Skip to main content
Log in

Absence of binding and impermeability to ferritins of gill endothelium in marine teleosts

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The surface binding characteristics and permeability properties of the endothelium of secondary lamellae from the gills of several species of marine teleosts were investigated by introducing cationized ferritin and native ferritin into the microcirculation under normal environmental conditions. Neither type of ferritin bound to the luminal surface of the gill endothelium. No transcellular movement of cationized ferritin was detected, either via transendothelial channels or individual vesicles, nor was passage of cationized ferritin through the tight intercellular junctions of the endothelium observed. Anionic binding sites in the endothelial basement membranes could not be identified. Binding and transport of ferritin were unaffected by normal changes in environmental temperatures over the range of -2 to + 15°C. These findings suggest that the endothelial cell surface of the gills from these fishes is a primary barrier to the extracapillary movement of blood borne constituents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References cited

  • Areekul, S. 1969. Reflection coefficients of neutral and sulfate-substituted dextran molecules in the isolated perfused rabbit ear. Acta Soc. Med. Upsal. 74: 129–138.

    PubMed  CAS  Google Scholar 

  • Bankston, P.W. and Milici, A.J. 1983. A survey of the binding of polycationic ferritin in several fenestrated capillary beds: Indication of heterogeneity in the luminal glycocalyx of fenestral diaphragms. Microvasc. Res. 26: 36–48.

    Article  PubMed  CAS  Google Scholar 

  • Boyd, R.B., DeVries, A.L., Eastman, J.T. and Pietra, G.G. 1980a. The secondary lamellae of the gills of cold water (high latitude) teleosts. A comparative light and electron microscopic study. Cell Tiss. Res.. 213: 361–367.

    Article  CAS  Google Scholar 

  • Boyd, R.B., DeVries, A.L., Eastman, J.T. and Pietra, G.G. 1980b. Permeability to protein tracers of gill secondary lamelae from high latitude fishes. Anat. Rec. 196: 22A.

  • Boyd, R.B. and DeVries, A.L. 1983. The seasonal distribution of anionic binding sites in the basement membrane of the kidney glomerulus of the winter flounder Pseudopleuronectes americanus. Cell Tiss. Res.. 234: 271–277.

    Article  CAS  Google Scholar 

  • Boyd, R.B. and DeVries, A.L. 1986. A comparison of anionic sites in the glomerular basement membranes from different classes of fishes. Cell Tiss. Res.. 245: 513–517.

    Article  CAS  Google Scholar 

  • Brightman, M.W. and Reese, T.E. 1969. Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol.. 40: 648–677.

    Article  PubMed  CAS  Google Scholar 

  • Brody, J.S., Vaccaro, C.A., Hill, N.S. and Rounds, S. 1984. Binding of charged ferritin to alveolar wall components and charge selectivity of macromolecular transport in permeability pulmonary edema in rats. Circ. Res. 55: 155–167.

    PubMed  CAS  Google Scholar 

  • Bundgaard, M. and Cserr, H.F. 1981. Impermeability of hagfish cerebral capillaries to radiolabelled polyethylene glycols and to microperoxidase. Brain Res. 206: 71–81.

    Article  PubMed  CAS  Google Scholar 

  • Bundgaard, M., Cserr, H.F. and Murray, M. 1979. Impermeability of hagfish cerebral capillaries to horseradish peroxidase. An ultrastructural study. Cell Tiss. Res.. 198: 65–77.

    Article  CAS  Google Scholar 

  • Caulfield, J.P. and Farquhar, M.G. 1974. The permeability of glomerular capillaries to graded dextrans. Identification of the basement membrane as the primary filtration barrier. J. Cell Biol.. 63: 883–903.

    Article  PubMed  CAS  Google Scholar 

  • Chang, R.L.S., Deen, W.M., Robertson, C.R. and Brenner, B.M. 1975a. Permselectivity of the glomerular capillary wall: III Restricted transport of polyanions. Kid. Int. 8: 212–218.

    CAS  Google Scholar 

  • Chang, R.L.S., Ueki, I.F., Troy, J.L., Deen, W.M., Robertson, C.R. and Brenner, B.M. 1975b. Permselectivity of the glomerular capillary wall to macromolecules II. Experimental studies in rats using neutral dextran. Biophys. J. 15: 887–906.

    Article  PubMed  CAS  Google Scholar 

  • Charonis, A.S. and Wissig, S.L. 1983. Anionic sites in basement membranes. Differences in their electrostatic properties in continuous and fenestrated capillaries. Microvasc. Res. 25: 265–285.

    Article  PubMed  CAS  Google Scholar 

  • DeVries, A.L. 1971. Glycoproteins as biological antifreeze agents in Antarctic fishes. Science 172: 1152–1155.

    PubMed  CAS  Google Scholar 

  • Duman, J.D. and DeVries, A.L. 1974. Freezing resistance in winter flounder Pseudopleuronectes americanus. Nature, Lond. 247: 237–238.

    Article  CAS  Google Scholar 

  • Eastman, J.T., DeVries, A.L., Coalson, R.E., Nordquist, R.E. and Boyd, R.B. 1979. Renal conservation of antifreeze peptide in Antarctic eelpout, Rhigophila dearborni. Nature, Lond. 282: 217–218.

    Article  CAS  Google Scholar 

  • Elger, M., Kaune, R. and Hentschel, H. 1984. Glomerular intermittency in a freshwater teleost, Carassius auratus gibelio, after transfer to salt water. J. Comp. Physiol. 154B: 225–231.

    Google Scholar 

  • Gordon, J.R. and Bernfield, M.R. 1980. The basal lamina of the postnatal mammary epithelium contains glycosaminoglycans in a precise ultrastructural organization. Dev. Biol. 74: 118–135.

    Article  PubMed  CAS  Google Scholar 

  • Hickman, C.P. Jr. and Trump, B.F. 1969. The kidney. In Fish Physiology. Vol. 1. pp. 91–239. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.

    Google Scholar 

  • Hopwood, D., Milne, G., Khan, M.A., Crisp, M. and Walker, M. 1983. Anionic groups in basement membranes. Histochem. J. 15: 491–494.

    Article  PubMed  CAS  Google Scholar 

  • Johansson, B.R. 1983. Distribution of anionic binding sites in extravascular space of skeletal muscle demonstrated with polycationized ferritin. J. Ultrastruct. Res. 83: 176–183.

    Article  PubMed  CAS  Google Scholar 

  • Kanwar, Y.S. and Farquhar, M.G. 1979. Anionic sites in the glomerular basement membrane. J. Cell Biol.. 81: 137–153.

    Article  PubMed  CAS  Google Scholar 

  • Loudon, M.F., Michel, C.C. and White, I.F. 1979. The labelling of vesicles in frog endothelial cells with ferritin. J. Physiol. 296: 97–112.

    PubMed  CAS  Google Scholar 

  • Nagy, Z., Peters, H. and Huttner, I. 1983. Charge-related alterations of the cerebral endothelium. Lab. Invest. 49: 662–671.

    PubMed  CAS  Google Scholar 

  • O'Morchoe, C.C.C., Jones, W.R. III, Jarosz, H.M., O'Morchoe, P.J. and Fox, L.M. 1984. Temperature dependence of protein transport across lymphatic endothelium in vitro. J. Cell Biol.. 98: 629–640.

    Article  PubMed  Google Scholar 

  • Pietra, G.G., Sampson, P., Lanken, P.N., Hansen-Flaschen, J. and Fishman, A.P. 1983. Transcapillary movement of cationized ferritin in the isolated perfused rat lung. Lab. Invest. 49: 54–61.

    PubMed  CAS  Google Scholar 

  • Randall, D.J. 1970. Gas exchange in fish. In Fish Physiology. Vol. IV. pp. 253–292. Edited by W.S. Hoar and D.J. Randall. Academic Press. New York.

    Google Scholar 

  • Reese, T.S. and Karnovsky, M.J. 1967. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol.. 34: 207–217.

    Article  PubMed  CAS  Google Scholar 

  • Rennke, H.G. and Venkatachalam, M.A. 1977. Glomerular permeability: In vivo tracer studies with polyanionic and polycationic ferritins. Kid. Int. 11: 44–53.

    CAS  Google Scholar 

  • Schneeberger, E.E. 1988. Interaction of plasma proteins with negatively charged sites on the pulmonary capillary endothelium of the rat. Cell Tiss. Res.. 251: 417–423.

    Article  CAS  Google Scholar 

  • Simionescu, D. and Simionescu, M. 1983. Differentiated distribution of the cell surface charge on the alveolar-capillary unit. Characteristic paucity of anionic sites on the air-blood barrier. Microvasc. Res. 25: 85–100.

    Article  PubMed  CAS  Google Scholar 

  • Simionescu, M. and Simionescu, N. 1978. Constitutive endocytosis of the endothelial cell. J. Cell Biol.. 79: 381a.

  • Simionescu, M., Simionescu, N. and Palade, G.E. 1982. Preferential distribution of anionic sites on the basement membrane and the abluminal aspect of the endothelium in fenestrated capillaries. J. Cell Biol.. 95: 425–434.

    Article  PubMed  CAS  Google Scholar 

  • Simionescu, M., Simionescu, N. and Palade, G.E. 1984. Partial chemical characterization of the anionic sites in the basal lamina of fenestrated capillaries. Microvasc. Res. 28: 352–367.

    Article  PubMed  CAS  Google Scholar 

  • Simionescu, N., Simionescu, M. and Palace, G.E. 1981. Differentiated microdomains on the luminal surface of the capillary endothelium. I. Preferential distribution of anionic sites. J. Cell Biol.. 90: 605–613.

    Article  PubMed  CAS  Google Scholar 

  • Slaughter, D., Fletcher, G.L., Ananthanarayanan, V.S. and Hew, C.L. 1981. Antifreeze proteins from the sea raven, Hemitripterus americanus. J. Biol. Chem. 256: 2022–2026.

    PubMed  CAS  Google Scholar 

  • Stefanini, M., DeMartino, C. and Zamboni, L. 1967. Fixation of ejaculated spermatazoa for electron microscopy. Nature, Lond. 216: 173–174.

    Article  CAS  Google Scholar 

  • Takusagawa, K., Ariji, F., Shida, K., Sato, T., Asoo, N. and Konno, K. 1982. Electron microscopic observations on pulmonary connective tissue stained by Ruthenium Red. Histochem. J. 14: 257–271.

    Article  PubMed  CAS  Google Scholar 

  • Tsujii, T. 1988. The role of renal macrophages in the aglomerular kidney of the sea-horse (teleost) in the removal of exogenous macromolecules from the circulating blood. Arch. Histol. Cytol. 51: 327–339.

    PubMed  CAS  Google Scholar 

  • Tsujii, T., Naito, I., Ukita, S., Ono, T. and Seno, S. 1984a. The anionic barrier system in the mesonephric renal glomerulus of the arctic lamprey, Entosphenus japonicus (Martens) (Cyclostomata). Cell Tiss. Res.. 235: 491–496.

    Article  CAS  Google Scholar 

  • Tsujii, T., Naito, I., Ukita, S., Ono, T. and Seno, S. 1984b. The Anionic barrier system on the mesonephric renal glomerulus of the brown hagfish, Paramyxine atami Dean (Cyclostomi). Anat. Rec. 208: 337–347.

    Article  PubMed  CAS  Google Scholar 

  • Vaccaro, C.A. and Brody, J.S. 1979. Ultrastructural localization and characterization of proteoglycans in the pulmonary alveolus. Am. Rev. Resp. Dis. 120: 901–910.

    PubMed  CAS  Google Scholar 

  • Vorbrodt, A.W., Dobrogowska, D.H., Lossinsky, A.S. and Wisniewski, H.M. 1986. Ultrastructural localization of lectin receptors on the luminal and abluminal aspects of brain micro-blood vessels. J. Histochem. Cytochem. 34: 251–261.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boyd, R.B., Atkin, J., Thompson, V.W. et al. Absence of binding and impermeability to ferritins of gill endothelium in marine teleosts. Fish Physiol Biochem 8, 53–60 (1990). https://doi.org/10.1007/BF00004431

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00004431

Keywords

Navigation