Blood–brain barrier models: in vitro to in vivo translation in preclinical development of CNS-targeting biotherapeutics

Bibliography

• Arrowsmith J, Miller P. Trial watch: phase II and phase III attrition rates 2011-2012. Nat Rev Drug Discov 2013;12:569
   PubMed Web of Science ®Google Scholar
• Abbott NJ, Patabendige AAK, Dolman DEM, et al. Structure and function of the blood-brain barrier. Neurobiol Dis 2010;37:13-25
   PubMed Web of Science ®Google Scholar
• Talevi A, Bellera CL, Di Ianni M, et al. CNS drug development - lost in translation? Mini Rev Med Chem 2012;12:959-70
   PubMed Web of Science ®Google Scholar
• Abbott NJ. Prediction of blood-brain barrier permeation in drug discovery from in vivo, in vitro and in silico models. Drug Discov Today Technol 2004;1:407-16
   PubMedGoogle Scholar
• Neuwelt EA, Bauer B, Fahlke C, et al. Engaging neuroscience to advance translational research in brain barrier biology. Nat Rev Neurosci 2011;12:169-82
   PubMed Web of Science ®Google Scholar
• Siegenthaler JA, Sohet F, Daneman R. “Sealing off the CNS”: cellular and molecular regulation of blood-brain barriergenesis. Curr Opin Neurobiol 2013;23:1057-64
   PubMed Web of Science ®Google Scholar
• Obermeier B, Daneman R, Ransohoff RM. Development, maintenance and disruption of the blood-brain barrier. Nat Med 2013;19:1584-96
   PubMed Web of Science ®Google Scholar
• Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006;7:41-53
   PubMed Web of Science ®Google Scholar
• Ogunshola OO. In vitro modeling of the blood-brain barrier: simplicity versus complexity. Curr Pharm Des 2011;17:2755-61
   PubMed Web of Science ®Google Scholar
• Cecchelli R, Dehouck B, Descamps L, et al. In vitro model for evaluating drug transport across the blood-brain barrier. Adv Drug Deliv Rev 1999;36:165-78
   PubMed Web of Science ®Google Scholar
• Tóth A, Veszelka S, Nakagawa S, et al. Patented in vitro blood-brain barrier models in CNS drug discovery. Recent Pat CNS Drug Discov 2011;6:107-18
   PubMedGoogle Scholar
• Nakagawa S, Deli MA, Kawaguchi H, et al. A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem Int 2009;54:253-63
   PubMed Web of Science ®Google Scholar
• Culot M, Lundquist S, Vanuxeem D, et al. An in vitro blood-brain barrier model for high throughput (HTS) toxicological screening. Toxicol Vitr 2008;22:799-811
   PubMed Web of Science ®Google Scholar
• Booth R, Kim H. Characterization of a microfluidic in vitro model of the blood-brain barrier (μBBB). Lab Chip 2012;12:1784-92
   PubMed Web of Science ®Google Scholar
• Griep LM, Wolbers F, de Wagenaar B, et al. BBB on chip: microfluidic platform to mechanically and biochemically modulate blood-brain barrier function. Biomed Microdevices 2013;15:145-50
   PubMed Web of Science ®Google Scholar
• Cucullo L, Hossain M, Tierney W, Janigro D. A new dynamic in vitro modular capillaries-venules modular system: cerebrovascular physiology in a box. BMC Neurosci 2013;14:18
   PubMedGoogle Scholar
• Cucullo L, Couraud P-O, Weksler B, et al. Immortalized human brain endothelial cells and flow-based vascular modeling: a marriage of convenience for rational neurovascular studies. J Cereb Blood Flow Metab 2008;28:312-28
   PubMed Web of Science ®Google Scholar
• Hellinger E, Veszelka S, Tóth AE, et al. Comparison of brain capillary endothelial cell-based and epithelial (MDCK-MDR1, Caco-2, and VB-Caco-2) cell-based surrogate blood-brain barrier penetration models. Eur J Pharm Biopharm 2012;82:340-51
   PubMed Web of Science ®Google Scholar
• Garberg P, Ball M, Borg N, et al. In vitro models for the blood-brain barrier. Toxicol Vitr 2005;19:299-334
   PubMed Web of Science ®Google Scholar
• Nakagawa S, Deli MA, Nakao S, et al. Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol Neurobiol 2007;27:687-94
   PubMed Web of Science ®Google Scholar
• Watson PMD, Paterson JC, Thom G, et al. Modelling the endothelial blood-CNS barriers: a method for the production of robust in vitro models of the rat blood-brain barrier and blood-spinal cord barrier. BMC Neurosci 2013;14:59
   PubMed Web of Science ®Google Scholar
• Coisne C, Dehouck L, Faveeuw C, et al. Mouse syngenic in vitro blood-brain barrier model: a new tool to examine inflammatory events in cerebral endothelium. Lab Investig 2005;85:734-46
   PubMed Web of Science ®Google Scholar
• Patabendige A, Skinner RA, Abbott NJ. Establishment of a simplified in vitro porcine blood-brain barrier model with high transendothelial electrical resistance. Brain Res 2013;1521:1-15
   PubMed Web of Science ®Google Scholar
• Freeman R, Niego B, R Croucher D, et al. t-PA, but not desmoteplase, induces plasmin-dependent opening of a blood-brain barrier model under normoxic and ischaemic conditions. Brain Res 2014;1565:63-73
   PubMed Web of Science ®Google Scholar
• Muruganandam A, Tanha J, Narang S, Stanimirovic D. Selection of phage-displayed llama single-domain antibodies that transmigrate across human blood-brain barrier endothelium. FASEB J 2002;16:240-2
   PubMed Web of Science ®Google Scholar
• Salcedo Gómez PM, Amano M, Yashchuk S, et al. GRL-04810 and GRL-05010, difluoride-containing nonpeptidic HIV-1 protease inhibitors (PIs) that inhibit the replication of multi-PI-resistant HIV-1 in vitro and possess favorable lipophilicity that may allow blood-brain barrier penetration. Antimicrob Agents Chemother 2013;57:6110-21
   PubMed Web of Science ®Google Scholar
• Montesano R, Pepper MS, Möhle-Steinlein U, et al. Increased proteolytic activity is responsible for the aberrant morphogenetic behavior of endothelial cells expressing the middle T oncogene. Cell 1990;62:435-45
   PubMed Web of Science ®Google Scholar
• Roux F, Durieu-Trautmann O, Chaverot N, et al. Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J Cell Physiol 1994;159:101-13
   PubMed Web of Science ®Google Scholar
• Muruganandam A, Herx LM, Monette R, et al. Development of immortalized human cerebromicrovascular endothelial cell line as an in vitro model of the human blood-brain barrier. FASEB J 1997;11:1187-97
   PubMed Web of Science ®Google Scholar
• Weksler BB, Subileau EA, Perrière N, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 2005;19:1872-4
   PubMed Web of Science ®Google Scholar
• Weksler B, Romero IA, Couraud PO. The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids Barriers CNS 2013;10:16
   PubMedGoogle Scholar
• Yousif LF, Di Russo J, Sorokin L. Laminin isoforms in endothelial and perivascular basement membranes. Cell Adh Migr 2013;7:101-10
   PubMed Web of Science ®Google Scholar
• Hartmann C, Zozulya A, Wegener J, Galla HJ. The impact of glia-derived extracellular matrices on the barrier function of cerebral endothelial cells: an in vitro study. Exp Cell Res 2007;313:1318-25
   PubMed Web of Science ®Google Scholar
• Kröll S, El-Gindi J, Thanabalasundaram G, et al. Control of the blood-brain barrier by glucocorticoids and the cells of the neurovascular unit. Ann N Y Acad Sci 2009;1165:228-39
   Google Scholar
• Lai CH, Kuo KH, The critical component to establish in vitro BBB model: pericyte. Brain Res Brain Res Rev 2005;50:258-65
   PubMed Web of Science ®Google Scholar
• Abbott NJ. Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 2005;25:5-23
   PubMed Web of Science ®Google Scholar
• Paolinelli R, Corada M, Ferrarini L, et al. Wnt activation of immortalized brain endothelial cells as a tool for generating a standardized model of the blood brain barrier in vitro. PLoS One 2013;8:e70233
   PubMed Web of Science ®Google Scholar
• Mizee MR, Wooldrik D, Lakeman KAM, et al. Retinoic acid induces blood-brain barrier development. J Neurosci 2013;33:1660-71
   PubMed Web of Science ®Google Scholar
• Uchida Y, Ohtsuki S, Katsukura Y, et al. Quantitative targeted absolute proteomics of human blood-brain barrier transporters and receptors. J Neurochem 2011;117:333-45
   PubMed Web of Science ®Google Scholar
• Ohtsuki S, Hirayama M, Ito S, et al. Quantitative targeted proteomics for understanding the blood-brain barrier: towards pharmacoproteomics. Expert Rev Proteomics 2014;11:303-13
   PubMed Web of Science ®Google Scholar
• Yu YJ, Zhang Y, Kenrick M, et al. Boosting brain uptake of a therapeutic antibody by reducing its affinity for a transcytosis target. Sci Transl Med 2011;3:84ra44
   PubMed Web of Science ®Google Scholar
• Couch JA, Yu YJ, Zhang Y, et al. Addressing safety liabilities of TfR bispecific antibodies that cross the blood-brain barrier. Sci Transl Med 2013;5(183):183ra571
   Google Scholar
• Durieu-Trautmann O, Foignant-Chaverot N, Perdomo J, et al. Immortalization of brain capillary endothelial cells with maintenance of structural characteristics of the blood-brain barrier endothelium. Vitr Cell Dev Biol 1991;27A:771-8
   PubMedGoogle Scholar
• Stins MF, Badger J, Sik Kim K. Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog 2001;30:19-28
   PubMed Web of Science ®Google Scholar
• Eigenmann DE, Xue G, Kim KS, et al. 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;10:33
   PubMedGoogle Scholar
• Prudhomme JG, Sherman IW, Land KM, et al. Studies of Plasmodium falciparum cytoadherence using immortalized human brain capillary endothelial cells. Int J Parasitol 1996;26:647-55
   PubMed Web of Science ®Google Scholar
• Major EO, Miller AE, Mourrain P, et al. Establishment of a line of human fetal glial cells that supports JC virus multiplication. Proc Natl Acad Sci USA 1985;82:1257-61
   PubMed Web of Science ®Google Scholar
• Shimizu F, Sano Y, Abe M-A, et al. Peripheral nerve pericytes modify the blood-nerve barrier function and tight junctional molecules through the secretion of various soluble factors. J Cell Physiol 2011;226:255-66
   PubMed Web of Science ®Google Scholar
• Urich E, Lazic SE, Molnos J, et al. Transcriptional profiling of human brain endothelial cells reveals key properties crucial for predictive in vitro blood-brain barrier models. In: Arai K, editor. PLoS One 2012;7:e38149
   PubMedGoogle Scholar
• Lippmann ES, Azarin SM, Kay JE, et al. Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol 2012;30:783-91
   PubMed Web of Science ®Google Scholar
• Lippmann ES, Al-Ahmad A, Azarin SM, et al. A retinoic acid-enhanced, multicellular human blood-brain barrier model derived from stem cell sources. Sci Rep 2014;4:4160
   PubMed Web of Science ®Google Scholar
• Crone C, Olesen SP. Electrical resistance of brain microvascular endothelium. Brain Res 1982;241:49-55
   PubMed Web of Science ®Google Scholar
• Butt AM, Jones HC, Abbott NJ. Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study. J Physiol 1990;429:47-62
   PubMed Web of Science ®Google Scholar
• Cecchelli R, Aday S, Sevin E, et al. A stable and reproducible human blood-brain barrier model derived from hematopoietic stem cells. PLoS One 2014;9:e99733
   PubMed Web of Science ®Google Scholar
• Boyer-Di Ponio J, El-Ayoubi F, Glacial F, et al. Instruction of circulating endothelial progenitors in vitro towards specialized blood-brain barrier and arterial phenotypes. PLoS One 2014;9:e84179
   PubMed Web of Science ®Google Scholar
• DeSalvo MK, Mayer N, Mayer F, Bainton RJ. Physiologic and anatomic characterization of the brain surface glia barrier of Drosophila. Glia 2011;59:1322-40
   PubMed Web of Science ®Google Scholar
• Pickart MA, Klee EW. Zebrafish approaches enhance the translational research tackle box. Transl Res 2014;163:65-78
   PubMed Web of Science ®Google Scholar
• Abdelilah-Seyfried S. Claudin-5a in developing zebrafish brain barriers: another brick in the wall. Bioessays 2010;32:768-76
   Google Scholar
• Eliceiri BP, Gonzalez AM, Baird A. Zebrafish model of the blood-brain barrier: morphological and permeability studies. Methods Mol Biol 2011;686:371-8
   PubMedGoogle Scholar
• Zhang L, Yu W, Schroedter I, et al. Galanin transgenic mice with elevated circulating galanin levels alleviate demyelination in a cuprizone-induced MS mouse model. PLoS One 2012;7:e33901
   PubMedGoogle Scholar
• Umans RA, Taylor MR. Zebrafish as a model to study drug transporters at the blood-brain barrier. Clin Pharmacol Ther 2012;92:567-70
   PubMed Web of Science ®Google Scholar
• Fleming A, Diekmann H, Goldsmith P. Functional characterisation of the maturation of the blood-brain barrier in larval zebrafish. PLoS One 2013;8:e77548
   PubMed Web of Science ®Google Scholar
• Stewart AM, Braubach O, Spitsbergen J, et al. Zebrafish models for translational neuroscience research: from tank to bedside. Trends Neurosci 2014;37:264-78
   PubMed Web of Science ®Google Scholar
• Watanabe K, Nishimura Y, Nomoto T, et al. In vivo assessment of the permeability of the blood-brain barrier and blood-retinal barrier to fluorescent indoline derivatives in zebrafish. BMC Neurosci 2012;13:101
   PubMedGoogle Scholar
• Bicker J, Alves G, Fortuna A, Falcão A. Blood-brain barrier models and their relevance for a successful development of CNS drug delivery systems: a review. Eur J Pharm Biopharm 2014;87:409-32
   PubMed Web of Science ®Google Scholar
• Takasato Y, Rapoport SI, Smith QR. An in situ brain perfusion technique to study cerebrovascular transport in the rat. Am J Physiol 1984;247:H484-93
   PubMed Web of Science ®Google Scholar
• Smith QR, Allen DD. In situ brain perfusion technique. Methods Mol Med 2003;89:209-18
   PubMedGoogle Scholar
• Moriki Y, Suzuki T, Fukami T, et al. Involvement of P-glycoprotein in blood-brain barrier transport of pentazocine in rats using brain uptake index method. Biol Pharm Bull 2004;27:932-5
   PubMed Web of Science ®Google Scholar
• Knight RA, Nagaraja TN, Ewing JR, et al. Quantitation and localization of blood-to-brain influx by magnetic resonance imaging and quantitative autoradiography in a model of transient focal ischemia. Magn Reson Med 2005;54:813-21
   PubMed Web of Science ®Google Scholar
• De Lange EC, Danhof M, de Boer AG, Breimer DD. Methodological considerations of intracerebral microdialysis in pharmacokinetic studies on drug transport across the blood-brain barrier. Brain Res Brain Res Rev 1997;25:27-49
   PubMed Web of Science ®Google Scholar
• Hammarlund-Udenaes M. The use of microdialysis in CNS drug delivery studies. Pharmacokinetic perspectives and results with analgesics and antiepileptics. Adv Drug Deliv Rev 2000;45:283-94
   PubMed Web of Science ®Google Scholar
• Lin JH. CSF as a surrogate for assessing CNS exposure: an industrial perspective. Curr Drug Metab 2008;9:46-59
   PubMed Web of Science ®Google Scholar
• De Lange ECM, Danhof M. Considerations in the use of cerebrospinal fluid pharmacokinetics to predict brain target concentrations in the clinical setting: implications of the barriers between blood and brain. Clin Pharmacokinet 2002;41:691-703
   PubMed Web of Science ®Google Scholar
• Abulrob A, Brunette E, Slinn J, et al. Dynamic analysis of the blood-brain barrier disruption in experimental stroke using time domain in vivo fluorescence imaging. Mol Imaging 2008;7:248-62
   PubMed Web of Science ®Google Scholar
• Nicolazzo JA, Charman SA, Charman WN. Methods to assess drug permeability across the blood-brain barrier. J Pharm Pharmacol 2006;58:281-93
   PubMed Web of Science ®Google Scholar
• Wunder A, Schoknecht K, Stanimirovic DB, et al. Imaging blood-brain barrier dysfunction in animal disease models. Epilepsia 2012;53(Suppl 6):14-21
   PubMedGoogle Scholar
• Hammarlund-Udenaes M, Fridén M, Syvänen S, Gupta A. On the rate and extent of drug delivery to the brain. Pharm Res 2008;25:1737-50
   PubMed Web of Science ®Google Scholar
• Stanimirovic DB, Kemmerich K, Haqqani AS, Farrington GK. Engineering and pharmacology of blood–brain barrier-permeable bispecific antibodies. Adv Pharmacol 2014;71:301-5
   PubMedGoogle Scholar
• Avdeef A. How well can in vitro brain microcapillary endothelial cell models predict rodent in vivo blood-brain barrier permeability? Eur J Pharm Sci 2011;43:109-24
   PubMed Web of Science ®Google Scholar
• Mabondzo A, Bottlaender M, Guyot A-C, et al. Validation of in vitro cell-based human blood-brain barrier model using clinical positron emission tomography radioligands to predict in vivo human brain penetration. Mol Pharm 2010;7:1805-15
   PubMedGoogle Scholar
• Loryan I, Sinha V, Mackie C, et al. Mechanistic understanding of brain drug disposition to optimize the selection of potential neurotherapeutics in drug discovery. Pharm Res 2014;31(8):2203-19
   PubMed Web of Science ®Google Scholar
• Pardridge WM, Boado RJ. Reengineering biopharmaceuticals for targeted delivery across the blood-brain barrier. Methods Enzymol. 1st edition. Elsevier Inc; 2012. pp 269-92
   Google Scholar
• Wolak DJ, Thorne RG. Diffusion of macromolecules in the brain: implications for drug delivery. Mol Pharm 2013;10:1492-504
   PubMed Web of Science ®Google Scholar
• Farrington GK, Caram-Salas N, Haqqani AS, et al. A novel platform for engineering blood-brain barrier-crossing bispecific biologics. FASEB J 2014;10.1096/fj.14–253369
   PubMed Web of Science ®Google Scholar
• Jones AR, Shusta E V. Blood-brain barrier transport of therapeutics via receptor-mediation. Pharm Res 2007;24:1759-71
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Drug targeting to the brain. Pharm Res 2007;24:1733-44
   PubMed Web of Science ®Google Scholar
• Tanha J, Muruganandam A, Stanimirovic D. Phage display technology for identifying specific antigens on brain endothelial cells. Methods Mol Med 2003;89:435-49
   PubMedGoogle Scholar
• Abulrob A, Sprong H, Van Bergen en Henegouwen P, Stanimirovic D. The blood-brain barrier transmigrating single domain antibody: mechanisms of transport and antigenic epitopes in human brain endothelial cells. J Neurochem 2005;95:1201-14
   PubMed Web of Science ®Google Scholar
• Haqqani AS, Caram-Salas N, Ding W, et al. Multiplexed evaluation of serum and CSF pharmacokinetics of brain-targeting single-domain antibodies using a NanoLC-SRM-ILIS method. Mol Pharm 2013;10:1542-56
   PubMed Web of Science ®Google Scholar
• Lundquist S, Renftel M, Brillault J, et al. Prediction of drug transport through the blood-brain barrier in vivo: a comparison between two in vitro cell models. Pharm Res 2002;19:976-81
   PubMed Web of Science ®Google Scholar
• Abbott NJ. Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem Int 2004;45:545-52
   PubMed Web of Science ®Google Scholar
• Wang Y, Tian Z, Thirumalai D, Zhang X. Neonatal Fc receptor (FcRn): a novel target for therapeutic antibodies and antibody engineering. J Drug Target 2014;22:269-78
   PubMed Web of Science ®Google Scholar
• Pangalos MN, Schechter LE, Hurko O. Drug development for CNS disorders: strategies for balancing risk and reducing attrition. Nat Rev Drug Discov 2007;6:521-32
   PubMed Web of Science ®Google Scholar