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Graphene-based nanomaterials have emerged as a novel type of materials with exceptional physicochemical properties and numerous applications in various areas. In this review, we summarize recent advances in studying interactions between graphene and biosystems. We first provide a brief introduction on graphene and its derivatives, and then discuss on the toxicology and biocompatibility of graphene, including the extracellular interactions between graphene and biomacromolecules, cellular studies of graphene, and in vivo toxicological effects. Next, we focus on various graphene-based practical applications in antibacterial materials, wound addressing, drug delivery, and water purification. We finally present perspectives on challenges and future developments in these exciting fields.


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Graphene-based nanomaterials in biosystems

Show Author's information Na Lu1Liqian Wang2Min Lv2Zisheng Tang3,4,5( )Chunhai Fan2,6( )
School of Materials Engineering,Shanghai University of Engineering Science,Shanghai,201620,China;
Division of Physical Biology and Bioimaging Center,Shanghai Synchrotron Radiation Facility, CAS Key Laboratory of Interfacial Physics and Technology, Shanghai Institute of Applied Physics, Chinese Academy of Sciences,Shanghai,201800,China;
Department of Endodontics,Shanghai Ninth People's Hospital, College of Stomatology, Shanghai Jiao Tong University School of Medicine,Shanghai,200011,China;
National Clinical Research Center of Oral Diseases,Shanghai,200011,China;
Shanghai Key Laboratory of Stomatology & Shanghai Research Institute of Stomatology,Shanghai,200011,China;
School of Chemistry and Chemical Engineering,Institute of Molecular Medicine, Renji Hospital, School of Medicine, Shanghai Jiao Tong University,Shanghai,200240,China;

Abstract

Graphene-based nanomaterials have emerged as a novel type of materials with exceptional physicochemical properties and numerous applications in various areas. In this review, we summarize recent advances in studying interactions between graphene and biosystems. We first provide a brief introduction on graphene and its derivatives, and then discuss on the toxicology and biocompatibility of graphene, including the extracellular interactions between graphene and biomacromolecules, cellular studies of graphene, and in vivo toxicological effects. Next, we focus on various graphene-based practical applications in antibacterial materials, wound addressing, drug delivery, and water purification. We finally present perspectives on challenges and future developments in these exciting fields.

Keywords: graphene-based nanomaterials, toxicology and biocompatibility, biomacromolecules, cells, living entities, applications

References(202)

1

Novoselov, K. S.; Geim, A. K.; Morozov, S. V.; Jiang, D.; Zhang, Y.; Dubonos, S. V.; Grigorieva, I. V.; Firsov, A. A. Electric field effect in atomically thin carbon films. Science 2004, 306, 666–669.

2

Huang, X.; Yin, Z. Y.; Wu, S. X.; Qi, X. Y.; He, Q. Y.; Zhang, Q. C.; Yan, Q. Y.; Boey, F.; Zhang, H. Graphene-based materials: Synthesis, characterization, properties, and applications. Small 2011, 7, 1876–1902.

3

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

4

Tang, L.H.; Wang, Y.; Li, J. H. The graphene/nucleic acid nanobiointerface. Chem. Soc. Rev. 2015, 44, 6954–6580.

5

Zheng, H. Z.; Ma, R. L.; Gao, M.; Tian, X.; Li, Y. Q.; Zeng, L. W.; Li, R. B. Antibacterial applications of graphene oxides: Structure-activity relationships, molecular initiating events and biosafety. Sci. Bull. 2018, 63, 133–142.

6

Park, S.; Ruoff, R. S. Chemical methods for the production of graphenes. Nat. Nanotechnol. 2009, 4, 217–224.

7

Ponomarenko, L. A.; Schedin, F.; Katsnelson, M. I.; Yang, R.; Hill, E. W.; Novoselov, K. S.; Geim, A. K. Chaotic dirac billiard in graphene quantum dots. Science 2008, 320, 356–358.

8

Slota, M.; Keerthi, A.; Myers, W. K.; Tretyakov, E.; Baumgarten, M.; Ardavan, A.; Sadeghi, H.; Lambert, C. J.; Narita, A.; Müllen, K. et al. Magnetic edge states and coherent manipulation of graphene nanoribbons. Nature 2018, 557, 691–695.

9

Rozpłoch, F.; Patyk, J.; Stankowski, J. Graphenes bonding forces in graphite. Acta Phys. Pol. A 2007, 112, 557–562.

10

Hernandez, Y.; Nicolosi, V.; Lotya, M.; Blighe, F. M.; Sun, Z. Y.; De, S.; McGovern, I. T.; Holland, B.; Byrne, M.; Gun'Ko, Y. K. et al. High-yield production of graphene by liquid-phase exfoliation of graphite. Nat. Nanotechnol. 2008, 3, 563–568.

11

Kim, K. S.; Zhao, Y.; Jang, H.; Lee, S. Y.; Kim, J. M.; Kim, K. S.; Ahn, J. H.; Kim, P.; Choi, J. Y.; Hong, B. H. Large-scale pattern growth of graphene films for stretchable transparent electrodes. Nature 2009, 457, 706–710.

12

Bae, S.; Kim, H.; Lee, Y.; Xu, X. F.; Park, J. S.; Zheng, Y.; Balakrishnan, J.; Lei, T.; Kim, H. R.; Song, Y. I. et al. Roll-to-roll production of 30-inch graphene films for transparent electrodes. Nat. Nanotechnol. 2010, 5, 574–578.

13

Chen, C. Y.; Avila, J.; Arezki, H.; Nguyen, V. L.; Shen, J. H.; Mucha- Kruczyński, M.; Yao, F.; Boutchich, M.; Chen, Y.; Lee, Y. H. et al. Large local lattice expansion in graphene adlayers grown on copper. Nat. Mater. 2018, 17, 450–455.

14

Berger, C.; Song, Z. M.; Li, X. B.; Wu, X. S.; Brown, N.; Naud, C.; Mayou, D.; Li, T. B.; Hass, J.; Marchenkov, A. N. et al. Electronic confinement and coherence in patterned epitaxial graphene. Science 2006, 312, 1191–1196.

15

Zhang, L. C.; Shi, Z. W.; Liu, D. H.; Yang, R.; Shi, D. X.; Zhang, G. Y. Vapour-phase graphene epitaxy at low temperatures. Nano Res. 2012, 5, 258–264.

16

Shao, Y.; Liu, Z. L.; Cheng, C.; Wu, X.; Liu, H.; Liu, C.; Wang, J. O.; Zhu, S. Y.; Wang, Y. Q.; Shi, D. X. et al. Epitaxial growth of flat antimonene monolayer: A new honeycomb analogue of graphene. Nano Lett. 2018, 18, 2133–2139.

17

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

18

Dikin, D. A.; Stankovich, S.; Zimney, E. J.; Piner, R. D.; Dommett, G. H. B.; Evmenenko, G.; Nguyen, S. T.; Ruoff, R. S. Preparation and characterization of graphene oxide paper. Nature 2007, 448, 457–460.

19

Marcano, D. C.; Kosynkin, D. V.; Berlin, J. M.; Sinitskii, A.; Sun, Z. Z.; Slesarev, A.; Alemany, L. B.; Lu, W.; Tour, J. M. Improved synthesis of graphene oxide. ACS Nano 2010, 4, 4806–4814.

20

Li, D.; Müller, M. B.; Gilje, S.; Kaner, R. B.; Wallace, G. G. Processable aqueous dispersions of graphene nanosheets. Nat. Nanotechnol. 2008, 3, 101–105.

21

Voiry, D.; Yang, J.; Kupferberg, J.; Fullon, R.; Lee, C.; Jeong, H. Y.; Shin, H. S.; Chhowalla, M. High-quality graphene via microwave reduction of solution-exfoliated graphene oxide. Science 2016, 353, 1413–1416.

22

Nam, J. M.; Thaxton, C. S.; Mirkin, C. A. Nanoparticle-based bio-bar codes for the ultrasensitive detection of proteins. Science 2003, 301, 1884–1886.

23

Wang, P. J.; Wan, Y.; Ali, A.; Deng, S. Y.; Su, Y.; Fan, C. H.; Yang, S. L. Aptamer-wrapped gold nanoparticles for the colorimetric detection of omethoate. Sci. China Chem. 2016, 59, 237–242.

24

Katz, E.; Willner, I. Integrated nanoparticle-biomolecule hybrid systems: Synthesis, properties, and applications. Angew. Chem. , Int. Ed. 2004, 43, 6042–6108.

25

Xu, Y.; Zhao, Y.; Zhang, Y. J.; Cui, Z. F.; Wang, L. H.; Fan, C. H.; Gao, J. M.; Sun, Y. H. Angiopep-2-conjugated Ag2S quantum dot for NIR-Ⅱ imaging of brain tumors. Acta Chim. Sin. 2018, 76, 393–399.

26

Cui, X. H.; Chen, H. Y.; Yang, T. Research progress on the preparation and application of nano-sized molybdenum disulfide. Acta Chim. Sin. 2016, 74, 392–400.

27

Lu, N.; Gao, A. R.; Dai, P. F.; Song, S. P.; Fan, C. H.; Wang, Y. L.; Li, T. CMOS-compatible silicon nanowire field-effect transistors for ultrasensitive and label-free microRNAs sensing. Small 2014, 10, 2022–2028.

28

Ramanathan, T.; Abdala, A. A.; Stankovich, S.; Dikin, D. A.; Herrera- Alonso, M.; Piner, R. D.; Adamson, D. H.; Schniepp, H. C.; Chen, X.; Ruoff, R. S. et al. Functionalized graphene sheets for polymer nanocomposites. Nat. Nanotechnol. 2008, 3, 327–331.

29

Stuart, M. A. C.; Huck, W. T. S.; Genzer, J.; Müller, M.; Ober, C.; Stamm, M.; Sukhorukov, G. B.; Szleifer, I.; Tsukruk, V. V.; Urban, M. et al. Emerging applications of stimuli-responsive polymer materials. Nat. Mater. 2010, 9, 101–113.

30

Huang, X.; Qi, X. Y.; Boey, F.; Zhang, H. Graphene-based composites. Chem. Soc. Rev. 2012, 41, 666–686.

31

Muszynski, R.; Seger, B.; Kamat, P. V. Decorating graphene sheets with gold nanoparticles. J. Phys. Chem. C 2008, 112, 5263–5266.

32

Cao, A. N.; Liu, Z.; Chu, S. S.; Wu, M. H.; Ye, Z. M.; Cai, Z. W.; Chang, Y. L.; Wang, S. F.; Gong, Q. H.; Liu, Y. F. A facile one-step method to produce graphene-CdS quantum dot nanocomposites as promising optoelectronic materials. Adv. Mater. 2010, 22, 103–106.

33

Ji, H. W.; Sun, H. J.; Qu, X. G. Antibacterial applications of graphene- based nanomaterials: Recent achievements and challenges. Adv. Drug Deliver. Rev. 2016, 105, 176–189.

34

Liu, J. W.; Cao, Z. H.; Lu, Y. Functional nucleic acid sensors. Chem. Rev. 2009, 109, 1948–1998.

35

Ge, Z. L.; Pei, H.; Wang, L. H.; Song, S. P.; Fan, C. H. Electrochemical single nucleotide polymorphisms genotyping on surface immobilized three-dimensional branched DNA nanostructure. Sci. China Chem. 2011, 54, 1273.

36

Seeman, N. C. DNA in a material world. Nature 2003, 421, 427–431.

37

Zhang, H. Z.; Zhang, Z. Q.; Wang, F.; Zhou, T.; Wang, X. F.; Zhang, G. D.; Liu, T. T.; Liu, S. Z. Application of structural DNA nanotechnology. Acta Phys. Chim. Sin. 2017, 33, 1520–1532.

38

Pinheiro, A. V.; Han, D. R.; Shih, W. M.; Yan, H. Challenges and opportunities for structural DNA nanotechnology. Nat. Nanotechnol. 2011, 6, 763–772.

39

Ye, D. K.; Zuo, X. L.; Fan, C. H. DNA nanostructure-based engineering of the biosensing interface for biomolecular detection. Prog. Chem. 2017, 29, 36–46.

40

Liu, D. G.; Park, S. H.; Reif, J. H.; LaBean, T. H. DNA nanotubes self- assembled from triple-crossover tiles as templates for conductive nanowires. Proc. Natl. Acad. Sci. USA 2004, 101, 717–722.

41

Lin, C. X.; Katilius, E.; Liu, Y.; Zhang, J. P.; Yan, H. Self-assembled signaling aptamer DNA arrays for protein detection. Angew. Chem. , Int. Ed. 2006, 45, 5296–5301.

42

Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440, 297–302.

43

Chao, J.; Zhang, Y. N.; Zhu, D.; Liu, B.; Cui, C. J.; Su, S.; Fan, C. H.; Wang, L. H. Hetero-assembly of gold nanoparticles on a DNA origami template. Sci. China Chem. 2016, 59, 730–734.

44

Han, D. R.; Pal, S.; Nangreave, J.; Deng, Z. T.; Liu, Y.; Yan, H. DNA origami with complex curvatures in three-dimensional space. Science 2011, 332, 342–346.

45

Fan, C. H.; Fang, X. H. Special topic for "single-molecule, single-particle and single-cell bioimaging". Sci. China Chem. 2017, 60, 1265–1266.

46

Gao, Z. S.; Deng, S. H.; Li, J.; Wang, K.; Li, J. J.; Wang, L. H.; Fan, C. H. Sub-diffraction-limit cell imaging using a super-resolution microscope with simplified pulse synchronization. Sci. China Chem. 2017, 60, 1305–1309.

47

Wang, S. P.; Deng, S. H.; Cai, X. Q.; Hou, S. G.; Li, J. J.; Gao, Z. S.; Li, J.; Wang, L. H.; Fan, C. H. Superresolution imaging of telomeres with continuous wave stimulated emission depletion (STED) microscope. Sci. China Chem. 2016, 59, 1519–1524.

48

Liu, Q.; Sun, Y.; Yang, T. S.; Feng, W.; Li, C. G.; Li, F. Y. Sub-10 nm hexagonal lanthanide-doped NaLuF4 upconversion nanocrystals for sensitive bioimaging in vivo. J. Am. Chem. Soc. 2016, 133, 17122–17125.

49

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

50

Dreaden, E. C.; Alkilany, A. M.; Huang, X. H.; Murphy, C. J.; El-Sayed, M. A. The golden age: Gold nanoparticles for biomedicine. Chem. Soc. Rev. 2012, 41, 2740–2779.

51

Su, Y. Y.; Peng, T. H.; Xing, F. F.; Li, D.; Fan, C. H. Nanoplasmonic biological sensing and imaging. Acta Chim. Sin. 2017, 75, 1036–1046.

52

Long, Y. T.; Fan, C. H. Nanosensors. Acta Chim. Sin. 2017, 75, 1021–1022.

53

Chao, J.; Fan, C. H. A photoelectrochemical sensing strategy for biomolecular detection. Sci. China Chem. 2015, 58, 834.

54

Patil, A. J.; Vickery, J. L.; Scott, T. B.; Mann, S. Aqueous stabilization and self-assembly of graphene sheets into layered bio-nanocomposites using DNA. Adv. Mater. 2009, 21, 3159–3164.

55

Lu, C. H.; Yang, H. H.; Zhu, C. L.; Chen, X.; Chen, G. N. A graphene platform for sensing biomolecules. Angew. Chem. , Int. Ed. 2009, 48, 4785–4787.

56

He, S. J.; Song, B.; Li, D.; Zhu, C. F.; Qi, W. P.; Wen, Y. Q.; Wang, L. H.; Song, S. P.; Fang, H. P.; Fan, C. A graphene nanoprobe for rapid, sensitive, and multicolor fluorescent DNA analysis. Adv. Funct. Mater. 2010, 20, 453–459.

57

Chang, H. X.; Tang, L. H.; Wang, Y.; Jiang, J. H.; Li, J. H. Graphene fluorescence resonance energy transfer aptasensor for the thrombin detection. Anal. Chem. 2010, 82, 2341–2346.

58

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.

59

Kotikam, V.; Fernandes, M.; Kumar, V. A. Comparing the interactions of DNA, polyamide (PNA) and polycarbamate nucleic acid (PCNA) oligomers with graphene oxide (GO). Phys. Chem. Chem. Phys. 2012, 14, 15003–15006.

60

Cui, L.; Chen, Z. R.; Zhu, Z.; Lin, X. Y.; Chen, X.; Yang, C. J. Stabilization of ssRNA on graphene oxide surface: An effective way to design highly robust RNA probes. Anal. Chem. 2013, 85, 2269–2275.

61

Zhang, H.; Jia, S. S.; Lv, M.; Shi, J. Y.; Zuo, X. L.; Su, S.; Wang, L. H.; Huang, W.; Fan, C. H.; Huang, Q. Size-dependent programming of the dynamic range of graphene oxide-DNA interaction-based ion sensors. Anal. Chem. 2014, 86, 4047–4051.

62

Xu, S. C.; Zhan, J.; Man, B. Y.; Jiang, S. Z.; Yue, W. W.; Gao, S. B.; Guo, C. G.; Liu, H. P.; Li, Z. H.; Wang, J. H. et al. Real-time reliable determination of binding kinetics of DNA hybridization using a multi-channel graphene biosensor. Nat. Commun. 2017, 8, 14902.

63

Heerema, S. J.; Vicarelli, L.; Pud, S.; Schouten, R. N.; Zandbergen, H. W.; Dekker, C. Probing DNA translocations with inplane current signals in a graphene nanoribbon with a nanopore. ACS Nano 2018, 12, 2623–2633.

64

Pei, H.; Li, J.; Lv, M.; Wang, J. Y.; Gao, J. M.; Lu, J. X.; Li, Y. P.; Huang, Q.; Hu, J.; Fan, C. H. A graphene-based sensor array for high-precision and adaptive target identification with ensemble aptamers. J. Am. Chem. Soc. 2012, 134, 13843–13849.

65

Feng, L. Y.; Li, W.; Ren, J. S.; Qu, X. G. Electrochemically and DNA- triggered cell release from ferrocene/β-cyclodextrin and aptamer modified dualfunctionalized graphene substrate. Nano Res. 2015, 8, 887–899.

66

Liu, M.; Song, J. P.; Shuang, S. M.; Dong, C.; Brennan, J. D.; Li, Y. F. A graphene-based biosensing platform based on the release of DNA probes and rolling circle amplification. ACS Nano 2014, 8, 5564–5573.

67

Liu, S. Z.; Zhang, Z. Q.; Wang, F.; Zhou, T.; Wang, X. F.; Zhang, G. D.; Liu, T. T.; Zhang, H. Z. Study on the synthesis of DNA via rolling circle amplification. Acta Phys. Chim. Sin 2017, 33, 2052–2057.

68

Li, F.; Liu, X. G.; Zhao, B.; Yan, J.; Li, Q.; Aldalbahi, A.; Shi, J. Y.; Song, S. P.; Fan, C. H.; Wang, L. H. Graphene nanoprobes for real-time monitoring of isothermal nucleic acid amplification. ACS Appl. Mater. Interfaces 2017, 9, 15245–15253.

69

Liu, X. Q.; Aizen, R.; Freeman, R.; Yehezkeli, O.; Willner, I. Multiplexed aptasensors and amplified DNA sensors using functionalized graphene oxide: Application for logic gate operations. ACS Nano 2012, 6, 3553–3563.

70

Tian, Y.; Wang, Y.; Xu, Y.; Liu, Y.; Li, D.; Fan, C. H. A highly sensitive chemiluminescence sensor for detecting mercury (Ⅱ) ions: A combination of Exonuclease Ⅲ-aided signal amplification and graphene oxide-assisted background reduction. Sci. China Chem 2015, 58, 514–518.

71

Gowtham, S.; Scheicher, R. H.; Ahuja, R.; Pandey, R.; Karna, S. P. Physisorption of nucleobases on graphene: Density-functional calculations. Phys. Rev. B 2007, 76, 033401.

72

Varghese, N.; Mogera, U.; Govindaraj, A.; Das, A.; Maiti, P. K.; Sood, A. K.; Rao, C. N. R. Binding of DNA nucleobases and nucleosides with graphene. Chemphyschem 2009, 10, 206–210.

73

Panigrahi, S.; Bhattacharya, A.; Banerjee, S.; Bhattacharyya, D. Interaction of nucleobases with wrinkled graphene surface: Dispersion corrected DFT and AFM studies. J. Phys. Chem. C 2012, 116, 4374–4379.

74

Zhang, Y. Y.; Li, M.; Li, Z. H.; Li, Q.; Aldalbahi, A.; Shi, J. Y.; Wang, L. H.; Fan, C. H.; Zuo, X. L. Recognizing single phospholipid vesicle collisions on carbon fiber nanoelectrode. Sci. China Chem. 2017, 60, 1474–1480.

75

Duan, X. X.; Li, Y.; Rajan, N. K.; Routenberg, D. A.; Modis, Y.; Reed, M. A. Quantification of the affinities and kinetics of protein interactions using silicon nanowire biosensors. Nat. Nanotechnol. 2012, 7, 401–407.

76

Li, J.; Kuang, Y.; Shi, J. F.; Zhou, J.; Medina, J. E.; Zhou, R.; Yuan, D.; Yang, C. H.; Wang, H. M.; Yang, Z. M. et al. Enzyme-instructed intracellular molecular self-assembly to boost activity of cisplatin against drug-resistant ovarian cancer cells. Angew. Chem. , Int. Ed. 2015, 127, 13505–13509.

77

Jung, J. H.; Cheon, D. S.; Liu, F.; Lee, K. B.; Seo, T. S. A graphene oxide based immuno-biosensor for pathogen detection. Angew. Chem. , Int. Ed. Int. Ed. 2010, 49, 5708–5711.

78

Wang, L. H.; Pu, K. Y.; Li, J.; Qi, X. Y.; Li, H.; Zhang, H.; Fan, C. H.; Liu, B. A graphene-conjugated oligomer hybrid probe for light-up sensing of lectin and Escherichia coli. Adv. Mater. 2011, 23, 4386–4391.

79

Chou, S. S.; De, M.; Luo, J. Y.; Rotello, V. M.; Huang, J. X.; Dravid, V. P. Nanoscale graphene oxide (nGO) as artificial receptors: Implications for biomolecular interactions and sensing. J. Am. Chem. Soc. 2012, 134, 16725–16733.

80

Tan, X. F.; Feng, L. Z.; Zhang, J.; Yang, K.; Zhang, S.; Liu, Z.; Peng, R. Functionalization of graphene oxide generates a unique interface for selective serum protein interactions. ACS Appl. Mater. Interaces 2013, 5, 1370–1377.

81

Gan, S. Y.; Zhong, L. J.; Han, D. X.; Niu, L.; Chi, Q. J. Probing bio-nano interactions between blood proteins and monolayer-stabilized graphene sheets. Small 2015, 11, 5814–5825.

82

Feng, B. Y.; Guo, L. J.; Wang, L. H.; Li, F.; Lu, J. X.; Gao, J. M.; Fan, C. H.; Huang, Q. A graphene oxide-based fluorescent biosensor for the analysis of peptide-receptor interactions and imaging in somatostatin receptor subtype 2 overexpressed tumor cells. Anal. Chem. 2013, 85, 7732–7737.

83

Zou, X. Q.; Wei, S.; Jasensky, J.; Xiao, M. Y.; Wang, Q. M.; Brooks, C. L.; Chen, Z. Molecular interactions between graphene and biological molecules. J. Am. Chem. Soc. 2017, 139, 1928–1936.

84

Chen, Y. J.; Chen, Z. H.; Sun, Y. X.; Lei, J. T.; Wei, G. H. Mechanistic insights into the inhibition and size effects of graphene oxide nanosheets on the aggregation of an amyloid-β peptide fragment. Nanoscale 2018, 10, 8989–8997.

85

Jang, H.; Ryoo, S. R.; Kim, Y. K.; Yoon, S.; Kim, H.; Han, S. W.; Choi, B. S.; Kim, D. E.; Min, D. H. Discovery of hepatitis C virus NS3 helicase inhibitors by a multiplexed, high-throughput helicase activity assay based on graphene oxide. Angew. Chem. , Int. Ed. 2013, 52, 2340–2344.

86

Song, Z. Y.; Wang, X. Y.; Zhu, G. X.; Nian, Q. G.; Zhou, H. Y.; Yang, D.; Qin, C. F.; Tang, R. K. Virus capture and destruction by label-free graphene oxide for detection and disinfection applications. Small 2015, 11, 1171–1176.

87

Deokar, A. R.; Nagvenkar, A. P.; Kalt, I.; Shani, L.; Yeshurun, Y.; Gedanken, A.; Sarid, R. Graphene-based "hot plate" for the capture and destruction of the herpes simplex virus type 1. Bioconjugate Chem. 2017, 28, 1115–1122.

88

Sametband, M.; Kalt, I.; Gedanken, A.; Sarid, R. Herpes simplex virus type-1 attachment inhibition by functionalized graphene oxide. ACS Appl. Mater. Interfaces 2014, 6, 1228–1235.

89

Gholami, M. F.; Lauster, D.; Ludwig, K.; Storm, J.; Ziem, B.; Severin, N.; Böttcher, C.; Rabe, J. P.; Herrmann, A.; Adeli, M. et al. Functionalized graphene as extracellular matrix mimics: Toward well-defined 2D nanomaterials for multivalent virus interactions. Adv. Funct. Mater. 2017, 27, 1606477.

90

Zhan, L.; Li, C. M.; Wu, W. B.; Huang, C. Z. A colorimetric immunoassay for respiratory syncytial virus detection based on gold nanoparticles- graphene oxide hybrids with mercury-enhanced peroxidase-like activity. Chem. Commun. 2014, 50, 11526–11528.

91

Afsahi, S.; Lerner, M. B.; Goldstein, J. M.; Lee, J.; Tang, X. L.; Bagarozzi, D. A. Jr.; Pan, D.; Locascio, L.; Walker, A.; Barron, F. et al. Novel graphene-based biosensor for early detection of Zika virus infection. Biosens. Bioelectron. 2018, 100, 85–88.

92

Lee, Y. M.; Jung, B.; Kim, Y. H.; Park, A. R.; Han, S.; Choe, W. S.; Yoo, P. J. Nanomesh-structured ultrathin membranes harnessing the unidirectional alignment of viruses on a graphene-oxide film. Adv. Mater. 2014, 26, 3899–3904.

93

Chen, H. Q.; Müller, M. B.; Gilmore, K. J.; Wallace, G. G.; Li, D. Mechanically strong, electrically conductive, and biocompatible graphene paper. Adv. Mater. 2008, 20, 3557–3561.

94

Lee, W. C.; Lim, C. H. Y. X.; Shi, H.; Tang, L. A. L.; 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.

95

Rastogi, S. K.; Raghavan, G.; Yang, G.; Cohen-Karni, T. Effect of graphene on nonneuronal and neuronal cell viability and stress. Nano Lett. 2017, 17, 3297–3301.

96

Guo, C. X.; Zheng, X. T.; Lu, Z. S.; Lou, X. W.; Li, C. M. Biointerface by cell growth on layered graphene-artificial peroxidase-protein nanostructure for in situ quantitative molecular detection. Adv. Mater. 2010, 22, 5164–5167.

97

Bardhan, N. M.; Kumar, P. V.; Li, Z. Y.; Ploegh, H. L.; Grossman, J. C.; Belcher, A. M.; Chen, G. Y. Enhanced cell capture on functionalized graphene oxide nanosheets through oxygen clustering. ACS Nano 2017, 11, 1548–1558.

98

Shah, S.; Yin, P. T.; Uehara, T. M.; Chueng, S. T. D.; Yang, L. T.; Lee, K. B. Guiding stem cell differentiation into oligodendrocytes using graphene- nanofiber hybrid scaffolds. Adv. Mater. 2014, 26, 3673–3680.

99

Li, W.; Wang, J. S.; Ren, J. S.; Qu, X. G. 3D graphene oxide-polymer hydrogel: Near-infrared light-triggered active scaffold for reversible cell capture and on-demand release. Adv. Mater. 2013, 25, 6737–6743.

100

Lu, J. Y.; Zhang, X. X.; Zhu, Q. Y.; Zhang, F. R.; Huang, W. T.; Ding, X. Z.; Xia, L. Q.; Luo, H. Q.; Li, N. B. Highly tunable and scalable fabrication of 3D flexible graphene micropatterns for directing cell alignment. ACS Appl. Mater. Interfaces 2018, 10, 17704–17713.

101

Chang, Y. L.; Yang, S. T.; Liu, J. H.; Dong, E. Y.; Wang, Y. W.; Cao, A. N.; Liu, Y. F.; Wang, H. F. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett 2011, 200, 201–210.

102

Chong, Y.; Ma, Y. F.; Shen, H.; Tu, X. L.; Zhou, X.; Xu, J. Y.; Dai, J. W.; Fan, S. J.; Zhang, Z. J. The in vitro and in vivo toxicity of graphene quantum dots. Biomaterials 2014, 35, 5041–5048.

103

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.

104

Vallabani, N. V. S.; 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.

105

Hu, W. B.; Peng, C.; Lv, M.; Li, X. M.; Zhang, Y. J.; Chen, N.; Fan, C. H.; Huang, Q. Protein corona-mediated mitigation of cytotoxicity of graphene oxide. ACS Nano 2011, 5, 3693–3700.

106

Chong, Y.; Ge, C. C.; Yang, Z. X.; Garate, J. A.; Gu, Z. L.; Weber, J. K.; Liu, J. J.; Zhou, R. H. Reduced cytotoxicity of graphene nanosheets mediated by blood-protein coating. ACS Nano 2015, 9, 5713–5724.

107

Zhang, H.; Cheng, P.; Yang, J. Z.; Lv, M.; Liu, R.; He, D. N.; Fan, C. H.; Huang, Q. Uniform ultrasmall graphene oxide nanosheets with low cytotoxicity and high cellular uptake. ACS Appl. Mater. Interfaces 2013, 5, 1761–1767.

108

Mittal, S.; Kumar, V.; Dhiman, N.; Chauhan, L. K. S.; Pasricha, R.; Pandey, A. K. Physico-chemical properties based differential toxicity of graphene oxide/reduced graphene oxide in human lung cells mediated through oxidative stress. Sci. Rep. 2016, 6, 39548.

109

Vranic, S.; Rodrigues, A. F.; Buggio, M.; Newman, L.; White, M. R. H.; Spiller, D. G.; Bussy, C.; Kostarelos, K. Live imaging of label-free graphene oxide reveals critical factors causing oxidative-stress-mediated cellular responses. ACS Nano 2018, 12, 1373–1389.

110

Li, R. B.; Guiney, L. M.; Chang, C. H.; Mansukhani, N. D.; Ji, Z. X.; Wang, X.; Liao, Y. P.; Jiang, W.; Sun, B. B.; Hersam, M. C. et al. Surface oxidation of graphene oxide determines membrane damage, lipid peroxidation, and cytotoxicity in macrophages in a pulmonary toxicity model. ACS Nano 2018, 12, 1390–1402.

111

Li, Y.; Liu, Y.; Fu, Y. J.; Wei, T. T.; Le Guyader, L.; Gao, G.; Liu, R. S.; Chang, Y. Z.; Chen, C. Y. The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials 2012, 33, 402–411.

112

Chen, G. Y.; Yang, H. J.; Lu, C. H.; Chao, Y. C.; Hwang, S. M.; Chen, C. L.; Lo, K. W.; Sung, L. Y.; Luo, W. Y.; Tuan, H. Y. et al. Simultaneous induction of autophagy and toll-like receptor signaling pathways by graphene oxide. Biomaterials 2012, 33, 6559–6569.

113

Wang, L.; Li, X. M.; Han, Y. P.; Wang, T.; Zhao, Y.; Ali, A.; El-Sayed, N. N.; Shi, J. Y.; Wang, W. F.; Fan, C. H. et al. Quantum dots protect against MPP+-induced neurotoxicity in a cell model of Parkinson's disease through autophagy induction. Sci. China Chem. 2016, 59, 1486–1491.

114

Pieper, H.; Chercheja, S.; Eigler, S.; Halbig, C. E.; Filipovic, M. R.; Mokhir, A. Endoperoxides revealed as origin of the toxicity of graphene oxide. Angew. Chem. , Int. Ed. 2016, 55, 405–407.

115

Zhu, J. Q.; Xu, M.; Gao, M.; Zhang, Z. H.; Xu, Y.; Xia, T.; Liu, S. J. Graphene oxide-induced perturbation to plasma membrane and cytoskeletal meshwork sensitize cancer cells to chemotherapeutic agents. ACS Nano 2017, 11, 2637–2651.

116

Zhang, W. D.; Wang, C.; Li, Z. J.; Lu, Z. Z.; Li, Y. Y.; Yin, J. J.; Zhou, Y. T.; Gao, X. F.; Fang, Y.; Nie, G. et al. Unraveling stress-induced toxicity properties of graphene oxide and the underlying mechanism. Adv. Mater. 2012, 24, 5391–5397.

117

Zhang, X. Y.; Yin, J. L.; Peng, C.; Hu, W. Q.; Zhu, Z. Y.; Li, W. X.; Fan, C. H.; Huang, Q. Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon 2011, 49, 986–995.

118

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

119

Li, B.; Zhang, X. Y.; Yang, J. Z.; Zhang, Y. J.; Li, W. X.; Fan, C. H.; Huang, Q. Influence of polyethylene glycol coating on biodistribution and toxicity of nanoscale graphene oxide in mice after intravenous injection. Int. J. Nanomedicine 2014, 9, 4697–4707.

120

Zhang, S.; Yang, K.; Feng, L. Z.; Liu, Z. In vitro and in vivo behaviors of dextran functionalized graphene. Carbon 2011, 49, 4040–4049.

121

Yang, K.; Gong, H.; Shi, X. Z.; Wan, J. M.; Zhang, Y. J.; Liu, Z. In vivo biodistribution and toxicology of functionalized nano-graphene oxide in mice after oral and intraperitoneal administration. Biomaterials 2013, 34, 2787–2795.

122

Syama, S.; Paul, W.; Sabareeswaran, A.; Mohanan, P. V. Raman spectroscopy for the detection of organ distribution and clearance of PEGylated reduced graphene oxide and biological consequences. Biomaterials 2017, 131, 121–130.

123

Nurunnabi, M.; Khatun, Z.; Huh, K. M.; Park, S. Y.; Lee, D. Y.; Cho, K. J.; Lee, Y. K. In vivo biodistribution and toxicology of carboxylated graphene quantum dots. ACS Nano 2013, 7, 6858–6867.

124

Ema, M.; Gamo, M.; Honda, K. A review of toxicity studies on graphene- based nanomaterials in laboratory animals. Regul. Toxicol. Pharmacol. 2017, 85, 7–24.

125

Gollavelli, G.; Ling, Y. C. Multi-functional graphene as an in vitro and in vivo imaging probe. Biomaterials 2012, 33, 2532–2545.

126

Akhavan, O.; Ghaderi, E.; Rahimi, K. Adverse effects of graphene incorporated in TiO2 photocatalyst on minuscule animals under solar light irradiation. J. Mater. Chem. 2012, 22, 23260–23266.

127

Xu, S.; Zhang, Z. Y.; Chu, M. Q. Long-term toxicity of reduced graphene oxide nanosheets: Effects on female mouse reproductive ability and offspring development. Biomaterials 2015, 54, 188–200.

128

Ma, J.; Liu, R.; Wang, X.; Liu, Q.; Chen, Y.; Valle, R. P.; Zuo, Y. Y.; Xia, T.; Liu, S. J. Crucial role of lateral size for graphene oxide in activating macrophages and stimulating pro-inflammatory responses in cells and animals. ACS Nano 2015, 9, 10498–10515.

129

Begum, P.; Ikhtiari, R.; Fugetsu, B. Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. Carbon 2011, 49, 3907–3919.

130

Zhang, P.; Zhang, R. R.; Fang, X. Z.; Song, T. Q.; Cai, X. D.; Liu, H. J.; Du, S. T. Toxic effects of graphene on the growth and nutritional levels of wheat (Triticum aestivum L. ): Short- and long-term exposure studies. J. Hazard. Mater. 2016, 317, 543–551.

131

Wang, Q. Q.; Zhao, S. Q.; Zhao, Y. L.; Rui, Q.; Wang, D. Y. Toxicity and translocation of graphene oxide in Arabidopsis plants under stress conditions. RSC Adv. 2014, 4, 60891–60901.

132

Zhao, S. Q.; Wang, Q. Q.; Zhao, Y. L.; Rui, Q.; Wang, D. Y. Toxicity and translocation of graphene oxide in Arabidopsis thaliana. Environ. Toxicol. Pharmacol. 2015, 39, 145–156.

133

Chen, L. Y.; Wang, C. L.; Li, H. L.; Qu, X. L.; Yang, S. T.; Chang, X. L. Bioaccumulation and toxicity of 13C-skeleton labeled graphene oxide in wheat. Environ. Sci. Technol. 2017, 51, 10146–10153.

134

Zhang, J. Y.; Liu, L. L.; Ren, L.; Feng, W. M.; Lv, P.; Wu, W.; Yan, Y. C. The single and joint toxicity effects of chlorpyrifos and beta-cypermethrin in zebrafish (Danio rerio) early life stages. J. Hazard. Mater. 2017, 334, 121–131.

135

Lopes, S.; Pinheiro, C.; Soares, A. M. V. M.; Loureiro, S. Joint toxicity prediction of nanoparticles and ionic counterparts: Simulating toxicity under a fate scenario. J. Hazard. Mater. 2016, 320, 1–9.

136

Hu, W. B.; Peng, C.; Luo, W. J.; Lv, M.; Li, X. M.; Li, D.; Huang, Q.; Fan, C. H. Graphene-based antibacterial paper. ACS Nano 2010, 4, 4317–4323.

137

Akhavan, O.; Ghaderi, E. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 2010, 4, 5731–5736.

138

Liu, S. B.; Zeng, T. H.; Hofmann, M.; Burcombe, E.; Wei, J.; Jiang, R. 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.

139

He, J. L.; Zhu, X. D.; Qi, Z. N.; Wang, C.; Mao, X. J.; Zhu, C. L.; He, Z. Y.; Li, M. Y.; Tang, Z. S. Killing dental pathogens using antibacterial graphene oxide. ACS Appl. Mater. Interfaces 2015, 7, 5605–5611.

140

Liu, S. B.; Hu, M.; Zeng, T. H.; Wu, R.; Jiang, R. R.; Wei, J.; Wang, L.; Kong, J.; Chen, Y. Lateral dimension-dependent antibacterial activity of graphene oxide sheets. Langmuir 2012, 28, 12364–12372.

141

Tu, Y. S.; Lv, M.; Xiu, P.; Huynh, T.; Zhang, M.; Castelli, M.; Liu, Z. R.; Huang, Q.; Fan, C. H.; Fang, H. P. et al. Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nat. Nanotechnol. 2013, 8, 594–601.

142

Perreault, F.; de Faria, A. F.; Nejati, S.; Elimelech, M. Antimicrobial properties of graphene oxide nanosheets: Why size matters. ACS Nano 2015, 9, 7226–7236.

143

Hui, L. W.; Huang, J. L.; Chen, G. X.; Zhu, Y. W.; Yang, L. H. Antibacterial property of graphene quantum dots (both source material and bacterial shape matter). ACS Appl. Mater. Interfaces 2016, 8, 20–25.

144

Kuo, W. S.; Chen, H. H.; Chen, S. Y.; Chang, C. Y.; Chen, P. C.; Hou, Y. I.; Shao, Y. T.; Kao, H. F.; Lilian Hsu, C. L.; Chen, Y. C. et al. Graphene quantum dots with nitrogen-doped content dependence for highly efficient dual-modality photodynamic antimicrobial therapy and bioimaging. Biomaterials 2017, 120, 185–194.

145

Feng, Q. L.; Wu, J.; Chen, G. Q.; Cui, F. Z.; Kim, T. N.; Kim, J. O. A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J. Biomed. Mater. Res. 2000, 52, 662–668.

DOI
146

Das, M. R.; Sarma, R. K.; Borah, S. C.; Kumari, R.; Saikia, R.; Deshmukh, A. B.; Shelke, M. V.; Sengupta, P.; Szunerits, S.; Boukherroub, R. The synthesis of citrate-modified silver nanoparticles in an aqueous suspension of graphene oxide nanosheets and their antibacterial activity. Colloid. Surf. B: Biointerfaces 2013, 105, 128–136.

147

Yu, L.; Zhang, Y. T.; Zhang, B.; Liu, J. D. Enhanced antibacterial activity of silver nanoparticles/halloysite nanotubes/graphene nanocomposites with sandwich-like structure. Sci. Rep. 2014, 4, 4551.

148

Shen, J. F.; Shi, M.; Li, N.; Yan, B.; Ma, H. W.; Hu, Y. Z.; Ye, M. X. Facile synthesis and application of Ag-chemically converted graphene nanocomposite. Nano Res. 2010, 3, 339–349.

149

Prasad, K.; Lekshmi, G. S.; Ostrikov, K.; Lussini, V.; Blinco, J.; Mohandas, M.; Vasilev, K.; Bottle, S.; Bazaka, K.; Ostrikov, K. Synergic bactericidal effects of reduced graphene oxide and silver nanoparticles against Gram-positive and Gram-negative bacteria. Sci. Rep. 2017, 7, 1591.

150

Xu, W. P.; Zhang, L. C.; Li, J. P.; Lu, Y.; Li, H. H.; Ma, Y. N.; Wang, W. D.; Yu, S. H. Facile synthesis of silver@graphene oxide nanocomposites and their enhanced antibacterial properties. J. Mater. Chem. 2011, 21, 4593–4597.

151

Ocsoy, I.; Paret, M. L.; Ocsoy, M. A.; Kunwar, S.; Chen, T.; You, M. X.; Tan, W. H. Nanotechnology in plant disease management: DNA-directed silver nanoparticles on graphene oxide as an antibacterial against Xanthomonas perforans. ACS Nano 2013, 7, 8972–8980.

152

Ocsoy, I.; Gulbakan, B.; Chen, T.; Zhu, G. Z.; Chen, Z.; Sari, M. M.; Peng, L.; Xiong, X. L.; Fang, X. H.; Tan, W. H. DNA-guided metal- nanoparticle formation on graphene oxide surface. Adv. Mater. 2013, 25, 2319–2325.

153

Meng, X. Y.; Wang, H. Y.; Chen, N.; Ding, P.; Shi, H. Y.; Zhai, X.; Su, Y. Y.; He, Y. A graphene–silver nanoparticle–silicon sandwich SERS chip for quantitative detection of molecules and capture, discrimination, and inactivation of bacteria. Anal. Chem. 2018, 90, 5646–5653.

154

Wei, Y. H.; Chen, S.; Kowalczyk, B.; Huda, S.; Gray, T. P.; Grzybowski, B. A. Synthesis of stable, low-dispersity copper nanoparticles and nanorods and their antifungal and catalytic properties. J. Phys. Chem. C 2010, 114, 15612–15616.

155

Lin, D. H.; Qin, T. Q.; Wang, Y. Q.; Sun, X. Y.; Chen, L. X. Graphene oxide wrapped SERS tags: Multifunctional platforms toward optical labeling, photothermal ablation of bacteria, and the monitoring of killing effect. ACS Appl. Mater. Interfaces 2014, 6, 1320–1329.

156

Wang, X. D.; Zhou, N. L.; Yuan, J.; Wang, W. Y.; Tang, Y. D.; Lu, C. Y.; Zhang, J.; Shen, J. Antibacterial and anticoagulation properties of carboxylated graphene oxide-lanthanum complexes. J. Mater. Chem. 2012, 22, 1673–1678.

157

Akhavan, O.; Ghaderi, E. Photocatalytic reduction of graphene oxide nanosheets on TiO2 thin film for photoinactivation of bacteria in solar light irradiation. J. Phys. Chem. C 2009, 113, 20214–20220.

158

Liu, J. C.; Liu, L.; Bai, H. W.; Wang, Y. J.; Sun, D. D. Gram-scale production of graphene oxide-TiO2 nanorod composites: Towards high- activity photocatalytic materials. Appl. Catal. B: Environ. 2011, 106, 76–82.

159

Kim, I. Y.; Park, S.; Kim, H.; Park, S.; Ruoff, R. S.; Hwang, S. J. Strongly-coupled freestanding hybrid films of graphene and layered titanate nanosheets: An effective way to tailor the physicochemical and antibacterial properties of graphene film. Adv. Funct. Mater. 2014, 24, 2288–2294.

160

Santos, C. M.; Tria, M. C. R.; Vergara, R. A. M. V.; Ahmed, F.; Advincula, R. C.; Rodrigues, D. F. Antimicrobial graphene polymer (PVK-GO) nanocomposite films. Chem. Commun. 2011, 47, 8892–8894.

161

Some, S.; Ho, S. M.; Dua, P.; Hwang, E.; Shin, Y. H.; Yoo, H.; Kang, J. S.; Lee, D. K.; Lee, H. Dual functions of highly potent graphene derivative-poly-L-lysine composites to inhibit bacteria and support human cells. ACS Nano 2012, 6, 7151–7161.

162

Li, Y. F.; Yuan, H. Y.; von dem Bussche, A.; Creighton, M.; Hurt, R. H.; Kane, A. B.; Gao, H. J. Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites. Proc. Natl. Acad. Sci. USA 2013, 110, 12295–12300.

163

Pham, V. T. H.; Truong, V. K.; Quinn, M. D. J.; Notley, S. M.; Guo, Y. C.; Baulin, V. A.; Al Kobaisi, M.; Crawford, R. J.; Ivanova, E. P. Graphene induces formation of pores that kill spherical and rod-shaped bacteria. ACS Nano 2015, 9, 8458–8467.

164

Yi, X.; Gao, H. J. Cell interaction with graphene microsheets: Near- orthogonal cutting versus parallel attachment. Nanoscale 2015, 7, 5457–5467.

165

Dallavalle, M.; Calvaresi, M.; Bottoni, A.; Melle-Franco, M.; Zerbetto, F. Graphene can wreak havoc with cell membranes. ACS Appl. Mater. Interfaces 2015, 7, 4406–4414.

166

Mangadlao, J. D.; Santos, C. M.; Felipe, M. J. L.; de Leon, A. C. C.; Rodrigues, D. F.; Advincula, R. C. On the antibacterial mechanism of graphene oxide (GO) Langmuir-Blodgett films. Chem. Commun. 2015, 51, 2886–2889.

167

Hui, L. W.; Piao, J. G.; Auletta, J.; Hu, K.; Zhu, Y. W.; Meyer, T.; Liu, H. T.; Yang, L. H. Availability of the basal planes of graphene oxide determines whether it is antibacterial. ACS Appl. Mater. Interfaces 2014, 6, 13183–13190.

168

Tan, K. H.; Sattari, S.; Donskyi, I. S.; Cuellar-Camacho, J. L.; Cheng, C.; Schwibbert, K.; Lippitz, A.; Unger, W. E. S.; Gorbushina, A.; Adeli, M. et al. Functionalized 2D nanomaterials with switchable binding to investigate graphene-bacteria interactions. Nanoscale 2018, 10, 9525–9537.

169

Lyon, D. Y.; Brunet, L.; Hinkal, G. W.; Wiesner, M. R.; Alvarez, P. J. J. Antibacterial activity of fullerene water suspensions (nC60) is not due to ROS-mediated damage. Nano Lett. 2008, 8, 1539–1543.

170

Niu, A. P.; Han, Y. J.; Wu, J.; Yu, N.; Xu, Q. Synthesis of one- dimensional carbon nanomaterials wrapped by silver nanoparticles and their antibacterial behavior. J. Phys. Chem. C 2010, 114, 12728–12735.

171

West, J. D.; Marnett, L. J. Endogenous reactive intermediates as modulators of cell signaling and cell death. Chem. Res. Toxicol. 2006, 19, 173–194.

172

Gurunathan, S.; Han, J. W.; Dayem, A. A.; Eppakayala, V.; Kim, J. H. Oxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosa. Int. J. Nanomedicine 2012, 7, 5901–5914.

173

Pang, W. C.; Wu, J. L.; Zhang, Q. F.; Li, G. F. Graphene oxide enhanced, radiation cross-linked, vitamin E stabilized oxidation resistant UHMWPE with high hardness and tensile properties. RSC Adv. 2017, 7, 55536–55546.

174

Chen, J. N.; Wang, X. P.; Han, H. Y. A new function of graphene oxide emerges: Inactivating phytopathogenic bacterium Xanthomonas oryzae pv. Oryzae. J. Nanopart. Res. 2013, 15, 1658.

175

Gurunathan, S.; Han, J. W.; Dayem, A. A.; Eppakayala, V.; Park, M. R.; Kwon, D. N.; Kim, J. H. Antibacterial activity of dithiothreitol reduced graphene oxide. J. Ind. Eng. Chem. 2013, 19, 1280–1288.

176

Krishnamoorthy, K.; Veerapandian, M.; Zhang, L. H.; Yun, K.; Kim, S. J. Antibacterial efficiency of graphene nanosheets against pathogenic bacteria via lipid peroxidation. J. Phys. Chem. C 2012, 116, 17280–17287.

177

Giglio, S.; Jiang, J. Y.; Saint, C. P.; Cane, D. E.; Monis, P. T. Isolation and characterization of the gene associated with geosmin production in cyanobacteria. Environ. Sci. Technol. 2008, 42, 8027–8032.

178

Li, J. H.; Wang, G.; Zhu, H. Q.; Zhang, M.; Zheng, X. H.; Di, Z. F.; Liu, X. Y.; Wang, X. Antibacterial activity of large-area monolayer graphene film manipulated by charge transfer. Sci. Rep. 2014, 4, 4359.

179

Carpio, I. E. M.; Santos, C. M.; Wei, X.; Rodrigues, D. F. Toxicity of a polymer-graphene oxide composite against bacterial planktonic cells, biofilms, and mammalian cells. Nanoscale 2012, 4, 4746–4756.

180

Chen, J. N.; Peng, H.; Wang, X.P.; Shao, F.; Yuan, Z. D.; Han, H. Y. Graphene oxide exhibits broad-spectrum antimicrobial activity against bacterial phytopathogens and fungal conidia by intertwining and membrane perturbation. Nanoscale 2014, 6, 1879–1889.

181

Kanchanapally, R.; Nellore, B. P. V.; Sinha, S. S.; Pedraza, F.; Jones, S. J.; Pramanik, A.; Chavva, S. R.; Tchounwou, C.; Shi, Y. L.; Vangara, A. et al. Antimicrobial peptide-conjugated graphene oxide membrane for efficient removal and effective killing of multiple drug resistant bacteria. RSC Adv. 2015, 5, 18881–18887.

182

Akhavan, O.; Ghaderi, E.; Esfandiar, A. Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by near-infrared irradiation. J. Phys. Chem. B 2011, 115, 6279–6288.

183

Luan, B. Q.; Huynh, T.; Zhao, L.; Zhou, R. H. Potential toxicity of graphene to cell functions via disrupting protein-protein interactions. ACS Nano 2015, 9, 663–669.

184

Zhao, J. M.; Deng, B.; Lv, M.; Li, J. Y.; Zhang, Y. J.; Jiang, H. Q.; Peng, C.; Li, J.; Shi, J. Y.; Huang, Q. et al. Graphene oxide-based antibacterial cotton fabrics. Adv. Healthc. Mater. 2013, 2, 1259–1266.

185

Karimi, L.; Yazdanshenas, M. E.; Khajavi, R.; Rashidi, A.; Mirjalili, M. Using graphene/TiO2 nanocomposite as a new route for preparation of electroconductive, self-cleaning, antibacterial and antifungal cotton fabric without toxicity. Cellulose 2014, 21, 3813–3827.

186

Fan, Z. J.; Liu, B.; Wang, J. Q.; Zhang, S. Y.; Lin, Q. Q.; Gong, P. W.; Ma, L. M.; Yang, S. R. A novel wound dressing based on Ag/graphene – Adv. Funct. Mater. 2014, 24, 3933–3943.

187

Zhou, Y. Z.; Chen, R.; He, T. T.; Xu, K.; Du, D.; Zhao, N.; Cheng, X. N.; Yang, J.; Shi, H. F.; Lin, Y. H. Biomedical potential of ultrafine Ag/AgCl nanoparticles coated on graphene with special reference to antimicrobial performances and burn wound healing. ACS Appl. Mater. Interfaces 2016, 8, 15067–15075.

188

Lu, B. G.; Li, T.; Zhao, H. T.; Li, X. D.; Gao, C. T.; Zhang, S. X.; Xie, E. Q. Graphene-based composite materials beneficial to wound healing. Nanoscale 2012, 4, 2978–2982.

189

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.

190

Pandey, H.; Parashar, V.; Parashar, R.; Prakash, R.; Ramteke, P. W.; Pandey, A. C. Controlled drug release characteristics and enhanced antibacterial effect of graphene nanosheets containing gentamicin sulfate. Nanoscale 2011, 3, 4104–4108.

191

Wang, Y.; Zhang, D.; Bao, Q.; Wu, J. J.; Wan, Y. Controlled drug release characteristics and enhanced antibacterial effect of graphene oxide-drug intercalated layered double hydroxide hybrid films. J. Mater. Chem. 2012, 22, 23106–23113.

192

Ghadim, E. E.; Manouchehri, F.; Soleimani, G.; Hosseini, H.; Kimiagar, S.; Nafisi, S. Adsorption properties of tetracycline onto graphene oxide: Equilibrium, kinetic and thermodynamic studies. PLoS One 2013, 8, e79254.

193

Huang, T. F.; Zhang, L.; Chen, H. L.; Gao, C. J. A cross-linking graphene oxide-polyethyleneimine hybrid film containing ciprofloxacin: One-step preparation, controlled drug release and antibacterial performance. J. Mater. Chem. B 2015, 3, 1605–1611.

194

Ding, H.; Zhang, F.; Zhao, C. C.; Lv, Y. L.; Ma, G. H.; Wei, W.; Tian, Z. Y. Beyond a carrier: Graphene quantum dots as a probe for programmatically monitoring anti-cancer drug delivery, release, and response. ACS Appl. Mater. Interfaces 2017, 9, 27396–27401.

195

Mo, R.; Jiang, T.; Sun, W.; Gu, Z. ATP-responsive DNA-graphene hybrid nanoaggregates for anticancer drug delivery. Biomaterials 2015, 50, 67–74.

196

Jiang, T.; Sun, W.; Zhu, Q.; Burns, N. A.; Khan, S. A.; Mo, R.; Gu, Z. Furin-mediated sequential delivery of anticancer cytokine and small- molecule drug shuttled by grapheme. Adv. Mater. 2015, 27, 1021–1028.

197

Zeng, X. K.; McCarthy, D. T.; Deletic, A.; Zhang, X. W. Silver/reduced graphene oxide hydrogel as novel bactericidal filter for point-of-use water disinfection. Adv. Funct. Mater. 2015, 25, 4344–4351.

198

Zeng, X. K.; Wang, Z. Y.; Meng, N.; McCarthy, D. T.; Deletic, A.; Pan, J. H.; Zhang, X. W. Highly dispersed TiO2 nanocrystals and carbon dots on reduced graphene oxide: Ternary nanocomposites for accelerated photocatalytic water disinfection. Appl. Catal. B: Environ. 2017, 202, 33–41.

199

Zeng, X. K.; Wang, Z. Y.; Wang, G.; Gengenbach, T. R.; McCarthy, D. T.; Deletic, A.; Yu, J. G.; Zhang, X. W. Highly dispersed TiO2 nanocrystals and WO3 Nanorods on reduced graphene oxide: Z-scheme photocatalysis system for accelerated photocatalytic water disinfection. Appl. Catal. B: Environ. 2017, 218, 163–173.

200

Nellore, B. P. V.; Kanchanapally, R.; Pedraza, F.; Sinha, S. S.; Pramanik, A.; Hamme, A. T.; Arslan, Z.; Sardar, D.; Ray, P. C. Bio-conjugated CNT-bridged 3D porous graphene oxide membrane for highly efficient disinfection of pathogenic bacteria and removal of toxic metals from water. ACS Appl. Mater. Interfaces 2015, 7, 19210–19218.

201

Armani, M. A.; Abu-Taleb, A.; Remalli, N.; Abdullah, M.; Srikanth, V. V. S. S.; Labhasetwar, N. K. Dragon's blood-aided synthesis of Ag/Ag2O core/shell nanostructures and Ag/Ag2O decked multi-layered graphene for efficient As(Ⅲ) uptake from water and antibacterial activity. RSC Adv. 2016, 6, 44145–44153.

202

Wang, Y. L.; El-Deen, A. G.; Li, P.; Oh, B. H. L.; Guo, Z. R.; Khin, M. M.; Vikhe, Y. S.; Wang, J.; Hu, R. G.; Boom, R. M. et al. High-performance capacitive deionization disinfection of water with graphene oxide- graft-quaternized chitosan nanohybrid electrode coating. ACS Nano 2015, 9, 10142–10157.

Publication history
Copyright
Acknowledgements

Publication history

Received: 12 June 2018
Revised: 12 September 2018
Accepted: 14 September 2018
Published: 15 October 2018
Issue date: February 2019

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Acknowledgements

Acknowledgements

This work was financially supported by the National Key Research and Development Program (No. 2016YFA0201200), the Shanghai Municipal Natural Science Foundation (No. 17ZR1412100), the Key Laboratory of Interfacial Physics and Technology, the Chinese Academy of Sciences (No. CASKL-IPT1603), the Talent Program of Shanghai University of Engineering Science, the Startup Foundation for Doctors of Shanghai University of Engineering Science, and the National Natural Science Foundation of China (Nos. 81870749, 21373260, 31470960 and 51375294).

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