Cell specificity of magnetic cell seeding approach to hydrogel colonization
Raminder Singh
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Department of Cardiology and Angiology, University Hospital Erlangen, Erlangen, Germany
Search for more papers by this authorAnna Wieser
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorSupachai Reakasame
Institute of Biomaterials, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorRainer Detsch
Institute of Biomaterials, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorBarbara Dietel
Department of Cardiology and Angiology, University Hospital Erlangen, Erlangen, Germany
Search for more papers by this authorChristoph Alexiou
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorAldo R. Boccaccini
Institute of Biomaterials, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorCorresponding Author
Iwona Cicha
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Correspondence to: I. Cicha; E-mail: [email protected] or [email protected]Search for more papers by this authorRaminder Singh
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Department of Cardiology and Angiology, University Hospital Erlangen, Erlangen, Germany
Search for more papers by this authorAnna Wieser
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorSupachai Reakasame
Institute of Biomaterials, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorRainer Detsch
Institute of Biomaterials, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorBarbara Dietel
Department of Cardiology and Angiology, University Hospital Erlangen, Erlangen, Germany
Search for more papers by this authorChristoph Alexiou
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorAldo R. Boccaccini
Institute of Biomaterials, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Search for more papers by this authorCorresponding Author
Iwona Cicha
Section of Experimental Oncology and Nanomedicine (SEON), Else Kröner-Fresenius-Stiftung-endowed Professorship for Nanomedicine, ENT Department, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany
Correspondence to: I. Cicha; E-mail: [email protected] or [email protected]Search for more papers by this authorDisclosure: The authors have declared no conflicts of interest.
Abstract
Tissue-engineered scaffolds require an effective colonization with cells. Superparamagnetic iron oxide nanoparticles (SPIONs) can enhance cell adhesion to matrices by magnetic cell seeding. We investigated the possibility of improving cell attachment and growth on different alginate-based hydrogels using fibroblasts and endothelial cells (ECs) loaded with SPIONs. Hydrogels containing pure alginate (Alg), alginate dialdehyde crosslinked with gelatin (ADA-G) and Alg blended with G or silk fibroin (SF) were prepared. Endothelial cells and fibroblasts loaded with SPIONs were seeded and grown on hydrogels for up to 7 days, in the presence of magnetic field during the first 24 h. Cell morphology (fluorescent staining) and metabolic activity (WST-8 assay) of magnetically-seeded versus conventionally seeded cells were compared. Magnetic seeding of ECs improved their initial attachment and further growth on Alg/G hydrogel surfaces. However, we did not achieve an efficient and stable colonization of ADA-G films with ECs even with magnetic cell seeding. Fibroblast showed good initial colonization and growth on ADA-G and on Alg/SF. This effect was further significantly enhanced by magnetic cell seeding. On pure Alg, initial attachment and spreading of magnetically-seeded cells was dramatically improved compared to conventionally-seeded cells, but the effect was transient and diminished gradually with the cessation of magnetic force. Our results demonstrate that magnetic seeding improves the strength and uniformity of initial cell attachment to hydrogel surface in cell-specific manner, which may play a decisive role for the outcome in tissue engineering applications. © 2017 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 105A: 2948–2956, 2017.
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REFERENCES
- 1Wheeldon I, Farhadi A, Bick AG, Jabbari E, Khademhosseini A. Nanoscale tissue engineering: spatial control over cell–materials interactions. Nanotechnology 2011; 22: 212001.
- 2Murphy SV, Atala A. Organ engineering–combining stem cells, biomaterials, and bioreactors to produce bioengineered organs for transplantation. BioEssays News Rev Mol Cell Develop Biol 2013; 35: 163–172.
- 3Hoffman AS. Hydrogels for biomedical applications. Adv Drug Deliv Rev 2012; 64: 18–23.
- 4Wohlrab S, Muller S, Schmidt A, Neubauer S, Kessler H, Leal-Egana A, Scheibel T. Cell adhesion and proliferation on RGD-modified recombinant spider silk proteins. Biomaterials 2012; 33: 6650–6659.
- 5Saarai A, Kasparkova V, Sedlacek T, Saha P. On the development and characterisation of crosslinked sodium alginate/gelatine hydrogels. J Mech Behav Biomed Mater 2013; 18: 152–166.
- 6Boanini E, Rubini K, Panzavolta S, Bigi A. Chemico-physical characterization of gelatin films modified with oxidized alginate. Acta Biomater 2010; 6: 383–388.
- 7Sarker B, Papageorgiou DG, Silva R, Zehnder T, Gul-E-Noor F, Bertmer M, Kaschta J, Chrissafis K, Detsch R, Boccaccini AR. Fabrication of alginate–gelatin crosslinked hydrogel microcapsules and evaluation of the microstructure and physico-chemical properties. J Mater Chem B 2014; 2: 1470–1482.
- 8Sarker B, Singh R, Silva R, Roether JA, Kaschta J, Detsch R, Schubert DW, Cicha I, Boccaccini AR. Evaluation of Fibroblasts Adhesion and proliferation on alginate–gelatin crosslinked hydrogel. PLoS One 2014; 9: e107952.
- 9Silva R, Singh R, Sarker B, Papageorgiou DG, Juhasz JA, Roether JA, Cicha I, Kaschta J, Schubert DW, Chrissafis K, Detsch R, Boccaccini AR. Hybrid hydrogels based on keratin and alginate for tissue engineering. J Mater Chem B 2014; 2: 5441–5451.
- 10Silva R, Singh R, Sarker B, Papageorgiou DG, Juhasz JA, Roether JA, Cicha I, Kaschta J, Schubert DW, Chrissafis K, Detsch R, Boccaccini AR. Soft-matrices based on silk fibroin and alginate for tissue engineering. Int J Biol Macromol 2016; 93: 1420–1431.
- 11Singh R, Sarker B, Silva R, Detsch R, Dietel B, Alexiou C, Boccaccini AR, Cicha I. Evaluation of hydrogel matrices for vessel bioplotting: Vascular cell growth and viability. J Biomed Mater Res A 2016; 104: 577–585.
- 12Li S, Sengupta D, Chien S. Vascular tissue engineering: From in vitro to in situ. Wiley Interdiscip Rev Syst Biol Med 2014; 6: 61–76.
- 13Tietze R, Lyer S, Durr S, Struffert T, Engelhorn T, Schwarz M, Eckert E, Goen T, Vasylyev S, Peukert W, Wiekhorst F, Trahms L, Dorfler A, Alexiou C. Efficient drug–delivery using magnetic nanoparticles—Biodistribution and therapeutic effects in tumour bearing rabbits. Nanomedicine 2013; 9: 961–971.
- 14Kobayashi T, Kakimi K, Nakayama E, Jimbow K. Antitumor immunity by magnetic nanoparticle-mediated hyperthermia. Nanomedicine 2014; 9: 1715–1726.
- 15Sapir Y, Polyak B, Cohen S. Cardiac tissue engineering in magnetically actuated scaffolds. Nanotechnology 2014; 25: 014009.
- 16Ventrelli L, Fujie T, Del Turco S, Basta G, Mazzolai B, Mattoli V. Influence of nanoparticle-embedded polymeric surfaces on cellular adhesion, proliferation, and differentiation. J Biomed Mater Res A 2014; 102: 2652–2661.
- 17Sapir Y, Cohen S, Friedman G, Polyak B. The promotion of in vitro vessel-like organization of endothelial cells in magnetically responsive alginate scaffolds. Biomaterials 2012; 33: 4100–4109.
- 18Sapir-Lekhovitser Y, Rotenberg MY, Jopp J, Friedman G, Polyak B, Cohen S. Magnetically actuated tissue engineered scaffold: Insights into mechanism of physical stimulation. Nanoscale 2016; 8: 3386–3399.
- 19Ito A, Ino K, Hayashida M, Kobayashi T, Matsunuma H, Kagami H, Ueda M, Honda H. Novel methodology for fabrication of tissue-engineered tubular constructs using magnetite nanoparticles and magnetic force. Tissue Eng 2005; 11: 1553–1561.
- 20Sasaki T, Iwasaki N, Kohno K, Kishimoto M, Majima T, Nishimura SI, Minami A. Magnetic nanoparticles for improving cell invasion in tissue engineering. J Biomed Mater Res A 2008; 86A: 969–978.
- 21Thevenot P, Sohaebuddin S, Poudyal N, Liu JP, Tang L. Magnetic nanoparticles to enhance cell seeding and distribution in tissue engineering scaffolds. Proc IEEE Conf Nanotechnol IEEE Conf Nanotechnol 2008; 2008: 646–649.
- 22Shimizu K, Ito A, Honda H. Mag-seeding of rat bone marrow stromal cells into porous hydroxyapatite scaffolds for bone tissue engineering. J Biosci Bioeng 2007; 104: 171–177.
- 23Shimizu K, Ito A, Arinobe M, Murase Y, Iwata Y, Narita Y, Kagami H, Ueda M, Honda H. Effective cell-seeding technique using magnetite nanoparticles and magnetic force onto decellularized blood vessels for vascular tissue engineering. J Biosci Bioeng 2007; 103: 472–478.
- 24Perea H, Aigner J, Hopfner U, Wintermantel E. Direct magnetic tubular cell seeding: A novel approach for vascular tissue engineering. Cells Tissues Org 2006; 183: 156–165.
- 25Gonzalez-Molina J, Riegler J, Southern P, Ortega D, Frangos CC, Angelopoulos Y, Husain S, Lythgoe MF, Pankhurst QA, Day RM. Rapid magnetic cell delivery for large tubular bioengineered constructs. J R Soc Interface 2012; 9: 3008–3016.
- 26Perea H, Aigner J, Heverhagen JT, Hopfner U, Wintermantel E. Vascular tissue engineering with magnetic nanoparticles: Seeing deeper. J Tissue Eng Regen Mater 2007; 1: 318–321.
- 27Khalafalla SE, Reimers GW. Preparation of dilution-stable aqueous magnetic fluids. IEEE Trans Magn 1980; 16: 178–183.
- 28Rockwood DN, Preda RC, Yucel T, Wang X, Lovett ML, Kaplan DL. Materials fabrication from Bombyx mori silk fibroin. Nat Protoc 2011; 6: 1612–1631.
- 29Sarker B, Singh R, Zehnder T, Forgber T, Alexiou C, Cicha I, Detsch R, Boccaccini AR. Macromolecular interactions in alginate–gelatin hydrogels regulate the behavior of human fibroblasts. J Bioactive Comp Polym 2017; 32: 309–324.
- 30Cicha I, Goppelt-Struebe M, Muehlich S, Yilmaz A, Raaz D, Daniel WG, Garlichs CD. Pharmacological inhibition of RhoA signaling prevents connective tissue growth factor induction in endothelial cells exposed to non-uniform shear stress. Atherosclerosis 2008; 196: 136–145.
- 31Gabbieri D, Dohmen PM, Koch C, Lembcke A, Rutsch W, Konertz W. Aortocoronary endothelial cell-seeded polytetrafluoroethylene graft: 9-year patency. Ann Thorac Surg 2007; 83: 1166–1168.
- 32Deutsch M, Meinhart J, Zilla P, Howanietz N, Gorlitzer M, Froeschl A, Stuempflen A, Bezuidenhout D, Grabenwoeger M. Long-term experience in autologous in vitro endothelialization of infrainguinal ePTFE grafts. J Vasc Surg 2009; 49: 352–362; discussion 362.
- 33Samal SK, Goranov V, Dash M, Russo A, Shelyakova T, Graziosi P, Lungaro L, Riminucci A, Uhlarz M, Banobre-Lopez M, Rivas J, Herrmannsdorfer T, Rajadas J, De Smedt S, Braeckmans K, Kaplan DL, Dediu VA. Multilayered magnetic gelatin membrane scaffolds. Acs Appl Mater Inter 2015; 7: 23098–23109.
- 34Kim JA, Choi JH, Kim M, Rhee WJ, Son B, Jung HK, Park TH. High-throughput generation of spheroids using magnetic nanoparticles for three-dimensional cell culture. Biomaterials 2013; 34: 8555–8563.
- 35Ghosh S, Kumar SR, Puri IK, Elankumaran S. Magnetic assembly of 3D cell clusters: Visualizing the formation of an engineered tissue. Cell Prolif 2016; 49: 134–144.
- 36Richards JM, Shaw CA, Lang NN, Williams MC, Semple SI, MacGillivray TJ, Gray C, Crawford JH, Alam SR, Atkinson AP, Forrest EK, Bienek C, Mills NL, Burdess A, Dhaliwal K, Simpson AJ, Wallace WA, Hill AT, Roddie PH, McKillop G, Connolly TA, Feuerstein GZ, Barclay GR, Turner ML, Newby DE. In vivo mononuclear cell tracking using superparamagnetic particles of iron oxide: Feasibility and safety in humans. Circ Cardiovasc Imaging 2012; 5: 509–517.