Varroa destructor parasitism has a greater effect on proteome changes than the deformed wing virus and activates TGF-β signaling pathways
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31253851
PubMed Central
PMC6599063
DOI
10.1038/s41598-019-45764-1
PII: 10.1038/s41598-019-45764-1
Knihovny.cz E-zdroje
- MeSH
- biologické markery MeSH
- biologické modely MeSH
- histony metabolismus MeSH
- Janus kinasy metabolismus MeSH
- protein-serin-threoninkinasy metabolismus MeSH
- proteiny Wnt metabolismus MeSH
- proteom * MeSH
- proteomika * MeSH
- reaktivní formy kyslíku metabolismus MeSH
- RNA-viry * MeSH
- signální transdukce MeSH
- symbióza * MeSH
- transformující růstový faktor beta * MeSH
- transkripční faktory STAT metabolismus MeSH
- Varroidae * MeSH
- včely metabolismus parazitologie virologie MeSH
- výpočetní biologie metody MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- biologické markery MeSH
- histony MeSH
- Janus kinasy MeSH
- protein-serin-threoninkinasy MeSH
- proteiny Wnt MeSH
- proteom * MeSH
- reaktivní formy kyslíku MeSH
- transformující růstový faktor beta * MeSH
- transkripční faktory STAT MeSH
Honeybee workers undergo metamorphosis in capped cells for approximately 13 days before adult emergence. During the same period, Varroa mites prick the defenseless host many times. We sought to identify proteome differences between emerging Varroa-parasitized and parasite-free honeybees showing the presence or absence of clinical signs of deformed wing virus (DWV) in the capped cells. A label-free proteomic analysis utilizing nanoLC coupled with an Orbitrap Fusion Tribrid mass spectrometer provided a quantitative comparison of 2316 protein hits. Redundancy analysis (RDA) showed that the combination of Varroa parasitism and DWV clinical signs caused proteome changes that occurred in the same direction as those of Varroa alone and were approximately two-fold higher. Furthermore, proteome changes associated with DWV signs alone were positioned above Varroa in the RDA. Multiple markers indicate that Varroa activates TGF-β-induced pathways to suppress wound healing and the immune response and that the collective action of stressors intensifies these effects. Furthermore, we indicate JAK/STAT hyperactivation, p53-BCL-6 feedback loop disruption, Wnt pathway activation, Wnt/Hippo crosstalk disruption, and NF-κB and JAK/STAT signaling conflict in the Varroa-honeybee-DWV interaction. These results illustrate the higher effect of Varroa than of DWV at the time of emergence. Markers for future research are provided.
Zobrazit více v PubMed
Allen MF, Ball BV, White RF, Antoniw JF. The detection of acute paralysis virus in Varroa jacobsoni by the use of a simple indirect ELISA. J. Apic. Res. 1986;25:100–105. doi: 10.1080/00218839.1986.11100700. DOI
Martin SJ, et al. Global honey bee viral landscape altered by a parasitic mite. Science. 2012;336:1304–1306. doi: 10.1126/science.1220941. PubMed DOI
Wilfert L, et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science. 2016;351:594–597. doi: 10.1126/science.aac9976. PubMed DOI
Ryabov EV, et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLOS Pathog. 2014;10:e1004230. doi: 10.1371/journal.ppat.1004230. PubMed DOI PMC
Erban T, et al. In-depth proteomic analysis of Varroa destructor: detection of DWV-complex, ABPV, VdMLV and honeybee proteins in the mite. Sci. Rep. 2015;5:13907. doi: 10.1038/srep13907. PubMed DOI PMC
Yang X, Cox-Foster DL. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. USA. 2005;102:7470–7475. doi: 10.1073/pnas.0501860102. PubMed DOI PMC
Shen M, Yang X, Cox-Foster D, Cui L. The role of Varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology. 2005;342:141–149. doi: 10.1016/j.virol.2005.07.012. PubMed DOI
Nazzi F, et al. Synergistic parasite–pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLOS Pathog. 2012;8:e1002735. doi: 10.1371/journal.ppat.1002735. PubMed DOI PMC
Di Prisco G, et al. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. Proc. Natl. Acad. Sci. USA. 2016;113:3203–3208. doi: 10.1073/pnas.1523515113. PubMed DOI PMC
Kuster RD, Boncristiani HF, Rueppell O. Immunogene and viral transcript dynamics during parasitic Varroa destructor mite infection of developing honey bee (Apis mellifera) pupae. J. Exp. Biol. 2014;217:1710–1718. doi: 10.1242/jeb.097766. PubMed DOI
Navajas M, et al. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics. 2008;9:301. doi: 10.1186/1471-2164-9-301. PubMed DOI PMC
Johnson RM, Evans JD, Robinson GE, Berenbaum MR. Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera) Proc. Natl. Acad. Sci. USA. 2009;106:14790–14795. doi: 10.1073/pnas.0906970106. PubMed DOI PMC
Doublet V, et al. Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens. BMC Genomics. 2017;18:207. doi: 10.1186/s12864-017-3597-6. PubMed DOI PMC
Winston, M. L. The biology of the honey bee, updated edn. (Harvard University Press, 1991).
Erban T, Petrova D, Harant K, Jedelsky PL, Titera D. Two-dimensional gel proteome analysis of honeybee, Apis mellifera, worker red-eye pupa hemolymph. Apidologie. 2014;45:53–72. doi: 10.1007/s13592-013-0230-9. DOI
Duay P, De Jong D, Engels W. Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie. 2003;34:61–65. doi: 10.1051/apido:2002052. DOI
Erban T, Harant K, Kamler M, Markovic M, Titera D. Detailed proteome mapping of newly emerged honeybee worker hemolymph and comparison with the red-eye pupal stage. Apidologie. 2016;47:805–817. doi: 10.1007/s13592-016-0437-7. DOI
Surlis C, Carolan JC, Coffey M, Kavanagh K. Quantitative proteomics reveals divergent responses in Apis mellifera worker and drone pupae to parasitization by Varroa destructor. J. Insect Physiol. 2018;107:291–301. doi: 10.1016/j.jinsphys.2017.12.004. PubMed DOI
de la Fuente J, et al. Tick–host–pathogen interactions: conflict and cooperation. PLOS Pathog. 2016;12:e1005488. doi: 10.1371/journal.ppat.1005488. PubMed DOI PMC
Hochberg Y. A sharper Bonferroni procedure for multiple tests of significance. Biometrika. 1988;75:800–802. doi: 10.1093/biomet/75.4.800. DOI
Brutscher LM, Daughenbaugh KF, Flenniken ML. Antiviral defense mechanisms in honey bees. Curr. Opin. Insect Sci. 2015;10:71–82. doi: 10.1016/j.cois.2015.04.016. PubMed DOI PMC
Brutscher LM, Daughenbaugh KF, Flenniken ML. Virus and dsRNA-triggered transcriptional responses reveal key components of honey bee antiviral defense. Sci. Rep. 2017;7:6448. doi: 10.1038/s41598-017-06623-z. PubMed DOI PMC
Chen YP, et al. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLOS Pathog. 2014;10:e1004261. doi: 10.1371/journal.ppat.1004261. PubMed DOI PMC
Richards EH, Jones B, Bowman A. Salivary secretions from the honeybee mite, Varroa destructor: effects on insect haemocytes and preliminary biochemical characterization. Parasitology. 2011;138:602–608. doi: 10.1017/S0031182011000072. PubMed DOI
Kazimirova M, Stibraniova I. Tick salivary compounds: their role in modulation of host defences and pathogen transmission. Front. Cell. Infect. Microbiol. 2013;3:43. doi: 10.3389/fcimb.2013.00043. PubMed DOI PMC
Xie L, et al. Transforming growth factor beta-regulated gene expression in a mouse mammary gland epithelial cell line. Breast Cancer Res. 2003;5:R187–R198. doi: 10.1186/bcr640. PubMed DOI PMC
Xu P, et al. Innate antiviral host defense attenuates TGF-beta function through IRF3-mediated suppression of Smad signaling. Mol. Cell. 2014;56:723–737. doi: 10.1016/j.molcel.2014.11.027. PubMed DOI PMC
Li N, et al. Influenza viral neuraminidase primes bacterial coinfection through TGF-beta–mediated expression of host cell receptors. Proc. Natl. Acad. Sci. USA. 2015;112:238–243. doi: 10.1073/pnas.1414422112. PubMed DOI PMC
Shukla A, et al. TGF-beta signalling is regulated by Schnurri-2-dependent nuclear translocation of CLIC4 and consequent stabilization of phospho-Smad2 and 3. Nat. Cell Biol. 2009;11:777–784. doi: 10.1038/ncb1885. PubMed DOI PMC
Shih S-C, Claffey KP. Role of AP-1 and HIF-1 transcription factors in TGF-beta activation of VEGF expression. Growth Factors. 2001;19:19–34. doi: 10.3109/08977190109001073. PubMed DOI
Kozubik A, Hofmanova J, Dusek L. Eicosanoid inhibitors enhance synergistically the effect of transforming growth factor beta1 on CCL 64 cell proliferation. Eur. J. Pharmacol. 1996;316:349–357. doi: 10.1016/S0014-2999(96)00691-7. PubMed DOI
Dennis EA, Norris PC. Eicosanoid storm in infection and inflammation. Nat. Rev. Immunol. 2015;15:511–523. doi: 10.1038/nri3859. PubMed DOI PMC
Tai H-H, Cho H, Tong M, Ding Y. NAD -linked 15-hydroxyprostaglandin dehydrogenase: structure and biological functions. Curr. Pharm. Des. 2006;12:955–962. doi: 10.2174/138161206776055958. PubMed DOI
Dodge GR, Kovalszky I, Hassell JR, Iozzo RV. Transforming growth factor beta alters the expression of heparan sulfate proteoglycan in human colon carcinoma cells. J. Biol. Chem. 1990;265:18023–18029. PubMed
Yung S, Chen X-R, Tsang RCW, Zhang Q, Chan TM. Reduction of perlecan synthesis and induction of TGF-beta1 in human peritoneal mesothelial cells due to high dialysate glucose concentration: implication in peritoneal dialysis. J. Am. Soc. Nephrol. 2004;15:1178–1188. doi: 10.1097/01.ASN.0000122826.40921.D7. PubMed DOI
Nakamura R, Nakamura F, Fukunaga S. Perlecan diversely regulates the migration and proliferation of distinct cell types in vitro. Cells Tissues Organs. 2015;200:374–393. doi: 10.1159/000440950. PubMed DOI
Nugent MA, Nugent HM, Iozzo RV, Sanchack K, Edelman ER. Perlecan is required to inhibit thrombosis after deep vascular injury and contributes to endothelial cell-mediated inhibition of intimal hyperplasia. Proc. Natl. Acad. Sci. USA. 2000;97:6722–6727. doi: 10.1073/pnas.97.12.6722. PubMed DOI PMC
Zhou Z, et al. Impaired angiogenesis, delayed wound healing and retarded tumor growth in perlecan heparan sulfate-deficient mice. Cancer Res. 2004;64:4699–4702. doi: 10.1158/0008-5472.CAN-04-0810. PubMed DOI
Finnson KW, et al. Identification of CD109 as part of the TGF-beta receptor system in human keratinocytes. FASEB J. 2006;20:1525–1527. doi: 10.1096/fj.05-5229fje. PubMed DOI
Zhang J-M, et al. CD109 attenuates TGF-beta1 signaling and enhances EGF signaling in SK-MG-1 human glioblastoma cells. Biochem. Biophys. Res. Commun. 2015;459:252–258. doi: 10.1016/j.bbrc.2015.02.093. PubMed DOI
Han JM, et al. AIMP2/p38, the scaffold for the multi-tRNA synthetase complex, responds to genotoxic stresses via p53. Proc. Natl. Acad. Sci. USA. 2008;105:11206–11211. doi: 10.1073/pnas.0800297105. PubMed DOI PMC
Kim MJ, et al. Downregulation of FUSE-binding protein and c-myc by tRNA synthetase cofactor p38 is required for lung cell differentiation. Nat. Genet. 2003;34:330–336. doi: 10.1038/ng1182. PubMed DOI
Cairns CA, White RJ. p53 is a general repressor of RNA polymerase III transcription. EMBO J. 1998;17:3112–3123. doi: 10.1093/emboj/17.11.3112. PubMed DOI PMC
Chiu Y-H, MacMillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell. 2009;138:576–591. doi: 10.1016/j.cell.2009.06.015. PubMed DOI PMC
Fleming SB. Viral inhibition of the IFN-induced JAK/STAT signalling pathway: development of live attenuated vaccines by mutation of viral-encoded IFNantagonists. Vaccines. 2016;4:23. doi: 10.3390/vaccines4030023. PubMed DOI PMC
Sayed M, Pelech S, Wong C, Marotta A, Salh B. Protein kinase CK2 is involved in G2 arrest and apoptosis following spindle damage in epithelial cells. Oncogene. 2001;20:6994–7005. doi: 10.1038/sj.onc.1204894. PubMed DOI
Gibson S, Qin H, Liu Y, Rowse A, Benveniste ET. CK2alpha protein levels and CK2 kinase activity are induced upon CD4+ T cell activation and are essential for Th17 cell differentiation. J. Immunol. 2014;192(1 Suppl.):64.10–LYM3P.736.
Bek S, Kemler R. Protein kinase CKII regulates the interaction of beta-catenin with alpha-catenin and its protein stability. J. Cell Sci. 2002;115:4743–4753. doi: 10.1242/jcs.00154. PubMed DOI
Dayal S, et al. Suppression of the deubiquitinating enzyme USP5 causes the accumulation of unanchored polyubiquitin and the activation of p53. J. Biol. Chem. 2009;284:5030–5041. doi: 10.1074/jbc.M805871200. PubMed DOI PMC
Hemann MT, Lowe SW. The p53–Bcl-2 connection. Cell Death Differ. 2006;13:1256–1259. doi: 10.1038/sj.cdd.4401962. PubMed DOI PMC
Rah B, et al. PAWR-mediated suppression of BCL2 promotes switching of 3-azido withaferin A (3-AWA)-induced autophagy to apoptosis in prostate cancer cells. Autophagy. 2015;11:314–331. doi: 10.1080/15548627.2015.1017182. PubMed DOI PMC
Margalit O, et al. BCL6 is regulated by p53 through a response element frequently disrupted in B-cell non-Hodgkin lymphoma. Blood. 2006;107:1599–1607. doi: 10.1182/blood-2005-04-1629. PubMed DOI
Arbouzova NI, Bach EA, Zeidler MP. Ken & Barbie selectively regulates the expression of a subset of Jak/STAT pathway target genes. Curr. Biol. 2006;16:80–88. doi: 10.1016/j.cub.2005.11.033. PubMed DOI
Issigonis M, Matunis E. The Drosophila BCL6 homolog Ken and Barbie promotes somatic stem cell self-renewal in the testis niche. Dev. Biol. 2012;368:181–192. doi: 10.1016/j.ydbio.2012.04.034. PubMed DOI PMC
Huynh KD, Fischle W, Verdin E, Bardwell VJ. BCoR, a novel corepressor involved in BCL-6 repression. Genes Dev. 2000;14:1810–1823. PubMed PMC
Dent AL, Vasanwala FH, Toney LM. Regulation of gene expression by the proto-oncogene BCL-6. Crit. Rev. Oncol. Hematol. 2002;41:1–9. doi: 10.1016/S1040-8428(01)00164-0. PubMed DOI
Walker SR, Nelson EA, Frank DA. STAT5 represses BCL6 expression by binding to a regulatory region frequently mutated in lymphomas. Oncogene. 2007;26:224–233. doi: 10.1038/sj.onc.1209775. PubMed DOI
Rayanade RJ, et al. Proteasome- and p53-dependent masking of signal transducer and activator of transcription (STAT) factors. J. Biol. Chem. 1997;272:4659–4662. doi: 10.1074/jbc.272.8.4659. PubMed DOI
Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res. 2009;19:128–139. doi: 10.1038/cr.2008.328. PubMed DOI PMC
Derynck R, Muthusamy BP, Saeteurn KY. Signaling pathway cooperation in TGF-beta-induced epithelial–mesenchymal transition. Curr. Opin. Cell Biol. 2014;31:56–66. doi: 10.1016/j.ceb.2014.09.001. PubMed DOI PMC
Liu W-T, et al. TGF-beta upregulates the translation of USP15 via the PI3K/AKT pathway to promote p53 stability. Oncogene. 2017;36:2715–2723. doi: 10.1038/onc.2016.424. PubMed DOI PMC
Cordenonsi M, et al. Integration of TGF-beta and Ras/MAPK signaling through p53 phosphorylation. Science. 2007;315:840–843. doi: 10.1126/science.1135961. PubMed DOI
Hall ET, Verheyen EM. Ras-activated Dsor1 promotes Wnt signaling in Drosophila development. J. Cell Sci. 2015;128:4499–4511. doi: 10.1242/jcs.175240. PubMed DOI
Campana WM, Hiraiwa M, O’Brien JS. Prosaptide activates the MAPK pathway by a G-protein-dependent mechanism essential for enhanced sulfatide synthesis by Schwann cells. FASEB J. 1998;12:307–314. doi: 10.1096/fasebj.12.3.307. PubMed DOI
Campana WM, Hiraiwa M, Addison KC, O’Brien JS. Induction of MAPK phosphorylation by prosaposin and prosaptide in PC12 cells. Biochem. Biophys. Res. Commun. 1996;229:706–712. doi: 10.1006/bbrc.1996.1869. PubMed DOI
Campana WM, Darin SJ, O’Brien JS. Phosphatidylinositol 3-kinase and Akt protein kinase mediate IGF-I- and prosaptide-induced survival in Schwann cells. J. Neurosci. Res. 1999;57:332–341. doi: 10.1002/(SICI)1097-4547(19990801)57:3<332::AID-JNR5>3.0.CO;2-0. PubMed DOI
Castellano E, Downward J. RAS interaction with PI3K: more than just another effector pathway. Genes Cancer. 2011;2:261–274. doi: 10.1177/1947601911408079. PubMed DOI PMC
Bhuin T, Roy JK. Rab proteins: the key regulators of intracellular vesicle transport. Exp. Cell Res. 2014;328:1–19. doi: 10.1016/j.yexcr.2014.07.027. PubMed DOI
Schnatwinkel C, et al. The Rab5 effector Rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLOS Biol. 2004;2:e261. doi: 10.1371/journal.pbio.0020261. PubMed DOI PMC
Macovei A, Petrareanu C, Lazar C, Florian P, Branza-Nichita N. Regulation of hepatitis B virus infection by Rab5, Rab7, and the endolysosomal compartment. J. Virol. 2013;87:6415–6427. doi: 10.1128/JVI.00393-13. PubMed DOI PMC
Scheffzek K, Ahmadian MR. GTPase activating proteins: structural and functional insights 18 years after discovery. Cell. Mol. Life Sci. 2005;62:3014–3038. doi: 10.1007/s00018-005-5136-x. PubMed DOI PMC
Luo L, et al. Genghis Khan (Gek) as a putative effector for Drosophila Cdc42 and regulator of actin polymerization. Proc. Natl. Acad. Sci. USA. 1997;94:12963–12968. doi: 10.1073/pnas.94.24.12963. PubMed DOI PMC
Malek M, et al. LAMTOR1 depletion induces p53-dependent apoptosis via aberrant lysosomal activation. Cell Death Dis. 2012;3:e300. doi: 10.1038/cddis.2012.39. PubMed DOI PMC
Sancak Y, et al. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell. 2010;141:290–303. doi: 10.1016/j.cell.2010.02.024. PubMed DOI PMC
Li F, Yin Y, Tan B, Kong X, Wu G. Leucine nutrition in animals and humans: mTOR signaling and beyond. Amino Acids. 2011;41:1185–1193. doi: 10.1007/s00726-011-0983-2. PubMed DOI
Dai F, Lin X, Chang C, Feng X-H. Nuclear export of Smad2 and Smad3 by RanBP3 facilitates termination of TGF-beta signaling. Dev. Cell. 2009;16:345–357. doi: 10.1016/j.devcel.2009.01.022. PubMed DOI PMC
Yoon S-O, et al. Ran-binding protein 3 phosphorylation links the Ras and PI3-kinase pathways to nucleocytoplasmic transport. Mol. Cell. 2008;29:362–375. doi: 10.1016/j.molcel.2007.12.024. PubMed DOI PMC
Predicala R, Zhou Y. The role of Ran-binding protein 3 during influenza A virus replication. J. Gen. Virol. 2013;94:977–984. doi: 10.1099/vir.0.049395-0. PubMed DOI
Baeg G-H, Zhou R, Perrimon N. Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev. 2005;19:1861–1870. doi: 10.1101/gad.1320705. PubMed DOI PMC
Hendriksen J, et al. RanBP3 enhances nuclear export of active beta-catenin independently of CRM1. J. Cell Biol. 2005;171:785–797. doi: 10.1083/jcb.200502141. PubMed DOI PMC
Sadot E, Geiger B, Oren M, Ben-Ze’ev A. Down-regulation of beta-catenin by activated p53. Mol. Cell. Biol. 2001;21:6768–6781. doi: 10.1128/MCB.21.20.6768-6781.2001. PubMed DOI PMC
Sotillos S, Krahn M, Espinosa-Vazquez JM, Hombria JC-G. Src kinases mediate the interaction of the apical determinant Bazooka/PAR3 with STAT92E and increase signalling efficiency in Drosophila ectodermal cells. Development. 2013;140:1507–1516. doi: 10.1242/dev.092320. PubMed DOI
Fernandez R, et al. The Drosophila shark tyrosine kinase is required for embryonic dorsal closure. Genes Dev. 2000;14:604–614. PubMed PMC
Tateno M, Nishida Y, Adachi-Yamada T. Regulation of JNK by Src during Drosophila development. Science. 2000;287:324–327. doi: 10.1126/science.287.5451.324. PubMed DOI
Evans IR, Rodrigues FSLM, Armitage EL, Wood W. Draper/CED-1 mediates an ancient damage response to control inflammatory blood cell migration in vivo. Curr. Biol. 2015;25:1606–1612. doi: 10.1016/j.cub.2015.04.037. PubMed DOI PMC
Lu X, Li Y. Drosophila Src42A is a negative regulator of RTK signaling. Dev. Biol. 1999;208:233–243. doi: 10.1006/dbio.1999.9196. PubMed DOI
Juarez MT, Patterson RA, Sandoval-Guillen E, McGinnis W. Duox, Flotillin-2, and Src42A are required to activate or delimit the spread of the transcriptional response to epidermal wounds in Drosophila. PLoS Genet. 2011;7:e1002424. doi: 10.1371/journal.pgen.1002424. PubMed DOI PMC
Si Y, et al. Src inhibits the Hippo tumor suppressor pathway through tyrosine phosphorylation of LATS1. Cancer Res. 2017;77:4868–4880. doi: 10.1158/0008-5472.CAN-17-0391. PubMed DOI
Losick VP, Jun AS, Spradling AC. Wound-induced polyploidization: regulation by Hippo and JNK signaling and conservation in mammals. Plos One. 2016;11:e0151251. doi: 10.1371/journal.pone.0151251. PubMed DOI PMC
Dhanasekaran DN, Reddy EP. JNK signaling in apoptosis. Oncogene. 2008;27:6245–6251. doi: 10.1038/onc.2008.301. PubMed DOI PMC
Komiya Y, Habas R. Wnt signal transduction pathways. Organogenesis. 2008;4:68–75. doi: 10.4161/org.4.2.5851. PubMed DOI PMC
Ohno S. Extrinsic Wnt signalling controls the polarity component aPKC. Nat. Cell Biol. 2007;9:738–740. doi: 10.1038/ncb0707-738. PubMed DOI
Archibald A, Al-Masri M, Liew-Spilger A, McCaffrey L. Atypical protein kinase C induces cell transformation by disrupting Hippo/Yap signaling. Mol. Biol. Cell. 2015;26:3578–3595. doi: 10.1091/mbc.E15-05-0265. PubMed DOI PMC
Graybill C, Wee B, Atwood SX, Prehoda KE. Partitioning-defective protein 6 (Par-6) activates atypical protein kinase C (aPKC) by pseudosubstrate displacement. J. Biol. Chem. 2012;287:21003–21011. doi: 10.1074/jbc.M112.360495. PubMed DOI PMC
Vyas P, Singh A, Murawala P, Joseph J. Nup358 interacts with Dishevelled and aPKC to regulate neuronal polarity. Biol. Open. 2013;2:1270–1278. doi: 10.1242/bio.20135363. PubMed DOI PMC
Wang Y-y, Zhao R, Zhe H. The emerging role of CaMKII in cancer. Oncotarget. 2015;6:11725–11734. PubMed PMC
Gupta RG, et al. HIV and SIV induce alterations in CNS CaMKII expression and activation: a potential mechanism for cognitive impairment. Am. J. Pathol. 2010;176:2776–2784. doi: 10.2353/ajpath.2010.090809. PubMed DOI PMC
Shah KS, Evans EC, Pizzorno MC. Localization of deformed wing virus (DWV) in the brains of the honeybee, Apis mellifera Linnaeus. Virol. J. 2009;6:182. doi: 10.1186/1743-422X-6-182. PubMed DOI PMC
Rines AK, Burke MA, Fernandez RP, Volpert OV, Ardehali H. Snf1-related kinase inhibits colon cancer cell proliferation through calcyclin-binding protein-dependent reduction of beta-catenin. FASEB J. 2012;26:4685–4695. doi: 10.1096/fj.12-212282. PubMed DOI PMC
Matsuzawa S-i, Reed JC. Siah-1, SIP, and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol. Cell. 2001;7:915–926. doi: 10.1016/S1097-2765(01)00242-8. PubMed DOI
Jamieson C, Lui C, Brocardo MG, Martino-Echarri E, Henderson BR. Rac1 augments Wnt signaling by stimulating beta-catenin–lymphoid enhancer factor-1 complex assembly independent of beta-catenin nuclear import. J. Cell Sci. 2015;128:3933–3946. doi: 10.1242/jcs.167742. PubMed DOI PMC
Wang Z-G, Jia M-K, Cao H, Bian P, Fang X-D. Knockdown of Coronin-1C disrupts Rac1 activation and impairs tumorigenic potential in hepatocellular carcinoma cells. Oncol. Rep. 2013;29:1066–1072. doi: 10.3892/or.2012.2216. PubMed DOI
Swaminathan K, Muller-Taubenberger A, Faix J, Rivero F, Noegel AA. A Cdc42- and Rac-interactive binding (CRIB) domain mediates functions of coronin. Proc. Natl. Acad. Sci. USA. 2014;111:E25–E33. doi: 10.1073/pnas.1315368111. PubMed DOI PMC
Dai P, et al. Modulation of TLR signaling by multiple MyD88-interacting partners including leucine-rich repeat Fli-I-interacting proteins. J. Immunol. 2009;182:3450–3460. doi: 10.4049/jimmunol.0802260. PubMed DOI
Liu J, et al. Identification of the Wnt signaling activator leucine-rich repeat in Flightless interaction protein 2 by a genome-wide functional analysis. Proc. Natl. Acad. Sci. USA. 2005;102:1927–1932. doi: 10.1073/pnas.0409472102. PubMed DOI PMC
Katoh Y, Katoh M. Comparative genomics on SLIT1, SLIT2, and SLIT3 orthologs. Oncol. Rep. 2005;14:1351–1355. PubMed
Ma X, et al. Hippo signaling promotes JNK-dependent cell migration. Proc. Natl. Acad. Sci. USA. 2017;114:1934–1939. doi: 10.1073/pnas.1621359114. PubMed DOI PMC
Tisdale EJ, Shisheva A, Artalejo CR. Overexpression of atypical protein kinase C in HeLa cells facilitates macropinocytosis via Src activation. Cell. Signal. 2014;26:1235–1242. doi: 10.1016/j.cellsig.2014.02.014. PubMed DOI PMC
Akhmetshina A, et al. Activation of canonical Wnt signalling is required for TGF-beta-mediated fibrosis. Nat. Commun. 2012;3:735. doi: 10.1038/ncomms1734. PubMed DOI PMC
Marchler-Bauer A, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–D203. doi: 10.1093/nar/gkw1129. PubMed DOI PMC
Kurzik-Dumke U, Lohmann E. Sequence of the new Drosophila melanogaster small heat-shock-related gene, lethal(2) essential for life [l(2) efl], at locus 59F4,5. Gene. 1995;154:171–175. doi: 10.1016/0378-1119(94)00827-F. PubMed DOI
Clements RT, et al. Phosphorylation and translocation of heat shock protein 27 and alphaB-crystallin in human myocardium after cardioplegia and cardiopulmonary bypass. J. Thorac. Cardiovasc. Surg. 2007;134:1461–1470. doi: 10.1016/j.jtcvs.2007.06.026. PubMed DOI
Clements RT, Feng J, Cordeiro B, Bianchi C, Sellke FW. p38 MAPK-dependent small HSP27 and alphaB-crystallin phosphorylation in regulation of myocardial function following cardioplegic arrest. Am. J. Physiol. Heart Circ. Physiol. 2011;300:H1669–H1677. doi: 10.1152/ajpheart.00272.2010. PubMed DOI PMC
Cubedo J, et al. Targeting the molecular mechanisms of ischemic damage: protective effects of alpha-crystallin-B. Int. J. Cardiol. 2016;215:406–416. doi: 10.1016/j.ijcard.2016.04.072. PubMed DOI
Azuma M, et al. TGF-beta1 inhibits NF-kappaB activity through induction of IkappaB-alpha expression in human salivary gland cells: a possible mechanism of growth suppression by TGF-beta1. Exp. Cell Res. 1999;250:213–222. doi: 10.1006/excr.1999.4503. PubMed DOI
Santoro MG, Rossi A, Amici C. NF-kappaB and virus infection: who controls whom. EMBO J. 2003;22:2552–2560. doi: 10.1093/emboj/cdg267. PubMed DOI PMC
Chaudhary P, et al. HSP70 binding protein 1 (HspBP1) suppresses HIV-1 replication by inhibiting NF-kappaB mediated activation of viral gene expression. Nucleic Acids Res. 2016;44:1613–1629. doi: 10.1093/nar/gkv1151. PubMed DOI PMC
Geisler R, Bergmann A, Hiromi Y, Nusslein-Volhard C. cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the IkappaB gene family of vertebrates. Cell. 1992;71:613–621. doi: 10.1016/0092-8674(92)90595-4. PubMed DOI
Liu B, et al. Toll receptor-mediated Hippo signaling controls innate immunity in Drosophila. Cell. 2016;164:406–419. doi: 10.1016/j.cell.2015.12.029. PubMed DOI PMC
Lecat A, et al. The c-Jun N-terminal kinase (JNK)-binding protein (JNKBP1) acts as a negative regulator of NOD2 protein signaling by inhibiting its oligomerization process. J. Biol. Chem. 2012;287:29213–29226. doi: 10.1074/jbc.M112.355545. PubMed DOI PMC
Koyano S, et al. A novel Jun N-terminal kinase (JNK)-binding protein that enhances the activation of JNK by MEK kinase 1 and TGF-beta-activated kinase 1. FEBS Lett. 1999;457:385–388. doi: 10.1016/S0014-5793(99)01084-4. PubMed DOI
Kriehuber E, et al. Balance between NF-kappaB and JNK/AP-1 activity controls dendritic cell life and death. Blood. 2005;106:175–183. doi: 10.1182/blood-2004-08-3072. PubMed DOI
Chu SH, et al. Down-regulation of Bcl-2 is mediated by NF-kappaB activation in Helicobacter pylori-induced apoptosis of gastric epithelial cells. Scand. J. Gastroenterol. 2011;46:148–155. doi: 10.3109/00365521.2010.525255. PubMed DOI
Meyer SN, et al. An ancient defense system eliminates unfit cells from developing tissues during cell competition. Science. 2014;346:1258236. doi: 10.1126/science.1258236. PubMed DOI PMC
Kopp E, et al. ECSIT is an evolutionarily conserved intermediate in the Toll/IL-1 signal transduction pathway. Genes Dev. 1999;13:2059–2071. doi: 10.1101/gad.13.16.2059. PubMed DOI PMC
Xiao C, et al. Ecsit is required for Bmp signaling and mesoderm formation during mouse embryogenesis. Genes Dev. 2003;17:2933–2949. doi: 10.1101/gad.1145603. PubMed DOI PMC
Sriskanthadevan-Pirahas S, Deshpande R, Lee B, Grewal SS. Ras/ERK-signalling promotes tRNA synthesis and growth via the RNA polymerase III repressor Maf1 in. Drosophila. PLOS Genet. 2018;14:e1007202. doi: 10.1371/journal.pgen.1007202. PubMed DOI PMC
Bhatt D, Ghosh S. Regulation of the NF-kappaB-mediated transcription of inflammatory genes. Front. Immunol. 2014;5:71. doi: 10.3389/fimmu.2014.00071. PubMed DOI PMC
Garber M, et al. A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol. Cell. 2012;47:810–822. doi: 10.1016/j.molcel.2012.07.030. PubMed DOI PMC
Barish GD, et al. Bcl-6 and NF-kappaB cistromes mediate opposing regulation of the innate immune response. Genes Dev. 2010;24:2760–2765. doi: 10.1101/gad.1998010. PubMed DOI PMC
Wang D, et al. BCL6 represses Smad signaling in transforming growth factor-beta resistance. Cancer Res. 2008;68:783–789. doi: 10.1158/0008-5472.CAN-07-0008. PubMed DOI
Scandura JM, Boccuni P, Massague J, Nimer SD. Transforming growth factor beta-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc. Natl. Acad. Sci. USA. 2004;101:15231–15236. doi: 10.1073/pnas.0406771101. PubMed DOI PMC
Rodrigues AB, et al. Activated STAT regulates growth and induces competitive interactions independently of Myc, Yorkie, Wingless and ribosome biogenesis. Development. 2012;139:4051–4061. doi: 10.1242/dev.076760. PubMed DOI PMC
Mitchell TJ, John S. Signal transducer and activator of transcription (STAT) signalling and T-cell lymphomas. Immunology. 2005;114:301–312. doi: 10.1111/j.1365-2567.2005.02091.x. PubMed DOI PMC
Zargar ZU, Tyagi S. Role of host cell factor-1 in cell cycle regulation. Transcription. 2012;3:187–192. doi: 10.4161/trns.20711. PubMed DOI PMC
Bowen-Walker PL, Gunn A. The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomol. Exp. Appl. 2001;101:207–217. doi: 10.1046/j.1570-7458.2001.00905.x. DOI
Fratini F, Cilia G, Mancini S, Felicioli A. Royal jelly: an ancient remedy with remarkable antibacterial properties. Microbiol. Res. 2016;192:130–141. doi: 10.1016/j.micres.2016.06.007. PubMed DOI
Seehuus S-C, Norberg K, Gimsa U, Krekling T, Amdam GV. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proc. Natl. Acad. Sci. USA. 2006;103:962–967. doi: 10.1073/pnas.0502681103. PubMed DOI PMC
Amdam GV, Norberg K, Hagen A, Omholt SW. Social exploitation of vitellogenin. Proc. Natl. Acad. Sci. USA. 2003;100:1799–1802. doi: 10.1073/pnas.0333979100. PubMed DOI PMC
Ararso Z, et al. Proteome comparisons between hemolymph of two honeybee strains (Apis mellifera ligustica) reveal divergent molecular basis in driving hemolymph function and high royal jelly secretion. J. Proteome Res. 2018;17:402–419. doi: 10.1021/acs.jproteome.7b00621. PubMed DOI
Peixoto LG, et al. Identification of major royal jelly proteins in the brain of the honeybee Apis mellifera. J. Insect Physiol. 2009;55:671–677. doi: 10.1016/j.jinsphys.2009.05.005. 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. USA. 2009;106:21091–21096. doi: 10.1073/pnas.0909938106. PubMed DOI PMC
Zhang Q-R, Xu W-H, Chen F-S, Li S. Molecular and biochemical characterization of juvenile hormone epoxide hydrolase from the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 2005;35:153–164. doi: 10.1016/j.ibmb.2004.10.010. PubMed DOI
Amdam GV, et al. Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees. Exp. Gerontol. 2004;39:767–773. doi: 10.1016/j.exger.2004.02.010. PubMed DOI
El-Bacha T, Da Poian AT. Virus-induced changes in mitochondrial bioenergetics as potential targets for therapy. Int. J. Biochem. Cell Biol. 2013;45:41–46. doi: 10.1016/j.biocel.2012.09.021. PubMed DOI
Ikeda Y, Tanaka K. Purification and characterization of isovaleryl coenzyme A dehydrogenase from rat liver mitochondria. J. Biol. Chem. 1983;258:1077–1085. PubMed
Ishizaki K, et al. The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell. 2005;17:2587–2600. doi: 10.1105/tpc.105.035162. PubMed DOI PMC
Vockley J, Ensenauer R. Isovaleric acidemia: new aspects of genetic and phenotypic heterogeneity. Am. J. Med. Genet. C Semin. Med. Genet. 2006;142C:95–103. doi: 10.1002/ajmg.c.30089. PubMed DOI PMC
Vogel RO, et al. Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Genes Dev. 2007;21:615–624. doi: 10.1101/gad.408407. PubMed DOI PMC
Paiva CN, Bozza MT. Are reactive oxygen species always detrimental to pathogens? Antioxid. Redox Signal. 2014;20:1000–1037. doi: 10.1089/ars.2013.5447. PubMed DOI PMC
Qiu Y, et al. An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc. Natl. Acad. Sci. USA. 2012;109:14858–14863. doi: 10.1073/pnas.1208650109. PubMed DOI PMC
Eiberg H, Mohr J. Identity of the polymorphisms for esterase D and S-formylglutathione hydrolase in red blood cells. Hum. Genet. 1986;74:174–175. doi: 10.1007/BF00282085. PubMed DOI
Yang X, et al. Catalytic strategy of S-adenosyl-L-homocysteine hydrolase: transition-state stabilization and the avoidance of abortive reactions. Biochemistry. 2003;42:1900–1909. doi: 10.1021/bi0262350. PubMed DOI
Dorokhov YL, Shindyapina AV, Sheshukova EV, Komarova TV. Metabolic methanol: molecular pathways and physiological roles. Physiol. Rev. 2015;95:603–644. doi: 10.1152/physrev.00034.2014. PubMed DOI
O’Connor T, Ireland LS, Harrison DJ, Hayes JD. Major differences exist in the function and tissue-specific expression of human aflatoxin B1 aldehyde reductase and the principal human aldo-keto reductase AKR1 family members. Biochem. J. 1999;343:487–504. doi: 10.1042/0264-6021:3430487. PubMed DOI PMC
Chen NH, et al. A glutathione-dependent detoxification system is required for formaldehyde resistance and optimal survival of Neisseria meningitidis in biofilms. Antioxid. Redox Signal. 2013;18:743–755. doi: 10.1089/ars.2012.4749. PubMed DOI PMC
Hill BG, Bhatnagar A. Beyond reactive oxygen species: aldehydes as arbitrators of alarm and adaptation. Circ. Res. 2009;105:1044–1046. doi: 10.1161/CIRCRESAHA.109.209791. PubMed DOI PMC
Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Front. Biosci. 2008;13:1227–1239. doi: 10.2741/2757. PubMed DOI PMC
Zhang C, Li X, Liu Q. Sorbitol dehydrogenase inhibitor protects the liver from ischemia/reperfusion-induced injury via elevated glycolytic flux and enhanced sirtuin 1 activity. Mol. Med. Rep. 2015;11:283–288. doi: 10.3892/mmr.2014.2715. PubMed DOI
Ciuchi E, Odetti P, Prando R. Relationship between glutathione and sorbitol concentrations in erythrocytes from diabetic patients. Metabolism. 1996;45:611–613. doi: 10.1016/S0026-0495(96)90032-3. PubMed DOI
Chen J, Adikari M, Pallai R, Parekh HK, Simpkins H. Dihydrodiol dehydrogenases regulate the generation of reactive oxygen species and the development of cisplatin resistance in human ovarian carcinoma cells. Cancer Chemother. Pharmacol. 2008;61:979–987. doi: 10.1007/s00280-007-0554-0. PubMed DOI PMC
Giannini EG, Testa R, Savarino V. Liver enzyme alteration: a guide for clinicians. Can. Med. Assoc. J. 2005;172:367–379. doi: 10.1503/cmaj.1040752. PubMed DOI PMC
Kucharski R, Maleszka J, Maleszka R. Novel cuticular proteins revealed by the honey bee genome. Insect Biochem. Mol. Biol. 2007;37:128–134. doi: 10.1016/j.ibmb.2006.10.009. PubMed DOI
Foster LJ. Interpretation of data underlying the link between colony collapse disorder (CCD) and an invertebrate iridescent virus. Mol. Cell. Proteomics. 2011;10:M110.006387. doi: 10.1074/mcp.M110.006387. PubMed DOI PMC
Tokarz R, Firth C, Street C, Cox-Foster DL, Lipkin WI. Lack of evidence for an association between iridovirus and colony collapse disorder. Plos One. 2011;6:e21844. doi: 10.1371/journal.pone.0021844. PubMed DOI PMC
Lanzi G, et al. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.) J. Virol. 2006;80:4998–5009. doi: 10.1128/JVI.80.10.4998-5009.2006. PubMed DOI PMC
McMahon DP, et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. Biol. Sci. 2016;283:20160811. doi: 10.1098/rspb.2016.0811. PubMed DOI PMC
R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, http://www.R-project.org (2016).
Mann, M. Filter aided sample preparation (FASP) method. Matthias Mann Lab, http://www.biochem.mpg.de/226356/FASP (2016).
Hebert AS, et al. The one hour yeast proteome. Mol. Cell. Proteomics. 2014;13:339–347. doi: 10.1074/mcp.M113.034769. PubMed DOI PMC
Erban T, Harant K, Chalupnikova J, Kocourek F, Stara J. Beyond the survival and death of the deltamethrin-threatened pollen beetle Meligethes aeneus: an in-depth proteomic study employing a transcriptome database. J. Proteomics. 2017;150:281–289. doi: 10.1016/j.jprot.2016.09.016. PubMed DOI
Cox J, et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics. 2014;13:2513–2526. doi: 10.1074/mcp.M113.031591. PubMed DOI PMC
Cox J, et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011;10:1794–1805. doi: 10.1021/pr101065j. PubMed DOI
Cox J, Mann M. 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinformatics. 2012;13(Suppl. 16):S12. doi: 10.1186/1471-2105-13-S16-S12. PubMed DOI PMC
Anderson MJ, Ellingsen KE, McArdle BH. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 2006;9:683–693. doi: 10.1111/j.1461-0248.2006.00926.x. PubMed DOI
Oksanen, J. et al. vegan: Community Ecology Package. CRAN - The Comprehensive R ArchiveNetwork, http://CRAN.R-project.org/package=vegan (2016).
Warnes, G. R. et al. gplots: Various R Programming Tools for Plotting Data. CRAN - The Comprehensive R Archive Network, https://cran.rproject.org/web/packages/gplots/index.html (2016).
Szklarczyk D, et al. The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–D368. doi: 10.1093/nar/gkw937. PubMed DOI PMC
Hajnicka V, Vancova-Stibraniova I, Slovak M, Kocakova P, Nuttall PA. Ixodid tick salivary gland products target host wound healing growth factors. Int. J. Parasitol. 2011;41:213–223. doi: 10.1016/j.ijpara.2010.09.005. PubMed DOI
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI