• This record comes from PubMed

Multiple functions of CREB-binding protein during postembryonic development: identification of target genes

. 2017 Dec 29 ; 18 (1) : 996. [epub] 20171229

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
GM070559-11 NIGMS NIH HHS - United States
2351177000 Cooperative State Research, Education, and Extension Service - International

Links

PubMed 29284404
PubMed Central PMC5747157
DOI 10.1186/s12864-017-4373-3
PII: 10.1186/s12864-017-4373-3
Knihovny.cz E-resources

BACKGROUND: Juvenile hormones (JH) and ecdysteroids control postembryonic development in insects. They serve as valuable targets for pest management. Hence, understanding the molecular mechanisms of their action is of crucial importance. CREB-binding protein (CBP) is a universal transcriptional co-regulator. It controls the expression of several genes including those from hormone signaling pathways through co-activation of many transcription factors. However, the role of CBP during postembryonic development in insects is not well understood. Therefore, we have studied the role of CBP in postembryonic development in Tribolium, a model coleopteran insect. RESULTS: CBP is ubiquitously expressed in the red flour beetle, Tribolium castaneum. RNA interference (RNAi) mediated knockdown of CBP resulted in a decrease in JH induction of Kr-h1 gene expression in Tribolium larvae and led to a block in their development. Moreover, the injection of CBP double-stranded RNA (dsRNA) showed lethal phenotypes within 8 days of injection. RNA-seq and subsequent differential gene expression analysis identified CBP target genes in Tribolium. Knockdown of CBP caused a decrease in the expression of 1306 genes coding for transcription factors and other proteins associated with growth and development. Depletion of CBP impaired the expression of several JH response genes (e.g., Kr-h1, Hairy, early trypsin) and ecdysone response genes (EcR, E74, E75, and broad complex). Further, GO enrichment analyses of the downregulated genes showed enrichment in different functions including developmental processes, pigmentation, anatomical structure development, regulation of biological and cellular processes, etc. CONCLUSION: These data suggest diverse but crucial roles for CBP during postembryonic development in the coleopteran model insect, Tribolium. It can serve as a target for RNAi mediated pest management of this stored product pest.

Erratum In

PubMed

See more in PubMed

Nijhout HF, Callier V. Developmental mechanisms of body size and wing-body scaling in insects. Annu Rev Entomol. 2015;60:141–156. doi: 10.1146/annurev-ento-010814-020841. PubMed DOI

Hall BL, Thummel CS. The RXR homolog ultraspiracle is an essential component of the Drosophila ecdysone receptor. Development. 1998;125(23):4709–4717. PubMed

Huet F, Ruiz C, Richards G. Puffs and PCR: the in vivo dynamics of early gene expression during ecdysone responses in Drosophila. Development. 1993;118(2):613–627. PubMed

Yao T-P, Forman BM, Jiang Z, Cherbas L, Chen J-D, McKeown M, Cherbas P, Evans RM. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature. 1993;366(6454):476–479. doi: 10.1038/366476a0. 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

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, Tang HY, Makohon-Moore SC, Salhadar S, Gokhale RH, Warner RD, Koyama T, Riddiford LM, Shingleton AW. Juvenile hormone regulates body size and perturbs insulin signaling in Drosophila. Proc Natl Acad Sci U S A. 2014;111(19):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. J Biol Chem. 2011;286(49):41924–41936. doi: 10.1074/jbc.M111.269845. PubMed DOI PMC

Abdou M, Peng C, Huang J, Zyaan O, Wang S, Li S, Wang J. Wnt signaling cross-talks with JH signaling by suppressing met and gce expression. PLoS One. 2011;6(11):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. J Biol Chem. 2011;286(10):8437–8447. doi: 10.1074/jbc.M110.191684. PubMed DOI PMC

Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M. Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci U S A. 2011;108(52):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. Proc Natl Acad Sci U S A. 2011;108(2):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(7):e1005394. doi: 10.1371/journal.pgen.1005394. PubMed DOI PMC

Lozano J, Kayukawa T, Shinoda T, Belles XA. Role for Taiman in Insect Metamorphosis. PLoS Genet. 2014;10(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 Biochem Mol Biol. 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. Mech Dev. 2008;125(1–2):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. Proc Natl Acad Sci U S A. 2012;109(41):16576–16581. doi: 10.1073/pnas.1214209109. PubMed DOI PMC

Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M, Mita K, Imanishi S, Kiuchi M, Ishikawa Y, et al. Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci U S A. 2012;109(29):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. Dev Biol. 2009;325(2):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. Sci Rep. 2011;1:163. doi: 10.1038/srep00163. PubMed DOI PMC

Zou Z, Saha TT, Roy S, Shin SW, Backman TWH, Girke T, White KP, Raikhel AS. Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proc Natl Acad Sci U S A. 2013;110(24):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. Genet Res. 2000;75(2):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(1):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 Biochem Mol Biol. 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. Sci Rep. 2013;3:1570. PubMed PMC

Vo N, Goodman RH. CREB-binding protein and p300 in transcriptional regulation. J Biol Chem. 2001;276(17):13505–13508. doi: 10.1074/jbc.R000025200. 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

Janknecht R, Wells NJ, Hunter T. TGF-β-stimulated cooperation of Smad proteins with the coactivators CBP/p300. Genes Dev. 1998;12(14):2114–2119. doi: 10.1101/gad.12.14.2114. PubMed DOI PMC

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

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. doi: 10.1038/386735a0. PubMed DOI

Heldin C-H, Moustakas A. Role of Smads in TGFβ signaling. Cell Tissue Res. 2012;347(1):21–36. doi: 10.1007/s00441-011-1190-x. PubMed DOI

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

Bodai L, Zsindely N, Gaspar R, Kristo I, Komonyi O, Boros IM. Ecdysone induced gene expression is associated with acetylation of histone H3 lysine 23 in Drosophila melanogaster. PLoS One. 2012;7(7):e40565. doi: 10.1371/journal.pone.0040565. PubMed DOI PMC

Weinert BT, Wagner SA, Horn H, Henriksen P, Liu WR, Olsen JV, Jensen LJ, Choudhary C. Proteome-wide mapping of the Drosophila acetylome demonstrates a high degree of conservation of lysine acetylation. Sci Signal. 2011;4(183):ra48. doi: 10.1126/scisignal.2001902. PubMed DOI

Fernandez-Nicolas A, Belles X. CREB-binding protein contributes to the regulation of endocrine and developmental pathways in insect hemimetabolan pre-metamorphosis. Biochim Biophys Acta. 2016;1860(3):508–515. doi: 10.1016/j.bbagen.2015.12.008. PubMed DOI

Parthasarathy R, Sun Z, Bai H, Palli SR. Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol. 2010;40(5):405–414. doi: 10.1016/j.ibmb.2010.03.006. PubMed DOI PMC

Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature. 1993;365(6449):855–859. doi: 10.1038/365855a0. PubMed DOI

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

Waltzer L, Bienz M. A function of CBP as a transcriptional co-activator during Dpp signalling. EMBO J. 1999;18(6):1630–1641. doi: 10.1093/emboj/18.6.1630. PubMed DOI PMC

Holmqvist P-H, Boija A, Philip P, Crona F, Stenberg P, Mannervik M. Preferential genome targeting of the CBP co-activator by Rel and Smad proteins in early Drosophila melanogaster embryos. PLoS Genet. 2012;8(6):e1002769. doi: 10.1371/journal.pgen.1002769. PubMed DOI PMC

Peterson AJ, O’Connor MB. Strategies for exploring TGF-β signaling in Drosophila. Methods. 2014;68(1):183–193. doi: 10.1016/j.ymeth.2014.03.016. PubMed DOI PMC

Tropberger P, Pott S, Keller C, Kamieniarz-Gdula K, Caron M, Richter F, Li G, Mittler G, Liu ET, Buhler M, et al. Regulation of transcription through acetylation of H3K122 on the lateral surface of the histone octamer. Cell. 2013;152(4):859–872. doi: 10.1016/j.cell.2013.01.032. PubMed DOI

Zeng J, Yi SV. DNA methylation and genome evolution in honeybee: gene length, expression, functional enrichment covary with the evolutionary signature of DNA methylation. Genome Biol Evol. 2010;2:770–780. doi: 10.1093/gbe/evq060. PubMed DOI PMC

Zheng WW, Dong XM, Yin RH, Xu FF, Ning HM, Zhang MJ, Xu CW, Yang Y, Ding YL, Wang ZD, et al. EDAG positively regulates erythroid differentiation and modifies GATA1 acetylation through recruiting p300. Stem Cells. 2014;32(8):2278–2289. doi: 10.1002/stem.1723. PubMed DOI

Varghese J, Cohen SM. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in drosophila. Genes Dev. 2007;21(18):2277–2282. doi: 10.1101/gad.439807. PubMed DOI PMC

Parthasarathy R, Palli SR. Molecular analysis of juvenile hormone analogaction in controlling the metamorphosis of the redflour beetle, Tribolium castaneum. Arch Insect Biochem. 2009;70:57–70. doi: 10.1002/arch.20288. 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

Beckstead RB, Lam G, Thummel CS. The genomic response to 20-hydroxyecdysone at the onset of Drosophila metamorphosis. Genome Biol. 2005;6(12):R99. doi: 10.1186/gb-2005-6-12-r99. PubMed DOI PMC

Kang P, Chang K, Liu Y, Bouska M, Birnbaum A, Karashchuk G, Thakore R, Zheng W, Post S, Brent CS, Li S, Tatar M, Bai H. Drosophila Kruppel homolog 1 represses lipolysis through interaction with dFOXO. Sci Rep. 2017;7(1):16369. PubMed PMC

Schuh R, Aicher W, Gaul U, Côte S, Preiss A, Maier D, Seifert E, Nauber U, Schröder C, Kemler R. A conserved family of nuclear proteins containing structural elements of the finger protein encoded by Krüppel, a drosophila segmentation gene. Cell. 1986;47(6):1025–1032. doi: 10.1016/0092-8674(86)90817-2. PubMed DOI

Bayer CA, Holley B, Fristrom JW. A switch inBroad-ComplexZinc-finger isoform expression is regulated posttranscriptionally during the metamorphosis of Drosophila imaginal discs. Dev Biol. 1996;177(1):1–14. doi: 10.1006/dbio.1996.0140. PubMed DOI

Karim FD, Guild GM, Thummel CS. The Drosophila broad-complex plays a key role in controlling ecdysone-regulated gene expression at the onset of metamorphosis. Development. 1993;118(3):977–988. PubMed

Zhou B, Riddiford LM. Hormonal regulation and patterning of the broad-complex in the epidermis and wing discs of the tobacco hornworm, Manduca sexta. Dev Biol. 2001;231(1):125–137. doi: 10.1006/dbio.2000.0143. PubMed DOI

Konopova B, Jindra M. Broad-complex acts downstream of met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development. 2008;135(3):559–568. doi: 10.1242/dev.016097. PubMed DOI

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

Suzuki Y, Truman JW, Riddiford LM. The role of broad in the development of Tribolium castaneum: implications for the evolution of the holometabolous insect pupa. Development. 2008;135(3):569–577. doi: 10.1242/dev.015263. PubMed DOI

Thummel CS. The Drosophila E74 promoter contains essential sequences downstream from the start site of transcription. Genes Dev. 1989;3(6):782–792. doi: 10.1101/gad.3.6.782. PubMed DOI

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

Noriega F, Shah D, Wells M. Juvenile hormone controls early trypsin gene transcription in the midgut ofAedes aegypti. Insect Mol Biol. 1997;6(1):63–66. doi: 10.1046/j.1365-2583.1997.00154.x. PubMed DOI

Bitra K, Palli SR. The members of bHLH transcription factor superfamily are required for female reproduction in the red flour beetle, Tribolium castaneum. J Insect Physiol. 2010;56(10):1481–1489. doi: 10.1016/j.jinsphys.2010.03.005. PubMed DOI PMC

Faiola F, Liu X, Lo S, Pan S, Zhang K, Lymar E, Farina A, Martinez E. Dual regulation of c-Myc by p300 via acetylation-dependent control of Myc protein turnover and coactivation of Myc-induced transcription. Mol Cell Biol. 2005;25(23):10220–10234. doi: 10.1128/MCB.25.23.10220-10234.2005. PubMed DOI PMC

King-Jones K, Thummel CS. Nuclear receptors--a perspective from Drosophila. Nat Rev Genet. 2005;6(4):311. doi: 10.1038/nrg1581. PubMed DOI

Kino T, Nordeen SK, Chrousos GP. Conditional modulation of glucocorticoid receptor activities by CREB-binding protein (CBP) and p300. J Steroid Biochem Mol Biol. 1999;70(1):15–25. doi: 10.1016/S0960-0760(99)00100-4. PubMed DOI

Gizard F, Lavallée B, DeWitte F, Hum DW. A novel zinc finger protein TReP-132 interacts with CBP/p300 to regulate human CYP11A1 gene expression. J Biol Chem. 2001;276(36):33881–33892. doi: 10.1074/jbc.M100113200. PubMed DOI

Monté D, DeWitte F, Hum DW. Regulation of the human P450scc gene by steroidogenic factor 1 is mediated by CBP/p300. J Biol Chem. 1998;273(8):4585–4591. doi: 10.1074/jbc.273.8.4585. PubMed DOI

Namiki T, Niwa R, Sakudoh T, Shirai K-I, Takeuchi H, Kataoka H. Cytochrome P450 CYP307A1/spook: a regulator for ecdysone synthesis in insects. Biochem Bioph Res Co. 2005;337(1):367–374. doi: 10.1016/j.bbrc.2005.09.043. 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

Thummel CS, Burtis KC, Hogness DS. Spatial and temporal patterns of E74 transcription during Drosophila development. Cell. 1990;61(1):101–111. doi: 10.1016/0092-8674(90)90218-4. PubMed DOI

Segraves WA, Hogness DS. The E75 ecdysone-inducible gene responsible for the 75B early puff in drosophila encodes two new members of the steroid receptor superfamily. Genes Dev. 1990;4(2):204–219. doi: 10.1101/gad.4.2.204. PubMed DOI

Dubrovsky EB, Dubrovskaya VA, Berger EM. Hormonal regulation and functional role of Drosophila E75A orphan nuclear receptor in the juvenile hormone signaling pathway. Dev Biol. 2004;268(2):258–270. doi: 10.1016/j.ydbio.2004.01.009. PubMed DOI

Cáceres L, Necakov AS, Schwartz C, Kimber S, Roberts IJ, Krause HM. Nitric oxide coordinates metabolism, growth, and development via the nuclear receptor E75. Genes Dev. 2011;25(14):1476–1485. doi: 10.1101/gad.2064111. PubMed DOI PMC

Dubrovsky EB, Dubrovskaya VA, Bernardo T, Otte V, DiFilippo R, Bryan H. The drosophila FTZ-F1 nuclear receptor mediates juvenile hormone activation of E75A gene expression through an intracellular pathway. J Biol Chem. 2011;286(38):33689–33700. doi: 10.1074/jbc.M111.273458. PubMed DOI PMC

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

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

Kim J, Sebring A, Esch JJ, Kraus ME, Vorwerk K, Magee J, Carroll SB. Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature. 1996;382(6587):133–138. doi: 10.1038/382133a0. PubMed DOI

Brummel T, Abdollah S, Haerry TE, Shimell MJ, Merriam J, Raftery L, Wrana JL, O’Connor MB. The drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev. 1999;13(1):98–111. doi: 10.1101/gad.13.1.98. PubMed DOI PMC

Gibbens YY, Warren JT, Gilbert LI, O’Connor MB. Neuroendocrine regulation of drosophila metamorphosis requires TGFβ/Activin signaling. Development. 2011;138(13):2693–2703. doi: 10.1242/dev.063412. PubMed DOI PMC

Pascual N, Maestro JL, Chiva C, Andreu D, Bellés X. Identification of a tachykinin-related peptide with orexigenic properties in the German cockroach. Peptides. 2008;29(3):386–392. doi: 10.1016/j.peptides.2007.11.010. PubMed DOI

Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S. Functional specialization among insect chitinase family genes revealed by RNA interference. Proc Natl Acad Sci U S A. 2008;105(18):6650–6655. doi: 10.1073/pnas.0800739105. PubMed DOI PMC

Zhou X, Tarver MR, Scharf ME. Hexamerin-based regulation of juvenile hormone-dependent gene expression underlies phenotypic plasticity in a social insect. Development. 2007;134(3):601–610. doi: 10.1242/dev.02755. PubMed DOI

Zdybicka-Barabas A, Cytryńska M. Apolipophorins and insect immune response. ISJ. 2013;10:58–68.

Patnaik BB, Patnaik HH, Park KB, Jo YH, Lee YS, Han YS. Silencing of apolipophorin-III causes abnormal adult morphological phenotype and susceptibility to Listeria monocytogenes infection in Tenebrio molitor. Entomol Res. 2015;45(2):116–121. doi: 10.1111/1748-5967.12099. DOI

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

Bond ND, Nelliot A, Bernardo MK, Ayerh MA, Gorski KA, Hoshizaki DK, Woodard CT. ssFTZ-F1 and matrix metalloproteinase 2 are required for fat-body remodeling in drosophila. Dev Biol. 2011;360(2):286–296. doi: 10.1016/j.ydbio.2011.09.015. PubMed DOI

Huang Y, Dennehey B, Shi X. Histone lysine methylation, demethylation, and hormonal gene regulation. In: Mandal SS, editor. Gene regulation, epigenetics and hormone signaling: Weiheim: Wiley-VCH Verlag GmbH & Co. KGaA; 2017. p. 59–100.

Haliscak JP, Beeman RW. Status of malathion resistance in five genera of beetles infesting farm-stored corn, wheat, and oats in the United States. J Econ Entomol. 1983;76(4):717–722. doi: 10.1093/jee/76.4.717. DOI

Parthasarathy R, Tan A, Sun Z, Chen Z, Rankin M, Palli S. 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

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

Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L. WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 2006;34(suppl 2):W293–W297. doi: 10.1093/nar/gkl031. PubMed DOI PMC

Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014;42(D1):D199–D205. doi: 10.1093/nar/gkt1076. PubMed DOI PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...