Acid-sensitive Outwardly Rectifying Anion Channels in Human Erythrocytes

Overview

Journal J Membr Biol

Date 2009 Jul 3

PMID 19572091

Citations 6

Authors

Yuliya V Kucherenko

Daniel Morsdorf

Florian Lang

Affiliations

Soon will be listed here.

Abstract

Acid-sensitive outwardly rectifying anion channels (ASOR) have been described in several mammalian cell types. The present whole-cell patch-clamp study elucidated whether those channels are expressed in erythrocytes. To this end whole-cell recordings were made in human erythrocytes from healthy donors treated with low pH and high osmotic pressure. When the pipette solution had a reduced Cl(-) concentration, treatment of the cells with Cl(-)-containing normal and hyperosmotic (addition of sucrose and polyethelene glycol 1000 [PEG-1000] to the Ringer) media with low pH significantly increased the conductance of the cells at positive voltages. Channel activity was highest in the PEG-1000 media (95 and 300 mM PEG-1000, pH 4.5 and 4.3, respectively) where the current-voltage curves demonstrated strong outward rectification and reversed at -40 mV. Substitution of the Cl(-)-containing medium with Cl(-)-free medium resulted in a decrease of the conductance at hyperpolarizing voltages, a shift in reversal potential (to 0 mV) and loss of outward rectification. The chloride currents were inhibited by chloride channels blockers DIDS and NPPB (IC(50) for both was approximately 1 mM) but not with niflumic acid and amiloride. The observations reveal expression of ASOR in erythrocytes.

Citing Articles

To Be or Not to Be an Ion Channel: Cryo-EM Structures Have a Say.

Chen G, Li J, Zhang J, Zeng B Cells. 2023; 12(14).

PMID: 37508534 PMC: 10378246. DOI: 10.3390/cells12141870.

Cell Death Induction and Protection by Activation of Ubiquitously Expressed Anion/Cation Channels. Part 2: Functional and Molecular Properties of ASOR/PAC Channels and Their Roles in Cell Volume Dysregulation and Acidotoxic Cell Death.

Okada Y, Sato-Numata K, Sabirov R, Numata T Front Cell Dev Biol. 2021; 9:702317.

PMID: 34307382 PMC: 8299559. DOI: 10.3389/fcell.2021.702317.

Acid- and Volume-Sensitive Chloride Currents in Human Chondrocytes.

Kittl M, Winklmayr M, Helm K, Lettner J, Gaisberger M, Ritter M Front Cell Dev Biol. 2020; 8:583131.

PMID: 33282866 PMC: 7691427. DOI: 10.3389/fcell.2020.583131.

Acid- and Volume-Sensitive Chloride Currents in Microglial Cells.

Kittl M, Helm K, Beyreis M, Mayr C, Gaisberger M, Winklmayr M Int J Mol Sci. 2019; 20(14).

PMID: 31311135 PMC: 6678294. DOI: 10.3390/ijms20143475.

Characterization of constitutive and acid-induced outwardly rectifying chloride currents in immortalized mouse distal tubular cells.

Valinsky W, Touyz R, Shrier A Biochim Biophys Acta Gen Subj. 2017; 1861(8):2007-2019.

PMID: 28483640 PMC: 5482324. DOI: 10.1016/j.bbagen.2017.05.004.

References

Nobles M, Higgins C, Sardini A . Extracellular acidification elicits a chloride current that shares characteristics with ICl(swell). Am J Physiol Cell Physiol. 2004; 287(5):C1426-35. DOI: 10.1152/ajpcell.00549.2002. View

Mo L, Hellmich H, Fong P, Wood T, Embesi J, Wills N . Comparison of amphibian and human ClC-5: similarity of functional properties and inhibition by external pH. J Membr Biol. 1999; 168(3):253-64. DOI: 10.1007/s002329900514. View

Frohlich O, Leibson C, Gunn R . Chloride net efflux from intact erythrocytes under slippage conditions. Evidence for a positive charge on the anion binding/transport site. J Gen Physiol. 1983; 81(1):127-52. PMC: 2215566. DOI: 10.1085/jgp.81.1.127. View

Friedrich T, Breiderhoff T, Jentsch T . Mutational analysis demonstrates that ClC-4 and ClC-5 directly mediate plasma membrane currents. J Biol Chem. 1999; 274(2):896-902. DOI: 10.1074/jbc.274.2.896. View

Tomlinson F, Anderson R, Meyer F . Brain pHi, cerebral blood flow, and NADH fluorescence during severe incomplete global ischemia in rabbits. Stroke. 1993; 24(3):435-43. DOI: 10.1161/01.str.24.3.435. View

Marshall W, Bryson S, Sapp M . Volume regulation in glutathione-treated brook trout (Salvelinus fontinalis) erythrocytes. Fish Physiol Biochem. 2013; 8(1):19-28. DOI: 10.1007/BF00004428. View

Kasinathan R, Foller M, Koka S, M Huber S, Lang F . Inhibition of eryptosis and intraerythrocytic growth of Plasmodium falciparum by flufenamic acid. Naunyn Schmiedebergs Arch Pharmacol. 2006; 374(4):255-64. DOI: 10.1007/s00210-006-0122-x. View

M Huber S, Duranton C, Lang F . Patch-clamp analysis of the "new permeability pathways" in malaria-infected erythrocytes. Int Rev Cytol. 2005; 246:59-134. DOI: 10.1016/S0074-7696(05)46003-9. View

Duranton C, Tanneur V, Lang C, Brand V, Koka S, Kasinathan R . A high specificity and affinity interaction with serum albumin stimulates an anion conductance in malaria-infected erythrocytes. Cell Physiol Biochem. 2008; 22(5-6):395-404. DOI: 10.1159/000185483. View

10.

Iyer R, Iverson T, Accardi A, Miller C . A biological role for prokaryotic ClC chloride channels. Nature. 2002; 419(6908):715-8. DOI: 10.1038/nature01000. View

11.

Kaplan J, Pring M, Passow H . Band-3 protein-mediated anion conductance of the red cell membrane. Slippage vs ionic diffusion. FEBS Lett. 1983; 156(1):175-9. DOI: 10.1016/0014-5793(83)80272-5. View

12.

Verloo P, Kocken C, van der Wel A, Tilly B, Hogema B, Sinaasappel M . Plasmodium falciparum-activated chloride channels are defective in erythrocytes from cystic fibrosis patients. J Biol Chem. 2003; 279(11):10316-22. DOI: 10.1074/jbc.M311540200. View

13.

Bernhardt I, Weiss E, Robinson H, Wilkins R, Bennekou P . Differential effect of HOE642 on two separate monovalent cation transporters in the human red cell membrane. Cell Physiol Biochem. 2007; 20(5):601-6. DOI: 10.1159/000107543. View

14.

Wadiche J, Amara S, Kavanaugh M . Ion fluxes associated with excitatory amino acid transport. Neuron. 1995; 15(3):721-8. DOI: 10.1016/0896-6273(95)90159-0. View

15.

Yamamoto S, Ehara T . Acidic extracellular pH-activated outwardly rectifying chloride current in mammalian cardiac myocytes. Am J Physiol Heart Circ Physiol. 2005; 290(5):H1905-14. DOI: 10.1152/ajpheart.00965.2005. View

16.

Diewald L, Rupp J, Dreger M, Hucho F, Gillen C, Nawrath H . Activation by acidic pH of CLC-7 expressed in oocytes from Xenopus laevis. Biochem Biophys Res Commun. 2002; 291(2):421-4. DOI: 10.1006/bbrc.2002.6462. View

17.

Okada Y, Maeno E, Shimizu T, Manabe K, Mori S, Nabekura T . Dual roles of plasmalemmal chloride channels in induction of cell death. Pflugers Arch. 2004; 448(3):287-95. DOI: 10.1007/s00424-004-1276-3. View

18.

Estevez R, Boettger T, Stein V, Birkenhager R, Otto E, Hildebrandt F . Barttin is a Cl- channel beta-subunit crucial for renal Cl- reabsorption and inner ear K+ secretion. Nature. 2001; 414(6863):558-61. DOI: 10.1038/35107099. View

19.

Yasui M, Hazama A, Kwon T, Nielsen S, Guggino W, Agre P . Rapid gating and anion permeability of an intracellular aquaporin. Nature. 2000; 402(6758):184-7. DOI: 10.1038/46045. View

20.

Morgan J, Leake D . Acidic pH increases the oxidation of LDL by macrophages. FEBS Lett. 1993; 333(3):275-9. DOI: 10.1016/0014-5793(93)80669-l. View