Browse > Article
http://dx.doi.org/10.5656/KSAE.2014.08.0.027

Effect of Cellular Phospholipase A2 Inhibition on Enhancement of Bt Insecticidal Activity  

Eom, Seonghyeon (Department of Bioresource Sciences, Andong National University)
Park, Jiyeong (Department of Bioresource Sciences, Andong National University)
Kim, Kunwoo (Department of Bioresource Sciences, Andong National University)
Kim, Yonggyun (Department of Bioresource Sciences, Andong National University)
Publication Information
Korean journal of applied entomology / v.53, no.3, 2014 , pp. 271-280 More about this Journal
Abstract
Some bacterial metabolites of Xenorhabdus nematophila (Xn) inhibit phospholipase $A_2$ ($PLA_2$) activity to shutdown eicosanoid biosynthesis in target insects. However, little has been known about the target insect $PLA_2$ of these bacterial metabolites. Eight bacterial metabolites identified in Xn culture broth exhibited significant insecticidal activities against larvae of both lepidopteran species of Plutella xylostella and Spodoptera exigua. Moreover, these bacterial metabolites significantly enhanced insecticidal activities of Bacillus thuringiensis (Bt). To determine target $PLA_2$, we cloned and over-expressed cellular $PLA_2$ ($SecPLA_2$) of S. exigua. Purified $SecPLA_2$ catalyzed phospholipids derived from the fat body and released several polyunsaturated fatty acids. Most Xn metabolites significantly inhibited $SecPLA_2$ activity, but were different in their inhibitory activities. There was a positive correlation between the inhibition of $SecPLA_2$ and the enhancement of Bt insecticidal activity. These results indicate that $SecPLA_2$ is a molecular target inhibited by Xn metabolite.
Keywords
$cPLA_2$; Eicosanoid; Xenorhabdus nematophila; Bacillus thuringiensis; Immunosuppression;
Citations & Related Records
Times Cited By KSCI : 5  (Citation Analysis)
연도 인용수 순위
1 Shrestha, S., Kim, Y., 2009. Biochemical characteristics of immune-associated phospholipase $A_2$ and its inhibition by an entomopathogenic bacterium, Xenorhabdus nematophila. J. Microbiol. 47, 774-782.   DOI
2 Stanley, D., Kim, Y., 2014. Eicosanoid signaling in insects; from discovery to plant protection. Crit. Rev. Plant Sci. 33, 20-63.   DOI
3 Stanley-Samuelson, D.W., Dadd, R.H., 1981. Arachidonic acid and other tissue fatty acids of Culex pipiens reared with various concentrations of dietary arachidonic acid. J. Insect Physiol. 27, 571-578.   DOI   ScienceOn
4 Park, Y. and Kim, Y. 2003. Xenorhabdus nematophilus inhibits p-bromophenacyl bromide (BPB)-sensitive $PLA_2$ of Spodoptera exigua. Arch. Insect Biochem. Physiol. 54, 143-142.   DOI   ScienceOn
5 Stanley-Samuelson, D.W., Dadd, R.H., 1983. Long-chain polyunsaturated fatty acids: patterns of occurrence in insects. Insect Biochem. 13, 549-588.   DOI   ScienceOn
6 Uozumi, N., Kume, K., Nagase, T., Nakatani, N., Ishii, S., Tashiro, F., Komagata, Y., Maki, K., Ikuta, K., Ouchi, Y., Miyazaki, J., Shimizu, T., 1997. Role of cytosolic phospholipase $A_2$ in allergic response and parturition. Nature 390, 618-622.   DOI   ScienceOn
7 Zhang, X., Candas, M., Griko, N.B., Taussig, R., Bulla, L.A., Jr., 2006. A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc. Natl. Acad. Sci. USA 103, 9897-9902.   DOI   ScienceOn
8 Park, Y., Kim, Y., 2005. Inhibitory effect of an entomopathogenic bacterium, Xenorhabdus nematophila, on the release of arachidonic acid from the membrane preparation of Spodoptera exigua. J. Asia Pac. Entomol. 8, 61-67.   과학기술학회마을   DOI
9 Park, Y., Kim, Y., 2013. RNA interference of cadherin gene expression in Spodoptera exigua reveals its significance as a specific Bt target. J. Invertebr. Pathol. 114, 285-291.   DOI   ScienceOn
10 Park, Y., Kim, Y., Stanley, D., 2004a. The bacterium Xenorhabdus nematophila inhibits phospholipase $A_2$ from insect, prokaryote, and vertebrate sources. Naturwissenschaften 91, 371-373.
11 Park, Y., Kim, Y., Tunaz, H., Stanley, D.W., 2004b. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits hemocytic phospholipase $A_2$ ($PLA_2$) in tobacco hornworm, Manduca sexta. J. Invertebr. Pathol. 86, 65-71.   DOI   ScienceOn
12 SAS Institute, Inc. 1989. SAS/STAT user's guide, release 6.03, Ed. Cary, N.C.
13 Roh, J.Y., Choi, J.Y., Li, M.S., Jin, B.R., Je, Y.H., 2007. Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J. Microbiol. Biotechnol. 17, 547-559.
14 Radvanyi, F., Jordan, L., Russo-Marie, F., Bon, C., 1989. A sensitive and continuous fluorometric assay for phospholipase $A_2$ using pyrene-labeled phospholipids in the presence of serum albumin. Anal. Biochem. 177, 103-109.   DOI   ScienceOn
15 Rahman, M.M., Roberts, H.L.S., Sarjan, M., Asgari, S., Schmidt, O., 2004. Induction and transmission of Bacillus thuringiensis tolerance in the flour moth Ephestia kuehniella. Proc. Natl. Acad. Sci. USA 101, 2696-2699.   DOI   ScienceOn
16 Richards, E.H., Dani, M.P., 2010. A recombinant immunosuppressive protein from Pimpla hypochondriaca (rVPr1) increases the susceptibility of Lacanobia oleracea and Mamestra brassicae larvae to Bacillus thuringiensis. J. Invertebr. Pathol. 104, 51-57.   DOI   ScienceOn
17 Schaloske, R.H., Dennis, E.A., 2006. The phospholipase $A_2$ superfamily and its group numbering system. Biochim. Biophys. Acta 61, 1246-1259.
18 Seo, S., Kim, Y., 2010. Study on development of novel biopesticides using entomopathogenic bacterial culture broth of Xenorhabdus and Photorhabdus. Kor. J. Appl. Entomol. 49, 241-249.   과학기술학회마을   DOI
19 Seo, S., Lee, S., Hong, Y., Kim, Y., 2012. Phospholipase $A_2$ inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp. temperata. Appl. Environ. Entomol. 78, 3816-3823.   DOI
20 Shrestha, S., Hong, Y., Kim, Y., 2010. Two chemical derivatives of metabolites suppress cellular immune responses and enhance pathogenicity of Bacillus thuringiensis against the diamondback moth, Plutella xylostella. J. Asia Pac. Entomol. 13, 55-60.   과학기술학회마을   DOI   ScienceOn
21 Bravo, A., Gomez, I., Porta, H., Garcia-Gomez, B.I., Rodriguez- Almazan, C., Pardo, L., Soberon, M., 2012. Evolution of Bacillus thuringiensis Cry toxins insecticidal activity. Microbial Biotechnol. 6, 17-26.
22 Akhurst, R.J., 1980. Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J. Gen. Microbiol. 121, 303-309.
23 Broderick, N.A., Raffa, K.F., Handelsman, J., 2010. Chemical modulators of the innate immune response alter gypsi moth larval susceptibility to Bacillus thuringiensis. BMC Microbiol. 10, 129.   DOI   ScienceOn
24 Blomquist, G.J., Borgeson, C.E., Vundla, M., 1991. Polyunsaturated fatty acids and eicosanoids in insects. Insect Biochem. 21, 99-106.   DOI   ScienceOn
25 Bravo, A., Likitvivatanavong, S., Gill, S.S., Soberon, M., 2011. Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem. Mol. Biol. 41, 423-431.   DOI   ScienceOn
26 Broderick, N.A., Raffa, K.F., Handelsman, J., 2006. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl. Acad. Sci. USA 103, 15196-15199.   DOI   ScienceOn
27 Burke, J.E., Dennis, E.A., 2009. Phospholipase $A_2$ structure/function, mechanism, and signaling. J. Lipid Res. 50, 5237-5242.
28 Christie, W.W., 2003. Lipid analysis, in: Christie, W.W. (Ed.), Isolation, separation, identification and structural analysis of lipids. The Oily Press, Bridgewater, UK, pp. 373-387.
29 Darboux, I., Pauchet, Y., Castella, C., Silva-Filha, M.H., Nielsen-LeRoux, C., Charles, J.F., Pauron, D., 2002. Loss of the membrane anchor of the target receptor is a mechanism of bioinsecticide resistance. Proc. Natl. Acad. Sci. USA 99, 5830-5835.   DOI   ScienceOn
30 Crickmore, N., Zeigler, D.R., Feitelson, J., Schnepf, E., Van Rie, J., Lereclus, D., 1998. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 807-813.
31 Eom, S., Park, Y., Kim, Y., 2014. Sequential immunosuppressive activities of bacterial secondary metabolites from the entomopathogenic bacterium, Xenorhabdus nematophila. J. Microbiol. 52, 161-168.   DOI   ScienceOn
32 Crickmore, N., Baum, J., Bravo, A., Lereclus, D., Narva, K, Sampson, K., Schnepf, E., Sun, M., Zeigler, D.R., 2014. 'Bacillus thuringiensis toxin nomenclature'. http://www.btnomenclature.info.
33 Cripps, C., Borgeson, C., Blomquist, G.J., de Renobales, M., 1990. The $\Delta^{12}$ desatuase from the house cricket Acheta domesticus (Orthoptera: Gryllidae): Characterization and form of substrate. Arch. Biochem. Biophys. 278, 46-51.   DOI   ScienceOn
34 Dubovskiy, I.M., Krukova, N.A., Glupov, V.V., 2008. Phagocytic activity and encapsulation rate of Galleria mellonella larval haemocytes during bacterial infection by Bacillus thuringiensis. J. Invertebr. Pathol. 98, 360-362.   DOI   ScienceOn
35 ffrench-Constant, R.H., Waterfield, N., Daborn, P., 2005. Insecticidal toxins from Photorhabdus and Xenorhabdus. in: Gilbert, L.I., Iatrou, K., Gill, S.S., (Eds.), Comprehensive molecular insect science. Elsevier, New York, pp. 239-253.
36 Folch, J., Lees, M., Stanley, G.H.S., 1957. A simple method for the isolation and purification of total lipid from animal tissue. J. Biol. Chem., 226, 497-509.
37 Gahan, L.J., Gould, F., Heckel, D.G., 2001. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293, 857-860.   DOI   ScienceOn
38 Hwang, J., Park, Y., Kim, Y., 2013. An entomopathogenic bacterium, Xenorhabdus nematophila, suppresses expression of antimicrobial peptides controlled by Toll and IMD pathways by blocking eicosanoid biosynthesis. Arch. Insect Biochem. Physiol. 83, 151-169.   DOI   ScienceOn
39 Goh, H.G., Lee, S.G. Lee, B.P., Choi, G.M., Kim, J.H., 1990. Simple mass-rearing of beet armyworm, Spodoptera exigua. Kor. J. Appl. Entomol. 29, 180-183.   과학기술학회마을
40 Garbutt, J., Bonsall, M.B., Wright, D.J., Raymond, B., 2011. Antagonistic competition moderates virulence in Bacillus thuringiensis. Ecol. Lett. 14, 765-772.   DOI   ScienceOn
41 Grizanova, E.V., Dubovskiy, I.M., Whitten, M.M.A., Glupov, V.V., 2014. Contributions of cellular and humoral immunity of Galleria mellonella larvae in defence against oral infection by Bacillus thuringiensis. J. Invertebr. Pathol. 119, 40-46.   DOI   ScienceOn
42 Jung, S., Kim, Y., 2006. Synergistic effect of entomopathogenic bacteria (Xenorhabdus sp. and Photorhabdus temperata ssp. temperata) on the pathogenicity of Bacillus thuringiensis ssp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Environ. Entomol. 35, 1584-1589.   DOI   ScienceOn
43 Jurenka, R.A., Stanley-Samuelson, D.W., Loher, W., Blomquist, G.J., 1988. De novo biosynthesis of arachidonic acid and 5,11,14-eicosatrienoic acid in the cricket Teleogryllus commodus. Biochim. Biophys. Acta 963, 21-27.   DOI   ScienceOn
44 Kaya, H.K., Gaugler, R., 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38, 181-206.   DOI   ScienceOn
45 Kim, Y., D. Ji, S. Cho and Y. Park. 2005. Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase $A_2$ to induce host immunodepression. J. Invertebr. Physiol. 89, 258-264.   DOI   ScienceOn
46 Metcalfe, L.D., Schmitz, A.A., 1961. The rapid preparation of fatty acid esters for gas chromatographic analysis. Anal. Chem. 33, 363-364.   DOI
47 Martinez-Ramirez, A.C., Gould, F., Ferre, J., 1999. Histopathological effects and growth reduction in a susceptible and a resistant strain of Heliothis virescens (Lepidoptera: Noctuidae) caused by sublethal doses of pure Cry1A crystal proteins from Bacillus thuringiensis. Biocontrol Sci. Technol. 9, 239-246.   DOI
48 Kwon, S., Kim, Y., 2007. Immunosuppressive action of pyriproxyfen, a juvenile hormone analog, enhances pathogenicity of Bacillus thuringiensis subsp. kurstaki against diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Biol. Control 42, 72-76.   DOI   ScienceOn
49 Ma, G., Roberts, H., Sarjan, M., Featherstone, N., Lahnstein, J., Akhurst, R., Schmidt, O., 2005. Is the mature endotoxin Cry1Ac from Bacillus thuringiensis inactivated by a coagulation reaction in the gut lumen of resistant, Helicoverpa armigera larvae? Insect Biochem. Mol. Biol. 35, 729-739.   DOI   ScienceOn
50 Oppert, B., Kramer, K.J., Johnson, D.E., Macintosh, S.C., Mcgaughey, W.H., 1994. Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpunctella. Biochem. Biophys. Res. Commun. 198, 940-947.   DOI   ScienceOn
51 Park, Y., Kim, Y., 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophila, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J. Insect Physiol. 46, 1469-1476.   DOI   ScienceOn
52 de Maagd, R.A., Bravo, A., Crickmore, N., 2001. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. 17, 193-199.   DOI   ScienceOn
53 Jurenka, R.A., de Renobales, M., Blomquist, G.J., 1987. De novo biosynthesis of polyunsaturated fatty acids in the cockroach, Periplaneta americana. Arch. Biochem. Biophys. 255, 184-193.   DOI   ScienceOn
54 Bravo, A., Gill, S.S., Soberon, M., 2005. Bacillus thuringiensis mechanisms and use, in: Gilbert, L.I., Iatrou, K., Gill, S.S., (Eds.), Comprehensive molecular insect science. Elsevier, New York, pp. 175-206.