Photodynamic therapy (PDT) is a clinically-approved but rather under-exploited treatment modality for cancer and pre-cancerous superficial lesions. It utilises a cold laser or LED to activate a photochemical reaction between a light activated drug (photosensitiser-drug) and oxygen to generate cytotoxic oxygen species. These free radical species damage cellular components leading to cell death. Despite its benefits, the complexity, limited potency and side effects of PDT have led to poor general usage. However, the research area is very active with an increasing understanding of PDT-related cell biology, photophysics and significant progress in molecular targeting of disease. Monoclonal antibody therapy is maturing and the next wave of antibody therapies includes antibody-drug conjugates (ADCs), which promise to be more potent and curable. These developments could lift antibody-directed phototherapy (ADP) to success. ADP promises to increase specificity and potency and improve drug pharmacokinetics, thus delivering better PDT drugs whilst retaining its other benefits. Whole antibody conjugates with first generation ADP-drugs displayed problems with aggregation, poor pharmacokinetics and loss of immuno-reactivity. However, these early ADP-drugs still showed improved selectivity and potency. Improved PS-drug chemistry and a variety of conjugation strategies have led to improved ADP-drugs with retained antibody and PS-drug function. More recently, recombinant antibody fragments have been used to deliver ADP-drugs with superior drug loading, more favourable pharmacokinetics, enhanced potency and target cell selectivity. These improvements offer a promise of better quality PDT drugs.
References
[1]
Deonarain, M.P. Recombinant antibodies for cancer therapy. Expert Opin. Biol. Ther. 2008, 8, 1123–1141, doi:10.1517/14712598.8.8.1123.
Brown, S.B.; Brown, E.A.; Walker, I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 2004, 5, 497–508, doi:10.1016/S1470-2045(04)01529-3.
[14]
Dolmans, D.E.J.G.J.; Fukumura, D.; Jain, R.K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3, 380–387, doi:10.1038/nrc1071.
[15]
Brown, S.B.; Mellish, K.J. Verteporfin: A milestone in opthalmology and photodynamic therapy. Expert Opin. Pharmacother. 2001, 2, 351–361, doi:10.1517/14656566.2.2.351.
[16]
Babilas, P.; Schreml, S.; Landthaler, M.; Szeimies, R.-M. Photodynamic therapy in dermatology: State-of-the-art. Photodermatol. Photoimmunol. Photomed. 2010, 26, 118–132, doi:10.1111/j.1600-0781.2010.00507.x.
[17]
Celli, J.P.; Spring, B.Q.; Rizvi, I.; Evans, C.L.; Samkoe, K.S.; Verma, S.; Pogue, B.W.; Hasan, T. Imaging and photodynamic therapy: mechanisms, monitoring, and optimization. Chem. Rev. 2010, 110, 2795–2838, doi:10.1021/cr900300p.
[18]
Bonnett, R. Chemical Aspects of Photodynamic Therapy; Gordon and Breach Science Publishers: Amsterdam, The Netherlands, 2000.
[19]
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.; et al. Photodynamic therapy of cancer: An update. CA Cancer J. Clin. 2011, 61, 250–281, doi:10.3322/caac.20114.
[20]
Lou, P.-J.; Jones, L.; Hopper, C. Clinical outcomes of photodynamic therapy for head-and-neck cancer. Technol. Cancer Res. Treat. 2003, 2, 311–317.
[21]
Hopper, C.; Niziol, C.; Sidhu, M. The cost-effectiveness of Foscan mediated photodynamic therapy (Foscan-PDT) compared with extensive palliative surgery and palliative chemotherapy for patients with advanced head and neck cancer in the UK. Oral Oncol. 2004, 40, 372–382, doi:10.1016/j.oraloncology.2003.09.003.
[22]
Nyst, H.J.; Tan, I.B.; Stewart, F.A.; Balm, A.J.M. Is photodynamic therapy a good alternative to surgery and radiotherapy in the treatment of head and neck cancer? Photodiagnosis Photodyn. Ther. 2009, 6, 3–11, doi:10.1016/j.pdpdt.2009.03.002.
Schweitzer, V.G.; Somers, M.L. PHOTOFRIN-mediated photodynamic therapy for treatment of early stage (Tis-T2N0M0) SqCCa of oral cavity and oropharynx. Lasers Surg. Med. 2010, 42, 1–8.
[25]
Fien, S.M.; Oseroff, A.R. Photodynamic therapy for non-melanoma skin cancer. J. Natl. Compr. Canc. Netw. 2007, 5, 531–540.
Moore, C.M.; Pendse, D.; Emberton, M. Photodynamic therapy for prostate cancer—A review of current status and future promise. Nat. Clin. Pract. Urol. 2009, 6, 18–30, doi:10.1038/ncpuro1274.
[28]
Trachtenberg, J.; Weersink, R.A.; Davidson, S.R.H.; Haider, M.A.; Bogaards, A.; Gertner, M.R.; Evans, A.; Scherz, A.; Savard, J.; Chin, J.L.; et al. Vascular-targeted photodynamic therapy (padoporfin, WST09) for recurrent prostate cancer after failure of external beam radiotherapy: a study of escalating light doses. BJU Int. 2008, 102, 556–562, doi:10.1111/j.1464-410X.2008.07753.x.
[29]
Selbo, P.K.; Weyergang, A.; Bonsted, A.; Bown, S.G.; Berg, K. Photochemical internalization of therapeutic macromolecular agents: A novel strategy to kill multidrug-resistant cancer cells. J. Pharmacol. Exp. Ther. 2006, 319, 604–612, doi:10.1124/jpet.106.109165.
[30]
Josefsen, L.B.; Boyle, R.W. Photodynamic therapy: Novel third-generation photosensitizers one step closer? Br. J. Pharmacol. 2008, 154, 1–3, doi:10.1038/bjp.2008.98.
[31]
Maisch, T. Anti-microbial photodynamic therapy: Useful in the future? Lasers Med. Sci. 2007, 22, 83–91.
Tandon, Y.K.; Yang, M.F.; Baron, E.D. Role of photodynamic therapy in psoriasis: A brief review. Photodermatol. Photoimmunol. Photomed. 2008, 24, 222–230, doi:10.1111/j.1600-0781.2008.00376.x.
[34]
van der Snoek, E.M.; Robinson, D.J.; van Hellemond, J.J.; Neumann, H.A. A review of photodynamic therapy in cutaneous leishmaniasis. J. Eur. Acad. Dermatol. Venereol. 2008, 22, 918–922, doi:10.1111/j.1468-3083.2008.02805.x.
[35]
Wilson, B.C.; Patterson, M.S. The physics, biophysics and technology of photodynamic therapy. Phys. Med. Biol. 2008, 53, R61–R109, doi:10.1088/0031-9155/53/9/R01.
[36]
Choudhary, S.; Nouri, K.; Elsaie, M.L. Photodynamic therapy in dermatology: A review. Lasers Med. Sci. 2009, 24, 971–980, doi:10.1007/s10103-009-0716-x.
[37]
Dai, T.; Huang, Y.Y.; Hamblin, M.R. Photodynamic therapy for localized infections—State of the art. Photodiagnosis Photodyn. Ther. 2009, 6, 170–188, doi:10.1016/j.pdpdt.2009.10.008.
[38]
Huang, Z.; Xu, H.; Meyers, A.D.; Musani, A.I.; Wang, L.; Tagg, R.; Barqawi, A.B.; Chen, Y.K. Photodynamic therapy for treatment of solid tumors—Potential and technical challenges. Technol. Cancer Res. Treat. 2008, 7, 309–320.
[39]
Allison, R.R.; Mota, H.C.; Bagnato, V.S.; Sibata, C.H. Bio-nanotechnology and photodynamic therapy—State of the art review. Photodiagnosis Photodyn. Ther. 2008, 5, 19–28, doi:10.1016/j.pdpdt.2008.02.001.
[40]
Mang, T.S. Lasers and light sources for PDT: Past, present and future. Photodiagnosis Photodyn. Ther. 2004, 1, 43–48, doi:10.1016/S1572-1000(04)00012-2.
[41]
Firczuk, M.; Nowis, D.; Go？？b, J. PDT-induced inflammatory and host responses. Photochem. Photobiol. Sci. 2011, 10, 653–663, doi:10.1039/c0pp00308e.
[42]
Freitas, I.; Baronzio, G.F. Tumor hypoxia, reoxygenation and oxygenation strategies: Possible role in photodynamic therapy. J. Photochem. Photobiol. B Biol. 1991, 11, 3–30, doi:10.1016/1011-1344(91)80264-I.
[43]
Ferrari, M. Frontiers in cancer nanomedicine: Directing mass transport through biological barriers. Trends Biotechnol. 2010, 28, 181–188, doi:10.1016/j.tibtech.2009.12.007.
[44]
Castano, A.P.; Demidova, T.N.; Hamblin, M.R. Mechanisms in photodynamic therapy: Part three—Photosensitizer pharmacokinetics, biodistribution, tumor localization and modes of tumor destruction. Photodiagnosis Photodyn. Ther. 2005, 2, 91–106, doi:10.1016/S1572-1000(05)00060-8.
[45]
Sternberg, E.D.; Dolphin, D.; Brückner, C. Porphyrin-based photosensitizers for use in photodynamic therapy. Tetrahedron 1998, 54, 4151–4202, doi:10.1016/S0040-4020(98)00015-5.
[46]
Konan, Y.N.; Gurny, R.; Allemann, E. State of the art in the delivery of photosensitizers for photodynamic therapy. J. Photochem. Photobiol. B 2002, 66, 89–106, doi:10.1016/S1011-1344(01)00267-6.
[47]
Sharman, W.M.; van Lier, J.E.; Allen, C.M. Targeted photodynamic therapy via receptor mediated delivery systems. Adv. Drug Deliv. Rev. 2004, 56, 53–76, doi:10.1016/j.addr.2003.08.015.
[48]
Bechet, D.; Couleaud, P.; Frochot, C.; Viriot, M.L.; Guillemin, F.; Barberi-Heyob, M. Nanoparticles as vehicles for delivery of photodynamic therapy agents. Trends Biotechnol. 2008, 26, 612–621, doi:10.1016/j.tibtech.2008.07.007.
Macdonald, I.J.; Dougherty, T.J. Basic principles of photodynamic therapy. J. Porphyr. Phthalocyanines 2001, 05, 105–129, doi:10.1002/jpp.328.
[51]
Hamblin, M.R.; Mróz, P.; Mroz, P. Advances in Photodynamic Therapy: Basic, Translational and Clinical; Artech House: Norwood, MA, USA, 2008.
[52]
Winterbourn, C.C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 2008, 4, 278–286, doi:10.1038/nchembio.85.
[53]
Redmond, R.W.; Kochevar, I.E. Spatially resolved cellular responses to singlet oxygen. Photochem. Photobiol. 2006, 82, 1178–1186, doi:10.1562/2006-04-14-IR-874.
[54]
Robertson, C.A.; Evans, D.H.; Abrahamse, H. Photodynamic therapy (PDT): A short review on cellular mechanisms and cancer research applications for PDT. J. Photochem. Photobiol. B Biol. 2009, 96, 1–8, doi:10.1016/j.jphotobiol.2009.04.001.
[55]
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, 1–21, doi:10.1039/b108586g.
[56]
Boyle, R.W.; Dolphin, D. Structure and biodistribution relationships of photodynamic sensitizers. Photochem. Photobiol. 1996, 64, 469–485, doi:10.1111/j.1751-1097.1996.tb03093.x.
[57]
Castano, A.P.; Demidova, T.N.; Hamblin, M.R. Mechanisms in photodynamic therapy: Part one—Photosensitizers, photochemistry and cellular localization. Photodiagnosis Photodyn. Ther. 2004, 1, 279–293, doi:10.1016/S1572-1000(05)00007-4.
[58]
Mojzisova, H.; Bonneau, S.; Brault, D. Structural and physico-chemical determinants of the interactions of macrocyclic photosensitizers with cells. Eur. Biophys. J. 2007, 36, 943–953, doi:10.1007/s00249-007-0204-9.
Tsaytler, P.A.; C O'Flaherty, M.; Sakharov, D.V.; Krijgsveld, J.; Egmond, M.R. Immediate protein targets of photodynamic treatment in carcinoma cells. J. Proteome Res. 2008, 7, 3868–3878, doi:10.1021/pr800189q.
[61]
Baglo, Y.; Sousa, M.M.L.; Slupphaug, G.; Hagen, L.; H？v？g, S.; Helander, L.; Zub, K.A.; Krokan, H.E.; Gederaas, O.A. Photodynamic therapy with hexyl aminolevulinate induces carbonylation, posttranslational modifications and changed expression of proteins in cell survival and cell death pathways. Photochem. Photobiol. Sci. 2011, 10, 1137–1145, doi:10.1039/c0pp00369g.
[62]
Moor, A.C. Signaling pathways in cell death and survival after photodynamic therapy. J. Photochem. Photobiol. B Biol. 2000, 57, 1–13, doi:10.1016/S1011-1344(00)00065-8.
[63]
Castano, A.P.; Demidova, T.N.; Hamblin, M.R. Mechanisms in photodynamic therapy: Part two—Cellular signaling, cell metabolism and modes of cell death. Photodiagnosis Photodyn. Ther. 2005, 2, 1–23, doi:10.1016/S1572-1000(05)00030-X.
[64]
Buytaert, E.; Dewaele, M.; Agostinis, P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim. Biophys. Acta 2007, 1776, 86–107.
[65]
Pazos, M.d.C.; Nader, H.B. Effect of photodynamic therapy on the extracellular matrix and associated components. Braz. J. Med. Biol. Res. 2007, 40, 1025–1035, doi:10.1590/S0100-879X2006005000142.
[66]
Castano, A.P.; Mroz, P.; Hamblin, M.R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 2006, 6, 535–545, doi:10.1038/nrc1894.
[67]
van Duijnhoven, F.H.; Aalbers, R.I.J.M.; Rovers, J.P.; Terpstra, O.T.; Kuppen, P.J.K. The immunological consequences of photodynamic treatment of cancer, a literature review. Immunobiology 2003, 207, 105–113, doi:10.1078/0171-2985-00221.
[68]
Korbelik, M. Cancer vaccines generated by photodynamic therapy. Photochem. Photobiol. Sci. 2011, 10, 664–669, doi:10.1039/c0pp00343c.
[69]
Wilson, B.C.; Patterson, M.S.; Lilge, L. Implicit and explicit dosimetry in photodynamic therapy: A New paradigm. Lasers Med. Sci. 1997, 12, 182–199, doi:10.1007/BF02765099.
[70]
Caldwell, J.; Gardner, I.; Swales, N. An introduction to drug disposition: The basic principles of absorption, distribution, metabolism, and excretion. Toxicol. Pathol. 1995, 23, 102–114, doi:10.1177/019262339502300202.
[71]
Ochsner, M. Photophysical and photobiological processes in the photodynamic therapy of tumours. J. Photochem. Photobiol. B 1997, 39, 1–18, doi:10.1016/S1011-1344(96)07428-3.
[72]
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, 2120–2126.
[73]
Bachor, R.; Hautmann, R.; Hasan, T. Comparison of two routes of photosensitizer administration for photodynamic therapy of bladder cancer. Urol. Res. 1994, 22, 21–23, doi:10.1007/BF00431544.
[74]
Kwitniewski, M.; Juzeniene, A.; Glosnicka, R.; Moan, J. Immunotherapy: A way to improve the therapeutic outcome of photodynamic therapy? Photochem. Photobiol. Sci. 2008, 7, 1011–1017, doi:10.1039/b806710d.
[75]
Bown, S.G.; Rogowska, A.Z.; Whitelaw, D.E.; Lees, W.R.; Lovat, L.B.; Ripley, P.; Jones, L.; Wyld, P.; Gillams, A.; Hatfield, A.W. Photodynamic therapy for cancer of the pancreas. Gut 2002, 50, 549–557, doi:10.1136/gut.50.4.549.
[76]
Nelson, A.L.; Reichert, J.M. Development trends for therapeutic antibody fragments. Nat. Biotechnol. 2009, 27, 331–337, doi:10.1038/nbt0409-331.
[77]
Deyev, S.M.; Lebedenko, E.N. Multivalency: The hallmark of antibodies used for optimization of tumor targeting by design. Bioessays 2008, 30, 904–918, doi:10.1002/bies.20805.
Roopenian, D.C.; Akilesh, S. FcRn: The neonatal Fc receptor comes of age. Nat. Rev. Immunol. 2007, 7, 715–725, doi:10.1038/nri2155.
[80]
Golay, J.; Introna, M. Mechanism of action of therapeutic monoclonal antibodies: Promises and pitfalls of in vitro and in vivo assays. Arch. Biochem. Biophys. 2012, 526, 146–153, doi:10.1016/j.abb.2012.02.011.
[81]
Arnold, J.N.; Wormald, M.R.; Sim, R.B.; Rudd, P.M.; Dwek, R.A. The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 2007, 25, 21–50, doi:10.1146/annurev.immunol.25.022106.141702.
[82]
Rothlisberger, D.; Honegger, A.; Pluckthun, A. Domain interactions in the Fab fragment: a comparative evaluation of the single-chain Fv and Fab format engineered with variable domains of different stability. J. Mol. Biol. 2005, 347, 773–789, doi:10.1016/j.jmb.2005.01.053.
[83]
Quintero-Hernández, V.; Del Pozo-Yauner, L.; Pedraza-Escalona, M.; Juárez-González, V.R.; Alcántara-Recillas, I.; Possani, L.D.; Becerril, B. Evaluation of three different formats of a neutralizing single chain human antibody against toxin Cn2: Neutralization capacity versus thermodynamic stability. Immunol. Lett. 2012, 143, 152–160, doi:10.1016/j.imlet.2012.01.010.
[84]
Carmichael, J.A.; Power, B.E.; Garrett, T.P.J.; Yazaki, P.J.; Shively, J.E.; Raubischek, A.A.; Wu, A.M.; Hudson, P.J. The crystal structure of an anti-CEA scFv diabody assembled from T84.66 scFvs in V(L)-to-V(H) orientation: implications for diabody flexibility. J. Mol. Biol. 2003, 326, 341–351.
[85]
Kipriyanov, S.M.; Moldenhauer, G.; Braunagel, M.; Reusch, U.; Cochlovius, B.; Le Gall, F.; Kouprianova, O.A.; Von der Lieth, C.W.; Little, M. Effect of domain order on the activity of bacterially produced bispecific single-chain Fv antibodies. J. Mol. Biol. 2003, 330, 99–111, doi:10.1016/S0022-2836(03)00526-6.
Todorovska, A.; Roovers, R.C.; Dolezal, O.; Kortt, A.A.; Hoogenboom, H.R.; Hudson, P.J. Design and application of diabodies, triabodies and tetrabodies for cancer targeting. J. Immunol. Methods 2001, 248, 47–66, doi:10.1016/S0022-1759(00)00342-2.
[88]
Kenanova, V.; Wu, A.M. Tailoring antibodies for radionuclide delivery. Expert Opin. Drug Deliv. 2006, 3, 53–70, doi:10.1517/17425247.3.1.53.
[89]
Yuan, F.; Dellian, M.; Fukumura, D.; Leunig, M.; Berk, D.A.; Torchilin, V.P.; Jain, R.K. Vascular permeability in a human tumor xenograft: Molecular size dependence and cutoff size. Cancer Res. 1995, 55, 3752–3756.
[90]
Batra, S.K.; Jain, M.; Wittel, U.A.; Chauhan, S.C.; Colcher, D. Pharmacokinetics and biodistribution of genetically engineered antibodies. Curr. Opin. Biotechnol. 2002, 13, 603–608, doi:10.1016/S0958-1669(02)00352-X.
[91]
Rudnick, S.I.; Adams, G.P. Affinity and avidity in antibody-based tumor targeting. Cancer Biother. Radiopharm. 2009, 24, 155–161, doi:10.1089/cbr.2009.0627.
[92]
Dahle, J.; Bagdonas, S.; Kaalhus, O.; Olsen, G.; Steen, H.B.; Moan, J. The bystander effect in photodynamic inactivation of cells. Biochim. Biophys. Acta 2000, 1475, 273–280, doi:10.1016/S0304-4165(00)00077-5.
[93]
Rubio, N.; Fleury, S.P.; Redmond, R.W. Spatial and temporal dynamics of in vitro photodynamic cell killing: Extracellular hydrogen peroxide mediates neighbouring cell death. Photochem. Photobiol. Sci. 2009, 8, 457–464, doi:10.1039/b815343d.
[94]
Birchler, M.; Viti, F.; Zardi, L.; Spiess, B.; Neri, D. Selective targeting and photocoagulation of ocular angiogenesis mediated by a phage-derived human antibody fragment. Nat. Biotechnol. 1999, 17, 984–988, doi:10.1038/13679.
[95]
Conlon, K.A.; Berrios, M. Light-induced proteolysis of myosin heavy chain by Rose Bengal-conjugated antibody complexes. J. Photochem. Photobiol. B 2001, 65, 22–28, doi:10.1016/S1011-1344(01)00241-X.
[96]
Conlon, K.A.; Rosenquist, T.; Berrios, M. Site-directed photochemical disruption of the actin cytoskeleton by actin-binding Rose Bengal-conjugates. J. Photochem. Photobiol. B 2002, 68, 140–146, doi:10.1016/S1011-1344(02)00382-2.
Giuntini, F.; Alonso, C.M.A.; Boyle, R.W. Synthetic approaches for the conjugation of porphyrins and related macrocycles to peptides and proteins. Photochem. Photobiol. Sci. 2011, 10, 759–791, doi:10.1039/c0pp00366b.
[100]
Mew, D.; Lum, V.; Wat, C.K.; Towers, G.H.; Sun, C.H.; Walter, R.J.; Wright, W.; Berns, M.W.; Levy, J.G. Ability of specific monoclonal antibodies and conventional antisera conjugated to hematoporphyrin to label and kill selected cell lines subsequent to light activation. Cancer Res. 1985, 45, 4380–4386.
[101]
Mew, D.; Wat, C.K.; Towers, G.H.; Levy, J.G. Photoimmunotherapy: treatment of animal tumors with tumor-specific monoclonal antibody-hematoporphyrin conjugates. J. Immunol. 1983, 130, 1473–1477.
[102]
Steele, J.K.; Liu, D.; Stammers, A.T.; Whitney, S.; Levy, J.G. Suppressor deletion therapy: selective elimination of T suppressor cells in vivo using a hematoporphyrin conjugated monoclonal antibody permits animals to reject syngeneic tumor cells. Cancer Immunol. Immunother. 1988, 26, 125–131.
[103]
Carcenac, M.; Dorvillius, M.; Garambois, V.; Glaussel, F.; Larroque, C.; Langlois, R.; Hynes, N.E.; van Lier, J.E.; Pèlegrin, A. Internalisation enhances photo-induced cytotoxicity of monoclonal antibody-phthalocyanine conjugates. Br. J. Cancer 2001, 85, 1787–1793, doi:10.1054/bjoc.2001.2170.
[104]
Carcenac, M.; Larroque, C.; Langlois, R.; van Lier, J.E.; Artus, J.C.; Pèlegrin, A. Preparation, phototoxicity and biodistribution studies of anti-carcinoembryonic antigen monoclonal antibody-phthalocyanine conjugates. Photochem. Photobiol. 1999, 70, 930–936.
[105]
Savellano, M.D.; Hasan, T. Targeting cells that overexpress the epidermal growth factor receptor with polyethylene glycolated BPD verteporfin photosensitizer immunoconjugates. Photochem. Photobiol. 2003, 77, 431–439, doi:10.1562/0031-8655(2003)077<0431:TCTOTE>2.0.CO;2.
[106]
Savellano, M.D.; Pogue, B.W.; Hoopes, P.J.; Vitetta, E.S.; Paulsen, K.D. Multiepitope HER2 targeting enhances photoimmunotherapy of HER2-overexpressing cancer cells with pyropheophorbide-a immunoconjugates. Cancer Res. 2005, 65, 6371–6379, doi:10.1158/0008-5472.CAN-05-0426.
[107]
Bhatti, M.; Yahioglu, G.; Milgrom, L.R.; Garcia-Maya, M.; Chester, K.A.; Deonarain, M.P. Targeted photodynamic therapy with multiply-loaded recombinant antibody fragments. Int. J. Cancer 2008, 122, 1155–1163.
[108]
Soukos, N.S.; Hamblin, M.R.; Keel, S.; Fabian, R.L.; Deutsch, T.F.; Hasan, T. Epidermal growth factor receptor-targeted immunophotodiagnosis and photoimmunotherapy of oral precancer in vivo. Cancer Res. 2001, 61, 4490–4496.
[109]
Fabbrini, M.; Trachsel, E.; Soldani, P.; Bindi, S.; Alessi, P.; Bracci, L.; Kosmehl, H.; Zardi, L.; Neri, D.; Neri, P. Selective occlusion of tumor blood vessels by targeted delivery of an antibody-photosensitizer conjugate. Int. J. Cancer 2006, 118, 1805–1813, doi:10.1002/ijc.21412.
[110]
Palumbo, A.; Hauler, F.; Dziunycz, P.; Schwager, K.; Soltermann, A.; Pretto, F.; Alonso, C.; Hofbauer, G.F.; Boyle, R.W.; Neri, D. A chemically modified antibody mediates complete eradication of tumours by selective disruption of tumour blood vessels. Br. J. Cancer 2011, 104, 1106–1115, doi:10.1038/bjc.2011.78.
[111]
Vrouenraets, M.B.; Visser, G.W.M.; Stigter, M.; Oppelaar, H.; Snow, G.B.; van Dongen, G.A.M.S. Comparison of aluminium (III) phthalocyanine tetrasulfonate- and meta-tetrahydroxyphenylchlorin-monoclonal antibody conjugates for their efficacy in photodynamic therapy in vitro. Int. J. Cancer 2002, 98, 793–798.
[112]
Vrouenraets, M.B.; Visser, G.W.; Stewart, F.A.; Stigter, M.; Oppelaar, H.; Postmus, P.E.; Snow, G.B.; van Dongen, G.A. Development of meta-tetrahydroxyphenylchlorin-monoclonal antibody conjugates for photoimmunotherapy. Cancer Res. 1999, 59, 1505–1513.
[113]
Vrouenraets, M.B.; Visser, G.W.; Loup, C.; Meunier, B.; Stigter, M.; Oppelaar, H.; Stewart, F.A.; Snow, G.B.; van Dongen, G.A. Targeting of a hydrophilic photosensitizer by use of internalizing monoclonal antibodies: A new possibility for use in photodynamic therapy. Int. J. Cancer 2000, 88, 108–114, doi:10.1002/1097-0215(20001001)88:1<108::AID-IJC17>3.0.CO;2-H.
[114]
Vrouenraets, M.B.; Visser, G.W.; Stigter, M.; Oppelaar, H.; Snow, G.B.; van Dongen, G.A. Targeting of aluminum (III) phthalocyanine tetrasulfonate by use of internalizing monoclonal antibodies: improved efficacy in photodynamic therapy. Cancer Res. 2001, 61, 1970–1975.
[115]
Sutton, J.M.; Clarke, O.J.; Fernandez, N.; Boyle, R.W. Porphyrin, chlorin, and bacteriochlorin isothiocyanates: Useful reagents for the synthesis of photoactive bioconjugates. Bioconjug. Chem. 2002, 13, 249–263, doi:10.1021/bc015547x.
[116]
Hudson, R.; Carcenac, M.; Smith, K.; Madden, L.; Clarke, O.J.; Pèlegrin, A.; Greenman, J.; Boyle, R.W. The development and characterisation of porphyrin isothiocyanate-monoclonal antibody conjugates for photoimmunotherapy. Br. J. Cancer 2005, 92, 1442–1449, doi:10.1038/sj.bjc.6602517.
[117]
Staneloudi, C.; Smith, K.A.; Hudson, R.; Malatesti, N.; Savoie, H.; Boyle, R.W.; Greenman, J. Development and characterization of novel photosensitizer: scFv conjugates for use in photodynamic therapy of cancer. Immunology 2007, 120, 512–517, doi:10.1111/j.1365-2567.2006.02522.x.
[118]
Smith, K.; Malatesti, N.; Cauchon, N.; Hunting, D.; Lecomte, R.; van Lier, J.E.; Greenman, J.; Boyle, R.W. Mono- and tri-cationic porphyrin-monoclonal antibody conjugates: Photodynamic activity and mechanism of action. Immunology 2011, 132, 256–265, doi:10.1111/j.1365-2567.2010.03359.x.
[119]
Malatesti, N.; Smith, K.; Savoie, H.; Greenman, J.; Boyle, R.W. Synthesis and in vitro investigation of cationic 5,15-diphenyl porphyrin-monoclonal antibody conjugates as targeted photodynamic sensitisers. Int. J. Oncol. 2006, 28, 1561–1569.
[120]
Alonso, C.M.A.; Palumbo, A.; Bullous, A.J.; Pretto, F.; Neri, D.; Boyle, R.W. Site-specific and stoichiometric conjugation of cationic porphyrins to antiangiogenic monoclonal antibodies. Bioconjug. Chem. 2010, 21, 302–313, doi:10.1021/bc9003537.
[121]
Hamblin, M.R.; Del Governatore, M.; Rizvi, I.; Hasan, T. Biodistribution of charged 17.1A photoimmunoconjugates in a murine model of hepatic metastasis of colorectal cancer. Br. J. Cancer 2000, 83, 1544–1551, doi:10.1054/bjoc.2000.1486.
[122]
Duska, L.R.; Hamblin, M.R.; Bamberg, M.P.; Hasan, T. Biodistribution of charged F(ab')2 photoimmunoconjugates in a xenograft model of ovarian cancer. Br. J. Cancer 1997, 75, 837–844, doi:10.1038/bjc.1997.149.
[123]
Duska, L.R.; Hamblin, M.R.; Miller, J.L.; Hasan, T. Combination photoimmunotherapy and cisplatin: effects on human ovarian cancer ex vivo. J. Natl. Cancer Inst. 1999, 91, 1557–1563, doi:10.1093/jnci/91.18.1557.
[124]
Hamblin, M.R.; Miller, J.L.; Hasan, T. Effect of charge on the interaction of site-specific photoimmunoconjugates with human ovarian cancer cells. Cancer Res. 1996, 56, 5205–5210.
[125]
Del Governatore, M.; Hamblin, M.R.; Shea, C.R.; Rizvi, I.; Molpus, K.G.; Tanabe, K.K.; Hasan, T. Experimental photoimmunotherapy of hepatic metastases of colorectal cancer with a 17.1A chlorin(e6) immunoconjugate. Cancer Res. 2000, 60, 4200–4205.
[126]
Molpus, K.L.; Hamblin, M.R.; Rizvi, I.; Hasan, T. Intraperitoneal photoimmunotherapy of ovarian carcinoma xenografts in nude mice using charged photoimmunoconjugates. Gynecol. Oncol. 2000, 76, 397–404, doi:10.1006/gyno.1999.5705.
[127]
Del Governatore, M.; Hamblin, M.R.; Piccinini, E.E.; Ugolini, G.; Hasan, T. Targeted photodestruction of human colon cancer cells using charged 17.1A chlorin e6 immunoconjugates. Br. J. Cancer 2000, 82, 56–64.
[128]
Jiang, F.N.; Jiang, S.; Liu, D.; Richter, A.; Levy, J.G. Development of technology for linking photosensitizers to a model monoclonal antibody. J. Immunol. Methods 1990, 134, 139–149, doi:10.1016/0022-1759(90)90122-C.
[129]
Jiang, F.N.; Allison, B.; Liu, D.; Levy, J.G. Enhanced photodynamic killing of target cells by either monoclonal antibody or low density lipoprotein mediated delivery systems. J. Control Release 1992, 19, 41–58, doi:10.1016/0168-3659(92)90064-X.
[130]
Jiang, F.N.; Liu, D.J.; Neyndorff, H.; Chester, M.; Jiang, S.Y.; Levy, J.G. Photodynamic killing of human squamous cell carcinoma cells using a monoclonal antibody-photosensitizer conjugate. J. Natl. Cancer Inst. 1991, 83, 1218–1225, doi:10.1093/jnci/83.17.1218.
[131]
Berthiaume, F.; Reiken, S.R.; Toner, M.; Tompkins, R.G.; Yarmush, M.L. Antibody-targeted photolysis of bacteria in vivo. Biotechnology (N.Y.) 1994, 12, 703–706.
[132]
Strong, L.H.; Berthiaume, F.; Yarmush, M.L. Control of fibroblast populated collagen lattice contraction by antibody targeted photolysis of fibroblasts. Lasers Surg. Med. 1997, 21, 235–247, doi:10.1002/(SICI)1096-9101(1997)21:3<235::AID-LSM3>3.0.CO;2-R.
[133]
Thorpe, W.P.; Toner, M.; Ezzell, R.M.; Tompkins, R.G.; Yarmush, M.L. Dynamics of photoinduced cell plasma membrane injury. Biophys. J. 1995, 68, 2198–2206, doi:10.1016/S0006-3495(95)80402-9.
[134]
Lu, X.M.; Fischman, A.J.; Stevens, E.; Lee, T.T.; Strong, L.; Tompkins, R.G.; Yarmush, M.L. Sn-chlorin e6 antibacterial immunoconjugates. An in vitro and in vivo analysis. J. Immunol. Methods 1992, 156, 85–99, doi:10.1016/0022-1759(92)90014-K.
[135]
Hasan, T.; Lin, A.; Yarmush, D.; Oseroff, A.; Yarmush, M. Monoclonal antibody-chromophore conjugates as selective phototoxins. J. Control Release 1989, 10, 107–117, doi:10.1016/0168-3659(89)90022-9.
[136]
Goff, B.A.; Hermanto, U.; Rumbaugh, J.; Blake, J.; Bamberg, M.; Hasan, T. Photoimmunotherapy and biodistribution with an OC125-chlorin immunoconjugate in an in vivo murine ovarian cancer model. Br. J. Cancer 1994, 70, 474–480, doi:10.1038/bjc.1994.330.
[137]
Goff, B.A.; Bamberg, M.; Hasan, T. Photoimmunotherapy of human ovarian carcinoma cells ex vivo. Cancer Res. 1991, 51, 4762–4767.
[138]
Goff, B.A.; Blake, J.; Bamberg, M.P.; Hasan, T. Treatment of ovarian cancer with photodynamic therapy and immunoconjugates in a murine ovarian cancer model. Br. J. Cancer 1996, 74, 1194–1198, doi:10.1038/bjc.1996.516.
[139]
Savellano, M.D.; Owusu-Brackett, N.; Son, J.; Ganga, T.; Leung, N.L.; Savellano, D.H. Photodynamic Tumor Eradication With a Novel Targetable Photosensitizer: Strong Vascular Effects and Dependence on Treatment Repetition Versus Potentiation. Photochem. Photobiol. 2012, doi:10.1111/php.12018.
[140]
Dumontet, C.; Jordan, M.A. Microtubule-binding agents: A dynamic field of cancer therapeutics. Nat. Rev. Drug Discov. 2010, 9, 790–803, doi:10.1038/nrd3253.
[141]
Pèlegrin, A.; Folli, S.; Buchegger, F.; Mach, J.P.; Wagnières, G.; van den Bergh, H. Antibody-fluorescein conjugates for photoimmunodiagnosis of human colon carcinoma in nude mice. Cancer 1991, 67, 2529–2537, doi:10.1002/1097-0142(19910515)67:10<2529::AID-CNCR2820671024>3.0.CO;2-B.
[142]
Kuimova, M.K.; Bhatti, M.; Deonarain, M.; Yahioglu, G.; Levitt, J.A.; Stamati, I.; Suhling, K.; Phillips, D. Fluorescence characterisation of multiply-loaded anti-HER2 single chain Fv-photosensitizer conjugates suitable for photodynamic therapy. Photochem. Photobiol. Sci. 2007, 6, 933–939, doi:10.1039/b708320c.
[143]
Bhatti, M.; MacRobert, A.; Henderson, B.; Shepherd, P.; Cridland, J.; Wilson, M. Antibody-targeted lethal photosensitization of Porphyromonas gingivalis. Antimicrob. Agents Chemother. 2000, 44, 2615–2618, doi:10.1128/AAC.44.10.2615-2618.2000.
[144]
Stuchinskaya, T.; Moreno, M.; Cook, M.J.; Edwards, D.R.; Russell, D.A. Targeted photodynamic therapy of breast cancer cells using antibody-phthalocyanine-gold nanoparticle conjugates. Photochem. Photobiol. Sci. 2011, 10, 822–831, doi:10.1039/c1pp05014a.
Serebrovskaya, E.O.; Edelweiss, E.F.; Stremovskiy, O.A.; Lukyanov, K.A.; Chudakov, D.M.; Deyev, S.M. Targeting cancer cells by using an antireceptor antibody-photosensitizer fusion protein. Proc. Natl. Acad. Sci. USA 2009, 106, 9221–9225.
[149]
Oseroff, A.R.; Ohuoha, D.; Hasan, T.; Bommer, J.C.; Yarmush, M.L. Antibody-targeted photolysis: Selective photodestruction of human T-cell leukemia cells using monoclonal antibody-chlorin e6 conjugates. Proc. Natl. Acad. Sci. USA 1986, 83, 8744–8748.
Savellano, M.D.; Hasan, T. Photochemical targeting of epidermal growth factor receptor: A mechanistic study. Clin. Cancer Res. 2005, 11, 1658–1668, doi:10.1158/1078-0432.CCR-04-1902.
[152]
Kaspar, M.; Zardi, L.; Neri, D. Fibronectin as target for tumor therapy. Int. J. Cancer 2006, 118, 1331–1339, doi:10.1002/ijc.21677.
[153]
Pini, A.; Viti, F.; Santucci, A.; Carnemolla, B.; Zardi, L.; Neri, P.; Neri, D. Design and use of a phage display library. Human antibodies with subnanomolar affinity against a marker of angiogenesis eluted from a two-dimensional gel. J. Biol. Chem. 1998, 273, 21769–21776.
[154]
Stamati, I.; Kuimova, M.K.; Lion, M.; Yahioglu, G.; Phillips, D.; Deonarain, M.P. Novel photosensitisers derived from pyropheophorbide-a: uptake by cells and photodynamic efficiency in vitro. Photochem. Photobiol. Sci. 2010, 9, 1033–1041, doi:10.1039/c0pp00038h.
[155]
Folli, S.; Wagnières, G.; Pèlegrin, A.; Calmes, J.M.; Braichotte, D.; Buchegger, F.; Chalandon, Y.; Hardman, N.; Heusser, C.; Givel, J.C. Immunophotodiagnosis of colon carcinomas in patients injected with fluoresceinated chimeric antibodies against carcinoembryonic antigen. Proc. Natl. Acad. Sci. USA 1992, 89, 7973–7977, doi:10.1073/pnas.89.17.7973.
[156]
Collins, H.A.; Khurana, M.; Moriyama, E.H.; Mariampillai, A.; Dahlstedt, E.; Balaz, M.; Kuimova, M.K.; Drobizhev, M.; Yang, V.X.D.; Phillips, D.; et al. Blood-vessel closure using photosensitizers engineered for two-photon excitation. Nat. Photonics. 2008, 2, 420–424, doi:10.1038/nphoton.2008.100.
[157]
Khurana, M.; Collins, H.A.; Karotki, A.; Anderson, H.L.; Cramb, D.T.; Wilson, B.C. Quantitative in vitro demonstration of two-photon photodynamic therapy using photofrin and visudyne. Photochem. Photobiol. 2007, 83, 1441–1448, doi:10.1111/j.1751-1097.2007.00185.x.
[158]
Pawlicki, M.; Collins, H.A.; Denning, R.G.; Anderson, H.L. Two-photon absorption and the design of two-photon dyes. Angew. Chem. Int. Ed. Engl. 2009, 48, 3244–3266, doi:10.1002/anie.200805257.
[159]
Kuroki, M.; Hachimine, K.; Abe, H.; Shibaguchi, H.; Kuroki, M.; Maekawa, S.-I.; Yanagisawa, J.; Kinugasa, T.; Tanaka, T.; Yamashita, Y. Sonodynamic therapy of cancer using novel sonosensitizers. Anticancer Res. 2007, 27, 3673–3677.
[160]
Ma, X.; Pan, H.; Yi, J. Combination sonodynamic therapy with immunoadjuvant may be a promising new modality for cancer treatment. Med. Hypotheses 2009, 72, 418–420, doi:10.1016/j.mehy.2008.10.024.
[161]
Yamaguchi, S.; Kobayashi, H.; Narita, T.; Kanehira, K.; Sonezaki, S.; Kudo, N.; Kubota, Y.; Terasaka, S.; Houkin, K. Sonodynamic therapy using water-dispersed TiO2-polyethylene glycol compound on glioma cells: Comparison of cytotoxic mechanism with photodynamic therapy. Ultrason. Sonochem. 2011, 18, 1197–1204, doi:10.1016/j.ultsonch.2010.12.017.
Huang, X.; Qian, W.; El-Sayed, I.H.; El-Sayed, M.A. The potential use of the enhanced nonlinear properties of gold nanospheres in photothermal cancer therapy. Lasers Surg. Med. 2007, 39, 747–753, doi:10.1002/lsm.20577.
[164]
El-Sayed, I.H.; Huang, X.; El-Sayed, M.A. Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles. Cancer Lett. 2006, 239, 129–135, doi:10.1016/j.canlet.2005.07.035.
[165]
Liu, Y.; Chen, W.; Wang, S.; Joly, A.G. Investigation of water-soluble X-ray luminescence nanoparticles for photodynamic activation. Appl. Phys. Lett. 2008, 92, 043901, doi:10.1063/1.2835701.
[166]
Samia, A.C.S.; Dayal, S.; Burda, C. Quantum dot-based energy transfer: perspectives and potential for applications in photodynamic therapy. Photochem. Photobiol. 2006, 82, 617–625, doi:10.1562/2005-05-11-IR-525.
[167]
Juzenas, P.; Chen, W.; Sun, Y.-P.; Coelho, M.A.N.; Generalov, R.; Generalova, N.; Christensen, I.L. Quantum dots and nanoparticles for photodynamic and radiation therapies of cancer. Adv. Drug Deliv. Rev. 2008, 60, 1600–1614, doi:10.1016/j.addr.2008.08.004.
[168]
Chen, W.; Zhang, J. Using nanoparticles to enable simultaneous radiation and photodynamic therapies for cancer treatment. J. Nanosci. Nanotechnol. 2006, 6, 1159–1166, doi:10.1166/jnn.2006.327.
[169]
Vaidya, A.; Sun, Y.; Feng, Y.; Emerson, L.; Jeong, E.-K.; Lu, Z.-R. Contrast-enhanced MRI-guided photodynamic cancer therapy with a pegylated bifunctional polymer conjugate. Pharm. Res. 2008, 25, 2002–2011, doi:10.1007/s11095-008-9608-1.
[170]
Huang, P.; Li, Z.; Lin, J.; Yang, D.; Gao, G.; Xu, C.; Bao, L.; Zhang, C.; Wang, K.; Song, H.; Hu, H.; Cui, D. Photosensitizer-conjugated magnetic nanoparticles for in vivo simultaneous magnetofluorescent imaging and targeting therapy. Biomaterials 2011, 32, 3447–3458, doi:10.1016/j.biomaterials.2011.01.032.
[171]
Detty, M.R. Direct 1270 nm irradiation as an alternative to photosensitized generation of singlet oxygen to induce cell death. Photochem. Photobiol. 2012, 88, 2–4, doi:10.1111/j.1751-1097.2011.01047.x.
[172]
Laptev, R.; Nisnevitch, M.; Siboni, G.; Malik, Z.; Firer, M.A. Intracellular chemiluminescence activates targeted photodynamic destruction of leukaemic cells. Br. J. Cancer 2006, 95, 189–196.
[173]
Embleton, M.L.; Nair, S.P.; Cookson, B.D.; Wilson, M. Antibody-directed photodynamic therapy of methicillin resistant Staphylococcus aureus. Microb. Drug Resist. 2004, 10, 92–97, doi:10.1089/1076629041310000.
[174]
Berki, T.; Németh, P. Novel method for in vitro depletion of T cells by monoclonal antibody-targeted photosensitization. J. Immunol. Methods 1998, 211, 139–146.
