Conductive Polymer PEDOT:PSS-Based Platform for Embryonic Stem-Cell Differentiation

. 2022 Jan 20 ; 23 (3) : . [epub] 20220120

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35163031

Grantová podpora
21-01057S Czech Science Foundation
18-18235S Czech Science Foundation
CZ.02.1.01/0.0/0.0/16_026/0008451 European Regional Development Fund

Organic semiconductors are constantly gaining interest in regenerative medicine. Their tunable physico-chemical properties, including electrical conductivity, are very promising for the control of stem-cell differentiation. However, their use for combined material-based and electrical stimulation remains largely underexplored. Therefore, we carried out a study on whether a platform based on the conductive polymer poly(3,4-ethylenedioxythiophene):polystyrene sulfonate (PEDOT:PSS) can be beneficial to the differentiation of mouse embryonic stem cells (mESCs). The platform was prepared using the layout of a standard 24-well cell-culture plate. Polyethylene naphthalate foil served as the substrate for the preparation of interdigitated gold electrodes by physical vapor deposition. The PEDOT:PSS pattern was fabricated by precise screen printing over the gold electrodes. The PEDOT:PSS platform was able to produce higher electrical current with the pulsed-direct-current (DC) electrostimulation mode (1 Hz, 200 mV/mm, 100 ms pulse duration) compared to plain gold electrodes. There was a dominant capacitive component. In proof-of-concept experiments, mESCs were able to respond to such electrostimulation by membrane depolarization and elevation of cytosolic calcium. Further, the PEDOT:PSS platform was able to upregulate cardiomyogenesis and potentially inhibit early neurogenesis per se with minor contribution of electrostimulation. Hence, the present work highlights the large potential of PEDOT:PSS in regenerative medicine.

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Sachinidis A., Fleischmann B.K., Kolossov E., Wartenberg M., Sauer H., Hescheler J. Cardiac specific differentiation of mouse embryonic stem cells. Cardiovasc. Res. 2003;58:278–291. doi: 10.1016/S0008-6363(03)00248-7. PubMed DOI

Keller G. Embryonic stem cell differentiation: Emergence of a new era in biology and medicine. Genes Dev. 2005;19:1129–1155. doi: 10.1101/gad.1303605. PubMed DOI

Heng B.C., Cao T., Stanton L.W., Robson P., Olsen B. Strategies for directing the differentiation of stem cells into the osteogenic lineage in vitro. J. Bone Miner. Res. 2004;19:1379–1394. doi: 10.1359/JBMR.040714. PubMed DOI

Amin M., Kushida Y., Wakao S., Kitada M., Tatsumi K., Dezawa M. Cardiotrophic growth factor-driven induction of human muse cells into cardiomyocyte-like phenotype. Cell Transplant. 2018;27:285–298. doi: 10.1177/0963689717721514. PubMed DOI PMC

Tian H.-C., Liu J.-Q., Kang X.-Y., Wei D.-X., Zhang C., Du J.-C., Yang B., Chen X., Yang C.-S. Biotic and abiotic molecule dopants determining the electrochemical performance, stability and fibroblast behavior of conducting polymer for tissue interface. RSC Adv. 2014;4:47461–47471. doi: 10.1039/C4RA07265K. DOI

Chen C., Bai X., Ding Y., Lee I.-S. Electrical stimulation as a novel tool for regulating cell behavior in tissue engineering. Biomater. Res. 2019;23:25. doi: 10.1186/s40824-019-0176-8. PubMed DOI PMC

Broughton K.M., Wang B.J., Firouzi F., Khalafalla F., Dimmeler S., Fernandez-Aviles F., Sussman M.A. Mechanisms of cardiac repair and regeneration. Circ. Res. 2018;122:1151–1163. doi: 10.1161/CIRCRESAHA.117.312586. PubMed DOI PMC

Du Pré B.C., Doevendans P.A., van Laake L.W. Stem cells for cardiac repair: An introduction. J. Geriatr. Cardiol. JGC. 2013;10:186. PubMed PMC

Parsa H., Ronaldson K., Vunjak-Novakovic G. Bioengineering methods for myocardial regeneration. Adv. Drug Deliv. Rev. 2016;96:195–202. doi: 10.1016/j.addr.2015.06.012. PubMed DOI PMC

Thrivikraman G., Boda S.K., Basu B. Unraveling the mechanistic effects of electric field stimulation towards directing stem cell fate and function: A tissue engineering perspective. Biomaterials. 2018;150:60–86. doi: 10.1016/j.biomaterials.2017.10.003. PubMed DOI

Ma R., Liang J., Huang W., Guo L., Cai W., Wang L., Paul C., Yang H.-T., Kim H.W., Wang Y. Electrical Stimulation Enhances Cardiac Differentiation of Human Induced Pluripotent Stem Cells for Myocardial Infarction Therapy. Antioxid. Redox Signal. 2018;28:371–384. doi: 10.1089/ars.2016.6766. PubMed DOI PMC

Radisic M., Park H., Shing H., Consi T., Schoen F.J., Langer R., Freed L.E., Vunjak-Novakovic G. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl. Acad. Sci. USA. 2004;101:18129–18134. doi: 10.1073/pnas.0407817101. PubMed DOI PMC

Cao H., Kang B.J., Lee C.-A., Shung K.K., Hsiai T.K. Electrical and mechanical strategies to enable cardiac repair and regeneration. IEEE Rev. Biomed. Eng. 2015;8:114–124. doi: 10.1109/RBME.2015.2431681. PubMed DOI PMC

Gueye M.N., Carella A., Faure-Vincent J., Demadrille R., Simonato J.-P. Progress in understanding structure and transport properties of PEDOT-based materials: A critical review. Prog. Mater. Sci. 2020;108:100616. doi: 10.1016/j.pmatsci.2019.100616. DOI

Rivnay J., Owens R.M., Malliaras G.G. The rise of organic bioelectronics. Chem. Mater. 2013;26:679–685. doi: 10.1021/cm4022003. DOI

Stritesky S., Markova A., Vitecek J., Safarikova E., Hrabal M., Kubac L., Kubala L., Weiter M., Vala M. Printing inks of electroactive polymer PEDOT:PSS: The study of biocompatibility, stability, and electrical properties. J. Biomed. Mater. Res. Part A. 2018;106:1121–1128. doi: 10.1002/jbm.a.36314. PubMed DOI

Dijk G., Rutz A.L., Malliaras G.G. Stability of PEDOT:PSS-Coated Gold Electrodes in Cell Culture Conditions. Adv. Mater. Technol. 2020;5:1900662. doi: 10.1002/admt.201900662. DOI

Moyen E., Hama A., Ismailova E., Assaud L., Malliaras G., Hanbücken M., Owens R.M. Nanostructured conducting polymers for stiffness controlled cell adhesion. Nanotechnology. 2016;27:074001. doi: 10.1088/0957-4484/27/7/074001. PubMed DOI

Ritzau-Reid K.I., Spicer C.D., Gelmi A., Grigsby C.L., Ponder J.F., Jr., Bemmer V., Creamer A., Vilar R., Serio A., Stevens M.M. An electroactive oligo-EDOT platform for neural tissue engineering. Adv. Funct. Mater. 2020;30:2003710. doi: 10.1002/adfm.202003710. PubMed DOI PMC

Heo D.N., Acquah N., Kim J., Lee S.-J., Castro N.J., Zhang L.G. Directly induced neural differentiation of human adipose-derived stem cells using three-dimensional culture system of conductive microwell with electrical stimulation. Tissue Eng. Part A. 2018;24:537–545. doi: 10.1089/ten.tea.2017.0150. PubMed DOI

Aggas J.R., Abasi S., Phipps J.F., Podstawczyk D.A., Guiseppi-Elie A. Microfabricated and 3-D printed electroconductive hydrogels of PEDOT:PSS and their application in bioelectronics. Biosens. Bioelectron. 2020;168:112568. doi: 10.1016/j.bios.2020.112568. PubMed DOI

Iandolo D., Sheard J., Levy G.K., Pitsalidis C., Tan E., Dennis A., Kim J.-S., Markaki A.E., Widera D., Owens R.M. Biomimetic and electroactive 3D scaffolds for human neural crest-derived stem cell expansion and osteogenic differentiation. MRS Commun. 2020;10:179–187. doi: 10.1557/mrc.2020.10. DOI

Tomaskovic-Crook E., Zhang P., Ahtiainen A., Kaisvuo H., Lee C.-Y., Beirne S., Aqrawe Z., Svirskis D., Hyttinen J., Wallace G.G., et al. Human neural tissues from neural stem cells using conductive biogel and printed polymer microelectrode arrays for 3D electrical stimulation. Adv. Healthc. Mater. 2019;8:1900425. doi: 10.1002/adhm.201900425. PubMed DOI

Tsai N.-C., She J.-W., Wu J.-G., Chen P., Hsiao Y.-S., Yu J. Poly (3,4-ethylenedioxythiophene) polymer composite bioelectrodes with designed chemical and topographical cues to manipulate the behavior of pc12 neuronal cells. Adv. Mater. Interfaces. 2019;6:1801576. doi: 10.1002/admi.201801576. DOI

Pires F., Ferreira Q., Rodrigues C.A., Morgado J., Ferreira F.C. Neural stem cell differentiation by electrical stimulation using a cross-linked PEDOT substrate: Expanding the use of biocompatible conjugated conductive polymers for neural tissue engineering. Biochim. Biophys. Acta Gen. Subj. 2015;1850:1158–1168. doi: 10.1016/j.bbagen.2015.01.020. PubMed DOI

Decataldo F., Druet V., Pappa A.-M., Tan E., Savva A., Pitsalidis C., Inal S., Kim J.-S., Fraboni B., Owens R.M., et al. BMP-2 functionalized PEDOT:PSS-based OECTs for stem cell osteogenic differentiation monitoring. Flex. Print. 2019;4:044006. doi: 10.1088/2058-8585/ab5bfc. DOI

Roshanbinfar K., Vogt L., Greber B., Diecke S., Boccaccini A.R., Scheibel T., Engel F.B. Electroconductive biohybrid hydrogel for enhanced maturation and beating properties of engineered cardiac tissues. Adv. Funct. Mater. 2018;28:1803951. doi: 10.1002/adfm.201803951. DOI

Yoshida S., Sumomozawa K., Nagamine K., Nishizawa M. Hydrogel Microchambers Integrated with Organic Electrodes for Efficient Electrical Stimulation of Human iPSC-Derived Cardiomyocytes. Macromol. Biosci. 2019;19:1900060. doi: 10.1002/mabi.201900060. PubMed DOI

Menzies K.L., Jones L. The impact of contact angle on the biocompatibility of biomaterials. Optom. Vis. Sci. 2010;87:387–399. doi: 10.1097/OPX.0b013e3181da863e. PubMed DOI

Safarikova E., Sindlerova L.S., Stritesky S., Kubala L., Vala M., Weiter M., Vitecek J. Evaluation and improvement of organic semiconductors’ biocompatibility towards fibroblasts and cardiomyocytes. Sens. Actuators B Chem. 2018;260:418–425. doi: 10.1016/j.snb.2017.12.108. DOI

Radaszkiewicz K.A., Sykorova D., Bino L., Kudova J., Bebarova M., Prochazkova J., Kotasova H., Kubala L., Pachernik J. The acceleration of cardiomyogenesis in embryonic stem cells in vitro by serum depletion does not increase the number of developed cardiomyocytes. PLoS ONE. 2017;12:e0173140. doi: 10.1371/journal.pone.0173140. PubMed DOI PMC

Lanza R., Gearhart J., Hogan B., Melton D., Pedersen R., Thomas E.D., Thomson J.A., West M. Essentials of Stem Cell Biology. Elsevier; Amsterdam, The Netherlands: 2005.

Hernandez D., Millard R., Sivakumaran P., Wong R.C., Crombie D.E., Hewitt A.W., Liang H., Hung S.S., Pebay A., Shepherd R.K., et al. Electrical stimulation promotes cardiac differentiation of human induced pluripotent stem cells. Stem Cells Int. 2015;2016:1718041. doi: 10.1155/2016/1718041. PubMed DOI PMC

Sauer H., Bekhite M.M., Hescheler J., Wartenberg M. Redox control of angiogenic factors and CD31-positive vessel-like structures in mouse embryonic stem cells after direct current electrical field stimulation. Exp. Cell Res. 2005;304:380–390. doi: 10.1016/j.yexcr.2004.11.026. PubMed DOI

Yamada M., Tanemura K., Okada S., Iwanami A., Nakamura M., Mizuno H., Ozawa M., Ohyama-Goto R., Kitamura N., Kawano M., et al. Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells. 2007;25:562–570. doi: 10.1634/stemcells.2006-0011. PubMed DOI

Serena E., Figallo E., Tandon N., Cannizzaro C., Gerecht S., Elvassore N., Vunjak-Novakovic G. Electrical stimulation of human embryonic stem cells: Cardiac differentiation and the generation of reactive oxygen species. Exp. Cell Res. 2009;315:3611–3619. doi: 10.1016/j.yexcr.2009.08.015. PubMed DOI PMC

Tandon N., Marsano A., Maidhof R., Numata K., Montouri-Sorrentino C., Cannizzaro C., Voldman J., Vunjak-Novakovic G. Surface-patterned electrode bioreactor for electrical stimulation. Lab Chip. 2010;10:692–700. doi: 10.1039/b917743d. PubMed DOI PMC

Chan Y.-C., Ting S., Lee Y.-K., Ng K.-M., Zhang J., Chen Z., Siu C.-W., Oh S.K.W., Tse H.-F. Electrical stimulation promotes maturation of cardiomyocytes derived from human embryonic stem cells. J. Cardiovasc. Transl. Res. 2013;6:989–999. doi: 10.1007/s12265-013-9510-z. PubMed DOI

Nuccitelli R. Endogenous ionic currents and DC electric fields in multicellular animal tissues. Bioelectromagnetics. 1992;13:147–157. doi: 10.1002/bem.2250130714. PubMed DOI

Proctor C.M., Rivnay J., Malliaras G.G. Understanding volumetric capacitance in conducting polymers. J. Polym. Sci. B Polym. Phys. 2016;54:1433–1436. doi: 10.1002/polb.24038. DOI

Winther-Jensen B., Winther-Jensen O., Forsyth M., MacFarlane D.R. High rates of oxygen reduction over a vapor phase-polymerized PEDOT electrode. Science. 2008;321:671–674. doi: 10.1126/science.1159267. PubMed DOI

Cottis P.P., Evans D., Fabretto M., Pering S., Murphy P., Hojati-Talemi P. Metal-free oxygen reduction electrodes based on thin PEDOT films with high electrocatalytic activity. RSC Adv. 2014;4:9819–9824. doi: 10.1039/c3ra46167j. DOI

Kudova J., Prochazkova J., Vasicek O., Perecko T., Sedlackova M., Pesl M., Pachernik J., Kubala L. HIF-1alpha deficiency attenuates the cardiomyogenesis of mouse embryonic stem cells. PLoS ONE. 2016;11:e0158358. doi: 10.1371/journal.pone.0158358. PubMed DOI PMC

Vecera J., Kudova J., Kucera J., Kubala L., Pachernik J. Neural Differentiation Is Inhibited through HIF1α/β-Catenin Signaling in Embryoid Bodies. Stem Cells Int. 2017;2017:8715798. doi: 10.1155/2017/8715798. PubMed DOI PMC

Humpolicek P., Radaszkiewicz K.A., Kasparkova V., Stejskal J., Trchova M., Kucekova Z., Vicarova H., Pachernik J., Lehocky M., Minarik A. Stem cell differentiation on conducting polyaniline. RSC Adv. 2015;5:68796–68805. doi: 10.1039/C5RA12218J. DOI

Radaszkiewicz K.A., Beckerova D., Woloszczukova L., Radaszkiewicz T.W., Lesakova P., Blanarova O.V., Kubala L., Humpolicek P., Pachernik J. 12-O-Tetradecanoylphorbol-13-acetate increases cardiomyogenesis through PKC/ERK signaling. Sci. Rep. 2020;10:15922. doi: 10.1038/s41598-020-73074-4. PubMed DOI PMC

Tandon N., Cannizzaro C., Chao P.-H.G., Maidhof R., Marsano A., Au H.T.H., Radisic M., Vunjak-Novakovic G. Electrical stimulation systems for cardiac tissue engineering. Nat. Protoc. 2009;4:155–173. doi: 10.1038/nprot.2008.183. PubMed DOI PMC

Sauer H., Rahimi G., Hescheler J., Wartenberg M. Effects of electrical fields on cardiomyocyte differentiation of embryonic stem cells. J. Cell. Biochem. 1999;75:710–723. doi: 10.1002/(SICI)1097-4644(19991215)75:4<710::AID-JCB16>3.0.CO;2-Z. PubMed DOI

Coelho N.M., González-Garcia C., Planell J., Salmerón-Sánchez M., Altankov G. Different assembly of type IV collagen on hydrophilic and hydrophobic substrata alters endothelial cells interaction. Eur. Cell. Mater. 2010;19:262–272. doi: 10.22203/eCM.v019a25. PubMed DOI

Nagy A., Rossant J., Nagy R., Abramow-Newerly W., Roder J.C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA. 1993;90:8424–8428. doi: 10.1073/pnas.90.18.8424. PubMed DOI PMC

Dahlmann J., Kensah G., Kempf H., Skvorc D., Gawol A., Elliott D.A., Dräger G., Zweigerdt R., Martin U., Gruh I. The use of agarose microwells for scalable embryoid body formation and cardiac differentiation of human and murine pluripotent stem cells. Biomaterials. 2013;34:2463–2471. doi: 10.1016/j.biomaterials.2012.12.024. PubMed DOI

Schneider C.A., Rasband W.S., Eliceiri K.W., Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., et al. NIH image to imageJ: 25 years of image analysis. Nat. Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC

Adams D.S., Levin M. Measuring resting membrane potential using the fluorescent voltage reporters DiBAC4 (3) and CC2-DMPE. Cold Spring Harb. Protoc. 2012;2012:pdb-prot067702. doi: 10.1101/pdb.prot067702. PubMed DOI PMC

Lan J.-Y., Williams C., Levin M., Black L.D. Depolarization of cellular resting membrane potential promotes neonatal cardiomyocyte proliferation in vitro. Cell. Mol. Bioeng. 2014;7:432–445. doi: 10.1007/s12195-014-0346-7. PubMed DOI PMC

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