Journal of Cluster Science

, Volume 29, Issue 6, pp 1291–1303 | Cite as

Silver Nanoparticles Synthesized Using Eysenhardtia polystachya and Assessment of the Inhibition of Glycation in Multiple Stages In Vitro and in the Zebrafish Model

  • Rosa Martha Perez GutierrezEmail author
  • Felipe Fernando Martinez Jeronimo
  • Abraham Heriberto Garcia Campoy
  • Carlos Hoyo Vadillo
Original Paper


The aim was to investigate the inhibitory activities on AGE formation by testing silver nanoparticles fabricated using a methanol extract of Eysenhardtia polystachya (EP–AgNPs) and characterized using various physicochemical techniques. The in vitro glucose-albumin assay was used, and cell viability was carried out in RAW264.7 cells. For In vivo testing, we induced diabetes in adult zebrafish with by providing a high blood glucose concentration. EP–AgNPs showed an absorption peak at 413 nm in the UV–Vis spectrum, indicating surface plasmon resonance of the nanoparticles. TEM indicated that most of the particles were spherical, with a diameter of 10–12 nm, a polydispersity index of 0.197, and a zeta potential of − 32.25 mV, suggesting high stability of the nanoparticles. The biocompatible nature of the EP–AgNPs was demonstrated in RAW264.7 cells. EP–AgNPs markedly reduced the formation of AGEs, Amadorin-product/fructosamine, Nε-(carboxymethyl)-lysine, amyloid cross β-structure, and protein carbonyl content in BSA-glucose system and increased total thiol-group after 4 weeks in hyperglycemic zebrafish, EP–AgNPs provided a protective effect against glycation. Data suggest that the inhibitory activity of EP–AgNPs on formation of AGEs is developed through a multiple-stage mechanism of glycation. EP–AgNPs could therefore be an antiglycation agent for prevention diabetic complications.


Eysenhardtia polystachya Green synthesis Antiglycation activity Diabetes Danio rerio 


Compliance with Ethical Standards

Conflict of interest

All of the authors have declared that no competing interests exist.


  1. 1.
    S. Yamagishi and T. Matsu (2010). Oxid. Med. Cell. Longev. 3, 101.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    J. R. Baker, P. A. Metcalf, R. N. Johnson, D. Newman, and P. Rietz (1985). Clin. Chem. 31, 1550.PubMedGoogle Scholar
  3. 3.
    S. Y. Goh and M. E. Cooper (2008). J. Clin. Endocrinol. Metab. 93, 1143.CrossRefPubMedGoogle Scholar
  4. 4.
    M. Aramsri, S. Weerachat, C. B. Chan, and A. Sirichai (2013). Molecules 18, 6439. Scholar
  5. 5.
    T. Nakagawa, T. Yokozawa, K. Terasawa, S. Shu, and L. R. Juneja (2002). J. Agric. Food Chem. 50, 2418.CrossRefPubMedGoogle Scholar
  6. 6.
    T. Kayalvizhi, S. Ravikumar, and P. Venkatachalam (2016). J. Environ. Eng. 142, C4016002.CrossRefGoogle Scholar
  7. 7.
    S. Marin and G. M. Lemnaru (2015). Curr. Top. Med. Chem. 15, 1596.CrossRefPubMedGoogle Scholar
  8. 8.
    D. F. Emerich and C. G. Thanos (2006). Biomol. Eng. 23, 171.CrossRefPubMedGoogle Scholar
  9. 9.
    S. Gurunathan, J. Raman, S. N. Abd Malek, P. A. John, and S. Vikineswary (2013). Int. J. Nanomed. 8, 4399.Google Scholar
  10. 10.
    J. S. Kim, E. Kuk, K. N. Yu, J. H. Kim, S. J. Park, and H. J. Lee (2007). Nanomed. Nanotechnol. 3, 95.CrossRefGoogle Scholar
  11. 11.
    A. Ledezma, J. Romero, M. Hernández, I. Moggio, E. Arias, and E. Padron (2014). Superficies Vacio. 27, 133.Google Scholar
  12. 12.
    J. Sanchez-Rodriguez, E. Vacas-Cordoba, R. Gomez, F. J. De La Mata, and M. A. Muñoz-Fernández (2015). Antiviral Res. 113, 33.CrossRefPubMedGoogle Scholar
  13. 13.
    L. Al Shaal, R. Shegokar, and R. H. Müller (2011). Int. J. Pharm. 20, 133. Scholar
  14. 14.
    S. Hua, E. Marks, J. Jennifer, and J. Simon (2015). Nanomed. Nanotechnol. Biol. Med.. Scholar
  15. 15.
    T. S. Mohamed Saleem and R. Pradeep Kumar (2010). J. Exp. Pharmacol. 29, 32.Google Scholar
  16. 16.
    M. Teimouri, F. Khosravi-Nejad, F. Attar, A. Akbar Saboury, and M. Falahati (2018). J. Clean. Prod. 184, 740. Scholar
  17. 17.
    G. Benelli and C. M. Lukehart (2017). J. Clust. Sci. 28, 1. Scholar
  18. 18.
    G. Benelli (2016). Enzyme Microb. Technol. 95, 58.CrossRefPubMedGoogle Scholar
  19. 19.
    V. Sujitha, K. Murugan, and M. Paulpandi (2015). Parasitol. Res. 114, 3315. Scholar
  20. 20.
    G. D. Saratale, R. G. Saratale, G. Benelli, G. Kumar, A. Pugazhendhi, D. Kim, and H. Shin (2017). J. Clust. Sci. 28, 1709. Scholar
  21. 21.
    P. Anbazhagan, K. Murugan, A. Jaganathan, V. Sujitha, C. M. Samidoss, S. Jayashanthani, P. Amuthavalli, A. Higuchi, S. Kumar, H. Wei, M. Nicoletti, A. Canale, and G. Benelli (2017). J. Clust. Sci. 28, 91. Scholar
  22. 22.
    G. R. Saratale, H. S. Shin, G. Kumar, G. Benelli, D. S. Kim, and G. D. Saratale (2018). Artif. Cells Nanomed. Biotechnol. 46, 211. Scholar
  23. 23.
    R. M. G. Perez, R. Vargas, G. S. Perez, and S. Zavala (1998). Phytoter. Res. 12, 144.CrossRefGoogle Scholar
  24. 24.
    D. T. Burns, B. G. Dalgarno, P. Ggargan, and J. Grimshaw (1984). Phytochemistry 3, 167.CrossRefGoogle Scholar
  25. 25.
    L. Alvarez, M. Y. Rios, C. Esquivel, M. I. Chavez, G. Delgado, and G. Aguilar (1999). J. Nat. Prod. 61, 767.CrossRefGoogle Scholar
  26. 26.
    R. M. G. Perez and E. G. Baez (2014). Pharmcog. Mag. 10, S404.CrossRefGoogle Scholar
  27. 27.
    R. M. G. Perez, A. H. G. Campoy, A. M. Ramirez (2016). Oxid. Med. Cell. Longev. Article ID 9156510, 13 p. Scholar
  28. 28.
    R. M. G. Perez, A. H. G. Campoy, and J. M. M. Flores (2017). NESSA J. Pharm. Pharmacol. 1, 3.Google Scholar
  29. 29.
    M. C. Fishman (1999). Proc. Natl. Acad. Sci. USA 96, 10554.CrossRefPubMedGoogle Scholar
  30. 30.
    L. Segalat (2007). ACS Chem. Biol. 2, 231.CrossRefPubMedGoogle Scholar
  31. 31.
    C. Parng, W. L. Seng, C. Semino, and P. McGrath (2002). Assay Drug Dev. Technol. 1, 41.CrossRefPubMedGoogle Scholar
  32. 32.
    S. G. Vancott, Y. Beckham, and G. M. Kelly (1997). Biochem. Cell. Biol. 75, 479.CrossRefGoogle Scholar
  33. 33.
    S. Amnon and P. Gut (2015). Cell. Mol. Life Sci. 72, 2249. Scholar
  34. 34.
    D. Suvakanta, N. M. Padala, N. Lilakanta, and C. Prasanta (2010). Acta Poloniae Pharma-Drug Res. 67, 217.Google Scholar
  35. 35.
    C. Berkland, M. J. Kipper, B. Narasimhan, K. K. Kim, and D. W. Pac (2004). J. Controll. Rel. 94, 129.CrossRefGoogle Scholar
  36. 36.
    T. Higuchi (1963). J. Pharm. Sci. 52, 1145.CrossRefPubMedGoogle Scholar
  37. 37.
    R. W. Korsmeyer and N. Peppas in T. J. Roseman, S. Z. Mansdorf, and D. Marcel (eds.), A controlled release delivery systems (Inc., Nueva, York, 1983).Google Scholar
  38. 38.
    P. Ritger and N. Peppas (1987). J. Control Rel. 5, 23.CrossRefGoogle Scholar
  39. 39.
    L. Rong-Rong, H. Hai-Feng, B. Fan, L. Ying, W. Chun-Zhen, H. Xiao-Xing, X. Li-Ping, and H. You-Jia (2016). Chin. J. Nat. Med. 14, 0527.Google Scholar
  40. 40.
    G. L. Pedroso, T. O. Hammes, T. D. Escobar, L. B. Fracasso, L. F. Forgiarini, and T. R. Dailveira (2012). J. Vis. Exp. 26, e3865. Scholar
  41. 41.
    J. Chompoo, A. Upadhayay, W. Kishimoto, T. Makise, and S. Tawata (2011). Food Chem. 129, 709.CrossRefPubMedGoogle Scholar
  42. 42.
    A. Ardestani and R. Yazdanparast (2007). Int. J. Biol. Macromol. 41, 572.CrossRefPubMedGoogle Scholar
  43. 43.
    R. L. Levine, D. Garland, C. N. Oliver, A. Amici, and I. Climent (1990). Methods Enzymol. 186, 464.CrossRefPubMedGoogle Scholar
  44. 44.
    G. L. Ellman (1959). Arch. Biochem. Biophys. 82, 70.CrossRefPubMedGoogle Scholar
  45. 45.
    R. Tupe and V. Agte (2010). Brit. J. Nutr. 103, 370.CrossRefPubMedGoogle Scholar
  46. 46.
    W. Klunk, R. F. Jacob, and R. P. Mason (1999). Methods Enzymol. 309, 285.CrossRefPubMedGoogle Scholar
  47. 47.
    I. Sadowska-BartoszI, S. Galiniak, and G. Bartosz (2014). Molecules 19, 4880.CrossRefGoogle Scholar
  48. 48.
    O. Velgosova and A. Mrazikova (2017). AIP Conf. Proc. 1918, 020004.CrossRefGoogle Scholar
  49. 49.
    C. Dipankar and S. Murugan (2012). Colloid Surf. B Biointerfaces 98, 112.CrossRefPubMedGoogle Scholar
  50. 50.
    V. K. Preethi, L. Chitra, G. Kavitha, R. Vijayan, S. Penislusshiyan, V. Sudha, S. Palanivel, and P. Thayumanavan (2017). Artif. Cells Nanomed. Biotechnol.. Scholar
  51. 51.
    B. Menagen, P. Rami, A. David (2017). Sci. Rep. 7, 4161.
  52. 52.
    S. P. Patil and S. T. Kumbhar (2017). Biochem. Biophys. Rep. 10, 76.Google Scholar
  53. 53.
    T. J. Maybry, K. R. Markham, and M. B. Thomas The Ultraviolet Spectra of Flavones and Flavonols. The Systematic Identification of Flavonoids (Springer, Berlin, 1970), pp. 41–164.Google Scholar
  54. 54.
    S. Rout and R. Banerjee (2007). Bioresour. Technol. 98, 3159.CrossRefPubMedGoogle Scholar
  55. 55.
    B. C. Nelson, ME, Walker ML, Riley (2016). Antioxidants. 5, 15. Scholar
  56. 56.
    K. Logaranjan, A. J. Raiza, S. C. Gopinath, Y. Chen, and K. Pandian (2016). Nanoscale Res. Letts. 11, 520. Scholar
  57. 57.
    K. Jyoti, B. Mamta, S. Ajeet (2016). J. Radiat. Res. Appl. Sci. 9, 217.
  58. 58.
    G. Ferreira, A. R. Hernandez-Martinez, H. P. Gustavo Molina, M. Cruz-Soto, G. Luna, and M. Estevez (2015). Mat. Sci. Eng. C 57, 49.CrossRefGoogle Scholar
  59. 59.
    X. Huang, L. Li, T. Liu, N. Hao, H. Liu, D. Chen, and F. Tang (2011). ACS Nano. 5, 5390.CrossRefPubMedGoogle Scholar
  60. 60.
    S. Ashe, D. Nayak, M. Kumari, and B. Nayak (2016). ACS Appl. Mater. Interfaces 8, 30005.CrossRefPubMedGoogle Scholar
  61. 61.
    M. Ansari, M. Habibi-Rezaei, S. Salahshour-Kordestani, A. A. Movahedi, and N. Poursasan (2015). Protein Pept. Lett. 22, 594.CrossRefPubMedGoogle Scholar
  62. 62.
    S. Yu, W. Zhang, W. Liu, W. Zhu, R. Guo, Y. Wang, D. Zhang, and J. Wang (2015). Nanotechnology 26, 145703. Scholar
  63. 63.
    F. Kazemi, A. Divsalar, and A. A. Saboury (2018). Int. J. Biol. Macromol. 109, 1329. Scholar
  64. 64.
    V. V. Mossine, M. Linetsky, and G. V. Glinsky (1999). Chem. Res. Toxicol. 12, 230–236.CrossRefPubMedGoogle Scholar
  65. 65.
    D. L. Price, P. M. Rhett, S. R. Thorpe, and J. W. Baynes (2001). J. Biol. Chem. 276, 48967.CrossRefPubMedGoogle Scholar
  66. 66.
    B. Bouna, L. M. Kron-Batenburg, and P. Wu (2003). J. Biol. Chem. 278, 171.Google Scholar
  67. 67.
    V. P. Singh, A. Bali, N. Singh, and A. S. Jaggi (2014). Korean J. Physiol. Pharmacol. 18, 1.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Rosa Martha Perez Gutierrez
    • 1
    Email author
  • Felipe Fernando Martinez Jeronimo
    • 2
  • Abraham Heriberto Garcia Campoy
    • 1
  • Carlos Hoyo Vadillo
    • 3
  1. 1.Laboratorio de Investigación de Productos NaturalesEscuela Superior de Ingenieria Quimica e Industrias extractivas IPNMexico, D.F.Mexico
  2. 2.Hidrobiologia ExperimentalEscuela Nacional de Ciencias Biologicas IPNCiudad de MexicoMexico
  3. 3.Dpto. FarmacologíaCinvestavCiudad de MexicoMexico

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