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Structure and distribution of gap junctions in lens epithelium and fiber cells

Summary

We report a comparative study of gap junctions in lens epithelia of frog, rabbit, rat and human, using a “double mounting” method for freeze-fracture electron microscopy. The gap junctions on the narrow sides of hexagonal cortical fiber cells of various species were also studied with the same technique. Gap junctions were commonly present between epithelial cells of the entire undifferentiated epithelium, between fiber cells on both wide and narrow sides, and between epithelial cells and fiber cells. Structural diversity of gap junctions, based on connexon arrangements, was evident in lens epithelia among the four species studied. Gap junctions with random arrays of connexons were found predominantly in frog lens epithelium, while the crystalline and striated configurations were mainly observed in the epithelia of human and rat, and of rabbit, respectively. On the other hand, there was no structural variation of gap junctions observed on either wide or narrow sides of lens fiber cells from any species studied. Only the random-type gap junction was found. However, the distribution of gap junctions was unique on the narrow sides. There was a single row of junctional plaques along the middle of the narrow sides, whereas the wide sides showed an uneven distribution pattern. The gap junctions between epithelial cells and fiber cells had a random packing of connexons.

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References

  1. Alcala J, Katar M, Maisel H (1983) Lipid composition of chick lens fiber cell gap junctions. Curr Eye Res 2:569–578

  2. Benedetti EL, Dunia I, Bloemendal H (1974) Development of junctions during differentiation of lens fibers. Proc Natl Acad Sci 71:5073–5077

  3. Benedetti EL, Dunia I, Bentzel CJ, Vermorken AIM, Kibbelaar M, Bloemendal H (1976) A portrait of plasma membrane specializations in eye lens epithelium and fibers. Biochim Biophys Acta 457:353–384

  4. Bennett MVL (1973) Function of electrotonic junctions in embryonic and adult tissues. Fed Proc 32:65–75

  5. Bok D, Dockstader J, Horwitz J (1982) Immunocytochemical localization of the lens main intrinsic polypeptide (MIP26) in communicating junctions. J Cell Biol 92:213–220

  6. Chylack LT Jr (1978) Classification of human cataracts. Arch Ophthalmol 96:888–892

  7. Fitzgerald PG, Bok D, Horwitz J (1983) Immunocytochemical localization of the main intrinsic polypeptide (MIP) in ultrathin frozen sections of rat lens. J Cell Biol 97:1491–1499

  8. Freddo TF (1984) Intercellular junctions of the iris epithelial in Macaca mulatta. Invest Ophthalmol Vis Sci 25:1094–1104

  9. Friend DS, Gilula NB (1972) Variations in tight and gap junctions in mammalian tissues. J Cell Biol 53:758–776

  10. Gilula NB, Reeves OR, Steinbach A (1972) Metabolic coupling, ionic coupling and cell contacts. Nature 235:262–265

  11. Goodenough DA (1979) Lens gap junctions: A structural hypothesis for nonregulated low-resistance intercellular pathways. Invest Ophthalmol Vis Sci 18:1104–1122

  12. Goodenough DA, Dick JSB II, Lyons JE (1980) Lens metabolic cooperation: A study of mouse lens transport and permeability visualized with freeze-substitution autoradiography and electron microscopy. J Cell Biol 86:576–589

  13. Green CR, Severs NJ (1984) Gap junction connexon configuration in rapidly frozen myocardium and isolated intercalated disks. J Cell Biol 99:453–463

  14. Harding CV, Susan SR, Murphy H (1976) Scanning electron microscopy of the adult rabbit lens. Ophthalmic Res 8:443–455

  15. Harding CV, Maisel H, Chylack LT, Susan SR, Lo WK, Bobrowski WF (1985) The structure of the human cataractous lens. In: Maisel H (ed) The ocular lens. Marcel Dekker Inc., New York, pp 367–404

  16. Hertzberg EL (1980) Biochemical and immunological approaches to the study of gap junctional communication. In Vitro 16:1057–1067

  17. Hertzberg EL, Skibbens RV (1984) A protein homologous to the 27000 dalton liver gap junction protein is present in a wide variety of species and tissues. Cell 39:61–69

  18. Hertzberg EL, Anderson DJ, Friedlander M, Gilula NB (1982) Comparative analysis of the major polypeptides from liver gap junctions and lens fiber junctions. J Cell Biol 92:53–59

  19. Jamieson JD, Palade GE (1967) Intercellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. J Cell Biol 34:577–596

  20. Kistler J, Kirkland B, Bullivant S (1985) Identification of a 70000-D. protein in lens membrane junctional domains. J Cell Biol 101:28–35

  21. Kreutziger GO (1976) Lateral membrane morphology and gap junction structure in rabbit corneal endothelium. Exp Eye Res 23:285–293

  22. Kuszak J, Maisel H, Harding CV (1978) Gap junctions of chick lens fiber cells. Exp Eye Res 27:495–498

  23. Kuszak J, Alcala J, Maisel H (1980) The surface morphology of embryonic and adult chick lens-fiber cells. Am J Anat 159:395–410

  24. Kuwabara T (1975) The maturation of the lens cell: A morphologic study. Exp Eye Res 20:427–443

  25. Larsen WJ (1977) Structural diversity of gap junctions. A review. Tissue Cell 9:373–394

  26. Leeson TS (1971) Lens of the rat eye: An electron microscope and freeze-etch study. Exp Eye Res 11:78–82

  27. Lo W-K, Harding CV (1982) A comparative study of gap junctions in lens epithelia. Invest Ophthalmol Vis Sci 22 (Suppl):147

  28. Lo W-K, Harding CV (1983) Tight junctions in the lens epithelia of human and frog: Freeze-fracture and protein tracer studies. Invest Ophthalmol Vis Sci 24:396–402

  29. Lo W-K, Harding CV (1984) Square arrays and their role in ridge formation in human lens fibers. J Ultrastruct Res 86:228–245

  30. Lo W-K, Harding CV, Maisel H (1980) Gap junctions in the human cataractous lens. J Cell Biol 87:56a

  31. Maisel H, Harding CV, Alcala JR, Kuszak J, Bradley R (1981) The morphology of the lens. In: Blomendal E (ed) Molecular and cellular biology of the eye lens, John Wiley and Sons, New York, pp 49–84

  32. Meda O, Findlay I, Kolod E, Orci L, Petersen OH (1983) Short and reversible uncoupling evokes little change in the gap junctions of pancreatic acinar cells. J Ultrastruct Res 83:69–84

  33. Nicholson BJ, Takemoto LJ, Hunkapiller MW, Hood LE, Revel JP (1983) Differences between liver gap junction protein and lens MIP26 from rat: implication for tissue specificity of gap junctions. Cell 32:967–978

  34. Paul DL, Goodenough DA (1983) Preparation, characterization and localization of antisera against bovine MP26, an integral protein from lens fiber plasma membrane. J Cell Biol 96:625–632

  35. Peracchia C (1980) Structural correlates of gap junction permeation. Int Rev Cytol 66:81–146

  36. Pitts JD, Simms JW (1977) Permeability of junctions between animal cells. Intercellular transfer of nucleotides but not of macromolecules. Exp Cell Res 104:153–163

  37. Raviola G, Raviola E (1978) Intercellular junctions in the ciliary epithelium. Invest Ophthalmol 17:958–981

  38. Raviola E, Goodenough DA, Raviola G (1980) Structure of rapidly frozen gap junctions. J Cell Biol 87:273–279

  39. Revel JP, Nicholsen BJ, Yancey SB (1984) Molecular organization of gap junctions. Fed Proc 43:2672–2677

  40. Sas DF, Johnson KR, Menko AS, Johnson RG (1985) Junctions between lens fiber cells are labeled with a monoclonal antibody shown to be specific for MP26. J Cell Biol 100:216–225

  41. Simionescu M, Simionescu N (1976) Segemental differentiations of cell junctions in the vascular endothelium. Arteries and veins. J Cell Biol 68:705–723

  42. Subak-Shapre H, Burk RR, Pitts JD (1969) Metabolic cooperation between biochemically marked mammalian cells in tissue culture. J Cell Sci 4:353–367

  43. Tanaka M, Russel P, Smith S, Uga S, Kuwabara T, Kinoshita JH (1980) Membrane alterations during cataract development in the Nakano mouse lens. Invest Ophthalmol Vis Sci 19:619–629

  44. Waggoner PR, Maisel H (1978) Immunofluorescent study of a chick lens fiber cell membrane polypeptide. Exp Eye Res 27:151–157

  45. Zampighi G, Simon SA, Robertson JD, McIntosh TJ, Costello MJ (1982) On the structural organization of isolated bovine lens fiber junctions. J Cell Biol 93:175–189

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Correspondence to Dr. Woo-Kuen Lo.

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Lo, W., Harding, C.V. Structure and distribution of gap junctions in lens epithelium and fiber cells. Cell Tissue Res. 244, 253–263 (1986). https://doi.org/10.1007/BF00219200

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Key words

  • Gap junction
  • Lens
  • Epithelium
  • Fiber cells
  • Freeze-fracture
  • Vertebrales