Blood-brain interfaces and cerebral drug bioavailability

Revue Neurologique

Volumn 165, Issue 12, 2009, Pages 1029-1038

  Ghersi Egea, J F ^a   Monkkonen K S ^a   Schmitt, C ^a   Honnorat, J ^a   Fevre Montange M ^a   Strazielle, N ^b  

^a UNIVERSITÉ LYON 1   (France)

^b Brain i   (France)

Author keywords

Blood brain barrier; Blood CSF barrier; Brain development; Ependyma; Multidrug resistance

Indexed keywords

ARTICLE; BLOOD BRAIN BARRIER; BRAIN DEVELOPMENT; BRAIN TUMOR; DRUG BIOAVAILABILITY; NONHUMAN; POSTNATAL DEVELOPMENT;

EID: 71549157096     PISSN: 00353787     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurol.2009.09.011     Document Type: Article

References (66)

1. Abramovitz M., Homma H., Ishigaki S., Tansey F., Cammer W., and Listowsky I. Characterization and localization of glutathione-S-transferases in rat brain and binding of hormones, neurotransmitters, and drugs. J Neurochem 50 (1988) 50-57
2. Aoki I., Wu Y.J., Silva A.C., Lynch R.M., and Koretsky A.P. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 22 (2004) 1046-1059
3. Aronica E., Gorter J.A., Redeker S., van Vliet E.A., Ramkema M., Scheffer G.L., et al. Localization of breast cancer resistance protein (BCRP) in microvessel endothelium of human control and epileptic brain. Epilepsia 46 (2005) 849-857
4. Batisson M., Strazielle N., Hejmadi M., Thomas D., Ghersi-Egea J.F., Etienne J., et al. Toxic shock syndrome toxin-1 challenges the neuroprotective functions of the choroidal epithelium and induces neurotoxicity. J Infect Dis 194 (2006) 341-349
5. Bauer B., Hartz A.M., and Miller D.S. Tumor necrosis factor alpha and endothelin-1 increase P-glycoprotein expression and transport activity at the blood-brain barrier. Mol Pharmacol 71 (2007) 667-675
6. Bock N.A., Paiva F.F., Nascimento G.C., Newman J.D., and Silva A.C. Cerebrospinal fluid to brain transport of manganese in a non-human primate revealed by MRI. Brain Res 1198 (2008) 160-170
7. Bredel M. Anticancer drug resistance in primary human brain tumors. Brain Res Brain Res Rev 35 (2001) 161-204
8. Bronger H., Konig J., Kopplow K., Steiner H.H., Ahmadi R., Herold-Mende C., et al. ABCC drug efflux pumps and organic anion uptake transporters in human gliomas and the blood-tumor barrier. Cancer Res 65 (2005) 11419-11428
9. Brown D.A., and Sawchenko P.E. Time course and distribution of inflammatory and neurodegenerative events suggest structural bases for the pathogenesis of experimental autoimmune encephalomyelitis. J Comp Neurol 502 (2007) 236-260
10. Caley D.W., and Maxwell D.S. Development of the blood vessels and extracellular spaces during postnatal maturation of rat cerebral cortex. J Comp Neurol 138 (1970) 31-47
11. Catala M. Embryonic and fetal development of structures associated with the cerebro-spinal fluid in man and other species. Part I: The ventricular system, meninges and choroid plexuses. Arch Anat Cytol Pathol 46 (1998) 153-169
12. Charo I.F., and Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354 (2006) 610-621
13. Choudhuri S., and Klaassen C.D. Structure, function, expression, genomic organization, and single nucleotide polymorphisms of human ABCB1 (MDR1), ABCC (MRP), and ABCG2 (BCRP) efflux transporters. Int J Toxicol 25 (2006) 231-259
14. Cooray H.C., Blackmore C.G., Maskell L., and Barrand M.A. Localisation of breast cancer resistance protein in microvessel endothelium of human brain. Neuroreport 13 (2002) 2059-2063
15. Dauchy S., Dutheil F., Weaver R.J., Chassoux F., Daumas-Duport C., Couraud P.O., et al. ABC transporters, cytochromes P450 and their main transcription factors: expression at the human blood-brain barrier. J Neurochem 107 (2008) 1518-1528
16. Davson H., and Segal M.B. Physiology of the CSF and the blood-brain barriers (1996), CRC Press, Boca Raton, New York, London, Tokyo
17. Dziegielewska K.M., Ek J., Habgood M.D., and Saunders N.R. Development of the choroid plexus. Microsc Res Tech 52 (2001) 5-20
18. Ek C.J., Dziegielewska K.M., Stolp H., and Saunders N.R. Functional effectiveness of the blood-brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 496 (2006) 13-26
19. Fenstermacher J.D. The pharmacology of the blood-brain barrier. In: Neuwelt E. (Ed). Implications of the blood-brain barrier and its manipulation (1989), Plenum, New York 137-155
20. Furuse M., Furuse K., Sasaki H., and Tsukita S. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol 153 (2001) 263-272
21. Gazzin S., Strazielle N., Schmitt C., Fevre-Montange M., Ostrow J.D., Tiribelli C., et al. Differential expression of the multidrug resistance-related proteins ABCb1 and ABCc1 between blood-brain interfaces. J Comp Neurol 510 (2008) 497-507
22. Ghersi-Egea J.F., Finnegan W., Chen J.L., and Fenstermacher J.D. Rapid distribution of intraventricularly administered sucrose into cerebrospinal fluid cisterns via subarachnoid velae in rat. Neuroscience 75 (1996) 1271-1288
23. Ghersi-Egea J.F., Gazzin S., and Strazielle N. Blood-Brain Interfaces and Bilirubin-induced neurological diseases. Cur Pharm Des 15 (2009) 2893-2907
24. Ghersi-Egea J.F., Strazielle N., Murat A., Jouvet A., Buenerd A., and Belin M.F. Brain protection at the blood-cerebrospinal fluid interface involves a glutathione-dependent metabolic barrier mechanism. J Cereb Blood Flow Metab 26 (2006) 1165-1175
25. Johansson P.A., Dziegielewska K.M., Liddelow S.A., and Saunders N.R. The blood-CSF barrier explained: when development is not immaturity. Bioessays 30 (2008) 237-248
26. Johnson A.K., and Gross P.M. Sensory circumventricular organs and brain homeostatic pathways. Faseb J 7 (1993) 678-686
27. Keep R.F., and Jones H.C. A morphometric study on the development of the lateral ventricle choroid plexus, choroid plexus capillaries and ventricular ependyma in the rat. Brain Res Dev Brain Res 56 (1990) 47-53
28. Khuth S.T., Strazielle N., Giraudon P., Belin M.F., and Ghersi-Egea J.F. Impairment of blood-cerebrospinal fluid barrier properties by retrovirus-activated T lymphocytes: reduction in cerebrospinal fluid-to-blood efflux of prostaglandin E2. J Neurochem 94 (2005) 1580-1593
29. Kusuhara H., and Sugiyama Y. Efflux transport systems for organic anions and cations at the blood-CSF barrier. Adv Drug Deliv Rev 56 (2004) 1741-1763
30. Leggas M., Adachi M., Scheffer G.L., Sun D., Wielinga P., Du G., et al. Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24 (2004) 7612-7621
31. Leslie E.M., Deeley R.G., and Cole S.P. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol Appl Pharmacol 204 (2005) 216-237
32. Lippoldt A., Liebner S., Andbjer B., Kalbacher H., Wolburg H., Haller H., et al. Organization of choroid plexus epithelial and endothelial cell tight junctions and regulation of claudin-1,-2 and -5 expression by protein kinase C. Neuroreport 11 (2000) 1427-1431
33. Loscher W., and Potschka H. Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 6 (2005) 591-602
34. Mercier C., Masseguin C., Roux F., Gabrion J., and Scherrmann J.M. Expression of P-glycoprotein (ABCB1) and Mrp1 (ABCC1) in adult rat brain: focus on astrocytes. Brain Res 1021 (2004) 32-40
35. Millgard K., Milinowska D.H., and Saunders N.R. Lack of correlation between tight junction morphology and permeability properties in developing choroid plexus. Nature 264 (1976) 293-294
36. Mönkkönen K.S., Hakumaki J.M., Hirst R.A., Miettinen R.A., O'Callaghan C., Mannisto P.T., et al. Intracerebroventricular antisense knockdown of G alpha i2 results in ciliary stasis and ventricular dilatation in the rat. BMC Neurosci 8 (2007) 26
37. Mönkkönen K.S., Hirst R.A., Laitinen J.T., and O'Callaghan C. PACAP27 regulates ciliary function in primary cultures of rat brain ependymal cells. Neuropeptides 42 (2008) 633-640
38. Mottino A.D., and Catania V.A. Hepatic drug transporters and nuclear receptors: regulation by therapeutic agents. World J Gastroenterol 14 (2008) 7068-7074
39. Nehlig A. Cerebral energy metabolism, glucose transport and blood flow: changes with maturation and adaptation to hypoglycaemia. Diabetes Metab 23 (1997) 18-29
40. Nehlig A., Pereira de Vasconcelos A., and Boyet S. Postnatal changes in local cerebral blood flow measured by the quantitative autoradiographic [14C]iodoantipyrine technique in freely moving rats. J Cereb Blood Flow Metab 9 (1989) 579-588
41. Pardridge W.M. Advances in cell biology of blood-brain barrier transport. Semin Cell Biol 2 (1991) 419-426
42. Petito C.K., and Adkins B. Choroid plexus selectively accumulates T-lymphocytes in normal controls and after peripheral immune activation. J Neuroimmunol 162 (2005) 19-27
43. Philbert M.A., Beiswanger C.M., Manson M.M., Green J.A., Novak R.F., Primiano T., et al. Glutathione S-transferases and gamma-glutamyl transpeptidase in the rat nervous systems: a basis for differential susceptibility to neurotoxicants. Neurotoxicology 16 (1995) 349-362
44. Rampon C., Weiss N., Deboux C., Chaverot N., Miller F., Buchet D., et al. Molecular mechanism of systemic delivery of neural precursor cells to the brain: assembly of brain endothelial apical cups and control of transmigration by CD44. Stem Cells 26 (2008) 1673-1682
45. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., et al. C-C chemokine receptor 6-regulated entry of T(H)-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat Immunol 22 (2009) 22
46. Regina A., Demeule M., Laplante A., Jodoin J., Dagenais C., Berthelet F., et al. Multidrug resistance in brain tumors: roles of the blood-brain barrier. Cancer Metastasis Rev 20 (2001) 13-25
47. Robey R.W., Lazarowski A., and Bates S.E. P-glycoprotein-a clinical target in drug-refractory epilepsy?. Mol Pharmacol 73 (2008) 1343-1346
48. Saunders N.R., Habgood M.D., and Dziegielewska K.M. Barrier mechanisms in the brain. II. Immature brain. Clin Exp Pharmacol Physiol 26 (1999) 85-91
49. Schinkel A.H., and Jonker J.W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55 (2003) 3-29
50. Schinkel A.H., Wagenaar E., Mol C.A., and van Deemter L. P-glycoprotein in the blood-brain barrier of mice influences the brain penetration and pharmacological activity of many drugs. J Clin Invest 97 (1996) 2517-2524
51. Schumacher U., and Mollgard K. The multidrug-resistance P-glycoprotein (Pgp, MDR1) is an early marker of blood-brain barrier development in the microvessels of the developing human brain. Histochem Cell Biol 108 (1997) 179-182
52. Shen D.D., Artru A.A., and Adkison K.K. Principles and applicability of CSF sampling for the assessment of CNS drug delivery and pharmacodynamics. Adv Drug Deliv Rev 56 (2004) 1825-1857
53. Spudich A., Kilic E., Xing H., Kilic U., Rentsch K.M., Wunderli-Allenspach H., et al. Inhibition of multidrug resistance transporter-1 facilitates neuroprotective therapies after focal cerebral ischemia. Nat Neurosci 9 (2006) 487-488
54. Staud F., and Pavek P. Breast cancer resistance protein (BCRP/ABCG2). Int J Biochem Cell Biol 37 (2005) 720-725
55. Strazielle N., Belin M.F., and Ghersi-Egea J.F. Choroid plexus controls brain availability of anti-HIV nucleoside analogs via pharmacologically inhibitable organic anion transporters. Aids 17 (2003) 1473-1485
56. Strazielle N., and Ghersi-Egea J.F. Demonstration of a coupled metabolism-efflux process at the choroid plexus as a mechanism of brain protection toward xenobiotics. J Neurosci 19 (1999) 6275-6289
57. Strazielle N., and Ghersi-Egea J.F. Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol 59 (2000) 561-574
58. Strazielle N., and Ghersi-Egea J.F. Factors affecting delivery of antiviral drugs to the brain. Rev Med Virol 15 (2005) 105-133
59. Strazielle N., Khuth S.T., and Ghersi-Egea J.F. Detoxification systems, passive and specific transport for drugs at th blood-CSF barrier in normal and pathological situations. Adv Drug Deliv Rev 56 (2004) 1717-1740
60. Strazielle N., Mutin M., and Ghersi-Egea J.F. The choroid plexuses: a dynamic interface between the blood and the cerebrospinal fluid. Morphologie 89 (2005) 90-101
61. Szmydynger-Chodobska J., Strazielle N., Zink B.J., Ghersi-Egea J.F., and Chodobski A. The role of the choroid plexus in neutrophil invasion after traumatic brain injury. J Cereb Blood Flow Metab 29 (2009) 1503-1516
62. Varatharajan L., and Thomas S.A. The transport of anti-HIV drugs across blood-CNS interfaces: Summary of current knowledge and recommendations for further research. Antiviral Res 25 (2009) 25
63. Virgintino D., Errede M., Girolamo F., Capobianco C., Robertson D., Vimercati A., et al. Fetal blood-brain barrier P-glycoprotein contributes to brain protection during human development. J Neuropathol Exp Neurol 67 (2008) 50-61
64. Vorbrodt A.W., Dobrogowska D.H., and Tarnawski M. Immunogold study of interendothelial junction-associated and glucose transporter proteins during postnatal maturation of the mouse blood-brain barrier. J Neurocytol 30 (2001) 705-716
65. Wijnholds J., deLange E.C., Scheffer G.L., van den Berg D.J., Mol C.A., van der Valk M., et al. Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier. J Clin Invest 105 (2000) 279-285
66. Wolburg H., Wolburg-Buchholz K., Kraus J., Rascher-Eggstein G., Liebner S., Hamm S., et al. Localization of claudin-3 in tight junctions of the blood-brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol (Berl) 105 (2003) 586-592