Apoptosis induction in lung and prostate cancer cells through silver nanoparticles synthesized from Pinus roxburghii bioactive fraction

JBIC Journal of Biological Inorganic Chemistry - Tập 25 - Trang 23-37 - 2019
Reena Kumari1, Adesh K. Saini2, Amit Kumar2, Reena V. Saini1
1School of Biotechnology, Faculty of Applied Sciences and Biotechnology, Shoolini University, Himachal Pradesh, India
2Faculty of Basic Sciences, Shoolini University of Biotechnology and Management Sciences, Himachal Pradesh, India

Tóm tắt

The current study was carried out to synthesize silver nanoparticles (AgNPs) via bioactive fraction of Pinus roxburghii needles using a simple, cost-effective, and eco-friendly green chemistry method. As butanol fraction of P. roxburghii exhibited maximum anticancer activity on lung adenocarcinomas (A549) as compared to other fractions therefore, butanol fraction was used to synthesize silver nanoparticles (PNb–AgNPs). The characterization studies by UV–Vis spectroscopy, Fourier transform infrared spectroscopy (FTIR), X-ray diffraction (XRD), energy-dispersive X-ray spectroscopy (EDS) and selected area electron diffraction (SAED) confirmed the synthesis of the nanoparticles. The field emission scanning electron microscopy (FESEM) and high-resolution transmission electron microscopy (HRTEM) analysis showed the spherical structure of nanoparticles with an average diameter of approximately 80 nm. Interestingly, PNb–AgNPs exhibited significant cytotoxicity towards both A549 and prostatic small cell carcinomas (PC-3) with IC50 values of 11.28 ± 1.28 μg/ml and 56.27 ± 1.17 μg/ml, respectively, while lacking toxicity against normal human breast epithelial cells (fR2) and human peripheral blood lymphocytes (PBL). Further, enhanced reactive oxygen species generation, mitochondrial depolarization, apoptotic cell population (sub-G1) and DNA fragmentation observed in cancer cells were treated with PNb–AgNPs. Apoptosis was demonstrated by caspase-3 and PARP-1 activation in PNb–AgNPs-pretreated cancer cells. These results strongly suggest that PNb–AgNPs are capable of inducing cancer cell death and could act as a therapeutic nanoformulation for cancer.

Tài liệu tham khảo

Thakor AS, Gambhir SS (2013) Nanooncology: the future of cancer diagnosis and therapy. CA Cancer J Clin 63:395–418 Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. Ca Cancer J Clin 68:394–424 Stylianopoulos T (2013) EPR-effect: utilizing size-dependent nanoparticle delivery to solid tumors. Ther Deliv 4:421–423 Conde J, Doria G, Baptista P (2012) Noble metal nanoparticles applications in cancer. J Drug Deliv 1:1–12 Sharma A, Goyal AK, Rath G (2018) Recent advances in metal nanoparticles in cancer therapy. J Drug Target 26:617–632 Treuel L, Jiang X, Nienhaus GU (2013) New views on cellular uptake and trafficking of manufactured nanoparticles. J R Soc Interface 10:20120939 Barapatre A, Aadil KR, Jha H (2016) Synergistic antibacterial and antibiofilm activity of silver nanoparticles biosynthesized by lignin-degrading fungus. Bioresour Bioprocess 3:1–13 Perez-Diaz M, Alvarado-Gomez E, Magana-Aquino M, Sanchez-Sanchez R, Velasquillo C, Gonzalez C, Ganem-Rondero A, Martínez-Castañon G, Zavala-Alonso N, Martinez-Gutierrez F (2016) Anti-biofilm activity of chitosan gels formulated with silver nanoparticles and their cytotoxic effect on human fibroblasts. Mater Sci Eng C 60:317–323 Nakkala JR, Mata R, Raja K, Chandra VK, Sadras SR (2018) Green synthesized silver nanoparticles: catalytic dye degradation, in vitro anticancer activity and in vivo toxicity in rats. Mater Sci Eng C 91:372–381 Padinjarathil H, Joseph MM, Unnikrishnan BS, Preethi GU, Shiji R, Archana MG, Maya S, Syama HP, Sreelekha TT (2018) Galactomannan endowed biogenic silver nanoparticles exposed enhanced cancer cytotoxicity with excellent biocompatibility. Int J Biol Macromol 118:1174–1182 Jain S, Mehata MS (2017) Medicinal plant leaf extract and pure flavonoid mediated green synthesis of silver nanoparticles and their enhanced antibacterial property. Sci Rep 7:15867 Sankar R, Maheshwari R, Karthik S, Shivashangari KS, Ravikumar V (2014) Anticancer activity of Ficus religiosa engineered copper oxide nanoparticles. Mater Sci Eng C Mater Biol Appl 44:234–239 Azizi S, Mohamad R, Rahim RA, Mohammadinejad R, Ariff AB (2017) Hydrogel beads bio-nanocomposite based on κ-carrageenan and green synthesized silver nanoparticles for biomedical applications. Int J Biol Macromol 104:423–431 Wang L, Wu Y, Xie J, Wu S, Wu Z (2018) Characterization, antioxidant and antimicrobial activities of green synthesized silver nanoparticles from Psidium guajava L. leaf aqueous extracts. Mater Sci Eng C 86:1–8 Qasim M, Udomluck N, Chang J, Park H, Kim K (2018) Antimicrobial activity of silver nanoparticles encapsulated in poly-N-isopropylacrylamide-based polymeric nanoparticles. Int J Nanomed 13:235–249 Moldovan B, David L, Vulcu A, Olenic L, Perde-Schrepler M, Fischer-Fodor E, Baldea I, Clichici S, Filip GA (2017) In vitro and in vivo anti-inflammatory properties of green synthesized silver nanoparticles using Viburnum opulus L. fruits extract. Mater Sci Eng C Mater Biol Appl 79:720–727 Baharar J, Ramezani T, Mousavi M, Asadi-Samani M (2017) Antioxidant and anti-inflammatory activity of green synthesized silver nanoparticles using Salvia officinalis extract. Ann Trop Med Public Health 10:1265–1270 Sangaonkar GM, Pawar KD (2018) Garcinia indica mediated biogenic synthesis of silver nanoparticles with antibacterial and antioxidant activities. Colloids and Surf B: Biointerfaces 164:210–217 Maity P, Bepari M, Pradhan A, Baral R, Roy S, Choudhury SM (2018) Synthesis and characterization of biogenic metal nanoparticles and its cytotoxicity and anti-neoplasticity through the induction of oxidative stress, mitochondrial dysfunction and apoptosis. Colloids and Surf B: Biointerfaces 161:111–120 Khandel P, Yadaw RK, Soni DK, Kanwar L, Shahi SK (2018) Biogenesis of metal nanoparticles and their pharmacological applications: present status and application prospects. J Nanostruct Chem 8:217–254 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:E940 Keat CL, Aziz A, Eid AM, Elmarzugi NA (2015) Biosynthesis of nanoparticles and silver nanoparticles. Bioresour Bioprocess 2:47 Chaudhary AK, Ahmad S, Mazumder A (2014) Protective effect of Cedrus deodara and Pinus roxburghii experimentally induced gastric ulcers in rat. Int J Pharm Pharm Sci 6:587–591 Puri A, Srivastava AK, Singhal B, Mishra SK, Srivastava S, Lakshmi V (2011) Antidyslipidemic and antioxidant activity of Pinus roxburghii needles. Med Chem Res 20:1589–1593 Kaushik D, Kumarm A, Kaushik P, Rana AC (2012) Analgesic and anti-inflammatory activity of Pinus roxburghii Sarg. Adv Pharmacol Sci 2012:6. https://doi.org/10.1155/2012/245431 Khan I, Singh V, Chaudhary AK (2012) Hepatoprotective activity of Pinus roxburghii Sarg. wood oil against carbon tetrachloride and ethanol induced hepatotoxicity. Bangladesh J Pharmacol 7:94–99 Kaushik P, Khokra SL, Rana AC, Kaushik D (2015) Evaluation of anticancer activity of Pinus roxburghii Sarg. against IMR-32 human neuroblastoma cancer cell line. IJPCR 7:105–108 Maimoona A, Naeem I, Saddiqe Z, Ali N, Ahmed G, Shah I (2011) Analysis of total flavonoids and phenolics in different fractions of bark and needle extracts of Pinus roxburghii and Pinus wallichiana. J Med Plant Res 5:2724–2728 Chandan G, Chahal A, Saini AK, Saini RV (2016) Comparative analysis of the antioxidant and immunomodulatory potential of the fractions from leaves of Ocimum spp. (O. sanctum, O. basilicum, O. gratissimum). IJBPAS 5:2901–2917 Hira I, Kumar A, Kumari R, Saini AK, Saini RV (2018) Pectin-guar gum-zinc oxide nanocomposite enhances human lymphocytes cytotoxicity towards lung and breast carcinomas. Mater Sci Eng C 90:494–503 Hassan SE, Fouda A, Radwan AA, Salem SS, Barghoth MG, Awad MA, Abdo AM, El-Gamal MS (2019) Endophytic actinomycetes Streptomyces spp mediated biosynthesis of copper oxide nanoparticles as a promising tool for biotechnological applications. J Biol Inorg Chem 24:377–393 Lopez-Chaves C, Soto-Alvaredo J, Montes-Bayon M, Bettmer J, Llopis J, Sanchez-Gonzalez C (2018) Gold nanoparticles: distribution, bioaccumulation and toxicity, in vitro and in vivo studies. Nanomedicine 14:1–12 Baracca A, Sgarbi G, Solaini G, Lenaz G (2003) Rhodamine 123 as a probe of mitochondrial membrane potential: evaluation of proton flux through F0 during ATP synthesis. Biochem Biophys Acta 1606:137–146 Giri K, Ghosh U, Bhattacharyya NP, Basak S (2003) Caspase 8 mediated apoptotic cell death induced by L-sheet forming polyalanine peptides. FEBS Lett 555:380–384 Kaushik P, Kaushik D, Khokra SL (2013) Ethnobotany and phytopharmacology of Pinus roxburghii Sargent: a plant review. J Integr Med 11:371–376 Naeem I, Taskeen A, Mubeen H, Maimoona A (2010) Characterization of flavonols present in barks and needles of Pinus wallichiana and Pinus roxburghii. Asian J Chem 22:41–44 Haghparasti Z, Shahri MM (2018) Green synthesis of water-soluble nontoxic inorganic polymer nanocomposites containing silver nanoparticles using white tea extract and assessment of their in vitro antioxidant and cytotoxicity activities. Mater Sci Eng C 87:139–148 Nelaturi PD, Sriramaia NH, Nagaraj S, Kotakadi VS, Veeran AV, Kutty M, Pamidimukkala K (2017) An in vitro cytotoxic and genotoxic properties of Allamanda cathartica L. Latex green NPs on human peripheral blood mononuclear cells. Nano Biomed Eng 9:314–323 Behravan M, Panahi AH, Naghizadeh A, Ziaee M, Mahdavi R, Mirzapour A (2019) Facile green synthesis of silver nanoparticles using Berberis vulgaris leaf and root aqueous extract and its antibacterial activity. Int J Biol Macromol 124:148–154 Maciollek A, Ritter H (2014) One pot synthesis of silver nanoparticles using a cyclodextrin containing polymer as reductant and stabilizer. Beilstein J Nanotechnol 5:380–385 Coates J (2000) Interpretation of infrared spectra, a practical approach. In: Meyers RA (ed) Encyclopedia of analytical chemistry. Wiley, Chichester, pp 10881–10882 George BPA, Kumar N, Abrahamse H, Ray SS (2018) Apoptotic efficacy of multifaceted biosynthesized silver nanoparticles on human adenocarcinoma cells. Sci Rep 8:14368 El-Naggar NE, Hussein MH, El-Sawah AA (2017) Bio-fabrication of silver nanoparticles by phycocyanin, characterization, in vitro anticancer activity against breast cancer cell line and in vivo cytotoxicity. Sci Rep 7:10844 Dakshayani SS, Marulasiddeshwara MB, Kumar MNS, Ramesh G, Kumar PR, Devaraja S, Hosamani R (2019) Antimicrobial, anticoagulant and antiplatelet activities of green synthesized silver nanoparticles using Selaginella (Sanjeevini) plant extract. Int J Biol Macromol 131:787–797 Kummara S, Patil MB, Uriah T (2016) Synthesis, characterization, biocompatible and anticancer activity of green and chemically synthesized silver nanoparticles—a comparative study. Biomed Pharmacother 84:10–21 Stojnev S, Ristic-Petrovic A, Jankovic-Velickovic L (2013) Reactive oxygen species, apoptosis and cancer. Vojnosanit Pregl 70:675–678 Sankar R, Karthik A, Prabu A, Karthik S, Shivashangari KS, Ravikumar V (2013) Origanum vulgare mediated biosynthesis of silver nanoparticles for its antibacterial and anticancer activity. Colloids and Surf B: Biointerfaces 108:80–84 Giampazolias E, Tait SWG (2016) Mitochondria and the hallmarks of cancer. FEBS J 283:803–814 Hwang I, Lee J, Hwang JH, Kim K, Lee DG (2012) Silver nanoparticles induce apoptotic cell death in Candida albicans through the increase of hydroxyl radicals. FEBS J 279:1327–1338 Kajstura M, Halicka HD, Pryjma J, Darzynkiewicz Z (2007) Discontinuous fragmentation of nuclear DNA during apoptosis revealed by discrete ‘‘Sub-G1’’ peaks on DNA content histograms. Cytometry Part A 71A:125–131 Dadashpour M, Amandi AF, Moghaddam MP, Maleki MJ, Soozangar N, Jeddi F, Nouri M, Zarghami N, Soltanahmadi YP (2018) Biomimetic synthesis of silver nanoparticles using Matricaria chamomilla extract and their potential anticancer activity against human lung cancer cells. Mater Sci Eng C 92:902–912 Afsar T, Trembley JH, Salomon CE, Razak S, Khan MR, Ahmed K (2016) Growth inhibition and apoptosis in cancer cells induced by polyphenolic compounds of Acacia hydaspica: involvement of multiple signal transduction pathways. Sci Rep 6:23077 Gurunathan S, Han JW, Eppakayala V, Jeyaraj M, Kim JH (2013) Cytotoxicity of biologically synthesized silver nanoparticles in MDA-MB-231 human breast cancer cells. Biomed Res Int 2013:535796 Lyakhovich A, Surralles J (2010) Constitutive activation of Caspase-3 and poly ADP ribose polymerase cleavage in Fanconi anemia cells. Mol Cancer Res 8:46–56 Chaitanya GV, Steven AJ, Babu PP (2010) PARP-1 cleavage fragments: signatures of cell-death proteases in neurodegeneration. Cell Commun Signal 8:31