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An eco-friendly synthesis of Enterococcus sp.–mediated gold nanoparticle induces cytotoxicity in human colorectal cancer cells

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Abstract

Gold nanoparticles (AuNPs) have become frequently used materials in biotechnological and biomedical applications including cancer. They can be commonly synthesized by biological and chemical methods. In the present study, we synthesized Enterococcus-mediated AuNPs and evaluated their cytotoxicity in human colorectal cancer cell line (HT-29). AuNPs are synthesized intracellularly using Enterococcus sp. RMAA. Characterization of AuNPs has done using UV spectrophotometry and transmission electron microscope. Cytotoxicity was evaluated by MTT assay. Intercellular reactive oxygen species (ROS) expression and apoptosis-related morphology were evaluated by dichlorodihydrofluorescein diacetate and acridine orange/ethidium bromide staining via fluorescence microscopy. JC-1 staining and caspase 3 immunofluorescence expression were analyzed by confocal microscopy. Enterococcus sp. RMAA–mediated AuNPs are spherical and induced concentration-dependent cytotoxicity in HT-29 cells. AuNP treatments also induced ROS and caspase-3 expressions and reduced the mitochondrial membrane potential. Morphology related to apoptotic changes was also noticed after AuNP treatments in HT-29 cells. The present study revealed that Enterococcus-derived AuNPs induced apoptotic cell death in HT-29 cells and suggests that AuNPs could be used as a pro apoptotic agent for colon cancer treatment.

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References

  • Abdel-Daim MM, Eissa IAM, Abdeen A, Abdel-Latif HMR, Ismail M, MAO D, Hassan AM (2019) Lycopene and resveratrol ameliorate zinc oxide nanoparticles-induced oxidative stress in Nile tilapia, Oreochromis niloticus. Environ Toxicol Pharmacol 69:44–50

    Article  CAS  Google Scholar 

  • Ahmed S, Annu IS, Yudha SS (2016) Biosynthesis of gold nanoparticles: a green approach. J Photochem Photobiol B 161:141–153

    Article  CAS  Google Scholar 

  • Aminabad NS, Farshbaf M, Akbarzadeh A, (2019) Recent Advances of Gold Nanoparticles in Biomedical Applications: State of the Art. Cell Biochemistry and Biophysics 77 (2):123-137

  • Baneshi M, Dadfarnia S, Shabani AMH, Sabbagh SK, Haghgoo S, Bardania H (2019) A novel theranostic system of AS1411 aptamer-functionalized albumin nanoparticles loaded on iron oxide and gold nanoparticles for doxorubicin delivery. Int J Pharm 564:145–152

    Article  CAS  Google Scholar 

  • Cabrera GFS, Balbin MM, Eugenio PJG, Zapanta CS, Monserate JJ, Salazar JR, Mingala CN (2017) Green synthesis of gold nanoparticles reduced and stabilized by sodium glutamate and sodium dodecyl sulfate. Biochem Biophys Res Commun 484:774–780

    Article  CAS  Google Scholar 

  • Cabuzu D, Cirja A, Puiu R, Grumezescu AM (2015) Biomedical applications of gold nanoparticles. Curr Top Med Chem 15:1605–1613

    Article  CAS  Google Scholar 

  • Chen Y, Wang Y, Shi Y, Dai G (2017) Timing of chemotherapy-induced neutropenia predicts prognosis in metastatic colon cancer patients: a retrospective study in mFOLFOX6-treated patients. BMC Cancer 17:242

    Article  CAS  Google Scholar 

  • Cheng Y, Chen Y, Zhou C, Shen L, Tu F, Xu J, Liu C (2019) For colorectal cancer patients with type II diabetes, could metformin improve the survival rate? A meta-analysis. Clin Res Hepatol Gastroenterol 2019:pii S2210-7401(19):30134–30132

    Google Scholar 

  • Daraee H, Eatemadi A, Abbasi E, Fekri Aval S, Kouhi M, Akbarzadeh A (2016) Application of gold nanoparticles in biomedical and drug delivery. Artif Cells Nanomed Biotechnol 44:410–422

    Article  CAS  Google Scholar 

  • de Araújo RF Jr, de Araújo AA, Pessoa JB, Freire Neto FP, da Silva GR, Leitão Oliveira AL, de Carvalho TG, Silva HF, Eugênio M, Sant’Anna C, Gasparotto LH (2017) Anti-inflammatory, analgesic and anti-tumor properties of gold nanoparticles. Pharmacol Rep 69:119–129

    Article  CAS  Google Scholar 

  • El-Seedi HR, El-Shabasy RM, Khalifa SAM, Saeed A, Shah A, Shah R, Iftikhar FJ, AbdelDaim MM, Omri A, Hajrahand NH, Sabir JSM, Zou X, Halabi MF, Sarhan W, Guo W (2019) Metal nanoparticles fabricated by green chemistry using natural extracts: biosynthesis, mechanisms, and applications. RSC Adv 9:24539–24559

    Article  CAS  Google Scholar 

  • Estaquier J, Vallette F, Vayssiere JL, Mignotte B (2012) The mitochondrial pathways of apoptosis. Adv Exp Med Biol 942:157–183

    Article  CAS  Google Scholar 

  • Ezhilarasan D (2018) Herbal therapy for cancer. In: Shanmugam PST (ed). Understanding cancer therapies. CRC Press, pp129–166

  • Ezhilarasan D, Apoorva VS, Ashok Vardhan N (2019) Syzygium cumini extract induced reactive oxygen species-mediated apoptosis in human oral squamous carcinoma cells. J Oral Pathol Med 48:115–121

    CAS  Google Scholar 

  • Farooq MU, Novosad V, Rozhkova EA, Wali H, Ali A, Fateh AA, Neogi PB, Neogi A, Wang Z (2018) Gold nanoparticles-enabled efficient dual delivery of anticancer therapeutics to HeLa cells. Sci Rep 8:2907

    Article  CAS  Google Scholar 

  • Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386

    Article  CAS  Google Scholar 

  • Gheena S, Ezhilarasan D (2019) Syringic acid triggers reactive oxygen species-mediated cytotoxicity in HepG2 cells. Hum Exp Toxicol 38:694–702

    Article  CAS  Google Scholar 

  • Gohel A, McCarthy MB, Gronowicz G (1999) Estrogen prevents glucocorticoid-induced apoptosis in osteoblasts in vivo and in vitro. Endocrinology 140:5339–5347

    Article  CAS  Google Scholar 

  • Hou XS, Wang HS, Mugaka BP, Yang GJ, Ding Y (2018) Mitochondria: promising organelle targets for cancer diagnosis and treatment. Biomater Sci 6:2786–2797

    Article  CAS  Google Scholar 

  • Jung ST, Sohn DK, Hong CW, Kim BC, Park JW, Han KS, Chang HJ, Choi HS, Oh JH (2013) Importance of early follow-up colonoscopy in patients at high risk for colorectal polyps. Ann Coloproctol 29:243–247

    Article  Google Scholar 

  • Kandeil MA, Mohammed ET, Hashem KS, Aleya L, Abdel-Daim MM (2019) Moringa seed extract alleviates titanium oxide nanoparticles (TiO2-NPs)-induced cerebral oxidative damage, and increases cerebral mitochondrial viability. Environ Sci Pollut Res Int doi:1–16. https://doi.org/10.1007/s11356-019-05514-2

  • Ke S, Zhou T, Yang P, Wang Y, Zhang P, Chen K, Ren L, Ye S (2017) Gold nanoparticles enhance TRAIL sensitivity through Drp1-mediated apoptotic and autophagic mitochondrial fission in NSCLC cells. Int J Nanomedicine 12:2531–2551

    Article  CAS  Google Scholar 

  • Ke Y, Al Aboody MS, Alturaiki W, Alsagaby SA, Alfaiz FA, Veeraraghavan VP, Mickymaray S (2019) Photosynthesized gold nanoparticles from Catharanthus roseus induces caspase-mediated apoptosis in cervical cancer cells (HeLa). Artif Cells Nanomed Biotechnol 47:1938–1946

    Article  CAS  Google Scholar 

  • Khanna P, Kaur A, Goyal D (2019) Algae-based metallic nanoparticles: synthesis, characterization and applications. J Microbiol Methods 163:105656

    Article  CAS  Google Scholar 

  • Kumar D, Mutreja I, Chitcholtan K, Sykes P (2017) Cytotoxicity and cellular uptake of different sized gold nanoparticles in ovarian cancer cells. Nanotechnology 28:475101

    Article  CAS  Google Scholar 

  • Lakshmi T, Ezhilarasan D, Vijayaragavan R, Bhullar SK, Rajendran R (2017) Acacia catechu ethanolic bark extract induces apoptosis in human oral squamous carcinoma cells. J Adv Pharm Technol Res 8:143–149

    Article  CAS  Google Scholar 

  • Leve F, Bonfim DP, Fontes G, Morgado-Díaz JA (2019) Gold nanoparticles regulate tight junctions and improve cetuximab effect in colon cancer cells. Nanomedicine (London) 14:1565–1578

    Article  CAS  Google Scholar 

  • Li J, Li Q, Ma X, Tian B, Li T, Yu J, Dai S, Weng Y, Hua Y (2016) Biosynthesis of gold nanoparticles by the extreme bacterium Deinococcus radiodurans and an evaluation of their antibacterial properties. Int J Nanomedicine 11:5931–5944

    Article  CAS  Google Scholar 

  • Liu K, Liu PC, Liu R, Wu X (2015) Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Med Sci Monit Basic Res 21:15–20

    Article  Google Scholar 

  • Liu R, Pei Q, Shou T, Zhang W, Hu J, Li W (2019) Apoptotic effect of green synthesized gold nanoparticles from Curcuma wenyujin extract against human renal cell carcinoma A498 cells. Int J Nanomedicine 14:4091–4103

    Article  CAS  Google Scholar 

  • Malarkodi C, Rajeshkumar S, Vanaja M, Paulkumar K, Gnanajobitha G, Annadurai G (2013) Eco-friendly synthesis and characterization of gold nanoparticles using Klebsiella pneumonia. Journal of Nanostructure in Chemistry 3:30

    Article  Google Scholar 

  • Marley AR, Nan H (2016) Epidemiology of colorectal cancer. Int J Mol Epidemiol Genet 7:105–114

    Google Scholar 

  • Martínez-Torres AC, Zarate-Triviño DG, Lorenzo-Anota HY, Ávila-Ávila A, Rodríguez-Abrego C, Rodríguez-Padilla C (2018) Chitosan gold nanoparticles induce cell death in HeLa and MCF-7 cells through reactive oxygen species production. Int J Nanomedicine 13:3235–3250

    Article  Google Scholar 

  • Mateo D, Morales P, Ávalos A, Haza A (2014) Oxidative stress contributes to gold nanoparticle-induced cytotoxicity in human tumor cells. Toxicol Mech Methods 24:161–172

    Article  CAS  Google Scholar 

  • Menon S, Rajeshkumar S, Venkat Kumar S (2017) A review on biogenic synthesis of gold nanoparticles, characterization, and its applications. Resource-Efficient Technologies 3:516–527

    Article  Google Scholar 

  • Ovais M, Khalil AT, Ayaz M, Ahmad I, Nethi SK, Mukherjee S (2018) Biosynthesis of metal nanoparticles via microbial enzymes: a mechanistic approach. Int J Mol Sci 19:E4100

    Article  Google Scholar 

  • PonselviInduja M, Ezhilarasan D, Ashok Vardhan N (2018) Evolvulus alsinoides methanolic extract triggers apoptosis in HepG2 cells. Avicenna J Phytomed 8:504–512

    Google Scholar 

  • Pooja D, Sistla R (2019) Design of eco-friendly gold nanoparticles for cancer treatment. Methods Mol Biol 1974:215–221

    Article  CAS  Google Scholar 

  • Pourali P, Badiee H, Sahebali Manafi B, Noorani TB, Rezaei A, Yahyaei B (2017) Biosynthesis of gold nanoparticles by two bacterial and fungal strains, Bacillus cereus and Fusarium oxysporum, and assessment and comparison of their nanotoxicity in vitro by direct and indirect assays. Electron J Biotechnol 29:86–93

    Article  CAS  Google Scholar 

  • Rajeshkumar S (2016) Anticancer activity of eco-friendly gold nanoparticles against lung and liver cancer cells. Journal of Genetic Engineering and Biotechnology 14:195–202

    Article  CAS  Google Scholar 

  • Rohit Singh T, Ezhilarasan D (2019) Ethanolic extract of Lagerstroemia Speciosa (L.) Pers., induces apoptosis and cell cycle arrest in HepG2 cells. Nutr Cancer 2019:1–11

    Google Scholar 

  • Senapati S, Ahmad A, Khan MI, Sastry M, Kumar R (2005) Extracellular biosynthesis of bimetallic Au-Ag alloy nanoparticles. Small 1:517–520

    Article  CAS  Google Scholar 

  • Shalini S, Dorstyn L, Dawar S, Kumar S (2015) Old, new and emerging functions of caspases. Cell Death Differ 22:526–539

    Article  CAS  Google Scholar 

  • Shawky SM, Awad AM, Abugable AA, El-Khamisy SF (2018) Gold nanoparticles - an optical biosensor for RNA quantification for cancer and neurologic disorders diagnosis. Int J Nanomedicine 13:8137–8151

    Article  CAS  Google Scholar 

  • Shebi S, Ezhilarasan D, Thomas J, Chandrasekaran N, Mukherjee A (2019) Gracilaria foliifera (Forssk.) Børgesen ethanolic extract triggers apoptosis via activation of p53 expression in HepG2 cells. Phcog Mag 15:259–263

    Article  CAS  Google Scholar 

  • Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67:7–30

    Article  Google Scholar 

  • Sivandzade F, Bhalerao A, Cucullo L (2019) Analysis of the mitochondrial membrane potential using the cationic JC-1 dye as a sensitive fluorescent probe. Bio Protoc 9(pii):e3128

    Google Scholar 

  • Solai Prakash AK, Devaraj E (2019) Cytotoxic potentials of S. cumini methanolic seed kernel extract in human hepatoma HepG2 cells. Environ Toxicol 34:1313–1319

    Article  CAS  Google Scholar 

  • Sun H, Jia J, Jiang C, Zhai S (2018) Gold nanoparticle-induced cell death and potential applications in nanomedicine. Int J Mol Sci 19(pii):E754

    Article  CAS  Google Scholar 

  • Sunderam V, Thiyagarajan D, Lawrence AV, Mohammed SSS, Selvaraj A (2019) In-vitro antimicrobial and anticancer properties of green synthesized gold nanoparticles using Anacardium occidentale leaves extract. Saudi J Biol Sci 26:455–459

    Article  CAS  Google Scholar 

  • Surapaneni SK, Bashir S, Tikoo K (2018) Gold nanoparticles-induced cytotoxicity in triple negative breast cancer involves different epigenetic alterations depending upon the surface charge. Sci Rep 8:12295

    Article  CAS  Google Scholar 

  • Taggart LE, McMahon SJ, Currell FJ, Prise KM, Butterworth KT (2014) The role of mitochondrial function in gold nanoparticle mediated radiosensitisation. Cancer Nanotechnol 5:5

    Article  CAS  Google Scholar 

  • Tiloke C, Phulukdaree A, Anand K, Gengan RM, Chuturgoon AA (2016) Moringa oleifera gold nanoparticles modulate oncogenes, tumor suppressor genes, and caspase-9 splice variants in A549 cells. J Cell Biochem 117:2302–2314

    Article  CAS  Google Scholar 

  • Wang L, Xu J, Yan Y, Liu H, Li F (2019) Synthesis of gold nanoparticles from leaf Panax notoginseng and its anticancer activity in pancreatic cancer PANC-1 cell lines. Artif Cells Nanomed Biotechnol 47:1216–1223

    Article  CAS  Google Scholar 

  • Xu DC, Arthurton L, Baena-Lopez LA (2018) Learning on the fly: the interplay between caspases and cancer. Biomed Res Int 2018:5473180

    Google Scholar 

  • Zahin N, Anwar R, Tewari D, Kabir MT, Sajid A, Mathew B, Uddin MS, Aleya L, Abdel-Daim MM (2019) Nanoparticles and its biomedical applications in health and diseases: special focus on drug delivery. Environ Sci Pollut Res Int 2019:1–18. https://doi.org/10.1007/s11356-019-05211-0

    Article  CAS  Google Scholar 

  • Zhang C, Zhou Z, Zhi X, Ma Y, Wang K, Wang Y, Zhang Y, Fu H, Jin W, Pan F, Cui D (2015) Insights into the distinguishing stress-induced cytotoxicity of chiral gold nanoclusters and the relationship with GSTP1. Theranostics 5:134–149

    Article  CAS  Google Scholar 

  • Zhang L, Song R, Gu D, Zhang X, Yu B, Liu B, Xie J (2017) The role of GLI1 for 5-Fu resistance in colorectal cancer. Cell Biosci 7:17

    Article  CAS  Google Scholar 

  • Zhang X, Tan Z, Jia K, Zhang W, Dang M (2019) Rabdosia rubescens Linn: green synthesis of gold nanoparticles and their anticancer effects against human lung cancer cells A549. Artif Cells Nanomed Biotechnol 47:2171–2178

    Article  CAS  Google Scholar 

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Acknowledgments

Authors wish to thank Dr. R. Parameshwari, Researcher, Sri Ramachandra Institute of Higher Education and Research, Chennai, India, for the scientific assistance.

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Authors and Affiliations

  1. Department of Pharmacology, Saveetha Dental College, Saveetha Institute of Medical and Technical Sciences (SIMATS), Chennai, Tamil Nadu, 600077, India

    Mathivadani Vairavel & Ezhilarasan Devaraj

  2. Biomedical Research Unit and Laboratory Animal Centre, Saveetha Dental College (SDC), Saveetha Institute of Medical and Technical Sciences, Chennai, Tamil Nadu, 600077, India

    Ezhilarasan Devaraj

  3. Nanomedicine Laboratory, Department of Pharmacology, Saveetha Dental College, Saveetha Institute of Medical and Technical Sciences (SIMATS), Chennai, Tamil Nadu, 600077, India

    Rajeshkumar Shanmugam

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  1. Mathivadani Vairavel
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  2. Ezhilarasan Devaraj
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Correspondence to Ezhilarasan Devaraj.

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Vairavel, M., Devaraj, E. & Shanmugam, R. An eco-friendly synthesis of Enterococcus sp.–mediated gold nanoparticle induces cytotoxicity in human colorectal cancer cells. Environ Sci Pollut Res 27, 8166–8175 (2020). https://doi.org/10.1007/s11356-019-07511-x

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