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Eicosanoids and biogenic monoamines modulate the nodulation process and phenoloxidase activity in flesh flies

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Abstract

Insects have innate immunity comprising cellular and humoral defense reactions. Nodulation is a predominant cellular immune response to bacterial infections and the prophenoloxidase (PPO)-activating system acts in nodulation with a melanization reaction that darkens the nodules and produces reactive oxygen species that probably kill the bacteria. Although several eicosanoid actions have been reported in insect immune functions, these actions are relatively understudied among dipterans. We addressed this gap by exploring nodulation reactions to bacterial infections in the 3rd instar of the flesh fly Thomsonea argyrostoma. The Gram-positive bacterium, Micrococcus luteus, was injected either alone or coupled with eicosanoids biosynthesis inhibitors (EBIs). Nodulation exhibits a maximum at 24 h post injection. At zero time of control larvae, a constitutive level of phenoloxidase (PO) was found in plasma. Intrahemocoelic injection of M. luteus induces biosynthesis of PPO in hemocytes, and also its release into and activation in plasma via M. luteus challenge. EBIs suppress nodulation and PPO content of both hemocytes and plasma, but not PO content of plasma. The results imply the mediation of eicosanoids in PPO biosynthesis in hemocytes and its release, but not its activation in plasma. The injection of biogenic monoamines Octopamine (OA) and 5-hydroxytryptamine (5-HT) elevates nodulation and PPO biosynthesis and its activation in plasma.

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Abbreviations

5-HT:

5-hydroxytryptamine

BSA:

Bovine serum albumin

COXs:

Cyclooxygenases

Dex:

Dexamethazone

EBIs:

Eicosanoid biosynthesis inhibitors

hPI:

Hours post-injection

Ibu:

Ibuprofen

OA:

Octopamine

PBS:

Phosphate buffered saline

Phe:

Phenidone

PO:

Phenoloxidase

PPO:

Prophenoloxidase

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Acknowledgements

The author would like to thank Dr Satyavathi Valluri (Centre of Excellence for Genetics and Genomics of Silkmoths, Laboratory of Molecular Genetics, Centre for DNA Fingerprinting and Diagnostics, Hyderabad, India) for critical reading of the manuscript. We express our gratitude to the three anonymous reviewers for their meticulous review of our manuscript and their numerous perceptive remarks and recommendations.

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Authors and Affiliations

  1. Department of Entomology, Faculty of Science, Cairo University, Giza, 12613, Egypt

    Moataza A. Dorrah, Mona M. Ali & Taha T. M. Bassal

  2. Department of Biotechnology, Faculty of Science, Cairo University, Giza, 12613, Egypt

    Mona M. Ali

  3. Department of Zoology, Faculty of Science, King Saud University, Riyadh, 11451, Saudi Arabia

    Rasha K. Al‑Akeel

  4. Department of Biology, Faculty of Applied Sciences, Umm Al-Qura University, Makkah, 24381, Saudi Arabia

    Mariam S. Al‑Ghamdi

  5. Department of Biology, College of Science and Arts, Najran University, King Abdulaziz Road, Najran, 1988, Saudi Arabia

    Abdulrhman A. Almadiy

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  1. Moataza A. Dorrah
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  3. Rasha K. Al‑Akeel
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  5. Abdulrhman A. Almadiy
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TTMB and MAD conceived and designed research. MMA collected and reared experimental insects. MMA conducted experiments. AAA, RKA, and MSA analyzed data. TTMB, RKA, and MAD wrote and reviewed the manuscript. All authors read and approved the final manuscript.

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Correspondence to Abdulrhman A. Almadiy or Taha T. M. Bassal.

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Dorrah, M.A., Ali, M.M., Al‑Akeel, R.K. et al. Eicosanoids and biogenic monoamines modulate the nodulation process and phenoloxidase activity in flesh flies. Int J Trop Insect Sci 44, 711–722 (2024). https://doi.org/10.1007/s42690-024-01196-7

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