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ROS enhancement by silicon nanoparticles in X-ray irradiated aqueous suspensions and in glioma C6 cells

  • Pedro M. David Gara
  • Natalia I. Garabano
  • Manuel J. Llansola Portoles
  • M. Sergio Moreno
  • Diego Dodat
  • Oscar R. Casas
  • Mónica C. Gonzalez
  • Mónica L. Kotler
Research Paper

Abstract

The capability of silicon nanoparticles to increase the yield of reactive species upon 4 MeV X-ray irradiation of aqueous suspensions and C6 glioma cell cultures was investigated. ROS generation was detected and quantified using several specific probes. The particles were characterized by FTIR, XPS, TEM, DLS, luminescence, and adsorption spectroscopy before and after irradiation to evaluate the effect of high energy radiation on their structure. The total concentration of O2 •−/HO2 , HO, and H2O2 generated upon 4-MeV X-ray irradiation of 6.4 μM silicon nanoparticle aqueous suspensions were on the order of 10 μM per Gy, ten times higher than that obtained in similar experiments but in the absence of particles. Cytotoxic 1O2 was generated only in irradiation experiments containing the particles. The particle surface became oxidized to SiO2 and the luminescence yield reduced with the irradiation dose. Changes in the surface morphology did not affect, within the experimental error, the yields of ROS generated per Gy. X-ray irradiation of glioma C6 cell cultures with incorporated silicon nanoparticles showed a marked production of ROS proportional to the radiation dose received. In the absence of nanoparticles, the cells showed no irradiation-enhanced ROS generation. The obtained results indicate that silicon nanoparticles of <5 nm size have the potential to be used as radiosensitizers for improving the outcomes of cancer radiotherapy. Their capability of producing 1O2 upon X-ray irradiation opens novel approaches in the design of therapy strategies.

Keywords

Silicon nanoparticles Radiotherapy Glioma C6 cells ROS X-rays Singlet molecular oxygen 

Notes

Acknowledgments

This research was supported by the grant PIP 112-200801-00356 from CONICET, Argentina. The authors thank Lic. M. Martinez from the Physical Department at CIO La Plata for his help with the irradiation of the samples, Dr. Aldo Rubbert from INIFTA for the XPS spectrum, B. Soria from CEQUINOR, UNLP for the FTIR spectra, and A. Wolosiuk from CNEA, Bs.As. for the DLS measurements. P.M.D.G. thanks Fundación Avanzar for a postgraduate fellowship. N.I.G. and M.J.L.P. thank CONICET for a studentship. M.C.G. and M.L.K. are research members of CONICET.

Supplementary material

11051_2012_741_MOESM1_ESM.pdf (376 kb)
Supplementary material 1 (PDF 375 kb)

References

  1. Babich H, Borenfreund E (1990) Applications of the neutral red cytotoxicity assay to in vitro toxicology. ATLA 18:129–144Google Scholar
  2. Bertolini G, Coche A (1968) Semiconductor detectors. North Holland Publishing Co., New YorkGoogle Scholar
  3. Bosio GN, David Gara PM, Garcia Einschlag FS, Gonzalez MC, del Panno MT et al (2008) Photodegradation of soil organic matter and its effect on gram-negative bacterial growth. Photochem Photobiol 84:1126–1132CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  5. Carter JD, Cheng NN, Qu Y, Suarez GD, Guo T (2007) Nanoscale energy deposition by X-ray absorbing nanostructures. J Phys Chem B 111:11622–11625CrossRefGoogle Scholar
  6. Chen M, Mikecz A (2005) Formation of nucleoplasmic protein aggregates impairs nuclear function in response to SiO2 nanoparticles. Exp Cell Res 305:51–62CrossRefGoogle Scholar
  7. Cooney RR, Sewall SL, Dias EA, Sagar DM, Anderson KEH et al (2007) Unified picture of electron and hole relaxation pathways in semiconductor quantum dots. Phys Rev B 75:245311CrossRefGoogle Scholar
  8. Dennis EJ, Dolmaris GC, Fucamara D, Jain RK (2003) TIMELINE: photodynamic therapy for cancer. Nat Rev Cancer 3:380–387CrossRefGoogle Scholar
  9. Erogbogbo F, Tien CA, Chang CW, Yong KT, Law WC et al (2011) Bioconjugation of luminescent silicon quantum dots for selective uptake by cancer cells. Bioconjugate Chem 22:1081–1088CrossRefGoogle Scholar
  10. Hackley VA, Clogston JD (2007) Measuring the size of nanoparticles in aqueous media using batch-mode dynamic light scattering. NIST-NCL joint assay protocol PCC-1, Version 1.0. http://ncl.cancer.gov/NCL_Method_NIST-NCL_PCC-1.pdf. Accessed 13 July 2011
  11. Hall EJ, Giaccia AJ (2006) Radiobiology for the radiologist. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  12. Hubbell JH (1999) Review of photon interaction cross section data in the medical and biological context. Phys Med Biol 44:R1–R22CrossRefGoogle Scholar
  13. Hubbell JH, Seltzer SM (2010) Tables of X-ray mass attenuation coefficients and mass energy-absorption coefficients from 1 keV to 20 MeV for elements Z = 1 to 92 and 48 additional substances of dosimetric interest. Ionizing Radiation Division, Physics Laboratory, NIST. http://www.nist.gov/pml/data/xraycoef/index.cfm. Accessed 13 July 2011
  14. Isakovic A, Markovic Z, Nikolic N, Todorovic-Markovic B, Vranjes-Djuric S et al (2006) Inactivation of nanocrystalline C60 cytotoxicity by [gamma]-irradiation. Biomaterials 27:5049–5058CrossRefGoogle Scholar
  15. Juzenas P, Chen W, Sun Y-P, Coelho MAN, Generalov R et al (2008) Quantum dots and nanoparticles for photodynamic and radiation therapies of cancer. Adv Drug Deliv Rev 60:1600–1614CrossRefGoogle Scholar
  16. Kang Z, Liu Y, Lee S-T (2011) Small-sized silicon nanoparticles: new nanolights and nanocatalysts. Nanoscale 3:777–791CrossRefGoogle Scholar
  17. Knoll GF (1989) Radiation detection and measurement. Wiley, New YorkGoogle Scholar
  18. Kohn T, Nelson KL (2006) Sunlight-mediated inactivation of MS2 coliphage via exogenous singlet oxygen produced by sensitizers in natural waters. Environ Sci Technol 41:192–197CrossRefGoogle Scholar
  19. Kovalev D, Fujii M (2005) Silicon nanocrystals: photosensitizers for oxygen molecules. Adv Mater 17:2531–2544CrossRefGoogle Scholar
  20. Kravets VG, Meier C, Konjhodzic D, Lorke A, Wiggers H (2005) Infrared properties of silicon nanoparticles. J Appl Phys 97:1–5CrossRefGoogle Scholar
  21. Lide DR (2009) Handbook of chemistry and physics. CRC Press. Inc., Boca RatonGoogle Scholar
  22. Llansola Portolés MJ, Rodriguez Nieto F, Soria DB, Amalvy JI, Peruzzo PJ et al (2009) Photophysical properties of blue-emitting silicon nanoparticles. J Phys Chem C 113:13694–13702CrossRefGoogle Scholar
  23. Llansola Portolés MJ, David Gara PM, Kotler ML, Bertolotti S, San Roman E et al (2010) Silicon nanoparticle photophysics and singlet oxygen generation. Langmuir 26:10953–10960CrossRefGoogle Scholar
  24. Mitrasinovic PM, Mihajlovic ML (2008) Recent advances in radiation therapy of cancer cells: a step towards an experimental and systems biology framework. Curr Radiopharm 1:22–29CrossRefGoogle Scholar
  25. Orrenius S (2007) Reactive oxygen species in mitochondria-mediated cell death. Drug Metab Rev 39:443–455CrossRefGoogle Scholar
  26. Ouyang M, Yuan C, Muisener RJ, Boulares A, Koberstein JT (2000) Conversion of some siloxane polymers to silicon oxide by UV/ozone photochemical processes. Chem Mater 12:1591–1596CrossRefGoogle Scholar
  27. Ozcan I, Bouchemal K, Segura-Sanchez F, Abac O, Ozer O, Guneri T, Ponchel G (2009) Effects of sterilization techniques on the PEGylated poly (fÁ-benzyl-L-glutamate) (PBLG) nanoparticles. Acta Pharmaceut Sci 51:211–218Google Scholar
  28. Park Y-S, Liz M, Kasuya LM, Kobayashi Y et al (2006) X-ray absorption of gold nanoparticles with thin silica shell. J Nanosci Nanotechnol 6:3503–3506CrossRefGoogle Scholar
  29. Park J-H, Gu L, von Maltzahn G, Ruoslahti E, Bhatia SN et al (2009) Biodegradable luminescent porous silicon nanoparticles for in vivo applications. Nat Mater 8:331–336CrossRefGoogle Scholar
  30. Propst EK, Kohl PA (1994) The electrochemical oxidation of silicon and formation of porous silicon in acetonitrile. J Electrochem Soc 141:1006–1013CrossRefGoogle Scholar
  31. Repetto G, del Peso A, Zurita JL (2008) Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat Protoc 3:1125–1131CrossRefGoogle Scholar
  32. Ross AB, Mallard WG, Helman WP (1998) NDRL-NIST solution kinetics database: Ver. 4.0. http://kinetics.nist.gov/solution/. Accessed 13 July 2011
  33. Ryckman JD, Reed RA, Weller RA, Fleetwood DM, Weiss SM (2010) Enhanced room temperature oxidation in silicon and porous silicon under 10 keV X-ray irradiation. J Appl Phys 108:113528–113534CrossRefGoogle Scholar
  34. Schärtl W (2007) Light scattering from polymer solutions and nanoparticle dispersions. Springer, BerlinGoogle Scholar
  35. Seino S, Yamamoto TA, Hashimoto K, Okuda S, Chitose N et al (2003) Gamma-ray irradiation effect on aqueous phenol solutions dispersing TiO2 or Al2O3 nanoparticles. Rev Adv Mater Sci 4:70–74Google Scholar
  36. Soffietti R, Leoncini B, Rudà R (2007) New developments in the treatment of malignant gliomas. Expert Rev Neurother 7:1313–1326CrossRefGoogle Scholar
  37. St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277:44784–44790CrossRefGoogle Scholar
  38. Takahashi J, Misawa M (2007) Analysis of potential radiosensitizing materials for X-ray-induced photodynamic therapy. NanoBiotechnology 3:116–126CrossRefGoogle Scholar
  39. Wang PW, Bater S, Zhang LP, Ascherl M, Craig JH (1995) XPS investigation of electron beam effects on a trimethylsilane dosed Si(100) surface. Appl Surf Sci 90:413–417CrossRefGoogle Scholar
  40. Wang L, Yang W, Read P, Larner J, Sheng K (2010) Tumor cell apoptosis induced by nanoparticle conjugate in combination with radiation therapy. Nanotechnology 21:475103–475110CrossRefGoogle Scholar
  41. Yang CS, Oh KS, Ryu JY, Kim DC, Shou-Yong J et al (2001) A study on the formation and characteristics of the Si–O–C–H composite thin films with low dielectric constant for advanced semiconductor devices. Thin Solid Films 390:113–118CrossRefGoogle Scholar
  42. Yang W, Read PW, Mi JM, Baisden JM, Reardon KA et al (2008) Semiconductor nanoparticles as energy mediators for photosensitizer-enhanced radiotherapy. Int J Radiat Oncol 72:633–635CrossRefGoogle Scholar
  43. Yoffe AD (2001) Semiconductor quantum dots and related systems: electronic, optical, luminescence and related properties of low dimensional systems. Adv Phys 50:1–208CrossRefGoogle Scholar
  44. Zhang XD, Guo ML, Wu HY, Sun YM, Ding YQ et al (2009) Irradiation stability and cytotoxicity of gold nanoparticles for radiotherapy. Int J Nanomed 4:165–173CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Pedro M. David Gara
    • 1
    • 3
  • Natalia I. Garabano
    • 2
  • Manuel J. Llansola Portoles
    • 3
  • M. Sergio Moreno
    • 4
  • Diego Dodat
    • 1
  • Oscar R. Casas
    • 1
  • Mónica C. Gonzalez
    • 3
  • Mónica L. Kotler
    • 2
  1. 1.CITOMA, Fundación Avanzar, Instituto de Terapia Radiante S.A., CIO La PlataLa PlataArgentina
  2. 2.Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, UBAUniversity of Buenos AiresBuenos AiresArgentina
  3. 3.INIFTA, Departamento de Química, Facultad de Ciencias ExactasUNLPLa PlataArgentina
  4. 4.Centro Atómico BarilocheSan Carlos de BarilocheArgentina

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