Transport of the δ-opioid receptor agonist [D-penicillamine2,5] enkephalin across the blood-brain barrier involves transcytosis

Journal of Pharmaceutical Sciences

Volumn 88, Issue 4, 1999, Pages 392-397

  Egleton, Richard D ^a   Davis, Thomas P ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENOSOBENZENE; DELTA OPIATE RECEPTOR AGONIST; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; METENKEPHALIN DERIVATIVE; SUCROSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN PERFUSION; CATTLE; CONTROLLED STUDY; DRUG PENETRATION; DRUG TRANSPORT; ENDOTHELIUM CELL; MEMBRANE PERMEABILITY; MONOLAYER CULTURE; NONHUMAN; RAT; TRANSCYTOSIS; VASCULAR ENDOTHELIUM;

EID: 0032927601     PISSN: 00223549     EISSN: None     Source Type: Journal    
DOI: 10.1021/js980410+     Document Type: Article

References (35)

1. This work was supported by NIDA grants no. DA-06284 and RO1-DA-11271.
2. Egleton, R. D.; Davis, T. P. Bioavailability and transport of peptides and peptide drugs into the brain. Peptides 1997, 18, 1431-1439.
3. Abbruscato, T. J.; Thomas, S. A.; Hruby, V. J.; Davis, T. P. Brain and spinal cord distribution of biphalin: Correlation with opioid receptor density and mechanism of CNS entry. J. Neurochem. 1997, 69, 1236-1245.
4. Abbruscato, T. J.; Thomas, S. A.; Hruby, V. J.; Davis, T. P. Blood-brain barrier permeability and bioavailability of a highly potent and μ-selective opioid receptor antagonist, CTAP: Comparison with morphine. J. Pharm. Exp. Ther. 1997, 280, 402-409.
5. Mosberg, H. I.; Hurst, R.; Hruby, V. J., Gee, K.; Yamamura, H. I.; Galligan, J. J.; Burks, T. F. Bis-penicillamine enkephalins possess highly improved specificity toward delta opioid receptors. Proc. Natl. Acad. Sci., U.S.A. 1983, 80, 5871-5874.
6. Weber, S. J.; Greene, D. L.; Sharma, S. D.; Yamamura, H. I.; Kramer, T. H.; Burks, T. F.; Hruby, V. J.; Hersh, L. B.; Davis, T. P. Distribution and analgesia of [3H][D-Pen2, D-Pen5] enkephalin and two halogenated analogues after intravenous administration. J. Pharm. Exp. Ther. 1991, 259, 1109-1117.
7. Weber, S. J.; Greene, D. L.; Hruby, V. J.; Yamamura, H. I.; Porreca, F.; Davis, T. P. Whole body and brain distribution of [3H]cyclic[D-Pen2, D-Pen5] enkephalin after inraperitoneal, intravenous, oral and subcutaneous administration. J. Pharm. Exp. Ther. 1992, 263, 1308-1316.
8. Dupont, A.; Cusan, L.; Garon, M.; Alvarado-Urbina, G.; Labrie, F. Extremely rapid degradation of [3H] methionine-enkephalin by various rat tissues in vivo and in vitro. Life Sci. 1977, 21, 907-914.
9. Weber, S. J.; Abbruscato, T. J.; Brownson, E. A.; Lipkowski, A. W.; Polt, P.; Misicka, A.; Haaseth, R. C.; Bartosz, H.; Hruby, V. J.; Davis, T. P. Assessment of an in vitro blood-brain barrier model using several [Met5]enkephalin opioid analogues. J. Pharm. Exp. Ther. 1993, 266, 1649-1655.
10. Williams, S. A.; Abbruscato, T. J.; Hruby, V. J.; Davis, T. P. Permeability of a δ-opioid receptor selective enkephalin [D-penicillamine2,5]enkephalin, across the blood-brain and blood-cerebrospinal fluid barriers. J. Neurochem. 1996, 66, 1289-1299.
11. Thomas, S. A.; Abbruscato, T. J.; Hruby, V. J.; Davis, T. P. The entry of [D-penicillamine2,5]enkephalin into the central nervous system: saturation kinetics and specificity. J. Pharm. Exp. Ther. 1997, 280, 1235-1240.
12. Tamai, I.; Sai, Y.; Kobayashi, H.; Kamata, M.; Wakamiya, T.; Tsuji, A. Structure-internalization relationship for adsorptive-mediated endocytosis of basic peptides at the blood-brain barrier. J. Pharmacol. Exp. Ther. 1997, 280, 410-415.
13. Rose, J. M.; Audus, K. L. Receptor-mediated angiotensin II transcytosis by brain microvessel endothelial cells. Peptides 1998, 19, 1023-1030.
14. Audus, K. L.; Borchardt, R. T. Characterization of an in vitro blood-brain barrier model system for studying drug transport and metabolism. Pharm. Res. 1986, 3, 81-87.
15. Audus, K. L.; Borchardt R. T. Bovine brain microvessel endothelial cell monolayers as a model system for the blood-brain barrier. Ann. N. Y. Acad. Sci. 1987, 507, 9-18.
16. Wiley: H. S.; Cunningham, D. D. A cellular parameter for quantitating receptor mediated endocytosis. J. Biol. Chem. 1982, 257, 4222-4229.
17. Preston, J. E.; Al-Sarraf, H.; Segal, M. B. Permeability of the developing blood-brain barrier to 14C-mannitol using the rat in situ brain perfusion technique. Dev. Brain Res. 1995, 87, 69-76.
18. Zlokovic, B. V.; Begley, D. J.; Djuricic, B. M.; Mitrovic, D. M. Measurement of solute transport across the blood-brain barrier in the perfused guinea-pig brain: Method and application to N-methylaminoisobutyric acid. J. Neurochem. 1986, 46, 1444-1451.
19. Tallarida, R. J.; Murray, B. M. Analysis of Variance. Manual of Pharmacologic Calculations with Computer Programs, 2nd ed.; Springer-Verlag: New York, 1987; pp 110-124.
20. Bailey, N. T. J. Regression Analysis. Statistical Methods in Biology; English University Press: London, 1959; pp 91-99.
21. Roosterman, D.; Roth, A.; Kreienkamp, H. J.; Richter, D.; Meyerhof, W. Distinct agonist-mediated endocytosis of cloned rat somatostatin receptor expresssed in insulinoma cells. J. Neuroendocrinol. 1997, 9, 741-751.
22. Liebl, B.; Muckter, H.; Doklea, E.; Reichl, F. X.; Fichtl, B.; Forth, W. Influence of glucose on the toxicity of oxophenylarsine in MDCK cells. Arch. Toxicol. 1995, 69, 421-424.
23. Pardridge, W. M.; Triguero, D.; Yang, J. P. A. Comparisons of in vitro and in vivo models of transcytosis through the blood-brain barrier. J. Pharm. Exp. Ther. 1990, 253, 884-891.
24. Miller, D. W.; Keller, B. T.; Borchardt, R. T. Identification and distribution of insulin receptors on cultured bovine brain microvessel endothelial cells: Possible function in insulin processing in the blood-brain barrier. J. Cell Physiol. 1994, 161, 333-341.
25. Frost, S. C.; Lane, M. D.; Gibbs, E. M. Effect of phenylarsine oxide on fluid phase endocytosis: Further evidence for activation of the glucose transporter. J. Cell. Physiol. 1989, 141, 464-474.
26. Lazari, M. F.; Porto, C. S.; Freymuller, E.; Abreu, L. C.; Picarelli, Z. P. Receptor-mediated endocytosis of angiotensin II in rat myometrial cells. Biochem. Pharmacol. 1997, 54, 399-408.
27. Dehouck, M. P.; Jolliet-Riant, P.; Bree, F.; Fruchart, J. C.; Cecchelli, R.; Tillement, J. P. Drug transfer across the blood-brain barrier: Correlation between in vitro and in vivo models. J. Neurochem. 1992, 58, 1790-1797.
28. Raub, T. J.; Kneutzel, S. I.; Sawada, G. A. Barrier tightening by a factor released from astroglioma cells. Exp. Cell. Res. 1992, 199, 330-340.
29. Abbruscato, T. J.; Davis, T. P. Combination of hypoxia/ aglycemia compromises blood-brain barrier integrity. J. Pharm. Exp. Ther., in press.
30. Egleton, R. D.; Abbruscato, T. J.; Thomas, S. A.; Davis, T. P. Transport of opioid peptides into the central nervous system. J. Pharm. Sci. 1998, 87, 1433-1439.
31. Zlokovic, B. V.; Banks, W. A.; Kadi, H. E.; Erchegyi, J.; Mackic, J. B.; McComb, J. G.; Kastin, A. J. Transport, uptake and metabolism of blood-bourne vasopressin by the blood-brain barrier. Brain Res. 1992, 590, 213-218.
32. Bradley, J. R.; Johnson, D. R.; Pober, J. S. Four different classes of inhibitors of receptor mediated endocytosis decrease tumour necrosis factor-induced gene expression in human endothelial cells. J. Immunol. 1993, 150, 5544-5555.
33. Koenig, J. A.; Edwardson, J. M. Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol. Sci. 1997, 18, 276-287.
34. Jefferies, W. A.; Brandon, M. R.; Hunt, S. V.; Williams, A. F.; Gatter, K. C.; Mason, D. Y. Transferrin receptor on the endothelium of brain capillaries. Nature 1984, 312, 162-163.
35. Zlokovic, B. V.; Hyman, S.; McComb, J. G.; Lipovac, M. N.; Tang, G.; Davson, H. Kinetics of arginine-vasopressin uptake at the blood-brain barrier. Biochim. Biophys. Acta 1990, 1025, 191-198.