Facilitation of drug entry into the CNS via transient permeation of blood brain barrier: Laboratory and preliminary clinical evidence from bradykinin receptor agonist, Cereport

Brain Research Bulletin

Volumn 60, Issue 3, 2003, Pages 297-306

  Borlongan, C V ^a,b   Emerich, D F ^c  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Sertoli Technologies Incorporated   (United States)

Author keywords

Analgesics; BBB; Brain tumor; Chemotherapeutics; Immunosuppressants; Neuroprotection; Pain; Parkinson's disease

Indexed keywords

ANALGESIC AGENT; ANTIINFECTIVE AGENT; BRADYKININ RECEPTOR AGONIST; CARBOPLATIN; CYCLOSPORIN A; LOBRADIMIL; LOPERAMIDE; NEUROPROTECTIVE AGENT;

ABDOMINAL PAIN; ADJUVANT CHEMOTHERAPY; ANALGESIC ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BRAIN TUMOR; CARDIOTOXICITY; CENTRAL NERVOUS SYSTEM; DIARRHEA; DRUG BIOAVAILABILITY; DRUG DOSE REGIMEN; DRUG EFFECT; DRUG EFFICACY; DRUG PENETRATION; DRUG POTENTIATION; DRUG SAFETY; DRUG TRANSPORT; DYSPEPSIA; FACILITATION; FECES INCONTINENCE; HEADACHE; IMMUNE DEFICIENCY; LIVER TOXICITY; MEMBRANE PERMEABILITY; NAUSEA; NEPHROTOXICITY; NEUROPROTECTION; NONHUMAN; PAIN; PARKINSON DISEASE; PRIORITY JOURNAL; URINARY URGENCY; XEROSTOMIA;

EID: 0038399929     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0361-9230(03)00043-1     Document Type: Article

References (88)

1. Barth R., Yang W., Moeschberger M., Goodman J., Bartus R. Enhanced delivery of boronophenylalanine for neutron capture therapy of brain tumors using the bradykinin analogue, Cereport (RMP-7). Neurosurgery. 47:1999;189-198.
2. Bartus R.T. The blood-brain barrier as a target for pharmacological modulation. Curr. Opin. Drug Discov. Dev. 2:1999;152-167.
3. Bartus R.T., Elliott P.J., Dean R.L., Hayward N.J., Nagle R.L., Huff M.R., Snodgrass P.A., Blunt D.G. Controlled modulation of BBB permeability using the bradykinin agonist, RMP-7. Exp. Neurol. 142:1996;14-28.
4. Bartus R.T., Elliott P., Hayward N., Dean R., McEwan E.L., Fisher S.K. Permeability of the BBB by the bradykinin agonist, RMP-7: evidence for a sensitive, auto-regulated, receptor-mediated system. Immunopharmacology. 33:1999;270-278.
5. Bartus R., Snodgrass P., Dean R., Kim B., Black K., Emerich D. Use of Cereport (RMP-7) to increase delivery of carboplatin to gliomas: insight and parameters for intracarotid infusion via a single-lumen cannula. Drug Deliv. 6:1999;15-21.
6. Bartus R., Snodgrass P., Dean R., Kordower J., Emerich D. Evidence that Cereport's ability to increase permeability of rat gliomas is dependent upon extent of tumor growth: implications for treating newly emerging tumor colonies. Exp. Neurol. 161:2000;234-244.
7. Bartus R., Snodgrass P., Marsh J., Agostino M., Perkins A., Emerich D. Intravenous Cereport (RMP-7) modifies topographic uptake profile of carboplatin within rat glioma and brain surrounding tumor, elevates platinum levels and enhances survival. J. Pharm. Exp. Ther. 293:2000;903-911.
8. A. Betz, An overview of the multiple functions of the blood-brain barrier, in: J. Frankenheim, R. Brown (Eds.), Bioavailability of Drugs to the Brain and the Blood-Brain Barrier, U.S. Government Printing Office, Washington, D.C., 1992, pp. 54-72.
9. Bhoola K., Figueroa C., Worthy K. Bioregulation of kinins: kallikreins, kininogens and kinases. Pharm. Rev. 44:1992;1-80.
10. Black K. Biochemical opening of the blood-brain barrier. Adv. Drug Deliv. Rev. 15:1995;37-52.
11. Black K., Cloughesy T., Huang S., Gobin Y., Zhou Y., Grous J., Nelson G., Farahani K., Hoh K., Phelps M. Intracarotid infusion of RMP-7, a bradykinin analog, and transport of gallium-68 ethylenediamine tetraacetic acid into human gliomas. J. Neurosurg. 86:1997;603-609.
12. Boddy A., Thomas H. RMP-7: potential as an adjuvant to the drug treatment of brain tumors. CNS Drugs. 7:1997;257-263.
13. Boogerd W., Sande J.V.D., Zandwijk N.V. Teniposide sometimes effective in brain metastases from non-small cell lung cancer. J. Neurooncol. 41:1999;285-289.
14. Borlongan C.V., Emerich D.F., Hoffer B.J., Bartus R.T. Bradykinin receptor agonist facilitates low-dose Cyclosporine-A protection against 6-hydroxydopamine neurotoxicity. Brain Res. 956:2002;211-220.
15. R. Burch, D. Kyle, T. Stormann, Molecular Biology and Pharmacology of Bradykinin Receptors, R.G. Landes Company, Austin, 1993.
16. Cloughesy T., Black K., Gobin Y., Farahani K., Nelson G., Villablanca P., Kabbinavar F., Vinuela F., Wortel C. Intra-arterial Cereport (RMP-7) and carboplatin: a dose escalation study for recurrent malignant gliomas. Neurosurgery. 44:1999;270-278.
17. Constantini L.C., Chaturvedi P., Armistead D.M., McCaffrey P.G., Deacon T.W., Isacson O. A novel immunophilin ligand: distinct branching effects on dopaminergic neurons in culture and neurotrophic actions after oral administration in an animal model of Parkinson's disease. Neurobiol. Dis. 5:1998;97-106.
18. H. Davson, M. Segal, Physiology of the CSF and Blood-Brain Barriers, CRC Press, Boca Raton, FL, 1996.
19. R. DelMaestro, Angiogenesis, in: M. Berger, C. Wilson (Eds.), The Gliomas, WB Saunders, Philadelphia, 1999, pp. 87-106.
20. Doctrow S.R., Abelleira S.M., Curry L.A., Heller-Harrion R., Kozarich J.W., Malfroy B., McCarroll L.A., Morgan K.G., Morrow A.R., Musso G.F., Smart J.L., Straub J.A., Turnbull B., Gloff C.A. The bradykinin analog RMP-7 increases intracellular free calcium levels in rat brain microvascular endothelial cells. J. Pharm. Exp. Ther. 271:1994;229-237.
21. Dray A., Perkins M. Bradykinin and inflammatory pain. TINS. 16:1993;99-104.
22. 2 agonist RMP-7. Immunopharmacology. 33:1996;205-208.
23. Elliott P.J., Hayward N.J., Dean R.L., Blunt D.G. Intravenous RMP-7 selectively increases uptake of carboplatin into rat brain tumors. Cancer Res. 56:1996;3998-4005.
24. Elliott P.J., Hayward N.J., Huff M.R., Nagle T.L., Black K.L., Bartus R.T. Unlocking the blood-brain barrier: a role for RMP-7 in brain tumor therapy. Exp. Neurol. 141:1996;214-224.
25. Emerich D., Dean R., Marsh J., Pink M., Baker K., Lafreniere D., Bartus R. Intravenous Cereport (RMP-7) enhances delivery of carboplatin and increases survival in rats with metastatic tumors in the brain. Pharm. Res. 17:2000;1212-1219.
26. Emerich D., Snodgrass P., Dean R., Agostino M., Hasler B., Pink M., Xiong H., Kim B.S., Bartus R. Enhanced uptake of carboplatin into brain tumors with intravenous Cereport (RMP-7): dramatic differences as a function of dosing parameters. Br. J. Cancer. 80:1999;964-970.
27. 2 receptors increases delivery of chemotherpaeutic agents into solid peripheral tumors, enhancing their efficacy. J. Pharm. Exp. Ther. 296:2000;623-631.
28. Emerich D., Snodgrass P., Dean R., Lafreniere D., Agostino M., Wiens T., Xiong H., Hasler B., Marsh J., Pink M., Kim B.S., Bartus R. Bradykinin modulation of tumor vasculature II: activation of nitric oxide and phospholipase A2/prostaglandin signaling pathways synergistically modify vascular physiology and morphology to enhance delivery of chemotherapeutic agents to tumors. J. Pharm. Exp. Ther. 296:2000;632-641.
29. Emerich D., Snodgrass P., Pink M., Bloom F., Bartus R. Central analgesic actions of loperamide following transient permeation of the blood brain barrier with Cereport (RMP-7). Brain Res. 801:1998;259-266.
30. Erdös E. Some old and some new ideas on kinin metabolism. J. Cardiovasc. Pharmacol. 15:1990;S20-S24.
31. Fike J., Gobbel G., Mesiwala A., Shin H., Nakagawa M., Lamboen K., Seilhan T., Elliott P. Cerebrovascular effects of the bradykinin analog RMP-7 in normal and irradiated dog brain. J. Neurooncol. 37:1998;199-215.
32. J.M. Ford, K.A. Miles, M.P. Hayball, P.W. Bearcroft, N.M. Bleehen, C.S. Osborn, A simplified technique for measurement of blood-brain barrier permeability using CT: preliminary results of the effect of RMP-7, in: Quantitative Imaging in Oncology, British Institute of Radiology, London, UK, 1996.
33. Ford J., Osborn C., Barton T., Bleehen N. A Phase I study of intravenous Cereport (RMP-7) with carboplatin patients with progression of malignant glioma. Eur. J. Cancer. 34:1998;1807-1811.
34. Gregor A., Lind M., Newman H., Grant R., Hadley D., Barton C., Osborn C. Phase II studies of RMP-7 and carboplatin in the treatment of recurrent high grade glioma. J. Neurooncol. 44:1999;137-145.
35. J. Grous, P. Elliott, R. Bartus, Development of RMP-7: a novel bradykinin agonist that increases delivery of chemotherapeutics to gliomas, in: S. Salmon (Ed.), Adjuvant Therapy of Cancer, Lippincott-Raven, Philadelphia, 1997, pp. 19-31.
36. Hamayoun P., Harik S. Bradykinin receptors of cerebral microvessels stimulate phosphoinositide turnover. J. Cereb. Blood Flow Metab. 11:1991;557-566.
37. 2) receptor. Biochem. Biophys. Res. Commun. 184:1992;260-268.
38. Hochberg F., Pruit A. Assumptions from the radiotherapy of glioblastoma. Neurology. 30:1980;907-911.
39. Ikeda K., Ichikawa T., Wakimoto H., Silver J.T.S., Finkelstein D., Harsh IV G., Louis D., Bartus R., Hochberg F., Chiocca E. Oncolytic virus therapy of multiple tumors in the brain requires suppression of innate and elicited antiviral responses. Nat. Med. 5:1999;881-887.
40. Inamura T., Black K.L. Bradykinin selectively opens blood-tumor barrier in experimental brain tumors. J. Cereb. Blood Flow Metab. 14:1994;862-870.
41. Inamura T., Nomura T., Bartus R., Black K. Intracarotid infusion of RMP-7, a bradykinin analog: a method for selective drug delivery to brain tumors. J. Neurosurg. 81:1994;752-758.
42. Jain R. Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Cancer Metastatis. Rev. 9:1990;253.
43. Jain R. Haemodynamic and transport barriers to the treatment of solid tumors. Int. J. Radiat. Biol. 60:1991;85-100.
44. R. Jain, Critical Issues in Tumor Microcirculation, Angiogenesis and Metastasis: Biological Significance and Clinical Relevance, Cambridge, MA, 1998.
45. J. Kozarich, G. Musso, B. Malfroy-Camine, Increasing Blood-Brain Barrier Permeability with Permeabilizer Peptides, Alkermes, Inc., United States, 1993.
46. Kumakura S., Kamo I., Tsurufuji S. Role of bradykinin in the vascular permeability response induced by carrageenin in rats. Br. J. Pharmacol. 93:1988;739-746.
47. Lesser G., Grossman S. The chemotherapy of high grade astrocytomas. Semin. Oncol. 21:1994;220-235.
48. Marceau F., Gendreau M., Barabe J., Pierre S.S., Regoli D. The degradation of bradykinin (BK) and of des-Arg9-BK in plasma. Can. J. Physiol. Pharmacol. 39:1981;131-138.
49. Matsukado K., Inamura T., Nakano S., Fukui M., Bartus R.T., Black K.L. Enhanced tumor uptake of carboplatin and survival in glioma-bearing rats by intracarotid infusion of bradykinin analog, RMP-7. Neurosurgery. 39:1996;125-134.
50. McCarthy D., Potter D., Nicolaides E. An in vivo estimation of the potencies and half-lives of synthetic bradykinin and kallidin. J. Pharmacol. Exp. Ther. 148:1965;117-122.
51. 1 bradykinin receptor. J. Biol. Chem. 269:1994;21583-21586.
52. 2 kinin receptor-mediated internalization of bradykinin in DDT1 MF-2 smooth muscle cells is paralleled by sequestration of the occupied receptors. Arch. Biochem. Biophys. 301:1993;336-344.
53. Nakano S., Matsukado K., Black K. Enhanced cytokines delivery and intercellular adhesion molecule 1 (ICAM-1) expression in glioma by intracarotid infusion of bradykinin analog, RMP-7. Neurol. Res. 19:1997;501-508.
54. D. Nelson, J. McDonald, L. Lapham, R. Qazi, P. Rubin, Central nervous system tumors, in: R. Rubin, S. McDonald, R. Qazi (Eds.), Clinical Oncology, WB Saunders Co, Philadelphia, 1992, pp. 617-644.
55. Nomura T., Inamura T., Black K. Intracarotid infusion of bradykinin selectively increases blood-tumor permeability in 9L and C6 brain tumors. Brain Res. 658:1994;62-66.
56. C. Osborn, S. Stenning, G. Downing, Survival following treatment with RMP-7 and carboplatin in malignant glioma who grade III-IV: comparison with matched controls, in: ECCO, 1997.
57. Pardridge W. Transport of small molecules through the blood-brain barrier: biology and methodology. Adv. Drug Deliv. Rev. 15:1995;5-36.
58. Pardridge W.M. Drug and gene delivery to the brain. The vascular route. Neuron. 36:2002;555-558.
59. P. Postmus, Treatment of brain metastases for small cell lung cancer. Is there a difference with other metastatic sites? Probl. CNS Dis. Lung Cancer 108 (1995).
60. 2 receptors. Eur. J. Pharm. 294:1995;173-182.
61. Quinn P., Bibby M., Cox J., Crawford S. The influence of hydralazine on the vasculature, blood perfusion and chemosensitivity of MAC tumours. Br. J. Cancer. 66:1993;1993.
62. S. Rapoport, Blood-Brain Barrier in Physiology and Medicine, New York, Raven Press, 1976.
63. Raymond J., Robertson D., Dinsdale H. Pharmacological modification of bradykinin induced breakdown of the blood-brain barrier. Can. J. Physiol. Pharmacol. 13:1986;214-220.
64. Regoli D., Barabe J. Pharmacology of bradykinin and related kinins. Pharmacol. Rev. 32:1980;1-46.
65. Regoli D., Drapeau G., Dion S., Couture R. New selective agonists for neurokinin receptors: pharmacological tools for receptor characterization. TIPS. 9:1988;290-295.
66. 1 receptors for kinins in the rabbit by a bacterial lipopolysaccharide. Eur. J. Pharmacol. 71:1981;105-115.
67. Regoli D., Rhaleb N., Drapeau G., Dion S. Kinin receptor subtypes. J. Cardiovasc. Pharmacol. 12:1990;S30-S38.
68. 2-receptor antagonists. Hypertension. 17:1991;107-115.
69. Riley M., Kim N., Watson V., Gobin Y., LeBel C., Bartus R. Intraarterial administration of the bradykinin agonist, RMP-7 and carboplatin: a toxicologic evaluation in swine. J. Neurooncol. 361:1998;67-178.
70. Roberts R., Gullick W. Bradykinin receptors undergo ligand-induced desensitization. Biochemistry. 29:1990;1975-1979.
71. Sanovich E., Bartus R.T., Friden P.M., Dean R.L., Le H.Q., Brightman M.W. Pathway across blood-brain barrier opened by the bradykinin agonist, RMP-7. Brain Res. 705:1995;125-135.
72. Z. Siddik, J. Grous, S. Chang, F. Barker, S. Huhn, M. Nicholas, J. Rabbitt, M. Page, W. Graney, M. Prados, Pharmacokinetics of carboplatin and RMP-7 in patients with recurrect malignant glioma, in: ASCO Annual Meeting, Philadelphia, PA, 1996.
73. 2 receptors following increased permeability of the blood brain barrier by intravenous Cereport, in: Society for Neuroscience, New Orleans, 2000.
74. Snyder S.H., Sabatini D.M., Lai M.M., Steiner J.P., Hamilton G.S., Suzdak P.D. Neural actions of immunophilin ligands. Trends Pharmacol. Sci. 19:1998;21-26.
75. St Croix B., Rago C., Velculescu V., Traverso G., Romans K., Montgomery E., Lal A., Riggins G., Lengauer C., Vogelstein B., Kinzler K. Genes expressed in human tumor endothelium. Science. 289:2000;1197-1202.
76. Steiner J.P., Connolly M.A., Valentine H.L., Hamilton G.S., Dawson T.M., Hester L., Snyder S.H. Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A. Nat. Med. 3:1997;421-428.
77. Stewart P., Farrell C., DelMaestro R. The effect of cellular microenvironment on vessels in the brain. Part 1: vessel structure in tumour, peritumour and brain from humans with malignant glioma. Int. J. Radiat. Biol. 60:1991;125-130.
78. Straub J.A., Akiyama A., Parmar P. In vitro plasma metabolism of RMP-7. Pharm. Res. 11:1994;1673-1676.
79. Sugita M., Black K. Cyclic GMP-specific phosphodiesterase inhibition and intracarotid bradykinin infusion enhances permeability into brain tumors. Cancer Res. 58:1998;914-920.
80. Thomas H., Newell D., Calvert A., Bailey N., Lind M., Osborn C., Smith E., Bleehen N., Boddy A. Clinical studies with the novel bradykinin analog RMP-7 and carboplatin in patients with glioma. Br. J. Cancer. 73:1996;15.
81. Uchino H., Elmer E., Uchino K., Lindvall O., Siesjo B.K. Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischaemia in the rat. Acta Physiol. Scand. 155:1995;469-471.
82. Unterberg A., Wahl M., Baethmann A. Effects of bradykinin on permeability and diameter of pial vessels in vivo. J. Cereb. Blood Flow Metab. 4:1984;574-585.
83. Wahl M., Young A., Edvinnson L., Wagner F. Effects of bradykinin on pial arteries and arterioles in vitro and in situ. J. Cereb. Blood Flow Metab. 3:1983;231-237.
84. Walner K., Galichih J., Krol G., Aribit E., Malkin N. Patterns of failure following treatment of glioblastoma and anaplatic astrocytoma. Int. J. Radiat. Biol. Oncol. Phys. 16:1989;1405-1409.
85. Wolsing D., Rosenbaum J. The mechanism for the rapid desensitization in bradykinin-stimulated inositol monophosphate production in NG108-15 cells involves interaction of a single receptor with multiple signaling pathways. J. Pharm. Exp. Ther. 266:1993;253-261.
86. Yong T., Gao X., Koizumi S., Conlon J., Rennard S., Mayhan W., Rubinstein I. Role of peptidases in bradykinin-induced increase in vascular permeability in vivo. Circ. Res. 70:1992;952-959.
87. Yung W., Mechtler L., Gleason M. Intravenous carboplatin for recurrent malignant glioma: a phase II study. J. Clin. Oncol. 9:1991;860-864.
88. B. Zlokovic, J. McComb, L. Perlmutter, M. Weiss, H. Davson, Neuroactive peptides and amino acid at the blood-brain barrier: possible implications for drug abuse, in: J. Frankenheim, R. Brown (Eds.), Bioavailability of Drugs to the Brain and the Blood-Brain Barrier, U.S. Government Printing Office, Washington, D.C., 1992, pp. 26-42.