Versatility of unsaturated polyesters from electrospun macrolactones: RGD immobilization to increase cell attachment.


Journal

Journal of biomedical materials research. Part A
ISSN: 1552-4965
Titre abrégé: J Biomed Mater Res A
Pays: United States
ID NLM: 101234237

Informations de publication

Date de publication:
02 2022
Historique:
revised: 19 07 2021
received: 29 10 2020
accepted: 21 07 2021
pubmed: 30 7 2021
medline: 1 4 2022
entrez: 29 7 2021
Statut: ppublish

Résumé

Poly(globalide) (PGl), an aliphatic polyester derived from unsaturated macrocylic lactone, can be cross-linked during electrospinning and drug-loaded for regenerative medicine applications. However, it lacks intrinsic recognition sites for cell adhesion and proliferation. In order to improve their cell adhesiveness, and therefore their therapeutic potential, we aimed to functionalize electrospun PGl fibers with RGD sequence generating a biomimetic scaffold. First, an amine compound was attached to the surface double bonds of the PGl fibers. Subsequently, the amino groups were coupled with RGD sequences. X-ray photoelectron spectroscopy (XPS) analysis confirmed the functionalization. The obtained fibers were more hydrophilic, as observed by contact angle analysis, and presented smaller Young's modulus, although similar tensile strength compared with non-functionalized cross-linked fibers. In addition, the functionalization process did not significantly alter fibers morphology, as observed by scanning electron microscopy (SEM). Finally, in vitro analysis evidenced the increase in human mesenchymal stromal cells (hMSC) adhesion (9.88 times higher DNA content after 1 day of culture) and proliferation (3.57 times higher DNA content after 8 days of culture) compared with non-functionalized non-cross-linked fibers. This is the first report demonstrating the functionalization of PGl fibers with RGD sequence, improving PGl therapeutic potential and further corroborating the use of this highly versatile material toward regenerative medicine applications.

Identifiants

pubmed: 34322978
doi: 10.1002/jbm.a.37282
doi:

Substances chimiques

Oligopeptides 0
Polyesters 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

257-265

Subventions

Organisme : Science Foundation Ireland
ID : 13/RC/2073
Pays : Ireland

Informations de copyright

© 2021 The Authors. Journal of Biomedical Materials Research Part A published by Wiley Periodicals LLC.

Références

Seyednejad H, Ghassemi AH, van Nostrum CF, Vermonden T, Hennink WE. Functional aliphatic polyesters for biomedical and pharmaceutical applications. J Control Release. 2011;152:168-176.
Nair LS, Laurencin CT. Biodegradable polymers as biomaterials. Prog Polym Sci. 2007;32:762-798.
Labet M, Thielemans W. Synthesis of polycaprolactone: a review. Chem Soc Rev. 2009;38:3484-3504.
Pham QP, Sharma U, Mikos AG. Electrospun poly(epsilon-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules. 2006;7:2796-2805.
Albertsson A-C, Varma IK. Aliphatic Polyesters: Synthesis, Properties and Applications. Degradable Aliphatic Polyesters. Berlin, Heidelberg: Springer Berlin Heidelberg; 2002:1-40.
Brannigan RP, Dove AP. Synthesis, properties and biomedical applications of hydrolytically degradable materials based on aliphatic polyesters and polycarbonates. Biomater Sci. 2016;5:9-21.
Mo XM, Xu CY, Kotaki M, Ramakrishna S. Electrospun P(LLA-CL) nanofiber: a biomimetic extracellular matrix for smooth muscle cell and endothelial cell proliferation. Biomaterials. 2004;25:1883-1890.
Gang EH, Ki CS, Kim JW, et al. Highly porous three-dimensional poly(lactide-co-glycolide) (PLGA) microfibrous scaffold prepared by electrospinning method: a comparison study with other PLGA type scaffolds on its biological evaluation. Fiber Polym. 2012;13:685-691.
Zhan J, Singh A, Zhang Z, Huang L, Elisseeff JH. Multifunctional aliphatic polyester nanofibers for tissue engineering. Biomatter. 2012;2:202-212.
Rogina A. Electrospinning process: versatile preparation method for biodegradable and natural polymers and biocomposite systems applied in tissue engineering and drug delivery. Appl Surf Sci. 2014;296:221-230.
Vasita R, Dhirendra SK. Nanofibers and their applications in tissue engineering. Int J Nanomedicine. 2006;1:15-30.
Yang F, Murugan R, Wang S, Ramakrishna S. Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials. 2005;26:2603-2610.
Liu H, Ding X, Zhou G, Li P, Wei X, Fan Y. Electrospinning of Nanofibers for tissue engineering applications. J Nanomater. 2013;495708.
Mota C, Puppi D, Dinucci D, Errico C, Bártolo P, Chiellini F. Dual-scale polymeric constructs as scaffolds for tissue engineering. Materials. 2011;4:527-542.
Dash TK, Konkimalla VB. Poly-e-caprolactone based formulations for drug delivery and tissue engineering: a review. J Control Release. 2012;158:15-33.
Hersel U, Dahmen C, Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials. 2003;24:4385-4415.
Lee K-B, Yoon KR, Woo SI, Choi IS. Surface modification of poly(glycolic acid) (PGA) for biomedical applications. J Pharm Sci. 2003;92:933-937.
Szentivanyi A, Chakradeo T, Zernetsch H, Glasmacher B. Electrospun cellular microenvironments: understanding controlled release and scaffold structure. Adv Drug Deliv Rev. 2011;63:209-220.
Yoshida S, Hagiwara K, Hasebe T, Hotta A. Surface modification of polymers by plasma treatments for the enhancement of biocompatibility and controlled drug release. Surf Coat Technol. 2013;233:99-107.
Arnaout MA, Mahalingam B, Xiong JP. Integrin structure, allostery, and bidirectional signaling. Annu Rev Cell Dev Biol. 2005;21:381-410.
Takada Y, Ye X, Simon S. The integrins. Genome Biol. 2007;8:215.
Shin H, Jo S, Mikos AG. Biomimetic materials for tissue engineering. Biomaterials. 2003;24:4353-4364.
Zhang Z, Lai Y, Yu L, Ding J. Effects of immobilizing sites of RGD peptides in amphiphilic block copolymers on efficacy of cell adhesion. Biomaterials. 2010;31:7873-7882.
Ranieri JP, Bellamkonda R, Bekos EJ, Vargo TG, Gardella JA Jr, Aebischer P. Neuronal cell attachment to fluorinated ethylene propylene films with covalently immobilized laminin oligopeptides YIGSR and IKVAV. II. J Biomed Mater Res. 1995;29:779-785.
Bellis SL. Advantages of RGD peptides for directing cell association with biomaterials. Biomaterials. 2011;32:4205-4210.
Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol. 1996;12(1):697-715.
Abdul Kafi M, El-Said WA, Kim TH, Choi JW. Cell adhesion, spreading, and proliferation on surface functionalized with RGD nanopillar arrays. Biomaterials. 2012;33:731-739.
Wang X, Yan C, Ye K, He Y, Li Z, Ding J. Effect of RGD nanospacing on differentiation of stem cells. Biomaterials. 2013;34:2865-2874.
de Luca AC, Stevens JS, Schroeder SL, et al. Immobilization of cell-binding peptides on poly-e-caprolactone film surface to biomimic the peripheral nervous system. J Biomed Mater Res A. 2013;101:491-501.
Huang Y, Ren J, Ren T, et al. Bone marrow stromal cells cultured on poly (lactide-co-glycolide)/nano-hydroxyapatite composites with chemical immobilization of Arg-Gly-Asp peptide and preliminary bone regeneration of mandibular defect thereof. J Biomed Mater Res A. 2010;95:993-1003.
Zhang H, Lin C-Y, Hollister SJ. The interaction between bone marrow stromal cells and RGD-modified three-dimensional porous polycaprolactone scaffolds. Biomaterials. 2009;30:4063-4069.
Wilson JA, Ates Z, Pflughaupt RL, Dove A, Heise A. Polymers from macrolactones: from pheromones to functional materials. Prog Polym Sci. 2019;91:29-50.
Chiaradia V, Hanay SB, Kimmins SD, et al. Crosslinking of electrospun fibres from unsaturated polyesters by bis-triazolinediones (TAD). Polymers. 2019;11:1808.
Ates Z, Heise A. Functional films from unsaturated poly(macrolactones) by thiol-ene cross-linking and functionalisation. Polym Chem. 2014;5:2936-2941.
Ates Z, Audouin F, Harrington A, O'Connor B, Heise A. Functional brush-decorated poly (globalide) films by ARGET-ATRP for bioconjugation. Macromol Biosci. 2014;14:16001608.
Savin CL, Peptu C, Kroneková Z, et al. Polyglobalide-based porous networks containing poly(ethylene glycol) structures prepared by photoinitiated thiol-ene coupling. Biomacromolecules. 2018;19:3331-3342.
Guindani C, Dozoretz P, Araújo PHH, Ferreira SRS, De Oliveira D. N-acetylcysteine side-chain functionalization of poly(globalide-co-ε-caprolactone) through thiol-ene reaction. Mater Sci Eng C. 2019;94:477-483.
Van Der Meulen I, Li Y, Deumens R, Joosten EJ, Koning CE, Heise A. Copolymers from unsaturated macrolactones: toward the design of cross-linked biodegradable polyesters. Biomacromolecules. 2011;12:837-843.
de Oliveira FCS, Oliveira D, Sawkins MJ, et al. Direct UV-triggered thiol-ene cross-linking of electrospun polyester fibers from unsaturated poly(macrolactone)s and their drug loading by solvent swelling. Biomacromolecules. 2017;18(12):4292-4298.
Polloni AE, Chiaradia V, RJFC DA, et al. Polyesters with main and side chain phosphoesters as structural motives for biocompatible electrospun fibres. Polym Chem. 2020;11:2157-2165.
Santiago LY, Nowak RW, Peter Rubin J, Marra KG. Peptide-surface modification of poly(caprolactone) with laminin-derived sequences for adipose-derived stem cell applications. Biomaterials. 2006;27:2962-2969.
Schneider C, Rasband W, Eliceiri K. NIH image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671-675.
Barreto S, Gonzalez-Vazquez A, Cameron AR, Cavanagh B, Murray DJ, O'Brien FJ. Identification of the mechanisms by which age alters the mechanosensitivity of mesenchymal stromal cells on substrates of differing stiffness: implications for osteogenesis and angiogenesis. Acta Biomater. 2017;53:59-69.
Baji A, Mai Y-W, Wong S-C, Abtahi M, Chen P. Electrospinning of polymer nanofibers: effects on oriented morphology, structures and tensile properties. Compos Sci Technol. 2010;70:703-718.
Oh SH, Kang SG, Kim ES, Cho SH, Lee JH. Fabrication and characterization of hydrophilic poly(lactic-co-glycolic acid)/poly(vinyl alcohol) blend cell scaffolds by melt-molding particulate-leaching method. Biomaterials. 2003;24:4011-4021.
Pourcelle V, Devouge S, Garinot M, Preat V, Marchand-Brynaert J. PCL-PEG-based nanoparticles grafted with GRGDS peptide: preparation and surface analysis by XPS. Biomacromolecules. 2007;8:3977-3983.
Wohlrab S, Muller S, Schmidt A, et al. Cell adhesion and proliferation on RGD-modified recombinant spider silk proteins. Biomaterials. 2012;33:6650-6659.
Jin Yoon J, Ho Song S, Sung Lee D, Park TG. Immobilization of cell adhesive RGD peptide onto the surface of highly porous biodegradable polymer scaffolds fabricated by a gas foaming/salt leaching method. Biomaterials. 2004;25:5613-5620.
Li B, Chen J, Wang JH. RGD peptide-conjugated poly(dimethylsiloxane) promotes adhesion, proliferation, and collagen secretion of human fibroblasts. J Biomed Mater Res A. 2006;79:989-998.
Han F, Zhu C, Guo Q, Yang H, Li B. Cellular modulation by the elasticity of biomaterials. J Mater Chem B. 2016;4:9-26.
Jhala D, Vasita R. A review on extracellular matrix mimicking strategies for an artificial stem cell niche. Polym Rev. 2015;55:561-595.
Kalra A, Lowe A, Al-Jumaily AM. Mechanical behaviour of skin: a review. J Mater Sci Eng. 2016;5:1000254.
Griffin MF, Leung BC, Premakumar Y, Szarko M, Butler PE. Comparison of the mechanical properties of different skin sites for auricular and nasal reconstruction. J Otolaryngol Head Neck Surg. 2017;46:33.
Kim CH, Khil MS, Kim HY, Lee HU, Jahng KY. An improved hydrophilicity via electrospinning for enhanced cell attachment and proliferation. J Biomed Mater Res B. 2006;78B:283-290.
Zamani F, Amani-Tehran M, Latifi M, Shokrgozar MA. The influence of surface nanoroughness of electrospun PLGA nanofibrous scaffold on nerve cell adhesion and proliferation. J Mater Sci Mater Med. 2013;24:1551-1560.
Jeon H, Lee H, Kim G. A surface-modified poly(ɛ-caprolactone) scaffold comprising variable nanosized surface-roughness using a plasma treatment. Tissue Eng Part C Methods. 2014;20:951-963.
Perlin L, MacNeil S, Rimmer S. Production and performance of biomaterials containing RGD peptides. Soft Matter. 2008;4:2331-2349.
Wang X, Ye K, Li Z, Yan C, Ding J. Adhesion, proliferation, and differentiation of mesenchymal stem cells on RGD nanopatterns of varied nanospacings. Organogenesis. 2013;9:280-286.

Auteurs

Fernando Cabral Sales de Oliveira (FCS)

Department of Chemistry, RCSI University of Medicine and Health Science, Dublin, Ireland.

Ronaldo Jose Farias Correa do Amaral (RJFC)

Kearney Lab, Department of Anatomy and Regenerative Medicine, RCSI University of Medicine and Health Science, Dublin, Ireland.
Tissue Engineering Research Group (TERG), Department of Anatomy, RCSI University of Medicine and Health Science, Dublin, Ireland.
CÚRAM, SFI Research Centre for Medical Devices, National University of Ireland Galway (NUIG) & RCSI, Galway, Ireland.

Luiza Erthal Cardoso Dos Santos (LEC)

School of Pharmacy and Pharmaceutical Sciences, Trinity College Dublin (TCD), Dublin, Ireland.
Trinity Biomedical Sciences Institute, TCD, Dublin, Ireland.

Cian Cummins (C)

Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Dublin, Ireland.
AMBER, The SFI Centre for Advanced Materials and Bioengineering, TCD & RCSI, Dublin, Ireland.

Michael M Morris (MM)

Centre for Research on Adaptive Nanostructures and Nanodevices (CRANN), Dublin, Ireland.
AMBER, The SFI Centre for Advanced Materials and Bioengineering, TCD & RCSI, Dublin, Ireland.

Cathal J Kearney (CJ)

Kearney Lab, Department of Anatomy and Regenerative Medicine, RCSI University of Medicine and Health Science, Dublin, Ireland.
Tissue Engineering Research Group (TERG), Department of Anatomy, RCSI University of Medicine and Health Science, Dublin, Ireland.
AMBER, The SFI Centre for Advanced Materials and Bioengineering, TCD & RCSI, Dublin, Ireland.

Andreas Heise (A)

Department of Chemistry, RCSI University of Medicine and Health Science, Dublin, Ireland.
CÚRAM, SFI Research Centre for Medical Devices, National University of Ireland Galway (NUIG) & RCSI, Galway, Ireland.
AMBER, The SFI Centre for Advanced Materials and Bioengineering, TCD & RCSI, Dublin, Ireland.

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