Abstract
Polyaniline nanoparticles (PANI-Nps) have been used in several applications; however, there are few publications related to the use in the photothermal therapy. PANI-Nps have high optical absorbance in the near-infrared region and in this wavelength range, biological systems are relatively transparent. For this reason, these materials can be used to absorb energy and to generate heat that destroys cancer cells selectively. PANI-Nps with average size of ca. 200 nm and neutral zeta potential were synthesized and characterized by DLS, SEM, and zeta potential. The kinetics of incorporation of PANI-Nps into LM2 cell line was monitored using UV–Vis spectrophotometry. The analysis of cell viability after PANI-Nps exposure shows that these nanoparticles are not cytotoxic even at high concentration and show no change in cell morphology and metabolic activity. Furthermore, we found that nanoparticle cell uptake reaches the maximum value c.a. 3 h after incubation. Cells were targeted by Pani-Nps and irradiated, resulting in significant elevation of intracellular ROS and heat production. One of the mechanisms of PANI-Nps-mediated photothermal killing of cancer cells apparently involved oxidative stress resulting in apoptotic cell death.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acevedo DA, Lasagni AF, Barbero CA, Mücklich F (2007) Simple fabrication method of conductive polymeric arrays by using direct laser interference micro-/nanopatterning. Adv Mater 19:1272–1275. doi:10.1002/adma.200601693
Ahmed K, Zaidi SF (2013) Treating cancer with heat: hyperthermia as promising strategy to enhance apoptosis. J Pak Med Assoc 63:504–508
Allison SD (2007) Liposomal drug delivery. J Infus Nurs 30:89–95. doi:10.1097/01.NAN.0000264712.26219.67
Balasubramanian SK, Jittiwat J, Manikandan J et al (2010) Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials 31:2034–2042. doi:10.1016/j.biomaterials.2009.11.079
Bovis MJ, Woodhams JH, Loizidou M et al (2012) Improved in vivo delivery of m-THPC via pegylated liposomes for use in photodynamic therapy. J Control Release 157:196–205. doi:10.1016/j.jconrel.2011.09.085
Casas A, Perotti C, Saccoliti M et al (2002) ALA and ALA hexyl ester in free and liposomal formulations for the photosensitisation of tumour organ cultures. Br J Cancer 86:837–842. doi:10.1038/sj.bjc.6600144
Choi EB, Choi J, Bae SR et al (2014) Colourimetric redox-polyaniline nanoindicator for in situ vesicular trafficking of intracellular transport. Nano Res. doi:10.1007/s12274-014-0597-6
Chu M, Shao Y, Peng J et al (2013) Near-infrared laser light mediated cancer therapy by photothermal effect of Fe3O4 magnetic nanoparticles. Biomaterials 34:4078–4088. doi:10.1016/j.biomaterials.2013.01.086
Fery-Forgues S (2013) Fluorescent organic nanocrystals and non-doped nanoparticles for biological applications. Nanoscale 5:8428–8442. doi:10.1039/c3nr02657d
Fu G, Liu W, Feng S, Yue X (2012) Prussian blue nanoparticles operate as a new generation of photothermal ablation agents for cancer therapy. Chem Commun 48:11567–11569. doi:10.1039/c2cc36456e
Gaspar D, Freire JM, Pacheco TR et al (2015) Apoptotic human neutrophil peptide-1 anti-tumor activity revealed by cellular biomechanics. Biochim Biophys Acta 1853:308–316. doi:10.1016/j.bbamcr.2014.11.006
Häcker G (2000) The morphology of apoptosis. Cell Tissue Res 301:5–17
Haley B, Frenkel E (2008) Nanoparticles for drug delivery in cancer treatment. Urol Oncol 26:57–64. doi:10.1016/j.urolonc.2007.03.015
Heeger AJ (1993) Polyaniline with surfactant counterions: conducting polymer materials which are processible in the conducting form. Synth Met 57:3471–3482. doi:10.1016/0379-6779(93)90462-6
Hiura TS, Li N, Kaplan R et al (2000) The role of a mitochondrial pathway in the induction of apoptosis by chemicals extracted from diesel exhaust particles. J Immunol 165:2703–2711
Hong C, Lee J, Zheng H et al (2011) Porous silicon nanoparticles for cancer photothermotherapy. Nanoscale Res Lett 6:321. doi:10.1186/1556-276X-6-321
Hou C-H, Lin F-L, Hou S-M, Liu J-F (2014) Hyperthermia induces apoptosis through endoplasmic reticulum and reactive oxygen species in human osteosarcoma cells. Int J Mol Sci 15:17380–17395. doi:10.3390/ijms151017380
Huang N, Wang H, Zhao J et al (2010) Single-wall carbon nanotubes assisted photothermal cancer therapy: animal study with a murine model of squamous cell carcinoma. Lasers Surg Med 42:638–648. doi:10.1002/lsm.20968
Hurle JM, Merino R (1999) When Cells Die: A Comprehensive Evaluation of Apoptosis and Programmed Cell Death (1998). Lockshin RA, Zakeri Z, Tilly JL (eds). New York: Wiley-Liss, 504 pp. £65 hardback; ISBN 0-471-16569-7. BioEssays 21:92–92. doi: 10.1002/(SICI)1521-1878(199901)21:1<92::AID-BIES15>3.0.CO;2-U
Ibarra LE, Yslas EI, Molina MA et al (2013) Near-infrared mediated tumor destruction by photothermal effect of PANI-Np in vivo. Laser Phys 23:066004. doi:10.1088/1054-660X/23/6/066004
Ibarra LE, Tarres L, Bongiovanni S et al (2015) Assessment of polyaniline nanoparticles toxicity and teratogenicity in aquatic environment using Rhinella arenarum model. Ecotoxicol Environ Saf 114:84–92. doi:10.1016/j.ecoenv.2015.01.013
Jaque D, Maestro LM, del Rosal B et al (2014) Nanoparticles for photothermal therapies. Nanoscale. doi:10.1039/C4NR00708E
Kampinga HH (2006) Cell biological effects of hyperthermia alone or combined with radiation or drugs: a short introduction to newcomers in the field. Int J Hyperth 22:191–196. doi:10.1080/02656730500532028
Kievit FM, Veiseh O, Bhattarai N et al (2009) PEI–PEG–chitosan copolymer coated iron oxide nanoparticles for safe gene delivery: synthesis, complexation, and transfection. Adv Funct Mater 19:2244–2251. doi:10.1002/adfm.200801844
Kucekova Z, Humpolicek P, Kasparkova V et al (2014) Colloidal polyaniline dispersions: antibacterial activity, cytotoxicity and neutrophil oxidative burst. Colloids Surf B Biointerfaces 116:411–417. doi:10.1016/j.colsurfb.2014.01.027
Kumari A, Yadav SK, Yadav SC (2010) Biodegradable polymeric nanoparticles based drug delivery systems. Colloids Surf B Biointerfaces 75:1–18. doi:10.1016/j.colsurfb.2009.09.001
Lee ES, Na K, Bae YH (2003) Polymeric micelle for tumor pH and folate-mediated targeting. J Control Release 91:103–113
Lee ES, Gao Z, Bae YH (2008) Recent progress in tumor pH targeting nanotechnology. J Control Release 132:164–170. doi:10.1016/j.jconrel.2008.05.003
Lee YJ, Lee G-J, Kang SW et al (2013) Label-free and quantitative evaluation of cytotoxicity based on surface nanostructure and biophysical property of cells utilizing AFM. Micron 49:54–59. doi:10.1016/j.micron.2013.02.014
Li K, Liu B (2014) Polymer-encapsulated organic nanoparticles for fluorescence and photoacoustic imaging. Chem Soc Rev. doi:10.1039/c4cs00014e
Li D, Huang J, Kaner RB (2009) Polyaniline nanofibers: a unique polymer nanostructure for versatile applications. Acc Chem Res 42:135–145. doi:10.1021/ar800080n
Markovic ZM, Harhaji-Trajkovic LM, Todorovic-Markovic BM et al (2011) In vitro comparison of the photothermal anticancer activity of graphene nanoparticles and carbon nanotubes. Biomaterials 32:1121–1129. doi:10.1016/j.biomaterials.2010.10.030
Marquis BJ, Love SA, Braun KL, Haynes CL (2009) Analytical methods to assess nanoparticle toxicity. Analyst 134:425–439. doi:10.1039/b818082b
Mocan T, Matea CT, Cojocaru I et al (2014) Photothermal treatment of human pancreatic cancer using PEGylated multi-walled carbon nanotubes induces apoptosis by triggering mitochondrial membrane depolarization mechanism. J Cancer 5:679–688. doi:10.7150/jca.9481
Ngamna O, Morrin A, Killard AJ et al (2007) Inkjet printable polyaniline nanoformulations. Langmuir 23:8569–8574. doi:10.1021/la700540g
Novák P, Müller K, Santhanam KSV, Haas O (1997) Electrochemically active polymers for rechargeable batteries. Chem Rev 97:207–282
Park E-J, Park K (2009) Oxidative stress and pro-inflammatory responses induced by silica nanoparticles in vivo and in vitro. Toxicol Lett 184:18–25. doi:10.1016/j.toxlet.2008.10.012
Passagne I, Morille M, Rousset M et al (2012) Implication of oxidative stress in size-dependent toxicity of silica nanoparticles in kidney cells. Toxicology 299:112–124. doi:10.1016/j.tox.2012.05.010
Pulskamp K, Diabaté S, Krug HF (2007) Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol Lett 168:58–74. doi:10.1016/j.toxlet.2006.11.001
Purschke M, Laubach H-J, Anderson RR, Manstein D (2010) Thermal injury causes DNA damage and lethality in unheated surrounding cells: active thermal bystander effect. J Investig Dermatol 130:86–92. doi:10.1038/jid.2009.205
Royall JA, Ischiropoulos H (1993) Evaluation of 2′,7′-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys 302:348–355. doi:10.1006/abbi.1993.1222
Schulze C, Kroll A, Lehr C-M et al (2008) Not ready to use—overcoming pitfalls when dispersing nanoparticles in physiological media. Nanotoxicology 2:51–61. doi:10.1080/17435390802018378
Shevach M, Fleischer S, Shapira A, Dvir T (2014) Gold nanoparticle-decellularized matrix hybrids for cardiac tissue engineering. Nano Lett 14:5792–5796. doi:10.1021/nl502673m
Sokolova V, Kozlova D, Knuschke T et al (2013) Mechanism of the uptake of cationic and anionic calcium phosphate nanoparticles by cells. Acta Biomater 9:7527–7535. doi:10.1016/j.actbio.2013.02.034
Stejskal J, Proke J (2014) Reprotonated polyanilines: the stability of conductivity at elevated temperature. Polym Degrad Stab 102:67–73. doi:10.1016/j.polymdegradstab.2014.02.001
Stejskal J, Sapurina I (2005) Polyaniline: thin films and colloidal dispersions (IUPAC Technical Report). Pure Appl Chem 77:815–826. doi:10.1351/pac200577050815
Stejskal J, Hajná M, Kašpárková V et al (2014) Purification of a conducting polymer, polyaniline, for biomedical applications. Synth Met 195:286–293. doi:10.1016/j.synthmet.2014.06.020
Stern ST, Adiseshaiah PP, Crist RM (2012) Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part Fibre Toxicol 9:20. doi:10.1186/1743-8977-9-20
Sultan RA (1990) Tumour ablation by laser in general surgery. Lasers Med Sci 5:185–193. doi:10.1007/BF02031380
Thurn KT, Arora H, Paunesku T et al (2011) Endocytosis of titanium dioxide nanoparticles in prostate cancer PC-3M cells. Nanomedicine 7:123–130. doi:10.1016/j.nano.2010.09.004
Verma A, Stellacci F (2010) Effect of surface properties on nanoparticle-cell interactions. Small 6:12–21. doi:10.1002/smll.200901158
Villalba P, Ram MK, Gomez H et al (2012) Cellular and in vitro toxicity of nanodiamond-polyaniline composites in mammalian and bacterial cell. Mater Sci Eng, C 32:594–598. doi:10.1016/j.msec.2011.12.017
Virji S, Huang J, Kaner RB, Weiller BH (2004) Polyaniline nanofiber gas sensors: examination of response mechanisms. Nano Lett 4:491–496. doi:10.1021/nl035122e
Wang C, Cheng L, Liu Z (2011a) Drug delivery with upconversion nanoparticles for multi-functional targeted cancer cell imaging and therapy. Biomaterials 32:1110–1120. doi:10.1016/j.biomaterials.2010.09.069
Wang D-C, Chen K-Y, Tsai C-H et al (2011b) AFM membrane roughness as a probe to identify oxidative stress-induced cellular apoptosis. J Biomech 44:2790–2794. doi:10.1016/j.jbiomech.2011.08.021
Weissleder R (2001) A clearer vision for in vivo imaging. Nat Biotechnol 19:316–317. doi:10.1038/86684
Welch A (1984) The thermal response of laser irradiated tissue. IEEE J Quantum Electron 20:1471–1481. doi:10.1109/JQE.1984.1072339
Xu P, Xu J, Liu S, Yang Z (2012) Nano copper induced apoptosis in podocytes via increasing oxidative stress. J Hazard Mater 241–242:279–286. doi:10.1016/j.jhazmat.2012.09.041
Yang J, Choi J, Bang D et al (2011) Convertible organic nanoparticles for near-infrared photothermal ablation of cancer cells. Angew Chem Int Ed Engl 50:441–444. doi:10.1002/anie.201005075
Yoo D, Jeong H, Preihs C et al (2012) Double-effector nanoparticles: a synergistic approach to apoptotic hyperthermia. Angew Chem Int Ed Engl 51:12482–12485. doi:10.1002/anie.201206400
Yslas EI, Ibarra LE, Peralta DO et al (2012) Polyaniline nanofibers: acute toxicity and teratogenic effect on Rhinella arenarum embryos. Chemosphere 87:1374–1380. doi:10.1016/j.chemosphere.2012.02.033
Yuan H, Khoury CG, Wilson CM et al (2012) In vivo particle tracking and photothermal ablation using plasmon-resonant gold nanostars. Nanomedicine. doi:10.1016/j.nano.2012.02.005
Zhang X, Wu D, Zhao B et al (2011) Size-dependent in vivo toxicity of PEG-coated gold nanoparticles. Int J Nanomedicine 6:2071–2081
Zhang S, Li Y, He X et al (2014) Photothermolysis mediated by gold nanorods modified with EGFR monoclonal antibody induces Hep-2 cells apoptosis in vitro and in vivo. Int J Nanomedicine 9:1931–1946. doi:10.2147/IJN.S59870
Zhao J, Zhou R, Fu X et al (2014) Cell-penetrable lysine dendrimers for anti-cancer drug delivery: synthesis and preliminary biological evaluation. Arch Pharm 347:469–477. doi:10.1002/ardp.201300415
Zhou J, Lu Z, Zhu X et al (2013) NIR photothermal therapy using polyaniline nanoparticles. Biomaterials 34:9584–9592. doi:10.1016/j.biomaterials.2013.08.075
Acknowledgments
The authors are grateful to the Secretaría de Ciencia y Técnica (SECYT) of Universidad Nacional de Río Cuarto and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) for their financial support. L. Ibarra thanks CONICET for a research fellowship. V. Rivarola, C. Barbero, and E.I. Yslas hold the posts as Scientific Researchers at the CONICET. The authors also are thankful to Dr. Diego Acevedo for the images of AFM microscopy.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Edith Inés Yslas and Luis Exequiel Ibarra have contributed equally.
Rights and permissions
About this article
Cite this article
Yslas, E.I., Ibarra, L.E., Molina, M.A. et al. Polyaniline nanoparticles for near-infrared photothermal destruction of cancer cells. J Nanopart Res 17, 389 (2015). https://doi.org/10.1007/s11051-015-3187-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11051-015-3187-y