In vivo toxicity and antitumor activity of newly green synthesized reduced graphene oxide/silver nanocomposites

Mohamed M. El-Zahed , Zakaria A. Baka , Mohamed I. Abou-Dobara , Ahmed K. El-Sayed , Magy M. Aboser , Ayman Hyder

Bioresources and Bioprocessing ›› 2021, Vol. 8 ›› Issue (1) : 44

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Bioresources and Bioprocessing ›› 2021, Vol. 8 ›› Issue (1) : 44 DOI: 10.1186/s40643-021-00400-7
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In vivo toxicity and antitumor activity of newly green synthesized reduced graphene oxide/silver nanocomposites

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Abstract

A novel biosynthesis of dual reduced graphene oxide/silver nanocomposites (rGO/AgNC) using the crude metabolite of Escherichia coli D8 (MF06257) strain and sunlight is introduced in this work. Physicochemical analysis of these rGO/AgNC revealed that they are sheet-like structures having spherically shaped silver nanoparticles (AgNPs) with an average particle size of 8 to 17 nm, and their absorption peak ranged from 350 to 450 nm. The biosynthesized rGO/AgNC were characterized by UV–vis and FT-IR spectra, X-ray diffraction, Zeta potential and transmission electron microscopy. After the injection of these nanocomposites to mice, their uptake by the kidney and liver has been proven by the ultrastructural observation and estimation of the hepatic and renal silver content. These nanocomposites caused a moderate toxicity for both organs. Changes in the liver and kidney functions and histopathological effects had been observed. The rGO/AgNC revealed a remarkable antitumor effect. They showed a dose-dependent cytotoxic effect on Ehrlich ascites carcinoma (EAC) cells in vitro. Treatment of mice bearing EAC tumors intraperitoneally with 10 mg/kg rGO/AgNC showed an antiproliferative effect on EAC cells, reduced ascites volume, and maintained mice survival. The results indicate that this green synergy of silver nanoparticles with reduced graphene oxide may have a promising potential in cancer therapy.

Keywords

Reduced graphene oxide / Silver nanoparticles / In vivo toxicity / Nanocomposites / Antitumor / Ehrlich ascites carcinoma

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Mohamed M. El-Zahed, Zakaria A. Baka, Mohamed I. Abou-Dobara, Ahmed K. El-Sayed, Magy M. Aboser, Ayman Hyder. In vivo toxicity and antitumor activity of newly green synthesized reduced graphene oxide/silver nanocomposites. Bioresources and Bioprocessing, 2021, 8(1): 44 DOI:10.1186/s40643-021-00400-7

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References

[1]

Ali AA, Madkour M, Sagheer FA, Zaki MI, Abdel Nazeer A. Low-temperature catalytic CO oxidation over non-noble, efficient chromia in reduced graphene oxide and graphene oxide nanocomposites. Catalysts, 2020, 10(1): 105.

[2]

Alsharaeh E, Alazzam S, Ahmed F, Arshi N, Al-Hindawi M, Sing GK. Green synthesis of silver nanoparticles and their reduced graphene oxide nanocomposites as antibacterial agents: A bio-inspired approach. Acta Metallurgica Sinica (english Letters), 2017, 30(1): 45-52.

[3]

Anand A, Unnikrishnan B, Wei S-C, Chou CP, Zhang L-Z, Huang C-C. Graphene oxide and carbon dots as broad-spectrum antimicrobial agents—a minireview. Nanoscale Horizons, 2019, 4(1): 117-137.

[4]

AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano, 2009, 3(2): 279-290.

[5]

Awwad AM, Salem NM, Aqarbeh MM, Abdulaziz FM. Green synthesis, characterization of silver sulfide nanoparticles and antibacterial activity evaluation. Chem Int, 2020, 6(1): 42-48.

[6]

Bao Q, Zhang D, Qi P. Synthesis and characterization of silver nanoparticle and graphene oxide nanosheet composites as a bactericidal agent for water disinfection. J Colloid Interface Sci, 2011, 360(2): 463-470.

[7]

Ceran ÖB, Şimşek B, Şara ON. Preparation and characterization novel dioctyl terephthalate blended polyvinyl alcohol-composite films incorporated with the graphene oxide and silver nanoparticles. Polym Testing, 2020, 82: 106315.

[8]

Choi YJ, Gurunathan S, Kim JH. Graphene oxide–silver nanocomposite enhances cytotoxic and apoptotic potential of salinomycin in human ovarian cancer stem cells (OvCSCs): a novel approach for cancer therapy. Int J Mol Sci, 2018, 19(3): 710.

[9]

Chook SW, Chia CH, Zakaria S, Ayob MK, Chee KL, Huang NM, Neoh HM, Lim HN, Jamal R, Rahman R. Antibacterial performance of Ag nanoparticles and AgGO nanocomposites prepared via rapid microwave-assisted synthesis method. Nanoscale Res Lett, 2012, 7(1): 1-7.

[10]

Cobos M, De-La-Pinta I, Quindós G, Fernández MJ, Fernández MD. Graphene oxide–silver nanoparticle nanohybrids: Synthesis, characterization, and antimicrobial properties. Nanomaterials, 2020, 10(2): 376.

[11]

Danaei M, Dehghankhold M, Ataei S, Hasanzadeh Davarani F, Javanmard R, Dokhani A, Mozafari MR. Impact of particle size and polydispersity index on the clinical applications of lipidic nanocarrier systems. Pharmaceutics, 2018, 10(2): 57.

[12]

de Faria AF, Martinez DST, Meira SMM, de Moraes ACM, Brandelli A, Souza Filho AG, Alves OL. Anti-adhesion and antibacterial activity of silver nanoparticles supported on graphene oxide sheets. Colloids Surf B, 2014, 113: 115-124.

[13]

Dhanavel S, Revathy TA, Sivaranjani T, Sivakumar K, Palani P, Narayanan V, Stephen A. 5-Fluorouracil and curcumin co-encapsulated chitosan/reduced graphene oxide nanocomposites against human colon cancer cell lines. Polym Bull, 2020, 77(1): 213-233.

[14]

Eldeeb E, Fahmy S, Elbakry K, Hyder A. A single dose of the antineoplastics hydroxyurea or cisplatin has praziquantel-like effects on Schistosoma mansoni worms and host mouse liver. Biomed Pharmacother, 2018, 99: 570-575.

[15]

El-Dein MMN, Baka ZA, Abou-Dobara MI, El-Sayed AK, El-Zahed MM. extracellular biosynthesis, optimization, characterization and antimicrobial potential of Escherichia coli D8 silver nanoparticles. J Microbiol Biotechnol Food Sci, 2021, 10(4): 648-656.

[16]

Elsharawy K, Abou-Dobara M, El-Gammal H, Hyder A. Chitosan coating does not prevent the effect of the transfer of green silver nanoparticles biosynthesized by Streptomyces malachitus into fetuses via the placenta. Reprod Biol, 2020, 20(1): 97-105.

[17]

El-Sonbaty SM. Fungus-mediated synthesis of silver nanoparticles and evaluation of antitumor activity. Cancer Nanotechnology, 2013, 4(4–5): 73-79.

[18]

Faria AF, Martinez DST, Moraes ACM, Maia da Costa MEH, Barros EB, Souza Filho AG, Paula AJ, Alves OL. Unveiling the role of oxidation debris on the surface chemistry of graphene through the anchoring of Ag nanoparticles. Chem Mater, 2012, 24(21): 4080-4087.

[19]

Galvez AM, Ramos KM, Teja AJ, Baculi R. Bacterial exopolysaccharide-mediated synthesis of silver nanoparticles and their application on bacterial biofilms. J Microbiol Biotechnol Food Sci, 2021, 2021: 970-978.

[20]

Gao H, Qian J, Cao S, Yang Z, Pang Z, Pan S, Zhang Q. Precise glioma targeting of and penetration by aptamer and peptide dual-functioned nanoparticles. Biomaterials, 2012, 33(20): 5115-5123.

[21]

George G, Sisupal SB, Tomy T, Kumaran A, Vadivelu P, Suvekbala V, Ragupathy L. Facile, environmentally benign and scalable approach to produce pristine few layers graphene suitable for preparing biocompatible polymer nanocomposites. Sci Rep, 2018, 8(1): 1-14.

[22]

Gomathi AC, Rajarathinam SRX, Sadiq AM, Rajeshkumar S. Anticancer activity of silver nanoparticles synthesized using aqueous fruit shell extract of Tamarindus indica on MCF-7 human breast cancer cell line. J Drug Deliv Sci Technol, 2020, 55: 101376.

[23]

Gurunathan S, Han JW, Park JH, Kim E, Choi Y-J, Kwon D-N, Kim J-H. Reduced graphene oxide-silver nanoparticle nanocomposite: a potential anticancer nanotherapy. Int J Nanomed, 2015, 10: 6257-6276.

[24]

Hajipour P, Bahrami A, Eslami A, Hosseini-Abari A. Chemical bath synthesis of CuO-GO-Ag nanocomposites with enhanced antibacterial properties. J Alloy Compd, 2020, 821: 153456.

[25]

Hu C, Liu Y, Qin J, Nie G, Lei B, Xiao Y, Zheng M, Rong J. Fabrication of reduced graphene oxide and sliver nanoparticle hybrids for Raman detection of absorbed folic acid: a potential cancer diagnostic probe. ACS Appl Mater Interfaces, 2013, 5(11): 4760-4768.

[26]

Hummers WS Jr, Offeman RE. Preparation of graphitic oxide. J Am Chem Soc, 1958, 80(6): 1339.

[27]

Idumah CI, Hassan A, Ihuoma DE. Recently emerging trends in polymer nanocomposites packaging materials. Polym Plast Technol Mater, 2019, 58(10): 1054-1109.

[28]

Jain RK, Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat Rev Clin Oncol, 2010, 7(11): 653.

[29]

Jebaranjitham JN, Mageshwari C, Saravanan R, Mu N. Fabrication of amine functionalized graphene oxide–AgNPs nanocomposite with improved dispersibility for reduction of 4-nitrophenol. Compos B Eng, 2019, 171: 302-309.

[30]

Jose PPA, Kala MS, Joseph AV, Kalarikkal N, Thomas S. Reduced graphene oxide/silver nanohybrid as a multifunctional material for antibacterial, anticancer, and SERS applications. Appl Phys A, 2020, 126(1): 1-16.

[31]

Konios D, Stylianakis MM, Stratakis E, Kymakis E. Dispersion behaviour of graphene oxide and reduced graphene oxide. J Colloid Interface Sci, 2014, 430: 108-112.

[32]

Li J, Liu C. Ag/graphene heterostructures: synthesis, characterization and optical properties. Wiley Online Library, 2010

[33]

Ma J, Liu J, Zhu W, Qin W. Solubility study on the surfactants functionalized reduced graphene oxide. Colloids Surf A, 2018, 538: 79-85.

[34]

Ma R, Wang Y, Qi H, Shi C, Wei G, Xiao L, Huang Z, Liu S, Yu H, Teng C. Nanocomposite sponges of sodium alginate/graphene oxide/polyvinyl alcohol as potential wound dressing: In vitro and in vivo evaluation. Compos B Eng, 2019, 167: 396-405.

[35]

Morimoto N, Kubo T, Nishina Y. Tailoring the oxygen content of graphite and reduced graphene oxide for specific applications. Sci Rep, 2016, 6(1): 1-8.

[36]

Mukheem A, Muthoosamy K, Manickam S, Sudesh K, Shahabuddin S, Saidur R, Akbar N, Sridewi N. Fabrication and characterization of an electrospun PHA/graphene silver nanocomposite scaffold for antibacterial applications. Materials, 2018, 11(9): 1673.

[37]

Mukherjee S, Chowdhury D, Kotcherlakota R, Patra S. Potential theranostics application of bio-synthesized silver nanoparticles (4-in-1 system). Theranostics, 2014, 4(3): 316-335.

[38]

Narayanan KB, Kim HD, Han SS. Biocompatibility and hemocompatibility of hydrothermally derived reduced graphene oxide using soluble starch as a reducing agent. Colloids Surf B, 2020, 185: 110579.

[39]

Nasr HA, Nassar OM, El-Sayed MH, Kobisi AA. Characterization and antimicrobial activity of lemon peel mediated green synthesis of silver nanoparticles. Int J Biol Chem, 2020, 12(2): 56-63.

[40]

Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nanolevel. Science, 2006, 311(5761): 622-627.

[41]

Ninomiya S, Inomata M, Tajima M, Ali AT, Ueda Y, Shiraishi N, Kitano S. Effect of bevacizumab, a humanized monoclonal antibody to vascular endothelial growth factor, on peritoneal metastasis of MNK-45P human gastric cancer in mice. J Surg Res, 2009, 154(2): 196-202.

[42]

Novoselov KS, Fal VI, Colombo L, Gellert PR, Schwab MG, Kim K. A roadmap for graphene. Nature, 2012, 490(7419): 192-200.

[43]

Ozaslan M, Karagoz ID, Kilic IH, Guldur ME. Ehrlich ascites carcinoma. Afr J Biotech, 2011, 10(13): 2375-2378.

[44]

Pasricha R, Gupta S, Srivastava AK. A facile and novel synthesis of Ag–graphene-based nanocomposites. Small, 2009, 5(20): 2253-2259.

[45]

Patil MP, Seo YB, Lim HK, Kim G-D. Biofabrication of gold nanoparticles using Agrimonia pilosa extract and their antioxidant and cytotoxic activity. Green Chem Lett Rev, 2019, 12(3): 208-216.

[46]

Pei X, Zhu Z, Gan Z, Chen J, Zhang X, Cheng X, Wang J. PEGylated nano-graphene oxide as a nanocarrier for delivering mixed anticancer drugs to improve anticancer activity. Sci Rep, 2020, 10(1): 1-15.

[47]

Peña A, Sánchez NS, Calahorra M. Effects of chitosan on Candida albicans: conditions for its antifungal activity. Biomed Res Int, 2013

[48]

Pooresmaeil M, Namazi H. Preparation and characterization of polyvinyl alcohol/β-cyclodextrin/GO-Ag nanocomposite with improved antibacterial and strength properties. Polym Adv Technol, 2019, 30(2): 447-456.

[49]

Rahmanian N, Eskandani M, Barar J, Omidi Y. Recent trends in targeted therapy of cancer using graphene oxide-modified multifunctional nanomedicines. J Drug Target, 2017, 25(3): 202-215.

[50]

Rasoulzadehzali M, Namazi H. Facile preparation of antibacterial chitosan/graphene oxide-Ag bio-nanocomposite hydrogel beads for controlled release of doxorubicin. Int J Biol Macromol, 2018, 116: 54-63.

[51]

Ruiz-Herrera J, Victoria Elorza M, Valentín E, Sentandreu R. Molecular organization of the cell wall of Candida albicans and its relation to pathogenicity. FEMS Yeast Res, 2006, 6(1): 14-29.

[52]

Sabayan B, Goudarzian N, Moslemin MH, Mohebat R (2020) Green synthesis and high efficacy method for reduced graphene oxide by Zataria Multiflora extract. J Environ Treat Techniques 8(1), 488–496. https://www.researchgate.net/profile/Nooredin-Goudarzian/publication/338980183_Green_Synthesis_and_High_Efficacy_Method_for_Reduced_Graphene_Oxide_by_Zataria_Multiflora_Extract/links/5e35c42092851c7f7f1478ea/Green-Synthesis-and-High-Efficacy-Method-for-Reduced-Graphene-Oxide-by-Zataria-Multiflora-Extract.pdf

[53]

Saikia I, Sonowal S, Pal M, Boruah PK, Das MR, Tamuly C. Biosynthesis of gold decorated reduced graphene oxide and its biological activities. Mater Lett, 2016, 178: 239-242.

[54]

Soica C, Pinzaru I, Trandafirescu C, Andrica F, Danciu C, Mioc M, Coricovac D, Sitaru C, Dehelean C (2018) Silver-, gold-, and iron-based metallic nanoparticles: biomedical applications as theranostic agents for cancer. In: Design of nanostructures for theranostics applications, pp 161–242. Elsevier. doi: https://doi.org/10.1016/B978-0-12-813669-0.00005-1

[55]

Some S, Gwon AR, Hwang E, Bahn GH, Yoon Y, Kim Y, Lee H. Cancer therapy using ultrahigh hydrophobic drug-loaded graphene derivatives. Sci Rep, 2014, 4(1): 1-9.

[56]

Stobinski L, Lesiak B, Malolepszy A, Mazurkiewicz M, Mierzwa B, Zemek J, Jiricek P, Bieloshapka I. Graphene oxide and reduced graphene oxide studied by the XRD, TEM and electron spectroscopy methods. J Elect Spectrosc Relat Phenomena, 2014, 195: 145-154.

[57]

Strober W. Trypan blue exclusion test of cell viability. Curr Prot Immunol, 2015, 111(1): A3-B.

[58]

Sugiura K. relative sensitivity of the solid and ascites forms of sarcoma 180 and Ehrlich carcinoma to inhibitory compounds*. Ann N Y Acad Sci, 1958, 76(3): 575-585.

[59]

Vazquez-Muñoz R, Avalos-Borja M, Castro-Longoria E. Ultrastructural analysis of Candida albicans when exposed to silver nanoparticles. PLoS ONE, 2014, 9(10): e108876.

[60]

Yuan Y-G, Gurunathan S. Combination of graphene oxide–silver nanoparticle nanocomposites and cisplatin enhances apoptosis and autophagy in human cervical cancer cells. Int J Nanomed, 2017, 12: 6537.

[61]

Yun H, Kim JD, Choi HC, Lee CW. Antibacterial activity of CNT-Ag and GO-Ag nanocomposites against gram-negative and gram-positive bacteria. Bull Korean Chem Soc, 2013, 34(11): 3261-3264.

[62]

Yusof HM, Mohamad R, Zaidan UH. Sustainable microbial cell nanofactory for zinc oxide nanoparticles production by zinc-tolerant probiotic Lactobacillus plantarum strain TA4. Microb Cell Fact, 2020, 19(1): 1-17.

[63]

Zaidi SA. Effective imprinting of an anticancer drug, 6-thioguanine, via mussel-inspired self-polymerization of dopamine over reduced graphene oxide. Analyst, 2019, 144(7): 2345-2352.

[64]

Zainy M, Huang NM, Vijay Kumar S, Lim HN, Chia CH, Harrison I. Simple and scalable preparation of reduced graphene oxide–silver nanocomposites via rapid thermal treatment. Mater Lett, 2012, 89: 180-183.

[65]

Zhang Z, Xu F, Yang W, Guo M, Wang X, Zhang B, Tang J. A facile one-pot method to high-quality Ag-graphene composite nanosheets for efficient surface-enhanced Raman scattering. Chem Commun, 2011, 47(22): 6440-6442.

[66]

Zhang C, Feng X, He L, Zhang Y, Shao L. The interrupted effect of autophagic flux and lysosomal function induced by graphene oxide in p62-dependent apoptosis of F98 cells. J Nanobiotechnol, 2020, 18(1): 1-17.

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