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. 2000 Nov;79(5):2572–2582. doi: 10.1016/S0006-3495(00)76497-6

Mechanism generating endocochlear potential: role played by intermediate cells in stria vascularis.

S Takeuchi 1, M Ando 1, A Kakigi 1
PMCID: PMC1301139  PMID: 11053131

Abstract

The endocochlear DC potential (EP) is generated by the stria vascularis, and essential for the normal function of hair cells. Intermediate cells are melanocytes in the stria vascularis. To examine the contribution of the membrane potential of intermediate cells (E(m)) to the EP, a comparison was made between the effects of K(+) channel blockers on the E(m) and those on the EP. The E(m) of dissociated guinea pig intermediate cells was measured in the zero-current clamp mode of the whole-cell patch clamp configuration. The E(m) changed by 55.1 mV per 10-fold changes in extracellular K(+) concentration. Ba(2+), Cs(+), and quinine depressed the E(m) in a dose-dependent manner, whereas tetraethylammonium at 30 mM and 4-aminopyridine at 10 mM had no effect. The reduction of the E(m) by Ba(2+) and Cs(+) was enhanced by lowering the extracellular K(+) concentration from 3.6 mM to 1.2 mM. To examine the effect of the K(+) channel blockers on the EP, the EP of guinea pigs was maintained by vascular perfusion, and K(+) channel blockers were administered to the artificial blood. Ba(2+), Cs(+) and quinine depressed the EP in a dose-dependent manner, whereas tetraethylammonium at 30 mM and 4-aminopyridine at 10 mM did not change the EP. A 10-fold increase in the K(+) concentration in the artificial blood caused a minor decrease in the EP of only 10.6 mV. The changes in the EP were similar to those seen in the E(m) obtained at the lower extracellular K(+) concentration of 1.2 mM. On the basis of these results, we propose that the EP is critically dependent on the voltage jump across the plasma membrane of intermediate cells, and that K(+) concentration in the intercellular space in the stria vascularis may be actively controlled at a concentration lower than the plasma level.

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Selected References

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  1. Ando M., Takeuchi S. Immunological identification of an inward rectifier K+ channel (Kir4.1) in the intermediate cell (melanocyte) of the cochlear stria vascularis of gerbils and rats. Cell Tissue Res. 1999 Oct;298(1):179–183. doi: 10.1007/s004419900066. [DOI] [PubMed] [Google Scholar]
  2. Armstrong C. M., Taylor S. R. Interaction of barium ions with potassium channels in squid giant axons. Biophys J. 1980 Jun;30(3):473–488. doi: 10.1016/S0006-3495(80)85108-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baker P. F., Blaustein M. P., Keynes R. D., Manil J., Shaw T. I., Steinhardt R. A. The ouabain-sensitive fluxes of sodium and potassium in squid giant axons. J Physiol. 1969 Feb;200(2):459–496. doi: 10.1113/jphysiol.1969.sp008703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cable J., Huszar D., Jaenisch R., Steel K. P. Effects of mutations at the W locus (c-kit) on inner ear pigmentation and function in the mouse. Pigment Cell Res. 1994 Feb;7(1):17–32. doi: 10.1111/j.1600-0749.1994.tb00015.x. [DOI] [PubMed] [Google Scholar]
  5. Crouch J. J., Sakaguchi N., Lytle C., Schulte B. A. Immunohistochemical localization of the Na-K-Cl co-transporter (NKCC1) in the gerbil inner ear. J Histochem Cytochem. 1997 Jun;45(6):773–778. doi: 10.1177/002215549704500601. [DOI] [PubMed] [Google Scholar]
  6. Diwan J. J. Effect of quinine on mitochondrial K+ and Mg++ flux. Biochem Biophys Res Commun. 1986 Mar 28;135(3):830–836. doi: 10.1016/0006-291x(86)91003-x. [DOI] [PubMed] [Google Scholar]
  7. Duhm J. Furosemide-sensitive K+ (Rb+) transport in human erythrocytes: modes of operation, dependence on extracellular and intracellular Na+, kinetics, pH dependency and the effect of cell volume and N-ethylmaleimide. J Membr Biol. 1987;98(1):15–32. doi: 10.1007/BF01871042. [DOI] [PubMed] [Google Scholar]
  8. Hagiwara S., Miyazaki S., Rosenthal N. P. Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J Gen Physiol. 1976 Jun;67(6):621–638. doi: 10.1085/jgp.67.6.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hilding D. A., Ginzberg R. D. Pigmentation of the stria vascularis. The contribution of neural crest melanocytes. Acta Otolaryngol. 1977 Jul-Aug;84(1-2):24–37. doi: 10.3109/00016487709123939. [DOI] [PubMed] [Google Scholar]
  10. Ikeda K., Morizono T. Electrochemical profiles for monovalent ions in the stria vascularis: cellular model of ion transport mechanisms. Hear Res. 1989 Jun 1;39(3):279–286. doi: 10.1016/0378-5955(89)90047-6. [DOI] [PubMed] [Google Scholar]
  11. Iwano T., Yamamoto A., Omori K., Akayama M., Kumazawa T., Tashiro Y. Quantitative immunocytochemical localization of Na+,K+-ATPase alpha-subunit in the lateral wall of rat cochlear duct. J Histochem Cytochem. 1989 Mar;37(3):353–363. doi: 10.1177/37.3.2537354. [DOI] [PubMed] [Google Scholar]
  12. Kikuchi T., Kimura R. S., Paul D. L., Adams J. C. Gap junctions in the rat cochlea: immunohistochemical and ultrastructural analysis. Anat Embryol (Berl) 1995 Feb;191(2):101–118. doi: 10.1007/BF00186783. [DOI] [PubMed] [Google Scholar]
  13. Kobayashi T., Rokugo M., Marcus D. C., Comegys T. H., Thalmann R. Prolonged maintenance of endocochlear potential by vascular perfusion with media devoid of oxygen carriers. Arch Otorhinolaryngol. 1984;239(3):243–247. doi: 10.1007/BF00464250. [DOI] [PubMed] [Google Scholar]
  14. Konishi T., Hamrick P. E., Walsh P. J. Ion transport in guinea pig cochlea. I. Potassium and sodium transport. Acta Otolaryngol. 1978 Jul-Aug;86(1-2):22–34. doi: 10.3109/00016487809124717. [DOI] [PubMed] [Google Scholar]
  15. Kuijpers W., Bonting S. L. Studies on (Na+-K+)-activated ATPase. XXIV. Localization and properties of ATPase in the inner ear of the guinea pig. Biochim Biophys Acta. 1969 Apr;173(3):477–485. doi: 10.1016/0005-2736(69)90012-1. [DOI] [PubMed] [Google Scholar]
  16. Marcus D. C., Rokugo M., Thalmann R. Effects of barium and ion substitutions in artificial blood on endocochlear potential. Hear Res. 1985 Jan;17(1):79–86. doi: 10.1016/0378-5955(85)90133-9. [DOI] [PubMed] [Google Scholar]
  17. Melichar I., Syka J. Electrophysiological measurements of the stria vascularis potentials in vivo. Hear Res. 1987;25(1):35–43. doi: 10.1016/0378-5955(87)90077-3. [DOI] [PubMed] [Google Scholar]
  18. Offner F. F., Dallos P., Cheatham M. A. Positive endocochlear potential: mechanism of production by marginal cells of stria vascularis. Hear Res. 1987;29(2-3):117–124. doi: 10.1016/0378-5955(87)90160-2. [DOI] [PubMed] [Google Scholar]
  19. Salt A. N., Melichar I., Thalmann R. Mechanisms of endocochlear potential generation by stria vascularis. Laryngoscope. 1987 Aug;97(8 Pt 1):984–991. [PubMed] [Google Scholar]
  20. Steel K. P., Barkway C. Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development. 1989 Nov;107(3):453–463. doi: 10.1242/dev.107.3.453. [DOI] [PubMed] [Google Scholar]
  21. Takeuchi S., Ando M. Dye-coupling of melanocytes with endothelial cells and pericytes in the cochlea of gerbils. Cell Tissue Res. 1998 Aug;293(2):271–275. doi: 10.1007/s004410051118. [DOI] [PubMed] [Google Scholar]
  22. Takeuchi S., Ando M. Inwardly rectifying K+ currents in intermediate cells in the cochlea of gerbils: a possible contribution to the endocochlear potential. Neurosci Lett. 1998 May 15;247(2-3):175–178. doi: 10.1016/s0304-3940(98)00318-8. [DOI] [PubMed] [Google Scholar]
  23. Takeuchi S., Ando M., Irimajiri A. Changes in the volume of marginal cells induced by isotonic 'Cl- depletion/restoration': involvement of the Cl- channel and Na+-K+-Cl- cotransporter. Hear Res. 1997 Nov;113(1-2):99–109. doi: 10.1016/s0378-5955(97)00134-2. [DOI] [PubMed] [Google Scholar]
  24. Takeuchi S., Ando M., Kozakura K., Saito H., Irimajiri A. Ion channels in basolateral membrane of marginal cells dissociated from gerbil stria vascularis. Hear Res. 1995 Mar;83(1-2):89–100. doi: 10.1016/0378-5955(94)00191-r. [DOI] [PubMed] [Google Scholar]
  25. Takeuchi S., Ando M. Voltage-dependent outward K(+) current in intermediate cell of stria vascularis of gerbil cochlea. Am J Physiol. 1999 Jul;277(1 Pt 1):C91–C99. doi: 10.1152/ajpcell.1999.277.1.C91. [DOI] [PubMed] [Google Scholar]
  26. Takeuchi S., Irimajiri A. A novel, volume-correlated Cl- conductance in marginal cells dissociated from the stria vascularis of gerbils. J Membr Biol. 1996 Mar;150(1):47–62. doi: 10.1007/s002329900029. [DOI] [PubMed] [Google Scholar]
  27. Takeuchi S., Irimajiri A. Maxi-K+ channel in plasma membrane of basal cells dissociated from the stria vascularis of gerbils. Hear Res. 1996 May;95(1-2):18–25. doi: 10.1016/0378-5955(96)00016-0. [DOI] [PubMed] [Google Scholar]
  28. Takeuchi S., Kakigi A., Takeda T., Saito H., Irimajiri A. Intravascularly applied K(+)-channel blockers suppress differently the positive endocochlear potential maintained by vascular perfusion. Hear Res. 1996 Nov 1;101(1-2):181–185. doi: 10.1016/s0378-5955(96)00151-7. [DOI] [PubMed] [Google Scholar]
  29. Vetter D. E., Mann J. R., Wangemann P., Liu J., McLaughlin K. J., Lesage F., Marcus D. C., Lazdunski M., Heinemann S. F., Barhanin J. Inner ear defects induced by null mutation of the isk gene. Neuron. 1996 Dec;17(6):1251–1264. doi: 10.1016/s0896-6273(00)80255-x. [DOI] [PubMed] [Google Scholar]
  30. Wada J., Kambayashi J., Marcus D. C., Thalmann R. Vascular perfusion of the cochlea: effect of potassium-free and rubidium-substituted media. Arch Otorhinolaryngol. 1979;225(2):79–81. doi: 10.1007/BF00455206. [DOI] [PubMed] [Google Scholar]
  31. Wada J., Paloheimo S., Thalmann I., Bohne B. A., Thalmann R. Maintenance of cochlear function with artificial oxygen carriers. Laryngoscope. 1979 Sep;89(9 Pt 1):1457–1473. doi: 10.1002/lary.5540890911. [DOI] [PubMed] [Google Scholar]
  32. Wang J., Li Q. H., Dong W. J., Chen J. S. Effects of K(+)-channel blockers on cochlear potentials in the guinea pig. Hear Res. 1993 Aug;68(2):152–158. doi: 10.1016/0378-5955(93)90119-l. [DOI] [PubMed] [Google Scholar]
  33. Wangemann P. Comparison of ion transport mechanisms between vestibular dark cells and strial marginal cells. Hear Res. 1995 Oct;90(1-2):149–157. doi: 10.1016/0378-5955(95)00157-2. [DOI] [PubMed] [Google Scholar]
  34. Wangemann P., Liu J., Marcus D. C. Ion transport mechanisms responsible for K+ secretion and the transepithelial voltage across marginal cells of stria vascularis in vitro. Hear Res. 1995 Apr;84(1-2):19–29. doi: 10.1016/0378-5955(95)00009-s. [DOI] [PubMed] [Google Scholar]
  35. Wangemann P., Shen Z., Liu J. K(+)-induced stimulation of K+ secretion involves activation of the IsK channel in vestibular dark cells. Hear Res. 1996 Oct;100(1-2):201–210. doi: 10.1016/0378-5955(96)00127-x. [DOI] [PubMed] [Google Scholar]

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