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Membrane Recycling, Adsorptive and Receptor-Mediated Endocytosis by Primary Bovine Cerebral Microvessel Endothelial Cell Monolayers in Vitro

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Pharmaceutical Applications of Cell and Tissue Culture to Drug Transport

Part of the book series: NATO ASI Series ((NSSA,volume 218))

Abstract

Within recent years, we have realized that the blood-brain barrier (BBB) is an interactive, highly selective interface between the brain interstitial space and blood-borne molecules. It is the unique functional and morphological characteristics of the endothelial cells which comprise the majority of the BBB surface area that define this specialized structure. However, increasing evidence shows that communication between the endothelia and surrounding cell types is responsible for expression of the BBB phenotype1.

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References

  1. R.C. Janzer and M.C. Raff, Astrocytes induce blood-brain barrier properties in endothelial cells, Nature (Lond.) 325: 253–257 (1987).

    Article  CAS  Google Scholar 

  2. W.M. Pardridge, Recent advances in blood-brain barrier transport, Ann. Rev. Pharmacol. Toxicol. 28: 25–39 (1988).

    Article  CAS  Google Scholar 

  3. H.J.L. Frank and W.M. Pardridge, A direct in vitro demonstration of insulin binding to isolated brain microvessels, Diabetes 30: 757–761 (1980).

    Article  Google Scholar 

  4. A.L. McCall, J. Valente, R. Cordero, N.B. Ruderman, and K. Tornheim, Metabolic characterization of isolated cerebral microvessels: ATP and ADP concentrations, Microvasc. Res. 35: 325–333 (1988).

    Article  PubMed  CAS  Google Scholar 

  5. I. Sussman, M.P. Carson, A.L. McCall., V. Schultz, N.B. Ruderman, and K. Tornheim, Energy state of bovine cerebral microvessels: comparison of isolation methods, Microvasc. Res. 35: 167–178 (1988).

    Article  PubMed  CAS  Google Scholar 

  6. W.M. Pardridge, Receptor-mediated peptide transport through the blood-brain barrier, Endocrine Rev. 7: 314–330 (1986).

    Article  CAS  Google Scholar 

  7. J.B. Fishman, J.B, Rubin, J.V. Handrahan, J.R. Connor, and R.E. Fine, Receptor-mediated transcytosis of transferrin across the blood-brain barrier, J. Neurosci. Res. 18: 299–304 (1987).

    Article  PubMed  CAS  Google Scholar 

  8. D. Triguero, J.B. Buciak, J. Yang, and W.M. Pardridge, Blood-brain barrier transport of cationized immunoglobulin G: enhanced delivery compared to native protein, Proc. Natl. Acad. Sci. (USA) 86: 4761–4765 (1989).

    Article  CAS  Google Scholar 

  9. P.D. Bowman, S.R. Ennis, K.E. Rarey, A.L. Betz, and G.W. Goldstein, Brain microvessel endothelial cells in tissue culture: a model for study of blood-brain barrier permeability, Ann. Neurol. 14: 396–402 (1983).

    Article  PubMed  CAS  Google Scholar 

  10. K.L. Audus and R.T. Borchardt, Bovine brain microvessel endothelial cell monolayers as a model system for the blood-brain barrier, Ann. N.Y. Acad. Sci. 507: 9–18 (1987).

    Article  PubMed  CAS  Google Scholar 

  11. D.N. McKinley and H.S. Wiley, Reassessment of fluid-phase endocytosis and diacytosis in monolayer cultures of human fibroblasts, J. Cell. Physiol. 136: 389–397 (1988).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  13. J.A. Swanson, B.D. Yirinec, and S.C. Silverstein, Phorbol esters and horseradish peroxidase stimulate pinocytosis and redirect the flow of pinocytosed fluid in macrophages, J. Cell Biol. 100: 851–859 (1985).

    Article  PubMed  CAS  Google Scholar 

  14. F.L. Guillot, K.L. Audus and T.J. Raub, Fluid-phase endocytosis by primary cultures of bovine brain microvessel endothelial cell mono-layers, Microvasc. Res., in press (1989).

    Google Scholar 

  15. P.F. Davies, S.C. Seiden, and S.M. Schwartz, Enhanced rates of fluid pinocytosis during exponential growth and monolayer regeneration by cultured arterial endothelial cells. J. Cell. Physiol. 102: 119–127 (1980).

    Article  PubMed  CAS  Google Scholar 

  16. J.M. Besterman, J.A. Aihart, R.C. Woodworth, and R.B. Low, Exocy-cytosis of pinocytosed fluid in cultured cells: kinetic evidence for rapid turnover and compartmentation, J. Cell Biol. 91: 716–727 (1981).

    Article  PubMed  CAS  Google Scholar 

  17. S.K. Williams and R.C. Wagner, Regulation of micropinocytosis in capillary endothelium by multivalent cations, Microvasc. Res. 21: 175–182 (1981).

    Article  PubMed  CAS  Google Scholar 

  18. C.R. Newton and T.J. Raub, Characterization of the transferrin receptor in primary cultures of bovine brain capillary endothelial cells, J. Cell Biol. 107: 770a.

    Google Scholar 

  19. R.D. Broadwell, B.J. Balin, M. Salcman, and R.S. Kaplan, Brain-blood barrier? Yes and no, Proc. Natl. Acad. Sci. USA 80: 7352–7356 (1983).

    Article  PubMed  CAS  Google Scholar 

  20. R.M. Steinman, I.S. Mellman, W.A. Muller, and Z.A. Cohn, Endocytosis and the recycling of plasma membrane, J. Cell Biol. 96: 1–27 (1983).

    Article  PubMed  CAS  Google Scholar 

  21. I. Mellman, Molecular sorting during endocytosis, Kidney Intl. 32: S–184–S–195 (1987).

    Google Scholar 

  22. T.J. Raub and K.L. Audus, Adsorptive endocytosis by cultured bovine brain endothelial cells, J. Cell Biol. 105: 312a.

    Google Scholar 

  23. T.J. Raub and K.L. Audus, Adsorptive endocytosis and recycling of ricin agglutinin by cultured monolayers of primary bovine brain microvessel endothelial cells, submitted to J. Cell Sci.

    Google Scholar 

  24. D.Z. Gerhart, M.S. Zionis, and L.R. Drewes, Light and electron microscopic localization of D-galactosyl residues in capillary endothelial cells of the canine cerebral cortex, J. Histochem. Cytochem. 34: 641–648 (1986).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  26. P.L. Debbage, H.-J. Gabius, K. Bise, and F. Marguth, Cellular glyco-conjugates and their potential endogenous receptors in the cerebral microvasculature of man: a glycohistochemical study, Eur.J. Cell Biol. 46: 425–434 (1988).

    PubMed  CAS  Google Scholar 

  27. R.D. Broadwell, B.J. Balin, and M. Salcman, Transcytotic pathway for blood-borne protein through the blood-brain barrier, Proc. Natl. Acad. Sci. USA 85: 632–636 (1988).

    Article  PubMed  CAS  Google Scholar 

  28. G. Griffiths and K. Simons, The trans Golgi network: sorting at the exit site of the Golgi complex, Science 234: 438–443 (1986).

    Article  PubMed  CAS  Google Scholar 

  29. W. Stoorvogel, H.J. Geuze, J.M. Griffith, and G.J. Strous, The pathways of endocytosed transferrin and secretory protein are connected in the trans-Golgi reticulum, J. Cell Biol. 106: 1821–1829 (1988).

    Article  PubMed  CAS  Google Scholar 

  30. T.J. Raub, J.B. Denny, and R.M. Roberts, Cell surface glycoproteins of CHO cells. I. Internalization and rapid recycling, Exp. Cell Res. 165: 73–91 (1986).

    Article  PubMed  CAS  Google Scholar 

  31. A.K. Kumagai, J.B. Eisenberg, and W.M. Pardridge, Absorptive-mediated endocytosis of cationized albumin and a β-endorphin-cationized albumin chimeric peptide by isolated brain capillaries, J. Biol. Chem. 262: 15214–15219 (1987).

    PubMed  CAS  Google Scholar 

  32. K.R. Smith and R.T. Borchardt, Permeability and mechanism of albumin, cationized albumin, and glycosylated albumin transcellular transport across monolayers of cultured bovine brain capillary endothelial cells, Pharm. Res. 6: 466–473 (1989).

    Article  PubMed  CAS  Google Scholar 

  33. M.W. Brightman, 1989, The anatomic basis of the blood-brain barrier, in: “Implications of the Blood-Brain Barrier and its Manipulation, Vol. 1,” E.A. Neuwelt, ed., Plenum Medical Book Co., New York, pp. 53–83.

    Google Scholar 

  34. P. Wang-Iverson, P.M. DeRosa, and W.V. Brown, 1988, Plasma lipo-protein interaction with endothelial cells, in: “Endothelial Cells, Vol. 1,” U.S. Ryan, ed., CRC Press, Boca Raton, Florida, pp. 179–187.

    Google Scholar 

  35. S. Meresse, C. Delbart, J.-C. Fruchart, and R. Cecchelli, Low-density lipoprotein receptors on endothelium of brain capillaries, J. Neurochem. 53: 340–345 (1989).

    Article  PubMed  CAS  Google Scholar 

  36. R.E. Pitas, J. Boyles, R.W. Mahley, and D.M. Bissell, Uptake of chemically modified low density lipoproteins in vivo is mediated by specific endothelial cells, J. Cell Biol. 100: 103–117 (1985).

    Article  PubMed  CAS  Google Scholar 

  37. J. Gaffney, D. West, F. Arnold, A. Sattar, and S. Kumar, Differences in the uptake of modified low density lipoproteins by tissue cultured endothelial cells, J. Cell Sci. 79: 317–325 (1985).

    PubMed  CAS  Google Scholar 

  38. M.P. Carson and C.C. Haudenschild, Microvascular endothelium and pericytes: high yield, low passage cultures, In Vitro Cell. Develop. Biol. 22: 344–354 (1986).

    Article  CAS  Google Scholar 

  39. H.V. Vinters, S. Reave, P. Costello, J.P. Girvin, and S.A. Moore, Isolation and culture of cells derived from human cerebral micro-vessels, Cell Tiss. Res. 249: 657–667 (1987).

    Article  CAS  Google Scholar 

  40. M. Simionescu, N. Ghinea, A. Fixman, M. Lasser, L. Kukes, N. Simionescu, and G.E. Palade, The cerebral microvasculature of the rat: structure and luminal surface properties during early development, J. Submicrosc. Cytol. Pathol. 20: 243–261 (1988).

    PubMed  CAS  Google Scholar 

  41. J.E. Schnitzer, W.W. Carley, and G.E. Palade, Albumin interacts specifically with a 60-kDa microvascular endothelium glycoprotein, Proc. Natl. Acad. Sci. USA 85: 6773–6777 (1988).

    Article  PubMed  CAS  Google Scholar 

  42. N. Ghinea, M. Eskenasy, M. Simionescu, and N. Simionescu, Endothelial albumin binding proteins are membrane-associated components exposed on the cell surface, J. Biol. Chem. 264: 4755–4758 (1989).

    PubMed  CAS  Google Scholar 

  43. L. Ghitescu, A. Fixman, M. Simionescu, and N. Simionescu, Specific binding sites for albumin restricted to plasmalemmal vesicles of continuous capillary endothelium: receptor-mediated transcytosis, J. Cell Biol. 102: 1304–1311 (1986).

    Article  PubMed  CAS  Google Scholar 

  44. W.A. Jeffries, M.R. Brandon, S.V. Hunt, A.F. Williams, K.C. Gatter, and D.Y. Mason, Transferrin receptor on endothelium of brain capillaries, Nature (Lond.) 312: 162–163 (1984).

    Article  Google Scholar 

  45. J.M. Hill, M.R. Ruff, R.J. Weber, and C.B. Pert, Transferrin receptors in rat brain: neuropeptide-like pattern and relationship to iron distribution, Proc. Natl. Acad. Sci. USA 82: 4553–4557 (1985).

    Article  PubMed  CAS  Google Scholar 

  46. R. Soda and M. Tavassoli, Transendothelial transport (transcytosis) of iron-transferrin complex in the bone marrow, J. Ultrastruc. Res. 88: 18–29 (1984).

    Article  CAS  Google Scholar 

  47. W.M. Pardridge, J. Eisenberg, and J. Yang, Human blood-brain barrier transferrin receptor, Metab. 36: 892–895 (1987).

    Article  CAS  Google Scholar 

  48. B. Bloch, T. Popovici, S. Chouham, M.J. Levin, D. Tuil, and A. Kahn, Transferrin gene expression in choroid plexus of the adult rat brain, Brain Res. Bull. 18: 573–576 (1987).

    Article  PubMed  CAS  Google Scholar 

  49. J.E. Lamb, F. Ray, J.H. Ward, J.P. Kushner, and J. Kaplan, Internali-zation and subcellular localization of transferrin and transferrin receptors in HeLa cells, J. Biol. Chem. 258: 8751–8758 (1983).

    PubMed  CAS  Google Scholar 

  50. J.A. Hanover and R.B. Dickson, 1985, Transferrin: receptor-mediated endocytosis and iron delivery, in: “Endocytosis,” I. Pastan and M.C. Willingham, eds., Plenum Press, New York, pp. 131–161.

    Chapter  Google Scholar 

  51. S.S. Buys, L.H. Gren, and J. Kaplan, Phorbol esters and calcium ionophores inhibit internalization and accelerate recycling of receptors in macrophages, J. Biol. Chem. 262: 12970–12976 (1987).

    PubMed  CAS  Google Scholar 

  52. T.E. McGraw, K.W. Dunn, and F.R. Maxfield, Phorbol ester treatment increases the exocytic rate of the transferrin receptor recycling pathway independent of serine-24 phosphorylation, J. Cell Biol. 106: 1061–1066 (1988).

    Article  PubMed  CAS  Google Scholar 

  53. R.C. Wagner, C.S. Robinson, P.J. Cross, and J.J. Devenny, Endocytosis and exocytosis of transferrin by isolated capillary endothelium, Microvasc. Res. 25: 387–396 (1983).

    Article  PubMed  CAS  Google Scholar 

  54. M. Marsh and A. Helenius, Adsorptive endocytosis of Semliki Forest virus, J. Molec. Biol. 142: 439–454 (1980).

    Article  PubMed  CAS  Google Scholar 

  55. W.M. Pardridge, J. Eisenberg, and J. Yang, Human blood-brain barrier insulin receptor, J. Neurochem. 44: 1771–1778 (1985).

    Article  PubMed  CAS  Google Scholar 

  56. B.T. Keller, K.R. Smith, and R.T. Borchardt, Transport barriers to absorption of peptides, Pharm. Weekblad Sci. 10: 38–39 (1988).

    Google Scholar 

  57. R.G. Rosenfeld, H. Pham, B.T. Keller, R.T. Borchardt, and W.M. Pardridge, Demonstration and structural comparison of receptors for insulin-like growth factor-I and-II (IGF-I and-II) in brain and blood-brain barrier, Biochim. Biophys. Res. Commun. 149: 159–166 (1987).

    Article  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Drug Delivery Systems Research, The Upjohn Company, Kalamazoo, Michigan, USA

    Thomas J. Raub

  2. Department of Biology, Kalamazoo College, Kalamazoo, Michigan, USA

    Carolyn R. Newton

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  1. Thomas J. Raub
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Editors and Affiliations

  1. SmithKline Beecham Pharmaceuticals, King of Prussia, Pennsylvania, USA

    Glynn Wilson

  2. University of Nottingham, Nottingham, UK

    S. S. Davis  & L. Illum  & 

  3. INSERM, Paris, France

    Alain Zweibaum

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© 1991 Plenum Press, New York

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Raub, T.J., Newton, C.R. (1991). Membrane Recycling, Adsorptive and Receptor-Mediated Endocytosis by Primary Bovine Cerebral Microvessel Endothelial Cell Monolayers in Vitro . In: Wilson, G., Davis, S.S., Illum, L., Zweibaum, A. (eds) Pharmaceutical Applications of Cell and Tissue Culture to Drug Transport. NATO ASI Series, vol 218. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-0286-6_16

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  • DOI: https://doi.org/10.1007/978-1-4757-0286-6_16

  • Publisher Name: Springer, Boston, MA

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  • Online ISBN: 978-1-4757-0286-6

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