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Immunotherapy: a way to improve the therapeutic outcome of photodynamic therapy?

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Abstract

Photodynamic therapy (PDT) is a treatment for cancer and non-cancerous lesions involving light and a sensitizing drug, a so-called photosensitizer. Photosensitizers for PDT usually accumulate in tumour tissues with some selectivity. Thus, malignant and abnormal cells can be destroyed by PDT which acts by producing singlet oxygen and possible other reactive oxygen species. However, the efficiency of PDT is often limited by shallow light penetration into tissue. In some cases one treatment modality cannot cure a patient because of treatment limitations and/or side effects. In recent years, many preclinical studies have indicated that the therapeutic outcome of PDT can be improved, doses and side effects lowered by combination with immunotherapy. Most experiments have been done with animals and cell lines. This review summarizes the current knowledge about different immunotherapeutic approaches which can be used to improve effectiveness and extend the applications of PDT in clinics.

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Abbreviations

ALA:

5-Aminolevulinic acid

AlPcS4:

Aluminum(iii) phthalocyanine tetrasulfonate

BCG:

Bacillus Calmette-Guerin

BPD:

Benzoporphyrin derivative

Ce6:

Chlorin e6

CMA:

Chlorin e6 monoethylenediamine monoamide

DBPMAF or GcMAF:

Vitamin D3-binding protein-derived macrophage-activating factor

DC:

Dendritic cells

EGFR:

Epidermal growth factor receptor

GC:

Glycated chitosan

G-CSF:

Granulocyte colony-stimulating factor

GM-CSF:

Granulocyte-macrophage colony-stimulating factor

HLA:

Human leukocyte antigen

Hp:

Haematoporphyrin

HpD:

Haematoporphyrin derivative

IFN:

Interferon

IL:

Interleukin

IN:

Inulin

mAb:

Monoclonal antibody

Lu-Tex:

Lutetium texaphyrin

MCWE:

Mycobacterium cell wall extract

MHC:

Major histocompatibility complex

mTHPC:

meta-tetra(hydroxyphenyl)chlorin

NK:

Natural killer

NPe6:

Mono-l-aspartyl chlorin e6

PDT:

Photodynamic therapy

PIT:

Photoimmunotherapy

PPa:

Pheophorbide a

SPG:

Schizophyllan

TNF:

Tumour necrosis factor

UV:

Ultraviolet

VEGF:

Vascular endothelial growth factor

VEGFR:

Vascular endothelial growth factor receptor

ZnPc:

Zinc phthalocyanine

References

  1. I. J. Elenkov, R. L. Wilder, G. P. Chrousos, E. S. Vizi, The sympathetic nerve-an integrative interface between two supersystems: the brain and the immune system, Pharmacol. Rev., 2000, 52, 595–638.

    CAS  PubMed  Google Scholar 

  2. D. Nowis, T. Stoklosa, M. Legat, T. Issat, M. Jakobisiak, J. Golab, The influence of photodynamic therapy on the immune response, Photodiagn. Photodyn. Ther., 2005, 2, 283–298.

    Article  CAS  Google Scholar 

  3. A. P. Castano, P. Mroz, M. R. Hamblin, Photodynamic therapy and anti-tumour immunity, Nat. Rev. Cancer, 2006, 6, 535–545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. W. J. de Vree, M. C. Essers, J. F. Koster, W. Sluiter, Role of interleukin 1 and granulocyte colony-stimulating factor in photofrin-based photodynamic therapy of rat rhabdomyosarcoma tumors, Cancer Res., 1997, 57, 2555–2558.

    PubMed  Google Scholar 

  5. J. Sun, I. Cecic, C. S. Parkins, M. Korbelik, Neutrophils as inflammatory and immune effectors in photodynamic therapy-treated mouse SCCVII tumours, Photochem. Photobiol. Sci., 2002, 1, 690–695.

    Article  CAS  PubMed  Google Scholar 

  6. D. Nowis, M. Makowski, T. Stoklosa, M. Legat, T. Issat, J. Golab, Direct tumor damage mechanisms of photodynamic therapy, Acta Biochim. Pol., 2005, 52, 339–352.

    Article  CAS  PubMed  Google Scholar 

  7. F. H. van Duijnhoven, R. I. J. M. Aalbers, J. P. Rovers, O. T. Terpstra, P. J. K. Kuppen, The immunological consequences of photodynamic treatment of cancer, a literature review, Immunobiology, 2003, 207, 105–113.

    Article  PubMed  Google Scholar 

  8. S. O. Gollnick, S. S. Evans, H. Baumann, B. Owczarczak, P. Maier, L. Vaughan, W. C. Wang, E. Unger, B. W. Henderson, Role of cytokines in photodynamic therapy-induced local and systemic inflammation, Br. J. Cancer, 2003, 88, 1772–1779.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. M. B. Jameson, B. C. Baguley, P. Kestell, L. Zhao, J. W. Paxton, P. I. Thompson, S. Waller, Pharmacokinetics of 5,6-dimethylxanthenone-4-acetic acid (AS1404), a novel vascular disrupting agent, in phase I clinical trial, Cancer Chemother. Pharmacol., 2007, 59, 681–687.

    Article  CAS  PubMed  Google Scholar 

  10. D. A. Bellnier, Potentiation of photodynamic therapy in mice with recombinant human tumor necrosis factor-alpha, J. Photochem. Photobiol., B, 1991, 8, 203–210.

    Article  CAS  Google Scholar 

  11. D. A. Bellnier, S. O. Gollnick, S. H. Camacho, W. R. Greco, R. T. Cheney, Treatment with the tumor necrosis factor-alpha-inducing drug 5,6-dimethylxanthenone-4-acetic acid enhances the antitumor activity of the photodynamic therapy of RIF-1 mouse tumors, Cancer Res., 2003, 63, 7584–7590.

    CAS  PubMed  Google Scholar 

  12. S. Mocellin, C. R. Rossi, P. Pilati, D. Nitti, Tumor necrosis factor, cancer and anticancer therapy, Cytokine Growth Factor Rev., 2005, 16, 35–53.

    Article  CAS  PubMed  Google Scholar 

  13. L. M. Ching, D. Goldsmith, W. R. Joseph, H. Körner, J. D. Sedgwick, B. C. Baguley, Induction of intratumoral tumor necrosis factor (TNF) synthesis and hemorrhagic necrosis by 5,6-dimethylxanthenone-4-acetic acid (DMXAA) in TNF knockout mice, Cancer Res., 1999, 59, 3304–3307.

    CAS  PubMed  Google Scholar 

  14. W. R. Joseph, Z. Cao, K. G. Mountjoy, E. S. Marshall, B. C. Baguley, L. M. Ching, Stimulation of tumors to synthesize tumor necrosis factor-alpha in situ using 5,6-dimethylxanthenone-4-acetic acid: a novel approach to cancer therapy, Cancer Res., 1999, 59, 633–638.

    CAS  PubMed  Google Scholar 

  15. I. Cecic, C. S. Parkins, M. Korbelik, Induction of systemic neutrophil response in mice by photodynamic therapy of solid tumors, Photochem. Photobiol., 2001, 74, 712–720.

    Article  CAS  PubMed  Google Scholar 

  16. W. J. de Vree, M. C. Essers, H. S. de Bruijn, W. M. Star, J. F. Koster, W. Sluiter, Evidence for an important role of neutrophils in the efficacy of photodynamic therapy in vivo, Cancer Res., 1996, 56, 2908–2911.

    PubMed  Google Scholar 

  17. P. C. Kousis, B. W. Henderson, P. G. Maier, S. O. Gollnick, Photodynamic therapy enhancement of antitumor immunity is regulated by neutrophils, Cancer Res., 2007, 67, 10501–10510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. E. Fernandez-Varon, L. Villamayor, Granulocyte and granulocyte macrophage colony-stimulating factors as therapy in human and veterinary medicine, Vet. J., 2007, 174, 33–41.

    Article  CAS  PubMed  Google Scholar 

  19. G. Krosl, M. Korbelik, J. Krosl, G. J. Dougherty, Potentiation of photodynamic therapy-elicited antitumor response by localized treatment with granulocyte-macrophage colony-stimulating factor, Cancer Res., 1996, 56, 3281–3286.

    CAS  PubMed  Google Scholar 

  20. J. Golab, G. Wilczynski, R. Zagozdzon, T. Stoklosa, A. Dabrowska, J. Rybczynska, M. Wasik, E. Machaj, T. Olda, K. Kozar, R. Kaminski, A. Giermasz, A. Czajka, W. Lasek, W. Feleszko, M. Jakobisiak, Potentiation of the anti-tumour effects of Photofrin-based photodynamic therapy by localized treatment with G-CSF, Br. J. Cancer, 2000, 82, 1485–1491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. D. N. Sauder, Immunomodulatory and pharmacologic properties of imiquimod, J. Am. Acad. Dermatol., 2000, 43, S6–11.

    Article  CAS  PubMed  Google Scholar 

  22. X. Wang, H. Wang, M. Guo, Z. Huang, Combination of immunotherapy and photodynamic therapy in the treatment of Bowenoid papulosis, Photodiagn. Photodynamic Ther., 2007, 4, 88–93.

    Article  CAS  Google Scholar 

  23. M. Korbelik, P. D. Cooper, Potentiation of photodynamic therapy of cancer by complement: the effect of gamma-inulin, Br. J. Cancer, 2007, 96, 67–72.

    Article  CAS  PubMed  Google Scholar 

  24. US Pat., 4138479, 1979

  25. US Pat., 5051408, 1991

  26. K. Schroder, P. J. Hertzog, T. Ravasi, D. A. Hume, Interferon-gamma: an overview of signals, mechanisms and functions, J. Leuk. Biol., 2004, 75, 163–189.

    Article  CAS  Google Scholar 

  27. M. Korbelik, J. Sun, I. Cecic, K. Serrano, Adjuvant treatment for complement activation increases the effectiveness of photodynamic therapy of solid tumors, Photochem. Photobiol. Sci., 2004, 3, 812–816.

    Article  CAS  PubMed  Google Scholar 

  28. R. Di Paola, E. Mazzon, C. Muia, C. Crisafulli, T. Genovese, P. Di Bella, E. Esposito, M. Menegazzi, R. Meli, H. Suzuki, S. Cuzzocrea, Protective effect of Hypericum perforatum in zymosan-induced multiple organ dysfunction syndrome: relationship to its inhibitory effect on nitric oxide production and its peroxynitrite scavenging activity, Nitric Oxide, 2007, 16, 118–130.

    Article  CAS  PubMed  Google Scholar 

  29. A. Kunamneni, T. T. Abdelghani, P. Ellaiah, Streptokinase-the drug of choice for thrombolytic therapy, J. Thromb. Thrombolysis, 2007, 23, 9–23.

    Article  CAS  PubMed  Google Scholar 

  30. D. M. Klinman, Immunotherapeutic uses of CpG oligodeoxynucleotides, Nat. Rev. Immunol., 2004, 4, 249–258.

    Article  CAS  PubMed  Google Scholar 

  31. J. A. Chabalgoity, G. Dougan, P. Mastroeni, R. J. Aspinall, Live bacteria as the basis for immunotherapies against cancer, Expert Rev. Vaccines, 2002, 1, 495–505.

    Article  CAS  PubMed  Google Scholar 

  32. F. G. Perabo, S. C. Muller, Current and new strategies in immunotherapy for superficial bladder cancer, Urology, 2004, 64, 409–421.

    Article  PubMed  Google Scholar 

  33. M. Korbelik, I. Cecic, Enhancement of tumour response to photodynamic therapy by adjuvant mycobacterium cell-wall treatment, J. Photochem. Photobiol., B, 1998, 44, 151–158.

    Article  CAS  Google Scholar 

  34. M. Korbelik, J. Sun, J. J. Posakony, Interaction between photodynamic therapy and BCG immunotherapy responsible for the reduced recurrence of treated mouse tumors, Photochem. Photobiol., 2001, 73, 403–409.

    Article  CAS  PubMed  Google Scholar 

  35. M. Szygula, A. Pietrusa, M. Adamek, B. Wojciechowski, A. Kawczyk-Krupka, A. Cebula, W. Duda, A. Sieron, Combined treatment of urinary bladder cancer with the use of photodynamic therapy (PDT) and subsequent BCG-therapy: a pilot study, Photodiagn. Photodyn. Ther., 2004, 1, 241–246.

    Article  CAS  Google Scholar 

  36. M. D. Shelley, H. Kynaston, J. Court, T. J. Wilt, B. Coles, K. Burgon, M. D. Mason, A systematic review of intravesical bacillus Calmette-Guérin plus transurethral resection vs. transurethral resection alone in Ta and T1 bladder cancer, BJU Int., 2001, 88, 209–216.

    Article  CAS  PubMed  Google Scholar 

  37. S. Krege, G. Giani, R. Meyer, T. Otto, H. Rubben, F. Noll, G. Jakse, S. T. Muller, H. J. Melchior, L. Weissbach, B. Terhorst, P. Lenz, P. Faul, H. Sommerkamp, B. Kopper, R. Hautmann, L. Knebel Keller, F. Eisenberger, W. Schaffner, A randomized multicenter trial of adjuvant therapy in superficial bladder cancer: transurethral resection only versus transurethral resection plus mitomycin C versus transurethral resection plus bacillus Calmette-Guerin. Participating Clinics, J. Urol., 1996, 156, 962–966.

    Article  CAS  PubMed  Google Scholar 

  38. J. P. Meyer, R. Persad, D. A. Gillatt, Use of bacille Calmette-Guerin in superficial bladder cancer, Postgrad. Med. J., 2002, 78, 449–454.

    Article  PubMed  PubMed Central  Google Scholar 

  39. M. Uehara, K. Sano, Z. L. Wang, J. Sekine, H. Ikeda, T. Inokuchi, Enhancement of the photodynamic antitumor effect by streptococcal preparation OK-432 in the mouse carcinoma, Cancer Immunol. Immunother., 2000, 49, 401–409.

    Article  CAS  PubMed  Google Scholar 

  40. The Comparative Toxicogenomics Database (CTD) http://ctd.mdibl.org/

  41. M. Uehara, T. Inokuchi, Hyperthermic photodynamic therapy combined with topical administration of OK-432 in the mouse carcinoma, Oral Oncol., 2003, 39, 184–189.

    Article  CAS  PubMed  Google Scholar 

  42. G. Krosl, M. Korbelik, Potentiation of photodynamic therapy by immunotherapy: the effect of schizophyllan (SPG), Cancer Lett., 1994, 84, 43–49.

    Article  CAS  PubMed  Google Scholar 

  43. W. R. Chen, M. Korbelik, K. E. Bartels, H. Liu, J. Sun, Nordquist RE, Enhancement of laser cancer treatment by a chitosan-derived immunoadjuvant, Photochem. Photobiol., 2005, 81, 190–195.

    Article  CAS  PubMed  Google Scholar 

  44. M. Korbelik, V. R. Naraparaju, N. Yamamoto, Macrophage-directed immunotherapy as adjuvant to photodynamic therapy of cancer, Br. J. Cancer, 1997, 75, 202–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. N. Yamamoto, H. Suyama, N. Yamamoto, N. Ushijima, Immunotherapy of metastatic breast cancer patients with vitamin D-binding protein-derived macrophage activating factor (GcMAF), Int. J. Cancer, 2008, 122, 461–467.

    Article  CAS  PubMed  Google Scholar 

  46. O. Kisker, S. Onizuka, C. M. Becker, M. Fannon, E. Flynn, R. D’Amato, B. Zetter, J. Folkman, R. Ray, N. Swamy, S. Pirie-Shepherd, Vitamin D binding protein-macrophage activating factor (DBP-maf) inhibits angiogenesis and tumor growth in mice, Neoplasia, 2003, 5, 32–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. M. Korbelik, J. Sun, Cancer treatment by photodynamic therapy combined with adoptive immunotherapy using genetically altered natural killer cell line, Int. J. Cancer, 2001, 93, 269–274.

    Article  CAS  PubMed  Google Scholar 

  48. C. Staneloudi, K. A. Smith, R. Hudson, N. Malatesti, H. Savoie, R. W. Boyle, J. Greenman, Development and characterization of novel photosensitizer: scFv conjugates for use in photodynamic therapy of cancer, Immunology, 2007, 120, 512–517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. M. Bhatti, G. Yahioglu, L. R. Milgrom, M. Garcia-Maya, K. A. Chester, M. P. Deonarain, Targeted photodynamic therapy with multiply-loaded recombinant antibody fragments, Int. J. Cancer, 2008, 122, 1155–1163.

    Article  CAS  PubMed  Google Scholar 

  50. M. D. Savellano, B. W. Pogue, P. J. Hoopes, E. S. Vitetta, K. D. Paulsen, Multiepitope HER2 targeting enhances photoimmunotherapy of HER2-overexpressing cancer cells with pyropheophorbide-a immunoconjugates, Cancer Res., 2005, 65, 6371–6379.

    Article  CAS  PubMed  Google Scholar 

  51. M. B. Vrouenraets, G. W. Visser, M. Stigter, H. Oppelaar, G. B. Snow, G. A. van Dongen, Targeting of aluminum (III) phthalocyanine tetrasulfonate by use of internalizing monoclonal antibodies: improved efficacy in photodynamic therapy, Cancer Res., 2001, 61, 1970–1975.

    CAS  PubMed  Google Scholar 

  52. M. D. Savellano, T. Hasan, Targeting cells that overexpress the epidermal growth factor receptor with polyethylene glycolated BPD verteporfin photosensitizer immunoconjugates, Photochem. Photobiol., 2003, 77, 431–439.

    Article  CAS  PubMed  Google Scholar 

  53. M. B. Vrouenraets, G. W. Visser, F. A. Stewart, M. Stigter, H. Oppelaar, P. E. Postmus, G. B. Snow, G. A. van Dongen, Development of meta-tetrahydroxyphenylchlorin-monoclonal antibody conjugates for photoimmunotherapy, Cancer Res., 1999, 59, 1505–1513.

    CAS  PubMed  Google Scholar 

  54. D. Mew, C. K. Wat, G. H. Towers, J. G. Levy, Photoimmunotherapy: treatment of animal tumors with tumor-specific monoclonal antibody-hematoporphyrin conjugates, J. Immunol., 1983, 130, 1473–1477.

    CAS  PubMed  Google Scholar 

  55. B. A. Goff, J. Blake, M. P. Bamberg, T. Hasan, Treatment of ovarian cancer with photodynamic therapy and immunoconjugates in a murine ovarian cancer model, Br. J. Cancer, 1996, 74, 1194–1198.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. M. Del Governatore, M. R. Hamblin, C. R. Shea, I. Rizvi, K. G. Molpus, K. K. Tanabe, T. Hasan, Experimental photoimmunotherapy of hepatic metastases of colorectal cancer with a 17.1A chlorin(e6) immunoconjugate, Cancer Res., 2000, 60, 4200–4205.

    PubMed  Google Scholar 

  57. N. S. Soukos, M. R. Hamblin, S. Keel, R. L. Fabian, T. F. Deutsch, T. Hasan, Epidermal growth factor receptor-targeted immunophotodiagnosis and photoimmunotherapy of oral precancer in vivo, Cancer Res., 2001, 61, 4490–4496.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. M. D. Savellano, T. Hasan, Photochemical targeting of epidermal growth factor receptor: a mechanistic study, Clin. Cancer Res., 2005, 11, 1658–1668.

    Article  CAS  PubMed  Google Scholar 

  59. A. Jalili, M. Makowski, T. Switaj, D. Nowis, G. M. Wilczynski, E. Wilczek, M. Chorazy-Massalska, A. Radzikowska, W. Maslinski, L. Bialy, J. Sienko, A. Sieron, M. Adamek, G. Basak, P. Mroz, I. W. Krasnodebski, M. Jakobisiak, J. Golab, Effective photoimmunotherapy of murine colon carcinoma induced by the combination of photodynamic therapy and dendritic cells, Clin. Cancer Res., 2004, 10, 4498–4508.

    Article  CAS  PubMed  Google Scholar 

  60. H. Saji, W. Song, K. Furumoto, H. Kato, E. G. Engleman, Systemic antitumor effect of intratumoral injection of dendritic cells in combination with local photodynamic therapy, Clin. Cancer Res., 2006, 12, 2568–2574.

    Article  CAS  PubMed  Google Scholar 

  61. M. Korbelik, G. J. Dougherty, Photodynamic therapy-mediated immune response against subcutaneous mouse tumors, Cancer Res., 1999, 59, 1941–1946.

    CAS  PubMed  Google Scholar 

  62. M. G. del Carmen, I. Rizvi, Y. Chang, A. C. Moor, E. Oliva, M. Sherwood, B. Pogue, T. Hasan, Synergism of epidermal growth factor receptor-targeted immunotherapy with photodynamic treatment of ovarian cancer in vivo, J. Natl. Cancer Inst., 2005, 97, 1516–1524.

    Article  PubMed  CAS  Google Scholar 

  63. B. J. Moeller, R. A. Richardson, M. W. Dewhirst, Hypoxia and radiotherapy: opportunities for improved outcomes in cancer treatment, Cancer Metastasis Rev., 2007, 26, 241–248.

    Article  CAS  PubMed  Google Scholar 

  64. L. Wyld, M. W. Reed, N. J. Brown, The influence of hypoxia and pH on aminolaevulinic acid-induced photodynamic therapy in bladder cancer cells in vitro, Br. J. Cancer, 1998, 77, 1621–1627.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. D. A. Chan, A. J. Giaccia, Hypoxia, gene expression, and metastasis, Cancer Metastasis Rev., 2007, 26, 333–339.

    Article  CAS  PubMed  Google Scholar 

  66. D. Liao, R. S. Johnson, Hypoxia: a key regulator of angiogenesis in cancer, Cancer Metastasis Rev., 2007, 26, 281–290.

    Article  CAS  PubMed  Google Scholar 

  67. Q. Zhou, M. Olivo, K. Y. Lye, S. Moore, A. Sharma, B. Chowbay, Enhancing the therapeutic responsiveness of photodynamic therapy with the antiangiogenic agents SU5416 and SU6668 in murine nasopharyngeal carcinoma models, Cancer Chemother. Pharmacol., 2005, 56, 569–577.

    Article  CAS  PubMed  Google Scholar 

  68. A. Ferrario, K. F. von Tiehl, N. Rucker, M. A. Schwarz, P. S. Gill, C. J. Gomer, Antiangiogenic treatment enhances photodynamic therapy responsiveness in a mouse mammary carcinoma, Cancer Res., 2000, 60, 4066–4069.

    CAS  PubMed  Google Scholar 

  69. A. Ferrario, C. J. Gomer, Avastin enhances photodynamic therapy treatment of Kaposi’s sarcoma in a mouse tumor model, J. Environ. Pathol. Toxicol. Oncol., 2006, 25, 251–259.

    Article  CAS  PubMed  Google Scholar 

  70. R. Bhuvaneswari, G. Y. Yuen, S. K. Chee, M. Olivo, Hypericin-mediated photodynamic therapy in combination with Avastin (bevacizumab) improves tumor response by downregulating angiogenic proteins, Photochem. Photobiol. Sci., 2007, 6, 1275–1283.

    Article  CAS  PubMed  Google Scholar 

  71. F. Jiang, X. Zhang, S. N. Kalkanis, Z. Zhang, H. Yang, M. Katakowski, X. Hong, X. Zheng, Z. Zhu, M. Chopp, Combination therapy with antiangiogenic treatment and photodynamic therapy for the nude mouse bearing U87 glioblastoma, Photochem. Photobiol., 2008, 84, 128–137.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. R. K. Jain, Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy, Science, 2005, 307, 58–62.

    Article  CAS  PubMed  Google Scholar 

  73. R. K. Jain, D. G. Duda, J. W. Clark, J. S. Loeffler, Lessons from phase III clinical trials on anti-VEGF therapy for cancer, Nat. Clin. Pract. Oncol., 2006, 3, 24–40.

    Article  CAS  PubMed  Google Scholar 

  74. S. O. Gollnick, L. Vaughan, B. W. Henderson, Generation of effective antitumor vaccines using photodynamic therapy, Cancer Res., 2002, 62, 1604–1608.

    CAS  PubMed  Google Scholar 

  75. M. Korbelik, J. Sun, Photodynamic therapy-generated vaccine for cancer therapy, Cancer Immunol. Immunother., 2006, 55, 900–909.

    Article  CAS  PubMed  Google Scholar 

  76. M. Korbelik, B. Stott, J. Sun, Photodynamic therapy-generated vaccines: relevance of tumour cell death expression, Br. J. Cancer, 2007, 97, 1381–1387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. J. E. Vance, R. Steenbergen, Metabolism and functions of phosphatidylserine, Prog. Lipid Res., 2005, 44, 207–234.

    Article  CAS  PubMed  Google Scholar 

  78. S. Mocellin, S. Mandruzzato, V. Bronte, M. Lise, D. Nitti, Part I: Vaccines for solid tumours, Lancet Oncol., 2004, 5, 681–689.

    Article  CAS  PubMed  Google Scholar 

  79. J. Copier, S. Ward, A. Dalgleish, Cell based cancer vaccines: regulatory and commercial development, Vaccine, 2007, 25, 2, B35–46.

    Article  CAS  PubMed  Google Scholar 

  80. O. J. Finn, Cancer vaccines: between the idea and the reality, Nat. Rev. Immunol., 2003, 3, 630–641.

    Article  CAS  PubMed  Google Scholar 

  81. N. L. Berinstein, Enhancing cancer vaccines with immunomodulators, Vaccine, 2007, 25, 2, B72–88.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Microbiology and Serology, National Salmonella Centre, Medical University of Gdansk, ul. Do Studzienki 38, 80-227, Gdansk, Poland

    Mateusz Kwitniewski

  2. Department of Radiation Biology, Institute for Cancer Research, Norwegian Radium Hospital, Rikshospitalet University Hospital, Montebello, Oslo, 0310, Norway

    Mateusz Kwitniewski, Asta Juzeniene & Johan Moan

  3. R & D Immunolab Company Ltd, ul. Al. Zwycięstwa 96/98, 81-451, Gdynia, Poland

    Renata Glosnicka

  4. Institute of Physics, University of Oslo, Blindern, 0316, Oslo, Norway

    Johan Moan

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  1. Mateusz Kwitniewski
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Correspondence to Mateusz Kwitniewski.

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Kwitniewski, M., Juzeniene, A., Glosnicka, R. et al. Immunotherapy: a way to improve the therapeutic outcome of photodynamic therapy?. Photochem Photobiol Sci 7, 1011–1017 (2008). https://doi.org/10.1039/b806710d

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