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

Tissue Barriers

Volumn 4, Issue 1, 2016, Pages

  van der Helm, Marinke W ^a   van der Meer, Andries D ^b   Eijkel, Jan C T ^a   van den Berg, Albert ^a   Segerink, Loes I ^a  

^a UNIVERSITY OF TWENTE   (Netherlands)

^b UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

BBBs on chips; blood brain barrier; endothelial cells; microfabrication; microfluidics; organs on chips

Indexed keywords

LACTATE DEHYDROGENASE; PROTEIN ZO1; TUMOR NECROSIS FACTOR ALPHA;

BIOTECHNOLOGICAL PROCEDURES; BLOOD BRAIN BARRIER; ELECTRIC RESISTANCE; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; FLUORESCENCE MICROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; MICROFLUIDICS; ORGAN ON CHIP TECHNOLOGY; PHASE CONTRAST MICROSCOPY; REVIEW; SHEAR STRESS; TRANSENDOTHELIAL ELECTRICAL RESISTANCE; ANIMAL; CAPILLARY PERMEABILITY; CYTOLOGY; ENDOTHELIUM CELL; METABOLISM; MICROCHIP ANALYSIS; PROCEDURES;

ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; ENDOTHELIAL CELLS; HUMANS; MICROCHIP ANALYTICAL PROCEDURES; MICROFLUIDICS;

EID: 84960868535     PISSN: 21688362     EISSN: 21688370     Source Type: Journal    
DOI: 10.1080/21688370.2016.1142493     Document Type: Review

References (76)

1. N.J.Abbott. 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
2. Y.Serlin, I.Shelef, B.Knyazer, A.Friedman. 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
3. W.M.Pardridge. 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
4. N.J.Abbott, L.Rönnbäck, E.Hansson. Astrocyte–endothelial interactions at the blood–brain barrier. Nat Rev Neurosci 2006; 7: 41- 53; PMID: 16371949; http://dx.doi.org/ 10.1038/nrn1824
5. N.J.Abbott. 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
6. A.Wolff, M.Antfolk, B.Brodin, M.Tenje. 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
7. D.Huh, Y.S.Torisawa, G.A.Hamilton, H.J.Kim, D.E.Ingber. Microengineered physiological biomimicry: organs-on-chips. Lab chip 2012; 12: 2156- 64; PMID: 22555377; http://dx.doi.org/ 10.1039/c2lc40089h
8. S.Perrin. Preclinical research: Make mouse studies work. Nature 2014; 507: 423- 5; PMID: 24678540; http://dx.doi.org/ 10.1038/507423a
9. D.Pamies, T.Hartung, H.T.Hogberg. Biological and medical applications of a brain-on-a-chip. Exp Biol Med 2014; 239: 1096- 107; http://dx.doi.org/ 10.1177/1535370214537738
10. D.G.Hackam. Translating animal research into clinical benefit. BMJ: Br Med J 2007; 334: 163; http://dx.doi.org/ 10.1136/bmj.39104.362951.80
11. H.B.van der Worp, D.W.Howells, E.S.Sena, M.J.Porritt, S.Rewell, V.O'Collins, M.R.Macleod. 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
12. N.Shanks, R.Greek, J.Greek. Are animal models predictive for humans? Philosophy Ethics Humanities Med 2009; 4: 2; http://dx.doi.org/ 10.1186/1747-5341-4-2
13. S.Perrin. Preclinical research: Make mouse studies work. Nature 2014; 507:423-5; http://dx.doi.org/ 10.1038/507423a
14. R.Shawahna, X.Declèves, J.-M.Scherrmann. 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
15. P.Naik, L.Cucullo. 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
16. A.D.van der Meer, A.van den Berg. Organs-on-chips: breaking the in vitro impasse. Integrative Biol 2012; 4: 461- 70; http://dx.doi.org/ 10.1039/c2ib00176d
17. N.J.Abbott, D.M.Dolman, S.Yusof, A.Reichel. In Vitro Models of CNS Barriers. In: M.Hammarlund-Udenaes, E.C.M.de Lange, R.G.Thorne, eds. Drug Delivery to the Brain: Springer New York, 2014: 163- 97
18. K.Hatherell, P.O.Couraud, I.A.Romero, B.Weksler, G.J.Pilkington. 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
19. S.N.Bhatia, D.E.Ingber. Microfluidic organs-on-chips. Nat Biotechnol 2014; 32: 760- 72; PMID: 25093883; http://dx.doi.org/ 10.1038/nbt.2989
20. C.Moraes, G.Mehta, S.Lesher-Perez, S.Takayama. 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
21. D.Huh, B.D.Matthews, A.Mammoto, M.Montoya-Zavala, H.Y.Hsin, D.E.Ingber. Reconstituting organ-level lung functions on a chip. Science 2010; 328: 1662- 8; PMID: 20576885; http://dx.doi.org/ 10.1126/science.1188302
22. H.J.Kim, D.Huh, G.Hamilton, D.E.Ingber. 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
23. H.J.Kim, D.E.Ingber. 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
24. E.Westein, A.D.van der Meer, M.J.E.Kuijpers, J.P.Frimat, A.van den Berg, J.W.M.Heemskerk. 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
25. M.Nedergaard. Garbage Truck of the Brain. Science (New York, NY) 2013; 340: 1529- 30; http://dx.doi.org/ 10.1126/science.1240514
26. J.J.Iliff, M.Nedergaard. Is there a cerebral lymphatic system? Stroke; J Cerebral Circulation 2013; 44: S93- S5; http://dx.doi.org/ 10.1161/STROKEAHA.112.678698
27. A.D.van der Meer, F.Wolbers, I.Vermes, A.van den Berg. Blood-brain Barrier (BBB): An Overview of the Research of the Blood-brain Barrier Using Microfluidic Devices. In: A.van den Berg, L.I.Segerink, eds. Microfluidics for Med Applications, 2014: 40- 56
28. G.Adriani, D.Ma, A.Pavesi, E.Goh, R.D.Kamm. A microfluidic model of the blood brain barrier. 4th THERMIS World Congress. Boston, USA: Tissue Engineering Part A, 2015: S40- S
29. J.Yeste, X.Illa, A.Guimerà, R.Villa. 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
30. M.W.van der Helm, M.Odijk, J.-P.Frimat, J.C.Eijkel, A.van den Berg, L.I.Segerink. 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
31. H.Xu, Z.Y.Li, Y.Yu, J.H.Qin. 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
32. H.Xu, M.Zhang, L.Wang, J.H.Qin. 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
33. B.L.Benson, A.C.Cotleur, F.Shimizu, Y.Takeshita, R.C.Winger, A.Huang, G.Marsh, G.Ligresti, W.A.Muller, T.Kanda, 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
34. A.D.van der Meer, D.E.Ingber, A.Herland. Blood brain barrier-on-chip. 14th Annual World Preclinical Congress, Boston, USA, 2015
35. R.Booth, H.Kim. 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
36. R.Booth, H.Kim. 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
37. A.D.Wong, M.Ye, A.F.Levy, J.D.Rothstein, D.E.Bergles, P.C.Searson. The blood-brain barrier: an engineering perspective. Frontiers Neuroengineering 2013; 6: 7; http://dx.doi.org/ 10.3389/fneng.2013.00007
38. S.Y.Desai, M.Marroni, L.Cucullo, L.Krizanac-Bengez, M.R.Mayberg, M.T.Hossain, G.G.Grant, D.Janigro. Mechanisms of endothelial survival under shear stress. Endothelium 2002; 9: 89- 102; PMID: 12200960; http://dx.doi.org/ 10.1080/10623320212004
39. J.H.Yeon, D.Na, K.Choi, S.W.Ryu, C.Choi, J.K.Park. 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
40. L.M.Griep, F.Wolbers, B.de Wagenaar, P.M.ter Braak, B.B.Weksler, I.A.Romero, P.O.Couraud, I.Vermes, A.D.van der Meer, A.van den Berg. 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
41. A.K.H.Achyuta, A.J.Conway, R.B.Crouse, E.C.Bannister, R.N.Lee, C.P.Katnik, A.A.Behensky, J.Cuevas, S.S.Sundaram. 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
42. B.Prabhakarpandian, M.C.Shen, J.B.Nichols, I.R.Mills, M.Sidoryk-Wegrzynowicz, M.Aschner, K.Pant. SyM-BBB: a microfluidic blood brain barrier model. Lab Chip 2013; 13: 1093- 101; PMID: 23344641; http://dx.doi.org/ 10.1039/c2lc41208j
43. S.P.Deosarkar, B.Prabhakarpandian, B.Wang, J.B.Sheffield, B.Krynska, M.F.Kiani. 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
44. H.Cho, J.H.Seo, K.H.Wong, Y.Terasaki, J.Park, K.Bong, K.Arai, E.H.Lo, D.Irimia. Three-Dimensional Blood-Brain Barrier Model for in vitro Studies of neurovascular pathology. Sci Rep 2015; 5: 15222
45. J.A.Kim, H.N.Kim, S.-K.Im, S.Chung, J.Y.Kang, N.Choi. 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
46. J.A.Brown, V.Pensabene, D.A.Markov, V.Allwardt, M.D.Neely, M.Shi, C.M.Britt, O.S.Hoilett, Q.Yang, B.M.Brewer, 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
47. K.L.Sellgren, B.T.Hawkins, S.Grego. 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
48. F.R.Walter, S.Valkai, A.Kincses, A.Petneházi, T.Czeller, S.Veszelka, P.Ormos, M.A.Deli, A.Dér. 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
49. G.V.Chaitanya, W.E.Cromer, S.R.Wells, M.H.Jennings, P.O.Couraud, I.A.Romero, B.Weksler, A.Erdreich-Epstein, J.M.Mathis, A.Minagar. 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
50. F.Yuan, M.Leunig, D.A.Berk, R.K.Jain. 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
51. G.Li, M.J.Simon, L.M.Cancel, Z.D.Shi, X.Ji, J.M.Tarbell, B.Morrison, III, B.M.Fu. 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
52. B.Srinivasan, A.R.Kolli, M.B.Esch, H.E.Abaci, M.L.Shuler, J.J.Hickman. TEER Measurement Techniques for In Vitro Barrier Model Systems. Jala 2015; 20: 107- 26; PMID: 25586998
53. M.Odijk, A.D.van der Meer, D.Levner, H.J.Kim, M.W.van der Helm, L.I.Segerink, J.-P.Frimat, G.A.Hamilton, D.E.Ingber, A.van den Berg. 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
54. R.Thuenauer, E.Rodriguez-Boulan, W.Romer. Microfluidic approaches for epithelial cell layer culture and characterisation. Analyst 2014; 139: 3206- 18; PMID: 24668405; http://dx.doi.org/ 10.1039/C4AN00056K
55. K.Benson, S.Cramer, H.J.Galla. 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
56. S.M.Krug, M.Fromm, D.Günzel. 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
57. E.S.Lippmann, A.Al-Ahmad, S.M.Azarin, S.P.Palecek, E.V.Shusta. A retinoic acid-enhanced, multicellular human blood-brain barrier model derived from stem cell sources. Scientific Rep 2014; 4: 4160
58. E.S.Lippmann, S.M.Azarin, J.E.Kay, R.A.Nessler, H.K.Wilson, A.Al-Ahmad, S.P.Palecek, E.V.Shusta. 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
59. M.Bellin, M.C.Marchetto, F.H.Gage, C.L.Mummery. 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
60. Y.R.He, Y.Yao, S.E.Tsirka, Y.Cao. Cell-Culture Models of the Blood-Brain Barrier. Stroke 2014; 45: 2514- 26; PMID: 24938839; http://dx.doi.org/ 10.1161/STROKEAHA.114.005427
61. A.Van der Meer, A.Poot, J.Feijen, I.Vermes. 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
62. R.Booth, S.Noh, H.Kim. 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
63. D.Gulino-Debrac. Mechanotransduction at the basis of endothelial barrier function. Tissue Barriers 2013; 1: e24180; PMID: 24665386; http://dx.doi.org/ 10.4161/tisb.24180
64. J.Shemesh, I.Jalilian, A.Shi, G.Heng Yeoh, M.L.Knothe Tate, M.Ebrahimi Warkiani. Flow-induced stress on adherent cells in microfluidic devices. Lab Chip 2015; 15: 4114- 27; PMID: 26334370; http://dx.doi.org/ 10.1039/C5LC00633C
65. Y.Son. 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
66. S.Vanapalli, D.Van den Ende, M.Duits, F.Mugele. Scaling of interface displacement in a microfluidic comparator. Appl Phys Lett 2007; 90: 114109; http://dx.doi.org/ 10.1063/1.2713800
67. C.M.Hovell, Y.J.Sei, Y.Kim. Microengineered Vascular Systems for Drug Development. J Lab Automation 2014:
68. Reproduced from R.Booth, H.Kim. 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
69. J.H.Yeon, D.Na, K.Choi, S.W.Ryu, C.Choi, J.K.Park. 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
70. L.M.Griep, F.Wolbers, B.de Wagenaar, P.M.ter Braak, B.B.Weksler, I.A.Romero, P.O.Couraud, I.Vermes, A.D.van der Meer, A.van den Berg. 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
71. Reproduced from A.K.H.Achyuta, A.J.Conway, R.B.Crouse, E.C.Bannister, R.N.Lee, C.P.Katnik, A.A.Behensky, J.Cuevas, S.S.Sundaram. 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
72. Reproduced from B.Prabhakarpandian, M.C.Shen, J.B.Nichols, I.R.Mills, M.Sidoryk-Wegrzynowicz, M.Aschner, K.Pant. 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
73. Reproduced with permission from J.A.Kim, H.N.Kim, S.K.Im, S.Chung, J.Y.Kang, N.Choi. Collagen-based brain microvasculature model in vitro using three-dimensional printed template. Biomicrofluidics 2015; 9: 024115. Copyright 2015, AIP Publishing LLC
74. Reprinted with permission from J.A.Brown, V.Pensabene, D.A.Markov, V.Allwardt, M.D.Neely, M.Shi, C.M.Britt, O.S.Hoilett, Q.Yang, B.M.Brewer, 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
75. Reprinted with permission from K.L.Sellgren, B.T.Hawkins, S.Grego. 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
76. Reprinted from Sensors and Actuators B: Chemical, 222, F.R.Walter, S.Valkai, A.Kincses, A.Petneházi, T.Czeller, S.Veszelka, P.Ormos, M.A.Deli, A.Dér. A versatile lab-on-a-chip tool for modeling biological barriers, 1209- 1219, Copyright 2016, with permission from Elsevier