Acidic and Basic pH Effect in Two Cytoplasmic and Endoplasmic Reticulum Luminal Spaces on Chloride Channel Electrophysiological Behavior
Background: In regard of chloride channel electrophysiological behavior importance in cellular homeostasis maintenance, some of diseases appearance because of chloride channels impairment, also reports of synchronization between chloride channels impairment and misadjusted pH and that presumably acid or basic pH in cytoplasmic and endoplasmic reticulum luminal spaces are effective on this behavior, current study was performed.
Materials and Methods: Research was performed by experimental method. Vesicles from rat liver tissue endoplasmic reticulum were extracted and assessed in 30 samples in 6 groups. Electrophysiological behaviors of channels were measured in control, acidic and basic pH in cis and Trans environments and according of channel conductance and Po this behavior was determined and judged statistically. Data were filtered at 1 kHz and stored at a sampling rate of 10 kHz for offline analysis by PClamp9. Statistical analysis was performed based on Markov noise free single channel analysis.
Results: Channel conductance was 72 pS and its current – Voltage relation curve was linear. Channel has Voltage dependent behavior and has grater Po in positive Voltages. Channel conductance in acidic pH remained at 72 pS as of control situation. Channel Po was not changed. In basic pH these findings were also repeated. Also, in cis and Trans spaces these behaviors were sawed.
Conclusion: It seems that in pH stream from 6 to 8.5, current channel electrophysiological behavior could be important in endoplasmic reticulum and cellular homeostasis maintenance especially in positive ion such as calcium ion accumulation situation in cytoplasm.
Jentsch TJ, Stein V, Weinreich F, Zdebik AA. Molecular structure and physiological function of chloride channels. Physiological reviews. 2002;82(2):503-68.
Edwards JC, Kahl CR. Chloride channels of intracellular membranes. FEBS letters. 2010;584(10):2102-11.
Xu H, Martinoia E, Szabo I. Organellar channels and transporters. Cell calcium. 2015;58(1):1-10.
Peinelt C, Apell H-J. Kinetics of the Ca 2+, H+, and Mg 2+ interaction with the ion-binding sites of the SR Ca-ATPase. Biophysical journal. 2002;82(1):170-81.
Chevet E, Cameron PH, Pelletier MF, Thomas DY, Bergeron JJ. The endoplasmic reticulum: integration of protein folding, quality control, signaling and degradation. Current opinion in structural biology. 2001;11(1):120-4.
Sitia R, Braakman I. Quality control in the endoplasmic reticulum protein factory. Nature. 2003;426(6968):891-4.
Matsuyama S, Reed J. Mitochondria-dependent apoptosis and cellular pH regulation. Cell death and differentiation. 2000;7(12):1155.
Aoyama K, Burns DM, Suh SW, Garnier P, Matsumori Y, Shiina H, et al. Acidosis causes endoplasmic reticulum stress and caspase-12-mediated astrocyte death. Journal of Cerebral Blood Flow & Metabolism. 2005;25(3):358-70.
Lagadic-Gossmann D, Huc L, Lecureur V. Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death & Differentiation. 2004;11(9):953-61.
Kadenbach B, Arnold S, Lee I, Hüttemann M. The possible role of cytochrome c oxidase in stress-induced apoptosis and degenerative diseases. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2004;1655:400-8.
Verkman AS, Galietta LJ. Chloride channels as drug targets. Nature reviews Drug discovery. 2009;8(2):153-71.
Webb BA, Chimenti M, Jacobson MP, Barber DL. Dysregulated pH: a perfect storm for cancer progression. Nature Reviews Cancer. 2011;11(9):671-7.
Cardone RA, Casavola V, Reshkin SJ. The role of disturbed pH dynamics and the Na+/H+ exchanger in metastasis. Nature Reviews Cancer. 2005;5(10):786-95.
Duan D. Phenomics of cardiac chloride channels: the systematic study of chloride channel function in the heart. The Journal of physiology. 2009;587(10):2163-77.
Novarino G, Fabrizi C, Tonini R, Denti MA, Malchiodi-Albedi F, Lauro GM, et al. Involvement of the intracellular ion channel CLIC1 in microglia-mediated β-amyloid-induced neurotoxicity. Journal of Neuroscience. 2004;24(23):5322-30.
Wang L, He S, Yanyang T, Ji P, Zong J, Zhang J, et al. Elevated expression of chloride intracellular channel 1 is correlated with poor prognosis in human gliomas. Journal of Experimental & Clinical Cancer Research. 2012;31(1):44.
Chen MJ, Sepramaniam S, Armugam A, Choy MS, Manikandan J, Melendez AJ, et al. Water and ion channels: crucial in the initiation and progression of apoptosis in central nervous system? Current neuropharmacology. 2008;6(2):102-16.
Suh KS, Yuspa SH. Intracellular chloride channels: critical mediators of cell viability and potential targets for cancer therapy. Current pharmaceutical design. 2005;11(21):2753-64.
Suh KS, Mutoh M, Gerdes M, Yuspa SH, editors. CLIC4, an intracellular chloride channel protein, is a novel molecular target for cancer therapy. Journal of Investigative Dermatology Symposium Proceedings; 2005: Elsevier.
Suh KS, Mutoh M, Gerdes M, Crutchley JM, Mutoh T, Edwards LE, et al. Antisense suppression of the chloride intracellular channel family induces apoptosis, enhances tumor necrosis factor α-induced apoptosis, and inhibits tumor growth. Cancer research. 2005;65(2):562-71.
Costa T, Rodbard D, PERT CB. Is the benzodiazepine receptor coupled to a chloride anion channel? Nature. 1979;277(5694):315-7.
Miller C, White MM. A voltage‐dependent chloride conductance channel from Torpedo electroplax membrane. Annals of the New York Academy of Sciences. 1980;341(1):534-51.
Riordan JR, Rommens JM, Kerem B-s, Alon N, Rozmahel R. Identification of the cystic fibrosis gene: cloning and characterization of complementary DNA. Science. 1989;245(4922):1066.
Grondin M, Marion M, Denizeau F, Averill-Bates DA. Tributyltin induces apoptotic signaling in hepatocytes through pathways involving the endoplasmic reticulum and mitochondria. Toxicology and applied pharmacology. 2007;222(1):57-68.
Rowland AA, Voeltz GK. Endoplasmic reticulum–mitochondria contacts: function of the junction. Nature reviews Molecular cell biology. 2012;13(10):607-25.
De Brito OM, Scorrano L. An intimate liaison: spatial organization of the endoplasmic reticulum–mitochondria relationship. The EMBO journal. 2010;29(16):2715-23.
Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013;32(7):805-18.
Toth A, Nickson P, Mandl A, Bannister ML, Toth K, Erhardt P. Endoplasmic reticulum stress as a novel therapeutic target in heart diseases. Cardiovascular & Haematological Disorders-Drug Targets (Formerly Current Drug Targets-Cardiovascular & Hematological Disorders). 2007;7(3):205-18.
Zhao L, Ackerman SL. Endoplasmic reticulum stress in health and disease. Current opinion in cell biology. 2006;18(4):444-52.
Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. The Journal of clinical investigation. 2005;115(10):2656-64.
Kan FW, Jolicoeur M, Paiement J. Freeze-fracture analysis of the effects of intermediates of the phosphatidylinositol cycle on fusion of rough endoplasmic reticulum membranes. Biochimica et Biophysica Acta (BBA)-Biomembranes. 1992;1107(2):331-41.
Singleton W, Gray M, Brown M, White J. Chromatographically homogeneous lecithin from egg phospholipids. Journal of the American Oil Chemists’ Society. 1965;42(1):53-6.
Mueller P, Rudin DO, Tien HT, Wescott WC. Methods for the formation of single bimolecular lipid membranes in aqueous solution. The Journal of Physical Chemistry. 1963;67(2):534-5.
Li X, Weinman SA. Chloride channels and hepatocellular function: prospects for molecular identification. Annual review of physiology. 2002;64(1):609-33.
Jentsch TJ, Günther W, Pusch M, Schwappach B. Properties of voltage-gated chloride channels of the ClC gene family. The Journal of Physiology. 1995;482(P):19S.
Malekova L, Tomaskova J, Novakova M, Stefanik P, Kopacek J, Lakatos B, et al. Inhibitory effect of DIDS, NPPB, and phloretin on intracellular chloride channels. Pflügers Archiv-European Journal of Physiology. 2007;455(2):349-57.
Zhang WK, Wang D, Duan Y, Loy MM, Chan HC, Huang P. Mechanosensitive gating of CFTR. Nature Cell Biology. 2010;12(5):507-12.
Picollo A, Pusch M. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature. 2005;436(7049):420-3.
Lange PF, Wartosch L, Jentsch TJ, Fuhrmann JC. ClC-7 requires Ostm1 as a β-subunit to support bone resorption and lysosomal function. Nature. 2006;440(7081):220-3.
Okkenhaug H, Weylandt K-H, Carmena D, Wells DJ, Higgins CF, Sardini A. The human ClC-4 protein, a member of the CLC chloride channel/transporter family, is localized to the endoplasmic reticulum by its N-terminus. The FASEB journal. 2006;20(13):2390-2.
Moreland JG, Davis AP, Matsuda JJ, Hook JS, Bailey G, Nauseef WM, et al. Endotoxin priming of neutrophils requires NADPH oxidase-generated oxidants and is regulated by the anion transporter ClC-3. Journal of Biological Chemistry. 2007;282(47):33958-67.
Thompson AN, Posson DJ, Parsa PV, Nimigean CM. Molecular mechanism of pH sensing in KcsA potassium channels. Proceedings of the National Academy of Sciences. 2008;105(19):6900-5.
Chen J-H, Cai Z, Sheppard DN. Direct sensing of intracellular pH by the cystic fibrosis transmembrane conductance regulator (CFTR) Cl− channel. Journal of Biological Chemistry. 2009;284(51):35495-506.
Hermida OT, Bezrukov SM, Rostovtseva TK. A Putative Role of Voltage-Dependent Anion Channel in Ischemia. Biophysical Journal. 2012;102(3):161a.
Teijido O, Rappaport SM, Chamberlin A, Noskov SY, Aguilella VM, Rostovtseva TK, et al. Acidification asymmetrically affects voltage-dependent anion channel implicating the involvement of salt bridges. Journal of Biological Chemistry. 2014;289(34):23670-82.
Barnes S, Bui Q. Modulation of calcium-activated chloride current via pH-induced changes of calcium channel properties in cone photoreceptors. J Neurosci. 1991;11(12):4015-23.
Arreola J, Begenisich T, Melvin JE. Conformation‐dependent regulation of inward rectifier chloride channel gating by extracellular protons. The Journal of physiology. 2002;541(1):103-12.
Mattson MP, Chan SL. Calcium orchestrates apoptosis. Nature cell biology. 2003;5(12):1041-3.
Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium–apoptosis link. Nature reviews Molecular cell biology. 2003;4(7):552-65.
Thammasit P, Sangboonruang S, Suwanpairoj S, Khamaikawin W, Intasai N, Kasinrerk W, et al. Intracellular Acidosis promotes mitochondrial apoptosis pathway: Role of EMMPRIN down-regulation via specific single-chain Fv intrabody. Journal of Cancer. 2015;6(3):276.
Giampietri C, Petrungaro S, Conti S, Facchiano A, Filippini A, Ziparo E. Cancer microenvironment and endoplasmic reticulum stress response. Mediators of inflammation. 2015;2015.
Vembar SS, Brodsky JL. One step at a time: endoplasmic reticulum-associated degradation. Nature reviews Molecular cell biology. 2008;9(12):944-57.
Wu MM, Grabe M, Adams S, Tsien RY, Moore H-PH, Machen TE. Mechanisms of pH regulation in the regulated secretory pathway. Journal of Biological Chemistry. 2001;276(35):33027-35.
Moolenaar WH. Effects of growth factors on intracellular pH regulation. Annual Review of Physiology. 1986;48(1):363-76.
Gerweck LE, Seetharaman K. Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer research. 1996;56(6):1194-8.
Brahimi-Horn MC, Pouysségur J. Hypoxia in cancer cell metabolism and pH regulation. Essays in biochemistry. 2007;43:165-78.
Bae Y, Fukushima S, Harada A, Kataoka K. Design of environment‐sensitive supramolecular assemblies for intracellular drug delivery: Polymeric micelles that are responsive to intracellular pH change. Angewandte Chemie. 2003;115(38):4788-91.
Izumi H, Torigoe T, Ishiguchi H, Uramoto H, Yoshida Y, Tanabe M, et al. Cellular pH regulators: potentially promising molecular targets for cancer chemotherapy. Cancer treatment reviews. 2003;29(6):541-9.
Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nature reviews Drug discovery. 2011;10(10):767-77.