iScience (Apr 2024)
Innexin hemichannel activation by Microplitis bicoloratus ecSOD monopolymer reduces ROS
- Jiang-Hui Meng,
- Yong-Biao Huang,
- Jin Long,
- Qiu-Chen Cai,
- Xin Qiao,
- Qiong-Li Zhang,
- Li-Dan Zhang,
- Xiang Yan,
- Rui Jing,
- Xing-Shan Liu,
- Sai-Jun Zhou,
- Yong-Sheng Yuan,
- Yin-Chen Ma,
- Li-Xiang Zhou,
- Nan-Nan Peng,
- Xing-Cheng Li,
- Cheng-Hui Cai,
- Hong-Mei Tang,
- André F. Martins,
- Jean X. Jiang,
- Kai-Jun Luo
Affiliations
- Jiang-Hui Meng
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Yong-Biao Huang
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Jin Long
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Qiu-Chen Cai
- Werner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, Eberhard Karls University Tübingen, 72076 Tübingen, Germany; Cluster of Excellence iFIT (EXC 2180) “Image-Guided and Functionally Instructed Tumor Therapies”, University of Tuebingen, 72076 Tübingen, Germany
- Xin Qiao
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Qiong-Li Zhang
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Li-Dan Zhang
- Department of Biochemistry and Structural Biology, University of Texas Health Science Center, San Antonio, TX 78229, USA
- Xiang Yan
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Rui Jing
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Xing-Shan Liu
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Sai-Jun Zhou
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Yong-Sheng Yuan
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Yin-Chen Ma
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Li-Xiang Zhou
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Nan-Nan Peng
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Xing-Cheng Li
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Cheng-Hui Cai
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- Hong-Mei Tang
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China
- André F. Martins
- Werner Siemens Imaging Center, Department of Preclinical Imaging and Radiopharmacy, Eberhard Karls University Tübingen, 72076 Tübingen, Germany; Cluster of Excellence iFIT (EXC 2180) “Image-Guided and Functionally Instructed Tumor Therapies”, University of Tuebingen, 72076 Tübingen, Germany
- Jean X. Jiang
- Department of Biochemistry and Structural Biology, University of Texas Health Science Center, San Antonio, TX 78229, USA
- Kai-Jun Luo
- School of Life Sciences, Yunnan University, Kunming, Yunnan 650500, P.R. China; Yunnan International Joint Laboratory of Virology & Immunology, Kunming, Yunnan 650500, P.R. China; Key Laboratory of the University in Yunnan Province for International Cooperation in Intercellular Communications and Regulations, Yunnan University, Kunming, Yunnan 650500, P.R. China; Corresponding author
- Journal volume & issue
-
Vol. 27,
no. 4
p. 109469
Abstract
Summary: The extracellular superoxide dismutases (ecSODs) secreted by Microplitis bicoloratus reduce the reactive oxygen species (ROS) stimulated by the Microplitis bicoloratus bracovirus. Here, we demonstrate that the bacterial transferase hexapeptide (hexapep) motif and bacterial-immunoglobulin-like (BIg-like) domain of ecSODs bind to the cell membrane and transiently open hemichannels, facilitating ROS reductions. RNAi-mediated ecSOD silencing in vivo elevated ROS in host hemocytes, impairing parasitoid larva development. In vitro, the ecSOD-monopolymer needed to be membrane bound to open hemichannels. Furthermore, the hexapep motif in the beta-sandwich of ecSOD49 and ecSOD58, and BIg-like domain in the signal peptides of ecSOD67 were required for cell membrane binding. Hexapep motif and BIg-like domain deletions induced ecSODs loss of adhesion and ROS reduction failure. The hexapep motif and BIg-like domain mediated ecSOD binding via upregulating innexins and stabilizing the opened hemichannels. Our findings reveal a mechanism through which ecSOD reduces ROS, which may aid in developing anti-redox therapy.