Oxygen-sensitive membrane transporters in vertebrate red cells.
Abstract: Oxygen is essential for all higher forms of animal life. It is required for oxidative phosphorylation, which forms the bulk of the energy supply of most animals. In many vertebrates, transport of O(2) from respiratory to other tissues, and of CO(2) in the opposite direction, involves red cells. These are highly specialised, adapted for their respiratory function. Intracellular haemoglobin, carbonic anhydrase and the membrane anion exchanger (AE1) increase the effective O(2)- and CO(2)-carrying capacity of red cells by approximately 100-fold. O(2) also has a pathological role. It is a very reactive species chemically, and oxidation, free radical generation and peroxide formation can be major hazards. Cells that come into contact with potentially damaging levels of O(2) have a variety of systems to protect them against oxidative damage. Those in red cells include catalase, superoxide dismutase and glutathione. In this review, we focus on a third role of O(2), as a regulator of membrane transport systems, a role with important consequences for the homeostasis of the red cell and also the organism as a whole. We show that regulation of red cell transporters by O(2) is widespread throughout the vertebrate kingdom. The effect of O(2) is selective but involves a wide range of transporters, including inorganic and organic systems, and both electroneutral and conductive pathways. Finally, we discuss what is known about the mechanism of the O(2) effect and comment on its physiological and pathological roles.
Publication Date: 2000-04-06
PubMed ID: 10751155DOI: 10.1242/jeb.203.9.1395Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Research Support
- Non-U.S. Gov't
- Review
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research focuses on the role of oxygen as a regulator of membrane transport systems in vertebrate red blood cells, which has significant implications for cell and organism homeostasis. It explores how oxygen control of red cell transporters is prevalent in the vertebrate kingdom, and affects a wide variety of transporters, both electroneutral and conductive.
Overview and Context
- The paper begins by establishing the essential role of oxygen in higher forms of animal life, specifically for oxidative phosphorylation – the main source of energy for most animals. It explains how oxygen, within the body, is transported from respiratory tissues to other parts of the body, and how carbon dioxide is transported in the opposite direction, by red blood cells.
- These red cells are described as specialized for carrying out this respiratory function and have an inbuilt enhancement system for oxygen and carbon dioxide carrying capacity. This system employs intracellular haemoglobin, carbonic anhydrase, and the membrane anion exchanger (AE1), which elevates the carrying capacity by approximately 100 times.
- The authors note a pathological role of oxygen. Due to its reactive nature, oxygen can induce oxidation, generate free radicals and form peroxides, which can pose significant dangers. Therefore, cells have protection mechanisms against oxidative damage – in red cells, these include catalase, superoxide dismutase and glutathione.
Oxygen as a Cellular Transport Regulator
- The main focus of the review is on the function of oxygen as a regulator of membrane transport systems. This role is explored in-depth as it bears important implications on the homeostasis of the red cell and the organism as a whole.
- Through the study, it has been demonstrated that oxygen’s regulatory impact on red cell transporters is seen throughout all vertebrates. It has a selective impact but affects a broad spectrum of transporters, including inorganic, organic, electroneutral, and conductive pathways.
Mechanisms and Implications of Oxygen Regulation
- Lastly, the research delves into what is known about the mechanism of the oxygen effect and provides commentary on its physiological and pathological roles. While detail is not provided in the abstract, the implication is that understanding how oxygen regulates membrane transport systems can provide fundamental insights into the functionality and endurance of cells under different oxygen conditions. This has broad implications not only for biology but also for medical applications where oxygen levels may be manipulated.
Cite This Article
APA
Gibson JS, Cossins AR, Ellory JC.
(2000).
Oxygen-sensitive membrane transporters in vertebrate red cells.
J Exp Biol, 203(Pt 9), 1395-1407.
https://doi.org/10.1242/jeb.203.9.1395
Publication
Researcher Affiliations
- Veterinary Preclinical Sciences and School of Biological Sciences, University of Liverpool, Liverpool L69 3BX, UK. jsgibson@sghms.ac.uk
MeSH Terms
- Animals
- Birds
- Carrier Proteins / blood
- Carrier Proteins / physiology
- Cattle
- Erythrocyte Membrane / metabolism
- Erythrocyte Membrane / physiology
- Ferrets
- Fishes
- Horses
- Humans
- Ion Transport / physiology
- Lampreys
- Oxygen / blood
- Oxygen / physiology
- Ranidae
- Sheep
Citations
This article has been cited 32 times.- Lu DC, Hannemann A, Gibson JS. Does Plasma Inhibit the Activity of KCl Cotransport in Red Cells From LK Sheep?. Front Physiol 2022;13:904280.
- Lee SM, Kang BJ, Lee S, Kim WH. Comparison of Hematological and Biochemical Results Derived from Arterial and Venous Blood Samples in Post-Anesthetic Dogs.. Animals (Basel) 2020 Nov 9;10(11).
- Ugurel E, Piskin S, Aksu AC, Eser A, Yalcin O. From Experiments to Simulation: Shear-Induced Responses of Red Blood Cells to Different Oxygen Saturation Levels.. Front Physiol 2019;10:1559.
- Lu DC, Hannemann A, Wadud R, Rees DC, Brewin JN, Low PS, Gibson JS. The role of WNK in modulation of KCl cotransport activity in red cells from normal individuals and patients with sickle cell anaemia.. Pflugers Arch 2019 Dec;471(11-12):1539-1549.
- Andreyeva AY, Soldatov AA, Krivchenko AI, Mindukshev IV, Gambaryan S. Hemoglobin deoxygenation and methemoglobinemia prevent regulatory volume decrease in crucian carp (Carassius carassius) red blood cells.. Fish Physiol Biochem 2019 Dec;45(6):1933-1940.
- Zheng S, Krump NA, McKenna MM, Li YH, Hannemann A, Garrett LJ, Gibson JS, Bodine DM, Low PS. Regulation of erythrocyte Na(+)/K(+)/2Cl(-) cotransport by an oxygen-switched kinase cascade.. J Biol Chem 2019 Feb 15;294(7):2519-2528.
- Huisjes R, Bogdanova A, van Solinge WW, Schiffelers RM, Kaestner L, van Wijk R. Squeezing for Life - Properties of Red Blood Cell Deformability.. Front Physiol 2018;9:656.
- Frlic O, Seliu0161kar A, Domanjko Petriu010d A, Blagus R, Heigenhauser G, Vengust M. Pulmonary Circulation Transvascular Fluid Fluxes Do Not Change during General Anesthesia in Dogs.. Front Physiol 2018;9:124.
- Chu H, McKenna MM, Krump NA, Zheng S, Mendelsohn L, Thein SL, Garrett LJ, Bodine DM, Low PS. Reversible binding of hemoglobin to band 3 constitutes the molecular switch that mediates O2 regulation of erythrocyte properties.. Blood 2016 Dec 8;128(23):2708-2716.
- Sega MF, Chu H, Christian JA, Low PS. Fluorescence assay of the interaction between hemoglobin and the cytoplasmic domain of erythrocyte membrane band 3.. Blood Cells Mol Dis 2015 Oct;55(3):266-71.
- Vadlapatla RK, Vadlapudi AD, Ponnaluri VK, Pal D, Mukherji M, Mitra AK. Molecular expression and functional activity of efflux and influx transporters in hypoxia induced retinal pigment epithelial cells.. Int J Pharm 2013 Sep 15;454(1):444-52.
- Numata T, Ogawa N, Takahashi N, Mori Y. TRP channels as sensors of oxygen availability.. Pflugers Arch 2013 Aug;465(8):1075-85.
- Rogers SC, Ross JG, d'Avignon A, Gibbons LB, Gazit V, Hassan MN, McLaughlin D, Griffin S, Neumayr T, Debaun M, DeBaun MR, Doctor A. Sickle hemoglobin disturbs normal coupling among erythrocyte O2 content, glycolysis, and antioxidant capacity.. Blood 2013 Feb 28;121(9):1651-62.
- Stefanovic M, Puchulu-Campanella E, Kodippili G, Low PS. Oxygen regulates the band 3-ankyrin bridge in the human erythrocyte membrane.. Biochem J 2013 Jan 1;449(1):143-50.
- Sega MF, Chu H, Christian J, Low PS. Interaction of deoxyhemoglobin with the cytoplasmic domain of murine erythrocyte band 3.. Biochemistry 2012 Apr 17;51(15):3264-72.
- Hannemann A, Weiss E, Rees DC, Dalibalta S, Ellory JC, Gibson JS. The Properties of Red Blood Cells from Patients Heterozygous for HbS and HbC (HbSC Genotype).. Anemia 2011;2011:248527.
- Castagnola M, Messana I, Sanna MT, Giardina B. Oxygen-linked modulation of erythrocyte metabolism: state of the art.. Blood Transfus 2010 Jun;8 Suppl 3(Suppl 3):s53-8.
- Matteucci E, Giampietro O. Electron Pathways through Erythrocyte Plasma Membrane in Human Physiology and Pathology: Potential Redox Biomarker?. Biomark Insights 2007 Sep 17;2:321-9.
- Rogers SC, Said A, Corcuera D, McLaughlin D, Kell P, Doctor A. Hypoxia limits antioxidant capacity in red blood cells by altering glycolytic pathway dominance.. FASEB J 2009 Sep;23(9):3159-70.
- Vitturi DA, Teng X, Toledo JC, Matalon S, Lancaster JR Jr, Patel RP. Regulation of nitrite transport in red blood cells by hemoglobin oxygen fractional saturation.. Am J Physiol Heart Circ Physiol 2009 May;296(5):H1398-407.
- Chu H, Breite A, Ciraolo P, Franco RS, Low PS. Characterization of the deoxyhemoglobin binding site on human erythrocyte band 3: implications for O2 regulation of erythrocyte properties.. Blood 2008 Jan 15;111(2):932-8.
- Gibson JS, Milner PI, White R, Fairfax TP, Wilkins RJ. Oxygen and reactive oxygen species in articular cartilage: modulators of ionic homeostasis.. Pflugers Arch 2008 Jan;455(4):563-73.
- Berenbrink M, Vu00f6lkel S, Koldkjaer P, Heisler N, Nikinmaa M. Two different oxygen sensors regulate oxygen-sensitive K+ transport in crucian carp red blood cells.. J Physiol 2006 Aug 15;575(Pt 1):37-48.
- Pedersen SF. The Na+/H+ exchanger NHE1 in stress-induced signal transduction: implications for cell proliferation and cell death.. Pflugers Arch 2006 Jun;452(3):249-59.
- Muzyamba MC, Campbell EH, Gibson JS. Effect of intracellular magnesium and oxygen tension on K+-Cl- cotransport in normal and sickle human red cells.. Cell Physiol Biochem 2006;17(3-4):121-8.
- Vengust M, Staempfli H, Viel L, Heigenhauser G. Transvascular fluid flux from the pulmonary vasculature at rest and during exercise in horses.. J Physiol 2006 Jan 15;570(Pt 2):397-405.
- Campanella ME, Chu H, Low PS. Assembly and regulation of a glycolytic enzyme complex on the human erythrocyte membrane.. Proc Natl Acad Sci U S A 2005 Feb 15;102(7):2402-7.
- Flatman PW. Activation of ferret erythrocyte Na+-K+-2Cl- cotransport by deoxygenation.. J Physiol 2005 Mar 1;563(Pt 2):421-31.
- Bogdanova AY, Ogunshola OO, Bauer C, Gassmann M. Pivotal role of reduced glutathione in oxygen-induced regulation of the Na(+)/K(+) pump in mouse erythrocyte membranes.. J Membr Biol 2003 Sep 1;195(1):33-42.
- Tuominen A, Rissanen E, Bogdanova A, Nikinmaa M. Intracellular pH regulation in rainbow trout (Oncorhynchus mykiss) hepatocytes: the activity of sodium/proton exchange is oxygen-dependent.. J Comp Physiol B 2003 Jun;173(4):301-8.
- Bogdanova AY, Nikinmaa M. Reactive oxygen species regulate oxygen-sensitive potassium flux in rainbow trout erythrocytes.. J Gen Physiol 2001 Feb;117(2):181-90.
- Dunham PB. Oxygen sensing and K(+)-Cl(-) cotransport.. J Physiol 2000 Jul 1;526 Pt 1(Pt 1):1.