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pharmaceutics Article Highly Red Light-Emitting Erbium- and Lutetium-Doped Core-Shell Upconverting Nanoparticles Surface-Modified with PEG-Folic Acid/TCPP for Suppressing Cervical Cancer HeLa Cells Kyungseop Lim 1, Hwang Kyung Kim 1 , Xuan Thien Le 1, Nguyen Thi Nguyen 1, Eun Seong Lee 2 , Kyung Taek Oh 3, Han-Gon Choi 4 and Yu Seok Youn 1,* 1 2 3 4 * Correspondence: ysyoun@skku.edu; Tel.: +82-31-290-7785 Received: 20 October 2020; Accepted: 13 November 2020; Published: 17 November 2020 School of Pharmacy, Sungkyunkwan University, 2066 Seobu-ro, Jangan-gu, Suwon, Gyeonggi-do 16419, Korea; imkyung424@naver.com (K.L.); hkkim0319@naver.com (H.K.K.); lexuanthien.dkh@gmail.com (X.T.L.); ngtnguyen1710@gmail.com (N.T.N.) Division of Biotechnology, The Catholic University of Korea, 43 Jibong-ro, Bucheon, Gyeonggi-do 14662, Korea; eslee@catholic.ac.kr College of Pharmacy, Chung-Ang University, 84 Heukseok-ro, Dongjak-gu, Seoul 06974, Korea; kyungoh@cau.ac.kr College of Pharmacy, Hanyang University, 55 Hanyangdaehak-ro, Sangnok-gu, Ansan 15588, Korea; hangon@hanyang.ac.kr Abstract: Photodynamic therapy (PDT) combined with upconverting nanoparticles (UCNPs) are viewed together as an effective method of ablating tumors. After absorbing highly tissue-penetrating near-infrared (NIR) light, UCNPs emit a shorter wavelength light (~660 nm) suitable for PDT. In this study, we designed and prepared highly red fluorescence-emitting silica-coated core-shell upconverting nanoparticles modified with polyethylene glycol (PEG5k)-folic acid and tetrakis(4-carboxyphenyl)porphyrin (TCPP) (UCNPs@SiO2-NH2@FA/PEG/TCPP) as an efficient photodynamic agent for killing tumor cells. The UCNPs consisted of two simple lanthanides, erbium and lutetium, as the core and shell, respectively. The unique core-shell combination enabled the UCNPs to emit red light without green light. TCPP, folic acid, and PEG were conjugated to the outer silica layer of UCNPs as a photosensitizing agent, a ligand for tumor attachment, and a dispersing stabilizer, respectively. The prepared UCNPs of ~50 nm diameter and −34.5 mV surface potential absorbed 808 nm light and emitted ~660 nm red light. Most notably, these UCNPs were physically well dispersed and stable in the aqueous phase due to PEG attachment and were able to generate singlet oxygen (1O2) with a high efficacy. The HeLa cells were treated with each UCNP sample (0, 1, 5, 10, 20, 30 μg/mL as a free TCPP). The results showed that the combination of UCNPs@SiO2-NH2@FA/PEG/TCPP and the 808 nm laser was significantly cytotoxic to HeLa cells, almost to the same degree as naïve TCPP plus the 660 nm laser based on MTT and Live/Dead assays. Furthermore, the UCNPs@SiO2-NH2@FA/PEG/TCPP was well internalized into HeLa cells and three-dimensional HeLa spheroids, presumably due to the surface folic acid and small size in conjunction with endocytosis and the nonspecific uptake. We believe that our UCNPs@SiO2-NH2@FA/PEG/TCPP will serve as a new platform for highly efficient and deep-penetrating photodynamic agents suitable for various tumor treatments. Keywords: upconverting nanoparticles; photodynamic therapy; tetrakis(4-carboxy-phenyl)porphyrin; near infrared; cancer; hypoxia Pharmaceutics 2020, 12, 1102; doi:10.3390/pharmaceutics12111102 www.mdpi.com/journal/pharmaceuticsPDF Image | Red LED Erbium Upconverting Nanoparticles v Cervical Cancer
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