Antibacterial and conductive injectable hydrogels based on quaternized chitosan-graft-polyaniline/oxidized dextran for tissue engineering

Acta Biomaterialia

Volumn 26, Issue , 2015, Pages 236-248

  Zhao, Xin ^a   Li, Peng ^a   Guo, Baolin ^a   Ma, Peter X ^a,b  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Antibacterial; Conductive polymers; Injectable hydrogels; Polyaniline; Quaternized chitosan

Indexed keywords

BIODEGRADATION; CELL CULTURE; CHITOSAN; DEXTRAN; ESCHERICHIA COLI; GELATION; POLYANILINE; SCAFFOLDS (BIOLOGY); STEM CELLS; TISSUE REGENERATION;

ANTI-BACTERIAL ACTIVITY; ANTIBACTERIALS; CHITOSAN HYDROGEL; CONDUCTIVE POLYMER; DEGRADABLE HYDROGEL; IN-SITU FORMING; INJECTABILITY; INJECTABLE HYDROGELS; OXIDIZED DEXTRANS; QUATERNIZED CHITOSANS;

HYDROGELS;

CHITOSAN; COPOLYMER; DEXTRAN; OXIDIZED DEXTRAN; POLYANILINE; UNCLASSIFIED DRUG; ANILINE DERIVATIVE; ANTIINFECTIVE AGENT; HYDROGEL;

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; BIODEGRADATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CHEMICAL STRUCTURE; COMPARATIVE STUDY; CONDUCTANCE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; CYTOTOXICITY; ELECTROCHEMICAL ANALYSIS; ESCHERICHIA COLI; FEMALE; GELATION; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; INJECTABLE HYDROGEL; MESENCHYMAL STEM CELL; MINIMUM INHIBITORY CONCENTRATION; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; SPRAGUE DAWLEY RAT; STAPHYLOCOCCUS AUREUS; SYNTHESIS; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE SCAFFOLD; ULTRAVIOLET SPECTROPHOTOMETRY; ADMINISTRATION AND DOSAGE; ANIMAL; CELL SURVIVAL; CHEMISTRY; DEVICE FAILURE ANALYSIS; DEVICES; DRUG EFFECTS; ELECTRIC CONDUCTIVITY; EQUIPMENT DESIGN; INJECTION; MATERIALS TESTING; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANILINE COMPOUNDS; ANIMALS; ANTI-BACTERIAL AGENTS; CELL SURVIVAL; CHITOSAN; DEXTRANS; ELECTRIC CONDUCTIVITY; EQUIPMENT DESIGN; EQUIPMENT FAILURE ANALYSIS; ESCHERICHIA COLI; HYDROGELS; INJECTIONS; MATERIALS TESTING; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84942292668     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2015.08.006     Document Type: Article

References (79)

1. F. Guilak, D.L. Butler, S.A. Goldstein, and F. Baaijens Biomechanics and mechanobiology in functional tissue engineering J. Biomech. 47 2014 1933 1940
2. R. Langer, and J.P. Vacanti Tissue engineering Science 260 1993 920 926
3. B.L. Guo, and P.X. Ma Synthetic biodegradable functional polymers for tissue engineering: a brief review Sci. China Chem. 57 2014 490 500
4. J. Leor, S. Aboulafia-Etzion, A. Dar, L. Shapiro, I.M. Barbash, A. Battler, and et al. Bioengineered cardiac grafts a new approach to repair the infarcted myocardium? Circulation 102 2000 Iii-56 Iii-61
5. P.J. Horner, and F.H. Gage Regenerating the damaged central nervous system Nature 407 2000 963 970
6. M.W. Tibbitt, and K.S. Anseth Hydrogels as extracellular matrix mimics for 3D cell culture Biotechnol. Bioeng. 103 2009 655 663
7. S.J. Hollister Porous scaffold design for tissue engineering Nat. Mater. 4 2005 518 524
8. D.W. Hutmacher Scaffolds in tissue engineering bone and cartilage Biomaterials 21 2000 2529 2543
9. K.Y. Lee, and D.J. Mooney Hydrogels for tissue engineering Chem. Rev. 101 2001 1869 1880
10. H. Yoshimoto, Y. Shin, H. Terai, and J. Vacanti A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering Biomaterials 24 2003 2077 2082
11. M.N. Rahaman, D.E. Day, B. Sonny Bal, Q. Fu, S.B. Jung, L.F. Bonewald, and et al. Bioactive glass in tissue engineering Acta Biomater. 7 2011 2355 2373
12. T.W. Gilbert, T.L. Sellaro, and S.F. Badylak Decellularization of tissues and organs Biomaterials 27 2006 3675 3683
13. B.L. Guo, Y. Sun, A. Finne-Wistrand, K. Mustafa, and A.C. Albertsson Electroactive porous tubular scaffolds with degradability and non-cytotoxicity for neural tissue regeneration Acta Biomater. 8 2012 144 153
14. L.C. Li, J. Ge, L. Wang, B.L. Guo, and P.X. Ma Electroactive nanofibrous biomimetic scaffolds by thermally induced phase separation J. Mater. Chem. B 2 2014 6119 6130
15. X.J. Ma, J. Ge, Y. Li, B.L. Guo, and P.X. Ma Nanofibrous electroactive scaffolds from a chitosan-grafted-aniline tetramer by electrospinning for tissue engineering RSC Adv. 4 2014 13652 13661
16. Z. Ma, C. Gao, Y. Gong, and J. Shen Cartilage tissue engineering PLLA scaffold with surface immobilized collagen and basic fibroblast growth factor Biomaterials 26 2005 1253 1259
17. Y. Ling, J. Rubin, Y. Deng, C. Huang, U. Demirci, J.M. Karp, and et al. A cell-laden microfluidic hydrogel Lab Chip 7 2007 756 762
18. J.L. Drury, and D.J. Mooney Hydrogels for tissue engineering: scaffold design variables and applications Biomaterials 24 2003 4337 4351
19. B.V. Slaughter, S.S. Khurshid, O.Z. Fisher, A. Khademhosseini, and N.A. Peppas Hydrogels in regenerative medicine Adv. Mater. 21 2009 3307 3329
20. L. Zhang, L. Wang, B.L. Guo, and P.X. Ma Cytocompatible injectable carboxymethyl chitosan/N-isopropylacrylamide hydrogels for localized drug delivery Carbohydr. Polym. 103 2014 110 118
21. L. Yu, and J. Ding Injectable hydrogels as unique biomedical materials Chem. Soc. Rev. 37 2008 1473 1481
22. E. Ruel-Gariépy, and J.-C. Leroux In situ-forming hydrogels - review of temperature-sensitive systems Eur. J. Pharm. Biopharm. 58 2004 409 426
23. Y.B. Wu, L. Wang, B.L. Guo, and P.X. Ma Injectable biodegradable hydrogels and microgels based on methacrylated poly(ethylene glycol)-co-poly(glycerol sebacate) multi-block copolymers: synthesis, characterization, and cell encapsulation J. Mater. Chem. B 2 2014 3674 3685
24. J. Zhao, B.L. Guo, and P.X. Ma Injectable alginate microsphere/PLGA-PEG-PLGA composite hydrogels for sustained drug release RSC Adv. 4 2014 17736 17742
25. Y.B. Wu, B.L. Guo, and P.X. Ma Injectable electroactive hydrogels formed via host guest interactions ACS Macro Lett. 3 2014 1145 1150
26. J.A. Fishman, and R.H. Rubin Infection in organ-transplant recipients N. Engl. J. Med. 338 1998 1741 1751
27. R.O. Darouiche Treatment of infections associated with surgical implants N. Engl. J. Med. 350 2004 1422 1429
28. J.R. Fuchs, B.A. Nasseri, and J.P. Vacanti Tissue engineering: a 21st century solution to surgical reconstruction Ann. Thorac. Surg. 72 2001 577 591
29. K. Kim, Y.K. Luu, C. Chang, D. Fang, B.S. Hsiao, B. Chu, and et al. Incorporation and controlled release of a hydrophilic antibiotic using poly (lactide-co-glycolide)-based electrospun nanofibrous scaffolds J. Control. Release 98 2004 47 56
30. Z.-C. Xing, W.-P. Chae, J.-Y. Baek, M.-J. Choi, Y. Jung, and I.-K. Kang In vitro assessment of antibacterial activity and cytocompatibility of silver-containing PHBV nanofibrous scaffolds for tissue engineering Biomacromolecules 11 2010 1248 1253
31. M.A. Fischbach, and C.T. Walsh Antibiotics for emerging pathogens Science 325 2009 1089 1093
32. Z.-X. Peng, B. Tu, Y. Shen, L. Du, L. Wang, S.-R. Guo, and et al. Quaternized chitosan inhibits icaA transcription and biofilm formation by Staphylococcus on a titanium surface Antimicrob. Agents Chemother. 55 2011 860 866
33. H. Tan, Z. Peng, Q. Li, X. Xu, S. Guo, and T. Tang The use of quaternised chitosan-loaded PMMA to inhibit biofilm formation and downregulate the virulence-associated gene expression of antibiotic-resistant staphylococcus Biomaterials 33 2012 365 377
34. C. Qin, Q. Xiao, H. Li, M. Fang, Y. Liu, X. Chen, and et al. Calorimetric studies of the action of chitosan-N-2-hydroxypropyl trimethyl ammonium chloride on the growth of microorganisms Int. J. Biol. Macromol. 34 2004 121 126
35. Z.-X. Peng, L. Wang, L. Du, S.-R. Guo, X.-Q. Wang, and T.-T. Tang Adjustment of the antibacterial activity and biocompatibility of hydroxypropyltrimethyl ammonium chloride chitosan by varying the degree of substitution of quaternary ammonium Carbohydr. Polym. 81 2010 275 283
36. P. Zhou, Y. Xia, X. Cheng, P. Wang, Y. Xie, and S. Xu Enhanced bone tissue regeneration by antibacterial and osteoinductive silica-HACC-zein composite scaffolds loaded with rhBMP-2 Biomaterials 35 2014 10033 10045
37. P. Zhou, Y. Xia, J. Wang, C. Liang, L. Yu, W. Tang, and et al. Antibacterial properties and bioactivity of HACC-and HACC-Zein-modified mesoporous bioactive glass scaffolds J. Mater. Chem. B 1 2013 685 692
38. I. Jun, S. Jeong, and H. Shin The stimulation of myoblast differentiation by electrically conductive sub-micron fibers Biomaterials 30 2009 2038 2047
39. H. Cui, J. Shao, Y. Wang, P. Zhang, X. Chen, and Y. Wei PLA-PEG-PLA and its electroactive tetraaniline copolymer as multi-interactive injectable hydrogels for tissue engineering Biomacromolecules 14 2013 1904 1912
40. N.C. Spitzer Electrical activity in early neuronal development Nature 444 2006 707 712
41. S.H. Ku, S.H. Lee, and C.B. Park Synergic effects of nanofiber alignment and electroactivity on myoblast differentiation Biomaterials 33 2012 6098 6104
42. B.L. Guo, L. Glavas, and A.C. Albertsson Biodegradable and electrically conducting polymers for biomedical applications Prog. Polym. Sci. 38 2013 1263 1286
43. B.L. Guo, A. Finne-Wistrand, and A.C. Albertsson Electroactive hydrophilic polylactide surface by covalent modification with tetraaniline Macromolecules 45 2012 652 659
44. B.L. Guo, A. Finne-Wistrand, and A.C. Albertsson Simple route to size-tunable degradable and electroactive nanoparticles from the self-assembly of conducting coil-rod-coil triblock copolymers Chem. Mater. 23 2011 4045 4055
45. Y.A. Ismail, S.R. Shin, K.M. Shin, S.G. Yoon, K. Shon, S.I. Kim, and et al. Electrochemical actuation in chitosan/polyaniline microfibers for artificial muscles fabricated using an in situ polymerization Sens. Actuators B 129 2008 834 840
46. G.-L. Yuan, N. Kuramoto, and S.-J. Su Template synthesis of polyaniline in the presence of phosphomannan Synth. Met. 129 2002 173 178
47. L.C. Li, J. Ge, B.L. Guo, and P.X. Ma In situ forming biodegradable electroactive hydrogels Polym. Chem. 5 2014 2880 2890
48. N. Shi, X. Guo, H. Jing, J. Gong, C. Sun, and K. Yang Antibacterial effect of the conducting polyaniline J. Mater. Sci. Technol. 22 2006 289 290
49. Z. Kucekova, V. Kasparkova, P. Humpolicek, P. Sevcikova, and J. Stejskal Antibacterial properties of polyaniline-silver films Chem. Pap. 67 2013 1103 1108
50. Q. Jia, S. Shan, L. Jiang, Y. Wang, and D. Li Synergistic antimicrobial effects of polyaniline combined with silver nanoparticles J. Appl. Polym. Sci. 125 2012 3560 3566
51. J. Cho, J. Grant, M. Piquette-Miller, and C. Allen Synthesis and physicochemical and dynamic mechanical properties of a water-soluble chitosan derivative as a biomaterial Biomacromolecules 7 2006 2845 2855
52. H. Zhang, A. Qadeer, D. Mynarcik, and W. Chen Delivery of rosiglitazone from an injectable triple interpenetrating network hydrogel composed of naturally derived materials Biomaterials 32 2011 890 898
53. X. Zhang, Y. Yang, J. Yao, Z. Shao, and X. Chen Strong collagen hydrogels by oxidized dextran modification ACS Sustain. Chem. Eng. 2 2014 1318 1324
54. S.P. Massia, J. Stark, and D.S. Letbetter Surface-immobilized dextran limits cell adhesion and spreading Biomaterials 21 2000 2253 2261
55. R. Jin, C. Hiemstra, Z. Zhong, and J. Feijen Enzyme-mediated fast in situ formation of hydrogels from dextran-tyramine conjugates Biomaterials 28 2007 2791 2800
56. P. Li, Y.F. Poon, W. Li, H.-Y. Zhu, S.H. Yeap, Y. Cao, and et al. A polycationic antimicrobial and biocompatible hydrogel with microbe membrane suctioning ability Nat. Mater. 10 2011 149 156
57. J. Zhao, X. Zhao, B.L. Guo, and P.X. Ma Multifunctional interpenetrating polymer network hydrogels based on methacrylated alginate for the delivery of small molecule drugs and sustained release of protein Biomacromolecules 15 2014 3246 3252
58. B. Balakrishnan, and A. Jayakrishnan Self-cross-linking biopolymers as injectable in situ forming biodegradable scaffolds Biomaterials 26 2005 3941 3951
59. H. Tan, C.R. Chu, K.A. Payne, and K.G. Marra Injectable in situ forming biodegradable chitosan-hyaluronic acid based hydrogels for cartilage tissue engineering Biomaterials 30 2009 2499 2506
60. 1H NMR determination of the doping level of doped polyaniline Macromol. Chem. Phys. 211 2010 1814 1819
61. C. Luo, H. Peng, L. Zhang, G.-L. Lu, Y. Wang, and J. Travas-Sejdic Formation of nano-/microstructures of polyaniline and its derivatives Macromolecules 44 2011 6899 6907
62. B.L. Guo, A. Finne-Wistrand, and A.C. Albertsson Facile synthesis of degradable and electrically conductive polysaccharide hydrogels Biomacromolecules 12 2011 2601 2609
63. B.L. Guo, J.F. Yuan, and Q.Y. Gao pH and ionic sensitive chitosan/carboxymethyl chitosan IPN complex films for the controlled release of coenzyme A Colloid Polym. Sci. 286 2008 175 181
64. D. Li, J. Huang, and R.B. Kaner Polyaniline nanofibers: a unique polymer nanostructure for versatile applications Acc. Chem. Res. 42 2008 135 145
65. M. Li, Y. Guo, Y. Wei, A.G. MacDiarmid, and P.I. Lelkes Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications Biomaterials 27 2006 2705 2715
66. T.H. Qazi, D. Dippold, J.E. Roether, E. Rosellini, N. Barbani, A.R. Boccaccini, and et al. Development and characterization of novel electrically conductive PANI-PGS composites for cardiac tissue engineering applications Acta Biomater. 10 2014 2434 2445
67. D.A. Stout Poly(lactic-co-glycolic acid): carbon nanofiber composites for myocardial tissue engineering applications Acta Biomater. 7 2011 3101 3112
68. S. Yang, K.-F. Leong, Z. Du, and C.-K. Chua The design of scaffolds for use in tissue engineering. Part I. Traditional factors Tissue Eng. 7 2001 679 689
69. L. Weng, A. Romanov, J. Rooney, and W. Chen Non-cytotoxic, in situ gelable hydrogels composed of N-carboxyethyl chitosan and oxidized dextran Biomaterials 29 2008 3905 3913
70. H. Zhang, A. Qadeer, and W. Chen In situ gelable interpenetrating double network hydrogel formulated from binary components: thiolated chitosan and oxidized dextran Biomacromolecules 12 2011 1428 1437
71. Y. Talukdar, J.T. Rashkow, G. Lalwani, S. Kanakia, and B. Sitharaman The effects of graphene nanostructures on mesenchymal stem cells Biomaterials 35 2014 4863 4877
72. H. Park, R. Bhalla, R. Saigal, M. Radisic, N. Watson, R. Langer, and et al. Effects of electrical stimulation in C2C12 muscle constructs J. Tissue Eng. Regen. Med. 2 2008 279 287
73. M.H. Xie, L. Wang, J. Ge, B.L. Guo, and P.X. Ma Strong electroactive biodegradable shape memory polymer networks based on star-shaped polylactide and aniline trimer for bone tissue engineering ACS Appl. Mater. Interfaces 7 2015 6772 6781
74. D. Cui, A. Szarpak, I. Pignot-Paintrand, A. Varrot, T. Boudou, C. Detrembleur, and et al. Contact-killing polyelectrolyte microcapsules based on chitosan derivatives Adv. Funct. Mater. 20 2010 3303 3312
75. P. Karunanithy, R.G.S.V. Prasad, V.S. Jakka, R.S.L. Aparna, A.R. Phani, G.S. Prabhakara, and et al. Enhanced antimicrobial activity of polyaniline grafted chitosan Adv. Sci. 5 2013 12 15 420-6(7)
76. M. Cabuk, M. Yavuz, H.I. Unal, and Y. Alan Synthesis, characterization, and enhanced antibacterial activity of chitosan-based biodegradable conducting graft copolymers Polym. Compos. 36 2014 497 509
77. X. Fei Liu, Y. Lin Guan, D. Zhi Yang, Z. Li, and K. De Yao Antibacterial action of chitosan and carboxymethylated chitosan J. Appl. Polym. Sci. 79 2001 1324 1335
78. M.C. Giano, Z. Ibrahim, S.H. Medina, K.A. Sarhane, J.M. Christensen, Y. Yamada, and et al. Injectable bioadhesive hydrogels with innate antibacterial properties Nat. Commun. 5 2014
79. N. Kojic, E.M. Pritchard, H. Tao, M.A. Brenckle, J.P. Mondia, B. Panilaitis, and et al. Focal infection treatment using laser-mediated heating of injectable silk hydrogels with gold nanoparticles Adv. Funct. Mater. 22 2012 3793 3798