A SWELL time to develop the molecular pharmacology of the volume-regulated anion channel (VRAC)

References

• Churchwell KB, Wright SH, Emma F, et al. NMDA receptor activation inhibits neuronal volume regulation after swelling induced by veratridine-stimulated Na+ influx in rat cortical cultures. J Neurosci. 1996;16(23):7447–7457.
   PubMed Web of Science ®Google Scholar
• Strange K. Cellular volume homeostasis. Adv Physiol Educ. 2004;28(1–4):155–159.
   PubMed Web of Science ®Google Scholar
• Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev. 2009;89(1):193–277.
   PubMed Web of Science ®Google Scholar
• Lang F, Lepple-Wienhues A, Paulmichl M, et al. Ion channels, cell volume, and apoptotic cell death. Cell Physiol Biochem. 1998;8:285–292.
   PubMedGoogle Scholar
• Wehner F, Olsen H, Tinel H, et al. Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Rev Physiol Biochem Pharmacol. 2003;148:1–80.
   PubMed Web of Science ®Google Scholar
• Evans DH. Osmotic and ionic regulation: cells and animals. Boca Raton: CRC Press; 2009. p. xvi, 590, 8 of plates.
   Google Scholar
• Strange K, Yamada T, Denton JS. A 30-year journey from volume-regulated anion currents to molecular structure of the LRRC8 channel. J Gen Physiol. 2019;151(2):100–117.
   PubMed Web of Science ®Google Scholar
• Voss FK, Ullrich F, Münch J, et al. Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science. 2014;344(6184):634–638.
   PubMed Web of Science ®Google Scholar
• Qiu Z, Dubin A, Mathur J, et al. SWELL1, a plasma membrane protein, is an essential component of volume-regulated anion channel. Cell. 2014;157(2):447–458.
   PubMed Web of Science ®Google Scholar
• Abascal F, Zardoya R. LRRC8 proteins share a common ancestor with pannexins, and may form hexameric channels involved in cell-cell communication. Bioessays. 2012;34(7):551–560.
   PubMed Web of Science ®Google Scholar
• Nakamura R, Numata T, Kasuya G, et al. Cryo-EM structure of the volume-regulated anion channel LRRC8D isoform identifies features important for substrate permeation. Commun Biol. 2020;3(1):240.
   PubMed Web of Science ®Google Scholar
• Kern DM, Oh S, Hite RK, Brohawn SG . Cryo-EM structures of the DCPIB-inhibited volume-regulated anion channel LRRC8A in lipid nanodiscs. Elife. 2019;8:e42636. doi: 10.7554/eLife.42636.
   PubMed Web of Science ®Google Scholar
• Kasuya G, Nakane T, Yokoyama T, et al. Cryo-EM structures of the human volume-regulated anion channel LRRC8. Nat Struct Mol Biol. 2018;25(9):797–804.
   PubMed Web of Science ®Google Scholar
• Kefauver JM, Saotome K, Dubin AE, et al. Structure of the human volume regulated anion channel. Elife. 2018;7. DOI:10.7554/eLife.38461
   PubMed Web of Science ®Google Scholar
• Deneka D, Sawicka M, Lam AKM, et al. Structure of a volume-regulated anion channel of the LRRC8 family. Nature. 2018;558(7709):254–259.
   PubMed Web of Science ®Google Scholar
• Zhou C, Chen X, Planells-Cases R, et al. Transfer of cGAMP into bystander cells via LRRC8 volume-regulated anion channels augments STING-mediated interferon responses and anti-viral immunity. Immunity. 2020;52(5):767–781 e6.
   PubMed Web of Science ®Google Scholar
• Lahey LJ, Mardjuki RE, et al. The LRRC8A:C heteromeric channel is a cGAMP Transporter and the Dominant cGAMP importer in human vasculature cells. bioRxiv. 2020;2020.02.13.948273.
   Google Scholar
• Alghanem AF, Abello J, et al. The SWELL1-LRRC8 complex regulates endothelial AKT-eNOS-mTOR signaling and vascular function. bioRxiv. 2020;2020.08.04.236182.
   Google Scholar
• Osei-Owusu J, Yang J, et al. Molecular biology and physiology of volume-regulated anion channel (VRAC). Curr Top Membr. 2018;81:177–203.
   PubMed Web of Science ®Google Scholar
• Chen L, König B, Liu T, et al. More than just a pressure relief valve: physiological roles of volume-regulated LRRC8 anion channels. Biol Chem. 2019;400(11):1481–1496.
   PubMed Web of Science ®Google Scholar
• Gunasekar SK, Xie L, Sah R. SWELL signalling in adipocytes: can fat ‘feel’ fat? Adipocyte. 2019;8(1):223–228.
   PubMed Web of Science ®Google Scholar
• Gunasekar SK, Litao Xie, et al. Small molecule SWELL1-LRRC8 complex induction improves glycemic control and nonalcoholic fatty liver disease in murine Type 2 diabetes. bioRxiv. 2021;2021.02.28.432901.
   Google Scholar
• Knauf PA, Rothstein A. Chemical modification of membranes. II. Permeation paths for sulfhydryl agents. J Gen Physiol. 1971;58(2):211–223.
   PubMed Web of Science ®Google Scholar
• Russell JM, Boron WF. Role of choloride transport in regulation of intracellular pH. Nature. 1976;264(5581):73–74.
   PubMed Web of Science ®Google Scholar
• Russell JM, Brodwick MS. Properties of chloride transport in barnacle muscle fibers. J Gen Physiol. 1979;73(3):343–368.
   PubMed Web of Science ®Google Scholar
• White MM, Miller C. A voltage-gated anion channel from the electric organ of Torpedo californica. J Biol Chem. 1979;254(20):10161–10166.
   PubMed Web of Science ®Google Scholar
• Ehrenspeck G, Brodsky WA. Effects of 4-acetamido-4’-isothiocyano-2,2-disulfonic stilbene on ion transport in turtle bladders. Biochim Biophys Acta. 1976;419(3):555–558.
   PubMedGoogle Scholar
• Kubo M, Okada Y. Volume-regulatory Cl- channel currents in cultured human epithelial cells. J Physiol. 1992;456:351–371.
   PubMed Web of Science ®Google Scholar
• Dick GM, Kong ID, Sanders KM. Effects of anion channel antagonists in canine colonic myocytes: comparative pharmacology of Cl-, Ca2+ and K+ currents. Br J Pharmacol. 1999;127(8):1819–1831.
   PubMed Web of Science ®Google Scholar
• Helix N, Strabaek D, Dahl BH, et al. Inhibition of the endogenous volume-regulated anion channel (VRAC) in HEK293 cells by acidic di-aryl-ureas. J Membr Biol. 2003;196(2):83–94.
   PubMed Web of Science ®Google Scholar
• Stott JB, deCourcey F, Ennis M, et al. Functional and pharmacological characterization of volume-regulated anion channels in human normal and cystic fibrosis bronchial and nasal epithelial cells. Eur J Pharmacol. 2014;740:183–191.
   PubMed Web of Science ®Google Scholar
• Boese SH, Kinne RHK, Wehner F. Single-channel properties of swelling-activated anion conductance in rat inner medullary collecting duct cells. Am J Physiol (Renal Fluid Electrolyte Physiol.40). 1996;271:F1224–F1233.
   PubMed Web of Science ®Google Scholar
• Sato-Numata K, Numata T, Inoue R, et al. Distinct pharmacological and molecular properties of the acid-sensitive outwardly rectifying (ASOR) anion channel from those of the volume-sensitive outwardly rectifying (VSOR) anion channel. Pflugers Arch. 2016;468(5):795–803.
   PubMed Web of Science ®Google Scholar
• Bakhramov A, Fenech C, Bolton TB. Chloride current activated by hypotonicity in cultured human astrocytoma cells. Exp Physiol. 1995;80(3):373–389.
   PubMed Web of Science ®Google Scholar
• Decher N, Lang HJ, Nilius B, et al. DCPIB is a novel selective blocker of ICl,swell and prevents swelling-induced shortening of Guinea-pig atrial action potential duration. Br J Pharmacol. 2001;134(7):1467–1479.
   PubMed Web of Science ®Google Scholar
• Abdullaev IF, Rudkouskaya A, Schools GP, et al. Pharmacological comparison of swelling-activated excitatory amino acid release and Cl− currents in cultured rat astrocytes. J Physiol. 2006;572(Pt 3):677–689.
   PubMed Web of Science ®Google Scholar
• Akita T, Okada Y. Regulation of bradykinin-induced activation of volume-sensitive outwardly rectifying anion channels by Ca2+ nanodomains in mouse astrocytes. J Physiol. 2011;589(Pt 16):3909–3927.
   PubMed Web of Science ®Google Scholar
• Harrigan TJ, Abdullaev IF, et al. Activation of microglia with zymosan promotes excitatory amino acid release via volume-regulated anion channels: the role of NADPH oxidases. J Neurochem. 2008;106(6):2449–2462.
   PubMed Web of Science ®Google Scholar
• Bantel C, Maze M, Trapp S. Neuronal preconditioning by inhalational anesthetics: evidence for the role of plasmalemmal adenosine triphosphate-sensitive potassium channels. Anesthesiology. 2009;110(5):986–995.
   PubMed Web of Science ®Google Scholar
• Schlichter LC, Mertens T, Liu B. Swelling activated Cl- channels in microglia: biophysics, pharmacology and role in glutamate release. Channels (Austin). 2011;5(2):128–137.
   PubMed Web of Science ®Google Scholar
• Yamada T, Figueroa EE, et al. LRRC8A homohexameric channels poorly recapitulate VRAC regulation and pharmacology. Am J Physiol Cell Physiol. 2021;320(3):C293–C303.
   PubMed Web of Science ®Google Scholar
• Sabirov RZ, Okada Y. ATP release via anion channels. Purinergic Signal. 2005;1(4):311–328.
   PubMedGoogle Scholar
• Sabirov RZ, Merzlyak PG, et al. The properties, functions, and pathophysiology of maxi-anion channels. Pflugers Arch. 2016;468(3):405–420.
   PubMed Web of Science ®Google Scholar
• Afzal A, Figueroa EE, Kharade SV, et al. The LRRC8 volume-regulated anion channel inhibitor, DCPIB, inhibits mitochondrial respiration independently of the channel. Physiol Rep. 2019;7(23):e14303.
   PubMed Web of Science ®Google Scholar
• Bowens NH, Dohare P, Kuo Y-H, et al. DCPIB, the proposed selective blocker of volume-regulated anion channels, inhibits several glutamate transport pathways in glial cells. Mol Pharmacol. 2013;83(1):22–32.
   PubMed Web of Science ®Google Scholar
• Minieri L, Pivonkova H, Caprini M, et al. The inhibitor of volume-regulated anion channels DCPIB activates TREK potassium channels in cultured astrocytes. Br J Pharmacol. 2013;168(5):1240–1254.
   PubMed Web of Science ®Google Scholar
• Fujii T, Takahashi Y, Takeshima H, et al. Inhibition of gastric H+,K+-ATPase by 4-(2-butyl-6,7-dichloro-2-cyclopentylindan-1-on-5-yl)oxybutyric acid (DCPIB), an inhibitor of volume-regulated anion channel. Eur J Pharmacol. 2015;765:34–41.
   PubMed Web of Science ®Google Scholar
• Deng W, Mahajan R, Baumgarten CM, et al. The ICl,swell inhibitor DCPIB blocks Kir channels that possess weak affinity for PIP2. Pflugers Arch. 2016;468(5):817–824.
   PubMed Web of Science ®Google Scholar
• Kurbannazarova RS, Bessonova SV, Okada Y, et al. Swelling-activated anion channels are essential for volume regulation of mouse thymocytes. Int J Mol Sci. 2011;12(12):9125–9137.
   PubMed Web of Science ®Google Scholar
• Klausen TK, Bergdahl A, Hougaard C, et al. Cell cycle-dependent activity of the volume- and Ca2+-activated anion currents in Ehrlich lettre ascites cells. J Cell Physiol. 2007;210(3):831–842.
   PubMed Web of Science ®Google Scholar
• Fan HT, Morishima S, Kida H, et al. Phloretin differentially inhibits volume-sensitive and cyclic AMP-activated, but not Ca-activated, Cl − channels. Br J Pharmacol. 2001;133(7):1096–1106.
   PubMed Web of Science ®Google Scholar
• Zhang J, Dawson VL, Dawson TM, et al. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science. 1994;263:687–689.
   PubMed Web of Science ®Google Scholar
• Tominaga M, Tominaga T, Miwa A, et al. Volume-sensitive chloride channel activity does not depend on endogenous P-glycoprotein. J Biol Chem. 1995;270(46):27887–27893.
   PubMed Web of Science ®Google Scholar
• Hechenberger M, Schwappach B, Fischer WN, et al. A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. J Biol Chem. 1996;271(52):33632–33638.
   PubMed Web of Science ®Google Scholar
• Wondergem R, Gong W, Monen SH, et al. Blocking swelling-activated chloride current inhibits mouse liver cell proliferation. J Physiol. 2001;532:661–672.
   PubMed Web of Science ®Google Scholar
• Chen L, Wang L, et al. Cell cycle-dependent expression of volume-activated chloride currents in nasopharyngeal carcinoma cells. Am J Physiol Cell Physiol. 2002;283(4):C1313–23.
   PubMed Web of Science ®Google Scholar
• Yang X, Zhu L, et al. Cisplatin activates volume-sensitive like chloride channels via purinergic receptor pathways in nasopharyngeal carcinoma cells. J Membr Biol. 2015;248(1):19–29.
   PubMed Web of Science ®Google Scholar
• Leaney JL, Marsh SJ, Brown DA. A swelling-activated chloride current in rat sympathetic neurones. J Physiol. 1997;501(3):555–564.
   PubMed Web of Science ®Google Scholar
• Zhang H, Cao HJ, et al. Volume regulated anion channel currents of rat hippocampal neurons and their contribution to oxygen-and-glucose deprivation induced neuronal death. PLoS One. 2011;6(2):e16803.
   PubMed Web of Science ®Google Scholar
• Inoue H, Mori S-I, Morishima S, et al. Volume-sensitive chloride channels in mouse cortical neurons: characterization and role in volume regulation. Eur J Neurosci. 2005;21(6):1648–1658.
   PubMed Web of Science ®Google Scholar
• Benfenati V, Caprini M, Nicchia GP, et al. Carbenoxolone inhibits volume-regulated anion conductance in cultured rat cortical astroglia. Channels (Austin). 2009;3(5):323–336.
   PubMed Web of Science ®Google Scholar
• Gaitan-Penas H, Gradogna A, et al. Investigation of LRRC8-mediated volume-regulated anion currents in xenopus oocytes. Biophys J. 2016;111(7):1429–1443.
   PubMed Web of Science ®Google Scholar
• Jayaraman S, Haggie P, Wachter RM, et al. Mechanism and cellular applications of a green fluorescent protein-based halide sensor. J Biol Chem. 2000;275(9):6047–6050.
   PubMed Web of Science ®Google Scholar
• Galietta LJ, Haggie PM, Verkman AS. Green fluorescent protein-based halide indicators with improved chloride and iodide affinities. FEBS Lett. 2001;499(3):220–224.
   PubMed Web of Science ®Google Scholar
• Tertyshnikova S, Dworetzky S, et al. Cell-based assay for the quantitative high throughput screening of gamma-aminobutyric acid-induced halide transport. Google Patents. 2006.
   Google Scholar
• Verkman AS, Galietta LJ. Chloride channels as drug targets. Nat Rev Drug Discov. 2009;8(2):153–171.
   PubMed Web of Science ®Google Scholar
• Yamaguchi T, Kohrogi H, Honda I, et al. A novel leukotriene antagonist, ONO-1078, Inhibits and reverses human bronchial contraction induced by leukotrienes C4 and D 4 and antigen in vitro. Am Rev Respir Dis. 1992;146(4):923–929.
   PubMedGoogle Scholar
• Yamaguchi T, Kohrogi H, Honda I, et al. Preventive effect of a novel leukotrienes antagonist ONO-1078 on leukotriene C4- and D4-induced human bronchial smooth muscle contraction. Arerugi. 1990;39(11):1477–1483.
   PubMedGoogle Scholar
• Heise CE, O’Dowd BF, Figueroa DJ, et al. Characterization of the human cysteinyl leukotriene 2 receptor. J Biol Chem. 2000;275(39):30531–30536.
   PubMed Web of Science ®Google Scholar
• Lynch KR, O’Neill GP, Liu Q, et al. Characterization of the human cysteinyl leukotriene CysLT1 receptor. Nature. 1999;399(6738):789–793.
   PubMed Web of Science ®Google Scholar
• Holm JB, Grygorczyk R, Lambert IH. Volume-sensitive release of organic osmolytes in the human lung epithelial cell line A549: role of the 5-lipoxygenase. Am J Physiol Cell Physiol. 2013;305(1):C48–60.
   PubMed Web of Science ®Google Scholar
• Figueroa EE, Kramer M, Strange K, et al. CysLT1 receptor antagonists pranlukast and zafirlukast inhibit LRRC8-mediated volume regulated anion channels independently of the receptor. Am J Physiol Cell Physiol. 2019;317(4):C857–C866.
   PubMed Web of Science ®Google Scholar
• Mo J, Lin D, Wang J, et al. Apoptosis in HepG2 cells induced by zinc pyrithione via mitochondrial dysfunction pathway: involvement of zinc accumulation and oxidative stress. Ecotoxicol Environ Saf. 2018;161:515–525.
   PubMed Web of Science ®Google Scholar
• Carraway RE, Dobner PR. Zinc pyrithione induces ERK- and PKC-dependent necrosis distinct from TPEN-induced apoptosis in prostate cancer cells. Biochim Biophys Acta. 2012;1823(2):544–557.
   PubMed Web of Science ®Google Scholar
• Shimizu T, Numata T, Okada Y. A role of reactive oxygen species in apoptotic activation of volume-sensitive Cl(-) channel. Proc Natl Acad Sci U S A. 2004;101(17):6770–6773.
   PubMed Web of Science ®Google Scholar
• Jiao J-D, Xu C-Q, Yue P, et al. Volume-sensitive outwardly rectifying chloride channels are involved in oxidative stress-induced apoptosis of mesangial cells. Biochem Biophys Res Commun. 2006;340(1):277–285.
   PubMed Web of Science ®Google Scholar
• Browe DM, Baumgarten CM. Angiotensin II (AT1) receptors and NADPH oxidase regulate Cl- current elicited by beta1 integrin stretch in rabbit ventricular myocytes. J Gen Physiol. 2004;124(3):273–287.
   PubMed Web of Science ®Google Scholar
• Gradogna A, Gavazzo P, Boccaccio A, et al. Subunit-dependent oxidative stress sensitivity of LRRC8 volume-regulated anion channels. J Physiol. 2017;595(21):6719–6733.
   PubMed Web of Science ®Google Scholar
• Tailler M, Senovilla L, Lainey E, et al. Antineoplastic activity of ouabain and pyrithione zinc in acute myeloid leukemia. Oncogene. 2012;31(30):3536–3546.
   PubMed Web of Science ®Google Scholar
• Srivastava G, Matta A, et al. Anticancer activity of pyrithione zinc in oral cancer cells identified in small molecule screens and xenograft model: implications for oral cancer therapy. Mol Oncol. 2015;9(8):1720–1735.
   PubMed Web of Science ®Google Scholar
• Okada Y, Numata T, Sato-Numata K, et al. Roles of volume-regulatory anion channels, VSOR and Maxi-Cl, in apoptosis, cisplatin resistance, necrosis, ischemic cell death, stroke and myocardial infarction. Curr Top Membr. 2019;83:205–283.
   PubMed Web of Science ®Google Scholar
• Figueroa EE, Denton JS. Zinc pyrithione activates the volume-regulated anion channel through an antioxidant-sensitive mechanism. Am J Physiol Cell Physiol. 2021;320(6):C1088–C1098.
   PubMedGoogle Scholar
• Yamada T, Strange K. Intracellular and extracellular loops of LRRC8 are essential for volume-regulated anion channel function. J Gen Physiol. 2018;150(7):1003–1015.
   PubMed Web of Science ®Google Scholar