A Nano Approach to Formulate Photosensitizers for Photodynamic
Therapy

Pragya       Pallavi; Palani       Sharmiladevi; Viswanathan       Haribabu; Koyeli       Girigoswami; Agnishwar       Girigoswami
Abstract

Conventional treatment modalities for tumors face a variety of pitfalls, including nonspecific interactions leading to multiple adverse effects. These adverse effects are being overcome through innovations that are highly intense and selective delivery of therapeutic agents. More recently, Photodynamic therapy (PDT) has gained its value over conventional chemo- and radiotherapies due to the use of photosensitizers (PS) with an illuminating light source. Photosensitizers have crossed three generations with Photofrin being the first clinically approved PS for PDT. Even though these PS have proved to have cytotoxic effects against tumor cells, they suffer the selective distribution and concentration into the tumor sites that are deeply localized. To overcome these disadvantages, nanoformulations are currently being employed due to their unmatched physicochemical and surface properties. These nanoformulations include the encapsulation of PS acting as a nanocarrier for the PS or the functionalization of PS onto the surface of nanoparticles. The design of such nanoformulations involved in PDT is critical and valuable to consider. Along with PDT, several multifunctional approaches are being uplifted in the current trend where combined therapy and diagnosis are of great importance. Furthermore, targeted, selective, and specific delivery of the PS-loaded nanoformulations with receptor- mediated endocytosis is of interest to achieve better internalization into the tumor site. ROS generation with the interaction of PS augments cell death mechanisms exhibited due to PDT, leading to the immunogenic response that further results in an adaptive immune memory that prevents recurrence of tumor metastasis. Therefore, this review concentrates on the mechanisms of PDT, examples of nanocarriers and nanoparticles that are employed in PDT, combined therapies, and theranostics with PDT. Moreover, molecular mechanisms of nano-based PDT agents in killing tumor sites and designing considerations for better PDT outcomes have been discussed.
Keywords: Nanoformulations, photodynamic therapy, PDT, photosensitizers, nano-based carriers, chemotherapy.
Graphical Abstract

[1] 
Baumann, M.; Krause, M.; Overgaard, J.; Debus, J.; Bentzen, S.M.; Daartz, J.; Richter, C.; Zips, D.; Bortfeld, T. Radiation oncology in the era of precision medicine. Nat. Rev. Cancer,  2016, 16(4), 234-249.
[http://dx.doi.org/10.1038/nrc.2016.18] [PMID: 27009394] 
[2] 
Vimaladevi, M.; Divya, K.C.; Girigoswami, A. Liposomal nanoformulations of rhodamine for targeted photodynamic inactivation of mul-tidrug resistant gram negative bacteria in sewage treatment plant. J. Photochem. Photobiol. B,  2016, 162, 146-152.
[http://dx.doi.org/10.1016/j.jphotobiol.2016.06.034] [PMID: 27371913] 
[3] 
Camerin, M.; Magaraggia, M.; Soncin, M.; Jori, G.; Moreno, M.; Chambrier, I.; Cook, M.J.; Russell, D.A. The in vivo efficacy of phthalo-cyanine-nanoparticle conjugates for the photodynamic therapy of amelanotic melanoma. Eur. J. Cancer,  2010, 46(10), 1910-1918.
[http://dx.doi.org/10.1016/j.ejca.2010.02.037] [PMID: 20356732] 
[4] 
Konan, Y.N.; Gurny, R.; Allémann, E. State of the art in the delivery of photosensitizers for photodynamic therapy. J. Photochem. Photobiol. B,  2002, 66(2), 89-106.
[http://dx.doi.org/10.1016/S1011-1344(01)00267-6] [PMID: 11897509] 
[5] 
Nowis, D.; Makowski, M. Stokłosa, T.; Legat, M.; Issat, T.; Gołab, J. Direct tumor damage mechanisms of photodynamic therapy. Acta Biochim. Pol.,  2005, 52(2), 339-352.
[http://dx.doi.org/10.18388/abp.2005_3447] [PMID: 15990919] 
[6] 
Sanabria, L.M.; Rodríguez, M.E.; Cogno, I.S.; Vittar, N.B.R.; Pansa, M.F.; Lamberti, M.J.; Rivarola, V.A. Direct and indirect photodynamic therapy effects on the cellular and molecular components of the tumor microenvironment. Biochimica et Biophysica Acta (BBA)-. Rev. Can.,  2013, 1835, 36-45.
[7] 
Krammer, B. Vascular effects of photodynamic therapy. Anticancer Res.,  2001, 21(6B), 4271-4277.
[PMID: 11908681] 
[8] 
Vanciková, Z. Principles of the photodynamic therapy and its impact on the immune system. Sb. Lek.,  1998, 99(1), 1-11.
[PMID: 9748793] 
[9] 
Nowis, D. Stokłosa, T.; Legat, M.; Issat, T.; Jakóbisiak, M.; Gołąb, J. The influence of photodynamic therapy on the immune response. Photodiagn. Photodyn. Ther.,  2005, 2(4), 283-298.
[http://dx.doi.org/10.1016/S1572-1000(05)00098-0] [PMID: 25048870] 
[10] 
Li, L.; Huh, K.M. Polymeric nanocarrier systems for photodynamic therapy. Biomater. Res.,  2014, 18, 19.
[http://dx.doi.org/10.1186/2055-7124-18-19] [PMID: 26331070] 
[11] 
Niedre, M.; Patterson, M.S.; Wilson, B.C. Direct near-infrared luminescence detection of singlet oxygen generated by photodynamic thera-py in cells in vitro and tissues in vivo. Photochem. Photobiol.,  2002, 75(4), 382-391.
[http://dx.doi.org/10.1562/0031-8655(2002)0750382DNILDO2.0.CO2] [PMID: 12003128] 
[12] 
Moan, J.; Berg, K. The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol.,  1991, 53(4), 549-553.
[http://dx.doi.org/10.1111/j.1751-1097.1991.tb03669.x] [PMID: 1830395] 
[13] 
Isaguliants, M.G.; Bartosch, B.; Ivanov, A.V. Redox biology of infection and consequent disease. Oxidative medicine and cellular longevity,  2020, 2020, 5829521.
[http://dx.doi.org/10.1155/2020/5829521] 
[14] 
Yaraki, M.T.; Wu, M.; Middha, E.; Wu, W.; Rezaei, S.D.; Liu, B.; Tan, Y.N. Gold nanostars-AIE theranostic nanodots with enhanced fluo-rescence and photosensitization towards effective image-guided photodynamic therapy. Nano-Micro Lett.,  2021, 13, 1-15.
[15] 
Tavakkoli Yaraki, M.; Daqiqeh Rezaei, S.; Middha, E.; Tan, Y.N. Synthesis and simulation study of right silver bipyramids via seed‐mediated growth cum selective oxidative etching approach. Part. Part. Syst. Charact.,  2020, 37, 2000027.
[http://dx.doi.org/10.1002/ppsc.202000027] 
[16] 
Yaraki, M.T.; Pan, Y.; Hu, F.; Yu, Y.; Liu, B.; Tan, Y.N. Nanosilver-enhanced AIE photosensitizer for simultaneous bioimaging and pho-todynamic therapy. Mater. Chem. Front.,  2020, 4, 3074-3085.
[http://dx.doi.org/10.1039/D0QM00469C] 
[17] 
Yaraki, M.T.; Hu, F.; Rezaei, S.D.; Liu, B.; Tan, Y.N. Metal-enhancement study of dual functional photosensitizers with aggregation-induced emission and singlet oxygen generation. Nanoscale Adv.,  2020, 2, 2859-2869.
[http://dx.doi.org/10.1039/D0NA00182A] 
[18] 
Yaraki, T.M.; Rezaei, D.S.; Tan, Y.N. Simulation guided design of silver nanostructures for plasmon-enhanced fluorescence, singlet oxy-gen generation and SERS applications. Phys. Chem. Chem. Phys.,  2020, 22(10), 5673-5687.
[http://dx.doi.org/10.1039/C9CP06029D] [PMID: 32103209] 
[19] 
Rabiee, N.; Yaraki, M.T.; Garakani, S.M.; Garakani, S.M.; Ahmadi, S.; Lajevardi, A.; Bagherzadeh, M.; Rabiee, M.; Tayebi, L.; Tahriri, M.; Hamblin, M.R. Recent advances in porphyrin-based nanocomposites for effective targeted imaging and therapy. Biomaterials,  2020, 232, 119707.
[http://dx.doi.org/10.1016/j.biomaterials.2019.119707] [PMID: 31874428] 
[20] 
Gomes, A.T.P.C.; Neves, M.G.P.M.S.; Cavaleiro, J.A.S. Cancer, photodynamic therapy and porphyrin-type derivatives. An. Acad. Bras. Cienc.,  2018, 90(1)(Suppl. 2), 993-1026.
[http://dx.doi.org/10.1590/0001-3765201820170811] [PMID: 29873666] 
[21] 
Garcez, A.S.; Ribeiro, M.S.; Tegos, G.P.; Núñez, S.C.; Jorge, A.O.; Hamblin, M.R. Antimicrobial photodynamic therapy combined with conventional endodontic treatment to eliminate root canal biofilm infection. Lasers Surg. Med.,  2007, 39(1), 59-66.
[http://dx.doi.org/10.1002/lsm.20415] [PMID: 17066481] 
[22] 
Amin, R.M.; Hauser, C.; Kinzler, I.; Rueck, A.; Scalfi-Happ, C. Evaluation of photodynamic treatment using aluminum phthalocyanine tetrasulfonate chloride as a photosensitizer: new approach. Photochem. Photobiol. Sci.,  2012, 11(7), 1156-1163.
[http://dx.doi.org/10.1039/c2pp05411f] [PMID: 22402592] 
[23] 
Allison, R.R. Radiobiological modifiers in clinical radiation oncology: current reality and future potential. Future Oncol.,  2014, 10(15), 2359-2379.
[http://dx.doi.org/10.2217/fon.14.174] [PMID: 25525845] 
[24] 
Fingar, V.H.; Wieman, T.J.; Park, Y.J.; Henderson, B.W. Implications of a pre-existing tumor hypoxic fraction on photodynamic therapy. J. Surg. Res.,  1992, 53(5), 524-528.
[http://dx.doi.org/10.1016/0022-4804(92)90101-5] [PMID: 1434604] 
[25] 
Kudinova, N.; Berezov, T. Photodynamic therapy of cancer: Search for ideal photosensitizer. Biochemistry (Moscow). Supplement Series B: Biomedical Chemistry,  2010, 4, 95-103.
[26] 
Allison, R.R.; Bagnato, V.S.; Sibata, C.H. Future of oncologic photodynamic therapy. Future Oncol.,  2010, 6(6), 929-940.
[http://dx.doi.org/10.2217/fon.10.51] [PMID: 20528231] 
[27] 
Allison, R.R.; Downie, G.H.; Cuenca, R.; Hu, X-H.; Childs, C.J.; Sibata, C.H. Photosensitizers in clinical PDT. Photodiagn. Photodyn. Ther.,  2004, 1(1), 27-42.
[http://dx.doi.org/10.1016/S1572-1000(04)00007-9] [PMID: 25048062] 
[28] 
Girigoswami, A.; Yassine, W.; Sharmiladevi, P.; Haribabu, V.; Girigoswami, K. Camouflaged nanosilver with excitation wavelength de-pendent high quantum yield for targeted theranostic. Sci. Rep.,  2018, 8(1), 16459.
[http://dx.doi.org/10.1038/s41598-018-34843-4] [PMID: 30405190] 
[29] 
Sharmiladevi, P.; Akhtar, N.; Haribabu, V.; Girigoswami, K.; Chattopadhyay, S.; Girigoswami, A. Excitation wavelength independent car-bon-decorated ferrite nanodots for multimodal diagnosis and stimuli responsive therapy. ACS Appl. Bio Mater.,  2019, 2, 1634-1642.
[http://dx.doi.org/10.1021/acsabm.9b00039] 
[30] 
Girigoswami, A.; Ramalakshmi, M.; Akhtar, N.; Metkar, S.K.; Girigoswami, K. ZnO Nanoflower petals mediated amyloid degradation - An in vitro electrokinetic potential approach. Mater. Sci. Eng. C,  2019, 101, 169-178.
[http://dx.doi.org/10.1016/j.msec.2019.03.086] [PMID: 31029310] 
[31] 
Haribabu, V.; Sharmiladevi, P.; Akhtar, N.; Farook, A.S.; Girigoswami, K.; Girigoswami, A. Label free ultrasmall fluoromagnetic ferrite-clusters for targeted cancer imaging and drug delivery. Curr. Drug Deliv.,  2019, 16(3), 233-241.
[http://dx.doi.org/10.2174/1567201816666181119112410] [PMID: 30451110] 
[32] 
Ensign, L.M.; Cone, R.; Hanes, J. Nanoparticle-based drug delivery to the vagina: a review. J. Control. Release,  2014, 190, 500-514.
[http://dx.doi.org/10.1016/j.jconrel.2014.04.033] [PMID: 24830303] 
[33] 
Obaid, G.; Broekgaarden, M.; Bulin, A-L.; Huang, H-C.; Kuriakose, J.; Liu, J.; Hasan, T. Photonanomedicine: a convergence of photody-namic therapy and nanotechnology. Nanoscale,  2016, 8(25), 12471-12503.
[http://dx.doi.org/10.1039/C5NR08691D] [PMID: 27328309] 
[34] 
Haribabu, V.; Farook, A.S.; Goswami, N.; Murugesan, R.; Girigoswami, A. Optimized Mn-doped iron oxide nanoparticles entrapped in dendrimer for dual contrasting role in MRI. J. Biomed. Mater. Res. B Appl. Biomater.,  2016, 104(4), 817-824.
[http://dx.doi.org/10.1002/jbm.b.33550] [PMID: 26460478] 
[35] 
Deepika, R.; Girigoswami, K.; Murugesan, R.; Girigoswami, A. Influence of divalent cation on morphology and drug delivery efficiency of mixed polymer nanoparticles. Curr. Drug Deliv.,  2018, 15(5), 652-657.
[http://dx.doi.org/10.2174/1567201814666170825160617] [PMID: 28847271] 
[36] 
Liu, S.; Wu, G.; Zhang, X.; Yu, J.; Liu, M.; Zhang, Y.; Wang, P.; Yin, X. Degradation and drug-release behavior of polylactic acid (PLA) medical suture coating with tea polyphenol (TP)-polycaprolactone (PCL)/polyglycolide (PGA). Fibers Polym.,  2019, 20, 229-235.
[http://dx.doi.org/10.1007/s12221-019-8829-8] 
[37] 
Hong, E.J.; Choi, D.G.; Shim, M.S. Targeted and effective photodynamic therapy for cancer using functionalized nanomaterials. Acta Pharm. Sin. B,  2016, 6(4), 297-307.
[http://dx.doi.org/10.1016/j.apsb.2016.01.007] [PMID: 27471670] 
[38] 
Karimi, M.; Sahandi Zangabad, P.; Baghaee-Ravari, S.; Ghazadeh, M.; Mirshekari, H.; Hamblin, M.R. Smart nanostructures for cargo de-livery: uncaging and activating by light. J. Am. Chem. Soc.,  2017, 139(13), 4584-4610.
[http://dx.doi.org/10.1021/jacs.6b08313] [PMID: 28192672] 
[39] 
Allen, T.M.; Cullis, P.R. Liposomal drug delivery systems: from concept to clinical applications. Adv. Drug Deliv. Rev.,  2013, 65(1), 36-48.
[http://dx.doi.org/10.1016/j.addr.2012.09.037] [PMID: 23036225] 
[40] 
Choi, K.H.; Chung, C-W.; Kim, C.H.; Kim, D.H.; Jeong, Y-I.; Kang, D.H. Effect of 5-aminolevulinic acid-encapsulate liposomes on photo-dynamic therapy in human cholangiocarcinoma cells. J. Nanosci. Nanotechnol.,  2014, 14(8), 5628-5632.
[http://dx.doi.org/10.1166/jnn.2014.8825] [PMID: 25935979] 
[41] 
Peng, Q.; Warloe, T.; Berg, K.; Moan, J.; Kongshaug, M.; Giercksky, K.E.; Nesland, J.M. 5-Aminolevulinic acid-based photodynamic therapy. Clinical research and future challenges. Cancer,  1997, 79(12), 2282-2308.
[http://dx.doi.org/10.1002/(SICI)1097-0142(19970615)79:12<2282::AID-CNCR2>3.0.CO;2-O] [PMID: 9191516] 
[42] 
Kazantzis, K.T.; Koutsonikoli, K.; Mavroidi, B.; Zachariadis, M.; Alexiou, P.; Pelecanou, M.; Politopoulos, K.; Alexandratou, E.; Sagnou, M. Curcumin derivatives as photosensitizers in photodynamic therapy: photophysical properties and in vitro studies with prostate cancer cells. Photochem. Photobiol. Sci.,  2020, 19(2), 193-206.
[http://dx.doi.org/10.1039/C9PP00375D] [PMID: 31956888] 
[43] 
Fahmy, S.A.; Azzazy, H.M.E.; Schaefer, J. Liposome photosensitizer formulations for effective cancer photodynamic therapy. Pharmaceutics,  2021, 13(9), 1345.
[http://dx.doi.org/10.3390/pharmaceutics13091345] [PMID: 34575424] 
[44] 
Gowsalya, K.; Yasothamani, V.; Vivek, R. Emerging indocyanine green formulated nanocarriers for multimodal cancer therapy: a review. Nanoscale Adv.,  2021, 3, 3332-3352.
[http://dx.doi.org/10.1039/D1NA00059D] 
[45] 
Ming, L.; Cheng, K.; Chen, Y.; Yang, R.; Chen, D. Enhancement of tumor lethality of ROS in photodynamic therapy. Cancer Med.,  2021, 10(1), 257-268.
[http://dx.doi.org/10.1002/cam4.3592] [PMID: 33141513] 
[46] 
Sarbadhikary, P.; George, B.P.; Abrahamse, H. Recent advances in photosensitizers as multifunctional theranostic agents for imaging-guided photodynamic therapy of cancer. Theranostics,  2021, 11(18), 9054-9088.
[http://dx.doi.org/10.7150/thno.62479] [PMID: 34522227] 
[47] 
Katifelis, H.; Gazouli, M. Cancer-targeted nanotheranostics: recent advances and future perspectives. Cancer Nanotheranostics,  2021, 97-115.
[http://dx.doi.org/10.1007/978-3-030-76263-6_4] 
[48] 
Sharmiladevi, P.; Girigoswami, K.; Haribabu, V.; Girigoswami, A. Nano-enabled theranostics for cancer. Materials Advances,  2021, 2, 2876-2891.
[http://dx.doi.org/10.1039/D1MA00069A] 
[49] 
Haribabu, V.; Girigoswami, K.; Sharmiladevi, P.; Girigoswami, A. Water-nanomaterial interaction to escalate twin-mode magnetic reso-nance imaging. ACS Biomater. Sci. Eng.,  2020, 6(8), 4377-4389.
[http://dx.doi.org/10.1021/acsbiomaterials.0c00409] [PMID: 33455176] 
[50] 
Reshetov, V.; Lassalle, H-P.; François, A.; Dumas, D.; Hupont, S.; Gräfe, S.; Filipe, V.; Jiskoot, W.; Guillemin, F.; Zorin, V.; Bezdetnaya, L. Photodynamic therapy with conventional and PEGylated liposomal formulations of mTHPC (temoporfin): comparison of treatment ef-ficacy and distribution characteristics in vivo. Int. J. Nanomedicine,  2013, 8, 3817-3831.
[http://dx.doi.org/10.2147/IJN.S51002] [PMID: 24143087] 
[51] 
Wu, P-T.; Lin, C-L.; Lin, C-W.; Chang, N-C.; Tsai, W-B.; Yu, J. Methylene-blue-encapsulated liposomes as photodynamic therapy nano agents for breast cancer cells. Nanomaterials (Basel),  2018, 9(1), 14.
[http://dx.doi.org/10.3390/nano9010014] [PMID: 30583581] 
[52] 
Lü, J-M.; Wang, X.; Marin-Muller, C.; Wang, H.; Lin, P.H.; Yao, Q.; Chen, C. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev. Mol. Diagn.,  2009, 9(4), 325-341.
[http://dx.doi.org/10.1586/erm.09.15] [PMID: 19435455] 
[53] 
McCarthy, J.R.; Perez, J.M.; Brückner, C.; Weissleder, R. Polymeric nanoparticle preparation that eradicates tumors. Nano Lett.,  2005, 5(12), 2552-2556.
[http://dx.doi.org/10.1021/nl0519229] [PMID: 16351214] 
[54] 
Boix-Garriga, E.; Acedo, P.; Casadó, A.; Villanueva, A.; Stockert, J.C.; Cañete, M.; Mora, M.; Sagristá, M.L.; Nonell, S. Poly(D, L-lactide-co-glycolide) nanoparticles as delivery agents for photodynamic therapy: enhancing singlet oxygen release and photototoxicity by surface PEG coating. Nanotechnology,  2015, 26(36), 365104.
[http://dx.doi.org/10.1088/0957-4484/26/36/365104] [PMID: 26293792] 
[55] 
Wang, Q.; Li, J-M.; Yu, H.; Deng, K.; Zhou, W.; Wang, C-X.; Zhang, Y.; Li, K-H.; Zhuo, R-X.; Huang, S-W. Fluorinated polymeric mi-celles to overcome hypoxia and enhance photodynamic cancer therapy. Biomater. Sci.,  2018, 6(11), 3096-3107.
[http://dx.doi.org/10.1039/C8BM00852C] [PMID: 30306153] 
[56] 
Zhao, L.; Kim, T-H.; Huh, K.M.; Kim, H-W.; Kim, S.Y. Self-assembled photosensitizer-conjugated nanoparticles for targeted photody-namic therapy. J. Biomater. Appl.,  2013, 28(3), 434-447.
[http://dx.doi.org/10.1177/0885328212459777] [PMID: 22983021] 
[57] 
Narsireddy, A.; Vijayashree, K.; Adimoolam, M.G.; Manorama, S.V.; Rao, N.M. Photosensitizer and peptide-conjugated PAMAM den-drimer for targeted in vivo photodynamic therapy. Int. J. Nanomedicine,  2015, 10, 6865-6878.
[PMID: 26604753] 
[58] 
Ambekar, R.S.; Choudhary, M.; Kandasubramanian, B. Recent advances in dendrimer-based nanoplatform for cancer treatment: A review. Eur. Polym. J.,  2020, 126, 109546.
[http://dx.doi.org/10.1016/j.eurpolymj.2020.109546] 
[59] 
Nishiyama, N.; Stapert, H.R.; Zhang, G-D.; Takasu, D.; Jiang, D-L.; Nagano, T.; Aida, T.; Kataoka, K. Light-harvesting ionic dendrimer porphyrins as new photosensitizers for photodynamic therapy. Bioconjug. Chem.,  2003, 14(1), 58-66.
[http://dx.doi.org/10.1021/bc025597h] [PMID: 12526693] 
[60] 
Spyropoulos-Antonakakis, N.; Sarantopoulou, E.; Trohopoulos, P.N.; Stefi, A.L.; Kollia, Z.; Gavriil, V.E.; Bourkoula, A.; Petrou, P.S.; Kakabakos, S.; Semashko, V.V.; Nizamutdinov, A.S.; Cefalas, A.C. Selective aggregation of PAMAM dendrimer nanocarriers and PA-MAM/ZnPc nanodrugs on human atheromatous carotid tissues: a photodynamic therapy for atherosclerosis. Nanoscale Res. Lett.,  2015, 10, 210.
[http://dx.doi.org/10.1186/s11671-015-0904-5] [PMID: 25991914] 
[61] 
Wacker, M.; Chen, K.; Preuss, A.; Possemeyer, K.; Roeder, B.; Langer, K. Photosensitizer loaded HSA nanoparticles. I: Preparation and photophysical properties. Int. J. Pharm.,  2010, 393(1-2), 253-262.
[http://dx.doi.org/10.1016/j.ijpharm.2010.04.022] [PMID: 20417701] 
[62] 
Ren, H.; Liu, J.; Su, F.; Ge, S.; Yuan, A.; Dai, W.; Wu, J.; Hu, Y. Relighting photosensitizers by synergistic integration of albumin and perfluorocarbon for enhanced photodynamic therapy. ACS Appl. Mater. Interfaces,  2017, 9(4), 3463-3473.
[http://dx.doi.org/10.1021/acsami.6b14885] [PMID: 28067039] 
[63] 
Jisha, V.S.; Arun, K.T.; Hariharan, M.; Ramaiah, D. Site-selective binding and dual mode recognition of serum albumin by a squaraine dye. J. Am. Chem. Soc.,  2006, 128(18), 6024-6025.
[http://dx.doi.org/10.1021/ja061301x] [PMID: 16669657] 
[64] 
Jisha, V.S.; Arun, K.T.; Hariharan, M.; Ramaiah, D. Site-selective interactions: squaraine dye-serum albumin complexes with enhanced fluorescence and triplet yields. J. Phys. Chem. B,  2010, 114(17), 5912-5919.
[http://dx.doi.org/10.1021/jp100369x] [PMID: 20380473] 
[65] 
Foley, M.S.; Beeby, A.; Parker, A.W.; Bishop, S.M.; Phillips, D. Excited triplet state photophysics of the sulphonated aluminium phthalo-cyanines bound to human serum albumin. J. Photochem. Photobiol. B,  1997, 38(1), 10-17.
[http://dx.doi.org/10.1016/S1011-1344(96)07434-9] [PMID: 9134751] 
[66] 
Cheng, Y.; Cheng, H.; Jiang, C.; Qiu, X.; Wang, K.; Huan, W.; Yuan, A.; Wu, J.; Hu, Y. Perfluorocarbon nanoparticles enhance reactive oxygen levels and tumour growth inhibition in photodynamic therapy. Nat. Commun.,  2015, 6, 8785.
[http://dx.doi.org/10.1038/ncomms9785] [PMID: 26525216] 
[67] 
Que, Y.; Liu, Y.; Tan, W.; Feng, C.; Shi, P.; Li, Y.; Xiaoyu, H. Enhancing photodynamic therapy efficacy by using fluorinated nanoplat-form. ACS Macro Lett.,  2016, 5, 168-173.
[http://dx.doi.org/10.1021/acsmacrolett.5b00935] 
[68] 
Wang, Y-G.; Kim, H.; Mun, S.; Kim, D.; Choi, Y. Indocyanine green-loaded perfluorocarbon nanoemulsions for bimodal (19)F-magnetic resonance/nearinfrared fluorescence imaging and subsequent phototherapy. Quant. Imaging Med. Surg.,  2013, 3(3), 132-140.
[PMID: 23833726] 
[69] 
Sharmiladevi, P.; Haribabu, V.; Girigoswami, K.; Sulaiman Farook, A.; Girigoswami, A. Effect of mesoporous nano water reservoir on MR relaxivity. Sci. Rep.,  2017, 7(1), 11179.
[http://dx.doi.org/10.1038/s41598-017-11710-2] [PMID: 28894269] 
[70] 
Wang, Z.; Hong, X.; Zong, S.; Tang, C.; Cui, Y.; Zheng, Q. BODIPY-doped silica nanoparticles with reduced dye leakage and enhanced singlet oxygen generation. Sci. Rep.,  2015, 5, 12602.
[http://dx.doi.org/10.1038/srep12602] [PMID: 26211417] 
[71] 
Bharathiraja, S.; Moorthy, M.S.; Manivasagan, P.; Seo, H.; Lee, K.D.; Oh, J. Chlorin e6 conjugated silica nanoparticles for targeted and effective photodynamic therapy. Photodiagn. Photodyn. Ther.,  2017, 19, 212-220.
[http://dx.doi.org/10.1016/j.pdpdt.2017.06.001] [PMID: 28583295] 
[72] 
Chai, S.; Guo, Y.; Zhang, Z.; Chai, Z.; Ma, Y.; Qi, L. Cyclodextrin-gated mesoporous silica nanoparticles as drug carriers for red light-induced drug release. Nanotechnology,  2017, 28(14), 145101.
[http://dx.doi.org/10.1088/1361-6528/aa5e74] [PMID: 28281469] 
[73] 
Rizzi, M.; Tonello, S.; Estevão, B.M.; Gianotti, E.; Marchese, L.; Renò, F. Verteporfin based silica nanoparticle for in vitro selective inhibi-tion of human highly invasive melanoma cell proliferation. J. Photochem. Photobiol. B,  2017, 167, 1-6.
[http://dx.doi.org/10.1016/j.jphotobiol.2016.12.021] [PMID: 28039784] 
[74] 
Ghosh, D.; Sarkar, D.; Girigoswami, A.; Chattopadhyay, N. A fully standardized method of synthesis of gold nanoparticles of desired dimension in the range 15 nm-60 nm. J. Nanosci. Nanotechnol.,  2011, 11(2), 1141-1146.
[http://dx.doi.org/10.1166/jnn.2011.3090] [PMID: 21456151] 
[75] 
Girigoswami, A.; Li, T.; Jung, C.; Mun, H.Y.; Park, H.G. Gold nanoparticle-based label-free detection of BRCA1 mutations utilizing DNA ligation on DNA microarray. J. Nanosci. Nanotechnol.,  2009, 9(2), 1019-1024.
[http://dx.doi.org/10.1166/jnn.2009.C077] [PMID: 19441445] 
[76] 
Stuchinskaya, T.; Moreno, M.; Cook, M.J.; Edwards, D.R.; Russell, D.A. Targeted photodynamic therapy of breast cancer cells using anti-body-phthalocyanine-gold nanoparticle conjugates. Photochem. Photobiol. Sci.,  2011, 10(5), 822-831.
[http://dx.doi.org/10.1039/c1pp05014a] [PMID: 21455532] 
[77] 
Cheng, L.; Wang, C.; Feng, L.; Yang, K.; Liu, Z. Functional nanomaterials for phototherapies of cancer. Chem. Rev.,  2014, 114(21), 10869-10939.
[http://dx.doi.org/10.1021/cr400532z] [PMID: 25260098] 
[78] 
Wu, Q.; Chen, G.; Gong, K.; Wang, J.; Ge, X.; Liu, X.; Guo, S.; Wang, F. MnO2-laden black phosphorus for MRI-guided synergistic PDT, PTT, and chemotherapy. Matter,  2019, 1, 496-512.
[http://dx.doi.org/10.1016/j.matt.2019.03.007] 
[79] 
Yan, L.; Luo, L.; Amirshaghaghi, A.; Miller, J.; Meng, C.; You, T.; Busch, T.M.; Tsourkas, A.; Cheng, Z. Dextran-benzoporphyrin deriva-tive (BPD) coated superparamagnetic iron oxide nanoparticle (SPION) micelles for T2-weighted magnetic resonance imaging and photody-namic therapy. Bioconjug. Chem.,  2019, 30(11), 2974-2981.
[http://dx.doi.org/10.1021/acs.bioconjchem.9b00676] [PMID: 31661959] 
[80] 
Cao, J.; An, H.; Huang, X.; Fu, G.; Zhuang, R.; Zhu, L.; Xie, J.; Zhang, F. Monitoring of the tumor response to nano-graphene oxide-mediated photothermal/photodynamic therapy by diffusion-weighted and BOLD MRI. Nanoscale,  2016, 8(19), 10152-10159.
[http://dx.doi.org/10.1039/C6NR02012G] [PMID: 27121639] 
[81] 
Liang, X.; Li, X.; Jing, L.; Yue, X.; Dai, Z. Theranostic porphyrin dyad nanoparticles for magnetic resonance imaging guided photodynam-ic therapy. Biomaterials,  2014, 35(24), 6379-6388.
[http://dx.doi.org/10.1016/j.biomaterials.2014.04.094] [PMID: 24818886] 
[82] 
Mahata, A.; Sarkar, D.; Bose, D.; Ghosh, D.; Girigoswami, A.; Das, P.; Chattopadhyay, N. Photophysics and rotational dynamics of a β-carboline analogue in nonionic micelles: effect of variation of length of the headgroup and the tail of the surfactant. J. Phys. Chem. B,  2009, 113(21), 7517-7526.
[http://dx.doi.org/10.1021/jp900575e] [PMID: 19413359] 
[83] 
Liu, J.; Tabata, Y. Photodynamic antitumor activity of fullerene modified with poly (ethylene glycol) with different molecular weights and terminal structures. J. Biomater. Sci. Polym. Ed.,  2011, 22(1-3), 297-312.
[http://dx.doi.org/10.1163/092050609X12609582066446] [PMID: 20557714] 
[84] 
Shi, J.; Wang, L.; Gao, J.; Liu, Y.; Zhang, J.; Ma, R.; Liu, R.; Zhang, Z. A fullerene-based multi-functional nanoplatform for cancer theranostic applications. Biomaterials,  2014, 35(22), 5771-5784.
[http://dx.doi.org/10.1016/j.biomaterials.2014.03.071] [PMID: 24746227] 
[85] 
Guo, Z.; Zheng, K.; Tan, Z.; Liu, Y.; Zhao, Z.; Zhu, G.; Ma, K.; Cui, C.; Wang, L.; Kang, T. Overcoming drug resistance with functional mesoporous titanium dioxide nanoparticles combining targeting, drug delivery and photodynamic therapy. J. Mater. Chem. B Mater. Biol. Med.,  2018, 6(46), 7750-7759.
[http://dx.doi.org/10.1039/C8TB01810C] [PMID: 32254897] 
[86] 
Li, J.; Guo, D.; Wang, X.; Wang, H.; Jiang, H.; Chen, B. The photodynamic effect of different size ZnO nanoparticles on cancer cell prolif-eration in vitro. Nanoscale Res. Lett.,  2010, 5(6), 1063-1071.
[http://dx.doi.org/10.1007/s11671-010-9603-4] [PMID: 20671778] 
[87] 
Hariharan, R.; Senthilkumar, S.; Suganthi, A.; Rajarajan, M. Synthesis and characterization of doxorubicin modified ZnO/PEG nanomateri-als and its photodynamic action. J. Photochem. Photobiol. B,  2012, 116, 56-65.
[http://dx.doi.org/10.1016/j.jphotobiol.2012.08.008] [PMID: 22982207] 
[88] 
Chen, W.; Zhang, J. Using nanoparticles to enable simultaneous radiation and photodynamic therapies for cancer treatment. J. Nanosci. Nanotechnol.,  2006, 6(4), 1159-1166.
[http://dx.doi.org/10.1166/jnn.2006.327] [PMID: 16736782] 
[89] 
Chen, W. Nanoparticle self-lighting photodynamic therapy for cancer treatment. J. Biomed. Nanotechnol.,  2008, 4, 369-376.
[http://dx.doi.org/10.1166/jbn.2008.001] 
[90] 
Cline, B.; Delahunty, I.; Xie, J. Nanoparticles to mediate X-ray-induced photodynamic therapy and Cherenkov radiation photodynamic therapy. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol.,  2019, 11(2), e1541.
[http://dx.doi.org/10.1002/wnan.1541] [PMID: 30063116] 
[91] 
Jaiganesh, T.; Rani, J.D.V.; Girigoswami, A. Spectroscopically characterized cadmium sulfide quantum dots lengthening the lag phase of Escherichia coli growth. Spectrochim. Acta A Mol. Biomol. Spectrosc.,  2012, 92, 29-32.
[http://dx.doi.org/10.1016/j.saa.2012.02.044] [PMID: 22407211] 
[92] 
Shao, L.; Gao, Y.; Yan, F. Semiconductor quantum dots for biomedicial applications. Sensors (Basel),  2011, 11(12), 11736-11751.
[http://dx.doi.org/10.3390/s111211736] [PMID: 22247690] 
[93] 
Ren, S.; Cheng, X.; Chen, M.; Liu, C.; Zhao, P.; Huang, W.; He, J.; Zhou, Z.; Miao, L. Hypotoxic and rapidly metabolic PEG-PCL-C3-ICG nanoparticles for fluorescence-guided photothermal/photodynamic therapy against OSCC. ACS Appl. Mater. Interfaces,  2017, 9(37), 31509-31518.
[http://dx.doi.org/10.1021/acsami.7b09522] [PMID: 28858474] 
[94] 
Bharathiraja, S.; Manivasagan, P.; Santha Moorthy, M.; Bui, N.Q.; Jang, B.; Phan, T.T.V.; Jung, W-K.; Kim, Y-M.; Lee, K.D.; Oh, J. Photo-based PDT/PTT dual model killing and imaging of cancer cells using phycocyanin-polypyrrole nanoparticles. Eur. J. Pharm. Biopharm.,  2018, 123, 20-30.
[http://dx.doi.org/10.1016/j.ejpb.2017.11.007] [PMID: 29154833] 
[95] 
Zhang, C.; Zhang, J.; Qin, Y.; Song, H.; Huang, P.; Wang, W.; Wang, C.; Li, C.; Wang, Y.; Kong, D. Co-delivery of doxorubicin and phe-ophorbide A by pluronic F127 micelles for chemo-photodynamic combination therapy of melanoma. J. Mater. Chem. B Mater. Biol. Med.,  2018, 6(20), 3305-3314.
[http://dx.doi.org/10.1039/C7TB03179C] [PMID: 32254388] 
[96] 
Wang, Y.; Zhao, J.; Chen, Z.; Zhang, F.; Wang, Q.; Guo, W.; Wang, K.; Lin, H.; Qu, F. Construct of MoSe2/Bi2Se3 nanoheterostructure: Multimodal CT/PT imaging-guided PTT/PDT/chemotherapy for cancer treating. Biomaterials,  2019, 217, 119282.
[http://dx.doi.org/10.1016/j.biomaterials.2019.119282] [PMID: 31260884] 
[97] 
Mokwena, M.G.; Kruger, C.A.; Ivan, M-T.; Heidi, A. A review of nanoparticle photosensitizer drug delivery uptake systems for photody-namic treatment of lung cancer. Photodiagn. Photodyn. Ther.,  2018, 22, 147-154.
[http://dx.doi.org/10.1016/j.pdpdt.2018.03.006] [PMID: 29588217] 
[98] 
Chaabane, W. User, S.D.; El-Gazzah, M.; Jaksik, R.; Sajjadi, E.; Rzeszowska-Wolny, J.; Łos, M.J. Autophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancer. Arch. Immunol. Ther. Exp. (Warsz.),  2013, 61(1), 43-58.
[http://dx.doi.org/10.1007/s00005-012-0205-y] [PMID: 23229678] 
[99] 
Vanden Berghe, T.; Kaiser, W.J.; Bertrand, M.J.; Vandenabeele, P. Molecular crosstalk between apoptosis, necroptosis, and survival sig-naling. Mol. Cell. Oncol.,  2015, 2(4), e975093.
[http://dx.doi.org/10.4161/23723556.2014.975093] [PMID: 27308513] 
[100] 
Nikoletopoulou, V.; Markaki, M.; Palikaras, K.; Tavernarakis, N. Crosstalk between apoptosis, necrosis and autophagy. Biochimica et Biophysica Acta (BBA)-. Molecular Cell Research,  2013, 1833, 3448-3459.
[101] 
Castano, A.P.; Demidova, T.N.; Hamblin, M.R. Mechanisms in photodynamic therapy: Part three-Photosensitizer pharmacokinetics, bio-distribution, tumor localization and modes of tumor destruction. Photodiagn. Photodyn. Ther.,  2005, 2(2), 91-106.
[http://dx.doi.org/10.1016/S1572-1000(05)00060-8] [PMID: 25048669] 
[102] 
Garg, A.D.; Nowis, D.; Golab, J.; Agostinis, P. Photodynamic therapy: illuminating the road from cell death towards anti-tumour immuni-ty. Apoptosis,  2010, 15(9), 1050-1071.
[http://dx.doi.org/10.1007/s10495-010-0479-7] [PMID: 20221698] 
[103] 
Garg, A.D.; Agostinis, P. ER stress, autophagy and immunogenic cell death in photodynamic therapy-induced anti-cancer immune re-sponses. Photochem. Photobiol. Sci.,  2014, 13(3), 474-487.
[http://dx.doi.org/10.1039/C3PP50333J] [PMID: 24493131] 
[104] 
Beltrán Hernández, I.; Yu, Y.; Ossendorp, F.; Korbelik, M.; Oliveira, S. Preclinical and clinical evidence of immune responses triggered in oncologic photodynamic therapy: Clinical recommendations. J. Clin. Med.,  2020, 9(2), 333.
[http://dx.doi.org/10.3390/jcm9020333] [PMID: 31991650] 
[105] 
Li, W.; Yang, J.; Luo, L.; Jiang, M.; Qin, B.; Yin, H.; Zhu, C.; Yuan, X.; Zhang, J.; Luo, Z.; Du, Y.; Li, Q.; Lou, Y.; Qiu, Y.; You, J. Target-ing photodynamic and photothermal therapy to the endoplasmic reticulum enhances immunogenic cancer cell death. Nat. Commun.,  2019, 10(1), 3349.
[http://dx.doi.org/10.1038/s41467-019-11269-8] [PMID: 31350406] 
[106] 
He, C.; Duan, X.; Guo, N.; Chan, C.; Poon, C.; Weichselbaum, R.R.; Lin, W. Core-shell nanoscale coordination polymers combine chemo-therapy and photodynamic therapy to potentiate checkpoint blockade cancer immunotherapy. Nat. Commun.,  2016, 7, 12499.
[http://dx.doi.org/10.1038/ncomms12499] [PMID: 27530650] 
[107] 
Yang, W.; Zhang, F.; Deng, H.; Lin, L.; Wang, S.; Kang, F.; Yu, G.; Lau, J.; Tian, R.; Zhang, M.; Wang, Z.; He, L.; Ma, Y.; Niu, G.; Hu, S.; Chen, X. Smart nanovesicle-mediated immunogenic cell death through tumor microenvironment modulation for effective photodynamic immunotherapy. ACS Nano,  2020, 14(1), 620-631.
[http://dx.doi.org/10.1021/acsnano.9b07212] [PMID: 31877023] 
[108] 
Master, A.; Livingston, M.; Sen Gupta, A. Photodynamic nanomedicine in the treatment of solid tumors: perspectives and challenges. J. Control. Release,  2013, 168(1), 88-102.
[http://dx.doi.org/10.1016/j.jconrel.2013.02.020] [PMID: 23474028] 
[109] 
Ganapathy, V.; Moghe, P.V.; Roth, C.M. Targeting tumor metastases: Drug delivery mechanisms and technologies. J. Control. Release,  2015, 219, 215-223.
[http://dx.doi.org/10.1016/j.jconrel.2015.09.042] [PMID: 26409123] 
[110] 
Prajapati, B. Nanoparticles as platforms for targeted drug delivery systems in cancer therapy. Nanotechnology,  2008, 3, 1-8.
[111] 
Kruger, C.A.; Abrahamse, H. Utilisation of targeted nanoparticle photosensitiser drug delivery systems for the enhancement of photody-namic therapy. Molecules,  2018, 23(10), 2628.
[http://dx.doi.org/10.3390/molecules23102628] [PMID: 30322132] 
[112] 
Barakat, N.S. BinTaleb, D; Al Salehi, A Target nanoparticles: an appealing drug delivery platform. J. Nanomed. Nanotechnol.,  2012, 3, 1-9.
[113] 
Alexis, F.; Pridgen, E.M.; Langer, R.; Farokhzad, O.C. Nanoparticle technologies for cancer therapy. Drug Deliv.,  2010, 55-86.
[http://dx.doi.org/10.1007/978-3-642-00477-3_2] 
[114] 
Kashef, N.; Huang, Y-Y.; Hamblin, M.R. Advances in antimicrobial photodynamic inactivation at the nanoscale. Nanophotonics,  2017, 6(5), 853-879.
[http://dx.doi.org/10.1515/nanoph-2016-0189] [PMID: 29226063] 
[115] 
Yin, R.; Agrawal, T.; Khan, U.; Gupta, G.K.; Rai, V.; Huang, Y-Y.; Hamblin, M.R. Antimicrobial photodynamic inactivation in nanomedi-cine: small light strides against bad bugs. Nanomedicine (Lond.),  2015, 10(15), 2379-2404.
[http://dx.doi.org/10.2217/nnm.15.67] [PMID: 26305189] 
[116] 
Nepal, D.; Balasubramanian, S.; Simonian, A.L.; Davis, V.A. Strong antimicrobial coatings: single-walled carbon nanotubes armored with biopolymers. Nano Lett.,  2008, 8(7), 1896-1901.
[http://dx.doi.org/10.1021/nl080522t] [PMID: 18507479] 
[117] 
Banerjee, I.; Douaisi, M.P.; Mondal, D.; Kane, R.S. Light-activated nanotube-porphyrin conjugates as effective antiviral agents. Nanotechnology,  2012, 23(10), 105101.
[http://dx.doi.org/10.1088/0957-4484/23/10/105101] [PMID: 22361811] 
[118] 
Bonfim, CMd; Monteleoni, LF; Calmon, MdF; Cândido, NM; Provazzi, PJS; Lino, VdS; Rabachini, T; Sichero, L; Villa, LL; Quintana, SM Antiviral activity of curcumin-nanoemulsion associated with photodynamic therapy in vulvar cell lines transducing different variants of HPV-16. Artif. Cells Nanomed. Biotechnol.,  2020, 48, 515-524.
[http://dx.doi.org/10.1080/21691401.2020.1725023] 
[119] 
Lin, S.; Liu, C.; Han, X.; Zhong, H.; Cheng, C. Viral nanoparticle system: an effective platform for photodynamic therapy. Int. J. Mol. Sci.,  2021, 22(4), 1728.
[http://dx.doi.org/10.3390/ijms22041728] [PMID: 33572365] 
[120] 
Kipshidze, N.; Yeo, N.; Kipshidze, N. Photodynamic therapy for COVID-19. Nat. Photonics,  2020, 14, 651-652.
[http://dx.doi.org/10.1038/s41566-020-00703-9] [PMID: 32818638] 
[121] 
Lim, M.E.; Lee, Y.L.; Zhang, Y.; Chu, J.J.H. Photodynamic inactivation of viruses using upconversion nanoparticles. Biomaterials,  2012, 33(6), 1912-1920.
[http://dx.doi.org/10.1016/j.biomaterials.2011.11.033] [PMID: 22153019] 
[122] 
Montaseri, H.; Kruger, C.A.; Abrahamse, H. Recent advances in porphyrin-based inorganic nanoparticles for cancer treatment. Int. J. Mol. Sci.,  2020, 21(9), 3358.
[http://dx.doi.org/10.3390/ijms21093358] [PMID: 32397477] 
[123] 
Yamini, S.; Gunaseelan, M.; Kumar, G.A.; Singh, S.; Dannangoda, G.C.; Martirosyan, K.S.; Sardar, D.K.; Sivakumar, S.; Girigoswami, A.; Senthilselvan, J. NaGdF4:Yb,Er-Ag nanowire hybrid nanocomposite for multifunctional upconversion emission, optical imaging, MRI and CT imaging applications. Mikrochim. Acta,  2020, 187(6), 317.
[http://dx.doi.org/10.1007/s00604-020-04285-9] [PMID: 32385722] 
[124] 
Pucelik, B. Sułek, A.; Dąbrowski, J.M. Bacteriochlorins and their metal complexes as NIR-absorbing photosensitizers: Properties, mecha-nisms, and applications. Coord. Chem. Rev.,  2020, 416, 213340.
[http://dx.doi.org/10.1016/j.ccr.2020.213340] 
Cite As
Current Nanoscience

A Nano Approach to Formulate Photosensitizers for Photodynamic Therapy

Abstract

Graphical Abstract
