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Controlled killing of human cervical cancer cells by combined action of blue light and C-doped TiO2 nanoparticles

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Abstract

In this study, C-doped TiO2 nanoparticles (C-TiO2) were prepared and tested as a photosensitizer for visible-light-driven photodynamic therapy against cervical cancer cells (HeLa). X-ray diffraction and Transmission Electron Microscopy confirmed the anatase form of nanoparticles, spherical shape, and size distribution from 5 to 15 nm. Ultraviolet–visible light spectroscopy showed that C doping of TiO2 enhances the optical absorption in the visible light range caused by a bandgap narrowing. The photo-cytotoxic activity of C-TiO2 was investigated in vitro against HeLa cells. The lack of dark cytotoxicity indicates good biocompatibility of C-TiO2. In contrast, a combination with blue light significantly reduced the survival of HeLa cells: illumination only decreased cell viability by 30% (15 min of illumination, 120 µW power), and 60% when HeLa cells were preincubated with C-TiO2. We have also confirmed blue light-induced C-TiO2-catalyzed generation of reactive oxygen species in vitro and intracellularly. Oxidative stress triggered by C-TiO2/blue light was the leading cause of HeLa cell death. Fluorescent labeling of treated HeLa cells showed distinct morphological changes after the C-TiO2/blue light treatment. Unlike blue light illumination, which caused the appearance of large necrotic cells with deformed nuclei, cytoplasm swelling, and membrane blebbing, a combination of C-TiO2/blue light leads to controlled cell death, thus providing a better outcome of local anticancer therapy.

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Availability of data and material

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Not applicable.

Abbreviations

∙OH:

: Hydroxyl radicals

ANOVA:

: Analysis of variance

AO:

Acridine orange

ATCC:

American Type Culture Collection

AVOs:

Acidic vesicular organelles

CB:

Conduction band

C-TiO2 :

Carbon-doped titanium dioxide

DCF:

Dichlorofluorescein

DCFH-DA:

2,7-Dichlorofluorescein diacetate

DEPMPO:

5–(Diethoxyphosphoryl)–5–methyl–1–pyrroline–N–oxide

DIC:

Differential interference contrast

DMEM:

Dulbecco’s Modified Eagle’s Medium

EDTA:

Ethylenediaminetetraacetic acid

EPR:

Electron paramagnetic spectroscopy

FBS:

Fetal bovine serum

H2DCFDA:

2′,7′-Dichlorodihydrofluorescein diacetate

HeLa:

Henrietta Lacks (in the text referred to the human epithelial cervical cancer cells)

HRTM:

High-resolution transmission electron microscopy

LSCM:

Laser scanning confocal microscopy

MTT:

3–(4,5–Dimethylthiazol–2–yl)–2,5–diphenyl–2H–tetrazolium bromide

NPs:

Nanoparticles

PBS:

Phosphate-buffered saline

PDT:

Photodynamic therapy

PI:

Propidium iodide

PS:

Photosensitizer

RCF:

Relative centrifugal force

ROS:

Reactive oxygen species

SRB:

Sulforhodamine B

TBHB:

Tert-butyl hydroperoxide

TEM:

Transmission electron microscopy

TiO2 :

Titanium dioxide

UV:

Ultraviolet

UV–Vis:

Ultraviolet–visible light

VB:

Valence band

XRPD:

X-ray powder diffraction

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Acknowledgements

This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant number 451-03-68/2020-14/200017, 451-03-68/2020-14/200146).

Funding

This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia, Serbian-Chinese bilateral project (grant number 451–00-478/2018–09/16), and by the Ministry of science and technology of the People's Republic of China (China-Serbia bilateral project SINO-SERBIA2018002).

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Authors and Affiliations

  1. Vinča Institute of Nuclear Sciences-National Institute of the Republic of Serbia, University of Belgrade, 11001, Belgrade, Serbia

    Milica Matijević, Jelena Žakula, Lela Korićanac, Marija Radoičić, Jelena Filipović Tričković, Ana Valenta Šobot, Marijana Petković, Milutin Stepić & Maja D. Nešić

  2. Department of Optical Science and Engineering, Fudan University, 200433, Shanghai, People’s Republic of China

    Xinyue Liang & Lan Mi

  3. Department of Chemistry, Faculty of Sciences and Mathematics, University of Niš, 18000, Niš, Serbia

    Maja N. Stanković

  4. Faculty of Physical Chemistry, University of Belgrade, 11000, Belgrade, Serbia

    Đura Nakarada & Miloš Mojović

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  1. Milica Matijević
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  2. Jelena Žakula
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Contributions

Milica Matijević: investigation, validation, methodology, formal analysis, writing—original Draft, visualization. Jelena Žakula, Lela Korićanac, Marija Radoičić, Xinyue Liang, Đura Nakarada, Jelena Filipović Tričković, and Ana Valenta Šobot: investigation, formal analysis, writing—original Draft. Maja Stanković: writing: review & editing, supervision. Miloš Mojović, Lan Mi, Marijana Petković and Milutin Stepić: resources, writing—review & editing, funding acquisition. Maja D. Nešić: conceptualization, writing—review & editing, methodology, project administration, supervision.

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Correspondence to Milica Matijević.

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Matijević, M., Žakula, J., Korićanac, L. et al. Controlled killing of human cervical cancer cells by combined action of blue light and C-doped TiO2 nanoparticles. Photochem Photobiol Sci 20, 1087–1098 (2021). https://doi.org/10.1007/s43630-021-00082-2

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