Skip to main content

Advertisement

Log in

Fungal-mediated synthesis of pharmaceutically active silver nanoparticles and anticancer property against A549 cells through apoptosis

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Generally, fungi have the ability to secrete large amounts of secondary metabolites which have the ability to reduce metal ions to metallic nanoparticles. In this report, silver nanoparticles (AgNPs) were synthesized by using an endophytic fungus isolated from the medicinal plant, Catharanthus roseus (Linn.). The endophytic fungus was identified as Botryosphaeria rhodina based on the ITS sequencing. The synthesized AgNPs were characterized by adopting various high-throughput techniques, scanning electron microscopy (SEM) equipped with energy dispersive X-ray analysis (EDAX), high-resolution transmission electron microscopy (HR-TEM) and UV–Visible spectrophotometer. In vitro anticancer efficacy of AgNPs was tested on A-549 cells. The synthesized AgNPs were effective in scavenging free radicals and induced hallmarks of apoptosis including nuclear and DNA fragmentation in lung (A549) cancer cell lines under in vitro conditions. The results suggested that the natural biomolecules in the endophytic fungi incorporated into the nanoparticles could be responsible for the synergetic cytotoxic activity against cancer cells. The AgNPs were found to have cytotoxicity IC50 of 40 μg/mL against A549 cells. To the best our knowledge, this is the first report demonstrating that AgNPs from Botryosphaeria rhodina could be able to induce apoptosis in various types of cancer cells as a novel strategy for cancer treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agrawal DC, Tsay HS, Shyur LF, Wu YC, Wang SY (eds) (2017) Medicinal plants and fungi. Rec Adv Res & Dev (Vol. 4). Singapore: Springer Singapore. https://doi.org/10.1007/978-981-10-5978-0

  • Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf B: Biointerfaces 8(4):313–318

    Google Scholar 

  • Akther T, Hemalatha S (2019) Mycosilver nanoparticles: synthesis, characterization and its efficacy against plant pathogenic fungi. Bio Nano Sci. https://doi.org/10.1007/s12668-019-0607-y

  • Akther T, Khan MS, Hemalatha S (2017) Extraction of flavonoids from various parts of Couropitaguianensis and its efficacy against pathogenic bacteria. Asian J Pharm Clin Res 10(4):354–358

    CAS  Google Scholar 

  • Akther T, Khan MS, Hemalatha S (2018a) A facile and rapid method for green synthesis of myco nanoparticles using endophytic fungi. Int J Nano Dimens 9(4):435–441

    CAS  Google Scholar 

  • Akther T, Khan MS, Hemalatha S (2018b) Novel silver nanoparticles synthesized from the anthers of CouropitaguianensisAbul. control growth and biofilm formation in human pathogens. Nano. Biomed Eng 10(3):250–257

    CAS  Google Scholar 

  • Alghuthaymi MA, Almoammar H, Rai M, Said-Galiev E, Abd-Elsalam KA (2015) Myconanoparticles: synthesis and their role in phytopathogens management. Biotech Equip 29:221–236

    CAS  Google Scholar 

  • Aruna JK, Sashidharb RB, Arunachalama J (2012) Aqueous extract of gum olibanum (Boswelliaserrata): A reductant and stabilizer for the biosynthesis of antibacterial silver nanoparticles. Process Biochem 47:1516–1520

    Google Scholar 

  • Barar J (2015) Bioimpacts of nanoparticle size: why it matters? Bio Impac 5(3):113–115. https://doi.org/10.15171/bi.2015.23

    Article  Google Scholar 

  • Barbara S, Christine B, Siegfried D, Anne-Katrin R, Karsten K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106(90):0953–7562

    Google Scholar 

  • Basavaraja S, Balaji SD, Lagashetty A, Rajasab AH, Venkataraman A (2008) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium semitectum. Mat Res B 43:1164–1170

    CAS  Google Scholar 

  • Begum SMFM, Priya S, Sundararajan R, Hemalatha S (2017) Novel anticancerous compounds from Sargassum wightii: In silico and in vitro approaches to test the antiproliferative efficacy. J Adv Pharm Edu Res 7(3):272–277

    CAS  Google Scholar 

  • Dan L, Liu Z, Yuan Y, Liu Y, Niu F (2015) Green synthesis of gallic acid-coated silver nanoparticles with high antimicrobial activity and low cytotoxicity to normal cells. Process Biochem 50:357–366

    Google Scholar 

  • Duran N, Marcarto PD, D’Souza GIH, Alves OL, Esposito E (2007) Antibacterial effect of silver nanoparticles produced by fungal process on textile fabrics and their effluent treatment. J Biomed Nanotechnol 3:203–208

    CAS  Google Scholar 

  • Fazeela SM, Chitra K, Benin J, Sundararajan R, Hemalatha S (2018) Gelidiella acerosa inhibits lung cancer proliferation. BMC Complement Altern Med 18:104

  • Ge L, Li Q, Wang M, Ouyang J, Li X, Xing MM (2014) Nano silver particles in medical applications: synthesis, performance, and toxicity. Int J Nanomedicine 9:2399–2407

    Google Scholar 

  • Gittins DI, Bethell D, Schiffrin DJ, Nichols RJ (2000) A nanometre-scale electronic switch consisting of a metal cluster and redox-addressable groups. Nature 408:67–69

    CAS  Google Scholar 

  • Gopinath V, MubarakAli D, Priyadarshini S, MeeraPriyadarshini N, Thajuddin N, Velusamy P (2012a) Biosynthesis of silver nanoparticles from Tribulus terrestris and its antimicrobial activity: a novel biological approach. Colloids Surf B: Biointerfaces 96:69–74

    CAS  Google Scholar 

  • Gopinath V, MubarakAli D, Priyadarshini S, Priyadharsshini NM, Thajuddin N, Velusamy P (2012b) Biosynthesis of silver nanoparticles from Tribulus terrestris and its antimicrobial activity: a novel biological approach. Coll Surf B 96:69–74

    CAS  Google Scholar 

  • Gopinath V, Priyadarshini S, MunFailoke AJ, EnrichoMarsili MAD, Velusamy P, Jamuna V (2015) Biogenic synthesis, characterization of antibacterial silver nanoparticles and its cell cytotoxicity. Arab J Chem 10(8):1107–1117

    Google Scholar 

  • He S, Guo Z, Zhang Y, Zhang S, Wang J, Gu N (2007) Biosynthesis of gold nanoparticles using the bacteria Rhodo pseudomonas capsulate. Mater Lett 61:3984–3987

    CAS  Google Scholar 

  • Jain PK, Lee KS, El-Sayed IH, El-Sayed MA (2006) Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: applications in biological imaging and biomedicine. J Phys Chem B 110:7238–7248

    CAS  Google Scholar 

  • Jain PK, Hunag XH, IH EI-S, MA EI-S (2008) Noble metals on the nanoscale: optical and photo thermal properties and some applications in imaging, sensing, biology and medicine. Acc Chem Res 41:1578–1586

    CAS  Google Scholar 

  • Jeyaraj M, Rajesh M, Arun R, MubarakAli D, Sathishkumar D, Sivanathan G, Dev K, Manickavasagam M, Premkumar K, Thajuddin N, Ganapathi A (2012) An investigation on the cytotoxicity and caspase-mediated apoptotic effect of biologically synthesized silver nanoparticles using Podophyllum hexandrum on human cerival carcinoma cells. Colloids Surf B: Biointerfaces 102:708–717

    Google Scholar 

  • Jia M, Chen L, Xin HL (2016) A friendly relationship between endophytic fungi and medicinal plants: a systematic review. Front Microbiol 7:906. https://doi.org/10.3389/fmicb.2016.00906

    Article  Google Scholar 

  • Kaufmann SH, Earnshaw WC (2000) Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256:42–49

    CAS  Google Scholar 

  • Kumar A, Patil D, Rajamohanan PR, Ahmad A (2013) Isolation, purification and characterization of vinblastine and vincristine from endophytic fungus Fusarium oxysporum isolated from Cathranthus roseus. PLoS One 8(9):1

    Google Scholar 

  • Kumar R, Lu SK, Minchom A, Sharp A, Davidson M, Gunapala R, Yap TA, Bhosle J, Popat S, O’Brien MER (2016) A phase 1b trial of the combination of an all-oral regimen of capecitabine and erlotinib in advanced non-small cell lung cancer in Caucasian patients. Cancer Chemother Pharmacol 77:375–383

    CAS  Google Scholar 

  • Kumari V, Kaushal K, Sharma AK, Mishra RC, Soni P (2018) Some phytochemicals found in medicinal plants used in cancer - a review. Med Chem (Los Angeles) 8:423–425

    Google Scholar 

  • Lamabam SD, Santa RJ (2014) Ultra-structures of silver nanoparticles biosynthesized using endophytic fungi. J Micros Ultrastruct 3(1):29–37

    Google Scholar 

  • Ma Q, Wawersik M, Matunis EL (2014) The Jak-STAT Target Chinmo prevents sex transformation of adult stem cells in the Drosophila testis niche. Dev Cell 31(4):474–486

    CAS  Google Scholar 

  • Manjunath HM, Joshi CG, Raju NG (2017) Bio-fabrication of gold nanoparticles using marine endophytic fungus Penicilliumcitrinum. IET Nanobiotech 11:40–44

    Google Scholar 

  • MubarakAli D, Divya C, Gunasekaran M, Thajuddin N (2011a) Biosynthesis and characterization of silicon-germanium oxide nanocomposite by diatom. Digest JNanomater Biostruc 6(1):117–120

    Google Scholar 

  • MubarakAli D, Sasikala M, Gunasekaran M, Thajuddin N (2011b) Biosynthesis and characterization of silver nanoparticles using marine Cyanobacterium, OscillatoriawilleiNTDM01. Digest J Nanomater Biostruct 6:385–390

    Google Scholar 

  • MubarakAli D, Thajuddin N, Jeganathan K, Gunasekaran M (2011c) Plant extract mediated synthesis of silver and gold nanoparticles and its antibacterial activity against clinically isolated pathogens. Colloids Surf B: Biointerfaces 85:360–365

    CAS  Google Scholar 

  • MubarakAli D, Gopinath V, Rameshbabu N, Thajuddin N (2012) Synthesis and characterization of CdS nanoparticles using C-phycoerythrin from the marine cyanobacteria. Matrl Lett 74:8–11

    CAS  Google Scholar 

  • Mukunthan K, Elumalai E, Patel TN, Murty VR (2011) Cathranthus roseus: a natural source for the synthesis of silver nanoparticles. A P J of Trop Biomed 1(4):270–274. https://doi.org/10.1016/S2221-1691(11)60041-5

    Article  CAS  Google Scholar 

  • Nayak B, Pinto Pereira LM (2006) Cathranthus roseus flower extract has wound-healing activity in Sprague Dawley rats. BMC Complement Altern Med 6:41. https://doi.org/10.1186/1472-6882-6-41

    Article  CAS  Google Scholar 

  • Nisa H, Kamili AN, Nawchoo IA, Shafi S, Shameem N, Bandh SA (2015) Fungal endophytes as prolific source of phytochemicals and other bioactive natural products: a review. Microb Pathog 82:50–59

    CAS  Google Scholar 

  • Oves M, Aslam M, Rauf MA, Qayyum S, Qari HA, Khan MS, Alam MZ, Tabrez S, Pugazhendhi A, Ismail IMI (2018) Antimicrobial and anticancer activities of silver nanoparticles synthesized from the root hair extract of Phoenix dactylifera. Mat Lett Eng: C 89:429–443

    CAS  Google Scholar 

  • Prior LR, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302

    CAS  Google Scholar 

  • Priyadarshini S, Gopinath V, MeeraPriyadharsshini N, MubarakAli D, Velusamy P (2013) Synthesis of anisotropic silver nanoparticles using novel strain, Bacillus flexus and its biomedical application. Colloids Surf B: Biointerfaces 102(1):232–237

    CAS  Google Scholar 

  • Pugazhendhi A, Prabakar D, Jacob JM, Karuppusamy I, Saratale RG (2018) Synthesis and characterization of silver nanoparticles using Gelidiumamansiiand its antimicrobial property against various pathogenic bacteria. Microb Pathog 114:41–45

    CAS  Google Scholar 

  • Pugazhendhi A, Shobana S, Nguyen DD, Banu JR, Sivagurunathan P, Chang SW, Ponnusamy VK, Kumar G (2019) Application of nanotechnology (nanoparticles) in dark fermentative hydrogen production. Int J Hydrog Energy 44(3):1431–1440

    CAS  Google Scholar 

  • Qui M, Xie RS, Zhang YH, Chen HM (2010) Isolation and identification of two flavanoid producing endophytic fungi from Ginkgo biloba L. Ann Microbiol 60:143–150

    Google Scholar 

  • Sanna VPN, Dessì G, Manconi P, Mariani A, Dedola S, Rassu M, Crosio C, Iaccarino C, Sechi M (2014) Single-step green synthesis and characterization of gold-conjugated polyphenol nanoparticles with antioxidant and biological activities. Int J Nanomedicine 9:17

    Google Scholar 

  • Saratale GD, Saratale RG, Benelli G, Kumar G, Pugazhendhi A, Kim DS, Shin HS (2017) Anti-diabetic potential of silver nanoparticles synthesized with Argyreia nervosa leaf extract high synergistic antibacterial activity with standard antibiotics against foodborne bacteria. J Clust Sci 28:1709–1727

    CAS  Google Scholar 

  • Saravanakumar K, Sabarathinam S, NipunBabu V, MubarakAli D, Kathiresane K, Myeong-Hyeon W (2018) Biosynthesis and characterization of copper oxide nanoparticles from indigenous fungi and its effect on photothermolysis of human lung carcinoma. J Photochem Photobiol B Biol 190:103–109

    Google Scholar 

  • Saravanan M, Arokiyaraj S, Lakshmic T, Pugazhendhid A (2018) Synthesis of silver nanoparticles from Phenerochaete chrysosporium (MTCC-787) and their antibacterial activity against human pathogenic bacteria. Microb Pathog 117:68–72

    CAS  Google Scholar 

  • Sastry M, Ahmad A, Islam NI, Kumar R (2003) Biosynthesis of metal nanoparticles using fungi and actinomycete. Curr Sci 85:162

    CAS  Google Scholar 

  • Sathish Kumar S, Fazeela M, Saroj Kumar S, Kulandaisamy S, Mahasampath Gowri S, Hemalatha S, Balasubramanian KK (2018) Synthesis, characterization, in vitro, and in silico studies of 4-(2′-hydroxybenzoyl) and 4-(2′-hydroxynaphthoyl)-thiabenzene-1-methyl-1-oxides. Synth Commun 48(5):553–560

    CAS  Google Scholar 

  • Shaligram NS, Bule M, Bhambure R, Singhal RS, Singh SK, Szakacs G, Ashok Pandey A (2009) Biosynthesis of silver nanoparticles using aqueous extract from the compactin producing fungal strain. Process Biochem 44:939–943

    CAS  Google Scholar 

  • Strobel G, Daisy B (2013) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    Google Scholar 

  • Strobel G, Daisy B, Castillo U, Harper J (2004) Natural Products from endophytic microorganisms. J Nat Prod 67:257–268

    CAS  Google Scholar 

  • Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-tieulent J, Jemal A (2012) Global Cancer Statistics. CA Cancer J Clin 65:87–108

    Google Scholar 

  • Ubaid R, Hemalatha S (2017) Marine endophytic actinomycetes assisted synthesis of copper nanoparticles (CuNPs): Characterization and antibacterial efficacy against human pathogens. Mater Lett 194:176–180

    Google Scholar 

  • Vaidyanathan R, Gopalram S, Kalishwaralal K, Deepak V, Pandian SRK, Gurunathan S (2010) Enhanced silver nanoparticle synthesis by optimization of nitrate reductase activity. Colloids Surf B: Biointerfaces 75(1):335–341

    CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Acad. Press, San Diego, pp 315–322

    Google Scholar 

  • Yang MZ, Ma MD, Yuan MQ, Huang ZY, Yang WX, Zhang HB (2016) Fungal endophytes as a metabolic fine-tuning regulator for wine grape. PLoS One 11:e0163186

    Google Scholar 

  • Yezhelyev MV, Gao X, Xing Y, Al-Hajj A, Nie S, O’Regan RM (2006) Emerging use of nanoparticles in diagnosis and treatment of breast cancer. Lancet Oncol 7:657–667

    CAS  Google Scholar 

  • Zhihong N, Alla P, Eugenia K (2010) Properties and emerging applications of self-assembled structures made from inorganic nanoparticles. Nat Nanotechnol 5:15–25

    Google Scholar 

Download references

Funding

This research was supported by a grant from the Advanced Level State Biotech Hub at Mizoram University sponsored by Department of Biotechnology (DBT), Govt. of India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hemalatha Srinivasan.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 732 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akther, T., Vabeiryureilai Mathipi, Nachimuthu Senthil Kumar et al. Fungal-mediated synthesis of pharmaceutically active silver nanoparticles and anticancer property against A549 cells through apoptosis . Environ Sci Pollut Res 26, 13649–13657 (2019). https://doi.org/10.1007/s11356-019-04718-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04718-w

Keywords

Navigation