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Environmental Science and Pollution Research

, Volume 26, Issue 13, pp 13649–13657 | Cite as

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

  • Tahira Akther
  • Vabeiryureilai Mathipi
  • Nachimuthu Senthil Kumar
  • MubarakAli Davoodbasha
  • Hemalatha SrinivasanEmail author
Research Article
  • 102 Downloads

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.

Keywords

Botryosphaeria rhodina Silver nanoparticles (AgNPs) FTIR SEM TEM Antioxidant activity Anticancer activity 

Notes

Funding information

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.

Supplementary material

11356_2019_4718_MOESM1_ESM.docx (729 kb)
ESM 1 (DOCX 732 kb)

References

  1. 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
  2. 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):313–318Google Scholar
  3. 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
  4. 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):354–358Google Scholar
  5. 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):435–441Google Scholar
  6. 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):250–257Google Scholar
  7. Alghuthaymi MA, Almoammar H, Rai M, Said-Galiev E, Abd-Elsalam KA (2015) Myconanoparticles: synthesis and their role in phytopathogens management. Biotech Equip 29:221–236Google Scholar
  8. 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 47:1516–1520Google Scholar
  9. Barar J (2015) Bioimpacts of nanoparticle size: why it matters? Bio Impac 5(3):113–115.  https://doi.org/10.15171/bi.2015.23 Google Scholar
  10. 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):0953–7562Google Scholar
  11. Basavaraja S, Balaji SD, Lagashetty A, Rajasab AH, Venkataraman A (2008) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium semitectum. Mat Res B 43:1164–1170Google Scholar
  12. 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):272–277Google Scholar
  13. 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 50:357–366Google Scholar
  14. 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 3:203–208Google Scholar
  15. Fazeela SM, Chitra K, Benin J, Sundararajan R, Hemalatha S (2018) Gelidiella acerosa inhibits lung cancer proliferation. BMC Complement Altern Med 18:104Google Scholar
  16. 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 9:2399–2407Google Scholar
  17. Gittins DI, Bethell D, Schiffrin DJ, Nichols RJ (2000) A nanometre-scale electronic switch consisting of a metal cluster and redox-addressable groups. Nature 408:67–69Google Scholar
  18. 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 96:69–74Google Scholar
  19. 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 96:69–74Google Scholar
  20. 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):1107–1117Google Scholar
  21. 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 61:3984–3987Google Scholar
  22. 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 110:7238–7248Google Scholar
  23. 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 41:1578–1586Google Scholar
  24. 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 102:708–717Google Scholar
  25. 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 Google Scholar
  26. Kaufmann SH, Earnshaw WC (2000) Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256:42–49Google Scholar
  27. 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):1Google Scholar
  28. 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 77:375–383Google Scholar
  29. 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) 8:423–425Google Scholar
  30. Lamabam SD, Santa RJ (2014) Ultra-structures of silver nanoparticles biosynthesized using endophytic fungi. J Micros Ultrastruct 3(1):29–37Google Scholar
  31. 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):474–486Google Scholar
  32. Manjunath HM, Joshi CG, Raju NG (2017) Bio-fabrication of gold nanoparticles using marine endophytic fungus Penicilliumcitrinum. IET Nanobiotech 11:40–44Google Scholar
  33. MubarakAli D, Divya C, Gunasekaran M, Thajuddin N (2011a) Biosynthesis and characterization of silicon-germanium oxide nanocomposite by diatom. Digest JNanomater Biostruc 6(1):117–120Google Scholar
  34. MubarakAli D, Sasikala M, Gunasekaran M, Thajuddin N (2011b) Biosynthesis and characterization of silver nanoparticles using marine Cyanobacterium, OscillatoriawilleiNTDM01. Digest J Nanomater Biostruct 6:385–390Google Scholar
  35. 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 85:360–365Google Scholar
  36. MubarakAli D, Gopinath V, Rameshbabu N, Thajuddin N (2012) Synthesis and characterization of CdS nanoparticles using C-phycoerythrin from the marine cyanobacteria. Matrl Lett 74:8–11Google Scholar
  37. 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 Google Scholar
  38. 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 Google Scholar
  39. 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 82:50–59Google Scholar
  40. 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 89:429–443Google Scholar
  41. 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 53:4290–4302Google Scholar
  42. 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):232–237Google Scholar
  43. 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 114:41–45Google Scholar
  44. 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):1431–1440Google Scholar
  45. Qui M, Xie RS, Zhang YH, Chen HM (2010) Isolation and identification of two flavanoid producing endophytic fungi from Ginkgo biloba L. Ann Microbiol 60:143–150Google Scholar
  46. 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 9:17Google Scholar
  47. 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 28:1709–1727Google Scholar
  48. 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 190:103–109Google Scholar
  49. 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 117:68–72Google Scholar
  50. Sastry M, Ahmad A, Islam NI, Kumar R (2003) Biosynthesis of metal nanoparticles using fungi and actinomycete. Curr Sci 85:162Google Scholar
  51. 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):553–560Google Scholar
  52. 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 44:939–943Google Scholar
  53. Strobel G, Daisy B (2013) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502Google Scholar
  54. Strobel G, Daisy B, Castillo U, Harper J (2004) Natural Products from endophytic microorganisms. J Nat Prod 67:257–268Google Scholar
  55. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-tieulent J, Jemal A (2012) Global Cancer Statistics. CA Cancer J Clin 65:87–108Google Scholar
  56. Ubaid R, Hemalatha S (2017) Marine endophytic actinomycetes assisted synthesis of copper nanoparticles (CuNPs): Characterization and antibacterial efficacy against human pathogens. Mater Lett 194:176–180Google Scholar
  57. 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):335–341Google Scholar
  58. 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 315–322Google Scholar
  59. 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:e0163186Google Scholar
  60. 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 7:657–667Google Scholar
  61. Zhihong N, Alla P, Eugenia K (2010) Properties and emerging applications of self-assembled structures made from inorganic nanoparticles. Nat Nanotechnol 5:15–25Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Tahira Akther
    • 1
  • Vabeiryureilai Mathipi
    • 2
  • Nachimuthu Senthil Kumar
    • 2
  • MubarakAli Davoodbasha
    • 1
  • Hemalatha Srinivasan
    • 1
    Email author
  1. 1.School of Life SciencesB.S. Abdur Rahman Crescent Institute of Science and TechnologyChennaiIndia
  2. 2.Department of BiotechnologyMizoram UniversityAizawlIndia

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