10.1007/s40097-021-00437-2

Cytotoxicity of aptamer-conjugated chitosan encapsulated mycogenic gold nanoparticles in human lung cancer cells

  • Xiaowen Hu1,
  • Kandasamy Saravanakumar1,
  • Anbazhagan Sathiyaseelan1,
  • Vinothkumar Rajamanickam2,
  • Myeong-Hyeon Wang*1,
  1. Department of Bio-Health Convergence, Kangwon National University, Chuncheon, 200-701, KR
  2. Key Laboratory of Imaging Diagnosis and Minimally Invasive Intervention Research, School of Medicine, Lishui Central Hospital, Lishui Hospital of Zhejiang University, The Fifth Affiliated Hospital of Wenzhou Medical University, Lishui, 323000, CN

Published in Issue 04-10-2021

How to Cite

Hu, X., Saravanakumar, K., Sathiyaseelan, A., Rajamanickam, V., & Wang, M.-H. (2021). Cytotoxicity of aptamer-conjugated chitosan encapsulated mycogenic gold nanoparticles in human lung cancer cells. Journal of Nanostructure in Chemistry, 12(4 (August 2022). https://doi.org/10.1007/s40097-021-00437-2
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Abstract

Abstract The present work investigated the cytotoxicity of aptamer (Apt)-conjugated chitosan (CST) encapsulated mycogenic ( Talaromyces purpureogenus (Tp)) gold nanoparticles (AuNPs) in human lung cancer cell line. A total of three steps were involved in the fabrication of Apt-CST-Tp-AuNPs: (i) mycogenic synthesis of Tp-AuNPs using mycelial extract of T. purpureogenus , (ii) encapsulation of the chitosan on Tp-AuNPs (CST-Tp-AuNPs), and (iii) conjugation of Apt in CST-Tp-AuNPs to form final material of Apt-CST-Tp-AuNPs. The nanoparticles Tp-AuNPs and Apt-CST-Tp-AuNPs were found to be hexagonal shaped with the size of 37.06 ± 6.70 nm and 62.05 ± 15.22 nm, respectively, observed by TEM analysis. But the DLS analysis showed the hydrodynamic size of Apt-CST-Tp-AuNPs was 91.67 ± 2.15 nm with a zeta potential of 47.31 ± 0.63 mV while Tp-AuNPs exhibited the hydrodynamic size of 56.13 ± 1.65 nm with a zeta potential of − 58.83 ± 1.64 mV. The size differences in the TEM and DLS analysis are attributed to the hydrodynamic nature of nanoparticles. The FTIR analysis demonstrated the capping of the mycelial extract on the surface of Tp-AuNPs and Apt-CST-Tp-AuNPs. The Apt-CST-Tp-AuNPs did not show cytotoxicity to human embryonic kidney cells (HEK293) while it showed ~ 60% of cell death in human lung cancer cells (A549). The annexin V FITC and PI staining results revealed that Apt-CST-Tp-AuNPs induced higher cell death (~ 8.60%) in A549 cells than Tp-AuNPs and CST-Tp-AuNPs. The Apt-CST-Tp-AuNPs triggered cytotoxicity in A549 cells through M1 phase cell cycle arrest and regulating the apoptosis-related protein (Bcl-2 and Bax) expressions. These results demonstrated the effective cytotoxic activity of Apt-CST-Tp-AuNPs in A549 cells. Graphic abstract

Keywords

  • Aptamer,
  • Endophytic fungi,
  • Gold nanoparticles,
  • Chitosan,
  • Human lung cancer

References

  1. Siegel et al. (2019) Cancer statistics, 2019 69(1) (pp. 7-34) https://doi.org/10.3322/caac.21551
  2. Mahalingaiah et al. (2019) Potential mechanisms of target-independent uptake and toxicity of antibody-drug conjugates (pp. 110-125) https://doi.org/10.1016/j.pharmthera.2019.04.008
  3. Moosavian and Sahebkar (2019) Aptamer-functionalized liposomes for targeted cancer therapy (pp. 144-154) https://doi.org/10.1016/j.canlet.2019.01.045
  4. Xu et al. (2018) Aptamer-functionalized albumin-based nanoparticles for targeted drug delivery (pp. 24-30) https://doi.org/10.1016/j.colsurfb.2018.07.008
  5. Yadav et al. (2015) Fungi as an efficient mycosystem for the synthesis of metal nanoparticles: progress and key aspects of research 37(11) (pp. 2099-2120) https://doi.org/10.1007/s10529-015-1901-6
  6. Huang et al. (2006) Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods 128(6) (pp. 2115-2120) https://doi.org/10.1021/ja057254a
  7. Huff et al. (2007) Hyperthermic effects of gold nanorods on tumor cells 2(1) (pp. 125-132) https://doi.org/10.2217/17435889.2.1.125
  8. Arokiyaraj et al. (2015) Green synthesis of Silver nanoparticles using aqueous extract of Taraxacum officinale and its antimicrobial activity (pp. 115-118) https://doi.org/10.22205/sijbs/2015/v1/i2/100433
  9. Singh et al. (2017) Mycosynthesis of bactericidal silver and polymorphic gold nanoparticles: physicochemical variation effects and mechanism 13(2) (pp. 191-207) https://doi.org/10.2217/nnm-2017-0235
  10. Sathiyaseelan et al. (2021) pH-controlled nucleolin targeted release of dual drug from chitosan-gold based aptamer functionalized nano drug delivery system for improved glioblastoma treatment https://doi.org/10.1016/j.carbpol.2021.117907
  11. Saravanakumar et al. (2021) Nucleolin targeted delivery of aptamer tagged Trichoderma derived crude protein coated gold nanoparticles for improved cytotoxicity in cancer cells (pp. 325-332) https://doi.org/10.1016/j.procbio.2021.01.022
  12. Saravanakumar et al. (2020) Dual stimuli-responsive release of aptamer AS1411 decorated erlotinib loaded chitosan nanoparticles for non-small-cell lung carcinoma therapy https://doi.org/10.1016/j.carbpol.2020.116407
  13. Khiralla, A., Spina, R., Yagi, S., Mohamed, L., Laurain, M.D.: Endophytic fungi: occurrence, classification, function and natural products. Pub. Univ. Lorraine. 1–19 (2016)
  14. Shankar et al. (2003) Bioreduction of chloroaurate ions by geranium leaves and its endophytic fungus yields gold nanoparticles of different shapes 13(7) (pp. 1822-1826) https://doi.org/10.1039/b303808b
  15. Musarrat et al. (2010) Production of antimicrobial silver nanoparticles in water extracts of the fungus Amylomyces rouxii strain KSU-09 101(22) (pp. 8772-8776) https://doi.org/10.1016/j.biortech.2010.06.065
  16. Verma et al. (2011) Biofabrication of anisotropic gold nanotriangles using extract of endophytic Aspergillus clavatus as a dual functional reductant and stabilizer 6(1) https://doi.org/10.1186/1556-276X-6-261
  17. Rehman et al. (2011) Silver nanoparticles: novel antimicrobial agent synthesized from an endophytic fungus Pestalotia sp. isolated from leaves of Syzygium cumini (L) (pp. 174-178)
  18. Kumari et al. (2018) Antiproliferative and antioxidative bioactive compounds in extracts of marine-derived endophytic fungus Talaromyces purpureogenus https://doi.org/10.3389/fmicb.2018.01777
  19. Pandit et al. (2019) Cicer arietinum (Bengal gram) husk as alternative for Talaromyces purpureogenus CFRM02 pigment production: Bioactivities and identification https://doi.org/10.1016/j.lwt.2019.108499
  20. Pandit et al. (2018) Functional attributes of a new molecule-2-hydroxymethyl-benzoic acid 2′-hydroxy-tetradecyl ester isolated from Talaromyces purpureogenus CFRM02 (pp. 89-96) https://doi.org/10.1016/j.foodchem.2018.02.034
  21. Bhatnagar et al. (2019) Biosynthesis of silver nanoparticles mediated by extracellular pigment from Talaromyces purpurogenus and their biomedical applications 9(7) https://doi.org/10.3390/nano9071042
  22. Hu et al. (2019) Mycosynthesis, characterization, anticancer and antibacterial activity of silver nanoparticles from endophytic fungus Talaromyces purpureogenus (pp. 3427-3438) https://doi.org/10.2147/IJN.S200817
  23. Azuma et al. (2015) Chitin, chitosan, and its derivatives for wound healing: old and new materials 6(1) (pp. 104-142) https://doi.org/10.3390/jfb6010104
  24. Abdelhamid et al. (2019) Synthesis of CdS-modified chitosan quantum dots for the drug delivery of Sesamol (pp. 90-99) https://doi.org/10.1016/j.carbpol.2019.03.024
  25. Dowaidar et al. (2018) Chitosan enhances gene delivery of oligonucleotide complexes with magnetic nanoparticles–cell-penetrating peptide 33(3) (pp. 392-401) https://doi.org/10.1177/0885328218796623
  26. Wang et al. (2019) Redox-responsive blend hydrogel films based on carboxymethyl cellulose/chitosan microspheres as dual delivery carrier (pp. 413-421) https://doi.org/10.1016/j.ijbiomac.2019.05.049
  27. Fathi et al. (2018) Chitosan-based multifunctional nanomedicines and theranostics for targeted therapy of cancer 38(6) (pp. 2110-2136) https://doi.org/10.1002/med.21506
  28. Abdelhamid et al. (2020) Carbonized chitosan encapsulated hierarchical porous zeolitic imidazolate frameworks nanoparticles for gene delivery https://doi.org/10.1016/j.micromeso.2020.110200
  29. Saravanakumar and Wang (2018) Trichoderma based synthesis of anti-pathogenic silver nanoparticles and their characterization, antioxidant and cytotoxicity properties (pp. 269-273) https://doi.org/10.1016/j.micpath.2017.12.005
  30. Saravanakumar et al. (2018) Zinc-chitosan nanoparticles induced apoptosis in human acute T-lymphocyte leukemia through activation of tumor necrosis factor receptor CD95 and apoptosis-related genes (pp. 1144-1153) https://doi.org/10.1016/j.ijbiomac.2018.08.017
  31. Saravanakumar et al. (2019) Enhanced cancer therapy with pH-dependent and aptamer functionalized doxorubicin loaded polymeric (poly D, L-lactic-co-glycolic acid) nanoparticles (pp. 143-151) https://doi.org/10.1016/j.abb.2019.07.004
  32. Saravanakumar et al. (2015) Anticancer potential of bioactive 16-methylheptadecanoic acid methyl ester derived from marine Trichoderma 13(3) (pp. 199-212) https://doi.org/10.1016/j.jab.2015.04.001
  33. Liu et al. (2018) Icariin possesses chondroprotective efficacy in a rat model of dexamethasone-induced cartilage injury through the activation of miR-206 targeting of cathepsin K 41(2) (pp. 1039-1047)
  34. Amendola and Meneghetti (2009) Size evaluation of gold nanoparticles by UV−VIS spectroscopy 113(11) (pp. 4277-4285) https://doi.org/10.1021/jp8082425
  35. Clarance et al. (2020) Green synthesis and characterization of gold nanoparticles using endophytic fungi Fusarium solani and its in-vitro anticancer and biomedical applications 27(2) (pp. 706-712) https://doi.org/10.1016/j.sjbs.2019.12.026
  36. Manjunath et al. (2017) Biofabrication of gold nanoparticles using marine endophytic fungus–Penicillium citrinum 11(1) (pp. 40-44) https://doi.org/10.1049/iet-nbt.2016.0065
  37. Huang and Yang (2004) Synthesis of chitosan-stabilized gold nanoparticles in the absence/presence of tripolyphosphate 5(6) (pp. 2340-2346) https://doi.org/10.1021/bm0497116
  38. Hamdy et al. (2018) Development of gold nanoparticles biosensor for ultrasensitive diagnosis of foot and mouth disease virus 16(1) https://doi.org/10.1186/s12951-018-0374-x
  39. Suvarna et al. (2007) Determinants of PF4/heparin immunogenicity 110(13) (pp. 4253-4260) https://doi.org/10.1182/blood-2007-08-105098
  40. Hemashekhar et al. (2019) Endophytic fungus Alternaria spp isolated from Rauvolfia tetraphylla root arbitrate synthesis of gold nanoparticles and evaluation of their antibacterial, antioxidant and antimitotic activities 10(3) https://doi.org/10.1088/2043-6254/ab38b0
  41. Uzma et al. (2018) Biogenesis of gold nanoparticles, role of fungal endophytes and evaluation of anticancer activity—a review (pp. 319-329)
  42. Parmar et al. (2020) 13-Endophytic fungi mediated biofabrication of nanoparticles and their potential applications (pp. 325-341) Woodhead Publishing https://doi.org/10.1016/B978-0-12-818734-0.00013-9
  43. Zambito, Y.: Nanoparticles based on chitosan derivatives. In: Advances in Biomaterials Science and Biomedical Applications, pp. 243–63 (2013)
  44. Chowdhury et al. (2018) Chitosan biopolymer functionalized gold nanoparticles with controlled cytotoxicity and improved antifilarial efficacy 1(3) (pp. 577-590) https://doi.org/10.1007/s42114-018-0040-7
  45. Sneha et al. (2014) Yucca-derived synthesis of gold nanomaterial and their catalytic potential https://doi.org/10.1186/1556-276X-9-627
  46. Brady and Boardman (1995) Introducing mineralogy students to x-ray diffraction through optical diffraction experiments using lasers 43(5) (pp. 471-476)
  47. Quideau et al. (2011) Plant polyphenols: chemical properties, biological activities, and synthesis 50(3) (pp. 586-621) https://doi.org/10.1002/anie.201000044
  48. Chai et al. (2012) Activation of the dormant secondary metabolite production by introducing gentamicin-resistance in a marine-derived Penicillium purpurogenum G59 10(3) (pp. 559-582) https://doi.org/10.3390/md10030559
  49. Sathiyaseelan et al. (2017) Fungal chitosan based nanocomposites sponges—an alternative medicine for wound dressing (pp. 1905-1915) https://doi.org/10.1016/j.ijbiomac.2017.03.188
  50. Choi and Ban (2016) Crystal structure of a DNA aptamer bound to PvLDH elucidates novel single-stranded DNA structural elements for folding and recognition 6(1) https://doi.org/10.1038/srep34998
  51. Houbraken et al. (2014) Chapter four-modern taxonomy of biotechnologically important Aspergillus and Penicillium species (pp. 199-249) Academic Press
  52. Wike et al. (1984) The relevance of tumour pH to the treatment of malignant disease 2(4) (pp. 343-366) https://doi.org/10.1016/S0167-8140(84)80077-8
  53. Saravanakumar et al. (2019) Novel metabolites from Trichoderma atroviride against human prostate cancer cells and their inhibitory effect on Helicobacter pylori and Shigella toxin producing Escherichia coli (pp. 19-26) https://doi.org/10.1016/j.micpath.2018.10.011
  54. Saravanakumar et al. (2019) Biosynthesis and characterization of copper oxide nanoparticles from indigenous fungi and its effect of photothermolysis on human lung carcinoma (pp. 103-109) https://doi.org/10.1016/j.jphotobiol.2018.11.017
  55. Narayani et al. (2019) In vitro anticancer activity of fucoidan extracted from Sargassum cinereum against Caco-2 cells (pp. 618-628) https://doi.org/10.1016/j.ijbiomac.2019.07.127
  56. Chandra and Tang (2009) Detection of apoptosis in cell-free systems (pp. 65-75) https://doi.org/10.1007/978-1-60327-017-5_5
  57. Messner et al. (2012) Apoptosis and necrosis: two different outcomes of cigarette smoke condensate-induced endothelial cell death 3(11) https://doi.org/10.1038/cddis.2012.162