Drug and bioactive molecule screening based on a bioelectrical impedance cell culture platform

International Journal of Nanomedicine

Volumn 9, Issue 1, 2014, Pages 5789-5809

  Ramasamy, Sakthivel ^a   Bennet, Devasier ^a   Kim, Sanghyo ^a  

^a Gachon University   (South Korea)

Author keywords

Electric cell substrate impedance sensing (ECIS); High throughput screening; Impedance based cell study; Real time drug evaluation; Screening of bioactive agents

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIVIRUS AGENT; CD31 ANTIGEN; DOXORUBICIN; FLUOROURACIL; ION CHANNEL; QUANTUM DOT; SKIN PROTECTIVE AGENT;

BINDING AFFINITY; BIOSENSOR; CELL CULTURE; CELL METABOLISM; CELL MIGRATION ASSAY; CELL SIGNALING ASSAY; DRUG BINDING; DRUG CYTOTOXICITY; DRUG DEVELOPMENT; DRUG EFFICACY; DRUG SAFETY; DRUG SCREENING; DRUG TARGETING; ELECTRIC CELL SUBSTRATE IMPEDANCE SENSING; ELECTRIC RESISTANCE; ENZYME ACTIVITY; EQUIPMENT DESIGN; HIGH THROUGHPUT SCREENING; IMPEDANCE; NANOANALYSIS; REVIEW; TOXICITY TESTING; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; CELL CULTURE TECHNIQUE; CELL LINE; DEVICES; HUMAN; PRECLINICAL STUDY; PROCEDURES;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; DRUG EVALUATION, PRECLINICAL; ELECTRIC IMPEDANCE; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS;

EID: 84916910933     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S71128     Document Type: Review

References (91)

1. Giaever I, Keese CR. A morphological biosensor for mammalian cells. Nature. 1993;366 (6455):591-592.
2. Asphahani F, Zhang M. Cellular impedance biosensors for drug screening and toxin detection. Analyst. 2007;132(9):835-841.
3. Ehret R, Baumann W, Brischwein M, Schwinde A, Stegbauer K, Wolf B. Monitoring of cellular behaviour by impedance measurements on interdigitated electrode structures. Biosens Bioelectron. 1997;12(1):29-41.
4. Grimnes S, Martinsen OG. Bioimpedance and Bioelectricity Basics. 1st ed. St Louis, MO; 2000.
5. Xu Y, Lv Y, Wang L, Xing W, Cheng J. A microfluidic device with passive air-bubble valves for real-time measurement of dose-dependent drug cytotoxicity through impedance sensing. Biosens Bioelectron. 2012;32(1):300-304.
6. Tran TB, Cho S, Min J. Hydrogel-based diffusion chip with electric cellsubstrate impedance sensing (ECIS) integration for cell viability assay and drug toxicity screening. Biosens Bioelectron. 2013;50:453-459.
7. Bennet D, Kim MG, Kim S. Light-induced anatomical alterations in retinal cells. Anal Biochem. 2013;436(2):84-92.
8. Luong JHT. An emerging impedance sensor based on cell-protein interactions: applications in cell biology and analytical biochemistry. Anal Lett. 2003;36(15):3147-3164.
9. Picollet-D’hahan N. Live cell analysis: when electric detection interfaces microfluidics. Journal of Biochips and Tissue Chips. 2011;S1:001.
10. Xiaoqiu H, Nguyen D, Greve DW, Domach MM. Simulation of microelectrode impedance changes due to cell growth. IEEE Sens J. 2004;4(5):576-583.
11. Giaever I, Keese CR. Micromotion of mammalian cells measured electrically. Proc Natl Acad Sci U S A. 1991;88(17):7896-7900.
12. Wegener J, Keese CR, Giaever I. Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp Cell Res. 2000;259(1):158-166.
13. Wang L, Wang H, Wang L, Mitchelson K, Yu Z, Cheng J. Analysis of the sensitivity and frequency characteristics of coplanar electrical cellsubstrate impedance sensors. Biosens Bioelectron. 2008;24(1):14-21.
14. Wang L, Zhu J, Deng C, Xing WL, Cheng J. An automatic and quantitative on-chip cell migration assay using self-assembled monolayers combined with real-time cellular impedance sensing. Lab Chip. 2008; 8(6):872-878.
15. Abhyankar VV, Lokuta MA, Huttenlocher A, Beebe DJ. Characterization of a membrane-based gradient generator for use in cell-signaling studies. Lab Chip. 2006;6(3):389-393.
16. Irimia D, Charras G, Agrawal N, Mitchison T, Toner M. Polar stimulation and constrained cell migration in microfluidic channels. Lab Chip. 2007;7(12):1783-1790.
17. Grover WH, Skelley AM, Liu CN, Lagally ET, Mathies RA. Monolithic membrane valves and diaphragm pumps for practical large-scale integration into glass microfluidic devices. Sens Actuators B Chem. 2003; 89(3):315-323.
18. van der Wijngaart W, Chugh D, Man E, Melin J, Stemme G. A lowtemperature thermopneumatic actuation principle for gas bubble microvalves. J Microelectromech Syst. 2007;16(3):765-774.
19. Toh YC, Lim TC, Tai D, Xiao G, van Noort D, Yu H. A microfluidic 3D hepatocyte chip for drug toxicity testing. Lab Chip. 2009;9(14): 2026-2035.
20. Asphahani F, Wang K, Thein M, et al. Single-cell bioelectrical impedance platform for monitoring cellular response to drug treatment. Phys Biol. 2011;8(1):015006.
21. Ozsvári B, Puskás LG, Nagy LI, et al. A cell-microelectronic sensing technique for the screening of cytoprotective compounds. Int J Mol Med. 2010;25(4):525-530.
22. Pflüger M, Kapuscik A, Lucas R, et al. A combined impedance and AlphaLISA-based approach to identify anti-inflammatory and barrier-protective compounds in human endothelium. J Biomol Screen. 2013;18(1):67-74.
23. Powers ME, Kim HK, Wang Y, Bubeck Wardenburg J. ADAM10 mediates vascular injury induced by Staphylococcus aureus α-hemolysin. J Infect Dis. 2012;206(3):352-356.
24. Xiao CD, Lachance B, Sunahara G, Luong JHT. Assessment of cytotoxicity using electric cell-substrate impedance sensing: concentration and time response function approach. Anal Chem. 2002; 74(22):5748-5753.
25. Male KB, Lachance B, Hrapovic S, Sunahara G, Luong JHT. Assessment of cytotoxicity of quantum dots and gold nanoparticles using cell-based. impedance spectroscopy. Anal Chem. 2008;80(14):5487-5493.
26. Bennet D, Kim S. A transdermal delivery system to enhance quercetin nanoparticle permeability. J Biomater Sci Polym Ed. 2013;24(2): 185-209.
27. Opp D, Wafula B, Lim J, Huang E, Lo JC, Lo CM. Use of electric cell-substrate impedance sensing to assess in vitro cytotoxicity. Biosens Bioelectron. 2009;24(8):2625-2629.
28. Curtis TM, Tabb J, Romeo L, Schwager SJ, Widder MW, van der Schalie WH. Improved cell sensitivity and longevity in a rapid impedancebased toxicity sensor. J Appl Toxicol. 2009;29(5):374-380.
29. Curtis TM, Widder MW, Brennan LM, et al. A portable cell-based impedance sensor for toxicity testing of drinking water. Lab Chip. 2009;9(15):2176-2183.
30. Liu F, Nordin AN, Li F, Voiculescu I. A lab-on-chip cell-based biosensor for label-free sensing of water toxicants. Lab Chip. 2014;14(7): 1270-1280.
31. Shih SC, Barbulovic-Nad I, Yang X, Fobel R, Wheeler AR. Digital microfluidics with impedance sensing for integrated cell culture and analysis. Biosens Bioelectron. 2013;42:314-320.
32. Xie F, Xu Y, Wang L, Mitchelson K, Xing W, Cheng J. Use of cellular electrical impedance sensing to assess in vitro cytotoxicity of anticancer drugs in a human kidney cell nephrotoxicity model. Analyst. 2012;137(6):1343-1350.
33. Tarantola M, Schneider D, Sunnick E, et al. Cytotoxicity of metal and semiconductor nanoparticles indicated by cellular micromotility. ACS Nano. 2009;3(1):213-222.
34. McGuinness RP, Proctor JM, Gallant DL, et al. Enhanced selectivity screening of GPCR ligands using a label-free cell based assay technology. Comb Chem High Throughput Screen. 2009;12(8): 812-823.
35. McLaughlin JN, Shen L, Holinstat M, Brooks JD, Dibenedetto E, Hamm HE. Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem. 2005;280(26):25048-25059.
36. Reddy L, Wang HS, Keese CR, Giaever I, Smith TJ. Assessment of rapid morphological changes associated with elevated cAMP levels in human orbital fibroblasts. Exp Cell Res. 1998;245(2): 360-367.
37. Zou ZW, Kai JH, Rust MJ, Han J, Ahn CH. Functionalized nano interdigitated electrodes arrays on polymer with integrated microfluidics for direct bio-affinity sensing using impedimetric measurement. Sens Actuators A Phys. 2007;136(2):518-526.
38. Yu N, Atienza JM, Bernard J, et al. Real-time monitoring of morphological changes in living cells by electronic cell sensor arrays: an approach to study G protein-coupled receptors. Anal Chem. 2005;78(1): 35-43.
39. Obr A, Röselová P, Grebeňová D, Kuželová K. Real-time monitoring of hematopoietic cell interaction with fibronectin fragment: the effect of histone deacetylase inhibitors. Cell Adh Migr. 2013;7(3):275-282.
40. Mei H, Paddock C, Campbell J, Albrecht R, Newman PJ. Enhancement of endothelial cell barrier function by antibody-driven affinity modulation of PECAM-1. Blood. 2013;122(21).
41. Gainor JP, Morton CA, Roberts JT, Vincent PA, Minnear FL. Plateletconditioned medium increases endothelial electrical resistance independently of cAMP/PKA and cGMP/PKG. Am J Physiol Heart Circ Physiol. 2001;281(5):H1992-H2001.
42. Minnear FL, Patil S, Bell D, Gainor JP, Morton CA. Platelet lipid(s) bound to albumin increases endothelial electrical resistance: mimicked by LPA. Am J Physiol Lung Cell Mol Physiol. 2001;281(6):L1337-L1344.
43. Lo CM, Keese CR, Giaever I. Cell-substrate contact: another factor may influence transepithelial electrical resistance of cell layers cultured on permeable filters. Exp Cell Res. 1999;250(2):576-580.
44. Hong J, Kandasamy K, Marimuthu M, Choi CS, Kim S. Electrical cell-substrate impedance sensing as a non-invasive tool for cancer cell study. Analyst. 2011;136(2):237-245.
45. Wang L, Wang L, Yin H, et al. Real-time, label-free monitoring of the cell cycle with a cellular impedance sensing chip. Biosens Bioelectron. 2010;25(5):990-995.
46. Chen J, Ye L, Zhang L, Jiang WG. Placenta growth factor, PLGF, influences the motility of lung cancer cells, the role of Rho associated kinase, Rock1. J Cell Biochem. 2008;105(1):313-320.
47. Jiang WG, Ablin RJ, Kynaston HG, Mason MD. The prostate transglutaminase (TGase-4, TGaseP) regulates the interaction of prostate cancer and vascular endothelial cells, a potential role for the ROCK pathway. Microvasc Res. 2009;77(2):150-157.
48. Jiang WG, Martin TA, Lewis-Russell JM, Douglas-Jones A, Ye L, Mansel RE. Eplin-alpha expression in human breast cancer, the impact on cellular migration and clinical outcome. Mol Cancer. 2008;7:71.
49. Zudaire E, Cuesta N, Murty V, et al. The aryl hydrocarbon receptor repressor is a putative tumor suppressor gene in multiple human cancers. J Clin Invest. 2008;118(2):640-650.
50. Naor D, Nedvetzki S, Golan I, Melnik L, Faitelson Y. CD44 in cancer. Crit Rev Clin Lab Sci. 2002;39(6):527-579.
51. Kuo YC, Su CH, Liu CY, Chen TH, Chen CP, Wang HS. Transforming growth factor-beta induces CD44 cleavage that promotes migration of MDA-MB-435s cells through the up-regulation of membrane type 1- matrix metalloproteinase. Int J Cancer. 2009;124(11):2568-2576.
52. Saxena NK, Sharma D, Ding X, et al. Concomitant activation of the JAK/STAT, PI3K/AKT, and ERK signaling is involved in leptinmediated promotion of invasion and migration of hepatocellular carcinoma cells. Cancer Res. 2007;67(6):2497-2507.
53. Kuznar J, Soler M, Farias G, Espinoza JC. Attachment and entry of infectious pancreatic necrosis virus (IPNV) into CHSE-214 cells. Arch Virol. 1995;140(10):1833-1840.
54. Campbell CE, Laane MM, Haugarvoll E, Giaever I. Monitoring viralinduced cell death using electric cell-substrate impedance sensing. Biosens Bioelectron. 2007;23(4):536-542.
55. McCoy MH, Wang E. Use of electric cell-substrate impedance sensing as a tool for quantifying cytopathic effect in influenza A virus infected MDCK cells in real-time. J Virol Methods. 2005;130(1-2):157-161.
56. Müller J, Thirion C, Pfaffl MW. Electric cell-substrate impedance sensing (ECIS) based real-time measurement of titer dependent cytotoxicity induced by adenoviral vectors in an IPI-2I cell culture model. Biosens Bioelectron. 2011;26(5):2000-2005.
57. Chiang ET, Persaud-Sawin DA, Kulkarni S, Garcia JG, Imani F. Bluetongue virus and double-stranded RNA increase human vascular permeability: role of p38 MAPK. J Clin Immunol. 2006;26(4):406-416.
58. Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 1997;57(4):765-772.
59. Kilani MM, Mohammed KA, Nasreen N, et al. Respiratory syncytial virus causes increased bronchial epithelial permeability. Chest. 2004;126(1):186-191.
60. Bennet D, Sanghyo K. In ECIS to assess human skin cell photo-oxidative damage. Proceedings of the International Conference on Advanced Nanomaterials and Emerging Engineering Technologies; Chennai; July 24-26, 2013. IEEE; 2013.
61. Bennet D, Kang SC, Gang J, Kim S. Photoprotective effects of apple peel nanoparticles. Int J Nanomedicine. 2014;9:93-108.
62. Bennet D, Kim S. Impedance-based cell culture platform to assess light-induced stress changes with antagonist drugs using retinal cells. Anal Chem. 2013;85(10):4902-4911.
63. Bennet D, Kim S. Effects of agmatine and resveratrol on RGC-5 cell behavior under light stimulation. Environ Toxicol Pharmacol. 2014;38(1):84-97.
64. Kramer N, Walzl A, Unger C, et al. In vitro cell migration and invasion assays. Mutat Res. 2013;752(1):10-24.
65. Keese CR, Wegener J, Walker SR, Giaever I. Electrical wound-healing assay for cells in vitro. Proc Natl Acad Sci U S A. 2004;101(6): 1554-1559.
66. Wu NL, Chiang YC, Huang CC, Fang JY, Chen DF, Hung CF. Zeaxanthin inhibits PDGF-BB-induced migration in human dermal fibroblasts. Exp Dermatol. 2010;19(8):e173-e181.
67. Burns AR, Bowden RA, MacDonell SD, et al. Analysis of tight junctions during neutrophil transendothelial migration. J Cell Sci. 2000; 113(Pt 1):45-57.
68. Earley S, Plopper GE. Disruption of focal adhesion kinase slows transendothelial migration of AU-565 breast cancer cells. Biochem Biophys Res Commun. 2006;350(2):405-412.
69. Waters CM, Long J, Gorshkova I, et al. Cell migration activated by platelet-derived growth factor receptor is blocked by an inverse agonist of the sphingosine 1-phosphate receptor-1. FASEB J. 2005;19(13):509-511.
70. Lo CM, Keese CR, Giaever I. Monitoring motion of confluent cells in tissue culture. Exp Cell Res. 1993;204(1):102-109.
71. Luong JH, Habibi-Rezaei M, Meghrous J, Xiao C, Male KB, Kamen A. Monitoring motility, spreading, and mortality of adherent insect cells using an impedance sensor. Anal Chem. 2001;73(8):1844-1848.
72. Huang CN, Lo CM, Hsu TC, Tsay GJ. Sera from patients with scleroderma inhibit fibroblast micromotions monitored electrically. J Rheumatol. 1999;26(6):1312-1317.
73. Lee CC, Putnam AJ, Miranti CK, et al. Overexpression of sprouty 2 inhibits HGF/SF-mediated cell growth, invasion, migration, and cytokinesis. Oncogene. 2004;23(30):5193-5202.
74. Feng R, Lu Y, Bowman LL, Qian Y, Castranova V, Ding M. Inhibition of activator protein-1, NF-kappaB, and MAPKs and induction of phase 2 detoxifying enzyme activity by chlorogenic acid. J Biol Chem. 2005;280(30):27888-27895.
75. Hadjout N, Laevsky G, Knecht DA, Lynes MA. Automated realtime measurement of chemotactic cell motility. Biotechniques. 2001;31(5):1130-1188.
76. Hu Z, Liu Q, Wang P. Cell-Based Biosensors: Principles and Applications. Artech House; 2010:150-178.
77. Park G, Choi CK, English AE, Sparer TE. Electrical impedance measurements predict cellular transformation. Cell Biol Int. 2009;33(3): 429-433.
78. Aas V, Torblå S, Andersen MH, Jensen J, Rustan AC. Electrical stimulation improves insulin responses in a human skeletal muscle cell model of hyperglycemia. Ann N Y Acad Sci. 2002;967:506-515.
79. Hu N, Zhou J, Su K, et al. An integrated label-free cell-based biosensor for simultaneously monitoring of cellular physiology multiparameter in vitro. Biomed Microdevices. 2013;15(3):473-480.
80. Large TH, Smith MW. Screening strategies for ion channel targets. In: Seethala R, Fernades PB, editors. Handbook of Drug Screening. New York: Basel; 2005:313-333.
81. Fei L, Arifuzzaman SM, Nordin AN, Spray D, Voiculescu I. Characterization of endothelial cells using electrochemical impedance spectroscopy. Proceedings of the Asia Pacific Conference on Circuits and Systems; Kuala Lumpur; December 6-9, 2010. IEEE; 2010.
82. Marimuthu M, Park C, Kim S, Choi CS. Real-time electrical measurement of L929 cellular spontaneous and synchronous oscillation. Int J Nanomedicine. 2012;7:83-92.
83. Young EF. Transient impedance changes in venous endothelial monolayers as a biological radiation dosimetry response. Journal of Electrical Bioimpedance. 2012;3:61-65.
84. Young EF, Smilenov LB. Impedance-based surveillance of transient permeability changes in coronary endothelial monolayers after exposure to ionizing radiation. Radiat Res. 2011;176(4):415-424.
85. Kumar P, Miller AI, Polverini PJ. p38 MAPK mediates gamma-irradiationinduced endothelial cell apoptosis, and vascular endothelial growth factor protects endothelial cells through the phosphoinositide 3-kinase-Akt- Bcl-2 pathway. J Biol Chem. 2004;279(41):43352-43360.
86. Han A, Frazier AB. Ion channel characterization using single cell impedance spectroscopy. Lab Chip. 2006;6(11):1412-1414.
87. Regard JB, Scheek S, Borbiev T, et al. Verge: a novel vascular early response gene. J Neurosci. 2004;24(16):4092-4103.
88. Clements RT, Minnear FL, Singer HA, Keller RS, Vincent PA. RhoA and Rho-kinase dependent and independent signals mediate TGF-beta-induced pulmonary endothelial cytoskeletal reorganization and permeability. Am J Physiol Lung Cell Mol Physiol. 2005; 288(2):L294-L306.
89. Huang F, Subbaiah PV, Holian O, et al. Lysophosphatidylcholine increases endothelial permeability: role of PKCalpha and RhoA cross talk. Am J Physiol Lung Cell Mol Physiol. 2005;289(2): L176-L185.
90. Qiao J, Huang F, Naikawadi RP, Kim KS, Said T, Lum H. Lysophosphatidylcholine impairs endothelial barrier function through the G protein-coupled receptor GPR4. Am J Physiol Lung Cell Mol Physiol. 2006;291(1):L91-L101.
91. Kim YV, Di Cello F, Hillaire CS, Kim KS. Differential Ca2+ signaling by thrombin and protease-activated receptor-1-activating peptide in human brain microvascular endothelial cells. Am J Physiol Cell Physiol. 2004;286(1):C31-C42.