Genet 11:e1005038 (2015).
Richard DS, Applebaum SW, Sliter TJ, Baker FC, Schooley DA, Reuter CC et al., Juvenile hormone bisepoxide biosynthesis in vitro by the ring gland of Drosophila melanogaster: a putative juvenile hormone in the higher Diptera. Proc Natl Acad Sci 86:1421-1425 (1989).
Kotaki T, Shinada T, Kaihara K, Ohfune Y and Numata H, Structure determination of a new juvenile hormone from a Heteropteran insect. Org Lett 11:5234-5237 (2009).
Dhadialla TS, Carlson GR and Le DP, New insecticides with Ecdysteroidal and juvenile hormone activity. Annu Rev Entomol 43:545-569 (1998).
Sparks TC and Nauen R, IRAC: mode of action classification and insecticide resistance management. Pest Biochem Physiol 121:122-128 (2015).
Wigglesworth VB, The physiology of ecdysis in Rhodnius Prolixus (Hemiptera). II. Factors controlling moulting and “Metamorphosis”. Q J Microsc Sci 77:191-222 (1934).
Wigglesworth VB, The function of the corpus allatum in the growth and reproduction of Rhodnius Prolixus (Hemiptera). Q J Microsc Sci 79:91-121 (1936).
Jindra M, Palli SR and Riddiford LM, The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181-204 (2013).
Jindra M, Bellés X and Shinoda T, Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci 11:39-46 (2015).
Ashok M, Turner C and Wilson TG, Insect juvenile hormone resistance gene homology with the bHLH-PAS family of transcriptional regulators. Proc Natl Acad Sci 95:2761-2766 (1998).
Moore AW, Barbel S, Jan LY and Jan YN, A genomewide survey of basic helix-loop-helix factors in Drosophila. Proc Natl Acad Sci 97:10436-10441 (2000).
Abdou MA, He Q, Wen D, Zyaan O, Wang J, Xu J et al., Drosophila met and Gce are partially redundant in transducing juvenile hormone action. Insect Biochem Mol Biol 41:938-945 (2011).
Minakuchi C, Zhou X and Riddiford LM, Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125:91-105 (2008).
Minakuchi C, Namiki T and Shinoda T, 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 325:341-350 (2009).
Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M et al., Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci 109:11729-11734 (2012).
Ashburner M, Effects of juvenile hormone on adult differentiation of Drosophila melanogaster. Nature 227:187-189 (1970).
Henrick CA, Willy WE and Staal GB, Insect juvenile hormone activity of alkyl (2E,4E)-3,7,11-trimethyl-2,4-dodecadienoates. Variations in the ester function and in the carbon chain. J Agric Food Chem 24:207-218 (1976).
Fain MJ and Riddiford LM, Titers in the Hemolymph during late larval development of the tobacco hornworm, Manduca sexta (L.). Biol Bull 149:506-521 (1975).
Imoto S, Nishioka T, Fujita T and Nakajima M, Hormonal requirements for the larval-pupal ecdysis induced in the cultured integument of Chilo suppressalis. J Insect Physiol 28:1025-1033 (1982).
Kitahara K, Nishioka T and Fujita T, Cultured integument of Chilo suppressalis as a bioassay system for juvenile hormones. Agric Biol Chem 47:2841-2847 (1983).
Miura K, Oda M, Makita S and Chinzei Y, Characterization of the Drosophila Methoprene-tolerant gene product. FEBS J 272:1169-1178 (2005).
Charles J-P, Iwema T, Epa VC, Takaki K, Rynes J and Jindra M, Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci 108:21128-21133 (2011).
Jindra M, Uhlirova M, Charles J-P, Smykal V and Hill RJ, Genetic evidence for function of the bHLH-PAS protein Gce/met as a juvenile hormone receptor. PLoS Genet 11:e1005394 (2015).
Bittova L, Jedlicka P, Dracinsky M, Kirubakaran P, Vondrasek J, Hanus R et al., Exquisite ligand stereoselectivity of a Drosophila juvenile hormone receptor contrasts with its broad agonist repertoire. J Biol Chem 294:410-423 (2019).
Miyakawa H and Iguchi T, Comparative luciferase assay for establishing reliable in vitro screening system of juvenile hormone agonists. J Appl Toxicol 37:1082-1090 (2017).
Ito-Harashima S, Matsuura M, Kawanishi M, Nakagawa Y and Yagi T, New reporter gene assays for detecting natural and synthetic molting hormone agonists using yeasts expressing ecdysone receptors of various insects. FEBS Open Biol 7:995-1008 (2017).
Thierbach G, Kalinowski J, Bachmann B and Pühler A, Cloning of a DNA fragment from Corynebacterium glutamicum conferring aminoethyl cysteine resistance and feedback resistance to aspartokinase. Appl Microbiol Biotechnol 32:443-448 (1990).
Sakuma M, Probit analysis of preference data. Appl Entomol Zool 33:339-347 (1998).
Manabe A, Ohfune Y and Shinada T, Stereoselective Total syntheses of insect juvenile hormones JH 0 and JH I. Synlett 23:1213-1216 (2012).
Ogura K, Nishino T, Koyama T and Seto S, Enzymic condensation of 3-methyl-2-alkenyl pyrophosphates with isopentenyl pyrophosphate. J Am Chem Soc 92:6036-6041 (1970).
Crispino GA and Sharpless KB, Enantioselective synthesis of juvenile hormone III in three steps from methyl Farnesoate. Synthesis 1993:777-779 (1993).
Okochi T and Mori K, New Enantioselective synthesis of (10R,11S)-(+)-juvenile hormones I and II. Eur J Org Chem 2001:2145-2150 (2001).
Mori K and Mori H, Synthesis of both the enantiomers of juvenile hormone III. Tetrahedron 43:4097-4106 (1987).
Ichikawa A, Ono H, Furuta K, Shiotsuki T and Shinoda T, Enantioselective separation of racemic juvenile hormone III by normal-phase high-performance liquid chromatography and preparation of [2H3]juvenile hormone III as an internal standard for liquid chromatography-mass spectrometry quantification. J Chromatogr A 1161:252-260 (2007).
Jindra M and Bittova L, The juvenile hormone receptor as a target of juvenoid “insect growth regulators”. Arch Insect Biochem Physiol 103:e21615 (2019).
Jones G, Teal P, Henrich VC, Krzywonos A, Sapa A, Wozniak M et al., Ligand binding pocket function of Drosophila USP is necessary for metamorphosis. Gen Comp Endocrinol 182:73-82 (2013).
Nishida S, Matsuo N, Hatakoshi M and Kishida H, Nitrogen-containing heterocyclic compounds, and their production and use. US Patent 4,970,222 (1990).
Hatakoshi M, Nishida S, Kishida H and Oouchi H, Development of new insect growth regulator, pyriproxyfen. Nippon Nōgeikagaku Kaishi 77:730-735 (2003).