Chemical functionalization of graphene to augment stem cell osteogenesis and inhibit biofilm formation on polymer composites for orthopedic applications

ACS Applied Materials and Interfaces

Volumn 7, Issue 5, 2015, Pages 3237-3252

  Kumar, Sachin ^a   Raj, Shammy ^a   Kolanthai, Elayaraja ^a   Sood, A K ^a   Sampath, S ^a   Chatterjee, Kaushik ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

antimicrobial properties; graphene; orthopedics; polymer composites; stem cell

Indexed keywords

BIOFILMS; BIOMECHANICS; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; COMPOSITE MATERIALS; FUNCTIONAL POLYMERS; GRAPHENE; MEDICAL APPLICATIONS; ORTHOPEDICS;

ANTI-MICROBIAL PROPERTIES; BIOMEDICAL APPLICATIONS; CHEMICAL FUNCTIONALIZATION; HUMAN MESENCHYMAL STEM CELLS; ORTHOPEDIC APPLICATIONS; POLY (EPSILONCAPROLACTONE); POLYMER COMPOSITE; REINFORCED COMPOSITES;

STEM CELLS;

ANTIINFECTIVE AGENT; GRAPHITE; POLYCAPROLACTONE; POLYESTER;

BIOFILM; BONE DEVELOPMENT; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ESCHERICHIA COLI; GROWTH, DEVELOPMENT AND AGING; HUMAN; MATERIALS TESTING; MESENCHYMAL STROMA CELL; OSTEOBLAST; PHYSIOLOGY; SURFACE PROPERTY;

ANTI-BACTERIAL AGENTS; BIOFILMS; CELL DIFFERENTIATION; CELLS, CULTURED; ESCHERICHIA COLI; GRAPHITE; HUMANS; MATERIALS TESTING; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; OSTEOGENESIS; POLYESTERS; SURFACE PROPERTIES;

EID: 84922796045     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am5079732     Document Type: Article

References (69)

1. Rafiee, M. A.; Rafiee, J.; Wang, Z.; Song, H.; Yu, Z.-Z.; Koratkar, N. Enhanced mechanical properties of nanocomposites at low graphene content ACS Nano 2009, 3, 3884-3890
2. Shahil, K. M.; Balandin, A. A. Graphene-multilayer graphene nanocomposites as highly efficient thermal interface materials Nano Lett. 2012, 12, 861-867
3. Zhang, H.-B.; Zheng, W.-G.; Yan, Q.; Yang, Y.; Wang, J.-W.; Lu, Z.-H.; Ji, G.-Y.; Yu, Z.-Z. Electrically conductive polyethylene terephthalate/graphene nanocomposites prepared by melt compounding Polymer 2010, 51, 1191-1196
4. Kumar, S.; Mishra, A.; Chatterjee, K. Effect of organically modified clay on mechanical properties, cytotoxicity and bactericidal properties of poly (-caprolactone) nanocomposites Mater. Res. Express 2014, 1, 045302
5. Ramanathan, T.; Abdala, A.; Stankovich, S.; Dikin, D.; Herrera-Alonso, M.; Piner, R.; Adamson, D.; Schniepp, H.; Chen, X.; Ruoff, R. Functionalized graphene sheets for polymer nanocomposites Nat. Nanotechnol. 2008, 3, 327-331
6. Ahamed, M.; Karns, M.; Goodson, M.; Rowe, J.; Hussain, S. M.; Schlager, J. J.; Hong, Y. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells Toxicol. Appl. Pharmacol. 2008, 233, 404-410
7. Bharali, D. J.; Klejbor, I.; Stachowiak, E. K.; Dutta, P.; Roy, I.; Kaur, N.; Bergey, E. J.; Prasad, P. N.; Stachowiak, M. K. Organically modified silica nanoparticles: A nonviral vector for in vivo gene delivery and expression in the brain Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 11539-11544
8. Zardini, H. Z.; Amiri, A.; Shanbedi, M.; Maghrebi, M.; Baniadam, M. Enhanced antibacterial activity of amino acids-functionalized multi walled carbon nanotubes by a simple method Colloids Surf., B 2012, 92, 196-202
9. Molday, R. S.; Mackenzie, D. Immunospecific ferromagnetic iron-dextran reagents for the labeling and magnetic separation of cells J. Immunol. Methods. 1982, 52, 353-367
10. Sanpui, P.; Chattopadhyay, A.; Ghosh, S. S. Induction of apoptosis in cancer cells at low silver nanoparticle concentrations using chitosan nanocarrier ACS Appl. Mater. Interfaces. 2011, 3, 218-228
11. Lerf, A.; He, H.; Forster, M.; Klinowski, J. Structure of graphite oxide revisited J. Phys. Chem. B 1998, 102, 4477-4482
12. Park, S. Y.; Park, J.; Sim, S. H.; Sung, M. G.; Kim, K. S.; Hong, B. H.; Hong, S. Enhanced differentiation of human neural stem cells into neurons on graphene Adv. Mater. 2011, 23, H263-H267
13. Bao, H.; Pan, Y.; Ping, Y.; Sahoo, N. G.; Wu, T.; Li, L.; Li, J.; Gan, L. H. Chitosan-functionalized graphene oxide as a nanocarrier for drug and gene delivery Small. 2011, 7, 1569-1578
14. Shan, C.; Yang, H.; Han, D.; Zhang, Q.; Ivaska, A.; Niu, L. Water-soluble graphene covalently functionalized by biocompatible poly- l -lysine Langmuir. 2009, 25, 12030-12033
15. Lee, W. C.; Lim, C. H. Y.; Shi, H.; Tang, L. A.; Wang, Y.; Lim, C. T.; Loh, K. P. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide ACS Nano 2011, 5, 7334-7341
16. Hong, S. W.; Lee, J. H.; Kang, S. H.; Hwang, E. Y.; Hwang, Y.-S.; Lee, M. H.; Han, D.-W.; Park, J.-C. Enhanced neural cell adhesion and neurite outgrowth on graphene-based biomimetic substrates BioMed. Res. Int. 2014, 2014
17. Liu, S.; Zeng, T. H.; Hofmann, M.; Burcombe, E.; Wei, J.; Jiang, R.; Kong, J.; Chen, Y. Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: Membrane and oxidative stress ACS Nano 2011, 5, 6971-6980
18. Liu, Y.; Luo, Y.; Wu, J.; Wang, Y.; Yang, X.; Yang, R.; Wang, B.; Yang, J.; Zhang, N. Graphene oxide can induce in vitro and in vivo mutagenesis Sci. Rep. 2013, 3, 3469
19. Depan, D.; Girase, B.; Shah, J.; Misra, R. Structure-process-property relationship of the polar graphene oxide-mediated cellular response and stimulated growth of osteoblasts on hybrid chitosan network structure nanocomposite scaffolds Acta Biomater. 2011, 7, 3432-3445
20. Girase, B.; Shah, J. S.; Misra, R. D. K. Cellular mechanics of modulated osteoblasts functions in graphene oxide reinforced elastomers Adv. Eng. Mater. 2012, 14, B101-B111
21. Higuchi, A.; Ling, Q.-D.; Ko, Y.-A.; Chang, Y.; Umezawa, A. Biomaterials for the feeder-free culture of human embryonic stem cells and induced pluripotent stem cells Chem. Rev. 2011, 111, 3021-3035
22. McClary, K. B.; Ugarova, T.; Grainger, D. W. Modulating fibroblast adhesion, spreading, and proliferation using self-assembled monolayer films of alkylthiolates on gold J. Biomed. Mater. Res. 2000, 50, 428-439
23. Ostuni, E.; Chapman, R. G.; Liang, M. N.; Meluleni, G.; Pier, G.; Ingber, D. E.; Whitesides, G. M. Self-assembled monolayers that resist the adsorption of proteins and the adhesion of bacterial and mammalian cells Langmuir 2001, 17, 6336-6343
24. Miller, R.; Guo, Z.; Vogler, E. A.; Siedlecki, C. A. Plasma coagulation response to surfaces with nanoscale chemical heterogeneity Biomaterials 2006, 27, 208-215
25. Bain, J. R.; Hoffman, A. S. Tissue-culture surfaces with mixtures of aminated and fluorinated functional groups. Part 2. Growth and function of transgenic rat insulinoma cells (βg i/17) J. Biomater. Sci. Polym. Ed. 2003, 14, 341-367
26. Woodruff, M. A.; Hutmacher, D. W. The return of a forgotten polymer-Polycaprolactone in the 21st century Prog. Polym. Sci. 2010, 35, 1217-1256
27. Hummers, W. S., Jr; Offeman, R. E. Preparation of graphitic oxide J. Am. Chem. Soc. 1958, 80, 1339-1339
28. Ren, P.-G.; Yan, D.-X.; Ji, X.; Chen, T.; Li, Z.-M. Temperature dependence of graphene oxide reduced by hydrazine hydrate Nanotechnology. 2011, 22, 055705
29. Cao, Y.; Feng, J.; Wu, P. Polypropylene-grafted graphene oxide sheets as multifunctional compatibilizers for polyolefin-based polymer blends J. Mater. Chem. 2012, 22, 14997-15005
30. Kumar, S.; Bose, S.; Chatterjee, K. Amine-functionalized multiwall carbon nanotubes impart osteoinductive and bactericidal properties in poly (ε-caprolactone) composites RSC Adv. 2014, 4, 19086-19098
31. Perreault, F.; Tousley, M. E.; Elimelech, M. Thin-film composite polyamide membranes functionalized with biocidal graphene oxide nanosheets Environ. Sci. Technol. Lett. 2013, 1, 71-76
32. Zhang, Y.; Ali, S. F.; Dervishi, E.; Xu, Y.; Li, Z.; Casciano, D.; Biris, A. S. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived pc12 cells ACS Nano 2010, 4, 3181-3186
33. Hsiao, M.-C.; Liao, S.-H.; Yen, M.-Y.; Liu, P.-I.; Pu, N.-W.; Wang, C.-A.; Ma, C.-C. M. Preparation of covalently functionalized graphene using residual oxygen-containing functional groups ACS Appl. Mater. Interfaces. 2010, 2, 3092-3099
34. Guo, Y.; Sun, X.; Liu, Y.; Wang, W.; Qiu, H.; Gao, J. One pot preparation of reduced graphene oxide (RGO) or Au (Ag) nanoparticle-RGO hybrids using chitosan as a reducing and stabilizing agent and their use in methanol electrooxidation Carbon 2012, 50, 2513-2523
35. Yu, G.; Wu, P. Effect of chemically modified graphene oxide on the phase separation behaviour and properties of an epoxy/polyetherimide binary system Polym. Chem. 2013, 5, 96-104
36. Pan, S.; Aksay, I. A. Factors controlling the size of graphene oxide sheets produced via the graphite oxide route ACS Nano 2011, 5, 4073-4083
37. Zhu, Y.; Stoller, M. D.; Cai, W.; Velamakanni, A.; Piner, R. D.; Chen, D.; Ruoff, R. S. Exfoliation of graphite oxide in propylene carbonate and thermal reduction of the resulting graphene oxide platelets ACS Nano 2010, 4, 1227-1233
38. Kudin, K. N.; Ozbas, B.; Schniepp, H. C.; PrudHomme, R. K.; Aksay, I. A.; Car, R. Raman spectra of graphite oxide and functionalized graphene sheets Nano Lett. 2008, 8, 36-41
39. Ferrari, A.; Meyer, J.; Scardaci, V.; Casiraghi, C.; Lazzeri, M.; Mauri, F.; Piscanec, S.; Jiang, D.; Novoselov, K.; Roth, S. Raman spectrum of graphene and graphene layers Phys. Rev. Lett. 2006, 97, 187401
40. Stankovich, S.; Dikin, D. A.; Piner, R. D.; Kohlhaas, K. A.; Kleinhammes, A.; Jia, Y.; Wu, Y.; Nguyen, S. T.; Ruoff, R. S. Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide Carbon. 2007, 45, 1558-1565
41. Singh, S. K.; Singh, M. K.; Kulkarni, P. P.; Sonkar, V. K.; Grácio, J. J.; Dash, D. Amine-modified graphene: Thrombo-protective safer alternative to graphene oxide for biomedical applications ACS Nano 2012, 6, 2731-2740
42. Wu, T. M.; Chen, E. C. Crystallization behavior of poly (ε-caprolactone)/multiwalled carbon nanotube composites J. Polym. Sci., Part B: Polym. Phys. 2006, 44, 598-606
43. Wang, S.; Zhang, Y.; Abidi, N.; Cabrales, L. Wettability and surface free energy of graphene films Langmuir 2009, 25, 11078-11081
44. Gong, L.; Kinloch, I. A.; Young, R. J.; Riaz, I.; Jalil, R.; Novoselov, K. S. Interfacial stress transfer in a graphene monolayer nanocomposite Adv. Mater. 2010, 22, 2694-2697
45. Kim, H.; Abdala, A. A.; Macosko, C. W. Graphene/polymer nanocomposites Macromolecules. 2010, 43, 6515-6530
46. Webb, K.; Hlady, V.; Tresco, P. A. Relationships among cell attachment, spreading, cytoskeletal organization, and migration rate for anchorage-dependent cells on model surfaces J. Biomed. Mater. Res. 2000, 49, 362
47. Webb, K.; Hlady, V.; Tresco, P. A. Relative importance of surface wettability and charged functional groups on NIH 3T3 fibroblast attachment, spreading, and cytoskeletal organization J. Biomed. Mater. Res. 1998, 41, 422
48. Wilson, C. J.; Clegg, R. E.; Leavesley, D. I.; Pearcy, M. J. Mediation of biomaterial-cell interactions by adsorbed proteins: A review Tissue Eng. 2005, 11, 1-18
49. Ko, Y.-M.; Lee, K.; Kim, B.-H. Effect of functional groups on biodegradation and pre-osteoblastic cell response on the plasma-polymerized magnesium surface Jpn. J. Appl. Phys. 2013, 52, 01AE01
50. Folkman, J.; Moscona, A. Role of cell shape in growth control Nature 1978, 273, 345-349
51. Kumar, G.; Tison, C. K.; Chatterjee, K.; Pine, P. S.; McDaniel, J. H.; Salit, M. L.; Young, M. F.; Simon, C. G., Jr. The determination of stem cell fate by 3d scaffold structures through the control of cell shape Biomaterials. 2011, 32, 9188-9196
52. Schakenraad, J.; Busscher, H.; Wildevuur, C. R.; Arends, J. The influence of substratum surface free energy on growth and spreading of human fibroblasts in the presence and absence of serum proteins J. Biomed. Mater. Res. 1986, 20, 773-784
53. Keselowsky, B. G.; Collard, D. M.; García, A. J. Surface chemistry modulates fibronectin conformation and directs integrin binding and specificity to control cell adhesion J. Biomed. Mater. Res., Part A 2003, 66, 247-259
54. Keselowsky, B. G.; Collard, D. M.; García, A. J. Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 5953-5957
55. Nitya, G.; Nair, G. T.; Mony, U.; Chennazhi, K. P.; Nair, S. V. In vitro evaluation of electrospun pcl/nanoclay composite scaffold for bone tissue engineering J. Mater. Sci.: Mater. Med. 2012, 23, 1749-1761
56. Gaharwar, A. K.; Mihaila, S. M.; Swami, A.; Patel, A.; Sant, S.; Reis, R. L.; Marques, A. P.; Gomes, M. E.; Khademhosseini, A. Bioactive silicate nanoplatelets for osteogenic differentiation of human mesenchymal stem cells Adv. Mater. 2013, 25, 3329-3336
57. Li, J.; Chen, Y.; Yin, Y.; Yao, F.; Yao, K. Modulation of nano-hydroxyapatite size via formation on chitosan-gelatin network film in situ Biomaterials. 2007, 28, 781-790
58. Landis, W. J.; Jacquet, R. Association of calcium and phosphate ions with collagen in the mineralization of vertebrate tissues Calcif. Tissue Int. 2013, 93, 329-337
59. Qian, L.; Zhang, H. Green synthesis of chitosan-based nanofibers and their applications Green Chem. 2010, 12, 1207-1214
60. An, Y. H.; Friedman, R. J. Concise review of mechanisms of bacterial adhesion to biomaterial surfaces J. Biomed. Mater. Res. 1998, 43, 338-348
61. Sousa, C.; Teixeira, P.; Oliveira, R. Influence of surface properties on the adhesion of staphylococcus epidermidis to acrylic and silicone Int. J. Biomater. 2009, 2009, 718017
62. Darouiche, R.; Landon, G.; Patti, J.; Nguyen, L.; Fernau, R.; McDevitt, D.; Greene, C.; Foster, T.; Klima, M. Role of Staphylococcus aureus surface adhesins in orthopaedic device infections: Are results model-dependent? J. Med. Microbiol. 1997, 46, 75-79
63. Montanaro, L.; Campoccia, D.; Arciola, C. R. Advancements in molecular epidemiology of implant infections and future perspectives Biomaterials 2007, 28, 5155-5168
64. Cheng, G.; Zhang, Z.; Chen, S.; Bryers, J. D.; Jiang, S. Inhibition of bacterial adhesion and biofilm formation on zwitterionic surfaces Biomaterials. 2007, 28, 4192-4199
65. Tiller, J. C.; Liao, C.-J.; Lewis, K.; Klibanov, A. M. Designing surfaces that kill bacteria on contact Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 5981-5985
66. Tu, Y.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z.; Huang, Q.; Fan, C.; Fang, H. Destructive extraction of phospholipids from escherichia coli membranes by graphene nanosheets Nat. Nanotechnol. 2013, 8, 594-601
67. Zhou, H.; Liu, Y.; Chi, W.; Yu, C.; Yu, Y. Preparation and antibacterial properties of Ag@ polydopamine/graphene oxide sheet nanocomposite Appl. Surf. Sci. 2013, 282, 181-185
68. Isquith, A.; Abbott, E.; Walters, P. Surface-bonded antimicrobial activity of an organosilicon quaternary ammonium chloride Appl. Microbiol. 1972, 24, 859-863
69. Kuila, T.; Bose, S.; Mishra, A. K.; Khanra, P.; Kim, N. H.; Lee, J. H. Chemical functionalization of graphene and its applications Prog. Mater. Sci. 2012, 57, 1061-1105