The Intimate and Mysterious Relationship Between Proton Channels and NADPH Oxidase

Overview

Journal FEBS Lett

Specialty Biochemistry

Date 2008 Dec 17

PMID 19084015

Citations 25

Authors

Boris Musset

Vladimir V Cherny

Deri Morgan

Thomas E DeCoursey

Affiliations

Soon will be listed here.

Abstract

Voltage gated proton channels and NADPH oxidase function cooperatively in phagocytes during the respiratory burst, when reactive oxygen species are produced to kill microbial invaders. Although these molecules are distinct entities, with no proven physical interaction, their presence and activity in many cells appears to be coordinated. We describe these interactions and discuss several types of mechanisms that might explain them.

Citing Articles

Phase partitioning of the neutrophil oxidative burst is coordinated by accessory pathways of glucose metabolism and mitochondrial activity.

Jobe T, Stephan J, Wells C, De Silva M, Lorkiewicz P, Hill B J Biol Chem. 2024; 301(1):108091.

PMID: 39675714 PMC: 11760813. DOI: 10.1016/j.jbc.2024.108091.

Transcendent Aspects of Proton Channels.

DeCoursey T Annu Rev Physiol. 2023; 86:357-377.

PMID: 37931166 PMC: 10938948. DOI: 10.1146/annurev-physiol-042222-023242.

Human‑made electromagnetic fields: Ion forced‑oscillation and voltage‑gated ion channel dysfunction, oxidative stress and DNA damage (Review).

Panagopoulos D, Karabarbounis A, Yakymenko I, Chrousos G Int J Oncol. 2021; 59(5).

PMID: 34617575 PMC: 8562392. DOI: 10.3892/ijo.2021.5272.

Oxidative Stress and NADPH Oxidase: Connecting Electromagnetic Fields, Cation Channels and Biological Effects.

Georgiou C, Margaritis L Int J Mol Sci. 2021; 22(18).

PMID: 34576203 PMC: 8470280. DOI: 10.3390/ijms221810041.

Role of the Intracellular Sodium Homeostasis in Chemotaxis of Activated Murine Neutrophils.

Najder K, Rugi M, Lebel M, Schroder J, Oster L, Schimmelpfennig S Front Immunol. 2020; 11:2124.

PMID: 33013896 PMC: 7506047. DOI: 10.3389/fimmu.2020.02124.

References

DeCoursey T . Voltage-gated proton channels and other proton transfer pathways. Physiol Rev. 2003; 83(2):475-579. DOI: 10.1152/physrev.00028.2002. View

Lambeth J . Nox enzymes, ROS, and chronic disease: an example of antagonistic pleiotropy. Free Radic Biol Med. 2007; 43(3):332-47. PMC: 2013737. DOI: 10.1016/j.freeradbiomed.2007.03.027. View

Nanda A, Grinstein S, Curnutte J . Abnormal activation of H+ conductance in NADPH oxidase-defective neutrophils. Proc Natl Acad Sci U S A. 1993; 90(2):760-4. PMC: 45745. DOI: 10.1073/pnas.90.2.760. View

Schwarzer C, Machen T, Illek B, Fischer H . NADPH oxidase-dependent acid production in airway epithelial cells. J Biol Chem. 2004; 279(35):36454-61. DOI: 10.1074/jbc.M404983200. View

Demaurex N, Grinstein S, Jaconi M, Schlegel W, Lew D, Krause K . Proton currents in human granulocytes: regulation by membrane potential and intracellular pH. J Physiol. 1993; 466:329-44. PMC: 1175481. View

Musset B, Morgan D, Cherny V, Macglashan Jr D, Thomas L, Rios E . A pH-stabilizing role of voltage-gated proton channels in IgE-mediated activation of human basophils. Proc Natl Acad Sci U S A. 2008; 105(31):11020-5. PMC: 2504794. DOI: 10.1073/pnas.0800886105. View

Thomas R, Meech R . Hydrogen ion currents and intracellular pH in depolarized voltage-clamped snail neurones. Nature. 1982; 299(5886):826-8. DOI: 10.1038/299826a0. View

Henderson L, Chappell J, Jones O . The superoxide-generating NADPH oxidase of human neutrophils is electrogenic and associated with an H+ channel. Biochem J. 1987; 246(2):325-9. PMC: 1148280. DOI: 10.1042/bj2460325. View

Ramsey I, Moran M, Chong J, Clapham D . A voltage-gated proton-selective channel lacking the pore domain. Nature. 2006; 440(7088):1213-6. PMC: 4084761. DOI: 10.1038/nature04700. View

10.

Morgan D, Cherny V, Finnegan A, Bollinger J, Gelb M, DeCoursey T . Sustained activation of proton channels and NADPH oxidase in human eosinophils and murine granulocytes requires PKC but not cPLA2 alpha activity. J Physiol. 2006; 579(Pt 2):327-44. PMC: 2075394. DOI: 10.1113/jphysiol.2006.124248. View

11.

Reeves E, Lu H, Jacobs H, Messina C, Bolsover S, Gabella G . Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature. 2002; 416(6878):291-7. DOI: 10.1038/416291a. View

12.

Rada B, Geiszt M, Kaldi K, Timar C, Ligeti E . Dual role of phagocytic NADPH oxidase in bacterial killing. Blood. 2004; 104(9):2947-53. DOI: 10.1182/blood-2004-03-1005. View

13.

Holmes B, Quie P, WINDHORST D, GOOD R . Fatal granulomatous disease of childhood. An inborn abnormality of phagocytic function. Lancet. 1966; 1(7449):1225-8. DOI: 10.1016/s0140-6736(66)90238-8. View

14.

Eder C, DeCoursey T . Voltage-gated proton channels in microglia. Prog Neurobiol. 2001; 64(3):277-305. DOI: 10.1016/s0301-0082(00)00062-9. View

15.

Eder C, FISCHER H, HADDING U, Heinemann U . Properties of voltage-gated currents of microglia developed using macrophage colony-stimulating factor. Pflugers Arch. 1995; 430(4):526-33. DOI: 10.1007/BF00373889. View

16.

Klebanoff S . Myeloperoxidase: friend and foe. J Leukoc Biol. 2005; 77(5):598-625. DOI: 10.1189/jlb.1204697. View

17.

Zhen L, King A, Xiao Y, Chanock S, Orkin S, Dinauer M . Gene targeting of X chromosome-linked chronic granulomatous disease locus in a human myeloid leukemia cell line and rescue by expression of recombinant gp91phox. Proc Natl Acad Sci U S A. 1993; 90(21):9832-6. PMC: 47666. DOI: 10.1073/pnas.90.21.9832. View

18.

Lee S, Letts J, MacKinnon R . Dimeric subunit stoichiometry of the human voltage-dependent proton channel Hv1. Proc Natl Acad Sci U S A. 2008; 105(22):7692-5. PMC: 2409406. DOI: 10.1073/pnas.0803277105. View

19.

Cherny V, DeCoursey T . pH-dependent inhibition of voltage-gated H(+) currents in rat alveolar epithelial cells by Zn(2+) and other divalent cations. J Gen Physiol. 1999; 114(6):819-38. PMC: 2230650. DOI: 10.1085/jgp.114.6.819. View

20.

DeCoursey T, Cherny V, Zhou W, Thomas L . Simultaneous activation of NADPH oxidase-related proton and electron currents in human neutrophils. Proc Natl Acad Sci U S A. 2000; 97(12):6885-9. PMC: 18770. DOI: 10.1073/pnas.100047297. View