Academic Journal
The involvement of Apolipophorin-III in orchestrating prophenoloxidase activation and NO production in Ostrinia furnacalis larvae.
| Τίτλος: | The involvement of Apolipophorin-III in orchestrating prophenoloxidase activation and NO production in Ostrinia furnacalis larvae. |
|---|---|
| Συγγραφείς: | Liu X; Department of Entomology, College of Plant Protection, Yangzhou University, Yangzhou, Jiangsu Province, China., Guo W; Department of Entomology, College of Plant Protection, Yangzhou University, Yangzhou, Jiangsu Province, China., Wang Z; Department of Entomology, College of Plant Protection, Yangzhou University, Yangzhou, Jiangsu Province, China., Li S; Department of Entomology, College of Plant Protection, Yangzhou University, Yangzhou, Jiangsu Province, China., Bi H; Department of Entomology, College of Plant Protection, Yangzhou University, Yangzhou, Jiangsu Province, China., Feng C; Department of Entomology, College of Plant Protection, Yangzhou University, Yangzhou, Jiangsu Province, China. |
| Πηγή: | Insect science [Insect Sci] 2026 Jun; Vol. 33 (3), pp. 987-1002. Date of Electronic Publication: 2025 Mar 23. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: Blackwell Pub Country of Publication: Australia NLM ID: 101266965 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1744-7917 (Electronic) Linking ISSN: 16729609 NLM ISO Abbreviation: Insect Sci Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Victoria, Australia : Blackwell Pub., c2005- |
| Ιατρικοί όροι (MeSH): | Catechol Oxidase*/metabolism , Moths*/immunology , Moths*/metabolism , Moths*/microbiology , Moths*/genetics , Moths*/growth & development , Moths*/enzymology , Enzyme Precursors*/metabolism , Nitric Oxide*/metabolism , Apolipoproteins*/metabolism , Apolipoproteins*/genetics , Insect Proteins*/metabolism , Insect Proteins*/genetics, Larva/immunology ; Larva/metabolism ; Larva/microbiology ; Larva/genetics ; Animals ; Immunity, Innate ; Amino Acid Sequence |
| Περίληψη: | Apolipophorin-III (ApoLp-III), a multifunctional protein with lipid transport and immune defense functions, widely exists in insects. Although the function of ApoLp-III as a pattern recognition receptor (PRR) in immunity has been relatively studied, the immune response mediated by ApoLp-III is still vague. To understand whether ApoLp-III is involved in the activation of the prophenoloxidase-activating system (PPO-AS), we examined the production of nitric oxide (NO), and the synthesis of antimicrobial peptides after immune recognition. The larvae of lepidopteran pest Ostrinia furnacalis were used as a model to address these questions by detecting the changes of phenoloxidase (PO) activity and NO concentration after the knockdown of OfApoLp-III and bacterial infections. In the present study, we reported the cloning and characterization of the OfApoLp-III complementary DNA, and found that OfApoLp-III is mainly expressed in the larval fat body. These investigations revealed that OfApoLp-III was an immune-related gene, its knockdown reduced the PO activity by 41.9%, and NO concentration reached 2.7-fold higher level than that after double-stranded GFP treatment. Our data indicated that OfApoLp-III was involved in increased expression of Moricin, activation of PPO, and reduction of NO production in O. furnacalis larvae after different bacterial infections, which were required for innate immunity. ApoLp-III is a candidate target for an integrated pest control strategy using the combined application of double-stranded RNA and biocontrol bacteria. (© 2025 Institute of Zoology, Chinese Academy of Sciences.) |
| References: | Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein‐dye binding. Analytical Biochemistry, 72, 248–254. Bredt, D.S. and Snyder, S.H. (1994) Nitric oxide: a physiologic messenger molecule. Annual Review of Biochemistry, 63, 175–195. Buchon, N., Silverman, N. and Cherry, S. (2014) Immunity in Drosophila melanogaster‐from microbial recognition to whole‐organism physiology. Nature Reviews Immunology, 14, 796–810. Carton, Y., Poirié, M. and Nappi, A.J. (2008) Insect immune resistance to parasitoids. Insect Science, 15, 67–87. Cerenius, L., Lee, B.L. and Söderhäll, K. (2008) The proPO‐system: pros and cons for its role in invertebrate immunity. Trends in Immunology, 29, 263–271. Chen, K.K., Wang, X.Y., Wei, X.Y., Chen, J.Q., Wei, Y.H., Jiang, H.B. et al. (2022) Nitric oxide‐induced calcineurin a mediates antimicrobial peptide production through the IMD pathway. Frontiers in Immunology, 13, 905419. Chu, Y., Zhou, F., Liu, Y., Hong, F., Wang, G.R. and An, C.J. (2015) Ostrinia furnacalis serpin‐3 regulates melanization cascade by inhibiting a prophenoloxidase‐activating protease. Insect Biochemistry and Molecular Biology, 61, 53–61. Contreras, E., Rausell, C. and Real, M.D. (2013) Tribolium castaneum Apolipophorin‐III acts as an immune response protein against Bacillus thuringiensis Cry3Ba toxic activity. Journal of Invertebrate Pathology, 113, 209–213. Dettloff, M., Wittwer, D., Weise, C. and Wiesner, A. (2001) Lipophorin of lower density is formed during immune responses in the lepidopteran insect Galleria mellonella. Cell and Tissue Research, 306, 449–458. Fang, F.C. and Vázquez‐Torres, A. (2019) Reactive nitrogen species in host‐bacterial interactions. Current Opinion in Immunology, 60, 96–102. Feng, C.J., Huang, J.H., Song, Q.S., Stanley, D., Lü, W.J., Zhang, Y. et al. (2011) Parasitization by Macrocentrus cingulum (Hymenoptera: Braconidae) influences expression of prophenoloxidase in Asian corn borer Ostrinia furnacalis. Archives of Insect Biochemistry and Physiology, 77, 99–117. Feng, C.J., Zhao, Y., Chen, K.K., Zhai, H.F., Wang, Z.Y., Jiang, H.B. et al. (2018) Clip domain prophenoloxidase activating protease is required for Ostrinia furnacalis Guenée to defend against bacterial infection. Developmental and Comparative Immunology, 87, 204–215. Got, B. (1988) Determination of instar of the European corn borer (lepidoptera: Pyralidae) based on a distribution model of head capsule widths. Annals of the Entomological Society of America, 1, 91–98. Huebbe, P. and Rimbach, G. (2017) Evolution of human apolipoprotein E (APOE) isoforms: gene structure, protein function and interaction with dietary factors. Ageing Research Reviews, 37, 146–161. Jiang, H., Vilcinskas, A. and Kanost, M.R. (2010) Immunity in lepidopteran insects. Advances in Experimental Medicine and Biology, 708, 181–204. Jiang, H.B., Wang, Y., Yu, X.Q., Zhu, Y.F. and Kanost, M. (2003) Prophenoloxidase‐activating proteinase‐3 (PAP‐3) from Manduca sexta hemolymph: a clip‐domain serine proteinase regulated by serpin‐1J and serine proteinase homologs. Insect Biochemistry and Molecular Biology, 33, 1049–1060. Iwański, B. and Andrejko, M. (2023) Changes in the apolipophorin III in Galleria mellonella larvae treated with Pseudomonas aeruginosa exotoxin A. Journal of Insect Physiology, 149, 104536. Kimbrell, D.A. and Beutler, B. (2001) The evolution and genetics of innate immunity. Nature Reviews Genetics, 2, 256–267. Li, E.T., Ji, J.Y., Kong, W.J., Shen, D.X., Li, C. and An, C.J. (2024) A C‐type lectin with dual carbohydrate recognition domains functions in innate immune response in Asian corn borer, Ostrinia furnacalis. Insect Science, 32, 172–192. https://doi.org/10.1111/1744‐7917.13382. Lu, A.R., Zhang, Q.L., Zhang, J., Yang, B., Wu, K., Xie, W. et al. (2014) Insect prophenoloxidase: the view beyond immunity. Frontiers in Physiology, 5, 252. Lundberg, J.O. and Weitzberg, E. (2022) Nitric oxide signaling in health and disease. Cell, 185, 2853–2878. Mahanta, D.K., Bhoi, T.K., Komal, J., Samal, I., Nikhil, R.M., Paschapur, A.U. et al. (2023) Insect‐pathogen crosstalk and the cellular‐molecular mechanisms of insect immunity: uncovering the underlying signaling pathways and immune regulatory function of non‐coding RNAs. Frontiers in Immunology, 14, 1169152. Miranda, K.M., Espey, M.G., Yamada, K., Krishna, M., Ludwick, N., Kim, S. et al. (2001) Unique oxidative mechanisms for the reactive nitrogen oxide species, nitroxyl anion. The Journal of Biological Chemistry, 276, 1720–1727. Mullen, L. and Goldsworthy, G. (2003) Changes in lipophorins are related to the activation of phenoloxidase in the haemolymph of Locusta migratoria in response to injection of immunogens. Insect Biochemistry and Molecular Biology, 33, 661–670. Noh, J.Y., Patnaik, B.B., Tindwa, H., Seo, G.W., Kim, D.H., Patnaik, H.H. et al. (2014) Genomic organization, sequence characterization and expression analysis of Tenebrio molitor apolipophorin‐III in response to an intracellular pathogen, Listeria monocytogenes. Gene, 534, 204–217. Qian, C., Wang, F., Zhu, B.J., Wei, G.Q., Li, S., Liu, C.L. et al. (2016) Identification and characterization of an Apolipophorin‐III gene from Actias selene Hübner (Lepidoptera: Saturniidae). Journal of Asia‐Pacific Entomology, 19, 103–108. Rivero, A. (2006) Nitric oxide: an antiparasitic molecule of invertebrates. Trends in Parasitology, 22, 219–225. Schmittgen, T.D. and Livak, K.J. (2008) Analyzing real‐time PCR data by the comparative C(T) method. Nature Protocols, 3, 1101–1108. Seo, S.J., Park, K.H. and Cho, K.H. (2008) Apolipophorin III from Hyphantria cunea shows different anti‐oxidant ability against LDL oxidation in the lipid‐free and lipid‐bound state. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology, 151, 433–439. Shan, T.S., Wang, Y., Bhattarai, K. and Jiang, H.B. (2023) An evolutionarily conserved serine protease network mediates melanization and Toll activation in Drosophila. Science Advances, 9, eadk2756. Söderhäll, K. and Cerenius, L. (1998) Role of the prophenoloxidase‐activating system in invertebrate immunity. Current Opinion in Immunology, 10, 23–28. Son, Y., Hwang, J. and Kim, Y. (2012) Functional study of the gene encoding apolipophorin III in development and immune responses in the beet armyworm, Spodoptera exigua. Journal of Asia‐Pacific Entomology, 15, 106–112. Stączek, S., Cytryńska, M. and Zdybicka‐Barabas, A. (2023) Unraveling the role of antimicrobial peptides in insects. International Journal of Molecular Sciences, 24, 5753. Stuehr, D.J. and Haque, M.M. (2019) Nitric oxide synthase enzymology in the 20 years after the Nobel Prize. British Journal of Pharmacology, 176, 177–188. Sun, D., Ziegler, R., Milligan, C.E., Fahrbach, S. and Schwartz, L.M. (1995) Apolipophorin III is dramatically up‐regulated during the programmed death of insect skeletal muscle and neurons. Journal of Neurobiology, 26, 119–129. Wang, J.J., Sykes, B.D. and Ryan, R.O. (2002) Structural basis for the conformational adaptability of apolipophorin III, a helix‐bundle exchangeable apolipoprotein. Proceedings of the National Academy of Sciences USA, 99, 1188–1193. Wang, Q.R., Yin, M.Y., Yuan, C.F., Liu, X.J., Hu, Z.H., Zou, Z. et al. (2020a) Identification of a conserved prophenoloxidase activation pathway in cotton bollworm Helicoverpa armigera. Frontiers in Immunology, 11, 785. Wang, W.X., Wang, Y.P., Deng, X.J., Dang, X.L., Tian, J.H., Yi, H.Y. et al. (2009) Molecular and functional characterization of a c‐type lysozyme from the Asian corn borer, Ostrinia furnacalis. Journal of Insect Science, 9, 17. Wang, Y., Kanost, M.R. and Jiang, H.B. (2022) A mechanistic analysis of bacterial recognition and serine protease cascade initiation in larval hemolymph of Manduca sexta. Insect Biochemistry and Molecular Biology, 148, 103818. Wang, Y., Yang, F., Cao, X.L., Huang, R.D., Paskewitz, S., Hartson, S.D. et al. (2020b) Inhibition of immune pathway‐initiating hemolymph protease‐14 by Manduca sexta serpin‐12, a conserved mechanism for the regulation of melanization and Toll activation in insects. Insect Biochemistry and Molecular Biology, 116, 103261. Wang, Z.Y., He, K.L., Zhang, F., Lu, X. and Babendreier, D. (2014) Mass rearing and release of Trichogramma for biological control of insect pests of corn in China. Biological Control, 68, 136–144. Weers, P.M. and Ryan, R.O. (2003) Apolipophorin III: a lipid‐triggered molecular switch. Insect Biochemistry and Molecular Biology, 33, 1249–1260. Weers, P.M. and Ryan, R.O. (2006) Apolipophorin III: role model apolipoprotein. Insect Biochemistry and Molecular Biology, 36, 231–240. Weers, P.M., Van Baal, J., Van Doorn, J.M., Ziegler, R. and Van der Horst, D.J. (1993) Biosynthetic route of locust apolipophorin III isoforms. Biological Chemistry Hoppe‐Seyler, 374, 863–869. Wen, D.H., Wang, X.L., Shang, L., Huang, Y., Li, T.A., Wu, C.F. et al. (2016) Involvement of a versatile pattern recognition receptor, apolipophorin‐III in prophenoloxidase activation and antibacterial defense of the Chinese oak silkworm, Antheraea pernyi. Developmental and Comparative Immunology, 65, 124–131. Whitten, M.M., Mello, C.B., Gomes, S.A., Nigam, Y., Azambuja, P., Garcia, E.S. et al. (2001) Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Experimental Parasitology, 98, 44–57. Whitten, M.M., Tew, I.F., Lee, B.L. and Ratcliffe, N.A. (2004) A novel role for an insect apolipoprotein (apolipophorin III) in beta‐1,3‐glucan pattern recognition and cellular encapsulation reactions. Journal of Immunology, 172, 2177–2185. Wijeratne, T.U. and Weers, P.M. (2019) Lipid‐bound apoLp‐III is less effective in binding to lipopolysaccharides and phosphatidylglycerol vesicles compared to the lipid‐free protein. Molecular and Cellular Biochemistry, 458, 61–70. Williams, M.J. (2007) Drosophila hemopoiesis and cellular immunity. Journal of Immunology, 178, 4711–4716. Wu, S.C., Liao, C.W., Pan, R.L. and Juang, J.L. (2012) Infection‐induced intestinal oxidative stress triggers organ‐to‐organ immunological communication in Drosophila. Cell Host and Microbe, 11, 410–417. Wu, T.Y., Zhao, Y., Wang, Z.Y., Song, Q.S., Wang, Z.X., Xu, Q.W. et al. (2018) β‐1,3‐Glucan recognition protein 3 activates the prophenoloxidase system in response to bacterial infection in Ostrinia furnacalis Guenée. Developmental and Comparative Immunology, 79, 31–43. Yang, F., Zhu, B., Liu, J., Liu, Y., Jiang, C., Sheng, Q. et al. (2020) The effect of acetylation on the protein stability of BmApoLp‐III in the silkworm, Bombyx mori. Insect Molecular Biology, 29, 104–111. Yu, H.Z., Wang, J., Zhang, S.Z., Toufeeq, S., Li, B., Li, Z. et al. (2018) Molecular characterisation of Apolipophorin‐III gene in Samia cynthia ricini and its roles in response to bacterial infection. Journal of Invertebrate Pathology, 159, 61–70. |
| Grant Information: | 32372517 National Natural Science Foundation of China; 32072417 National Natural Science Foundation of China |
| Contributed Indexing: | Keywords: Apolipophorin‐III; Ostrinia furnacalis; antimicrobial peptides; bacterial infection; innate immunity |
| Substance Nomenclature: | 0 (apolipophorin III) EC 1.10.3.- (pro-phenoloxidase) EC 1.10.3.1 (Catechol Oxidase) 0 (Enzyme Precursors) 31C4KY9ESH (Nitric Oxide) 0 (Apolipoproteins) 0 (Insect Proteins) |
| Entry Date(s): | Date Created: 20250324 Date Completed: 20260612 Latest Revision: 20260612 |
| Update Code: | 20260612 |
| DOI: | 10.1111/1744-7917.70030 |
| PMID: | 40123088 |
| Βάση Δεδομένων: | MEDLINE |
καταχωρήστε σχόλιο πρώτοι!