BACKGROUND: Epigenetic modifications including DNA methylation and post-translational modifications of histones are known to regulate gene expression. Antagonistic activities of histone acetyltransferases (HATs) and histone deacetylases (HDACs) mediate transcriptional reprogramming during insect development as shown in Drosophila melanogaster and other insects. Juvenile hormones (JH) play vital roles in the regulation of growth, development, metamorphosis, reproduction and other physiological processes. However, our current understanding of epigenetic regulation of JH action is still limited. Hence, we studied the role of CREB binding protein (CBP, contains HAT domain) and Trichostatin A (TSA, HDAC inhibitor) on JH action. RESULTS: Exposure of Tribolium castaneum cells (TcA cells) to JH or TSA caused an increase in expression of Kr-h1 (a known JH-response gene) and 31 or 698 other genes respectively. Knockdown of the gene coding for CBP caused a decrease in the expression of 456 genes including Kr-h1. Interestingly, the expression of several genes coding for transcription factors, nuclear receptors, P450 and fatty acid synthase family members that are known to mediate JH action were affected by CBP knockdown or TSA treatment. CONCLUSIONS: These data suggest that acetylation and deacetylation mediated by HATs and HDACs play an important role in JH action.

Department of Entomology College of Agriculture Food and Environment University of Kentucky Lexington KY 40546 USA

Faculty of Forestry and Wood Sciences EXTEMIT K Czech University of Life Sciences Kamýcká 1176 Prague 6 165 21 Suchdol Czech Republic

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Buszczak M, Segraves WA. Insect metamorphosis: out with the old, in with the new. Curr Biol. 2000;10(22):R830–R833. doi: 10.1016/S0960-9822(00)00792-2. PubMed DOI

Truman JW, Riddiford LM. Endocrine insights into the evolution of metamorphosis in insects. Annu Rev Entomol. 2002;47(1):467–500. doi: 10.1146/annurev.ento.47.091201.145230. PubMed DOI

Yamanaka N, Rewitz KF, O'Connor MB. Ecdysone control of developmental transitions: lessons from Drosophila research. Annu Rev Entomol. 2013;58:497–516. doi: 10.1146/annurev-ento-120811-153608. PubMed DOI PMC

Dubrovsky EB. Hormonal cross talk in insect development. Trends Endocrinol Metab. 2005;16(1):6–11. doi: 10.1016/j.tem.2004.11.003. PubMed DOI

Nakagawa Y, Henrich VC. Arthropod nuclear receptors and their role in molting. FEBS J. 2009;276(21):6128–6157. doi: 10.1111/j.1742-4658.2009.07347.x. PubMed DOI

Riddiford LM. How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocrinol. 2012;179(3):477–484. doi: 10.1016/j.ygcen.2012.06.001. PubMed DOI

Jindra M, Palli SR, Riddiford LM. The juvenile hormone signaling pathway in insect development. Annu Rev Entomol. 2013;58:181–204. doi: 10.1146/annurev-ento-120811-153700. PubMed DOI

Kayukawa T, Jouraku A, Ito Y, Shinoda T. Molecular mechanism underlying juvenile hormone-mediated repression of precocious larval–adult metamorphosis. Proc Natl Acad Sci U S A. 2017;201615423. PubMed PMC

Liu P, Peng H-J, Zhu J. Juvenile hormone-activated phospholipase C pathway enhances transcriptional activation by the methoprene-tolerant protein. Proc Natl Acad Sci U S A. 2015;112(15):E1871–E1879. doi: 10.1073/pnas.1423204112. PubMed DOI PMC

Li K, Jia QQ, Li S. Juvenile hormone signaling–a mini review. Insect science. 2018. PubMed

Bai H, Palli SR. Identification of G protein-coupled receptors required for vitellogenin uptake into the oocytes of the red flour beetle, Tribolium castaneum. Sci Rep. 2016;6:27648. doi: 10.1038/srep27648. PubMed DOI PMC

Cai M-J, Dong D-J, Wang Y, Liu P-C, Liu W, Wang J-X, Zhao X-F. G-protein-coupled receptor participates in 20-hydroxyecdysone signaling on the plasma membrane. Cell Communication and Signaling. 2014;12(1):9. doi: 10.1186/1478-811X-12-9. PubMed DOI PMC

Luft UC, Bychkov R, Gollasch M, Gross V, Roullet J-B, McCarron DA, Ried C, Hofmann F, Yagil Y, Yagil C. Farnesol blocks the L-type Ca2+ channel by targeting the α1C subunit. Arterioscler Thromb Vasc Biol. 1999;19(4):959–966. doi: 10.1161/01.ATV.19.4.959. PubMed DOI

Wyatt GR, Davey KG. Cellular and molecular actions of juvenile hormone. II. Roles of juvenile hormone in adult insects. Adv Insect Physiol. 1996;26:1–155. doi: 10.1016/S0065-2806(08)60030-2. DOI

Soller M, Bownes M, Kubli E. Control of oocyte maturation in sexually matureDrosophilafemales. Dev Biol. 1999;208(2):337–351. doi: 10.1006/dbio.1999.9210. PubMed DOI

Herndon L, Chapman T, Kalb J, Lewin S, Partridge L, Wolfner M. Mating and hormonal triggers regulate accessory gland gene expression in male Drosophila. J Insect Physiol. 1997;43(12):1117–1123. doi: 10.1016/S0022-1910(97)00062-0. PubMed DOI

Belgacem YH, Martin J-R. Neuroendocrine control of a sexually dimorphic behavior by a few neurons of the pars intercerebralis in Drosophila. Proc Natl Acad Sci U S A. 2002;99(23):15154–15158. doi: 10.1073/pnas.232244199. PubMed DOI PMC

Parthasarathy R, Tan A, Sun Z, Chen Z, Rankin M, Palli SR. Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mech Dev. 2009;126(7):563–579. doi: 10.1016/j.mod.2009.03.005. PubMed DOI PMC

Akimaru H, Chen Y, Dai P, Hou D-X, Nonaka M, Smolik SM, Armstrong S, Goodman RH, Ishii S. Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature. 1997;386(6626):735–738. doi: 10.1038/386735a0. PubMed DOI

Akimaru H, Hou D-X, Ishii S. Drosophila CBP is required for dorsal–dependent twist gene expression. Nat Genet. 1997;17(2):211–214. doi: 10.1038/ng1097-211. PubMed DOI

Hung H-C, Maurer C, Kay SA, Weber F. Circadian transcription depends on limiting amounts of the transcription co-activator nejire/CBP. J Biol Chem. 2007;282(43):31349–31357. doi: 10.1074/jbc.M702319200. PubMed DOI

McManus KJ, Hendzel MJ. CBP, a transcriptional coactivator and acetyltransferase. Biochem Cell Biol. 2001;79(3):253–266. doi: 10.1139/o01-076. PubMed DOI

Goodman RH, Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev. 2000;14(13):1553–1577. PubMed

Ylla G, Belles X. Corrigendum to “towards understanding the molecular basis of cockroach tergal gland morphogenesis. A transcriptomic approach”[insect Biochem. Mol. Biol. 63 (2015) 104–112] Insect Biochem Mol Biol. 2015;65:108. doi: 10.1016/j.ibmb.2015.08.006. PubMed DOI

Spannhoff A, Kim YK, Raynal NJM, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JPJ. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. 2011;12(3):238–243. doi: 10.1038/embor.2011.9. PubMed DOI PMC

Lockett GA, Wilkes F, Helliwell P, Maleszka R. Contrasting effects of histone deacetylase inhibitors on reward and aversive olfactory memories in the honey bee. Insects. 2014;5(2):377–398. doi: 10.3390/insects5020377. PubMed DOI PMC

Ozawa T, Mizuhara T, Arata M, Shimada M, Niimi T, Okada K, Okada Y, Ohta K. Histone deacetylases control module-specific phenotypic plasticity in beetle weapons. Proc Natl Acad Sci. 2016;113(52):15042-7. PubMed PMC

Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C, Ray A, Zwiebel LJ, Bonasio R, Reinberg D, Liebig J. Epigenetic (re) programming of caste-specific behavior in the ant Camponotus floridanus. Science. 2016;351(6268):aac6633. doi: 10.1126/science.aac6633. PubMed DOI PMC

Kayukawa T, Tateishi K, Shinoda T. Establishment of a versatile cell line for juvenile hormone signaling analysis in Tribolium castaneum. Sci Rep. 2013;3:1570. doi: 10.1038/srep01570. PubMed DOI PMC

Xu J, Roy A, Palli SR. CREB-binding protein plays key roles in juvenile hormone action in the red flour beetle, Tribolium Castaneum. Sci Rep. 2018;8(1):1426. doi: 10.1038/s41598-018-19667-6. PubMed DOI PMC

Goodman CL, Stanley D, Ringbauer JA, RW JB, Silver K, Park Y. A cell line derived from the red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae) In vitro cellular & developmental biology Animal. 2012;48(7):426–433. doi: 10.1007/s11626-012-9524-x. PubMed DOI

Zhang Z, Xu J, Sheng Z, Sui Y, Palli SR. Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J Biol Chem. 2011;286(10):8437–8447. doi: 10.1074/jbc.M110.191684. PubMed DOI PMC

Kalsi M, Palli SR. Cap n collar transcription factor regulates multiple genes coding for proteins involved in insecticide detoxification in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol. 2017;90:43–52. doi: 10.1016/j.ibmb.2017.09.009. PubMed DOI

Ma L, Pati PK, Liu M, Li QQ, Hunt AG. High throughput characterizations of poly (a) site choice in plants. Methods. 2014;67(1):74–83. doi: 10.1016/j.ymeth.2013.06.037. PubMed DOI PMC

Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Bucher G, Friedrich M, Grimmelikhuijzen CJ. The genome of the model beetle and pest Tribolium castaneum. Nature. 2008;452(7190):949–955. doi: 10.1038/nature06784. PubMed DOI

Roy A, Walker WB, Vogel H, Kushwaha S, Chattington S, Larsson M, Anderson P, Heckel D, Schlyter F. Data set for diet specific differential gene expression analysis in three Spodoptera moths. Data in brief. 2016;8:448–455. doi: 10.1016/j.dib.2016.04.029. PubMed DOI PMC

Kalsi M, Palli SR. Transcription factors, CncC and Maf, regulate expression of CYP6BQ genes responsible for deltamethrin resistance in Tribolium castaneum. Insect Biochem Mol Biol. 2015;65:47–56. doi: 10.1016/j.ibmb.2015.08.002. PubMed DOI

Parthasarathy R, Tan A, Palli SR. bHLH-PAS family transcription factor methoprene-tolerant plays a key role in JH action in preventing the premature development of adult structures during larval-pupal metamorphosis. Mech Dev. 2008;125:601-16. PubMed PMC

Xu J, Sheng Z, Palli SR. Juvenile hormone and insulin regulate trehalose homeostasis in the red flour beetle, Tribolium castaneum. PLoS Genet. 2013;9(6):e1003535. doi: 10.1371/journal.pgen.1003535. PubMed DOI PMC

Nijhout HF. Insect Hormones. Princeton: Princeton Univ. Press; 1994.

Staal G. Anti juvenile hormone agents. Annu Rev Entomol. 1986;31(1):391–429. doi: 10.1146/annurev.en.31.010186.002135. DOI

Tan A, Tanaka H, Tamura T, Shiotsuki T. Precocious metamorphosis in transgenic silkworms overexpressing juvenile hormone esterase. Proc Natl Acad Sci U S A. 2005;102(33):11751–11756. doi: 10.1073/pnas.0500954102. PubMed DOI PMC

Minakuchi C, Namiki T, Yoshiyama M, Shinoda T. RNAi-mediated knockdown of juvenile hormone acid O-methyltransferase gene causes precocious metamorphosis in the red flour beetle Tribolium castaneum. FEBS J. 2008;275(11):2919–2931. doi: 10.1111/j.1742-4658.2008.06428.x. PubMed DOI

Kayukawa T, Murata M, Kobayashi I, Muramatsu D, Okada C, Uchino K, Sezutsu H, Kiuchi M, Tamura T, Hiruma K. Hormonal regulation and developmental role of Krüppel homolog 1, a repressor of metamorphosis, in the silkworm Bombyx mori. Dev Biol. 2014;388(1):48–56. doi: 10.1016/j.ydbio.2014.01.022. PubMed DOI

Minakuchi C, Namiki T, Shinoda T. Kruppel 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. 2009;325(2):341–350. doi: 10.1016/j.ydbio.2008.10.016. PubMed DOI

Minakuchi C, Zhou X, Riddiford LM. Krüppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev. 2008;125(1):91–105. doi: 10.1016/j.mod.2007.10.002. PubMed DOI PMC

Parthasarathy R, Tan A, Bai H, Palli SR. Transcription factor broad suppresses precocious development of adult structures during larval-pupal metamorphosis in the red flour beetle, Tribolium castaneum. Mech Dev. 2008;125(3–4):299–313. doi: 10.1016/j.mod.2007.11.001. PubMed DOI PMC

Zhou B, Hiruma K, Shinoda T, Riddiford LM. Juvenile hormone prevents ecdysteroid-induced expression of broad complex RNAs in the epidermis of the tobacco hornworm, Manduca sexta. Dev Biol. 1998;203(2):233–244. doi: 10.1006/dbio.1998.9059. PubMed DOI

Dushay MS, Asling B, Hultmark D. Origins of immunity: relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proc Natl Acad Sci U S A. 1996;93(19):10343–10347. doi: 10.1073/pnas.93.19.10343. PubMed DOI PMC

Mosavi LK, Cammett TJ, Desrosiers DC, Zy P. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 2004;13(6):1435–1448. doi: 10.1110/ps.03554604. PubMed DOI PMC

Voronin D, Kiseleva E. Functional role of proteins containing ankyrin repeats. Cell Tiss Biol. 2008;49(12):989–999. PubMed

Flatt T, Heyland A, Rus F, Porpiglia E, Sherlock C, Yamamoto R, Garbuzov A, Palli SR, Tatar M, Silverman N. Hormonal regulation of the humoral innate immune response in Drosophila melanogaster. J Exp Biol. 2008;211(16):2712–2724. doi: 10.1242/jeb.014878. PubMed DOI PMC

Sheng Z, Xu J, Bai H, Zhu F, Palli SR. Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J Biol Chem. 2011;286(49):41924–41936. doi: 10.1074/jbc.M111.269845. PubMed DOI PMC

Comas D, Piulachs M-D, Bellés X. Induction of vitellogenin gene transcription in vitro by juvenile hormone in Blattella germanica. Mol Cell Endocrinol. 2001;183(1):93–100. doi: 10.1016/S0303-7207(01)00589-5. PubMed DOI

Chinzei Y, White B, Wyatt G. Vitellogenin mRNA in locust fat body: identification, isolation, and quantitative changes induced by juvenile hormone. Can J Biochem. 1982;60(3):243–251. doi: 10.1139/o82-029. PubMed DOI

Llano E, Adam G, Pendás AM, Quesada V, Sánchez LM, Santamaría I, Noselli S, López-Otín C. Structural and enzymatic characterization of Drosophila Dm2-MMP, a membrane-bound matrix metalloproteinase with tissue-specific expression. J Biol Chem. 2002;277(26):23321–23329. doi: 10.1074/jbc.M200121200. PubMed DOI

Llano E, Pendás AM, Aza-Blanc P, Kornberg TB, López-Otín C. Dm1-MMP, a matrix metalloproteinase fromDrosophila with a potential role in extracellular matrix remodeling during neural development. J Biol Chem. 2000;275(46):35978–35985. doi: 10.1074/jbc.M006045200. PubMed DOI

Knorr E, Schmidtberg H, Vilcinskas A, Altincicek B. MMPs regulate both development and immunity in the Tribolium model insect. PLoS One. 2009;4(3):e4751. doi: 10.1371/journal.pone.0004751. PubMed DOI PMC

Sevala VL, Davey K, Prestwich GD. Photoaffinity labeling and characterization of a juvenile hormone binding protein in the membranes of follicle cells of Locusta migratoria. Insect Biochem Mol Biol. 1995;25(2):267–273. doi: 10.1016/0965-1748(94)00065-P. DOI

Xiao W, Chen X, Liu X, Luo L, Ye S, Liu Y. Trichostatin a, a histone deacetylase inhibitor, suppresses proliferation and epithelial–mesenchymal transition in retinal pigment epithelium cells. J Cellular Mol Med. 2014;18(4):646–655. doi: 10.1111/jcmm.12212. PubMed DOI PMC

Medvedeva YA, Lennartsson A, Ehsani R, Kulakovskiy IV, Vorontsov IE, Panahandeh P, Khimulya G, Kasukawa T, Consortium F, Drabløs F. EpiFactors: a comprehensive database of human epigenetic factors and complexes. Database. 2015;2015:bav067. doi: 10.1093/database/bav067. PubMed DOI PMC

Dillon SC, Zhang X, Trievel RC, Cheng X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol. 2005;6(8):227. doi: 10.1186/gb-2005-6-8-227. PubMed DOI PMC

Takeuchi T, Watanabe Y, Takano-Shimizu T, Kondo S. Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev Dyn. 2006;235(9):2449–2459. doi: 10.1002/dvdy.20851. PubMed DOI

Vidal NM, Grazziotin AL, Iyer LM, Aravind L, Venancio TM. Transcription factors, chromatin proteins and the diversification of Hemiptera. Insect Biochem Mol Biol. 2016;69:1–13. doi: 10.1016/j.ibmb.2015.07.001. PubMed DOI PMC

Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell. 2007;128(4):735–745. doi: 10.1016/j.cell.2007.02.009. PubMed DOI

McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell. 1992;68(2):283–302. doi: 10.1016/0092-8674(92)90471-N. PubMed DOI

Hossain MS, Liu Y, Zhou S, Li K, Tian L, Li S. 20-Hydroxyecdysone-induced transcriptional activity of FoxO upregulates brummer and acid lipase-1 and promotes lipolysis in Bombyx fat body. Insect Biochem Mol Biol. 2013;43(9):829–838. doi: 10.1016/j.ibmb.2013.06.007. PubMed DOI

Zeng B, Huang Y, Xu J, Shiotsuki T, Bai H, Palli SR, Huang Y, Tan A. The FOXO transcription factor controls insect growth and development by regulating juvenile hormone degradation in the silkworm, Bombyx mori. J Biol Chem. 2017. 10.1074/jbc.M117.777797. PubMed PMC

Koyama T, Rodrigues MA, Athanasiadis A, Shingleton AW, Mirth CK. Nutritional control of body size through FoxO-Ultraspiracle mediated ecdysone biosynthesis. Elife. 2014;3:e03091. doi: 10.7554/eLife.03091. PubMed DOI PMC

Lin X, Yu N, Smagghe G. Gen comp Endocrinol. 2017. FoxO mediates the timing of pupation through regulating ecdysteroid biosynthesis in the red flour beetle, Tribolium castaneum. PubMed

Parthasarathy R, Palli SR. Molecular analysis of nutritional and hormonal regulation of female reproduction in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol. 2011;41(5):294–305. doi: 10.1016/j.ibmb.2011.01.006. PubMed DOI PMC

DeLuca HF. Overview of general physiologic features and functions of vitamin D. American J Clin Nutr. 2004;80(6):1689S–1696S. doi: 10.1093/ajcn/80.6.1689S. PubMed DOI

Martín D. Nuclear Receptor. In: Functions of nuclear receptors in insect development. Dordrecht, Heidelberg, London, New York: Springer; 2010. p. 31–61.

Fahrbach SE, Smagghe G, Velarde RA. Insect nuclear receptors. Annu Rev Entomol. 2012;57:83–106. doi: 10.1146/annurev-ento-120710-100607. PubMed DOI

Jarvela AMC, Pick L. Chapter two-the function and evolution of nuclear receptors in insect embryonic development. Curr Top Dev Biol. 2017;125:39–70. doi: 10.1016/bs.ctdb.2017.01.003. PubMed DOI

Carney GE, Wade AA, Sapra R, Goldstein ES, Bender M. DHR3, an ecdysone-inducible early-late gene encoding a Drosophila nuclear receptor, is required for embryogenesis. Proc Natl Acad Sci U S A. 1997;94(22):12024–12029. doi: 10.1073/pnas.94.22.12024. PubMed DOI PMC

Sullivan AA, Thummel CS. Temporal profiles of nuclear receptor gene expression reveal coordinate transcriptional responses during Drosophila development. Mol Endocrinol. 2003;17(11):2125–2137. doi: 10.1210/me.2002-0430. PubMed DOI

M-a Y, Murata T, Hirose S, Lavorgna G, Suzuki E, Ueda H. Temporally restricted expression of transcription factor betaFTZ-F1: significance for embryogenesis, molting and metamorphosis in Drosophila melanogaster. Development. 2000;127(23):5083–5092. PubMed

Cruz J, Martín D, Bellés X. Redundant ecdysis regulatory functions of three nuclear receptor HR3 isoforms in the direct-developing insect Blattella germanica. Mech Dev. 2007;124(3):180–189. doi: 10.1016/j.mod.2006.12.003. PubMed DOI

Broadus J, McCabe JR, Endrizzi B, Thummel CS, Woodard CT. The Drosophila βFTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol Cell. 1999;3(2):143–149. doi: 10.1016/S1097-2765(00)80305-6. PubMed DOI

Kozlova T, Pokholkova G, Tzertzinis G, Sutherland J, Zhimulev I, Kafatos F. Drosophila hormone receptor 38 functions in metamorphosis: a role in adult cuticle formation. Genetics. 1998;149(3):1465–1475. PubMed PMC

Baker KD, Shewchuk LM, Kozlova T, Makishima M, Hassell A, Wisely B, Caravella JA, Lambert MH, Reinking JL, Krause H. The Drosophila orphan nuclear receptor DHR38 mediates an atypical ecdysteroid signaling pathway. Cell. 2003;113(6):731–742. doi: 10.1016/S0092-8674(03)00420-3. PubMed DOI

Tan A, Palli SR. Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol. 2008;38(4):430–439. doi: 10.1016/j.ibmb.2007.09.012. PubMed DOI

Xu J, Tan A, Palli SR. The function of nuclear receptors in regulation of female reproduction and embryogenesis in the red flour beetle, Tribolium castaneum. J Insect Physiol. 2010;56(10):1471–1480. doi: 10.1016/j.jinsphys.2010.04.004. PubMed DOI PMC

Borras-Castells F, Nieva C, Maestro JL, Maestro O, Belles X, Martín D. Juvenile hormone biosynthesis in adult Blattella germanica requires nuclear receptors seven-up and FTZ-F1. Sci Rep. 2017;7:40234. doi: 10.1038/srep40234. PubMed DOI PMC

Tan Q-Q, Liu W, Zhu F, Lei C-L, Wang X-P. Fatty acid synthase 2 contributes to diapause preparation in a beetle by regulating lipid accumulation and stress tolerance genes expression. Sci Rep. 2017;7:40509. doi: 10.1038/srep40509. PubMed DOI PMC

Ishimaru Y, Tomonari S, Matsuoka Y, Watanabe T, Miyawaki K, Bando T, Tomioka K, Ohuchi H, Noji S, Mito T. TGF-β signaling in insects regulates metamorphosis via juvenile hormone biosynthesis. Proc Natl Acad Sci U S A. 2016;113(20):5634–5639. doi: 10.1073/pnas.1600612113. PubMed DOI PMC

Kirilly D, Wong JJ, Lim EK, Wang Y, Zhang H, Wang C, Liao Q, Wang H, Liou YC, Yu F. Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Neuron. 2011;72(1):86–100. doi: 10.1016/j.neuron.2011.08.003. PubMed DOI

Roy A, George S, Palli SR. Multiple functions of CREB-binding protein during postembryonic development: identification of target genes. BMC Genomics. 2017;18(1):996. doi: 10.1186/s12864-017-4373-3. PubMed DOI PMC

Saha TT, Shin SW, Dou W, Roy S, Zhao B, Hou Y, Wang XL, Zou Z, Girke T, Raikhel AS. Hairy and Groucho mediate the action of juvenile hormone receptor Methoprene-tolerant in gene repression. Proc Natl Acad Sci U S A. 2016;113(6):E735–E743. doi: 10.1073/pnas.1523838113. PubMed DOI PMC

Henchcliffe C, García-Alonso L, Tang J, Goodman CS. Genetic analysis of laminin a reveals diverse functions during morphogenesis in Drosophila. Development. 1993;118(2):325–337. PubMed

Dolezelova E, Zurovec M, Dolezal T, Simek P, Bryant PJ. The emerging role of adenosine deaminases in insects. Insect Biochem Mol Biol. 2005;35(5):381–389. doi: 10.1016/j.ibmb.2004.12.009. PubMed DOI

Van der Zee M, Da Fonseca RN, Roth S. TGFβ signaling in Tribolium: vertebrate-like components in a beetle. Dev Genes Evol. 2008;218(3–4):203–213. PubMed

Huang J, Tian L, Peng C, Abdou M, Wen D, Wang Y, Li S, Wang J. DPP-mediated TGFβ signaling regulates juvenile hormone biosynthesis by activating the expression of juvenile hormone acid methyltransferase. Development. 2011;138(11):2283–2291. doi: 10.1242/dev.057687. PubMed DOI

Zarin KN, Yang X, Bao R, Friedrich F, Beutel R, Friedrich M. The Pax gene eyegone facilitates repression of eye development in Tribolium. EvoDevo. 2011;2(1):8. doi: 10.1186/2041-9139-2-8. PubMed DOI PMC

Tang B, Chen J, Yao Q, Pan Z, Xu W, Wang S, Zhang W. Characterization of a trehalose-6-phosphate synthase gene from Spodoptera exigua and its function identification through RNA interference. J Insect Physiol. 2010;56(7):813–821. doi: 10.1016/j.jinsphys.2010.02.009. PubMed DOI

Chen J, Tang B, Chen H, Yao Q, Huang X, Chen J, Zhang D, Zhang W. Different functions of the insect soluble and membrane-bound trehalase genes in chitin biosynthesis revealed by RNA interference. PLoS One. 2010;5(4):e10133. doi: 10.1371/journal.pone.0010133. PubMed DOI PMC

Chen Q, Jin S, Zhang L, Shen Q, Wei P, Wei Z, Wang S, Tang B. Regulatory functions of trehalose-6-phosphate synthase in the chitin biosynthesis pathway in Tribolium castaneum (Coleoptera: Tenebrionidae) revealed by RNA interference. Bulletin of Entomol Res. 2017:1–12. PubMed

Lin X, Zhang L, Jiang Y. Distinct roles of met and interacting proteins on the expressions of takeout family genes in Brown Planthopper. Front Physiol. 2017;8. PubMed PMC

Z-p K, Huang J, Tobe SS, X-l Y. A potential insect growth regulator: synthesis and bioactivity of an allatostatin mimic. Peptides. 2009;30(7):1249–1253. doi: 10.1016/j.peptides.2009.03.010. PubMed DOI

Martin D, Piulachs M, Bellés X. Inhibition of vitellogenin production by allatostatin in the German cockroach. Mol Cell Endocrinol. 1996;121(2):191–196. doi: 10.1016/0303-7207(96)03864-6. PubMed DOI

Mayoral JG, Nouzova M, Navare A, Noriega FG. NADP+−dependent farnesol dehydrogenase, a corpora allata enzyme involved in juvenile hormone synthesis. Proc Natl Acad Sci U S A. 2009;106(50):21091–21096. doi: 10.1073/pnas.0909938106. PubMed DOI PMC

Rewitz K, Yamanaka N, O'Connor MB. Ecdysone control of developmental transitions: lessons from Drosophila research. Annu Rev Entomol. 2013;58:497–516. doi: 10.1146/annurev-ento-120811-153608. PubMed DOI PMC

Helvig C, Koener J, Unnithan G, Feyereisen R. CYP15A1, the cytochrome P450 that catalyzes epoxidation of methyl farnesoate to juvenile hormone III in cockroach corpora allata. Proc Natl Acad Sci U S A. 2004;101(12):4024–4029. doi: 10.1073/pnas.0306980101. PubMed DOI PMC

Guittard E, Blais C, Maria A, Parvy J-P, Pasricha S, Lumb C, Lafont R, Daborn PJ, Dauphin-Villemant C. CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev Biol. 2011;349(1):35–45. doi: 10.1016/j.ydbio.2010.09.023. PubMed DOI

Sutherland T, Unnithan G, Andersen J, Evans P, Murataliev M, Szabo L, Mash E, Bowers W, Feyereisen R. A cytochrome P450 terpenoid hydroxylase linked to the suppression of insect juvenile hormone synthesis. Proc Natl Acad Sci U S A. 1998;95(22):12884–12889. doi: 10.1073/pnas.95.22.12884. PubMed DOI PMC

Darakananda K. The role of the hedgehog signaling pathway in the regulation of larval and adult appendage patterning in the flour beetle, Tribolium Castaneum. Honors Thesis Collection. 2014:205.

Süren-Castillo S, Abrisqueta M, Maestro JL. FoxO inhibits juvenile hormone biosynthesis and vitellogenin production in the German cockroach. Insect Biochem Mol Biol. 2012;42(7):491–498. doi: 10.1016/j.ibmb.2012.03.006. PubMed DOI

Bellés X, Martín D, Piulachs M-D. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annu Rev Entomol. 2005;50:181–199. doi: 10.1146/annurev.ento.50.071803.130356. PubMed DOI

Tanji T, Ip YT. Regulators of the toll and Imd pathways in the Drosophila innate immune response. Trends Immunol. 2005;26(4):193–198. doi: 10.1016/j.it.2005.02.006. PubMed DOI

Noriega FG. Juvenile hormone biosynthesis in insects: what is new, what do we know, and what questions remain? Int Sch Res Notices. 2014;2014:16. PubMed PMC

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