CoChat
Sign Up
Cited by 221Graphene and Nanomaterials ApplicationsGraphene research and applicationsNanoparticles: synthesis and applications

Synthesis and Toxicity of Graphene Oxide Nanoparticles: A Literature Review of In Vitro and In Vivo Studies

Open access
Rhazouani, Asmaa, Gamrani, Halima, El Achaby, Mounir, Aziz, Khalid, Gebrati, Lhoucine, Uddin, Md Sahab, AZIZ, Faissal·2021·BioMed Research International
DOI 10.1155/2021/5518999PMC PMC8213470
Open this paper in CoChat — free accountOpen PDF

Abstract

Nanomaterials have been widely used in many fields in the last decades, including electronics, biomedicine, cosmetics, food processing, buildings, and aeronautics. The application of these nanomaterials in the medical field could improve diagnosis, treatment, and prevention techniques. Graphene oxide (GO), an oxidized derivative of graphene, is currently used in biotechnology and medicine for cancer treatment, drug delivery, and cellular imaging. Also, GO is characterized by various physicochemical properties, including nanoscale size, high surface area, and electrical charge. However, the toxic effect of GO on living cells and organs is a limiting factor that limits its use in the medical field. Recently, numerous studies have evaluated the biocompatibility and toxicity of GO in vivo and in vitro . In general, the severity of this nanomaterial’s toxic effects varies according to the administration route, the dose to be administered, the method of GO synthesis, and its physicochemical properties. This review brings together studies on the method of synthesis and structure of GO, characterization techniques, and physicochemical properties. Also, we rely on the toxicity of GO in cellular models and biological systems. Moreover, we mention the general mechanism of its toxicity.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1155/2021/5518999

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Cytotoxicity of excessively absorbed NGOs is manifested by interacting with cell membranes or producing reactive oxygen species, possibly resulting in injuries to lungs, kidneys, brain and reproductive systems.

    “For instance, it has been reported that the cytotoxicity of excessively absorbed NGOs is manifested by interacting with cell membranes or producing reactive oxygen species, possibly resulting in injuries to lungs, kidneys, brain and reproductive systems56.”

    From Bioengineered liver crosslinked with nano-graphene oxide enables efficient liver regeneration via MMP suppression and immunomodulation (2023) · cites this paper as [56]

    Sections 8.1 and 8.2 identify membrane interactions and reactive oxygen species as mechanisms of GO cytotoxicity. Sections 7.1, 7.5, and 7.6 report lung, kidney, and brain injury, although section 7.5 also reports studies finding no kidney damage. Section 7.7 describes developmental harm but reports normal reproductive activity in GO-exposed male mice; it does not establish injury to the reproductive system as claimed. Page numbers are unavailable in our copy. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 143

  1. [1]Zahin N. Anwar R. Tewari D. Nanoparticles and its biomedical applications in health and diseases: special focus on drug delivery Environmental Science and Pollution Research 2020 27 16 19151 19168 10.1007/s11356-019-05211-0 2-s2.0-85065699282 31079299 · DOI
  2. [3]Son S. J. Bai X. Lee S. B. Inorganic hollow nanoparticles and nanotubes in nanomedicine: Part 1. Drug/gene delivery applications Drug Discovery Today 2007 12 15-16 650 656 10.1016/j.drudis.2007.06.002 2-s2.0-34547790831 17706547 · DOI
  3. [4]Miao Z.-H. Wang H. Yang H. Li Z. Zhen L. Xu C. Y. Glucose-derived carbonaceous nanospheres for photoacoustic imaging and photothermal therapy ACS Applied Materials & Interfaces 2016 8 25 15904 15910 10.1021/acsami.6b03652 2-s2.0-84976544095 27281299 · DOI
  4. [5]Chakrabarti M. Kiseleva R. Vertegel A. Ray S. K. Carbon nanomaterials for drug delivery and cancer therapy Journal of Nanoscience and Nanotechnology 2015 15 8 5501 5511 10.1166/jnn.2015.10614 2-s2.0-84920842349 26369109 · DOI
  5. [6]Brodie B. C. On the atomic weight of graphite Philosophical Transactions of the Royal Society of London Series I 1859 149 249 259
  6. [7]Novoselov K. S. Electric field effect in atomically thin carbon films Science 2004 306 5696 666 669 10.1126/science.1102896 2-s2.0-7444220645 15499015 · DOI · Paper page
  7. [8]Ghosh S. Calizo I. Teweldebrhan D. Extremely high thermal conductivity of graphene: prospects for thermal management applications in nanoelectronic circuits Applied Physics Letters 2008 92 15 p. 151911 10.1063/1.2907977 2-s2.0-42349113188 · DOI
  8. [9]Wu Z.-S. Ren W. Gao L. Synthesis of graphene sheets with high electrical conductivity and good thermal stability by hydrogen arc discharge exfoliation ACS Nano 2009 3 2 411 417 10.1021/nn900020u 2-s2.0-65249179425 19236079 · DOI
  9. [10]Rafiee M. A. Rafiee J. Srivastava I. Fracture and fatigue in graphene nanocomposites Small 2010 6 2 179 183 10.1002/smll.200901480 2-s2.0-76749132192 19924737 · DOI
  10. [11]Nair R. R. Blake P. Grigorenko A. N. Fine structure constant defines visual transparency of graphene Science 2008 320 5881 p. 1308 10.1126/science.1156965 2-s2.0-45349092986 18388259 · DOI · Paper page
  11. [12]Cohen-Tanugi D. Grossman J. C. Water desalination across nanoporous graphene Nano Letters 2012 12 7 3602 3608 10.1021/nl3012853 2-s2.0-84863847073 22668008 · DOI
  12. [13]Schwierz F. Graphene transistors Nature Nanotechnology 2010 5 7 487 496 10.1038/nnano.2010.89 2-s2.0-77955231284 20512128 · DOI
  13. [14]Kim Y.-K. Min D.-H. Preparation of the hybrid film of poly(allylamine hydrochloride)-functionalized graphene oxide and gold nanoparticle and its application for laser-induced desorption/ionization of small molecules Langmuir 2012 28 4453 4458 10.1021/la204185p 2-s2.0-84863285085 22309433 · DOI
  14. [15]Min S. K. Kim W. Y. Cho Y. Kim K. S. Fast DNA sequencing with a graphene-based nanochannel device Nature Nanotechnology 2011 6 3 162 165 10.1038/nnano.2010.283 2-s2.0-79952446499 21297626 · DOI
  15. [16]Wang Y. Li Z. Wang J. Li J. Lin Y. Graphene and graphene oxide: biofunctionalization and applications in biotechnology Trends in Biotechnology 2011 29 5 205 212 10.1016/j.tibtech.2011.01.008 2-s2.0-79954657367 21397350 PMC7114214 · DOI
  16. [17]Paredes J. I. Villar-Rodil S. Martínez-Alonso A. Tascon J. M. D. Graphene oxide dispersions in organic solvents Langmuir 2008 24 10560 10564 10.1021/la801744a 2-s2.0-54549083300 18759411 · DOI · Paper page
  17. [18]Chung C. Kim Y. K. Shin D. Ryoo S. R. Hong B. H. Min D. H. Biomedical applications of graphene and graphene oxide Accounts of Chemical Research 2013 46 10 2211 2224 10.1021/ar300159f 2-s2.0-84880133779 23480658 · DOI
  18. [19]Wang Y. Li Z. Hu D. Lin C. T. Li J. Lin Y. Aptamer/graphene oxide nanocomplex for in situ molecular probing in living cells Journal of the American Chemical Society 2010 132 27 9274 9276 10.1021/ja103169v 2-s2.0-77955821689 20565095 · DOI
  19. [20]Ryoo S.-R. Kim Y. K. Kim M. H. Min D. H. Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies ACS Nano 2010 4 11 6587 6598 10.1021/nn1018279 2-s2.0-78649565787 20979372 · DOI
  20. [21]Li M. Liang Y. He J. Zhang H. Guo B. Two-pronged strategy of biomechanically active and biochemically multifunctional hydrogel wound dressing to accelerate wound closure and wound healing Chemistry of Materials 2020 32 23 9937 9953 10.1021/acs.chemmater.0c02823 · DOI
  21. [22]Liang Y. Zhao X. Hu T. Adhesive hemostatic conducting injectable composite hydrogels with sustained drug release and photothermal antibacterial activity to promote full-thickness skin regeneration during wound healing Small 2019 15 12 10.1002/smll.201900046 2-s2.0-85061902522 30786150 · DOI
  22. [23]Zhang B. He J. Shi M. Liang Y. Guo B. Injectable self-healing supramolecular hydrogels with conductivity and photo- thermal antibacterial activity to enhance complete skin regeneration Chemical Engineering Journal 2020 400 10.1016/j.cej.2020.125994 · DOI
  23. [24]Liang Y. Chen B. Li M. He J. Yin Z. Guo B. Injectable antimicrobial conductive hydrogels for wound disinfection and infectious wound healing Biomacromolecules 2020 21 5 1841 1852 10.1021/acs.biomac.9b01732 32388998 · DOI
  24. [25]Toda K. Furue R. Hayami S. Recent progress in applications of graphene oxide for gas sensing: a review Analytica Chimica Acta 2015 878 43 53 10.1016/j.aca.2015.02.002 2-s2.0-84929966303 26002325 · DOI
  25. [26]Zhu Y. Murali S. Cai W. Graphene and graphene oxide: synthesis, properties, and applications Advanced Materials 2010 22 35 3906 3924 10.1002/adma.201001068 2-s2.0-77956963862 20706983 · DOI
  26. [27]Brodie B. C. XIII. On the atomic weight of graphite Philosophical Transactions of the Royal Society of London 1859 149 249 259
  27. [28]Staudenmaier L. Verfahren zur darstellung der graphitsäure Berichte der Deutschen Chemischen Gesellschaft 1898 31 2 1481 1487 10.1002/cber.18980310237 2-s2.0-84981756708 · DOI
  28. [29]William S. Hummers J. R. Offeman R. E. Preparation of graphitic oxide Journal of the American Chemical Society 1958 80 6 p. 1339 10.1021/ja01539a017 2-s2.0-33947461960 · DOI
  29. [30]Pendolino F. Armata N. Synthesis, Characterization and Models of Graphene Oxide Graphene Oxide in Environmental Remediation Process 2017 Cham Springer International Publishing 5 21 10.1007/978-3-319-60429-9_2 2-s2.0-85021691622 · DOI
  30. [31]Marcano D. C. Kosynkin D. V. Berlin J. M. Improved synthesis of graphene oxide ACS Nano 2010 4 8 4806 4814 10.1021/nn1006368 2-s2.0-78650092372 20731455 · DOI
  31. [32]Sun L. Fugetsu B. Mass production of graphene oxide from expanded graphite Materials Letters 2013 109 207 210 10.1016/j.matlet.2013.07.072 2-s2.0-84882278487 · DOI
  32. [33]Peng L. Xu Z. Liu Z. An iron-based green approach to 1-h production of single-layer graphene oxide Nature Communications 2015 6 1 10.1038/ncomms6716 2-s2.0-84930024554 PMC4354147 25607686 · DOI
  33. [34]Pendolino F. Armata N. Masullo T. Cuttitta A. Temperature influence on the synthesis of pristine graphene oxide and graphite oxide Materials Chemistry and Physics 2015 164 71 77 10.1016/j.matchemphys.2015.08.024 2-s2.0-84941422301 · DOI
  34. [35]Chen M. Zhang C. Li X. A one-step method for reduction and self-assembling of graphene oxide into reduced graphene oxide aerogels Journal of Materials Chemistry A 2013 1 8 p. 2869 10.1039/c2ta00820c 2-s2.0-84876544921 · DOI
  35. [36]Zhang J. Liu Q. Ruan Y. Lin S. Wang K. Lu H. Monolithic crystalline swelling of graphite oxide: a bridge to ultralarge graphene oxide with high scalability Chemistry of Materials 2018 30 6 1888 1897 10.1021/acs.chemmater.7b04458 2-s2.0-85044670607 · DOI
  36. [37]Hofmann U. Holst R. Über die säurenatur und die methylierung von graphitoxyd Berichte der deutschen chemischen Gesellschaft (A and B Series) 1939 72 4 754 771 10.1002/cber.19390720417 · DOI
  37. [38]Ruess G. Über das graphitoxyhydroxyd (graphitoxyd) Monatshefte für Chemie und verwandte Teile anderer Wissenschaften 1947 76 3 381 417 10.1007/BF00898987 2-s2.0-34250553012 · DOI
  38. [39]Scholz W. Boehm H. P. Untersuchungen am graphitoxid. VI. Betrachtungen zur struktur des graphitoxids Zeitschrift für Anorganische und Allgemeine Chemie 1969 369 3-6 327 340 10.1002/zaac.19693690322 2-s2.0-84944193119 · DOI
  39. [40]Nakajima T. Matsuo Y. Formation process and structure of graphite oxide Carbon 1994 32 3 469 475 10.1016/0008-6223(94)90168-6 2-s2.0-0028199339 · DOI
  40. [41]Lerf A. He H. Forster M. Klinowski J. Structure of graphite oxide revisited The Journal of Physical Chemistry B 1998 102 23 4477 4482 10.1021/jp9731821 · DOI
  41. [42]Szabó T. Berkesi O. Forgó P. Evolution of surface functional groups in a series of progressively oxidized graphite oxides Chemistry of Materials 2006 18 11 2740 2749 10.1021/cm060258 · DOI
  42. [43]Rourke J. P. Pandey P. A. Moore J. J. The real graphene oxide revealed: stripping the oxidative debris from the graphene-like sheets Angewandte Chemie International Edition 2011 50 14 3173 3177 10.1002/anie.201007520 2-s2.0-79953008694 21432951 · DOI
  43. [44]Dimiev A. M. Alemany L. B. Tour J. M. Graphene oxide. Origin of acidity, its instability in water, and a new dynamic structural model ACS Nano 2013 7 1 576 588 10.1021/nn3047378 2-s2.0-84872861294 23215236 · DOI
  44. [45]Liu Z. Nørgaard K. Overgaard M. H. Direct observation of oxygen configuration on individual graphene oxide sheets Carbon 2018 127 141 148 10.1016/j.carbon.2017.10.100 2-s2.0-85032945518 · DOI
  45. [46]Yang H. Li H. Zhai J. Sun L. Yu H. Simple synthesis of graphene oxide using ultrasonic cleaner from expanded graphite Industrial & Engineering Chemistry Research 2014 53 46 17878 17883 10.1021/ie503586v 2-s2.0-84912569315 · DOI
  46. [47]Goldstein J. I. Newbury D. E. Echlin P. Scanning Electron Microscopy and X-Ray Microanalysis: Third Edition 2003 Springer US 10.1007/978-1-4615-0215-9 · DOI
  47. [48]Aunkor M. T. H. Mahbubul I. M. Saidur R. Metselaar H. S. C. Deoxygenation of graphene oxide using household baking soda as a reducing agent: a green approach RSC Advances 2015 5 86 70461 70472 10.1039/C5RA10520J 2-s2.0-84940473786 · DOI
  48. [49]Wang G. Yang J. Park J. Facile synthesis and characterization of graphene nanosheets The Journal of Physical Chemistry C 2008 112 22 8192 8195 10.1021/jp710931h 2-s2.0-53549119409 · DOI
  49. [50]Ferrari A. C. Basko D. M. Raman spectroscopy as a versatile tool for studying the properties of graphene Nature Nanotechnology 2013 8 4 235 246 10.1038/nnano.2013.46 2-s2.0-84876373110 23552117 · DOI · Paper page
  50. [52]Rattana S. Chaiyakun S. Witit-anun N. Preparation and characterization of graphene oxide nanosheets Procedia Engineering 2012 32 759 764 10.1016/j.proeng.2012.02.009 2-s2.0-84878644305 · DOI
  51. [53]Song J. Wang X. Chang C.-T. Preparation and characterization of graphene oxide Journal of Nanomaterials 2014 2014 6 10.1155/2014/276143 2-s2.0-84897498540 · DOI
  52. [54]Chen J. Li Y. Huang L. Li C. Shi G. High-yield preparation of graphene oxide from small graphite flakes via an improved Hummers method with a simple purification process Carbon 2015 81 826 834 10.1016/j.carbon.2014.10.033 2-s2.0-84922752677 · DOI
  53. [55]Jalili R. Aboutalebi S. H. Esrafilzadeh D. Organic solvent-based graphene oxide liquid crystals: a facile route toward the next generation of self-assembled layer-by-layer multifunctional 3D architectures ACS Nano 2013 7 5 3981 3990 10.1021/nn305906z 2-s2.0-84878326830 23574049 · DOI
  54. [56]Coats A. W. Redfern J. P. Thermogravimetric analysis. A review Analyst 1963 88 1053 906 924 10.1039/AN9638800906 2-s2.0-37049061460 · DOI
  55. [57]Kumar R. Kumar M. Kumar A. Surface modification of graphene oxide using esterification Materials Today: Proceedings 2019 18 1556 1561 10.1016/j.matpr.2019.06.626 2-s2.0-85073052747 · DOI
  56. [58]Park S. Ruoff R. S. Chemical methods for the production of graphenes Nature Nanotechnology 2009 4 4 217 224 10.1038/nnano.2009.58 2-s2.0-67049114637 19350030 · DOI
  57. [59]Bradder P. Ling S. K. Wang S. Liu S. Dye adsorption on layered graphite oxide Journal of Chemical & Engineering Data 2011 56 1 138 141 10.1021/je101049g 2-s2.0-78651388752 · DOI · Paper page
  58. [61]Dreyer D. R. Park S. Bielawski C. W. Ruoff R. S. The chemistry of graphene oxide Chemical Society Reviews 2010 39 1 228 240 10.1039/B917103G 2-s2.0-77949880674 20023850 · DOI · Paper page
  59. [62]Dong R. Ma P. X. Guo B. Conductive biomaterials for muscle tissue engineering Biomaterials 2020 229, article 119584 10.1016/j.biomaterials.2019.119584 31704468 · DOI
  60. [63]Navarro E. Baun A. Behra R. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi Ecotoxicology 2008 17 5 372 386 10.1007/s10646-008-0214-0 2-s2.0-44449087556 18461442 · DOI
  61. [64]Yan H. Tao X. Yang Z. Effects of the oxidation degree of graphene oxide on the adsorption of methylene blue Journal of Hazardous Materials 2014 268 191 198 10.1016/j.jhazmat.2014.01.015 2-s2.0-84893425588 24491443 · DOI
  62. [65]Šimšíková M. Šikola T. Interaction of graphene oxide with proteins and applications of their conjugates Journal of Nano Research 2017 5 2 10.15406/JNMR.2017.05.00109 · DOI
  63. [66]Liu Z. Robinson J. T. Sun X. Dai H. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs Journal of the American Chemical Society 2008 130 33 10876 10877 10.1021/ja803688x 2-s2.0-50249123111 18661992 PMC2597374 · DOI
  64. [67]Kuchlyan J. Kundu N. Banik D. Roy A. Sarkar N. Spectroscopy and fluorescence lifetime imaging microscopy to probe the interaction of bovine serum albumin with graphene oxide Langmuir 2015 31 51 13793 13801 10.1021/acs.langmuir.5b03648 2-s2.0-84952802116 26646418 · DOI
  65. [68]Šimšíková M. Interaction of graphene oxide with albumins: effect of size, pH, and temperature Archives of Biochemistry and Biophysics 2016 593 69 79 10.1016/j.abb.2016.02.015 2-s2.0-84958170493 26873532 · DOI
  66. [69]Amieva E. J.-C. López‐Barroso J. Martínez‐Hernández A. L. Velasco‐Santos C. Graphene-based materials functionalization with natural polymeric biomolecules Recent advances in graphene research 2016 IntechOpen 10.5772/64001 · DOI
  67. [70]Stankovich S. Dikin D. A. Piner R. D. Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide Carbon 2007 45 7 1558 1565 10.1016/j.carbon.2007.02.034 2-s2.0-34249742469 · DOI
  68. [71]Tang S. Cao Z. Adsorption of nitrogen oxides on graphene and graphene oxides: insights from density functional calculations The Journal of Chemical Physics 2011 134 4 10.1063/1.3541249 2-s2.0-79551579706 21280788 · DOI
  69. [72]Lv M. Yan L. Liu C. Non-covalent functionalized graphene oxide (GO) adsorbent with an organic gelator for co-adsorption of dye, endocrine-disruptor, pharmaceutical and metal ion Chemical Engineering Journal 2018 349 791 799 10.1016/j.cej.2018.04.153 2-s2.0-85047535460 · DOI
  70. [73]Emadi F. Amini A. Gholami A. Ghasemi Y. Functionalized graphene oxide with chitosan for protein nanocarriers to protect against enzymatic cleavage and retain collagenase activity Scientific Reports 2017 7, article 42258 10.1038/srep42258 2-s2.0-85012206960 PMC5301474 28186169 · DOI
  71. [74]Ruiz O. N. Fernando K. S. Wang B. Graphene oxide: a nonspecific enhancer of cellular growth ACS Nano 2011 5 10 8100 8107 10.1021/nn202699t 2-s2.0-80055022730 21932790 · DOI
  72. [75]Chen G.-Y. Pang D. P. Hwang S. M. Tuan H. Y. Hu Y. C. A graphene-based platform for induced pluripotent stem cells culture and differentiation Biomaterials 2012 33 2 418 427 10.1016/j.biomaterials.2011.09.071 2-s2.0-80055102865 22014460 · DOI
  73. [76]Yoon H. H. Bhang S. H. Kim T. Yu T. Hyeon T. Kim B. S. Dual roles of graphene oxide in chondrogenic differentiation of adult stem cells: cell-adhesion substrate and growth factor-delivery carrier Advanced Functional Materials 2014 24 41 6455 6464 10.1002/adfm.201400793 2-s2.0-84927125250 · DOI
  74. [77]Liu Y. Luo Y. Wu J. Graphene oxide can induce in vitro and in vivo mutagenesis Scientific Reports 2013 3 1 10.1038/srep03469 2-s2.0-84890619638 PMC6506447 24326739 · DOI
  75. [78]Zhao F. Meng H. Yan L. Wang B. Zhao Y. Nanosurface chemistry and dose govern the bioaccumulation and toxicity of carbon nanotubes, metal nanomaterials and quantum dots in vivo Science Bulletin 2015 60 10.1007/s11434-014-0700-0 2-s2.0-84928893881 · DOI
  76. [79]Wang K. Ruan J. Song H. Biocompatibility of graphene oxide Nanoscale Research Letters 2010 6 10.1007/s11671-010-9751-6 2-s2.0-79952696075 PMC3212228 27502632 · DOI
  77. [80]Chang Y. Yang S. T. Liu J. H. In vitro toxicity evaluation of graphene oxide on A549 cells Toxicology Letters 2011 200 3 201 210 10.1016/j.toxlet.2010.11.016 2-s2.0-78651073259 21130147 · DOI
  78. [81]Zhang Y. Ali S. F. Dervishi E. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells ACS Nano 2010 4 6 3181 3186 10.1021/nn1007176 2-s2.0-77955944437 20481456 · DOI
  79. [82]Lv M. Zhang Y. Liang L. Effect of graphene oxide on undifferentiated and retinoic acid-differentiated SH-SY5Y cells line Nanoscale 2012 4 13 3861 3866 10.1039/c2nr30407d 2-s2.0-84862560397 22653613 · DOI
  80. [83]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 Scientific Reports 2016 6 1 10.1038/srep39548 2-s2.0-85006966020 PMC5175188 28000740 · DOI
  81. [84]Yue H. Wei W. Yue Z. The role of the lateral dimension of graphene oxide in the regulation of cellular responses Biomaterials 2012 33 16 4013 4021 10.1016/j.biomaterials.2012.02.021 2-s2.0-84862818464 22381473 · DOI
  82. [85]Wang A. Pu K. Dong B. Role of surface charge and oxidative stress in cytotoxicity and genotoxicity of graphene oxide towards human lung fibroblast cells Journal of Applied Toxicology 2013 33 10 1156 1164 10.1002/jat.2877 2-s2.0-84880929455 23775274 · DOI
  83. [86]Liao K.-H. Lin Y.-S. Macosko C. W. Haynes C. L. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts ACS Applied Materials & Interfaces 2011 3 7 2607 2615 10.1021/am200428v 2-s2.0-80053633118 21650218 · DOI
  84. [87]Singh S. K. Singh M. K. Kulkarni P. P. Sonkar V. K. Grácio J. J. A. Dash D. Amine-modified graphene: thrombo-protective safer alternative to graphene oxide for biomedical applications ACS Nano 2012 6 3 2731 2740 10.1021/nn300172t 2-s2.0-84859118414 22376049 · DOI
  85. [88]Arbo M. D. Altknecht L. F. Cattani S. In vitro cardiotoxicity evaluation of graphene oxide Mutation Research/Genetic Toxicology and Environmental Mutagenesis 2019 841 8 13 10.1016/j.mrgentox.2019.03.004 2-s2.0-85063061181 31138412 · DOI
  86. [89]Sanchez V. C. Jachak A. Hurt R. H. Kane A. B. Biological interactions of graphene-family nanomaterials: an interdisciplinary review Chemical Research in Toxicology 2012 25 1 15 34 10.1021/tx200339h 2-s2.0-84855833077 21954945 PMC3259226 · DOI
  87. [90]Duch M. C. Budinger G. R. S. Liang Y. T. Minimizing oxidation and stable nanoscale dispersion improves the biocompatibility of graphene in the lung Nano Letters 2011 11 12 5201 5207 10.1021/nl202515a 2-s2.0-83655164368 22023654 PMC3237757 · DOI
  88. [91]Zhang X. Yin J. Peng C. Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration Carbon 2011 49 3 986 995 10.1016/j.carbon.2010.11.005 2-s2.0-78650251003 · DOI
  89. [92]Hu Q. Jiao B. Shi X. Valle R. P. Zuo Y. Y. Hu G. Effects of graphene oxide nanosheets on the ultrastructure and biophysical properties of the pulmonary surfactant film Nanoscale 2015 7 43 18025 18029 10.1039/c5nr05401j 2-s2.0-84946124800 26482703 PMC4854527 · DOI
  90. [93]Gosens I. Post J. A. de la Fonteyne L. J. J. Impact of agglomeration state of nano- and submicron sized gold particles on pulmonary inflammation Particle and Fibre Toxicology 2010 7 1 p. 37 10.1186/1743-8977-7-37 2-s2.0-78649577012 21126342 PMC3014867 · DOI
  91. [95]Kreyling W. G. Semmler-Behnke M. Takenaka S. Möller W. Differences in the biokinetics of inhaled nano- versus micrometer-sized particles Accounts of chemical research 2013 46 3 714 722 10.1021/ar300043r 2-s2.0-84875348429 22980029 PMC3556515 · DOI
  92. [96]Chen G.-Y. Chen C. L. Tuan H. Y. Graphene oxide triggers toll-like receptors/autophagy responses in vitro and inhibits tumor growth in vivo Advanced Healthcare Materials 2014 3 9 1486 1495 10.1002/adhm.201300591 2-s2.0-84908018022 24652749 · DOI
  93. [97]Zhang X. Hu W. Li J. Tao L. Wei Y. A comparative study of cellular uptake and cytotoxicity of multi-walled carbon nanotubes, graphene oxide, and nanodiamond Toxicology Research 2012 1 1 62 68 10.1039/c2tx20006f 2-s2.0-84865509906 · DOI
  94. [98]Ma 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 10 10498 10515 10.1021/acsnano.5b04751 2-s2.0-84945964202 26389709 PMC5522963 · DOI
  95. [99]Hashemi M. S. Gharbi S. Jafarinejad-Farsangi S. Ansari-Asl Z. Dezfuli A. S. Secondary toxic effect of graphene oxide and graphene quantum dots alters the expression of miR-21 and miR-29a in human cell lines Toxicology in Vitro 2020 65 p. 104796 10.1016/j.tiv.2020.104796 32070776 · DOI
  96. [100]Hu L. Fu Y. Rong L. Evaluating the cytotoxicity of graphene oxide using embryonic stem cells-derived cells Journal of Biomedical Materials Research Part A 2020 108 6 1321 1328 10.1002/jbm.a.36904 32064738 · DOI
  97. [101]Zhou T. Zhou X. Xing D. Controlled release of doxorubicin from graphene oxide based charge-reversal nanocarrier Biomaterials 2014 35 13 4185 4194 10.1016/j.biomaterials.2014.01.044 2-s2.0-84896820700 24513318 · DOI
  98. [102]Sood S. Jawahar N. Jain K. Gowthamarajan K. Nainar Meyyanathan S. Olanzapine loaded cationic solid lipid nanoparticles for improved oral bioavailability Current Nanoscience 2013 9 1 26 34 10.2174/157341313805117938 · DOI
  99. [103]Yang K. Gong H. Shi X. Wan J. Zhang Y. Liu Z. In vivo biodistribution and toxicology of functionalized nano-graphene oxide in mice after oral and intraperitoneal administration Biomaterials 2013 34 11 2787 2795 10.1016/j.biomaterials.2013.01.001 2-s2.0-84873077620 23340196 · DOI
  100. [104]Fu C. Liu T. Li L. Liu H. Liang Q. Meng X. Effects of graphene oxide on the development of offspring mice in lactation period Biomaterials 2015 40 23 31 10.1016/j.biomaterials.2014.11.014 2-s2.0-84919626465 25498802 · DOI
  101. [105]Mouchet F. Landois P. Sarremejean E. Characterisation and in vivo ecotoxicity evaluation of double-wall carbon nanotubes in larvae of the amphibian Xenopus laevis Aquatic Toxicology 2008 87 2 127 137 10.1016/j.aquatox.2008.01.011 2-s2.0-41349085342 18313771 · DOI
  102. [106]Itoh H. Nishino M. Hatabu H. Architecture of the lung: morphology and function Journal of Thoracic Imaging 2004 19 4 221 227 10.1097/01.rti.0000142835.06988.b0 2-s2.0-7244249974 15502608 · DOI
  103. [107]Xu W.-P. Zhang L. C. Li J. P. Facile synthesis of silver@graphene oxide nanocomposites and their enhanced antibacterial properties Journal of Materials Chemistry 2011 21 12 4593 4597 10.1039/c0jm03376f 2-s2.0-79952588835 · DOI
  104. [108]Zhao J. Deng B. Lv M. Graphene oxide-based antibacterial cotton fabrics Advanced Healthcare Materials 2013 2 9 1259 1266 10.1002/adhm.201200437 2-s2.0-84883663909 23483725 · DOI
  105. [109]Liang S. Xu S. Zhang D. He J. Chu M. Reproductive toxicity of nanoscale graphene oxide in male mice Nanotoxicology 2015 9 1 92 105 10.3109/17435390.2014.893380 2-s2.0-84925299963 24621344 · DOI
  106. [110]Ema M. Hougaard K. S. Kishimoto A. Honda K. Reproductive and developmental toxicity of carbon-based nanomaterials: a literature review Nanotoxicology 2016 10 4 391 412 10.3109/17435390.2015.1073811 2-s2.0-84960425843 26375634 · DOI
  107. [111]Mendonça M. C. P. Soares E. S. de Jesus M. B. Reduced graphene oxide induces transient blood-brain barrier opening: an in vivo study Journal of nanobiotechnology 2015 13 1 p. 78 10.1186/s12951-015-0143-z 2-s2.0-84945977154 PMC4628296 26518450 · DOI
  108. [112]Raslan A. Del Burgo L. S. Ciriza J. Pedraz J. L. Graphene oxide and reduced graphene oxide-based scaffolds in regenerative medicine International Journal of Pharmaceutics 2020 580 p. 119226 10.1016/j.ijpharm.2020.119226 32179151 · DOI
  109. [113]Qi Y. Liu Y. Xia T. Xu A. Liu S. Chen W. The biotransformation of graphene oxide in lung fluids significantly alters its inherent properties and bioactivities toward immune cells NPG Asia Materials 2018 10 5 385 396 10.1038/s41427-018-0039-0 2-s2.0-85046999786 · DOI
  110. [114]Hu X. Li D. Mu L. Biotransformation of graphene oxide nanosheets in blood plasma affects their interactions with cells Environmental Science: Nano 2017 4 7 1569 1578 10.1039/C7EN00328E 2-s2.0-85024118216 · DOI
  111. [115]Guarnieri D. Sánchez‐Moreno P. Del Rio Castillo A. E. Biotransformation and biological Interaction of graphene and graphene oxide during simulated oral ingestion Small 2018 14 24 10.1002/smll.201800227 2-s2.0-85047391199 29756263 · DOI
  112. [116]Hirn S. Semmler-Behnke M. Schleh C. Particle size-dependent and surface charge-dependent biodistribution of gold nanoparticles after intravenous administration European Journal of Pharmaceutics and Biopharmaceutics 2011 77 3 407 416 10.1016/j.ejpb.2010.12.029 2-s2.0-79952311136 21195759 PMC3051057 · DOI
  113. [117]Li B. Zhang X. Yang J. Influence of polyethylene glycol coating on biodistribution and toxicity of nanoscale graphene oxide in mice after intravenous injection International journal of nanomedicine 2014 9 10.2147/IJN.S66591 2-s2.0-84907874124 PMC4207078 25356071 · DOI
  114. [118]Han S. G. Kim J. K. Shin J. H. Pulmonary responses of Sprague-Dawley rats in single inhalation exposure to graphene oxide nanomaterials BioMed research international 2015 2015 9 10.1155/2015/376756 2-s2.0-84939166638 376756 26295037 PMC4534591 · DOI
  115. [119]Li B. Yang J. Huang Q. Biodistribution and pulmonary toxicity of intratracheally instilled graphene oxide in mice NPG Asia Materials 2013 5 4 p. e44 10.1038/am.2013.7 2-s2.0-84878970064 · DOI
  116. [120]Singh S. K. Singh M. K. Nayak M. K. Thrombus inducing property of atomically thin graphene oxide sheets ACS Nano 2011 5 6 4987 4996 10.1021/nn201092p 2-s2.0-79959799189 21574593 · DOI
  117. [121]Mao L. Hu M. Pan B. Xie Y. Petersen E. J. Biodistribution and toxicity of radio-labeled few layer graphene in mice after intratracheal instillation Particle and fibre toxicology 2015 13 10.1186/s12989-016-0120-1 2-s2.0-84957863572 PMC4750184 26864058 · DOI
  118. [122]Patlolla A. K. Rondalph J. Tchounwou P. B. Biochemical and histopathological evaluation of graphene oxide in Sprague-Dawley rats Austin journal of environmental toxicology 2017 3 PMC5831506 29503980
  119. [123]Patlolla A. K. Randolph J. Kumari S. A. Tchounwou P. B. Toxicity evaluation of graphene oxide in kidneys of Sprague-Dawley rats International journal of environmental research and public health 2016 13 4 p. 380 10.3390/ijerph13040380 2-s2.0-84962054080 27043588 PMC4847042 · DOI
  120. [124]Karsh E. H. Kadhim R. J. Jabir M. S. Effect of graphene oxide and gold nanoparticles on kidney parameters of male mice AIP Conference Proceedings 2020 2213 1 10.1063/5.0000167 · DOI
  121. [125]Jasim D. A. Murphy S. Newman L. The effects of extensive glomerular filtration of thin graphene oxide sheets on kidney physiology ACS Nano 2016 10 12 10753 10767 10.1021/acsnano.6b03358 2-s2.0-85007566107 27936585 PMC7614378 · DOI
  122. [126]Amrollahi-Sharifabadi M. Koohi M. K. Zayerzadeh E. Hablolvarid M. H. Hassan J. Seifalian A. M. In vivo toxicological evaluation of graphene oxide nanoplatelets for clinical application International Journal of Nanomedicine 2018 Volume 13 4757 4769 10.2147/IJN.S168731 2-s2.0-85054055801 30174424 PMC6110298 · DOI
  123. [127]Kim M. Eom H. J. Choi I. Hong J. Choi J. Graphene oxide-induced neurotoxicity on neurotransmitters, AFD neurons and locomotive behavior in Caenorhabditis elegans NeuroToxicology 2020 77 30 39 10.1016/j.neuro.2019.12.011 31862286 · DOI
  124. [128]Rauti R. Medelin M. Newman L. Graphene oxide flakes tune excitatory neurotransmission in vivo by targeting hippocampal synapses Nano letters 2019 19 5 2858 2870 10.1021/acs.nanolett.8b04903 2-s2.0-85065078086 30983361 · DOI
  125. [129]Li Y. Wang Y. Tu L. Sub-acute toxicity study of graphene oxide in the Sprague-Dawley rat International journal of environmental research and public health 2016 13 10.3390/ijerph13111149 2-s2.0-84996550848 PMC5129359 27869683 · DOI
  126. [130]Liu X. T. Mu X. Y. Wu X. L. Toxicity of multi-walled carbon nanotubes, graphene oxide, and reduced graphene oxide to zebrafish embryos Biomedical and Environmental Sciences 2014 27 9 676 683 10.3967/bes2014.103 2-s2.0-84908238594 25256857 · DOI
  127. [131]Chen Y. Hu X. Sun J. Zhou Q. Specific nanotoxicity of graphene oxide during zebrafish embryogenesis Nanotoxicology 2016 10 1 1 11 10.3109/17435390.2015.1005032 2-s2.0-84959566116 25704117 · DOI
  128. [132]Bangeppagari M. Park S. H. Kundapur R. R. Lee S. J. Graphene oxide induces cardiovascular defects in developing zebrafish (Danio rerio) embryo model: In-vivo toxicity assessment Science of the total environment 2019 673 810 820 10.1016/j.scitotenv.2019.04.082 2-s2.0-85064247928 31005017 · DOI
  129. [133]El-Yamany N. A. Mohamed F. F. Salaheldin T. A. Tohamy A. A. Abd El-Mohsen W. N. Amin A. S. Graphene oxide nanosheets induced genotoxicity and pulmonary injury in mice Experimental and Toxicologic Pathology 2017 69 6 383 392 10.1016/j.etp.2017.03.002 2-s2.0-85016829550 28359838 · DOI
  130. [134]Bengtson S. Kling K. Madsen A. M. No cytotoxicity or genotoxicity of graphene and graphene oxide in murine lung epithelial FE1 cells in vitro Environmental and Molecular Mutagenesis 2016 57 6 469 482 10.1002/em.22017 2-s2.0-84978835857 27189646 PMC5084775 · DOI
  131. [135]Mohamed H. R. H. Welson M. Yaseen A. E. El-Ghor A. A. Estimation of genomic instability and mutation induction by graphene oxide nanoparticles in mice liver and brain tissues Environmental Science and Pollution Research 2020 27 1 264 278 10.1007/s11356-019-06930-0 31786761 · DOI
  132. [136]Liu J.-H. Liu J. H. Yang S. T. Effect of size and dose on the biodistribution of graphene oxide in mice Nanomedicine 2012 7 12 1801 1812 10.2217/nnm.12.60 2-s2.0-84871327005 22830500 · DOI
  133. [137]Zhao S. Wang Y. Duo L. Biochemical toxicity, lysosomal membrane stability and DNA damage induced by graphene oxide in earthworms Environmental Pollution 2021 269 p. 116225 10.1016/j.envpol.2020.116225 33316493 · DOI
  134. [138]Zhang L. Ouyang S. Zhang H. Graphene oxide induces dose-dependent lung injury in rats by regulating autophagy Experimental and Therapeutic Medicine 2021 21 5 p. 462 10.3892/etm.2021.9893 33747194 PMC7967850 · DOI
  135. [139]Cao Z. Su M. Wang H. Carboxyl graphene oxide nanoparticles induce neurodevelopmental defects and locomotor disorders in zebrafish larvae Chemosphere 2021 270 p. 128611 10.1016/j.chemosphere.2020.128611 33092822 · DOI
  136. [140]Seabra A. B. Paula A. J. de Lima R. Alves O. L. Durán N. Nanotoxicity of graphene and graphene oxide Chemical research in toxicology 2014 27 2 159 168 10.1021/tx400385x 2-s2.0-84894281997 24422439 · DOI
  137. [141]Akhavan O. Ghaderi E. Toxicity of graphene and graphene oxide nanowalls against bacteria ACS Nano 2010 4 10 5731 5736 10.1021/nn101390x 2-s2.0-78049352115 20925398 · DOI
  138. [142]Hu W. Peng C. Lv M. Protein corona-mediated mitigation of cytotoxicity of graphene oxide ACS Nano 2011 5 5 3693 3700 10.1021/nn200021j 2-s2.0-80051487186 21500856 · DOI
  139. [143]Tu Y. Fang H. Destructive extraction of phospholipids from cell membranes by graphene and graphene oxide nanosheets SCIENTIA SINICA Physica, Mechanica & Astronomica 2016 46 6 10.1360/SSPMA2015-00428 2-s2.0-85018327643 · DOI
  140. [144]Chen M. Yin J. Liang Y. Oxidative stress and immunotoxicity induced by graphene oxide in zebrafish Aquatic toxicology 2016 174 54 60 10.1016/j.aquatox.2016.02.015 2-s2.0-84958955429 26921726 · DOI
  141. [145]Hu C. Wang Q. Zhao H. Wang L. Guo S. Li X. Ecotoxicological effects of graphene oxide on the protozoan Euglena gracilis Chemosphere 2015 128 184 190 10.1016/j.chemosphere.2015.01.040 2-s2.0-84925238969 25703902 · DOI
  142. [146]Li J. Zhang X. Jiang J. Systematic assessment of the toxicity and potential mechanism of graphene derivatives in vitro and in vivo Toxicological Sciences 2019 167 1 269 281 10.1093/toxsci/kfy235 2-s2.0-85059502009 30239936 · DOI
  143. [147]Mu Q. Su G. Li L. Size-dependent cell uptake of protein-coated graphene oxide nanosheets ACS Appl Mater Interfaces 2012 4 4 2259 2266 10.1021/am300253c 2-s2.0-84860322834 22409495 · DOI

Cited by

Sorted by citations

Authors
Rhazouani, A., Gamrani, H., El Achaby, M., Aziz, K., Gebrati, L., Uddin, M. S., & AZIZ, F.
Affiliations
  • Cadi Ayyad University (MA)
  • Université Ibn Zohr (MA)
  • Southeast University (BD)
Corresponding author
AZIZ, Faissal
ORCID
Venue
BioMed Research International
Publisher
Wiley
Published
2021-01
Volume
2021
Issue
1
Pages
5518999-5518999
ISSN
  • 1110-7243 (ISSN-L)
  • 2314-6133
  • 2314-6141
DOI
10.1155/2021/5518999
PMC
PMC8213470
OpenAlex
W3167660118
Cited by
221
References
2
Citations by year
2026: 33 · 2025: 43 · 2024: 47 · 2023: 49 · 2022: 41 · 2021: 8
FWCI
3.09
Type
journal article
Language
en
Open access
Licence
Locations
  • BioMed Research International (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • DUPC2: IHE Delft Partnership Programme for Water and Development
  • MENARA project
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Graphene and Nanomaterials Applications
  • Physical Sciences › Materials Science › Materials Chemistry › Graphene research and applications
  • Physical Sciences › Materials Science › Materials Chemistry › Nanoparticles: synthesis and applications
Keywords
graphene oxide, nanoparticle toxicity, graphene oxide synthesis, biocompatibility, physicochemical properties, cytotoxicity, in vivo toxicity, toxicity mechanisms, route of administration, dose-dependent effects, cancer therapy, drug delivery, cell imaging
MeSH terms
Algorithms, Animals, Biocompatible Materials, Crystallization, Graphite, Humans, Microscopy, Electron, Scanning, Magnetic Resonance Spectroscopy, Oxygen, Spectrum Analysis, Raman, Temperature, Thermogravimetry, X-Ray Diffraction, Reproducibility of Results, Drug Delivery Systems, Spectroscopy, Fourier Transform Infrared, Microscopy, Atomic Force, Microscopy, Electron, Transmission, Nanostructures, Nanomedicine, Rats, Nanoparticles, In Vitro Techniques

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review