Login Register Cart 0
Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

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

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Mini-Review Article

Factors Affecting Photodynamic Therapy and Anti-Tumor Immune Response

Author(s): Michael R. Hamblin* and Heidi Abrahamse

Volume 21, Issue 2, 2021

Published on: 17 March, 2020

Page: [123 - 136] Pages: 14

DOI: 10.2174/1871520620666200318101037

Price: $65

Abstract

Photodynamic Therapy (PDT) is a cancer therapy involving the systemic injection of a Photosensitizer (PS) that localizes to some extent in a tumor. After an appropriate time (ranging from minutes to days), the tumor is irradiated with red or near-infrared light either as a surface spot or by interstitial optical fibers. The PS is excited by the light to form a long-lived triplet state that can react with ambient oxygen to produce Reactive Oxygen Species (ROS) such as singlet oxygen and/or hydroxyl radicals, that kill tumor cells, destroy tumor blood vessels, and lead to tumor regression and necrosis. It has long been realized that in some cases, PDT can also stimulate the host immune system, leading to a systemic anti-tumor immune response that can also destroy distant metastases and guard against tumor recurrence. The present paper aims to cover some of the factors that can affect the likelihood and efficiency of this immune response. The structure of the PS, drug-light interval, rate of light delivery, mode of cancer cell death, expression of tumor-associated antigens, and combinations of PDT with various adjuvants all can play a role in stimulating the host immune system. Considering the recent revolution in tumor immunotherapy triggered by the success of checkpoint inhibitors, it appears that the time is ripe for PDT to be investigated in combination with other approaches in clinical scenarios.

Keywords: Photodynamic therapy, anti-tumor immune response, T-lymphocytes, photosensitizer, adjuvants, DAMPS, tumor antigens.

« Previous Next »
Graphical Abstract

[1]
Agostinis, P.; Berg, K.; Cengel, K.A.; Foster, T.H.; Girotti, A.W.; Gollnick, S.O.; Hahn, S.M.; Hamblin, M.R.; Juzeniene, A.; Kessel, D.; Korbelik, M.; Moan, J.; Mroz, P.; Nowis, D.; Piette, J.; Wilson, B.C.; Golab, J. Photodynamic therapy of cancer: An update. CA Cancer J. Clin., 2011, 61(4), 250-281.
[http://dx.doi.org/10.3322/caac.20114] [PMID: 21617154]
[2]
Moan, J.; Peng, Q. An outline of the hundred-year history of PDT. Anticancer Res., 2003, 23(5A), 3591-3600.
[PMID: 14666654]
[3]
Skupin-Mrugalska, P.; Sobotta, L.; Kucinska, M.; Murias, M.; Mielcarek, J.; Düzgüneş, N. Cellular changes, molecular pathways and the immune system following photodynamic treatment. Curr. Med. Chem., 2014, 21(35), 4059-4073.
[http://dx.doi.org/10.2174/0929867321666140826120300] [PMID: 25174920]
[4]
Mroz, P.; Vatansever, F.; Muchowicz, A.; Hamblin, M.R. Photodynamic therapy of murine mastocytoma induces specific immune responses against the cancer/testis antigen P1A. Cancer Res., 2013, 73(21), 6462-6470.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-2572] [PMID: 24072749]
[5]
Allison, R.R. Photodynamic therapy: Oncologic horizons. Future Oncol., 2014, 10(1), 123-124.
[http://dx.doi.org/10.2217/fon.13.176] [PMID: 24328413]
[6]
Redmond, R.W.; Gamlin, J.N. A compilation of singlet oxygen yields from biologically relevant molecules. Photochem. Photobiol., 1999, 70(4), 391-475.
[http://dx.doi.org/10.1111/j.1751-1097.1999.tb08240.x] [PMID: 10546544]
[7]
Mroz, P.; Hamblin, M.R. The immunosuppressive side of PDT. Photochem. Photobiol. Sci., 2011, 10(5), 751-758.
[http://dx.doi.org/10.1039/c0pp00345j] [PMID: 21437314]
[8]
Henderson, B.W.; Dougherty, T.J. How does photodynamic therapy work? Photochem. Photobiol., 1992, 55(1), 145-157.
[http://dx.doi.org/10.1111/j.1751-1097.1992.tb04222.x] [PMID: 1603846]
[9]
Wachowska, M.; Gabrysiak, M.; Muchowicz, A.; Bednarek, W.; Barankiewicz, J.; Rygiel, T.; Boon, L.; Mroz, P.; Hamblin, M.R.; Golab, J. 5-Aza-2′-deoxycytidine potentiates antitumour immune response induced by photodynamic therapy. Eur. J. Cancer, 2014, 50(7), 1370-1381.
[http://dx.doi.org/10.1016/j.ejca.2014.01.017] [PMID: 24559534]
[10]
Castano, A.P.; Mroz, P.; Hamblin, M.R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer, 2006, 6(7), 535-545.
[http://dx.doi.org/10.1038/nrc1894] [PMID: 16794636]
[11]
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]
[12]
Mroz, P.; Szokalska, A.; Wu, M.X.; Hamblin, M.R. Photodynamic therapy of tumors can lead to development of systemic antigen-specific immune response. PLoS One, 2010, 5(12)e15194
[http://dx.doi.org/10.1371/journal.pone.0015194] [PMID: 21179470]
[13]
Dougherty, T.J.; Gomer, C.J.; Henderson, B.W.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic therapy. J. Natl. Cancer Inst., 1998, 90(12), 889-905.
[http://dx.doi.org/10.1093/jnci/90.12.889] [PMID: 9637138]
[14]
Engbrecht, B.W.; Menon, C.; Kachur, A.V.; Hahn, S.M.; Fraker, D.L. Photofrin-mediated photodynamic therapy induces vascular occlusion and apoptosis in a human sarcoma xenograft model. Cancer Res., 1999, 59(17), 4334-4342.
[PMID: 10485481]
[15]
Kim, J.; Lim, W.; Kim, S.; Jeon, S.; Hui, Z.; Ni, K.; Kim, C. Im, Y.; Choi, H.; Kim, O. Photodynamic Therapy (PDT) resistance by PARP1 regulation on PDT-induced apoptosis with autophagy in head and neck cancer cells. J. Oral Pathol. Med., 2014, 43(9), 675-684.
[http://dx.doi.org/10.1111/jop.12195]] [PMID: 24931630]
[16]
Mroz, P.; Yaroslavsky, A.; Kharkwal, G.B.; Hamblin, M.R. Cell death pathways in photodynamic therapy of cancer. Cancers (Basel), 2011, 3(2), 2516-2539.
[http://dx.doi.org/10.3390/cancers3022516] [PMID: 23914299]
[17]
Dewaele, M.; Martinet, W.; Rubio, N.; Verfaillie, T.; de Witte, P.A.; Piette, J.; Agostinis, P. Autophagy pathways activated in response to PDT contribute to cell resistance against ROS damage. J. Cell. Mol. Med., 2011, 15(6), 1402-1414.
[http://dx.doi.org/10.1111/j.1582-4934.2010.01118.x] [PMID: 20626525]
[18]
Dougherty, T.J. An update on photodynamic therapy applications. J. Clin. Laser Med. Surg., 2002, 20(1), 3-7.
[http://dx.doi.org/10.1089/104454702753474931] [PMID: 11902352]
[19]
Oleinick, N.L.; Evans, H.H. The photobiology of photodynamic therapy: Cellular targets and mechanisms. Radiat. Res., 1998, 150(5)(Suppl.), S146-S156.
[http://dx.doi.org/10.2307/3579816] [PMID: 9806617]
[20]
Hamblin, M.R.; Newman, E.L. On the mechanism of the tumour-localising effect in photodynamic therapy. J. Photochem. Photobiol. B, 1994, 23(1), 3-8.
[http://dx.doi.org/10.1016/S1011-1344(94)80018-9] [PMID: 8021748]
[21]
Canti, G.; Lattuada, D.; Nicolin, A.; Taroni, P.; Valentini, G.; Cubeddu, R. Antitumor immunity induced by photodynamic therapy with aluminum disulfonated phthalocyanines and laser light. Anticancer Drugs, 1994, 5(4), 443-447.
[http://dx.doi.org/10.1097/00001813-199408000-00009] [PMID: 7949249]
[22]
Korbelik, M.; Dougherty, G.J. Photodynamic therapy-mediated immune response against subcutaneous mouse tumors. Cancer Res., 1999, 59(8), 1941-1946.
[PMID: 10213504]
[23]
Korbelik, M.; Krosl, G.; Krosl, J.; Dougherty, G.J. The role of host lymphoid populations in the response of mouse EMT6 tumor to photodynamic therapy. Cancer Res., 1996, 56(24), 5647-5652.
[PMID: 8971170]
[24]
Oleinick, N.L.; Morris, R.L.; Belichenko, I. The role of apoptosis in response to photodynamic therapy: What, where, why, and how. Photochem. Photobiol. Sci., 2002, 1(1), 1-21.
[http://dx.doi.org/10.1039/b108586g] [PMID: 12659143]
[25]
Garg, A.D.; Galluzzi, L.; Apetoh, L.; Baert, T.; Birge, R.B.; Bravo-San Pedro, J.M.; Breckpot, K.; Brough, D.; Chaurio, R.; Cirone, M.; Coosemans, A.; Coulie, P.G.; De Ruysscher, D.; Dini, L.; de Witte, P.; Dudek-Peric, A.M.; Faggioni, A.; Fucikova, J.; Gaipl, U.S.; Golab, J.; Gougeon, M.L.; Hamblin, M.R.; Hemminki, A.; Herrmann, M.; Hodge, J.W.; Kepp, O.; Kroemer, G.; Krysko, D.V.; Land, W.G.; Madeo, F.; Manfredi, A.A.; Mattarollo, S.R.; Maueroder, C.; Merendino, N.; Multhoff, G.; Pabst, T.; Ricci, J.E.; Riganti, C.; Romano, E.; Rufo, N.; Smyth, M.J.; Sonnemann, J.; Spisek, R.; Stagg, J.; Vacchelli, E.; Vandenabeele, P.; Vandenberk, L.; Van den Eynde, B.J.; Van Gool, S.; Velotti, F.; Zitvogel, L.; Agostinis, P. Molecular and translational classifications of DAMPs in immunogenic cell death. Front. Immunol., 2015, 6, 588.
[http://dx.doi.org/10.3389/fimmu.2015.00588] [PMID: 26635802]
[26]
Jiang, X.; Wang, X. Cytochrome C-mediated apoptosis. Annu. Rev. Biochem., 2004, 73, 87-106.
[http://dx.doi.org/10.1146/annurev.biochem.73.011303.073706] [PMID: 15189137]
[27]
Srivastava, M.; Ahmad, N.; Gupta, S.; Mukhtar, H. Involvement of Bcl-2 and Bax in photodynamic therapy-mediated apoptosis. Antisense Bcl-2 oligonucleotide sensitizes RIF 1 cells to photodynamic therapy apoptosis. J. Biol. Chem., 2001, 276(18), 15481-15488.
[http://dx.doi.org/10.1074/jbc.M006920200] [PMID: 11278320]
[28]
Verfaillie, T.; van Vliet, A.; Garg, A.D.; Dewaele, M.; Rubio, N.; Gupta, S.; de Witte, P.; Samali, A.; Agostinis, P. Pro-apoptotic signaling induced by photo-oxidative ER stress is amplified by Noxa, not Bim. Biochem. Biophys. Res. Commun., 2013, 438(3), 500-506.
[http://dx.doi.org/10.1016/j.bbrc.2013.07.107] [PMID: 23916707]
[29]
Kessel, D.; Evans, C.L. Promotion of proapoptotic signals by lysosomal photodamage: Mechanistic aspects and influence of autophagy. Photochem. Photobiol., 2016, 92(4), 620-623.
[http://dx.doi.org/10.1111/php.12592] [PMID: 27096545]
[30]
Ahmad, N.; Gupta, S.; Feyes, D.K.; Mukhtar, H. Involvement of Fas (APO-1/CD-95) during photodynamic-therapy-mediated apoptosis in human epidermoid carcinoma A431 cells. J. Invest. Dermatol., 2000, 115(6), 1041-1046.
[http://dx.doi.org/10.1046/j.1523-1747.2000.00147.x] [PMID: 11121139]
[31]
Linder, B.; Kögel, D. Autophagy in cancer cell death. Biology (Basel), 2019, 8(4)E82
[http://dx.doi.org/10.3390/biology8040082] [PMID: 31671879]
[32]
Kessel, D. Autophagic death probed by photodynamic therapy. Autophagy, 2015, 11(10), 1941-1943.
[http://dx.doi.org/10.1080/15548627.2015.1078960] [PMID: 26313747]
[33]
Kessel, D. Pathways to paraptosis after ER photodamage in OVCAR-5 cells. Photochem. Photobiol., 2019, 95(5), 1239-1242.
[http://dx.doi.org/10.1111/php.13103] [PMID: 30924537]
[34]
Haapasalo, K.; Meri, S. Regulation of the complement system by pentraxins. Front. Immunol., 2019, 10, 1750.
[http://dx.doi.org/10.3389/fimmu.2019.01750] [PMID: 31428091]
[35]
Garg, A.D.; Krysko, D.V.; Vandenabeele, P.; Agostinis, P. DAMPs and PDT-mediated photo-oxidative stress: Exploring the unknown. Photochem. Photobiol. Sci., 2011, 10(5), 670-680.
[http://dx.doi.org/10.1039/c0pp00294a] [PMID: 21258717]
[36]
Voskoboinik, I.; Whisstock, J.C.; Trapani, J.A. Perforin and granzymes: Function, dysfunction and human pathology. Nat. Rev. Immunol., 2015, 15(6), 388-400.
[http://dx.doi.org/10.1038/nri3839] [PMID: 25998963]
[37]
Chraa, D.; Naim, A.; Olive, D.; Badou, A. T lymphocyte subsets in cancer immunity: Friends or foes. J. Leukoc. Biol., 2019, 105(2), 243-255.
[http://dx.doi.org/10.1002/JLB.MR0318-097R] [PMID: 30387907]
[38]
Chen, K.; Kolls, J.K. Interluekin-17A (IL17A). Gene, 2017, 614, 8-14.
[http://dx.doi.org/10.1016/j.gene.2017.01.016] [PMID: 28122268]
[39]
Hendrzak-Henion, J.A.; Knisely, T.L.; Cincotta, L.; Cincotta, E.; Cincotta, A.H. Role of the immune system in mediating the antitumor effect of benzophenothiazine photodynamic therapy. Photochem. Photobiol., 1999, 69(5), 575-581.
[http://dx.doi.org/10.1111/j.1751-1097.1999.tb03330.x] [PMID: 10333764]
[40]
Rocha, L.B.; Gomes-da-Silva, L.C.; Dąbrowski, J.M.; Arnaut, L.G. Elimination of primary tumours and control of metastasis with rationally designed bacteriochlorin photodynamic therapy regimens. Eur. J. Cancer, 2015, 51(13), 1822-1830.
[http://dx.doi.org/10.1016/j.ejca.2015.06.002] [PMID: 26139544]
[41]
Castellino, F.; Germain, R.N. Cooperation between CD4+ and CD8+ T cells: When, where, and how. Annu. Rev. Immunol., 2006, 24, 519-540.
[http://dx.doi.org/10.1146/annurev.immunol.23.021704.115825] [PMID: 16551258]
[42]
Castano, A.P.; Mroz, P.; Wu, M.X.; Hamblin, M.R. Photodynamic therapy plus low-dose cyclophosphamide generates antitumor immunity in a mouse model. Proc. Natl. Acad. Sci. USA, 2008, 105(14), 5495-5500.
[http://dx.doi.org/10.1073/pnas.0709256105] [PMID: 18378905]
[43]
Brackett, C.M.; Muhitch, J.B.; Evans, S.S.; Gollnick, S.O. IL-17 promotes neutrophil entry into tumor-draining lymph nodes following induction of sterile inflammation. J. Immunol., 2013, 191(8), 4348-4357.
[http://dx.doi.org/10.4049/jimmunol.1103621] [PMID: 24026079]
[44]
de Vree, W.J.; Essers, M.C.; de Bruijn, H.S.; Star, W.M.; Koster, J.F.; Sluiter, W. Evidence for an important role of neutrophils in the efficacy of photodynamic therapy in vivo. Cancer Res., 1996, 56(13), 2908-2911.
[PMID: 8674038]
[45]
Schuitmaker, J.J.; de Koster, B.M.; Elferink, J.G. The effects of photodynamic therapy on human neutrophil migration using bacteriochlorin A. Photochem. Photobiol., 1998, 68(6), 841-845.
[http://dx.doi.org/10.1111/j.1751-1097.1998.tb05293.x] [PMID: 9867034]
[46]
Sun, J.; Cecic, I.; Parkins, C.S.; Korbelik, M. Neutrophils as inflammatory and immune effectors in photodynamic therapy-treated mouse SCCVII tumours. Photochem. Photobiol. Sci., 2002, 1(9), 690-695.
[http://dx.doi.org/10.1039/b204254a]] [PMID: 12665307]
[47]
Cecic, I.; Korbelik, M. Mediators of peripheral blood neutrophilia induced by photodynamic therapy of solid tumors. Cancer Lett., 2002, 183(1), 43-51.
[http://dx.doi.org/10.1016/S0304-3835(02)00092-7] [PMID: 12049813]
[48]
Kousis, P.C.; Henderson, B.W.; Maier, P.G.; Gollnick, S.O. Photodynamic therapy enhancement of antitumor immunity is regulated by neutrophils. Cancer Res., 2007, 67(21), 10501-10510.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-1778] [PMID: 17974994]
[49]
Gollnick, S.O.; Evans, S.S.; Baumann, H.; Owczarczak, B.; Maier, P.; Vaughan, L.; Wang, W.C.; Unger, E.; Henderson, B.W. Role of cytokines in photodynamic therapy-induced local and systemic inflammation. Br. J. Cancer, 2003, 88(11), 1772-1779.
[http://dx.doi.org/10.1038/sj.bjc.6600864] [PMID: 12771994]
[50]
Korbelik, M.; Cecic, I. Complement activation cascade and its regulation: relevance for the response of solid tumors to photodynamic therapy. J. Photochem. Photobiol. B, 2008, 93(1), 53-59.
[http://dx.doi.org/10.1016/j.jphotobiol.2008.04.005] [PMID: 18715798]
[51]
Korbelik, M.; Cecic, I.; Merchant, S.; Sun, J. Acute phase response induction by cancer treatment with photodynamic therapy. Int. J. Cancer, 2008, 122(6), 1411-1417.
[http://dx.doi.org/10.1002/ijc.23248] [PMID: 18033689]
[52]
Park, M.J.; Bae, J.H.; Chung, J.S.; Kim, S.H.; Kang, C.D. Induction of NKG2D ligands and increased sensitivity of tumor cells to NK cell-mediated cytotoxicity by hematoporphyrin-based photodynamic therapy. Immunol. Invest., 2011, 40(4), 367-382.
[http://dx.doi.org/10.3109/08820139.2010.551435] [PMID: 21314289]
[53]
Belicha-Villanueva, A.; Riddell, J.; Bangia, N.; Gollnick, S.O. The effect of photodynamic therapy on tumor cell expression of Major Histocompatibility Complex (MHC) class I and MHC class I-related molecules. Lasers Surg. Med., 2012, 44(1), 60-68.
[http://dx.doi.org/10.1002/lsm.21160] [PMID: 22246985]
[54]
Kabingu, E.; Vaughan, L.; Owczarczak, B.; Ramsey, K.D.; Gollnick, S.O. CD8+ T cell-mediated control of distant tumours following local photodynamic therapy is independent of CD4+ T cells and dependent on natural killer cells. Br. J. Cancer, 2007, 96(12), 1839-1848.
[http://dx.doi.org/10.1038/sj.bjc.6603792] [PMID: 17505510]
[55]
Volkman, A.; Gowans, J.L. The origin of macrophages from bone marrow in the rat. Br. J. Exp. Pathol., 1965, 46, 62-70.
[PMID: 14295560]
[56]
Guilliams, M.; Ginhoux, F.; Jakubzick, C.; Naik, S.H.; Onai, N.; Schraml, B.U.; Segura, E.; Tussiwand, R.; Yona, S. Dendritic cells, monocytes and macrophages: A unified nomenclature based on ontogeny. Nat. Rev. Immunol., 2014, 14(8), 571-578.
[http://dx.doi.org/10.1038/nri3712] [PMID: 25033907]
[57]
Steinman, R.M.; Cohn, Z.A. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J. Exp. Med., 1973, 137(5), 1142-1162.
[http://dx.doi.org/10.1084/jem.137.5.1142] [PMID: 4573839]
[58]
Makala, L.H.; Nagasawa, H. Dendritic cells: A specialized complex system of antigen presenting cells. J. Vet. Med. Sci., 2002, 64(3), 181-193.
[http://dx.doi.org/10.1292/jvms.64.181] [PMID: 11999435]
[59]
Martinez, F.O.; Gordon, S. The M1 and M2 paradigm of macrophage activation: Time for reassessment. F1000Prime Rep., 2014, 6, 13.
[http://dx.doi.org/10.12703/P6-13] [PMID: 24669294]
[60]
Qian, B.Z.; Pollard, J.W. Macrophage diversity enhances tumor progression and metastasis. Cell, 2010, 141(1), 39-51.
[http://dx.doi.org/10.1016/j.cell.2010.03.014] [PMID: 20371344]
[61]
Mantovani, A.; Marchesi, F.; Malesci, A.; Laghi, L.; Allavena, P. Tumour-associated macrophages as treatment targets in oncology. Nat. Rev. Clin. Oncol., 2017, 14(7), 399-416.
[http://dx.doi.org/10.1038/nrclinonc.2016.217] [PMID: 28117416]
[62]
Korbelik, M.; Krosl, G. Photofrin accumulation in malignant and host cell populations of various tumours. Br. J. Cancer, 1996, 73(4), 506-513.
[http://dx.doi.org/10.1038/bjc.1996.88] [PMID: 8595166]
[63]
Demidova, T.N.; Hamblin, M.R. Macrophage-targeted photodynamic therapy. Int. J. Immunopathol. Pharmacol., 2004, 17(2), 117-126.
[http://dx.doi.org/10.1177/039463200401700203] [PMID: 15171812]
[64]
Collin, M.; Bigley, V. Human dendritic cell subsets: An update. Immunology, 2018, 154(1), 3-20.
[http://dx.doi.org/10.1111/imm.12888] [PMID: 29313948]
[65]
Worbs, T.; Hammerschmidt, S.I.; Förster, R. Dendritic cell migration in health and disease. Nat. Rev. Immunol., 2017, 17(1), 30-48.
[http://dx.doi.org/10.1038/nri.2016.116] [PMID: 27890914]
[66]
Preise, D.; Oren, R.; Glinert, I.; Kalchenko, V.; Jung, S.; Scherz, A.; Salomon, Y. Systemic antitumor protection by vascular-targeted photodynamic therapy involves cellular and humoral immunity. Cancer Immunol. Immunother., 2009, 58(1), 71-84.
[http://dx.doi.org/10.1007/s00262-008-0527-0] [PMID: 18488222]
[67]
Jalili, A.; Makowski, M.; Switaj, T.; Nowis, D.; Wilczynski, G.M.; Wilczek, E.; Chorazy-Massalska, M.; Radzikowska, A.; Maslinski, W.; Biały, L.; Sienko, J.; Sieron, A.; Adamek, M.; Basak, G.; Mróz, P.; Krasnodebski, I.W.; Jakóbisiak, M.; Gołab, J. Effective photoimmunotherapy of murine colon carcinoma induced by the combination of photodynamic therapy and dendritic cells. Clin. Cancer Res., 2004, 10(13), 4498-4508.
[http://dx.doi.org/10.1158/1078-0432.CCR-04-0367] [PMID: 15240542]
[68]
Saji, H.; Song, W.; Furumoto, K.; Kato, H.; Engleman, E.G. Systemic antitumor effect of intratumoral injection of dendritic cells in combination with local photodynamic therapy. Clin. Cancer Res., 2006, 12(8), 2568-2574.
[http://dx.doi.org/10.1158/1078-0432.CCR-05-1986] [PMID: 16638867]
[69]
Ly, L.V.; Sluijter, M.; Versluis, M.; Luyten, G.P.; van Stipdonk, M.J.; van der Burg, S.H.; Melief, C.J.; Jager, M.J.; van Hall, T. Peptide vaccination after T-cell transfer causes massive clonal expansion, tumor eradication, and manageable cytokine storm. Cancer Res., 2010, 70(21), 8339-8346.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-2288] [PMID: 20940397]
[70]
Mathé, G. Suppressor T-cells. Biomed. Pharmacother., 1999, 53(5-6), 213-217.
[http://dx.doi.org/10.1016/S0753-3322(99)80090-0] [PMID: 10424241]
[71]
Chess, L.; Jiang, H. Resurrecting CD8+ suppressor T cells. Nat. Immunol., 2004, 5(5), 469-471.
[http://dx.doi.org/10.1038/ni0504-469] [PMID: 15116110]
[72]
Peng, G.L.; Li, L.; Guo, Y.W.; Yu, P.; Yin, X.J.; Wang, S.; Liu, C.P. CD8+ cytotoxic and FoxP3+ regulatory T lymphocytes serve as prognostic factors in breast cancer. Am. J. Transl. Res., 2019, 11(8), 5039-5053.
[PMID: 31497220]
[73]
Corsini, E.; Oukka, M.; Pieters, R.; Kerkvliet, N.I.; Ponce, R.; Germolec, D.R. Alterations in regulatory T-cells: Rediscovered pathways in immunotoxicology. J. Immunotoxicol., 2011, 8(4), 251-257.
[http://dx.doi.org/10.3109/1547691X.2011.598885] [PMID: 21848365]
[74]
Oleinika, K.; Nibbs, R.J.; Graham, G.J.; Fraser, A.R. Suppression, subversion and escape: the role of regulatory T cells in cancer progression. Clin. Exp. Immunol., 2013, 171(1), 36-45.
[http://dx.doi.org/10.1111/j.1365-2249.2012.04657.x] [PMID: 23199321]
[75]
Nicolini, A.; Mancini, P.; Ferrari, P.; Anselmi, L.; Tartarelli, G.; Bonazzi, V.; Carpi, A.; Giardino, R. Oral low-dose cyclophosphamide in Metastatic Hormone Refractory Prostate Cancer (MHRPC). Biomed. Pharmacother., 2004, 58(8), 447-450.
[http://dx.doi.org/10.1016/j.biopha.2004.08.006] [PMID: 15464874]
[76]
Madondo, M.T.; Quinn, M.; Plebanski, M. Low dose cyclophosphamide: Mechanisms of T cell modulation. Cancer Treat. Rev., 2016, 42, 3-9.
[http://dx.doi.org/10.1016/j.ctrv.2015.11.005] [PMID: 26620820]
[77]
Zhao, J.; Cao, Y.; Lei, Z.; Yang, Z.; Zhang, B.; Huang, B. Selective depletion of CD4+CD25+Foxp3+ regulatory T cells by low-dose cyclophosphamide is explained by reduced intracellular ATP levels. Cancer Res., 2010, 70(12), 4850-4858.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-0283] [PMID: 20501849]
[78]
Gollnick, S.O.; Vaughan, L.; Henderson, B.W. Generation of effective antitumor vaccines using photodynamic therapy. Cancer Res., 2002, 62(6), 1604-1608.
[PMID: 11912128]
[79]
Korbelik, M.; Sun, J. Photodynamic therapy-generated vaccine for cancer therapy. Cancer Immunol. Immunother., 2006, 55(8), 900-909.
[http://dx.doi.org/10.1007/s00262-005-0088-4] [PMID: 16215717]
[80]
Garg, A.D.; Vandenberk, L.; Koks, C.; Verschuere, T.; Boon, L.; Van Gool, S.W.; Agostinis, P. Dendritic cell vaccines based on immunogenic cell death elicit danger signals and T cell-driven rejection of high-grade glioma. Sci. Transl. Med., 2016, 8(328)328ra27
[http://dx.doi.org/10.1126/scitranslmed.aae0105] [PMID: 26936504]
[81]
Zheng, Y.; Yin, G.; Le, V.; Zhang, A.; Lu, Y.; Yang, M.; Fei, Z.; Liu, J. .Hypericin-based photodynamic therapy induces a tumorspecific immune response and an effective DC-based cancer immunotherapy. Biochem. Pharmacol., 2014, S0006-2952(14), 00075-00076.
[http://dx.doi.org/10.1016/j.bcp.2014.01.036] [PMID: 24508834]
[82]
Garg, A.D.; Nowis, D.; Golab, J.; Agostinis, P. Photodynamic therapy: Illuminating the road from cell death towards anti-tumour immunity. Apoptosis, 2010, 15(9), 1050-1071.
[http://dx.doi.org/10.1007/s10495-010-0479-7] [PMID: 20221698]
[83]
Korbelik, M.; Cecic, I. Enhancement of tumour response to photodynamic therapy by adjuvant mycobacterium cell-wall treatment. J. Photochem. Photobiol. B, 1998, 44(2), 151-158.
[http://dx.doi.org/10.1016/S1011-1344(98)00138-9] [PMID: 9757597]
[84]
Henderson, B.W.; Busch, T.M.; Snyder, J.W. Fluence rate as a modulator of PDT mechanisms. Lasers Surg. Med., 2006, 38(5), 489-493.
[http://dx.doi.org/10.1002/lsm.20327] [PMID: 16615136]
[85]
Sitnik, T.M.; Henderson, B.W. The effect of fluence rate on tumor and normal tissue responses to photodynamic therapy. Photochem. Photobiol., 1998, 67(4), 462-466.
[http://dx.doi.org/10.1111/j.1751-1097.1998.tb05228.x] [PMID: 9559590]
[86]
Henderson, B.W.; Gollnick, S.O.; Snyder, J.W.; Busch, T.M.; Kousis, P.C.; Cheney, R.T.; Morgan, J. Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors. Cancer Res., 2004, 64(6), 2120-2126.
[http://dx.doi.org/10.1158/0008-5472.CAN-03-3513] [PMID: 15026352]
[87]
Fefer, A.; McCoy, J.L.; Perk, K.; Glynn, J.P. Immunologic, virologic, and pathologic studies of regression of autochthonous Moloney sarcoma virus-induced tumors in mice. Cancer Res., 1968, 28(8), 1577-1585.
[PMID: 4876979]
[88]
Miller, B.E.; Miller, F.R.; Leith, J.; Heppner, G.H. Growth interaction in vivo between tumor subpopulations derived from a single mouse mammary tumor. Cancer Res., 1980, 40(11), 3977-3981.
[PMID: 7471048]
[89]
Koppi, T.A.; Halliday, W.J. Regulation of cell-mediated immunologic reactivity to Moloney murine sarcoma virus-induced tumors. I. Cell and serum activity detected by leukocyte adherence inhibition. J. Natl. Cancer Inst., 1981, 66(6), 1089-1096.
[http://dx.doi.org/10.1093/jnci/66.6.1089] [PMID: 6264193]
[90]
Dietz, M.; Longley, C.; Fouchey, S.P.; Hall, L.; Rich, M.A.; Furmanski, P. Spontaneous regression of Friend virus-induced erythroleukemia. II. regression of Friend murine leukemia virus-induced lymphocytic leukemia. J. Natl. Cancer Inst., 1977, 59(3), 957-961.
[http://dx.doi.org/10.1093/jnci/59.3.957] [PMID: 197250]
[91]
Patel, A.; Halliday, G.M.; Barnetson, R.S. CD4+ T lymphocyte infiltration correlates with regression of a UV-induced squamous cell carcinoma. J. Dermatol. Sci., 1995, 9(1), 12-19.
[http://dx.doi.org/10.1016/0923-1811(94)00344-E] [PMID: 7727352]
[92]
Pelletier, H.; Olsson, N.O.; Lizard, G.; Martin, F. Cytotoxic activity of lymphocytes infiltrating progressive and regressive tumor variants from a rat colonic cancer. Immunobiology, 1991, 182(2), 188-196.
[http://dx.doi.org/10.1016/S0171-2985(11)80203-2] [PMID: 1885206]
[93]
Khar, A.; Anjum, R. Host-tumor interactions during the regression of a rat histiocytoma, AK-5. Immunol. Rev., 2001, 184, 244-257.
[http://dx.doi.org/10.1034/j.1600-065x.2001.1840122.x] [PMID: 12086317]
[94]
Jaffee, E.M.; Pardoll, D.M. Murine tumor antigens: Is it worth the search? Curr. Opin. Immunol., 1996, 8(5), 622-627.
[http://dx.doi.org/10.1016/S0952-7915(96)80077-X] [PMID: 8902386]
[95]
Clarke, S.R.; Barnden, M.; Kurts, C.; Carbone, F.R.; Miller, J.F.; Heath, W.R. Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol. Cell Biol., 2000, 78(2), 110-117.
[http://dx.doi.org/10.1046/j.1440-1711.2000.00889.x] [PMID: 10762410]
[96]
Castano, A.P.; Liu, Q.; Hamblin, M.R. A green fluorescent protein-expressing murine tumour but not its wild-type counterpart is cured by photodynamic therapy. Br. J. Cancer, 2006, 94(3), 391-397.
[http://dx.doi.org/10.1038/sj.bjc.6602953] [PMID: 16421588]
[97]
Kemmler, C.B.; Clambey, E.T.; Kedl, R.M.; Slansky, J.E. Elevated tumor-associated antigen expression suppresses variant peptide vaccine responses. J. Immunol., 2011, 187(9), 4431-4439.
[http://dx.doi.org/10.4049/jimmunol.1101555] [PMID: 21940675]
[98]
McWilliams, J.A.; Sullivan, R.T.; Jordan, K.R.; McMahan, R.H.; Kemmler, C.B.; McDuffie, M.; Slansky, J.E. Age-dependent tolerance to an endogenous tumor-associated antigen. Vaccine, 2008, 26(15), 1863-1873.
[http://dx.doi.org/10.1016/j.vaccine.2008.01.052] [PMID: 18329760]
[99]
Reginato, E.; Lindenmann, J.; Langner, C.; Schweintzger, N.; Bambach, I.; Smolle-Jüttner, F.; Wolf, P. Photodynamic therapy downregulates the function of regulatory T cells in patients with esophageal squamous cell carcinoma. Photochem. Photobiol. Sci., 2014, 13(9), 1281-1289.
[http://dx.doi.org/10.1039/C4PP00186A] [PMID: 25005268]
[100]
Guo, Z.S.; Hong, J.A.; Irvine, K.R.; Chen, G.A.; Spiess, P.J.; Liu, Y.; Zeng, G.; Wunderlich, J.R.; Nguyen, D.M.; Restifo, N.P.; Schrump, D.S. De novo induction of a cancer/testis antigen by 5-aza-2′-deoxycytidine augments adoptive immunotherapy in a murine tumor model. Cancer Res., 2006, 66(2), 1105-1113.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-3020] [PMID: 16424047]
[101]
Kleinovink, J.W.; van Driel, P.B.; Snoeks, T.J.; Prokopi, N.; Fransen, M.F.; Cruz, L.J.; Mezzanotte, L.; Chan, A.; Löwik, C.W.; Ossendorp, F. Combination of photodynamic therapy and specific immunotherapy efficiently eradicates established tumors. Clin. Cancer Res., 2016, 22(6), 1459-1468.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0515] [PMID: 26546617]
[102]
Lin, K.Y.; Guarnieri, F.G.; Staveley-O’Carroll, K.F.; Levitsky, H.I.; August, J.T.; Pardoll, D.M.; Wu, T.C. Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res., 1996, 56(1), 21-26.
[PMID: 8548765]
[103]
Ljunggren, H.G.; Kärre, K. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J. Exp. Med., 1985, 162(6), 1745-1759.
[http://dx.doi.org/10.1084/jem.162.6.1745] [PMID: 3877776]
[104]
Playfair, J.H. Strain differences in the immune response of mice. I. The neonatal response to sheep red cells. Immunology, 1968, 15(1), 35-50.
[PMID: 5664400]
[105]
Li, J.K.; Balic, J.J.; Yu, L.; Jenkins, B. TLR agonists as adjuvants for cancer vaccines. Adv. Exp. Med. Biol., 2017, 1024, 195-212.
[http://dx.doi.org/10.1007/978-981-10-5987-2_9] [PMID: 28921471]
[106]
Korbelik, M.; Sun, J.; Posakony, J.J. Interaction between photodynamic therapy and BCG immunotherapy responsible for the reduced recurrence of treated mouse tumors. Photochem. Photobiol., 2001, 73(4), 403-409.
[http://dx.doi.org/10.1562/0031-8655(2001)073<0403:IBPTAB>2.0.CO;2] [PMID: 11332036]
[107]
Xia, Y.; Gupta, G.K.; Castano, A.P.; Mroz, P.; Avci, P.; Hamblin, M.R. CpG oligodeoxynucleotide as immune adjuvant enhances photodynamic therapy response in murine metastatic breast cancer. J. Biophotonics, 2014, 7(11-12), 897-905.
[http://dx.doi.org/10.1002/jbio.201300072] [PMID: 23922221]
[108]
Bhatta, A.K.; Wang, P.; Keyal, U.; Zhao, Z.; Ji, J.; Zhu, L.; Wang, X.; Zhang, G. Therapeutic effect of Imiquimod enhanced ALA-PDT on cutaneous squamous cell carcinoma. Photodiagn. Photodyn. Ther., 2018, 23, 273-280.
[http://dx.doi.org/10.1016/j.pdpdt.2018.07.010] [PMID: 30030167]
[109]
Brown, G.D.; Willment, J.A.; Whitehead, L. C-type lectins in immunity and homeostasis. Nat. Rev. Immunol., 2018, 18(6), 374-389.
[http://dx.doi.org/10.1038/s41577-018-0004-8] [PMID: 29581532]
[110]
Korbelik, M.; Sun, J.; Cecic, I.; Serrano, K. Adjuvant treatment for complement activation increases the effectiveness of photodynamic therapy of solid tumors. Photochem. Photobiol. Sci., 2004, 3(8), 812-816.
[http://dx.doi.org/10.1039/b315663j] [PMID: 15295639]
[111]
Krosl, G.; Korbelik, M. Potentiation of photodynamic therapy by immunotherapy: The effect of Schizophyllan (SPG). Cancer Lett., 1994, 84(1), 43-49.
[http://dx.doi.org/10.1016/0304-3835(94)90356-5] [PMID: 8076362]
[112]
Akramiene, D.; Aleksandraviciene, C.; Grazeliene, G.; Zalinkevicius, R.; Suziedelis, K.; Didziapetriene, J.; Simonsen, U.; Stankevicius, E.; Kevelaitis, E. Potentiating effect of beta-glucans on photodynamic therapy of implanted cancer cells in mice. Tohoku J. Exp. Med., 2010, 220(4), 299-306.
[http://dx.doi.org/10.1620/tjem.220.299] [PMID: 20410681]
[113]
Korbelik, M.; Banáth, J.; Zhang, W.; Gallagher, P.; Hode, T.; Lam, S.S.K.; Chen, W.R. N-dihydrogalactochitosan as immune and direct antitumor agent amplifying the effects of photodynamic therapy and photodynamic therapy-generated vaccines. Int. Immunopharmacol., 2019, 75105764
[http://dx.doi.org/10.1016/j.intimp.2019.105764] [PMID: 31352327]
[114]
Korbelik, M.; Zhang, W.; Saw, K.M.; Szulc, Z.M.; Bielawska, A.; Separovic, D. Cationic ceramides and analogues, LCL30 and LCL85, as adjuvants to photodynamic therapy of tumors. J. Photochem. Photobiol. B, 2013, 126, 72-77.
[http://dx.doi.org/10.1016/j.jphotobiol.2013.06.013] [PMID: 23911762]
[115]
Korbelik, M.; Cooper, P.D. Potentiation of photodynamic therapy of cancer by complement: the effect of gamma-inulin. Br. J. Cancer, 2007, 96(1), 67-72.
[http://dx.doi.org/10.1038/sj.bjc.6603508] [PMID: 17146472]
[116]
Korbelik, M.; Banáth, J.; Saw, K.M.; Zhang, W.; Čiplys, E. Calreticulin as cancer treatment adjuvant: combination with photodynamic therapy and photodynamic therapy-generated vaccines. Front. Oncol., 2015, 5, 15.
[http://dx.doi.org/10.3389/fonc.2015.00015] [PMID: 25692097]
[117]
Gutting, T.; Burgermeister, E.; Härtel, N.; Ebert, M.P. Checkpoints and beyond - Immunotherapy in colorectal cancer. Semin. Cancer Biol., 2019, 55, 78-89.
[http://dx.doi.org/10.1016/j.semcancer.2018.04.003] [PMID: 29716829]
[118]
Hargadon, K.M.; Johnson, C.E.; Williams, C.J. Immune checkpoint blockade therapy for cancer: An overview of FDA-approved immune checkpoint inhibitors. Int. Immunopharmacol., 2018, 62, 29-39.
[http://dx.doi.org/10.1016/j.intimp.2018.06.001] [PMID: 29990692]
[119]
Lo, B.; Abdel-Motal, U.M. Lessons from CTLA-4 deficiency and checkpoint inhibition. Curr. Opin. Immunol., 2017, 49, 14-19.
[http://dx.doi.org/10.1016/j.coi.2017.07.014] [PMID: 28806575]
[120]
Sharpe, A.H.; Pauken, K.E. The diverse functions of the PD1 inhibitory pathway. Nat. Rev. Immunol., 2018, 18(3), 153-167.
[http://dx.doi.org/10.1038/nri.2017.108] [PMID: 28990585]
[121]
Kleinovink, J.W.; Fransen, M.F.; Löwik, C.W.; Ossendorp, F. Photodynamic-immune checkpoint therapy eradicates local and distant tumors by CD8+ T cells. Cancer Immunol. Res., 2017, 5(10), 832-838.
[http://dx.doi.org/10.1158/2326-6066.CIR-17-0055] [PMID: 28851692]
[122]
Bao, R.; Wang, Y.; Lai, J.; Zhu, H.; Zhao, Y.; Li, S.; Li, N.; Huang, J.; Yang, Z.; Wang, F.; Liu, Z. Enhancing anti-PD-1/PD-L1 immune checkpoint inhibitory cancer therapy by CD276-targeted photodynamic ablation of tumor cells and tumor vasculature. Mol. Pharm., 2019, 16(1), 339-348.
[http://dx.doi.org/10.1021/acs.molpharmaceut.8b00997] [PMID: 30452269]
[123]
Duan, X.; Chan, C.; Guo, N.; Han, W.; Weichselbaum, R.R.; Lin, W. Photodynamic therapy mediated by nontoxic core-shell nanoparticles synergizes with immune checkpoint blockade to elicit antitumor immunity and antimetastatic effect on breast cancer. J. Am. Chem. Soc., 2016, 138(51), 16686-16695.
[http://dx.doi.org/10.1021/jacs.6b09538] [PMID: 27976881]
[124]
Xu, J.; Xu, L.; Wang, C.; Yang, R.; Zhuang, Q.; Han, X.; Dong, Z.; Zhu, W.; Peng, R.; Liu, Z. Near-infrared-triggered photodynamic therapy with multitasking upconversion nanoparticles in combination with checkpoint blockade for immunotherapy of colorectal cancer. ACS Nano, 2017, 11(5), 4463-4474.
[http://dx.doi.org/10.1021/acsnano.7b00715] [PMID: 28362496]
[125]
Yan, S.; Zeng, X.; Tang, Y.; Liu, B.F.; Wang, Y.; Liu, X. Activating antitumor immunity and antimetastatic effect through polydopamine-encapsulated core-shell upconversion nanoparticles. Adv. Mater., 2019, 31(46)e1905825
[http://dx.doi.org/10.1002/adma.201905825] [PMID: 31566283]
[126]
Liu, Y.; Pan, Y.; Cao, W.; Xia, F.; Liu, B.; Niu, J.; Alfranca, G.; Sun, X.; Ma, L.; de la Fuente, J.M.; Song, J.; Ni, J.; Cui, D. A tumor microenvironment responsive biodegradable CaCO3/MnO2- based nanoplatform for the enhanced photodynamic therapy and improved PD-L1 immunotherapy. Theranostics, 2019, 9(23), 6867-6884.
[http://dx.doi.org/10.7150/thno.37586] [PMID: 31660074]
[127]
Wang, D.; Wang, T.; Liu, J.; Yu, H.; Jiao, S.; Feng, B.; Zhou, F.; Fu, Y.; Yin, Q.; Zhang, P.; Zhang, Z.; Zhou, Z.; Li, Y. Acid-activatable versatile micelleplexes for PD-L1 blockade-enhanced cancer photodynamic immunotherapy. Nano Lett., 2016, 16(9), 5503-5513.
[http://dx.doi.org/10.1021/acs.nanolett.6b01994] [PMID: 27525587]
[128]
He, C.; Duan, X.; Guo, N.; Chan, C.; Poon, C.; Weichselbaum, R.R.; Lin, W. Core-shell nanoscale coordination polymers combine chemotherapy and photodynamic therapy to potentiate checkpoint blockade cancer immunotherapy. Nat. Commun., 2016, 7, 12499.
[http://dx.doi.org/10.1038/ncomms12499] [PMID: 27530650]
[129]
Abdel-Hady, E.S.; Martin-Hirsch, P.; Duggan-Keen, M.; Stern, P.L.; Moore, J.V.; Corbitt, G.; Kitchener, H.C.; Hampson, I.N. Immunological and viral factors associated with the response of vulval intraepithelial neoplasia to photodynamic therapy. Cancer Res., 2001, 61(1), 192-196.
[PMID: 11196160]
[130]
Kabingu, E.; Oseroff, A.R.; Wilding, G.E.; Gollnick, S.O. Enhanced systemic immune reactivity to a Basal cell carcinoma associated antigen following photodynamic therapy. Clin. Cancer Res., 2009, 15(13), 4460-4466.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-0400] [PMID: 19549769]
[131]
Thong, P.S.; Olivo, M.; Kho, K.W.; Bhuvaneswari, R.; Chin, W.W.; Ong, K.W.; Soo, K.C. Immune response against angiosarcoma following lower fluence rate clinical photodynamic therapy. J. Environ. Pathol. Toxicol. Oncol., 2008, 27(1), 35-42.
[http://dx.doi.org/10.1615/JEnvironPatholToxicolOncol.v27.i1.40] [PMID: 18551894]
[132]
Thong, P.S.; Ong, K.W.; Goh, N.S.; Kho, K.W.; Manivasager, V.; Bhuvaneswari, R.; Olivo, M.; Soo, K.C. Photodynamic-therapy-activated immune response against distant untreated tumours in recurrent angiosarcoma. Lancet Oncol., 2007, 8(10), 950-952.
[http://dx.doi.org/10.1016/S1470-2045(07)70318-2] [PMID: 17913664]
[133]
Morrison, S.A.; Hill, S.L.; Rogers, G.S.; Graham, R.A. Efficacy and safety of continuous low-irradiance photodynamic therapy in the treatment of chest wall progression of breast cancer. J. Surg. Res., 2014, 192(2), 235-241.
[http://dx.doi.org/10.1016/j.jss.2014.06.030] [PMID: 25043529]
[134]
Santos, L.L.; Oliveira, J.; Monteiro, E.; Santos, J.; Sarmento, C. Treatment of head and neck cancer with photodynamic therapy with redaporfin: A clinical case report. Case Rep. Oncol., 2018, 11(3), 769-776.
[http://dx.doi.org/10.1159/000493423] [PMID: 30627091]
[135]
Arimatsu, A.; Tomii, K.; Fujiwara, H.; Hasegawa, G.; Shigehara, Y.; Tachibana, T. Photodynamic therapy can prevent recurrence of lymphomatoid papulosis. Photodiagn. Photodyn. Ther., 2019, 25, 334-335.
[http://dx.doi.org/10.1016/j.pdpdt.2019.01.007] [PMID: 30625399]
[136]
Hamblin, M.R. Photodynamic therapy for cancer: What’s Past is Prologue. A contribution to the Thomas J Dougherty, PhD memorial issue. Photochem. Photobiol., in press
[137]
Anzengruber, F.; Avci, P.; de Freitas, L.F.; Hamblin, M.R. T-cell mediated anti-tumor immunity after photodynamic therapy: Why does it not always work and how can we improve it? Photochem. Photobiol. Sci., 2015, 14(8), 1492-1509.
[http://dx.doi.org/10.1039/C4PP00455H] [PMID: 26062987]
[138]
Dąbrowski, J.M.; Arnaut, L.G. Photodynamic Therapy (PDT) of cancer: From local to systemic treatment. Photochem. Photobiol. Sci., 2015, 14(10), 1765-1780.
[http://dx.doi.org/10.1039/C5PP00132C] [PMID: 26219737]
[139]
Hartmann, J.; Schüßler-Lenz, M.; Bondanza, A.; Buchholz, C.J. Clinical development of CAR T cells-challenges and opportunities in translating innovative treatment concepts. EMBO Mol. Med., 2017, 9(9), 1183-1197.
[http://dx.doi.org/10.15252/emmm.201607485] [PMID: 28765140]
[140]
Krishnamurthy, A.; Jimeno, A. Bispecific antibodies for cancer therapy: A review. Pharmacol. Ther., 2018, 185, 122-134.
[http://dx.doi.org/10.1016/j.pharmthera.2017.12.002] [PMID: 29269044]
[141]
Gubin, M.M. Cancer immunology and immunotherapy: Taking a place in mainstream oncology keystone symposia meeting summary. Cancer Immunol. Res., 2017, 5(6), 434-438.
[http://dx.doi.org/10.1158/2326-6066.CIR-17-0224] [PMID: 28576922]
[142]
Slaney, C.Y.; Kershaw, M.H.; Darcy, P.K. Trafficking of T cells into tumors. Cancer Res., 2014, 74(24), 7168-7174.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-2458] [PMID: 25477332]
[143]
Block, K.I.; Gyllenhaal, C.; Lowe, L.; Amedei, A.; Amin, A.; Amin, A.; Aquilano, K.; Arbiser, J.; Arreola, A.; Arzumanyan, A.; Ashraf, S.S. Designing a broad-spectrum integrative approach for cancer prevention and treatment. Semin. Cancer Biol., 2015, 35, S276-S304.
[http://dx.doi.org/10.1016/j.semcancer.2015.09.007]

Rights & Permissions Print Cite
Article Metrics
63
© 2024 Bentham Science Publishers | Privacy Policy