Microfluidic organ-on-chip technology for blood-brain barrier research

References

• Abbott NJ. Blood–brain barrier structure and function and the challenges for CNS drug delivery. J Inherited Metab dis 2013; 36:437-49; PMID:23609350; http://dx.doi.org/10.1007/s10545-013-9608-0
   PubMed Web of Science ®Google Scholar
• Serlin Y, Shelef I, Knyazer B, Friedman A. Anatomy and physiology of the blood–brain barrier. Seminars Cell Dev Biol 2015; 38:2-6; http://dx.doi.org/10.1016/j.semcdb.2015.01.002
   PubMed Web of Science ®Google Scholar
• Pardridge WM. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2005; 2:3-14; PMID:15717053; http://dx.doi.org/10.1602/neurorx.2.1.3
   PubMedGoogle Scholar
• Abbott NJ, Rönnbäck L, Hansson E. Astrocyte–endothelial interactions at the blood–brain barrier. Nat Rev Neurosci 2006; 7:41-53; PMID:16371949; http://dx.doi.org/10.1038/nrn1824
   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 2004; 1:407-16; http://dx.doi.org/10.1016/j.ddtec.2004.11.014
   Google Scholar
• Wolff A, Antfolk M, Brodin B, Tenje M. In Vitro blood-brain barrier models—an overview of established models and new microfluidic approaches. J Pharmaceutical Sci 2015; 104:2727-46; http://dx.doi.org/10.1002/jps.24329
   PubMed Web of Science ®Google Scholar
• Huh D, Torisawa YS, Hamilton GA, Kim HJ, Ingber DE. Microengineered physiological biomimicry: organs-on-chips. Lab chip 2012; 12:2156-64; PMID:22555377; http://dx.doi.org/10.1039/c2lc40089h
   PubMed Web of Science ®Google Scholar
• Perrin S. Preclinical research: Make mouse studies work. Nature 2014; 507:423-5; PMID:24678540; http://dx.doi.org/10.1038/507423a
   PubMed Web of Science ®Google Scholar
• Pamies D, Hartung T, Hogberg HT. Biological and medical applications of a brain-on-a-chip. Exp Biol Med 2014; 239:1096-107; http://dx.doi.org/10.1177/1535370214537738
   Web of Science ®Google Scholar
• Hackam DG. Translating animal research into clinical benefit. BMJ: Br Med J 2007; 334:163; http://dx.doi.org/10.1136/bmj.39104.362951.80
   PubMed Web of Science ®Google Scholar
• van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, O'Collins V, Macleod MR. Can animal models of disease reliably inform human studies. PLoS Med 2010; 7:e1000245; PMID:20361020; http://dx.doi.org/10.1371/journal.pmed.1000245
   PubMed Web of Science ®Google Scholar
• Shanks N, Greek R, Greek J. Are animal models predictive for humans? Philosophy Ethics Humanities Med 2009; 4:2; http://dx.doi.org/10.1186/1747-5341-4-2
   PubMedGoogle Scholar
• Perrin S. Preclinical research: Make mouse studies work. Nature 2014; 507:423-5; http://dx.doi.org/10.1038/507423a
   PubMed Web of Science ®Google Scholar
• Shawahna R, Declèves X, Scherrmann J-M. Hurdles with using in vitro models to predict human blood-brain barrier drug permeability: a special focus on transporters and metabolizing enzymes. Curr Drug Metab 2013; 14:120-36; PMID:23215812; http://dx.doi.org/10.2174/138920013804545232
   PubMed Web of Science ®Google Scholar
• Naik P, Cucullo L. In vitro blood–brain barrier models: Current and perspective technologies. J Pharmaceutical Sci 2012; 101:1337-54; http://dx.doi.org/10.1002/jps.23022
   PubMed Web of Science ®Google Scholar
• van der Meer AD, van den Berg A. Organs-on-chips: breaking the in vitro impasse. Integrative Biol 2012; 4:461-70; http://dx.doi.org/10.1039/c2ib00176d
   PubMed Web of Science ®Google Scholar
• Abbott NJ, Dolman DM, Yusof S, Reichel A. In Vitro Models of CNS Barriers. In: Hammarlund-Udenaes M, de Lange ECM, Thorne RG, eds. Drug Delivery to the Brain: Springer New York, 2014:163-97
   Google Scholar
• Hatherell K, Couraud PO, Romero IA, Weksler B, Pilkington GJ. Development of a three-dimensional, all-human< i> in vitro model of the blood–brain barrier using mono-, co-, and tri-cultivation Transwell models. J Neurosci Methods 2011; 199:223-9; PMID:21609734; http://dx.doi.org/10.1016/j.jneumeth.2011.05.012
   PubMed Web of Science ®Google Scholar
• Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat Biotechnol 2014; 32:760-72; PMID:25093883; http://dx.doi.org/10.1038/nbt.2989
   PubMed Web of Science ®Google Scholar
• Moraes C, Mehta G, Lesher-Perez S, Takayama S. Organs-on-a-Chip: A Focus on Compartmentalized Microdevices. Annals Biomed Engineering 2012; 40:1211-27; http://dx.doi.org/10.1007/s10439-011-0455-6
   PubMed Web of Science ®Google Scholar
• Huh D, Matthews BD, Mammoto A, Montoya-Zavala M, Hsin HY, Ingber DE. Reconstituting organ-level lung functions on a chip. Science 2010; 328:1662-8; PMID:20576885; http://dx.doi.org/10.1126/science.1188302
   PubMed Web of Science ®Google Scholar
• Kim HJ, Huh D, Hamilton G, Ingber DE. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 2012; 12:2165-74; PMID:22434367; http://dx.doi.org/10.1039/c2lc40074j
   PubMed Web of Science ®Google Scholar
• Kim HJ, Ingber DE. Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation. Integrative Biol 2013; 5:1130-40; PMID:23817533; http://dx.doi.org/10.1039/c3ib40126j
   PubMed Web of Science ®Google Scholar
• Westein E, van der Meer AD, Kuijpers MJE, Frimat JP, van den Berg A, Heemskerk JWM. Atherosclerotic geometries exacerbate pathological thrombus formation poststenosis in a von Willebrand factor-dependent manner. Proc Natl Acad Sci 2013; 110:1357-62; PMID:23288905; http://dx.doi.org/10.1073/pnas.1209905110
   PubMed Web of Science ®Google Scholar
• Nedergaard M. Garbage Truck of the Brain. Science (New York, NY) 2013; 340:1529-30; http://dx.doi.org/10.1126/science.1240514
   Google Scholar
• Iliff JJ, Nedergaard M. Is there a cerebral lymphatic system? Stroke; J Cerebral Circulation 2013; 44:S93-S5; http://dx.doi.org/10.1161/STROKEAHA.112.678698
   PubMed Web of Science ®Google Scholar
• van der Meer AD, Wolbers F, Vermes I, van den Berg A. Blood-brain Barrier (BBB): An Overview of the Research of the Blood-brain Barrier Using Microfluidic Devices. In: van den Berg A, Segerink LI, eds. Microfluidics for Med Applications, 2014:40-56
   Google Scholar
• Adriani G, Ma D, Pavesi A, Goh E, Kamm RD. A microfluidic model of the blood brain barrier. 4th THERMIS World Congress. Boston, USA: Tissue Engineering Part A, 2015:S40-S
   Google Scholar
• Yeste J, Illa X, Guimerà A, Villa R. A novel strategy to monitor microfluidic in-vitro blood-brain barrier models using impedance spectroscopy. Bio-MEMS and Medical Microdevices II. Barcelona, Spain: SPIE Conference Proceedings, 2015:95180N-N-6
   Google Scholar
• van der Helm MW, Odijk M, Frimat J-P, Eijkel JC, van den Berg A, Segerink LI. Simple and stable transendothelial electrical resistance measurements in organs-on-chips. The 19th International Conference on Miniaturized Systems for Chemistry and Life Sciences. Gyeongju, South Korea, 2015
   Google Scholar
• Xu H, Li ZY, Yu Y, Qin JH. Microfluidic high-throughput 3D blood-brain barrier model in vitro for drug testing in brain tumor. The 19th International Conference on Miniaturized Systems for Chemistry and Life Sciences. Gyeongju, South Korea, 2015
   Google Scholar
• Xu H, Zhang M, Wang L, Qin JH. Organ-on-a-chip for drug testing in brain diseases. The 19th International Conference on Miniaturized Systems for Chemistry and Life Sciences. Gyeongju, South Korea, 2015
   Google Scholar
• Benson BL, Cotleur AC, Shimizu F, Takeshita Y, Winger RC, Huang A, Marsh G, Ligresti G, Muller WA, Kanda T, et al. Leukocyte-endothelial interactions at the blood-brain barrier studied in fully-human flow-based in vitro models incorporating microfluidics. 14th Annual World Preclinical Congress. Boston, USA, 2015
   Google Scholar
• van der Meer AD, Ingber DE, Herland A. Blood brain barrier-on-chip. 14th Annual World Preclinical Congress, Boston, USA, 2015
   Google Scholar
• Booth R, Kim H. Characterization of a microfluidic in vitro model of the blood-brain barrier (mu BBB). Lab Chip 2012; 12:1784-92; PMID:22422217; http://dx.doi.org/10.1039/c2lc40094d
   PubMed Web of Science ®Google Scholar
• Booth R, Kim H. Permeability Analysis of Neuroactive Drugs Through a Dynamic Microfluidic In Vitro Blood-Brain Barrier Model. Annals Biomed Engineering 2014; 42:2379-91; http://dx.doi.org/10.1007/s10439-014-1086-5
   PubMed Web of Science ®Google Scholar
• Wong AD, Ye M, Levy AF, Rothstein JD, Bergles DE, Searson PC. The blood-brain barrier: an engineering perspective. Frontiers Neuroengineering 2013; 6:7; http://dx.doi.org/10.3389/fneng.2013.00007
   PubMedGoogle Scholar
• Desai SY, Marroni M, Cucullo L, Krizanac-Bengez L, Mayberg MR, Hossain MT, Grant GG, Janigro D. Mechanisms of endothelial survival under shear stress. Endothelium 2002; 9:89-102; PMID:12200960; http://dx.doi.org/10.1080/10623320212004
   PubMed Web of Science ®Google Scholar
• Yeon JH, Na D, Choi K, Ryu SW, Choi C, Park JK. Reliable permeability assay system in a microfluidic device mimicking cerebral vasculatures. Biomed Microdevices 2012; 14:1141-8; PMID:22821236; http://dx.doi.org/10.1007/s10544-012-9680-5
   PubMed Web of Science ®Google Scholar
• Griep LM, Wolbers F, de Wagenaar B, ter Braak PM, Weksler BB, Romero IA, Couraud PO, Vermes I, van der Meer AD, van den Berg A. BBB ON CHIP: microfluidic platform to mechanically and biochemically modulate blood-brain barrier function. Biomed Microdevices 2013; 15:145-50; PMID:22955726; http://dx.doi.org/10.1007/s10544-012-9699-7
   PubMed Web of Science ®Google Scholar
• Achyuta AKH, Conway AJ, Crouse RB, Bannister EC, Lee RN, Katnik CP, Behensky AA, Cuevas J, Sundaram SS. A modular approach to create a neurovascular unit-on-a-chip. Lab Chip 2013; 13:542-53; PMID:23108480; http://dx.doi.org/10.1039/C2LC41033H
   PubMed Web of Science ®Google Scholar
• Prabhakarpandian B, Shen MC, Nichols JB, Mills IR, Sidoryk-Wegrzynowicz M, Aschner M, Pant K. SyM-BBB: a microfluidic blood brain barrier model. Lab Chip 2013; 13:1093-101; PMID:23344641; http://dx.doi.org/10.1039/c2lc41208j
   PubMed Web of Science ®Google Scholar
• Deosarkar SP, Prabhakarpandian B, Wang B, Sheffield JB, Krynska B, Kiani MF. A Novel Dynamic Neonatal Blood-Brain Barrier on a Chip. PLoS One 2015; 10:e0142725; PMID:26555149; http://dx.doi.org/10.1371/journal.pone.0142725
   PubMedGoogle Scholar
• Cho H, Seo JH, Wong KH, Terasaki Y, Park J, Bong K, Arai K, Lo EH, Irimia D. Three-Dimensional Blood-Brain Barrier Model for in vitro Studies of neurovascular pathology. Sci Rep 2015; 5:15222
   PubMed Web of Science ®Google Scholar
• Kim JA, Kim HN, Im S-K, Chung S, Kang JY, Choi N. Collagen-based brain microvasculature model in vitro using three-dimensional printed template. Biomicrofluidics 2015; 9:024115; PMID:25945141http://dx.doi.org/10.1063/1.4917508
   PubMed Web of Science ®Google Scholar
• Brown JA, Pensabene V, Markov DA, Allwardt V, Neely MD, Shi M, Britt CM, Hoilett OS, Yang Q, Brewer BM, et al. Recreating blood-brain barrier physiology and structure on chip: A novel neurovascular microfluidic bioreactor. Biomicrofluidics 2015; 9:054124; PMID:26576206; http://dx.doi.org/10.1063/1.4934713
   PubMed Web of Science ®Google Scholar
• Sellgren KL, Hawkins BT, Grego S. An optically transparent membrane supports shear stress studies in a three-dimensional microfluidic neurovascular unit model. Biomicrofluidics 2015; 9:061102; PMID:26594261; http://dx.doi.org/10.1063/1.4935594
   PubMed Web of Science ®Google Scholar
• Walter FR, Valkai S, Kincses A, Petneházi A, Czeller T, Veszelka S, Ormos P, Deli MA, Dér A. A versatile lab-on-a-chip tool for modeling biological barriers. Sensors Actuators B: Chem 2016; 222:1209-19; http://dx.doi.org/10.1016/j.snb.2015.07.110
   Web of Science ®Google Scholar
• Chaitanya GV, Cromer WE, Wells SR, Jennings MH, Couraud PO, Romero IA, Weksler B, Erdreich-Epstein A, Mathis JM, Minagar A. Gliovascular and cytokine interactions modulate brain endothelial barrier in vitro. J Neuroinflammation 2011; 8:162; PMID:22112345; http://dx.doi.org/10.1186/1742-2094-8-162
   PubMed Web of Science ®Google Scholar
• Yuan F, Leunig M, Berk DA, Jain RK. Microvascular permeability of albumin, vascular surface area, and vascular volume measured in human adenocarcinoma LS174T using dorsal chamber in SCID mice. Microvascular Res 1993; 45:269-89; http://dx.doi.org/10.1006/mvre.1993.1024
   PubMed Web of Science ®Google Scholar
• Li G, Simon MJ, Cancel LM, Shi ZD, Ji X, Tarbell JM, Morrison B, III, Fu BM. Permeability of endothelial and astrocyte cocultures: in vitro blood–brain barrier models for drug delivery studies. Annals Biomed Engineering 2010; 38:2499-511; http://dx.doi.org/10.1007/s10439-010-0023-5
   PubMed Web of Science ®Google Scholar
• Srinivasan B, Kolli AR, Esch MB, Abaci HE, Shuler ML, Hickman JJ. TEER Measurement Techniques for In Vitro Barrier Model Systems. Jala 2015; 20:107-26; PMID:25586998
   PubMed Web of Science ®Google Scholar
• Odijk M, van der Meer AD, Levner D, Kim HJ, van der Helm MW, Segerink LI, Frimat J-P, Hamilton GA, Ingber DE, van den Berg A. Measuring direct current trans-epithelial electrical resistance in organ-on-a-chip microsystems. Lab Chip 2015; 15:745-52; PMID:25427650; http://dx.doi.org/10.1039/C4LC01219D
   PubMed Web of Science ®Google Scholar
• Thuenauer R, Rodriguez-Boulan E, Romer W. Microfluidic approaches for epithelial cell layer culture and characterisation. Analyst 2014; 139:3206-18; PMID:24668405; http://dx.doi.org/10.1039/C4AN00056K
   PubMed Web of Science ®Google Scholar
• Benson K, Cramer S, Galla HJ. Impedance-based cell monitoring: barrier properties and beyond. Fluids Barriers CNS 2013; 10:5; PMID:23305242; http://dx.doi.org/10.1186/2045-8118-10-5
   PubMedGoogle Scholar
• Krug SM, Fromm M, Günzel D. Two-Path impedance spectroscopy for measuring paracellular and transcellular epithelial resistance. Biophysical J 2009; 97:2202-11; http://dx.doi.org/10.1016/j.bpj.2009.08.003
   PubMed Web of Science ®Google Scholar
• 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. Scientific Rep 2014; 4:4160
   PubMed Web of Science ®Google Scholar
• Lippmann ES, Azarin SM, Kay JE, Nessler RA, Wilson HK, Al-Ahmad A, Palecek SP, Shusta EV. Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat Biotechnol 2012; 30:783-91; PMID:22729031; http://dx.doi.org/10.1038/nbt.2247
   PubMed Web of Science ®Google Scholar
• Bellin M, Marchetto MC, Gage FH, Mummery CL. Induced pluripotent stem cells: the new patient? Nat Rev Mol Cell Biol 2012; 13:713-26; PMID:23034453; http://dx.doi.org/10.1038/nrm3448
   PubMed Web of Science ®Google Scholar
• He YR, Yao Y, Tsirka SE, Cao Y. Cell-Culture Models of the Blood-Brain Barrier. Stroke 2014; 45:2514-26; PMID:24938839; http://dx.doi.org/10.1161/STROKEAHA.114.005427
   PubMed Web of Science ®Google Scholar
• Van der Meer A, Poot A, Feijen J, Vermes I. Analyzing shear stress-induced alignment of actin filaments in endothelial cells with a microfluidic assay. Biomicrofluidics 2010; 4:011103; http://dx.doi.org/10.1063/1.3366720
   PubMed Web of Science ®Google Scholar
• Booth R, Noh S, Kim H. A multiple-channel, multiple-assay platform for characterization of full-range shear stress effects on vascular endothelial cells. Lab Chip 2014; 14:1880-90; PMID:24718713; http://dx.doi.org/10.1039/c3lc51304a
   PubMed Web of Science ®Google Scholar
• Gulino-Debrac D. Mechanotransduction at the basis of endothelial barrier function. Tissue Barriers 2013; 1:e24180; PMID:24665386; http://dx.doi.org/10.4161/tisb.24180
   PubMedGoogle Scholar
• Shemesh J, Jalilian I, Shi A, Heng Yeoh G, Knothe Tate ML, Ebrahimi Warkiani M. Flow-induced stress on adherent cells in microfluidic devices. Lab Chip 2015; 15:4114-27; PMID:26334370; http://dx.doi.org/10.1039/C5LC00633C
   PubMed Web of Science ®Google Scholar
• Son Y. Determination of shear viscosity and shear rate from pressure drop and flow rate relationship in a rectangular channel. Polymer 2007; 48:632-7; http://dx.doi.org/10.1016/j.polymer.2006.11.048
   Web of Science ®Google Scholar
• Vanapalli S, Van den Ende D, Duits M, Mugele F. Scaling of interface displacement in a microfluidic comparator. Appl Phys Lett 2007; 90:114109; http://dx.doi.org/10.1063/1.2713800
   Web of Science ®Google Scholar
• Hovell CM, Sei YJ, Kim Y. Microengineered Vascular Systems for Drug Development. J Lab Automation 2014:2211068214560767
   Google Scholar
• Reproduced from Booth R, Kim H. Characterization of a microfluidic in vitro model of the blood-brain barrier (mu BBB). Lab Chip 2012; 12:1784-92, with permission of The Royal Society of Chemistry; PMID:22422217; http://dx.doi.org/10.1039/c2lc40094d
   PubMed Web of Science ®Google Scholar
• Yeon JH, Na D, Choi K, Ryu SW, Choi C, Park JK. With kind permission from Springer Science+Business Media: Biomedical Microdevices, Reliable permeability assay system in a microfluidic device mimicking cerebral vasculatures 2012; 14:1141-1148, figure 1b; PMID:22821236
   PubMedGoogle Scholar
• Griep LM, Wolbers F, de Wagenaar B, ter Braak PM, Weksler BB, Romero IA, Couraud PO, Vermes I, van der Meer AD, van den Berg A. With kind permission from Springer Science+Business Media: Biomedical Microdevices, BBB ON CHIP: microfluidic platform to mechanically and biochemically modulate blood-brain barrier function 2013; 15:145-150, figure 1a and 1c; PMID:22955726
   PubMedGoogle Scholar
• Reproduced from Achyuta AKH, Conway AJ, Crouse RB, Bannister EC, Lee RN, Katnik CP, Behensky AA, Cuevas J, Sundaram SS. A modular approach to create a neurovascular unit-on-a-chip. Lab Chip 2013; 13:542-53, with permission of The Royal Society of Chemistry; PMID:23108480; http://dx.doi.org/10.1039/C2LC41033H
   PubMed Web of Science ®Google Scholar
• Reproduced fromPrabhakarpandian B, Shen MC, Nichols JB, Mills IR, Sidoryk-Wegrzynowicz M, Aschner M, Pant K. SyM-BBB: a microfluidic blood brain barrier model. Lab Chip 2013; 13:1093-101, with permission of The Royal Society of Chemistry; PMID:23344641; http://dx.doi.org/10.1039/c2lc41208j
   PubMed Web of Science ®Google Scholar
• Reproduced with permission from Kim JA, Kim HN, Im SK, Chung S, Kang JY, Choi N. Collagen-based brain microvasculature model in vitro using three-dimensional printed template. Biomicrofluidics 2015; 9:024115. Copyright 2015, AIP Publishing LLC
   Web of Science ®Google Scholar
• Reprinted with permission from Brown JA, Pensabene V, Markov DA, Allwardt V, Neely MD, Shi M, Britt CM, Hoilett OS, Yang Q, Brewer BM, et al. Recreating blood-brain barrier physiology and structure on chip: A novel neurovascular microfluidic bioreactor. Biomicrofluidics 2015; 9:054124. Copyright 2015, AIP Publishing LLC
   PubMed Web of Science ®Google Scholar
• Reprinted with permission from Sellgren KL, Hawkins BT, Grego S. An optically transparent membrane supports shear stress studies in a three-dimensional microfluidic neurovascular unit model. Biomicrofluidics 2015; 9:061102. Copyright 2015, AIP Publishing LLC
   Web of Science ®Google Scholar
• Reprinted from Sensors and Actuators B: Chemical, 222, Walter FR, Valkai S, Kincses A, Petneházi A, Czeller T, Veszelka S, Ormos P, Deli MA, Dér A. A versatile lab-on-a-chip tool for modeling biological barriers, 1209-1219, Copyright 2016, with permission from Elsevier
   Google Scholar