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The Effect of Extracellular Vesicles on the Regulation of Mitochondria Under Hypoxia Yaodan Zhang1,Jintan1,Yuyangmiao2 and Qiang Zhang 1

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The Effect of Extracellular Vesicles on the Regulation of Mitochondria Under Hypoxia Yaodan Zhang1,Jintan1,Yuyangmiao2 and Qiang Zhang 1 Zhang et al. Cell Death and Disease (2021) 12:358 https://doi.org/10.1038/s41419-021-03640-9 Cell Death & Disease REVIEW ARTICLE Open Access The effect of extracellular vesicles on the regulation of mitochondria under hypoxia Yaodan Zhang1,JinTan1,YuyangMiao2 and Qiang Zhang 1 Abstract Mitochondria are indispensable organelles for maintaining cell energy metabolism, and also are necessary to retain cell biological function by transmitting information as signal organelles. Hypoxia, one of the important cellular stresses, can directly regulates mitochondrial metabolites and mitochondrial reactive oxygen species (mROS), which affects the nuclear gene expression through mitochondrial retrograde signal pathways, and also promotes the delivery of signal components into cytoplasm, causing cellular injury. In addition, mitochondria can also trigger adaptive mechanisms to maintain mitochondrial function in response to hypoxia. Extracellular vesicles (EVs), as a medium of information transmission between cells, can change the biological effects of receptor cells by the release of cargo, including nucleic acids, proteins, lipids, mitochondria, and their compositions. The secretion of EVs increases in cells under hypoxia, which indirectly changes the mitochondrial function through the uptake of contents by the receptor cells. In this review, we focus on the mitochondrial regulation indirectly through EVs under hypoxia, and the possible mechanisms that EVs cause the changes in mitochondrial function. Finally, we discuss the significance of this EV-mitochondria axis in hypoxic diseases. 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; Facts Open Questions ● Hypoxia directly regulates mitochondrial ● Which specific substances contained in EVs plays a metabolism and mitochondrial compositions via key role in the regulation of mitochondria? HIF1α, and mitochondria can also trigger quality ● What are the specific mechanisms by which the control mechanisms to adapt to hypoxia. contents of EVs enter directly into the mitochondria ● As a medium of information transmission between of recipient cells? cells, extracellular vesicles can be regulated by ● Whether is there a mutual regulatory relationship hypoxia. among several pathways of mitochondrial transfer ● Extracellular vesicles containing mitochondria and between cells, including EVs, tunneling nanotubes, mitochondrial DNA transferred between cells to exophers etc? induce inflammatory response of receptor cells. ● Extracellular vesicles can also regulate mitochondrial Introduction function through a variety of mechanisms. Mitochondria are important organelles for maintaining cell energy metabolism. However, researchers over the last few decades have shown that mitochondria are necessary to maintain cell biological function by trans- mitting information as signal organelles. mROS and the Correspondence: Qiang Zhang ([email protected]) change of metabolites induced by hypoxic may cause the 1 Department of Geriatrics, Tianjin Medical University General Hospital, Tianjin changes of nuclear gene expression, which is called Geriatrics Institute, Tianjin, China 2Tianjin Medical University, Tianjin, China mitochondrial retrograde signaling (MtRS) pathways. Edited by J.-E. Ricci © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Official journal of the Cell Death Differentiation Association Zhang et al. Cell Death and Disease (2021) 12:358 Page 2 of 14 Mitochondria trigger multiple mechanisms to adapt to increasingly important role in the intercellular commu- – hypoxia, including the changes of oxidative phosphor- nication by exchanging contents between cells6,8 10.In ylation, mitophagy, mitochondrial fission, and fusion1. addition, each cell type may secrete different contents of Hypoxia plays a crucial role in progression of disease as EVs according to its physiological and stress state. Also, the main pathological mechanism of hypoxic diseases. the production, secretion and uptake of EVs can be In hypoxic diseases such as tumor2, ischemic disease3, affected well, which results in the corresponding biologi- mitochondria have multifunctional effects on cell damage cal changes of receptor cells. and disease progression, and targeting mitochondria could be a therapeutic direction. For instance, it has been Hypoxia shown that metformin can inhibit cellular respiration and Hypoxia refers to oxygen limitation in tissue. In animals, mitochondrial complex I activity of tumor cell to inhibit oxygen can be exchanged in the lungs, and more than 95% cancer progression4, and the combination of metformin of the oxygen will enter the capillaries through the exchange and PD1 checkpoint blockers led to increased tumor- system of alveolar-capillary. Most tissues of the body obtain infiltrating T cells function and tumor clearance5. Thus, sufficient oxygen from capillaries to meet their basic meta- targeting mitochondria through drug intervention may bolic requirements. Developing tumors rapidly outgrow change the disease process that are mediated by dys- their oxygen supply, the hypoxic tumor microenvironment functional mitochondria. ([PO2] < 10 mmHg, 1 mmHg O2 = 0.13% O2)isformed.It In recent years, it has been found that EVs can be has been known that hypoxic condition promotes tumor released by almost all types of cells. Hypoxia causes sig- progression, and it is necessary to improve hypoxic condi- nificant changes of the cargo, quantitative impact of tion to treat tumor11. secretion and the function of EVs. Mitochondria and their Different tissues have different oxygen tension, with components can also spread between cells through EVs levels of large intestine as low as 0.5% O2 and up to 13% and other pathways, promoting inflammation, cancer O2 in the lungs. However, the tissue oxygen levels of many progression, and the recovery of cellular function of major organs are 3–7%. Under the condition of mam- damaged mitochondria. As a carrier of intercellular malian cell culture, different degrees of the decline of cell information transmission, EVs can carry active molecules oxygen concentration, such as hypoxia (0.5–2% O2) and and act on mitochondria of receptor cells, which cause the severe O2 depletion (anoxic, <0.5% O2) have different change of mitochondrial function. Thus, the change of degrees of cell damage12,13. In mild hypoxia (4% oxygen), mitochondria function and composition is not only the non-cancerous macrophages migration is more related to result of direct stimulation by hypoxia, but also likely the HIF-1a-PDK1-mediated glycolytic reprogramming, and indirectly effect of EVs released by different physiological cytochrome C oxidase activity does not impair14, while and pathological states of cells. We will review how EVs the decline in mitochondrial oxygen availability may be and their contents change mitochondrial composition, the result of suppressing cytochrome C oxidase activity in function, and possible mechanisms, which will provide severely hypoxic conditions. Different cellular oxygen ideas for the future application of EVs targeting mito- concentrations regulate the glucose oxidation through chondrial pathway in hypoxic status. different pathways, which may be the reason for different cellular stress responses. It is reported that moderate Extracellular vesicles, hypoxia and mitochondria hypoxia (2.5% O2) in cultured spermatogonial stem Extracellular vesicles cells can maintain mild ROS levels, which triggers EVs are membrane vesicles secreted by almost all cells, the expression of the anti-apoptotic genes and promotes which can be divided into two main categories: exosomes the proliferation15. Osrodek et al. showed that the phe- and microvesicles, based on their biogenesis6. Micro- notype of melanoma cells and their response to drugs vesicles are formed by the outward budding of the plasma were different in hyperoxia (21% O2), normoxia (6% O2) membrane, whereas exosomes are originated from intra- and hypoxia (1% O2), which might partly explain the luminal vesicles (ILVs), which formed by the inward differences between results in vitro and in vivo16. Thus, budding of endosomal membrane in multivesicular the definition of hypoxia needs to be further regulated for endosomes (MVEs) and released by the fusion of MVEs experiments in vitro. and plasma membrane. Different EV subtypes have dif- ferent sizes, density ranges, and contents, but they cannot The role of mitochondria as signaling organelles be fully distinguished because of the overlap and technical Mitochondria as the main oxygen-consuming organs limitations7. Although the physical characteristics, bio- are a cellular organelle with two membranes. The outer genesis and contents of different subpopulations of EVs membrane encloses
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