Биомедицинское применение наноматериалов на основе графена в доставке генов, тканевой инженерии, биосенсорике и для разработки антибактериальных средств

Графен и оксид графена стали перспективными материалами в различных биомедицинских приложениях благодаря своим уникальным физико-химическим свойствам. В этом обзоре представлен всесторонний обзор их использования в доставке генов, тканевой инженерии, биосенсорах и антибактериальных и противомикробных агентах. В доставке генов материалы на основе графена предлагают эффективные платформы доставки с улучшенным клеточным поглощением и минимальной цитотоксичностью, что является многообещающим достижением в генной терапии. Кроме того, в тканевой инженерии графен и оксид графена демонстрируют превосходную биосовместимость, электропроводность и механические свойства, облегчая адгезию клеток, пролиферацию и дифференциацию для регенерации тканей. Более того, биосенсоры на основе графена демонстрируют высокую чувствительность, селективность и стабильность, что позволяет быстро и точно обнаруживать биомолекулы для диагностических и терапевтических целей. В этом обзоре освещаются последние достижения, проблемы и будущие перспективы графена и оксида графена в революционных биомедицинских технологиях, прокладывая путь для инновационных решений в здравоохранении. 

1. Abdelhalim A.O.E., Semenov K.N., Nerukh D.A., Murin I V., Maistrenko D.N., Molchanov O.E., Sharoyko V.V. Functionalisation of graphene as a tool for developing nanomaterials with predefined properties. J. Mol. Liq., 2022, 348, 118368.

2. Saharan R., Paliwal S.K., Tiwari A., Tiwari V., Singh R., Beniwal S.K., Dahiya P., Sagadevan S. Exploring graphene and its potential in delivery of drugs and biomolecules. J. Drug. Deliv. Sci. Technol., 2023, 84, 104446.

3. Lin J., Huang Y., Huang P. Graphene-Based Nanomaterials in Bioimaging, In Biomedical Applications of Functionalized Nanomaterials: Concepts, Development and Clinical Translation, 2018, Elsevier, P. 247–287.

4. Cao Z., Bian Y., Hu T., Yang Y., Cui Z., Wang T., Yang S., Weng X., Liang R., Tan C. Recent advances in two-dimensional nanomaterials for bone tissue engineering. J. of Materiomics, 2023, 9 (5), P. 930–958.

5. Prasad S.V.S., Kumar M., Arulananth T.S., Ravi B., Kumar B., Kiran Kumar B. Graphene/ZnO nanocomposite based optical biosensors. Mater Today Proc, 2023.

6. Kumar P., Huo P., Zhang R., Liu B. Antibacterial Properties of Graphene-Based Nanomaterials. Nanomaterials, 2019, 9 (5), 737.

7. Palmieri V., Papi M. Can graphene take part in the fight against COVID-19? Nano Today, 2020, 33, 100883.

8. Zhang Y., Zhang L., Zhou C. Review of chemical vapor deposition of graphene and related applications. Acc. Chem. Res., 2013, 46 (10), P. 2329– 2339.

9. Mu˜noz R., G´omez-Aleixandre C. Review of CVD synthesis of graphene. Chemical Vapor Deposition, 2013, 19 (10–12), P. 297–322.

10. Li X., Colombo L., Ruoff R.S. Synthesis of Graphene Films on Copper Foils by Chemical Vapor Deposition. Advanced Materials, 2016, 28 (29), P. 6247–6252.

11. Chen K., Shi L., Zhang Y., Liu Z. Scalable chemical-vapour-deposition growth of three-dimensional graphene materials towards energy-related applications. Chem. Soc. Rev., 2018, 47 (9), P. 3018–3036.

12. Yang X., Zhang G., Prakash J., Chen Z., Gauthier M., Sun S. Chemical vapour deposition of graphene: layer control, the transfer process, characterisation, and related applications. Int. Rev. Phys. Chem., 2019, 38 (2), P. 149–199.

13. Mattevi C., Kim H., Chhowalla M. A review of chemical vapour deposition of graphene on copper. J. Mater. Chem., 2011, 21 (10), P. 3324–3334.

14. Zhou H., Yu W.J., Liu L., Cheng R., Chen Y., Huang X., Liu Y., Wang Y., Huang Y., Duan X. Chemical vapour deposition growth of large single crystals of monolayer and bilayer graphene. Nat. Commun., 2013, 4 (1), P. 1–8.

15. Yu P., Lowe S.E., Simon G.P., Zhong Y.L. Electrochemical exfoliation of graphite and production of functional graphene. Curr. Opin. Colloid Interface Sci., 2015, 20 (5–6), P. 329–338.

16. Rao K.S., Senthilnathan J., Liu Y.F., Yoshimura M. Role of peroxide ions in formation of graphene nanosheets by electrochemical exfoliation of graphite. Sci. Rep., 2014, 4 (1),P. 1–6.

17. Wan H., Wei C., Zhu K., Zhang Y., Gong C., Guo J., Zhang J., Yu L. Zhang J. Preparation of graphene sheets by electrochemical exfoliation of graphite in confined space and their application in transparent conductive films. ACS Appl. Mater. Interfaces, 2017, 9 (39), P. 34456–34466.

18. Mir A., Shukla A. Bilayer-rich graphene suspension from electrochemical exfoliation of graphite. Mater. Des., 2018, 156, P. 62–70.

19. Melezhik A.V., Pershin V.F., Memetov N.R. Tkachev A.G. Mechanochemical synthesis of graphene nanoplatelets from expanded graphite compound. Nanotechnol. Russ., 2016, 11 (7–8), P. 421–429.

20. Abdelhalim A.O.E., Semenov K.N., Nerukh D.A., Murin I. V., Maistrenko D.N., Molchanov O.E., Sharoyko V.V. Functionalisation of graphene as a tool for developing nanomaterials with predefined properties. J. Mol. Liq., 2022, 348, 118368.

21. Abdelhalim A.O.E., Sharoyko V.V., Ageev S.V., Farafonov V.S., Nerukh D.A., Postnov V.N., Petrov A.V., Semenov K.N. Graphene Oxide of Extra High Oxidation: A Wafer for Loading Guest Molecules. J. Phys. Chem. Lett., 2021, 12 (41), P. 10015–10024.

22. Abdelhalim A.O.E., Meshcheriakov A.A., Maistrenko D.N., Molchanov O.E., Ageev S.V., Ivanova D.A., Iamalova N.R., Luttsev M.D., Vasina L.V., Sharoyko V.V., Semenov K.N. Graphene oxide enriched with oxygen-containing groups: on the way to an increase of antioxidant activity and biocompatibility. Colloids Surf B Biointerfaces, 2021, 112232.

23. Taneva S.G., Krumova S., Bog´ar F., Kincses A., Stoichev S., Todinova S., Danailova A., Horv´ath J., N´asztor Z., Kelemen L., D´er A. Insights into graphene oxide interaction with human serum albumin in isolated state and in blood plasma. Int. J. Biol. Macromol., 2021, 175, P. 19–29.

24. Anirudhan T.S., Chithra Sekhar V., Athira V.S. Graphene oxide based functionalized chitosan polyelectrolyte nanocomposite for targeted and pH responsive drug delivery. Int. J. Biol. Macromol., 2020, 150, P. 468–479.

25. Hummers W.S., Offeman R.E) Preparation of Graphitic Oxide. J. Am. Chem. Soc., 1958, 80 (6), P. 1339–1339.

26. Brodie B.C. On the atomic weight of graphite. Philos. Trans. R. Soc. Lond., 1859, 149 (1859), P. 249–259.

27. Staudenmaier L. Verfahren zur Darstellung der Graphits¨aure. Berichte der deutschen chemischen Gesellschaft, 1898, 31 (2), P. 1481–1487.

28. Abdelhalim A.O.E., Sharoyko V.V., Meshcheriakov A.A., Martynova S.D., Ageev S.V., Iurev G.O., Al Mulla H., Petrov A.V., Solovtsova I.L., Vasina L.V., Murin I.V., Semenov K.N. Reduction and functionalization of graphene oxide with L-cysteine: Synthesis, characterization and biocompatibility. Nanomedicine, 2020, 29, 102284.

29. Lavin-Lopez M.P., Paton-Carrero A., Sanchez-Silva L., Valverde J.L., Romero A. Influence of the reduction strategy in the synthesis of reduced graphene oxide. Advanced Powder Technology, 2017, 28 (12), P. 3195–3203.

30. Guex L.G., Sacchi B., Peuvot K.F., Andersson R.L., Pourrahimi A.M., Str¨om V., Farris S., Olsson R.T. Experimental review: Chemical reduction of graphene oxide (GO) to reduced graphene oxide (rGO) by aqueous chemistry. Nanoscale, 2017, 9 (27), P. 9562–9571.

31. De Silva K.K.H., Huang H.H., Joshi R.K., Yoshimura M. Chemical reduction of graphene oxide using green reductants. Carbon N.Y., 2017, 119, P. 190–199.

32. Wang J., Salihi E.C., siller L. Green reduction of graphene oxide using alanine. Materials Science and Engineering C, 2017, 72, P. 1–6.

33. Alam S.N., Sharma N., Kumar L. Synthesis of Graphene Oxide (GO) by Modified Hummers Method and Its Thermal Reduction to Obtain Reduced Graphene Oxide (rGO)*. Graphene, 2017, 06 (01), P. 1–18.

34. Saleem H., Haneef M., Abbasi H.Y. Synthesis route of reduced graphene oxide via thermal reduction of chemically exfoliated graphene oxide. Mater. Chem. Phys., 2018, 204, P. 1–7.

35. Oliveira A.E.F., Braga G.B., Tarley C.R.T., Pereira A.C. Thermally reduced graphene oxide: synthesis, studies and characterization. J. Mater. Sci., 2018, 53 (17), P. 12005–12015.

36. Schedy A., Oetken M. The thermal reduction of graphene oxide – A simple and exciting manufacturing process of graphene. CHEMKON, 2020, 27 (5), P. 244–249.

37. Liu Z., Navik R., Tan H., Xiang Q., Wahyudiono Goto M., Ibarra R.M., Zhao Y. Graphene-based materials prepared by supercritical fluid technology and its application in energy storage. J. Supercrit. Fluids, 2022, 188, 105672.

38. Mann R., Mitsidis D., Xie Z., McNeilly O., Ng Y.H., Amal R., Gunawan C. Antibacterial Activity of Reduced Graphene Oxide. J. Nanomater., 2021, 2021, P. 1–10.

39. Robinson J.T., Perkins F.K., Snow E.S., Wei Z., Sheehan P.E. Reduced Graphene Oxide Molecular Sensors. Nano Lett., 2008, 8 (10), P. 3137–3140.

40. Dong N., Ye Q., Zhang D., Xiao Y., Dai H. Reduced graphene oxide as an effective promoter to the layered manganese oxide-supported Ag catalysts for the oxidation of ethyl acetate and carbon monoxide. J. Hazard Mater., 2022, 431, 128518.

41. Zhao J., Tang L., Xiang J., Ji R., Yuan J., Zhao J., Yu R., Tai Y., Song L. Chlorine doped graphene quantum dots: Preparation, properties, and photovoltaic detectors. Appl. Phys. Lett., 2014, 105 (11).

42. Mueller M.L., Yan X., McGuire J.A., Li L. Triplet States and Electronic Relaxation in Photoexcited Graphene Quantum Dots. Nano Lett., 2010, 10 (7), P. 2679–2682.

43. Tang L., Ji R., Li X., Teng K.S., Lau S.P. Energy-level structure of nitrogen-doped graphene quantum dots. J. Mater. Chem. C Mater., 2013, 1 (32), 4908.

44. Peng J., Gao W., Gupta B.K., Liu Z., Romero-Aburto R., Ge L., Song L., Alemany L.B., Zhan X., Gao G., Vithayathil S.A., Kaipparettu B.A., Marti A.A., Hayashi T., Zhu J.-J., Ajayan P.M. Graphene Quantum Dots Derived from Carbon Fibers. Nano Lett., 2012, 12 (2), P. 844–849.

45. 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 (5874), P. 356–358.

46. Shen J., Zhu Y., Yang X., Zong J., Zhang J., Li C. One-pot hydrothermal synthesis of graphenequantum dots surface-passivated by polyethylene glycol and their photoelectric conversion under near-infrared light. New J. Chem., 2012, 36 (1), P. 97–101.

47. Gupta V., Chaudhary N., Srivastava R., Sharma G.D., Bhardwaj R., Chand S. Luminscent Graphene Quantum Dots for Organic Photovoltaic Devices. J. Am. Chem. Soc., 2011, 133 (26), P. 9960–9963.

48. Lin L., Zhang S. Creating high yield water soluble luminescent graphene quantum dots via exfoliating and disintegrating carbon nanotubes and graphite flakes. Chemical Communications, 2012, 48 (82), 10177.

49. Danaeifar M. Recent advances in gene therapy: genetic bullets to the root of the problem. Clin. Exp. Med., 2022, 23 (4), P. 1107–1121.

50. Wong J.K.L., Mohseni R., Hamidieh A.A., MacLaren R.E., Habib N., Seifalian A.M. Will Nanotechnology Bring New Hope for Gene Delivery? Trends Biotechnol., 2017, 35 (5), P. 434–451.

51. Yin H., Kanasty R.L., Eltoukhy A.A., Vegas A.J., Dorkin J.R., Anderson D.G. Non-viral vectors for gene-based therapy. Nat. Rev. Genet., 2014, 15 (8), P. 541–555.

52. Cao X., Zheng S., Zhang S., Wang Y., Yang X., Duan H., Huang Y., Chen Y. Functionalized Graphene Oxide with Hepatocyte Targeting as Anti-Tumor Drug and Gene Intracellular Transporters. J. Nanosci. Nanotechnol., 2015, 15 (3), P. 2052–2059.

53. Choi H.Y., Lee T.-J., Yang G.-M., Oh J., Won J., Han J., Jeong G.-J., Kim J., Kim J.-H., Kim B.-S., Cho S.-G. Efficient mRNA delivery with graphene oxide-polyethylenimine for generation of footprint-free human induced pluripotent stem cells. J. of Controlled Release, 2016, 235, P. 222–235.

54. Goenka S., Sant V., Sant S. Graphene-based nanomaterials for drug delivery and tissue engineering. J. of Controlled Release, 2014, 173, P. 75–88.

55. Teimouri M., Nia A.H., Abnous K., Eshghi H., Ramezani M. Graphene oxide–cationic polymer conjugates: Synthesis and application as gene delivery vectors. Plasmid., 2016, 84–85, P. 51–60.

56. Hu H., Tang C., Yin C. Folate conjugated trimethyl chitosan/graphene oxide nanocomplexes as potential carriers for drug and gene delivery. Mater. Lett., 2014, 125, P. 82–85.

57. Yin D., Li Y., Lin H., Guo B., Du Y., Li X., Jia H., Zhao X., Tang J., Zhang L. Functional graphene oxide as a plasmid-based Stat3 siRNA carrier inhibits mouse malignant melanoma growth in vivo. Nanotechnology, 2013, 24 (10), 105102.

58. Zhi F., Dong H., Jia X., Guo W., Lu H., Yang Y., Ju H., Zhang X., Hu Y. Functionalized Graphene Oxide Mediated Adriamycin Delivery and miR-21 Gene Silencing to Overcome Tumor Multidrug Resistance In Vitro. PLoS One, 2013, 8 (3), e60034.

59. Cheng F.-F., Chen W., Hu L.-H., Chen G., Miao H.-T., Li C., Zhu J.-J. Highly dispersible PEGylated graphene/Au composites as gene delivery vector and potential cancer therapeutic agent. J. Mater. Chem. B, 2013, 1 (38), 4956.

60. Tripathi S.K., Goyal R., Gupta K.C., Kumar P. Functionalized graphene oxide mediated nucleic acid delivery. Carbon N.Y., 2013, 51, P. 224–235.

61. He Y., Zhang L., Chen Z., Liang Y., Zhang Y., Bai Y., Zhang J., Li Y. Enhanced chemotherapy efficacy by co-delivery of shABCG2 and doxorubicin with a pH-responsive charge-reversible layered graphene oxide nanocomplex. J. Mater. Chem. B, 2015, 3 (31), P. 6462–6472.

62. Yin F., Hu K., Chen Y., Yu M., Wang D., Wang Q., Yong K.-T., Lu F., Liang Y., Li Z. SiRNA Delivery with PEGylated Graphene Oxide Nanosheets for Combined Photothermal and Genetherapy for Pancreatic Cancer. Theranostics, 2017, 7 (5), P. 1133–1148.

63. Feng L., Zhang S., Liu Z. Graphene based gene transfection. Nanoscale, 2011, 3 (3), 1252.

64. Teng Y.D., Lavik E.B., Qu X., Park K.I., Ourednik J., Zurakowski D., Langer R., Snyder E.Y. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proceedings of the National Academy of Sciences, 2002, 99 (5), P. 3024–3029.

65. Solanki A., Chueng S.D., Yin P.T., Kappera R., Chhowalla M., Lee K. Axonal Alignment and Enhanced Neuronal Differentiation of Neural Stem Cells on Graphene? Nanoparticle Hybrid Structures. Advanced Materials, 2013, 25 (38), P. 5477–5482.

66. Setia Budi H., Javed Ansari M., Abdalkareem Jasim S., Abdelbasset W.K., Bokov D., Fakri Mustafa Y., Najm M.A.A., Kazemnejadi M. Preparation of antibacterial Gel/PCL nanofibers reinforced by dicalcium phosphate-modified graphene oxide with control release of clindamycin for possible application in bone tissue engineering. Inorg. Chem. Commun., 2022, 139, 109336.

67. Amiryaghoubi N., Fathi M., Barar J., Omidian H., Omidi Y. Recent advances in graphene-based polymer composite scaffolds for bone/cartilage tissue engineering. J. Drug Deliv. Sci. Technol., 2022, 72, 103360.

68. Sharifi S., Ebrahimian-Hosseinabadi M., Dini G., Toghyani S. Magnesium-zinc-graphene oxide nanocomposite scaffolds for bone tissue engineering. Arabian J. of Chemistry, 2023, 16 (6), 104715.

69. Ghosal K., Mondal P., Bera S., Ghosh S. Graphene family nanomaterials-opportunities and challenges in tissue engineering applications. FlatChem, 2021, 30, 100315.

70. Challa A.A., Saha N., Szewczyk P.K., Karbowniczek J.E., Stachewicz U., Ngwabebhoh F.A., Saha P. Graphene oxide produced from spent coffee grounds in electrospun cellulose acetate scaffolds for tissue engineering applications. Mater Today Commun., 2023, 35, 105974.

71. Motiee E.-S., Karbasi S., Bidram E., Sheikholeslam M. Investigation of physical, mechanical and biological properties of polyhydroxybutyrate-chitosan/graphene oxide nanocomposite scaffolds for bone tissue engineering applications. Int. J. Biol. Macromol., 2023, 247, 125593.

72. Babakhani A., Peighambardoust S.J., Olad A. Fabrication of magnetic nanocomposite scaffolds based on polyvinyl alcohol-chitosan containing hydroxyapatite and clay modified with graphene oxide: Evaluation of their properties for bone tissue engineering applications. J. Mech. Behav. Biomed. Mater, 2024, 150, 106263.

73. Amiryaghoubi N., Fathi M., Barar J., Omidian H., Omidi Y. Hybrid polymer-grafted graphene scaffolds for microvascular tissue engineering and regeneration. Eur. Polym. J., 2023, 193, 112095.

74. Saravanan S., Sareen N., Abu-El-Rub E., Ashour H., Sequiera G.L., Ammar H.I., Gopinath V., Shamaa A.A., Sayed S.S.E., Moudgil M., Vadivelu J., Dhingra S. Graphene Oxide-Gold Nanosheets Containing Chitosan Scaffold Improves Ventricular Contractility and Function After Implantation into Infarcted Heart. Sci. Rep., 2018, 8 (1), 15069.

75. Park J., Kim B., Han J., Oh J., Park S., Ryu S., Jung S., Shin J.-Y., Lee B.S., Hong B.H., Choi D., Kim B.-S. Graphene Oxide Flakes as a Cellular Adhesive: Prevention of Reactive Oxygen Species Mediated Death of Implanted Cells for Cardiac Repair. ACS Nano, 2015, 9 (5), P. 4987–4999.

76. Shin Y.C., Lee J.H., Jin L., Kim M.J., Kim Y.-J., Hyun J.K., Jung T.-G., Hong S.W., Han D.-W. Stimulated myoblast differentiation on graphene oxide-impregnated PLGA-collagen hybrid fibre matrices. J. Nanobiotechnology, 2015, 13 (1), 21.

77. Chaudhuri B., Bhadra D., Moroni L., Pramanik K. Myoblast differentiation of human mesenchymal stem cells on graphene oxide and electrospun graphene oxide–polymer composite fibrous meshes: importance of graphene oxide conductivity and dielectric constant on their biocompatibility. Biofabrication, 2015, 7 (1), 015009.

78. Shahmoradi S., Golzar H., Hashemi M., Mansouri V., Omidi M., Yazdian F., Yadegari A., Tayebi L. Optimizing the nanostructure of graphene oxide/silver/arginine for effective wound healing. Nanotechnology, 2018, 29 (47), 475101.

79. Boga J.C., Miguel S.P., de Melo-Diogo D., Mendonc¸a A.G., Louro R.O., Correia I.J. In vitro characterization of 3D printed scaffolds aimed at bone tissue regeneration. Colloids Surf B Biointerfaces, 2018, 165, P. 207–218.

80. Faghihi S., Karimi A., Jamadi M., Imani R., Salarian R. Graphene oxide/poly(acrylic acid)/gelatin nanocomposite hydrogel: Experimental and numerical validation of hyperelastic model. Materials Science and Engineering: C, 2014, 38, P. 299–305.

81. Liu H., Cheng J., Chen F., Bai D., Shao C., Wang J., Xi P., Zeng Z. Gelatin functionalized graphene oxide for mineralization of hydroxyapatite: biomimetic and in vitro evaluation. Nanoscale, 2014, 6 (10), 5315.

82. Yu P., Bao R.-Y., Shi X.-J., Yang W., Yang M.-B. Self-assembled high-strength hydroxyapatite/graphene oxide/chitosan composite hydrogel for bone tissue engineering. Carbohydr. Polym., 2017, 155, P. 507–515.

83. Wang L., Lu R., Hou J., Nan X., Xia Y., Guo Y., Meng K., Xu C., Wang X., Zhao B. Application of injectable silk fibroin/graphene oxide hydrogel combined with bone marrow mesenchymal stem cells in bone tissue engineering. Colloids Surf A Physicochem. Eng. Asp., 2020, 604, 125318.

84. Qin H., Ji Y., Li G., Xu X., Zhang C., Zhong W., Xu S., Yin Y., Song J. MicroRNA-29b/graphene oxide–polyethyleneglycol–polyethylenimine complex incorporated within chitosan hydrogel promotes osteogenesis. Front Chem., 2022, 10.

85. Khan M.R., Huang C., Ullah R., Ullah H., Qazi I.M., Nawaz T., Adnan M., Khan A., Su H., Ren L. Effects of Various Polymeric Films on the Pericarp Microstructure and Storability of Longan (cv. Shixia) Fruit Treated with Propyl Disulfide Essential Oil from the Neem (Azadirachta indica) Plant. Polymers (Basel), 2022, 14 (3), 536.

86. Xue B., Sheng H., Li Y., Li L., Di W., Xu Z., Ma L., Wang X., Jiang H., Qin M., Yan Z., Jiang Q., Liu J.-M., Wang W., Cao Y. Stretchable and self-healable hydrogel artificial skin. Natl. Sci. Rev., 2022, 9 (7).

87. Zhao, P., Zhang Y., Chen X., Xu C., Guo J., Deng M., Qu X., Huang P., Feng Z., Zhang J. Versatile Hydrogel Dressing with Skin Adaptiveness and Mild Photothermal Antibacterial Activity for Methicillin?Resistant Staphylococcus Aureus?Infected Dynamic Wound Healing. Advanced Science, 2023, 10 (11).

88. Zhou J., Yang X., Liu W., Wang C., Shen Y., Zhang F., Zhu H., Sun H., Chen J., Lam J., Mikos A.G., Wang C. Injectable OPF/graphene oxide hydrogels provide mechanical support and enhance cell electrical signaling after implantation into myocardial infarct. Theranostics, 2018, 8 (12), P. 3317–3330.

89. Yuan Z., Qin Q., Yuan M., Wang H., Li R. Development and novel design of clustery graphene oxide formed Conductive Silk hydrogel cell vesicle to repair and routine care of myocardial infarction: Investigation of its biological activity for cell delivery applications. J. Drug Deliv. Sci. Technol., 2020, 60, 102001.

90. Chinemerem Nwobodo D., Ugwu M.C., Oliseloke Anie C., Al-Ouqaili M.T.S., Chinedu Ikem J., Victor Chigozie U., Saki M. Antibiotic resistance: The challenges and some emerging strategies for tackling a global menace. J. Clin. Lab. Anal., 2022, 36 (9).

91. Mitsunaga M., Ito K., Nishimura T., Miyata H., Miyakawa K., Morita T., Ryo A., Kobayashi H., Mizunoe Y., Iwase T. Antimicrobial strategy for targeted elimination of different microbes, including bacterial, fungal and viral pathogens. Commun. Biol., 2022, 5 (1), 647.

92. Kulakova I.I., Lisichkin G.V. Potential Directions in the Use of Graphene Nanomaterials in Pharmacology and Biomedicine (Review). Pharm. Chem. J., 2022, 56 (1), P. 1–11.

93. Bousiakou L.G., Qindeel R., Al-Dossary O.M., Kalkani H. Synthesis and characterization of graphene oxide (GO) sheets for pathogen inhibition: Escherichia coli, Staphylococcus aureus and Pseudomonas aeruginosa. J. King Saud. Univ. Sci., 2022, 34 (4), 102002.

94. Dan S., Bagheri H., Shahidizadeh A., Hashemipour H. Performance of graphene Oxide/SiO2 Nanocomposite-based: Antibacterial Activity, dye and heavy metal removal. Arabian J. of Chemistry, 2023, 16 (2), 104450.

95. Tariq M., Khan A.U., Rehman A.U., Ullah S., Jan A.U., Zakareya Khan Z.U.H., Muhammad N., Islam Z.U., Yuan Q. Green synthesis of Zno@GO nanocomposite and its’ efficient antibacterial activity. Photodiagnosis Photodyn. Ther., 2021, 35, 102471.

96. Bhatt S., Punetha V.D., Pathak R., Punetha M. Graphene in nanomedicine: A review on nano-bio factors and antibacterial activity. Colloids Surf B Biointerfaces, 2023, 226, 113323.

97. Abdollahzadeh S., Sayadi M.H., Shekari H. Synthesis of biodegradable antibacterial nanocomposite (metal–organic frameworks supported by chitosan and graphene oxide) with high stability and photocatalytic activities. Inorg. Chem. Commun., 2023, 156, 111302.

98. Bentedlaouti K., Belouatek A., Kebaili N. Antibacterial and antioxidant activities of graphene and graphene oxide synthesis coated silver nanoparticules. J. Cryst. Growth, 2024, 627, 127527.

99. Khan A., Zaid M., Ameen F., Khan Mo.A., Kumar S., Al-Masri A.A., Islam M.A. Colossal antibacterial, antibiofilm and solar light-driven photocatalytic activity of nanoenhanced conjugate of bimetallic Ag-Zr nanoparticles with graphene oxide. J. Mol. Struct., 2024, 1300, 137223.

100. Dwitya S.S., Hsueh Y.-H., Wang S.S.-S., Lin K.-S. Ultrafine nitrogen-doped graphene quantum dot structure and antibacterial activities against Bacillus subtilis 3610. Mater. Chem. Phys., 2023, 295, 127135.

101. Avatefi Hemmat M., Asghari S., Bakhshesh M., Mahmoudifard M. Copper iodide decorated graphene oxide as a highly efficient antibacterial and antiviral nanocomposite. Inorg. Chem. Commun., 2023, 156, 111214.

102. Fardinpour P., Ghafouri Taleghani H., Reza Zakerimehr M. Facile green synthesis of graphene oxide/copper oxide nanocomposites using ginger essential oil and its enhanced antibacterial properties. Materials Science and Engineering: B, 2024, 300, 117100.

103. Aissou T., Jann J., Faucheux N., Fortier L.-C., Braidy N., Veilleux J. Suspension plasma sprayed copper-graphene coatings for improved antibacterial properties. Appl. Surf. Sci., 2023, 639, 158204.

104. Yang F., Huo D., Zhang J., Lin T., Zhang J., Tan S., Yang L. Fabrication of graphene oxide/copper synergistic antibacterial coating for medical titanium substrate. J. Colloid Interface Sci., 2023, 638, P. 1–13.

105. Abdelhalim A.O.E., Galal A., Hussein M.Z., El Sayed I.E.-T. Graphene Functionalization by 1,6-Diaminohexane and Silver Nanoparticles for Water Disinfection. J. Nanomater., 2016, 2016, P. 1–7.

106. Derakhshi M., Ashkarran A.A., Bahari A., Bonakdar S. Shape selective silver nanostructures decorated amine-functionalized graphene: A promising antibacterial platform. Colloids Surf. A Physicochem. Eng. Asp., 2018, 545, P. 101–109.

107. Chen P., Ze R., Xia X., Zhang Z., Lu K., Wei L., Zhou B. Composite porphyrin-based conjugated microporous polymer/graphene oxide capable of photo-triggered combinational antibacterial therapy and wound healing. Biomaterials Advances, 2023, 154, 213662.

108. Wang Z., Liu G., Chen W., Zhang L., Qi Z., Bai G., Fan Y., Liu C., Xiao C., Li W., Chang Y., Liang G., Zhou Z., Yu P., Song Z., Ning C. Contribution of surface plasmonic resonance to enhanced photocatalytic antibacterial performance of graphene-based two-dimensional heterojunction. Chemical Engineering J., 2023, 460, 141720.

109. Sun J., Liu X., Lyu C., Hu Y., Zou D., He Y.S., Lu J. Synergistic antibacterial effect of graphene-coated titanium loaded with levofloxacin. Colloids Surf. B Biointerfaces, 2021, 208, 112090.

110. Kumar S., Singh H., Feder-kubis J., Nguyen D.D. Recent advances in nanobiosensors for sustainable healthcare applications: A systematic literature review. Environ. Res., 2023, 238 (P2), 117177.

111. Arshad F., Nabi F., Iqbal S., Khan R.H. Applications of graphene-based electrochemical and optical biosensors in early detection of cancer biomarkers. Colloids Surf. B Biointerfaces, 2022, 212, 112356.

112. Oliveira M.E., Lopes B.V., Rossato J.H.H., Maron G.K., Gallo B.B., La Rosa A.B., Balboni R.D.C., Alves M.L.F., Ferreira M.R.A., da Silva Pinto L., Conceic¸˜ao F.R., Piva E., de Pereira C.M.P., Escote M.T., Carre˜no N.L.V. Electrochemical Biosensor Based on Laser-Induced Graphene for COVID-19 Diagnosing: Rapid and Low-Cost Detection of SARS-CoV-2 Biomarker Antibodies. Surfaces, 2022, 5 (1), P. 187–201.

113. Bai Y., Xu T., Zhang X. Graphene-Based Biosensors for Detection of Biomarkers. Micromachines, 2020, 11 (1), 60.

114. Pe˜na-Bahamonde J., Nguyen H.N., Fanourakis S.K., Rodrigues D.F. Recent advances in graphene-based biosensor technology with applications in life sciences. J. Nanobiotechnology, 2018, 16 (1), P. 1–17.

115. Sharifi M., Hasan A., Attar F., Taghizadeh A., Falahati M. Development of point-of-care nanobiosensors for breast cancers diagnosis. Talanta, 2020, 217.

116. Irkham I., Ibrahim A.U., Pwavodi P.C., Al-Turjman F., Hartati Y.W. Smart Graphene-Based Electrochemical Nanobiosensor for Clinical Diagnosis: Review. Sensors (Basel), 2023, 23 (4).

117. Achi F., Attar A.M., Ait Lahcen A. Electrochemical nanobiosensors for the detection of cancer biomarkers in real samples: Trends and challenges. TrAC Trends in Analytical Chemistry, 2023, 117423.

118. Wu T., Shen J., Li Z., Xing F., Xin W., Wang Z., Liu G., Han X., Man Z., Fu S. Microfluidic-integrated graphene optical sensors for real-time and ultra-low flow velocity detection. Appl. Surf. Sci., 2021, 539, 148232.

119. Mondal R., Dam P., Chakraborty J., Paret M.L., Kati A., Altuntas S., Sarkar R., Ghorai S., Gangopadhyay D., Mandal A.K., Husen A. Potential of nanobiosensor in sustainable agriculture: the state-of-art. Heliyon, , 8 (12), e12207.

120. Bakhshpour M., G¨okt¨urk I., G¨ur S.D., Yilmaz F., Denizli A. Sensor Applications for Detection in Agricultural Products, Foods, and Water, in Pesticides Bioremediation, 2022, Springer International Publishing, Cham, P. 311–352.

121. Hern´andez R., Vall´es C., Benito A.M., Maser W.K., Xavier Rius F., Riu J. Graphene-based potentiometric biosensor for the immediate detection of living bacteria. Biosens. Bioelectron., 2014, 54, P. 553–557.

122. Cai Y., Chen D., Chen Y., Li T., Wang L., Jiang J., Guo Z., Jaffrezic-Renault N., Zhang Z., Huang S. An electrochemical biosensor based on graphene intercalated functionalized black phosphorus/gold nanoparticles nanocomposites for the detection of bacterial enzyme. Microchemical J., 2023, 193, 109255.

123. Yang X., Yin Z.Z., Zheng G., Zhou M., Zhang H., Li J., Cai W., Kong Y. Molecularly imprinted miniature electrochemical biosensor for SARS-CoV-2 spike protein based on Au nanoparticles and reduced graphene oxide modified acupuncture needle. Bioelectrochemistry, 2023, 151, 108375.

124. Gao J., Wang C., Chu Y., Han Y., Gao Y., Wang Y., Wang C., Liu H., Han L., Zhang Y. Graphene oxide-graphene Van der Waals heterostructure transistor biosensor for SARS-CoV-2 protein detection. Talanta, 2022, 240, 123197.

125. Malla P., Liu C.H., Wu W.C., Kabinsing P., Sreearunothai P. Synthesis and characterization of Au-decorated graphene oxide nanocomposite for magneto-electrochemical detection of SARS-CoV-2 nucleocapsid gene. Talanta, 2023, 262, 124701.

126. Lahcen A.A., Rauf S., Aljedaibi A., de Oliveira Filho J.I., Beduk T., Mani V., Alshareef H.N., Salama K.N. Laser-scribed graphene sensor based on gold nanostructures and molecularly imprinted polymers: Application for Her-2 cancer biomarker detection. Sens Actuators B Chem., 2021, 347, 130556.

127. Wu T.Z., Jian C.R., Govindasamy M., Li Y.C., Lin Y.T., Su C.Y., Samukawa S., Huang C.H. Crumpled graphene induced by commercial Heat-Shrinkable material for chemiresistive biosensors toward cancer biomarker detection. Microchemical J., 2023, 195, 109469.

128. Yan M., Fu L. ling Feng H. chao Namadchian M. Application of Ag nanoparticles decorated on graphene nanosheets for electrochemical sensing of CEA as an important cancer biomarker. Environ. Res., 2023, 239, 117363.

129. Rajaji U., Muthumariyappan A., Chen S.M., Chen T.W., Ramalingam R.J. A novel electrochemical sensor for the detection of oxidative stress and cancer biomarker (4-nitroquinoline N-oxide) based on iron nitride nanoparticles with multilayer reduced graphene nanosheets modified electrode. Sens Actuators B Chem., 2019, 291, P. 120–129.

130. Rauf S., Mishra G.K., Azhar J., Mishra R.K., Goud K.Y., Nawaz M.A.H., Marty J.L., Hayat A. Carboxylic group riched graphene oxide based disposable electrochemical immunosensor for cancer biomarker detection. Anal. Biochem., 2018, 545, P. 13–19.

131. Kumar S., Gupta N., Malhotra B.D. Ultrasensitive biosensing platform based on yttria doped zirconia-reduced graphene oxide nanocomposite for detection of salivary oral cancer biomarker. Bioelectrochemistry, 2021, 140, 107799.

132. Singh V.K., Kumar S., Pandey S.K., Srivastava S., Mishra M., Gupta G., Malhotra B.D., Tiwari R.S., Srivastava A. Fabrication of sensitive bioelectrode based on atomically thin CVD grown graphene for cancer biomarker detection. Biosens. Bioelectron., 2018, 105, P. 173–181.

133. Sadeghi M., Kashanian S., Naghib S.M., Haghiralsadat F., Tofighi D. An Efficient Electrochemical Biosensor Based on Pencil Graphite Electrode Mediated by 2D Functionalized Graphene Oxide to Detect HER2 Breast Cancer Biomarker. Int. J. Electrochem. Sci., 2022, 17 (4), 220459.

134. Chen T.W., Rajaji U., Chen S.M., Li Y.L., Ramalingam R.J. Ultrasound-assisted synthesis of α-MnS (alabandite) nanoparticles decorated reduced graphene oxide hybrids: Enhanced electrocatalyst for electrochemical detection of Parkinson’s disease biomarker. Ultrason. Sonochem., 2019, 56, P. 378–385.