Journal Home > Volume 12 , Issue 5

Graphene oxide (GO) possesses excellent mechanical strength, biocompatibility, colloidal stability, large surface area and high adsorption capability. It has driven to cancer nanotechnology to defeat cancer therapy obstacles, via integration into three-dimensional (3D) hydrogel network with biocompatible polymers as nanocomposites carrier, and controllable release of anticancer drugs. Specifically, the surface of GO affords π-π stacking and hydrophilic interactions with anticancer drugs. Additionally, modification of GO with various polymers such as natural and synthetic polymers enhances its biodegradability, drug loading, and target delivery. In this review, GO based hydrogels research accomplishments are reviewed on the aspects of crosslinking strategies, preparation methods, the model drug, polymer conjugation and modification with targeting ligands. Moreover, swelling kinetics, drug release profile and biological activity in vivo and in vitro are discussed. The biocompatibility of GO based hydrogels is also discussed from the perspective of its nano-bio interfaces. Apart from that, the clinical potential of GO based hydrogels and its major challenges are addressed in detail. Finally, this review concludes with a summary and invigorating future perspectives of GO based hydrogels for anticancer drug delivery. It is anticipated that this review can stimulate a new research gateway to facilitate the development of anticancer drug delivery by harnessing the unique properties of GO based hydrogels, such as large surface area, chemical purity, high loading capacity of drug, chemical stability, and the nature of lipophilic for cell membrane penetration.


menu
Abstract
Full text
Outline
About this article

Graphene oxide-based hydrogels as a nanocarrier for anticancer drug delivery

Show Author's information Abdullah A. Ghawanmeh1Gomaa A. M. Ali1,2H. Algarni3,4Shaheen M. Sarkar5Kwok Feng Chong1( )
Faculty of Industrial Sciences & Technology,Universiti Malaysia Pahang,Gambang,26300,Kuantan, Malaysia;
Chemistry Department,Faculty of Science, Al-Azhar University,Assiut,71524,Egypt;
Department of Physics, Faculty of Sciences,King Khalid University,Abha 61413, P. O. Box,9004,Saudi Arabia;
Research Center for Advanced Materials Science (RCAMS),King Khalid University,Abha 61413, P. O. Box,9004,Saudi Arabia;
Bernal Institute, Department of Chemical Sciences,University of Limerick,Castletroy V94, Limerick,Ireland;

Abstract

Graphene oxide (GO) possesses excellent mechanical strength, biocompatibility, colloidal stability, large surface area and high adsorption capability. It has driven to cancer nanotechnology to defeat cancer therapy obstacles, via integration into three-dimensional (3D) hydrogel network with biocompatible polymers as nanocomposites carrier, and controllable release of anticancer drugs. Specifically, the surface of GO affords π-π stacking and hydrophilic interactions with anticancer drugs. Additionally, modification of GO with various polymers such as natural and synthetic polymers enhances its biodegradability, drug loading, and target delivery. In this review, GO based hydrogels research accomplishments are reviewed on the aspects of crosslinking strategies, preparation methods, the model drug, polymer conjugation and modification with targeting ligands. Moreover, swelling kinetics, drug release profile and biological activity in vivo and in vitro are discussed. The biocompatibility of GO based hydrogels is also discussed from the perspective of its nano-bio interfaces. Apart from that, the clinical potential of GO based hydrogels and its major challenges are addressed in detail. Finally, this review concludes with a summary and invigorating future perspectives of GO based hydrogels for anticancer drug delivery. It is anticipated that this review can stimulate a new research gateway to facilitate the development of anticancer drug delivery by harnessing the unique properties of GO based hydrogels, such as large surface area, chemical purity, high loading capacity of drug, chemical stability, and the nature of lipophilic for cell membrane penetration.

Keywords: graphene oxide, drug delivery, hydrogel, nanocarrier, cancer nanotechnology

References(249)

1

Santra, S.; Malhotra, A. Fluorescent nanoparticle probes for imaging of cancer. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2011, 3, 501-510.

2

Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D. M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 2015, 136, E359-E386.

3

Potash, J.; Anderson, K. C. AACR cancer progress report 2014: Transforming lives through research. Clin. Cancer Res. 2014, 20, 4977.

4

Wang, X.; Yang, L.; Chen, Z. G.; Shin, D. M. Application of nanotechnology in cancer therapy and imaging. CA-Cancer J. Clin. 2008, 58, 97-110.

5

Ruenraroengsak, P.; Cook, J. M.; Florence, A. T. Nanosystem drug targeting: Facing up to complex realities. J. Control. Release 2010, 141, 265-276.

6

Nichols, J. W.; Bae, Y. H. Odyssey of a cancer nanoparticle: From injection site to site of action. Nano Today 2012, 7, 606-618.

7

Yezhelyev, M. V.; Gao, X. H.; Xing, Y.; Al-Hajj, A.; Nie, S. M.; O'Regan, R. M. Emerging use of nanoparticles in diagnosis and treatment of breast cancer. Lancet Oncol. 2006, 7, 657-667.

8

Haley, B.; Frenkel, E. Nanoparticles for drug delivery in cancer treatment. Urol. Oncol. 2008, 26, 57-64.

9

LaVan, D. A.; McGuire, T.; Langer, R. Small-scale systems for in vivo drug delivery. Nat. Biotechnol. 2003, 21, 1184-1191.

10

Liu, M. J.; Kono, K.; Fréchet, J. M. Water-soluble dendritic unimolecular micelles: Their potential as drug delivery agents. J. Control. Release 2000, 65, 121-131.

11

Kim, C. S.; Duncan, B.; Creran, B.; Rotello, V. M. Triggered nanoparticles as therapeutics. Nano Today 2013, 8, 439-447.

12

Ge, Z. S.; Liu, S. Y. Functional block copolymer assemblies responsive to tumor and intracellular microenvironments for site-specific drug delivery and enhanced imaging performance. Chem. Soc. Rev. 2013, 42, 7289-7325.

13

Issels, R. D. Hyperthermia adds to chemotherapy. Eur. J. Cancer 2008, 44, 2546-2554.

14

De La Rica, R.; Aili, D.; Stevens, M. M. Enzyme-responsive nanoparticles for drug release and diagnostics. Adv. Drug Deliv. Rev. 2012, 64, 967-978.

15

Gerweck, L. E.; Seetharaman, K. Cellular pH gradient in tumor versus normal tissue: Potential exploitation for the treatment of cancer. Cancer Res. 1996, 56, 1194-1198.

16

Deng, C.; Jiang, Y. J.; Cheng, R.; Meng, F. H.; Zhong, Z. Y. Biodegradable polymeric micelles for targeted and controlled anticancer drug delivery: Promises, progress and prospects. Nano Today 2012, 7, 467-480.

17

Lee, E. S.; Oh, K. T.; Kim, D.; Youn, Y. S.; Bae, Y. H. Tumor pH-responsive flower-like micelles of poly(L-lactic acid)-b-poly(ethylene glycol)-b-poly(L- histidine). J. Control. Release 2007, 123, 19-26.

18

Hamidi, M.; Azadi, A.; Rafiei, P. Hydrogel nanoparticles in drug delivery. Adv. Drug Deliv. Rev. 2008, 60, 1638-1649.

19

Min, K. H.; Park, K.; Kim, Y. -S.; Bae, S. M.; Lee, S.; Jo, H. G.; Park, R. -W.; Kim, I. -S.; Jeong, S. Y.; Kim, K. et al. Hydrophobically modified glycol chitosan nanoparticles-encapsulated camptothecin enhance the drug stability and tumor targeting in cancer therapy. J. Control. Release 2008, 127, 208-218.

20

Vinogradov, S. V.; Bronich, T. K.; Kabanov, A. V. Nanosized cationic hydrogels for drug delivery: Preparation, properties and interactions with cells. Adv. Drug Deliv. Rev. 2002, 54, 135-147.

21

Nahar, M.; Dutta, T.; Murugesan, S.; Asthana, A.; Mishra, D.; Rajkumar, V.; Tare, M.; Saraf, S.; Jain, N. K. Functional polymeric nanoparticles: An efficient and promising tool for active delivery of bioactives. Crit. Rev. Ther. Drug Carrier Syst. 2006, 23, 259-318.

22

Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Long-circulating and target- specific nanoparticles: Theory to practice. Pharmacol. Rev. 2001, 53, 283-318.

23

Peppas, N. A.; Mikos, A. G. Preparation methods and structure of hydrogels. In Hydrogels in Medicine and Pharmacy. Peppas, N., Ed.; CRC Press: Boca Raton, FL, 1986; pp 1-27.

24

Brannon-Peppas, L. Preparation and characterization of crosslinked hydrophilic networks. In Adsorbent Polymer Technology. Brannon-Peppas, L.; Harland, R. S., Eds.; Elsevier: Amsterdam, 1990; pp 45-66.

25

Peppas, N. A.; Khare, A. R. Preparation, structure and diffusional behavior of hydrogels in controlled release. Adv. Drug Deliv. Rev. 1993, 11, 1-35.

26

Hacker, M.; Mikos, A. Synthetic polymers. In Principles of Regenerative Medicine. Atala, A.; Lanza, R.; Thomson, J. A.; Nerem, R. M., Eds.; Academic press; San Diego, 2011; pp 587-622.

27

Das, N. Preparation methods and properties of hydrogel: A review. Int. J. Pharm. Pharm. Sci. 2013, 5, 112-117.

28

Goenka, S.; Sant, V.; Sant, S. Graphene-based nanomaterials for drug delivery and tissue engineering. J. Control. Release 2014, 173, 75-88.

29

Novoselov, K. S.; Fal'ko, V. I.; Colombo, L.; Gellert, P. R.; Schwab, M. G.; Kim, K. A roadmap for graphene. Nature 2012, 490, 192-200.

30

Ali, G. A. M.; Makhlouf, S. A.; Yusoff, M. M.; Chong, K. F. Structural and electrochemical characteristics of graphene nanosheets as supercapacitor electrodes. Rev. Adv. Mater. Sci. 2015, 41, 35-43.

31

Allen, M. J.; Tung, V. C.; Kaner, R. B. Honeycomb carbon: A review of graphene. Chem. Rev. 2010, 110, 132-145.

32

Geim, A. K. Graphene: Status and prospects. Science 2009, 324, 1530-1534.

33

Wang, Y.; Li, Z. H.; Wang, J.; Li, J. H.; Lin, Y. H. Graphene and graphene oxide: Biofunctionalization and applications in biotechnology. Trends Biotechnol. 2011, 29, 205-212.

34

Butler, S. Z.; Hollen, S. M.; Cao, L. Y.; Cui, Y.; Gupta, J. A.; Gutiérrez, H. R.; Heinz, T. F.; Hong, S. S.; Huang, J. X.; Ismach, A. F. et al. Progress, challenges, and opportunities in two-dimensional materials beyond graphene. ACS Nano 2013, 7, 2898-2926.

35

Huang, P.; Xu, C.; Lin, J.; Wang, C.; Wang, X. S.; Zhang, C. L.; Zhou, X. J.; Guo, S. W.; Cui, D. X. Folic acid-conjugated graphene oxide loaded with photosensitizers for targeting photodynamic therapy. Theranostics 2011, 1, 240-250.

36

Zhang, J. L.; Yang, H. J.; Shen, G. X.; Cheng, P.; Zhang, J. Y.; Guo, S. W. Reduction of graphene oxide via L-ascorbic acid. Chem. Commun. 2010, 46, 1112-1114.

37

Zhang, J. L.; Zhang, F.; Yang, H. J.; Huang, X. L.; Liu, H.; Zhang, J. Y.; Guo, S. W. Graphene oxide as a matrix for enzyme immobilization. Langmuir 2010, 26, 6083-6085.

38

Haubner, K.; Murawski, J.; Olk, P.; Eng, L. M.; Ziegler, C.; Adolphi, B.; Jaehne, E. The route to functional graphene oxide. ChemPhysChem 2010, 11, 2131-2139.

39

Nurunnabi, M.; Parvez, K.; Nafiujjaman, M.; Revuri, V.; Khan, H. A.; Feng, X. L.; Lee, Y. -K. Bioapplication of graphene oxide derivatives: Drug/gene delivery, imaging, polymeric modification, toxicology, therapeutics and challenges. RSC Adv. 2015, 5, 42141-42161.

40

Yang, K.; Wan, J.; Zhang, S.; Zhang, Y.; Lee, S. -T.; Liu, Z. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano 2011, 5, 516-522.

41

Wang, C. Y.; Wang, X. Q.; Lu, T.; Liu, F. S.; Guo, B. F.; Wen, N. Y.; Du, Y. W.; Lin, H.; Tang, J.; Zhang, L. Multi-functionalized graphene oxide complex as a plasmid delivery system for targeting hepatocellular carcinoma therapy. RSC Adv. 2016, 6, 22461-22468.

42

Li, H.; Luo, R. M.; Lam, K. Y. Modeling of environmentally sensitive hydrogels for drug delivery: An overview and recent developments. Front. Drug Des. Discov. 2006, 2, 295-331.

43

Ahmed, E. M. Hydrogel: Preparation, characterization, and applications: A review. J. Adv. Res. 2015, 6, 105-121.

44

Cha, C.; Shin, S. R.; Gao, X. G.; Annabi, N.; Dokmeci, M. R.; Tang, X. S.; Khademhosseini, A. Controlling mechanical properties of cell-laden hydrogels by covalent incorporation of graphene oxide. Small 2014, 10, 514-523.

45

Holloway, J. L.; Ma, H.; Rai, R.; Burdick, J. A. Modulating hydrogel crosslink density and degradation to control bone morphogenetic protein delivery and in vivo bone formation. J. Control. Release 2014, 191, 63-70.

46

Lee, S. C.; Kwon, I. K.; Park, K. Hydrogels for delivery of bioactive agents: A historical perspective. Adv. Drug Deliv. Rev. 2013, 65, 17-20.

47

Wichterle, O.; Lím, D. Hydrophilic gels for biological use. Nature 1960, 185, 117-118.

48

Buwalda, S. J.; Boere, K. W. M.; Dijkstra, P. J.; Feijen, J.; Vermonden, T.; Hennink, W. E. Hydrogels in a historical perspective: From simple networks to smart materials. J. Control. Release 2014, 190, 254-273.

49

Sharma, K.; Kumar, V.; Kaith, B. S.; Kalia, S.; Swart, H. C. Conducting polymer hydrogels and their applications. In Conducting Polymer Hybrids. Kumar; V.; Kalia, S.; Swart, H. C., Eds.; Springer: Switzerland, 2017; pp 193-221.

50

Haque, M. A.; Kurokawa, T.; Gong, J. P. Super tough double network hydrogels and their application as biomaterials. Polymer 2012, 53, 1805-1822.

51

Varaprasad, K.; Raghavendra, G. M.; Jayaramudu, T.; Yallapu, M. M.; Sadiku, R. A mini review on hydrogels classification and recent developments in miscellaneous applications. Mater. Sci. Eng. C 2017, 79, 958-971.

52

Akhtar, M. F.; Hanif, M.; Ranjha, N. M. Methods of synthesis of hydrogels… A review. Saudi Pharm. J. 2016, 24, 554-559.

53

Zu, Y. G.; Zhang, Y.; Zhao, X. H.; Shan, C.; Zu, S. C.; Wang, K. L.; Li, Y.; Ge, Y. L. Preparation and characterization of chitosan-polyvinyl alcohol blend hydrogels for the controlled release of nano-insulin. Int. J. Biol. Macromol. 2012, 50, 82-87.

54

Lugao, A. B.; Malmonge, S. M. Use of radiation in the production of hydrogels. Nucl. Instrum. Meth. Phys. Res. B 2001, 185, 37-42.

55

Sperinde, J. J.; Griffith, L. G. Synthesis and characterization of enzymatically- cross-linked poly(ethylene glycol) hydrogels. Macromolecules 1997, 30, 5255-5264.

56

Ullah, F.; Othman, M. B. H.; Javed, F.; Ahmad, Z.; Akil, H. M. Classification, processing and application of hydrogels: A review. Mater. Sci. Eng. C 2015, 57, 414-433.

57

Daoud Attieh, M.; Zhao, Y.; Elkak, A.; Falcimaigne-Cordin, A.; Haupt, K. Enzyme-initiated free-radical polymerization of molecularly imprinted polymer nanogels on a solid phase with an immobilized radical source. Angew. Chem., Int. Ed. 2017, 56, 3339-3343.

58

Chen, Q.; Zhu, L.; Zhao, C.; Wang, Q. M.; Zheng, J. A robust, one-pot synthesis of highly mechanical and recoverable double network hydrogels using thermoreversible sol-gel polysaccharide. Adv. Mater. 2013, 25, 4171-4176.

59

Zhang, L.; Zheng, G. -J.; Guo, Y. -T.; Zhou, L.; Du, J.; He, H. Preparation of novel biodegradable pHEMA hydrogel for a tissue engineering scaffold by microwave-assisted polymerization. Asian Pac. J. Trop. Med. 2014, 7, 136-140.

60

Atzet, S.; Curtin, S.; Trinh, P.; Bryant, S.; Ratner, B. Degradable poly(2- hydroxyethyl methacrylate)-co-polycaprolactone hydrogels for tissue engineering scaffolds. Biomacromolecules 2008, 9, 3370-3377.

61

Sharma, R.; Kalia, S.; Kaith, B. S.; Kumar, A.; Thakur, P.; Pathania, D.; Srivastava, M. K. Ggum-poly(itaconic acid) based superabsorbents via two-step free-radical aqueous polymerization for environmental and antibacterial applications. J. Polym. Environ. 2017, 25, 176-191.

62

Sarika, P. R.; Cinthya, K.; Jayakrishnan, A.; Anilkumar, P. R.; James, N. R. Modified gum arabic cross-linked gelatin scaffold for biomedical applications. Mater. Sci. Eng. C 2014, 43, 272-279.

63

Coviello, T.; Grassi, M.; Rambone, G.; Santucci, E.; Carafa, M.; Murtas, E.; Riccieri, F. M.; Alhaique, F. Novel hydrogel system from scleroglucan: Synthesis and characterization. J. Control. Release 1999, 60, 367-378.

64

Chung, T. -W.; Chou, T. -H.; Wu, K. -Y. Gelatin/PLGA hydrogel films and their delivery of hydrophobic drugs. J. Taiwan Inst. Chem. E. 2016, 60, 8-14.

65

Chen, Y. -Y.; Wu, H. -C.; Sun, J. -S.; Dong, G. -C.; Wang, T. -W. Injectable and thermoresponsive self-assembled nanocomposite hydrogel for long-term anticancer drug delivery. Langmuir 2013, 29, 3721-3729.

66

Yoshimura, T.; Hirao, N.; Fujioka, R. Preparation and characterization of biodegradable hydrogels based on ulvan, a polysaccharide from green seaweeds. Polym. Renew. Resour. 2016, 7, 33-41.

67

Riahi, N.; Liberelle, B.; Henry, O.; De Crescenzo, G. Impact of RGD amount in dextran-based hydrogels for cell delivery. Carbohyd. Polym. 2017, 161, 219-227.

68

Noteborn, W. E. M.; Gao, Y.; Jesse, W.; Kros, A.; Kieltyka, R. E. Dual- crosslinked human serum albumin-polymer hydrogels for affinity-based drug delivery. Macromol. Mater. Eng. 2017, 302, 1700243.

69

Kuijpers, A. J.; Van Wachem, P. B.; Van Luyn, M. J.; Engbers, G. H. M.; Krijgsveld, J.; Zaat, S. A. J.; Dankert, J.; Feijen, J. In vivo and in vitro release of lysozyme from cross-linked gelatin hydrogels: A model system for the delivery of antibacterial proteins from prosthetic heart valves. J. Control. Release 2000, 67, 323-336.

70

Omobono, M. A.; Zhao, X.; Furlong, M. A.; Kwon, C. H.; Gill, T. J.; Randolph, M. A.; Redmond, R. W. Enhancing the stiffness of collagen hydrogels for delivery of encapsulated chondrocytes to articular lesions for cartilage regeneration. J. Biomed. Mater. Res. A 2015, 103, 1332-1338.

71

Ghorpade, V. S.; Yadav, A. V.; Dias, R. J. Citric acid crosslinked cyclodextrin/hydroxypropylmethylcellulose hydrogel films for hydrophobic drug delivery. Int. J. Biol. Macromol. 2016, 93, 75-86.

72

Seki, Y.; Altinisik, A.; Demircioğlu, B.; Tetik, C. Carboxymethylcellulose (CMC)-hydroxyethylcellulose (HEC) based hydrogels: Synthesis and characterization. Cellulose 2014, 21, 1689-1698.

73

Gupta, A. P.; Arora, G. Preparation and characterization of guar-gum/polyvinylalcohol blend films. J. Mater. Sci. Eng. B 2011, 1, 28-33.

74

Rudick, J. G. Innovative macromolecular syntheses via isocyanide multicomponent reactions. J. Polym. Sci. A: Polym. Chem. 2013, 51, 3985-3991.

75

De Nooy, A. E.; Capitani, D.; Masci, G.; Crescenzi, V. Ionic polysaccharide hydrogels via the Passerini and Ugi multicomponent condensations: Synthesis, behavior and solid-state NMR characterization. Biomacromolecules 2000, 1, 259-267.

76

El-Gendy, A. A.; Abou-Yousef, H.; Adel, A.; El-Shinnawy, N. Bio-based hydrogel formed by gamma irradiation. Egypt. J. Chem. 2016, 59, 647-662.

77

Tohfafarosh, M.; Baykal, D.; Kiel, J. W.; Mansmann, K.; Kurtz, S. M. Effects of gamma and e-beam sterilization on the chemical, mechanical and tribological properties of a novel hydrogel. J. Mech. Behav. Biomed. Mater. 2016, 53, 250-256.

78

Wach, R. A.; Rokita, B.; Bartoszek, N.; Katsumura, Y.; Ulanski, P.; Rosiak, J. M. Hydroxyl radical-induced crosslinking and radiation-initiated hydrogel formation in dilute aqueous solutions of carboxymethylcellulose. Carbohyd. Polym. 2014, 112, 412-415.

79

Fekete, T.; Borsa, J.; Takács, E.; Wojnárovits, L. Synthesis of cellulose derivative based superabsorbent hydrogels by radiation induced crosslinking. Cellulose 2014, 21, 4157-4165.

80

Park, J. -S.; Kuang, J.; Gwon, H. -J.; Lim, Y. -M.; Jeong, S. -I.; Shin, Y. -M.; Khil, M. S.; Nho, Y. -C. Synthesis and characterization of zinc chloride containing poly(acrylic acid) hydrogel by gamma irradiation. Radiat. Phys. Chem. 2013, 88, 60-64.

81

Yamdej, R.; Pangza, K.; Srichana, T.; Aramwit, P. Superior physicochemical and biological properties of poly(vinyl alcohol)/sericin hydrogels fabricated by a non-toxic gamma-irradiation technique. J. Bioact. Compat. Polym. 2017, 32, 32-44.

82

Banaei, M.; Dehshiri, S.; Shirmardi, S. P. Physical Swelling Properties study of a PVP hydrogel in aqueous solutions by using electron beam (EB) irradiation. J. Nucl. Ene. Sci. Power Generat. Technol. 2016, 5, DOI: 10.4172/2325-9809.1000147.

83

Fekete, T.; Borsa, J.; Takács, E.; Wojnárovits, L. Synthesis of carboxymethylcellulose/starch superabsorbent hydrogels by gamma-irradiation. Chem. Cent. J. 2017, 11, 46.

84

Elbarbary, A. M.; Ghobashy, M. M. Phosphorylation of chitosan/HEMA interpenetrating polymer network prepared by γ-radiation for metal ions removal from aqueous solutions. Carbohyd. Polym. 2017, 162, 16-27.

85

Sperinde, J. J.; Griffith, L. G. Control and prediction of gelation kinetics in enzymatically cross-linked poly(ethylene glycol) hydrogels. Macromolecules 2000, 33, 5476-5480.

86

Arora, A.; Mahajan, A.; Katti, D. S. TGF-β1 presenting enzymatically cross-linked injectable hydrogels for improved chondrogenesis. Colloids Surf. B: Biointerfaces 2017, 159, 838-848.

87

Broguiere, N.; Isenmann, L.; Zenobi-Wong, M. Novel enzymatically cross-linked hyaluronan hydrogels support the formation of 3D neuronal networks. Biomaterials 2016, 99, 47-55.

88

Wu, C. Z.; Strehmel, C.; Achazi, K.; Chiappisi, L.; Dernedde, J.; Lensen, M. C.; Gradzielski, M.; Ansorge-Schumacher, M. B.; Haag, R. Enzymatically cross-linked hyperbranched polyglycerol hydrogels as scaffolds for living cells. Biomacromolecules 2014, 15, 3881-3890.

89

Da Silva, M. A.; Bode, F.; Grillo, I.; Dreiss, C. A. Exploring the kinetics of gelation and final architecture of enzymatically cross-linked chitosan/gelatin gels. Biomacromolecules 2015, 16, 1401-1409.

90

Le Thi, P.; Lee, Y.; Nguyen, D. H.; Park, K. D. In situ forming gelatin hydrogels by dual-enzymatic cross-linking for enhanced tissue adhesiveness. J. Mater. Chem. B 2017, 5, 757-764.

91

Gulrez, S. K. H.; Al-Assaf, S.; Phillips, G. O. Hydrogels: Methods of preparation, characterisation and applications. In Progress in Molecular and Environmental Bioengineering. Carpi, A., Ed.; InTech: UK, 2011; pp 117-150.

92

Gyles, D. A.; Castro, L. D.; Silva, J. O. C., Jr.; Ribeiro-Costa, R. M. A review of the designs and Prominent Biomedical Advances of Natural and Synthetic Hydrogel Formulations. Eur. Polym. J. 2017, 88, 373-392.

93

Agrawal, G.; Pich, A. Polymer gels as EAPs: Materials. In Electromechanically Active Polymers. Carpi, F., Ed.; Springer International Publishing: Switzerland, 2016; pp 1-27.

94

Hennink, W. E.; Van Nostrum, C. F. Novel crosslinking methods to design hydrogels. Adv. Drug Deliv. Rev. 2012, 64, 223-236.

95

Yang, C. H.; Wang, M. X.; Haider, H.; Yang, J. H.; Sun, J. -Y.; Chen, Y. M.; Zhou, J. X.; Suo, Z. G. Strengthening alginate/polyacrylamide hydrogels using various multivalent cations. ACS Appl. Mater. Interfaces 2013, 5, 10418-10422.

96

Girgin, B.; Korkmaz, O.; Yavaşer, R.; Karagözler, A. A. Production and drug release assesment of melatonin-loaded alginate/gum arabic beads. J. Turkish Chem. Soc. Sect. A: Chem. 2016, 3, 205-216.

97

Rezvanain, M.; Ahmad, N.; Amin, M. C. I. M.; Ng, S. -F. Optimization, characterization, and in vitro assessment of alginate-pectin ionic cross- linked hydrogel film for wound dressing applications. Int. J. Biol. Macromol. 2017, 97, 131-140.

98

Li, G.; Zhang, G. P.; Sun, R.; Wong, C. -P. Mechanical strengthened alginate/polyacrylamide hydrogel crosslinked by barium and ferric dual ions. J. Mater. Sci. 2017, 52, 8538-8545.

99

Hirschberg, J. H. K. K.; Brunsveld, L.; Ramzi, A.; Vekemans, J. A. J. M.; Sijbesma, R. P.; Meijer, E. W. Helical self-assembled polymers from cooperative stacking of hydrogen-bonded pairs. Nature 2000, 407, 167-170.

100

Li, G.; Yan, Q.; Xia, H. S.; Zhao, Y. Therapeutic-ultrasound-triggered shape memory of a melamine-enhanced poly(vinyl alcohol) physical hydrogel. ACS Appl. Mater. Interfaces 2015, 7, 12067-12073.

101

Shi, S. J.; Peng, X.; Liu, T. Q.; Chen, Y. -N.; He, C. C.; Wang, H. L. Facile preparation of hydrogen-bonded supramolecular polyvinyl alcohol- glycerol gels with excellent thermoplasticity and mechanical properties. Polymer 2017, 111, 168-176.

102

Li, G.; Zhang, H. J.; Fortin, D.; Xia, H. S.; Zhao, Y. Poly (vinyl alcohol)- Poly(ethylene glycol) double-network hydrogel: A general approach to shape memory and self-healing functionalities. Langmuir 2015, 31, 11709-11716.

103

Li, J. F.; Wang, Z. L.; Wen, L. G.; Nie, J.; Yang, S. G.; Xu, J.; Cheng, S. Z. D. Highly elastic fibers made from hydrogen-bonded polymer complex. ACS Macro Lett. 2016, 5, 814-818.

104

Dai, X. Y.; Zhang, Y. Y.; Gao, L.; Bai, T.; Wang, W.; Cui, Y. L.; Liu, W. G. A Mechanically strong, highly stable, thermoplastic, and self-healable supramolecular polymer hydrogel. Adv. Mater. 2015, 27, 3566-3571.

105

Hassan, C. M.; Peppas, N. A. Structure and applications of poly(vinyl alcohol) hydrogels produced by conventional crosslinking or by freezing/thawing methods. In Biopolymers· PVA Hydrogels, Anionic Polymerisation Nano-composites. Advances in Polymer Science. Springer: Berlin, 2000; pp 37-65.

106

Förster, S.; Antonietti, M. Amphiphilic block copolymers in structure- controlled nanomaterial hybrids. Adv. Mater. 1998, 10, 195-217.

DOI
107

Lee, D. S.; Jeong, B.; Bae, Y. H.; Kim, S. W. New thermoreversible and biodegradable block copolymer hydrogels. Proc. Control. Release Soc. 1996, (23), 228-229.

108

Jeong, B.; Bae, Y. H.; Kim, S. W. Thermoreversible gelation of PEG- PLGA-PEG triblock copolymer aqueous solutions. Macromolecules 1999, 32, 7064-7069.

109

Buwalda, S. J.; Nottelet, B.; Coudane, J. Robust & thermosensitive poly(ethylene glycol)-poly(ε-caprolactone) star block copolymer hydrogels. Polym. Degrad. Stabil. 2017, 137, 173-183.

110

Hom, W. L.; Bhatia, S. R. Significant enhancement of elasticity in alginate-clay nanocomposite hydrogels with PEO-PPO-PEO copolymers. Polymer 2017, 109, 170-175.

111

Cappello, J.; Crissman, J.; Dorman, M.; Mikolajczak, M.; Textor, G.; Marquet, M.; Ferrari, F. Genetic engineering of structural protein polymers. Biotechnol. Progr. 1990, 6, 198-202.

112

McGrath, K. P.; Fournier, M. J.; Mason, T. L.; Tirrell, D. A. Genetically directed syntheses of new polymeric materials. Expression of artificial genes encoding proteins with repeating-(AlaGly) 3ProGluGly-elements. J. Am. Chem. Soc. 1992, 114, 727-733.

113

Vagias, A.; Sergelen, K.; Koynov, K.; Košovan, P.; Dostalek, J.; Jonas, U.; Knoll, W.; Fytas, G. Diffusion and permeation of labeled IgG in grafted hydrogels. Macromolecules 2017, 50, 4770-4779.

114

Li, H. B.; Kong, N.; Laver, B.; Liu, J. Q. Hydrogels constructed from engineered proteins. Small 2016, 12, 973-987.

115

Yang, W. Z.; Wang, M. M.; Ma, L. L.; Li, H. Y.; Huang, L. Synthesis and characterization of biotin modified cholesteryl pullulan as a novel anticancer drug carrier. Carbohyd. Polym. 2014, 99, 720-727.

116

Xin, C.; Chen, J.; Liang, H. S.; Wan, J. W.; Li, J.; Li, B. Confirmation and measurement of hydrophobic interaction in sol-gel system of konjac glucomannan with different degree of deacetylation. Carbohyd. Polym. 2017, 174, 337-342.

117

Becerra, J.; Sudre, G.; Royaud, I.; Montserret, R.; Verrier, B.; Rochas, C.; Delair, T.; David, L. Tuning the hydrophilic/hydrophobic balance to control the structure of chitosan films and their protein release behavior. AAPS PharmSciTech 2017, 18, 1070-1083.

118

Bai, H.; Li, C.; Shi, G. Q. Functional composite materials based on chemically converted graphene. Adv. Mater. 2011, 23, 1089-1115.

119

Schniepp, H. C.; Li, J. -L.; McAllister, M. J.; Sai, H.; Herrera-Alonso, M.; Adamson, D. H.; Prud'homme, R. K.; Car, R.; Saville, D. A.; Aksay, I. A. Functionalized single graphene sheets derived from splitting graphite oxide. J. Phys. Chem. B 2006, 110, 8535-8539.

120

Hummers, W. S., Jr.; Offeman, R. E. Preparation of graphitic oxide. J. Am. Chem. Soc. 1958, 80, 1339.

121

Lerf, A.; He, H. Y.; Forster, M.; Klinowski, J. Structure of graphite oxide revisited. J. Phys. Chem. B 1998, 102, 4477-4482.

122

Nasrollahzadeh, M.; Babaei, F.; Fakhri, P.; Jaleh, B. Synthesis, charac-terization, structural, optical properties and catalytic activity of reduced graphene oxide/copper nanocomposites. RSC Adv. 2015, 5, 10782-10789.

123

Zhang, Q.; Wu, Z. N.; Li, N.; Pu, Y. Q.; Wang, B.; Zhang, T.; Tao, J. S. Advanced review of graphene-based nanomaterials in drug delivery systems: Synthesis, modification, toxicity and application. Mater. Sci. Eng. C 2017, 77, 1363-1375.

124

Travlou, N. A.; Kyzas, G. Z.; Lazaridis, N. K.; Deliyanni, E. A. Functionalization of graphite oxide with magnetic chitosan for the preparation of a nanocomposite dye adsorbent. Langmuir 2013, 29, 1657-1668.

125

Sun, X. M.; Liu, Z.; Welsher, K.; Robinson, J. T.; Goodwin, A.; Zaric, S.; Dai, H. J. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 2008, 1, 203-212.

126

Liu, Z.; Robinson, J. T.; Sun, X. M.; Dai, H. J. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J. Am. Chem. Soc. 2008, 130, 10876-10877.

127

Chen, L.; Zhong, X. Y.; Yi, X.; Huang, M.; Ning, P.; Liu, T.; Ge, C. C.; Chai, Z. F.; Liu, Z.; Yang, K. Radionuclide 131I labeled reduced graphene oxide for nuclear imaging guided combined radio- and photothermal therapy of cancer. Biomaterials 2015, 66, 21-28.

128

Jiang, B.; Qu, Y. Y.; Zhang, L. H.; Liang, Z.; Zhang, Y. K. 4-Mercapto-phenylboronic acid functionalized graphene oxide composites: Preparation, characterization and selective enrichment of glycopeptides. Anal. Chim. Acta 2016, 912, 41-48.

129

Hu, H. Q.; Yu, J. H.; Li, Y. Y.; Zhao, J.; Dong, H. Q. Engineering of a novel pluronic F127/graphene nanohybrid for pH responsive drug delivery. J. Biomed. Mater. Res. A 2012, 100, 141-148.

130

Liu, S. L.; Ling, J.; Li, K. W.; Yao, F.; Oderinde, O.; Zhang, Z. H.; Fu, G. D. Bio-inspired and lanthanide-induced hierarchical sodium alginate/graphene oxide composite paper with enhanced physicochemical properties. Compos. Sci. Technol. 2017, 145, 62-70.

131

Peng, X.; He, C. C.; Liu, J. Q.; Wang, H. L. Biomimetic jellyfish-like PVA/graphene oxide nanocomposite hydrogels with anisotropic and pH-responsive mechanical properties. J. Mater. Sci. 2016, 51, 5901-5911.

132

Stankovich, S.; Piner, R. D.; Chen, X. Q.; Wu, N. Q.; Nguyen, S. T.; Ruoff, R. S. Stable aqueous dispersions of graphitic nanoplatelets via the reduction of exfoliated graphite oxide in the presence of poly(sodium 4-styrenesulfonate). J. Mater. Chem. 2006, 16, 155-158.

133

Yang, Y.; Zhang, Y. M.; Chen, Y.; Zhao, D.; Chen, J. T.; Liu, Y. Construction of a graphene oxide based noncovalent multiple nanosupramolecular assembly as a scaffold for drug delivery. Chem. —Eur. J 2012, 18, 4208-4215.

134

Wang, J.; Chen, Z. M.; Chen, B. L. Adsorption of polycyclic aromatic hydrocarbons by graphene and graphene oxide nanosheets. Environ. Sci. Technol. 2014, 48, 4817-4825.

135

Azadbakht, A.; Roushani, M.; Abbasi, A. R.; Derikvand, Z.; Menati, S. Bifunctional impedimetric sensors based on azodicarboxamide supported on modified graphene nanosheets. Mater. Sci. Eng. C 2016, 69, 221-230.

136

Yu, Y.; Shu, Y.; Ye, L. In situ crosslinking of poly (vinyl alcohol)/graphene oxide-glutamic acid nano-composite hydrogel as microbial carrier: Intercalation structure and its wastewater treatment performance. Chem. —Eng. J. 2018, 336, 306-314.

137

Park, Y. H.; Park, S. Y.; In, I. Direct noncovalent conjugation of folic acid on reduced graphene oxide as anticancer drug carrier. J. Ind. Eng. Chem. 2015, 30, 190-196.

138

Hu, X. G.; Zhou, Q. X. Health and ecosystem risks of graphene. Chem. Rev. 2013, 113, 3815-3835.

139

Seabra, A. B.; Paula, A. J.; de Lima, R.; Alves, O. L.; Durán, N. Nanotoxicity of graphene and graphene oxide. Chem. Res. Toxicol. 2014, 27, 159-168.

140

Zhao, J.; Wang, Z. Y.; White, J. C.; Xing, B. S. Graphene in the aquatic environment: Adsorption, dispersion, toxicity and transformation. Environ. Sci. Technol. 2014, 48, 9995-10009.

141

Tonelli, F. M.; Goulart, V. A.; Gomes, K. N.; Ladeira, M. S.; Santos, A. K.; Lorençon, E.; Ladeira, L. O.; Resende, R. R. Graphene-based nanomaterials: Biological and medical applications and toxicity. Nanomedicine 2015, 10, 2423-2450.

142

Bitounis, D.; Ali-Boucetta, H.; Hong, B. H.; Min, D. H.; Kostarelos, K. Prospects and challenges of graphene in biomedical applications. Adv. Mater. 2013, 25, 2258-2268.

143

Bianco, A. Graphene: Safe or toxic? The two faces of the medal. Angew. Chem., Int. Ed. 2013, 52, 4986-4997.

144

Yang, K.; Li, Y. J.; Tan, X. F.; Peng, R.; Liu, Z. Behavior and toxicity of graphene and its functionalized derivatives in biological systems. Small 2013, 9, 1492-1503.

145

Sanchez, V. C.; Jachak, A.; Hurt, R. H.; Kane, A. B. Biological interactions of graphene-family nanomaterials: An interdisciplinary review. Chem. Res. Toxicol. 2012, 25, 15-34.

146

Jastrzębska, A. M.; Kurtycz, P.; Olszyna, A. R. Recent advances in graphene family materials toxicity investigations. J. Nanopart. Res. 2012, 14, 1320.

147

Zhang, B. M.; Wang, Y.; Zhai, G. X. Biomedical applications of the graphene-based materials. Mater. Sci. Eng. C 2016, 61, 953-964.

148

Wong, C. H. A.; Sofer, Z.; Kubešová, M.; Kučera, J.; Matějková, S.; Pumera, M. Synthetic routes contaminate graphene materials with a whole spectrum of unanticipated metallic elements. Proc. Natl. Acad. Sci. USA 2014, 111, 13774-13779.

149

Ambrosi, A.; Chua, C. K.; Khezri, B.; Sofer, Z.; Webster, R. D.; Pumera, M. Chemically reduced graphene contains inherent metallic impurities present in parent natural and synthetic graphite. Proc. Natl. Acad. Sci. USA 2012, 109, 12899-12904.

150

Mullick Chowdhury, S.; Dasgupta, S.; McElroy, A. E.; Sitharaman, B. Structural disruption increases toxicity of graphene nanoribbons. J. Appl. Toxicol. 2014, 34, 1235-1246.

151

Zhang, Y. B.; Ali, S. F.; Dervishi, E.; Xu, Y.; Li, Z. R.; 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.

152

Vallabani, N. V.; Mittal, S.; Shukla, R. K.; Pandey, A. K.; Dhakate, S. R.; Pasricha, R.; Dhawan, A. Toxicity of graphene in normal human lung cells (BEAS-2B). J. Biomed. Nanotechnol. 2011, 7, 106-107.

153

Sasidharan, A.; Panchakarla, L. S.; Chandran, P.; Menon, D.; Nair, S.; Rao, C. N. R.; Koyakutty, M. Differential nano-bio interactions and toxicity effects of pristine versus functionalized graphene. Nanoscale 2011, 3, 2461-2464.

154

Horváth, L.; Magrez, A.; Burghard, M.; Kern, K.; Forró, L.; Schwaller, B. Evaluation of the toxicity of graphene derivatives on cells of the lung luminal surface. Carbon 2013, 64, 45-60.

155

Akhavan, O.; Ghaderi, E.; Akhavan, A. Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials 2012, 33, 8017-8025.

156

Muthoosamy, K.; Bai, R. G.; Manickam, S. Graphene and graphene oxide as a docking station for modern drug delivery system. Curr. Drug Deliv. 2014, 11, 701-718.

157

Yang, K.; Feng, L. Z.; Shi, X. Z.; Liu, Z. Nano-graphene in biomedicine: Theranostic applications. Chem. Soc. Rev. 2013, 42, 530-547.

158

Yang, X. Y.; Zhang, X. Y.; Liu, Z. F.; Ma, Y. F.; Huang, Y.; Chen, Y. S. High-efficiency loading and controlled release of doxorubicin hydrochloride on graphene oxide. J. Phys. Chem. C 2008, 112, 17554-17558.

159

Ni, Y. N.; Zhang, F. Y.; Kokot, S. Graphene oxide as a nanocarrier for loading and delivery of medicinal drugs and as a biosensor for detection of serum albumin. Anal. Chim. Acta 2013, 769, 40-48.

160

Wang, Z. H.; Gao, Y. L.; Xia, J. F.; Zhang, F. F.; Xia, Y. Z.; Li, Y. H. Synthesis and characterization of glycyrrhizin-decorated graphene oxide for hepatocyte-targeted delivery. C. R. Chim. 2012, 15, 708-713.

161

Zhang, Q.; Li, W. W.; Kong, T.; Su, R. G.; Li, N.; Song, Q.; Tang, M. L.; Liu, L. W.; Cheng, G. S. Tailoring the interlayer interaction between doxorubicin-loaded graphene oxide nanosheets by controlling the drug content. Carbon 2013, 51, 164-172.

162

Ma, D.; Lin, J. T.; Chen, Y. Y.; Xue, W.; Zhang, L. -M. In situ gelation and sustained release of an antitumor drug by graphene oxide nanosheets. Carbon 2012, 50, 3001-3007.

163

Zhou, L.; Zhou, L.; Wei, S. H.; Ge, X. F.; Zhou, J. H.; Jiang, H. J.; Li, F. Y.; Shen, J. Combination of chemotherapy and photodynamic therapy using graphene oxide as drug delivery system. J. Photochem. Photobiol. B 2014, 135, 7-16.

164

Zhou, L.; Wang, W.; Tang, J.; Zhou, J. H.; Jiang, H. J.; Shen, J. Graphene oxide noncovalent photosensitizer and its anticancer activity in vitro. Chem. —Eur. J. 2011, 17, 12084-12091.

165

Hasanzade, Z.; Raissi, H. Solvent/co-solvent effects on the electronic properties and adsorption mechanism of anticancer drug thioguanine on graphene oxide surface as a nanocarrier: Density functional theory investigation and a molecular dynamics. Appl. Surf. Sci. 2017, 422, 1030-1041.

166

Bardajee, G. R.; Hooshyar, Z. Drug release study by a novel thermo sensitive nanogel based on salep modified graphene oxide. J. Polym. Res. 2017, 24, 49.

167

Chen, P.; Wang, X.; Wang, G.; Duo, Y. R.; Zhang, X. Y.; Hu, X. H.; Zhang, X. J. Double network self-healing graphene hydrogel by two step method for anticancer drug delivery. Mater. Technol. 2014, 29, 210-213.

168

Zhang, H. J.; Zhai, D. D.; He, Y. Graphene oxide/polyacrylamide/carboxymethyl cellulose sodium nanocomposite hydrogel with enhanced mechanical strength: Preparation, characterization and the swelling behavior. RSC Adv. 2014, 4, 44600-44609.

169

Kavitha, T.; Kang, I. -K.; Park, S. -Y. Poly(N-vinyl caprolactam) grown on nanographene oxide as an effective nanocargo for drug delivery. Colloids Surf. B: Biointerfaces 2014, 115, 37-45.

170

Kundu, A.; Nandi, S.; Das, P.; Nandi, A. K. Fluorescent graphene oxide via polymer grafting: An efficient nanocarrier for both hydrophilic and hydrophobic drugs. ACS Appl. Mater. Interfaces 2015, 7, 3512-3523.

171

Pourjavadi, A.; Shakerpoor, A.; Tehrani, Z. M.; Bumajdad, A. Magnetic graphene oxide mesoporous silica hybrid nanoparticles with dendritic pH sensitive moieties coated by PEGylated alginate-co-poly (acrylic acid) for targeted and controlled drug delivery purposes. J. Polym. Res. 2015, 22, 156.

172

Mahkam, M.; Rafi, A. A.; Faraji, L.; Zakerzadeh, E. Preparation of poly (methacrylic acid)-graphene oxide nanocomposite as a pH-sensitive drug carrier through in-situ copolymerization of methacrylic acid with polymerizable graphene. Polym. -Plast. Technol. Eng. 2015, 54, 916-922.

173

Zhao, X. B.; Yang, L. W.; Li, X. R.; Jia, X.; Liu, L.; Zeng, J.; Guo, J. S.; Liu, P. Functionalized graphene oxide nanoparticles for cancer cell-specific delivery of antitumor drug. Bioconjugate Chem. 2015, 26, 128-136.

174

He, C.; Shi, Z. -Q.; Cheng, C.; Nie, C. -X.; Zhou, M.; Wang, L. -R.; Zhao, C. -S. Highly swellable and biocompatible graphene/heparin-analogue hydrogels for implantable drug and protein delivery. RSC Adv. 2016, 6, 71893-71904.

175

Bardajee, G. R.; Hooshyar, Z.; Farsi, M.; Mobini, A.; Sang, G. Synthesis of a novel thermo/pH sensitive nanogel based on salep modified graphene oxide for drug release. Mater. Sci. Eng. C 2017, 72, 558-565.

176

Raafat, A. I.; Ali, A. E. -H. pH-controlled drug release of radiation synthesized graphene oxide/(acrylic acid-co-sodium alginate) interpenetrating network. Polym. Bull. 2017, 74, 2045-2062.

177

Dai, Z. Q.; Lu, Q. F.; Quan, Q. G.; Mo, R. J.; Zhou, C. X.; Hong, P. Z.; Li, C. Y. Novel low temperature (< 37℃) chitosan hydrogel fabrication under the synergistic effect of graphene oxide. New J. Chem. 2017, 41, 671-676.

DOI
178

Dragutan, I.; Dragutan, V.; Demonceau, A. Editorial of special issue ruthenium complex: The expanding chemistry of the ruthenium complexes. Molecules 2015, 20, 17244-17274.

179

Lee, Y.; Bae, J. W.; Thi, T. T. H.; Park, K. M.; Park, K. D. Injectable and mechanically robust 4-arm PPO-PEO/graphene oxide composite hydrogels for biomedical applications. Chem. Commun. 2015, 51, 8876-8879.

180

Yang, H. H.; Bremner, D. H.; Tao, L.; Li, H. Y.; Hu, J.; Zhu, L. M. Carboxymethyl chitosan-mediated synthesis of hyaluronic acid-targeted graphene oxide for cancer drug delivery. Carbohyd. Polym. 2016, 135, 72-78.

181

Xu, Z. Y.; Wang, S.; Li, Y. J.; Wang, M. W.; Shi, P.; Huang, X. Y. Covalent functionalization of graphene oxide with biocompatible poly(ethylene glycol) for delivery of paclitaxel. ACS Appl. Mater. Interfaces 2014, 6, 17268-17276.

182

Wu, T.; Zhang, B.; Liang, Y. Y.; Liu, T.; Bu, J. Y.; Lin, L. X.; Wu, Z. M.; Liu, H. X.; Wen, S. P.; Tan, S. Z. et al. Heparin-modified graphene oxide loading anti-cancer drug and growth factor with heat stability, long-term release property and lower cytotoxicity. RSC Adv. 2015, 5, 84334-84342.

183

Gu, Y. M.; Guo, Y. Z.; Wang, C. Y.; Xu, J. K.; Wu, J. P.; Kirk, T. B.; Ma, D.; Xue, W. A polyamidoamne dendrimer functionalized graphene oxide for DOX and MMP-9 shRNA plasmid co-delivery. Mater. Sci. Eng. C 2017, 70, 572-585.

184

Chen, H.; Wang, Z. Y.; Zong, S. F.; Wu, L.; Chen, P.; Zhu, D.; Wang, C. L.; Xu, S. H.; Cui, Y. P. SERS-fluorescence monitored drug release of a redox-responsive nanocarrier based on graphene oxide in tumor cells. ACS Appl. Mater. Interfaces 2014, 6, 17526-17533.

185

Khoee, S.; Bafkary, R.; Fayyazi, F. DOX delivery based on chitosan- capped graphene oxide-mesoporous silica nanohybride as pH-responsive nanocarriers. J. Sol-Gel Sci. Technol. 2017, 81, 493-504.

186

Wu, H. X.; Shi, H. L.; Wang, Y. P.; Jia, X. Q.; Tang, C. Z.; Zhang, J. M.; Yang, S. P. Hyaluronic acid conjugated graphene oxide for targeted drug delivery. Carbon 2014, 69, 379-389.

187

Zhang, B.; Yan, Y. Y.; Shen, Q. J.; Ma, D.; Huang, L. H.; Cai, X.; Tan, S. Z. A colon targeted drug delivery system based on alginate modificated graphene oxide for colorectal liver metastasis. Mater. Sci. Eng. C 2017, 79, 185-190.

188

Pan, Q. X.; Lv, Y.; Williams, G. R.; Tao, L.; Yang, H. H.; Li, H. Y.; Zhu, L. M. Lactobionic acid and carboxymethyl chitosan functionalized graphene oxide nanocomposites as targeted anticancer drug delivery systems. Carbohyd. Polym. 2016, 151, 812-820.

189

Tan, J. T.; Meng, N.; Fan, Y. T.; Su, Y. T.; Zhang, M.; Xiao, Y. H.; Zhou, N. L. Hydroxypropyl-β-cyclodextrin-graphene oxide conjugates: Carriers for anti-cancer drugs. Mater. Sci. Eng. C 2016, 61, 681-687.

190

Lei, H. L.; Xie, M.; Zhao, Y. W.; Zhang, F.; Xu, Y. G.; Xie, J. M. Chitosan/sodium alginate modificated graphene oxide-based nanocomposite as a carrier for drug delivery. Ceram. Int. 2016, 42, 17798-17805.

191

Chen, J. Q.; Liu, H. Y.; Zhao, C. B.; Qin, G. Q.; Xi, G. N.; Li, T.; Wang, X. P.; Chen, T. S. One-step reduction and PEGylation of graphene oxide for photothermally controlled drug delivery. Biomaterials 2014, 35, 4986-4995.

192

Hou, L.; Shi, Y. Y.; Jiang, G. X.; Liu, W.; Han, H. L.; Feng, Q. H.; Ren, J. X.; Yuan, Y. J.; Wang, Y. C.; Shi, J. J. et al. Smart nanocomposite hydrogels based on azo crosslinked graphene oxide for oral colon-specific drug delivery. Nanotechnology 2016, 27, 315105.

193

Liu, J. Q.; Cui, L.; Kong, N.; Barrow, C. J.; Yang, W. R. RAFT controlled synthesis of graphene/polymer hydrogel with enhanced mechanical property for pH-controlled drug release. Eur. Polym. J. 2014, 50, 9-17.

194

Byun, E.; Lee, H. Enhanced loading efficiency and sustained release of doxorubicin from hyaluronic acid/graphene oxide composite hydrogels by a mussel-inspired catecholamine. J. Nanosci. Nanotechnol. 2014, 14, 7395-7401.

195

Lv, Y.; Tao, L.; Bligh, S. W. A.; Yang, H. H.; Pan, Q. X.; Zhu, L. M. Targeted delivery and controlled release of doxorubicin into cancer cells using a multifunctional graphene oxide. Mater. Sci. Eng. C 2016, 59, 652-660.

196

Angelopoulou, A.; Voulgari, E.; Diamanti, E. K.; Gournis, D.; Avgoustakis, K. Graphene oxide stabilized by PLA-PEG copolymers for the controlled delivery of paclitaxel. Eur. J. Pharm. Biopharm. 2015, 93, 18-26.

197

Fan, L. H.; Ge, H. Y.; Zou, S. Q.; Xiao, Y.; Wen, H. G.; Li, Y.; Feng, H.; Nie, M. Sodium alginate conjugated graphene oxide as a new carrier for drug delivery system. Int. J. Biol. Macromol. 2016, 93, 582-590.

198

Xu, X.; Wang, J.; Wang, Y.; Zhao, L.; Li, Y.; Liu, C. Formation of graphene oxide-hybridized nanogels for combinative anticancer therapy. Nanomedicine 2018, 14, 2387-2395.

199

Yu, D. N.; Ruan, P.; Meng, Z. Y.; Zhou, J. P. The structure-dependent electric release and enhanced oxidation of drug in graphene oxide-based nanocarrier loaded with anticancer herbal drug berberine. J. Pharm. Sci. 2015, 104, 2489-2500.

200

Guo, Q. F.; Cao, H.; Li, X. H.; Liu, S. W. Thermosensitive hydrogel drug delivery system containing doxorubicin loaded CS-GO nanocarriers for controlled release drug in situ. Mater. Technol. 2015, 30, 294-300.

201

Pourjavadi, A.; Tehrani, Z. M.; Jokar, S. Chitosan based supramolecular polypseudorotaxane as a pH-responsive polymer and their hybridization with mesoporous silica-coated magnetic graphene oxide for triggered anticancer drug delivery. Polymer 2015, 76, 52-61.

202

Mu, S. S.; Li, G. W.; Liang, Y. Y.; Wu, T.; Ma, D. Hyperbranched polyglycerol-modified graphene oxide as an efficient drug carrier with good biocompatibility. Mater. Sci. Eng. C 2017, 78, 639-646.

203

Hu, X. H.; Li, D.; Tan, H. P.; Pan, C. B.; Chen, X. X. Injectable graphene oxide/graphene composite supramolecular hydrogel for delivery of anti-cancer drugs. J. Macromol. Sci. A 2014, 51, 378-384.

204

Yuan, Y.; Yan, Z. M.; Mu, R. J.; Wang, L.; Gong, J. N.; Hong, X.; Haruna, M. H.; Pang, J. The effects of graphene oxide on the properties and drug delivery of konjac glucomannan hydrogel. J. Appl. Polym. Sci. 2017, 134, 45327.

205

Ye, Y. F.; Hu, X. H. A pH-sensitive injectable nanoparticle composite hydrogel for anticancer drug delivery. J. Nanomater. 2016, 2016, Article ID 9816461.

206

Saeednia, L.; Yao, L.; Berndt, M.; Cluff, K.; Asmatulu, R. Structural and biological properties of thermosensitive chitosan-graphene hybrid hydrogels for sustained drug delivery applications. J. Biomed. Mater. Res. A 2017, 105, 2381-2390.

207

Tian, J. W.; Luo, Y. P.; Huang, L. W.; Feng, Y. Q.; Ju, H. X.; Yu, B. -Y. Pegylated folate and peptide-decorated graphene oxide nanovehicle for in vivo targeted delivery of anticancer drugs and therapeutic self- monitoring. Biosens. Bioelectron. 2016, 80, 519-524.

208

Huang, Y. -P.; Hung, C. -M.; Hsu, Y. -C.; Zhong, C. -Y.; Wang, W. -R.; Chang, C. -C.; Lee, M. -J. Suppression of breast cancer cell migration by small interfering RNA delivered by polyethylenimine-functionalized graphene oxide. Nanoscale Res. Lett. 2016, 11, 247.

209

Masoudipour, E.; Kashanian, S.; Maleki, N. A targeted drug delivery system based on dopamine functionalized nano graphene oxide. Chem. Phys. Lett. 2017, 668, 56-63.

210

Alibolandi, M.; Mohammadi, M.; Taghdisi, S. M.; Ramezani, M.; Abnous, K. Fabrication of aptamer decorated dextran coated nano-graphene oxide for targeted drug delivery. Carbohyd. Polym. 2017, 155, 218-229.

211

Ma, N. X.; Liu, J.; He, W. X.; Li, Z. H.; Luan, Y. X.; Song, Y. M.; Garg, S. Folic acid-grafted bovine serum albumin decorated graphene oxide: An efficient drug carrier for targeted cancer therapy. J. Colloid Interface Sci. 2017, 490, 598-607.

212

Deb, A.; Vimala, R. Natural and synthetic polymer for graphene oxide mediated anticancer drug delivery—A comparative study. Int. J. Biol. Macromol. 2018, 107, 2320-2333.

213

Cui, X. J.; Dong, L. L.; Zhong, S. L.; Shi, C.; Sun, Y. X.; Chen, P. Sonochemical fabrication of folic acid functionalized multistimuli-responsive magnetic graphene oxide-based nanocapsules for targeted drug delivery. Chem. Eng. J. 2017, 326, 839-848.

214

Shi, Y. F.; Xiong, Z. P.; Lu, X. F.; Yan, X.; Cai, X.; Xue, W. Novel carboxymethyl chitosan-graphene oxide hybrid particles for drug delivery. J. Mater. Sci. : Mater. Med. 2016, 27, 169.

215

Wang, J.; Liu, C. H.; Shuai, Y.; Cui, X. Y.; Nie, L. Controlled release of anticancer drug using graphene oxide as a drug-binding effector in konjac glucomannan/sodium alginate hydrogels. Colloids Surf. B: Biointerfaces 2014, 113, 223-229.

216

Deng, L.; Li, Q. J.; Al-Rehili, S.; Omar, H.; Almalik, A.; Alshamsan, A.; Zhang, J. F.; Khashab, N. M. Hybrid iron oxide-graphene oxide- polysaccharides microcapsule: A micro-matryoshka for on-demand drug release and antitumor therapy in vivo. ACS Appl. Mater. Interfaces 2016, 8, 6859-6868.

217

Khatamian, M.; Divband, B.; Farahmand-Zahed, F. Synthesis and characterization of zinc (Ⅱ)-loaded zeolite/graphene oxide nanocomposite as a new drug carrier. Mater. Sci. Eng. C 2016, 66, 251-258.

218

Rasoulzadeh, M.; Namazi, H. Carboxymethyl cellulose/graphene oxide bio-nanocomposite hydrogel beads as anticancer drug carrier agent. Carbohyd. Polym. 2017, 168, 320-326.

219

Zhang, H. J.; Yan, T.; Xu, S.; Feng, S. N.; Huang, D. D.; Fujita, M.; Gao, X. -D. Graphene oxide-chitosan nanocomposites for intracellular delivery of immunostimulatory CpG oligodeoxynucleotides. Mater. Sci. Eng. C 2017, 73, 144-151.

220

Sudhakar, K.; Moloi, S. J.; Rao, K. M. Graphene oxide/poly(N-isopropyl acrylamide)/sodium alginate-based dual responsive composite beads for controlled release characteristics of chemotherapeutic agent. Iran. Polym. J. 2017, 26, 521-530.

221

Wang, R.; Shou, D.; Lv, O. Y.; Kong, Y.; Deng, L. H.; Shen, J. pH- Controlled drug delivery with hybrid aerogel of chitosan, carboxymethyl cellulose and graphene oxide as the carrier. Int. J. Biol. Macromol. 2017, 103, 248-253.

222

Hurt, R. H.; Monthioux, M.; Kane, A. Toxicology of carbon nanomaterials: Status, trends, and perspectives on the special issue. Carbon 2006, 44, 1028-1033.

223

Poland, C. A.; Duffin, R.; Kinloch, I.; Maynard, A.; Wallace, W. A. H.; Seaton, A.; Stone, V.; Brown, S.; MacNee, W.; Donaldson, K. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos- like pathogenicity in a pilot study. Nat. Nanotechnol. 2008, 3, 423-428.

224

Sanchez, V. C.; Weston, P.; Yan, A. H.; Hurt, R. H.; Kane, A. B. A 3-dimensional in vitro model of epithelioid granulomas induced by high aspect ratio nanomaterials. Part. Fibre Toxicol. 2011, 8, 17.

225

Li, S. H.; Peng, Z. L.; Han, X.; Leblanc, R. M. Interactions between graphene oxide and biomolecules from surface chemistry and spectroscopy. In Recent Progress in Colloid and Surface Chemistry with Biological Applications. American Chemical Society: USA, 2015; pp 43-64.

226

Jachak, A. C.; Creighton, M.; Qiu, Y.; Kane, A. B.; Hurt, R. H. Biological interactions and safety of graphene materials. MRS Bull. 2012, 37, 1307-1313.

227

Hu, C. W.; Liu, L.; Li, X. L.; Xu, Y. D.; Ge, Z. G.; Zhao, Y. J. Effect of graphene oxide on copper stress in Lemna minor L. : Evaluating growth, biochemical responses, and nutrient uptake. J. Hazard. Mater. 2018, 341, 168-176.

228

Gao, W. The chemistry of graphene oxide. In Graphene Oxide. Springer: Switzerland, 2015; pp 61-95.

229

Li, S. H.; Mulloor, J. J.; Wang, L. Y.; Ji, Y. W.; Mulloor, C. J.; Micic, M.; Orbulescu, J.; Leblanc, R. M. Strong and selective adsorption of lysozyme on graphene oxide. ACS Appl. Mater. Interfaces 2014, 6, 5704-5712.

230

Han, S.; Su, L. Q.; Zhai, M. H.; Ma, L.; Liu, S. W.; Teng, Y. A molecularly imprinted composite based on graphene oxide for targeted drug delivery to tumor cells. J. Mater. Sci. 2019, 54, 3331-3341.

231

Gurunathan, S.; Kang, M. -H.; Qasim, M.; Kim, J. -H. Nanoparticle-mediated combination therapy: Two-in-one approach for cancer. Int. J. Mol. Sci. 2018, 19, 3264.

232

Zamani, M.; Rostami, M.; Aghajanzadeh, M.; Manjili, H. K.; Rostamizadeh, K.; Danafar, H. Mesoporous titanium dioxide@ zinc oxide-graphene oxide nanocarriers for colon-specific drug delivery. J. Mater. Sci. 2018, 53, 1634-1645.

233

Vovusha, H.; Sanyal, S.; Sanyal, B. Interaction of nucleobases and aromatic amino acids with graphene oxide and graphene flakes. J. Phys. Chem. Lett. 2013, 4, 3710-3718.

234

Liu, B. W.; Salgado, S.; Maheshwari, V.; Liu, J. W. DNA adsorbed on graphene and graphene oxide: Fundamental interactions, desorption and applications. Curr. Opin. Colloid Interface Sci. 2016, 26, 41-49.

235

Banerjee, S.; Wilson, J.; Shim, J.; Shankla, M.; Corbin, E. A.; Aksimentiev, A.; Bashir, R. Slowing DNA transport using graphene-DNA interactions. Adv. Funct. Mater. 2015, 25, 936-946.

236

Wu, M.; Kempaiah, R.; Huang, P. -J. J.; Maheshwari, V.; Liu, J. W. Adsorption and desorption of DNA on graphene oxide studied by fluorescently labeled oligonucleotides. Langmuir 2011, 27, 2731-2738.

237

Becheru, D. F.; Vlăsceanu, G. M.; Banciu, A.; Vasile, E.; Ioniţă, M.; Burns, J. S. Optical graphene-based biosensor for nucleic acid detection; influence of graphene functionalization and ionic strength. Int. J. Mol. Sci. 2018, 19, 3230.

238

Liu, X. Y.; Sen, S.; Liu, J. Y.; Kulaots, I.; Geohegan, D.; Kane, A.; Puretzky, A. A.; Rouleau, C. M.; More, K. L.; Palmore, G. T. R. et al. Antioxidant deactivation on graphenic nanocarbon surfaces. Small 2011, 7, 2775-2785.

239

Shubha, P.; Namratha, K.; Mithali, K.; Divya, V.; Thakur, M. S.; Byrappa, K. Green technology enabled graphene oxide reduction using Justichia wynaadensis extract and assessment of in vitro antioxidant and antibacterial activity. Adv. Sci. Lett. 2018, 24, 5726-5730.

240

Lu, X. L.; Feng, X. D.; Werber, J. R.; Chu, C. C.; Zucker, I.; Kim, J. -H.; Osuji, C. O.; Elimelech, M. Enhanced antibacterial activity through the controlled alignment of graphene oxide nanosheets. Proc. Natl. Acad. Sci. USA 2017, E9793-E9801.

241

Tang, Z.; Zhao, L.; Yang, Z.; Liu, Z.; Gu, J.; Bai, B.; Liu, J.; Xu, J.; Yang, H. Mechanisms of oxidative stress, apoptosis, and autophagy involved in graphene oxide nanomaterial anti-osteosarcoma effect. Int. J. Nanomed. 2018, 13, 2907-2919.

242

Simsikova, M.; Sikola, T. Interaction of graphene oxide with proteins and applications of their conjugates. J. Nanomed. Res 2017, 5, 00109.

243

Lee, D. Y.; Khatun, Z.; Lee, J. -H.; Lee, Y. -K.; In, I. Blood compatible graphene/heparin conjugate through noncovalent chemistry. Biomacromolecules 2011, 12, 336-341.

244

Hashim, N. C.; Rafie, S. M. M.; Ismail, N. S.; Nordin, D. Effect of the interaction of graphene oxide nanoparticles on a biological model cell membrane. Eurasian J. Anal. Chem. 2018, 13. DOI: 10.29333/ejac/97221.

245

Frost, R.; Jönsson, G. E.; Chakarov, D.; Svedhem, S.; Kasemo, B. Graphene oxide and lipid membranes: Interactions and nanocomposite structures. Nano Lett. 2012, 12, 3356-3362.

246

Chen, J. L.; Zhou, G. Q.; Chen, L.; Wang, Y.; Wang, X. G.; Zeng, S. W. Interaction of graphene and its oxide with lipid membrane: A molecular dynamics simulation study. J. Phys. Chem. C 2016, 120, 6225-6231.

247

Duan, G. X.; Zhang, Y. Z.; Luan, B. Q.; Weber, J. K.; Zhou, R. W.; Yang, Z. X.; Zhao, L.; Xu, J. Y.; Luo, J. D.; Zhou, R. H. Graphene-induced pore formation on cell membranes. Sci. Rep. 2017, 7, 42767.

248

Banerjee, A. N. Prospects and challenges of graphene-based nanomaterials in nanomedicine. Glob. J. Nano. 2016, 1, 555552.

249

Snitka, V. Graphene based materials: Opportunities and challenges in nanomedicine. J. Nanomed. Res. 2015, 2, 00035.

Publication history
Copyright
Acknowledgements

Publication history

Received: 22 October 2018
Revised: 12 January 2019
Accepted: 15 January 2019
Published: 04 March 2019
Issue date: May 2019

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Acknowledgements

Acknowledgements

The authors would like to acknowledge the funding from the Ministry of Education Malaysia in the form of FRGS (RDU160118: FRGS/1/2016/STG07/UMP/02/3, RDU170113: FRGS/1/2017/STG07/UMP/01/1), Universiti Malaysia Pahang grant RDU170357 and King Khalid University, the Ministry of Education in Saudi Arabia for supporting this research through grant (RCAMS/KKU/002-18) under research center for advanced material science.

Return