CREB-binding protein plays key roles in juvenile hormone action in the red flour beetle, Tribolium Castaneum
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, N.I.H., Extramural, Research Support, U.S. Gov't, Non-P.H.S.
Grant support
R01 GM070559
NIGMS NIH HHS - United States
PubMed
29362416
PubMed Central
PMC5780420
DOI
10.1038/s41598-018-19667-6
PII: 10.1038/s41598-018-19667-6
Knihovny.cz E-resources
- MeSH
- Acetylation MeSH
- Gene Knockout Techniques MeSH
- Histones metabolism MeSH
- Insect Proteins genetics metabolism MeSH
- Juvenile Hormones pharmacology MeSH
- CREB-Binding Protein genetics metabolism MeSH
- Tribolium genetics growth & development metabolism MeSH
- Gene Expression Regulation, Developmental drug effects MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, N.I.H., Extramural MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Names of Substances
- Histones MeSH
- Insect Proteins MeSH
- Juvenile Hormones MeSH
- CREB-Binding Protein MeSH
Juvenile hormones (JH) and ecdysteroids regulate many biological and metabolic processes. CREB-binding protein (CBP) is a transcriptional co-regulator with histone acetyltransferase (HAT) activity. Therefore, CBP is involved in activation of many transcription factors that regulate expression of genes associated with postembryonic development in insects. However, the function of CBP in JH action in insects is not well understood. Hence, we studied the role of CBP in JH action in the red flour beetle, Tribolium castaneum and the Tribolium cell line. CBP knockdown caused a decrease in JH induction of genes, Kr-h1, 4EBP and G13402 in T. castaneum larvae, adults and TcA cells whereas, Trichostatin A [TSA, a histone deacetylase (HDAC) inhibitor] induced the expression of these JH-response genes. Western blot analysis with specific antibodies revealed the requirement of CBP for the acetylation of H3K18 and H3K27 in both T. castaneum and TcA cells. Chromatin immunoprecipitation (Chip) assays showed the importance of CBP-mediated acetylation of H3K27 for JH induction of Kr-h1, 4EBP, and G13402 in TcA cells. These data suggest that CBP plays an important role in JH action in the model insect, T.castaneum.
See more in PubMed
Jindra M, Palli SR, Riddiford LM. The juvenile hormone signaling pathway in insect development. Annual Review of Entomology. 2013;58(181–204):120811–153700. PubMed
Jindra M, Belles X, Shinoda T. Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci. 2015;11:39–46. doi: 10.1016/j.cois.2015.08.004. PubMed DOI
Mirth CK, et al. Juvenile hormone regulates body size and perturbs insulin signaling in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2014;111:7018–7023. doi: 10.1073/pnas.1313058111. 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. The Journal of biological chemistry. 2011;286:41924–41936. doi: 10.1074/jbc.M111.269845. PubMed DOI PMC
Abdou M, et al. Wnt signaling cross-talks with JH signaling by suppressing Met and gce expression. PloS one. 2011;6:e26772. doi: 10.1371/journal.pone.0026772. PubMed DOI PMC
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. The Journal of biological chemistry. 2011;286:8437–8447. doi: 10.1074/jbc.M110.191684. PubMed DOI PMC
Charles JP, et al. Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proceedings of the National Academy of Sciences of the United States of America. 2011;108:21128–21133. doi: 10.1073/pnas.1116123109. PubMed DOI PMC
Li M, Mead EA, Zhu J. Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proceedings of the National Academy of Sciences of the United States of America. 2011;108:638–643. doi: 10.1073/pnas.1013914108. PubMed DOI PMC
Jindra M, Uhlirova M, Charles JP, Smykal V, Hill RJ. Genetic Evidence for Function of the bHLH-PAS Protein Gce/Met As a Juvenile Hormone Receptor. PLoS Genet. 2015;11:e1005394. doi: 10.1371/journal.pgen.1005394. PubMed DOI PMC
Lozano J, Kayukawa T, Shinoda T, Belles X. A Role for Taiman in Insect Metamorphosis. Plos Genetics. 2014;10:e1004769. doi: 10.1371/journal.pgen.1004769. PubMed DOI PMC
Belles X, Santos CG. The MEKRE93 (Methoprene tolerant-Kruppel homolog 1-E93) pathway in the regulation of insect metamorphosis, and the homology of the pupal stage. Insect biochemistry and molecular biology. 2014;52:60–68. doi: 10.1016/j.ibmb.2014.06.009. PubMed DOI
Minakuchi C, Zhou X, Riddiford LM. Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mechanisms of Development. 2008;125:91–105. doi: 10.1016/j.mod.2007.10.002. PubMed DOI PMC
Shin SW, Zou Z, Saha TT, Raikhel AS. bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:16576–16581. doi: 10.1073/pnas.1214209109. PubMed DOI PMC
Kayukawa T, et al. Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proceedings of the National Academy of Sciences of the United States of America. 2012;109:11729–11734. doi: 10.1073/pnas.1204951109. PubMed DOI PMC
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. Devlopmental Biology. 2009;325:341–350. doi: 10.1016/j.ydbio.2008.10.016. PubMed DOI
Lozano J, Belles X. Conserved repressive function of Kruppel homolog 1 on insect metamorphosis in hemimetabolous and holometabolous species. Scientific reports. 2011;1:163. doi: 10.1038/srep00163. PubMed DOI PMC
Zou Z, et al. Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:E2173–E2181. doi: 10.1073/pnas.1305293110. PubMed DOI PMC
Benevolenskaya EV, Frolov MV, Birchler JA. Kruppel homolog (Kr h) is a dosage-dependent modifier of gene expression in Drosophila. Genetical research. 2000;75:137–142. doi: 10.1017/S0016672399004437. PubMed DOI
Pecasse F, Beck Y, Ruiz C, Richards G. Kruppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis. Dev Biol. 2000;221:53–67. doi: 10.1006/dbio.2000.9687. PubMed DOI
Cui Y, Sui Y, Xu J, Zhu F, Palli SR. Juvenile hormone regulates Aedes aegypti Kruppel homolog 1 through a conserved E box motif. Insect biochemistry and molecular biology. 2014;52:23–32. doi: 10.1016/j.ibmb.2014.05.009. PubMed DOI PMC
Kayukawa T, Tateishi K, Shinoda T. Establishment of a versatile cell line for juvenile hormone signaling analysis in Tribolium castaneum. Scientific reports. 2013;3:1570. doi: 10.1038/srep01570. PubMed DOI PMC
Lyko F, et al. The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS biology. 2010;8:e1000506. doi: 10.1371/journal.pbio.1000506. PubMed DOI PMC
Shi YY, et al. Genomewide analysis indicates that queen larvae have lower methylation levels in the honey bee (Apis mellifera) Die Naturwissenschaften. 2013;100:193–197. doi: 10.1007/s00114-012-1004-3. PubMed DOI
Lockett GA, Helliwell P, Maleszka R. Involvement of DNA methylation in memory processing in the honey bee. Neuroreport. 2010;21:812–816. doi: 10.1097/WNR.0b013e32833ce5be. PubMed DOI
Weinert BT, et al. Proteome-wide mapping of the Drosophila acetylome demonstrates a high degree of conservation of lysine acetylation. Science signaling. 2011;4:ra48. doi: 10.1126/scisignal.2001902. PubMed DOI
Kellner WA, Ramos E, Van Bortle K, Takenaka N, Corces VG. Genome-wide phosphoacetylation of histone H3 at Drosophila enhancers and promoters. Genome research. 2012;22:1081–1088. doi: 10.1101/gr.136929.111. PubMed DOI PMC
Mukherjee K, Fischer R, Vilcinskas A. Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Frontiers in zoology. 2012;9:25. doi: 10.1186/1742-9994-9-25. PubMed DOI PMC
Kirilly D, et al. Intrinsic epigenetic factors cooperate with the steroid hormone ecdysone to govern dendrite pruning in Drosophila. Neuron. 2011;72:86–100. doi: 10.1016/j.neuron.2011.08.003. PubMed DOI
Bodai L, et al. Ecdysone induced gene expression is associated with acetylation of histone H3 lysine 23 in Drosophila melanogaster. PloS one. 2012;7:e40565. doi: 10.1371/journal.pone.0040565. PubMed DOI PMC
Tropberger P, et al. Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell. 2013;152:859–872. doi: 10.1016/j.cell.2013.01.032. PubMed DOI
Corrado P, et al. Acetylation of FOXO3a transcription factor in response to imatinib of chronic myeloid leukemia. Leukemia. 2009;23:405–406. doi: 10.1038/leu.2008.186. PubMed DOI
Fukuoka M, et al. Negative regulation of forkhead transcription factor AFX (Foxo4) by CBP-induced acetylation. International journal of molecular medicine. 2003;12:503–508. PubMed
Pramanik KC, Fofaria NM, Gupta P, Srivastava SK. CBP-mediated FOXO-1 acetylation inhibits pancreatic tumor growth by targeting SirT. Molecular cancer therapeutics. 2014;13:687–698. doi: 10.1158/1535-7163.MCT-13-0863. PubMed DOI PMC
Jing E, Gesta S, Kahn CR. SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell metabolism. 2007;6:105–114. doi: 10.1016/j.cmet.2007.07.003. PubMed DOI PMC
van der Heide LP, Smidt MP. Regulation of FoxO activity by CBP/p300-mediated acetylation. Trends in biochemical sciences. 2005;30:81–86. doi: 10.1016/j.tibs.2004.12.002. PubMed DOI
Sekaric P, Shamanin VA, Luo J, Androphy EJ. hAda3 regulates p14ARF-induced p53 acetylation and senescence. Oncogene. 2007;26:6261–6268. doi: 10.1038/sj.onc.1210462. PubMed DOI
Zhao Y, et al. Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1) Molecular and cellular biology. 2006;26:2782–2790. doi: 10.1128/MCB.26.7.2782-2790.2006. PubMed DOI PMC
Sykes SM, et al. Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Molecular cell. 2006;24:841–851. doi: 10.1016/j.molcel.2006.11.026. PubMed DOI PMC
Li AG, et al. Mechanistic insights into maintenance of high p53 acetylation by PTEN. Molecular cell. 2006;23:575–587. doi: 10.1016/j.molcel.2006.06.028. PubMed DOI
Goodman CL, et al. A cell line derived from the red flour beetle Tribolium castaneum (Coleoptera: Tenebrionidae). In Vitro Cellular & Developmental Biology. Animal. 2012;48:426–433. PubMed
Parthasarathy R, Sun Z, Bai H, Palli SR. Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle. Tribolium castaneum. Insect Biochemistry And Molecular Biology. 2010;40:405–414. doi: 10.1016/j.ibmb.2010.03.006. PubMed DOI PMC
Lambert JR, Nordeen SK. CBP recruitment and histone acetylation in differential gene induction by glucocorticoids and progestins. Molecular Endocrinology. 2003;17:1085–1094. doi: 10.1210/me.2001-0183. PubMed DOI
Mujtaba S, et al. Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Molecular Cell. 2004;13:251–263. doi: 10.1016/S1097-2765(03)00528-8. PubMed DOI
Yanagi Y, Masuhiro Y, Mori M, Yanagisawa J, Kato S. p300/CBP acts as a coactivator of the cone-rod homeobox transcription factor. Biochemical And Biophysical Research Communications. 2000;269:410–414. doi: 10.1006/bbrc.2000.2304. PubMed DOI
Aoyagi S, Archer TK. Dynamic histone acetylation/deacetylation with progesterone receptor-mediated transcription. Molecular Endocrinology. 2007;21:843–856. doi: 10.1210/me.2006-0244. PubMed DOI
Roy, A., George, S. & Palli, S. R. Multiple functions of CREB-binding protein during postembryonic development: Identification of target genes. BMC genomics 18, 996 (2017). PubMed PMC
Frankel S, Woods J, Ziafazeli T, Rogina B. RPD3 histone deacetylase and nutrition have distinct but interacting effects on Drosophila longevity. Aging. 2015;7:1112–1129. doi: 10.18632/aging.100856. PubMed DOI PMC