Skip to main content
Log in

Light-triggered modulation of cell antioxidant defense by polymer semiconducting nanoparticles in a model organism

  • Research Letter
  • Published:
MRS Communications Aims and scope Submit manuscript

Abstract

Photovoltaic organic semiconductors are emerging in many therapeutic applications, including drug delivery and optical control of cell function. However, for their safe use the possible concomitant elicitation of undesired responses in target cells need to be carefully evaluated. Here we describe molecular responses activated by semiconducting polymer nanoparticles based on poly(3-hexyl)thiophene (P3HT) in the model Hydra vulgaris, previously shown to respond to P3HT-NP photostimulation and showed a decrease in the total antioxidant capacity and an increase in the DNA and protein oxidation levels, paving the way to a novel use of photovoltaic devices to control intracellular redox equilibrium.

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.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. N.A. Repina, A. Rosenbloom, A. Mukherjee, D.V. Schaffer, and R.S. Kane: At light speed: advances in optogenetic systems for regulating cell signaling and behavior. Annu. Rev. Chem. Biomol. Eng. 8, 13 (2017).

    Article  Google Scholar 

  2. T. Kushibiki, S. Okawa, T. Hirasawa, and M. Ishihara: Optogenetics: novel tools for controlling mammalian cell functions with light. Int. J. Photoenergy 2014, 10 (2014).

    Article  Google Scholar 

  3. B. Tandon, A. Magaz, R. Balint, J.J. Blaker, and S.H. Cartmell: Electroactive biomaterials: vehicles for controlled delivery of therapeutic agents for drug delivery and tissue regeneration. Adv. Drug Deliv. Rev. (in press). doi: 10.1016/j.addr.2017.12.012.

  4. M.R. Antognazza, N. Martino, D. Ghezzi, P. Feyen, E. Colombo, D. Endeman, F. Benfenati, and G. Lanzani: Shedding light on living cells. Adv. Mater. 27, 7662 (2015).

    Article  CAS  Google Scholar 

  5. M. Zangoli, F. Di Maria, E. Zucchetti, C. Bossio, M.R. Antognazza, G. Lanzani, R. Mazzaro, F. Corticelli, M. Baroncini, and G. Barbarella: Engineering thiophene-based nanoparticles to induce phototransduction in live cells under illumination. Nanoscale 9, 9202 (2017).

    Article  CAS  Google Scholar 

  6. L. Lu, T. Zheng, Q. Wu, A.M. Schneider, D. Zhao, and L. Yu: Recent advances in bulk heterojunction polymer solar cells. Chem. Rev. 115, 12666 (2015).

    Article  CAS  Google Scholar 

  7. D. Ghezzi, M.R. Antognazza, M. Dal Maschio, E. Lanzarini, F. Benfenati, and G. Lanzani: A hybrid bioorganic interface for neuronal photoactivation. Nat. Commun. 2, 166 (2011).

    Article  Google Scholar 

  8. V. Benfenati, N. Martino, M.R. Antognazza, A. Pistone, S. Toffanin, S. Ferroni, G. Lanzani, and M. Muccini: Photostimulation of whole-cell conductance in primary rat neocortical astrocytes mediated by organic semiconducting thin films. Adv. Healthcare Mater. 3, 392 (2014).

    Article  CAS  Google Scholar 

  9. N. Martino, P. Feyen, M. Porro, C. Bossio, E. Zucchetti, D. Ghezzi, F. Benfenati, G. Lanzani, and M.R. Antognazza: Photothermal cellular stimulation in functional bio-polymer interfaces. Sci. Rep. 5, 8911 (2015).

    Article  CAS  Google Scholar 

  10. P. Feyen, E. Colombo, D. Endeman, M. Nova, L. Laudato, N. Martino, M.R. Antognazza, G. Lanzani, F. Benfenati, and D. Ghezzi: Light-evoked hyperpolarization and silencing of neurons by conjugated polymers. Sci. Rep. 6, 22718 (2016).

    Article  CAS  Google Scholar 

  11. F. Lodola, N. Martino, G. Tullii, G. Lanzani, and M.R. Antognazza: Conjugated polymers mediate effective activation of the mammalian ion channel transient receptor potential vanilloid 1. Sci. Rep. 7, 8477 (2017).

    Article  CAS  Google Scholar 

  12. D. Ghezzi, M.R. Antognazza, R. Maccarone, S. Bellani, E. Lanzarini, N. Martino, M. Mete, G. Pertile, S. Bisti, G. Lanzani, and F. Benfenati: A polymer optoelectronic interface restores light sensitivity in blind rat retinas. Nat. Photonics 7, 400 (2013).

    Article  CAS  Google Scholar 

  13. J.F. Maya-Vetencourt, D. Ghezzi, M.R. Antognazza, E. Colombo, M. Mete, P. Feyen, A. Desii, A. Buschiazzo, M. Di Paolo, S. Di Marco, F. Ticconi, L. Emionite, D. Shmal, C. Marini, I. Donelli, G. Freddi, R. Maccarone, S. Bisti, G. Sambuceti, G. Pertile, G. Lanzani, and F. Benfenati: A fully organic retinal prosthesis restores vision in a rat model of degenerative blindness. Nat. Mater. 16, 681 (2017).

    Article  CAS  Google Scholar 

  14. A. Ambrosone, M. Roopin, B. Pelaz, A.M. Abdelmonem, L.M. Ackermann, L. Mattera, M. Allocca, A. Tino, M. Klapper, W.J. Parak, O. Levy, and C. Tortiglione: Dissecting common and divergent molecular pathways elicited by CdSe/ZnS quantum dots in freshwater and marine sentinel invertebrates. Nanotoxicology 11, 289 (2017).

    Article  CAS  Google Scholar 

  15. M. Moros, A. Ambrosone, G. Stepien, F. Fabozzi, V. Marchesano, A. Castaldi, A. Tino, J.M. de la Fuente, and C. Tortiglione: Deciphering intracellular events triggered by mild magnetic hyperthermia in vitro and in vivo. Nanomedicine 10, 2167 (2015).

    Article  CAS  Google Scholar 

  16. Tortiglione: An ancient model organism to test in vivo novel functional nanocrystals in Biomedical Engineering: from theory to application edited by R. Fazel-Rezai (InTech—Open Access Publisher 2011), pp. 225.

  17. C. Tortiglione, M.R. Antognazza, A. Tino, C. Bossio, V. Marchesano, A. Bauduin, M. Zangoli, S.V. Morata, and G. Lanzani: Semiconducting polymers are light nanotransducers in eyeless animals. Sci. Adv. 3, e1601699 (2017).

    Article  Google Scholar 

  18. B. Wang, H. Yuan, C. Zhu, Q. Yang, F. Lv, L. Liu, and S. Wang: Polymer-drug conjugates for intracellar molecule-targeted photoinduced inactivation of protein and growth inhibition of cancer cells. Sci. Rep. 2, 766 (2012).

    Article  Google Scholar 

  19. R.M. Giron, J. Marco-Martinez, S. Bellani, A. Insuasty, H.C. Rojas, G. Tullii, M.R. Antognazza, S. Filippone, and N. Martin: Synthesis of modified fullerenes for oxygen reduction reactions. J. Mater. Chem. A 4, 14284 (2016).

    Article  Google Scholar 

  20. G. Tullii, A. Desii, C. Bossio, S. Bellani, M. Colombo, N. Martino, M.R. Antognazza, and G. Lanzani: Bimodal functioning of a mesoporous, light sensitive polymer/electrolyte interface. Org. Electron. 46, 88 (2017).

    Article  CAS  Google Scholar 

  21. I. Dalle-Donne, D. Giustarini, R. Colombo, R. Rossi, and A. Milzani: Protein carbonylation in human diseases. Trends Mol. Med. 9, 169 (2003).

    Article  CAS  Google Scholar 

  22. K. Kannan and S.K. Jain: Oxidative stress and apoptosis. Pathophysiology 7, 153 (2000).

    Article  CAS  Google Scholar 

  23. J. Pecher and S. Mecking: Nanoparticles of conjugated polymers. Chem. Rev. 110, 6260 (2010).

    Article  CAS  Google Scholar 

  24. P.K. Smith, R.I. Krohn, G.T. Hermanson, A.K. Mallia, F.H. Gartner, M.D. Provenzano, E.K. Fujimoto, N.M. Goeke, B.J. Olson, and D.C. Klenk: Measurement of protein using bicinchoninic acid. Anal Biochem. 150, 76 (1985).

    Article  CAS  Google Scholar 

  25. E. Zucchetti, M. Zangoli, I. Bargigia, C. Bossio, F. Di Maria, G. Barbarella, C. D’Andrea, G. Lanzani, and M.R. Antognazza: Poly(3-hexylthiophene) nanoparticles for biophotonics: study of the mutual interaction with living cells. J. Mater. Chem. B 5, 565 (2017).

    Article  CAS  Google Scholar 

  26. A. Ambrosone, L. Mattera, V. Marchesano, A. Quarta, A.S. Susha, A. Tino, A.L. Rogach, and C. Tortiglione: Mechanisms underlying toxicity induced by CdTe quantum dots determined in an invertebrate model organism. Biomaterials 33, 1991 (2012).

    Article  CAS  Google Scholar 

  27. A.A.V. Marchesano, J. Bartelmess, F. Strisciante, A. Tino, L. Echegoyen, C. Tortiglione, and S. Giordani: Impact of carbon nano-onions on hydra vulgaris as a Model organism for nanoecotoxicology. Nanomaterials 5, 1331 (2015).

    Article  CAS  Google Scholar 

  28. A. Ambrosone and C. Tortiglione: Methodological approaches for nanotoxicology using cnidarian models. Toxicol. Mech. Methods 23, 207 (2013).

    Article  CAS  Google Scholar 

  29. E. Mosconi, P. Salvatori, M.I. Saba, A. Mattoni, S. Bellani, F. Bruni, B. Santiago Gonzalez, M.R. Antognazza, S. Brovelli, G. Lanzani, H. Li, J.-L. Brédas, and F. De Angelis: Surface polarization drives photoinduced charge separation at the P3HT/water interface. ACS Energy Lett. 1, 454 (2016).

    Article  CAS  Google Scholar 

  30. A. Lewinska, M. Wnuk, E. Slota, and G. Bartosz: Total anti-oxidant capacity of cell culture media. Clin. Exp. Pharmacol. Physiol. 34, 781 (2007).

    Article  CAS  Google Scholar 

  31. I.S. Young: Measurement of total antioxidant capacity. J. Clin. Pathol. 54, 339 (2001).

    Article  CAS  Google Scholar 

  32. A. Valavanidis, T. Vlachogianni, and C. Fiotakis: 8-hydroxy-2′-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J. Environ. Sci. Health C Environ. Carcinog. Ecotoxicol. Rev. 27, 120 (2009).

    Article  CAS  Google Scholar 

  33. V. Rajendran, M. Lehnig, and C.M. Niemeyer: Photocatalytic activity of colloidal CdS nanoparticles with different capping ligands. J. Mater. Chem. 19, 6348 (2009).

    Article  CAS  Google Scholar 

  34. N. Waiskopf, Y. Ben-Shahar, M. Galchenko, I. Carmel, G. Moshitzky, H. Soreq, and U. Banin: Photocatalytic reactive oxygen species formation by semiconductor-metal hybrid nanoparticles. Toward light-induced modulation of biological processes. Nano Lett. 16, 4266 (2016).

    Article  CAS  Google Scholar 

  35. J. Ge, M. Lan, B. Zhou, W. Liu, L. Guo, H. Wang, Q. Jia, G. Niu, X. Huang, H. Zhou, X. Meng, P. Wang, C.S. Lee, W. Zhang, and X. Han: A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nat. Commun. 5, 4596 (2014).

    Article  CAS  Google Scholar 

  36. B. Poljsak, D. Suput, and I. Milisav: Achieving the Balance between ROS and antioxidants: when to use the synthetic antioxidants. Oxid. Med. Cell. Longev. 2013, 956792 (2013).

    Article  Google Scholar 

  37. M. Schieber and N.S. Chandel: ROS function in redox signaling and oxidative stress. Curr. Biol. 24, R453 (2014).

    Article  CAS  Google Scholar 

Download references

Acknowledgment

Technical assistance of Giuseppe Marino and Ilaria Panico (ISASI-CNR, Pozzuoli) for animal culturing is gratefully acknowledged. We also thank for technical assistance in animal irradiation using white light LED source Dr. Massimo Rippa (ISASI-CNR, Pozzuoli). MM acknowledges the European Union’s Horizon 2020 research and innovation programme (Marie Skiodowska-Curie grant agreement No. 660228).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudia Tortiglione.

Additional information

These authors contributed equally to this work.

Supplementary material

Supplementary material

The supplementary material for this article can be found at {rs|https://doi.org/10.1557/mrc.2018.104|url|}.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moros, M., Lewinska, A., Onorato, G. et al. Light-triggered modulation of cell antioxidant defense by polymer semiconducting nanoparticles in a model organism. MRS Communications 8, 918–925 (2018). https://doi.org/10.1557/mrc.2018.104

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1557/mrc.2018.104

Navigation