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. 1986 Jan 1;102(1):194–199. doi: 10.1083/jcb.102.1.194

Evidence for two physiologically distinct gap junctions expressed by the chick lens epithelial cell

PMCID: PMC2114033  PMID: 3079768

Abstract

Lens epithelial cells communicate with two different cell types. They communicate with other epithelial cells via gap junctions on their lateral membranes, and with fiber cells via junctions on their apices. We tested independently these two routes of cell-cell communication to determine if treatment with a 90% CO2-equilibrated medium caused a decrease in junctional permeability; the transfer of fluorescent dye was used as the assay. We found that the high-CO2 treatment blocked intraepithelial dye transfer but not fiber-to-epithelium dye transfer. The lens epithelial cell thus forms at least two physiologically distinct classes of gap junctions.

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Selected References

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  1. Anderson E., Albertini D. F. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol. 1976 Nov;71(2):680–686. doi: 10.1083/jcb.71.2.680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Azarnia R., Larsen W. J., Loewenstein W. R. The membrane junctions in communicating and noncommunicating cells, their hybrids, and segregants. Proc Natl Acad Sci U S A. 1974 Mar;71(3):880–884. doi: 10.1073/pnas.71.3.880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benedetti E. L., Dunia I., Bentzel C. J., Vermorken A. J., Kibbelaar M., Bloemendal H. A portrait of plasma membrane specializations in eye lens epithelium and fibers. Biochim Biophys Acta. 1976 Dec 14;457(3-4):353–384. doi: 10.1016/0304-4157(76)90004-6. [DOI] [PubMed] [Google Scholar]
  4. Burt J. M., Frank J. S., Berns M. W. Permeability and structural studies of heart cell gap junctions under normal and altered ionic conditions. J Membr Biol. 1982;68(3):227–238. doi: 10.1007/BF01872267. [DOI] [PubMed] [Google Scholar]
  5. Caveney S. Intercellular communication in a positional field: movement of small ions between insect epidermal cells. Dev Biol. 1974 Oct;40(2):311–322. doi: 10.1016/0012-1606(74)90133-x. [DOI] [PubMed] [Google Scholar]
  6. Epstein M. L., Gilula N. B. A study of communication specificity between cells in culture. J Cell Biol. 1977 Dec;75(3):769–787. doi: 10.1083/jcb.75.3.769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fentiman I., Taylor-Papadimitriou J., Stoker M. Selective contact-dependent cell communication. Nature. 1976 Dec 23;264(5588):760–762. doi: 10.1038/264760a0. [DOI] [PubMed] [Google Scholar]
  8. Fisher S. K., Linberg K. A. Intercellular junctions in the early human embryonic retina. J Ultrastruct Res. 1975 Apr;51(1):69–78. doi: 10.1016/s0022-5320(75)80009-8. [DOI] [PubMed] [Google Scholar]
  9. Flagg-Newton J. L., Loewenstein W. R. Asymmetrically permeable membrane channels in cell junction. Science. 1980 Feb 15;207(4432):771–773. doi: 10.1126/science.7352287. [DOI] [PubMed] [Google Scholar]
  10. Flagg-Newton J., Simpson I., Loewenstein W. R. Permeability of the cell-to-cell membrane channels in mammalian cell juncton. Science. 1979 Jul 27;205(4404):404–407. doi: 10.1126/science.377490. [DOI] [PubMed] [Google Scholar]
  11. Gaunt S. J., Subak-Sharpe J. H. Selectivity in metabolic cooperation between cultured mammalian cells. Exp Cell Res. 1979 May;120(2):307–320. doi: 10.1016/0014-4827(79)90391-4. [DOI] [PubMed] [Google Scholar]
  12. Gilula N. B., Reeves O. R., Steinbach A. Metabolic coupling, ionic coupling and cell contacts. Nature. 1972 Feb 4;235(5336):262–265. doi: 10.1038/235262a0. [DOI] [PubMed] [Google Scholar]
  13. Goodenough D. A., Dick J. S., 2nd, Lyons J. E. Lens metabolic cooperation: a study of mouse lens transport and permeability visualized with freeze-substitution autoradiography and electron microscopy. J Cell Biol. 1980 Aug;86(2):576–589. doi: 10.1083/jcb.86.2.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gros D. B., Nicholson B. J., Revel J. P. Comparative analysis of the gap junction protein from rat heart and liver: is there a tissue specificity of gap junctions? Cell. 1983 Dec;35(2 Pt 1):539–549. doi: 10.1016/0092-8674(83)90188-5. [DOI] [PubMed] [Google Scholar]
  15. Hama K. Fine structure of the afferent synapse and gap junctions on the sensory hair cell in the saccular macula of goldfish: a freeze-fracture study. J Neurocytol. 1980 Dec;9(6):845–860. doi: 10.1007/BF01205023. [DOI] [PubMed] [Google Scholar]
  16. Hertzberg E. L., Anderson D. J., Friedlander M., Gilula N. B. Comparative analysis of the major polypeptides from liver gap junctions and lens fiber junctions. J Cell Biol. 1982 Jan;92(1):53–59. doi: 10.1083/jcb.92.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Johnson R. G., Herman W. S., Preus D. M. Homocellular and heterocellular gap junctions in Limulus: a thin-section and freeze-fracture study. J Ultrastruct Res. 1973 May;43(3):298–312. doi: 10.1016/s0022-5320(73)80040-1. [DOI] [PubMed] [Google Scholar]
  18. Johnston M. F., Ramón F. Electrotonic coupling in internally perfused crayfish segmented axons. J Physiol. 1981 Aug;317:509–518. doi: 10.1113/jphysiol.1981.sp013840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kogon M., Pappas G. D. Atypical gap junctions in the ciliary epithelium of the albino rabbit eye. J Cell Biol. 1975 Sep;66(3):671–676. doi: 10.1083/jcb.66.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kuszak J. R., Rae J. L., Pauli B. U., Weinstein R. S. Rotary replication of lens gap junction. J Ultrastruct Res. 1982 Nov;81(2):249–256. doi: 10.1016/s0022-5320(82)90080-6. [DOI] [PubMed] [Google Scholar]
  21. Kuszak J., Maisel H., Harding C. V. Gap junctions of chick lens fiber cells. Exp Eye Res. 1978 Oct;27(4):495–498. doi: 10.1016/0014-4835(78)90026-x. [DOI] [PubMed] [Google Scholar]
  22. Larsen W. J. Structural diversity of gap junctions. A review. Tissue Cell. 1977;9(3):373–394. doi: 10.1016/0040-8166(77)90001-5. [DOI] [PubMed] [Google Scholar]
  23. Miller T. M., Goodenough D. A. Gap junction structures after experimental alteration of junctional channel conductance. J Cell Biol. 1985 Nov;101(5 Pt 1):1741–1748. doi: 10.1083/jcb.101.5.1741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nadol J. B., Jr, Mulroy M. J., Goodenough D. A., Weiss T. F. Tight and gap junctions in a vertebrate inner ear. Am J Anat. 1976 Nov;147(3):281–301. doi: 10.1002/aja.1001470304. [DOI] [PubMed] [Google Scholar]
  25. Nicholson B. J., Takemoto L. J., Hunkapiller M. W., Hood L. E., Revel J. P. Differences between liver gap junction protein and lens MIP 26 from rat: implications for tissue specificity of gap junctions. Cell. 1983 Mar;32(3):967–978. doi: 10.1016/0092-8674(83)90081-8. [DOI] [PubMed] [Google Scholar]
  26. Noirot C., Noirot-Timothée C. Fine structure of the rectum in cockroaches (Dictyoptera): general organization and intercellular junctions. Tissue Cell. 1976;8(2):345–368. doi: 10.1016/0040-8166(76)90057-4. [DOI] [PubMed] [Google Scholar]
  27. Peracchia C. Calcium effects on gap junction structure and cell coupling. Nature. 1978 Feb 16;271(5646):669–671. doi: 10.1038/271669a0. [DOI] [PubMed] [Google Scholar]
  28. Potter D. D., Furshpan E. J., Lennox E. S. Connections between cells of the developing squid as revealed by electrophysiological methods. Proc Natl Acad Sci U S A. 1966 Feb;55(2):328–336. doi: 10.1073/pnas.55.2.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rae J. L., Kuszak J. R. The electrical coupling of epithelium and fibers in the frog lens. Exp Eye Res. 1983 Mar;36(3):317–326. doi: 10.1016/0014-4835(83)90114-8. [DOI] [PubMed] [Google Scholar]
  30. Revel J. P., Yee A. G., Hudspeth A. J. Gap junctions between electrotonically coupled cells in tissue culture and in brown fat. Proc Natl Acad Sci U S A. 1971 Dec;68(12):2924–2927. doi: 10.1073/pnas.68.12.2924. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schuetze S. M., Goodenough D. A. Dye transfer between cells of the embryonic chick lens becomes less sensitive to CO2 treatment with development. J Cell Biol. 1982 Mar;92(3):694–705. doi: 10.1083/jcb.92.3.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sheridan J. D. Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo. J Cell Biol. 1968 Jun;37(3):650–659. doi: 10.1083/jcb.37.3.650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Spray D. C., Stern J. H., Harris A. L., Bennett M. V. Gap junctional conductance: comparison of sensitivities to H and Ca ions. Proc Natl Acad Sci U S A. 1982 Jan;79(2):441–445. doi: 10.1073/pnas.79.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Staehelin L. A. Three types of gap junctions interconnecting intestinal epithelial cells visualized by freeze-etching. Proc Natl Acad Sci U S A. 1972 May;69(5):1318–1321. doi: 10.1073/pnas.69.5.1318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stewart W. W. Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell. 1978 Jul;14(3):741–759. doi: 10.1016/0092-8674(78)90256-8. [DOI] [PubMed] [Google Scholar]
  36. Warner A. E., Lawrence P. A. Electrical coupling across developmental boundaries in insect epidermis. Nature. 1973 Sep 7;245(5419):47–48. doi: 10.1038/245047a0. [DOI] [PubMed] [Google Scholar]
  37. Warner A. E., Lawrence P. A. Permeability of gap junctions at the segmental border in insect epidermis. Cell. 1982 Feb;28(2):243–252. doi: 10.1016/0092-8674(82)90342-7. [DOI] [PubMed] [Google Scholar]

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