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Mediation of inducible nitric oxide and immune-reactive lysozymes biosynthesis by eicosanoid and biogenic amines in flesh flies

Published online by Cambridge University Press:  10 January 2018

Amr A. Mohamed ,
Mona M. Ali ,
Moataza A. Dorrah  and
Taha T. M. Bassal
Amr A. Mohamed
Affiliation:
Department of Entomology, Faculty of Science, Cairo University, Giza, PO Box 12613, Egypt
Mona M. Ali
Affiliation:
Department of Entomology, Faculty of Science, Cairo University, Giza, PO Box 12613, Egypt
Moataza A. Dorrah
Affiliation:
Department of Entomology, Faculty of Science, Cairo University, Giza, PO Box 12613, Egypt
Taha T. M. Bassal*
Affiliation:
Department of Entomology, Faculty of Science, Cairo University, Giza, PO Box 12613, Egypt
*
*E-mail: taha@sci.cu.edu.eg
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Abstract

Nitric oxide (NO) plays various roles in insect immunity: as a cytotoxic component and as a signalling molecule; and immune-reactive lysozymes (IrLys) provide a first line of humoral immune functions against invading bacteria. Although there is considerable literature on eicosanoid and biogenic monoamine actions on insect immunity, there is no information on the role(s) of these chemicals in inducing NO and IrLys. We addressed this gap by challenging third instar Sarcophaga (Liopygia) argyrostoma (Robineau-Desvoidy) with the Gram-positive bacterium Micrococcus luteus. Here, we report that bacterial challenge induces elevation of NO and IrLys concentrations in haemocytes and in the fat body. The plasma pool content is comparatively low. Eicosanoid biosynthesis inhibitors (EBIs) lead to suppression of both NO and IrLys levels. Control larvae have low constitutive levels of NO and lysozyme concentrations. Octopamine (OA) elicits elevation of NO and IrLys concentrations. A similar effect is obtained by 5-hydroxytryptamine (5-HT) for NO. These data indicate immune-mediating roles of eicosanoids, OA and 5-HT in NO and IrLys activities.

Keywords

Nitric oxidelysozymeseicosanoidsbiogenic monoaminesSarcophaga
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 38 , Issue 1 , March 2018 , pp. 93 - 104
Copyright
Copyright © icipe 2018 

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Footnotes

†

Both authors contributed equally to this work.

Authors' contributions

Conceptualization: TTMB, MAD and AAM. Data curation: TTMB and AAM. Formal analysis: MMA, AAM and MAD. Funding acquisition: MMA and AAM. Investigation: AAM and MMA. Methodology: TTMB, AAM and MAD. Resources: MAD, MMA and AAM. Software and Statistics: AAM. Supervision: TTMB and MAD. Validation: TTMB, AAM and MAD. Visualization: MMA and AAM. Writing – original draft: TTMB and AAM. Writing – review and editing: TTMB and AAM.

References

Abraham, E. G., Nagaraju, J., Salunke, D. M., Gupta, H. M. and Datta, R. K. (1995) Purification and partial characterization of an induced antibacterial protein in the silkworm, Bombyx mori . Journal of Invertebrate Pathology 65, 17–24.CrossRefGoogle ScholarPubMed
Adamo, S. A. (2008) Norepinephrine and octopamine: linking stress and immune function across phyla. Invertebrate Survival Journal 5, 12–19.Google Scholar
Ajjuri, R. R. and O'Donnell, J. M. (2013) Novel whole-tissue quantitative assay of nitric oxide levels in Drosophila neuroinflammatory response. Journal of Visualized Experiments 82, 50892.Google Scholar
Alderton, W. K., Cooper, C. E. and Knowles, R. G. (2001) Nitric oxide synthases: structure, function and inhibition. Biochemical Journal 357, 593–615.CrossRefGoogle ScholarPubMed
Azambuja, P., Feder, D., Mello, C. B., Gomes, S. A. O. and Garcia, E. S. (1999) Immunity in Rhodnius prolixus: Trypanosomatid-vector interactions. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro 94, Suppl I, S219–S222.CrossRefGoogle ScholarPubMed
Baines, D. and Downer, R. G. H. (1994) Octopamine enhances phagocytosis in cockroach hemocytes: involvement of inositol triphosphate. Archives of Insect Biochemistry and Physiology 26, 249–261.CrossRefGoogle Scholar
Baines, D., Desantis, T. and Downer, R. G. H. (1992) Octopamine and 5-hydroxy trypamine enhance the phagocytic and nodule formation activities of cockroach (Periplaneta americana) hemocytes. Journal of Insect Physiology 38, 905–914.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Brey, P. T. (1994) The impact of stress on insect immunity. Bulletin de I'Institut Pasteur 92, 101–118.Google Scholar
Colasanti, M., Gradoni, L., Mattu, M., Persichini, T., Salvati, L., Venturini, G. and Ascenzi, P. (2002) Molecular basis for the anti-parasitic effect of NO. International Journal of Molecular Medicine 9, 131–134.Google Scholar
Dunphy, G. B. and Downer, R. G. H. (1994) Octopamine, a modulator of the haemocytic nodulation response of non-immune Galleria mellonella larvae. Journal of Insect Physiology 40, 267–272.CrossRefGoogle Scholar
Durmus, Y., Büyükgüzel, E., Terzi, B., Tunaz, H., Stanley, D. and Büyükgüzel, K. (2008) Eicosanoids mediate melanotic nodulation reactions to viral infection in larvae of the parasitic wasp, Pimpla turionellae. Journal of Insect Physiology 54, 17–24.CrossRefGoogle ScholarPubMed
Faraldo, A. C., Sá-Nunes, A., Del Bel, E. A., Faccioli, L. H. and Lello, E. (2005) Nitric oxide production in blowfly hemolymph after yeast inoculation. Nitric Oxide 13, 196–203.CrossRefGoogle ScholarPubMed
Finney, D. J. (1971) Probit Analysis 3rd edn. Cambridge. University Press, New York. 333 pp.Google Scholar
Foley, E. and O'Farrell, P. H. (2003) Nitric oxide contributes to induction of innate immune responses to Gram-negative bacteria in Drosophila . Genes & Development 17, 115–125.CrossRefGoogle ScholarPubMed
Gillespie, J. P., Kanost, M. R. and Trenczek, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.CrossRefGoogle ScholarPubMed
Gillespie, J. P., Koshinsky, H. A. and Khachatourians, G. G. (1993) The occurrence of inducible anti-Escherichia coli activity in hemolymph from the migratory grasshopper, Melanoplus sanguinipes. Comparative Biochemistry and Physiology - Part C 104, 111–115.CrossRefGoogle ScholarPubMed
Grassberger, M. and Reiter, C. (2002) Effect of temperature on development of Liopygia (= Sarcophaga) argyrostoma (Robineau-Desvoidy) (Diptera: Sarcophagidae) and its forensic implications. Journal of Forensic Sciences 47, 1332–1336.CrossRefGoogle ScholarPubMed
Green, L. C., Wagner, D. A., Glogowski, J., Skipper, P. L., Wishnok, J. S. and Tannenbaum, S. R. (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Analytical Biochemistry 126, 131–138.CrossRefGoogle ScholarPubMed
Halliwell, B. and Gutteridge, J. M. C. (1999) Free radicals, other reactive species and disease, pp. 617–783. In Free Radicals in Biology and Medicine 3rd edn. (edited by Halliwell, B. and Gutteridge, J. M. C.). Clarendon Press, Oxford.Google Scholar
Hillyer, J. F. (2016) Insect immunology and hematopoiesis. Developmental and Comparative Immunology 58, 102–118.CrossRefGoogle ScholarPubMed
Hillyer, J. F. and Estévez-Lao, T. Y. (2009) Nitric oxide is an essential component of the hemocyte-mediated mosquito immune response against bacteria. Developmental and Comparative Immunology 34, 141–149.CrossRefGoogle ScholarPubMed
Hillyer, J. F., Estévez-Lao, T. Y. and Mirzai, H. E. (2015) The neurotransmitters serotonin and glutamate accelerate the heart rate of the mosquito Anopheles gambiae . Comparative Biochemistry and Physiology – Part A 188, 49–57.CrossRefGoogle ScholarPubMed
Hogg, N., Darley-Usmar, V. M., Wilson, M. T. and Moncada, S. (1992) Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochemical Journal 281, 419–424.CrossRefGoogle ScholarPubMed
Huang, J., Wu, S. F., Li, X. H., Adamo, S. A. and Ye, G. Y. (2012) The characterization of a concentration-sensitive α-adrenergic-like octopamine receptor found on insect immune cells and its possible role in mediating stress hormone effects on immune function. Brain, Behavior, and Immunity 26, 942–950.CrossRefGoogle ScholarPubMed
Imler, J. L. and Bulet, P. (2005) Antimicrobial peptides in Drosophila: structures, activities and gene regulation, vol. 86, pp. 1–21. In Mechanisms of Epithelial Defense (edited by Kabelitz, D. and Schroder, J.M.). Karger, Basel.Google Scholar
Jenzano, J. W., Hogan, S. L. and Lundblad, R. L. (1986) Factors influencing measurement of human salivary lysozyme in lysoplate and turbidimetric assays. Journal of Clinical Microbiology 24, 963–967.CrossRefGoogle ScholarPubMed
Jiang, Q., Zhou, Z., Wang, L., Yang, C., Wang, J., Wu, T. and Song, L. (2014) Mutual modulation between norepinephrine and nitric oxide in haemocytes during the mollusc immune response. Scientific Reports 4, 6963.CrossRefGoogle ScholarPubMed
Kim, G. S. and Kim, Y. (2010) Up-regulation of circulating hemocyte population in response to bacterial challenge is mediated by octopamine and 5-hydroxytryptamine via Rac1 signal in Spodoptera exigua . Journal of Insect Physiology 56, 559–566.CrossRefGoogle ScholarPubMed
Kim, G. S., Nalini, M., Kim, Y. and Lee, D. W. (2009) Octopamine and 5-hydroxytryptamine mediate hemocytic phagocytosis and nodule formation via eicosanoids in the beet armyworm, Spodoptera exigua . Archives of Insect Biochemistry and Physiology 70, 162–176.CrossRefGoogle ScholarPubMed
Kim, J. W. and Yoe, S. M. (2003) Purification of lysozyme from hemolymph of tobacco cutworm, Spodoptera litura . Korean Journal of Entomology 33, 287–291.CrossRefGoogle Scholar
Kocur, M., Pačova, Z. and Martinec, T. (1972) Taxonomic status of Micrococcus luteus (Schroeter 1872) Cohn 1872, and designation of the neotype strain. International Journal of Systematic and Evolutionary Microbiology 22, 218–223.Google Scholar
Leitão, A. B. and Sucena, É. (2015) Drosophila sessile hemocyte clusters are true hematopoietic tissues that regulate larval blood cell differentiation. eLife 4, e06166.CrossRefGoogle ScholarPubMed
Leonard, C., Söderhäll, K. and Ratcliffe, N. A. (1985) Studies on prophenoloxidase and protease activity of Blaberus craniifer haemocytes. Insect Biochemistry 15, 803–810.CrossRefGoogle Scholar
Luckhart, S., Vodovotz, Y., Cui, L. and Rosenberg, R. (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Sciences USA 95, 5700–5705.CrossRefGoogle ScholarPubMed
Marin, D., Dunphy, G. B. and Mandato, C. A. (2005) Cyclic AMP affects the haemocyte responses of larval Galleria mellonella to selected antigens. Journal of Insect Physiology 51, 575–586.CrossRefGoogle ScholarPubMed
Márkus, R., Laurinyecz, B., Kurucz, É., Honti, V., Bajusz, I., Sipos, B., Somogyi, K., Kronhamn, J., Hultmark, D. and Andó, I. (2009) Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster . Proceedings of the National Academy of Sciences USA 106, 4805–4809.CrossRefGoogle ScholarPubMed
Miller, J. S., Nguyen, T. and Stanley-Samuelson, D. W. (1994) Eicosanoids mediate insect nodulation responses to bacterial infections. Proceedings of the National Academy of Sciences USA 91, 12418–12422.CrossRefGoogle ScholarPubMed
Mink, S. N., Jacobs, H., Cheng, Z. Q., Kasian, K., Santos-Martinez, L. E. and Light, R. B. (2009) Lysozyme, a mediator of sepsis that intrinsically generates hydrogen peroxide to cause cardiovascular dysfunction. American Journal of Physiology, Heart and Circulatory Physiology 297, H930–H948.CrossRefGoogle ScholarPubMed
Mohamed, A. A., Elmogy, M., Dorrah, M. A., Yousef, H. A. and Bassal, T. T. M. (2013) Antibacterial activity of lysozyme in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). European Journal of Entomology 110, 559–565.CrossRefGoogle Scholar
Mohamed, A. A., Zhang, L., Dorrah, M. A., Elmogy, M., Yousef, H. A., Bassal, T. T. and Duvic, B. (2016) Molecular characterization of a c-type lysozyme from the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). Developmental and Comparative Immunology 61, 60–69.CrossRefGoogle ScholarPubMed
Morishima, I., Horiba, T., Iketami, M., Nishioka, E. and Yamano, Y. (1995) Parallel induction of cecropin and lysozyme in larvae of the silkworm Bombyx mori . Developmental and Comparative Immunology 19, 357–363.CrossRefGoogle ScholarPubMed
Morishima, I., Yamano, Y., Inoue, K. and Matsuo, N. (1997) Eicosanoids mediate induction of immune genes in the fat body of the silkworm, Bombyx mori. FEBS Letters 419, 83–86.Google ScholarPubMed
Müller, U. (1997) The nitric oxide system in insects. Progress in Neurobiology 51, 363–381.CrossRefGoogle ScholarPubMed
Nappi, A. J., Vass, E., Frey, F. and Carton, Y. (2000) Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4, 423–430.CrossRefGoogle ScholarPubMed
Orr, G. L., Gole, J. W. D. and Downer, R. G. H. (1985) Characterization of an octopamine-sensitive adenylate cyclase in hemocyte membrane fragments of the American cockroach Periplaneta americana L. Insect Biochemistry 15, 695–701.CrossRefGoogle Scholar
Papaefthimiou, C. and Theophilidis, G. (2011) Octopamine—a single modulator with double action on the heart of two insect species (Apis mellifera macedonica and Bactrocera oleae): Acceleration vs. inhibition. Journal of Insect Physiology 57, 316–325.CrossRefGoogle ScholarPubMed
Park, H. Y., Park, S. S., Shin, S. W., Park, D. S., Kim, M. G., Oh, H. W. and Joo, C. K. (1997) Protein purification and nucleotide sequence of a lysozyme from the bacteria-induced larvae of the fall webworm, Hyphantria cunea . Archives of Insect Biochemistry and Physiology 35, 335–345.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Peeters, T. L. and Vantrappen, G. R. (1977) Factors influencing lysozyme determinations by the lysoplate method. Clinica Chimica Acta 74, 217–225.CrossRefGoogle ScholarPubMed
Prescott, L. M., Harley, J. P. and Klein, D. A. (1993) Microbiology 2nd edn. Wm. C. Brown Communications, Dubuque, Iowa. 55 pp.Google Scholar
Qi, Y. X., Huang, J., Li, M. Q., Wu, Y. S., Xia, R. Y. and Ye, G. Y. (2016) Serotonin modulates insect hemocyte phagocytosis via two different serotonin receptors. eLife 5, e12241.CrossRefGoogle ScholarPubMed
Qin, Q. W., Ototake, M., Noguchi, K., Soma, G., Yokomizo, Y. and Nakanishi, T. (2001) Tumor necrosis factor alpha (TNFalpha)-like factor produced by macrophages in rainbow trout, Oncorhynchus mykiss . Fish and Shellfish Immunology 11, 245–256.CrossRefGoogle ScholarPubMed
Rao, X. and Yu, X. (2011) Lipoteichoic acid and lipopolysaccharide can activate antimicrobial peptide expression in the tobacco hornworm Manduca sexta . Developmental and Comparative Immunology 34, 1119–1128.CrossRefGoogle Scholar
Roeder, T. (2005) Tyramine and octopamine: ruling behavior and metabolism. Annual Review of Entomology 50, 447–477.CrossRefGoogle ScholarPubMed
Shrestha, S. and Kim, Y. (2008) Eicosanoids mediate prophenoloxidase release from oenocytoids in the beet armyworm Spodoptera exigua . Insect Biochemistry and Molecular Biology 38, 99–112.CrossRefGoogle ScholarPubMed
Shrestha, S. and Kim, Y. (2009) Various eicosanoids modulate the cellular and humoral immune responses of the beet armyworm, Spodoptera exigua . Bioscience, Biotechnology, and Biochemistry 73, 2077–2084.CrossRefGoogle ScholarPubMed
Shrestha, S., Park, J., Ahn, S.-J. and Kim, Y. (2015) PGE2 mediates oenocytoid cell lysis via a sodium-potassium-chloride cotransporter. Archives of Insect Biochemistry and Physiology 89, 218–229.CrossRefGoogle Scholar
Söderhäll, K. and Smith, V. J. (1983) Separation of the hemocyte populations of Carcinus maenas and other marine decapods, and prophenoloxidase distribution. Developmental and Comparative Immunology 7, 229–239.CrossRefGoogle Scholar
Srikanth, K., Park, J., Stanley, D. W. and Kim, Y. (2011) Plasmatocyte-spreading peptide influences hemocyte behavior via eicosanoids. Archives of Insect Biochemistry and Physiology 78, 145–160.CrossRefGoogle ScholarPubMed
Stanley, D. W. (2000) Eicosanoids in Invertebrate Signal Transduction Systems. Princeton University Press, Princeton, NJ.Google Scholar
Stanley, D. W. and Kim, Y. (2014) Eicosanoid signaling in insects: from discovery to plant protection. Critical Reviews in Plant Sciences 33, 20–63.CrossRefGoogle Scholar
Stanley-Samuelson, D. W., Jensen, E., Nickerson, K. W., Tiebel, K., Ogg, C. L. and Howard, R. W. (1991) Insect immune response to bacterial infection is mediated by eicosanoids. Proceedings of the National Academy of Sciences USA 88, 1064–1068.CrossRefGoogle ScholarPubMed
Vilcinskas, A. and Matha, V. (1997) Antimycotic activity of lysozyme and its contribution to antifungal humoral defense reactions in Galleria mellonella . Animal Biology 6, 19–29.Google Scholar
Wasserman, S. L. and Itagaki, H. (2003) The olfactory responses of the antenna and maxillary palp of the fleshfly, Neobellieria bullata (Diptera: Sarcophagidae), and their sensitivity to blockage of nitric oxide synthase. Journal of Insect Physiology 49, 271–280.CrossRefGoogle ScholarPubMed
Whitten, M. M., Mello, C. B., Gomes, S. A., Nigam, Y., Azambuja, P., Garcia, E. S. and Ratcliffe, N. A. (2001) Role of superoxide and reactive nitrogen intermediates in Rhodnius prolixus (Reduviidae)/Trypanosoma rangeli interactions. Experimental Parasitology 98, 44–57.CrossRefGoogle ScholarPubMed
Williams, M., Wiklund, M.-L., Wikman, S. and Hultmark, D. (2006) Rac1 signalling in the Drosophila larval cellular immune response. Journal of Cell Science 119, 2015–2024.CrossRefGoogle ScholarPubMed
Yajima, M., Takada, M., Takahashi, N., Kikuchi, H., Natori, S., Oshima, Y. and 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. Biochemical Journal 371, 205–210.CrossRefGoogle ScholarPubMed
Yamamoto, Y. and Gaynor, R. B. (2001) Therapeutic potential of inhibition of the NF-κB pathway in the treatment of inflammation and cancer. Journal of Clinical Investigation 107, 135– 142.CrossRefGoogle ScholarPubMed
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