Functional analysis of an upregulated calmodulin gene related to the acaricidal activity of curcumin against Tetranychus cinnabarinus (Boisduval).
RNAi
Tetranychus cinnabarinus
calmodulin
curcumin
heterologous expression
Journal
Pest management science
ISSN: 1526-4998
Titre abrégé: Pest Manag Sci
Pays: England
ID NLM: 100898744
Informations de publication
Date de publication:
Feb 2021
Feb 2021
Historique:
received:
06
12
2019
revised:
01
08
2020
accepted:
31
08
2020
pubmed:
1
9
2020
medline:
15
1
2021
entrez:
1
9
2020
Statut:
ppublish
Résumé
Curcumin is a promising botanical acaricidal compound with activity against Tetranychus cinnabarinus. Calmodulin (CaM) is a key calcium ion (Ca A CaM gene was cloned from T. cinnabarinus (designated TcCaM). TcCaM was upregulated and the protein was activated in mites by curcumin. The susceptibility of mites to curcumin was decreased after inhibiting CaM function with anti-CaM drug trifluoperazine (TFP) and silencing CaM transcription with RNAi, suggesting that the CaM gene is involved in the acaricidal activity of curcumin against mites. Moreover, the TFP pre-treated Sf9 cells were resistant to curcumin-mediated increase in [Ca These results confirm that the overexpressed CaM gene is involved in the acaricidal activity of curcumin, and the mode of action of curcumin may be via activating CaM function, and thereby disrupting Ca
Sections du résumé
BACKGROUND
BACKGROUND
Curcumin is a promising botanical acaricidal compound with activity against Tetranychus cinnabarinus. Calmodulin (CaM) is a key calcium ion (Ca
RESULTS
RESULTS
A CaM gene was cloned from T. cinnabarinus (designated TcCaM). TcCaM was upregulated and the protein was activated in mites by curcumin. The susceptibility of mites to curcumin was decreased after inhibiting CaM function with anti-CaM drug trifluoperazine (TFP) and silencing CaM transcription with RNAi, suggesting that the CaM gene is involved in the acaricidal activity of curcumin against mites. Moreover, the TFP pre-treated Sf9 cells were resistant to curcumin-mediated increase in [Ca
CONCLUSION
CONCLUSIONS
These results confirm that the overexpressed CaM gene is involved in the acaricidal activity of curcumin, and the mode of action of curcumin may be via activating CaM function, and thereby disrupting Ca
Substances chimiques
Acaricides
0
Calmodulin
0
Curcumin
IT942ZTH98
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
719-730Subventions
Organisme : National Science Foundation of China
ID : 31572041
Organisme : National Science Foundation of China
ID : 31972288
Informations de copyright
© 2020 Society of Chemical Industry.
Références
Zhang Y, Zhang Z, Yutaka S, Liu Q and Ji J, On the causes of mite pest outbreaks in mono- and poly-cultured moso bamboo forests. Chin J Appl Ecol 15:1161-1165 (2004).
Çakmak I, Başpinar H and Madanlar N, Control of the carmine spider mite Tetranychus cinnabarinus boisduval by the predatory mite Phytoseiulus persimilis (Athias-Henriot) in protected strawberries in Aydin, Tukey. Turk J Agric For 29:259-265 (2005).
Sarwar M, Management of spider mite Tetranychus cinnabarinus (Boisduval) (Tetranychidae) infestation in cotton by releasing the predatory mite Neoseiulus pseudolongispinosus (Xin, Liang and Ke) (Phytoseiidae). Biol Control 65:37-42 (2013).
Hou QL, Luo JX, Zhang BC, Jiang GF, Ding W and Zhang YQ, 3D-QSAR and molecular docking studies on the TcPMCA1-mediated detoxification of scopoletin and coumarin derivatives. Int J Mol Sci 18:1380 (2017).
Hidaka H, Ishiko T, Furuhashi T, Kamohara H, Suzuki S, Miyazaki M et al., Curcumin inhibits interleukin 8 production and enhances interleukin 8 receptor expression on the cell surface: impact on human pancreatic carcinoma cell growth by autocrine regulation. Cancer 95:1206-1214 (2010).
Li N, Chen X, Liao J, Yang G, Wang S, Josephson Y et al., Inhibition of 7,12-dimethylbenz[a]anthracene (DMBA)-induced oral carcinogenesis in hamsters by tea and curcumin. Carcinogenesis 23:1307-1313 (2002).
Zhang YQ, Wei D and Zhao ZM, Biological activities of curcuminoids against Tetranychus cinnabarinus Boisduval (Acari:Tetranychidae). Acta Ent Sin 50:1304-1308 (2007).
Tripathi AK, Prajapati V, Verma N, Bahl JR, Bansal RP, Khanuja SPS et al., Bioactivities of the leaf essential oil of Curcuma longa on three species of stored-product beetles (Coleoptera). J Econ Entomol 95:183-189 (2002).
Martins CVB, Silva DLD, Neres ATM, Magalhães TFF, Watanabe GA, Modolo LV et al., Curcumin as a promising antifungal of clinical interest. J Antimicrob Chemother 63:337 (2009).
Brouet I and Ohshima H, Curcumin, an anti-tumour promoter and anti-inflammatory agent, inhibits induction of nitric oxide synthase in activated macrophages. Biochem Biophys Res Commun 206:533-540 (1995).
Sharma OP, Antioxidant activity of curcumin and related compounds. Biochem Pharmacol 25:1811-1812 (1976).
Swatson WS, Katohkurasawa M, Shaulsky G and Alexander S, Curcumin affects gene expression and reactive oxygen species via a PKA dependent mechanism in Dictyostelium discoideum. PLos One 12:e0187562 (2017).
Mukhopadhyay A, Bueso-Ramos C, Chatterjee D, Pantazis P and Aggarwal BB, Curcumin downregulates cell survival mechanisms in human prostate cancer cell lines. Oncogene 20:7597-7609 (2001).
Zhang YQ, Ding W, Zhao ZM, Wu J and Fan YH, Acaricidal bioactivity of different growth period Artemisia annua extracts against Tetranychus cinnabarinus. Chin J Ecol 26:1969-1973 (2007).
Luo JX, Ding W, Zhang YQ, Yang ZG, Yang LI and Ding LJ, Acaricidal activity of bisdemethoxycurcumin and N-methylpyrazolebisdemethoxycurcumin against Tetranychus cinnabarinus (Boisduval) and their effects on enzymes activity in the mite. Sci Agric Sin 46:2833-2844 (2013).
Liu X, Wu D, Zhang Y, Hong Z, Lai T and Wei D, RNA-seq analysis reveals candidate targets for curcumin against Tetranychus cinnabarinus. Biomed Res Int 2016:1-10 (2016).
Berridge MJ, Bootman MD and Roderick HL, Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517-529 (2003).
Pang ZP, Cao P, Xu W and Südhof TC, Calmodulin controls synaptic strength via presynaptic activation of calmodulin kinase II. J Neurosci 30:4132-4142 (2010).
Shirasaki Y, Kanazawa Y, Morishima Y and Makino M, Involvement of calmodulin in neuronal cell death. Brain Res 1083:189-195 (2006).
Shim JS, Lee J, Park HJ, Park SJ and Kwon HJ, A new curcumin derivative, HBC, interferes with the cell cycle progression of colon cancer cells via antagonization of the Ca/calmodulin function. Chem Biol 11:1455-1463 (2004).
Babu YS, Sack JS, Greenhough TJ, Bugg CE, Means AR and Cook WJ, Three-dimensional structure of calmodulin. Nature 315:37-40 (1985).
Copley RR, Schultz J, Ponting CP and Bork P, Protein families in multicellular organisms. Curr Opin Struct Biol 9:408-415 (1999).
Dolmetsch RE, Pajvani U, Fife K, Spotts JM and Greenberg ME, Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294:333-339 (2001).
Duan JY, Li-Ming DU, Hao WU, Yuan LH and Gang G, Preliminary study of action mechanism of tomatine toxicity to Helicoverpa armigera. Acta Bot Boreali-Occidentalia Sin 26:117-120 (2006).
Iwanaga M, Dohmae N, Fonagy A, Takio K, Kawasaki H, Maeda S et al., Isolation and characterization of calmodulin in the pheromone gland of the silkworm, Bombyx mori. Comp Biochem Phys B 120:761-767 (1998).
Zhou H, Zhang YQ, Lai T, Liu XJ, Guo FY, Guo T et al., Acaricidal mechanism of scopoletin against Tetranychus cinnabarinus. Front Physiol 10:1-17 (2019).
Busvine JR, Recommended methods for measurement of pest resistance to pesticides. Food and Agricultural Organization of the United Nations, Rome (1980).
Zhou H, Zhang YQ, Lai T, Wang D, Liu JL, Guo FY et al., Silencing Chitinase genes increases susceptibility of Tetranychus cinnabarinus (Boisduval) to scopoletin. Biomed Res Int 7:1-13 (2017).
Michel AP, Mian MA, Davila-Olivas NH and Cañas LA, Detached leaf and whole plant assays for soybean aphid resistance: differential responses among resistance sources and biotypes. J Econ Entomol 103:949-957 (2010).
Hill CB, Li Y and Hartman GL, Resistance to the soybean aphid in soybean germplasm. Crop Sci 44:98-106 (2004).
Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ, Stuart JJ et al., Hessian fly-associated bacteria: transmission, essentiality, and composition. PLoS One 6:e23170 (2011).
Tamura K, Peterson D, Peterson N, Stecher G, Nei M and Kumar S, MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739 (2011).
Misener S and Krawetz SA, Bioinformatics Methods and Protocols. Humana Press, Totowa, NJ (2000).
Sun W, Jin Y, He L, Lu WC and Li M, Suitable reference gene selection for different strains and developmental stages of the carmine spider mite, Tetranychus cinnabarinus, using quantitative real-time PCR. J Insect Sci 10:208-208 (2010).
Livak KJ and Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method. Methods 25:402-408 (2001).
He G, Guo F, Zhu T, Shao D, Feng R, Yin D et al., Lobe-related concentration- and Ca2+-dependent interactions of calmodulin with C- and N-terminal tails of the CaV1.2 channel. J Physiol Sci 63:345-353 (2013).
Dedman JR and Kaetzel MA, Calmodulin purification and fluorescent labeling. Method Enzymol 102:1-8 (1983).
Garg UC, Rai N, Singh Y, Dhaunsi GS, Sidhu GS, Ganguly NK et al., A spectrophotometric method for calmodulin assay. Biotechniques 6:294-296 (1988).
Lanzetta PA, Alvarez LJ, Reinach PS and Candia OA, An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100:95-97 (1979).
Benaim G, Zurini M and Carafoli E, Different conformational states of the purified Ca2+-ATPase of the erythrocyte plasma membrane revealed by controlled trypsin proteolysis. J Biol Chem 259:8471-8477 (1984).
Luo JX, Lai T, Guo T, Chen F, Zhang L, Ding W et al., Synthesis and acaricidal activities of scopoletin phenolic ether derivatives: QSAR, molecular docking study and in silico ADME predictions. Molecules 23:995 (2018).
Ao J, Gao L, Yuan T and Jiang G, Interaction mechanisms between organic UV filters and bovine serum albumin as determined by comprehensive spectroscopy exploration and molecular docking. Chemosphere 119:590-600 (2015).
Bhatnagar K and Singh VP, Ca2+ dependence and inhibitory effects of trifluoperazine on plasma membrane ATPase of thermoactinomyces vulgaris. Curr Microbiol 49:28-31 (2004).
Scharff O and Foder B, Effect of trifluoperazine, compound 48/80, TMB-8 and verapamil on the rate of calmodulin binding to erythrocyte Ca2+-ATPase. Biochim Biophys Acta 772:29-36 (1984).
Penniston JT and Enyedi A, Modulation of the plasma membrane Ca2+ pump. J Membr Biol 165:101-109 (1998).
Carafoli E, The calcium pumping ATPase of the plasma membrane. Annu Rev Physiol 53:531-547 (1991).
Krizaj D, Steven JD, Johnson J, Strehler EE and Copenhagen DR, Cell-specific expression of plasma membrane calcium ATPase isoforms in retinal neurons. J Comput Neurol 451:1-21 (2002).
Pottorf WJ and Thayer SA, Transient rise in intracellular calcium produces a long-lasting increase in plasma membrane calcium pump activity in rat sensory neurons. J Neurochem 83:1002-1008 (2002).
Zenisek D and Matthews G, The role of mitochondria in presynaptic calcium handling at a ribbon synapse. Neuron 25:229-237 (2000).
Castillo K, Delgado R and Bacigalupo J, Plasma membrane Ca2+-ATPase in the cilia of olfactory receptor neurons: possible role in Ca2+ clearance. Eur J Neurosci 26:2524-2531 (2007).
Xu X, Chen D, Ye B, Zhong F and Chen G, Curcumin induces the apoptosis of non-small cell lung cancer cells through a calcium signaling pathway. Int J Mol Med 35:1610-1616 (2015).
Wang WH, Chiang IT, Ding K, Chung JG and Hwang JJ, Curcumin-induced apoptosis in human hepatocellular carcinoma J5 cells: critical role of Ca2+-dependent pathway. Evidence-Based Complementary Altern Med 12:512907 (2012).
Bakhshi J, Weinstein L, Poksay KS, Nishinaga B, Bredesen DE and Rao RV, Coupling endoplasmic reticulum stress to the cell death program in mouse melanoma cells: effect of curcumin. Apoptosis 13:904-914 (2008).
Chin D and Means AR, Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322-328 (2000).
Yap K, Ames JB, Swindells MB and Ikura M, Diversity of conformational states and changes within the EF-hand protein superfamily. Proteins 37:499-507 (2015).
Kawasaki H and Kretsinger RH, Structural and functional diversity of EF-hand proteins: evolutionary perspectives. Protein Sci 26:1898-1920 (2017).
Ning W, Zhong X, Song X, Gu X, Lai W, Yue X et al., Molecular and biochemical characterization of calmodulin from Echinococcus granulosus. Parasite Vector 10:597 (2017).
Gulati P, Gaspers LD, Dann SG, Joaquin M, Nobukuni T, Natt F et al., Amino acids activate mTOR Complex1 via Ca2+/CaM signaling to hVps34. Cell Metab 7:456-465 (2008).
Dick IE, Tadross MR, Haoya L, Hock TL, Wanjun Y and Yue DT, A modular switch for spatial Ca2+ selectivity in the calmodulin regulation of CaV channels. Nature 451:830-834 (2008).
Demaria CD, Soong TW, Alseikhan BA, Alvania RS and Yue DT, Calmodulin bifurcates the local Ca2+ signal that modulates P/Q-type Ca2+ channels. Nature 411:484-489 (2001).
Zühlke RD, Pitt GS, Tsien RW and Reuter H, Ca2+-sensitive inactivation and facilitation of L-type Ca2+ channels both depend on specific amino acid residues in a consensus calmodulin-binding motif in the α1C subunit. J Biol Chem 275:21121-21129 (2000).
Xu ZF, Wu Q, Xu Q and He L, Functional analysis reveals glutamate-gated chloride and γ-amino butyric acid channels as targets of avermectins in the carmine spider mite. Toxicol Sci 155:258-269 (2016).
Wei P, Li J, Liu X, Nan C, Shi L, Zhang Y et al., Functional analysis of four up-regulated carboxylesterase genes associated with fenpropathrin resistance in Tetranychus cinnabarinus (Boisduval). Pest Manag Sci 75:252-261 (2018).
Shi XZ, Guo ZJ, Zhu X, Wang SL, Xu BY, Xie W et al., RNA interference of the inhibitory glutamate receptor in Plutella xylostella (Lepidoptera: Plutellidae). Acta Ent Sin 55:1331-1336 (2012).
Rinkevich FD and Scott JG, Limitations of RNAi of α6 nicotinic acetylcholine receptor subunits for assessing the in vivo sensitivity to spinosad. Insect Sci 20:101-108 (2013).
Wan PJ, Guo WY, Yang Y, Lü FG, Lu WP and Li GQ, RNAi suppression of the ryanodine receptor gene results in decreased susceptibility to chlorantraniliprole in Colorado potato beetle Leptinotarsa decemlineata. J Insect Physiol 63:48-55 (2014).
Gary W and Roy J, Post-translational modifications in the context of therapeutic proteins. Nat Biotechnol 24:1241-1252 (2006).
Shen XM, Liao CY, Lu XP, Zhe W, Wang JJ and Wei D, Involvement of three esterase genes from Panonychus citri (McGregor) in fenpropathrin resistance. Int J Mol Sci 17:1-15 (2016).
Gong D, Chi X, Wei J, Zhou G, Huang G, Zhang L et al., Modulation of cardiac ryanodine receptor 2 by calmodulin. Nature 361:1112-1115 (2019).
Hoeflich KP and Ikura M, Calmodulin in action: diversity in target recognition and activation mechanisms. Cell 108:739-742 (2002).
Vandonselaar M, Hickie RA, Quail W and Delbaere LTJ, Trifluoperazine-induced conformational change in Ca2+-calmodulin. Nat Struct Biol 1:795-801 (1994).
Kurokawa H, Osawa M, Kurihara H, Katayama N, Tokumitsu H, Swindells MB et al., Target-induced conformational adaptation of calmodulin revealed by the crystal structure of a complex with nematode Ca2+/calmodulin-dependent kinase kinase peptide. J Mol Biol 312:59-68 (2001).
Fallon JL and Quiocho FA, A closed compact structure of native Ca2+-calmodulin. Structure 11:1303-1307 (2003).
Vertessy BG, Harmat V, Cskei Z, Náray-Szabó G, Orosz F and Ovádi J, Simultaneous binding of drugs with different chemical structures to Ca2+-calmodulin: crystallographic and spectroscopic studies. Biochemistry 37:15300-15310 (1998).
Steiner RF, Albaugh S, Fenselau C, Murphy C and Vestling M, A mass spectrometry method for mapping the interface topography of interacting proteins, illustrated by the melittin-calmodulin system. Anal Biochem 196:120-125 (1991).