Passage of a δ-opioid receptor selective enkephalin, [D-penicillamine2,5] enkephalin, across the blood-brain and the blood-cerebrospinal fluid barriers

Journal of Neurochemistry

Volumn 66, Issue 3, 1996, Pages 1289-1299

  Williams, Sarah A ^a   Abbruscato, Thomas J ^a   Hruby, Victor J ^b   Davis, Thomas P ^a  

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

^b University of Arizona   (United States)

Author keywords

Blood brain barrier; Blood CSF barrier; Brain perfusion; Enkephalin; Peptide; D Penicillamine2,5 enkephalin

Indexed keywords

ENKEPHALIN; PENICILLAMINE; SIGMA OPIATE RECEPTOR;

ANALGESIA; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CEREBROSPINAL FLUID; DRUG TRANSPORT; DRUG UPTAKE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ENKEPHALIN, D-PENICILLAMINE (2,5)-; ENKEPHALIN, LEUCINE; ENKEPHALINS; MODELS, BIOLOGICAL; PERFUSION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, DELTA; SUCROSE;

ANIMALIA;

EID: 0029670938     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.66031289.x     Document Type: Article

References (76)

1. Audus K. L., Chikhale P. J., Miller D. W., Thompson S. E., and Borchardt R. T. (1992) Brain uptake of drugs: the influence of chemical and biological factors. Adv. Drug Res. 23, 1-64.
2. Banks W. A. and Kastin A. J. (1985) Peptides and the blood-brain barrier: lipophilicity as a predictor of permeability. Brain Res. Bull. 15, 287-292.
3. Banks W. A. and Kastin A. J. (1987) Saturable transport of peptides across the blood-brain barrier. Life Sci. 41, 1319-1338.
4. Banks W. A. and Kastin A. J (1990) Peptide transport systems for opiates across the blood-brain barrier. Am. J. Physiol. 259, E1-E10.
5. Banks W. A., Schally A. V., Barrera C. M., Fasold M. B., Durham D. A., Csernus V. J., Groot K., and Kastin A. J. (1990) Permeability of the murine blood-brain barrier to some octapeptide analogs of somatostatin. Proc. Natl. Acad. Sci. USA 87, 6762-6766.
6. Banks W. A., Kastin A. J., and Davis T. P. (1992) Permeability of the blood-brain barrier to peptides: an approach to the development of therapeutically useful analogs. Peptides 13, 1289-1294.
7. Barré J., Chamouard J. M , Houin G., and Tillement J. P. (1985) Equilibrium dialysis, ultrafiltration and ultracentrifugation compared for determining the plasma-protein-binding characteristics of valproic acid. Clin. Chem. 31, 60-64.
8. 1]-peptide T-amide is transported from brain to blood by a saturable mechanism. Brain Res. Bull. 19, 629-633.
9. Barrera C. M., Kastin A. J , Fasold M. B., and Banks W. A. (1991) Bi-directional saturable transport of LHRH across the blood-brain barrier. Am. J. Physiol. 261, E312-E318.
10. Begley D. J., Squires L. K., Zlokovic B. V., Mitrovic D. M., Hughes C. C. W., Revest P. A., and Greenwood J. (1990) Permeability of the blood-brain barrier to the immunosuppressive cyclic peptide cyclosporin A. J. Neurochem. 55, 1222-1230.
11. Blasberg R., Patlak C. S., and Fenstermacher J. D. (1975) Intrathecal chemotherapy: brain tissue profiles after ventriculo-cisternal perfusion. J. Pharmacol. Exp. Ther. 195, 78-83.
12. Blasberg R. G., Fenstermacher J. D., and Patlak C. S. (1983) Transport of α-aminoisobutyric acid across brain capillary and cellular membranes. J. Cereb. Blood Flow Metab. 3, 8-32.
13. Bouldin T. W. and Krigman M. R. (1975) Differential permeability of cerebral capillary and choroid plexus to lanthanum ion. Brain Res. 99, 444-448.
14. Bowman P. D , Ennis S. R., Rarey K. E., Betz A. L., and Goldstein G. W. (1983) Brain microvessel endothelial cells in tissue culture: a model for study of blood-brain barrier permeability. Ann. Neurol 14, 396-402.
15. Bradbury M W. B. (1979) The Concept of a Blood-Brain Barrier. Wiley, Chichester.
16. Broadwell R. D. (1989) Transcytosis of macromolecules through the blood-brain barrier: a cell biological perspective and critical appraisal. Acta Neuropathol. (Berl.) 79, 117-128.
17. Brownlees J. and Williams C. H. (1993) Peptidases, peptides, and the mammalian blood-brain barrier. J. Neurochem. 60, 793-803.
18. Brownson E. A., Abbruscato T. J., Gillespie T. J., Hruby V. J., and Davis T. P. (1994) Effect of peptidases at the blood-brain barrier on the permeability of enkephalin. J. Pharmacol. Exp. Ther. 270, 675-680.
19. Collins J. M. and Dedrick R. L. (1983) Distributed model for drug delivery to CSF and brain tissue. Am. J. Physiol. 245, R303-R310.
20. Collins J. M., Klecker R. W., Kelley J. A., Roth J S., McCully C. L., Balis F. M., and Poplack D. G. (1988) Pyrimidine dideoxynucleosides: selectivity of penetration into cerebrospinal fluid. J. Pharmacol. Exp. Ther. 245, 466-470.
21. Cserr H. F., Cooper D. N., Suri P K., and Patlak C. S. (1981) Efflux of radiolabeled polyethylene glycols and albumin from rat brain. Am. J. Physiol. 240, F319-F328.
22. Davis T. P. (1990) Methods of measuring neuropeptides and their metabolism, in The Roles of Neuropeptides in Stress Pathogenesis and Systemic Disease (Kaufman P G., McCubbin J. A., and Nemeroff C. B., eds), pp. 149-177. Academic Press, Orlando, Florida.
23. Davson H., Kleeman C. R., and Levin E (1961) Blood-brain barrier and extracellular space. J. Physiol (Lond.) 159, 67P-68P.
24. Emmerson P. J., Liu M.-R., Woods J. H., and Medzihradsky F. (1994) Binding affinity and selectivity of opioids at mu, delta and kappa receptors in monkey brain membranes J. Pharmacol. Exp. Ther. 271, 1630-1637
25. Erchegyi J., Kastin A. J., Zadina J. E., and Qiu X.-D. (1991) Isolation of a heptapeptide Val-Val-Tyr-Pro-Trp-Thr-Gln (valorphin) and some opiate activity. Int. J. Pept. Protein Res. 39, 477-488.
26. Ermisch A., Brust P., Kretzschmar R., and Rühle H.-J. (1993) Peptides and the blood-brain barrier. Physiol. Rev. 73, 489-527.
27. Fishman J. B., Rubin J. B., Handrahan J. V., Connor J. R., and Fine R. E. (1987) Receptor-mediated transcytosis of transferrin across the blood-brain barrier. J. Neurosci. Res. 18, 299-304.
28. Frederickson R. C. A., Smithwick E. L., Shuman R , and Bemis K. G. (1981) Metkephamid, a systemically active analog of methionine enkephalin with potent opioid d-receptor activity. Science 211, 603-605.
29. Galligan J. J., Mosberg H. I., Hurst R., Hruby V. J., and Burks T. F. (1984) Cerebral delta opioid receptors mediate analgesia but not the intestinal motility effects of intracerebroventricularly administered opioids. J. Pharmacol. Exp. Ther. 229, 641-648.
30. Gjedde A. (1981) High- and low-affinity transport of D-glucose from blood to brain. J. Neurochem. 36, 1463-1471.
31. Gjedde A. (1982) Calculation of cerebral glucose phosphorylation from brain uptake of glucose analogues in vivo: a re-examination. Brain Res. 4, 237-274.
32. Hambrook J. M., Morgan B. A., Rance M. J., and Smith C. F. (1976) Mode of deactivation of the enkephalins by rat and human plasma and rat brain homogenates. Nature 262, 782-783.
33. Heyman J. S., Mulvaney S. A., Mosberg H. I., and Porreca F. (1987) Opioid δ-receptor involvement in supraspinal and spinal antinociception in mice. Brain Res. 420, 100-108.
34. 5] enkephalin. J. Med. Chem. 34, 1823-1830.
35. Karman R., Kuhlenkamp J. F., Cokhtens M., and Kaplowitz N. (1992) Transport of glutathione at blood-brain barrier of the rat: inhibition by glutathione analogs and age dependence. J. Pharmacol. Exp. Ther. 263, 964-970.
36. Keep R. F. and Jones H. C. (1990) A morphometric study on the development of the lateral ventricle choroid plexus, choroid plexus capillaries and ventricular ependyma in the rat. Dev. Brain Res. 56, 47-53.
37. Kumagai A. K., Eisenberg J. B., and Pardridge W. M. (1987) Absorptive-mediated endocytosis of cationized albumin and a β-endorphin-cationized albumin chimeric peptide by isolated brain capillaries. J. Biol. Chem. 262, 15214-15219.
38. Lord J. A. H., Waterfield A. A., Hughes J., and Kosterlitz H. W. (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267, 495-499.
39. Lowry O. H., Rosebrough N. J., Farr A. L., and Randall R. I. (1951) Protein measurements with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
40. Mansour A., Fox C. A , Akil H., and Watson S. J. (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 18, 22-29.
41. Martin W. R., Eades C. G., Thompson J. A., Huppler R. E., and Gilbert P. E. (1976) The effects of morphine and nalorphine-like drugs in the non-dependent and chronically dependent chronic spinal dog. J. Pharmacol. Exp. Ther. 197, 517-532.
42. Mosberg H. I., Hurst R., Hruby V. J., Gee K., Yamamura H. I., Galligan J. J., and Burks T. F. (1983) Bis-penicillamine enkephalins possess highly improved specificity toward delta opioid receptors. Proc. Natl. Acad. Sci. USA 80, 5871-5874.
43. Ohno K., Pettigrew K. D., and Rapoport S. I. (1978) Lower limits of cerebrovascular permeability to non-electrolytes in the conscious rat. Am. J. Physiol. 235, H299-H307.
44. Pardridge W. M. (1983) Brain metabolism: a perspective from the blood-brain barrier. Physiol. Rev. 63, 1481-1535.
45. Pardridge W. M., Eisenberg J., and Yang J. (1985) Human blood-brain barrier insulin receptor. J. Neurochem. 44, 1771-1778.
46. Pardridge W. M., Triguero D., Yang J., and Cancilla P. A. (1990) Comparison of in vitro and in vivo models of drug transcytosis through the blood-brain barrier. J. Pharmacol. Exp. Ther. 253, 884-891.
47. Patlak C. S., Fenstermacher J. D., and Blasberg R. G. (1983) Graphical evaluation of blood-brain barrier transfer constants from multiple-time uptake data. J. Cereb. Blood Flow Metab. 3, 1-7.
48. Paulus H. (1969) A rapid and sensitive method for measuring the binding of radioactive ligands to proteins. Anal. Biochem. 32, 91-100.
49. Pert C. B. and Snyder S. H. (1973) Opiate receptor: demonstration in nervous tissue. Science 179, 1011-1014.
50. Poduslo J. F., Curran G. L., and Berg C. T. (1994) Macromolecular permeability across the blood-nerve and blood-brain barriers. Proc. Natl. Acad. Sci. USA 91, 5705-5709.
51. Porreca F., Mosberg H. I., Hurst R., Hruby V. J., and Burks R. F (1984) Roles of mu, delta and kappa opioid receptors in spinal and supraspinal mediation of gastrointestinal transit effects and hot-plate analgesia in the mouse. J. Pharmacol. Exp. Ther. 230, 341-348.
52. 14C-mannitol using the rat in situ brain perfusion technique. Dev. Brain Res. 87, 69-76.
53. Rapoport S. I., Klee W. A., Pettigrew K. D., and Ohno K. (1980) Entry of opioid peptides into the central nervous system. Science 207, 84-86.
54. Shimura T., Tabata S., Ohnishi T., Terasaki T., and Tsuji A. (1991) Transport mechanism of a new behaviorally highly potent adrenocorticotropic hormone (ACTH) analog, ebiratide, through the blood-brain barrier. J. Pharmacol. Exp. Ther. 258, 459-465.
55. Shook J. E., Pelton J. T., Hruby V. J., and Burks T. F. (1987) Peptide opioid antagonist separates peripheral and central opioid antitransit effects. J. Pharmacol. Exp. Ther. 243, 492-500.
56. Smith Q. R. and Rapoport S. I. (1986) Cerebrovascular permeability coefficients to sodium, potassium and chloride. J. Neurochem. 46, 1732-1742.
57. Szentesvanyi I., Patlak C. S., Ellis R. A., and Cserr H. F. (1984) Drainage of interstitial fluid from different regions of the rat brain. Am. J. Physiol 246, F835-F844.
58. Terasaki T., Ichihirai K., Sato H., Kang Y. S., and Tsuji A. (1989) Absorptive-mediated endocytosis of a dynorphin-like analgesic peptide, E-2078, into the blood-brain barrier. J. Pharmacol. Exp. Ther. 251, 351-357.
59. Triguero D., Buciak J., and Pardridge W. M. (1990) Capillary depletion method for quantification of blood-brain barrier transport of circulating peptides and plasma proteins. J. Neurochem. 54, 1882-1888.
60. 4] deltorphin with δ-opioid receptor subtypes in vivo. Eur. J. Pharmacol. 252, 133-137.
61. Ward S. J. and Takemori A. E. (1983) Relative involvement of mu, kappa and delta receptor mechanisms in opiate-mediated antinociception in mice. J. Pharmacol. Exp. Ther. 224, 525-530.
62. 5]-enkephalin and two halogenated analogs after intravenous administration. J. Pharmacol. Exp. Ther. 259, 1109-1117.
63. 5] enkephalin after intraperitoneal, intravenous, oral and subcutaneous administration. J. Pharmacol. Exp. Ther. 263, 1308-1316.
64. 5] enkephalin opioid analogs. J. Pharmacol. Exp. Ther. 266, 1649-1655.
65. Williams S. A., Davson H., and Segal M. B. (1993) Thymidine entry into the brain and cerebrospinal fluid (CSF) of the anaesthetized guinea-pig using the in situ brain perfusion technique. J. Physiol. (Lond.) 459, 178P.
66. Yoburn B. C., Lutfy K., and Candido J. (1991) Species differences in μ- and δ-opioid receptors. Eur. J. Pharmacol. 193, 105-108.
67. Zlokovic B. V., Begley D. J., Djuricic B. M., and Mitrovic D. M. (1986) Measurement of solute transport across the blood-brain barrier in the perfused guinea-pig brain: method and application to N-methyl-α-aminoisobutyric acid. J. Neurochem. 46, 1444-1451.
68. Zlokovic B. V., Segal M. B., Davson H., and Mitrovic D. M. (1988a) Unidirectional uptake of enkephalins at the blood-tissue interface of the blood-cerebrospinal fluid barrier: a saturable mechanism. Regul. Pept. 20, 33-44.
69. Zlokovic B. V., Segal M. B., Davson H., and Jankov R. M. (1988b) Passage of delta sleep-inducing peptide (DSIP) across the blood-cerebrospinal fluid barrier. Peptides 9, 533-538.
70. Zlokovic B. V., Mackic J. B., Djuricic B. M., and Davson H. (1989a) Kinetic analysis of leucine-enkephalin cellular uptake at the luminal side of the blood-brain barrier of an in situ perfused guinea-pig brain. J. Neurochem. 53, 1333-1340.
71. Zlokovic B. V., Susic V. T., Davson H., Begley D. J., Jankov R. M., Mitrovic D. M., and Lipovac M. N. (1989b) Saturable mechanism for delta-sleep-inducing peptide (DSIP) at the blood-brain barrier of the vascularly perfused guinea-pig brain. Peptides 10, 249-254.
72. Zlokovic B. V., Hyman S., McComb J. G., Lipovac M. N., Tang G., and Davson H. (1990) Kinetics of arginine-vasopressin uptake at the blood-brain barrier. Biochim. Biophys. Acta 1025, 191-198.
73. Zlokovic B. V., Segal M. B., McComb J. G., Hyman S., Weiss M. H., and Davson H. (1991) Kinetics of circulating vasopressin by choroid plexus. Am. J. Physiol. 260, F216-F224.
74. Zlokovic B. V., Banks W. A., Kadi H. E., Erchegyi J., Mackic J. B., McComb J. G., and Kastin A. J. (1992) Transport, uptake and metabolism of blood-bourne vasopressin by the blood-brain barrier. Brain Res. 590, 213-218.
75. Zlokovic B. V., Ghiso J., Mackic J. B., McComb J. G., Weiss M. H., and Frangione B. (1993) Blood-brain barrier transport of circulating Alzheimer's amyloid β. Biochem. Biophys. Res. Commun. 197, 1034-1040.
76. Zlokovic B. V., Mackic J. B., McComb J. G., Weiss M. H., Kaplowitz N., and Kannan R. (1994) Evidence for transcapulary transport of reduced glutathione in vascular perfused guinea-pig. Biochem. Biophys. Res. Commun. 201, 402-408.