Triazine–Carbosilane Dendrimersomes Enhance Cellular Uptake and Phototoxic Activity of Rose Bengal in Basal Cell Skin Carcinoma Cells

References

• Basset-Seguin N, Herms F. Update on the management of basal cell carcinoma. Acta Derm Venereol. 2020;100(11):284–290. doi:10.2340/00015555-3495
   Web of Science ®Google Scholar
• Olivo M, Bhuvaneswari R, Lucky SS, Dendukuri N, Thong PSP. Targeted therapy of cancer using photodynamic therapy in combination with multi-faceted anti-tumor modalities. Pharmaceuticals. 2010;3(5):1507–1529. doi:10.3390/ph3051507
   Google Scholar
• Kucinska M, Skupin-Mrugalska P, Szczolko W, et al. Phthalocyanine derivatives possessing 2-(morpholin-4-yl) ethoxy groups as potential agents for photodynamic therapy. J Med Chem. 2015;58(5):2240–2255. doi:10.1021/acs.jmedchem.5b00052
   PubMed Web of Science ®Google Scholar
• Sztandera K, Gorzkiewicz M, Klajnert-Maculewicz B. Nanocarriers in photodynamic therapy—in vitro and in vivo studies. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2020;12(3):1–24. doi:10.1002/wnan.1599
   Web of Science ®Google Scholar
• Pham TC, Nguyen VN, Choi Y, Lee S, Yoon J. Recent strategies to develop innovative photosensitizers for enhanced photodynamic therapy. Chem Rev. 2021;121(21):13454–13619. doi:10.1021/acs.chemrev.1c00381
   PubMed Web of Science ®Google Scholar
• Redmond RW, Gamlin JN. A compilation of singlet oxygen yields from biologically relevant molecules. Photochem Photobiol. 1999;70(4):391–475. doi:10.1111/j.1751-1097.1999.tb08240.x
   PubMed Web of Science ®Google Scholar
• Vanerio N, Stijnen M, De Mol BAJM, Kock LM. Biomedical applications of photo- and sono-activated rose bengal: a review. Photobiomodulation Photomed Laser Surg. 2019;37(7):383–394. doi:10.1089/photob.2018.4604
   PubMed Web of Science ®Google Scholar
• Demartis S, Obinu A, Gavini E, Giunchedi P, Rassu G. Nanotechnology-based rose Bengal: a broad-spectrum biomedical tool. Dye Pigment. 2021;188:109236. doi:10.1016/j.dyepig.2021.109236
   Web of Science ®Google Scholar
• Qidwai A, Annu NB. Role of nanocarriers in photodynamic therapy. Photodiagnosis Photodyn Ther. 2020;30:101782. doi:10.1016/j.pdpdt.2020.101782
   PubMed Web of Science ®Google Scholar
• Xie J, Wang Y, Choi W, et al. Overcoming barriers in photodynamic therapy harnessing nano-formulation strategies. Chem Soc Rev. 2021;50(16):9152–9201. doi:10.1039/d0cs01370f
   PubMed Web of Science ®Google Scholar
• Antimisiaris SG, Marazioti A, Kannavou M, et al. Overcoming barriers by local drug delivery with liposomes. Adv Drug Deliv Rev. 2021;174:53–86. doi:10.1016/j.addr.2021.01.019
   PubMed Web of Science ®Google Scholar
• Ghaffari M, Dehghan G, Baradaran B, et al. Co-delivery of curcumin and Bcl-2 siRNA by PAMAM dendrimers for enhancement of the therapeutic efficacy in HeLa cancer cells. Colloids Surf B Biointerfaces. 2020;188:110762. doi:10.1016/j.colsurfb.2019.110762
   PubMed Web of Science ®Google Scholar
• Duncan R, Izzo L. Dendrimer biocompatibility and toxicity. Adv Drug Deliv Rev. 2005;57(15):2215–2237. doi:10.1016/j.addr.2005.09.019
   PubMed Web of Science ®Google Scholar
• Tripathi PK, Tripathi S. Dendrimers for anticancer drug delivery. Pharm Appl Dendrimers. 2019;4:131–150.
   Google Scholar
• Sztandera K, Gorzkiewicz M, Dias Martins AS, et al. Noncovalent interactions with PAMAM and PPI dendrimers promote the cellular uptake and photodynamic activity of rose bengal: the role of the dendrimer structure. J Med Chem. 2021;64(21):15758–15771. doi:10.1021/acs.jmedchem.1c01080
   PubMed Web of Science ®Google Scholar
• Zhou D, Fei Z, Jin L, et al. Dual-responsive polymersomes as anticancer drug carriers for the co-delivery of doxorubicin and paclitaxel. J Mater Chem B. 2021;9(3):801–808. doi:10.1039/D0TB02462G
   PubMed Web of Science ®Google Scholar
• Laskar P, Dufès C. Emergence of cationic polyamine dendrimersomes: design, stimuli sensitivity and potential biomedical applications. Nanoscale Adv. 2021;3(21):6007–6026. doi:10.1039/D1NA00536G
   PubMed Web of Science ®Google Scholar
• Laskar P, Somani S, Campbell SJ, et al. Camptothecin-based dendrimersomes for gene delivery and redox-responsive drug delivery to cancer cells. Nanoscale. 2019;11(42):20058–20071. doi:10.1039/C9NR07254C
   PubMed Web of Science ®Google Scholar
• Laskar P, Somani S, Altwaijry N, et al. Redox-sensitive, cholesterol-bearing PEGylated poly (propylene imine)-based dendrimersomes for drug and gene delivery to cancer cells. Nanoscale. 2018;10(48):22830–22847. doi:10.1039/C8NR08141G
   PubMed Web of Science ®Google Scholar
• Apartsin E, Knauer N, Arkhipova V, et al. pH-sensitive dendrimersomes of hybrid triazine-carbosilane dendritic amphiphiles-smart vehicles for drug delivery. Nanomaterials. 2020;10(10):1899. doi:10.3390/nano10101899
   Web of Science ®Google Scholar
• Percec V, Wilson DA, Leowanawat P, et al. Self-assembly of janus dendrimers into uniform dendrimersomes and other complex architectures. Science (80-). 2010;328(5981):1009–1014. doi:10.1126/science.1185547
   PubMed Web of Science ®Google Scholar
• Hu FF, Sun YW, Zhu YL, Huang YN, Li ZW, Sun ZY. Enthalpy-driven self-assembly of amphiphilic Janus dendrimers into onion-like vesicles: a Janus particle model. Nanoscale. 2019;11(37):17350–17356. doi:10.1039/C9NR05885K
   PubMed Web of Science ®Google Scholar
• Estrella V, Chen T, Lloyd M, et al. Acidity generated by the tumor microenvironment drives local invasion. Cancer Res. 2013;73(5):1524–1535. doi:10.1158/0008-5472.CAN-12-2796
   PubMed Web of Science ®Google Scholar
• Fuentes-Paniagua E, Peña-González CE, Galán M, Gómez R, De La Mata FJ, Sánchez-Nieves J. Thiol-ene synthesis of cationic carbosilane dendrons: a new family of synthons. Organometallics. 2013;32(6):1789–1796. doi:10.1021/om301217g
   Web of Science ®Google Scholar
• Jones OT, Ranmuthu CKI, Hall PN, Funston G, Walter FM. Recognising skin cancer in primary care. Adv Ther. 2020;37(1):603–616. doi:10.1007/s12325-019-01130-1
   PubMed Web of Science ®Google Scholar
• Dabrzalska M, Janaszewska A, Zablocka M, Mignani S, Majoral JP, Klajnert-Maculewicz B. Complexing methylene blue with phosphorus dendrimers to increase photodynamic activity. Molecules. 2017;22(3). doi:10.3390/molecules22030345
   PubMed Web of Science ®Google Scholar
• Lutkus LV, Rickenbach SS, McCormick TM. Singlet oxygen quantum yields determined by oxygen consumption. J Photochem Photobiol a Chem. 2019;378:131–135. doi:10.1016/j.jphotochem.2019.04.029
   Web of Science ®Google Scholar
• Demartis S, Rassu G, Murgia S, Casula L, Giunchedi P, Gavini E. Improving dermal delivery of rose bengal by deformable lipid nanovesicles for topical treatment of melanoma. Mol Pharm. 2021;18(11):4046–4057. doi:10.1021/acs.molpharmaceut.1c00468
   PubMed Web of Science ®Google Scholar
• Ali MFM. Topical delivery and photodynamic evaluation of a multivesicular liposomal Rose Bengal. Lasers Med Sci. 2011;26(2):267–275. doi:10.1007/s10103-010-0859-9
   PubMed Web of Science ®Google Scholar
• Forouz F, Dabbaghi M, Namjoshi S, Mohammed Y, Roberts MS, Grice JE. Development of an oil-in-water self-emulsifying microemulsion for cutaneous delivery of rose Bengal: investigation of anti-melanoma properties. Pharmaceutics. 2020;12(10):1–17. doi:10.3390/pharmaceutics12100947
   Web of Science ®Google Scholar
• Torres-Martínez A, Bedrina B, Falomir E, et al. Non-polymeric nanogels as versatile nanocarriers: intracellular transport of the photosensitizers rose bengal and hypericin for photodynamic therapy. ACS Appl Bio Mater. 2021;4(4):3658–3669. doi:10.1021/acsabm.1c00139
   PubMedGoogle Scholar
• Yeh HP, Del Valle AC, Syu MC, Qian Y, Chang YC, Huang YF. A new photosensitized oxidation-responsive nanoplatform for controlled drug release and photodynamic cancer therapy. ACS Appl Mater Interfaces. 2018;10(25):21160–21172. doi:10.1021/acsami.8b05205
   PubMed Web of Science ®Google Scholar
• Yan Y, Li J, Zheng J, et al. Poly (l-lysine)-based star-block copolymers as pH-responsive nanocarriers for anionic drugs. Colloids Surf B Biointerfaces. 2012;95:137–143. doi:10.1016/j.colsurfb.2012.02.034
   PubMed Web of Science ®Google Scholar
• Wang HY, Hou L, Li HL, et al. A nanosystem loaded with perfluorohexane and rose bengal coupled upconversion nanoparticles for multimodal imaging and synergetic chemo-photodynamic therapy of cancer. Biomater Sci. 2020;8(9):2488–2506. doi:10.1039/C9BM02081K
   PubMed Web of Science ®Google Scholar
• Han S, Hwang BW, Jeon EY, et al. Upconversion nanoparticles/hyaluronate-rose bengal conjugate complex for noninvasive photochemical tissue bonding. ACS Nano. 2017;11(10):9979–9988. doi:10.1021/acsnano.7b04153
   PubMed Web of Science ®Google Scholar
• Chen K, Chang C, Liu Z, et al. Hyaluronic acid targeted and pH-responsive nanocarriers based on hollow mesoporous silica nanoparticles for chemo-photodynamic combination therapy. Colloids Surf B Biointerfaces. 2020;194:111166. doi:10.1016/j.colsurfb.2020.111166
   PubMed Web of Science ®Google Scholar
• Mignani S, Rodrigues J, Roy R, et al. Exploration of biomedical dendrimer space based on in-vivo physicochemical parameters: key factor analysis (Part 2). Drug Discov Today. 2019;24(5):1184–1192. doi:10.1016/j.drudis.2019.03.001
   PubMed Web of Science ®Google Scholar
• Dias AP, da Silva Santos S, da Silva JV, et al. Dendrimers in the context of nanoMedicine. Int J Pharm. 2020;5:573.
   Google Scholar
• Sandoval-Yañez C, Rodriguez CC. Dendrimers: amazing platforms for bioactive molecule delivery systems. Materials. 2020;13(3):570. doi:10.3390/ma13030570
   PubMed Web of Science ®Google Scholar
• Bolu BS, Sanyal R, Sanyal A. Drug delivery systems from self-assembly of dendron-polymer conjugates. Molecules. 2018;23(7):1570. doi:10.3390/molecules23071570
   PubMed Web of Science ®Google Scholar
• Mendes LP, Pan J, Torchilin VP. Dendrimers as nanocarriers for nucleic acid and drug delivery in cancer therapy. Molecules. 2017;22(9):1401. doi:10.3390/molecules22091401
   PubMed Web of Science ®Google Scholar
• Dzmitruk V, Apartsin E, Ihnatsyeu-Kachan A, Abashkin V, Shcharbin D, Bryszewska M. Dendrimers show promise for siRNA and microRNA therapeutics. Pharmaceutics. 2018;10(3):126. doi:10.3390/pharmaceutics10030126
   PubMed Web of Science ®Google Scholar
• Knauer N, Pashkina E, Apartsin E. Topological aspects of the design of nanocarriers for therapeutic peptides and proteins. Pharmaceutics. 2019;11(2):91. doi:10.3390/pharmaceutics11020091
   PubMed Web of Science ®Google Scholar
• Peterca M, Percec V, Leowanawat P, Bertin A. Predicting the size and properties of dendrimersomes from the lamellar structure of their amphiphilic janus dendrimers. J Am Chem Soc. 2011;133(50):20507–20520. doi:10.1021/ja208762u
   PubMed Web of Science ®Google Scholar
• Apartsin E, Caminade AM. Supramolecular self-associations of amphiphilic dendrons and their properties. Chem – a Eur J. 2021;27(72):17976–17998. doi:10.1002/chem.202102589
   PubMed Web of Science ®Google Scholar
• Fernandez J, Acosta G, Pulido D, et al. Carbosilane dendron-peptide nanoconjugates as antimicrobial agents. Mol Pharm. 2019;16(6):2661–2674. doi:10.1021/acs.molpharmaceut.9b00222
   PubMed Web of Science ®Google Scholar
• Sepúlveda-Crespo D, De La Mata FJ, Gómez R, Muñoz-Fernández MA. Sulfonate-ended carbosilane dendrimers with a flexible scaffold cause inactivation of HIV-1 virions and gp120 shedding. Nanoscale. 2018;10(19):8998–9011. doi:10.1039/C8NR01664J
   PubMed Web of Science ®Google Scholar
• Krasheninina OA, Apartsin EK, Fuentes E, et al. Complexes of pro-apoptotic siRNAs and carbosilane dendrimers: formation and effect on cancer cells. Pharmaceutics. 2019;11(1):25. doi:10.3390/pharmaceutics11010025
   PubMed Web of Science ®Google Scholar
• Sánchez-Milla M, Muñoz-Moreno L, Sánchez-Nieves J, et al. Anticancer activity of dendriplexes against advanced prostate cancer from protumoral peptides and cationic carbosilane dendrimers. Biomacromolecules. 2019;20(3):1224–1234. doi:10.1021/acs.biomac.8b01632
   PubMed Web of Science ®Google Scholar
• Carloni R, Del Olmo NS, Ortega P, et al. Exploring the interactions of ruthenium (II) carbosilane metallodendrimers and precursors with model cell membranes through a dual spin-label spin-probe technique using EPR. Biomolecules. 2019;9(10):540. doi:10.3390/biom9100540
   PubMed Web of Science ®Google Scholar
• Gutierrez-Ulloa CE, Buyanova MY, Apartsin EK, Venyaminova AG, de la Mata FJ, Gómez R. Carbon nanotubes decorated with cationic carbosilane dendrons and their hybrids with nucleic acids. ChemNanoMat. 2018;4(2):220–230. doi:10.1002/cnma.201700351
   Web of Science ®Google Scholar
• Pędziwiatr-Werbicka E, Gorzkiewicz M, Horodecka K, et al. Silver nanoparticles surface-modified with carbosilane dendrons as carriers of anticancer siRNA. Int J Mol Sci. 2020;21(13):1–17. doi:10.3390/ijms21134647
   Web of Science ®Google Scholar
• González-García E, Gutiérrez Ulloa CE, de la Mata FJ, Marina ML, García MC. Sulfonate-terminated carbosilane dendron-coated nanotubes: a greener point of view in protein sample preparation. Anal Bioanal Chem. 2017;409(22):5337–5348. doi:10.1007/s00216-017-0479-3
   PubMed Web of Science ®Google Scholar
• Gutierrez-Ulloa CE, Buyanova MY, Apartsin EK, et al. Amphiphilic carbosilane dendrons as a novel synthetic platform toward micelle formation. Org Biomol Chem. 2017;15(35):7352–7364. doi:10.1039/C7OB01331K
   PubMed Web of Science ®Google Scholar
• Mencia G, Lozano-Cruz T, Valiente M, de la Mata J, Cano J, Gómez R. New ionic carbosilane dendrons possessing fluorinated tails at different locations on the skeleton. Molecules. 2020;25(4):807. doi:10.3390/molecules25040807
   PubMed Web of Science ®Google Scholar
• Mencia G, Lozano-Cruz T, Valiente M, et al. Evaluation of pH-dependent amphiphilic carbosilane dendrons in micelle formation, drug loading and HIV-1 infection. Org Biomol Chem. 2020;18(47):9639–9652. doi:10.1039/D0OB01867H
   PubMed Web of Science ®Google Scholar
• Filippi M, Catanzaro V, Patrucco D, Botta M, Tei L, Terreno E. First in vivo MRI study on theranostic dendrimersomes. J Control Release. 2017;248:45–52. doi:10.1016/j.jconrel.2017.01.010
   PubMed Web of Science ®Google Scholar
• Haba Y, Harada A, Takagishi T, Kono K. Synthesis of biocompatible dendrimers with a peripheral network formed by linking of polymerizable groups. Polymer. 2005;46(6):1813–1820. doi:10.1016/j.polymer.2005.01.004
   Web of Science ®Google Scholar
• Dabrzalska M, Zablocka M, Mignani S, Majoral JP, Klajnert-Maculewicz B. Phosphorus dendrimers and photodynamic therapy. Spectroscopic studies on two dendrimer-photosensitizer complexes: cationic phosphorus dendrimer with rose bengal and anionic phosphorus dendrimer with methylene blue. Int J Pharm. 2015;492(1–2):266–274. doi:10.1016/j.ijpharm.2015.06.014
   PubMed Web of Science ®Google Scholar
• Fröhlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomedicine. 2012;7:5577–5591. doi:10.2147/IJN.S36111
   PubMed Web of Science ®Google Scholar
• Dabrzalska M, Janaszewska A, Zablocka M, Mignani S, Majoral JP, Klajnert-Maculewicz B. Cationic phosphorus dendrimer enhances photodynamic activity of rose bengal against basal cell carcinoma cell lines. Mol Pharm. 2017;14(5):1821–1830. doi:10.1021/acs.molpharmaceut.7b00108
   PubMed Web of Science ®Google Scholar
• Gorzkiewicz M, Klajnert-Maculewicz B. Chapter 10 in dendrimers for drug delivery. In: Sharma A, Keservan R, editors. Dendrimers as Nanocarriers for Anticancer Drugs. Apple Academic Press; 2018:327–374.
   Google Scholar
• Honary S, Zahir F. Effect of zeta potential on the properties of nano-drug delivery systems - A review (Part 1 and 2). Trop J Pharm Res. 2013;12(2):255–264.
   Web of Science ®Google Scholar
• Gorzkiewicz M, Deriu MA, Studzian M, et al. Fludarabine-specific molecular interactions with maltose-modified poly (propyleneimine) dendrimer enable effective cell entry of the active drug form: comparison with clofarabine. Biomacromolecules. 2019;20(3):1429–1442. doi:10.1021/acs.biomac.9b00010
   PubMed Web of Science ®Google Scholar
• Fox LJ, Richardson RM, Briscoe WH. PAMAM dendrimer - cell membrane interactions. Adv Colloid Interface Sci. 2018;257:1–18. doi:10.1016/j.cis.2018.06.005
   PubMed Web of Science ®Google Scholar
• Hong S, Leroueil PR, Janus EK, et al. Interaction of polycationic polymers with supported lipid bilayers and cells: nanoscale hole formation and enhanced membrane permeability. Bioconjug Chem. 2006;17(3):728–734. doi:10.1021/bc060077y
   PubMed Web of Science ®Google Scholar