Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2022 Jul 23;15(10):9253–9263. doi: 10.1007/s12274-022-4613-y

Electrically controlled mRNA delivery using a polypyrrole-graphene oxide hybrid film to promote osteogenic differentiation of human mesenchymal stem cells

Huijung Kim 1,#, Kübra Solak 2,#, Yoojoong Han 1, Yeon-Woo Cho 1, Kyeong-Mo Koo 1, Chang-Dae Kim 1, Zhengtang Luo 3, Hyungbin Son 1, Hyung-Ryong Kim 4,✉, Ahmet Mavi 5,6,✉, Tae-Hyung Kim 1,✉
PMCID: PMC9308036  PMID: 35911478

Abstract

Direct messenger ribonucleic acid (mRNA) delivery to target cells or tissues has revolutionized the field of biotechnology. However, the applicability of regenerative medicine is limited by the technical difficulties of various mRNA-loaded nanocarriers. Herein, we report a new conductive hybrid film that could guide osteogenic differentiation of human adipose-derived mesenchymal stem cells (hADMSCs) via electrically controlled mRNA delivery. To find optimal electrical conductivity and mRNA-loading capacity, the polypyrrole-graphene oxide (PPy-GO) hybrid film was electropolymerized on indium tin oxide substrates. We found that the fluorescein sodium salt, a molecule partially mimicking the physical and chemical properties of mRNAs, can be effectively absorbed and released by electrical stimulation (ES). The hADMSCs cultivated on the PPy-GO hybrid film loaded with pre-osteogenic mRNAs showed the highest osteogenic differentiation under electrical stimulation. This platform can load various types of RNAs thus highly promising as a new nucleic acid delivery tool for the development of stem cell-based therapeutics.

graphic file with name 12274_2022_4613_Fig1_HTML.jpg

Electronic Supplementary Material

Supplementary material (electrochemical and FT-IR analysis on the film, additional SEM, AFM and C-AFM images of the film, optical and fluorescence images of cells, and the primers used for RT-qPCR analysis) is available in the online version of this article at 10.1007/s12274-022-4613-y.

Keywords: messenger ribonucleic acid (mRNA) delivery, polypyrrole, graphene oxide, electrical release, mesenchymal stem cells

Electronic Supplementary Material

12274_2022_4613_MOESM1_ESM.pdf (1.6MB, pdf)

Electrically controlled mRNA delivery using a polypyrrole-graphene oxide hybrid film to promote osteogenic differentiation of human mesenchymal stem cells

Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (Nos. NRF-2019M3A9H2031820, NRF-2021R1A2C1010747, and NRF-2022R1A2C4002217), Korean Fund for Regenerative Medicine funded by Ministry of Science and ICT, and Ministry of Health and Welfare (Grant No. RS-2022-00070316) and the Bio & Medical Technology Development Program funded by the Ministry of Science, ICT and Future Planning, Republic of Korea (NRF-2017M3A9E4047243) and K. S. also thankful for The Council of Higher Education (CoHE, 100/2000) PhD Scholarship Program, Turkey.

Footnotes

Huijung Kim and Kübra Solak contributed equally to this work.

Contributor Information

Hyung-Ryong Kim, Email: hrkimdp@gmail.com.

Ahmet Mavi, Email: amavi@atauni.edu.tr.

Tae-Hyung Kim, Email: thkim0512@cau.ac.kr.

References

  • [1].Schlake T, Thess A, Fotin-Mleczek M, Kallen K J. Developing mRNA-vaccine technologies. RNA Biol. 2012;9:1319–1330. doi: 10.4161/rna.22269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [2].Sorrentino S. Human extracellular ribonucleases: Multiplicity, molecular diversity and catalytic properties of the major RNase types. Cell. Mol. Life Sci. CMLS. 1998;54:785–794. doi: 10.1007/s000180050207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [3].Liu M A. A comparison of plasmid DNA and mRNA as vaccine technologies. Vaccines. 2019;7:37. doi: 10.3390/vaccines7020037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [4].Ahammad I, Lira S S. Designing a novel mRNA vaccine against SARS-CoV-2: An immunoinformatics approach. Int. J. Biol. Macromol. 2020;162:820–837. doi: 10.1016/j.ijbiomac.2020.06.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [5].Pardi N, Hogan M J, Weissman D. Recent advances in mRNA vaccine technology. Curr. Opin. Immunol. 2020;65:14–20. doi: 10.1016/j.coi.2020.01.008. [DOI] [PubMed] [Google Scholar]
  • [6].van Tendeloo V F I, Ponsaerts P, Berneman Z N. mRNA-based gene transfer as a tool for gene and cell therapy. Curr. Opin. Mol. Ther. 2007;9:423–431. [PubMed] [Google Scholar]
  • [7].Chanda P K, Sukhovershin R, Cooke J P. mRNA-enhanced cell therapy and cardiovascular regeneration. Cells. 2021;10:187. doi: 10.3390/cells10010187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [8].Wang P P, Logeart-Avramoglou D, Petite H, Goncalves C, Midoux P, Perche F, Pichon C. Co-delivery of NS1 and BMP2 mRNAs to murine pluripotent stem cells leads to enhanced BMP-2 expression and osteogenic differentiation. Acta Biomater. 2020;108:337–346. doi: 10.1016/j.actbio.2020.03.045. [DOI] [PubMed] [Google Scholar]
  • [9].Strauer B E, Kornowski R. Stem cell therapy in perspective. Circulation. 2003;107:929–934. doi: 10.1161/01.CIR.0000057525.13182.24. [DOI] [PubMed] [Google Scholar]
  • [10].Frith J E, Kusuma G D, Carthew J, Li F Y, Cloonan N, Gomez G A, Cooper-White J J. Mechanically-sensitive miRNAs bias human mesenchymal stem cell fate via mTOR signalling. Nat. Commun. 2018;9:257. doi: 10.1038/s41467-017-02486-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [11].Cheon E J, Kim S H, Lee D K, Jo Y K, Ki M R, Park C J, Jang H S, Ahn J S, Pack S P, Jun S H. Osteostimulating ability of β-tricalcium phosphate/collagen composite as a practical bone-grafting substitute: In vitro and in vivo comparison study with commercial one. Biotechnol. Bioprocess Eng. 2021;26:923–932. doi: 10.1007/s12257-021-0059-4. [DOI] [Google Scholar]
  • [12].Herberts C A, Kwa M S, Hermsen H P. Risk factors in the development of stem cell therapy. J. Transl. Med. 2011;9:29. doi: 10.1186/1479-5876-9-29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [13].Kang E S, Kim H, Han Y, Cho Y W, Son H, Luo Z T, Kim T H. Enhancing osteogenesis of adipose-derived mesenchymal stem cells using gold nanostructure/peptide-nanopatterned graphene oxide. Colloids Surf. B Biointerf. 2021;204:111807. doi: 10.1016/j.colsurfb.2021.111807. [DOI] [PubMed] [Google Scholar]
  • [14].Dai Y F, Ma W, Zhang T, Yang J W, Zang C H, Liu K P, Wang X B, Wang J W, Wu Z, Zhang X K, et al. Long noncoding RNA expression profiling during the neuronal differentiation of glial precursor cells from rat dorsal root ganglia. Biotechnol. Bioprocess Eng. 2020;25:356–373. doi: 10.1007/s12257-019-0317-x. [DOI] [Google Scholar]
  • [15].Sharma A. Role of stem cell derived exosomes in tumor biology. Int. J. Cancer. 2018;142:1086–1092. doi: 10.1002/ijc.31089. [DOI] [PubMed] [Google Scholar]
  • [16].Hao Z C, Lu J, Wang S Z, Wu H, Zhang Y T, Xu S G. Stem cell-derived exosomes: a promising strategy for fracture healing. Cell Prolif. 2017;50:e12359. doi: 10.1111/cpr.12359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [17].Sun Y, Ye X Z, Cai M X, Liu X N, Xiao J, Zhang C Y, Wang Y Y, Yang L, Liu J F, Li S N, et al. Osteoblast-targeting-peptide modified nanoparticle for siRNA/microRNA delivery. ACS Nano. 2016;10:5759–5768. doi: 10.1021/acsnano.5b07828. [DOI] [PubMed] [Google Scholar]
  • [18].Khorsand B, Elangovan S, Hong L, Dewerth A, Kormann M S D, Salem A K. A comparative study of the bone regenerative effect of chemically modified RNA encoding BMP-2 or BMP-9. AAPS J. 2017;19:438–446. doi: 10.1208/s12248-016-0034-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [19].Evans C H, Huard J. Gene therapy approaches to regenerating the musculoskeletal system. Nat. Rev. Rheumatol. 2015;11:234–242. doi: 10.1038/nrrheum.2015.28. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [20].Wang P P, Perche F, Logeart-Avramoglou D, Pichon C. RNA-based therapy for osteogenesis. Int. J. Pharm. 2019;569:118594. doi: 10.1016/j.ijpharm.2019.118594. [DOI] [PubMed] [Google Scholar]
  • [21].Leng Q P, Liang Z, Lv Y G. Demineralized bone matrix scaffold modified with mRNA derived from osteogenically pre-differentiated MSCs improves bone repair. Mater. Sci. Eng. C. 2021;119:111601. doi: 10.1016/j.msec.2020.111601. [DOI] [PubMed] [Google Scholar]
  • [22].Kang J, Kim M G. Advancements in DNA-assisted immunosensors. BioChip J. 2020;14:18–31. doi: 10.1007/s13206-020-4103-9. [DOI] [Google Scholar]
  • [23].Wang W, Kong T, Zhang D, Zhang J, Cheng G. Labelfree microRNA detection based on fluorescence quenching of gold nanoparticles with a competitive hybridization. Anal. Chem. 2015;87:10822–10829. doi: 10.1021/acs.analchem.5b01930. [DOI] [PubMed] [Google Scholar]
  • [24].Giacca M, Zacchigna S. Virus-mediated gene delivery for human gene therapy. J. Control. Release. 2012;161:377–388. doi: 10.1016/j.jconrel.2012.04.008. [DOI] [PubMed] [Google Scholar]
  • [25].Baglio S R, Rooijers K, Koppers-Lalic D, Verweij F J, Pérez Lanzón M, Zini N, Naaijkens B, Perut F, Niessen H W M, Baldini N, et al. Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species. Stem Cell Res. Ther. 2015;6:127. doi: 10.1186/s13287-015-0116-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [26].Tapparo M, Bruno S, Collino F, Togliatto G, Deregibus M C, Provero P, Wen S C, Quesenberry P J, Camussi G. Renal regenerative potential of extracellular vesicles derived from miRNA-engineered mesenchymal stromal cells. Int. J. Mol. Sci. 2019;20:2381. doi: 10.3390/ijms20102381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [27].Sharei A, Zoldan J, Adamo A, Sim W Y, Cho N, Jackson E, Mao S, Schneider S, Han M J, Lytton-Jean A, et al. A vector-free microfluidic platform for intracellular delivery. Proc. Natl. Acad. Sci. USA. 2013;110:2082–2087. doi: 10.1073/pnas.1218705110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [28].Yoon C S, Park J H. Ultrasound-mediated gene delivery. Expert Opin. Drug Deliv. 2010;7:321–330. doi: 10.1517/17425241003596329. [DOI] [PubMed] [Google Scholar]
  • [29].Evans C H. The vicissitudes of gene therapy. Bone Joint Res. 2019;8:469–471. doi: 10.1302/2046-3758.810.BJR-2019-0265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [30].Zolghadrnasab M, Mousavi A, Farmany A, Arpanaei A. Ultrasound-mediated gene delivery into suspended plant cells using polyethyleneimine-coated mesoporous silica nanoparticles. Ultrason. Sonochem. 2021;73:105507. doi: 10.1016/j.ultsonch.2021.105507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [31].Somiari S, Glasspool-Malone J, Drabick J J, Gilbert R A, Heller R, Jaroszeski M J, Malone R W. Theory and in vivo application of electroporative gene delivery. Mol. Ther. 2000;2:178–187. doi: 10.1006/mthe.2000.0124. [DOI] [PubMed] [Google Scholar]
  • [32].Nussbaum J, Minami E, Laflamme M A, Virag J A I, Ware C B, Masino A, Muskheli V, Pabon L, Reinecke H, Murry C E. Transplantation of undifferentiated murine embryonic stem cells in the heart: Teratoma formation and immune response. FASEB J. 2007;21:1345–1357. doi: 10.1096/fj.06-6769com. [DOI] [PubMed] [Google Scholar]
  • [33].Geetha S, Rao C R K, Vijayan M, Trivedi D C. Biosensing and drug delivery by polypyrrole. Anal. Chim. Acta. 2006;568:119–125. doi: 10.1016/j.aca.2005.10.011. [DOI] [PubMed] [Google Scholar]
  • [34].Suhito I R, Han Y, Kim D S, Son H, Kim T H. Effects of two-dimensional materials on human mesenchymal stem cell behaviors. Biochem. Biophys. Res. Commun. 2017;493:578–584. doi: 10.1016/j.bbrc.2017.08.149. [DOI] [PubMed] [Google Scholar]
  • [35].Kang E S, Song I, Kim D S, Lee U, Kim J K, Son H, Min J, Kim T H. Size-dependent effects of graphene oxide on the osteogenesis of human adipose-derived mesenchymal stem cells. Colloids Surf. B Biointerf. 2018;169:20–29. doi: 10.1016/j.colsurfb.2018.04.053. [DOI] [PubMed] [Google Scholar]
  • [36].Kim C H, Han Y, Choi Y, Kwon M, Son H, Luo Z T, Kim T H. Extremely uniform graphene oxide thin film as a universal platform for one-step biomaterial patterning. Small. 2021;17:2103596. doi: 10.1002/smll.202103596. [DOI] [PubMed] [Google Scholar]
  • [37].Wu B Y, Zhao N, Hou S H, Zhang C. Electrochemical synthesis of polypyrrole, reduced graphene oxide, and gold nanoparticles composite and its application to hydrogen peroxide biosensor. Nanomaterials. 2016;6:220. doi: 10.3390/nano6110220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [38].Fahlgren A, Bratengeier C, Gelmi A, Semeins C M, Klein-Nulend J, Jager E W H, Bakker A D. Biocompatibility of polypyrrole with human primary osteoblasts and the effect of dopants. PLoS One. 2015;10:e0134023. doi: 10.1371/journal.pone.0134023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [39].Xu C H, Sun J, Gao L. Synthesis of novel hierarchical graphene/polypyrrolenanosheet composites and their superior electrochemical performance. J. Mater. Chem. 2011;21:11253–11258. doi: 10.1039/c1jm11275a. [DOI] [Google Scholar]
  • [40].Leng Q P, Chen L N, Lv Y G. RNA-based scaffolds for bone regeneration: Application and mechanisms of mRNA, miRNA and siRNA. Theranostics. 2020;10:3190–3205. doi: 10.7150/thno.42640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [41].Zhou M, Heinze J. Electropolymerization of pyrrole and electrochemical study of polypyrrole: 1. Evidence for structural diversity of polypyrrole. Electrochim. Acta. 1999;44:1733–1748. doi: 10.1016/S0013-4686(98)00293-X. [DOI] [Google Scholar]
  • [42].Bozzini B, Bocchetta P, Alemán B, Amati M, Gianoncelli A, Gregoratti L, Sezen H, Taurino A, Kiskinova M. Electrodeposition and pyrolysis of Mn/polypyrrole nanocomposites: A study based on soft X-ray absorption, fluorescence and photoelectron microspectroscopies. J. Mater. Chem. A. 2015;3:19155–19167. doi: 10.1039/C5TA05572E. [DOI] [Google Scholar]
  • [43].Porcher M, Esnault C, Tran-Van F, Ghamouss F. Electrochemical deposition and characterization of polypyrrole in electrolyte based on pyrrolidinium hydrogenosulfate protic ionic liquid. J. Appl. Electrochem. 2016;46:1133–1145. doi: 10.1007/s10800-016-0989-2. [DOI] [Google Scholar]
  • [44].Jiang Y, Hu C G, Cheng H H, Li C X, Xu T, Zhao Y, Shao H B, Qu L T. Spontaneous, straightforward fabrication of partially reduced graphene oxide-polypyrrole composite films for versatile actuators. ACS Nano. 2016;10:4735–4741. doi: 10.1021/acsnano.6b01233. [DOI] [PubMed] [Google Scholar]
  • [45].Zhu M, Hao Y, Ma X, Feng L, Zhai Y X, Ding Y P, Cheng G S. Construction of a graphene/polypyrrole composite electrode as an electrochemically controlled release system. RSC Adv. 2019;9:12667–12674. doi: 10.1039/C9RA00800D. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [46].Li M X, Ji X Q, Cui L, Liu J Q. In situ preparation of graphene/polypyrrole nanocomposite via electrochemical codeposition methodology for anti-corrosion application. J. Mater. Sci. 2017;52:12251–12265. doi: 10.1007/s10853-017-1362-5. [DOI] [Google Scholar]
  • [47].McFail-Isom L, Shui X Q, Williams L D. Divalent cations stabilize unstacked conformations of DNA and RNA by interacting with base π systems. Biochemistry. 1998;37:17105–17111. doi: 10.1021/bi982201+. [DOI] [PubMed] [Google Scholar]
  • [48].Novoselov K S, Geim A K, Morozov S V, Jiang D, Zhang Y, Dubonos S V, Grigorieva I V, Firsov A A. Electric field effect in atomically thin carbon films. Science. 2004;306:666–669. doi: 10.1126/science.1102896. [DOI] [PubMed] [Google Scholar]
  • [49].Song S G, Kim Y J, Kang H L, Yoon S, Hong D K, Kim W H, Shin I S, Seong W K, Lee K N. Sensitivity improvement in electrochemical immunoassays using antibody immobilized magnetic nanoparticles with a clean ITO working electrode. BioChip J. 2020;14:308–316. doi: 10.1007/s13206-020-4309-x. [DOI] [Google Scholar]
  • [50].Ding F Y, Shi X W, Jiang Z W, Liu L, Cai J, Li Z Y, Chen S, Du Y M. Electrochemically stimulated drug release from dual stimuli responsive chitin hydrogel. J. Mater. Chem. B. 2013;1:1729–1737. doi: 10.1039/c3tb00517h. [DOI] [PubMed] [Google Scholar]
  • [51].Teodorescu F, Rolland L, Ramarao V, Abderrahmani A, Mandler D, Boukherroub R, Szunerits S. Electrochemically triggered release of human insulin from an insulin-impregnated reduced graphene oxide modified electrode. Chem. Commun. 2015;51:14167–14170. doi: 10.1039/C5CC05539C. [DOI] [PubMed] [Google Scholar]
  • [52].Al-Dhahebi A M, Gopinath S C B, Saheed M S M. Graphene impregnated electrospun nanofiber sensing materials: A comprehensive overview on bridging laboratory set-up to industry. Nano Converg. 2020;7:27. doi: 10.1186/s40580-020-00237-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [53].Zhang Q, Xu J, Song Q, Li N, Zhang Z L, Li K Y, Du Y Y, Wu L Q, Tang M L, Liu L W, et al. Synthesis of amphiphilic reduced graphene oxide with an enhanced charge injection capacity for electrical stimulation of neural cells. J. Mater. Chem. B. 2014;2:4331–4337. doi: 10.1039/C4TB00279B. [DOI] [PubMed] [Google Scholar]
  • [54].Wang W S, Li B L, Yang H L, Lin Z F, Chen L L, Li Z, Ge J Y, Zhang T, Xia H, Li L H, et al. Efficient elimination of multidrug-resistant bacteria using copper sulfide nanozymes anchored to graphene oxide nanosheets. Nano Res. 2020;13:2156–2164. doi: 10.1007/s12274-020-2824-7. [DOI] [Google Scholar]
  • [55].Zeng S W, Chen L, Wang Y, Chen J L. Exploration on the mechanism of DNA adsorption on graphene and graphene oxide via molecular simulations. J. Phys. D Appl. Phys. 2015;48:275402. doi: 10.1088/0022-3727/48/27/275402. [DOI] [Google Scholar]
  • [56].Wang J. On-demand electrochemical release of nucleic acids. Electroanalysis. 2001;13:635–638. doi: 10.1002/1521-4109(200105)13:8/9<635::AID-ELAN635>3.0.CO;2-J. [DOI] [Google Scholar]
  • [57].Lee K, Kang J H, Kim H M, Ahn J, Lim H, Lee J, Jeon W J, Lee J H, Kim K B. Direct electrophoretic microRNA preparation from clinical samples using nanofilter membrane. Nano Convergence. 2020;7:1. doi: 10.1186/s40580-019-0212-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [58].Leprince L, Dogimont A, Magnin D, Demoustier-Champagne S. Dexamethasone electrically controlled release from polypyrrole-coated nanostructured electrodes. J. Mater. Sci. Mater. Med. 2010;21:925–930. doi: 10.1007/s10856-010-4008-6. [DOI] [PubMed] [Google Scholar]
  • [59].Dong C J, Qiao F Y, Hou W S, Yang L, Lv Y G. Graphene-based conductive fibrous scaffold boosts sciatic nerve regeneration and functional recovery upon electrical stimulation. Appl. Mater. Today. 2020;21:100870. doi: 10.1016/j.apmt.2020.100870. [DOI] [Google Scholar]
  • [60].Wang Y, Zhang X M, Zhao B Y, Xu Z L, Lv Y G. Suspension state promotes drug resistance of breast tumor cells by inducing ABCC3 overexpression. Appl. Biochem. Biotechnol. 2020;190:410–422. doi: 10.1007/s12010-019-03084-0. [DOI] [PubMed] [Google Scholar]
  • [61].Kim T W, Ahn W B, Kim J M, Kim J H, Kim T H, Perez R A, Jang H S. Combined delivery of two different bioactive factors incorporated in hydroxyapatite microcarrier for bone regeneration. Tissue Eng. Regener. Med. 2020;17:607–624. doi: 10.1007/s13770-020-00257-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [62].Xu C, Xiao L, Cao Y X, He Y, Lei C, Xiao Y, Sun W J, Ahadian S, Zhou X T. Khademhosseini, A. et al. Mesoporous silica rods with cone shaped pores modulate inflammation and deliver BMP-2 for bone regeneration. Nano Res. 2020;13:2323–2331. doi: 10.1007/s12274-020-2783-z. [DOI] [Google Scholar]
  • [63].Wang W P, Zhou L, Wang S M, Luo Z, Hu Z D. Rapid and simple determination of adenine and guanine in DNA extract by micellar electrokinetic chromatography with indirect laser-induced fluorescence detection. Talanta. 2008;74:1050–1055. doi: 10.1016/j.talanta.2007.06.047. [DOI] [PubMed] [Google Scholar]
  • [64].George P M, LaVan D A, Burdick J A, Chen C Y, Liang E, Langer R. Electrically controlled drug delivery from biotin-doped conductive polypyrrole. Adv. Mater. 2006;18:577–581. doi: 10.1002/adma.200501242. [DOI] [Google Scholar]
  • [65].Wang L N, Liu X Y, Fu J Q, Ning X Y, Zhang M X, Jiang Z Y, Cheng G S, Zhu Y M, Zhang Z J. Release of methylene blue from graphene oxide-coated electrospun nanofibrous scaffolds to modulate functions of neural progenitor cells. Acta Biomater. 2019;88:346–356. doi: 10.1016/j.actbio.2019.02.036. [DOI] [PubMed] [Google Scholar]
  • [66].Samanta D, Meiser J L, Zare R N. Polypyrrole nanoparticles for tunable, pH-sensitive and sustained drug release. Nanoscale. 2015;7:9497–9504. doi: 10.1039/C5NR02196K. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

12274_2022_4613_MOESM1_ESM.pdf (1.6MB, pdf)

Electrically controlled mRNA delivery using a polypyrrole-graphene oxide hybrid film to promote osteogenic differentiation of human mesenchymal stem cells

Articles from Nano Research are provided here courtesy of Nature Publishing Group

RESOURCES