Functional Characterisation of the Maturation of the Blood-Brain Barrier in Larval Zebrafish

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Fleming, Angeleen ^a,b,c   Diekmann, Heike ^a,d   Goldsmith, Paul ^a,e  

^a VASTox plc   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e ROYAL VICTORIA INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN MATURATION; EMBRYO; FUNCTIONAL ANATOMY; HUMAN; LARVAL DEVELOPMENT; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; SPECIES COMPARISON; TANDEM MASS SPECTROMETRY; TRANSMISSION ELECTRON MICROSCOPY; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; FLUORESCENT DYES; GENE EXPRESSION REGULATION; LARVA; MOLECULAR SEQUENCE DATA; P-GLYCOPROTEIN; PHYLOGENY; SEQUENCE ALIGNMENT; TIGHT JUNCTION PROTEINS; TIGHT JUNCTIONS; ZEBRAFISH;

EID: 84885739130     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077548     Document Type: Article

References (36)

1. Daneman R, (2012) The blood-brain barrier in health and disease. Ann Neurol 72: 648-672. doi:10.1002/ana.23648. PubMed: 23280789.
2. Pardridge WM, (2002) Drug and gene delivery to the brain: the vascular route. Neuron 36: 555-558. doi:10.1016/S0896-6273(02)01054-1. PubMed: 12441045.
3. Kokel D, Rennekamp AJ, Shah AH, Liebel U, Peterson RT, (2012) Behavioral barcoding in the cloud: embracing data-intensive digital phenotyping in neuropharmacology. Trends Biotechnol 30: 421-425. doi:10.1016/j.tibtech.2012.05.001. PubMed: 22652049.
4. Sager JJ, Bai Q, Burton EA, (2010) Transgenic zebrafish models of neurodegenerative diseases. Brain Struct Funct 214: 285-302. doi:10.1007/s00429-009-0237-1. PubMed: 20162303.
5. Stewart AM, Desmond D, Kyzar E, Gaikwad S, Roth A, et al. (2012) Perspectives of zebrafish models of epilepsy: what, how and where next? Brain. Res Bull 87: 135-143. doi:10.1016/j.brainresbull.2011.11.020.
6. Xi Y, Noble S, Ekker M, (2011) Modeling neurodegeneration in zebrafish. Curr Neurol Neurosci Rep 11: 274-282. doi:10.1007/s11910-011-0182-2. PubMed: 21271309.
7. Jeong JY, Kwon HB, Ahn JC, Kang D, Kwon SH, et al. (2008) Functional and developmental analysis of the blood-brain barrier in zebrafish. Brain. Res Bull 75: 619-628. doi:10.1016/j.brainresbull.2007.10.043.
8. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, et al. (2003) Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol 161: 653-660. doi:10.1083/jcb.200302070. PubMed: 12743111.
9. Xie J, Farage E, Sugimoto M, Anand-Apte B, (2010) A novel transgenic zebrafish model for blood-brain and blood-retinal barrier development. BMC Dev Biol 10: 76. doi:10.1186/1471-213X-10-76. PubMed: 20653957.
10. Zheng PP, Romme E, van der Spek PJ, Dirven CM, Willemsen R, et al. (2010) Glut1/SLC2A1 is crucial for the development of the blood-brain barrier in vivo. Ann Neurol 68: 835-844. doi:10.1002/ana.22318. PubMed: 21194153.
11. Tam SJ, Richmond DL, Kaminker JS, Modrusan Z, Martin-McNulty B, et al. (2012) Death receptors DR6 and TROY regulate brain vascular development. Dev Cell 22: 403-417. doi:10.1016/j.devcel.2011.11.018. PubMed: 22340501.
12. Wolburg H, Lippoldt A, (2002) Tight junctions of the blood-brain barrier: development, composition and regulation. Vasc Pharmacol 38: 323-337. doi:10.1016/S1537-1891(02)00200-8. PubMed: 12529927.
13. Stewart PA, Hayakawa EM, (1987) Interendothelial junctional changes underlie the developmental 'tightening' of the blood-brain barrier. Brain Res 429: 271-281. PubMed: 3567665.
14. Lawson ND, Weinstein BM, (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318. doi:10.1006/dbio.2002.0711. PubMed: 12167406.
15. Westerfield M, Doerry E, Kirkpatrick AE, Driever W, Douglas SA, (1997) An on-line database for zebrafish development and genetics research. Seminars in Cell and Developmental Biology 8: 477-488. doi:10.1006/scdb.1997.0173. PubMed: 9441953.
16. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310. doi:10.1002/aja.1002030302. PubMed: 8589427.
17. Kaslin J, Panula P, (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J Comp Neurol 440: 342-377. doi:10.1002/cne.1390. PubMed: 11745628.
18. Petito CK, Schaefer JA, Plum F, (1977) Ultrastructural characteristics of the brain and blood-brain barrier in experimental seizures. Brain Res 127: 251-267. doi:10.1016/0006-8993(77)90539-X. PubMed: 861758.
19. Johansson BB, Lund S, (1978) Effect of sympathetic stimulation on the blood brain barrier dysfunction induced by amphetamine and by epileptic seizures. Acta Physiol Scand 104: 281-286. doi:10.1111/j.1748-1716.1978.tb06280.x. PubMed: 716982.
20. Hawkins BT, Egleton RD, (2006) Fluorescence imaging of blood-brain barrier disruption. J Neurosci Methods 151: 262-267. doi:10.1016/j.jneumeth.2005.08.006. PubMed: 16181683.
21. Kozler P, Pokorný J, (2003) Altered blood-brain barrier permeability and its effect on the distribution of Evans blue and sodium fluorescein in the rat brain applied by intracarotid injection. Physiol Res 52: 607-614. PubMed: 14535837.
22. Annilo T, Chen ZQ, Shulenin S, Costantino J, Thomas L, et al. (2006) Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics 88: 1-11. doi:10.1016/j.ygeno.2006.03.001. PubMed: 16631343.
23. Georges E, Bradley G, Gariepy J, Ling V, (1990) Detection of P-glycoprotein isoforms by gene-specific monoclonal antibodies. Proc Natl Acad Sci U S A 87: 152-156. doi:10.1073/pnas.87.1.152. PubMed: 1688652.
24. Hung CC, Chen CC, Lin CJ, Liou HH, (2008) Functional evaluation of polymorphisms in the human ABCB1 gene and the impact on clinical responses of antiepileptic drugs. Pharmacogenet Genomics 18: 390-402. doi:10.1097/FPC.0b013e3282f85e36. PubMed: 18408562.
25. Morita SY, Tsuda T, Horikami M, Teraoka R, Kitagawa S, et al. (2013) Bile salt-stimulated phospholipid efflux mediated by ABCB4 localized in nonraft membranes. J Lipid Res 54: 1221-1230. doi:10.1194/jlr.M032425. PubMed: 23468132.
26. Moitra K, Scally M, McGee K, Lancaster G, Gold B, et al. (2011) Molecular evolutionary analysis of ABCB5: the ancestral gene is a full transporter with potentially deleterious single nucleotide polymorphisms. PLOS ONE 6: e16318. doi:10.1371/journal.pone.0016318. PubMed: 21298007.
27. Fukunaga-Kalabis M, Martinez G, Nguyen TK, Kim D, Santiago-Walker A, et al. (2010) Tenascin-C promotes melanoma progression by maintaining the ABCB5-positive side population. Oncogene 29: 6115-6124. doi:10.1038/onc.2010.350. PubMed: 20729912.
28. Chen C, Hanson E, Watson JW, Lee JS, (2003) P-glycoprotein limits the brain penetration of nonsedating but not sedating H1-antagonists. Drug Metab Dispos 31: 312-318. doi:10.1124/dmd.31.3.312. PubMed: 12584158.
29. Levin VA, (1980) Relationship of octanol/water partition coefficient and molecular weight to rat brain capillary permeability. J Med Chem 23: 682-684. doi:10.1021/jm00180a022. PubMed: 7392035.
30. Schinkel AH, Wagenaar E, Mol CA, van Deemter L, (1996) P-glycoprotein in the blood-brain barrier of mice influences the brain penetration and pharmacological activity of many drugs. J Clin Invest 97: 2517-2524. doi:10.1172/JCI118699. PubMed: 8647944.
31. Terasaki T, Ohtsuki S, Hori S, Takanaga H, Nakashima E, et al. (2003) New approaches to in vitro models of blood-brain barrier drug transport. Drug Discov Today 8: 944-954. doi:10.1016/S1359-6446(03)02858-7. PubMed: 14554158.
32. Berghmans S, Butler P, Goldsmith P, Waldron G, Gardner I, et al. (2008) Zebrafish based assays for the assessment of cardiac, visual and gut function--potential safety screens for early drug discovery. J Pharmacol Toxicol Methods 58: 59-68. doi:10.1016/j.vascn.2008.05.130. PubMed: 18585469.
33. Alderton W, Berghmans S, Butler P, Chassaing H, Fleming A, et al. (2010) Accumulation and metabolism of drugs and CYP probe substrates in zebrafish larvae. Xenobiotica 40: 547-557. doi:10.3109/00498254.2010.493960. PubMed: 20528625.
34. Kalvass JC, Maurer TS, Pollack GM, (2007) Use of plasma and brain unbound fractions to assess the extent of brain distribution of thirty-four drugs: Comparison of unbound concentration ratios to in vivo P-glycoprotein efflux ratios. Drug Metab Dispos.
35. Delvecchio C, Tiefenbach J, Krause HM, (2011) The zebrafish: a powerful platform for in vivo, HTS drug discovery. Assay Drug Dev Technol 9: 354-361. doi:10.1089/adt.2010.0346. PubMed: 21309713.
36. MacRae CA, Peterson RT, Drug screening in the zebrafish: an overview. Drug Discovery Today: Disease Models.