Abstract
In this study, we aimed at the green synthesis of silver nanoparticles (AgNPs) using Lavandula angustifolia extract and the investigation of the anti-proliferative and apoptotic inducing effects of these nanoparticles in the U87MG glioblastoma cancer cell line. Green synthesized silver nanoparticles were characterized by various analytical techniques such as UV–Visible Spectrophotometer (UV–Vis), scanning electron microscopy (SEM) and Energy Dispersive X-ray (EDX). UV–Vis spectroscopy displayed a specific silver plasmon peak at 430 nm. U87MG cells were treated at increased concentrations with Lavandula angustifolia-AgNPs (La-AgNPs) (0–20 µg/mL) for 72 h and the anti-proliferative effects of green synthesized silver nanoparticles on U87MG cells were evaluated by MTT assay. The La- AgNPs induced a statistically significant dose-dependent decrease in proliferation and increased cytotoxicity in U87MG cells. The IC50 value is 7.536 µg/mL. Furthermore, the expression of apoptosis proteins caspase-3, caspase-8 and caspase-9 was analyzed using ELISA and caspase-3 and p53 using western blotting. The results suggest that La-AgNPs induce cell death in U87MG cells through the p53 mediated intrinsic apoptotic pathway. Together, the present findings suggest that La-AgNPs could be considered as a potential option for the treatment of glioblastoma.
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Adebayo EA, Ibikunle JB, Oke AM, Lateef A, Azeez MA, Oluwatoyin AO, AyanfeOluwa AV, Blessing OT, Comfort OO, Adekunle OO, Badmus JA, Asafa TB, Beukes LS, Gueguim-Kan EB, Hakeem AS (2019) Antimicrobial and antioxidant activity of silver, gold and silver-gold alloy nanoparticles phytosynthesized using extract of Opuntia ficus-indica. Rev Adv Mater Sci 58(1):313–326. https://doi.org/10.1515/rams-2019-0039
Adelere IA, Lateef A (2016) A novel approach to the green synthesis of metallic nanoparticles: the use of agro-wastes, enzymes and pigments. Nanotechnol Rev 5(6):567–587. https://doi.org/10.1515/ntrev-2016-0024
Ahmed S, Annu S, Ikram S, Yudha S (2016) Biosynthesis of gold nanoparticles: a green approach. J Photochem Photobiol B Biol 161:141–153. https://doi.org/10.1016/j.jphotobiol.2016.04.034
Aina DA, Owolo O, Lateef A, Aina FO, Hakeem AS, Adeoye-Isijola M, Okon V, Asafa TB, Elegbede JA, Olukanni OD, Adediji I (2019) Biomedical applications of Chasmanthera dependens stem extract mediated silver nanoparticles as antimicrobial, antioxidant, anticoagulant, thrombolytic, and larvicidal agents. Karbala Int J Mod Sci 5(2):71–80. https://doi.org/10.33640/2405-609X.1018
Akintayo GO, Lateef A, Azeez MA, Asafa TB, Oladipo IC, Badmus JA, Ojo SA, Elegbede JA, Gueguim-Kana EB, Beukes LS (2020) Synthesis, bioactivities and cytogenotoxicity of animal fur-mediated silver nanoparticles. IOP Conf Ser: Mat Sci Eng 805:012041. https://doi.org/10.1088/1757-899X/805/1/012041
Albrecht MA, Evan CW, Raston CR (2006) Green chemistry and the health implications of nanoparticles. J Green Chem 8:417–432. https://doi.org/10.1039/B517131H
Azeez MA, Durodola FA, Lateef A, Yekeen TA, Adubi AO, Oladipo IC, Adebayo EA, Badmus JA, Abawulem AO (2020) Green synthesized novel silver nanoparticles and their application as anticoagulant and thrombolytic agents: a perspective. IOP Conf Ser: Mat Sci Eng 805:012043. https://doi.org/10.1088/1757-899X/805/1/012043
Azizi M, Ghourchian H, Yazdian F, Bagherifam S, Bekhradnia S, Nyström B (2017) Anti-cancerous effect of albumin coated silver nanoparticles on MDA-MB 231 human breast cancer cell line. Sci Rep 7:5178. https://doi.org/10.1038/s41598-017-05461-3
Badmus JA, Oyemomi SA, Adedosu OT, Yekeen TA, Azeez MA, Adebayo EA, Lateef A, Badeggi UM, Botha S, Hussein AA, Marnewick JL (2020) Photo-assisted bio-fabrication of silver nanoparticles using Annona muricata leaf extract: exploring the antioxidant, anti-diabetic, antimicrobial, and cytotoxic activities. Heliyon 6(11):e05413. https://doi.org/10.1016/j.heliyon.2020.e05413
Batash R, Asna N, Schaffer P, Francis N, Schaffer M (2017) Glioblastoma multiforme, diagnosis and treatment recent literature review. Curr Med Chem 24(27):3002–3009. https://doi.org/10.2174/0929867324666170516123206
Baytop T (1999) Therapy with plants in Turkey (Past and Present) (in Turkish). Nobel Tip Press, Istanbul
Brown SA (1962) Biosynthesis of coumarin and herniarin in lavender. Science 137:977–978. https://doi.org/10.1126/science.137.3534.977
Buckner JC (2003) Factors influencing survival in high-grade gliomas. Semin Oncol 30(6 Suppl 19):10–14. https://doi.org/10.1053/j.seminoncol.2003.11.031
Burnett KM, Solterbeck LA, Strapp CM (2004) Scent and mood state following an anxiety-provoking task. Psychol Rep 95(2):707–722. https://doi.org/10.2466/pr0.95.2.707-722
Ceylan AA, Vomel N, Kaya N, Celik E, Nigdeli E (1988) A investigation on effects to yield and qulity of plant space in lavender (in Turkish). Ege Univ J Agric Fac 25(2):135–145
Chan EL, Zhang C, Cheung GS (2015) Cytotoxicity of a novel nano-silver particle endodontic irrigant. Cosmet Investig Dent 7:65–74. https://doi.org/10.2147/CCIDE.S68874
Dada AO, Adekola FA, Dada FE, Adelani-Akande AT, Bello MO, Okonkwo CR, Inyinbor AA, Oluyori AP, Olayanju A, Ajanaku KO, Adetunji CO (2019) Silver nanoparticle synthesis by Acalypha wilkesiana extract: phytochemical screening, characterization, influence of operational parameters, and preliminary antibacterial testing. Heliyon 5(10):e02517. https://doi.org/10.1016/j.heliyon.2019.e02517
Daphne J, Francis A, Mohanty R, Ojha N, Das N (2018) Green synthesis of antibacterial silver nanoparticles using yeast isolates and its characterization. J Phar Tech Res 11(1):83–92. https://doi.org/10.5958/0974-360X.2018.00016.1
D’Auria FD, Tecca M, Strippoli V, Salvatore G, Battinelli L, Mazzanti G (2005) Antifungal activity of Lavandula angustifolia essential oil against Candida albicans yeast and mycelial form. Med Mycol 43(5):391–396. https://doi.org/10.1080/13693780400004810
DeAngelis LM (2001) Brain tumors. N Engl J Med 344(2):114–123. https://doi.org/10.1056/NEJM200101113440207
Dehghanizade S, Arasteh J, Mirzaie A (2018) Green synthesis of silver nanoparticles using Anthemis atropatana extract: characterization and in vitro biological activities. Artif Cells Nanomed Biotechnol 46(1):160–168. https://doi.org/10.1080/21691401.2017.1304402
Donmez S (2020) Green synthesis of zinc oxide nanoparticles using Zingiber officinale root extract and their applications in glucose biosensor. El-Cezerî J Sci Eng 7(3):1191–1200. https://doi.org/10.31202/ecjse.729462
Elegbede JA, Elson CE, Qureshi A, Tanner MA, Gould MN (1984) Inhibition of DMBA-induced mammary cancer by the monoterpene d-limonene. Carcinogenesis 5(5):661–664. https://doi.org/10.1093/carcin/5.5.661
Eugenio M, Campanati L, Müller N, Romão LF, de Souza J, Alves-Leon S, de Souza W, Sant’Anna C (2018) Silver/silver chloride nanoparticles inhibit the proliferation of human glioblastoma cells. Cytotechnology 70(6):1607–1618. https://doi.org/10.1007/s10616-018-0253-1
Fridman JS, Lowe SW (2003) Control of apoptosis by p53. Oncogene 22(56):9030–9040. https://doi.org/10.1038/sj.onc.1207116
Gabbrielli G, Loggini F, Cioni PL, Giannaccini B, Mancuso E (1988) Activity of lavandino essential oil against non-tubercular opportunistic rapid grown mycobacteria. Pharmacol Res Commun 20(Suppl 5):37–40. https://doi.org/10.1016/s0031-6989(88)80836-1
Ghaffari-Moghaddam M, Hadi-Dabanlou R, Khajeh M, Rakhshanipour M, Shameli K (2014) Green synthesis of silver nanoparticles using plant extracts. Korean J Chem Eng 31:548–557. https://doi.org/10.1007/s11814-014-0014-6
Godwin OE, Egwaikhide PA (2020) Phytochemical and antimicrobial properties of Lavandula angustifolia. Int J Modern Chem 12(1):1–12
Goel N, Kim H, Lao RP (2005) An olfactory stimulus modifies nighttime sleep in young men and women. Chronobiol Int 22(5):889–904. https://doi.org/10.1080/07420520500263276
Gowramma B, Keerthi U, Rafi M, Muralidhara Rao D (2015) Biogenic silver nanoparticles production and characterization from native stain of Corynebacterium species and its antimicrobial activity. 3 Biotech 5(2):195–201. https://doi.org/10.1007/s13205-014-0210-4
Han J, Gurunathan S, Jeong JK, Choi YJ, Kwon DN, Park JK, Kim JH (2014) Oxidative stress mediated cytotoxicity of biologically synthesized silver nanoparticles in human lung epithelial adenocarcinoma cell line. Nanoscale Res Lett 9:459. https://doi.org/10.1186/1556-276x-9-459
Hohmann J, Zupkó I, Rédei D, Csányi M, Falkay G, Máthé I, Janicsák G (1999) Protective effects of the aerial parts of Salvia officinalis, Melissa officinalis and Lavandula angustifolia and their constituents against enzyme-dependent and enzyme-independent lipid peroxidation. Planta Med 65(6):576–578. https://doi.org/10.1055/s-2006-960830
Iacob G, Dinca EB (2009) Current data and strategy in glioblastoma multiforme. J Med Life 2(4):386–393
Ironside CV, Moss TH, Louis DN (2002) Astrocytic tumours. In diagnostic pathology of nervous system tumours, 1st edn. Churchill-Livingstone, London
Kalimuthu K, Babu RS, Venkataraman D, Bilal M, Gurunathan S (2008) Biosynthesis of silver nanocrystals by Bacillus licheniformis. Colloids Surf B Biointerfaces 65(1):150–153. https://doi.org/10.1016/j.colsurfb.2008.02.018
Kane FM, Brodie EE, Coull A, Coyne L, Howd A, Milne A, Niven CC, Robbins R (2004) The analgesic effect of odour and music upon dressing change. Br J Nurs 13(19):4–12. https://doi.org/10.12968/bjon.2004.13.Sup4.16343
Kantari C, Walczak H (2011) Caspase-8 and bid: caught in the act between death receptors and mitochondria. Biochem Biophys Acta 1813(2011):558–563. https://doi.org/10.1016/j.bbamcr.2011.01.026
Karim MN, Anderson SR, Singh S, Ramanathan R, Bansal V (2018) Nanostructured silver fabric as a free-standing nanozyme for colorimetric detection of glucose in urine. Biosens Bioelectron 110:8–15. https://doi.org/10.1016/j.bios.2018.03.025
Khan M, Khan ST, Khan M, Adil SF, Musarrat J, Al-Khedhairy AA, Al-Warthan A, Siddiqui MR, Alkhathlan HZ (2014) Antibacterial properties of silver nanoparticles synthesized using Pulicaria glutinosa plant extract as a green bioreductant. Int J Nanomedicine 9:3551–3565. https://doi.org/10.2147/IJN.S61983
Kruidering M, Evan GI (2000) Caspase-8 in apoptosis: the beginning of “the end”? IUBMB Life 50(2):85–90. https://doi.org/10.1080/713803693
Lateef A, Ojo SA, Elegbede JA (2016) The emerging roles of arthropods and their metabolites in the green synthesis of metallic nanoparticles. Nanotechnol Rev 5(6):601–622. https://doi.org/10.1515/ntrev-2016-0049
Lateef A, Folarin BI, Oladejo SM, Akinola PO, Beukes LS, Gueguim-Kana EB (2018) Characterization, antimicrobial, antioxidant, and anticoagulant activities of silver nanoparticles synthesized from Petiveria alliacea L. leaf extract. Prep Biochem Biotechnol 48(7):646–652. https://doi.org/10.1080/10826068.2018.1479864
Levin VA, Leibel SA, Gutin PH, Hellman S, Rosenberg SA, DeVita VT (2001) Cancer: principles and practice of oncology, 6th edn. Lippincott Williams & Wilkins, Philadelphia
Liang P, Shi H, Zhu W, Gui Q, Xu Y, Meng J, Guo X, Gong Z, Chen H (2017) Silver nanoparticles enhance the sensitivity of temozolomide on human glioma cells. Oncotarget 8(5):7533–7539. https://doi.org/10.18632/oncotarget.13503
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97–109. https://doi.org/10.1007/s00401-007-0243-4
Marslin G, Siram K, Maqbool Q, Selvakesavan RK, Kruszka D, Kachlicki P, Franklin G (2018) Secondary metabolites in the green synthesis of metallic nanoparticles. Materials (basel) 11(6):940. https://doi.org/10.3390/ma11060940
Murugesan K, Koroth J, Srinivasan PP, Singh A, Mukundan S, Karki SS, Choudhary B, Gupta CM (2019) Effects of green synthesised silver nanoparticles (ST06-AgNPs) using curcumin derivative (ST06) on human cervical cancer cells (HeLa) in vitro and EAC tumor bearing mice models. Int J Nanomedicine 14:5257–5270. https://doi.org/10.2147/IJN.S202404
Nadagouda MN, Speth TF, Varma RS (2011) Microwave-assisted green synthesis of silver nanostructures. Acc Chem Res 44(7):469–478. https://doi.org/10.1021/ar1001457
Newton HB (2010) Overview of the molecular genetics and molecular chemotherapy of GBM. In: Ray SK (ed) Molecular mechanisms of pathogenesis and current therapeutic strategies. Springer, London
Ohgaki H, Dessen P, Jourde B, Horstmann S, Nıshıkawa T, Dı Patre PL, Burkhard C, Schuler D, Probst-Hensch NM, Maıorka PC et al (2004) Genetic pathways to glioblastoma: a population-based study. Cancer Res 64(19):6892–6899. https://doi.org/10.1158/0008-5472.CAN-04-1337
Porter AG, Jänicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6(2):99–104. https://doi.org/10.1038/sj.cdd.4400476
Rautela A, Rani J, Debnath M (2019) Green synthesis of silver nanoparticles from Tectona grandis seeds extract: characterization and mechanism of antimicrobial action on different microorganisms. J Anal Sci Technol 10:5. https://doi.org/10.1186/s40543-018-0163-z
Raveendran P, Fu J, Wallen SL (2003) Completely “green” synthesis and stabilization of metal nanoparticles. J Am Chem Soc 125(46):13940–13941. https://doi.org/10.1021/ja029267j
Rychlik M (2008) Quantification of free coumarin and its liberation from glucosylated precursors by stable isotope dilution assays based on liquid chromatography-tandem mass spectrometric detection. J Agric Food Chem 56(3):796–801. https://doi.org/10.1021/jf0728348
Salehi S, Shandiz SA, Ghanbar F, Darvish MR, Ardestani MS, Mirzaie A, Jafari M (2016) Phytosynthesis of silver nanoparticles using Artemisia marschalliana Sprengel aerial part extract and assessment of their antioxidant, anticancer, and antibacterial properties. Int J Nanomedicine 11:1835–1846. https://doi.org/10.2147/IJN.S99882
Sastry M, Mayyaa KS, Bandyopadhyay K (1997) pH dependent changes in the optical properties of carboxylic acid derivatized silver colloid particles. Colloids Surf A Physicochem Eng Asp 127:221–228
Sastry M, Patil V, Sainkar SR (1998) Electrostatically controlled diffusion of carboxylic acid derivatized silver colloidal particles in thermally evaporated fatty amine films. J Phys Chem 102(8):1404–1410. https://doi.org/10.1039/A704355D
Sathornsumetee S, Rich JN (2008) Designer therapies for glioblastoma multiforme. Ann N Y Acad Sci 1142:108–132. https://doi.org/10.1196/annals.1444.009
Shimizu M, Shogawa H, Matsuzawa T, Yonezawa S, Hayashi T, Arisawa M, Suzuki S, Yoshizaki M, Morita N, Ferro E et al (1990) Anti-inflammatory constituents of topically applied crude drugs IV. Constituents and anti-inflammatory effect of Paraguayan crude drug “alhucema” (Lavandula latifolia Vill.). Chem Pharm Bull (tokyo) 38(8):2283–2284. https://doi.org/10.1248/cpb.38.2283
Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups, National Cancer Institute of Canada Clinical Trials Group (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996. https://doi.org/10.1056/NEJMoa043330
Thakkar KN, Mhatre SS, Parikh RY (2010) Biological synthesis of metallic nanoparticles. Nanomedicine 6(2):257–262. https://doi.org/10.1016/j.nano.2009.07.002
Urbańska K, Pająk B, Orzechowski A, Sokołowska J, Grodzik M, Sawosz E, Szmidt M, Sysa P (2015) The effect of silver nanoparticles (AgNPs) on proliferation and apoptosis of in ovo cultured glioblastoma multiforme (GBM) cells. Nanoscale Res Lett 10:98. https://doi.org/10.1186/s11671-015-0823-5
Wang Z, Liu S, Ma J, Qu G, Wang X, Yu S, He J, Liu J, Xia T, Jiang GB (2013) Silver nanoparticles induced RNA polymerase-silver binding and RNA transcription inhibition in erythroid progenitor cells. ACS Nano 7(5):4171–4186. https://doi.org/10.1021/nn400594s
Yuan YG, Wang YH, Xing HH, Gurunathan S (2017) Quercetin-mediated synthesis of graphene oxide–silver nanoparticle nanocomposites: a suitable alternative nanotherapy for neuroblastoma. Int J Nanomed 12:5819–5839. https://doi.org/10.2147/ijn.s140605
Zhang XF, Liu ZG, Shen W, Gurunathan S (2016) Silver nanoparticles: synthesis, characterization, properties, applications, and therapeutic approaches. Int J Mol Sci 17(9):1534. https://doi.org/10.3390/ijms17091534
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This research was supported by the Burdur Mehmet Akif Ersoy University Scientific Research Rrojects Unit [Project number: 0617-YL-19].
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AS and CAA designed the study, performed the synthesis and characterization of nanoparticles, cell culture and MTT assay, drafted the paper, and contributed equally to this work. SP participated in ELISA and Western blot analyses. AS and SP involved in statistical analysis. All authors have read and approved the final manuscript.
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Simsek, A., Pehlivanoglu, S. & Aydin Acar, C. Anti-proliferative and apoptotic effects of green synthesized silver nanoparticles using Lavandula angustifolia on human glioblastoma cells. 3 Biotech 11, 374 (2021). https://doi.org/10.1007/s13205-021-02923-4
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DOI: https://doi.org/10.1007/s13205-021-02923-4