Biosynthesis of Copper Oxide Nanoparticles Using Lactobacillus casei Subsp. Casei and its Anticancer and Antibacterial Activities

Author(s): Mehri Kouhkan, Parinaz Ahangar*, Leila Ashrafi Babaganjeh, Maryam Allahyari-Devin.

Journal Name: Current Nanoscience

Volume 16 , Issue 1 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: The present study reveals the synthesis of copper oxide nanoparticles (CuO NPs) by probiotic bacteria (Lactobacillus casei subsp. casei) and demonstrates the cytotoxic effects of these nanoparticles against gram negative and positive bacteria and cancer cell lines.

Methods: The CuO NPs are biosynthesized from Lactobacillus casei subsp. casei (L. casei) in an eco-friendly and cost-effective process. These nanoparticles are characterized using Fourier transform infrared spectroscopy (FT-IR), X-ray diffractometer (XRD), field emission scanning electron microscopy (FESEM), energy dispersive X-ray (EDX) and transmittance electron microscope (TEM) analysis. The antibacterial activity is examined by Well-diffusion, minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) assays using Broth microdilution. Anticancer effects of these nanoparticles are evaluated by methyl thiazolyl diphenyl-tetrazolium bromide (MTT) assay and Griess test.

Results: Our results confirm the biosynthesis of CuO NPs from L. casei. Antibacterial assays demonstrate that treatment of gram-negative and gram-positive bacteria with CuO NPs inhibits the growth of these bacteria. Furthermore, the cell viability of human cancer cells decreases while treated by nanoparticles. These nanoparticles increase nitric oxide (NO) secretion determined by NO production measurement.

Conclusion: These results suggest that CuO NPs may exert antibacterial effects as well as cytotoxic effects on cancer cells by suppressing their growth, increasing the oxidative stress and inducing apoptosis.

Keywords: Copper oxide nanoparticles, antibacterial activity, anticancer activity, breast cancer, gastric cancers, gram-negative and positive-bacteria.

[1]
Selvam, K.; Sudhakar, C.; Govarthanan, M.; Thiyagarajan, P.; Sengottaiyan, A.; Senthilkumar, B.; Selvankumar, T. Eco-friendly biosynthesis and characterization of silver nanoparticles using Tinospora cordifolia (Thunb.) Miers and evaluate its antibacterial, antioxidant potential. J. Radiat. Res. Appl. Sci., 2017, 10(1), 6-12.
[2]
Zhu, S.; Zhou, W. Optical properties and immunoassay applications of noble metal nanoparticles. J. Nanomater., 2010, 2010Article ID 562035
[3]
Chan, W.C.W.; Khademhosseini, A.; Möhwald, H.; Parak, W.J.; Miller, J.F.; Ozcan, A.; Weiss, P.S. Accelerating advances in science, engineering, and medicine through nanoscience and nanotechnology. ACS Nano, 2017, 11(4), 3423-3424.
[4]
Jin, R. The impacts of nanotechnology on catalysis by precious metal nanoparticles. Nanotechnol. Rev., 2012, 1, 31.
[5]
Swain, S.; Barik, S.K.; Behera, T.; Nayak, S.K.; Sahoo, S.K.; Mishra, S.S.; Swain, P. Green synthesis of gold nanoparticles using root and leaf extracts of Vetiveria zizanioides and Cannabis sativa and its antifungal activities. BioNanoScience, 2016, 6, 205-213.
[6]
Singh, P.; Kim, Y-J.; Zhang, D.; Yang, D-C. Biological synthesis of nanoparticles from plants and microorganisms. Trends Biotechnol., 2016, 34(7), 588-599.
[7]
Saratale, R.G.; Saratale, G.D.; Shin, H.S.; Jacob, J.M.; Pugazhendhi, A.; Bhaisare, M.; Kumar, G. New insights on the green synthesis of metallic nanoparticles using plant and waste biomaterials: Current knowledge, their agricultural and environmental applications. Environ. Sci. Pollut. Res. Int., 2018, 25(11), 10164-10183.
[8]
Nair, B.; Pradeep, T. Coalescence of nanoclusters and formation of submicron crystallites assisted by Lactobacillus strains. Cryst. Growth Des., 2002, 2, 293-298.
[9]
Patel, V.K.; Bhattacharya, S. High-performance nanothermite composites based on Aloe-vera-directed CuO nanorods. Appl. Mater. Interfaces, 2013, 5, 13364-13374.
[10]
Parikh, R.Y.; Singh, S.; Prasad, B.L.V.; Patole, M.S.; Sastry, M.; Shouche, Y.S. Extracellular synthesis of crystalline silver nanoparticles and molecular evidence of silver resistance from Morganella sp.: towards understanding biochemical synthesis mechanism. Chembiochem, 2008, 9(9), 1415-1422.
[11]
Iravani, S. Bacteria in nanoparticle synthesis: Current status and future prospects. Int. Sch. Res. Notices, 2014, 2014Article ID 359316
[12]
Akhtar, M.S.; Panwar, J.; Yun, Y-S. Biogenic synthesis of metallic nanoparticles by plant extracts. ACS Sustain. Chem. Eng., 2013, 1, 591-602.
[13]
Sivaraj, R.; Rahman, P.K.S.M.; Rajiv, P.; Narendhran, S.; Venckatesh, R. Biosynthesis and characterization of Acalypha indica mediated copper oxide nanoparticles and evaluation of its antimicrobial and anticancer activity. Spectrochim. Acta A, 2014, 129, 255-258.
[14]
Hasan, S.S.; Singh, S.; Parikh, R.; Dharne, M.; Patole, M.; Blv, P.; Shouche, Y. Bacterial synthesis of copper/copper oxide nanoparticles. J. Nanosci. Nanotechnol., 2008, 8(6), 3191-3196.
[15]
Raja Naika, R.; Lingaraju, K.; Manjunath, K.; Kumar, D.; Nagaraju, G.; Suresh, D.; Nagabhushana, H. Green synthesis of CuO nanoparticles using Gloriosa superba L. extract and their antibacterial activity. J. Taibah Univ. Sci., 2015, 9, 7-12.
[16]
Shantkriti, S.; Rani, P. Biological synthesis of copper nanoparticles using Pseudomonas fluorescens. Int. J. Curr. Microbiol. Appl. Sci., 2014, 3, 374-383.
[17]
Klaus, T.; Joerger, R.; Olsson, E.; Granqvist, C-G. Silver-based crystalline nanoparticles, microbially fabricated. Proc. Natl. Acad. Sci. USA, 1999, 96(24), 13611-13614.
[18]
Banks, J.M.; Williams, A.G. The role of the nonstarter lactic acid bacteria in cheddar cheese ripening. Int. J. Dairy Technol., 2004, 57(2‐3), 145-152.
[19]
Ashrafi Babaganjeh, L.; Ahangar, P.; Zarei, L. kouhkan, M. Biofabrication of silver nanoparticles using Lactobacillus casei subsp. casei and its efficacy against human pathogens bacteria and cancer cell lines. Med. Sci., 2018, 22(89), 99-110.
[20]
Kikuchi, F.; Kato, Y.; Furihata, K.; Kogure, T.; Imura, Y.; Yoshimura, E.; Suzuki, M. Formation of gold nanoparticles by glycolipids of Lactobacillus casei. Sci. Rep., 2016, 6, 34626.
[21]
Kalaiarasi, A.; Sankar, R.; Anusha, C.; Saravanan, K.; Aarthy, K.; Karthic, S.; Mathuram, T.L.; Ravikumar, V. Copper oxide nanoparticles induce anticancer activity in A549 lung cancer cells by inhibition of histone deacetylase. Biotechnol. Lett., 2018, 40, 249-256.
[22]
Thakkar, K.; Mhatre, S.; Parikh, R. Biological synthesis of metallic nanoparticles. Nanomedicine, 2010, 6(2), 257-262.
[23]
Sankar, R.; Baskaran, A.; Shivashangari, K.S.; Ravikumar, V. Inhibition of pathogenic bacterial growth on excision wound by green synthesized copper oxide nanoparticles leads to accelerated wound healing activity in Wistar Albino rats. J. Mater. Sci. Mater. Med., 2015, 26, 214.
[24]
Kahru, A.; Dubourguier, H-C. From ecotoxicology to nanoecotoxicology. Toxicology, 2010, 269(2), 105-119.
[25]
Aruoja, V.; Pokhrel, S.; Sihtmäe, M.; Mortimer, M.; Mädler, L.; Kahru, A. Toxicity of 12 metal-based nanoparticles to algae, bacteria and protozoa. Environ. Sci. Nano, 2015, 2, 630-644.
[26]
Ren, G.; Hu, D.; Cheng, E.W.C.; Vargas-Reus, M.A.; Reip, P.; Allaker, R.P. Characterisation of copper oxide nanoparticles for antimicrobial applications. Int. J. Antimicrob. Agents, 2009, 33(6), 587-590.
[27]
Rajeshkumar, S. Anticancer activity of eco-friendly gold nanoparticles against lung and liver cancer cells. J. Genet. Eng. Biotechnol., 2016, 14(1), 195-202.
[28]
Buttacavoli, M.; Albanese, N.N.; Di Cara, G.; Alduina, R.; Faleri, C.; Gallo, M.; Pizzolanti, G.; Gallo, G.; Feo, S.; Baldi, F.; Cancemi, P. Anticancer activity of biogenerated silver nanoparticles: An integrated proteomic investigation. Oncotarget, 2018, 9(11), 9685-9705.
[29]
Brigger, I.; Dubernet, C.; Couvreur, P. Nanoparticles in cancer therapy and diagnosis. Adv. Drug Deliv. Rev., 2012, 64, 24-36.
[30]
Chin, H.S.; Cheong, K.Y.; Razak, K.A. Review on oxides of antimony nanoparticles: Synthesis, properties, and applications. J. Mater. Sci., 2010, 45(22), 5993-6008.
[31]
Buttke, T.M.; Sandstrom, P.A. Oxidative stress as a mediator of apoptosis. Immunol. Today, 1994, 15(1), 7-10.
[32]
Hanot-Roy, M.; Tubeuf, E.; Guilbert, A.; Bado-Nilles, A.; Vigneron, P.; Trouiller, B.; Braun, A.; Lacroix, G. Oxidative stress pathways involved in cytotoxicity and genotoxicity of titanium dioxide (TiO2) nanoparticles on cells constitutive of alveolo-capillary barrier in vitro. Toxicol. In Vitro, 2016, 33, 125-135.
[33]
Pujalté, I.; Passagne, I.; Brouillaud, B.; Tréguer, M.; Durand, E.; Ohayon-Courtès, C.; L’Azou, B. Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part. Fibre Toxicol., 2011, 8(1), 10.
[34]
Ramaswamy, S.V.P.; Narendhran, S.; Sivaraj, R. Potentiating effect of ecofriendly synthesis of copper oxide nanoparticles using brown alga: Antimicrobial and anticancer activities. Bull. Mater. Sci., 2016, 39(2), 361-364.
[35]
Bhuvaneshwari, V.; Vaidehi, D.; Logpriya, S. Green synthesis of copper oxide nanoparticles for biological applications. Microbiol. Curr. Res., 2018, 2(1), 5-6.
[36]
Krithiga, N.; Jayachitra, A.; Rajalakshmi, A. Synthesis, characterization and analysis of the effect of copper oxide nanoparticles in biological systems. Indian J. NanoSci., 2013, 1(1), 6-15.
[37]
Bryan, N.S.; Grisham, M.B. Methods to detect nitric oxide and its metabolites in biological samples. Free Radic. Biol. Med., 2007, 43(5), 645-657.
[38]
Miranda, K.M.; Espey, M.G.; Wink, D.A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide, 2001, 5(1), 62-71.
[39]
Ahmad, A.; Mukherjee, P.; Senapati, S.; Mandal, D.; Khan, M.I.; Kumar, R.; Sastry, M. Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf. B Biointerfaces, 2003, 28(4), 313-318.
[40]
Iravani, S.; Korbekandi, H.; Mirmohammadi, S.V.; Zolfaghari, B. Synthesis of silver nanoparticles: Chemical, physical and biological methods. Res. Pharm. Sci., 2014, 9(6), 385-406.
[41]
Khan, A.; Rashid, A.; Younas, R.; Chong, R. A chemical reduction approach to the synthesis of copper nanoparticles. Int. Nano Lett., 2016, 6(1), 21-26.
[42]
Gawande, M.B.; Goswami, A.; Felpin, F-X.; Asefa, T.; Huang, X.; Silva, R.; Zou, X.; Zboril, R.; Varma, R.S. Cu and Cu-based nanoparticles: Synthesis and applications in catalysis. Chem. Rev., 2016, 116(6), 3722-3811.
[43]
Malviya, N.; Carpenter, G.; Oswal, N.; Gupta, N. Synthesis and characterization of CuO nano particles using precipitation method. AIP Conf. Proc., 2015, 1665050038
[44]
Zhang, Q.; Zhang, K.; Xu, D.; Yang, G.; Huang, H.; Nie, F.; Liu, C.; Yang, S. CuO nanostructures: Synthesis, characterization, growth mechanisms, fundamental properties, and applications. Prog. Mater. Sci., 2014, 60, 208-337.
[45]
Mishra, S.B.; Rao, C.V.; Ojha, S.K.; Vijayakumar, M.; Verma, A. An analytical review of plants for anti-diabetic activity with their phytoconstituent and mechanism of action: A review. Int. J. Pharmacol. Sci. Res., 2010, 1, 29-44.
[46]
Gopinath, V.; Priyadarshini, S.; Al-Maleki, A.R.; Alagiri, M.; Yahya, R.; Saravanan, S.; Vadivelu, J. In vitro toxicity, apoptosis and antimicrobial effects of phyto-mediated copper oxide nanoparticles. RSC Adv, 2016, 6, 110986-110995.
[47]
Volanti, D.P.; Keyson, D.; Cavalcante, L.S.; Simões, A.Z.; Joya, M.R.; Longo, E.; Varela, J.A.; Pizani, P.S.; Souza, A.G. Synthesis and characterization of CuO flower-nanostructure processing by a domestic hydrothermal microwave. J. Alloys Compd., 2008, 459(1), 537-542.
[48]
Kim, J.H.; Cho, H.; Ryu, S.E.; Choi, M.U. Effects of metal ions on the activity of protein tyrosine phosphatase VHR: Highly potent and reversible oxidative inactivation by Cu2+ ion. Arch. Biochem. Biophys., 2000, 382(1), 72-80.
[49]
Tavassoli Hojati, S.; Alaghemand, H.; Hamze, F.; Ahmadian Babaki, F.; Rajab-Nia, R.; Rezvani, M.B.; Kaviani, M.; Atai, M. Antibacterial, physical and mechanical properties of flowable resin composites containing zinc oxide nanoparticles. Dent. Mater., 2013, 29(5), 495-505.
[50]
Sondi, I.; Salopek-Sondi, B. Silver nanoparticles as antimicrobial agent: A case study on E. coli as a model for gram-negative bacteria. J. Colloid Interface Sci., 2004, 275(1), 177-182.
[51]
Pazos-Ortiz, E.; Roque-Ruiz, J.H.; Hinojos-Márquez, E.A.; López-Esparza, J.; Donohué-Cornejo, A.; Cuevas-González, J.C.; Espinosa-Cristóbal, L.F.; Reyes-López, S.Y. Dose-dependent antimicrobial activity of silver nanoparticles on polycaprolactone fibers against gram-positive and gram-negative bacteria. J. Nanomater., 2017, 2017 Article ID 4752314
[52]
Abbaszadegan, A.; Ghahramani, Y.; Gholami, A.; Hemmateenejad, B.; Dorostkar, S.; Nabavizadeh, M.; Sharghi, H. The effect of charge at the surface of silver nanoparticles on antimicrobial activity against gram-positive and gram-negative bacteria: A preliminary study. J. Nanomater., 2015, 2015 720654
[53]
Khan, M.F.; Hameedullah, M.; Ansari, A.H.; Ahmad, E.; Lohani, M.B.; Khan, R.H.; Alam, M.M.; Khan, W.; Husain, F.M.; Ahmad, I. Flower-shaped ZnO nanoparticles synthesized by a novel approach at near-room temperatures with antibacterial and antifungal properties. Int. J. Nanomedicine, 2014, 9, 853-864.
[54]
Khashan, K.S.; Sulaiman, G.M.; Abdulameer, F.A. Synthesis and antibacterial activity of CuO nanoparticles suspension induced by laser ablation in liquid. Arab. J. Sci. Eng., 2016, 41(1), 301-310.
[55]
Taran, M.; Rad, M.; Alavi, M. Antibacterial activity of copper oxide (CuO) nanoparticles biosynthesized by Bacillus sp. FU4: Optimization of experiment design. Pharm. Sci., 2017, 23(3), 198-206.
[56]
Abboud, Y.; Saffaj, T.; Chagraoui, A.; El Bouari, A.; Brouzi, K.; Tanane, O.; Ihssane, B. Biosynthesis, characterization and antimicrobial activity of copper oxide nanoparticles (CONPs) produced using brown alga extract (Bifurcaria bifurcata). Appl. Nanosci., 2014, 4(5), 571-576.
[57]
Emami-Karvani, Z.; Chehrazi, P. Antibacterial activity of ZnO nanoparticle on gram-positive and gram-negative bacteria. Afr. J. Microbiol. Res., 2012, 5, 1368-1373.
[58]
Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods, 1983, 65(1-2), 55-63.
[59]
Nagajyothi, P.C.; Pandurangan, M.; Tvm, S.; Hwan Kim, D.; Shim, J. Green synthesis: In-vitro anticancer activity of copper oxide nanoparticles against human cervical carcinoma cells. Arab. J. Chem., 2016, 10(2), 215-225.
[60]
Wang, Z.; Li, N.; Zhao, J.; White, J.C.; Qu, P.; Xing, B. CuO nanoparticle interaction with human epithelial cells: Cellular uptake, location, export, and genotoxicity. Chem. Res. Toxicol., 2012, 25(7), 1512-1521.
[61]
Shafagh, M.; Rahmani, F.; Delirezh, N. CuO nanoparticles induce cytotoxicity and apoptosis in human K562 cancer cell line via mitochondrial pathway, through reactive oxygen species and P53. Iran. J. Basic Med. Sci., 2015, 18(10), 993-1000.
[62]
Rehana, D.; Mahendiran, D.; Kumar, R.S.; Rahiman, A.K. Evaluation of antioxidant and anticancer activity of copper oxide nanoparticles synthesized using medicinally important plant extracts. Biomed. Pharmacother., 2017, 89, 1067-1077.
[63]
Germi, K.G.; Shabani, F.; Khodayari, A.; Azizian-Kalandaragh, Y. Structural and biological properties of CuO nanoparticles prepared under ultrasonic irradiation. Synth. React. Inorg. M, 2014, 44(9), 1286-1290.
[64]
Gnanavel, V.; Palanichamy, V.; Roopan, S.M. Biosynthesis and characterization of copper oxide nanoparticles and its anticancer activity on human colon cancer cell lines (HCT-116). J. Photochem. Photobiol. B, 2017, 171, 133-138.
[65]
Siddiqui, M.A.; Alhadlaq, H.A.; Ahmad, J.; Al-Khedhairy, A.A.; Musarrat, J.; Ahamed, M. Copper oxide nanoparticles induced mitochondria mediated apoptosis in human hepatocarcinoma cells. PLoS One, 2013, 8(8)e69534
[66]
Karlsson, H.; Cronholm, P.; Gustafsson, J.; Möller, L. Copper oxide nanoparticles are highly toxic: A comparison between metal oxide nanoparticles and carbon nanotubes. Chem. Res. Toxicol., 2008, 21, 1726-1732.
[67]
Vinardell, M.P.; Mitjans, M. Antitumor activities of metal oxide nanoparticles. Nanomaterials, 2015, 5(2), 1004-1021.
[68]
Nel, A.; Xia, T.; Madler, L.; Li, N. Toxic potential of materials at the nano level. Science, 2006, 311(5761), 622-627.
[69]
Ahamed, M.; Karns, M.; Goodson, M.; Rowe, J.; Hussain, S.M.; Schlager, J.J.; Hong, Y. DNA damage response to different surface chemistry of silver nanoparticles in mammalian cells. Toxicol. Appl. Pharmacol., 2008, 233(3), 404-410.
[70]
Kang, S.J.; Kim, B.M.; Lee, Y.J.; Hong, S.H.; Chung, H.W. Titanium dioxide nanoparticles induce apoptosis through the JNK/p38-caspase-8-Bid pathway in phytohemagglutinin-stimulated human lymphocytes. Biochem. Biophys. Res. Commun., 2009, 386(4), 682-687.
[71]
Fahmy, B.; Cormier, S.A. Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol. In Vitro, 2009, 23(7), 1365-1371.
[72]
Berntsen, P.; Park, C.Y.; Rothen-Rutishauser, B.; Tsuda, A.; Sager, T.M.; Molina, R.M.; Donaghey, T.C.; Alencar, A.M.; Kasahara, D.I.; Ericsson, T.; Millet, E.J.; Swenson, J.; Tschumperlin, D.J.; Butler, J.P.; Brain, J.D.; Fredberg, J.J.; Gehr, P.; Zhou, E.H. Biomechanical effects of environmental and engineered particles on human airway smooth muscle cells. Interface Focus, 2010, 7, 333-340.
[73]
Piret, J.P.; Jacques, D.; Audinot, J.N.; Mejia, J.; Boilan, E.; Noel, F.; Fransolet, M.; Demazy, C.; Lucas, S.; Saout, C.; Toussaint, O. Copper(II) oxide nanoparticles penetrate into HepG2 cells, exert cytotoxicity via oxidative stress and induce pro-inflammatory response. Nanoscale, 2012, 4(22), 7168-7184.
[74]
Antonini, J.M.; Lawryk, N.J.; Murthy, G.G.; Brain, J.D. Effect of welding fume solubility on lung macrophage viability and function in vitro. J. Toxicol. Environ. Health A, 1999, 58, 343-363.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 16
ISSUE: 1
Year: 2020
Page: [101 - 111]
Pages: 11
DOI: 10.2174/1573413715666190318155801
Price: $65

Article Metrics

PDF: 17
HTML: 1