The role of multidrug resistance-associated protein in the blood-brain barrier and opioid analgesia

Synapse

Volumn 67, Issue 9, 2013, Pages 609-619

  Su, Wendy ^a   Pasternak, Gavril W ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Analgesia; Efflux; MRP; Opioid; Peripheral; Tolerance; Transport; Transporter

Indexed keywords

MESSENGER RNA; MORPHINE; MULTIDRUG RESISTANCE PROTEIN;

ANALGESIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CHOROID PLEXUS; CONTROLLED STUDY; DOWN REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANALGESIA; EFFLUX; MRP; OPIOID; PERIPHERAL; TOLERANCE; TRANSPORT; TRANSPORTER;

ANALGESICS, OPIOID; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; DOWN-REGULATION; MALE; MICE; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION, GENETIC;

EID: 84880575825     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.21667     Document Type: Article

References (56)

1. Abe T, Kakyo M, Sakagami H, Tokui T, Nishio T, Tanemoto M, Nomura H, Hebert SC, Matsuno S, Kondo H, Yawo H. 1998. Molecular characterization and tissue distribution of a new organic anion transporter subtype (oatp3) that transports thyroid hormones and taurocholate and comparison with oatp2. J Biol Chem 273:22395-22401.
2. Aquilante CL, Letrent SP, Pollack GM, Brouwer KLR. 1999. Increased brain P-glycoprotein in morphine tolerant rats. Life Sci 66:L47-L51.
3. Banks WA, Kastin AJ. 1987. Saturable transport of peptides across the blood-brain barrier. Life Sci 41:1319-1338.
4. Banks WA, Kastin AJ. 1994. Opposite direction of transport across the blood-brain barrier for Tyr-MIF-1 and MIF-1: Comparison with morphine. Peptides 15:23-29.
5. Banks WA, Kastin AJ. 1996. Passage of peptides across the blood-brain barrier: Pathophysiological perspectives. Life Sci 59:1923-1943.
6. Banks WA, Kastin AJ, Ehrensing CA. 1993. Endogenous peptide Tyr-Pro-Trp-Gly-NH2 (Tyr-W-MIF-1) is transported from the brain to the blood by peptide transport system-1. J Neurosci Res 35:690-695.
7. Bodnar RJ, Pasternak GW, Mann PE, Paul D, Warren R, Donner DB. 1989. Mediation of anorexia by human, recombinant tumor necrosis factor through a peripheral action in the rat. Cancer Res 49:6280-6284.
8. Callaghan R, Riordan JR. 1993. Synthetic and natural opiates interact with P-glycoprotein in multidrug-resistant cells. J Biol Chem 268:16059-16064.
9. Chen C, Pollack GM. 1998. Altered disposition and antinociception of [D-Penicillamine2, 5] enkephalin in mdr1a-gene-deficient mice. J Pharmacol Exp Ther 287:545-552.
10. Cole SP, Deeley RG. 1996. Multidrug resistance associated with overexpression of MRP. Cancer Treat Res 87:39-62.
11. Cole SP, Deeley RG. 1998. Multidrug resistance mediated by the ATP-binding cassette transporter protein MRP. Bioessays 20:931-940.
12. Cole SP, Sparks KE, Fraser K, Loe DW, Grant CE, Wilson GM, Deeley RG. 1994. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54:5902-5910.
13. Cordon-Cardo C, O'Brien JP, Rittman-Grauer L, Biedler JL, Melamed MR, Bertino JR. 1989. Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-barrier sites. Proc Natl Acad Sci USA 86:695-698.
14. Drewe J, Ball HA, Beglinger C, Peng B, Kemmler A, Schächinger H, Haefeli WE. 2000. Effect of P-glycoprotein modulation on the clinical pharmacokinetics and adverse effects of morphine. Br J Clin Pharmacol 50:237-246.
15. Gao B, Hagenbuch B, Kullak-Ublick GA, Benke D, Aguzzi A, Meier PJ. 2000. Organic anion-transporting polypeptides mediate transport of opioid peptides across blood-brain barrier. J Pharmacol Exp Ther 294:73-79.
16. Goldberg IE, Rossi GC, Letchworth SR, Mathis JP, Ryan-Moro J, Leventhal L, Su W, Emmel D, Bolan EA, Pasternak GW. 1998. Pharmacological characterization of endomorphin-1 and endomorphin-2 in mouse brain. J Pharmacol Exp Ther 286:1007-1013.
17. Goodman JC, Robertson CS, Grossman RG, Narayan RK. 1990. Elevation of tumor necrosis factor in head injury. J Neuroimmunol 30:213-217.
18. Grant CE, Valdimarsson G, Hipfner DR, Almquist KC, Cole SP, Deeley RG. 1994. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res 54:357-361.
19. Hamabe W, Maeda T, Kiguchi N, Yamamoto C, Tokuyama S, Kishioka S. 2007. Negative relationship between morphine analgesia and P-glycoprotein expression levels in the brain. J Pharmacol Sci 105:353-360.
20. Hassan HE, Mercer SL, Cunningham CW, Coop A, Eddington ND. 2009. Evaluation of the P-glycoprotein (Abcb1) affinity status of a series of morphine analogs: Comparative study with meperidine analogs to identify opioids with minimal P-glycoprotein interactions. Int J Pharm 375:48-54.
21. Hegmann EJ, Bauer HC, Kerbel RS. 1992. Expression and functional activity of P-glycoprotein in cultured cerebral capillary endothelial cells. Cancer Res 6969-6975.
22. Hipfner DR, Deeley RG, Cole SP. 1999. Structural, mechanistic and clinical aspects of MRP1. Biochim Biophys Acta 1461:359-376.
23. Kalvass JC, Olson ER, Pollack GM. 2007. Pharmacokinetics and pharmacodynamics of alfentanil in P-glycoprotein-competent and P-glycoprotein-deficient mice: P-glycoprotein efflux alters alfentanil brain disposition and antinociception. Drug Metab Dispos 35:455-459.
24. King M, Su W, Chang A, Zuckerman A, Pasternak GW. 2001. Transport of opioids from the brain to the periphery by P-glycoprotein: Peripheral actions of central drugs. Nat Neurosci 4:268-274.
25. King MA, Pan Y-X, Mei J, Chang A, Xu J, Pasternak GW. 1997. Enhanced kappa opioid analgesia by antisense targeting the σ1 receptor. Eur J Pharmacol 331:R5-R6.
26. Kolesnikov Y, Pasternak GW. 1999. Topical opioids in mice: Analgesia and reversal of tolerance by a topical N-methyl-d-aspartate antagonist. J Pharmacol Exp Ther 290:247-252.
27. Kolesnikov Y, Jain S, Wilson R, Pasternak GW. 1996a. Peripheral kappa 1-opioid receptor-mediated analgesia in mice. Eur J Pharmacol 310:141-143.
28. Kolesnikov YA, Jain S, Wilson R, Pasternak GW. 1996b. Peripheral morphine analgesia: Synergy with central sites and a target of morphine tolerance. J Pharmacol Exp Ther 279:502-506.
29. Kolesnikov YA, Pan YX, Babey AM, Jain S, Wilson R, Pasternak GW. 1997. Functionally differentiating two neuronal nitric oxide synthase isoforms through antisense mapping: Evidence for opposing NO actions on morphine analgesia and tolerance. Proc Natl Acad Sci USA 94:8220-8225.
30. Le Bars D, Gozariu M, Cadden SW. 2001. Animal models of nociception. Pharmacol Rev 53:597-652.
31. Letrent SP, Pollack GM, Brouwer KR, Brouwer KLR. 1998. Effect of GF120918, a potent P-glycoprotein inhibitor, on morphine pharmacokinetics and pharmacodynamics in the rat. Pharm Res 15:599-605.
32. Letrent SP, Pollack GM, Brouwer KR, Brouwer KLR. 1999. Effects of a potent and specific P-glycoprotein inhibitor on the blood-brain barrier distribution and antinociceptive effect of morphine in the rat. Drug Metab Dispos 27:827-834.
33. Loe DW, Deeley RG, Cole SP. 1996. Biology of the multidrug resistance-associated protein, MRP. Eur J Cancer 32A:945-957.
34. Lotsch J, Skarke C, Liefhold J, Geisslinger G. 2004. Genetic predictors of the clinical response to opioid analgesics: Clinical utility and future perspectives. Clin Pharmacokinet 43:983-1013.
35. Marzolini C, Paus E, Buclin T, Kim RB. 2004. Polymorphisms in human MDR1 (P-glycoprotein): Recent advances and clinical relevance. Clin Pharmacol Ther 75:13-33.
36. McClain C, Cohen D, Phillips R, Ott L, Young B. 1991. Increased plasma and ventricular fluid interleukin-6 levels in patients with head injury. J Lab Clin Med 118:225-231.
37. Mercer SL, Coop A. 2011. Opioid analgesics and P-glycoprotein efflux transporters: A potential systems-level contribution to analgesic tolerance. Curr Top Med Chem 11:1157-1164.
38. Pan YX, Xu J, Bolan EA, Abbadie C, Chang A, Zuckerman A, Rossi GC, Pasternak GW. 1999. Identification and characterization of three new alternatively spliced mu opioid receptor isoforms. Mol Pharmacol 56:396-403.
39. Rao VV, Dahlheimer JL, Bardgett ME, Snyder AZ, Finch RA, Sartorelli AC, Piwnica-Worms D. 1999. Choroid plexus epithelial expression of MDR1 P glycoprotein and multidrug resistance-associated protein contribute to the blood-cerebrospinal-fluid drug-permeability barrier. Proc Natl Acad Sci USA 96:3900-3905.
40. Regina A, Koman A, Piciotti M, Hafny BE, Center MS, Bergmann R, Couraud P-O, Roux F. 1998. Mrp1 Multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvesel endothelial cells. J Neurochem 71:705-715.
41. Romero LI, Kakucska I, Lechan RM, Reichlin S. 1996. Interleukin-6 (IL-6) is secreted from the brain after intracerebroventricular injection of IL-1β in rats. Am J Physiol 270:R518-R524.
42. Rossi GC, Pasternak GW, Bodnar RJ. 1993. Synergistic brainstem interactions for morphine analgesia. Brain Res 624:171-180.
43. Rossi GC, Pan Y-X, Cheng J, Pasternak GW. 1994. Blockade of morphine analgesia by an antisense oligodeoxynucleotide against the mu receptor. Life Sci 54:L375-L379.
44. Rossi GC, Pan Y-X, Brown GP, Pasternak GW. 1995. Antisense mapping the MOR-1 opioid receptor: Evidence for alternative splicing and a novel morphine-6β-glucuronide receptor. FEBS Lett 369:192-196.
45. Rossi GC, Brown GP, Leventhal L, Yang K, Pasternak GW. 1996. Novel receptor mechanisms for heroin and morphine-6β -glucuronide analgesia. Neurosci Lett 216:1-4.
46. Rossi GC, Leventhal L, Bolan EA, Pasternak GW. 1997a. Pharmacological characterization of orphanin FQ/nociceptin and its fragments. J Pharmacol Exp Ther 282:858-865.
47. Rossi GC, Leventhal L, Pan YX, Cole J, Su W, Bodnar RJ, Pasternak GW. 1997b. Antisense mapping of MOR-1 in rats: Distinguishing between morphine and morphine-6beta-glucuronide antinociception. J Pharmacol Exp Ther 281:109-114.
48. Schinkel AH, Smit JJ, Van TO, Beijnen JH, Wagenaar E, Van DL, Mol CA, Van Der Valk MA, Robanus Manndage EC, Riele HP. 1994. Disruption of the mouse mdrla P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77:491-502.
49. Schinkel AH, Mol CAAM, Wagenarr E, Van Deemter L, Smit JJM, Borst P. 1995a. Multidrug resistance and the role of P-glycoprotein knockout mice. Eur J Cancer 31A:1295-1298.
50. Schinkel AH, Wagenarr E, Van DL, Mol CA, Borst P. 1995b. Absence of the mdrla P-Glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, diagoxin and cyclosporin A. J Clin Invest 96:1698-1705.
51. Schinkel AH, Wagenaar E, Mol CAAM, Van Deemter L. 1996. P-glycoprotein in the blood-barrier of mice influences the brain penetration and pharmacological activity of many drugs. J Clin Invest 97:2517-2524.
52. Standifer KM, Chien C-C, Wahlestedt C, Brown GP, Pasternak GW. 1994. Selective loss of δ opioid analgesia and binding by antisense oligodeoxynucleotides to a δ opioid receptor. Neuron 12:805-810.
53. Standifer KM, Rossi GC, Pasternak GW. 1996. Differential blockade of opioid analgesia by antisense oligodeoxynucleotides directed against various G-protein α subunits. Mol Pharmacol 50:293-298.
54. Tatsuta T, Naito M, Oh-hara T, Sugawara I, Tsuruo T. 1992. Functional involvement of P-glycoprotein in blood-brain barrier. J Biol Chem 267:20383-20391.
55. Thompson SJ, Koszdin K, Bernards CM. 2000. Opiate-induced analgesia is increased and prolonged in mice lacking P-glycoprotein. Anesthesiology 92:1392-1399.
56. Zong J, Pollack GM. 2000. Morphine antinociception is enhanced in mdr1a gene-deficient mice. Pharm Res 17:749-753.