Impedance spectroscopy in monitoring the maturation of stem cell-derived retinal pigment epithelium

Annals of Biomedical Engineering

Volumn 39, Issue 12, 2011, Pages 3055-3069

  Savolainen, V ^a,b   Juuti Uusitalo, K ^a,b   Onnela, N ^a,b   Vaajasaari, H ^a,b   Narkilahti, S ^a,b   Suuronen, R ^a,b,c   Skottman, H ^a,b   Hyttinen, J ^a,b  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

Electrical impedance spectroscopy; Epithelial cells; Human embryonic stem cells; Maturation; Permeability

Indexed keywords

BARRIER FUNCTIONS; DRUG DEVELOPMENT; ELECTRICAL IMPEDANCE SPECTROSCOPY; EMBRYONIC STEMS; EPITHELIAL CELLS; EQUIVALENT MODEL; HUMAN EMBRYONIC STEM CELLS; IMPEDANCE SPECTROSCOPY; IN-VITRO; INTACT CELLS; MATURATION; NYQUIST PLOTS; PERMEABILITY MEASUREMENTS; RC CIRCUITS; RETINAL PIGMENT EPITHELIUM; TETRAACETIC ACID; TIGHT JUNCTIONS; TRANSPLANTATION THERAPY;

ALDEHYDES; ANIMAL CELL CULTURE; CELL GROWTH; DRUG THERAPY; ELECTRIC IMPEDANCE; ELECTRIC IMPEDANCE MEASUREMENT; ELECTROCHEMICAL CORROSION; ETHYLENE; ETHYLENE GLYCOL; FUNCTION EVALUATION; LIVING SYSTEMS STUDIES; OPHTHALMOLOGY; STEM CELLS;

CYTOLOGY;

ARTICLE; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; ELECTROCHEMICAL IMPEDANCE SPECTROSCOPY; EMBRYONIC STEM CELL; GROWTH, DEVELOPMENT AND AGING; HUMAN; PHYSIOLOGY; PIGMENT EPITHELIUM; TIGHT JUNCTION;

CELL DIFFERENTIATION; CELL LINE; DIELECTRIC SPECTROSCOPY; EMBRYONIC STEM CELLS; HUMANS; RETINAL PIGMENT EPITHELIUM; TIGHT JUNCTIONS;

EID: 80755135461     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-011-0387-1     Document Type: Article

References (52)

1. S Amasheh N Meiri AH Gitter T Schöneberg J Mankertz JD Schulzke M Fromm 2002 Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells J. Cell Sci. 115 4969 4976 12432083 10.1242/jcs.00165 1:CAS:528:DC%2BD3sXis1Ojsw%3D%3D (Pubitemid 36061180)
2. S Arndt J Seebach K Psathaki H-J Galla J Wegener 2004 Bioelectrical impedance assay to monitor changes in cell shape during apoptosis Biosens. Bioelectron 19 6 583 594 14683642 10.1016/S0956-5663(03)00269-0 1:CAS:528:DC%2BD3sXpvVWrs74%3D (Pubitemid 37542351)
3. DE Buchholz ST Hikita TJ Rowland AM Friedrich CR Hinman LV Johnson DO Clegg 2009 Derivation of functional retinal pigmented epithelium from induced pluripotent stem cells Stem Cells 27 2427 2434 19658190 10.1002/stem.189 1:CAS:528:DC%2BD1MXhsFenur7E
4. JM Burke 2008 Epithelial phenotype and the RPE: is the answer blowing in the Wnt? Prog. Retin Eye Res. 27 6 579 595 18775790 10.1016/j.preteyeres.2008. 08.002 1:CAS:528:DC%2BD1cXhtlyiu73J
5. JM Burke CM Skumatz PE Irving BS McKay 1996 Phenotypic heterogeneity of retinal pigment epithelial cells in vitro and in situ Exp. Eye Res. 62 1 63 73 8674514 10.1006/exer.1996.0008 1:CAS:528:DyaK28XotlyjsQ%3D%3D (Pubitemid 26135474)
6. A Caramoy 2011 A reply to human retinal pigment epithelium (RPE) transplantation: outcome after autologous RPE-choroid sheet and RPE cell-suspension in a randomised clinical study Br. J. Ophthalmol. 95 431 20978168 10.1136/bjo.2010.191882
7. C-W Chang DM Defoe RB Caldwell 1997 Retinal pigment epithelial cells from dystrophic rats form normal tight junctions in vitro Invest. Ophthalmol. Vis. Sci. 38 188 195 9008643 1:STN:280:DyaK2s7mtFertA%3D%3D (Pubitemid 27051537)
8. C Clausen TE Machen JM Diamond 1983 Use of AC impedance analysis to study membrane changes related to acid secretion in amphibian gastric mucosa Biophys. J. 41 167 178 6601499 10.1016/S0006-3495(83)84417-8 1:CAS:528: DyaL3sXhtVCqt7c%3D
9. L da Cruz FK Chen A Ahmado J Greenwood P Coffey 2007 RPE transplantation and its role in retinal disease Prog. Retin Eye Res. 26 598 635 17920328 10.1016/j.preteyeres.2007.07.001 1:CAS:528:DC%2BD2sXht1amsrrI (Pubitemid 47615562)
10. + pump in primary cultures of xenopus retinal pigment epithelium Exp. Eye Res. 59 587 596 9492760 10.1006/exer.1994.1144 1:CAS:528:DyaK2MXisVGku78%3D (Pubitemid 24359878)
11. N Depaola JE Phelps L Florez CR Keese FL Minnear I Giaver P Vincent 2001 Electrical impedance of cultured endothelium under fluid flow Ann. Biomed. Eng. 29 648 656 11556721 10.1114/1.1385811 1:STN:280:DC%2BD3MrgvVansw%3D%3D (Pubitemid 32827291)
12. M Friedlander 2007 Fibrosis and diseases of the eye J. Clin. Invest. 117 3 576 586 17332885 10.1172/JCI31030 1:CAS:528:DC%2BD2sXis12htro%3D (Pubitemid 46348512)
13. M Fromm CE Palant CJ Bentzel U Hegel 1985 Protamine reversibly decreases paracellular cation permeability in necturus gallbladder J. Membr. Biol. 87 141 150 4078883 10.1007/BF01870660 1:CAS:528:DyaL2MXmtFahu7Y%3D (Pubitemid 16234454)
14. A Gitter J-D Schuzke D Sorgenfrei M Fromm 1997 Using chamber for high-frequency transmural impedance analysis of epithelial tissues J. Biochem. Biophys. Methods 35 81 88 9350514 10.1016/S0165-022X(97)00028-6 1:CAS:528:DyaK2sXmtVWht7g%3D (Pubitemid 27414539)
15. M Guo J Chen X Yun K Chen L Nie S Yao 2006 Monitoring of cell growth and assessment of cytotoxicity using electrochemical impedance spectroscopy Biochim. Biophys. Acta 1760 432 439 16388905 10.1016/j.bbagen.2005.11.011 1:CAS:528:DC%2BD28Xis1egsbY%3D
16. Hamilton, R. D.; and L. Leach. Isolation and properties of an in vitro human outer blood-retinal barrier model. In: The Blood Brain and Other Neural Barriers: Reviews and Protocols, Methods in Molecular Biology, edited by S. Nag, 2011, pp. 401-416.
17. NS Harhaj DA Antonetti 2004 Regulation of tight junctions and loss of barrier function in pathophysiology Int. J. Biochem. Cell Biol. 36 7 1206 1237 15109567 10.1016/j.biocel.2003.08.007 1:CAS:528:DC%2BD2cXjsVWnsb8%3D (Pubitemid 38519069)
18. M Hornof E Toropainen A Urtti 2005 Cell culture models of the ocular barriers Eur. J. Pharm. Biopharm. 60 2 207 225 15939234 10.1016/j.ejpb.2005.01. 009 1:CAS:528:DC%2BD2MXltFCrsrw%3D (Pubitemid 40804562)
19. MA Huber N Kraut H Beug 2005 Molecular requirements for epithelial mesenchymal transition during tumor progression Curr. Opin. Cell Biol. 17 548 558 16098727 10.1016/j.ceb.2005.08.001 1:CAS:528:DC%2BD2MXhtVWnsb7L (Pubitemid 41267170)
20. M Idelson R Alper A Obolensky E Ben-Shushan I Hemo N Yachimovich-Cohen H Khaner Y Smith O Wiser M Gropp MA Cohen S Even-Ram Y Berman-Zaken L Matzrafi G Rechavi E Banin B Reubinof 2009 Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells Cell Stem Cell 5 396 408 19796620 10.1016/j.stem.2009.07.002 1:CAS:528:DC%2BD1MXhsVCjtrvJ
21. A Janshoff J Wegener M Sieber H-J Galla 1996 Double-mode impedance analysis of epithelial cell monolayers cultured on shear wave resonators Eur. Biophys. J. 25 93 103 9035374 10.1007/s002490050021 1:STN:280: DyaK2s7osl2htQ%3D%3D (Pubitemid 27026513)
22. LG Johnson 2005 Applications of imaging techniques to studies of epithelial tight junctions Adv. Drug Deliv. Rev. 57 1 111 121 15518924 10.1016/j.addr.2004.08.004 1:CAS:528:DC%2BD2cXptFKqsbo%3D (Pubitemid 39424067)
23. DP Joseph SS Miller 1991 Apical and basal membrane ion transport mechanisms in bovine retinal pigment epithelium J. Physiol. 435 439 463 1722821 1:STN:280:DyaK387it1WgsQ%3D%3D
24. M Kaida F Cao CM Skumatz PE Irving JM Burke 2000 Time at confluence for human RPE cells: effects on the adherens junction and in vitro wound closure Invest. Ophthalmol. Vis. Sci. 41 10 3215 3224 10967086 1:STN:280: DC%2BD3cvivVahtw%3D%3D
25. I Klimanskaya J Hipp KA Rezai M West A Atala R Lanza 2004 Derivation and comparative assessment of retinal pigment epithelium from human embryonic stem cells using transcriptomics Cloning Stem Cells 6 3 217 245 15671670 1:CAS:528:DC%2BD2cXovFamtr0%3D (Pubitemid 39391307)
26. SM Krug M Fromm D Günzel 2009 Two-path impedance spectroscopy for measuring paracellular and transcellular epithelial resistance Biophys. J. 97 2202 2211 19843452 10.1016/j.bpj.2009.08.003 1:CAS:528:DC%2BD1MXhsVCiu7vO
27. E Lee RE MacLaren 2011 Sources of retinal pigment epithelium (RPE) for replacement therapy Br. J. Ophthalmol. 95 445 449 20601659 10.1136/bjo.2009. 171918 1:STN:280:DC%2BC3M3ns1SmtQ%3D%3D
28. CM Lo CR Keese I Giaever 1995 Impedance analysis of MDCK cells measured by electric cell-substrate impedance sensing Biophys. J. 69 6 2800 2807 8599686 10.1016/S0006-3495(95)80153-0 1:CAS:528:DyaK2MXpslOgtbs%3D
29. RD Lund S Wang I Klimanskaya T Holmes R Ramos-Kelsey B Lu S Girman N Bischoff Y Sauve R Lanza 2006 Human embryonic stem cell-derived cells rescue visual function in dystrophic RCS rats Cloning Stem Cells 8 3 189 199 17009895 10.1089/clo.2006.8.189 1:CAS:528:DC%2BD28XhtVWntr7N (Pubitemid 44735173)
30. RE MacLaren GS Uppal KS Balaggan A Tufail PM Munro AB Milliken RR Ali GS Rubin GW Aylward L da Cruz 2007 Autologous transplantation of the retinal pigment epithelium and choroid in the treatment of neovascular age-related macular degeneration Ophthalmology 114 3 561 570 17324698 10.1016/j.ophtha.2006. 06.049 (Pubitemid 46282940)
31. A Maminishkis S Chen S Jalickee T Banzon G Shi FE Wang T Ehalt JA Hammer SS Miller 2006 Confluent monolayers of cultured human fetal retinal pigment epithelium exhibit morphology and physiology of native tissue Invest. Ophthalmol. Vis. Sci. 47 8 3612 3624 16877436 10.1167/iovs.05-1622 (Pubitemid 351639731)
32. BS McKay PE Irving CM Skumatz JM Burke 1997 Cell-cell adhesion molecules and the development of an epithelial phenotype in cultured human retinal pigment epithelial cells Exp. Eye Res. 65 5 661 671 9367646 10.1006/exer.1997.0374 1:CAS:528:DyaK2sXnsFWlsb8%3D (Pubitemid 27489762)
33. SS Miller RH Steinberg 1977 Active transport of ions across frog retinal pigment epithelium Exp. Eye Res. 25 3 235 248 304010 10.1016/0014-4835(77)90090- 2 1:CAS:528:DyaE1cXjsVOltw%3D%3D (Pubitemid 8204209)
34. K Petrukhin 2007 New therapeutic targets in atrophic age-related macular degeneration Expert Opin. Ther. Targets 11 5 625 639 17465722 10.1517/14728222.11.5.625 1:CAS:528:DC%2BD2sXkslCltb0%3D (Pubitemid 46744687)
35. RH Quinn SS Miller 1992 Ion transport mechanisms in native human retinal pigment epithelium Invest. Ophthalmol. Vis. Sci. 33 3513 3527 1334477 1:STN:280:DyaK3s7gtVWgsg%3D%3D (Pubitemid 23001366)
36. AR Rahman C-M Lo S Bhansali 2009 A detailed model for high-frequency impedance characterization of ovarian cancer epithelial cell layer using ECIS electrodes IEEE Trans. BME 56 2 485 492 10.1109/TBME.2008.2008488
37. SA Rajasekaran J Hu J Gopal R Gallemore S Ryazantsev D Bok AK Rajasekaran 2003 Na, K-ATPase inhibition alters tight junction structure and permeability in human retinal pigment epithelial cells Am. J. Physiol. Cell Physiol. 284 6 C1497 C1507 12570983 1:CAS:528:DC%2BD3sXltVegsL8%3D
38. VP Ranta A Urtti 2006 Transscleral drug delivery to the posterior eye: prospects of pharmacokinetic modeling Adv. Drug Deliv. Rev. 58 1164 1181 17069929 10.1016/j.addr.2006.07.025 1:CAS:528:DC%2BD28Xht1CnsL3O
39. B Reiter R Kraft D Günzel S Zeissig J-D Schulzke M Fromm C Harteneck 2006 TRPV4-mediated regulation of epithelial permeability FASEB J. 20 1802 1812 16940152 10.1096/fj.06-5772com 1:CAS:528:DC%2BD28XptlKjsL8%3D (Pubitemid 44933794)
40. LJ Rizzolo 2007 Development and role of tight junctions in the retinal pigment epithelium Int. Rev. Cytol. 258 195 234 17338922 10.1016/S0074-7696(07) 58004-6 1:CAS:528:DC%2BD2sXmtFKlur4%3D (Pubitemid 46330486)
41. B Rothen-Rutishauser FK Riesen A Braun M Günthert H Wunderli-Allenspach 2002 Dynamics of tight and adherens junctions under EGTA treatment J. Membr. Biol. 188 2 151 162 12172640 10.1007/s00232-001-0182-2 1:CAS:528:DC%2BD38XlvFeru7c%3D (Pubitemid 34804259)
42. S Saika O Yamanaka KC Flanders Y Okada T Miyamoto T Sumioka K Shirai A Kitano K Miyazaki S Tanaka K Ikeda 2008 Epithelial-mesenchymal transition as a therapeutic target for prevention of ocular tissue fibrosis Endocr. Metab. Immune Disord. Drug Targets 8 69 76 18393925 10.2174/187153008783928343 1:CAS:528:DC%2BD1cXkvV2iu7c%3D
43. E Schifferdecker E Frömter 1978 The AC impedance of Necturus gallbladder epithelium Pflügers Arch. 377 125 133 569807 10.1007/BF00582842 1:STN:280:DyaE1M%2FpsFentA%3D%3D (Pubitemid 9037576)
44. H Skottman 2009 Derivation and characterization of three new human embryonic stem cell lines in Finland In Vitro Cell. Dev. Biol. Anim. 46 3-4 206 209
45. A Urtti 2006 Challenges and obstacles of ocular pharmacokinetics and drug delivery Adv. Drug Deliv. Rev. 58 11 1131 1135 17097758 10.1016/j.addr.2006.07. 027 1:CAS:528:DC%2BD28Xht1CnsL3M
46. H Vaajasaari T Ilmarinen K Juuti-Uusitalo K Rajala N Onnela S Narkilahti R Suuronen J Hyttinen H Uusitalo H Skottman 2011 Towards defined and xeno-free differentiation of functional human pluripotent stem cell-derived retinal pigment epithelial cells Mol. Vis. 17 558 575 21364903 1:CAS:528: DC%2BC3MXjtVyktLw%3D
47. A Vugler J Lawrence J Walsh A Carr C Gias M Semo A Ahmado L da Cruz P Andrews P Coffey 2007 Embryonic stem cells and retinal repair Mech. Dev. 124 11-12 807 829 17881192 10.1016/j.mod.2007.08.002 1:CAS:528:DC%2BD2sXht12hsr7K (Pubitemid 350051369)
48. S Wang B Lu S Girman T Holmes N Bischoff RD Lund 2008 Morphological and functional rescue in RCS rats after RPE cell line transplantation at a later stage of degeneration Invest. Ophthalmol. Vis. Sci. 49 1 416 421 18172120 10.1167/iovs.07-0992
49. J Wegener R Charles K Giaever I Giaever 2000 Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces Exp. Cell Res. 259 158 166 10942588 10.1006/excr.2000.4919 1:CAS:528:DC%2BD3cXls1ansbw%3D
50. J Wegener M Sieber H-J Galla 1996 Impedance analysis of epithelial and endothelial cell monolayers cultured on gold surfaces J. Biochem. Biophys. Methods 32 3 151 170 8844323 10.1016/0165-022X(96)00005-X 1:CAS:528: DyaK28XktVyitbo%3D (Pubitemid 26238459)
51. 2+ entry in retinal pigment epithelial cells is mediated by TRPC channels Invest. Ophthalmol. Vis. Sci. 48 5767 5772 18055830 10.1167/iovs.07-0412 (Pubitemid 351260882)
52. D Zhu X Deng C Spee S Sonoda C-L Hsieh E Barron M Pera DR Hinton 2010 Polarized secretion of PEDF from human embryonic stem cell-derived RPE promotes retinal progenitor cell survival Invest. Ophthalmol. Vis. Sci. 10 6413