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Intercellular junctions in the gill epithelium of the Atlantic hagfish, Myxine glutinosa

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Summary

The intramembrane organization of the occluding junctions in the gill epithelium of the Atlantic hagfish, Myxine glutinosa, was studied by means of freeze-fracture electron microscopy. Mitochondria-rich cells, characterized by assemblies of rod-shaped particles in the luminal plasma membrane and by an extensive intracellular amplification of the basolateral plasma membrane, are singly distributed between the pavement cells in the gill epithelium of this marine and stenohaline cyclostome. The occluding junctions between mitochondria-rich cells and pavement cells do not differ from those between adjacent pavement cells, concerning the number of superimposed strands (median 6, range 4–9) and their geometrical organization. These observations suggest that, in contrast to marine teleosts, the paracellular pathway plays a minor role in transepithelial ion movements in the hagfish gill epithelium. The findings are in agreement with the absence of hypoosmoregulatory mechanisms in hagfish, as have been evolved in various marine vertebrates. In addition, small communicating junctions are demonstrated between pavement cells; they possibly serve for a coordinated synthesis and secretion of mucus by the pavement cells.

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References

  • Adam H, Schirner H, Walvig F (1962) Versuche zur Narkose und Relaxation von Myxine glutinosa L. Zool Anz 168:216–228

    Google Scholar 

  • Alt JM, Stolte H, Eisenbach GM, Walvig F (1980) Renal electrolyte and fluid excretion in the Atlantic hagfish Myxine glutinosa. J Exp Biol 91:323–330

    Google Scholar 

  • Bachmann S, Sakai T, Kriz W (1986) Nephron and collecting duct structure in the kidney, rat. In: Jones TC, Mohr U, Hunt RD (eds) Urinary system. Springer, Berlin Heidelberg New York, pp 3–24

    Google Scholar 

  • Bartels H (1979) The air-blood barrier in the human lung. A freeze-fracture study. Cell Tissue Res 198:269–285

    CAS  PubMed  Google Scholar 

  • Bartels H (1984) Orthogonal arrays of particles in the gill epithelium of the Atlantic hagifsh, Myxine glutinosa. Cell Tissue Res 238:657–659

    Google Scholar 

  • Bartels H (1985) Assemblies of linear arrays of particles in the apical plasma membrane of mitochondria-rich cells in the gill epithelium of the Atlantic hagfish (Myxine glutinosa). Anat Rec 211:229–238

    Google Scholar 

  • Bartels H, Welsch U (1986) Mitochondria-rich cells in the gill epithelium of cyclostomes. A thin section and freeze fracture study. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Proceedings of the Second International Conference on Indo-Pacific Fishes. Ichthyological Society of Japan, Tokyo, pp 58–72

    Google Scholar 

  • Bartels H, Hilliard RW, Potter IC (1987a) Structural heterogeneity of the occluding junctions in the gill epithelium of seawater-adapted lampreys. Fed Proc 46:1273

    Google Scholar 

  • Bartels H, Hilliard RW, Potter IC (1987b) Structural changes in the plasma membrane of chloride cells in the gills of sea water- and fresh water-adapted lampreys. J Cell Biol 105:305a

    Google Scholar 

  • Brown D, Ilic V (1979) Freeze-fracture differences in plasma membranes of the stratum corneum and replacement layer cells of amphibian epidermis. J Ultrastruct Res 67:55–64

    Google Scholar 

  • Brown D, Ilic V, Orci L (1978) Rod-shaped particles in the plasma membrane of the mitochondria-rich cell of amphibian epidermis. Anat Rec 192:269–276

    Google Scholar 

  • Brown D, Gluck S, Hartwig J (1987) Structure of the novel membrane-coating material in proton-secreting epithelial cells and identification as an H+-ATPase. J Cell Biol 105:1637–1648

    Google Scholar 

  • Claude P (1978) Morphological factors influencing transepithelial permeability: a model for the resistance of the zonula occludens. J Membr Biol 39:219–232

    Google Scholar 

  • Claude P, Goodenough DA (1973) Fracture faces of zonulae occludents from “tight” and “leaky” epithelia. J Cell Biol 58:390–400

    Google Scholar 

  • Crone C (1981) Tight and leaky endothelia. In: Ussing HH, Bindslev N, Lassen NA, Sten-Knudsen O (eds) Water transport across epithelia, Alfred Benzon Symposium 15. Munksgaard, Copenhagen, pp 258–267

    Google Scholar 

  • Elger M (1987) The branchial circulation and the gill epithelia in the Atlantic hagfish, Myxine glutinosa L. Anat Embryol 175:489–504

    Google Scholar 

  • Ellis RA, Goertemiller CC Jr, Stetson DL (1977) Significance of extensive “leaky” cell junctions in the avian salt gland. Nature 268:555–556

    Google Scholar 

  • Ernst SA, Dodson WB, Karnaky KJ Jr (1980a) Structural diversity of occluding junctions in the low-resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus). J Cell Biol 87:488–497

    Google Scholar 

  • Ernst SA, Riddle CV, Karnaky KJ Jr (1980b) Relationship between localization of Na+-K+-ATPase, cellular fine structure, and reabsorptive and secretory electrolyte transport. In: Boulpaep EL (ed) Current Topics in Membranes and Transport, vol. 13. Academic Press, New York, pp 355–385

    Google Scholar 

  • Ernst SA, Hootman SR, Schreiber JH, Riddle CV (1981) Freezefracture and morphometric analysis of occluding junctions in rectal glands of elasmobranch fish. J Membr Biol 58:101–114

    Google Scholar 

  • Foskett JK, Machen TE (1985) Vibrating probe analysis of teleost opercular epithelium: correlation between active transport and leak pathways of individual chloride cells. J Membr Biol 85:25–35

    Google Scholar 

  • Foskett JK, Scheffey C (1982) The chloride cell: definitive identification as the salt-secretory cell in teleosts. Science 215:164–166

    PubMed  Google Scholar 

  • Foskett JK, Logsdon CD, Turner T, Machen TE, Bern HA (1981) Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. J Exp Biol 93:209–224

    Google Scholar 

  • Frömter E, Diamond J (1972) Route of passive ion permeation in epithelia. Nature New Biol 235:9–13

    Google Scholar 

  • Geisweid G, Wermbter G (1974) Die Feinstruktur des Nexus zwischen glatten Muskelzellen der Taenia coli im Gefrierätzbild. Cytobiologie 9:121–130

    Google Scholar 

  • Helman SI, Grantham JJ, Burg MB (1971) Effect of vasopressin on electrical resistance of renal cortical collecting tubules. Am J Physiol 220:1825–1832

    Google Scholar 

  • Higgins JT Jr, Cesaro L, Gebler B, Frömter E (1975) Electrical properties of amphibian urinary bladder epithelia. I. Inverse relationship between potential difference and resistance in tightly mounted preparations. Pflügers Arch 358:41–56

    Google Scholar 

  • Hofbauer M (1934) Anatomischer und histologischer Bau der Kiemensäcke von Myxine glutinosa. Biol Gen 12:330–348

    Google Scholar 

  • Hooper ML, Subak-Sharpe JH (1981) Metabolic cooperation between cells. Int Rev Cytol 69:45–104

    Google Scholar 

  • Hull BE, Staehelin LA (1976) Functional significance of the variations in the geometrical organization of tight junction networks. J Cell Biol 68:688–704

    Google Scholar 

  • Humbert F, Pricam C, Perrelet A, Orci L (1975) Specific plasma membrane differentiations in the cells of the kidney collecting tubule. J Ultrastruct Res 52:13–20

    Google Scholar 

  • Ishimura K, Takagaki K, Egawa K, Fujita H (1979) Characteristic figures of intercellular junctions of the hagfish intestinal epithelium. Freeze-fracture observation. Arch Histol Jpn 42:413–421

    Google Scholar 

  • Karnaky KJ Jr (1980) Ion-secreting epithelia: chloride cells in the head region of Fundulus heteroclitus. Am J Physiol 238:R185-R198

    Google Scholar 

  • Karnaky KJ Jr (1986) Structure and function of the chloride cell of Fundulus heteroclitus and other teleosts. Am Zool 26:209–224

    Google Scholar 

  • Karnaky KJ Jr, Degnan KJ, Zadunaisky JA (1977) Chloride transport across isolated opercular epithelium of killifish: a membrane rich in chloride cells. Science 195:203–205

    Google Scholar 

  • Katz U, v Driessche W, Scheffey C (1985) The role of mitochondria-rich cells in the chloride current conductance across toad skin. Biol Cell 55:245–250

    Google Scholar 

  • Kühn K, Stolte H, Reale E (1975) The fine structure of the kidney of the hagfish (Myxine glutinosa L.). A thin section and freeze-fracture study. Cell Tissue Res 164:201–213

    Google Scholar 

  • Landis DMD, Reese TS, Raviola E (1974) Difference in membrane structure between excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb. J Comp Neurol 155:67–92

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Laurent P (1984) Gill internal morphology. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol. 10, Part A. Academic Press, Orlando, pp 73–183

    Google Scholar 

  • Luciano L, Castellucci M, Reale E (1981) The brush cells of the common bile duct of the rat. Thin section, freeze-fracture and scanning electron microscopy. Cell Tissue Res 218:403–420

    Google Scholar 

  • Luciano L, Thiele J, Reale E (1979) Development of follicles and of occluding junctions between the follicular cells of the thyroid gland. A thin section and freeze-fracture study in the fetal rat. J Ultrastruct Res 66:164–181

    Google Scholar 

  • Luciano L, Reale E, Rechkemmer G, Engelhardt W v (1984) Structure of zonulae occludentes and the permeability of the epithelium to short-chain fatty acids in the proximal and the distal colon of guinea pig. J Membr Biol 82:145–156

    Google Scholar 

  • Mallatt J, Paulsen C (1986) Gill ultrastructure of the pacific hagfish Eptatretus stouti. Am J Anat 177:243–269

    Google Scholar 

  • Marinelli W, Strenger A (1956) Vergleichende Anatomie und Morphologie der Wirbeltiere. II. Myxine glutinosa (L.). F. Deuticke, Wien

    Google Scholar 

  • Marshall WS (1977) Transepithelial potential and short-circuit current across the isolated skin of Gillichthys mirabilis, acclimated to 5% and 100% sea water. J Comp Physiol 114:157–165

    Google Scholar 

  • McFarland W, Munz FW (1965) Regulation of body weight and serum composition by hagfish in various media. Comp Biochem Physiol 14:383–398

    Google Scholar 

  • McNutt NS (1977) Freeze-fracture techniques and applications to the structural analysis of the mammalian plasma membrane. In: Poste G, Nicolson GL (eds) Dynamic aspects of cell surface organization. North-Holland Publishing Company, Amsterdam New York, Oxford, p 75–126

    Google Scholar 

  • Morris R (1965) Studies on salt and water balance in Myxine glutinosa (L.). J Exp Biol 42:359–371

    Google Scholar 

  • Orci L, Humbert F, Brown D, Perrelet A (1981) Membrane ultrastructure in urinary tubules. Int Rev Cytol 73:183–242

    Google Scholar 

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

    Google Scholar 

  • Petersen OH, Findlay I (1987) Electrophysiology of the pancreas. Physiol Rev 67:1054–1116

    Google Scholar 

  • Pohla H, Lametschwandtner A, Adam H (1977) Die Vaskularisation der Kiemen von Myxine glutinosa L. (Cyclostomata). Zool Scripta 6:331–341

    Google Scholar 

  • Rauther M (1935) Zur Kenntnis der Myxinoiden-Kiemen. Gegenbaurs Morphol Jahrb 75:613–633

    Google Scholar 

  • Raviola E, Gilula NB (1973) Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci USA 70:1677–1681

    Google Scholar 

  • Reale E, Luciano L, Spitznas M (1978) Communicating junctions of the human sensory retina. A freeze fracture study. Graefes Arch Klin Exp Ophthalmol 208:77–92

    Google Scholar 

  • Rick R, Dörge A, v Arnim E, Thurau K (1978) Electron microprobe analysis of frog skin epithelium: evidence for a syncytial sodium transport compartment. J Membr Biol 39:313–331

    Google Scholar 

  • Riddle CV, Ernst SA (1979) Structural simplicity of the zonula occludens in the electrolyte secreting epithelium of the avian salt gland. J Membr Biol 45:21–35

    Google Scholar 

  • Robertson JD (1954) The chemical composition of the blood of some aquatic chordates, including members of the Tunicata, Cyclostomata and Osteichthyes. J Exp Biol 31:424–442

    Google Scholar 

  • Robertson JD (1976) Chemical composition of the blood fluids and muscle of the hagfish Myxine glutinosa and the rabbit-fish Chimaera monstrosa. J Zool 178:261–277

    Google Scholar 

  • Rosen S (1972) Localization of carbonic anhydrase activity in turtle and toad urinary bladder mucosa. J Histochem Cytochem 20:696–702

    Google Scholar 

  • Sardet C, Pisam M, Maetz J (1979) The surface epithelium of teleostean fish gills. Cellular and junctional adaptations of the chloride cell in relation to salt adaptation. J Cell Biol 80:96–117

    Google Scholar 

  • Schneeberger EE (1980) Heterogeneity of tight junction morphology in extrapulmonary and intrapulmonary airways of the rat. Anat Rec 198:193–208

    Google Scholar 

  • Schneeberger EE, Walters DV, Olver RE (1978) Development of intercellular junctions in the pulmonary epithelium of the foetal lamb. J Cell Sci 32:307–324

    Google Scholar 

  • Simionescu M, Simionescu N, Palade GE (1975) Segmental differentiation of cell junctions in the vascular endothelium. The microvasculature. J Cell Biol 67:863–885

    Google Scholar 

  • Stanton BA (1984) Regulation of ion transport in epithelia: role of membrane recruitment from cytoplasmic vesicles. Lab Invest 51:255–257

    Google Scholar 

  • Stetson DL, Steinmetz PR (1985) α and β Types of carbonic anhydrase-rich cells in turtle bladder. Am J Physiol 249:F553-F565

    Google Scholar 

  • Sugi Y, Hirakow R (1986) Freeze fracture studies on the sinoatrial and atrioventricular nodes of the caprine heart, with special reference to the nexus. Cell Tissue Res 245:273–279

    Google Scholar 

  • Ussing H (1960) The alkali metal ions in isolated systems and tissues. In: Eichler O, Farah A (eds) Handbuch der experimentellen Pharmakologie, vol 13. Springer, Berlin Heidelberg New York, pp 1–195

    Google Scholar 

  • Van Deurs B, Luft JH (1979) Effects of glutaraldehyde fixation on the structure of tight junctions. A quantitative freeze-fracture analysis. J Ultrastruct Res 68:160–172

    Google Scholar 

  • Wade JB (1976) Membrane structural specialization of the toad urinary bladder revealed by the freeze-fracture technique. II. The mitochondria-rich cell. J Membr Biol 29:111–126

    Google Scholar 

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  1. Department of Cell Biology and Electron Microscopy, Hannover Medical School, Hannover, Germany

    Helmut Bartels

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  1. Helmut Bartels
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Dedicated to Prof. H. Leonhardt on the occasion of his 70th birthday

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Bartels, H. Intercellular junctions in the gill epithelium of the Atlantic hagfish, Myxine glutinosa . Cell Tissue Res. 254, 573–583 (1988). https://doi.org/10.1007/BF00226507

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