Research progress of hypoxia-induced mitochondrial autophagy and glucose metabolism reprogramming in gastric precancerous lesions

Jiaxiang ZHANG; Yongxue ZHOU; Shuguang YAN; Weihan ZHAO; Fen DONG

doi:10.19401/j.cnki.1007-3639.2022.10.009

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Research progress of hypoxia-induced mitochondrial autophagy and glucose metabolism reprogramming in gastric precancerous lesions

Review | 更新时间：2025-12-31

- Research progress of hypoxia-induced mitochondrial autophagy and glucose metabolism reprogramming in gastric precancerous lesions
- China Oncology Vol. 32, Issue 10, Pages: 1007-1015(2022)
- 作者机构：
  
  1. 陕西中医药大学基础医学院，陕西咸阳 712046
  2. 陕西中医药大学附属医院消化科，陕西咸阳 712000
  3. 陕西中医药大学第二附属医院肿瘤科，陕西咸阳 712000
- 作者简介：
- 基金信息：
- DOI：10.19401/j.cnki.1007-3639.2022.10.009
  CLC： R735.2
- Received：26 January 2022，
  
  Revised：2022-06-03，
  
  Published Online：30 October 2022，
- 稿件说明：
移动端阅览
Jiaxiang ZHANG, Yongxue ZHOU, Shuguang YAN, et al. Research progress of hypoxia-induced mitochondrial autophagy and glucose metabolism reprogramming in gastric precancerous lesions[J]. China Oncology, 2022, 32(10): 1007-1015.
DOI：

Jiaxiang ZHANG, Yongxue ZHOU, Shuguang YAN, et al. Research progress of hypoxia-induced mitochondrial autophagy and glucose metabolism reprogramming in gastric precancerous lesions[J]. China Oncology, 2022, 32(10): 1007-1015. DOI： 10.19401/j.cnki.1007-3639.2022.10.009.

摘要

胃癌前病变（gastric precancerous lesions，GPL）是胃癌发生前的特殊组织病理学变化阶段，对GPL施以有效的干预是防止其恶化进展至胃癌的关键环节。GPL的胃黏膜组织炎症水平较高，大量的炎症细胞、炎症因子及炎症介质高水平代谢使耗氧量上升，导致了GPL阶段胃黏膜的缺氧微环境形成，这种缺氧状态利于线粒体自噬与糖代谢重编程的发生。线粒体自噬作为一种保守的生物学过程存在于机体多种组织细胞中，可通过形成自噬小体包裹功能损坏的线粒体并与溶酶体结合对目标线粒体进行消化、再利用，合适的自噬水平可防止GPL异型细胞的过度增殖，抑制GPL进展。然而，线粒体自噬活性在GPL病程中受到了抑制，同时GPL阶段细胞糖代谢重编程为糖酵解的活性升高。糖酵解是一种细胞缺氧状态下的能量代谢方式，它能加快细胞的能量供给，使异型细胞增殖加快进而加速GPL恶化。一些证据表明，线粒体自噬与糖代谢重编程之间可能存在一定的相互制约的关系，GPL过程中自噬的抑制一方面能引起糖酵解活性的提高，而另一方面，自噬水平的升高抑制了糖酵解的活性。目前尚不清楚自噬与糖酵解的具体关系及作用机制，但GPL胃黏膜由缺氧、细菌感染、炎症、氧化应激、信号分子活化紊乱等因素构成的复杂病理学环境可能是造成低自噬水平与高糖酵解活性的关键。参与缺氧适应的缺氧诱导因子1α（hypoxia inducible factor 1α，HIF-1α）在GPL阶段的胃黏膜中稳定表达，充当着启动自噬与糖酵解的开关，但HIF-1α在GPL的病理学过程中似乎更多参与了对糖酵解的调控，造成这种变化的原因可能就与上述病理学因素有关。幽门螺杆菌（helicobacter pylori，

H. pylori

）感染、磷脂酰肌醇3-激酶（phosphoinositide3-kinase，PI3K）/蛋白激酶B（protein kinase，AKT）/ 哺乳动物雷帕霉素靶蛋白（mammalian target of rapamycin，mTOR）信号转导通路活化等因素抑制了自噬的发生，而自噬抑制后活性氧（reactive oxygen species，ROS）的不断累积、

H. pylori

持续感染所引起的炎症加剧能促进核因子κB（nuclear factor kappa-B，NF-κB）、信号转导及转录激活蛋白3（signal transducer and activator of transcription 3，STAT3）以及PI3K/AKT/mTOR等信号转导通路间一系列信号交互与协同作用，进而间接作用于HIF-1α促进糖酵解或直接提高糖酵解水平。HIF-1α可能受GPL病理微环境及其上游复杂信号的调控更多参与了糖酵解的激活，从而无法充分活化缺氧启动自噬的BNIP-3，导致自噬水平的下调或抑制，而自噬的抑制又间接促进了糖酵解水平提高，形成恶性循环，最终导致GPL恶化。本文对缺氧诱导的线粒体自噬与糖代谢重编程对胃癌的癌前病变影响进行综述。

Abstract

Gastric precancerous lesions (GPL) are a special histopathological stage before

the occurrence of gastric cancer. Effective treatment of GPL is the key to preventing its progression to gastric cancer. GPL has a high level of inflammation in gastric mucosa

and a large number of inflammatory cells

inflammatory factors and inflammatory mediators are metabolized at a high level

which increases oxygen consumption and leads to the formation of a hypoxia microenvironment in gastric mucosa at the GPL stage

which is conducive to the initiation of mitochondrial autophagy and glucose metabolism reprogramming. As a conserved biological process

mitochondrial autophagy exists in various tissues and cells of the body. It can form autophagosome to wrap mitochondria with damaged functions and bind with lysosomes to digest and reuse target mitochondria. Appropriate autophagy level can prevent excessive proliferation of GPL heterotype cells and inhibit the progress of GPL. However

mitochondrial autophagy activity is inhibited during the course of GPL

and the activity of glycometabolic reprogramming into glycolysis is increased during GPL. Glycolysis is a way of energy metabolism in the hypoxia state of cells

which can accelerate the energy supply of cells and the proliferation of abnormal cells

and thus accelerate the deterioration of GPL. Some evidences suggest that there may be a mutually restricting relationship between mitochondrial autophagy and glycolysis reprogramming. The inhibition of autophagy in GPL can increase glycolysis activity on the one hand

while the increase of autophagy inhibits glycolysis activity on the other hand. At present

the specific relationship and mechanism of autophagy and glycolysis are not clear

however

the complex pathological environment of GPL gastric mucosa composed of hypoxia

bacterial infection

inflammation

oxidative stress

activation disorder of signal molecules and other factors may be the key to the low autophagy level and high glycolysis activity. Hypoxia-inducible factor 1α (HIF-1α)

which is involved in hypoxia adaptation

is stably expressed in ga

stric mucosa at the GPL stage and acts as a switch to initiate autophagy and glycolysis. However

HIF-1α seems to be more involved in the regulation of glycolysis in the pathological process of GPL. The cause of this change may be related to the above-mentioned pathological factors.

H. pylori

infection

activation of phosphoinositide 3-kinase (PI3K)/protein kinase (AKT)/mammalian target of rapamycin (mTOR) pathway and other factors inhibit autophagy. However

the continuous accumulation of reactive oxygen species (ROS) after autophagy inhibition and the aggravation of inflammation caused by

H. pylori

infection can promote a series of signal interactions and synergies among nuclear factor kappa-B (NF-Κb)

signal transducer and activator of transcription 3 (STAT3) and PI3K/AKT/mTOR signaling pathways

and thus indirectly affect HIF-1α to promote glycolysis or directly improve glycolysis level. HIF-1α may be more involved in the activation of glycolysis due to the regulation of GPL pathological microenvironment and its upstream complex signals

thus unable to fully activate BNIP-3 mediated hypoxia-initiated autophagy

leading to the down-regulation or inhibition of autophagy level

and the inhibition of autophagy indirectly promotes the improvement of glycolysis level

forming a vicious cycle

and ultimately leading to the deterioration of GPL. This article reviewed the research progress of hypoxia-induced mitochondrial autophagy and glucose metabolism reprogramming in gastric precancerous lesions.

关键词

Keywords

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