Effect of chronic exposure to morphine on the rat blood-brain barrier: Focus on the P-glycoprotein

Journal of Neurochemistry

Volumn 107, Issue 3, 2008, Pages 647-657

  Yousif, Salah ^a,b   Saubaméa, Bruno ^c   Cisternino, Salvatore ^a,b   Marie Claire, Cynthia ^a,b   Dauchy, Sandrine ^a,b   Scherrmann, Jean Michel ^a,b   Declèves, Xavier ^a,b  

^a CNRS   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Blood brain barrier; Hippocampus; Morphine; P glycoprotein; Rat

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CAVEOLIN 1; CAVEOLIN 2; CLAUDIN 5; GLUCOSE TRANSPORTER 1; GLYCOPROTEIN P; MESSENGER RNA; MORPHINE; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; OCCLUDIN; PROTEIN MDR1A; PROTEIN MDR1B; RNA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN CORTEX; BRAIN PERFUSION; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENE INDUCTION; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LONG TERM EXPOSURE; MALE; MDR1A GENE; MDR1B GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; IN SITU HYBRIDIZATION; MALE; MICROSCOPY, CONFOCAL; MORPHINE; NARCOTICS; P-GLYCOPROTEIN; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

RATTUS;

EID: 53749094452     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05647.x     Document Type: Article

References (39)

1. Aquilante C. L., Letrent S. P., Pollack G. M. Brouwer K. L. (2000) Increased brain P-glycoprotein in morphine tolerant rats. Life Sci. 66, PL47 PL51.
2. Bazzoni G. Dejana E. (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84, 869 901.
3. Bhattacharjee A. K., Nagashima T., Kondho T. Tamaki N. (2001) Quantification of early blood-brain barrier disruption by in situ brain perfusion technique. Brain Res. Brain Res. Protoc. 8, 126 131.
4. Brooks T. A., Hawkins B. T., Huber J. D., Egleton R. D. Davis T. P. (2005) Chronic inflammatory pain leads to increased blood-brain barrier permeability and tight junction protein alterations. Am. J. Physiol. Heart Circ. Physiol. 289, H738 H743.
5. Callaghan R. Riordan J. R. (1993) Synthetic and natural opiates interact with P-glycoprotein in multidrug-resistant cells. J. Biol. Chem. 268, 16059 16064.
6. Cattelotte J., André P., Ouellet M., Bourasset F., Scherrmann J. M. Cisternino S. (2008) In situ mouse carotid perfusion model: glucose and cholesterol transport in the eye and brain. J. Cereb. Blood Flow Metab. 28, 1449 1459.
7. Cisternino S., Rousselle C., Dagenais C. Scherrmann J. M. (2001) Screening of multidrug-resistance sensitive drugs by in situ brain perfusion in P-glycoprotein-deficient mice. Pharm. Res. 18, 183 190.
8. Cisternino S., Rousselle C., Debray M. Scherrmann J. M. (2003a) In vivo saturation of the transport of vinblastine and colchicine by P-glycoprotein at the rat blood-brain barrier. Pharm. Res. 20, 1607 1611.
9. Cisternino S., Rousselle C., Lorico A., Rappa G. Scherrmann J. M. (2003b) Apparent lack of Mrp1-mediated efflux at the luminal side of mouse blood-brain barrier endothelial cells. Pharm. Res. 20, 904 909.
10. Decleves X., Regina A., Laplanche J. L., Roux F., Boval B., Launay J. M. Scherrmann J. M. (2000) Functional expression of P-glycoprotein and multidrug resistance-associated protein (Mrp1) in primary cultures of rat astrocytes. J. Neurosci. Res. 60, 594 601.
11. Goralski K. B., Hartmann G., Piquette-Miller M. Renton K. W. (2003) Downregulation of mdr1a expression in the brain and liver during CNS inflammation alters the in vivo disposition of digoxin. Br. J. Pharmacol. 139, 35 48.
12. Habgood M. D., Bye N., Dziegielewska K. M., Ek C. J., Lane M. A., Potter A., Morganti-Kossmann C. Saunders N. R. (2007) Changes in blood-brain barrier permeability to large and small molecules following traumatic brain injury in mice. Eur. J. Neurosci. 25, 231 238.
13. Hamabe W., Maeda T., Fukazawa Y., Kumamoto K., Shang L. Q., Yamamoto A., Yamamoto C., Tokuyama S. Kishioka S. (2006) P-glycoprotein ATPase activating effect of opioid analgesics and their P-glycoprotein-dependent antinociception in mice. Pharmacol. Biochem. Behav. 85, 629 636.
14. Hong H., Lu Y., Ji Z. N. Liu G. Q. (2006) Up-regulation of P-glycoprotein expression by glutathione depletion-induced oxidative stress in rat brain microvessel endothelial cells. J. Neurochem. 98, 1465 1473.
15. Kaplan T. J., Skyers P. R., Tabori N. E., Drake C. T. Milner T. A. (2004) Ultrastructural evidence for mu-opioid modulation of cholinergic pathways in rat dentate gyrus. Brain Res. 1019, 28 38.
16. King M., Su W., Chang A., Zuckerman A. Pasternak G. W. (2001) Transport of opioids from the brain to the periphery by P-glycoprotein: peripheral actions of central drugs. Nat. Neurosci. 4, 268 274.
17. Kwan P., Sills G. J., Butler E., Gant T. W. Brodie M. J. (2003) Differential expression of multidrug resistance genes in naive rat brain. Neurosci. Lett. 339, 33 36.
18. Letrent S. P., Pollack G. M., Brouwer K. R. Brouwer K. L. (1999a) 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.
19. Letrent S. P., Polli J. W., Humphreys J. E., Pollack G. M., Brouwer K. R. Brouwer K. L. (1999b) P-glycoprotein-mediated transport of morphine in brain capillary endothelial cells. Biochem. Pharmacol. 58, 951 957.
20. Löscher W. Potschka H. (2005) Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog. Neurobiol. 76, 22 76.
21. Marie-Claire C., Courtin C., Roques B. P. Noble F. (2004) Cytoskeletal genes regulation by chronic morphine treatment in rat striatum. Neuropsychopharmacology 29, 2208 2215.
22. Mercier C., Decleves X., Masseguin C., Fragner P., Tardy M., Roux F., Gabrion J. Scherrmann J. M. (2003) P-glycoprotein (ABCB1) but not multidrug resistance-associated protein 1 (ABCC1) is induced by doxorubicin in primary cultures of rat astrocytes. J. Neurochem. 87, 820 830.
23. Moutsimilli L., Farley S., Dumas S., El Mestikawy S., Giros B. Tzavara E. T. (2005) Selective cortical VGLUT1 increase as a marker for antidepressant activity. Neuropharmacology 49, 890 900.
24. Nitta T., Hata M., Gotoh S., Seo Y., Sasaki H., Hashimoto N., Furuse M. Tsukita S. (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 161, 653 660.
25. Noble F., Szucs M., Kieffer B. Roques B. P. (2000) Overexpression of dynamin is induced by chronic stimulation of mu- but not delta-opioid receptors: relationships with mu-related morphine dependence. Mol. Pharmacol. 58, 159 166.
26. Regina A., Koman A., Piciotti M., El Hafny B., Center M. S., Bergmann R., Couraud P. O. Roux F. (1998) Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells. J. Neurochem. 71, 705 715.
27. Ruiz F., Fournié-Zaluski M. C., Roques B. P. Maldonado R. (1996) Similar decrease in spontaneous morphine abstinence by methadone and RB 101, an inhibitor of enkephalin catabolism. Br. J. Pharmacol. 119, 174 182.
28. Scherrmann J. M. (2005) Expression and function of multidrug resistance transporters at the blood-brain barriers. Expert Opin. Drug Metab. Toxicol. 1, 233 246.
29. Sharma H. S. Ali S. F. (2006) Alterations in blood-brain barrier function by morphine and methamphetamine. Ann. NY Acad. Sci. 1074, 198 224.
30. Smith Q. R. (1996) Brain perfusion systems for studies of drug uptake and metabolism in the central nervous system, in Models for Assessing Drug Absorption and Metabolism, Vol. 8 (Borchardt R. T., Smith P. L. Wilson G., eds), pp. 285 307. Plenum Press, New York.
31. Sugiyama D., Kusuhara H., Lee Y. J. Sugiyama Y. (2003) Involvement of multidrug resistance associated protein 1 (Mrp1) in the efflux transport of 17beta estradiol-D-17beta-glucuronide (E217betaG) across the blood-brain barrier. Pharm. Res. 20, 1394 1400.
32. Thompson S. J., Koszdin K. Bernards C. M. (2000) Opiate-induced analgesia is increased and prolonged in mice lacking P-glycoprotein. Anesthesiology 92, 1392 1399.
33. van Vliet E., Aronica E., Redeker S., Marchi N., Rizzi M., Vezzani A. Gorter J. (2004) Selective and persistent upregulation of mdr1b mRNA and P-glycoprotein in the parahippocampal cortex of chronic epileptic rats. Epilepsy Res. 60, 203 213.
34. Volk H. A., Burkhardt K., Potschka H., Chen J., Becker A. Loscher W. (2004) Neuronal expression of the drug efflux transporter P-glycoprotein in the rat hippocampus after limbic seizures. Neuroscience 123, 751 759.
35. Volk H., Potschka H. Loscher W. (2005) Immunohistochemical localization of P-glycoprotein in rat brain and detection of its increased expression by seizures are sensitive to fixation and staining variables. J. Histochem. Cytochem. 53, 517 531.
36. Yousif S., Marie-Claire C., Roux F., Scherrmann J. M. Decleves X. (2007) Expression of drug transporters at the blood-brain barrier using an optimized isolated rat brain microvessel strategy. Brain Res. 1134, 1 11.
37. Ziemann C., Riecke A., Rudell G., Oetjen E., Steinfelder H. J., Lass C., Kahl G. F. Hirsch-Ernst K. I. (2006) The role of prostaglandin E receptor-dependent signaling via cAMP in Mdr1b gene activation in primary rat hepatocyte cultures. J. Pharmacol. Exp. Ther. 317, 378 386.
38. Zong J. Pollack G. M. (2000) Morphine antinociception is enhanced in mdr1a gene-deficient mice. Pharm. Res. 17, 749 753.
39. Zong J. Pollack G. M. (2003) Modulation of P-glycoprotein transport activity in the mouse blood-brain barrier by rifampin. J. Pharmacol. Exp. Ther. 306, 556 562.