Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane

V. Endeward, R. Musa-Aziz, G. J. Cooper, L. M. Chen, M. F. Pelletier, L. V. Virkki, C. T. Supuran, Landon Stuart King, W. F. Boron, G. Gros

Research output: Contribution to journalArticle

Abstract

We report here the application of a previously described method to directly determine the CO2 permeability (PCO2) of the cell membranes of normal human red blood cells (RBCs) vs. those deficient in aquaporin 1 (AQP1), as well as AQP1-expressing Xenopus laevis oocytes. This method measures the exchange of 18O between CO2, HCO 3-, and H2O in cell suspensions. In addition, we measure the alkaline surface pH (pHS) transients caused by the dominant effect of entry of CO2 vs. HCO3- into oocytes exposed to step increases in [CO2]. We report that 1) AQP1 constitutes the major pathway for molecular CO2 in human RBCs; lack of AQP1 reduces PCO2 from the normal value of 0.15 ± 0.08 (SD; n=85) cm/s by 60% to 0.06 cm/s. Expression of AQP1 in oocytes increases P CO2 2-fold and doubles the alkaline pHS gradient. 2) pCMBS, an inhibitor of the AQP1 water channel, reduces PCO2 of RBCs solely by action on AQP1 as it has no effect in AQP1-deficient RBCs. 3) P CO2 determinations of RBCs and pHS measurements of oocytes indicate that DIDS inhibits the CO2 pathway of AQP1 by half. 4) RBCs have at least one other DIDS-sensitive pathway for CO2. We conclude that AQP1 is responsible for 60% of the high PCO2 of red cells and that another, so far unidentified, CO2 pathway is present in this membrane that may account for at least 30% of total PCO2.

Original languageEnglish (US)
Pages (from-to)1974-1981
Number of pages8
JournalFASEB Journal
Volume20
Issue number12
DOIs
StatePublished - Oct 2006

Fingerprint

Aquaporin 1
aquaporins
Erythrocyte Membrane
erythrocytes
Membranes
Blood
Erythrocytes
Oocytes
oocytes
4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid
Cells
Cell Membrane Permeability
Aquaporins
Xenopus laevis
membrane permeability
Cell membranes
normal values
cell suspension culture
Suspensions
Reference Values

Keywords

  • CO permeability
  • DIDS
  • Human red cell membrane
  • pCMBS

ASJC Scopus subject areas

  • Agricultural and Biological Sciences (miscellaneous)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry
  • Cell Biology

Cite this

Endeward, V., Musa-Aziz, R., Cooper, G. J., Chen, L. M., Pelletier, M. F., Virkki, L. V., ... Gros, G. (2006). Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB Journal, 20(12), 1974-1981. https://doi.org/10.1096/fj.04-3300com

Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. / Endeward, V.; Musa-Aziz, R.; Cooper, G. J.; Chen, L. M.; Pelletier, M. F.; Virkki, L. V.; Supuran, C. T.; King, Landon Stuart; Boron, W. F.; Gros, G.

In: FASEB Journal, Vol. 20, No. 12, 10.2006, p. 1974-1981.

Research output: Contribution to journalArticle

Endeward, V, Musa-Aziz, R, Cooper, GJ, Chen, LM, Pelletier, MF, Virkki, LV, Supuran, CT, King, LS, Boron, WF & Gros, G 2006, 'Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane', FASEB Journal, vol. 20, no. 12, pp. 1974-1981. https://doi.org/10.1096/fj.04-3300com
Endeward V, Musa-Aziz R, Cooper GJ, Chen LM, Pelletier MF, Virkki LV et al. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB Journal. 2006 Oct;20(12):1974-1981. https://doi.org/10.1096/fj.04-3300com
Endeward, V. ; Musa-Aziz, R. ; Cooper, G. J. ; Chen, L. M. ; Pelletier, M. F. ; Virkki, L. V. ; Supuran, C. T. ; King, Landon Stuart ; Boron, W. F. ; Gros, G. / Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. In: FASEB Journal. 2006 ; Vol. 20, No. 12. pp. 1974-1981.
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AU - Chen, L. M.

AU - Pelletier, M. F.

AU - Virkki, L. V.

AU - Supuran, C. T.

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AU - Gros, G.

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N2 - We report here the application of a previously described method to directly determine the CO2 permeability (PCO2) of the cell membranes of normal human red blood cells (RBCs) vs. those deficient in aquaporin 1 (AQP1), as well as AQP1-expressing Xenopus laevis oocytes. This method measures the exchange of 18O between CO2, HCO 3-, and H2O in cell suspensions. In addition, we measure the alkaline surface pH (pHS) transients caused by the dominant effect of entry of CO2 vs. HCO3- into oocytes exposed to step increases in [CO2]. We report that 1) AQP1 constitutes the major pathway for molecular CO2 in human RBCs; lack of AQP1 reduces PCO2 from the normal value of 0.15 ± 0.08 (SD; n=85) cm/s by 60% to 0.06 cm/s. Expression of AQP1 in oocytes increases P CO2 2-fold and doubles the alkaline pHS gradient. 2) pCMBS, an inhibitor of the AQP1 water channel, reduces PCO2 of RBCs solely by action on AQP1 as it has no effect in AQP1-deficient RBCs. 3) P CO2 determinations of RBCs and pHS measurements of oocytes indicate that DIDS inhibits the CO2 pathway of AQP1 by half. 4) RBCs have at least one other DIDS-sensitive pathway for CO2. We conclude that AQP1 is responsible for 60% of the high PCO2 of red cells and that another, so far unidentified, CO2 pathway is present in this membrane that may account for at least 30% of total PCO2.

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