The inner blood-retinal barrier molecular structure and transport biology

Advances in Experimental Medicine and Biology

Volumn 763, Issue , 2013, Pages 85-104

  Hosoya, Ken Ichi ^a   Tachikawa, Masanori ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLTETRAHYDROFOLIC ACID; AMINO ACID TRANSPORTER; CARNITINE TRANSPORTER 2; CARRIER PROTEIN; CATENIN; CHOLINE; CLAUDIN; CREATINE; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 2; FIBROBLAST GROWTH FACTOR 2; FOLIC ACID; GLUCOSE TRANSPORTER 1; GLYCINE TRANSPORTER 1; INTERLEUKIN 6; JUNCTIONAL ADHESION MOLECULE; L TYPE AMINO ACID TRANSPORTER 1; LYSOPHOSPHATIDIC ACID; NITRIC OXIDE; OCCLUDIN; REACTIVE OXYGEN METABOLITE; REDUCED FOLATE CARRIER; SCAVENGER RECEPTOR BI; SODIUM DEPENDENT MULTIVITAMIN TRANSPORTER; SPHINGOSINE 1 PHOSPHATE; TAURINE TRANSPORTER; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; ZONULA OCCLUDENS PROTEIN;

ACTIVE TRANSPORT; ARTICLE; ASTROCYTE; BLOOD RETINA BARRIER; CAPILLARY ENDOTHELIAL CELL; CELL FUNCTION; CELL JUNCTION; DIFFUSION; ENDOCYTOSIS; GLIA CELL; HUMAN; MUELLER CELL; NONHUMAN; PASSIVE TRANSPORT; PERICYTE; PRIORITY JOURNAL; RETINA NERVE CELL; TIGHT JUNCTION;

EID: 84934439739     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-4711-5_4     Document Type: Article

References (106)

1. Cunha-Vaz JG. The blood-retinal barriers system. Basic concepts and clinical evaluation. Exp Eye Res 2004; 78:715-721
2. Hosoya K, Tomi M. Advances in the cell biology of transport via the inner blood-retinal barrier: Establishment of cc1llincs and transport functions. BioI Pharm Bu112005; 28: 1-8
3. Schnaudigel O. Die vitale farbung mit trypanblau an auge. Graefe Arch Ophthal 1913; 86:93-105
4. Kim JR, Kim JH, Park JA, et al. Blood-neural barrier: Intercellular communication at glio-vascular interface. J Biochcm Mol BioI 2006; 39:339-345
5. Janzer RC, Raff MC. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 1987; 325:253-257
6. Janzer RC. The blood-brain barrier: Cellular basis. J Inherit Metab Dis 1993; 16:639-647
7. Gardner TW, Lieth E, Khin SA, et al. Astrocytes increase barrier properties and ZO-I expression in retinal vascular endothelial cells. Invest Ophthalmol Vis Sci 1997; 38:2423-2427
8. Tout S, Chan-Ling T, Hollander H, et al. The role of Muller cells in the formation ofthe blood-retinal barrier. Neuroscience 1993; 55:291-30 I.
9. Abukawa H, Tomi M, Kiyokawa J, et al. Modulation of retinal capillary endothelial cells by Muller glial cell-derived factors. Mol Vis 2009; 15:451-457
10. Abbott NJ. Astrocyte-endothelial interactions and blood-brain barrier permeability. J Anat 2002; 200: 629-638
11. Hori S, Ohtsuki S, Hosoya K, et al. A pericyte-derived angiopoietin-I multimeric complex induces occ1udin gene expression in brain capillary endothelial cells through Tie-2 activation in vitro. JNeurochem 2004; 89:503-513
12. Bandopadhyay R, Orte C, Lawrenson JG, et al. Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. J Neurocytol2001; 30:35-44
13. Matsugi T, Chen Q, Anderson DR. Contractile responses of cultured bovine retinal pericytes to angiotensin II. Arch Ophthalmol1997; 115:1281-1285
14. Chen Q, Anderson DR. Effect of CO, on intracellular pH and contraction of retinal capillary pericytes. Invest Ophthalmol Vis Sci 1997; 38:643-651
15. Matsugi T, Chen Q, Anderson DR. Adenosine-induced relaxation of cultured bovine retinal pericytes. Invest Ophthalmol Vis Sci 1997; 38:2695-2701
16. Hirase T, Staddon JM, Saitou M, et al. Occ1udin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 1997; 110: 1603-1613
17. Furuse M, Fujita K, Hiiragi T, et al. Claudin-I and-2: Novel integral membrane proteins localizing at tight junctions with no sequence similarity to oceludin. J Cell BioI 1998; 141: 1539-1550
18. Bazzoni G, Tonetti P, Manzi L, et al. Expression of junctional adhesion molecule-A prevents spontaneous and random motility. J Cell Sci 2005; 118:623-632
19. Tomi M, Hosoya K. Application of magnetically isolated rat retinal vascular endothelial cells for the determination of transporter gene expression levels at the inner blood-retinal barrier. J Neurochem 2004; 91:1244-1248
20. Tachikawa M, Toki H, Tomi M, et al. Gene expression profiles of ATP-binding cassette transporter A and C subfamilies in mouse retinal vascular endothelial cells. Microvasc Res 2008; 75:68-72
21. Anderson JM, Fanning AS, Lapierre L, et al. Zonula occ1udens (ZO)-I and ZO-2: Membrane-Associated guanylate kinase homologues (MAGuKs) of the tight junction. Biochem Soc Trans 1995; 23:470-475
22. Haskins J, Gu L, Wittchen ES, et al. ZO-3, a novel member of the MAG UK protein family found at the tight junction, interacts with ZO-I and occ1udin. J Cell BioI 1998; 141: 199-208
23. Bazzoni G, Dejana E. Endothelial cell-To-cell junctions: Molecular organization and role in vascular homeostasis. Physiol Rev 2004; 84:869-901
24. Wolburg H, Noell S, Mack A, et al. Brain endothelial cells and the glio-vascular complex. Cell Tissue Res 2009; 335:75-96
25. Kevil CG, Okayama N, Trocha SD, et al. Expression of zonula occ1udens and adherens junctional proteins in human venous and arterial endothelial cells: Role of occludin in endothelial solute barriers. Microcirculation 1998; 5:197-210
26. Antonetti DA, Barber AJ, Khin S, et al. Vascular permeability in experimental diabetes is associated with reduced endothelial occ1udin content: Vascular endothelial growth factor decreases occ1udin in retinal endothelial cells. Diabetes 1998; 47: 1953-1959
27. Yaccino JA, Chang YS, Hollis TM, et al. Physiological transport properties of cultured retinal microvascular endothelial cell monolayers. CurrEye Res 1997; 16:761-768
28. Mark KS, Burroughs AR, Brown RC, et al. Nitric oxide mediates hypoxia-induced changes in paracellular permeability of cerebral microvasculature. Am J Physiol Heart Circ Physiol 2004; 286:HI74-180
29. Kaur C, Sivakumar V, Foulds WS. Early response of neurons and glial cells to hypoxia in the retina. Invest Ophthalmol Vis Sci 2006; 47:1126-1141
30. Augustin AJ, Breipohl W, Boker T, et al.Increased lipid peroxide levels andmyeloperoxidase activity in the vitreous of patients suffering from proliferative diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 1993; 231:647-650
31. Saugstad OD, Rognum TO. High postmortem levels of hypoxanthine in the vitreous humor of premature babies with respiratory distress syndrome. Pediatrics 1988; 81:395-398
32. KaurC, Foulds WS, Ling EA. Blood-retinal barrier in hypoxic ischaemic conditions: Basic concepts, clinical features and management. Prog Retin Eye Res 2008; 27:622-647
33. Niemeyer G. Glucose concentration and retinal function. Clin Neurisci 1997; 4:327-335
34. Tachikawa M, Hosoya K, Ohtsuki S, et al. A novel relationship between creatine transport at the blood-brain and blood-retinal barriers, creatine biosynthesis and its use for brain and retinal energy homeostasis. Subcell Biochem 2007; 46:83-98
35. Hosoya K, Tachikawa M. Inner blood-retinal barrier transporters: Role ofretinal drug delivery. Pharm Res 2009; 26:2055-2065
36. Hosoya K, Tomi M. Inner blood-retinal barrier: Transport biology and methodology. In: Ehrhardt C, Kim KJ, eds. Drug Absorption Studies-In Situ, In Vitro and In Silico Models, New York: AAPS Press-Springer, 2008:321-338
37. Hosoya K, Tomi M, Ohtsuki S, et al. Conditionally immortalized retinal capillary endothelial cell lines (TR-iBRB) expressing differentiated endothelial cell functions derived from a transgenic rat. Exp Eye Res 2001; 72:163-172
38. Vera JC, Rivas CI, Fischbarg J, et al. Mammalian facilitative hexose transporters mediate the transport of dehydroascorbic acid. Nature 1993; 364:79-82
39. Takata K, Kasahara T, Kasahara M, et al. Ultracytochemicallocalization of the erythrocyte/HepG2-Type glucose transporter (GLUTl) in cells of the blood-retinal barrier in the rat. Invest Ophthalmol Vis Sci 1992; 33:377-383
40. Fernandes R, Suzuki K, Kumagai AK. Inner blood-retinal barrier GLUTl in long-Term diabetic rats: An immunogold electron microscopic study. Invest Ophthalmol Vis Sci 2003; 44:3150-3154
41. Puchowicz MA, Xu K, Magness D, et al. Comparison of glucose influx and blood flow in retina and brain of diabetic rats. J Cereb Blood Flow Metab 2004; 24:449-457
42. Hosoya K, Minamizono A, KatayamaK, et al. Vitamin C transport in oxidized form across the rat blood-retinal barrier. Invest Ophthalmol Vis Sci 2004; 45: 1232-1239
43. Hosoya K, Nakamura G, Akanuma S, et al. Dehydroascorbic acid uptake and intracellular ascorbic acid accumulation in cultured Muller glial cells (TR-MUL). Neurochem Int 2008; 52: 1351-1357
44. Ennis SR, Johnson JE, Pautler EL. In situ kinetics of glucose transport across the blood-retinal barrier in normal rats and rats with streptozocin-induced diabetes. Invest Ophthalmol Vis Sci 1982; 23:447-456
45. Minamizono A, Tomi M, HosoyaK.Inhibition of dehydroascorbic acid transport across the rat blood-retinal and-brain barriers in experimental diabetes. Bioi Pharm Bull 2006; 29:2148-2150
46. Nagase K, Tomi M, Tachikawa M, et al. Functional and molecular characterization of adenosine transport at the rat inner blood-retinal barrier. Biochim Biophys Acta 2006; 1758: 13-19
47. Baldwin SA, Beal PR, Yao SY, et al. The equilibrative nueleoside transporter family, SLC29. Pflugers Arch 2004; 447:735-743
48. Yao SY, Ng AM, Sundaram M, et al. Transport of antiviral 3'-deoxy-nuc1eoside drugs by recombinant human and rat equilibrative, nitrobenzylthioinosine (NBMPR)-insensitive (ENT2) nucleoside transporter proteins produced in Xenopus oocytes. Mol Membr BioI 2001 ; 18: 161-167
49. Tomi M, Kitade N, Hirose S, et al. Cationic amino acid transporter I-mediated L-Arginine transport at the inner blood-retinal barrier. J Neurochem 2009; 111 :716-725
50. TomquistP, Aim A. Carrier-mediated transport of amino acids through the blood-retinal and the blood-brain barriers. Gracfes Arch Clin Exp Ophthalmol1986; 224:21-25
51. Lin CT, Song GX, Wu JY. Ultrastructural demonstration ofL-glutamate decarboxylase andcysteinesulfinic acid decarboxylase in rat retina by immunocytochemistry. Brain Res 1985; 331:71-80
52. Tomi M, Terayama T, Isobe T, et al. Function and regulation of taurine transport at the inner blood-retinal barrier. Microvasc Res 2007; 73:100-106
53. Tomi M, TajimaA, TachikawaM, et al. Function oftaurine transporter (Slc6a6/TauT) asaGABA transporting protein and its relevance to GABA transport in rat retinal capillary endothelial cells. Biochim Biophys Acta 2008; 1778:2138-2142
54. Tomi M, Mori M, Tachikawa M, et al. L-Type amino acid transporter I-mediated L-leucine transport at the inner blood-retinal barrier. Invest Ophthalmol Vis Sci 2005; 46:2522-2530
55. Kageyama T, Nakamura M, Matsuo A, et al. The 4F2hc/LATl complex transports L-DOPA across the blood-brain barrier. Brain Res 2000; 879: 115-121
56. Bodis-Wollner I. Visual electrophysiology in Parkinson's disease: PERG, VEP and visual P300. Clin Electroencephalogr 1997; 28: 143-147
57. Bhaskar P A, Vanchilingam S, Bhaskar EA, et al. Effect of L-dopa on visual evoked potential in patients with Parkinson's disease. Neurology 1986; 36:1119-1121
58. Hosoya K, Yamamoto A, Akanuma S, et al. Lipophilicity and transporter Influence on blood-retinal barrier penneability: A comparison with blood-brain barrier penneability. Pharm Res in press;doi 10.10071 s11095.010.0272
59. Hosoya K, Kyoko H, Toyooka N, et al. Evaluation of amino acid-mustard transport as L-Type amino acid transporter I (LATl)-mediated alkylating agents. BioI Pharm Bull 2008; 31:2126-2130
60. Tomi M, Hosoya K, Takanaga H, et al. Induction ofxCT gene expression and L-eystine transport activity by diethyl maleate at the inner blood-retinal barrier. Invest Ophthalmol Vis Sci 2002; 43:774-779
61. Hosoya K, Saeki S, Terasaki T. Activation of carrier-mediated transport of L-eystine at the blood-brain and blood-retinal barriers in vivo. Mierovase Res 2001; 62:136-142
62. Okamoto M, Akanuma S, Taehikawa M, et al. Characteristics of glycine transport across the inner blood-retinal barrier. Neuroehem Int 2009; 55:789-795
63. TaehikawaM, Takeda Y, Tomi M, et al. InvolvementofOCTN2 in the transportofaeetyl-L-eamitine across the inner blood-retinal barrier. Invest Ophthalmol Vis Sci 2010; 51 :430-436
64. Nakashima T, Tomi M, Katayama K, et al. Blood-To-retina transport of creatine via creatine transporter (CRT) at the rat inner blood-retinal barrier. J Neuroehem 2004; 89: 1454-1461
65. Nakashima T, Tomi M, Taehikawa M, et al. Evidence for creatine biosynthesis in MUller glia. Glia 2005; 52:47-52
66. Hosoya K, Ichikawa T, Akanuma S, et al. Glycine and L-Arginine transport in cultured MUller glial cells (TR-MUL). Neuroehem Int 2010; 57:262-268
67. Arunehaipong K, Sattayasai N, Sattayasai J, et al. A biotin-coupled bifunctional enzyme exhibiting both glutamine synthetase activity and glutamate decarboxylase activity. Curr Eye Res 2009; 34:809-818
68. Ohkura Y, Akanuma SI, Taehikawa M, et al. Blood-To-retina transport of biotin via Na(+)-dependent multivitamin transporter (SMVT) at the inner blood-retinal barrier. Exp Eye Res 2010; 91:387-392
69. Tomi M, Arai K, Taehikawa M, et al. Na( + )-independent choline transport in rat retinal capillary endothelial cells. Neuroehem Res 2007; 32:1833-1842
70. Karlsson C, Maepea 0, Aim A. Choline transport through the blood-retinal and the blood-brain barrier in vivo. Acta Ophthalmol (Copenh) 1984; 62:763-766
71. Hosoya K, Fujita K, Taehikawa M. Involvement of reduced folate carrier I in the inner blood-retinal barrier transport of methyltetrahydrofolate. Drug Metab Pharmaeokinet 2008; 23 :285-292
72. AIm A, Tornquist P. Lactate transport through the blood-retinal and the blood-brain barrier in rats. Ophthalmic Res 1985; 17:181-184
73. GerhartDZ, Leino RL, Drewes LR. Distribution of mono carboxylate transporters MCTI and MCT2 in rat retina. Neuroscience 1999; 92:367-375
74. Hosoya K, Kondo T, Tomi M, et al. MCTI-mediated transport ofL-laetie acid at the inner blood-retinal barrier: A possible route for delivery of monoearboxylie acid drugs to the retina. Pharm Res 2001; 18: 1669-1676
75. Taehikawa M, Okayasu S, Hosoya K. Functional involvement of scavenger receptor elass B, type I, in the uptake of alpha-Tocopherol using cultured rat retinal capillary endothelial cells. Mol Vis 2007; 13 :2041-2047
76. Heacock AM, Dodd MS, Fisher SK. Regulation of volume-sensitive osmolyte efflux from human SH-S Y 5 Y neuroblastoma cells following activation of Iysophospholipid receptors. J Pharmaeol Exp Ther 2006; 317:685-693
77. Fisher SK, Cheema TA, Foster DJ. Volume-dependent osmolyte efflux from neural tissues: Regulation by G-protein-eoupled receptors. J Neuroehem 2008; 106: 1998-2014
78. McManus ML, Churchwell KB, Strange K. Regulation of cell volume in health and disease. N Engl J Med 1995; 333: 1260-1266
79. Pow DV, Sullivan R, Reye P, et al. Localization oftaurine transporters, taurine and1H taurine accumulation in the rat retina, pituitary and brain. Glia 2002; 37: 153-168
80. Taehikawa M, Tsuji K, Ikeda S, et al. Lysophospholipids enhance taurine release from rat retinal vascular endothelial cells under hypoosmotie stress. Mierovase Res 2009; 78:332-337
81. Nakakariya M, Shimada T, Irokawa M, et al. Predominant contribution of rat organic anion transporting polypeptide-2 (Oatp2) to hepatic uptake of beta-lac tam antibiotics. Pharm Res 2008; 25:578-585
82. Katayama K, Ohshima Y, Tomi M, et al. Application of micro dialysis to evaluate the efflux transport of estradiol17-beta glucuronide across the rat blood-retinal barrier. J Neurosei Methods 2006; 156:249-256
83. Noe B, Hagenbuch B, Stieger B, et al. Isolation of a multispeeifie organic anion and cardiac glycoside transporter from rat brain. Proe Natl Aead Sci USA 1994; 94: 10346-10350
84. Gao B, Wenzel A, Grimm C, et al. Localization of organic anion transport protein 2 in the apical region of rat retinal pigment epithelium. Invest Ophthalmol Vis Sci 2002; 43:510-514
85. Sugiyama D, Kusuhara H, Shitara Y, et al. Characterization of the efflux transport of 17beta-estradiol-D-17beta-glueuronide from the brain across the blood-brain barrier. J Pharmaeol Exp Ther 2001; 298:316-322
86. Kikuchi R, Kusuhara H, Sugiyama D, et al. Contribution of organic anion transporter 3 (Sle22a8) to the elimination of p-Aminohippurie acid and benzylpenicillin across the blood-brain barrier. J Pharmaeol Exp Ther 2003; 306:51-58
87. Somervaille TC, Hann IM, Harrison G, et al. MRC Childhood Leukaemia Working Party. Intraocularrelapse of childhood acute lymphoblastic leukaemia. Br J Haematol 2003; 121 :280-288
88. Betz AL, Goldstein GW. Transport ofhexoses, potassium and neutral amino acids into capillaries isolated from bovine retina. Exp Eye Res 1980; 30:593-605
89. Hosoya K, Makihara A, Tsujikawa Y, et al. Roles of inner blood-retinal barrier organic anion transporter 3 in the vitreous/retina-To-blood efflux transport of p-Aminohippuric acid, benzylpenicillin and 6-mercaptopurine. J Pharmacol Exp Ther 2009; 329:87-93
90. Yoneyama D, Shinozaki Y, Lu WL, et al. Involvement of system A in the retina-To-blood transport of L-proline across the inner blood-retinal barrier. Exp Eye Res 2010; 90:507-513
91. LaNoue KF, Berkich DA, Conway M et al. Role of specific aminotransferases in De novo glutamate synthesis and redox shuttling in the retina. J Neurosci Res 2001; 66:914-922
92. Levkovitch-Verbin H, Martin KR, Quigley HA et al. Measurement of amino acid levels in the vitreous humor ofrats after chronic intraocular pressure elevation or optic nerve transection. J Glaucoma 2002; 11 :396-405
93. Maines LW, Antonetti DA, Wolpert EB et al. Evaluation of the role ofP-glycoprotein in the uptake of paroxetine, c1ozapine, phenytoin and carbamazapine by bovine retinal endothelial cells. Neuropharmacology 2005; 49:610-617
94. Shen J, Cross ST, Tang-Liu DD et al. Evaluation of an immortalized retinal endothelial cell line as an in vitro model for drug transport studies across the blood-retinal barrier. Pharm Res 2003; 20:1357-1363
95. BenEzra D, Maftzir G. Ocular penetration of cyclosporin A. The rabbit eye. Invest Ophthalmol Vis Sci 1990; 31: 1362-1366
96. BenEzra D, Maftzir G. Ocular penetration of cyclosporine A in the rat eye. Arch Ophthalmol 1990; 108:584-587
97. BenEzra D, Maftzir G, De Courten C et al. Ocular penetration of cyclosporin A. Ill: The human eye. Br J Ophthalmol 1990; 74:350-352
98. Choudhuri S. Klaassen CD. Structure, function, expression, genomic organization and single nucleotide polymorphisms of human ABCB I (MDR I), ABCC (MRP) and ABCG2 (BCRP) efflux transporters. lnt J Toxicol2006; 25:231-259
99. Tagami M, KusuharaS, Honda S et al. Expression of A TP-binding cassette transporters at the inner blood-retinal barrier in a neonatal mouse model of oxygen-induced retinopathy. Brain Res 2009; 1283: 186-193
100. Smeets PH, van Aubel RA, Wouterse AC et al. Contribution of multidrug resistance protein 2 (MRP21 ABCC2) to the renal excretion ofp-Aminohippurate (PAH) and identification of MRP4 (ABCC4) as a novel PAH transporter. J Am Soc Nephrol 2004 15 2828-2835
101. Uchida Y, Kamiie J, Ohtsuki S et al. Multichannel liquid chromatography-Tandem mass spectrometry cocktail method for comprehensive substrate characterization of multi drug resistance-Associated protein 4 transporter. Pharm Res 2007; 24:2281-2296
102. Asashima T, Hori S, Ohtsuki S et al' A TP-binding cassette transporterG2 mediates the efflux of photo toxins on the luminal membrane of retinal capillary endothelial cells. Pharm Res 2006; 23: 1235-1242
103. Boulton M, Rozanowska M, Rozanowski B. Retinal photodamage. J Photochem Photobiol B 2001; 64:144-161
104. Dean M, Hamon Y, Chimini G. The human A TP-binding cassette (ABC) transporter superfamily. J Lipid Res 2001; 42: 1 007-1017
105. Tomi M, Hosoya K. The role of blood-ocular barrier transporters in retinal drug disposition: An overview. Expert Opin Drug Metab Toxicol 2010; 6: 1111-1124
106. Kamiie J, Ohtsuki S, Iwase R 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 2008; 25: 1469-1483