133
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Rf Hyperthermia by Encapsulated Fe3O4 Nanoparticles Induces Cancer Cell Death Via Time-Dependent Caspase-3 Activation

, ORCID Icon, , & ORCID Icon
Pages 355-379 | Received 09 May 2019, Accepted 03 Dec 2019, Published online: 29 Jan 2020

References

  • Kumar R , ChauhanA, JhaSK, KuanrBK. Localized cancer treatment by radio-frequency hyperthermia using magnetic nanoparticles immobilized on graphene oxide: from novel synthesis to in vitro studies. J. Mater. Chem. B6(33), 5385–5399 (2018).
  • Ahamed M , AlhadlaqHA, KhanMAM, AkhtarMJ. Selective killing of cancer cells by iron oxide nanoparticles mediated through reactive oxygen species via p53 pathway. J. Nanopart. Res.15(1), 1225 (2012).
  • Tao C , ZhuY. Magnetic mesoporous silica nanoparticles for potential delivery of chemotherapeutic drugs and hyperthermia. Dalton Trans.43(41), 15482–15490 (2014).
  • Jelovac D , ArmstrongDK. Recent progress in the diagnosis and treatment of ovarian cancer. CA Cancer J. Clin.61(3), 183–203 (2011).
  • Xie J , YanC, YanYet al. Multi-modal Mn–Zn ferrite nanocrystals for magnetically-induced cancer targeted hyperthermia: a comparison of passive and active targeting effects. Nanoscale8(38), 16902–16915 (2016).
  • Qu Y , LiJ, RenJ, LengJ, LinC, ShiD. Enhanced magnetic fluid hyperthermia by micellar magnetic nanoclusters composed of MnxZn1–xFe2O4 nanoparticles for induced tumor cell apoptosis. ACS Appl. Mater. Interfaces6(19), 16867–16879 (2014).
  • Zhao P , JiangH, SuD, FengJ, MaS, ZhuX. Inhibition of cell proliferation by mild hyperthermia at 43˚C with Paris Saponin I in the lung adenocarcinoma cell line PC-9. Mol. Med. Rep.11(1), 327–332 (2015).
  • Shellman YG , HoweWR, MillerLAet al. Hyperthermia induces endoplasmic reticulum-mediated apoptosis in melanoma and non-melanoma skin cancer cells. J. Invest. Dermatol.128(4), 949–956 (2008).
  • Yunok O , NohyunL, HyunWook K, JunghwanO. In vitro study on apoptotic cell death by effective magnetic hyperthermia with chitosan-coated MnFe2O4. Nanotechnology27(11), 115101 (2016).
  • Zhou J , WangX, DuLet al. Effect of hyperthermia on the apoptosis and proliferation of CaSki cells. Mol. Med. Rep.4(1), 187–191 (2011).
  • Ramirez-Nuñez AL , Jimenez-GarciaLF, GoyaGF, SanzB, Santoyo-SalazarJ. In vitro magnetic hyperthermia using polyphenol-coated Fe3O4@γFe2O3 nanoparticles from Cinnamomun verum and Vanilla planifolia: the concert of green synthesis and therapeutic possibilities. Nanotechnology29(7), 074001 (2018).
  • Fortin J-P , WilhelmC, ServaisJ, MénagerC, BacriJ-C, GazeauF. Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. J. Am. Chem. Soc.129(9), 2628–2635 (2007).
  • Hergt R , HiergeistR, ZeisbergerMet al. Magnetic properties of bacterial magnetosomes as potential diagnostic and therapeutic tools. J. Magn. Magn. Mater.293(1), 80–86 (2005).
  • Jang ES , LeeSY, ChaEJet al. Fluorescent dye labeled iron oxide/silica core/shell nanoparticle as a multimodal imaging probe. Pharm. Res.31(12), 3371–3378 (2014).
  • Haghniaz R , BhayaniKR, UmraniRD, PaknikarKM. Dextran stabilized lanthanum strontium manganese oxide nanoparticles for magnetic resonance imaging. RSC Adv.3(40), 18489–18497 (2013).
  • Thorat ND , KhotVM, SalunkheAB, PrasadAI, NingthoujamRS, PawarSH. Surface functionalized LSMO nanoparticles with improved colloidal stability for hyperthermia applications. J. Phys. D: Appl. Phys.46(10), 105003 (2013).
  • Zhang K , HollowayT, PradhanJet al. Synthesis and magnetic characterizations of La(1-x)Sr(x)MnO3 nanoparticles for biomedical applications. J. Nanosci. Nanotechnol.10(9), 5520–5526 (2010).
  • Javid A , AhmadianS, SabouryAA, KalantarSM, Rezaei-ZarchiS. Chitosan-coated superparamagnetic iron oxide nanoparticles for doxorubicin delivery: synthesis and anticancer effect against human ovarian cancer cells. Chem. Biol. Drug Des.82(3), 296–306 (2013).
  • Linh P , ChienN, DungDet al. Biocompatible nanoclusters of O-carboxymethyl chitosan-coated Fe3O4 nanoparticles: synthesis, characterization and magnetic heating efficiency. J. Mater. Sci.53(12), 8887–8900 (2018).
  • Branquinho LC , CarriãoMS, CostaASet al. Effect of magnetic dipolar interactions on nanoparticle heating efficiency: implications for cancer hyperthermia. Sci. Rep.3, 2887 (2013).
  • Landi GT . Role of dipolar interaction in magnetic hyperthermia. Phys. Rev. B.89(1), 014403 (2014).
  • Serantes D , BaldomirD, Martinez-BoubetaCet al. Influence of dipolar interactions on hyperthermia properties of ferromagnetic particles. J. Appl. Phys.108(7), 073918 (2010).
  • Calatayud MP , SolerE, TorresTEet al. Cell damage produced by magnetic fluid hyperthermia on microglial BV2 cells. Sci. Rep.7(1), 8627 (2017).
  • Goya GF , LimaE, ArelaroADet al. Magnetic hyperthermia with Fe3O4 nanoparticles: the influence of particle size on energy absorption. IEEE Trans. Magn.44(11), 4444–4447 (2008).
  • Nemati Z , AlonsoJ, MartinezLMet al. Enhanced magnetic hyperthermia in iron oxide nano-octopods: size and anisotropy effects. J. Phys. Chem. C.120(15), 8370–8379 (2016).
  • Rosensweig R . Heating magnetic fluid with alternating magnetic field. J. Magn. Magn. Mater.252, 370–374 (2002).
  • Noh S-H , NaW, JangJ-Tet al. Nanoscale magnetism control via surface and exchange anisotropy for optimized ferrimagnetic hysteresis. Nano Lett.12(7), 3716–3721 (2012).
  • Ghosh R , PradhanL, DeviYPet al. Induction heating studies of Fe3O4 magnetic nanoparticles capped with oleic acid and polyethylene glycol for hyperthermia. J. Mater. Chem.21(35), 13388–13398 (2011).
  • Fajaroh F , SetyawanH, WidiyastutiW, WinardiS. Synthesis of magnetite nanoparticles by surfactant-free electrochemical method in an aqueous system. Adv. Powder Technol.23(3), 328–333 (2012).
  • Levy M , LucianiN, AlloyeauDet al. Long term in vivo biotransformation of iron oxide nanoparticles. Biomaterials32(16), 3988–3999 (2011).
  • Thorat N , PatilR, KhotVet al. Highly water-dispersible surface-functionalized LSMO nanoparticles for magnetic fluid hyperthermia application. New J. Chem.37(9), 2733–2742 (2013).
  • Zhang W , ZuoX, NiuYet al. Novel nanoparticles with Cr3+ substituted ferrite for self-regulating temperature hyperthermia. Nanoscale9(37), 13929–13937 (2017).
  • Blanco-Andujar C , OrtegaD, SouthernP, PankhurstQ, ThanhN. High performance multi-core iron oxide nanoparticles for magnetic hyperthermia: microwave synthesis, and the role of core-to-core interactions. Nanoscale7(5), 1768–1775 (2015).
  • Ludwig R , StapfM, DutzS, MüllerR, TeichgräberU, HilgerI. Structural properties of magnetic nanoparticles determine their heating behavior – an estimation of the in vivo heating potential. Nanoscale Res. Lett.9(1), 602–602 (2014).
  • Bauer LM , SituSF, GriswoldMA, SamiaAC. High-performance iron oxide nanoparticles for magnetic particle imaging – guided hyperthermia (hMPI). Nanoscale8(24), 12162–12169 (2016).
  • Espinosa A , DiCorato R, Kolosnjaj-TabiJ, FlaudP, PellegrinoT, WilhelmC. Duality of iron oxide nanoparticles in cancer therapy: amplification of heating efficiency by magnetic hyperthermia and photothermal bimodal treatment. ACS Nano10(2), 2436–2446 (2016).
  • Li J , LiuX, ZhangHet al. Ferrocenyl–triphenyltin complexes as lysosome-targeted imaging and anticancer agents. Inorg. Chem.58(2), 1710–1718 (2019).
  • Livak KJ , SchmittgenTD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods25(4), 402–408 (2001).
  • Anjali , JhaSK, KuanrBK. Synthesis and characterization of iron oxide nanoparticles (IONPs) and their cytotoxicity effects on lung epithelial carcinoma cells. AIP Conf. Proc.1832(1), 050110 (2017).
  • Iyengar SJ , JoyM, MaityT, ChakrabortyJ, KotnalaRK, GhoshS. Colloidal properties of water dispersible magnetite nanoparticles by photon correlation spectroscopy. RSC Adv.6(17), 14393–14402 (2016).
  • Thorat ND , BoharaRA, MalgrasVet al. Multimodal superparamagnetic nanoparticles with unusually enhanced specific absorption rate for synergetic cancer therapeutics and magnetic resonance imaging. ACS Appl. Mater. Interfaces8(23), 14656–14664 (2016).
  • Thorat ND , PatilRM, KhotVMet al. Highly water-dispersible surface-functionalized LSMO nanoparticles for magnetic fluid hyperthermia application. New J. Chem.37(9), 2733–2742 (2013).
  • Sabuncu AC , GrubbsJ, QianS, Abdel-FattahTM, StaceyMW, BeskokA. Probing nanoparticle interactions in cell culture media. Colloids Surf. B. Biointerfaces95, 96–102 (2012).
  • Han J , KimB, ShinJYet al. Iron oxide nanoparticle-mediated development of cellular gap junction crosstalk to improve mesenchymal stem cells’ therapeutic efficacy for myocardial infarction. ACS Nano9(3), 2805–2819 (2015).
  • Rad AM , ArbabAS, IskanderASM, JiangQ, Soltanian-ZadehH. Quantification of superparamagnetic iron oxide (SPIO)-labeled cells using MRI. J. Magn. Reson. Imaging26(2), 366–374 (2007).
  • Lahiri BB , MuthukumaranT, PhilipJ. Magnetic hyperthermia in phosphate coated iron oxide nanofluids. J. Magn. Magn. Mater.407, 101–113 (2016).
  • Kumar R , ChauhanA, JhaSK, KuanrBK. Encapsulated lanthanum strontium manganese oxide in mesoporous silica shell: potential for cancer treatment by hyperthermia therapy. J. Alloys Compd.790, 433–446 (2019).
  • Kallumadil M , TadaM, NakagawaT, AbeM, SouthernP, PankhurstQA. Suitability of commercial colloids for magnetic hyperthermia. J. Magn. Magn. Mater.321(10), 1509–1513 (2009).
  • Dutz S , HergtR. Magnetic nanoparticle heating and heat transfer on a microscale: basic principles, realities and physical limitations of hyperthermia for tumour therapy. Int. J. Hyperthermia29(8), 790–800 (2013).
  • Falk MH , IsselsRD. Hyperthermia in oncology. Int. J. Hyperthermia17(1), 1–18 (2001).
  • Levi-Polyachenko NH , StewartJHIV. Clinical relevance of nanoparticle induced hyperthermia for drug delivery and treatment of abdominal cancers. Survival1(2), 24–37 (2011).
  • Conway EM , LiuL, NowakowskiB, Steiner-MosonyiM, RibeiroSP, MichalakM. Heat shock-sensitive expression of calreticulin. In vitro and in vivo up-regulation. J. Biol. Chem.270(28), 17011–17016 (1995).
  • Tulapurkar ME , AsiegbuBE, SinghIS, HasdayJD. Hyperthermia in the febrile range induces HSP72 expression proportional to exposure temperature but not to HSF-1 DNA-binding activity in human lung epithelial A549 cells. Cell Stress Chaperones14(5), 499–508 (2009).
  • Heshiki W , TomiharaK, YamazakiM, AraiN, NakamoriK, NoguchiM. Constitutive activation of caspase-3 in non-apoptotic oral squamous cell carcinoma cells. J. Cancer Sci. Ther.7, 75–80 (2015).
  • Kandasamy G , SudameA, BhatiP, ChakrabartyA, MaityD. Systematic investigations on heating effects of carboxyl-amine functionalized superparamagnetic iron oxide nanoparticles (SPIONs) based ferrofluids for in vitro cancer hyperthermia therapy. J. Mol. Liq.256, 224–237 (2018).
  • Conde-Leboran I , BaldomirD, Martinez-BoubetaCet al. A single picture explains diversity of hyperthermia response of magnetic nanoparticles. J. Phys. Chem. C119(27), 15698–15706 (2015).
  • Piñeiro-Redondo Y , Bañobre-LópezM, Pardiñas-BlancoI, GoyaG, López-QuintelaMA, RivasJ. The influence of colloidal parameters on the specific power absorption of PAA-coated magnetite nanoparticles. Nanoscale Res. Lett.6(1), 383 (2011).
  • Pon-On W , TithitoT, ManeeprakornW, PhenratT, TangIM. Investigation of magnetic silica with thermoresponsive chitosan coating for drug controlled release and magnetic hyperthermia application. Mater. Sci. Eng. C97, 23–30 (2019).
  • Patil RM , ShetePB, ThoratNDet al. Superparamagnetic iron oxide/chitosan core/shells for hyperthermia application: improved colloidal stability and biocompatibility. J. Magn. Magn. Mater.355, 22–30 (2014).
  • Müller R , HergtR, ZeisbergerM, GawalekW. Preparation of magnetic nanoparticles with large specific loss power for heating applications. J. Magn. Magn. Mater.289, 13–16 (2005).
  • Guardia P , DiCorato R, LartigueLet al. Water-soluble iron oxide nanocubes with high values of specific absorption rate for cancer cell hyperthermia treatment. ACS Nano6(4), 3080–3091 (2012).
  • Lartigue L , HugounenqP, AlloyeauDet al. Cooperative organization in iron oxide multi-core nanoparticles potentiates their efficiency as heating mediators and MRI contrast agents. ACS Nano6(12), 10935–10949 (2012).
  • Yoo D , JeongH, PreihsCet al. Double-effector nanoparticles: a synergistic approach to apoptotic hyperthermia. Angew. Chem. Int. Ed. Engl.51(50), 12482–12485 (2012).
  • Haghniaz R , UmraniRD, PaknikarKM. Hyperthermia mediated by dextran-coated La0.7Sr0.3MnO3 nanoparticles: in vivo studies. Int. J. Nanomedicine11, 1779–1791 (2016).
  • Oh Y , LeeN, KangHW, OhJ. In vitro study on apoptotic cell death by effective magnetic hyperthermia with chitosan-coated MnFe(2)O(4). Nanotechnology27(11), 115101 (2016).
  • Luo Z , ZhengK, FanQ, JiangX, XiongD. Hyperthermia exposure induces apoptosis and inhibits proliferation in HCT116 cells by upregulating miR-34a and causing transcriptional activation of p53. Exp. Ther. Med.14(6), 5379–5386 (2017).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.