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Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

Insights into Nano-Photo-Thermal Therapy of Cancer: The Kinetics of Cell Death and Effect on Cell Cycle

Author(s): Mousa Tabei, Elham Zeinizade, Jaber Beik, S. Kamran Kamrava, Zahra Nasiri, Habib Ghaznavi* and Ali Shakeri-Zadeh*

Volume 20, Issue 5, 2020

Page: [612 - 621] Pages: 10

DOI: 10.2174/1871520620666200129111332

Price: $65

Abstract

Background: Despite considerable advances in nano-photo-thermal therapy (NPTT), there have been a few studies reporting in-depth kinetics of cell death triggered by such a new modality of cancer treatment.

Objective: In this study, we aimed to (1) investigate the cell death pathways regulating the apoptotic responses to NPTT; and (2) ascertain the effect of NPTT on cell cycle progression.

Methods: Folate conjugated gold nanoparticle (F-AuNP) was firstly synthesized, characterized and then assessed to determine its potentials in targeted NPTT. The experiments were conducted on KB nasopharyngeal cancer cells overexpressing folate receptors (FRs), as the model, and L929 normal fibroblast cells with a low level of FRs, as the control. Cytotoxicity was evaluated by MTT assay and the cell death mode (i.e., necrosis or apoptosis) was determined through AnnexinV/FITC-propidium iodide staining. Next, the gene expression profiles of some key apoptotic factors involved in the mitochondrial signaling pathway were investigated using RT-qPCR. Finally, cell cycle phase distribution was investigated at different time points post NPTT using flow cytometric analysis.

Results: The obtained results showed that KB cell death following targeted NPTT was greater than that observed for L929 cells. The majority of KB cell death following NPTT was related to apoptosis. RT-qPCR analysis indicated that the elevated expression of Bax along with the depressed expression of Bcl-xL, Survivin and XIAP may involve in the regulation of apoptosis in response to NPTT. Flow cytometric analysis manifested that 16-24 hours after NPTT, the major proportion of KB cells was in the most radiosensitive phases of the cell cycle (G2/M).

Conclusion: This study extended the understanding of the signaling pathway involved in the apoptotic response to NPTT. Moreover, the potential effect of NPTT on sensitizing cancer cells to subsequent radiation therapy was highlighted.

Keywords: Nano-photo-thermal therapy, gold nanoparticles, folic acid, apoptosis, radiotherapy, MTT assay.

Graphical Abstract
[1]
Beik, J.; Khateri, M.; Khosravi, Z.; Kamrava, S.K.; Kooranifar, S.; Ghaznavi, H.; Shakeri-Zadeh, A. Gold nanoparticles in combinatorial cancer therapy strategies. Coord. Chem. Rev., 2019, 387, 299-324.
[http://dx.doi.org/10.1016/j.ccr.2019.02.025]
[2]
Beik, J.; Shiran, M.B.; Abed, Z.; Shiri, I.; Ghadimi-Daresajini, A.; Farkhondeh, F.; Ghaznavi, H.; Shakeri-Zadeh, A. Gold nanoparticle-induced sonosensitization enhances the antitumor activity of ultrasound in colon tumor-bearing mice. Med. Phys., 2018, 45, 4306-4314.
[http://dx.doi.org/10.1002/mp.13100] [PMID: 30043986]
[3]
Mirrahimi, M.; Abed, Z.; Beik, J.; Shiri, I.; Shiralizadeh Dezfuli, A.; Mahabadi, V.P.; Kamran Kamrava, S.; Ghaznavi, H.; Shakeri-Zadeh, A. A thermo-responsive alginate nanogel platform co-loaded with gold nanoparticles and cisplatin for combined cancer chemo-photothermal therapy. Pharmacol. Res., 2019, 143, 178-185.
[http://dx.doi.org/10.1016/j.phrs.2019.01.005] [PMID: 30611856]
[4]
Jaque, D.; Martínez Maestro, L.; del Rosal, B.; Haro-Gonzalez, P.; Benayas, A.; Plaza, J.L.; Martín Rodríguez, E.; García Solé, J. Nanoparticles for photothermal therapies. Nanoscale, 2014, 6(16), 9494-9530.
[http://dx.doi.org/10.1039/C4NR00708E] [PMID: 25030381]
[5]
Tripathi, R.M.; Shrivastav, A.; Shrivastav, B.R. Biogenic gold nanoparticles: As a potential candidate for brain tumor directed drug delivery. Artif. Cells Nanomed. Biotechnol., 2015, 43(5), 311-317.
[http://dx.doi.org/10.3109/21691401.2014.885445] [PMID: 24588231]
[6]
Yin, J.; Chen, D.; Wu, S.; Li, C.; Liu, L.; Shao, Y. Tumor-targeted nanoprobes for enhanced multimodal imaging and synergistic photothermal therapy: core-shell and dumbbell Gd-tailored gold nanorods. Nanoscale, 2017, 9(43), 16661-16673.
[http://dx.doi.org/10.1039/C7NR03847J] [PMID: 28809413]
[7]
Chen, W.; Ouyang, J.; Liu, H.; Chen, M.; Zeng, K.; Sheng, J.; Liu, Z.; Han, Y.; Wang, L.; Li, J.; Deng, L.; Liu, Y.N.; Guo, S. Black phosphorus nanosheet-based drug delivery system for synergistic photodynamic/photothermal/chemotherapy of cancer. Adv. Mater., 2017, 29(5) 1603864
[http://dx.doi.org/10.1002/adma.201603864] [PMID: 27882622]
[8]
Daraee, H.; Eatemadi, A.; Abbasi, E.; Fekri Aval, S.; Kouhi, M.; Akbarzadeh, A. Application of gold nanoparticles in biomedical and drug delivery. Artif. Cells Nanomed. Biotechnol., 2016, 44(1), 410-422.
[http://dx.doi.org/10.3109/21691401.2014.955107] [PMID: 25229833]
[9]
Alamzadeh, Z.; Beik, J.; Pirhajati Mahabadi, V.; Abbasian Ardekani, A.; Ghader, A.; Kamrava, S.K.; Shiralizadeh Dezfuli, A.; Ghaznavi, H.; Shakeri-Zadeh, A. Ultrastructural and optical characteristics of cancer cells treated by a nanotechnology based chemo-photothermal therapy method. J. Photochem. Photobiol. B, 2019, 192, 19-25.
[http://dx.doi.org/10.1016/j.jphotobiol.2019.01.005] [PMID: 30665146]
[10]
Eustis, S.; el-Sayed, M.A. Why gold nanoparticles are more precious than pretty gold: noble metal surface plasmon resonance and its enhancement of the radiative and nonradiative properties of nanocrystals of different shapes. Chem. Soc. Rev., 2006, 35(3), 209-217.
[http://dx.doi.org/10.1039/B514191E] [PMID: 16505915]
[11]
Yang, X.; Yang, M.; Pang, B.; Vara, M.; Xia, Y. Gold nanomaterials at work in biomedicine. Chem. Rev., 2015, 115(19), 10410-10488.
[http://dx.doi.org/10.1021/acs.chemrev.5b00193] [PMID: 26293344]
[12]
Anselmo, A.C.; Mitragotri, S. Nanoparticles in the clinic. Bioeng. Transl. Med., 2016, 1(1), 10-29.
[http://dx.doi.org/10.1002/btm2.10003] [PMID: 29313004]
[13]
Pattani, V.P.; Shah, J.; Atalis, A.; Sharma, A.; Tunnell, J.W. Role of apoptosis and necrosis in cell death induced by nanoparticle-mediated photothermal therapy. J. Nanopart. Res., 2015, 17, 20.
[http://dx.doi.org/10.1007/s11051-014-2822-3]
[14]
Melamed, J.R.; Edelstein, R.S.; Day, E.S. Elucidating the fundamental mechanisms of cell death triggered by photothermal therapy. ACS Nano, 2015, 9(1), 6-11.
[http://dx.doi.org/10.1021/acsnano.5b00021] [PMID: 25590560]
[15]
Li, J-L.; Gu, M. Surface plasmonic gold nanorods for enhanced two-photon microscopic imaging and apoptosis induction of cancer cells. Biomaterials, 2010, 31(36), 9492-9498.
[http://dx.doi.org/10.1016/j.biomaterials.2010.08.068] [PMID: 20932571]
[16]
Huang, X.; El-Sayed, I.H.; Qian, W.; El-Sayed, M.A. Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J. Am. Chem. Soc., 2006, 128(6), 2115-2120.
[http://dx.doi.org/10.1021/ja057254a] [PMID: 16464114]
[17]
Tong, L.; Zhao, Y.; Huff, T.B.; Hansen, M.N.; Wei, A.; Cheng, J.X. Gold nanorods mediate tumor cell death by compromising membrane integrity. Adv. Mater., 2007, 19, 3136-3141.
[http://dx.doi.org/10.1002/adma.200701974] [PMID: 19020672]
[18]
Chen, C-L.; Kuo, L-R.; Chang, C-L.; Hwu, Y-K.; Huang, C-K.; Lee, S-Y.; Chen, K.; Lin, S-J.; Huang, J-D.; Chen, Y-Y. In situ real-time investigation of cancer cell photothermolysis mediated by excited gold nanorod surface plasmons. Biomaterials, 2010, 31(14), 4104-4112.
[http://dx.doi.org/10.1016/j.biomaterials.2010.01.140] [PMID: 20181393]
[19]
Hashemian, A. Folate-conjugated gold nanoparticles (synthesis, characterization and design for cancer cells nanotechnology-based targeting). Int. J. Nanosci. Nanotechnol., 2009, 5(1), 25-34.
[20]
Brun, E.; Sanche, L.; Sicard-Roselli, C. Parameters governing gold nanoparticle X-ray radiosensitization of DNA in solution. Colloids Surf. B Biointerfaces, 2009, 72(1), 128-134.
[http://dx.doi.org/10.1016/j.colsurfb.2009.03.025] [PMID: 19414242]
[21]
Hehr, T.; Wust, P.; Bamberg, M.; Budach, W. Current and potential role of thermoradiotherapy for solid tumours. Onkologie, 2003, 26(3), 295-302.
[PMID: 12845217]
[22]
Kampinga, H.H.; Dikomey, E. Hyperthermic radiosensitization: mode of action and clinical relevance. Int. J. Radiat. Biol., 2001, 77(4), 399-408.
[http://dx.doi.org/10.1080/09553000010024687] [PMID: 11304434]
[23]
Kampinga, H.H. Cell biological effects of hyperthermia alone or combined with radiation or drugs: a short introduction to newcomers in the field. Int. J. Hyperthermia, 2006, 22(3), 191-196.
[http://dx.doi.org/10.1080/02656730500532028] [PMID: 16754338]
[24]
Beik, J.; Jafariyan, M.; Montazerabadi, A.; Ghadimi-Daresajini, A.; Tarighi, P.; Mahmoudabadi, A.; Ghaznavi, H.; Shakeri-Zadeh, A. The benefits of folic acid-modified gold nanoparticles in CT-based molecular imaging: radiation dose reduction and image contrast enhancement. Artif. Cells Nanomed. Biotechnol., 2018, 46(8), 1993-2001.
[PMID: 29233015]
[25]
Zeinizade, E.; Tabei, M.; Shakeri-Zadeh, A.; Ghaznavi, H.; Attaran, N.; Komeili, A.; Ghalandari, B.; Maleki, S.; Kamrava, S.K. Selective apoptosis induction in cancer cells using folate-conjugated gold nanoparticles and controlling the laser irradiation conditions., Artif. Cells Nanomed. Biotechnol., 2018, 46(sup1), 1026-1038.
[http://dx.doi.org/10.1080/21691401.2018.1443116] [PMID: 29486617]
[26]
Schmittgen, T.D.; Livak, K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc., 2008, 3(6), 1101-1108.
[http://dx.doi.org/10.1038/nprot.2008.73] [PMID: 18546601]
[27]
Pecorino, L. Molecular biology of cancer: Mechanisms, targets, and therapeutics; Oxford University Press: Oxford, UK, 2012.
[28]
Ali, M.R.; Ibrahim, I.M.; Ali, H.R.; Selim, S.A.; El-Sayed, M.A. Treatment of natural mammary gland tumors in canines and felines using gold nanorods-assisted plasmonic photothermal therapy to induce tumor apoptosis. Int. J. Nanomedicine, 2016, 11, 4849-4863.
[http://dx.doi.org/10.2147/IJN.S109470] [PMID: 27703351]
[29]
Fei, P.; Bernhard, E.J.; El-Deiry, W.S. Tissue-specific induction of p53 targets in vivo. Cancer Res., 2002, 62(24), 7316-7327.
[PMID: 12499275]
[30]
Kolesnick, R.N.; Haimovitz-Friedman, A.; Fuks, Z. The sphingomyelin signal transduction pathway mediates apoptosis for tumor necrosis factor, Fas, and ionizing radiation. Biochem. Cell Biol., 1994, 72(11-12), 471-474.
[http://dx.doi.org/10.1139/o94-063] [PMID: 7544586]
[31]
Pérez-Hernández, M.; Del Pino, P.; Mitchell, S.G.; Moros, M.; Stepien, G.; Pelaz, B.; Parak, W.J.; Gálvez, E.M.; Pardo, J.; de la Fuente, J.M. Dissecting the molecular mechanism of apoptosis during photothermal therapy using gold nanoprisms. ACS Nano, 2015, 9(1), 52-61.
[http://dx.doi.org/10.1021/nn505468v] [PMID: 25493329]
[32]
Zagar, T.M.; Oleson, J.R.; Vujaskovic, Z.; Dewhirst, M.W.; Craciunescu, O.I.; Blackwell, K.L.; Prosnitz, L.R.; Jones, E.L. Hyperthermia combined with radiation therapy for superficial breast cancer and chest wall recurrence: a review of the randomised data. Int. J. Hyperthermia, 2010, 26(7), 612-617.
[http://dx.doi.org/10.3109/02656736.2010.487194] [PMID: 20849256]
[33]
Huilgol, N.G.; Gupta, S.; Sridhar, C.R. Hyperthermia with radiation in the treatment of locally advanced head and neck cancer: a report of randomized trial. J. Cancer Res. Ther., 2010, 6(4), 492-496.
[http://dx.doi.org/10.4103/0973-1482.77101] [PMID: 21358087]
[34]
De Haas-Kock, D.F.; Buijsen, J.; Pijls-Johannesma, M.; Lutgens, L.; Lammering, G.; van Mastrigt, G.A.; De Ruysscher, D.K.; Lambin, P.; van der Zee, J. Concomitant hyperthermia and radiation therapy for treating locally advanced rectal cancer. Cochrane Database Syst. Rev., 2009, 8(3) CD006269
[http://dx.doi.org/10.1002/14651858.CD006269.pub2] [PMID: 19588384]
[35]
van der Zee, J.; González González, D.; van Rhoon, G.C.; van Dijk, J.D.; van Putten, W.L.; Hart, A.A. Dutch Deep Hyperthermia Group. Comparison of radiotherapy alone with radiotherapy plus hyperthermia in locally advanced pelvic tumours: a prospective, randomised, multicentre trial. Lancet, 2000, 355(9210), 1119-1125.
[http://dx.doi.org/10.1016/S0140-6736(00)02059-6] [PMID: 10791373]
[36]
Ma, N.; Jiang, Y-W.; Zhang, X.; Wu, H.; Myers, J.N.; Liu, P.; Jin, H.; Gu, N.; He, N.; Wu, F-G.; Chen, Z. Enhanced radiosensitization of gold nanospikes via hyperthermia in combined cancer radiation and photothermal therapy. ACS Appl. Mater. Interfaces, 2016, 8(42), 28480-28494.
[http://dx.doi.org/10.1021/acsami.6b10132] [PMID: 27689441]
[37]
Zhou, M.; Chen, Y.; Adachi, M.; Wen, X.; Erwin, B.; Mawlawi, O.; Lai, S.Y.; Li, C. Single agent nanoparticle for radiotherapy and radio-photothermal therapy in anaplastic thyroid cancer. Biomaterials, 2015, 57, 41-49.
[http://dx.doi.org/10.1016/j.biomaterials.2015.04.013] [PMID: 25913249]
[38]
Li, P.; Shi, Y.W.; Li, B.X.; Xu, W.C.; Shi, Z.L.; Zhou, C.; Fu, S. Photo-thermal effect enhances the efficiency of radiotherapy using Arg-Gly-Asp peptides-conjugated gold nanorods that target αvβ3 in melanoma cancer cells. J. Nanobiotechnology, 2015, 13, 52.
[http://dx.doi.org/10.1186/s12951-015-0113-5] [PMID: 26315288]
[39]
Xu, B.; Kim, S-T.; Lim, D-S.; Kastan, M.B. Two molecularly distinct G2/M checkpoints are induced by ionizing irradiation. Mol. Cell. Biol., 2002, 22(4), 1049-1059.
[http://dx.doi.org/10.1128/MCB.22.4.1049-1059.2002] [PMID: 11809797]
[40]
Geldof, A.A.; Plaizier, M.A.; Duivenvoorden, I.; Ringelberg, M.; Versteegh, R.T.; Newling, D.W.; Teule, G.J. Cell cycle perturbations and radiosensitization effects in a human prostate cancer cell line. J. Cancer Res. Clin. Oncol., 2003, 129(3), 175-182.
[http://dx.doi.org/10.1007/s00432-002-0412-8] [PMID: 12684891]
[41]
Gupta, N.; Hu, L.J.; Deen, D.F. Cytotoxicity and cell-cycle effects of paclitaxel when used as a single agent and in combination with ionizing radiation. Int. J. Radiat. Oncol. Biol. Phys., 1997, 37(4), 885-895.
[http://dx.doi.org/10.1016/S0360-3016(96)00535-4] [PMID: 9128966]
[42]
Lawrence, T.S.; Blackstock, A.W.; McGinn, C. The mechanism of action of radiosensitization of conventional chemotherapeutic agents. Semin. Radiat. Oncol., 2003, 13(1), 13-21.
[http://dx.doi.org/10.1053/srao.2003.50002]

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