ROS-mediated BNIP3-dependent mitophagy promotes coelomocyte survival in Apostichopus japonicus in response to Vibrio splendidus infection

Lian-Lian Sun; Yi-Na Shao; Mei-Xiang You; Cheng-Hua Li

doi:10.24272/j.issn.2095-8137.2021.460

Volume 43 Issue 2

Mar. 2022

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Article Navigation > Zoological Research > 2022 > 43(2): 285-300

Lian-Lian Sun, Yi-Na Shao, Mei-Xiang You, Cheng-Hua Li. ROS-mediated BNIP3-dependent mitophagy promotes coelomocyte survival in Apostichopus japonicus in response to Vibrio splendidus infection. Zoological Research, 2022, 43(2): 285-300. doi: 10.24272/j.issn.2095-8137.2021.460

Citation:

Lian-Lian Sun, Yi-Na Shao, Mei-Xiang You, Cheng-Hua Li. ROS-mediated BNIP3-dependent mitophagy promotes coelomocyte survival in Apostichopus japonicus in response to Vibrio splendidus infection. Zoological Research, 2022, 43(2): 285-300. doi: 10.24272/j.issn.2095-8137.2021.460

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ROS-mediated BNIP3-dependent mitophagy promotes coelomocyte survival in Apostichopus japonicus in response to Vibrio splendidus infection

doi: 10.24272/j.issn.2095-8137.2021.460

Lian-Lian Sun^{1, 3},
Yi-Na Shao^{1, 3},
Mei-Xiang You^{1, 3},
Cheng-Hua Li^{1, 2, 3
,
,}

1.
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, Zhejiang 315211, China
2.
Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, Shandong 266071, China
3.
State-Province Joint Laboratory of Marine Biotechnology and Engineering, Ningbo University, Ningbo, Zhejiang 315211, China

Funds: This work was supported by the National Natural Science Foundation of China (32073003, 32102825), Natural Science Foundation of Zhejiang Province (LZ19C190001), Key Project from Science Technology Department of Zhejiang Province (2019R52016), and K.C. Wong Magna Fund in Ningbo University

More Information

Corresponding author: E-mail: lichenghua@nbu.edu.cn
Received Date: 2022-01-20
Accepted Date: 2022-02-23

Published Online: 2022-03-01

Publish Date: 2022-03-18

Abstract

Abstract

Organisms produce high levels of reactive oxygen species (ROS) to kill pathogens or act as signaling molecules to induce immune responses; however, excessive ROS can result in cell death. To maintain ROS balance and cell survival, mitophagy selectively eliminates damaged mitochondria via mitophagy receptors in vertebrates. In marine invertebrates, however, mitophagy and its functions remain largely unknown. In the current study, Vibrio splendidus infection damaged mitochondrial morphology in coelomocytes and reduced mitochondrial membrane potential (ΔΨm) and mitophagosome formation. The colocalization of mitochondria and lysosomes further confirmed that lipopolysaccharide (LPS) treatment increased mitophagy flux. To explore the regulatory mechanism of mitophagy, we cloned Bcl2/adenovirus E1B 19 kDa protein-interacting protein 3 (BNIP3), a common mitophagy receptor, from sea cucumber Apostichopus japonicus (AjBNIP3) and confirmed that AjBNIP3 was significantly induced and accumulated in mitochondria after V. splendidus infection and LPS exposure. At the mitochondrial membrane, AjBNIP3 interacts with microtubule-associated protein 1 light chain 3 (LC3) on phagophore membranes to mediate mitophagy. After AjBNIP3 interference, mitophagy flux decreased significantly. Furthermore, AjBNIP3-mediated mitophagy was activated by ROS following the addition of exogenous hydrogen peroxide (H₂O₂), ROS scavengers, and ROS inhibitors. Finally, inhibition of BNIP3-mediated mitophagy by AjBNIP3 small interfering RNA (siRNA) or high concentrations of lactate increased apoptosis and decreased coelomocyte survival. These findings highlight the essential role of AjBNIP3 in damaged mitochondrial degradation during mitophagy. This mitophagy activity is required for coelomocyte survival in A. japonicus against V. splendidus infection.

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References(70)

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