Drosophila immune cells transport oxygen through PPO2 protein phase transition

Mingyu Shin, Eunji Chang, Daewon Lee, Nayun Kim, Bumsik Cho, Nuri Cha, Ferdinand Koranteng, Ji-Joon Song and Jiwon Shim ()
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Mingyu Shin: Hanyang University
Eunji Chang: Hanyang University
Daewon Lee: Hanyang University
Nayun Kim: Korea Advanced Institute of Science and Technology (KAIST)
Bumsik Cho: Hanyang University
Nuri Cha: Hanyang University
Ferdinand Koranteng: Hanyang University
Ji-Joon Song: Korea Advanced Institute of Science and Technology (KAIST)
Jiwon Shim: Hanyang University

Nature, 2024, vol. 631, issue 8020, 350-359

Abstract: Abstract Insect respiration has long been thought to be solely dependent on an elaborate tracheal system without assistance from the circulatory system or immune cells1,2. Here we describe that Drosophila crystal cells—myeloid-like immune cells called haemocytes—control respiration by oxygenating Prophenoloxidase 2 (PPO2) proteins. Crystal cells direct the movement of haemocytes between the trachea of the larval body wall and the circulation to collect oxygen. Aided by copper and a neutral pH, oxygen is trapped in the crystalline structures of PPO2 in crystal cells. Conversely, PPO2 crystals can be dissolved when carbonic anhydrase lowers the intracellular pH and then reassembled into crystals in cellulo by adhering to the trachea. Physiologically, larvae lacking crystal cells or PPO2, or those expressing a copper-binding mutant of PPO2, display hypoxic responses under normoxic conditions and are susceptible to hypoxia. These hypoxic phenotypes can be rescued by hyperoxia, expression of arthropod haemocyanin or prevention of larval burrowing activity to expose their respiratory organs. Thus, we propose that insect immune cells collaborate with the tracheal system to reserve and transport oxygen through the phase transition of PPO2 crystals, facilitating internal oxygen homeostasis in a process that is comparable to vertebrate respiration.

Date: 2024
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DOI: 10.1038/s41586-024-07583-x

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