Phagosomal chloride dynamics in the alveolar macrophage

Riazanski, Vladimir; Mauleon, Gerardo; Zimnicka, Adriana M.; Chen, Si; Nelson, Deborah J.

doi:10.1016/j.isci.2021.103636

Title: Phagosomal chloride dynamics in the alveolar macrophage

Journal Article · 16 December 2021 · iScience

DOI: https://doi.org/10.1016/j.isci.2021.103636 · OSTI ID:1893937

Riazanski, Vladimir ^[1]; Mauleon, Gerardo ^[1]; Zimnicka, Adriana M. ^[1]; Chen, Si ^[2]; Nelson, Deborah J. ^[1]

Univ. of Chicago, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Acidification in intracellular organelles is tightly linked to the influx of Cl^– counteracting proton translocation by the electrogenic V-ATPase. We quantified the dynamics of Cl^– transfer accompanying cargo incorporation into single phagosomes in alveolar macrophages (AMs). Phagosomal Cl^– concentration and acidification magnitude were followed in real time with maximal acidification achieved at levels of approximately 200 mM. Live cell confocal microscopy verified that phagosomal Cl^– influx utilized predominantly the Cl^– channel CFTR. Relative levels of elemental chlorine (Cl) in hard X-ray fluorescence microprobe (XFM) analysis within single phagosomes validated the increase in Cl^– content. XFM revealed the complex interplay between elemental K content inside the phagosome and changes in Cl^– during phagosomal particle uptake. Cl^–-dependent changes in phagosomal membrane potential were obtained using second harmonic generation (SHG) microscopy. These studies provide a mechanistic insight for screening studies in drug development targeting pulmonary inflammatory disease.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of Health (NIH); National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1893937

Journal Information:: iScience, Journal Name: iScience Journal Issue: 1 Vol. 25; ISSN 2589-0042

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Cell Cl and transepithelial Na transport in toad urinary bladder Butt, A. G.; McLaughlin, C. W.; Bowler, J. M. The Journal of Membrane Biology, Vol. 142, Issue 1 https://doi.org/10.1007/BF00233379	journal	October 1994
CFTR Activation Raises Extracellular pH of NIH/3T3 Mouse Fibroblasts and C127 Epithelial Cells Luckie, D. B.; Singh, C. N.; Wine, J. J. Journal of Membrane Biology, Vol. 179, Issue 3 https://doi.org/10.1007/s002320010052	journal	February 2001
Altered GABAergic function accompanies hippocampal degeneration in mice lacking ClC-3 voltage-gated chloride channels Dickerson, Linda W.; Bonthius, Daniel J.; Schutte, Brian C. Brain Research, Vol. 958, Issue 2 https://doi.org/10.1016/S0006-8993(02)03519-9	journal	December 2002
Changes in the volume of marginal cells induced by isotonic ‘Cl− depletion/restoration’: involvement of the Cl− channel and Na+-K+-Cl− cotransporter Takeuchi, Shunji; Ando, Motonori; Irimajiri, Akihiko Hearing Research, Vol. 113, Issue 1-2 https://doi.org/10.1016/S0378-5955(97)00134-2	journal	November 1997
Hyperacidification in cystic fibrosis: links with lung disease and new prospects for treatment Poschet, Jens; Perkett, Elizabeth; Deretic, Vojo Trends in Molecular Medicine, Vol. 8, Issue 11 https://doi.org/10.1016/S1471-4914(02)02414-0	journal	November 2002
From the inside out: Ion fluxes at the centre of endocytic traffic Chadwick, Sarah R.; Grinstein, Sergio; Freeman, Spencer A. Current Opinion in Cell Biology, Vol. 71 https://doi.org/10.1016/j.ceb.2021.02.006	journal	August 2021
TPC Proteins Are Phosphoinositide- Activated Sodium-Selective Ion Channels in Endosomes and Lysosomes Wang, Xiang; Zhang, Xiaoli; Dong, Xian-ping Cell, Vol. 151, Issue 2 https://doi.org/10.1016/j.cell.2012.08.036	journal	October 2012
A TRP Channel in the Lysosome Regulates Large Particle Phagocytosis via Focal Exocytosis Samie, Mohammad; Wang, Xiang; Zhang, Xiaoli Developmental Cell, Vol. 26, Issue 5 https://doi.org/10.1016/j.devcel.2013.08.003	journal	September 2013
Kinetic Separation of Oxidative and Non-oxidative Metabolism in Single Phagosomes from Alveolar Macrophages: Impact on Bacterial Killing Riazanski, Vladimir; Sui, Zihao; Nelson, Deborah J. iScience, Vol. 23, Issue 11 https://doi.org/10.1016/j.isci.2020.101759	journal	November 2020
Second-Harmonic Generation Imaging of Membrane Potential with Photon Counting Jiang, Jiang; Yuste, Rafael Microscopy and Microanalysis, Vol. 14, Issue 6 https://doi.org/10.1017/S1431927608080811	journal	November 2008
The Bionanoprobe: Synchrotron-Based Hard X-ray Fluorescence Microscopy for 2D/3D Trace Element Mapping Chen, Si; Paunesku, Tatjana; Yuan, Ye Microscopy Today, Vol. 23, Issue 3 https://doi.org/10.1017/S1551929515000401	journal	April 2015
Quantifying Trace Elements in Individual Aquatic Protist Cells with a Synchrotron X-ray Fluorescence Microprobe Twining, Benjamin S.; Baines, Stephen B.; Fisher, Nicholas S. Analytical Chemistry, Vol. 75, Issue 15 https://doi.org/10.1021/ac034227z	journal	August 2003
Direct Measurement of Free Chloride Concentrations in the Phagolysosomes of Human Neutrophils Painter, Richard G.; Wang, Guoshun Analytical Chemistry, Vol. 78, Issue 9 https://doi.org/10.1021/ac0521706	journal	March 2006
CFTR Expression in Human Neutrophils and the Phagolysosomal Chlorination Defect in Cystic Fibrosis Painter, Richard G.; Valentine, Vincent G.; Lanson,, Nicholas A. Biochemistry, Vol. 45, Issue 34 https://doi.org/10.1021/bi060490t	journal	August 2006
Defective acidification of intracellular organelles in cystic fibrosis Barasch, Jonathan; Kiss, Brian; Prince, Alice Nature, Vol. 352, Issue 6330 https://doi.org/10.1038/352070a0	journal	July 1991
The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel Dong, Xian-Ping; Cheng, Xiping; Mills, Eric Nature, Vol. 455, Issue 7215 https://doi.org/10.1038/nature07311	journal	September 2008
Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung Pezzulo, Alejandro A.; Tang, Xiao Xiao; Hoegger, Mark J. Nature, Vol. 487, Issue 7405 https://doi.org/10.1038/nature11130	journal	July 2012
CFTR regulates phagosome acidification in macrophages and alters bactericidal activity Di, Anke; Brown, Mary E.; Deriy, Ludmila V. Nature Cell Biology, Vol. 8, Issue 9 https://doi.org/10.1038/ncb1456	journal	August 2006
Microfluidic control of cell pairing and fusion Skelley, Alison M.; Kirak, Oktay; Suh, Heikyung Nature Methods, Vol. 6, Issue 2 https://doi.org/10.1038/nmeth.1290	journal	January 2009
Presynaptic CLC-3 determines quantal size of inhibitory transmission in the hippocampus Riazanski, Vladimir; Deriy, Ludmila V.; Shevchenko, Pavel D. Nature Neuroscience, Vol. 14, Issue 4 https://doi.org/10.1038/nn.2775	journal	March 2011
Patch-clamp technique to characterize ion channels in enlarged individual endolysosomes Chen, Cheng-Chang; Cang, Chunlei; Fenske, Stefanie Nature Protocols, Vol. 12, Issue 8 https://doi.org/10.1038/nprot.2017.036	journal	July 2017
X-ray ptychographic and fluorescence microscopy of frozen-hydrated cells using continuous scanning Deng, Junjing; Vine, David J.; Chen, Si Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00569-y	journal	March 2017
Imaging membrane potential in dendritic spines Nuriya, M.; Jiang, J.; Nemet, B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 3 https://doi.org/10.1073/pnas.0510092103	journal	January 2006
The spine neck filters membrane potentials Araya, Roberto; Jiang, Jiang; Eisenthal, Kenneth B. Proceedings of the National Academy of Sciences, Vol. 103, Issue 47 https://doi.org/10.1073/pnas.0608755103	journal	November 2006
In situ measurement of the electrical potential across the phagosomal membrane using FRET and its contribution to the proton-motive force Steinberg, Benjamin E.; Touret, Nicolas; Vargas-Caballero, Mariana Proceedings of the National Academy of Sciences, Vol. 104, Issue 22 https://doi.org/10.1073/pnas.0700783104	journal	May 2007
Listeria monocytogenes exploits cystic fibrosis transmembrane conductance regulator (CFTR) to escape the phagosome Radtke, Andrea L.; Anderson, Kelsi L.; Davis, Michael J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1013262108	journal	January 2011
TRPC6 channel translocation into phagosomal membrane augments phagosomal function Riazanski, Vladimir; Gabdoulkhakova, Aida G.; Boynton, Lin S. Proceedings of the National Academy of Sciences, Vol. 112, Issue 47 https://doi.org/10.1073/pnas.1518966112	journal	November 2015
The cytoskeleton of digitonin-treated rat hepatocytes. Fiskum, G.; Craig, S. W.; Decker, G. L. Proceedings of the National Academy of Sciences, Vol. 77, Issue 6 https://doi.org/10.1073/pnas.77.6.3430	journal	June 1980
Regulation of Phagosomal Acidification Hackam, David J.; Rotstein, Ori D.; Zhang, Wei-Jian Journal of Biological Chemistry, Vol. 272, Issue 47 https://doi.org/10.1074/jbc.272.47.29810	journal	November 1997
An Apical PDZ Protein Anchors the Cystic Fibrosis Transmembrane Conductance Regulator to the Cytoskeleton Short, Douglas B.; Trotter, Kevin W.; Reczek, David Journal of Biological Chemistry, Vol. 273, Issue 31 https://doi.org/10.1074/jbc.273.31.19797	journal	July 1998
Disease-causing Mutations in the Cystic Fibrosis Transmembrane Conductance Regulator Determine the Functional Responses of Alveolar Macrophages Deriy, Ludmila V.; Gomez, Erwin A.; Zhang, Guangping Journal of Biological Chemistry, Vol. 284, Issue 51 https://doi.org/10.1074/jbc.M109.057372	journal	December 2009
Chloride Concentration in Endosomes Measured Using a Ratioable Fluorescent Cl− Indicator Sonawane, N. D.; Thiagarajah, Jay R.; Verkman, A. S. Journal of Biological Chemistry, Vol. 277, Issue 7 https://doi.org/10.1074/jbc.M110818200	journal	February 2002
ClC-3 Chloride Channels Facilitate Endosomal Acidification and Chloride Accumulation Hara-Chikuma, Mariko; Yang, Baoxue; Sonawane, N. D. Journal of Biological Chemistry, Vol. 280, Issue 2 https://doi.org/10.1074/jbc.M407030200	journal	January 2005
Selective Role of Intracellular Chloride in the Regulation of the Intrinsic but Not Extrinsic Pathway of Apoptosis in Jurkat T-cells Heimlich, Gerd; Cidlowski, John A. Journal of Biological Chemistry, Vol. 281, Issue 4 https://doi.org/10.1074/jbc.M507367200	journal	January 2006
Cystic Fibrosis Transmembrane Conductance Regulator-independent Phagosomal Acidification in Macrophages Haggie, Peter M.; Verkman, A. S. Journal of Biological Chemistry, Vol. 282, Issue 43 https://doi.org/10.1074/jbc.M705296200	journal	October 2007
CLC Chloride Channels and Transporters: From Genes to Protein Structure, Pathology and Physiology Jentsch, Thomas J. Critical Reviews in Biochemistry and Molecular Biology, Vol. 43, Issue 1 https://doi.org/10.1080/10409230701829110	journal	January 2008
A cation counterflux supports lysosomal acidification Steinberg, Benjamin E.; Huynh, Kassidy K.; Brodovitch, Alexandre Journal of Cell Biology, Vol. 189, Issue 7 https://doi.org/10.1083/jcb.200911083	journal	June 2010
A voltage-dependent K+ channel in the lysosome is required for refilling lysosomal Ca2+ stores Wang, Wuyang; Zhang, Xiaoli; Gao, Qiong Journal of Cell Biology, Vol. 216, Issue 6 https://doi.org/10.1083/jcb.201612123	journal	May 2017
A model of lysosomal pH regulation Ishida, Yoichi; Nayak, Smita; Mindell, Joseph A. Journal of General Physiology, Vol. 141, Issue 6 https://doi.org/10.1085/jgp.201210930	journal	May 2013
Reversible Membrane Permeabilization of Mammalian Cells Treated with Digitonin and Its Use for Inducing Nuclear Reprogramming byXenopusEgg Extracts Miyamoto, Kei; Yamashita, Teruyoshi; Tsukiyama, Tomoyuki Cloning and Stem Cells, Vol. 10, Issue 4 https://doi.org/10.1089/clo.2008.0020	journal	December 2008
Revisiting CFTR inhibition: a comparative study of CFTR _inh ‐172 and GlyH ‐101 inhibitors Melis, N.; Tauc, M.; Cougnon, M. British Journal of Pharmacology, Vol. 171, Issue 15 https://doi.org/10.1111/bph.12726	journal	July 2014
Chloride flux in phagocytes Wang, Guoshun Immunological Reviews, Vol. 273, Issue 1 https://doi.org/10.1111/imr.12438	journal	August 2016
Chloride/bicarbonate exchange in human erythrocytes. Lambert, A.; Lowe, A. G. The Journal of Physiology, Vol. 275, Issue 1 https://doi.org/10.1113/jphysiol.1978.sp012177	journal	February 1978
Chloride and the endosomal-lysosomal pathway: emerging roles of CLC chloride transporters Jentsch, Thomas J. The Journal of Physiology, Vol. 578, Issue 3 https://doi.org/10.1113/jphysiol.2006.124719	journal	January 2007
Cystic Fibrosis Transmembrane Regulator Inhibitors CFTR_inh-172 and GlyH-101 Target Mitochondrial Functions, Independently of Chloride Channel Inhibition Kelly, Mairead; Trudel, Stephanie; Brouillard, Franck Journal of Pharmacology and Experimental Therapeutics, Vol. 333, Issue 1 https://doi.org/10.1124/jpet.109.162032	journal	January 2010
Disruption of the CFTR Gene Produces a Model of Cystic Fibrosis in Newborn Pigs Rogers, Christopher S.; Stoltz, David A.; Meyerholz, David K. Science, Vol. 321, Issue 5897 https://doi.org/10.1126/science.1163600	journal	September 2008
The Development of Lung Disease in Cystic Fibrosis Pigs Wine, Jeffrey J. Science Translational Medicine, Vol. 2, Issue 29 https://doi.org/10.1126/scitranslmed.3001130	journal	April 2010
Lysosomal Acidification Mechanisms Mindell, Joseph A. Annual Review of Physiology, Vol. 74, Issue 1 https://doi.org/10.1146/annurev-physiol-012110-142317	journal	March 2012
Evidence against the acidification hypothesis in cystic fibrosis Gibson, Gregory A.; Hill, Warren G.; Weisz, Ora A. American Journal of Physiology-Cell Physiology, Vol. 279, Issue 4 https://doi.org/10.1152/ajpcell.2000.279.4.C1088	journal	October 2000
Proton leak and CFTR in regulation of Golgi pH in respiratory epithelial cells Chandy, Grischa; Grabe, Michael; Moore, Hsiao-Ping H. American Journal of Physiology-Cell Physiology, Vol. 281, Issue 3 https://doi.org/10.1152/ajpcell.2001.281.3.C908	journal	September 2001
Role of Cftr genotype in the response to chronic Pseudomonas aeruginosa lung infection in mice van Heeckeren, Anna M.; Schluchter, Mark D.; Drumm, Mitchell L. American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 287, Issue 5 https://doi.org/10.1152/ajplung.00387.2003	journal	November 2004
The porcine lung as a potential model for cystic fibrosis Rogers, Christopher S.; Abraham, William M.; Brogden, Kim A. American Journal of Physiology-Lung Cellular and Molecular Physiology, Vol. 295, Issue 2 https://doi.org/10.1152/ajplung.90203.2008	journal	August 2008
Optical Recording of Fast Neuronal Membrane Potential Transients in Acute Mammalian Brain Slices by Second-Harmonic Generation Microscopy Dombeck, Daniel A.; Sacconi, Leonardo; Blanchard-Desce, Mireille Journal of Neurophysiology, Vol. 94, Issue 5 https://doi.org/10.1152/jn.00416.2005	journal	November 2005
CLC Chloride Channels and Transporters: Structure, Function, Physiology, and Disease Jentsch, Thomas J.; Pusch, Michael Physiological Reviews, Vol. 98, Issue 3 https://doi.org/10.1152/physrev.00047.2017	journal	July 2018
Production of CFTR-null and CFTR-ΔF508 heterozygous pigs by adeno-associated virus–mediated gene targeting and somatic cell nuclear transfer Rogers, Christopher S.; Hao, Yanhong; Rokhlina, Tatiana Journal of Clinical Investigation, Vol. 118, Issue 4 https://doi.org/10.1172/JCI34773	journal	April 2008
Cystic fibrosis neutrophils have normal intrinsic reactive oxygen species generation McKeon, D. J.; Cadwallader, K. A.; Idris, S. European Respiratory Journal, Vol. 35, Issue 6 https://doi.org/10.1183/09031936.00089709	journal	October 2009
The role of chloride anion and CFTR in killing of Pseudomonas aeruginosa by normal and CF neutrophils Painter, R. G.; Bonvillain, R. W.; Valentine, V. G. Journal of Leukocyte Biology, Vol. 83, Issue 6 https://doi.org/10.1189/jlb.0907658	journal	March 2008
Defective acidification of the biosynthetic pathway in cystic fibrosis Barasch, Jonathan; Al-Awqati, Qais Journal of Cell Science, Vol. 1993, Issue Supplement_17 https://doi.org/10.1242/jcs.1993.Supplement_17.32	journal	December 1993
Chloride channels of intracellular organelles and their potential role in cystic fibrosis. al-Awqati, Q.; Barasch, J.; Landry, D. Journal of Experimental Biology, Vol. 172, Issue 1 https://doi.org/10.1242/jeb.172.1.245	journal	November 1992
Reactive-Oxygen-Species-Mediated P. aeruginosa Killing Is Functional in Human Cystic Fibrosis Macrophages Cifani, Noemi; Pompili, Barbara; Anile, Marco PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0071717	journal	August 2013
Neutrophil-Mediated Phagocytic Host Defense Defect in Myeloid Cftr-Inactivated Mice Ng, Hang Pong; Zhou, Yun; Song, Kejing PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0106813	journal	September 2014
Second Harmonic Generation in Neurons: Electro-Optic Mechanism of Membrane Potential Sensitivity Jiang, Jiang; Eisenthal, Kenneth B.; Yuste, Rafael Biophysical Journal, Vol. 93, Issue 5 https://doi.org/10.1529/biophysj.107.111021	journal	September 2007
Alterations in Ceramide Concentration and pH Determine the Release of Reactive Oxygen Species by Cftr-Deficient Macrophages on Infection Zhang, Yang; Li, Xiang; Grassmé, Heike The Journal of Immunology, Vol. 184, Issue 9 https://doi.org/10.4049/jimmunol.0902851	journal	March 2010
High lumenal chloride in the lysosome is critical for lysosome function Chakraborty, Kasturi; Leung, KaHo; Krishnan, Yamuna eLife, Vol. 6 https://doi.org/10.7554/eLife.28862	journal	July 2017

Similar Records

Acute toxicity of lead particulates on pulmonary alveolar macrophages. Ultrastructural and microanalytical studies

Journal Article · 1983 · Lab. Invest.; (United States) · OSTI ID:6252246

deVries, C R; Ingram, P; Walker, S R; +3 more

Acute toxicity of lead particulates on pulmonary alveolar macrophages. Ultrastructural and microanalytical studies

Journal Article · 1983 · Lab. Invest.; (United States) · OSTI ID:5776764

deVries, C R; Ingram, P; Walker, S R; +3 more

Proton efflux from corn roots induced by tripropyltin

Journal Article · 1981 · Plant Physiol.; (United States) · OSTI ID:5714854

Chastain, C J; Hanson, J B

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Biological sciences
Cell biology
Specialized functions of cells

Title: Phagosomal chloride dynamics in the alveolar macrophage

Citation Formats

References (64)

Similar Records

Related Subjects