Nuclear receptor estrogen-related receptor modulates antimicrobial peptide expression for host innate immunity in Tribolium castaneum

Insect Biochemistry and Molecular Biology - Tập 148 - Trang 103816 - 2022
Byungyoon Choi1, Woo-Ram Park1, Yu-Ji Kim1, Seulgi Mun2, Su-Jin Park3, Jae-Ho Jeong4, Hueng-Sik Choi5, Don-Kyu Kim1
1Department of Integrative Food, Bioscience and Biotechnology, Chonnam National University, Gwangju, 61186, Republic of Korea
2Department of Applied Biology, Chonnam National University, Gwangju 61186, Republic of Korea
3Functional Biomaterial Research Center, Korea Research Institute of Bioscience and Biotechnology, Jeongeup, 56212, Republic of Korea
4Department of Microbiology, Chonnam National University Medical School, Gwangju, 61468, Republic of Korea
5School of Biological Sciences and Technology Chonnam National University Gwangju 61186 Republic of Korea

Tài liệu tham khảo

An, 2012, Insect neuropeptide bursicon homodimers induce innate immune and stress genes during molting by activating the NF-κB transcription factor Relish, PLoS One, 7, 10.1371/journal.pone.0034510 Arakane, 2009, Molecular and functional analyses of amino acid decarboxylases involved in cuticle tanning in Tribolium castaneum, J. Biol. Chem., 284, 16584, 10.1074/jbc.M901629200 Attia, 2020, Stored grain pest prevalence and insecticide resistance in Egyptian populations of the red flour beetle Tribolium castaneum (Herbst) and the rice weevil Sitophilus oryzae (L.), J. Stored Prod. Res., 87, 10.1016/j.jspr.2020.101611 Beeman, 1990, A gene for lindane + cyclodiene resistance in the red flour beetle (Coleoptera: tenebrionidae), J. Econ. Entomol., 83, 1745, 10.1093/jee/83.5.1745 Belvin, 1996, A conserved signaling pathway: the Drosophila toll-dorsal pathway, Annu. Rev. Cell Dev. Biol., 12, 393, 10.1146/annurev.cellbio.12.1.393 Bulet, 1999, Antimicrobial peptides in insects; structure and function, Dev. Comp. Immunol., 23, 329, 10.1016/S0145-305X(99)00015-4 Bulet, 2004, Anti-microbial peptides: from invertebrates to vertebrates, Immunol. Rev., 198, 169, 10.1111/j.0105-2896.2004.0124.x De Gregorio, 2002, The Toll and Imd pathways are the major regulators of the immune response in Drosophila, EMBO J., 21, 2568, 10.1093/emboj/21.11.2568 Dushay, 1996, Origins of immunity: Relish, a compound Rel-like gene in the antibacterial defense of Drosophila, Proc. Natl. Acad. Sci. U.S.A., 93, 10343, 10.1073/pnas.93.19.10343 Ganesan, 2011, NF-κB/Rel proteins and the humoral immune responses of Drosophila melanogaster, Curr. Top. Microbiol. Immunol., 349, 25 Gentleman, 2004, Bioconductor: open software development for computational biology and bioinformatics, Genome Biol., 5, R80, 10.1186/gb-2004-5-10-r80 Greschik, 2002, Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3, Mol. Cell, 9, 303, 10.1016/S1097-2765(02)00444-6 Hoffmann, 1992, Insect defensins: inducible antibacterial peptides, Immunol. Today, 13, 411, 10.1016/0167-5699(92)90092-L Huan, 2020, Antimicrobial peptides: classification, design, application and research progress in multiple fields, Front. Microbiol., 11, 10.3389/fmicb.2020.582779 Huang da, 2009, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat. Protoc., 4, 44, 10.1038/nprot.2008.211 Jang, 2020, Bacterial but not fungal challenge up-regulates the transcription of Coleoptericin genes in Tenebrio molitor, Entomol. Res., 50, 440, 10.1111/1748-5967.12465 Jang, 2020, In silico identification and expression analyses of Defensin genes in the mealworm beetle Tenebrio molitor, Entomol. Res., 50, 575, 10.1111/1748-5967.12468 Jo, 2019, Regulation of the expression of nine antimicrobial peptide genes by TmIMD confers resistance against Gram-negative bacteria, Sci. Rep., 9, 10.1038/s41598-019-46222-8 Keshavarz, 2020, Author Correction: TmRelish is required for regulating the antimicrobial responses to Escherichia coli and Staphylococcus aureus in Tenebrio molitor, Sci. Rep., 10, 7013, 10.1038/s41598-020-63872-1 Kim, 2019, Emerging role of the orphan nuclear receptor estrogen-related receptor gamma in liver metabolic diseases, Liver Research, 3, 99, 10.1016/j.livres.2019.03.001 Kim, 2014, Inverse agonist of estrogen-related receptor γ controls Salmonella typhimurium infection by modulating host iron homeostasis, Nat. Med., 20, 419, 10.1038/nm.3483 Kim, 2014, PKB/Akt phosphorylation of ERRγ contributes to insulin-mediated inhibition of hepatic gluconeogenesis, Diabetologia, 57, 2576, 10.1007/s00125-014-3366-x Kim, 2019, Estrogen-related receptor γ controls sterol regulatory element-binding protein-1c expression and alcoholic fatty liver, Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 1864 Kim, 2012, Orphan nuclear receptor estrogen-related receptor γ (ERRγ) is key regulator of hepatic gluconeogenesis, J. Biol. Chem., 287, 21628, 10.1074/jbc.M111.315168 Kim, 2022, Nuclear receptor HR96 up-regulates cytochrome P450 for insecticide detoxification in Tribolium castaneum, Pest Manag. Sci., 78, 230, 10.1002/ps.6626 Kim, 2014, Molting-associated suppression of symbiont population and up-regulation of antimicrobial activity in the midgut symbiotic organ of the Riptortus-Burkholderia symbiosis, Dev. Comp. Immunol., 43, 10, 10.1016/j.dci.2013.10.010 Kim, 2020, Estrogen-related receptor γ increases poly(I:C)-mediated type I IFN expression in mouse macrophages, J. Leukoc. Biol., 109, 865, 10.1002/JLB.2HI1219-762R King-Jones, 2006, The DHR96 nuclear receptor regulates xenobiotic responses in Drosophila, Cell Metabol., 4, 37, 10.1016/j.cmet.2006.06.006 Konopova, 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, 10.1073/pnas.0703719104 Kovalenko, 2019, The Drosophila nuclear receptors EcR and ERR jointly regulate the expression of genes involved in carbohydrate metabolism, Insect Biochem. Mol. Biol., 112, 10.1016/j.ibmb.2019.103184 Lemaitre, 2007, The host defense of Drosophila melanogaster, Annu. Rev. Immunol., 25, 697, 10.1146/annurev.immunol.25.022106.141615 Liu, 2017, Exploiting innate immunity for biological pest control, Adv. Insect Physiol, 52, 199, 10.1016/bs.aiip.2017.02.001 Long, 2020, Estrogen-related receptor participates in regulating glycolysis and influences embryonic development in silkworm Bombyx mori, Insect Mol. Biol., 29, 160, 10.1111/imb.12619 Lorenzen, 2002, Cloning and characterization of the Tribolium castaneum eye-color genes encoding tryptophan oxygenase and kynurenine 3-monooxygenase, Genetics, 160, 225, 10.1093/genetics/160.1.225 MartÍn, 2010, Functions of nuclear receptors in insect development, 31 Misra, 2017, ERRγ: a junior orphan with a senior role in metabolism, Trends Endocrinol. Metabol., 28, 261, 10.1016/j.tem.2016.12.005 Misra, 2017, Estrogen related receptor is required for the testicular development and for the normal sperm axoneme/mitochondrial derivatives in Drosophila males, Sci. Rep., 7, 10.1038/srep40372 Nemeth, 2006, Regulation of iron metabolism by hepcidin, Annu. Rev. Nutr., 26, 323, 10.1146/annurev.nutr.26.061505.111303 Olefsky, 2001, Nuclear receptor minireview series, J. Biol. Chem., 276, 36863, 10.1074/jbc.R100047200 Ostberg, 2003, A triple mutant of the Drosophila ERR confers ligand-induced suppression of activity, Biochemistry, 42, 6427, 10.1021/bi027279b Park, 2021, Aphid estrogen-related receptor controls glycolytic gene expression and fecundity, Insect Biochem. Mol. Biol., 130, 10.1016/j.ibmb.2021.103529 Pilátová, 2012, Burkholderia thailandensis is virulent in Drosophila melanogaster, PLoS One, 7, 10.1371/journal.pone.0049745 Razzaque, 2004, Estrogen receptor-related receptor gamma has an exceptionally broad specificity of DNA sequence recognition, Gene, 340, 275, 10.1016/j.gene.2004.07.010 Sagisaka, 2001, Purification, characterization and gene expression of a glycine and proline-rich antibacterial protein family from larvae of a beetle, Allomyrina dichotoma, Insect Mol. Biol., 10, 293, 10.1046/j.0962-1075.2001.00261.x Sanyal, 2002, Differential regulation of the orphan nuclear receptor small heterodimer partner (SHP) gene promoter by orphan nuclear receptor ERR isoforms, J. Biol. Chem., 277, 1739, 10.1074/jbc.M106140200 Senger, 2004, Immunity regulatory DNAs share common organizational features in Drosophila, Mol. Cell, 13, 19, 10.1016/S1097-2765(03)00500-8 Sheehan, 2018, Innate humoral immune defences in mammals and insects: the same, with differences, Virulence, 9, 1625, 10.1080/21505594.2018.1526531 Shrestha, 2010, Activation of immune-associated phospholipase A2 is functionally linked to Toll/Imd signal pathways in the red flour beetle, Tribolium castaneum, Dev. Comp. Immunol., 34, 530, 10.1016/j.dci.2009.12.013 Shukla, 2012, Doublesex target genes in the red flour beetle, Tribolium castaneum. Sci. Rep., 2, 948, 10.1038/srep00948 Sonoda, 2007, Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense, Genes Dev., 21, 1909, 10.1101/gad.1553007 Sun, 2016, Ecdysone titer determined by 3DE-3β-reductase enhances the immune response in the silkworm, J. Immunol., 196, 1646, 10.4049/jimmunol.1500158 Tan, 2008, Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum, Insect Biochem. Mol. Biol., 38, 430, 10.1016/j.ibmb.2007.09.012 Tennessen, 2011, The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth, Cell Metabol., 13, 139, 10.1016/j.cmet.2011.01.005 Tian, 2010, Genome-wide regulation of innate immunity by juvenile hormone and 20-hydroxyecdysone in the Bombyx fat body, BMC Genom., 11, 549, 10.1186/1471-2164-11-549 Trapnell, 2009, TopHat: discovering splice junctions with RNA-Seq, Bioinformatics, 25, 1105, 10.1093/bioinformatics/btp120 Tremblay, 2007, The NR3B subgroup: an ovERRview, Nucl. Recept. Signal., 5, e009, 10.1621/nrs.05009 Valanne, 2011, The Drosophila Toll signaling pathway, J. Immunol., 186, 649, 10.4049/jimmunol.1002302 Verma, 2012, Immune response and anti-microbial peptides expression in Malpighian tubules of Drosophila melanogaster is under developmental regulation, PLoS One, 7, 10.1371/annotation/4b02305d-dcb8-40db-8f1f-1f7f0da51544 Verma, 2015, Early gene Broad complex plays a key role in regulating the immune response triggered by ecdysone in the Malpighian tubules of Drosophila melanogaster, Mol. Immunol., 66, 325, 10.1016/j.molimm.2015.03.249 Vilcinskas, 2013, Evolutionary plasticity of insect immunity, J. Insect Physiol., 59, 123, 10.1016/j.jinsphys.2012.08.018 Wang, 2017, Hormone and receptor interplay in the regulation of mosquito lipid metabolism, Proc. Natl. Acad. Sci. U.S.A., 114, E2709 Wu, 2021, The response of the estrogen-related receptor to 20-hydroxyecdysone in Bombyx mori: insight into the function of estrogen-related receptor in insect 20-hydroxyecdysone signaling pathway, Front. Physiol., 12 Yi, 2014, Insect antimicrobial peptides and their applications, Appl. Microbiol. Biotechnol., 98, 5807, 10.1007/s00253-014-5792-6 Yokoi, 2012, Antimicrobial peptide gene induction, involvement of Toll and IMD pathways and defense against bacteria in the red flour beetle, Tribolium castaneum, Results Immunol., 2, 72, 10.1016/j.rinim.2012.03.002 Zanchi, 2017, Evolution of defence cocktails: antimicrobial peptide combinations reduce mortality and persistent infection, Mol. Ecol., 26, 5334, 10.1111/mec.14267 Zhang, 2018, Morphological changes in different caste adult ant specificities of Polyrhachis vicina Roger (Hymenoptera, Formicidae) caused in estrogen-related receptor, Gen. Comp. Endocrinol., 266, 29, 10.1016/j.ygcen.2018.04.002 Zou, 2007, Comparative genomic analysis of the Tribolium immune system, Genome Biol., 8, R177, 10.1186/gb-2007-8-8-r177