Human brain microvascular endothelial cells derived from the BC1 iPS cell line exhibit a blood-brain barrier phenotype

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Katt, Moriah E ^a   Xu, Zinnia S ^a,b   Gerecht, Sharon ^a   Searson, Peter C ^a  

^a Johns Hopkins University   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; LUCIFER YELLOW; OCCLUDIN; PROTEIN ZO1; RETINOIC ACID; RHODAMINE 123; TACRINE; VASCULAR ENDOTHELIAL CADHERIN; CADHERIN; LEUKOCYTE ANTIGEN; TJP1 PROTEIN, HUMAN;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; CELL DIFFERENTIATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; PHENOTYPE; PLURIPOTENT STEM CELL; POLARIZATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; BRAIN; CAPILLARY; CELL LINE; ENDOTHELIUM CELL; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PHYSIOLOGY; TIGHT JUNCTION; TRANSPORT AT THE CELLULAR LEVEL;

ANTIGENS, CD; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CADHERINS; CAPILLARIES; CELL LINE; CLAUDIN-5; ENDOTHELIAL CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; OCCLUDIN; PHENOTYPE; RHODAMINE 123; TIGHT JUNCTIONS; UP-REGULATION; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84963865043     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0152105     Document Type: Article

References (47)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the bloodbrain barrier. Neurobiol Dis. 2010;37(1):13-25. Epub 2009/08/12. doi:10.1016/j.nbd.2009.07.030 PMID: 19664713.
2. Wong AD, Ye M, Levy AF, Rothstein JD, Bergles DE, Searson PC. The blood-brain barrier: an engineering perspective. Front Neuroeng. 2013;6:7. doi:10.3389/fneng.2013.00007 PMID: 24009582; PubMed Central PMCID: PMC3757302.
3. Neuwelt E, Abbott N, Abrey L, Banks WA, Blakley B, Davis T, et al. Strategies to advance translational research into brain barriers. Lancet Neurology. 2008;7(1):84-96. PMID: ISI:000252063300029.
4. Neuwelt EA, Bauer B, Fahlke C, Fricker G, Iadecola C, Janigro D, et al. Engaging neuroscience to advance translational research in brain barrier biology. Nature Reviews Neuroscience. 2011;12(3):169-82. Epub 2011/02/19. nrn2995 [pii] doi:10.1038/nrn2995 PMID: 21331083.
5. Keep RF. Neural progenitor cells and blood-brain barrier modeling. Journal of neurochemistry. 2011;119(3):417-8. doi:10.1111/J.1471-4159.2011.07425. X PMID: ISI:000297019300001.
6. Reichel A, Begley DJ, Abbottt NJ. An overview of in vitro techniques for blood brain barrier studies. In: Nag S, editor. Methods in Molecular Medicine, V 89: The Blood Brain Barrier. Totowa, NJ: Humana; 2003. p. 307-24. PMID: 12958429
7. Ohtsuki S, Terasaki T. Contribution of carrier-mediated transport systems to the blood-brain barrier as a supporting and protecting interface for the brain; Importance for CNS drug discovery and development. Pharm Res. 2007;24(9):1745-58. doi:10.1007/S11095-007-9374-5 PMID: ISI:000248618700016.
8. Summerfield SG, Read K, Begley DJ, Obradovic T, Hidalgo IJ, Coggon S, etal. Central nervous system drug disposition: the relationship between in situ brain permeability and brain free fraction. J Pharmacol ExpTher. 2007;322(1):205-13. Epub 2007/04/05. doi:10.1124/jpet.107.121525 PMID: 17405866.
9. Lundquist S, Renftel M, Brillault J, Fenart L, Cecchelli R, Dehouck MP. Prediction of drug transport through the blood-brain barrier in vivo: A comparison between two in vitro cell models. Pharm Res. 2002;19(7):976-81. doi:10.1023/A:1016462205267 PMID: ISI:000176899900009.
10. Weksler B, Romero IA, Couraud PO. The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids Barriers CNS. 2013;10(1):16. Epub 2013/03/28. doi:10.1186/2045-8118-10-16 PMID: 23531482; PubMed Central PMCID: PMC3623852.
11. Eigenmann DE, Xue G, Kim KS, Moses AV, Hamburger M, Oufir M. Comparative study of four immortalized human brain capillary endothelial cell lines, hCMEC/D3, hBMEC, TY10, and BB19, and optimization of culture conditions, for an in vitro blood-brain barrier model for drug permeability studies. Fluids Barriers CNS. 2013;10(1):33. Epub 2013/11/23. doi:10.1186/2045-8118-10-33 PMID: 24262108.
12. Steiner O, Coisne C, Engelhardt B, Lyck R. Comparison of immortalized bEnd5 and primary mouse brain microvascular endothelial cells as in vitro blood-brain barrier models for the study of T cell extravasation. Journal of Cerebral Blood Flow and Metabolism. 2011;31(1):315-27. doi:10.1038/jcbfm. 2010.96 PMID: ISI:000285870700033.
13. Urich E, Patsch C, Aigner S, Graf M, Iacone R, Freskgard PO. Multicellular self-assembled spheroidal model of the blood brain barrier. Sci Rep. 2013;3:1500. Epub 2013/03/21. doi:10.1038/srep01500 PMID: 23511305; PubMed Central PMCID: PMC3603320.
14. Lippmann ES, Azarin SM, Kay JE, Nessler RA, Wilson HK, Al-Ahmad A, etal. Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol. 2012;30(8):783-91. Epub 2012/06/26. doi:10.1038/nbt.2247 PMID: 22729031; PubMed Central PMCID: PMC3467331.
15. Yu J, Hu K, Smuga-Otto K, Tian S, Stewart R, Slukvin II, etal. Human induced pluripotent stem cells free of vector and transgene sequences. Science. 2009;324(5928):797-801. Epub 2009/03/28. doi:10.1126/science.1172482 PMID: 19325077; PubMed Central PMCID: PMC2758053.
16. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, etal. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318(5858):1917-20. Epub 2007/11/22. doi:10.1126/science.1151526 PMID: 18029452.
17. Lippmann ES, Al-Ahmad A, Azarin SM, Palecek SP, Shusta EV. A retinoic acid-enhanced, multicellular human blood-brain barrier model derived from stem cell sources. Sci Rep. 2014;4:4160. Epub 2014/02/25. doi:10.1038/srep04160 PMID: 24561821; PubMed Central PMCID: PMC3932448.
18. Cecchelli R, Aday S, Sevin E, Almeida C, Culot M, Dehouck L, etal. A Stable and Reproducible Human Blood-Brain Barrier Model Derived from Hematopoietic Stem Cells. Plos One. 2014;9(6). Artn e99733 doi:10.1371/journal.pone.0099733 PMID: WOS:000338503400035.
19. Chou BK, Mali P, Huang X, Ye Z, Dowey SN, Resar LM, etal. Efficient human iPScell derivation by a non-integrating plasmid from blood cells with unique epigenetic and gene expression signatures. Cell Res. 2011;21(3):518-29. Epub 2011/01/19. doi:10.1038/cr.2011.12 PMID: 21243013; PubMed Central PMCID: PMC3193421.
20. Zou CL, Chou BK, Dowey SN, Tsang K, Huang XS, Liu CF, et al. Efficient Derivation and Genetic Modifications of Human Pluripotent Stem Cells on Engineered Human Feeder Cell Lines. Stem Cells and Development. 2012;21(12):2298-311. doi:10.1089/Scd.2011.0688 PMID: WOS:000307295500020.
21. Zou C, Chou BK, Dowey SN, Tsang K, Huang X, Liu CF, etal. Efficient derivation and genetic modifications of human pluripotent stem cells on engineered human feeder cell lines. Stem Cells Dev. 2012;21(12):2298-311. Epub 2012/01/10. doi:10.1089/scd.2011.0688 PMID: 22225458; PubMed Central PMCID: PMC3411364.
22. Lelong-Rebel IH, Cardarelli CO. Differential phosphorylation patterns of P-glycoprotein reconstituted into a proteoliposome system: insight into additional unconventional phosphorylation sites. Anticancer research. 2005;25(6B):3925-35. Epub 2005/11/29. PMID: 16309179.
23. Ye M, Sanchez HM, Hultz M, Yang Z, Bogorad M, Wong AD, etal. Brain microvascular endothelial cells resist elongation due to curvature and shear stress. Sci Rep. 2014;4:4681. Epub 2014/04/16. doi:10. 1038/srep04681 PMID: 24732421; PubMed Central PMCID: PMC3986701.
24. Staudt T, Lang MC, Medda R, Engelhardt J, Hell SW. 2, 2'-thiodiethanol: a new water soluble mounting medium for high resolution optical microscopy. Microsc Res Tech. 2007;70(1):1-9. Epub 2006/11/30. doi:10.1002/jemt.20396 PMID: 17131355.
25. Wilson HK, Canfield SG, Hjortness MK, Palecek SP, Shusta EV. Exploring the effects of cell seeding density on the differentiation of human pluripotent stem cells to brain microvascular endothelial cells. Fluids and Barriers of the CNS. 2015;12(1):13.
26. Cecchelli R, Berezowski V, Lundquist S, Culot M, Renftel M, Dehouck MP, etal. Modelling of the bloodbrain barrier in drug discovery and development. Nature Reviews Drug Discovery. 2007;6(8):650-61. PMID: ISI:000248486400020.
27. de Boer AG, van der Sandt ICJ, Gaillard PJ. The role of drug transporters at the blood-brain barrier. Annual Review of Pharmacology and Toxicology. 2003;43:629-56. PMID: ISI:000181434600025.
28. Giacomini KM, Huang SM, Tweedie DJ, Benet LZ, Brouwer KL, Chu X, et al. Membrane transporters in drug development. Nat Rev Drug Discov. 2010;9(3):215-36. Epub 2010/03/02. doi:10.1038/nrd3028 PMID: 20190787; PubMed Central PMCID: PMC3326076.
29. Chiba H, Osanai M, Murata M, Kojima T, Sawada N. Transmembrane proteins of tightjunctions. Biochimica EtBiophysicaActa-Biomembranes. 2008;1778(3):588-600. doi:10.1016/j.bbamem.2007.08.017 PMID: ISI:000254691500004.
30. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, etal. Size-selective loosening of the bloodbrain barrier in claudin-5-deficient mice. J Cell Biol. 2003;161(3):653-60. PMID: 12743111.
31. Morita K, Sasaki H, Furuse M, Tsukita S. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol. 1999;147(1):185-94. Epub 1999/10/06. PMID: 10508865; PubMed Central PMCID: PMC2164984.
32. Hewitt KJ, Agarwal R, Morin PJ. The claudin gene family: expression in normal and neoplastic tissues. BMC Cancer. 2006;6:186. PMID: 16836752.
33. Krause G, Winkler L, Piehl C, Blasig I, Piontek J, Muller SL. Structure and function of extracellular claudin domains. Ann N Y Acad Sci. 2009;1165:34-43. Epub 2009/06/23. doi:10.1111/j.1749-6632.2009. 04057.x PMID: 19538285.
34. Piontek J, Winkler L, Wolburg H, Muller SL, Zuleger N, Piehl C, etal. Formation of tight junction: determinants of homophilic interaction between classic claudins. Faseb Journal. 2008;22(1):146-58. doi:10.1096/Fj.07-8319com PMID: ISI:000252309900018.
35. Gunzel D, Yu AS. Claudins and the modulation of tight junction permeability. Physiol Rev. 2013;93(2):525-69. Epub 2013/04/17. doi:10.1152/physrev. 00019.2012 PMID: 23589827; PubMed Central PMCID: PMC3768107.
36. Matsuo H, Tsukada S, Nakata T, Chairoungdua A, Kim DK, Cha SH, etal. Expression of a system L neutral amino acid transporter at the blood-brain barrier. Neuroreport. 2000;11(16):3507-11. Epub 2000/11/30. PMID: 11095508.
37. Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability. Journal of Cell Science. 2008;121(13):2115-22. doi:10.1242/Jcs.017897 PMID: ISI:000256879900002.
38. Butt AM, Jones HC, Abbott NJ. Electrical-Resistance across the Blood-Brain-Barrier in Anesthetized Rats-a Developmental-Study. Journal of Physiology-London. 1990;429:47-62. PMID: ISI: A1990ED21800004.
39. Irvine JD, Takahashi L, Lockhart K, Cheong J, Tolan JW, Selick HE, etal. MDCK (Madin-Darby canine kidney) cells: A tool for membrane permeability screening. J PharmSci. 1999;88(1):28-33. Epub 1999/01/06. doi:10.1021/js9803205 PMID: 9874698.
40. Summers WK. Tacrine, and Alzheimer's treatments. J Alzheimers Dis. 2006;9(3 Suppl):439-45. Epub 2006/08/18. PMID: 16914883.
41. Vetkin DO, Gainullina ET, Karavaev VA, Nurmukhametov RN, Ryzhikov SB, Taranchenko VF. Study of cholinesterase active site using a fluorescent probe. Biology Bulletin. 2004;31(2):121-5. doi:10.1023/B:Bibu.0000022465.09009.9a PMID: WOS:000221163100004.
42. Castro DJ, Haghighat S, Saxton RE, Reisler E, Jongwaard N, Castro DJ, etal. Biodistribution of rhodamine-123 in nude mice heterotransplanted with human squamous cell carcinomas. Laryngoscope. 1992;102(8):868-74. Epub 1992/08/01. doi:10.1288/00005537-199208000-00005 PMID: 1495351.
43. Wang Q, Rager JD, Weinstein K, Kardos PS, Dobson GL, Li J, etal. Evaluation of the MDR-MDCK cell line as a permeability screen for the blood-brain barrier. IntJ Pharm. 2005;288(2):349-59. Epub 2004/12/29. doi:10.1016/j.ijpharm.2004.10.007 PMID: 15620875.
44. Seetharaman S, Barrand MA, Maskell L, Scheper RJ. Multidrug resistance-related transport proteins in isolated human brain microvessels and in cells cultured from these isolates. J Neurochem. 1998;70(3):1151-9. Epub 1998/03/07. PMID: 9489736.
45. Mizee MR, Wooldrik D, Lakeman KAM, van het Hof B, Drexhage JAR, Geerts D, et al. Retinoic Acid Induces Blood-Brain Barrier Development. Journal of Neuroscience. 2013;33(4):1660-71. doi:10. 1523/Jneurosci.1338-12.2013 PMID: WOS:000313956900035.
46. Sung JH, Yu KH, Park JS, Tsuruo T, Kim DD, Shim CK, etal. Saturable distribution of tacrine into the striatal extracellular fluid of the rat: evidence of involvement of multiple organic cation transporters in the transport. Drug Metab Dispos. 2005;33(3):440-8. Epub 2004/11/18. doi:10.1124/dmd. 104.002220 PMID: 15547049.
47. Swenson ES, Price JG, Brazelton T, Krause DS. Limitations of green fluorescent protein as a cell lineage marker. Stem Cells. 2007;25(10):2593-600. Epub 2007/07/07. doi:10.1634/stemcells.2007-0241 PMID: 17615263.