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Newly isolated sporopollenin microcages from Cedrus libani and Pinus nigra as carrier for Oxaliplatin; xCELLigence RTCA-based release assay

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Abstract

Sporopollenin-mediated control drug delivery has been studied extensively owing to its desirable physicochemical and biological properties. Herein, sporopollenin was successfully extracted from C. libani and P. nigra pollens followed by loading of a commonly known anticancer drug Oxaliplatin. Drug loading and physicochemical features were confirmed by using light microscopy, FT-IR, SEM and TGA. For the first-time, real-time cell analyzer system xCELLigence was employed to record the Oxaliplatin loaded sporopollenin-mediated cell death (CaCo-2 and Vero cells) in real time. Both the release assays confirmed the slow release of oxaliplatin from sporopollenin for around 40–45 h. The expression of MYC and FOXO-3 genes has been significantly increased in CaCo2 cell and decreased non-cancerous Vero cell confirming the fact that sporopollenin-mediated control release of oxaliplatin is promoting apoptosis cell death preventing the spread of negative effects on nearby healthy cells. All the results suggested that C. libani and P. nigra can be suitable candidates for the slow delivery of drugs.

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References

  1. Agrawal M et al. (2020) Recent strategies and advances in the fabrication of nano lipid carriers and their application towards brain targeting. Journal of Controlled Release

  2. Alan Ş, Yıldırım Ö, Pınar N, Seçil D, Keçeli T, Çeter T, Mısırlıgil Z (2009) Betula pendula Roth (syn = B. verrucosa) polenine duyarlı hastalarda IgE reaktivite profilleri. Asthma Allergy Immunol 7:100–105

    Google Scholar 

  3. Alshehri SM, Al-Lohedan HA, Al-Farraj E, Alhokbany N, Chaudhary AA, Ahamad T (2016) Macroporous natural capsules extracted from Phoenix dactylifera L. spore and their application in oral drugs delivery. Int J Pharm 504:39–47

    CAS  PubMed  Google Scholar 

  4. Brown JM, Attardi LD (2005) The role of apoptosis in cancer development and treatment response. Nat Rev Cancer 5:231–237

    CAS  PubMed  Google Scholar 

  5. Caminade A-M, Turrin C-O (2014) Dendrimers for drug delivery. J Mater Chem B 2:4055–4066

    CAS  PubMed  Google Scholar 

  6. Diego-Taboada A, Beckett S, Atkin S, Mackenzie G (2014) Hollow pollen shells to enhance drug delivery. Pharmaceutics 6:80–96

    PubMed  PubMed Central  Google Scholar 

  7. Diego-Taboada A et al (2013) Protein free microcapsules obtained from plant spores as a model for drug delivery: ibuprofen encapsulation, release and taste masking. J Mater Chem B 1:707–713

    CAS  PubMed  Google Scholar 

  8. Domínguez E, Mercado JA, Quesada MA, Heredia A (1999) Pollen sporopollenin: degradation and structural elucidation. Sex Plant Reprod 12:171–178

    Google Scholar 

  9. Du WW, Fang L, Yang W, Wu N, Awan FM, Yang Z, Yang BB (2017) Induction of tumor apoptosis through a circular RNA enhancing Foxo3 activity. Cell Death Differ 24:357–370

    CAS  PubMed  Google Scholar 

  10. Duro-Castano A, Talelli M, Rodríguez-Escalona G, Vicent M (2019) Smart polymeric nanocarriers for drug delivery. In: Smart polymers and their applications. Elsevier, pp 439–479

  11. Fan T-F et al (2020) Degradation of the sporopollenin exine capsules (SECs) in human plasma. Appl Mater Today 19:100594. https://doi.org/10.1016/j.apmt.2020.100594

    Article  Google Scholar 

  12. Fan T et al (2018) Extraction of cage-like sporopollenin exine capsules from dandelion pollen grains. Sci Rep 8:1–11

    Google Scholar 

  13. Kumar A, Montemagno C, Choi H-J (2017) Smart microparticles with a pH-responsive macropore for targeted oral drug delivery. Sci Rep 7:1–15

    Google Scholar 

  14. Li W et al (2019) AuNPs as an important inorganic nanoparticle applied in drug carrier systems. Artif Cells Nanomed Biotechnol 47:4222–4233

    CAS  PubMed  Google Scholar 

  15. Madaan K, Kumar S, Poonia N, Lather V, Pandita D (2014) Dendrimers in drug delivery and targeting: drug-dendrimer interactions and toxicity issues. J Pharm Bioallied Sci 6:139

    PubMed  PubMed Central  Google Scholar 

  16. Mir SH, Hasan P, Danish EY, Aslam M (2020) Pd-induced phase separation in poly (methyl methacrylate) telopolymer: synthesis of nanostructured catalytic Pd nanorods. Colloid Polym Sci 1–8

  17. Mir SH, Nagahara LA, Thundat T, Mokarian-Tabari P, Furukawa H, Khosla A (2018) Organic-inorganic hybrid functional materials: an integrated platform for applied technologies. J Electrochem Soc 165:B3137

    CAS  Google Scholar 

  18. Mir SH, Ochiai B (2016) Development of hierarchical polymer@ Pd nanowire-network: synthesis and application as highly active recyclable catalyst and printable conductive ink. ChemistryOpen 5:213–218

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Mir SH, Ochiai B (2016) Fabrication of polymer-Ag honeycomb hybrid film by metal complexation induced phase separation at the air/water interface. Macromol Mater Eng 301:1026–1031

    CAS  Google Scholar 

  20. Mir SH, Ochiai B (2017) One-pot fabrication of hollow polymer@ Ag nanospheres for printable translucent conductive coatings. Adv Mater Interfaces 4:1601198

    Google Scholar 

  21. Mir SH, Ochiai B (2018) Conductive polymer-Ag honeycomb thin film: the factors affecting the complexity of the microstructure. J Electrochem Soc 165:B3030

    CAS  Google Scholar 

  22. Mujtaba M, Murat K, Ceter T (2018) Differentiation of thermal properties of pollens on genus level. Commun Fac Sci Univ Ankara Ser C Biol 27:177–184

    Google Scholar 

  23. Mujtaba M, Murat K, Ceter T (2018) An investigation of pollen grain thermal diversity on species level. Commun Fac Sci Univ Ankara Ser C Biol 27:170–176

    Google Scholar 

  24. Mujtaba M, Sargin I, Akyuz L, Ceter T, Kaya M (2017) Newly isolated sporopollenin microcages from Platanus orientalis pollens as a vehicle for controlled drug delivery. Mater Sci Eng, C 77:263–270. https://doi.org/10.1016/j.msec.2017.02.176

    Article  CAS  Google Scholar 

  25. Mundargi RC, Tan E-L, Seo J, Cho N-J (2016) Encapsulation and controlled release formulations of 5-fluorouracil from natural Lycopodium clavatum spores. J Ind Eng Chem 36:102–108

    CAS  Google Scholar 

  26. O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT (2005) c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839–843

    PubMed  Google Scholar 

  27. Paunov VN, Mackenzie G, Stoyanov SD (2007) Sporopollenin micro-reactors for in situ preparation, encapsulation and targeted delivery of active components. J Mater Chem 17:609–612

    CAS  Google Scholar 

  28. Pomelli CS, D’Andrea F, Mezzetta A, Guazzelli L (2020) Exploiting pollen and sporopollenin for the sustainable production of microstructures. N J Chem

  29. Sargin I et al (2017) Controlled release and anti-proliferative effect of imatinib mesylate loaded sporopollenin microcapsules extracted from pollens of Betula pendula. Int J Biol Macromol 105:749–756

    CAS  PubMed  Google Scholar 

  30. Sargın İ, Arslan G (2015) Chitosan/sporopollenin microcapsules: preparation, characterisation and application in heavy metal removal. Int J Biol Macromol 75:230–238

    PubMed  Google Scholar 

  31. Shen Y et al (2010) Prodrugs forming high drug loading multifunctional nanocapsules for intracellular cancer drug delivery. J Am Chem Soc 132:4259–4265

    CAS  PubMed  Google Scholar 

  32. Simpson MG (2019) Plant systematics. Academic Press, London

    Google Scholar 

  33. Sin A, Pınar N, Mısırlıgil Z, Çeter T, Yıldız A, Alan Ş (2007) Polen Allerjisi (Türkiye Allerjik Bitkilerine Genel Bir Bakış) Ankara: Engin Yayınevi

  34. Soppimath KS, Aminabhavi TM, Kulkarni AR, Rudzinski WE (2001) Biodegradable polymeric nanoparticles as drug delivery devices. J Controlled Release 70:1–20

    CAS  Google Scholar 

  35. Stella B, Andreana I, Zonari D, Arpicco S (2019) Pentamidine-loaded Lipid and Polymer Nanocarriers as Tunable Anticancer Drug Delivery Systems. J Pharm Sci

  36. Taylor RC, Cullen SP, Martin SJ (2008) Apoptosis: controlled demolition at the cellular level Nature reviews. Mol Cell Biol 9:231–241

    CAS  Google Scholar 

  37. Tirkistani FA (1998) Thermal analysis of some chitosan Schiff bases. Polym Degrad Stabil 60:67–70

    CAS  Google Scholar 

  38. Tong R, Cheng J (2008) Paclitaxel-initiated, controlled polymerization of lactide for the formulation of polymeric nanoparticulate delivery vehicles. Angew Chem Int Ed 47:4830–4834

    CAS  Google Scholar 

  39. Tummala S, Gowthamarajan K, Satish Kumar M, Wadhwani A (2016) Oxaliplatin immuno hybrid nanoparticles for active targeting: an approach for enhanced apoptotic activity and drug delivery to colorectal tumors. Drug Deliv 23:1773–1787

    CAS  PubMed  Google Scholar 

  40. Uthappa U, Kurkuri MD, Kigga M (2019) Nanotechnology advances for the development of various drug carriers. In: Nanobiotechnology in bioformulations. Springer, Berlin, pp 187–224

  41. Vader P, Mol EA, Pasterkamp G, Schiffelers RM (2016) Extracellular vesicles for drug delivery. Adv Drug Deliv Rev 106:148–156

    CAS  PubMed  Google Scholar 

  42. Vivek R, Thangam R, Nipunbabu V, Ponraj T, Kannan S (2014) Oxaliplatin-chitosan nanoparticles induced intrinsic apoptotic signaling pathway: a “smart” drug delivery system to breast cancer cell therapy. Int J Biol Macromol 65:289–297

    CAS  PubMed  Google Scholar 

  43. Wang Y et al (2018) Pollen-inspired microparticles with strong adhesion for drug delivery. Appl Mater Today 13:303–309

    Google Scholar 

  44. Watson JS et al (2007) Rapid determination of spore chemistry using thermochemolysis gas chromatography-mass spectrometry and micro-Fourier transform infrared spectroscopy. Photochem Photobiol Sci 6:689–694

    CAS  PubMed  Google Scholar 

  45. Wu L, Man C, Wang H, Lu X, Ma Q, Cai Y, Ma W (2013) PEGylated multi-walled carbon nanotubes for encapsulation and sustained release of oxaliplatin. Pharm Res 30:412–423

    CAS  PubMed  Google Scholar 

  46. Yang H, Yan R, Chen H, Lee DH, Zheng C (2007) Characteristics of hemicellulose, cellulose and lignin pyrolysis. Fuel 86:1781–1788

    CAS  Google Scholar 

  47. Yang Y et al (2019) Recent advance in polymer based microspheric systems for controlled protein and peptide delivery. Curr Med Chem 26:2285–2296

    CAS  PubMed  Google Scholar 

  48. Yoo HS, Lee KH, Oh JE, Park TG (2000) In vitro and in vivo anti-tumor activities of nanoparticles based on doxorubicin–PLGA conjugates. J Controlled Release 68:419–431

    CAS  Google Scholar 

  49. Zhang D et al (2016) Preparation, characterisation and antitumour activity of β-, γ-and HP-β-cyclodextrin inclusion complexes of oxaliplatin. Spectrochim Acta Part A Mol Biomol Spectrosc 152:501–508

    CAS  Google Scholar 

  50. Zuluaga-Domínguez C, Serrato-Bermudez J, Quicazán M (2018) Influence of drying-related operations on microbiological, structural and physicochemical aspects for processing of bee-pollen. Eng Agric Environ Food 11:57–64

    Google Scholar 

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Acknowledgements

MM would like to thanks the scientific and technological council of Turkey (TÜBİTAK) for supporting his thesis under program number TÜBİTAK-2215. The authors would like to acknowledge the technical and human support provided by Biotechnology Institute, Ankara University, and Scientific and Technological Application and Research Center, Aksaray University, Turkey.

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Mujtaba, M., Yilmaz, B.A., Cansaran-Duman, D. et al. Newly isolated sporopollenin microcages from Cedrus libani and Pinus nigra as carrier for Oxaliplatin; xCELLigence RTCA-based release assay. Polym. Bull. 79, 519–540 (2022). https://doi.org/10.1007/s00289-020-03531-7

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