A polydopamine peptide coating enables adipose-derived stem cell growth on the silicone surface of cochlear implant electrode arrays
Corresponding Author
Philipp Schendzielorz
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Correspondence to: P. Schendzielorz; e-mail: [email protected]Search for more papers by this authorKristen Rak
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorKatrin Radeloff
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorJohannes Völker
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorThomas Gehrke
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorAgmal Scherzad
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorNorbert Kleinsasser
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorRudolf Hagen
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorAndreas Radeloff
Department of Oto-Rhino-Laryngology, Head and Neck Surgery, Carl von Ossietzky-University, Oldenburg, Germany
Search for more papers by this authorCorresponding Author
Philipp Schendzielorz
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Correspondence to: P. Schendzielorz; e-mail: [email protected]Search for more papers by this authorKristen Rak
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorKatrin Radeloff
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorJohannes Völker
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorThomas Gehrke
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorAgmal Scherzad
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorNorbert Kleinsasser
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorRudolf Hagen
Department of Oto-Rhino-Laryngology, Plastic, Aesthetic, and Reconstructive Head and Neck Surgery, Comprehensive Hearing Center, University of Wuerzburg, Josef-Schneider-Straße 11, 97080 Wuerzburg, Germany
Search for more papers by this authorAndreas Radeloff
Department of Oto-Rhino-Laryngology, Head and Neck Surgery, Carl von Ossietzky-University, Oldenburg, Germany
Search for more papers by this authorAbstract
The simultaneous application of neurotrophic factors with cochlear implantation is proposed to enhance the bioelectrical interface between electrodes and auditory neurons, and thus improve speech intelligibility in patients with cochlear implants (CIs). In cell-based approaches, the goal is to colonize CIs with cells producing neurotrophic factors. This study aims to evaluate whether a polydopamine (PD) functionalization of the hydrophobic silicone surface of the electrode carrier enables colonization of adipose-derived stem cells known to deliver neurotrophic factors. Surface characteristics of PD-coated silicone samples and electrode carriers were determined, and the proliferation and viability of adipose-derived stem cells (ASCs) on these surfaces were subsequently analyzed. A homogenous PD coating and cell growth with regular morphology was observed on coated silicone samples and electrode arrays. Hydrophilicity and cell viability was significantly enhanced by PD surface modification. Insertion forces of coated electrode arrays did not increase compared with untreated CIs. Hence, PD coating of the silicone surface of CIs might allow for sufficient colonization with ASCs as a continuous source of neurotrophic factors. © 2017 Wiley Periodicals, Inc. J Biomater Res Part A: 106B: 1431–1438, 2018.
REFERENCES
- 1 Wilson BS, Dorman MF. Cochlear implants: current designs and future possibilities. J Rehabil Res Dev 2008; 45(5): 695–730.
- 2 Srinivasan AG, Shannon RV, Landsberger DM. Improving virtual channel discrimination in a multi-channel context. Hear Res 2012; 286(1–2): 19–29.
- 3
O'Leary SJ,
Richardson RR,
McDermott HJ. Principles of design and biological approaches for improving the selectivity of cochlear implant electrodes. J Neural Eng 2009; 6(5): 055002.
10.1088/1741-2560/6/5/055002 Google Scholar
- 4
Wise AK,
Fallon JB,
Neil AJ,
Pettingill LN,
Geaney MS,
Skinner SJ,
Shepherd RK. Combining cell-based therapies and neural prostheses to promote neural survival. Neurotherapeutics 2011; 8(4): 774–787.
10.1007/s13311-011-0070-0 Google Scholar
- 5 Gillespie LN, Shepherd RK. Clinical application of neurotrophic factors: the potential for primary auditory neuron protection. Eur J Neurosci 2005; 22(9): 2123–2133.
- 6
Glueckert R,
Bitsche M,
Miller JM,
Zhu Y,
Prieskorn DM,
Altschuler RA,
Schrott-Fischer A. Deafferentation-associated changes in afferent and efferent processes in the guinea pig cochlea and afferent regeneration with chronic intrascalar brain-derived neurotrophic factor and acidic fibroblast growth factor. J Comp Neurol 2008; 507(4): 1602–1621.
10.1002/cne.21619 Google Scholar
- 7 Landry TG, Wise AK, Fallon JB, Shepherd RK. Spiral ganglion neuron survival and function in the deafened cochlea following chronic neurotrophic treatment. Hear Res 2011; 282(1–2): 303–313.
- 8 Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7(2): 211–228.
- 9 Kalbermatten DF, Schaakxs D, Kingham PJ, Wiberg M. Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat. Cell Tissue Res 2011; 344(2): 251–260.
- 10 Kingham PJ, Kolar MK, Novikova LN, Novikov LN, Wiberg M. Stimulating the neurotrophic and angiogenic properties of human adipose-derived stem cells enhances nerve repair. Stem Cells Dev 2014; 23(7): 741–754.
- 11
Schendzielorz P,
Scherzed A,
Rak K,
Volker J,
Hagen R,
Mlynski R,
Frolich K,
Radeloff A. A hydrogel coating for cochlear implant arrays with encapsulated adipose-derived stem cells allows brain-derived neurotrophic factor delivery. Acta Otolaryngol 2014; 134(5): 497–505.
10.3109/00016489.2013.878809 Google Scholar
- 12 Wilson A, Butler PE, Seifalian AM. Adipose-derived stem cells for clinical applications: a review. Cell Prolif 2011; 44(1): 86–98.
- 13 Dundua A, Franzka S, Ulbricht M. Improved antifouling properties of polydimethylsiloxane films via formation of polysiloxane/polyzwitterion interpenetrating networks. Macromol Rapid Commun 2016; 37(24): 2030–2036.
- 14
Fatona A,
Chen Y,
Reid M,
Brook MA,
Moran-Mirabal JM. One-step in-mould modification of PDMS surfaces and its application in the fabrication of self-driven microfluidic channels. Lab Chip 2015; 15(22): 4322–4330.
10.1039/C5LC00741K Google Scholar
- 15 Lei ZY, Liu T, Li WJ, Shi XH, Fan DL. Biofunctionalization of silicone rubber with microgroove-patterned surface and carbon-ion implantation to enhance biocompatibility and reduce capsule formation. Int J Nanomedicine 2016; 11: 5563–5572.
- 16 Jensen C, Gurevich L, Patriciu A, Struijk JJ, Zachar V, Pennisi CP. Increased connective tissue attachment to silicone implants by a water vapor plasma treatment. J Biomed Mater Res A 2012; 100(12): 3400–3407.
- 17 Lee H, Dellatore SM, Miller WM, Messersmith PB. Mussel-inspired surface chemistry for multifunctional coatings. Science 2007; 318(5849): 426–430.
- 18 Lim K, Chua RR, Bow H, Tambyah PA, Hadinoto K, Leong SS. Development of a catheter functionalized by a polydopamine peptide coating with antimicrobial and antibiofilm properties. Acta Biomater 2015; 15: 127–138.
- 19 Wang R, Neoh KG, Shi Z, Kang ET, Tambyah PA, Chiong E. Inhibition of Escherichia coli and Proteus mirabilis adhesion and biofilm formation on medical grade silicone surface. Biotechnol Bioeng 2012; 109(2): 336–345.
- 20 Radeloff A, Unkelbach MH, Mack MG, Settevendemie C, Helbig S, Mueller J, Hagen R, Mlynski R. A coated electrode carrier for cochlear implantation reduces insertion forces. Laryngoscope 2009; 119(5): 959–963.
- 21
Schendzielorz P,
Rak K,
Nguyen J,
Frolich K,
Scherzad A,
Hagen R,
Radeloff A. Human adipose-derived stem cells enhance the survival and neuritogenesis of auditory neurons. Neuroreport 2015; 26(13): 797–801.
10.1097/WNR.0000000000000427 Google Scholar
- 22 Fetoni AR, Lattanzi W, Eramo SL, Barba M, Paciello F, Moriconi C, Rolesi R, Michetti F, Troiani D, Paludetti G. Grafting and early expression of growth factors from adipose-derived stem cells transplanted into the cochlea, in a Guinea pig model of acoustic trauma. Front Cell Neurosci 2014; 8: 334.
- 23 Liu XL, Zhang W, Tang SJ. Intracranial transplantation of human adipose-derived stem cells promotes the expression of neurotrophic factors and nerve repair in rats of cerebral ischemia-reperfusion injury. Int J Clin Exp Pathol 2014; 7(1): 174–183.
- 24 Chuah YJ, Koh YT, Lim K, Menon NV, Wu Y, Kang Y. Simple surface engineering of polydimethylsiloxane with polydopamine for stabilized mesenchymal stem cell adhesion and multipotency. Sci Rep 2015; 5: 18162.
- 25 Lee H, Scherer NF, Messersmith PB. Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci U S A 2006; 103(35): 12999–13003.
- 26 Ball V, Del Frari D, Toniazzo V, Ruch D. Kinetics of polydopamine film deposition as a function of pH and dopamine concentration: insights in the polydopamine deposition mechanism. J Colloid Interface Sci 2012; 386(1): 366–372.
- 27 Hauser J, Zietlow J, Koller M, Esenwein SA, Halfmann H, Awakowicz P, Steinau HU. Enhanced cell adhesion to silicone implant material through plasma surface modification. J Mater Sci Mater Med 2009; 20(12): 2541–2548.
- 28 Ding X, Yang C, Lim TP, Hsu LY, Engler AC, Hedrick JL, Yang YY. Antibacterial and antifouling catheter coatings using surface grafted PEG-b-cationic polycarbonate diblock copolymers. Biomaterials 2012; 33(28): 6593–6603.
- 29 Lee JH, Lee YJ, Cho HJ, Shin H. Guidance of in vitro migration of human mesenchymal stem cells and in vivo guided bone regeneration using aligned electrospun fibers. Tissue Eng Part A 2014; 20(15–16): 2031–2042.
- 30 Ku SH, Lee JS, Park CB. Spatial control of cell adhesion and patterning through mussel-inspired surface modification by polydopamine. Langmuir 2010; 26(19): 15104–15108.
- 31 Lee H, Rho J, Messersmith PB. facile conjugation of biomolecules onto surfaces via mussel adhesive protein inspired coatings. Adv Mater 2009; 21(4): 431–434.
- 32 Ku SH, Ryu J, Hong SK, Lee H, Park CB. General functionalization route for cell adhesion on non-wetting surfaces. Biomaterials 2010; 31(9): 2535–2541.
- 33 Taskin MB XR, Gregersen H, Nygaard JV, Besenbacher F, Chen M. Three-dimensional polydopamine functionalized coiled microfibrous scaffolds enhance human mesenchymal stem cells colonization and mild myofibroblastic differentiation. ACS Appl Mater Interfaces 2016; 8(25): 15864–15873
- 34 Ko E, Yang K, Shin J, Cho SW. Polydopamine-assisted osteoinductive peptide immobilization of polymer scaffolds for enhanced bone regeneration by human adipose-derived stem cells. Biomacromolecules 2013; 14(9): 3202–3213.
- 35 Yang K, Lee JS, Kim J, Lee YB, Shin H, Um SH, Kim JB, Park KI, Lee H, Cho SW. Polydopamine-mediated surface modification of scaffold materials for human neural stem cell engineering. Biomaterials 2012; 33(29): 6952–6964.
- 36 Schendzielorz P, Schmitz T, Moseke C, Gbureck U, Frolich K, Rak K, Groll J, Hagen R, Radeloff A. Plasma-assisted hydrophilization of cochlear implant electrode array surfaces enables adhesion of neurotrophin-secreting cells. ORL J Otorhinolaryngol Relat Spec 2014; 76(5): 257–265.
- 37 Kontorinis G, Scheper V, Wissel K, Stover T, Lenarz T, Paasche G. In vitro modifications of the scala tympani environment and the cochlear implant array surface. Laryngoscope 2012; 122(9): 2057–63.
- 38 Bettinger CJ, Bruggeman JP, Misra A, Borenstein JT, Langer R. Biocompatibility of biodegradable semiconducting melanin films for nerve tissue engineering. Biomaterials 2009; 30(17): 3050–3057.
