Ion Channels and Transporters in Autophagy

Overview

Journal Autophagy

Specialty Cell Biology

Date 2021 Mar 4

PMID 33657975

Citations 13

Authors

Ruoxi Zhang

Rui Kang

Daniel J Klionsky

Daolin Tang

Affiliations

Soon will be listed here.

Abstract

Ion exchange between intracellular and extracellular spaces is the basic mechanism for controlling cell metabolism and signal transduction. This process is mediated by ion channels and transporters on the plasma membrane, or intracellular membranes that surround various organelles, in response to environmental stimuli. Macroautophagy (hereafter referred to as autophagy) is one of the lysosomal-dependent degradation pathways that maintains homeostasis through the degradation and recycling of cellular components (e.g., dysfunctional proteins and damaged organelles). Although autophagy-related (ATG) proteins play a central role in regulating the formation of autophagy-related member structures (e.g., phagophores, autophagosomes, and autolysosomes), the autophagic process also involves changes in expression and function of ion channels and transporters. Here we discuss current knowledge of the mechanisms that regulate autophagy in mammalian cells, with special attention to the ion channels and transporters. We also highlight prospects for the development of drugs targeting ion channels and transporters in autophagy.

Citing Articles

Persistent Activation of the P2X7 Receptor Underlies Chronic Inflammation and Carcinogenic Changes in the Intestine.

Santana P, de Lima I, Silva E Souza K, Barbosa P, de Souza H Int J Mol Sci. 2024; 25(20).

PMID: 39456655 PMC: 11507540. DOI: 10.3390/ijms252010874.

SEC31a-ATG9a Interaction Mediates the Recruitment of COPII Vesicles for Autophagosome Formation.

Nie J, Ma S, Wu L, Li Y, Cao J, Li M Adv Sci (Weinh). 2024; 11(44):e2405127.

PMID: 39361436 PMC: 11600210. DOI: 10.1002/advs.202405127.

Role of Autophagy and AMPK in Cancer Stem Cells: Therapeutic Opportunities and Obstacles in Cancer.

Kovale L, Singh M, Kim J, Ha J Int J Mol Sci. 2024; 25(16).

PMID: 39201332 PMC: 11354724. DOI: 10.3390/ijms25168647.

Targeting paraptosis in cancer: opportunities and challenges.

Chen F, Tang H, Cai X, Lin J, Xiang L, Kang R Cancer Gene Ther. 2024; 31(3):349-363.

PMID: 38177306 DOI: 10.1038/s41417-023-00722-y.

TRPM2 protects against cisplatin-induced acute kidney injury and mitochondrial dysfunction via modulating autophagy.

Yu B, Jin L, Yao X, Zhang Y, Zhang G, Wang F Theranostics. 2023; 13(13):4356-4375.

PMID: 37649595 PMC: 10465213. DOI: 10.7150/thno.84655.

References

Sun X, Cao Y, Hu L, Yang Y, Li J, Wang F . ASICs mediate the modulatory effect by paeoniflorin on α-synuclein autophagic degradation. Brain Res. 2011; 1396:77-87. DOI: 10.1016/j.brainres.2011.04.011. View

Fliegert R, Bauche A, Wolf Perez A, Watt J, Rozewitz M, Winzer R . 2'-Deoxyadenosine 5'-diphosphoribose is an endogenous TRPM2 superagonist. Nat Chem Biol. 2017; 13(9):1036-1044. PMC: 5563452. DOI: 10.1038/nchembio.2415. View

Sun-Wada G, Wada Y . Role of vacuolar-type proton ATPase in signal transduction. Biochim Biophys Acta. 2015; 1847(10):1166-72. DOI: 10.1016/j.bbabio.2015.06.010. View

Zhang X, Hu M, Yang Y, Xu H . Organellar TRP channels. Nat Struct Mol Biol. 2018; 25(11):1009-1018. PMC: 6785982. DOI: 10.1038/s41594-018-0148-z. View

Wallings R, Connor-Robson N, Wade-Martins R . LRRK2 interacts with the vacuolar-type H+-ATPase pump a1 subunit to regulate lysosomal function. Hum Mol Genet. 2019; 28(16):2696-2710. PMC: 6687951. DOI: 10.1093/hmg/ddz088. View

Tian X, Gala U, Zhang Y, Shang W, Jaiswal S, di Ronza A . A voltage-gated calcium channel regulates lysosomal fusion with endosomes and autophagosomes and is required for neuronal homeostasis. PLoS Biol. 2015; 13(3):e1002103. PMC: 4374850. DOI: 10.1371/journal.pbio.1002103. View

Mauvezin C, Neufeld T . Bafilomycin A1 disrupts autophagic flux by inhibiting both V-ATPase-dependent acidification and Ca-P60A/SERCA-dependent autophagosome-lysosome fusion. Autophagy. 2015; 11(8):1437-8. PMC: 4590655. DOI: 10.1080/15548627.2015.1066957. View

Bultynck G, Kiviluoto S, Henke N, Ivanova H, Schneider L, Rybalchenko V . The C terminus of Bax inhibitor-1 forms a Ca2+-permeable channel pore. J Biol Chem. 2011; 287(4):2544-57. PMC: 3268414. DOI: 10.1074/jbc.M111.275354. View

Wartosch L, Stauber T . A role for chloride transport in lysosomal protein degradation. Autophagy. 2010; 6(1):158-9. DOI: 10.4161/auto.6.1.10590. View

10.

Wyrsch P, Blenn C, Bader J, Althaus F . Cell death and autophagy under oxidative stress: roles of poly(ADP-Ribose) polymerases and Ca(2+). Mol Cell Biol. 2012; 32(17):3541-53. PMC: 3422003. DOI: 10.1128/MCB.00437-12. View

11.

Levine B, Kroemer G . Biological Functions of Autophagy Genes: A Disease Perspective. Cell. 2019; 176(1-2):11-42. PMC: 6347410. DOI: 10.1016/j.cell.2018.09.048. View

12.

Graves A, Curran P, Smith C, Mindell J . The Cl-/H+ antiporter ClC-7 is the primary chloride permeation pathway in lysosomes. Nature. 2008; 453(7196):788-92. DOI: 10.1038/nature06907. View

13.

Decuypere J, Kindt D, Luyten T, Welkenhuyzen K, Missiaen L, De Smedt H . mTOR-Controlled Autophagy Requires Intracellular Ca(2+) Signaling. PLoS One. 2013; 8(4):e61020. PMC: 3614970. DOI: 10.1371/journal.pone.0061020. View

14.

Zheng Y, Chen Z, Gu Z, Yang X, Yu M, Zhao C . Starvation-induced autophagy is up-regulated via ROS-mediated ClC-3 chloride channel activation in the nasopharyngeal carcinoma cell line CNE-2Z. Biochem J. 2019; 476(9):1323-1333. DOI: 10.1042/BCJ20180979. View

15.

Raffaello A, Mammucari C, Gherardi G, Rizzuto R . Calcium at the Center of Cell Signaling: Interplay between Endoplasmic Reticulum, Mitochondria, and Lysosomes. Trends Biochem Sci. 2016; 41(12):1035-1049. PMC: 5123979. DOI: 10.1016/j.tibs.2016.09.001. View

16.

Huang P, Xu M, Wu Y, Rizvi Syeda A, Dong X . Multiple facets of TRPML1 in autophagy. Cell Calcium. 2020; 88:102196. DOI: 10.1016/j.ceca.2020.102196. View

17.

Vicencio J, Ortiz C, Criollo A, Jones A, Kepp O, Galluzzi L . The inositol 1,4,5-trisphosphate receptor regulates autophagy through its interaction with Beclin 1. Cell Death Differ. 2009; 16(7):1006-17. DOI: 10.1038/cdd.2009.34. View

18.

Sui H, Luo M, Miao Y, Cheng W, Wen S, Zhao B . Cystic fibrosis transmembrane conductance regulator ameliorates lipopolysaccharide-induced acute lung injury by inhibiting autophagy through PI3K/AKT/mTOR pathway in mice. Respir Physiol Neurobiol. 2019; 273:103338. DOI: 10.1016/j.resp.2019.103338. View

19.

Hou X, Xiao H, Zhang Y, Zeng X, Huang M, Chen X . Transient receptor potential channel 6 knockdown prevents apoptosis of renal tubular epithelial cells upon oxidative stress via autophagy activation. Cell Death Dis. 2018; 9(10):1015. PMC: 6170481. DOI: 10.1038/s41419-018-1052-5. View

20.

Qi X, Man S, Malireddi R, Karki R, Lupfer C, Gurung P . Cathepsin B modulates lysosomal biogenesis and host defense against Francisella novicida infection. J Exp Med. 2016; 213(10):2081-97. PMC: 5030800. DOI: 10.1084/jem.20151938. View