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. 1982;328:87–104. doi: 10.1113/jphysiol.1982.sp014254

Ungulate cardiac Purkinje fibres: the influence of intracellular pH on the electrical cell-to-cell coupling

Walter R Reber 1, Robert Weingart 1
PMCID: PMC1225648  PMID: 6290650

Abstract

1. Passive electrical properties of sheep cardiac Purkinje fibres were assessed by performing linear cable analysis. In a separate set of experiments pHi was monitored using recessed-tip pH-sensitive micro-electrodes.

2. In Tris-buffered Tyrode solution (nominally CO2-free), the pHi was 7·27, in bicarbonate-buffered solution equilibrated with 6% CO2, the mean pHi was 7·02.

3. Application of 15 mM-NH4Cl produced a rapid intracellular alkalinization (0·19 pH units), followed by a slower acidification. Removal of NH4Cl gave rise to a slow and transient intracellular acidification (0·5 pH units).

4. The biphasic and transient shift in pHi, induced by the NH4Cl treatment, was accompanied by a change of the inside longitudinal resistance per unit fibre length, ri, displaying a similar time course. The increase in pHi produced a maximum decrease in ri of 16·4%, while the decrease in pHi yielded a maximum increase in ri of 30·4%.

5. Changing from bicarbonate-buffered Tyrode solution equilibrated with 6% CO2 to Tris-buffered Tyrode solution led to an increase in pHi (0·26 pH units). A subsequent change to bicarbonate-buffered Tyrode solution equilibrated with 15% CO2 produced a decrease in pHi (0·48 pH units). Both changes were sustained.

6. This CO2 protocol gave rise to corresponding changes in ri; the intracellular alkalosis was associated with a decrease in ri (21·2%), and the intracellular acidosis was accompanied by an increase in ri (30%).

7. Based on recent findings showing an interaction between pHi and pCai (Hess & Weingart, 1980), it is concluded that the changes in ri are directly caused by protons and not indirectly via secondary changes of the [Ca2+]i.

8. The pHi-dependent changes in ri are likely to reflect alterations of the nexal resistance, rn, because the cytoplasmic resistance, rc, has the inverse sensitivity to pHi.

9. Unlike pCai, pHi would seem to be able to modify the cell-to-cell coupling by increasing or decreasing ri over a rather narrow range, without ever producing electrical uncoupling.

10. Because of basic differences in the action of calcium and protons on the cell-to-cell coupling (magnitude of the effect, operative concentration range), it is tempting to conclude that there is more than one kind of binding site which controls the nexal conductance.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aickin C. C., Thomas R. C. An investigation of the ionic mechanism of intracellular pH regulation in mouse soleus muscle fibres. J Physiol. 1977 Dec;273(1):295–316. doi: 10.1113/jphysiol.1977.sp012095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alvarez-Leefmans F. J., Rink T. J., Tsien R. Y. Free calcium ions in neurones of Helix aspersa measured with ion-selective micro-electrodes. J Physiol. 1981 Jun;315:531–548. doi: 10.1113/jphysiol.1981.sp013762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker P. F., Honerjäger P. Influence of carbon dioxide on level of ionised calcium in squid axons. Nature. 1978 May 11;273(5658):160–161. doi: 10.1038/273160a0. [DOI] [PubMed] [Google Scholar]
  4. Boron W. F., De Weer P. Intracellular pH transients in squid giant axons caused by CO2, NH3, and metabolic inhibitors. J Gen Physiol. 1976 Jan;67(1):91–112. doi: 10.1085/jgp.67.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brown R. H., Jr, Noble D. Displacement of activator thresholds in cardiac muscle by protons and calcium ions. J Physiol. 1978 Sep;282:333–343. doi: 10.1113/jphysiol.1978.sp012466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carafoli E., Crompton M. The regulation of intracellular calcium by mitochondria. Ann N Y Acad Sci. 1978 Apr 28;307:269–284. doi: 10.1111/j.1749-6632.1978.tb41957.x. [DOI] [PubMed] [Google Scholar]
  7. Dahl G., Isenberg G. Decoupling of heart muscle cells: correlation with increased cytoplasmic calcium activity and with changes of nexus ultrastructure. J Membr Biol. 1980 Mar 31;53(1):63–75. doi: 10.1007/BF01871173. [DOI] [PubMed] [Google Scholar]
  8. De Mello W. C. Influence of intracellular injection of H+ on the electrical coupling in cardiac Purkinje fibres. Cell Biol Int Rep. 1980 Jan;4(1):51–58. doi: 10.1016/0309-1651(80)90009-0. [DOI] [PubMed] [Google Scholar]
  9. De Mello W. C. Passive electrical properties of the atrio-ventricular node. Pflugers Arch. 1977 Oct 19;371(1-2):135–139. doi: 10.1007/BF00580781. [DOI] [PubMed] [Google Scholar]
  10. Deitmer J. W., Ellis D. Interactions between the regulation of the intracellular pH and sodium activity of sheep cardiac Purkinje fibres. J Physiol. 1980 Jul;304:471–488. doi: 10.1113/jphysiol.1980.sp013337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ellis D., Thomas R. C. Direct measurement of the intracellular pH of mammalian cardiac muscle. J Physiol. 1976 Nov;262(3):755–771. doi: 10.1113/jphysiol.1976.sp011619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fabiato A., Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol. 1978 Mar;276:233–255. doi: 10.1113/jphysiol.1978.sp012231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hermsmeyer K. Angiotensin II increases electrical coupling in mammalian ventricular myocardium. Circ Res. 1980 Oct;47(4):524–529. doi: 10.1161/01.res.47.4.524. [DOI] [PubMed] [Google Scholar]
  14. Hille B., Woodhull A. M., Shapiro B. I. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301–318. doi: 10.1098/rstb.1975.0011. [DOI] [PubMed] [Google Scholar]
  15. Iwatsuki N., Petersen O. H. Pancreatic acinar cells: the effect of carbon dioxide, ammonium chloride and acetylcholine on intercellular communication. J Physiol. 1979 Jun;291:317–326. doi: 10.1113/jphysiol.1979.sp012815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Karmann U., Held D. R. Equations treating the pH and (HCO-3) of buffered media as functions of PCO2. Respir Physiol. 1972 Jul;15(3):343–349. doi: 10.1016/0034-5687(72)90075-8. [DOI] [PubMed] [Google Scholar]
  17. Lea T. J., Ashley C. C. Increase in free Ca2+ in muscle after exposure to CO2. Nature. 1978 Sep 21;275(5677):236–238. doi: 10.1038/275236a0. [DOI] [PubMed] [Google Scholar]
  18. Loewenstein W. R. Junctional intercellular communication and the control of growth. Biochim Biophys Acta. 1979 Feb 4;560(1):1–65. doi: 10.1016/0304-419x(79)90002-7. [DOI] [PubMed] [Google Scholar]
  19. MEVES H., VOLKNER K. G. Die Wirkung von CO2 auf das Ruhemembranpotential und die elektrischen Konstanten der quergestreiften Muskelfaser. Pflugers Arch. 1958;265(5):457–476. doi: 10.1007/BF00369773. [DOI] [PubMed] [Google Scholar]
  20. Marrannes R., De Hemptinne A., Leusen I. Correlation between conduction velocity transients in isolated heart fibres and pH changes (intersititial and intracellular) [proceedings]. Arch Int Physiol Biochim. 1979 Oct;87(4):770–772. [PubMed] [Google Scholar]
  21. Micro-electrode measurement of the intracellular pH and buffering power of mouse soleus muscle fibres. J Physiol. 1977 Jun;267(3):791–810. doi: 10.1113/jphysiol.1977.sp011838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Moynihan J. B. Carbonic anhydrase activity in mammalian skeletal and cardiac muscle. Biochem J. 1977 Dec 15;168(3):567–569. doi: 10.1042/bj1680567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nakamaru Y., Schwartz A. The influence of hydrogen ion concentration on calcium binding and release by skeletal muscle sarcoplasmic reticulum. J Gen Physiol. 1972 Jan;59(1):22–32. doi: 10.1085/jgp.59.1.22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nishiye H., Mashima H., Ishida A. Ca binding of isolated cardiac nexus membranes related to intercellular uncoupling. Jpn J Physiol. 1980;30(1):131–136. doi: 10.2170/jjphysiol.30.131. [DOI] [PubMed] [Google Scholar]
  25. Nonner W., Spalding B. C., Hille B. Low intracellular pH and chemical agents slow inactivation gating in sodium channels of muscle. Nature. 1980 Mar 27;284(5754):360–363. doi: 10.1038/284360a0. [DOI] [PubMed] [Google Scholar]
  26. Peracchia C., Peracchia L. L. Gap junction dynamics: reversible effects of hydrogen ions. J Cell Biol. 1980 Dec;87(3 Pt 1):719–727. doi: 10.1083/jcb.87.3.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Peracchia C. Structural correlates of gap junction permeation. Int Rev Cytol. 1980;66:81–146. doi: 10.1016/s0074-7696(08)61972-5. [DOI] [PubMed] [Google Scholar]
  28. Pollack G. H. Intercellular coupling in the atrioventricular node and other tissues of the rabbit heart. J Physiol. 1976 Feb;255(1):275–298. doi: 10.1113/jphysiol.1976.sp011280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rink T. J., Tsien R. Y., Warner A. E. Free calcium in Xenopus embryos measured with ion-selective microelectrodes. Nature. 1980 Feb 14;283(5748):658–660. doi: 10.1038/283658a0. [DOI] [PubMed] [Google Scholar]
  30. Rose B., Rick R. Intracellular pH, intracellular free Ca, and junctional cell-cell coupling. J Membr Biol. 1978 Dec 29;44(3-4):377–415. doi: 10.1007/BF01944230. [DOI] [PubMed] [Google Scholar]
  31. Schaer H. Decrease in ionized calcium by bicarbonate in physiological solutions. Pflugers Arch. 1974 Mar 11;347(3):249–254. doi: 10.1007/BF00592601. [DOI] [PubMed] [Google Scholar]
  32. Spray D. C., Harris A. L., Bennett M. V. Gap junctional conductance is a simple and sensitive function of intracellular pH. Science. 1981 Feb 13;211(4483):712–715. doi: 10.1126/science.6779379. [DOI] [PubMed] [Google Scholar]
  33. Thomas R. C. Intracellular pH of snail neurones measured with a new pH-sensitive glass mirco-electrode. J Physiol. 1974 Apr;238(1):159–180. doi: 10.1113/jphysiol.1974.sp010516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Turin L., Warner A. E. Intracellular pH in early Xenopus embryos: its effect on current flow between blastomeres. J Physiol. 1980 Mar;300:489–504. doi: 10.1113/jphysiol.1980.sp013174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Turin L., Warner A. Carbon dioxide reversibly abolishes ionic communication between cells of early amphibian embryo. Nature. 1977 Nov 3;270(5632):56–57. doi: 10.1038/270056a0. [DOI] [PubMed] [Google Scholar]
  36. WEIDMANN S. The electrical constants of Purkinje fibres. J Physiol. 1952 Nov;118(3):348–360. doi: 10.1113/jphysiol.1952.sp004799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wanke E., Carbone E., Testa P. L. The sodium channel and intracellular H+ blockage in squid axons. Nature. 1980 Sep 4;287(5777):62–63. doi: 10.1038/287062a0. [DOI] [PubMed] [Google Scholar]
  38. van Bogaert P. P., Vereecke J. S., Carmeliet E. E. The effect of raised pH on pacemaker activity and ionic currents in cardiac Purkinje fibers. Pflugers Arch. 1978 Jun 21;375(1):45–52. doi: 10.1007/BF00584147. [DOI] [PubMed] [Google Scholar]

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