Multi-disciplinary research approaches on the brain barrier transport system, a dynamic interface

Brain and Nerve

Volumn 65, Issue 2, 2013, Pages 121-136

  Tachikawa, Masanori ^a   Uchida, Yasuo ^a   Terasaki, Tetsuya ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Blood brain barrier; Blood cerebrospinal fluid barrier; Drug delivery; Quantitative targeted absolute proteomics; Transporter

Indexed keywords

ABC TRANSPORTER; AMYLOID BETA PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CARRIER PROTEIN; CENTRAL NERVOUS SYSTEM AGENTS; LAT1 PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 4; ORGANIC CATION TRANSPORTER; PROSTAGLANDIN; SLC7A5 PROTEIN; UNCLASSIFIED DRUG;

BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM DISEASE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG TARGETING; HUMAN; IN VIVO STUDY; MEDICAL RESEARCH; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; PROTEIN EXPRESSION; PROTEOMICS; REVIEW;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CENTRAL NERVOUS SYSTEM AGENTS; DRUG DISCOVERY; HUMANS; MEMBRANE TRANSPORT PROTEINS;

EID: 84874618154     PISSN: 18816096     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (72)

1. Kamiie J, Ohtsuki S, Iwase R, Ohmine K, Katsukura Y, et al: Quantitative atlas of membrane transporter proteins: development and application of a highly sensitive simultaneous LC/MS/MS method combined with novel in-silico peptide selection criteria. Pharm Res 25: 1469-1483, 2008
2. Ito K, Uchida Y, Ohtsuki S, Aizawa S, Kawakami H, et al: Quantitative membrane protein expression at the blood-brain barrier of adult and younger cynomolgus monkeys. J Pharm Sci 100: 3939-3950, 2011
3. Uchida Y, Ohtsuki S, Katsukura Y, Ikeda C, Suzuki T, et al: Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. J Neurochem 117: 333-345, 2011
4. Agus DB, Gambhir SS, Pardridge WM, Spielholz C, Baselga J, et al: Vitamin C crosses the blood-brain barrier in the oxidized form through the glucose transporters. J Clin Invest 100: 2842-2848, 1997 (Pubitemid 28007554)
5. Janigro D: Blood-brain barrier, ion homeostatis and epilepsy: possible implications towards the understanding of ketogenic diet mechanisms. Epilepsy Res 37: 223-232, 1999
6. Lauritzen F, de Lanerolle NC, Lee TS, Spencer DD, Kim JH, et al: Monocarboxylate transporter 1 is deficient on microvessels in the human epileptogenic hippocampus. Neurobiol Dis 41: 577-584, 2011
7. Kang YS, Terasaki T, Tsuji A: Acidic drug transport in vivo through the blood-brain barrier: a role of the transport carrier for monocarboxylic acids. J Pharmacobiodyn 13: 158-163, 1990 (Pubitemid 20165387)
8. Kageyama T, Nakamura M, Matsuo A, Yamasaki Y, Takakura Y, et al: The 4F2hc/LAT1 complex transports L-DOPA across the blood-brain barrier. Brain Res 879: 115-121, 2000
9. Gomes P, Soares-da-Silva P: L-DOPA transport properties in an immortalised cell line of rat capillary cerebral endothelial cells, RBE 4. Brain Res 829: 143-150, 1999 (Pubitemid 29251694)
10. Abbott NJ, Romero IA: Transporting therapeutics across the blood-brain barrier. Mol Med Today 2:106-113, 1996 (Pubitemid 126407728)
11. Peura L, Malmioja K, Laine K, Leppanen J, Gynther M, et al: Large amino acid transporter 1 (LAT1) prodrugs of valproic acid: new prodrug design ideas for central nervous system delivery. Mol Pharm 8: 1857-1866, 2011
12. Gynther M, Laine K, Ropponen J, Leppanen J, Mannila A, et al: Large neutral amino acid transporter enables brain drug delivery via prodrugs. J Med Chem 51: 932-936, 2008 (Pubitemid 351304700)
13. Gynther M, Jalkanen A, Lehtonen M, Forsberg M, Laine K, et al: Brain uptake of ketoprofen-lysine prodrug in rats. Int J Pharm 399: 121-128, 2010
14. del Amo EM, Urtti A, Yliperttula M: Pharmacokinetic role of L-type amino acid transporters LAT1 and LAT2. Eur J Pharm Sci 35: 161-174, 2008
15. de Vries NA, Zhao J, Kroon E, Buckle T, Beijnen JH, et al: P-glycoprotein and breast cancer resistance protein: two dominant transporters working together in limiting the brain penetration of topotecan. Clin Cancer Res 13: 6440-6449, 2007 (Pubitemid 350075034)
16. Polli JW, Olson KL, Chism JP, John-Williams LS, Yeager RL, et al: An unexpected synergist role of P-glycoprotein and breast cancer resistance protein on the central nervous system penetration of the tyrosine kinase inhibitor lapatinib (N-{3-chloro-4-[(3-fluorobenzyl)oxy]phenyl}-6-[5-({[2-(methylsulfonyl) ethyl] amino}methyl)-2-furyl]-4-quinazolinamine; GW572016). Drug Metab Dispos 37: 439-442, 2009
17. Kodaira H, Kusuhara H, Ushiki J, Fuse E, Sugiyama Y: Kinetic analysis of the cooperation of P-glycoprotein (P-gp/Abcb1) and breast cancer resistance protein (Bcrp/Abcg2) in limiting the brain and testis penetration of erlotinib, flavopiridol, and mitoxantrone. J Pharmacol Exp Ther 333: 788-796, 2010
18. Tega Y, Akanuma SI, Kubo Y, Terasaki T, Hosoya KI: Blood-to-brain influx transport of nicotine at the rat blood-brain barrier: involvement of a pyrilamine-sensitive organic cation transport process. Neurochem Int (in press)
19. Cisternino S, Chapy H, Andre P, Smirnova M, Debray M, et al: Coexistence of passive and proton antiporter-mediated processes in nicotine transport at the mouse blood-brain barrier. AAPS J, 2012 Dec 5 [Epub ahead of print]
20. André P, Debray M, Scherrmann JM, Cisternino S: Clonidine transport at the mouse blood-brain barrier by a new H+ antiporter that interacts with addictive drugs. J Cereb Blood Flow Metab 29: 1293-1304, 2009
21. Okura T, Hattori A, Takano Y, Sato T, Hammarlund-Udenaes M, et al: Involvement of the pyrilamine transporter, a putative organic cation transporter, in blood-brain barrier transport of oxycodone. Drug Metab Dispos 36: 2005-2013, 2008
22. Kubo Y, Kusagawa Y, Tachikawa M, Akanuma SI, Hosoya KI: Involvement of a novel organic cation transporter in verapamil transport across the inner blood-retinal barrier. Pharm Res, 2012 Nov 22 [Epub ahead of print]
23. Bostrom E, Simonsson US, Hammarlund-Udenaes M: In vivo blood-brain barrier transport of oxycodone in the rat: indications for active influx and implications for pharmacokinetics/pharmacodynamics. Drug Metab Dispos 34: 1624-1631, 2006 (Pubitemid 44285405)
24. Yanai K, Tashiro M: The physiological and pathophysiological roles of neuronal histamine: an insight from human positron emission tomography studies. Pharmacol Ther 113: 1-15, 2007 (Pubitemid 44969926)
25. Yamazaki M, Terasaki T, Yoshioka K, Nagata O, Kato H, et al: Carrier-mediated transport of H1-antagonist at the blood-brain barrier: a common transport system of H1-antagonists and lipophilic basic drugs. Pharm Res 11: 1516-1518, 1994 (Pubitemid 24339666)
26. Akanuma S, Hosoya K, Ito S, Tachikawa M, Terasaki T, et al: Involvement of multidrug resistance-associated protein 4 in efflux transport of prostaglandin E (2) across mouse blood-brain barrier and its inhibition by intravenous administration of cephalosporins. J Pharmacol Exp Ther 333: 912-919, 2010
27. Akanuma S, Uchida Y, Ohtsuki S, Kamiie J, Tachikawa M, et al: Molecular-weight-dependent, anionic-substrate-preferential transport of beta-lactam antibiotics via multidrug resistance-associated protein 4. Drug Metab Pharmacokinet 26: 602-611, 2011
28. Tachikawa M, Ozeki G, Higuchi T, Akanuma S, Tsuji K, et al: Role of the blood-cerebrospinal fluid barrier transporter as a cerebral clearance system for prostaglandin E (2) produced in the brain. J Neurochem 123: 750-760, 2012
29. Akanuma S, Uchida Y, Ohtsuki S, Tachikawa M, Terasaki T, et al: Attenuation of prostaglandin E2 elimination across the mouse blood-brain barrier in lipopolysaccharide-induced inflammation and additive inhibitory effect of cefmetazole. Fluids Barriers CNS 8: 24, 2011
30. Huang ZL, Urade Y, Hayaishi O: Prostaglandins and adenosine in the regulation of sleep and wakefulness. Curr Opin Pharmacol 7: 33-38, 2007 (Pubitemid 46238038)
31. Tachikawa M, Tsuji K, Yokoyama R, Higuchi T, Ozeki G, et al: A clearance system for prostaglandin D2, a sleep-promoting factor, in cerebrospinal fluid: role of the blood-cerebrospinal barrier transporters. J Pharmacol Exp Ther 343: 608-616, 2012
32. Egleton RD, Abbruscato TJ, Thomas SA, Davis TP: Transport of opioid peptides into the central nervous system. J Pharm Sci 87: 1433-1439, 1998 (Pubitemid 28514153)
33. Gao B, Hagenbuch B, Kullak-Ublick GA, Benke D, Aguzzi A, et al: Organic anion-transporting polypeptides mediate transport of opioid peptides across blood-brain barrier. J Pharmacol Exp Ther 294: 73-79, 2000 (Pubitemid 30434672)
34. Dagenais C, Ducharme J, Pollack GM: Uptake and efflux of the peptidic delta-opioid receptor agonist. Neurosci Lett 301: 155-158, 2001
35. Ito S, Ohtsuki S, Katsukura Y, Funaki M, Koitabashi Y, et al: Atrial natriuretic peptide is eliminated from the brain by natriuretic peptide receptor-C-mediated brain-to-blood efflux transport at the blood-brain barrier. J Cereb Blood Flow Metab 31: 457-466, 2011
36. Shibata M, Yamada S, Kumar SR, Calero M, Bading J, et al: Clearance of Alzheimer's amyloid-ss (1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106:1489-1499, 2000 (Pubitemid 32038587)
37. Cirrito JR, Deane R, Fagan AM, Spinner ML, Parsadanian M, et al: P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model. J Clin Invest 115: 3285-3290, 2005 (Pubitemid 41567593)
38. Xiong H, Callaghan D, Jones A, Bai J, Rasquinha I, et al: ABCG2 is upregulated in Alzheimer's brain with cerebral amyloid angiopathy and may act as a gatekeeper at the blood-brain barrier for Abeta (1-40) peptides. J Neurosci 29: 5463-5475, 2009
39. Fitz NF, Cronican AA, Saleem M, Fauq AH, Chapman R, et al: Abcal deficiency affects Alzheimer's diseaselike phenotype in human ApoE4 but not in ApoE3-targeted replacement mice. J Neurosci 32: 13125-13136, 2012
40. Fujiyoshi M, Tachikawa M, Ohtsuki S, Ito S, Uchida Y, et al: Amyloid-beta peptide (1-40) elimination from cerebrospinal fluid involves low-density lipoprotein receptor-related protein 1 at the blood-cerebrospinal fluid barrier. J Neurochem 118: 407-415, 2011
41. Ito S, Ueno T, Ohtsuki S, Terasaki T: Lack of brain-to-blood efflux transport activity of low-density lipoprotein receptor-related protein-1 (LRP-1) for amyloid-beta peptide (1-40) in mouse: involvement of an LRP-1-independent pathway. J neurochem 113: 1356-1363, 2010
42. Akanuma S, Ohtsuki S, Doi Y, Tachikawa M, Ito S, et al: ATP-binding cassette transporter Al (ABCA1) deficiency does not attenuate the brain-to-blood efflux transport of human amyloid-beta peptide (1-40) at the blood-brain barrier. Neurochem Int 52: 956-961, 2008
43. Ito S, Ohtsuki S, Nezu Y, Koitabashi Y, Murata S, et al: 1 alpha,25-Dihydroxyvitamin D3 enhances cerebral clearance of human amyloid-beta peptide (1-40) from mouse brain across the blood-brain barrier. Fluids Barriers CNS 8: 20, 2011
44. Kasai Y, Tachikawa M, Hirose S, Akanuma S, Hosoya K: Transport systems of serine at the brain barriers and in brain parenchymal cells. J Neurochem 118: 304-313, 2011
45. Hiramatsu M: A role for guanidino compounds in the brain. Mol Cell Biochem 244: 57-62, 2003
46. Tachikawa M, Fujinawa J, Takahashi M, Kasai Y, Fukaya M, et al: Expression and possible role of creatine transporter in the brain and at the blood-cerebrospinal fluid barrier as a transporting protein of guanidinoacetate, an endogenous convulsant. J Neurochem 107: 768-778, 2008
47. Tachikawa M, Kasai Y, Yokoyama R, Fujinawa J, Ganapathy V, et al: The blood-brain barrier transport and cerebral distribution of guanidinoacetate in rats: involvement of creatine and taurine transporters. J Neurochem 111: 499-509, 2009
48. Tachikawa M, Kasai Y, Takahashi M, Fujinawa J, Kitaichi K, et al: The blood-cerebrospinal fluid barrier is a major pathway of cerebral creatinine clearance: involvement of transporter-mediated process. J Neurochem 107: 432-442, 2008
49. Feldmann M, Koepp M: P-glycoprotein imaging in temporal lobe epilepsy: in vivo PET experiments with the Pgp substrate [11C]-verapamil. Epilepsia 53: 60-63, 2012
50. Zibell G, Unkruer B, Pekcec A, Hartz AM, Bauer B, et al: Prevention of seizure-induced up-regulation of endothelial P-glycoprotein by COX-2 inhibition. Neuropharmacology 56: 849-855, 2009
51. Cannon RE, Peart JC, Hawkins BT, Campos CR, Miller DS: Targeting blood-brain barrier sphingolipid signaling reduces basal P-glycoprotein activity and improves drug delivery to the brain. Proc Natl Acad Sci U S A 109: 15930-15935, 2012
52. Takashima T, Yokoyama C, Mizuma H, Yamanaka H, Wada Y, et al: Developmental changes in P-glycoprotein function in the blood-brain barrier of nonhuman primates: PET study with R-11C-verapamil and 11C-oseltamivir. J Nucl Med 52: 950-957, 2011
53. Weksler BB, Subileau EA, Perrieere N, Chameau P, Holloway K, et al: Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 19: 1872-1874, 2005 (Pubitemid 41598779)
54. Ohtsuki S, Ikeda C, Uchida Y, Sakamoto Y, Miller F, et al: Quantitative targeted absolute proteomic analysis of transporters, receptors and junction proteins for validation of human cerebral microvascular endothelial cell line hCMEC/D3 as a human blood-brain barrier model. Mol Pharm 10: 289-296, 2013
55. Lippmann ES, Azarin SM, Kay JE, Nessler RA, Wilson HK, et al: Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol 30: 783-791, 2012
56. Uchida Y, Ohtsuki S, Kamiie J, Terasaki T: Blood-brain barrier (BBB) pharmacoproteomics: reconstruction of in vivo brain distribution of 11 P-glycoprotein substrates based on the BBB transporter protein concentration, in vitro intrinsic transport activity, and unbound fraction in plasma and brain in mice. J Pharmacol Exp Ther 339: 579-588, 2011
57. Ohtsuki S, Uchida Y, Kubo Y, Terasaki T: Quantitative targeted absolute proteomics-based ADME research as a new path to drug discovery and development: methodology, advantages, strategy, and prospects. J Pharm Sci 100: 3547-3559, 2011
58. Farrell CL, Pardridge WM: Ultrastructural localization of blood-brain barrier-specific antibodies using immunogold-silver enhancement techniques. J Neurosci Methods 37: 103-110, 1991
59. Gerhart DZ, Enerson BE, Zhdankina OY, Leino RL, Drewes LR: Expression of monocarboxylate transporter MCT1 by brain endothelium and glia in adult and suckling rats. Am J Physiol 273: E207-E213, 1997
60. Tsuji A, Terasaki T, Takabatake Y, Tenda Y, Tamai I, et al: P-glycoprotein as the drug efflux pump in primary cultured bovine brain capillary endothelial cells. Life Sci 51: 1427-1437, 1992
61. Cooray HC, Blackmore CG, Maskell L, Barrand MA: Localisation of breast cancer resistance protein in microvessel endothelium of human brain. Neuroreport 13: 2059-2063, 2002 (Pubitemid 36005925)
62. Hori S, Ohtsuki S, Tachikawa M, Kimura N, Kondo T, et al: Functional expression of rat ABCG2 on the luminal side of brain capillaries and its enhancement by astrocyte-derived soluble factor(s). J Neurochem 90: 526-536, 2004 (Pubitemid 38989383)
63. Leggas M, Adachi M, Scheffer GL, Sun D, Wielinga P, et al: Mrp4 confers resistance to topotecan and protects the brain from chemotherapy. Mol Cell Biol 24: 7612-7621, 2004 (Pubitemid 39121487)
64. Mori S, Takanaga H, Ohtsuki S, Deguchi T, Kang YS, et al: Rat organic anion transporter 3 (rOAT3) is responsible for brain-to-blood efflux of homovanillic acid at the abluminal membrane of brain capillary endothelial cells. J Cereb Blood Flow Metab 23: 432-440, 2003 (Pubitemid 36403025)
65. Gao B, Stieger B, Noe B, Fritschy JM, Meier PJ: Localization of the organic anion transporting polypeptide 2 (Oatp2) in capillary endothelium and choroid plexus epithelium of rat brain. T J Histochem Cytochem 47: 1255-1264, 1999
66. Tetsuka K, Takanaga H, Ohtsuki S, Hosoya K, Terasaki T: The 1-isomer-selective transport of aspartic acid is mediated by ASCT2 at the blood-brain barrier. J Neurochem 87: 891-901, 2003 (Pubitemid 37444565)
67. Yamazaki M, Fukuoka H, Nagata O, Kato H, Ito Y, et al: Transport mechanism of an H1-antagonist at the blood-brain barrier: transport mechanism of mepyramine using the carotid injection technique. Biol Pharm Bull 17: 676-679, 1994 (Pubitemid 24186116)
68. Smith QR, Takasato Y, Rapoport SI: Kinetic analysis of L-leucine transport across the blood-brain barrier. Brain Res 311: 167-170, 1984 (Pubitemid 14020814)
69. Smith QR, Momma S, Aoyagi M, Rapoport SI: Kinetics of neutral amino acid transport across the blood-brain barrier. Brain Res 311: 167-170, 1984 (Pubitemid 14020814)
70. Wade LA, Katzman R: Synthetic amino acids and the nature of L-DOPA transport at the blood-brain barrier. J Neurochem 25: 837-842, 1975
71. Pardridge WM: Recent advances in blood-brain barrier transport. Annu Rev Pharmacol Toxicol 28: 25-39, 1988
72. Ito S, Ohtsuki S, Terasaki T: Functional characterization of the brain-to-blood efflux clearance of human amyloid-beta peptide (1-40) across the rat blood-brain barrier. Neurosci Res 56: 246-252, 2006 (Pubitemid 44572534)