Impedance analysis of GPCR-mediated changes in endothelial barrier function: overview and fundamental considerations for stable and reproducible measurements

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 10, 2015, Pages 2193-2218

  Stolwijk, Judith A ^a,b   Matrougui, Khalid ^c   Renken, Christian W ^b   Trebak, Mohamed ^a  

^a SUNY POLYTECHNIC INSTITUTE   (United States)

^b Applied BioPhysics Inc   (United States)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

Barrier function; ECIS; Endothelial cells; Impedance; Resistance; TEER

Indexed keywords

G PROTEIN COUPLED RECEPTOR; HISTAMINE; SPHINGOSINE 1 PHOSPHATE; THROMBIN;

ARTICLE; BIOPHYSICS; CAPILLARY ENDOTHELIAL CELL; CELL CULTURE; CELL JUNCTION; DATA ANALYSIS; ELECTRIC CELL SUBSTRATE IMPEDANCE SENSING; ELECTRIC RESISTANCE; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; ELECTRODE; ENDOTHELIUM CELL; HUMAN; IMPEDANCE; MOLECULAR BIOLOGY; MONITORING; PRIORITY JOURNAL; REPRODUCIBILITY; TRANSENDOTHELIAL ELECTRICAL RESISTANCE; AGONISTS; ALGORITHM; CYTOLOGY; ELECTROPHYSIOLOGY; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGY; PROCEDURES; VASCULAR ENDOTHELIUM;

ALGORITHMS; CELLS, CULTURED; ELECTRIC IMPEDANCE; ELECTROPHYSIOLOGY; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; MEMBRANE POTENTIALS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84941422122     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1674-0     Document Type: Article

References (125)

1. Adam AP, Sharenko AL, Pumiglia K, Vincent PA (2010) Src-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J Biol Chem 285(10):7045–7055. doi:10.1074/jbc.M109.079277
2. Aman J, van Bezu J, Damanafshan A, Huveneers S, Eringa EC, Vogel SM, Groeneveld AB, Vonk Noordegraaf A, van Hinsbergh VW, van Nieuw Amerongen GP (2012) Effective treatment of edema and endothelial barrier dysfunction with imatinib. Circulation 126(23):2728–2738. doi:10.1161/CIRCULATIONAHA.112.134304
3. Anderson JM, Van Itallie CM (2009) Physiology and function of the tight junction. Cold Spring Harbor Perspect Biol 1(2):a002584. doi:10.1101/cshperspect.a002584
4. Artus C, Glacial F, Ganeshamoorthy K, Ziegler N, Godet M, Guilbert T, Liebner S, Couraud PO (2014) The Wnt/planar cell polarity signaling pathway contributes to the integrity of tight junctions in brain endothelial cells. J Cerebral Blood Flow Metabol Off J Int Soc Cerebral Blood Flow Metabol 34(3):433–440. doi:10.1038/jcbfm.2013.213
5. Atienza JM, Yu N, Wang X, Xu X, Abassi Y (2006) Label-free and real-time cell-based kinase assay for screening selective and potent receptor tyrosine kinase inhibitors using microelectronic sensor array. J Biomol Screen 11(6):634–643. doi:10.1177/1087057106289334
6. Atienza JM, Zhu J, Wang X, Xu X, Abassi Y (2005) Dynamic monitoring of cell adhesion and spreading on microelectronic sensor arrays. J Biomol Screen 10(8):795–805. doi:10.1177/1087057105279635
7. Bagnaninchi PO, Drummond N (2011) Real-time label-free monitoring of adipose-derived stem cell differentiation with electric cell-substrate impedance sensing. Proc Natl Acad Sci U S A 108(16):6462–6467. doi:10.1073/pnas.1018260108
8. Barsoukov E, Macdonald JR (2005) Impedance spectroscopy: theory, experiment, and applications. Wiley, Hoboken
9. Bazzoni G (2006) Endothelial tight junctions: permeable barriers of the vessel wall. Thromb Haemost 95(1):36–42
10. Becker PM, Verin AD, Booth MA, Liu F, Birukova A, Garcia JG (2001) Differential regulation of diverse physiological responses to VEGF in pulmonary endothelial cells. Am J Physiol Lung Cell Molec Physiol 281(6):L1500–L1511
11. Becker PM, Waltenberger J, Yachechko R, Mirzapoiazova T, Sham JS, Lee CG, Elias JA, Verin AD (2005) Neuropilin-1 regulates vascular endothelial growth factor-mediated endothelial permeability. Circ Res 96(12):1257–1265. doi:10.1161/01.RES.0000171756.13554.49
12. Benson K, Cramer S, Galla HJ (2013) Impedance-based cell monitoring: barrier properties and beyond. Fluids Barriers CNS 10(1):5. doi:10.1186/2045-8118-10-5
13. Bernas MJ, Cardoso FL, Daley SK, Weinand ME, Campos AR, Ferreira AJ, Hoying JB, Witte MH, Brites D, Persidsky Y, Ramirez SH, Brito MA (2010) Establishment of primary cultures of human brain microvascular endothelial cells to provide an in vitro cellular model of the blood–brain barrier. Nat Protoc 5(7):1265–1272. doi:10.1038/nprot.2010.76
14. Birukova AA, Cokic I, Moldobaeva N, Birukov KG (2009) Paxillin is involved in the differential regulation of endothelial barrier by HGF and VEGF. Am J Respir Cell Mol Biol 40(1):99–107. doi:10.1165/rcmb.2008-0099OC
15. Bogatcheva NV, Zemskova MA, Kovalenkov Y, Poirier C, Verin AD (2009) Molecular mechanisms mediating protective effect of cAMP on lipopolysaccharide (LPS)-induced human lung microvascular endothelial cells (HLMVEC) hyperpermeability. J Cell Physiol 221(3):750–759. doi:10.1002/jcp.21913
16. Bogatcheva NV, Zemskova MA, Poirier C, Mirzapoiazova T, Kolosova I, Bresnick AR, Verin AD (2011) The suppression of myosin light chain (MLC) phosphorylation during the response to lipopolysaccharide (LPS): beneficial or detrimental to endothelial barrier? J Cell Physiol 226(12):3132–3146. doi:10.1002/jcp.22669
17. Cecchelli R, Aday S, Sevin E, Almeida C, Culot M, Dehouck L, Coisne C, Engelhardt B, Dehouck MP, Ferreira L (2014) A stable and reproducible human blood–brain barrier model derived from hematopoietic stem cells. PLoS One 9(6):e99733. doi:10.1371/journal.pone.0099733
18. Chatterjee A, Snead C, Yetik-Anacak G, Antonova G, Zeng J, Catravas JD (2008) Heat shock protein 90 inhibitors attenuate LPS-induced endothelial hyperpermeability. Am J Physiol Lung Cell Molec Physiol 294(4):L755–L763. doi:10.1152/ajplung.00350.2007
19. Chen XL, Nam JO, Jean C, Lawson C, Walsh CT, Goka E, Lim ST, Tomar A, Tancioni I, Uryu S, Guan JL, Acevedo LM, Weis SM, Cheresh DA, Schlaepfer DD (2012) VEGF-induced vascular permeability is mediated by FAK. Dev Cell 22(1):146–157. doi:10.1016/j.devcel.2011.11.002
20. Cohen-Kashi Malina K, Cooper I, Teichberg VI (2009) Closing the gap between the in-vivo and in-vitro blood–brain barrier tightness. Brain Res 1284:12–21. doi:10.1016/j.brainres.2009.05.072
21. Cooper JA, Del Vecchio PJ, Minnear FL, Burhop KE, Selig WM, Garcia JG, Malik AB (1987) Measurement of albumin permeability across endothelial monolayers in vitro. J Appl Physiol 62(3):1076–1083
22. Daniels BP, Cruz-Orengo L, Pasieka TJ, Couraud PO, Romero IA, Weksler B, Cooper JA, Doering TL, Klein RS (2013) Immortalized human cerebral microvascular endothelial cells maintain the properties of primary cells in an in vitro model of immune migration across the blood brain barrier. J Neurosci Methods 212(1):173–179. doi:10.1016/j.jneumeth.2012.10.001
23. Davies PF, Remuzzi A, Gordon EJ, Dewey CF Jr, Gimbrone MA Jr (1986) Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro. Proc Natl Acad Sci U S A 83(7):2114–2117
24. Davis GE, Senger DR (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 97(11):1093–1107. doi:10.1161/01.RES.0000191547.64391.e3
25. De Blasio BF, Laane M, Walmann T, Giaever I (2004) Combining optical and electrical impedance techniques for quantitative measurement of confluence in MDCK-I cell cultures. BioTechniques 36 (4):650–654, 656, 658 passim
26. de Vries HE, Blom-Roosemalen MC, de Boer AG, van Berkel TJ, Breimer DD, Kuiper J (1996) Effect of endotoxin on permeability of bovine cerebral endothelial cell layers in vitro. J Pharmacol Experiment Therapeutics 277(3):1418–1423
27. DeMaio L, Tarbell JM, Scaduto RC Jr, Gardner TW, Antonetti DA (2004) A transmural pressure gradient induces mechanical and biological adaptive responses in endothelial cells. Am J Physiol Heart Circulat Physiol 286(2):H731–H741. doi:10.1152/ajpheart.00427.2003
28. DePaola N, Phelps JE, Florez L, Keese CR, Minnear FL, Giaever I, Vincent P (2001) Electrical impedance of cultured endothelium under fluid flow. Ann Biomed Eng 29(8):648–656
29. Dewi BE, Takasaki T, Kurane I (2004) In vitro assessment of human endothelial cell permeability: effects of inflammatory cytokines and dengue virus infection. J Virol Methods 121(2):171–180. doi:10.1016/j.jviromet.2004.06.013
30. Dubrovskyi O, Birukova AA, Birukov KG (2013) Measurement of local permeability at subcellular level in cell models of agonist- and ventilator-induced lung injury. Lab Investig J Technical Methods Pathol 93(2):254–263. doi:10.1038/labinvest.2012.159
31. Ehret R, Baumann W, Brischwein M, Schwinde A, Stegbauer K, Wolf B (1997) Monitoring of cellular behaviour by impedance measurements on interdigitated electrode structures. Biosensors Bioelectro 12(1):29–41
32. Ehret R, Baumann W, Brischwein M, Schwinde A, Wolf B (1998) On-line control of cellular adhesion with impedance measurements using interdigitated electrode structures. Med Biol Eng Comput 36(3):365–370
33. Estrada R, Zeng Q, Lu H, Sarojini H, Lee JF, Mathis SP, Sanchez T, Wang E, Kontos CD, Lin CY, Hla T, Haribabu B, Lee MJ (2008) Up-regulating sphingosine 1-phosphate receptor-2 signaling impairs chemotactic, wound-healing, and morphogenetic responses in senescent endothelial cells. J Biol Chem 283(44):30363–30375. doi:10.1074/jbc.M804392200
34. Faurobert E, Rome C, Lisowska J, Manet-Dupe S, Boulday G, Malbouyres M, Balland M, Bouin AP, Keramidas M, Bouvard D, Coll JL, Ruggiero F, Tournier-Lasserve E, Albiges-Rizo C (2013) CCM1-ICAP-1 complex controls beta1 integrin-dependent endothelial contractility and fibronectin remodeling. J Cell Biol 202(3):545–561. doi:10.1083/jcb.201303044
35. Franke RP, Grafe M, Schnittler H, Seiffge D, Mittermayer C, Drenckhahn D (1984) Induction of human vascular endothelial stress fibres by fluid shear stress. Nature 307(5952):648–649
36. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D (2001) Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108(5):689–701. doi:10.1172/JCI12450
37. Garcia JG, Siflinger-Birnboim A, Bizios R, Del Vecchio PJ, Fenton JW 2nd, Malik AB (1986) Thrombin-induced increase in albumin permeability across the endothelium. J Cell Physiol 128(1):96–104. doi:10.1002/jcp.1041280115
38. Giaever I, Keese CR (1984) Monitoring fibroblast behavior in tissue culture with an applied electric field. Proc Natl Acad Sci U S A 81(12):3761–3764
39. Giaever I, Keese CR (1991) Micromotion of mammalian cells measured electrically. Proc Natl Acad Sci U S A 88(17):7896–7900
40. Heijink IH, van Oosterhout A, Kapus A (2010) Epidermal growth factor receptor signalling contributes to house dust mite-induced epithelial barrier dysfunction. Euro Respirat J 36(5):1016–1026. doi:10.1183/09031936.00125809
41. Herron CR, Lowery AM, Hollister PR, Reynolds AB, Vincent PA (2011) p120 regulates endothelial permeability independently of its NH2 terminus and Rho binding. Am J Physiol Heart Circulat Physiol 300(1):H36–H48. doi:10.1152/ajpheart.00812.2010
42. Hofmann U, Michaelis S, Winckler T, Wegener J, Feller KH (2013) A whole-cell biosensor as in vitro alternative to skin irritation tests. Biosens Bioelectron 39(1):156–162. doi:10.1016/j.bios.2012.07.075
43. Hoheisel D, Nitz T, Franke H, Wegener J, Hakvoort A, Tilling T, Galla HJ (1998) Hydrocortisone reinforces the blood–brain barrier in a serum-free culture system. Biochem Biophys Res Commun 224(1):312–316
44. Janshoff A, Wegener J, Sieber M, Galla HJ (1996) Double-mode impedance analysis of epithelial cell monolayers cultured on shear wave resonators. Eur Biophys J 25:93–103
45. Karczewski J, Troost FJ, Konings I, Dekker J, Kleerebezem M, Brummer RJ, Wells JM (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am J Physiol Gastrointestinal Liver Physiol 298(6):G851–G859. doi:10.1152/ajpgi.00327.2009
46. Keese CR, Bhawe K, Wegener J, Giaever I (2002) Real-time impedance assay to follow the invasive activities of metastatic cells in culture. BioTechniques 33 (4):842–844, 846, 848–850
47. Keese CR, Wegener J, Walker SR, Giaever I (2004) Electrical wound-healing assay for cells in vitro. Proc Natl Acad Sci U S A 101(6):1554–1559. doi:10.1073/pnas.0307588100
48. Kim YV, Di Cello F, Hillaire CS, Kim KS (2004) Differential Ca2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am J Physiol Cell Physiol 286(1):C31–C42. doi:10.1152/ajpcell.00157.2003
49. Kobayashi K, Tsubosaka Y, Hori M, Narumiya S, Ozaki H, Murata T (2013) Prostaglandin D2-DP signaling promotes endothelial barrier function via the cAMP/PKA/Tiam1/Rac1 pathway. Arterioscler Thromb Vasc Biol 33(3):565–571. doi:10.1161/ATVBAHA.112.300993
50. Kobayashi N, Nishi T, Hirata T, Kihara A, Sano T, Igarashi Y, Yamaguchi A (2006) Sphingosine 1-phosphate is released from the cytosol of rat platelets in a carrier-mediated manner. J Lipid Res 47(3):614–621. doi:10.1194/jlr. M500468-JLR200
51. Konya V, Ullen A, Kampitsch N, Theiler A, Philipose S, Parzmair GP, Marsche G, Peskar BA, Schuligoi R, Sattler W, Heinemann A (2013) Endothelial E-type prostanoid 4 receptors promote barrier function and inhibit neutrophil trafficking. The Journal of allergy and clinical immunology 131 (2):532–540 e531-532. doi:10.1016/j.jaci.2012.05.008
52. Kuo YC, Su CH, Liu CY, Chen TH, Chen CP, Wang HS (2009) Transforming growth factor-beta induces CD44 cleavage that promotes migration of MDA-MB-435 s cells through the up-regulation of membrane type 1-matrix metalloproteinase. Int J Cancer J Int du Cancer 124(11):2568–2576. doi:10.1002/ijc.24263
53. Lamontagne D, Pohl U, Busse R (1992) Mechanical deformation of vessel wall and shear stress determine the basal release of endothelium-derived relaxing factor in the intact rabbit coronary vascular bed. Circ Res 70(1):123–130
54. Lien CF, Mohanta SK, Frontczak-Baniewicz M, Swinny JD, Zablocka B, Gorecki DC (2012) Absence of glial alpha-dystrobrevin causes abnormalities of the blood–brain barrier and progressive brain edema. J Biol Chem 287(49):41374–41385. doi:10.1074/jbc.M112.400044
55. Liu Q, Yu J, Xiao L, Tang JC, Zhang Y, Wang P, Yang M (2009) Impedance studies of bio-behavior and chemosensitivity of cancer cells by micro-electrode arrays. Biosens Bioelectron 24(5):1305–1310. doi:10.1016/j.bios.2008.07.044
56. Lo CM, Keese CR, Giaever I (1993) Monitoring motion of confluent cells in tissue culture. Exp Cell Res 204(1):102–109. doi:10.1006/excr.1993.1014
57. Lo CM, Keese CR, Giaever I (1994) pH changes in pulsed CO2 incubators cause periodic changes in cell morphology. Exp Cell Res 213(2):391–397. doi:10.1006/excr.1994.1214
58. Lo CM, Keese CR, Giaever I (1999) Cell-substrate contact: another factor may influence transepithelial electrical resistance of cell layers cultured on permeable filters. Exp Cell Res 250(2):576–580. doi:10.1006/excr.1999.4538
59. Lorenowicz MJ, Fernandez-Borja M, Kooistra MR, Bos JL, Hordijk PL (2008) PKA and Epac1 regulate endothelial integrity and migration through parallel and independent pathways. Eur J Cell Biol 87(10):779–792. doi:10.1016/j.ejcb.2008.05.004
60. Lovelady DC, Friedman J, Patel S, Rabson DA, Lo CM (2009) Detecting effects of low levels of cytochalasin B in 3 T3 fibroblast cultures by analysis of electrical noise obtained from cellular micromotion. Biosens Bioelectron 24(7):2250–2254. doi:10.1016/j.bios.2008.09.033
61. Luissint AC, Federici C, Guillonneau F, Chretien F, Camoin L, Glacial F, Ganeshamoorthy K, Couraud PO (2012) Guanine nucleotide-binding protein Galphai2: a new partner of claudin-5 that regulates tight junction integrity in human brain endothelial cells. J Cerebral Blood Flow Metabol Off J Int Soc Cerebral Blood Flow Metabol 32(5):860–873. doi:10.1038/jcbfm.2011.202
62. Lvovich VF (2012) Impedance spectroscopy: applications to electrochemical and dielectricphenomena. Wiley, Hoboken
63. Lynch JJ, Ferro TJ, Blumenstock FA, Brockenauer AM, Malik AB (1990) Increased endothelial albumin permeability mediated by protein kinase C activation. J Clin Invest 85(6):1991–1998. doi:10.1172/JCI114663
64. McAdams ET, Lackermeier A, McLaughlin JA, Macken D, Jossinet J (1995) The linear and nonlinear electrical properties of the electrode-electrolyte interface. Biosens Bioelectron 10:76–74
65. McLaughlin JN, Shen L, Holinstat M, Brooks JD, Dibenedetto E, Hamm HE (2005) Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem 280(26):25048–25059. doi:10.1074/jbc.M414090200
66. Mehta D, Malik AB (2006) Signaling mechanisms regulating endothelial permeability. Physiol Rev 86(1):279–367. doi:10.1152/physrev.00012.2005
67. Michaelis S, Rommel CE, Endell J, Goring P, Wehrsporn R, Steinem C, Janshoff A, Galla HJ, Wegener J (2013) Macroporous silicon chips for laterally resolved, multi-parametric analysis of epithelial barrier function. Lab Chip 12:2329–2336
68. Michaelis S, Wegener J, Robelek R (2013) Label-free monitoring of cell-based assays: combining impedance analysis with SPR for multiparametric cell profiling. Biosens Bioelectron 49:63–70
69. Michel CC (1996) Transport of macromolecules through microvascular walls. Cardiovasc Res 32(4):644–653
70. Monaghan-Benson E, Wittchen ES (2011) In vitro analyses of endothelial cell permeability. Methods Mol Biol 763:281–290. doi:10.1007/978-1-61779-191-8_19
71. Moore E, Rawley O, Wood T, Galvin P (2009) Monitoring of cell growth in vitro using biochips packaged with indium tin oxide sensors. Sensors Actators B-Chem 139:187–193
72. Moy AB, Blackwell K, Kamath A (2002) Differential effects of histamine and thrombin on endothelial barrier function through actin-myosin tension. Am J Physiol Heart Circulat Physiol 282(1):H21–H29
73. Murata N, Sato K, Kon J, Tomura H, Yanagita M, Kuwabara A, Ui M, Okajima F (2000) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352(Pt 3):809–815
74. Murata T, Aritake K, Tsubosaka Y, Maruyama T, Nakagawa T, Hori M, Hirai H, Nakamura M, Narumiya S, Urade Y, Ozaki H (2013) Anti-inflammatory role of PGD2 in acute lung inflammation and therapeutic application of its signal enhancement. Proc Natl Acad Sci U S A 110(13):5205–5210. doi:10.1073/pnas.1218091110
75. Mycielska ME, Djamgoz MB (2004) Cellular mechanisms of direct-current electric field effects: galvanotaxis and metastatic disease. J Cell Sci 117(Pt 9):1631–1639. doi:10.1242/jcs.01125
76. Nakagawa S, Deli MA, Kawaguchi H, Shimizudani T, Shimono T, Kittel A, Tanaka K, Niwa M (2009) A new blood–brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem Int 54(3–4):253–263. doi:10.1016/j.neuint.2008.12.002
77. Panke O, Weigel W, Schmidt S, Steude A, Robitzki AA (2011) A cell-based impedance assay for monitoring transient receptor potential (TRP) ion channel activity. Biosens Bioelectron 26(5):2376–2382. doi:10.1016/j.bios.2010.10.015
78. Paolinelli R, Corada M, Ferrarini L, Devraj K, Artus C, Czupalla CJ, Rudini N, Maddaluno L, Papa E, Engelhardt B, Couraud PO, Liebner S, Dejana E (2013) Wnt activation of immortalized brain endothelial cells as a tool for generating a standardized model of the blood brain barrier in vitro. PLoS One 8(8):e70233. doi:10.1371/journal.pone.0070233
79. Parker JC, Stevens T, Randall J, Weber DS, King JA (2006) Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers. Am J Physiol Lung Cell Molec Physiol 291(1):L30–L37. doi:10.1152/ajplung.00317.2005
80. Rahman ARA, Lo CM, Bhansali S (2006) A micro-electrode array biosensor for impedance spectroscopy of human umbilical vein endothelial cells. Sens Actuators B-Chem 118:115–120
81. Ramirez-Icaza G, Mohammed KA, Nasreen N, Van Horn RD, Hardwick JA, Sanders KL, Tian J, Ramirez-Icaza C, Johnson MT, Antony VB (2004) Th2 cytokines IL-4 and IL-13 downregulate paxillin expression in bronchial airway epithelial cells. J Clin Immunol 24(4):426–434. doi:10.1023/B:JOCI.0000029111.27168.c6
82. Rehder D, Iden S, Nasdala I, Wegener J, Brickwedde MK, Vestweber D, Ebnet K (2006) Junctional adhesion molecule-a participates in the formation of apico-basal polarity through different domains. Exp Cell Res 312(17):3389–3403. doi:10.1016/j.yexcr.2006.07.004
83. Riethmuller C, Jungmann P, Wegener J, Oberleithner H (2006) Bradykinin shifts endothelial fluid passage from para- to transcellular routes. Pflugers Arch - Eur J Physiol 453(2):157–165. doi:10.1007/s00424-006-0121-2
84. Rosen H, Stevens RC, Hanson M, Roberts E, Oldstone MB (2013) Sphingosine-1-phosphate and its receptors: structure, signaling, and influence. Annu Rev Biochem 82:637–662. doi:10.1146/annurev-biochem-062411-130916
85. Schiller KR, Maniak PJ, O’Grady SM (2010) Cystic fibrosis transmembrane conductance regulator is involved in airway epithelial wound repair. Am J Physiol Cell Physiol 299(5):C912–C921. doi:10.1152/ajpcell.00215.2010
86. Schlegel N, Waschke J (2009) Impaired cAMP and Rac 1 signaling contribute to TNF-alpha-induced endothelial barrier breakdown in microvascular endothelium. Microcirculation 16(6):521–533. doi:10.1080/10739680902967427
87. Schneider D, Tarantola M, Janshoff A (2011) Dynamics of TGF-beta induced epithelial-to-mesenchymal transition monitored by electric cell-substrate impedance sensing. Biochim Biophys Acta 1813(12):2099–2107. doi:10.1016/j.bbamcr.2011.07.016
88. Schnoor M, Lai FP, Zarbock A, Klaver R, Polaschegg C, Schulte D, Weich HA, Oelkers JM, Rottner K, Vestweber D (2011) Cortactin deficiency is associated with reduced neutrophil recruitment but increased vascular permeability in vivo. J Experiment Med 208(8):1721–1735. doi:10.1084/jem.20101920
89. Seebach J, Dieterich P, Luo F, Schillers H, Vestweber D, Oberleithner H, Galla HJ, Schnittler HJ (2000) Endothelial barrier function under laminar fluid shear stress. Lab Investig J Tech Methods Pathol 80(12):1819–1831
90. Shinde AV, Motiani RK, Zhang X, Abdullaev IF, Adam AP, Gonzalez-Cobos JC, Zhang W, Matrougui K, Vincent PA, Trebak M (2013) STIM1 controls endothelial barrier function independently of Orai1 and Ca2+ entry. Sci Signal 6(267):ra18. doi:10.1126/scisignal.2003425
91. Shivanna M, Rajashekhar G, Srinivas SP (2010) Barrier dysfunction of the corneal endothelium in response to TNF-alpha: role of p38 MAP kinase. Invest Ophthalmol Vis Sci 51(3):1575–1582. doi:10.1167/iovs. 09-4343
92. Solly K, Wang X, Xu X, Strulovici B, Zheng W (2004) Application of real-time cell electronic sensing (RT-CES) technology to cell-based assays. Assay Drug Dev Technol 2(4):363–372. doi:10.1089/1540658041850544
93. Spindler V, Peter D, Harms GS, Asan E, Waschke J (2011) Ultrastructural analysis reveals cAMP-dependent enhancement of microvascular endothelial barrier functions via Rac1-mediated reorganization of intercellular junctions. Am J Pathol 178(5):2424–2436. doi:10.1016/j.ajpath.2011.01.014
94. Stamatovic SM, Keep RF, Andjelkovic AV (2008) Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr Neuropharmacol 6(3):179–192. doi:10.2174/157015908785777210
95. Stolwijk JA, Hartmann C, Balani P, Albermann S, Keese CR, Giaever I, Wegener J (2011) Impedance analysis of adherent cells after in situ electroporation: non-invasive monitoring during intracellular manipulations. Biosens Bioelectron 26:4720–4727
96. Sun M, Fu H, Cheng H, Cao Q, Zhao Y, Mou X, Zhang X, Liu X, Ke Y (2012) A dynamic real-time method for monitoring epithelial barrier function in vitro. Anal Biochem 425(2):96–103. doi:10.1016/j.ab.2012.03.010
97. Szulcek R, Beckers CM, Hodzic J, de Wit J, Chen Z, Grob T, Musters RJ, Minshall RD, van Hinsbergh VW, van Nieuw Amerongen GP (2013) Localized RhoA GTPase activity regulates dynamics of endothelial monolayer integrity. Cardiovasc Res 99(3):471–482. doi:10.1093/cvr/cvt075
98. Szulcek R, Bogaard HJ, van Nieuw Amerongen GP (2014) Electric cell-substrate impedance sensing for the quantification of endothelial proliferation, barrier function, and motility. Journal of visualized experiments: JoVE (85). doi:10.3791/51300
99. Tang VW, Goodenough DA (2003) Paracellular ion channel at the tight junction. Biophys J 84(3):1660–1673. doi:10.1016/S0006-3495(03)74975-3
100. Tarantola M, Marel AK, Sunnick E, Adam H, Wegener J, Janshoff A (2010) Dynamics of human cancer cell lines monitored by electrical and acoustic fluctuation analysis. Integ Biol Quant Biosci Nano Macro 2(2–3):139–150. doi:10.1039/b920815a
101. ten Klooster JP, Jaffer ZM, Chernoff J, Hordijk PL (2006) Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J Cell Biol 172(5):759–769. doi:10.1083/jcb.200509096
102. Tiruppathi C, Malik AB, Del Vecchio PJ, Keese CR, Giaever I (1992) Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc Natl Acad Sci U S A 89(17):7919–7923
103. Turner MR (1992) Flows of liquid and electrical current through monolayers of cultured bovine arterial endothelium. J Physiol 449:1–20
104. Utoguchi N, Ikeda K, Saeki K, Oka N, Mizuguchi H, Kubo K, Nakagawa S, Nayumi T (1995) Ascorbic acid stimulates barrier function of cultured endothelial cell monolayer. J Cell Physiol 163(2):393–399
105. Van Itallie CM, Anderson JM (2004) The role of claudins in determining paracellular charge selectivity. Proc Am Thorac Soc 1(1):38–41. doi:10.1513/pats.2306013
106. von Wedel-Parlow M, Schrot S, Lemmen J, Treeratanapiboon L, Wegener J, Galla HJ (2011) Neutrophils cross the BBB primarily on transcellular pathways: an in vitro study. Brain Res 1367:62–76. doi:10.1016/j.brainres.2010.09.076
107. von Wedel-Parlow M, Wolte P, Galla HJ (2009) Regulation of major efflux transporters under inflammatory conditions at the blood–brain barrier in vitro. J Neurochem 111(1):111–118. doi:10.1111/j.1471-4159.2009.06305.x
108. Wallez Y, Huber P (2008) Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim Biophys Acta 1778(3):794–809. doi:10.1016/j.bbamem.2007.09.003
109. Wang Y, Alexander JS (2011) Analysis of endothelial barrier function in vitro. Methods Mol Biol 763:253–264. doi:10.1007/978-1-61779-191-8_17
110. Wang Z, Ginnan R, Abdullaev IF, Trebak M, Vincent PA, Singer HA (2010) Calcium/Calmodulin-dependent protein kinase II delta 6 (CaMKIIdelta6) and RhoA involvement in thrombin-induced endothelial barrier dysfunction. J Biol Chem 285(28):21303–21312. doi:10.1074/jbc.M110.120790
111. Wegener J, Abrams D, Willenbrink W, Galla HJ, Janshoff A (2004) Automated multi-well device to measure transepithelial electrical resistances under physiological conditions. BioTechniques 37 (4):590, 592–594, 596–597
112. Wegener J, Hakvoort A, Galla HJ (2000) Barrier function of porcine choroid plexus epithelial cells is modulated by cAMP-dependent pathways in vitro. Brain Res 853(1):115–124
113. Wegener J, Keese CR, Giaever I (2000) Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp Cell Res 259(1):158–166. doi:10.1006/excr.2000.4919
114. Wegener J, Seebach J (2014) Experimental tools to monitor the dynamics of endothelial barrier function: a survey of in vitro approaches. Cell Tissue Res 355(3):485–514. doi:10.1007/s00441-014-1810-3
115. Weidenfeller C, Schrot S, Zozulya A, Galla HJ (2005) Murine brain capillary endothelial cells exhibit improved barrier properties under the influence of hydrocortisone. Brain Res 1053(1–2):162–174. doi:10.1016/j.brainres.2005.06.049
116. Wilhelm I, Fazakas C, Krizbai IA (2011) In vitro models of the blood–brain barrier. Acta Neurobiol Exp 71(1):113–128
117. Wilkerson BA, Grass GD, Wing SB, Argraves WS, Argraves KM (2012) Sphingosine 1-phosphate (S1P) carrier-dependent regulation of endothelial barrier: high density lipoprotein (HDL)-S1P prolongs endothelial barrier enhancement as compared with albumin-S1P via effects on levels, trafficking, and signaling of S1P1. J Biol Chem 287(53):44645–44653. doi:10.1074/jbc.M112.423426
118. Will C, Fromm M, Muller D (2008) Claudin tight junction proteins: novel aspects in paracellular transport. Periton Dial Int J Int Soc Periton Dial 28(6):577–584
119. Wolf P, Rothermel A, Beck-Sickinger AG, Robitzki AA (2008) Microelectrode chip based real time monitoring of vital MCF-7 mamma carcinoma cells by impedance spectroscopy. Biosens Bioelectron 24(2):253–259. doi:10.1016/j.bios.2008.03.040
120. Xiao C, Lachance B, Sunahara G, Luong JH (2002) Assessment of cytotoxicity using electric cell-substrate impedance sensing: concentration and time response function approach. Anal Chem 74(22):5748–5753
121. Xiao C, Luong JH (2003) On-line monitoring of cell growth and cytotoxicity using electric cell-substrate impedance sensing (ECIS). Biotechnol Prog 19(3):1000–1005. doi:10.1021/bp025733x
122. Xu M, Waters CL, Hu C, Wysolmerski RB, Vincent PA, Minnear FL (2007) Sphingosine 1-phosphate rapidly increases endothelial barrier function independently of VE-cadherin but requires cell spreading and Rho kinase. Am J Physiol Cell Physiol 293(4):C1309–C1318. doi:10.1152/ajpcell.00014.2007
123. Yin F, Watsky MA (2005) LPA and S1P increase corneal epithelial and endothelial cell transcellular resistance. Invest Ophthalmol Vis Sci 46(6):1927–1933. doi:10.1167/iovs. 04-1256
124. Yoshida Y, Okano M, Wang S, Kobayashi M, Kawasumi M, Hagiwara H, Mitsumata M (1995) Hemodynamic-force-induced difference of interendothelial junctional complexes. Ann N Y Acad Sci 748:104–120, discussion 120–101
125. Yuan SY, Rigor RR (2010) Methods for measuring permeability. In: Yuan SY, Rigor RR (eds) Regulation of endothelial barrier function. Morgan & Claypool Life Sciences; 2010., San Rafael (CA)