Description of D-glucosamine immobilization kinetics onto poly(lactic acid) surface via a multistep physicochemical approach for preparation of novel active biomaterials
Ahmed E. Swilem
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Department of Chemistry, Faculty of Science, Ain Shams University, Abbassia, Cairo, 11566 Egypt
Search for more papers by this authorCorresponding Author
Marian Lehocký
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Correspondence to: M. Lehocký; e-mail: [email protected]Search for more papers by this authorPetr Humpolíček
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Search for more papers by this authorZdenka Kucekova
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Search for more papers by this authorIgor Novák
Polymer Institute, Slovak Academy of Sciences, Dúbravská cesta 9, Bratislava, Slovakia, 845 41
Search for more papers by this authorMatej Mičušík
Polymer Institute, Slovak Academy of Sciences, Dúbravská cesta 9, Bratislava, Slovakia, 845 41
Search for more papers by this authorHassan A. Abd El-Rehim
Department of Polymers, National Center for Radiation Research and Technology, Atomic Energy Authority, Nasr City, Cairo, 11371 Egypt
Search for more papers by this authorEl-Sayed A. Hegazy
Department of Polymers, National Center for Radiation Research and Technology, Atomic Energy Authority, Nasr City, Cairo, 11371 Egypt
Search for more papers by this authorAshraf A. Hamed
Department of Chemistry, Faculty of Science, Ain Shams University, Abbassia, Cairo, 11566 Egypt
Search for more papers by this authorJaroslav Kousal
Faculty of Mathematics and Physics, Charles University Prague, V Holesovickach 2, Prague 8, 18000 Czech Republic
Search for more papers by this authorAhmed E. Swilem
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Department of Chemistry, Faculty of Science, Ain Shams University, Abbassia, Cairo, 11566 Egypt
Search for more papers by this authorCorresponding Author
Marian Lehocký
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Correspondence to: M. Lehocký; e-mail: [email protected]Search for more papers by this authorPetr Humpolíček
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Search for more papers by this authorZdenka Kucekova
Centre of Polymer Systems, Tomas Bata University in Zlín, Trida Tomase Bati 5678, Zlín, 760 01 Czech Republic
Search for more papers by this authorIgor Novák
Polymer Institute, Slovak Academy of Sciences, Dúbravská cesta 9, Bratislava, Slovakia, 845 41
Search for more papers by this authorMatej Mičušík
Polymer Institute, Slovak Academy of Sciences, Dúbravská cesta 9, Bratislava, Slovakia, 845 41
Search for more papers by this authorHassan A. Abd El-Rehim
Department of Polymers, National Center for Radiation Research and Technology, Atomic Energy Authority, Nasr City, Cairo, 11371 Egypt
Search for more papers by this authorEl-Sayed A. Hegazy
Department of Polymers, National Center for Radiation Research and Technology, Atomic Energy Authority, Nasr City, Cairo, 11371 Egypt
Search for more papers by this authorAshraf A. Hamed
Department of Chemistry, Faculty of Science, Ain Shams University, Abbassia, Cairo, 11566 Egypt
Search for more papers by this authorJaroslav Kousal
Faculty of Mathematics and Physics, Charles University Prague, V Holesovickach 2, Prague 8, 18000 Czech Republic
Search for more papers by this authorAbstract
Poly(lactic acid) (PLA) has shown much success in the preparation of tissue engineering scaffolds as it can be fabricated with a tailored architecture. However, the PLA surface has drawbacks including the lack of biofunctional motifs which are essential for high affinity to biological cells. Therefore, this study describes a multistep physicochemical approach for the immobilization of d-glucosamine (GlcN), a naturally occurring monosaccharide having many biological functions, on the PLA surface aiming at enhancing the cell proliferation activity. In this approach, poly(acrylic acid) (PAAc) spacer arms are first introduced into the PLA surface via plasma post-irradiation grafting technique. Then, covalent coupling or physical adsorption of GlcN with/on the PAAc spacer is carried out. Factors affecting the grafting yield are controlled to produce a suitable spacer for bioimmobilization. X-ray photon spectroscopic (XPS) analyses confirm the immobilization of GlcN on the PLA surface. The XPS results reveal also that increasing the yield of grafted PAAc spacer on the PLA surface increases the amount of covalently immobilized GlcN, but actually inhibits the immobilization process using the physical adsorption method. Contact angle measurements and atomic force microscopy (AFM) show a substantial increase of surface energy and roughness of PLA surface, respectively, upon the multistep modification procedure. The cytocompatibility of the modified surfaces is assessed using a mouse embryonic fibroblast (MEF) cell line. Observation from the cell culture basically demonstrates the potential of GlcN immobilization in improving the cytocompatibility of the PLA surface. Moreover, the covalent immobilization of GlcN seems to produce more cytocompatible surfaces if compared with the physical adsorption method. © 2017 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 105A: 3176–3188, 2017.
REFERENCES
- 1 Berthiaume F, Maguire TJ, Yarmush ML. Tissue engineering and regenerative medicine: History, progress, and challenges. Annu Rev Chem Biomol Eng 2011; 2: 403–430.
- 2 Khan F, Tanaka M, Ahmad SR. Fabrication of polymeric biomaterials: A strategy for tissue engineering and medical devices. J Mater Chem B 2015; 3: 8224–8249.
- 3 Place ES, George JH, Williams CK, Stevens MM. Synthetic polymer scaffolds for tissue engineering. Chem Soc Rev 2009; 38: 1139–1151.
- 4 Shoichet MS. Polymer scaffolds for biomaterials applications. Macromolecule 2010; 43: 581–591.
- 5 Lopes MS, Jardini AL, Filho RM. Poly (lactic acid) production for tissue engineering applications. Proc Eng 2012; 42: 1402–1413.
- 6 Chu CR, Coutts RD, Yoshioka M, Harwood FL, Monosov AZ, Amiel D. Articular cartilage repair using allogeneic perichondrocyte seeded biodegradable porous polylactic acid (PLA): A tissue-engineering study. J Biomed Mater Res 1995; 29: 1147–1154.
- 7 Liao SS, Cui FZ, Zhang W, Feng QL. Hierarchically biomimetic bone scaffold materials: Nano-HA/collagen/PLA composite. J Biomed Mater Res 2004; 69: 158–165.
- 8 Yamada K, Miyamoto S, Nagata I, Kikuchi H, Ikada Y, Iwata H, Yamamoto K. Development of a dural substitute from synthetic bioabsorbable polymers. J Neurosurg 1997; 86: 1012–1017.
- 9 Ito Y. Covalently immobilized biosignal molecule materials for tissue engineering. Soft Matter 2008; 4: 46–56.
- 10 Ma Z, Mao Z, Gao C. Surface modification and property analysis of biomedical polymers used for tissue engineering. Colloid Surface B 2007; 60: 137–157.
- 11 Elbert DL, Hubbell JA. Surface treatments of polymers for biocompatibility. Annu Rev Mater Sci 1996; 26: 365–394.
- 12 Alferiev IS, Connolly JM, Stachelek SJ, Ottey A, Rauova L, Levy RJ. Surface heparinization of polyurethane via bromoalkylation of hard segment nitrogens. Biomacromolecules 2006; 7: 317–322.
- 13 Goddard JM, Hotchkiss JH. Polymer surface modification for the attachment of bioactive compounds. Prog Polym Sci 2007; 32: 698–725.
- 14 Kulik EA, Kato K, Ivanchenko MI, Ikada Y. Trypsin immobilization on to polymer surface through grafted layer and its reaction with inhibitors. Biomaterials 1993; 14: 763–769.
- 15 Karbassi E, Asadinezhad A, Lehocky M, Humpolicek P, Vesel A, Novak I, Saha P. Antibacterial performance of alginic acid coating on polyethylene film. Int J Mol Sci 2014; 15: 14684–14696.
- 16 Desmet T, Morent R, Geyter ND, Leys C, Schacht E, Dubruel P. Nonthermal plasma technology as a versatile strategy for polymeric biomaterials surface modification: A review. Biomacromolecules 2009; 10: 2351–2378.
- 17 Mozetič M, Primc G, Vesel A, Zaplotnik R, Modic M, Junkar I, Recek N, Klanjšek-Gunde M, Guhy L, Sunkara MK, Assensio MC, Milošević S, Lehocky M, Sedlarik V, Gorjanc M, Kutasi K, Stana-Kleinschek K. Application of extremely non-equilibrium plasmas in the processing of nano and biomedical materials. Plasma Sources Sci Technol 2015; 24: 15–26.
- 18 Gupta B, Krishnanand K, Deopura BL. Oxygen plasma-induced graft polymerization of acrylic acid on polycaprolactone monofilament. Eur Polym J 2012; 48: 1940–1948.
- 19 Gupta B, Hilborn JG, Bisson I, Frey P. Plasma-induced graft polymerization of acrylic acid onto poly(ethylene terephthalate) films. J Appl Polym Sci 2001; 81: 2993–3001.
- 20 Cummings RD. The repertoire of glycan determinants in the human glycome. Mol BioSyst 2009; 5: 1087–1104.
- 21 Kooyk YV, Rabinovich GA. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol 2008; 9: 593–601.
- 22 Du J, Yarema KJ. Carbohydrate engineered cells for regenerative medicine. Adv Drug Deliv Rev 2010; 62: 671–682.
- 23 Derfoul A, Miyoshi AD, Freeman DE, Tuan RS. Glucosamine promotes chondrogenic phenotype in both chondrocytes and mesenchymal stem cells and inhibits MMP-13 expression and matrix degradation. Osteoarthr Cartil 2007; 15: 646–655.
- 24 Matheson AJ, Perry CM. Glucosamine—A review of its use in the management of osteoarthritis. Drugs Aging 2003; 20: 1041–1060.
- 25 Varghese S, Theprungsirikul P, Sahani S, Hwang N, Yarema KJ, Elisseeff JH. Glucosamine modulates chondrocyte proliferation, matrix synthesis, and gene expression. Osteoarthr Cartil 2007; 15: 59–68.
- 26 Schnaar RL, Freeze HH. A “glyconutrient sham”. Glycobiology 2008; 18: 652–657.
- 27 Dodge GR, Jimenez SA. Glucosamine sulfate modulates the levels of aggrecan and matrix metalloproteinase-3 synthesized by cultured human osteoarthritis articular chondrocytes. Osteoarthr Cartil 2003; 11: 424–432.
- 28 Chan PS, Caron JP, Rosa GJM, Orth MW. Glucosamine and chondroitin sulfate regulate gene expression and synthesis of nitric oxide and prostaglandin E-2 in articular cartilage explants. Osteoarthr Cartil 2005; 13: 387–394.
- 29 Hwang NS, Varghese S, Theprungsirikul P, Canver A, Elisseeff J. Enhanced chondrogenic differentiation of murine embryonic stem cells in hydrogels with glucosamine. Biomaterials 2006; 27: 6015–6023.
- 30 McCarty MF. Glucosamine for wound healing. Med Hypotheses 1996; 47: 273–275.
- 31 Russo L, Gloria A, Russo T, D'Amora U, Taraballi F, De Santis R, Ambrosio L, Nicotra F, Cipolla L. Glucosamine grafting on poly(ɛ-caprolactone): A novel glycated polyester as a substrate for tissue engineering. RSC Adv 2013; 3: 6286–6289.
- 32 Suo H, Xu K, Zheng X. Using glucosamine to improve the properties of photocrosslinked gelatin scaffolds. J Biomater Appl 2015; 29: 977–987.
- 33 Swilem AE, Lehocký M, Humpolíček P, Kucekova Z, Junkar I, Mozetič M, Hamed AA, Novák I. Developing a biomaterial interface based on poly(lactic acid) via plasma-assisted covalent anchorage of d-glucosamine and its potential for tissue regeneration. Colloid Surface B 2016; 148: 59–65.
- 34
Good RJ, Van Oss CJ. The modern theory of contact angles and the hydrogen bond components of surface energies. In: ME Schrader, GI Loeb, editors. Modern Approaches to Wettability: Theory and Applications. New York: Plenum Press; 1992. p 127.
10.1007/978-1-4899-1176-6_1 Google Scholar
- 35 Hobbs C, Hong S, Taylor J. Effect of surface roughness on fouling of RO and NF membranes during filtration of a high organic surficial groundwater. J Water Supply Res T 2006; 55: 7–8.
- 36 Gupta B, Krishnanand K, Deopura BL, Atthoff B. Surface modification of polycaprolactone monofilament by low pressure oxygen plasma. J Appl Polym Sci 2013; 127: 1744–1750.
- 37
Kill G,
Hunter DH,
McIntyre NS. Reactions of polyethylene surfaces with the downstream products of an air plasma: Gas phase and surface spectroscopic studies. J Polym Sci Pol Chem 1996; 34: 2299–2310.
10.1002/(SICI)1099-0518(19960915)34:12<2299::AID-POLA3>3.0.CO;2-S CAS Web of Science® Google Scholar
- 38 Cheng Z, Teoh SH. Surface modification of ultra thin poly (ɛ-caprolactone) films using acrylic acid and collagen. Biomaterials 2004; 25: 1991–2001.
- 39 Hergelová B, Zahoranová A, Kováčik D, Stupavská M, Černák M. Polylactic acid surface activation by atmospheric pressure dielectric barrier discharge plasma. Open Chem 2015; 13: 564–569.
- 40 Xia Y, Boey F, Venkatraman SS. Surface modification of poly(l-lactic acid) with biomolecules to promote endothelialization. Biointerphases 2010; 5: 32–40.
- 41 Más BA, Cattani SMM, Rangel RCC, Ribeiro GA, Cruz NC, Leite FL, Nascente PAP, Duek EAR. Surface characterization and osteoblast-like cells culture on collagen modified PLDLA scaffolds. Mater Res 2014; 17: 1523–3154.
- 42 Renò F, D'Angelo D, Gottardi G, Rizzi M, Aragno D, Piacenza G, Cartasegna F, Biasizzo M, Trotta F, Cannas M. Atmospheric pressure plasma surface modification of poly(d,l-lactic acid) increases fibroblast, osteoblast and keratinocyte adhesion and proliferation. Plasma Process Polym 2012; 9: 491–502.
- 43 Grøndahl L, Chandler-Temple A, Trau M. Polymeric grafting of acrylic acid onto poly(3-hydroxybutyrate-co-3-hydroxyvalerate): Surface functionalization for tissue engineering applications. Biomacromolecules 2005; 6: 2197–2203.
- 44 Meiron TS, Marmur A, Saguy IS. Contact angle measurement on rough surfaces. J Colloid Interface Sci 2004; 274: 637–644.
- 45 Gentleman MM, Gentleman E. The role of surface free energy in osteoblast–biomaterial interactions. Int Mater Rev 2014; 59: 417–429.
- 46 Hill MJ, Cheah C, Sarkar D. Interfacial energetics approach for analysis of endothelial cell and segmental polyurethane interactions. Colloid Surface B 2016; 144: 46–56.
- 47 Nori A, Yim EKF, Hen S, Leong KW. Cell substrate interactions. In: A Atala, R Lanza, JA Thomson, RM Nerem, editors. Principles of Regenerative Medicine. New York: Academic Press; 2010. p 669670.
- 48 Anselme K, Ploux L, Ponche A. Cell/material interfaces: Influence of surface chemistry and surface topography on cell adhesion. J Adhes Sci Technol 2010; 24: 831–852.
- 49 Gupta B, Plummer C, Bisson I, Frey P, Hilborn J. Plasma-induced graft polymerization of acrylic acid onto poly(ethylene terephthalate) films: characterization and human smooth muscle cell growth on grafted films. Biomaterials 2002; 23: 863–871.