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Cited by 169Ion Transport and Channel RegulationIon channel regulation and functionATP Synthase and ATPases Research

Stoichiometry and Ion Dependencies of the Intracellular-pH-Regulating Mechanism in Squid Giant Axons

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Boron, W F, Russell, J M·1983·The Journal of general physiology
DOI 10.1085/jgp.81.3.373PMC PMC2215574
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Abstract

The ion transport system responsible for intracellular pH (pHi) regulation in squid giant axons was examined in experiments with pH-sensitive microelectrodes and isotopic fluxes of Na+ and Cl-. In one study, axons were acid-loaded and the rate of the subsequent pHi recovery was used to calculate the acid extrusion rate. There was an absolute dependence of acid extrusion on external Na+, external HCO-3 (at constant pH), and internal Cl-. Furthermore, the dependence of the acid extrusion rate on each of these three parameters was described by Michaelis-Menten kinetics. Acid extrusion was stimulated by an acid pHi, required internal ATP, and was blocked by external 4-acetamido-4'-isothiocyanostilbene-2,2'-disulfonate (SITS). Under a standard set of conditions (i.e., [HCO-3]o = 12 mM, pHo = 8.00, [Na+]o = 425 mM, [Cl-]i = 150 mM, [ATP]i = 4 mM, pHi = 6.5, and 16 degrees C), the mean acid extrusion rate was 7.5 pmol X cm-2 X s-1. In a second study under the above standard conditions, the unidirectional Na+ efflux (measured with 22Na) mediated by the pHi-regulating system was found to be approximately 0, whereas the mean influx was about 3.4 pmol X cm-2 X s-1. This net influx required external HCO-3, internal Cl-, and acid pHi, internal ATP, and was blocked by SITS. In the final series of experiments under the above standard conditions, the unidirectional Cl- influx (measured with 36Cl) mediated by the pHi-regulating system was found to be approximately 0, whereas the mean efflux was approximately 3.9 pmol X cm-2 X s-1. This net efflux required external HCO-3, external Na+, an acid pHi, internal ATP, and was blocked by SITS. We conclude that the pHi-regulating system mediates the obligate net influx of HCO-3 (or equivalent species) and Na+ and the net efflux of Cl- in the stoichiometry of 2:1:1. The transport system is stimulated by intracellular acid loads, requires ATP, and is blocked by SITS.

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  • pH-buffering mechanisms such as Na+/H+ antiporters or histone deacetylation consume cellular energy and can alter gene transcription and reduce cellular growth through changes in the acetylation state of chromatin.

    “However, such mechanisms (e.g., Na+/H+ antiporters or histone deacetylation) consume cellular energy and can alter gene transcription and reduce cellular growth through changes in the acetylation state of chromatin (Boron and Russell, 1983; Bowen and Levinson, 1984; Boron, 2004).”

    From Toward Best Practices for Controlling Mammalian Cell Culture Environments (2022) · cites this paper as Boron and Russell, 1983

    The opening summary (p. 373) reports that the squid axon's pH-regulating transport system requires ATP, supporting an energy requirement for the mechanism studied. The discussion (p. 397) identifies Na+/H+ exchange as a distinct pH-regulating system, but does not establish its energy requirement. The paper does not address histone deacetylation, chromatin acetylation, gene transcription, or cellular growth. (LLM, conf=0.88)

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Authors
Boron, W. F., & Russell, J. M.
ORCID
Boron, W F
Venue
The Journal of general physiology
Publisher
Rockefeller University Press
Published
1983-03-01
Volume
81
Issue
3
Pages
373-399
ISSN
  • 0022-1295 (ISSN-L)
  • 1540-7748
DOI
10.1085/jgp.81.3.373
PMC
PMC2215574
OpenAlex
W2163004322
Cited by
169
References
15
Citations by year
2026: 1 · 2025: 1 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 2 · 2018: 1 · 2016: 1 · 2015: 1 · 2013: 2 · 2012: 1
FWCI
6.52
Type
journal article
Language
en
Open access
Licence
cc-by-nc-sa
Locations
  • The Journal of General Physiology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
Keywords
intracellular pH regulation, squid giant axon, acid extrusion, bicarbonate transport, sodium transport, chloride transport, satellite image time series, ATP dependence, Michaelis-Menten kinetics, acid load, pH-sensitive microelectrodes
MeSH terms
Acids, Animals, Bicarbonates, Biomechanical Phenomena, Chemistry, Chlorides, Hydrogen-Ion Concentration, Intracellular Membranes, Ions, Mathematics, Membrane Potentials, Models, Biological, Sodium, Decapodiformes, Chemical Phenomena

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