Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

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

Review Article

Recent Developments of Nanoparticles in the Treatment of Photodynamic Therapy for Cervical Cancer

Author(s): Wenwen Guo, Chao Sun, Guan Jiang* and Yong Xin*

Volume 19, Issue 15, 2019

Page: [1809 - 1819] Pages: 11

DOI: 10.2174/1871520619666190411121953

Price: $65

Abstract

Photodynamic therapy (PDT) is a photoactivation or photosensitization process, wherein the photosensitizer (PS) is activated under appropriate wavelengths. Conventional antitumor therapy for cervical cancer includes surgery, radiotherapy, and chemotherapy. However, these techniques are accompanied by some evident shortcomings. PDT is considered an emerging minimally invasive treatment for cervical cancer. In recent years, new PSs have been synthesized because of the long absorption wavelength, good solubility, and high tumor targeting ability. Studies also showed that the synergistic combination of nanomaterials with PSs resulted in considerable benefits compared with the use of small-molecule PSs alone. The compounds can act both as a drug delivery system and PS and enhance the photodynamic effect. This review summarizes the application of some newly synthesized PSs and PS-combined nanoparticles in cervical cancer treatment to enhance the efficiency of PDT. The mechanism and influencing factors of PDT are further elaborated.

Keywords: Photodynamic therapy, photosensitizer, nanoparticle, drug delivery system, cervical cancer, radiotherapy.

Graphical Abstract

[1]
Sadalla, J.C.; Andrade, J.M.; Genta, M.L.; Baracat, E.C. Cervical cancer: What’s new? Rev. Assoc. Med. Bras., 2015, 61(6), 536-542.
[2]
Li, H.; Wu, X.; Cheng, X. Advances in diagnosis and treatment of metastatic cervical cancer. J. Gynecol. Oncol., 2016, 27(4)e43
[3]
Tsikouras, P.; Zervoudis, S.; Manav, B.; Tomara, E.; Iatrakis, G.; Romanidis, C.; Bothou, A.; Galazios, G. Cervical cancer: Screening, diagnosis and staging. J. BUON, 2016, 21(2), 320-325.
[4]
Chen, J.; Gu, W.; Yang, L.; Chen, C.; Shao, R.; Xu, K.; Xu, Z.P. Nanotechnology in the management of cervical cancer. Rev. Med. Virol., 2015, 25(Suppl. 1), 72-83.
[5]
Yu, Y.; Xu, S.; You, H.; Zhang, Y.; Yang, B.; Sun, X.; Yang, L.; Chen, Y.; Fu, S.; Wu, J. In vivo synergistic anti-tumor effect of paclitaxel nanoparticles combined with radiotherapy on human cervical carcinoma. Drug Deliv., 2017, 24(1), 75-82.
[6]
Conte, C.; Maiolino, S.; Pellosi, D.S.; Miro, A.; Ungaro, F.; Quaglia, F. Polymeric nanoparticles for cancer photodynamic therapy. Top. Curr. Chem., 2016, 370, 61-112.
[7]
Chen, Q.; Ke, H.; Dai, Z.; Liu, Z. Nanoscale theranostics for physical stimulus-responsive cancer therapies. Biomaterials, 2015, 73, 214-230.
[8]
Lucky, S.S.; Soo, K.C.; Zhang, Y. Nanoparticles in photodynamic therapy. Chem. Rev., 2015, 115(4), 1990-2042.
[9]
Eshghi, H.; Sazgarnia, A.; Rahimizadeh, M.; Attaran, N.; Bakavoli, M.; Soudmand, S. Protoporphyrin IX-gold nanoparticle conjugates as an efficient photosensitizer in cervical cancer therapy. Photodiagn. Photodyn. Ther., 2013, 10(3), 304-312.
[10]
Shen, Y.; Shuhendler, A.J.; Ye, D.; Xu, J.J.; Chen, H.Y. Two-photon excitation nanoparticles for photodynamic therapy. Chem. Soc. Rev., 2016, 45(24), 6725-6741.
[11]
Castano, A.P.; Demidova, T.N.; Hamblin, M.R. Mechanisms in photodynamic therapy: Part one-photosensitizers, photochemistry and cellular localization. Photodiagn. Photodyn. Ther., 2004, 1(4), 279-293.
[12]
Schmitt, J.; Heitz, V.; Sour, A.; Bolze, F.; Ftouni, H.; Nicoud, J.F.; Flamigni, L.; Ventura, B. Diketopyrrolopyrrole-porphyrin conjugates with high two-photon absorption and singlet oxygen generation for two-photon photodynamic therapy. Angew. Chem. Int. Ed. Engl., 2015, 54(1), 169-173.
[13]
Wang, H.; Yang, X.; Shao, W.; Chen, S.; Xie, J.; Zhang, X.; Wang, J.; Xie, Y. Ultrathin black phosphorus nanosheets for efficient singlet oxygen generation. J. Am. Chem. Soc., 2015, 137(35), 11376-11382.
[14]
Lu, K.; He, C.; Lin, W. A chlorin-based nanoscale metal-organic framework for photodynamic therapy of colon cancers. J. Am. Chem. Soc., 2015, 137(24), 7600-7603.
[15]
Kharkwal, G.B.; Sharma, S.K.; Huang, Y.Y.; Dai, T.; Hamblinm, M.R. Photodynamic therapy for infections: Clinical applications. Lasers Surg. Med., 2011, 43(7), 755-767.
[16]
Dolmans, D.E.; Fukumura, D.; Jain, R.K. Photodynamic therapy for cancer. Nat. Rev. Cancer, 2003, 3(5), 380-387.
[17]
Calixto, G.M.; Bernegossi, J.; de Freitas, L.M.; Fontana, C.R.; Chorilli, M. Nanotechnology-based drug delivery systems for photodynamic therapy of cancer: A review. Molecules, 2016, 21(3), 342.
[18]
Ding, H.; Yu, H.; Dong, Y.; Tian, R.; Huang, G.; Boothman, D.A.; Sumer, B.D.; Gao, J. Photoactivation switch from type II to type I reactions by electron-rich micelles for improved photodynamic therapy of cancer cells under hypoxia. J. Control. Release, 2011, 156(3), 276-280.
[19]
Ge, J.; Lan, M.; Zhou, B.; Liu, W.; Guo, L.; Wang, H.; Jia, Q.; Niu, G.; Huang, X.; Zhou, H.; Meng, X.; Wang, P.; Lee, C-S.; Zhang, W.; Han, X. A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nat. Commun., 2014, 5, 4596.
[20]
Zhou, Z.; Song, J.; Nie, L.; Chen, X. Reactive oxygen species generating systems meeting challenges of photodynamic cancer therapy. Chem. Soc. Rev., 2016, 45(23), 6597-6626.
[21]
Yoo, J.O.; Ha, K.S. New insights into the mechanisms for photodynamic therapy-induced cancer cell death. Int. Rev. Cell Mol. Biol., 2012, 295, 139-174.
[22]
Mielczarek-Badora, E.; Szulc, M. Photodynamic therapy and its role in periodontitis treatment. Postepy Hig. Med. Dosw., 2013, 67, 1058-1065.
[23]
Chen, Y.; Shea, C.R.; Calzavara-Pinton, P. Molecular mechanism of photodynamic therapy. J. Central South Univ. Med. Sci., 2014, 39(1), 102-108.
[24]
Feng, J.B.; Bai, Y.X. The development of photodynamic therapy for malignant tumor. Pract. Oncol. J., 2012, 26(6), 573-576.
[25]
Topaloglu, N.; Guney, M.; Aysan, N.; Gulsoy, M.; Yuksel, S. The role of reactive oxygen species in the antibacterial photodynamic treatment: Photoinactivation vs. proliferation. Lett. Appl. Microbiol., 2016, 62(3), 230-236.
[26]
Bartosz, G. Reactive oxygen species: Destroyers or messengers? Biochem. Pharmacol., 2009, 77(8), 1303-1315.
[27]
Salunkhe, P.; Topfer, T.; Buer, J.; Tummler, B. Genome-wide transcriptional profiling of the steady-state response of Pseudomonas aeruginosa to hydrogen peroxide. J. Bacteriol., 2005, 187(8), 2565-2572.
[28]
Kotulska, M.; Kulbacka, J.; Saczko, J. Advances in photodynamic therapy assisted by electroporation. Curr. Drug Metab., 2013, 14(3), 309-318.
[29]
Edinger, A.L.; Thompson, C.B. Death by design: Apoptosis, necrosis and autophagy. Curr. Opin. Cell Biol., 2004, 16(6), 663-669.
[30]
Buytaert, E.; Dewaele, M.; Agostinis, P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim. Biophys. Acta, 2007, 1776(1), 86-107.
[31]
Granville, D.J.; Cassidy, B.A.; Ruehlmann, D.O.; Choy, J.C.; Brenner, C.; Kroemer, G.; van Breemen, C.; Margaron, P.; Hunt, D.W.; McManus, B.M. Mitochondrial release of apoptosis-inducing factor and cytochrome c during smooth muscle cell apoptosis. Am. J. Pathol., 2001, 159(1), 305-311.
[32]
Yokota, T.; Ikeda, H.; Inokuchi, T.; Sano, K.; Koji, T. Enhanced cell death in NR-S1 tumor by photodynamic therapy: Possible involvement of Fas and Fas ligand system. Lasers Surg. Med., 2000, 26(5), 449-460.
[33]
Reiter, I.; Schwamberger, G.; Krammer, B. Effect of photodynamic pretreatment on the susceptibility of murine tumor cells to macrophage antitumor mechanisms. Photochem. Photobiol., 1997, 66(3), 384-388.
[34]
Agostinis, P.; Buytaert, E.; Breyssens, H.; Hendrickx, N. Regulatory pathways in photodynamic therapy induced apoptosis. Photochem. Photobiol. Sci., 2004, 3(8), 721-729.
[35]
Buytaert, E.; Callewaert, G.; Vandenheede, J.R.; Agostinis, P. Deficiency in apoptotic effectors Bax and Bak reveals an autophagic cell death pathway initiated by photodamage to the endoplasmic reticulum. Autophagy, 2006, 2(3), 238-240.
[36]
Scherz-Shouval, R.; Elazar, Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol., 2007, 17(9), 422-427.
[37]
Reiners, J.J., Jr; Agostinis, P.; Berg, K.; Oleinick, N.L.; Kessel, D. Assessing autophagy in the context of photodynamic therapy. Autophagy, 2010, 6(1), 7-18.
[38]
Janku, F.; McConkey, D.J.; Hong, D.S.; Kurzrock, R. Autophagy as a target for anticancer therapy. Nat. Rev. Clin. Oncol., 2011, 8(9), 528-539.
[39]
Galluzzi, L.; Vanden Berghe, T.; Vanlangenakker, N.; Buettner, S.; Eisenberg, T.; Vandenabeele, P.; Madeo, F.; Kroemer, G. Programmed necrosis from molecules to health and disease. Int. Rev. Cell Mol. Biol., 2011, 289, 1-35.
[40]
Yoo, J.O.; Lim, Y.C.; Kim, Y.M.; Ha, K.S. Differential cytotoxic responses to low- and high-dose photodynamic therapy in human gastric and bladder cancer cells. J. Cell. Biochem., 2011, 112(10), 3061-3071.
[41]
Christofferson, D.E.; Yuan, J. Necroptosis as an alternative form of programmed cell death. Curr. Opin. Cell Biol., 2010, 22(2), 263-268.
[42]
Saini, R.; Lee, N.V.; Liu, K.Y.; Poh, C.F. Prospects in the application of photodynamic therapy in oral cancer and premalignant lesions. Cancers, 2016, 8(9), 83.
[43]
Li, R.; Zhang, Y.; Mohamed, M.A.; Wei, X.; Cheng, C. Macrophages play an essential role in the long effects of low-dose photodynamic therapy on vessel permeability. Int. J. Biochem. Cell Biol., 2016, 71, 55-61.
[44]
Golstein, P.; Kroemer, G. Cell death by necrosis: Towards a molecular definition. Trends Biochem. Sci., 2007, 32(1), 37-43.
[45]
Harvey, E.H.; Webber, J.; Kessel, D.; Fromm, D. Killing tumor cells: the effect of photodynamic therapy using mono-L-aspartyl chlorine and NS-398. Am. Surg., 2005, 189(3), 302-305.
[46]
Ferrario, A.; Chantrain, C.F.; von Tiehl, K.; Buckley, S.; Rucker, N.; Shalinsky, D.R.; Shimada, H.; DeClerck, Y.A.; Gomer, C.J. The matrix metalloproteinase inhibitor prinomastat enhances photodynamic therapy responsiveness in a mouse tumor model. Cancer Res., 2004, 64(7), 2328-2332.
[47]
Wachowska, M.; Muchowicz, A.; Demkow, U. Immunological aspects of antitumor photodynamic therapy outcome. Cent. Eur. J. Immunol., 2015, 40(4), 481-485.
[48]
Kubiak, M.; Lysenko, L.; Gerber, H.; Nowak, R. Cell reactions and immune responses to photodynamic therapy in oncology. Postepy Hig. Med. Dosw., 2016, 70, 735-742.
[49]
de Vree, W.J.; Essers, M.C.; Koster, J.F.; Sluiter, W. Role of interleukin 1 and granulocyte colony-stimulating factor in photofrin-based photodynamic therapy of rat rhabdomyosarcoma tumors. Cancer Res., 1997, 57(13), 2555-2558.
[50]
Golab, J.; Wilczyński, G.; Zagozdzon, R.; Stokłosa, T.; Dabrowska, A.; Rybczyńska, J.; Wasik, M.; Machaj, E.; Ołda, T.; Kozar, K.; Kamiński, R.; Giermasz, A.; Czajka, A.; Lasek, W.; Feleszko, W.; Jakóbisiak, M. Potentiation of the anti-tumour effects of Photofrin-based photodynamic therapy by localized treatment with G-CSF. Br. J. Cancer, 2000, 82(8), 1485-1491.
[51]
Mroz, P.; Hamblin, M.R. The immunosuppressive side of PDT. Photochem. Photobiol. Sci., 2011, 10(5), 751-758.
[52]
Elmets, C.A.; Bowen, K.D. Immunological suppression in mice treated with hematoporphyrin derivative photoradiation. Cancer Res., 1986, 46(1), 1608-1611.
[53]
Yu, M.; Guo, F.; Wang, J.; Tan, F.; Li, N. Photosensitizer-loaded pH-responsive hollow gold nanospheres for single light-induced photothermal/photodynamic therapy. ACS Appl. Mater. Interfaces, 2015, 7(32), 17592-17597.
[54]
Gao, L.; Zhang, C.; Gao, D.; Liu, H.; Yu, X.; Lai, J.; Wang, F.; Lin, J.; Liu, Z. Enhanced anti-tumor efficacy through a combination of integrin alphavbeta6-targeted photodynamic therapy and immune checkpoint inhibition. Theranostics, 2016, 6(5), 627-637.
[55]
Maeding, N.; Verwanger, T.; Krammer, B. Boosting tumor-specific immunity using PDT. Cancers, 2016, 8(10)E91
[56]
Hani, U.; Osmani, R.A.; Bhosale, R.R.; Shivakumar, H.G.; Kulkarni, P.K. Current perspectives on novel drug delivery systems and approaches for management of cervical cancer: A comprehensive review. Curr. Drug Targets, 2016, 17(3), 337-352.
[57]
Huang, H.F.; Yan, X.; Guo, H.Q. Nanotechnology and photodynamic therapy of bladder cancer. J. Clin. Urol., 2010, 25(2), 158-160.
[58]
Li, W.; Tan, G.; Cheng, J. A novel photosensitizer 3(1),13(1)-Phenylhydrazine-mppa (BPHM) and its in vitro photodynamic therapy against HeLa cells. Molecules, 2016, 21(5), 557-568.
[59]
Li, P.X.; Mu, J.H.; Xiao, H.L.; Li, D.H. Antitumor effect of photodynamic therapy with a novel targeted photosensitizer on cervical carcinoma. Oncol. Rep., 2015, 33(1), 125-132.
[60]
Ferreira, D.P.; Conceição, D.S.; Fernandes, F.; Sousa, T.; Calhelha, R.C.; Ferreira, I.C.; Santos, P.F.; Vieira Ferreira, L.F. Characterization of a squaraine/chitosan system for photodynamic therapy of cancer. J. Phys. Chem. B, 2016, 120, 1212-1220.
[61]
Ahn, J.C.; Biswas, R.; Moon, J.H.; Chung, P.S. Cellular uptake of 9-hydroxypheophorbide-alpha and its photoactivation to induce ER stress-related apoptosis in human cervical cancer cells. Lasers Med. Sci., 2014, 29(1), 289-299.
[62]
Zhang, C.Y.; Zhang, L.J.; Li, J.W.; Li, J.H.; Wu, Z.M.; Zhang, L.X.; Chen, N.; Yan, Y.J.; Chen, Z.L. In vitro and in vivo antitumor activity of a novel chlorin derivative for photodynamic therapy. Neoplasma, 2016, 63(1), 37-43.
[63]
Saczko, J.; Skrzypek, W.; Chwiłkowska, A.; Choromańska, A.; Poła, A.; Gamian, A.; Kulbacka, J. Photo-oxidative action in cervix carcinoma cells induced by HPD - mediated photodynamic therapy. Exp. Oncol., 2009, 31(4), 195-199.
[64]
Lincoln, R.; Durantini, A.M.; Greene, L.E.; Martínez, S.R.; Knox, R.; Becerra, M.C.; Cosa, G. Meso-Acetoxymethyl BODIPY dyes for photodynamic therapy: Improved photostability of singlet oxygen photosensitizers. Photochem. Photobiol. Sci., 2017, 16(2), 178-184.
[65]
Hodgkinson, N.; Kruger, C.A.; Mokwena, M.; Abrahamse, H. Cervical cancer cells (HeLa) response to photodynamic therapy using a zinc phthalocyanine photosensitizer. J. Photochem. Photobiol. Bol. Biol., 2017, 177, 32-38.
[66]
Magalhaes, A.F.; Graca, V.C.; Calhelha, R.; Ferreira, I.; Santos, P. Aminosquaraines as potential photodynamic agents: Synthesis and evaluation of in vitro cytotoxicity. Bioorg. Med. Chem. Lett., 2017, 27(18), 4467-4470.
[67]
de Freitas, L.M.; Serafim, R.B.; de Sousa, J.F.; Moreira, T.F.; Dos Santos, C.T.; Baviera, A.M.; Valente, V.; Soares, C.P.; Fontana, C.R. Photodynamic therapy combined to cisplatin potentiates cell death responses of cervical cancer cells. BMC Cancer, 2017, 17(1), 123.
[68]
Ung, P.; Clerc, M.; Huang, H.; Qiu, K.; Chao, H.; Seitz, M.; Boyd, B.; Graham, B.; Gasser, G. Extending the excitation wavelength of potential photosensitizers via appendage of a kinetically stable terbium (III) macrocyclic complex for applications in photodynamic therapy. Inorg. Chem., 2017, 56(14), 7960-7974.
[69]
Wei, X.Q.; Ma, H.Q.; Liu, A.H.; Zhang, Y.Z. Synergistic anticancer activity of 5-aminolevulinic acid photodynamic therapy in combination with low-dose cisplatin on Hela cells. Asian Pac. J. Cancer Prev., 2013, 14(5), 3023-3028.
[70]
Villanueva, A.; Stockert, J.C.; Canete, M.; Acedo, P. A new protocol in photodynamic therapy: Enhanced tumour cell death by combining two different photosensitizers. Photochem. Photobiol. Sci., 2010, 9(3), 295-297.
[71]
Xie, Y.; Huang, G.W.; Huang, Y.Y. Photodynamic therapy with nanoparticles for cancer treatment: A review. Chinese J. Laser Med. Surg., 2009, 18(1), 55-58.
[72]
Xia, C.H.; Wang, B.Q.; Wang, Y. Research progress of photodynamic antitumor of nano-Ti02 photosensitizer. J. Qiqihaer Med. College, 2011, 32(12), 1975-1976.
[73]
Vega, D.L.; Lodge, P.; Vivero-Escoto, J.L. Redox-responsive porphyrin-based polysilsesquioxane nanoparticles for photodynamic therapy of cancer cells. Int. J. Mol. Sci., 2015, 17(1)E56
[74]
Wieder, M.E.; Hone, D.C.; Cook, M.J.; Handsley, M.M.; Gavrilovic, J.; Russell, D.A. Intracellular photodynamic therapy with photosensitizer-nanoparticle conjugates: Cancer therapy using a ‘Trojan horse’. Photochem. Photobiol. Sci., 2006, 5(8), 727-734.
[75]
Li, L.; Li, Y. Research progress of nanoparticles in photodynamic therapy. Dent. Health, 2016, 3(9), 253-254.
[76]
Matsumura, Y.; Maeda, H. A new concept for macromolecular therapeutics in cancer chemotherapy: Mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res., 1986, 46(12 Pt 1), 6387-6392.
[77]
Fang, J.; Nakamura, H.; Maeda, H. The EPR effect: Unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev., 2011, 63(3), 136-151.
[78]
Azzopardi, E.A.; Ferguson, E.L.; Thomas, D.W. The enhanced permeability retention effect: A new paradigm for drug targeting in infection. J. Antimicrob. Chemother., 2013, 68(2), 257-274.
[79]
Stylianopoulos, T.; Jain, R.K. Design considerations for nanotherapeutics in oncology. Nanomed. Nanotechnol. Biol. Med, 2015, 11(8), 1893-1907.
[80]
Butler, T.P.; Grantham, F.H.; Gullino, P.M. Bulk transfer of fluid in the interstitial compartment of mammary tumors. Cancer Res., 1975, 35(11 Pt 1), 3084-3088.
[81]
Jain, R.K. Normalizing tumor microenvironment to treat cancer: Bench to bedside to biomarkers. J. Clin. Oncol., 2013, 31(17), 2205-2218.
[82]
Torchilin, V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv. Drug Deliv. Rev., 2011, 63(3), 131-135.
[83]
Prabhakar, U.; Maeda, H.; Jain, R.K.; Sevick-Muraca, E.M.; Zamboni, W.; Farokhzad, O.C.; Barry, S.T.; Gabizon, A.; Grodzinski, P.; Blakey, D.C. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res., 2013, 73(8), 2412-2417.
[84]
Maeda, H.; Nakamura, H.; Fang, J. The EPR effect for macromolecular drug delivery to solid tumors: Improvement of tumor uptake, lowering of systemic toxicity, and distinct tumor imaging in vivo. Adv. Drug Deliv. Rev., 2013, 65(1), 71-79.
[85]
Hashizume, H.; Baluk, P.; Morikawa, S.; McLean, J.W.; Thurston, G.; Roberge, S.; Jain, R.K.; McDonald, D.M. Openings between defective endothelial cells explain tumor vessel leakiness. Am. J. Pathol., 2000, 156(4), 1363-1380.
[86]
Gindy, M.E.; Prud’homme, R.K. Multifunctional nanoparticles for imaging, delivery and targeting in cancer therapy. Expert Opin. Drug Deliv., 2009, 6(8), 865-878.
[87]
Kim, K.; Kim, J.H.; Park, H.; Kim, Y.S.; Park, K.; Nam, H.; Lee, S.; Park, J.H.; Park, R.W.; Kim, I.S.; Choi, K.; Kim, S.Y.; Park, K.; Kwon, I.C. Tumor-homing multifunctional nanoparticles for cancer theragnosis: Simultaneous diagnosis, drug delivery, and therapeutic monitoring. J. Control. Release, 2010, 146(2), 219-227.
[88]
Harrington, K.J.; Mohammadtaghi, S.; Uster, P.S.; Glass, D.; Peters, A.M.; Vile, R.G.; Stewart, J.S. Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes. Clin. Cancer Res., 2001, 7(2), 243-254.
[89]
Tanaka, N.; Kanatani, S.; Tomer, R.; Sahlgren, C.; Kronqvist, P.; Kaczynska, D.; Louhivuori, L.; Kis, L.; Lindh, C.; Mitura, P.; Stepulak, A.; Corvigno, S.; Hartman, J.; Micke, P.; Mezheyeuski, A.; Strell, C.; Carlson, J.W.; Fernández Moro, C.; Dahlstrand, H.; Östman, A.; Matsumoto, K.; Wiklund, P.; Oya, M.; Miyakawa, A.; Deisseroth, K.; Uhlén, P. Whole tissue biopsy phenotyping of three-dimensional tumours reveals patterns of cancer heterogeneity. Nat. Biomed. Eng., 2017, 1, 796-806.
[90]
Ellahioui, Y.; Patra, M.; Mari, C. Mesoporous silica nanoparticles functionalised with a photoactive ruthenium(ii) complex: Exploring the formulation of a metal-based photodynamic therapy photosensitiser. Dalton Trans., 2018, 48(18), 5940-5951.
[91]
Ikeda, A.; Doi, Y.; Nishiguchi, K.; Kitamura, K.; Hashizume, M.; Kikuchi, J.; Yogo, K.; Ogawa, T.; Takeya, T. Induction of cell death by photodynamic therapy with water-soluble lipid-membrane-incorporated [60]fullerene. Org. Biomol. Chem., 2007, 5(8), 1158-1160.
[92]
Flak, D.; Yate, L.; Nowaczyk, G.; Jurga, S. Hybrid ZnPc@TiO2 nanostructures for targeted photodynamic therapy, bioimaging and doxorubicin delivery. Mater. Sci. Eng. C Mater. Biol. Appl., 2017, 78, 1072-1085.
[93]
Akiyama, M.; Ikeda, A.; Shintani, T.; Doi, Y.; Kikuchi, J.; Ogawa, T.; Yogo, K.; Takeya, T.; Yamamoto, N. Solubilisation of [60]fullerenes using block copolymers and evaluation of their photodynamic activities. Org. Biomol. Chem., 2008, 6(6), 1015-1019.
[94]
Benito, M.; Martin, V.; Blanco, M.D.; Teijon, J.M.; Gomez, C. Cooperative effect of 5-aminolevulinic acid and gold nanoparticles for photodynamic therapy of cancer. J. Pharm. Sci., 2013, 102(8), 2760-2769.
[95]
Ai, J.; Xu, Y.; Lou, B.; Li, D.; Wang, E. Multifunctional AS1411-functionalized fluorescent gold nanoparticles for targeted cancer cell imaging and efficient photodynamic therapy. Talanta, 2014, 118, 54-60.
[96]
Yu, J.; Hsu, C.H.; Huang, C.C.; Chang, P.Y. Development of therapeutic Au-methylene blue nanoparticles for targeted photodynamic therapy of cervical cancer cells. ACS Appl. Mater. Interfaces, 2015, 7(1), 432-441.
[97]
Barras, A.; Boussekey, L.; Courtade, E.; Boukherroub, R. Hypericin-loaded lipid nanocapsules for photodynamic cancer therapy in vitro. Nanoscale, 2013, 5(21), 10562-10572.
[98]
Jain, R.K.; Stylianopoulos, T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol., 2010, 7(11), 653-664.
[99]
Shi, L.; Wang, X.L.; Wang, H.W. Application of nanoparticle vectors in photodynamic therapy of tumors. J. Int. Oncol., 2012, 39(3), 193-196.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy