Abstract
MAP kinase phosphatase 3 (MKP3), a member of the dual-specificity protein phosphatase (DUSP) superfamily, has been widely studied for its role in development, cancer, and environmental stress in many organisms. However, the functions of MKP3 in various insects have not been well studied, including honeybees. In this study, we isolated an MKP3 gene from Apis cerana cerana and explored the role of this gene in the resistance to oxidation. We found that AccMKP3 is highly conserved in different species and shares the closest evolutionary relationship with AmMKP3. We determined the expression patterns of AccMKP3 under various stresses. qRT-PCR results showed that AccMKP3 was highly expressed during the pupal stages and in adult muscles. We further found that AccMKP3 was induced in all the stress treatments. Moreover, we discovered that the enzymatic activities of peroxidase, superoxide dismutase, and catalase increased and that the expression levels of several antioxidant genes were affected after AccMKP3 was knocked down. Collectively, these results suggest that AccMKP3 may be associated with antioxidant processes involved in response to various environmental stresses.
Similar content being viewed by others
References
Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565. https://doi.org/10.1098/rsbl.2009.0986
Ali A, Rashid MA, Huang QY, Lei CL (2017) Influence of UV-A radiation on oxidative stress and antioxidant enzymes in Mythimna separata (Lepidoptera: Noctuidae). Environ Sci Pollut Res Int 24:8392–8398. https://doi.org/10.1007/s11356-017-8514-7
Asghari MH, Moloudizargari M, Bahadar H, Abdollahi M (2017) A review of the protective effect of melatonin in pesticide-induced toxicity. Expert Opin Drug Metab Toxicol 13:545–554. https://doi.org/10.1080/17425255.2016.1214712
Bafana A, Khan F, Suguna K (2017) Structural and functional characterization of mercuric reductase from Lysinibacillus sphaericus strain G1. Biometals 30:809–819. https://doi.org/10.1007/s10534-017-0050-x
Burmeister C, Kai L, Heinick A, Hussein A, Domagalski M, Walter RD, Liebau E (2008) Oxidative stress in Caenorhabditis elegans: protective effects of the Omega class glutathione transferase (GSTO-1). FASEB J 22:343–354. https://doi.org/10.1096/fj.06-7426com
Camps M, Nichols A, Gillieron C, Antonsson B, Muda M, Chabert C et al (1998) Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science 280:1262–1265
Camps M, Nichols A, Arkinstall S (2000) Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J 14:6–16
Chen X, Yao P, Chu X, Hao L, Guo X, Xu B (2015) Isolation of arginine kinase from Apis cerana cerana and its possible involvement in response to adverse stress. Cell Stress Chaperones 20:169–183. https://doi.org/10.1007/s12192-014-0535-2
Corona M, Robinson GE (2006) Genes of the antioxidant system of the honey bee: annotation and phylogeny. Insect Mol Biol 15:687–701. https://doi.org/10.1111/j.1365-2583.2006.00695.x
de Carvalho LP, de Melo EJT (2018) Further aspects of Toxoplasma gondii elimination in the presence of metals. Parasitol Res 117:1245–1256. https://doi.org/10.1007/s00436-018-5806-x
Emanuele S, D’Anneo A, Calvaruso G, Cernigliaro C, Giuliano M, Lauricella M (2018) The double-edged sword profile of redox signaling: oxidative events as molecular switches in the balance between cell physiology and cancer. Chem Res Toxicol 31:201–210. https://doi.org/10.1021/acs.chemrestox.7b00311
Ericsson A, Kotarsky K, Svensson M, Sigvardsson M, Agace W (2006) Functional characterization of the CCL25 promoter in small intestinal epithelial cells suggests a regulatory role for caudal-related homeobox (Cdx) transcription factors. J Immunol 176:3642–3651
Farooq A, Chaturvedi G, Mujtaba S, Plotnikova O, Zeng L, Dhalluin C, Ashton R, Zhou MM (2001) Solution structure of ERK2 binding domain of MAPK phosphatase MKP-3: structural insights into MKP-3 activation by ERK2. Mol Cell 7:387–399
Furukawa T, Horii A (2004) Molecular pathology of pancreatic cancer: in quest of tumor suppressor genes. Pancreas 28:253–256
Geng XM, Liu X, Ji M, Hoffmann WA, Grunden A, Xiang QY (2016) Enhancing heat tolerance of the little dogwood cornus canadensis L. f. with introduction of a superoxide reductase gene from the hyperthermophilic archaeon Pyrococcus furiosus. Front. Plant Sci 7:26. https://doi.org/10.3389/fpls.2016.00026
Graves JA, Metukuri M, Scott D, Rothermund K, Prochownik EV (2009) Regulation of reactive oxygen species homeostasis by peroxiredoxins and c-Myc. J Biol Chem 284:6520–6529. https://doi.org/10.1074/jbc.M807564200
Gray EM (2013) Thermal acclimation in a complex life cycle: the effects of larval and adult thermal conditions on metabolic rate and heat resistance in Culex pipiens (Diptera: Culicidae). J Insect Physiol 59:1001–1007. https://doi.org/10.1016/j.jinsphys.2013.08.001
Harrison JF, Fewell JH (2002) Environmental and genetic influences on flight metabolic rate in the honey bee, Apis mellifera. Comp Biochem Physiol A Mol Integr Physiol 133:323–333
Hayes JD, Mcmahon M (2009) NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 34:176–188. https://doi.org/10.1016/j.tibs.2008.12.008
Jeong DG et al (2014) The family-wide structure and function of human dual-specificity protein phosphatases. Acta Crystallogr D Biol Crystallogr 70:421–435. https://doi.org/10.1107/S1399004713029866
Jia H, Ma M, Zhai N, Liu Z, Wang H, Guo X, Xu B (2017) Roles of a mitochondrial AccSCO2 gene from Apis cerana cerana in oxidative stress responses. J Inorg Biochem 175:9–19. https://doi.org/10.1016/j.jinorgbio.2017.06.015
Karkali K, Panayotou G (2012) The Drosophila DUSP puckered is phosphorylated by JNK and p38 in response to arsenite-induced oxidative stress. Biochem Biophys Res Commun 418:301–306. https://doi.org/10.1016/j.bbrc.2012.01.015
Kim SH et al (2002) Isolation and characterization of a Drosophila homologue of mitogen-activated protein kinase phosphatase-3 which has a high substrate specificity towards extracellular-signal-regulated kinase. Biochem J 361:143–151
Koga S, Kojima S, Kishimoto T, Kuwabara S, Yamaguchi A (2012) Over-expression of map kinase phosphatase-1 (MKP-1) suppresses neuronal death through regulating JNK signaling in hypoxia/re-oxygenation. Brain Res 1436:137–146. https://doi.org/10.1016/j.brainres.2011.12.004
Lee SB, Shin JS, Han HS, Lee HH, Park JC, Lee KT (2018) Kaempferol 7-O-beta-D-glucoside isolated from the leaves of Cudrania tricuspidata inhibits LPS-induced expression of pro-inflammatory mediators through inactivation of NF-κB, AP-1, and JAK-STAT in RAW 264.7 macrophages. Chem Biol Interact 284:101–111. https://doi.org/10.1016/j.cbi.2018.02.022
Li G, Zhao H, Wang H, Guo X, Guo X, Sun Q, Xu B (2016) Characterization of a decapentapletic gene (AccDpp) from Apis cerana cerana and its possible involvement in development and response to oxidative stress. PLoS One 11:e0149117. https://doi.org/10.1371/journal.pone.0149117
Li C et al (2018) BHDPC is a novel neuroprotectant that provides anti-neuroinflammatory and neuroprotective effects by inactivating NF-κB and activating PKA/CREB. Front Pharmacol 9:614. https://doi.org/10.3389/fphar.2018.00614
Liu S, Sun JP, Zhou B, Zhang ZY (2006) Structural basis of docking interactions between ERK2 and MAP kinase phosphatase 3. Proc Natl Acad Sci U S A 103:5326–5331. https://doi.org/10.1073/pnas.0510506103
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Mates JM, Segura JA, Alonso FJ, Marquez J (2012) Oxidative stress in apoptosis and cancer: an update. Arch Toxicol 86:1649–1665. https://doi.org/10.1007/s00204-012-0906-3
Matsumura T, Matsumoto H, Hayakawa Y (2017) Heat stress hardening of oriental armyworms is induced by a transient elevation of reactive oxygen species during sublethal stress. Arch Insect Biochem Physiol:96. https://doi.org/10.1002/arch.21421
Mazaira GI, Daneri-Becerra C, Zgajnar NR, Lotufo CM, Galigniana MD (2018) Gene expression regulation by heat-shock proteins: the cardinal roles of HSF1 and Hsp90. Biochem Soc Trans 46:51–65. https://doi.org/10.1042/BST20170335
Molnar C, de Celis JF (2013) Tay bridge is a negative regulator of EGFR signalling and interacts with Erk and Mkp3 in the Drosophila melanogaster wing. PLoS Genet 9:e1003982. https://doi.org/10.1371/journal.pgen.1003982
Moskovitz J, Oien DB (2010) Protein carbonyl and the methionine sulfoxide reductase system. Antioxid Redox Signal 12:405–415. https://doi.org/10.1089/ars.2009.2809
Muda M et al (1996) The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J Biol Chem 271:27205–27208
Muda M et al (1998) The mitogen-activated protein kinase phosphatase-3 N-terminal noncatalytic region is responsible for tight substrate binding and enzymatic specificity. J Biol Chem 273:9323–9329. https://doi.org/10.1074/jbc.273.15.9323
Oehrl W, Cotsiki M, Panayotou G (2013) Differential regulation of M3/6 (DUSP8) signaling complexes in response to arsenite-induced oxidative stress. Cell Signal 25:429–438. https://doi.org/10.1016/j.cellsig.2012.11.010
Palacios C, Collins MK, Perkins GR (2001) The JNK phosphatase M3/6 is inhibited by protein-damaging stress. Curr Biol 11:1439–1443
Patterson KI, Brummer T, O’Brien PM, Daly RJ (2009) Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem J 418:475–489
Ratnieks FLW (2006) Asian honey bees: biology, conservation and human interactions. Nature 442:249–249
Schatzman SS, Culotta VC (2018) Chemical warfare at the microorganismal level: a closer look at the superoxide dismutase enzymes of pathogens. ACS Infect Dis 4:893–903. https://doi.org/10.1021/acsinfecdis.8b00026
Sharda PR, Bonham CA, Mucaki EJ, Butt Z, Vacratsis PO (2009) The dual-specificity phosphatase hYVH1 interacts with Hsp70 and prevents heat-shock-induced cell death. Biochem J 418:391–1401. https://doi.org/10.1042/BJ20081484
Shi W, Sun J, Xu B, Li H (2013) Molecular characterization and oxidative stress response of a cytochrome P450 gene (CYP4G11) from Apis cerana cerana. Z Naturforsch C 68:509–521
Stewart AE, Dowd S, Keyse SM, McDonald NQ (1999) Crystal structure of the MAPK phosphatase Pyst1 catalytic domain and implications for regulated activation. Nat Struct Biol 6:174–181. https://doi.org/10.1038/5861
Takagaki K, Shima H, Tanuma N, Nomura M, Satoh T, Watanabe M, Kikuchi K (2007) Characterization of a novel low-molecular-mass dual specificity phosphatase-4 (LDP-4) expressed in brain. Mol Cell Biochem 296:177–184. https://doi.org/10.1007/s11010-006-9313-5
Tang T, Huang DW, Zhou CQ, Li X, Xie QJ, Liu FS (2012) Molecular cloning and expression patterns of copper/zinc superoxide dismutase and manganese superoxide dismutase in Musca domestica. Gene 505:211–220. https://doi.org/10.1016/j.gene.2012.06.025
Wong VC et al (2012) Tumor suppressor dual-specificity phosphatase 6 (DUSP6) impairs cell invasion and epithelial-mesenchymal transition (EMT)-associated phenotype. Int J Cancer 130:83–95. https://doi.org/10.1002/ijc.25970
Zhang YY, Wu JW, Wang ZX (2011) Mitogen-activated protein kinase (MAPK) phosphatase 3-mediated cross-talk between MAPKs ERK2 and p38alpha. J Biol Chem 286:16150–16162. https://doi.org/10.1074/jbc.M110.203786
Zhao G, Wang C, Wang H, Gao L, Liu Z, Xu B, Guo X (2018) Characterization of the CDK5 gene in Apis cerana cerana (AccCDK5) and a preliminary identification of its activator gene, AccCDK5r1. Cell Stress Chaperones 23:13–28. https://doi.org/10.1007/s12192-017-0820-y
Zhu M, Zhang W, Liu F, Chen X, Li H, Xu B (2016) Characterization of an Apis cerana cerana cytochrome P450 gene (AccCYP336A1) and its roles in oxidative stresses responses. Gene 584:120–128. https://doi.org/10.1016/j.gene.2016.02.016
Funding
This work was financially supported by Funds of the National Natural Science Foundation of China (No. 31572470) and the Earmarked Fund for the China Agriculture Research System (No. CARS-44).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Chao, Y., Wang, C., Jia, H. et al. Identification of an Apis cerana cerana MAP kinase phosphatase 3 gene (AccMKP3) in response to environmental stress. Cell Stress and Chaperones 24, 1137–1149 (2019). https://doi.org/10.1007/s12192-019-01036-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-019-01036-5