RESEARCH ARTICLE

Silica-based nanoarchitecture for an optimal combination of photothermal and chemodynamic therapy functions of Cu2–xS cores with red emitting carbon dots

  • Alexey Stepanov , 1 ,
  • Svetlana Fedorenko 1 ,
  • Kirill Kholin 2 ,
  • Irek Nizameev 3 ,
  • Alexey Dovzhenko 4 ,
  • Rustem Zairov 1,4 ,
  • Tatiana Gerasimova 1 ,
  • Alexandra Voloshina 1 ,
  • Anna Lyubina 1 ,
  • Guzel Sibgatullina 5 ,
  • Dmitry Samigullin 3,5 ,
  • Asiya Mustafina 1
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  • 1. Arbuzov Institute of Organic and Physical Chemistry, FRC Kazan Scientific Center of RAS, Kazan 420088, Russia
  • 2. Department of Physics, Kazan National Research Technological University, Kazan 420015, Russia
  • 3. Department of Nanotechnology in Electronics, Kazan National Research Technical University named after A.N. Tupolev-KAI, Kazan 420111, Russia
  • 4. Kazan (Volga region) Federal University, Kazan 420008, Russia
  • 5. Kazan Institute of Biochemistry and Biophysics, FRC Kazan Scientific Center of RAS, Kazan 420111, Russia
aleksestepanov@yandex.ru

Received date: 15 Jun 2023

Accepted date: 09 Aug 2023

Published date: 15 Dec 2023

Copyright

2023 Higher Education Press

Abstract

This study introduces multifunctional silica nanoparticles that exhibit both high photothermal and chemodynamic therapeutic activities, in addition to luminescence. The activity of the silica nanoparticles is derived from their plasmonic properties, which are a result of infusing the silica nanoparticles with multiple Cu2–xS cores. This infusion process is facilitated by a recoating of the silica nanoparticles with a cationic surfactant. The key factors that enable the internal incorporation of the Cu2–xS cores and the external deposition of red-emitting carbon dots are identified. The Cu2–xS cores within the silica nanoparticles exhibit both self-boosting generation of reactive oxygen species and high photothermal conversion efficacy, which are essential for photothermal and chemodynamic activities. The silica nanoparticles’ small size (no more than 70 nm) and high colloidal stability are prerequisites for their cell internalization. The internalization of the red-emitting silica nanoparticles within cells is visualized using fluorescence microscopy techniques. The chemodynamic activity of the silica nanoparticles is associated with their dark cytotoxicity, and the mechanisms of cell death are evaluated using an apoptotic assay. The photothermal activity of the silica nanoparticles is demonstrated by significant cell death under near-infrared (1064 nm) irradiation.

Cite this article

Alexey Stepanov , Svetlana Fedorenko , Kirill Kholin , Irek Nizameev , Alexey Dovzhenko , Rustem Zairov , Tatiana Gerasimova , Alexandra Voloshina , Anna Lyubina , Guzel Sibgatullina , Dmitry Samigullin , Asiya Mustafina . Silica-based nanoarchitecture for an optimal combination of photothermal and chemodynamic therapy functions of Cu2–xS cores with red emitting carbon dots[J]. Frontiers of Chemical Science and Engineering, 2023 , 17(12) : 2144 -2155 . DOI: 10.1007/s11705-023-2362-4

Competing interests

The authors declare that they have no competing interests.

Acknowledgments

The reported study was funded by RFBR and CNR, project number 20-53-7802. Authors gratefully acknowledge to Assigned Spectral-Analytical Center of FRC Kazan Scientific Center of RAS for providing necessary facilities to carry out physical-chemical measurements. The authors thanks to Interdisciplinary Center for Analytical Microscopy at KFU for assistance with the confocal microscopy experiments.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11705-023-2362-4 and is accessible for authorized users.
1
Kim M, Lee J H. Plasmonic photothermal nanoparticles for niomedical applications. Advancement of Science, 2019, 6: 1900471

2
Nikam A N, Pandey A, Fernandes G, Kulkarni S, Mutalik S P, Padya B S, George S D, Mutalik S. Copper sulphide based heterogeneous nanoplatforms for multimodal therapy and imaging of cancer: recent advances and toxicological perspectives. Coordination Chemistry Reviews, 2020, 419: 213356

DOI

3
Sun H, Zhang Y, Chen S, Wang R, Chen Q, Li J, Luo Y, Wang X, Chen H. Photothermal Fenton nanocatalysts for synergetic cancer therapy in the second near-infrared window. ACS Applied Materials & Interfaces, 2020, 12(27): 30145–30154

DOI

4
Goel S, Chen F, Cai W. Synthesis and biomedical applications of copper sulfide nanoparticles: from sensors to theranostics. Small, 2014, 10(4): 631–645

DOI

5
Tian Q, Jiang F, Zou R, Liu Q, Chen Z, Zhu M, Yang S, Wang J, Wang J, Hu J. Hydrophilic Cu9S5 nanocrystals: a photothermal agent with a 25.7% heat conversion efficiency for photothermal ablation of cancer cells in vivo. ACS Nano, 2011, 5(12): 9761–9771

DOI

6
Marin R, Skripka A, Besteiro L V, Benayas A, Wang Z, Govorov A O, Canton P, Vetrone F. Highly efficient copper sulfide-based near-infrared photothermal agents: exploring the limits of macroscopic heat conversion. Small, 2018, 14(49): 1803282

DOI

7
Li Y, Lu W, Huang Q, Li C, Chen W. Copper sulfide nanoparticles for photothermal ablation of tumor cells. Nanomedicine, 2010, 5(8): 1161–1171

DOI

8
Yan C, Tian Q, Yang S. Recent advances in the rational design of copper chalcogenide to enhance the photothermal conversion efficiency for the photothermal ablation of cancer cells. RSC Advances, 2017, 7(60): 37887–37897

DOI

9
Li S L, Chu X, Dong H L, Hou H Y, Liu Y. Recent advances in augmenting Fenton chemistry of nanoplatforms for enhanced chemodynamic therapy. Coordination Chemistry Reviews, 2023, 479: 215004

DOI

10
Behzadi S, Serpooshan V, Tao W, Hamaly M A, Alkawareek M Y, Dreaden E C, Brown D, Alkilany A M, Farokhzad O C, Mahmoudi M. Cellular uptake of nanoparticles: journey inside the cell. Chemical Society Reviews, 2017, 46(14): 4218–4244

DOI

11
Xu M, Yang G, Bi H, Xu J, Dong S, Jia T, Wang Z, Zhao R, Sun Q, Gai S. . An intelligent nanoplatform for imaging-guided photodynamic/photothermal/chemo-therapy based on upconversion nanoparticles and CuS integrated black phosphorus. Chemical Engineering Journal, 2020, 382: 122822

DOI

12
Wang J, Shah Z H, Zhang S, Lu R. Silica-based nanocomposites via reverse microemulsions: classifications, preparations, and applications. Nanoscale, 2014, 6(9): 4418–4437

DOI

13
Wei W, Wei M, Liu S. Silica nanoparticles as a carrier for signal amplification. Reviews in Analytical Chemistry, 2012, 31(3–4): 163–176

DOI

14
Yu M, Zhao Z. Plasmon-enhanced up-conversion luminescence and oxygen vacancy defect-induced yellow light in annealed Cu8S5@SiO2@Er2O3 nanocomposites. Journal of Luminescence, 2020, 225: 117361

DOI

15
Yu M, Tang P, Zhang Q, Zhao Z, Huang S. Plasmon-enhanced up-conversion luminescence in multiple Cu2–xS@SiO2-embedded Er(OH)CO3 composites. Journal of Alloys and Compounds, 2021, 853: 156906

DOI

16
Liu K, Liu K, Liu J, Ren Q, Zhao Z, Wu X, Li D, Yuan F, Ye K, Li B. Copper chalcogenide materials as photothermal agents for cancer treatment. Nanoscale, 2020, 12(5): 2902–2913

DOI

17
Wang L, Ma X, Cai K, Li X. Morphological effect of copper sulfide nanoparticles on their near infrared laser activated photothermal and photodynamic performance. Materials Research Express, 2019, 6(10): 105406

DOI

18
Mutalik C, Okoro G, Krisnawati D I, Jazidie A, Rahmawati E Q, Rahayu D, Hsu W T, Kuo T R. Copper sulfide with morphology-dependent photodynamic and photothermal antibacterial activities. Journal of Colloid and Interface Science, 2022, 607: 1825–1835

DOI

19
Dimitriev O, Slominskii Y, Giancaspro M, Rizzi F, Depalo N, Fanizza E, Yoshida T. Giancaspro, Rizzi F, Depalo N, Fanizza E, Yoshida T. Assembling near-infrared dye on the surface of near-infrared silica-coated copper sulphide plasmonic nanoparticles. Nanomaterials, 2023, 13(3): 510

DOI

20
Fanizza E, Mastrogiacomo R, Pugliese O, Guglielmelli A, Sio L D, Castaldo R, Scavo M P, Giancaspro M, Rizzi F, Gentile G. . NIR-absorbing mesoporous silica-coated copper sulphide nanostructures for light-to-thermal energy conversion. Nanomaterials, 2022, 12(15): 2545

DOI

21
Luo B, Huang X, Ye Y, Cai J, Feng Y, Cai X, Wang X. CuS NP-based nanocomposite with photothermal and augmented-photodynamic activity for magnetic resonance imaging-guided tumor synergistic therapy. Journal of Inorganic Chemistry, 2022, 235: 111940

22
Wang Y, An L, Lin J, Tian Q, Yang S. A hollow Cu9S8 theranostic nanoplatform based on a combination of increased active sites and photothermal performance in enhanced chemodynamic therapy. Chemical Engineering Journal, 2020, 385: 123925

DOI

23
Fedorenko S, Stepanov A, Bochkova O, Kholin K, Dovjenko A, Zairov R, Nizameev I, Gerasimova T, Strelnik I, Voloshina A. . Tailoring of silica nanoarchitecture to optimize Cu2–xS based image-guided chemodynamic therapy agent. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 2021, 626: 126996

DOI

24
Fedorenko S, Farvaeva D, Stepanov A, Bochkova O, Kholin K, Nizameev I, Drobyshev S, Gerasimova T, Voloshina A, Fanizza E. . Tricks for organic-capped Cu2–xS nanoparticles encapsulation into silica nanocomposites co-doped with red emitting luminophore for NIR activated-photothermal/chemodynamic therapy. Journal of Photochemistry and Photobiology A Chemistry, 2022, 433: 114187

DOI

25
Ren G, Yu L, Zhu B, Tang M, Chai F, Wang C, Su Z. Orange emissive carbon dots for colorimetric and fluorescent sensing of 2,4,6-trinitrophenol by fluorescence conversion. RSC Advances, 2018, 8(29): 16095–16102

DOI

26
Davydov N, Mustafina A, Burilov V, Zvereva E, Katsyuba S, Vagapova L, Konovalov A, Antipin I. Complex formation of d-metal ions at the interface of TbIII -doped silica nanoparticles as a basis of substrate-responsive TbIII-centered luminescence. ChemPhysChem, 2012, 13(14): 3357–3364

DOI

27
Donahue N D, Acar H, Wilhelm S. Concepts of nanoparticle cellular uptake, intracellular trafficking, and kinetics in nanomedicine. Advanced Drug Delivery Reviews, 2019, 143: 68–96

DOI

28
Manzanares D, Ceña V. Endocytosis: the nanoparticle and submicron nanocompounds gateway into the cell. Pharmaceutics, 2020, 12(4): 371

DOI

29
Augustine R, Hasan A, Primavera R, Wilson R J, Thakor A S, Kevadiya B D. Cellular uptake and retention of nanoparticles: insights on particle properties and interaction with cellular components. Materials Today. Communications, 2020, 25: 101692

DOI

30
Fedorenko S V, Mustafina A R, Mukhametshina A R, Jilkin M E, Mukhametzyanov T A, Solovieva A O, Pozmogova T N, Shestopalova L V, Shestopalov M A, Kholin K V. . Cellular imaging by green luminescence of Tb(III)-doped aminomodified silica nanoparticles. Materials Science and Engineering A, 2017, 76: 551–558

31
Elistratova J, Mukhametshina A, Kholin K, Nizameev I, Mikhailov M, Sokolov M, Khairullin R, Miftakhova R, Shammas G, Kadirov M. . Interfacial uploading of luminescent hexamolybdenum cluster units onto amino-decorated silica nanoparticles as new design of nanomaterial for cellular imaging and photodynamic therapy. Journal of Colloid and Interface Science, 2019, 538: 387–396

DOI

32
de la Torre C, Gavara R, Garcia-Fernandez A, Mikhaylov M, Sokolov M N, Miravet J F, Sancenon F, Martinez-Manez R, Galindo F. Enhancement of photoactivity and cellular uptake of (Bu4N)2[Mo6I8(CH3COO)6] complex by loading on porous MCM-41 support. Photodynamic studies as an anticancer agent. Biomaterials Advances, 2022, 140: 213057

DOI

33
Zhang Z, Zhu H, Peng N, Song J, Sun R, Wang J, Zhu F, Wang Y. Red emissive carbon dots-based probe for rapid identification and continuous tracking of Gram-positive bacteria in tumor cells. Materials Letters, 2023, 341: 134233

DOI

34
Wang X, Cao Y, Hu X, Cai L, Wang H, Fang G, Wang S. A novel fluorescent biomimetic sensor based on cerium, nitrogen co-doped carbon quantum dots embedded in cobalt-based metal organic framework@molecularly imprinted polymer for selective and sensitive detection of oxytetracycline. Microchemical Journal, 2023, 190: 108606

DOI

35
Luo F, Zhu M, Liu Y, Sun J, Gao F. Ratiometric and visual determination of copper ions with fluorescent nanohybrids of semiconducting polymer nanoparticles and carbon dots. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy, 2023, 295: 122574

DOI

36
Wang Y, Wu R, Zhang Y, Cheng S, Zhang Y. High quantum yield nitrogen doped carbon dots for Ag+ sensing and bioimaging. Journal of Molecular Structure, 2023, 1283: 135212

DOI

37
Sajwan R K, Solanki P R. Gold@carbon quantum dots nanocomposites based two-in-one sensor: a novel approach for sensitive detection of aminoglycosides antibiotics in food samples. Food Chemistry, 2023, 415: 135590

DOI

38
Bochkova O, Dovjenko A, Zairov R, Kholin K, Biktimirova R, Fedorenko S, Nizameev I, Laskin A, Voloshina A, Lyubina A. . Silica-supported assemblage of CuII ions with carbon dots for self-boosting and glutathione-induced ROS generation. Coatings, 2022, 12(1): 97

DOI

39
Yu Y, Song M, Chen C, Du Y, Li C, Han Y, Yan F, Shi Z, Feng S. Bortezomib-encapsulated CuS/carbon dot nanocomposites for enhanced photothermal therapy via stabilization of polyubiquitinated substrates in the proteasomal degradation pathway. ACS Nano, 2020, 14(8): 10688–10703

DOI

40
Roper D K, Ahn W, Hoepfner M. Microscale heat transfer transduced by surface plasmon resonant gold nanoparticles. Journal of Physical Chemistry C, 2007, 111(9): 3636–3641

DOI

41
Ain N, Abdul Nasir J, Khan Z, Butler I S, Rehman Z. Copper sulfide nanostructures: synthesis and biological applications. RSC Advances, 2022, 12(12): 7550–7567

DOI

42
Zhang L, Pan H, Li Y, Li F, Huang X. Constructing Cu7S4@SiO2/DOX multifunctional nanoplatforms for synergistic photothermal-chemotherapy on melanoma tumors. Frontiers in Bioengineering and Biotechnology Sec. Biomaterials, 2020, 8: 579439

43
An N, Wang Y, Li M, Lin H, Qu F. The synthesis of core-shell Cu9S5@mSiO2-ICG@PEG-LA for photothermal and photodynamic therapy. New Journal of Chemistry, 2018, 42(22): 18318–18327

DOI

44
Tang Z, Liu Y, He M, Bu W. Chemodynamic therapy: tumour microenvironment mediated Fenton and Fenton-like reactions. Angewandte Chemie International Edition, 2019, 58(4): 946–956

DOI

45
Gao F, Liu J, Gong P, Yang Y, Jiang Y. Carbon dots as potential antioxidants for the scavenging of multi-reactive oxygen and nitrogen species. Chemical Engineering Journal, 2023, 462: 142338

DOI

46
Zhang K, Meng X, Yang Z, Dong H, Zhang X. Enhanced cancer therapy by hypoxia-responsive copper metal-organic frameworks nanosystem. Biomaterials, 2020, 258: 120278

DOI

47
Komarnicka U K, Pucelik B, Wojtala D, Lesiów M K, Stochel G, Kyzioł A. Evaluation of anticancer activity in vitro of a stable copper(I) complex with phosphine-peptide conjugate. Scientific Reports, 2021, 11(1): 23943

DOI

48
Tsvetkov T, Coy S, Petrova B, Dreishpoon M, Verma A, Abdusamad M, Rossen J, Joesch-Cohen L, Humeidi R, Spangler Ryan D, Eaton J K, Frenkel E, Kocak M, Corsello S M, Lutsenko S, Kanarek N, Santagata S, Golub T R. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science, 2022, 375(6586): 1254–1261

DOI

49
McBride H M, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Current Biology, 2006, 16(14): R551–R560

DOI

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