Korean journal of applied entomology (한국응용곤충학회지)

Korean Society of Applied Entomology (한국응용곤충학회)
권호 표지
DOI QR코드

DOI QR Code

Molecular Action of Prostaglandin to Mediate Insect Immunity and Its Application to Develop Novel Insect Control Techniques

곤충 면역반응을 중개하는 프로스타글란딘의 분자적 기작과 해충방제 응용

  • Kim, Yonggyun (Department of Plant Medicals, College of Life Sciences, Andong National University)
  • 김용균 (안동대학교 생명과학대학 식물의학과)
  • Received : 2021.12.30
  • Accepted : 2022.02.04
  • Published : 2022.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Like vertebrates, insects synthesize various eicosanoids after the committed catalytic step of phospholipase A2 (PLA2). However, the subsequent biosynthetic steps exhibit some deviation from those of vertebrates. Due to little composition of arachidonic acid in insect phospholipids, PLA2 releases linoleic acid, which is another polyunsaturated fatty acid and relatively rich in insect phospholipids, to synthesize arachidonic acid via chain extension and desaturation. Resulting arachidonic acid is then oxygenated into a prostaglandin (PG), PGH2, by a specific peroxidase called peroxynectin, but not by cyclooxygenase. PGH2 is then isomerized to various PGs such as PGA2, PGD2, PGE2, PGI2, and a thromboxane (TXB2). All four epoxyeicosatrienoic acids such as 5,6-EET, 8,9-EET, 11,12-EET, and 14,15-EET are also synthesized from arachidonic acid by oxygenation of vertebrate types of monooxygenases. However, the other type of eicosanoids called leukotrienes are found in insect tissues but their synthetic pathway is unclear. Eicosanoids mediate various insect physiological processes such as metabolism, excretion, immunity, and reproduction. Thus, identification of novel compounds interrupting eicosanoid biosynthesis would be a novel approach to develop insecticides. This review focuses on PGs and their immune mediation.

척추동물과 유사하게 곤충도 인지질분해효소(phospholipase A2)의 촉매 작용으로 다양한 아이코사노이드를 합성한다. 그러나 일련의 아이코사노이드 생합성과정은 척추동물과 차이를 보이는데, 이는 곤충의 인지질에는 전구물질인 아라키도닉산의 함량이 낮기 때문이다. 대신에 비교적 풍부하게 존재하는 다가불포화지방산인 리놀레익산을 기반으로 사슬 연장 및 불포화반응으로 아라키도닉산을 합성하여 척추동물과 같이 아이코사노이드 전구물질로 이용하는 것 같다. 이렇게 해서 형성된 아라키도닉산은 다시 척추동물의 cyclooxygenase와 유사한 peroxynectin이 PGH2 형태의 프로스타글란딘(prostaglandin: PG) 전구물질을 형성하게 된다. 이후 여러 이성체 효소들의 특이적 반응에 의해 PGA2, PGD2, PGE2, PGI2, TXB2의 다양한 PG가 생성된다. 반면에 또 다른 형태의 아이코사노이드인 에폭시아이코사트리에노익산(epoxyeicosatrienoic acid: EET)은 척추동물과 유사한 단일산화효소의 산화반응으로 아라키도닉산을 전구물질로 5,6-EET, 8,9-EET, 11,12-EET, 14,15-EET를 형성하게 된다. 그러나 세 번째 아이코사노이드 부류인 류코트리엔(leukotriene)의 경우 곤충 체내 존재는 확인되었지만 생합성 과정은 아직 밝혀지지 않았다. 이들 아이코사노이드가 곤충의 대사, 배설, 면역 및 생식에 관여하는 생리작용을 중개한다. 따라서 아이코사노이드 생합성 과정을 교란하는 물질 탐색은 새로운 살충제 개발 전략이 된다. 본 종설은 이 가운데 PG의 곤충 면역 중개 기작을 소개한다.

Keywords

Acknowledgement

저자가 곤충생리학 학문 분야에 첫걸음을 내딛는 데 바르게 지도하여 주신 부경생 교수님께 본 종설 논문 작성을 통해 깊은 감사와 그리움을 전합니다. 이 논문은 안동대학교 기본연구지원사업에 의하여 지원되었다.

References

  1. Ahmed, S., Kim, Y., 2019. PGE2 mediates cytoskeletal rearrangement of hemocytes via Cdc42, a small G protein, to activate actin-remodeling factors in Spodoptera exigua (Lepidoptera: Noctuidae). Arch. Insect Biochem. Physiol. 102, e21607. https://doi.org/10.1002/arch.21607
  2. Ahmed, S., Kim, Y., 2020. Prostaglandin catabolism in Spodoptera exigua, a lepidopteran insect. J. Exp. Biol. 223, jeb233221. https://doi.org/10.1242/jeb.233221
  3. Ahmed, S., Kim, Y., 2021. PGE2 mediates hemocyte-spreading behavior by activating aquaporin via cAMP and rearranging actin cytoskeleton via Ca2+. Dev. Comp. Immunol. 125, 104230. https://doi.org/10.1016/j.dci.2021.104230
  4. Ahmed, S., Stanley, D., Kim, Y., 2018. An insect prostaglandin E2 synthase acts in immunity and reproduction. Front. Physiol. e01231.
  5. Ahmed, S., Hasan, A., Kim, Y., 2019. Overexpression of PGE2 synthase by in vivo transient expression enhances immunocompetency along with fitness cost in a lepidopteran insect. J. Exp. Biol. 222, jeb207019. https://doi.org/10.1242/jeb.207019
  6. Ahmed, S., Al Baki, M.A., Lee, J., Seo, D.Y., Lee, D., Kim, Y., 2021. The first report of prostacyclin and its physiological roles in insects. Gen. Comp. Endocrinol. 301, 113659. https://doi.org/10.1016/j.ygcen.2020.113659
  7. Al Baki, M.A., Roy, C.M., Lee, D.H., Stanley, D., Kim, Y., 2021. The prostanoids, thromboxanes, mediate hemocytic immunity to bacterial infection in the lepidopteran Spodoptera exigua. Dev. Comp. Immunol. 120, 104069. https://doi.org/10.1016/j.dci.2021.104069
  8. Amiri-Besheli, B., Khambay, B., Cameron, S., Deadman, M., Butt, T.M., 2000. Inter- and intra-specific variation in destruxin production by the insect pathogenic Metarhizium, and its significance to pathogenesis. Mycol. Res. 104, 447-452. https://doi.org/10.1017/S095375629900146X
  9. Baines, D., Desantis, T., Downer, R.G.H., 1992. Octopamine and 5-hydroxytryptamine enhance the phagocytic and nodule formation activities of cockroach (Periplaneta americana) haemocytes. J. Insect Physiol. 38, 905-914. https://doi.org/10.1016/0022-1910(92)90102-J
  10. Barletta, A.B.F., Trisnadi, N., Ramirez, J.L., Barillas-Mury, C., 2019. Mosquito midgut prostaglandin release establishes systemic immune priming. iScience 19, 54-62. https://doi.org/10.1016/j.isci.2019.07.012
  11. Benfarhat-Touzri, D., Ben Amira, A., Ben khedher, S., Givaudan, A., Jaoua, S., Tounsi, S., 2014. Combinatorial effect of Bacillus thuringiensis kurstaki and Photorhabdus luminescens against Spodoptera littoralis (Lepidoptera: Noctuidae). J. Basic Microbiol. 54, 1160-1165. https://doi.org/10.1002/jobm.201300142
  12. Bergstrom, S., Ryhage, R., Samuelsson, B., Sjovall, J., 1962. The structure of prostaglandin E, F1 and F2. Acta Chem. Scandin. 16, 501-502. https://doi.org/10.3891/acta.chem.scand.16-0501
  13. Borkman, M., Storlien, L.H., Pan, D.A., Jenkins, A.B., Chisholm, D.J., Campbell, L.V., 1993. The relation between insulin sensitivity and the fatty-acid composition of skeletal-muscle phospholipids. N. Engl. J. Med. 328, 238-244. https://doi.org/10.1056/NEJM199301283280404
  14. Bouarab, K., Adas, F., Gaquerel, E., Kloareg, B., Salaun, J.P., Potin, P., 2004. The innate immunity of a marine red alga involves oxylipins from both the eicosanoid and octadecanoid pathways. Plant Physiol. 135, 1838-1848. https://doi.org/10.1104/pp.103.037622
  15. Braune, S., Kupper, J.H., Jung, F., 2020. Effect of prostanoids on human platelet function: an overview. Int. J. Mol. Sci. 21, 9020. https://doi.org/10.3390/ijms21239020
  16. Clark, K.D., Pech, L.L., Strand, M.R., 1997. Isolation and identification of a plasmatocyte-spreading peptide from the hemolymph of the lepidopteran insect Pseudoplusia includens. J. Biol. Chem. 272, 23440-23447. https://doi.org/10.1074/jbc.272.37.23440
  17. Clem, R.J., 2005. The role of apoptosis in defense against baculovirus infection in insects. Curr. Top. Microbiol. Immunol. 289, 113-129.
  18. Davidson, F.F., Dennis, E.A., 1990a. Amino acid sequence and circular dichroism of Indian cobra (Naja naja naja) venom acidic phospholipase A2. Biochim. Biophys. Acta 1037, 7-15. https://doi.org/10.1016/0167-4838(90)90095-W
  19. Davidson, F.F., Dennis, E.A., 1990b. Evolutionary relationships and implications for the regulation of phospholipase A2 from snake venom to human secreted forms. J. Mol. Evol. 31, 228-238. https://doi.org/10.1007/BF02109500
  20. Dennis, E.A., 1994. Diversity of group types, regulation, and function of phospholipase A2. J. Biol. Chem. 269, 13057-13060. https://doi.org/10.1016/S0021-9258(17)36794-7
  21. Dudler, T., Chen, W.Q., Wang, S., Schneider, T., Annand, R.R., Dempcy, R.O., Crameri, R., Gmachl, M., Suter, M., Gelb, M.H., 1992. High-level expression in Escherichia coli and rapid purification of enzymatically active honey bee venom phospholipase A2. Biochim. Biophys. Acta 1165, 201-210. https://doi.org/10.1016/0005-2760(92)90188-2
  22. Eom, S., Park, Y., Kim, H., Kim, Y., 2014. Development of a high efficient "Dual Bt-Plus" insecticide using a primary form of an entomopathogenic bacterium, Xenorhabdus nematophila. J. Microbiol. Biotechnol. 24, 507-521. https://doi.org/10.4014/jmb.1310.10116
  23. Ferre, J., Real, M.D., van Rie, J., Jansens, S., Peferoen, M., 1991. Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in a midgut membrane receptor. Proc. Natl. Acad. Sci. U. S. A. 88, 5119-5123. https://doi.org/10.1073/pnas.88.12.5119
  24. Frappier, F., Ferron, P., Pais, M., 1975. Chimie des champignons entomopathogenes - le beauvellide, nouveau cyclodepsipeptide isole d'un Beauveria tenella. Phytochemistry 14, 2703-2705. https://doi.org/10.1016/0031-9422(75)85254-X
  25. Gillespie, J.P., Kanost, M.R., Trenczek, T., 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42, 611-643. https://doi.org/10.1146/annurev.ento.42.1.611
  26. Goettel, M.S., Eilenberg, J., Glare, T., 2005. Entomopathogenic fungi and their role in regulaion of insect populations. in: Gilbert, L.I., Iatrou, K., Gill, S.S. (Eds.), Comprehensive Mol Insect Science, vol 6, Elsevier, New York, pp 361-405.
  27. Groen, C.M., Jayo, A., Parsons, M., Tootle, T.L., 2015. Prostaglandins regulate nuclear localization of Fascin and its function in nucleolar architecture. Mol. Biol. Cell. 26, 1901-1917. https://doi.org/10.1091/mbc.E14-09-1384
  28. Hajek, A.E., St. Leger, R.J., 1994. Interactions between fungal pathogens and insect hosts. Annu. Rev. Entomol. 39, 293-322. https://doi.org/10.1146/annurev.en.39.010194.001453
  29. Hamill, R.L., Higgens, C.E., Boaz, H.E., Gorman, M., 1969. The structure of beauvericin, a new depsipeptide antibiotic toxic to Artemia salina. Tetrahed. Lett. 49, 4255-4258.
  30. Han, G.D., Na, J., Chun, Y.S., Kumar, S., Kim, W., Kim, Y., 2017. Chlorine dioxide enhances lipid peroxidation through inhibiting calcium-independent cellular PLA2 in larvae of the Indianmeal moth, Plodia interpunctella. Pestic. Biochem. Physiol. 143, 48-56. https://doi.org/10.1016/j.pestbp.2017.09.010
  31. Hasan, Shabbir, A., Kim, Y. 2019. Biosynthetic pathway of arachidonic acid in Spodoptera exigua in response to bacterial challenge. Insect Biochem. Mol. Biol. 111, 103179. https://doi.org/10.1016/j.ibmb.2019.103179
  32. Herrero, S., Ansems, M., Van Oers, M.M., Vlak, J.M., Bakker, P.L., de Maagd, R.A., 2007. REPAT, a new family of proteins induced by bacterial toxins and baculovirus infection in Spodoptera exigua. Insect Biochem. Mol. Biol. 37, 1109-1118. https://doi.org/10.1016/j.ibmb.2007.06.007
  33. Hrithik, T.H., Vatanparast, M., Ahmed, S., Kim, Y., 2021. Repat33 acts as a downstream component of eicosanoid signaling pathway mediating immune responses of Spodoptera exigua, a lepidopteran insect. Insects 12, 449. https://doi.org/10.3390/insects12050449
  34. Imler, J.L., Bulet, P., 2005. Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem. Immunol. Allergy 86, 1-21. https://doi.org/10.1159/000086648
  35. Ishibashi, K., 2006. Aquaporin subfamily with unusual NPA boxes. Biochem. Biophy. Acta 1758, 989-993. https://doi.org/10.1016/j.bbamem.2006.02.024
  36. Jallouli, W., Boukedi, H., Sellami, S., Frikha, F., Abdelkefi-Mesrati, L., Tounsi, S., 2018. Combinatorial effect of Photorhabdus luminescens TT01 and Bacillus thuringiensis Vip3Aa16 toxin against Agrotis segetum. Toxicon. 142, 52-57. https://doi.org/10.1016/j.toxicon.2017.12.054
  37. Jeffs, L.B., Khachatourians, G.G., 1997. Toxic properties of Beauveria pigments on erythrocyte membranes. Toxicon. 35, 1351-1356. https://doi.org/10.1016/S0041-0101(97)00025-1
  38. Ji, D., Yi, Y., Kim, G.H., Choi, Y.H., Kim, P., Baek, N.I., Kim, Y., 2004. Identification of an antibacterial compound, benzylideneacetone, from Xenorhabdus nematophila against major plant-pathogenic bacteria. FEMS Microbiol. Lett. 239, 241-248. https://doi.org/10.1016/j.femsle.2004.08.041
  39. Jiang, H., Kanost, M.R., 2000. The clip-domain family of serine proteinases in arthropods. Insect Biochem. Mol. Biol. 30, 95-105. https://doi.org/10.1016/S0965-1748(99)00113-7
  40. Jung, S., Kim, Y., 2006a. 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. https://doi.org/10.1603/0046-225X(2006)35[1584:SEOEBX]2.0.CO;2
  41. Jung, S., Kim, Y., 2006b. Synergistic effect of Xenorhabdus nematophila K1 and Bacillus thuringiensis subsp. aizawai against Spodoptera exigua (Lepidoptera: Noctuidae). Biol. Control. 39, 201-209. https://doi.org/10.1016/j.biocontrol.2006.07.002
  42. Jung, S., Kwoen, M., Choi, J.M., Je, Y.H., Kim, Y., 2006. Parasitism of Cotesia spp. enhances susceptibility of Plutella xylostella to other pathogens. J. Asia Pac. Entomol. 9, 255-263. https://doi.org/10.1016/S1226-8615(08)60300-3
  43. Jung, J., Sajjadian, S.M, Kim, Y., 2019. Hemolin, an immunoglobulin-like peptide, opsonizes nonself targets for phagocytosis and encapsulation in Spodoptera exigua, a lepidopteran insect. J. Asia Pac. Entomol. 22, 947-956. https://doi.org/10.1016/j.aspen.2019.08.002
  44. Kanost, M.R., Jiang, H., Yu, X.Q., 2004. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev. 198, 97-105. https://doi.org/10.1111/j.0105-2896.2004.0121.x
  45. Kim, Y., Stanley, D., 2021. Eicosanoid signaling in insect immunology: new genes and unresolved issues. Genes 12, 211. https://doi.org/10.3390/genes12020211
  46. Kim, G., Madanagopal, N., Lee, D., Kim, Y., 2009. Octopamine and 5-hydroxytryptamine mediate hemocytic phagocytosis and nodule formation via eicosanoids in the beet armyworm, Spodoptera exigua. Arch. Insect Biochem. Physiol. 70, 162-176. https://doi.org/10.1002/arch.20286
  47. Kim, Y., Lee, S., Seo, S., Kim, K., 2016. Fatty acid composition of different tissues of Spodoptera exigua larvae and a role of cellular phospholipase A2. Korean J. Appl. Entomol. 55, 129-138. https://doi.org/10.5656/KSAE.2016.04.0.011
  48. Kim, Y.. Stanley, D., Ahmed, S., An, C., 2018a. Eicosanoid-mediated immunity in insects. Dev. Comp. Immunol. 83, 130-143. https://doi.org/10.1016/j.dci.2017.12.005
  49. Kim, H., Choi, D., Jung, J., Kim, Y., 2018b. Eicosanoid mediation of immune responses at early bacterial infectin stage and its inhibition by Photorhabdus temperata subsp. temperata, an entomopathogenic bacterium. Arch. Insect Biochem. Physiol. 99, e21502. https://doi.org/10.1002/arch.21502
  50. Kim, Y., Ahmed, S., Al Baki, M.A., Kumar, S., Kim, K., Park, Y., Stanley, D., 2020. Deletion mutant of PGE2 receptor using CRISPR-Cas9 exhibits larval immunosuppression and adult infertility in a lepidopteran insect, Spodoptera exigua. Dev. Comp. Immunol. 111, 103743. https://doi.org/10.1016/j.dci.2020.103743
  51. Kodaira, Y., 1961. Biochemical studies on the muscardine fungi in the silkworms, Bombyx mori. J. Fac. Text. Sci. Technol. Sinshu Uni. Sericult. 5, 1-68.
  52. Kramer, R.M., Hession, C., Johansen, B., Hayes, G., McGray, P., Chow, E.P., Tizard, R., Pepinsky, R.B., 1989. Structure and properties of a human non-pancreatic phospholipase A2. J. Biol. Chem. 264, 5768-5775. https://doi.org/10.1016/S0021-9258(18)83616-X
  53. Krasnoff, S.B., Gupta, S., 1994. Identification of the antibiotic phomalactone from the entomopathogenic fungus Hirsutella thompsonii var. synnematosa. J. Chem. Ecol. 20, 293-302. https://doi.org/10.1007/BF02064437
  54. Krasnoff, S.B., Gupta, S., St. Leger, R.J., Renwick, J.A., Roberts, D.W., 1991. Antifungal and insecticidal properties of efrapeptins: metabolites of the fungus Tolypocladium niveum. J. Invertebr. Pathol. 58, 180-188. https://doi.org/10.1016/0022-2011(91)90062-U
  55. Kwon, H., Yang, Y., Kumar, S., Lee, D.W., Bajracharya, P., Calkins, T.L., Kim, Y., Pietrantonio, P.V., 2020. Characterization of the first insect prostaglandin (PGE2) receptor: MansePGE2R is expressed in oenocytoids and lipoteichoic acid (LTA) increases transcript expression. Insect Biochem. Mol. Biol. 117, 103290. https://doi.org/10.1016/j.ibmb.2019.103290
  56. Kwon, H., Hall, D.R., Smith, R.C., 2021. Prostaglandin E2 signaling mediates oenocytoid immune cell function and lysis, limiting bacteria and Plasmodium oocyst survival in Anopheles gambiae. Front. Immunol. 12, 680020. https://doi.org/10.3389/fimmu.2021.680020
  57. Lavine, M.D., Strand, M.R., 2002. Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 32, 1295-1309. https://doi.org/10.1016/S0965-1748(02)00092-9
  58. Lee, K.A., Kim, S.H., Kim, E.K., Ha, E.M., You, H., Kim, B., Kim, M.J., Kwon, Y., Ryu, J.H., Lee, W.J., 2013. Bacterial-derived uracil as a modulator of mucosal immunity and gut-microbe homeostasis in Drosophila. Cell 153, 797-811. https://doi.org/10.1016/j.cell.2013.04.009
  59. Lee, S.J., Yang, Y.T., Kim, S., Lee, M.R., Kim, J.C., Park, S.E., Hossain, M.S., Shin, T.Y., Nai, Y.S., Kim, J.S., 2019. Transcriptional response of bean bug (Riptortus pedestris) upon infection with entomopathogenic fungus, Beauveria bassiana JEF-007. Pest Manag. Sci. 75, 333-345. https://doi.org/10.1002/ps.5117
  60. Lemaitre, B., Hoffmann, J., 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697-743. https://doi.org/10.1146/annurev.immunol.25.022106.141615
  61. Loeb, M.J., Martin, P.A., Hakim, R.S., Goto, S., Takeda, M., 2001. Regeneration of cultured midgut cells after exposure to sublethal doses of toxin from two strains of Bacillus thuringiensis. J. Insect Physiol. 47, 599-606. https://doi.org/10.1016/S0022-1910(00)00150-5
  62. Ma, G., Roberts, H., Sarjan, M., Featherstone, N., Lahnstein, J., Akhust, R., Schmidt, O.. 2005. Is the mature endotoxin Cry1Ac from Bacillus thuringiensis inactivated by a coagulation reaction in the gut lumen of resistant Heliocoverpa armigera larvae? Insect Biochem. Mol. Biol. 35, 729-739. https://doi.org/10.1016/j.ibmb.2005.02.011
  63. Mastore, M., Caramella, S., Quadroni, S., Brivio, M.F., 2021. Drosophila suzukii susceptibility to the oral administration of Bacillus thuringiensis, Xenorhabdus nematophila and its secondary metabolites. Insects 12, 635. https://doi.org/10.3390/insects12070635
  64. Matha, V., Weiser, J., Olejnicek, J., 1988. The effect of tolypin in Tolypocladium niveum crude extract against mosquito and blackfly larvae in the laboratory. Folia Parasitol. 35, 381-383.
  65. Mazet, I., Vey, A., 1995. Hirsutellin A, a toxic protein produced in vitro by Hirsutella thompsonii. Microbiol. Reading 141, 1343-1348. https://doi.org/10.1099/13500872-141-6-1343
  66. Merchant, D., Ertl, R.L., Rennard, S.I., Stanley, D.W., Miller, J.S., 2008. Eicosanoids mediate insect hemocyte migration. J. Insect Physiol. 54, 215-221. https://doi.org/10.1016/j.jinsphys.2007.09.004
  67. Miller, J.S., 2005. Eicosanoids influence in vitro elongation of plasmatocytes from the tobacco hornworm, Manduca sexta. Arch. Insect Biochem. Physiol. 59, 42-51. https://doi.org/10.1002/arch.20052
  68. Mollah, M.M.I., Kim, Y., 2020. Virulent secondary metabolites of entomopathogenic bacteria genera, Xenorhabdus and Photorhabdus, inhibit phospholipase A2 to suppress host insect immunity. BMC Microbiol. 20, 359. https://doi.org/10.1186/s12866-020-02042-9
  69. Mollah, M.M.I., Dekebo, A., Kim, Y., 2020. Immunosuppressive activities of novel PLA2 inhibitors from Xenorhabdus hominickii, an entomopathogenic bacterium. Insects 11, 505. https://doi.org/10.3390/insects11080505
  70. Morishima, I., Yamano, Y., Inoue, K., Matsuo, N., 1997. Eicosanoids mediate induction of immune genes in the fat body of the silkworm, Bombyx mori. FEBS Lett. 419, 83-86. https://doi.org/10.1016/S0014-5793(97)01418-X
  71. Omoto, C., McCoy, C.W., 1998. Toxicity of purified fungal toxin hirsutellin A to the citrus rust mite Phyllocoprura oleivora. J. Invertebr. Pathol. 72, 319-322. https://doi.org/10.1006/jipa.1998.4813
  72. Ovchinnikov, Y.A., Ivanov, V.T., Mikhaleva, I.I., 1971. The synthesis and some properties of beauvericin. Tetrahed. Lett. 2, 159-162. https://doi.org/10.1016/S0040-4039(01)96385-3
  73. 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. https://doi.org/10.1016/S0022-1910(00)00071-8
  74. Park, J., Kim, Y., 2011. Benzylideneacetone suppresses both cellular and humoral immune responses of Spodoptera exigua and enhances fungal pathogenicity. J. Asia Pac. Entomol. 14, 423-427. https://doi.org/10.1016/j.aspen.2011.06.001
  75. Park, J., Kim, Y., 2012. Change in hemocyte populations of the beet armyworm, Spodoptera exigua, in response to bacterial infection and eicosanoid mediation. Korean J. Appl. Entomol. 51, 349-356. https://doi.org/10.5656/KSAE.2012.09.0.038
  76. Park, J., Stanley, D., Kim, Y. 2013. Rac1 mediates cytokine-stimulated hemocyte spreading via prostaglandin biosynthesis in the beet armyworm, Spodoptera exigua. J. Insect Physiol. 59, 682-689. https://doi.org/10.1016/j.jinsphys.2013.04.012
  77. Park, Y., Kumar, S., Kanumuri, R., Stanley, D., Kim, Y., 2015. A novel calcium-independent cellular PLA2 acts in insect immunity and larval growth. Insect Biochem. Mol. Biol. 66, 13-23. https://doi.org/10.1016/j.ibmb.2015.09.012
  78. Park, Y., Kang, S., Mohamad, M.D., Kim, H., Jung, J., Kim, Y., 2017. Identification and bacterial characteristics of Xenorhabdus hominickii ANU101 from an entomopathogenic nematode, Steinernema monticolum. J Invertebr Pathol 144, 74-87. https://doi.org/10.1016/j.jip.2017.02.002
  79. Phelps, P.K., Miller, J.S., Stanley, D.W., 2003. Prostaglandins, not lipoxygenase products, mediate insect microaggregation reactions to bacterial challenge in isolated hemocyte preparations. Comp. Biochem. Physiol. 136A, 409-416. https://doi.org/10.1016/S1095-6433(03)00199-5
  80. Quiot, J.M., Vey, A., Vago, C., Pais, M., 1980. Action antivirale d'une mycotoxine. Etude d'une toxine de l'hyphomycete Metarhizium anisopliae (Metsch.) Sorok. en culture cellulaire. CR. Acad. Sci. Ser. D (Paris) 291, 763-766.
  81. 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. U. S. A. 101, 2696-2699. https://doi.org/10.1073/pnas.0306669101
  82. Rivero, A., 2006. Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol. 22, 219-225. https://doi.org/10.1016/j.pt.2006.02.014
  83. Roberts, D.W., Hajek, A.E., 1992. Entomopathogenic fungi as bioinsecticides. in: Leatham, G.F. (Ed.), Frontiers in Industrial Mycology. Chapman and Hall, New York, pp 144-159.
  84. Roy, M.C., Nam, K., Kim, J., Stanley, D., Kim, Y., 2021. Thromboxane mobilizes insect blood cells to infection foci. Front. Immunol. 12, 791319 https://doi.org/10.3389/fimmu.2021.791319
  85. Ryu, Y., Oh, Y., Yoon, J., Cho, W., Baek, K., 2003. Molecular characterization of a gene encoding the Drosophila melanogaster phospholipase A2. Biochim. Biophys. Acta 1628, 206-210. https://doi.org/10.1016/S0167-4781(03)00143-X
  86. Sadekuzzaman, M., Gautam, N., Kim, Y., 2017a. A novel calcium-independent phospholipase A2 and its physiological roles in development and immunity of a lepidopteran insect, Spodoptera exigua. Dev. Comp. Immunol. 77, 210-220. https://doi.org/10.1016/j.dci.2017.08.014
  87. Sadekuzzaman, M.D., Park, Y., Jung, J., Lee, S., Kim, K., Kim, Y., 2017b. An entomopathogenic bacterium, Xenorhabdus hominickii ANU101, produces oxindole and suppresses host insect immune response by inhibiting eicosanoid biosynthesis. J. Invertebr. Pathol. 145, 13-22. https://doi.org/10.1016/j.jip.2017.03.004
  88. Sadekuzzaman, M.D., Stanley, D., Kim, Y., 2018. Nitric Oxide mediates insect cellular immunity via phospholipase A2 activation. J. Innate Immun. 10, 1-12. https://doi.org/10.1159/000485754
  89. Sajjadian, S.M., Kim, Y., 2020. PGE2 upregulates gene expression of dual oxidase in a lepidopteran insect midgut via cAMP signalling pathway. Open Biol. 10, 200197. https://doi.org/10.1098/rsob.200197
  90. Sajjadian, S.M., Vatanparast, M., Stanley, D., Kim, Y., 2019a. Secretion of secretory phospholipase A2 into Spodoptera exigua larval midgut lumen and its role in lipid digestion. Insect Mol. Biol. 28, 773-784. https://doi.org/10.1111/imb.12588
  91. Sajjadian, S.M., Vatanparast, M., Kim, Y., 2019b. Toll/IMD signal pathways mediate cellular immune responses via induction of intracellular PLA2 expression. Arch. Insect Biochem. Physiol. 101, e21559. https://doi.org/10.1002/arch.21559
  92. Sajjadian, S.M., Ahmed, S., Al Baki, M.A., Kim, Y., 2020. Prostaglandin D2 synthase and its functional association with immune and reproductive processes in a lepidopteran insect, Spodoptera exigua. Gen. Comp. Endocrinol. 287, 113352. https://doi.org/10.1016/j.ygcen.2019.113352
  93. Scarpati, M., Qi, Y., Govid, S., Singh, S., 2019. A combined computational strategy of sequence and structural analysis predicts the existence of a functional eicosanoid pathway in Drosophila melanogaster. PLoS ONE 14, e0211897. https://doi.org/10.1371/journal.pone.0211897
  94. Seilhamer, J.J., Pruzanski, W., Vadas, P., Plant, S., Miller, J.A., Kloss, J., Johnson, L.K., 1989. Cloning and recombinant expression of phospholipase A2 present in rheumatoid arthritic synovial fluid. J. Biol. Chem. 264, 5335-5338. https://doi.org/10.1016/S0021-9258(18)83549-9
  95. Seo, S., Kim, Y., 2011. Development of "Bt-Plus" biopesticide using entomopathogenic bacteria (Xenorhabdus nematophila and Photorhabdus temperata ssp. temperata) metabolites. Korean J. Appl. Entomol. 50, 171-178. https://doi.org/10.5656/KSAE.2011.07.0.24
  96. Seo, S., Jang, H., Kim, K., Kim, Y., 2010. Comparative analysis of immunsuppressive metabolites synthesized by an entomopathogenic bacterium, Photorhabdus temperata ssp. temperata, to select economic bacterial culture media. Korean J. Appl. Entomol. 49, 409-416. https://doi.org/10.5656/KSAE.2010.49.4.409
  97. Seo, S., Jeon, M.Y., Chun, W.S., Lee, S.H,, Seo, J.A., Yi, Y.G., Hong, Y.P., Kim, Y., 2011. Structure-activity analysis of benzylideneacetone for effective control of plant pests. Korean J. Appl. Entomol. 50, 107-113. https://doi.org/10.5656/KSAE.2011.04.0.15
  98. Seo, S., Lee, S., Hong, Y., Kim, Y., 2012. Phospholipase A2 inhibitors synthesized by two entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus temperata subsp temperata. Appl. Environ. Microbiol. 78, 3816-3823. https://doi.org/10.1128/AEM.00301-12
  99. Shafeeq, T., Ahmed, S., Kim, Y., 2018. Toll immune signal activates cellular immune response via eicosanoid. Dev. Comp. Immunol. 84, 408-419. https://doi.org/10.1016/j.dci.2018.03.015
  100. Shao, Z., Cui, Y., Liu, X., Yi, H., Ji, J., Yu, Z., 1998. Processing of delta-endotoxin of Bacillus thuringiensis subsp. kurstaki HD-1 in Heliothis armigera midgut juice and the effects of protease inhibitors. J. Invertebr. Pathol. 72, 73-81. https://doi.org/10.1006/jipa.1998.4757
  101. Shin, T.Y., Lee, M.R., Park, S.E., Lee, S.J., Kim, W.J., Kim, J.S., 2020. Pathogenesis-related genes of entomopathogenic fungi. Arch. Insect Biochem. Physiol. 105, e21747. https://doi.org/10.1002/arch.21747
  102. Shrestha, S., Kim, Y., 2008. Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm Spodoptera exigua. Insect Biochem. Mol. Biol. 38, 99-112. https://doi.org/10.1016/j.ibmb.2007.09.013
  103. Shrestha, S., Kim, Y., 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, 530-537. https://doi.org/10.1016/j.dci.2009.12.013
  104. Shrestha, S., Park, Y., Stanley, D., Kim, Y., 2010. Genes encoding phospholipase A2 mediate insect nodulation reactions to bacterial challenge. J. Insect Physiol. 56, 324-332. https://doi.org/10.1016/j.jinsphys.2009.11.008
  105. Shrestha, S., Stanley, D., Kim, Y., 2011. PGE2 induces oenocytoid cell lysis via a G protein-coupled receptor in the beet armyworm, Spodoptera exigua. J. Insect Physiol. 57, 1537-1544. https://doi.org/10.1016/j.jinsphys.2011.08.006
  106. Shrestha, S., Park, J., Ahn, S., Kim, Y., 2015. PGE2 mediates oenocytoid cell lysis via a sodium-potassium-chloride cotransporter. Arch. Insect Biochem. Physiol. 89, 218-229. https://doi.org/10.1002/arch.21238
  107. Srikanth, K., Park, J., Kim, Y., Stanley, D., 2011. Plasmatocyte-spreading peptide influences hemocyte behavior via eicosanoids. Arch. Insect Biochem. Physiol. 78, 145-160. https://doi.org/10.1002/arch.20450
  108. Stanley, D., 2000. Eicosanoids in invertebrate signal transduction systems. Princeton University Press, Princeton, New Jersey.
  109. Stanley, D., Kim, Y., 2020. Why most insects have very low proportions of C20 polyunsaturated fatty acids: the oxidative stress hypothesis. Arch. Insect Biochem. Physiol. 103, e21622. https://doi.org/10.1002/arch.21622
  110. Strand, M.R., 2008. The insect cellular immune response. Insect Sci. 15, 1-14. https://doi.org/10.1111/j.1744-7917.2008.00183.x
  111. Suzuki, A., Kanaoka, M., Isogai, A., Murakpshi, S., Ichinoe, M., Tamura, S., 1977. Bassianolide, a new insecticidal cyclodepsipeptide from Beauveria bassiana and Verticillium lecanii. Tetrahed. Lett. 25, 2167-2170. https://doi.org/10.1016/S0040-4039(01)81189-8
  112. Tabashnik, B.E., Brevault, T., Carriere, Y., 2013. Insect resistance to Bt crops: lessons from the first billion acres. Nat. Biotech. 31, 510-521. https://doi.org/10.1038/nbt.2597
  113. Terry, B.J., Liu, W.C., Cianci, C.W., Proszynski, E., Fernandes, P., Bush, K., Meyers, E., 1992. Inhibition of herpes simplex virus type 1 DNA polymerase by the natural product oosporein. J. Antibiotics 45, 286-288. https://doi.org/10.7164/antibiotics.45.286
  114. Tyurina, Y.Y., Tyurin, V.A., Epperly, M.W., Greenberger, J.S., Kagan, V.E., 2008. Oxidative lipidomics of gamma-irradiation-induced intestinal injury. Free Radic. Biol. Med. 44, 299-314. https://doi.org/10.1016/j.freeradbiomed.2007.08.021
  115. Tootle, T.L., Spradling, A.C., 2008. Drosophila Pxt: a cyclooxygenase-like facilitator of follicle maturation. Development 135, 839-847. https://doi.org/10.1242/dev.017590
  116. van Rie, J., McGaughey, W.H., Johnson, D.E., Barnett, B.D., van Mellaert, H., 1990. Mechanism of insect resistance to the microbial insecticide Bacillus thuringiensis. Science 247, 72-74. https://doi.org/10.1126/science.2294593
  117. Vasquez, A.M., Mouchlis, V.D., Dennis, E.A., 2018. Review of four major distinct types of human phospholipase A2. Adv. Biol. Regul. 67, 212-218. https://doi.org/10.1016/j.jbior.2017.10.009
  118. Vatanparast, M., Ahmed, S., Herrero, S., Kim, Y., 2018. A non-venomous sPLA2 of a lepidopteran insect: its physiological functions in development and immunity. Dev. Comp. Immunol. 89, 83-92. https://doi.org/10.1016/j.dci.2018.08.008
  119. Vatanparast, M., Ahmed, S., Sajjadian, S.M., Kim, Y., 2019. A prophylactic role of a secretory PLA2 of Spodoptera exigua against entomopathogens. Dev. Comp. Immunol. 95, 108-117. https://doi.org/10.1016/j.dci.2019.02.008
  120. Vey, A., Hoagland, R.E., Butt, T.M., 2001. Toxic metabolites of fungal biocontrol agents. in: Butt, T.M., Jackson, C., Magan, N. (Eds.), Fungal Biocontrol Agents, CABI Publishing, Wallingford, pp. 311-346.
  121. von Euler, U.S., 1936. On the specific vasodilating and plain muscle stimulating substances from accessory genital glands in men and certain animals (prostaglandin and vesiglandin). J. Physiol. 88, 213-234. https://doi.org/10.1113/jphysiol.1936.sp003433
  122. Wolf, M.J., Gross, R.W., 1996. The calcium-dependent association and functional coupling of calmodulin with myocardial phospholipase A2. Implications for cardiac cycle-dependent alterations in phospholipolysis. J. Biol. Chem. 271, 20989-20992. https://doi.org/10.1074/jbc.271.35.20989
  123. Yajima, M., Takada, M., Takahashi, N., Kikuchi, H., Natori, S., Oshima, Y., Kurata, S., 2003. A newly established in vitro culture using transgenic Drosophila reveals functional coupling between the phospholipase A2-generated fatty acid cascade and lipopolysaccharide-dependent activation of the immune deficiency (imd) pathway in insect immunity. Biochem J. 371, 205-210. https://doi.org/10.1042/BJ20021603
  124. Yamamoto, K., Hirowatari, A., 2021. Investigation of the substrate-binding site of a prostaglandin E synthase in Bombyx mori. Protein J. 40, 63-67. https://doi.org/10.1007/s10930-020-09956-3
  125. You, H.J., Woo, C.H., Choi, E.Y., Cho, S.H., Yoo, Y.J., Kim, J.H., 2005. Roles of Rac and p38 kinase in the activation of cytosolic phospholipase A2 in response to PMA. Biochem. J. 388, 527-535. https://doi.org/10.1042/BJ20041614
  126. Zhao, P., Li, J., Wang, Y., Jiang, H., 2007. Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochem. Mol. Biol. 37, 952-959. https://doi.org/10.1016/j.ibmb.2007.05.001