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A convergent fabrication of 1-aminopyridine-capped gold nanomaterials and reduced graphene oxide nanocomposites for ovarian cancer cells

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Abstract

Since their discovery, graphene nanocomposites have attracted much attention for their potential use in many biological applications. Herein, we examined the highly reduced graphene oxide (HRGO) and gold nanomaterial (AuNM)-based (HRGO/Au@AP) nanocomposite for ovarian cancer and apoptosis-inducing abilities, the nanomaterials’ anticancer activities against human ovarian cancer cell lines (SKOV3 and A2780). HRGO was functionalized with the 1-aminopyridine (AP) as a potential stabilizing agent to improve the sample’s solubility and bioavailability. The surface morphology and structure of the nanocomposites were examined by high-resolution transmission electron microscopy. The results of an anticancer study comparing HRGO, HRGO/Au, and HRGO/Au@AP nanocomposites showed a greater capacity to induce apoptosis, the apoptosis assays (AO-EB, DAPI, and Annexin V-FITC/PI staining) and reactive oxygen species (ROS) measurements on SKOV3 and A2780 cells. This data suggests that HRGO/Au@AP promotes potent apoptosis in human ovarian cancer cells.

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Data availability

The datasets used and analyzed during the current study are available from the corresponding author upon request.

References

  1. Matulonis UA, Sood AK, Fallowfield L, Howitt BE, Sehouli J, Karlan BY (2016) Ovarian cancer. Nat Rev Dis Primers 2:1–22

    Article  Google Scholar 

  2. Lee J, Minasian L, Kohn EC (2019) New strategies in ovarian cancer treatment. Cancer 125:4623–4629

    Article  CAS  PubMed  Google Scholar 

  3. Orr B, Edwards RP (2018) Diagnosis and treatment of ovarian cancer, Hematology/Oncology. Clinics 32:943–964

    Google Scholar 

  4. Momenimovahed Z, Tiznobaik A, Taheri S, Salehiniya H (2019) Ovarian cancer in the world: epidemiology and risk factors. Int J Women’s Health 11:287

    Article  Google Scholar 

  5. Stewart C, Ralyea C, Lockwood S (2019) Ovarian cancer: an integrated review. Semin Oncol Nurs 35:151–156

    Article  PubMed  Google Scholar 

  6. Doubeni CA, Doubeni AR, Myers AE (2016) Diagnosis and management of ovarian cancer. Am Fam Physician 93:937–944

    PubMed  Google Scholar 

  7. Lheureux S, Gourley C, Vergote I, Oza AM (2019) Epithelial ovarian cancer. The Lancet 393:1240–1253

    Article  Google Scholar 

  8. Reid BM, Permuth JB, Sellers TA (2017) Epidemiology of ovarian cancer: a review. Cancer Biol Med 14:9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hou P, Kuang H, Deng W, Lei Y (2022) Immobilized copper nanoparticles on biodegradable magnetic starch composite: investigation of its ovarian cancer, cytotoxicity, and antioxidant effects. J Exp Nanosci 17:496–508. https://doi.org/10.1080/17458080.2022.2110241

    Article  CAS  Google Scholar 

  10. Lu L, Zhao Q, Wang Z, Ju F (2022) Oak gum mediated sustainable synthesis of gold nanoparticles (Au NPs): evaluation of its antioxidant and anti-colon cancer effects. J Exp Nanosci 17:377–388. https://doi.org/10.1080/17458080.2022.2050905

    Article  CAS  Google Scholar 

  11. Abbasalipourkabir R, Salehzadeh A, Abdullah R (2016) Tamoxifen-loaded solid lipid nanoparticles-induced apoptosis in breast cancer cell lines. J Exp Nanosci 11:161–174. https://doi.org/10.1080/17458080.2015.1038660

    Article  CAS  Google Scholar 

  12. Huang Y, Zhu C, Xie R, Ni M (2021) Green synthesis of nickel nanoparticles using Fumaria officinalis as a novel chemotherapeutic drug for the treatment of ovarian cancer. J Exp Nanosci 16:368–381. https://doi.org/10.1080/17458080.2021.1975037

    Article  CAS  Google Scholar 

  13. Cortez AJ, Tudrej P, Kujawa KA, Lisowska KM (2018) Advances in ovarian cancer therapy. Cancer Chemother Pharmacol 81:17–38

    Article  CAS  PubMed  Google Scholar 

  14. Thapa RK, Kim JH, Jeong J-H, Shin BS, Choi H-G, Yong CS, Kim JO (2017) Silver nanoparticle-embedded graphene oxide-methotrexate for targeted cancer treatment. Colloids Surf, B 153:95–103

    Article  CAS  Google Scholar 

  15. Choi Y-J, Kim E, Han JW, Kim J-H, Gurunathan S (2016) A novel biomolecule-mediated reduction of graphene oxide: a multifunctional anti-cancer agent. Molecules 21:375

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lima-Sousa R, de Melo-Diogo D, Alves CG, Costa EC, Ferreira P, Louro RO, Correia IJ (2018) Hyaluronic acid functionalized green reduced graphene oxide for targeted cancer photothermal therapy. Carbohyd Polym 200:93–99

    Article  CAS  Google Scholar 

  17. Guo L, Shi H, Wu H, Zhang Y, Wang X, Wu D, An L, Yang S (2016) Prostate cancer targeted multifunctionalized graphene oxide for magnetic resonance imaging and drug delivery. Carbon 107:87–99

    Article  CAS  Google Scholar 

  18. Yang D, Feng L, Dougherty CA, Luker KE, Chen D, Cauble MA, Holl MMB, Luker GD, Ross BD, Liu Z (2016) In vivo targeting of metastatic breast cancer via tumor vasculature-specific nano-graphene oxide. Biomaterials 104:361–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Huang Y-S, Lu Y-J, Chen J-P (2017) Magnetic graphene oxide as a carrier for targeted delivery of chemotherapy drugs in cancer therapy. J Magn Magn Mater 427:34–40

    Article  CAS  Google Scholar 

  20. Tabish TA, Pranjol MZI, Hayat H, Rahat AAM, Abdullah TM, Whatmore JL, Zhang S (2017) In vitro toxic effects of reduced graphene oxide nanosheets on lung cancer cells. Nanotechnology 28:504001

    Article  PubMed  Google Scholar 

  21. Zhang H, Li T, Luo W, Peng GX, Xiong J (2022) Green synthesis of Ag nanoparticles from Leucus aspera and its application in anticancer activity against alveolar cancer. J Exp Nanosci 17:47–60. https://doi.org/10.1080/17458080.2021.2007886

    Article  CAS  Google Scholar 

  22. Zhang Q, Cui W, Guo H, Wang B, Wang H, Zhang J, Li W (2022) One-pot preparation of nano-scaled magnetic-pectin particles (Fe3O4@pectin NPs): cytotoxicity, antioxidant, and anti-liver cancer properties. J Exp Nanosci 17:326–338. https://doi.org/10.1080/17458080.2022.2063279

    Article  CAS  Google Scholar 

  23. Tsuji T, Yoshitomi H, Ishikawa Y, Koshizaki N, Suzuki M, Usukura J (2020) A method to selectively internalize submicrometer boron carbide particles into cancer cells using surface transferrin conjugation for developing a new boron neutron capture therapy agent. J Exp Nanosci 15:1–11. https://doi.org/10.1080/17458080.2019.1692178

    Article  CAS  Google Scholar 

  24. Yuan C, Jiang B, Xu X, Wan Y, Wang L, Chen J (2022) Anti-human ovarian cancer and cytotoxicity effects of nickel nanoparticles green-synthesized by Alhagi maurorum leaf aqueous extract. J Exp Nanosci 17:113–125. https://doi.org/10.1080/17458080.2021.2011860

    Article  CAS  Google Scholar 

  25. Martin C, Ruiz A, Keshavan S, Reina G, Murera D, Nishina Y, Fadeel B, Bianco A (2019) A biodegradable multifunctional graphene oxide platform for targeted cancer therapy. Adv Func Mater 29:1901761

    Article  Google Scholar 

  26. Li R, Wang Y, Du J, Wang X, Duan A, Gao R, Liu J, Li B (2021) Graphene oxide loaded with tumor-targeted peptide and anti-cancer drugs for cancer target therapy. Sci Rep 11:1–10

    Google Scholar 

  27. Dorniani D, Saifullah B, Barahuie F, Arulselvan P, Bin Hussein MZ, Fakurazi S, Twyman LJ (2016) Graphene oxide-gallic acid nanodelivery system for cancer therapy. Nanoscale Res Lett 11:1–9

  28. Yang H, Bremner DH, Tao L, Li H, Hu J, Zhu L (2016) Carboxymethyl chitosan-mediated synthesis of hyaluronic acid-targeted graphene oxide for cancer drug delivery. Carbohyd Polym 135:72–78

    Article  CAS  Google Scholar 

  29. Kumawat MK, Thakur M, Bahadur R, Kaku T, Prabhuraj RS, Ninawe A, Srivastava R (2019) Preparation of graphene oxide-graphene quantum dots hybrid and its application in cancer theranostics. Mater Sci Eng, C 103:109774

    Article  CAS  Google Scholar 

  30. AHAU-K Al-Marri MujeebAU - Khan, MerajuddinAU - Adil, Syed F.AU - Al-Warthan (2015) AbdulrahmanAU - Alkhathlan, Hamad Z.AU - Tremel, WolfgangAU - Labis, Joselito P.AU - Siddiqui, Mohammed Rafiq H.AU - Tahir, Muhammad N.TI - Pulicaria glutinosa extract: a too, no title. Int J Mol Sci 16:1131–1142. https://doi.org/10.3390/ijms16011131

  31. Feng H, Liu Y, Li J (2015) Highly reduced graphene oxide supported Pt nanocomposites as highly efficient catalysts for methanol oxidation. Chem Commun 51:2418–2420. https://doi.org/10.1039/C4CC09146A

    Article  CAS  Google Scholar 

  32. Lu G, Park S, Yu K, Ruoff RS, Ocola LE, Rosenmann D, Chen J (2011) Toward practical gas sensing with highly reduced graphene oxide: a new signal processing method to circumvent run-to-run and device-to-device variations. ACS Nano 5:1154–1164. https://doi.org/10.1021/nn102803q

    Article  CAS  PubMed  Google Scholar 

  33. Park S, An J, Jung I, Piner RD, An SJ, Li X, Velamakanni A, Ruoff RS (2009) Colloidal suspensions of highly reduced graphene oxide in a wide variety of organic solvents. Nano Lett 9:1593–1597. https://doi.org/10.1021/nl803798y

    Article  CAS  PubMed  Google Scholar 

  34. Baghban N, Khoradmehr A, Nabipour I, Tamadon A, Ullah M (2022) The potential of marine-based gold nanomaterials in cancer therapy: a mini-review. Gold Bulletin 55:53–63. https://doi.org/10.1007/s13404-021-00304-6

    Article  CAS  Google Scholar 

  35. Pannerec-Varna M, Ratajczak P, Bousquet G, Ferreira I, Leboeuf C, Boisgard R, Gapihan G, Verine J, Palpant B, Bossy E, Doris E, Poupon J, Fort E, Janin A (2013) In vivo uptake and cellular distribution of gold nanoshells in a preclinical model of xenografted human renal cancer. Gold Bulletin 46:257–265. https://doi.org/10.1007/s13404-013-0115-8

    Article  CAS  Google Scholar 

  36. Renault S, Baudrimont M, Mesmer-Dudons N, Gonzalez P, Mornet S, Brisson A (2008) Impacts of gold nanoparticle exposure on two freshwater species: a phytoplanktonic alga (Scenedesmus subspicatus) and a benthic bivalve (Corbicula fluminea). Gold Bulletin 41:116–126. https://doi.org/10.1007/BF03216589

    Article  CAS  Google Scholar 

  37. Rosyidah A, Kerdtoob S, Yudhistyra WI, Munfadlila AW (2023) Gold nanoparticle-based drug nanocarriers as a targeted drug delivery system platform for cancer therapeutics: a systematic review. Gold Bulletin 56:121–134. https://doi.org/10.1007/s13404-023-00331-5

    Article  CAS  Google Scholar 

  38. Ramalingam V, Revathidevi S, Shanmuganayagam TS, Muthulakshmi L, Rajaram R (2017) Gold nanoparticle induces mitochondria-mediated apoptosis and cell cycle arrest in nonsmall cell lung cancer cells. Gold Bulletin 50:177–189. https://doi.org/10.1007/s13404-017-0208-x

    Article  CAS  Google Scholar 

  39. Aishwarya S, Sanjay KR (2018) Conjugation study of 5-aminolevulinic acid with microbial synthesized gold nanoparticles to evaluate its effect on skin melanoma and epidermoid carcinoma cell lines using photodynamic cancer therapy. Gold Bulletin 51:11–19. https://doi.org/10.1007/s13404-017-0224-x

    Article  CAS  Google Scholar 

  40. Yadav P, Bandyopadhyay A, Chakraborty A, Islam SM, Sarkar K (2019) Enhancing the radiotherapeutic index of gamma radiation on cervical cancer cells by gold nanoparticles. Gold Bulletin 52:185–196. https://doi.org/10.1007/s13404-019-00260-2

    Article  CAS  Google Scholar 

  41. Torrisi L, Guglielmino S, Silipigni L, De Plano LM, Kovacik L, Lavrentiev V, Torrisi A, Fazio M, Fazio B, Di Marco G (2019) Study of gold nanoparticle transport by M13 phages towards disease tissues as targeting procedure for radiotherapy applications. Gold Bulletin 52:135–144. https://doi.org/10.1007/s13404-019-00266-w

    Article  CAS  Google Scholar 

  42. Fernandes N, Rodrigues CF, Moreira AF, Correia IJ (2020) Overview of the application of inorganic nanomaterials in cancer photothermal therapy, Biomaterials. Science 8:2990–3020

    CAS  Google Scholar 

  43. Tian Y, Qiang S, Wang L (2019) Gold nanomaterials for imaging-guided near-infrared in vivo cancer therapy. Frontiers in Bioengineering and Biotechnology 7:398

    Article  PubMed  PubMed Central  Google Scholar 

  44. Barabadi H, Vahidi H, Damavandi Kamali K, Hosseini O, Mahjoub MA, Rashedi M, Jazayeri Shoushtari F, Saravanan M (2020) Emerging theranostic gold nanomaterials to combat lung cancer: a systematic review. J Cluster Sci 31:323–330. https://doi.org/10.1007/s10876-019-01650-4

  45. Saravanan M, Vahidi H, Medina Cruz D, Vernet-Crua A, Mostafavi E, Stelmach R, Webster TJ, Mahjoub MA, Rashedi M, Barabadi H (2020) Emerging antineoplastic biogenic gold nanomaterials for breast cancer therapeutics: a systematic review. Int J Nanomedicine 15:3577–3595. https://doi.org/10.2147/IJN.S240293

  46. Ahmad R, Fu J, He N, Li S (2016) Advanced gold nanomaterials for photothermal therapy of cancer. J Nanosci Nanotechnol 16:67–80

    Article  CAS  PubMed  Google Scholar 

  47. Sekhon SS, Kaur P, Kim Y-H, Sekhon SS (2021) 2D graphene oxide–aptamer conjugate materials for cancer diagnosis. Npj 2D Mater Appl 5:1–19

  48. Sharma H, Mondal S (2020) Functionalized graphene oxide for chemotherapeutic drug delivery and cancer treatment: a promising material in nanomedicine. Int J Mol Sci 21:6280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  50. Zhu YH, Sun CY, Shen S, Khan MIU, Zhao YY, Liu Y, Wang YC, Wang J (2017) A micellar cisplatin prodrug simultaneously eliminates both cancer cells and cancer stem cells in lung cancer, Biomaterials. Science 5:1612–1621. https://doi.org/10.1039/c7bm00278e

    Article  CAS  Google Scholar 

  51. Mohamed Kasim MS, Sundar S, Rengan R (2018) Synthesis and structure of new binuclear ruthenium(II) arene benzil bis(benzoylhydrazone) complexes: investigation on antiproliferative activity and apoptosis induction. Inorg Chem Front 5:585–596. https://doi.org/10.1039/c7qi00761b

  52. Deng B, Ma P, Xie Y (2015) Reduction-sensitive polymeric nanocarriers in cancer therapy: a comprehensive review. Nanoscale 7:12773–12795. https://doi.org/10.1039/c5nr02878g

    Article  CAS  PubMed  Google Scholar 

  53. Swaminathan S, Haribabu J, Mohamed Subarkhan MK, Gayathri D, Balakrishnan N, Bhuvanesh N, Echeverria C, Karvembu R (2021) Impact of aliphatic acyl and aromatic thioamide substituents on the anticancer activity of Ru(ii)-p-cymene complexes with acylthiourea ligands—in vitro and in vivo studies. Dalton Trans 50:16311–16325. https://doi.org/10.1039/D1DT02611A

  54. T. Sathiya Kamatchi, M.K. Mohamed Subarkhan, R. Ramesh, H. Wang, J.G. Małecki, Investigation into antiproliferative activity and apoptosis mechanism of new arene Ru(ii) carbazole-based hydrazone complexes, Dalton Transactions. 49 (2020) 11385–11395. https://doi.org/10.1039/D0DT01476A.

  55. Kalaiarasi G, Mohamed Subarkhan M, Fathima Safwana CK, Sruthi S, Sathiya Kamatchi T, Keerthana B, Ashok Kumar SL (2022) New organoruthenium(II) complexes containing N, X-donor (X = O, S) heterocyclic chelators: synthesis, spectral characterization, in vitro cytotoxicity and apoptosis investigation. Inorg Chimica Acta 535:120863. https://doi.org/10.1016/j.ica.2022.120863

  56. Pilliadugula R, Haribabu J, Mohamed Subarkhan MK, Echeverria C, Karvembu R, Gopalakrishnan N ((2021)) Effect of morphology and (Sn, Cr) doping on in vitro antiproliferation properties of hydrothermally synthesized 1D GaOOH nanostructures, Journal of Science: Advanced Materials and Devices. 6:351–363. https://doi.org/10.1016/j.jsamd.2021.03.003

  57. Mohamed Subarkhan MK, Ren L, Xie B, Chen C, Wang Y, Wang H (2019) Novel tetranuclear ruthenium(II) arene complexes showing potent cytotoxic and antimetastatic activity as well as low toxicity in vivo. Eur J Med Chem 179. https://doi.org/10.1016/j.ejmech.2019.06.061

  58. Balaji S, Mohamed Subarkhan MK, Ramesh R, Wang H, Semeril D (2020) Synthesis and structure of arene Ru(II) N∧O-chelating complexes: in vitro cytotoxicity and cancer cell death mechanism. Organometallics 39:1366–1375. https://doi.org/10.1021/acs.organomet.0c00092.

  59. Mohan N, Mohamed Subarkhan MK, Ramesh R (2018) Synthesis, antiproliferative activity and apoptosis-promoting effects of arene ruthenium(II) complexes with N, O chelating ligands. J Organomet Chem 859. https://doi.org/10.1016/j.jorganchem.2018.01.022.

  60. Mohamed Subarkhan MK, Ramesh R, Liu Y (2016) Synthesis and molecular structure of arene ruthenium(II) benzhydrazone complexes: impact of substitution at the chelating ligand and arene moiety on antiproliferative activity. New J Chem 40. https://doi.org/10.1039/c6nj01936f

  61. Mohamed Subarkhan M, Prabhu RN, Raj Kumar R, Ramesh R (2016) Antiproliferative activity of cationic and neutral thiosemicarbazone copper(ii) complexes. RSC Advances 6:25082–25093. https://doi.org/10.1039/c5ra26071j

  62. Chen W, Yu D, Sun S-Y, Li F (2021) Nanoparticles for co-delivery of osimertinib and selumetinib to overcome osimertinib-acquired resistance in non-small cell lung cancer. Acta Biomater 129:258–268. https://doi.org/10.1016/j.actbio.2021.05.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Manuel Xavier HF, Nadar VM, Patel P, Umapathy D, Velanganni Joseph A, Manivannan S, Santhiyagu P, Pandi B, Muthusamy G, Rathinam Y, Ponnuchamy K (2020) Selective antibacterial and apoptosis-inducing effects of hybrid gold nanoparticles – a green approach. J Drug Deliv Sci Technol 59:101890. https://doi.org/10.1016/j.jddst.2020.101890

  64. Mishra A, Singh A, Kushwaha HR, Mishra A (2022) Cytotoxic effect of cobalt oxide–graphene oxide nanocomposites on melanoma cell line. J Exp Nanosci 17:509–521. https://doi.org/10.1080/17458080.2022.2115483

    Article  CAS  Google Scholar 

  65. Zhuang X, Kang Y, Zhao L, Guo S (2022) Design and synthesis of copper nanoparticles for the treatment of human esophageal cancer: introducing a novel chemotherapeutic supplement. J Exp Nanosci 17:274–284. https://doi.org/10.1080/17458080.2022.2065264

    Article  CAS  Google Scholar 

  66. Peng D, Han B, Kong Y, Chen M, Zhang H (2022) Facile synthesis and characterization of Au nanoparticles-loaded kaolin mediated by Thymbra spicata extract and its application on bone regeneration in a rat calvaria defect model and screening system. J Exp Nanosci 17:86–99. https://doi.org/10.1080/17458080.2022.2028775

    Article  CAS  Google Scholar 

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Wei Luan, Meiyun Zheng, Youlin Yang -Supported with synthesis, Characterization. Yi Chen, Xiahui Zhang, Lingping Zhu-Molecular and biochemical analysis, Data curation, Formal analysis, and Validation. Dr. Chenxiao Lin -Helped with supervised the research.

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Luan, W., Zheng, M., Yang, Y. et al. A convergent fabrication of 1-aminopyridine-capped gold nanomaterials and reduced graphene oxide nanocomposites for ovarian cancer cells. Gold Bull 56, 167–178 (2023). https://doi.org/10.1007/s13404-023-00339-x

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