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Current Nanoscience

Editor-in-Chief

ISSN (Print): 1573-4137
ISSN (Online): 1875-6786

Research Article

Nano-sheets of Graphene Oxide Enhance the Combined Effect of Hyperthermia and Radiation Treatment in Pancreatic Cancer Cell Lines

Author(s): Mohammad H. Haqiqian, Dariush Sardari*, Mohammad Houshyari and Reza Moghadasali

Volume 17, Issue 5, 2021

Published on: 01 January, 2021

Page: [779 - 788] Pages: 10

DOI: 10.2174/1573413716666210101161703

Price: $65

Abstract

Background: Pancreatic cancer leaves little hope for survival among patients. This is due to its cancerous cell resistance to radiation and chemicals.

Objective: Synergistic effect between three modalities of pancreatic cancer treatment is investigated. These are radiation therapy, hyperthermia and graphene oxide nanosheets. The aim is to overcome resistance of pancreatic cancer cells against radiation therapy.

Methods: Cancerous cell lines were treated by each one of three modalities separately. Other samples were treated with various combinations of these modalities. Hyperthermia was accomplished by placing cell lines for 15 min in 42°C. In the course of radiation therapy, the cancerous cells were irradiated by 6 MV Linac for two cases of 2 Gy and 3 Gy. The cell line viability was readout by MTT assay 24 hours and 48 hours after treatment.

Results: In single modality treatment it was shown that 24h after the treatment, the group treated by RT 3 Gy had the highest cell killing result. Following up the result in 48h readout, hyperthermia and 3 Gy radiotherapy had similar results. In double modality treatment, for both 24h and 48h viability readout, the group graphene-oxide plus 2 Gy radiotherapy showed cell survival amounting to 69% and 43%, respectively being the lowest cell survival among all double combinations.

Conclusion: In triple modality treatment, the cell viability for 24h showed no significant improvement but in 48h, the hyperthermia plus Graphene-oxide and 3 Gy radiotherapy had very low cell viability. Significant sensitizing effect for GO, when combined with radiation therapy, was observed.

Keywords: Graphene oxide, nano-sheets, radiation therapy, hyperthermia, pancreatic cancer cell lines, combinational therapy.

Graphical Abstract
[1]
Haller, D.G. New perspectives in the management of pancreas cancer. Semin. Oncol., 2003, 30(11), 3-10.
[http://dx.doi.org/10.1016/S0093-7754(03)00296-3]
[2]
Ogawa, K.; Karasawa, K.; Ito, Y.; Ogawa, Y.; Jingu, K.; Onishi, H.; Aoki, S.; Wada, H.; Kokubo, M.; Etoh, H.; Kazumoto, T.; Takayama, M.; Negoro, Y.; Nemoto, K.; Nishimura, Y. JROSG Working Subgroup of Gastrointestinal Cancers. Intraoperative radiotherapy for resected pancreatic cancer: a multi-institutional retrospective analysis of 210 patients. Int. J. Radiat. Oncol. Biol. Phys., 2010, 77(3), 734-742.
[http://dx.doi.org/10.1016/j.ijrobp.2009.09.010] [PMID: 20207498]
[3]
Vincent, A.; Herman, J.; Schulick, R.; Hruban, R.H.; Goggins, M. Pancreatic cancer. Lancet, 2011, 378(9791), 607-620.
[http://dx.doi.org/10.1016/S0140-6736(10)62307-0] [PMID: 21620466]
[4]
Goral, V. Pancreatic cancer: Pathogenesis and diagnosis. Asian Pac. J. Cancer Prev., 2015, 16(14), 5619-5624.
[http://dx.doi.org/10.7314/APJCP.2015.16.14.5619] [PMID: 26320426]
[5]
van der Horst, A.; Versteijne, E.; Besselink, M.G.H.; Daams, J.G.; Bulle, E.B.; Bijlsma, M.F.; Wilmink, J.W.; van Delden, O.M.; van Hooft, J.E.; Franken, N.A.P.; van Laarhoven, H.W.M.; Crezee, J.; van Tienhoven, G. The clinical benefit of hyperthermia in pancreatic cancer: a systematic review. Int. J. Hyperthermia, 2018, 34(7), 969-979.
[http://dx.doi.org/10.1080/02656736.2017.1401126] [PMID: 29168401]
[6]
Le, N.; Sund, M.; Vinci, A. GEMS collaborating group of Pancreas 2000. Prognostic and predictive markers in pancreatic adenocarcinoma. Dig. Liver Dis., 2016, 48(3), 223-230.
[http://dx.doi.org/10.1016/j.dld.2015.11.001] [PMID: 26769569]
[7]
Gall, T.M.; Tsakok, M.; Wasan, H.; Jiao, L.R. Pancreatic cancer: current management and treatment strategies. Postgrad. Med. J., 2015, 91(1080), 601-607.
[http://dx.doi.org/10.1136/postgradmedj-2014-133222] [PMID: 26243882]
[8]
Hazard, L. The role of radiation therapy in pancreas cancer. Gastrointest. Cancer Res., 2009, 3(1), 20-28.
[PMID: 19343134]
[9]
Petrelli, F.; Comito, T.; Ghidini, A.; Torri, V.; Scorsetti, M.; Barni, S. Stereotactic body radiation therapy for locally advanced pancreatic cancer: a systematic review and pooled analysis of 19 trials. Int. J. Radiat. Oncol. Biol. Phys., 2017, 97(2), 313-322.
[http://dx.doi.org/10.1016/j.ijrobp.2016.10.030] [PMID: 28068239]
[10]
Datta, N.R.; Ordóñez, S.G.; Gaipl, U.S.; Paulides, M.M.; Crezee, H.; Gellermann, J.; Marder, D.; Puric, E.; Bodis, S. Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat. Rev., 2015, 41(9), 742-753.
[http://dx.doi.org/10.1016/j.ctrv.2015.05.009] [PMID: 26051911]
[11]
Rao, W.; Deng, Z.S.; Liu, J. A review of hyperthermia combined with radiotherapy/chemotherapy on malignant tumors. Crit. Rev. Biomed. Eng., 2010, 38(1), 101-116.
[http://dx.doi.org/10.1615/CritRevBiomedEng.v38.i1.80] [PMID: 21175406]
[12]
Alexander, A.A. Tripartite treatment by radiation, hyperthermia and anti-OX40 immunotherapy potentiates tumor growth delay and tumor microenvironment immunomodulation in pancreatic Cancer., M.Sc. Thesis., University of Maryland, Baltimore. 2017.
[13]
Mahmood, J.; Shukla, H.D.; Soman, S.; Samanta, S.; Singh, P.; Kamlapurkar, S.; Saeed, A.; Amin, N.P.; Vujaskovic, Z. Immunotherapy, radiotherapy and hyperthermia: A combined therapeutic approach in pancreatic cancer treatment. Cancers (Basel), 2018, 10(12), 469.
[http://dx.doi.org/10.3390/cancers10120469] [PMID: 30486519]
[14]
Kaur, P.; Hurwitz, M.D.; Krishnan, S.; Asea, A. Combined hyperthermia and radiotherapy for the treatment of cancer. Cancers (Basel), 2011, 3(4), 3799-3823.
[http://dx.doi.org/10.3390/cancers3043799] [PMID: 24213112]
[15]
Konings, A.W.T. Interaction of heat and radiation in vitro and in vivo in: Thermoradiotherapy and thermochemotherapy; Fessenden, P; Vernon, C.C., Ed.; Springer, 1995, pp. 89-102.
[http://dx.doi.org/10.1007/978-3-642-57858-8_4]
[16]
De Haas-Kock, D.F.M.; 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, (3)CD006269
[http://dx.doi.org/10.1002/14651858.CD006269.pub2] [PMID: 19588384]
[17]
Shibamoto, Y.; Nishimura, U.; Abe, M. Intraoperative radiotherapy and hyperthermia for unresectable pancreatic cancer. Hepatogastroenterology, 1996, 43(8), 326-332.
[PMID: 8714224]
[18]
Roesch, M.; Mueller-Huebenthal, B. Review: the role of hyperthermia in treating pancreatic tumors. Indian J. Surg. Oncol., 2015, 6(1), 75-81.
[http://dx.doi.org/10.1007/s13193-014-0316-5] [PMID: 25937768]
[19]
Liu, J.; Cui, L.; Losic, D. Graphene and graphene oxide as new nanocarriers for drug delivery applications. Acta Biomater., 2013, 9(12), 9243-9257.
[http://dx.doi.org/10.1016/j.actbio.2013.08.016] [PMID: 23958782]
[20]
Ma, Y.; Sun, L.; Huang, W.; Zhang, L.; Zhao, J.; Fan, Q.; Huang, W. Three-dimensional nitrogen-doped carbon nanotubes/graphene structure used as a metal-free electrocatalyst for the oxygen reduction reaction. J. Phys. Chem. C, 2011, 115, 24592-24597.
[http://dx.doi.org/10.1021/jp207736h]
[21]
Shen, H.; Zhang, L.; Liu, M.; Zhang, Z. Biomedical applications of graphene. Theranostics, 2012, 2(3), 283-294.
[http://dx.doi.org/10.7150/thno.3642] [PMID: 22448195]
[22]
Sun, X.; Liu, Z.; Welsher, K.; Robinson, J.T.; Goodwin, A.; Zaric, S.; Dai, H. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res., 2008, 1(3), 203-212.
[http://dx.doi.org/10.1007/s12274-008-8021-8] [PMID: 20216934]
[23]
Zhu, Y.; Murali, S.; Cai, W.; Li, X.; Suk, J.W.; Potts, J.R.; Ruoff, R.S. Graphene and graphene oxide: synthesis, properties, and applications. Adv. Mater., 2010, 22(35), 3906-3924.
[http://dx.doi.org/10.1002/adma.201001068] [PMID: 20706983]
[24]
Tian, B.; Wang, C.; Zhang, S.; Feng, L.; Liu, Z. Photothermally enhanced photodynamic therapy delivered by nano-graphene oxide. ACS Nano, 2011, 5(9), 7000-7009.
[http://dx.doi.org/10.1021/nn201560b] [PMID: 21815655]
[25]
Yu, Q.; Qiu, Y.; Li, J.; Tang, X.; Wang, X.; Cun, X.; Xu, S.; Liu, Y.; Li, M.; Zhang, Z.; He, Q. Targeting cancer-associated fibroblasts by dual-responsive lipid-albumin nanoparticles to enhance drug perfusion for pancreatic tumor therapy. J. Control. Release, 2020, 321, 564-575.
[http://dx.doi.org/10.1016/j.jconrel.2020.02.040] [PMID: 32112854]
[26]
Liao, Y.; Liu, S.; Fu, S.; Wu, J. HMGB1 in radiotherapy: A two headed signal regulating tumor radiosensitivity and immunity. OncoTargets Ther., 2020, 13, 6859-6871.
[http://dx.doi.org/10.2147/OTT.S253772] [PMID: 32764978]
[27]
Alsaedi, I.I.; Taqi, Z.J.; Hussien, A.M.; Sulaiman, G.M.; Jabir, M.S. Graphene nanoparticles induces apoptosis in MCF-7 cells through mitochondrial damage and NF-KB pathway. Mater. Res. Express, 2019, 6, 95413.
[http://dx.doi.org/10.1088/2053-1591/ab33af]
[28]
Yang, K.; Wan, J.; Zhang, S.; Zhang, Y.; Lee, S.T.; Liu, Z. In vivo pharmacokinetics, long-term biodistribution, and toxicology of PEGylated graphene in mice. ACS Nano, 2011, 5(1), 516-522.
[http://dx.doi.org/10.1021/nn1024303] [PMID: 21162527]
[29]
Gurunathan, S.; Arsalan Iqbal, M.; Qasim, M.; Park, C.H.; Yoo, H.; Hwang, J.H.; Uhm, S.J.; Song, H.; Park, C.; Do, J.T.; Choi, Y.; Kim, J.H.; Hong, K. Evaluation of graphene oxide induced cellular toxicity and transcriptome analysis in human embryonic kidney cells. Nanomaterials (Basel), 2019, 9(7), 969.
[http://dx.doi.org/10.3390/nano9070969] [PMID: 31269699]
[30]
Viseu, T.; Lopes, C.M. Fernandes. E.; Oliveira M.E.; Lúcio, M. A systematic review and critical analysis of the role of graphene-based nanomaterials in cancer theranostics. Pharmaceutics, 2018, 10, 282.
[http://dx.doi.org/10.3390/pharmaceutics10040282] [PMID: 30558378]
[31]
Gautam, S. Graphene Oxide: A Potential Drug Carrier for Cancer Therapy—Review. Res. Rev. J. Pharm. Sci., 2018, 8(3), 20-31.
[32]
Stankovich, S.; Dikin, D.A.; Dommett, G.H.B.; Kohlhaas, K.M.; Zimney, E.J.; Stach, E.A.; Piner, R.D.; Nguyen, S.T.; Ruoff, R.S. Graphene-based composite materials. Nature, 2006, 442(7100), 282-286.
[http://dx.doi.org/10.1038/nature04969] [PMID: 16855586]
[33]
Tadyszak, K.; Wychowaniec, J.K.; Litowczenko, J. Biomedical applications of graphene-based structures. Nanomaterials (Basel), 2018, 8(11), 11.
[http://dx.doi.org/10.3390/nano8110944] [PMID: 30453490]
[34]
Tang, L.; Li, X.; Ji, R.; Teng, K.S.; Tai, G.; Ye, J.; Wei, C.; Lau, S.P. Bottoms-up synthesis of large-scale graphene oxide nanosheets. J. Mater. Chem., 2012, 22, 5676-5683.
[http://dx.doi.org/10.1039/c2jm15944a]
[35]
Jalili-Firoozinezhad, S.; Moghadam, M.H.M.; Ghanian, M.H.; Ashtiani, M.K.; Alimadadi, H.; Baharvand, H.; Martin, I.; Scherbericha, A. Polycaprolactone-templated reduced-graphene oxide liquid crystal nanofibers towards biomedical application. RSC Advances, 2017, 7, 39628-39634.
[http://dx.doi.org/10.1039/C7RA06178A]
[36]
Antonius, R. Interpreting quantitative data with IBM SPSS statistics, 2nd ed; Sage Publications: London, 2013.
[http://dx.doi.org/10.4135/9781526435439]
[37]
Bahuguna, A.; Khan, I.; Bajpai, V.K.; Kang, S.C. MTT assay to evaluate the cytotoxic potential of a drug. Bangladesh J. Pharmacol., 2017, 12, 115-118.
[http://dx.doi.org/10.3329/bjp.v12i2.30892]
[38]
Kumar, P.; Nagarajan, A.; Uchil, P.D. Analysis of cell viability by the lactate dehydrogenase assay. Cold Spring Harb. Protoc., 2018, 2018(6)
[http://dx.doi.org/10.1101/pdb.prot095497] [PMID: 29858337]
[39]
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]
[40]
Hildebrandt, B.; Wust, P.; Ahlers, O.; Dieing, A.; Sreenivasa, G.; Kerner, T.; Felix, R.; Riess, H. The cellular and molecular basis of hyperthermia. Crit. Rev. Oncol. Hematol., 2002, 43(1), 33-56.
[http://dx.doi.org/10.1016/S1040-8428(01)00179-2] [PMID: 12098606]
[41]
Cherukuri, P.; Glazer, E.S.; Curley, S.A. Targeted hyperthermia using metal nanoparticles. Adv. Drug Deliv. Rev., 2010, 62(3), 339-345.
[http://dx.doi.org/10.1016/j.addr.2009.11.006] [PMID: 19909777]
[42]
Mittal, S.; Kumar, V.; Dhiman, N.; Chauhan, L.K.S.; Pasricha, R.; Pandey, A.K. Physico-chemical properties based differential toxicity of graphene oxide/reduced graphene oxide in human lung cells mediated through oxidative stress. Sci. Rep., 2016, 6, 39548.
[http://dx.doi.org/10.1038/srep39548] [PMID: 28000740]
[43]
Chang, Y.; Yang, S.T.; Liu, J.H.; Dong, E.; Wang, Y.; Cao, A.; Liu, Y.; Wang, H. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol. Lett., 2011, 200(3), 201-210.
[http://dx.doi.org/10.1016/j.toxlet.2010.11.016] [PMID: 21130147]
[44]
Wang, S.; Zhang, Q.; Luo, X.F.; Li, J.; He, H.; Yang, F.; Di, Y.; Jin, C Magnetic graphene-based nanotheranostic agent for dual-modality mapping guided photothermal therapy in regional lymph nodal metastasis of pancreatic cancer. Biomaterials., 2014, 35, 9473-83,26.
[http://dx.doi.org/10.1016/j.biomaterials.2014.07.064]
[45]
Yang, D.; Feng, L.; Dougherty, C.A.; Luker, K.E.; Chen, D.; Cauble, M.A.; Banaszak Holl, M.M.; Luker, G.D.; Ross, B.D.; Liu, Z.; Hong, H. In vivo targeting of metastatic breast cancer via tumor vasculature-specific nano-graphene oxide. Biomaterials, 2016, 104, 361-371.
[http://dx.doi.org/10.1016/j.biomaterials.2016.07.029] [PMID: 27490486]
[46]
Ahmed, K.; Zaidi, S.F. Mati-Ur-Rehman; Rehman, R.; Kondo, T. Hyperthermia and protein homeostasis: Cytoprotection and cell death. J. Therm. Biol., 2020, 91102615
[http://dx.doi.org/10.1016/j.jtherbio.2020.102615] [PMID: 32716865]
[47]
Maluta, S.; Schaffer, M.; Pioli, F.; Dall’oglio, S.; Pasetto, S.; Schaffer, P.M.; Weber, B.; Giri, M.G. Regional hyperthermia combined with chemoradiotherapy in primary or recurrent locally advanced pancreatic cancer: an open-label comparative cohort trial. Strahlenther. Onkol., 2011, 187(10), 619-625.
[http://dx.doi.org/10.1007/s00066-011-2226-6] [PMID: 21932025]
[48]
Yue, H.; Wei, W.; Yue, Z.; Wang, B.; Luo, N.; Gao, Y.; Ma, D.; Ma, G.; Su, Z. The role of the lateral dimension of graphene oxide in the regulation of cellular responses. Biomaterials, 2012, 33(16), 4013-4021.
[http://dx.doi.org/10.1016/j.biomaterials.2012.02.021] [PMID: 22381473]
[49]
Liu, Y.; Luo, Y.; Wu, J.; Wang, Y.; Yang, X.; Yang, R.; Wang, B.; Yang, J.; Zhang, N. Graphene oxide can induce in vitro and in vivo mutagenesis. Sci. Rep., 2013, 3, 3469.
[http://dx.doi.org/10.1038/srep03469] [PMID: 24326739]
[50]
Robinson, J.T.; Tabakman, S.M.; Liang, Y.; Wang, H.; Casalongue, H.S.; Vinh, D.; Dai, H. Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. J. Am. Chem. Soc., 2011, 133(17), 6825-6831.
[http://dx.doi.org/10.1021/ja2010175] [PMID: 21476500]
[51]
Podolska, M.J.; Barras, A.; Alexiou, C.; Frey, B.; Gaipl, U.; Boukherroub, R.; Szunerits, S.; Janko, C.; Muñoz, L.E. Graphene oxide nanosheets for localized hyperthermia-physicochemical characterization biocompatibility, and induction of tumor cell death. cells., 2020, 9, 776.
[52]
Ahmad, N.; Kaur, G. A study of population dynamics of normal and immune cells in presence of tumor cells. Int. J. Sci. Eng. Res., 2013, 4(4), 770-775.
[53]
Yin, F.; Hu, K.; Chen, Y.; Yu, M.; Wang, D.; Wang, Q.; Yong, K.T.; Lu, F.; Liang, Y.; Li, Z. SiRNA Delivery with PEGylated graphene oxide nanosheets for combined photothermal and genetherapy for pancreatic cancer. Theranostics, 2017, 7(5), 1133-1148.
[http://dx.doi.org/10.7150/thno.17841] [PMID: 28435453]

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