Stimulation of anti-tumor immunity by photodynamic therapy

Expert Review of Clinical Immunology

Volumn 7, Issue 1, 2011, Pages 75-91

  Mroz, Pawel ^a,b   Hashmi, Javad T ^a,b   Huang, Ying Ying ^a,b,c   Lange, Norbert ^d   Hamblin, Michael R ^a,b,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c GUANGXI MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

anti tumor immunity; cancer vaccines; cytotoxic T lymphocytes; damage associated molecular patterns; dendritic cells; photodynamic therapy; Toll like receptor agonists; tumor associated antigens

Indexed keywords

ADENOSINE TRIPHOSPHATE; BENZOPORPHYRIN DERIVATIVE; CALGRANULIN; CALRETICULIN; CANCER VACCINE; CYCLOPHOSPHAMIDE; GLYCOPROTEIN GP 96; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEMATOPORPHYRIN DERIVATIVE; HIGH MOBILITY GROUP B1 PROTEIN; MACROPHAGE ACTIVATING FACTOR; OLIGODEOXYNUCLEOTIDE; PHOTOFRIN; TUMOR NECROSIS FACTOR ALPHA; URATE; VERTEPORFIN; VITAMIN D BINDING PROTEIN;

ADAPTIVE IMMUNITY; ADENOCARCINOMA; APOPTOSIS; BREAST CARCINOMA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; COLON CARCINOMA; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DENDRITIC CELL; ENDOTHELIUM CELL; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSTIMULATION; INNATE IMMUNITY; LEWIS CARCINOMA; LOW DRUG DOSE; LUNG CANCER; LUNG CARCINOMA; MACROPHAGE; MONOCYTE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PHOTODYNAMIC THERAPY; REGULATORY T LYMPHOCYTE; REVIEW; SARCOMA; SINGLE DRUG DOSE; SQUAMOUS CELL CARCINOMA; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSITIONAL CELL CARCINOMA; TUMOR CELL; TUMOR IMMUNITY; TUMOR NECROSIS; TUMOR VASCULARIZATION;

ANIMALS; CELL LINE; HUMANS; IMMUNITY, INNATE; MICE; MICE, INBRED BALB C; MICE, SCID; NEOPLASMS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; T-LYMPHOCYTES; TREATMENT OUTCOME;

EID: 78650548783     PISSN: 1744666X     EISSN: None     Source Type: Journal    
DOI: 10.1586/eci.10.81     Document Type: Review

References (161)

1. Jemal A, Siegel R, Ward E et al. Cancer statistics, 2008. CA Cancer J. Clin. 58(2), 71-96 (2008).
2. Sheridan C. Fresh from the biologic pipeline - 2009. Nat. Biotechnol. 28(4), 307-310 (2010).
3. Simon R. Lost in translation: problems and pitfalls in translating laboratory observations to clinical utility. Eur. J. Cancer 44(18), 2707-2713 (2008).
4. Wu X, Lee VC, Chevalier E, Hwang ST. Chemokine receptors as targets for cancer therapy. Curr. Pharm. Des. 15(7), 742-757 (2009).
5. Klastersky J. Adverse effects of the humanized antibodies used as cancer therapeutics. Curr. Opin Oncol. 18(4), 316-320 (2006).
6. Barrett A, Roques T, Small M, Smith RD. How much will Herceptin really cost? Br. Med. J. 333(7578), 1118-1120 (2006).
7. La Porta CA. Mechanism of drug sensitivity and resistance in melanoma. Curr. Cancer Drug Targets 9(3), 391-397 (2009).
8. Laconi E, Pani P, Farber E. The resistance phenotype in the development and treatment of cancer. Lancet Oncol. 1, 235-241 (2000).
9. Bianco R, Damiano V, Gelardi T, Daniele G, Ciardiello F, Tortora G. Rational combination of targeted therapies as a strategy to overcome the mechanisms of resistance to inhibitors of EGFR signaling. Curr. Pharm. Des. 13(33), 3358-3367 (2007).
10. Robertson CA, Evans DH, Abrahamse H. Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT. J. Photochem. Photobiol. B. Biol. 96(1), 1-8 (2009).
11. Moan J, Peng Q. An outline of the hundred-year history of PDT. Anticancer Res. 23(5A), 3591-3600 (2003).
12. Ogilby PR. Singlet oxygen: there is indeed something new under the sun. Chem. Soc. Rev. 39(8), 3181-3209 (2010).
13. Robey RW, Steadman K, Polgar O, Bates SE. ABCG2-mediated transport of photosensitizers: potential impact on photodynamic therapy. Cancer Biol. Ther. 4(2), 187-194 (2005).
14. Xue LY, Chiu SM, Oleinick NL. Atg7 deficiency increases resistance of MCF-7 human breast cancer cells to photodynamic therapy. Autophagy 6(2), 248-255 (2010).
15. Detty MR, Gibson SL, Wagner SJ. Current clinical and preclinical photosensitizers for use in photodynamic therapy. J. Med. Chem. 47(16), 3897-3915 (2004).
16. Boyle RW, Dolphin D. Structure and biodistribution relationships of photodynamic sensitizers. Photochem. Photobiol. 64(3), 469-485 (1996).
17. Konan YN, Gurny R, Allemann E. State of the art in the delivery of photosensitizers for photodynamic therapy. J. Photochem. Photobiol. B. Biol. 66(2), 89-106 (2002).
18. Oleinick NL, Morris RL, Belichenko I. The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem. Photobiol. Sci. 1(1), 1-21 (2002).
19. Almeida RD, Manadas BJ, Carvalho AP, Duarte CB. Intracellular signaling mechanisms in photodynamic therapy. Biochim. Biophys. Acta 1704(2), 59-86 (2004).
20. Granville DJ, McManus BM, Hunt DW. Photodynamic therapy: shedding light on the biochemical pathways regulating porphyrin-mediated cell death. Histol. Histopathol. 16(1), 309-317 (2001).
21. Girotti AW. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J. Photochem. Photobiol. B. Biol. 63(1-3), 103-113 (2001).
22. Kessel D, Reiners JJ Jr. Initiation of apoptosis and autophagy by the Bcl-2 antagonist HA14-1. Cancer Lett. 249(2), 294-299 (2007).
23. Xue LY, Chiu SM, Azizuddin K, Joseph S, Oleinick NL. The death of human cancer cells following photodynamic therapy: apoptosis competence is necessary for Bcl-2 protection but not for induction of autophagy. Photochem. Photobiol. 83(5), 1016-1023 (2007).
24. Blum HF. Photodynamic Action and Diseases Caused by Light (No. 85). Reinhold Publishing Corporation, NY, USA, 239-250 (1941).
25. Castano AP, Mroz P, Hamblin MR. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 6(7), 535-545 (2006).
26. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81(1), 1-5 (2007).
27. Garg AD, Nowis D, Golab J, Agostinis P. Photodynamic therapy: illuminating the road from cell death towards anti-tumour immunity. Apoptosis 15(9), 1050-1071 (2010).
28. Garg AD, Nowis D, Golab J, Vandenabeele P, Krysko DV, Agostinis P. Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim. Biophys. Acta 1805(1), 53-71 (2010).
29. Seong SY, Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4(6), 469-478 (2004).
30. Melcher A, Gough M, Todryk S, Vile R. Apoptosis or necrosis for tumor immunotherapy: whats in a name? J. Mol. Med. 77(12), 824-833 (1999).
31. Melcher A, Todryk S, Hardwick N, Ford M, Jacobson M, Vile RG. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat. Med. 4(5), 581-587 (1998).
32. Tesniere A, Panaretakis T, Kepp O et al. Molecular characteristics of immunogenic cancer cell death. Cell Death Differ. 15(1), 3-12 (2008).
33. Scheffer SR, Nave H, Korangy F et al. Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int. J. Cancer. 103(2), 205-211 (2003).
34. Goldszmid RS, Idoyaga J, Bravo AI, Steinman R, Mordoh J, Wainstok R. Dendritic cells charged with apoptotic tumor cells induce long-lived protective CD4+ and CD8+ T cell immunity against B16 melanoma. J. Immunol. 171(11), 5940-5947 (2003).
35. Kepp O, Tesniere A, Schlemmer F et al. Immunogenic cell death modalities and their impact on cancer treatment. Apoptosis 14(4), 364-375 (2009).
36. Zitvogel L, Kroemer G. The immune response against dying tumor cells: avoid disaster, achieve cure. Cell Death Differ. 15(1), 1-2 (2008).
37. Korbelik M, Sun J, Cecic I. Photodynamic therapy-induced cell surface expression and release of heat shock proteins: relevance for tumor response. Cancer Res. 65(3), 1018-1026 (2005).
38. Gomer CJ, Ryter SW, Ferrario A, Rucker N, Wong S, Fisher AM. Photodynamic therapy-mediated oxidative stress can induce expression of heat shock proteins. Cancer Res. 56(10), 2355-2360 (1996).
39. Delves PJ, Roitt IM. The immune system. First of two parts. N. Engl. J. Med. 343(1), 37-49 (2000).
40. Dougherty TJ, Gomer CJ, Henderson BW et al. Photodynamic therapy. J. Natl Cancer Inst. 90(12), 889-905 (1998).
41. Korbelik M. Induction of tumor immunity by photodynamic therapy. J. Clin. Laser Med. Surg. 14(5), 329-334 (1996).
42. Gollnick SO, Evans SS, Baumann H et al. Role of cytokines in photodynamic therapy-induced local and systemic inflammation. Br. J. Cancer 88(11), 1772-1779 (2003).
43. Korbelik M. PDT-associated host response and its role in the therapy outcome. Lasers Surg. Med. 38(5), 500-508 (2006).
44. Krosl G, Korbelik M, Dougherty GJ. Induction of immune cell infiltration into murine SCCVII tumour by photofrin-based photodynamic therapy. Br. J. Cancer 71(3), 549-555 (1995).
45. Cecic I, Stott B, Korbelik M. Acute phase response-associated systemic neutrophil mobilization in mice bearing tumors treated by photodynamic therapy. Int. Immunopharmacol. 6(8), 1259-1266 (2006).
46. Korbelik M, Cecic I. Complement activation cascade and its regulation: relevance for the response of solid tumors to photodynamic therapy. J. Photochem. Photobiol. B. Biol. 93(1), 53-59 (2008).
47. Cecic I, Korbelik M. Deposition of complement proteins on cells treated by photodynamic therapy in vitro. J. Environ. Pathol. Toxicol. Oncol. 25(1-2), 189-203 (2006).
48. Cecic I, Sun J, Korbelik M. Role of complement anaphylatoxin C3a in photodynamic therapy-elicited engagement of host neutrophils and other immune cells. Photochem. Photobiol. 82(2), 558-562 (2006).
49. Stott B, Korbelik M. Activation of complement C3, C5, and C9 genes in tumors treated by photodynamic therapy. Cancer Immunol. Immunother. 56(5), 649-658 (2007). (Pubitemid 46348734)
50. Cecic I, Korbelik M. Mediators of peripheral blood neutrophilia induced by photodynamic therapy of solid tumors. Cancer Lett. 183(1), 43-51 (2002).
51. Korbelik M, Cecic I, Merchant S, Sun J. Acute phase response induction by cancer treatment with photodynamic therapy. Int. J. Cancer 122(6), 1411-1417 (2008).
52. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23 901-944 (2005).
53. Steubing RW, Yeturu S, Tuccillo A, Sun CH, Berns MW. Activation of macrophages by Photofrin II during photodynamic therapy. J. Photochem. Photobiol. B. Biol. 10(1-2), 133-145 (1991).
54. Evans S, Matthews W, Perry R, Fraker D, Norton J, Pass HI. Effect of photodynamic therapy on tumor necrosis factor production by murine macrophages. J. Natl Cancer Inst. 82(1), 34-39 (1990).
55. Yamamoto N, Homma S, Sery TW, Donoso LA, Hoober JK. Photodynamic immunopotentiation: in vitro activation of macrophages by treatment of mouse peritoneal cells with haematoporphyrin derivative and light. Eur. J. Cancer 27(4), 467-471 (1991).
56. Yamamoto N, Naraparaju VR. Immunotherapy of BALB/c mice bearing Ehrlich ascites tumor with vitamin D-binding protein-derived macrophage activating factor. Cancer Res. 57(11), 2187-2192 (1997).
57. Korbelik M, Krosl G. Enhanced macrophage cytotoxicity against tumor cells treated with photodynamic therapy. Photochem. Photobiol. 60(5), 497-502 (1994).
58. Marshall JF, Chan WS, Hart IR. Effect of photodynamic therapy on anti-tumor immune defenses: comparison of the photosensitizers hematoporphyrin derivative and chloro-aluminum sulfonated phthalocyanine. Photochem. Photobiol. 49(5), 627-632 (1989).
59. Krosl G, Korbelik M, Krosl J, Dougherty GJ. Potentiation of photodynamic therapy-elicited antitumor response by localized treatment with granulocyte-macrophage colony-stimulating factor. Cancer Res. 56(14), 3281-3286 (1996).
60. Delves PJ, Roitt IM. The immune system. N. Engl. J. Med. 343, 37-49 (2000).
61. Henderson BW, Gollnick SO, Snyder JW et al. Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors. Cancer Res. 64(6), 2120-2126 (2004).
62. Kousis PC, Henderson BW, Maier PG, Gollnick SO. Photodynamic therapy enhancement of antitumor immunity is regulated by neutrophils. Cancer Res. 67(21), 10501-10510 (2007).
63. Sluiter W, de Vree WJ, Pietersma A, Koster JF. Prevention of late lumen loss after coronary angioplasty by photodynamic therapy: role of activated neutrophils. Mol. Cell. Biochem. 157(1-2), 233-238 (1996).
64. de Vree WJ, Fontijne-Dorsman AN, Koster JF, Sluiter W. Photodynamic treatment of human endothelial cells promotes the adherence of neutrophils in vitro. Br. J. Cancer 73(11), 1335-1340 (1996).
65. Volanti C, Gloire G, Vanderplasschen A, Jacobs N, Habraken Y, Piette J. Downregulation of ICAM-1 and VCAM-1 expression in endothelial cells treated by photodynamic therapy. Oncogene 23(53), 8649-8658 (2004).
66. de Vree WJ, Essers MC, de Bruijn HS, Star WM, Koster JF, Sluiter W. Evidence for an important role of neutrophils in the efficacy of photodynamic therapy in vivo. Cancer Res. 56(13), 2908-2911 (1996).
67. Sun J, Cecic I, Parkins CS, Korbelik M. Neutrophils as inflammatory and immune effectors in photodynamic therapy-treated mouse SCCVII tumours. Photochem. Photobiol. Sci. 1(9), 690-695 (2002).
68. Cecic I, Parkins CS, Korbelik M. Induction of systemic neutrophil response in mice by photodynamic therapy of solid tumors. Photochem. Photobiol. 74(5), 712-720 (2001).
69. de Bruijn HS, Sluiter W, van der Ploeg-van den Heuvel A, Sterenborg HJ, Robinson DJ. Evidence for a bystander role of neutrophils in the response to systemic 5-aminolevulinic acid-based photodynamic therapy. Photodermatol. Photoimmunol. Photomed. 22(5), 238-246 (2006).
70. Kabingu E, Vaughan L, Owczarczak B, Ramsey KD, Gollnick SO. 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 96(12), 1839-1848 (2007).
71. Adams S, ONeill DW, Bhardwaj N. Recent advances in dendritic cell biology. J. Clin. Immunol. 25(3), 177-188 (2005).
72. Gabrilovich DI, Chen HL, Girgis KR et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 2(10), 1096-1103 (1996).
73. Yenari MA, Liu J, Zheng Z, Vexler ZS, Lee JE, Giffard RG. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann. NY Acad. Sci. 1053, 74-83 (2005).
74. Todryk S, Melcher AA, Hardwick N et al. Heat shock protein 70 induced during tumor cell killing induces Th1 cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J. Immunol. 163(3), 1398-1408 (1999).
75. Korbelik M, Sun J. Photodynamic therapy-generated vaccine for cancer therapy. Cancer Immunol. Immunother. 55(8), 900-909 (2006).
76. 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. 5(4), 443-447 (1994).
77. Korbelik M, Krosl G, Krosl J, Dougherty GJ. The role of host lymphoid populations in the response of mouse EMT6 tumor to photodynamic therapy. Cancer Res. 56(24), 5647-5652 (1996).
78. Korbelik M, Dougherty GJ. Photodynamic therapy-mediated immune response against subcutaneous mouse tumors. Cancer Res. 59(8), 1941-1946 (1999).
79. Hendrzak-Henion JA, Knisely TL, Cincotta L, Cincotta E, Cincotta AH. Role of the immune system in mediating the antitumor effect of benzophenothiazine photodynamic therapy. Photochem. Photobiol. 69(5), 575-581 (1999).
80. Van den Eynde BJ, van der Bruggen P. T cell defined tumor antigens. Curr. Opin. Immunol. 9(5), 684-693 (1997).
81. Van den Eynde B, Lethe B, Van Pel A, De Plaen E, Boon T. The gene coding for a major tumor rejection antigen of tumor P815 is identical to the normal gene of syngeneic DBA/2 mice. J. Exp. Med. 173(6), 1373-1384 (1991).
82. Van den Eynde B, Peeters O, De Backer O, Gaugler B, Lucas S, Boon T. A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma. J. Exp. Med. 182(3), 689-698 (1995).
83. van der Bruggen P, Traversari C, Chomez P et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254(5038), 1643-1647 (1991).
84. Gaugler B, Van den Eynde B, van der Bruggen P et al. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J. Exp. Med. 179(3), 921-930 (1994).
85. Traversari C, van der Bruggen P, Luescher IF et al. A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J. Exp. Med. 176(5), 1453-1457 (1992).
86. Coulie PG, Brichard V, Van Pel A et al. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 180(1), 35-42 (1994). (Pubitemid 24181053)
87. Brichard V, Van Pel A, Wolfel T et al. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 178(2), 489-495 (1993).
88. Bakker AB, Schreurs MW, de Boer AJ et al. Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J. Exp. Med. 179(3), 1005-1009 (1994).
89. Coulie PG, Lehmann F, Lethe B et al. A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma. Proc. Natl Acad. Sci. USA 92(17), 7976-7980 (1995).
90. Mandelboim O, Berke G, Fridkin M, Feldman M, Eisenstein M, Eisenbach L. CTL induction by a tumour-associated antigen octapeptide derived from a murine lung carcinoma. Nature 369(6475), 67-71 (1994).
91. Monach PA, Meredith SC, Siegel CT, Schreiber H. A unique tumor antigen produced by a single amino acid substitution. Immunity 2(1), 45-59 (1995).
92. Robbins PF, El-Gamil M, Li YF et al. A mutated b-catenin gene encodes a melanoma-specific antigen recognized by tumor infiltrating lymphocytes. J. Exp. Med. 183(3), 1185-1192 (1996).
93. Dubey P, Hendrickson RC, Meredith SC et al. The immunodominant antigen of an ultraviolet-induced regressor tumor is generated by a somatic point mutation in the DEAD box helicase p68. J. Exp. Med. 185(4), 695-705 (1997).
94. Wang M, Bronte V, Chen PW et al. Active immunotherapy of cancer with a nonreplicating recombinant fowlpox virus encoding a model tumor-associated antigen. J. Immunol. 154(9), 4685-4692 (1995).
95. McCabe BJ, Irvine KR, Nishimura MI et al. Minimal determinant expressed by a recombinant vaccinia virus elicits therapeutic antitumor cytolytic T lymphocyte responses. Cancer Res. 55(8), 1741-1747 (1995).
96. Marzo AL, Lake RA, Robinson BW, Scott B. T-cell receptor transgenic analysis of tumor-specific CD8 and CD4 responses in the eradication of solid tumors. Cancer Res. 59(5), 1071-1079 (1999).
97. Ramarathinam L, Sarma S, Maric M et al. Multiple lineages of tumors express a common tumor antigen, P1A, but they are not cross-protected. J. Immunol. 155(11), 5323-5329 (1995).
98. Uyttenhove C, Godfraind C, Lethe B et al. The expression of mouse gene P1A in testis does not prevent safe induction of cytolytic T cells against a P1A-encoded tumor antigen. Int. J. Cancer. 70(3), 349-356 (1997).
99. Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nat. Rev. Cancer 7(1), 11-22 (2007).
100. Castano AP, Liu Q, Hamblin MR. A green fluorescent protein-expressing murine tumour but not its wild-type counterpart is cured by photodynamic therapy. Br. J. Cancer 94(3),391-397 (2006).
101. Mroz P, Szokalska A, Wu MX, Hamblin M. Photodynamic therapy of tumors can lead to development of systemic antigen-specific immune response. PLoS ONE (2011) (In Press).
102. Abdel-Hady ES, Martin-Hirsch P, Duggan-Keen M et al. Immunological and viral factors associated with the response of vulval intraepithelial neoplasia to photodynamic therapy. Cancer Res. 61(1), 192-196 (2001).
103. Kabingu E, Oseroff AR, Wilding GE, Gollnick SO. Enhanced systemic immune reactivity to a Basal cell carcinoma associated antigen following photodynamic therapy. Clin. Cancer Res. 15(13), 4460-4466 (2009).
104. Gershon RK, Cohen P, Hencin R, Leibhaber SA. Suppressor T cells. J. Immunol. 108, 586-590 (1972).
105. Dejaco C, Duftner C, Grubeck-Loebenstein B, Schirmer M. Imbalance of regulatory T cells in human autoimmune diseases. Immunology 117(3), 289-300 (2006).
106. Yamaguchi T, Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin. Cancer Biol. 16(2), 115-123 (2006).
107. Antony PA, Restifo NP. CD4+CD25+ T regulatory cells, immunotherapy of cancer, and interleukin-2. J. Immunother. 28(2), 120-128 (2005).
108. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6(4), 331-337 (2005).
109. Scotto L, Naiyer AJ, Galluzzo S et al. Overlap between molecular markers expressed by naturally occurring CD4+CD25+ regulatory T cells and antigen specific CD4+CD25+ and CD8+CD28- T suppressor cells. Hum. Immunol. 65(11), 1297-1306 (2004).
110. Albers AE, Ferris RL, Kim GG, Chikamatsu K, DeLeo AB, Whiteside TL. Immune responses to p53 in patients with cancer: enrichment in tetramer+ p53 peptide-specific T cells and regulatory T cells at tumor sites. Cancer Immunol. Immunother. 54(11), 1072-1081 (2005).
111. Ziegler SF. FOXP3: of mice and men. Annu. Rev. Immunol. 24, 209-226 (2006).
112. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6(4), 295-307 (2006).
113. Curotto de Lafaille MA, Lino AC, Kutchukhidze N, Lafaille JJ. CD25- T cells generate CD25+Foxp3+ regulatory T cells by peripheral expansion. J. Immunol. 173(12), 7259-7268 (2004).
114. Chen W, Jin W, Hardegen N et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-b induction of transcription factor Foxp3. J. Exp. Med. 198(12), 1875-1886 (2003).
115. Bluestone JA, Tang Q. How do CD4+CD25+ regulatory T cells control autoimmunity? Curr. Opin. Immunol. 17(6), 638-642 (2005).
116. Tang Q, Boden EK, Henriksen KJ, Bour-Jordan H, Bi M, Bluestone JA. Distinct roles of CTLA-4 and TGF-b in CD4+CD25+ regulatory T cell function. Eur. J. Immunol. 34(11), 2996-3005 (2004).
117. Stephens GL, McHugh RS, Whitters MJ et al. Engagement of glucocorticoid-induced TNFR family-related receptor on effector T cells by its ligand mediates resistance to suppression by CD4+CD25+ T cells. J. Immunol. 173(8), 5008-5020 (2004).
118. Marie JC, Letterio JJ, Gavin M, Rudensky AY. TGF-b1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 201(7), 1061-1067 (2005).
119. Ghiringhelli F, Puig PE, Roux S et al. Tumor cells convert immature myeloid dendritic cells into TGF-b-secreting cells inducing CD4+CD25+ regulatory T cell proliferation. J. Exp. Med. 202(7), 919-929 (2005).
120. Veldhoen M, Moncrieffe H, Hocking RJ, Atkins CJ, Stockinger B. Modulation of dendritic cell function by naive and regulatory CD4+ T cells. J. Immunol. 176(10), 6202-6210 (2006).
121. Rudensky AY, Campbell DJ. In vivo sites and cellular mechanisms of T reg cell-mediated suppression. J. Exp. Med. 203(3), 489-492 (2006).
122. Ghiringhelli F, Larmonier N, Schmitt E et al. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur. J. Immunol. 34(2), 336-344 (2004).
123. Rollinghoff M, Starzinski-Powitz A, Pfizenmaier K, Wagner H. Cyclophosphamide-sensitive T lymphocytes suppress the in vivo generation of antigen-specific cytotoxic T lymphocytes. J. Exp. Med. 145(2), 455-459 (1977).
124. Glaser M. Regulation of specific cell-mediated cytotoxic response against SV40-induced tumor associated antigens by depletion of suppressor T cells with cyclophosphamide in mice. J. Exp. Med. 149(3), 774-779 (1979). (Pubitemid 9137688)
125. Berendt MJ, North RJ. T-cell-mediated suppression of anti-tumor immunity. An explanation for progressive growth of an immunogenic tumor. J. Exp. Med. 151(1), 69-80 (1980).
126. Loeffler M, Kruger JA, Reisfeld RA. Immunostimulatory effects of low-dose cyclophosphamide are controlled by inducible nitric oxide synthase. Cancer Res. 65(12), 5027-5030 (2005).
127. Castano AP, Hamblin MR. Anti-tumor immunity generated by photodynamic therapy in a metastatic murine tumor model. Proc. SPIE 5695, 7-16 (2005).
128. Muzio M, Mantovani A. Toll-like receptors. Microbes Infect. 2(3), 251-255 (2000).
129. Oshiumi H, Matsuo A, Matsumoto M, Seya T. Pan-vertebrate Toll-like receptors during evolution. Curr. Genomics 9(7), 488-493 (2008).
130. Armant MA, Fenton MJ. Toll-like receptors: a family of pattern-recognition receptors in mammals. Genome Biol. 3(8), reviews3011.1-reviews3011.6 (2002).
131. van Kooyk Y. C-type lectins on dendritic cells: key modulators for the induction of immune responses. Biochem. Soc. Trans. 36(Pt 6), 1478-1481 (2008).
132. Cambi A, Koopman M, Figdor CG. How C-type lectins detect pathogens. Cell Microbiol. 7(4), 481-488 (2005).
133. Chen WR, Korbelik M, Bartels KE, Liu H, Sun J, Nordquist RE. Enhancement of laser cancer treatment by a chitosan-derived immunoadjuvant. Photochem. Photobiol. 81(1), 190-195 (2005).
134. Krosl G, Korbelik M. Potentiation of photodynamic therapy by immunotherapy: the effect of schizophyllan (SPG). Cancer Lett. 84(1), 43-49 (1994).
135. 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. 3(8), 812-816 (2004).
136. Bellnier DA. Potentiation of photodynamic therapy in mice with recombinant human tumor necrosis factor-a. J. Photochem. Photobiol. B. Biol. 8(2), 203-210 (1991).
137. Korbelik M, Naraparaju VR, Yamamoto N. Macrophage-directed immunotherapy as adjuvant to photodynamic therapy of cancer. Br. J. Cancer 75(2), 202-207 (1997).
138. Golab J, Wilczynski G, Zagozdzon R et al. Potentiation of the anti-tumour effects of Photofrin-based photodynamic therapy by localized treatment with G-CSF. Br. J. Cancer 82(8), 1485-1491 (2000).
139. Korbelik M, Cooper PD. Potentiation of photodynamic therapy of cancer by complement: the effect of g-inulin. Br. J. Cancer 96(1), 67-72 (2007).
140. Weiner LM, Surana R, Murray J. Vaccine prevention of cancer: can endogenous antigens be targeted? Cancer Prev. Res. 3(4), 410-415 (2010).
141. Critchfield JM, Racke MK, Zuniga- Pflucker JC et al. T cell deletion in high antigen dose therapy of autoimmune encephalomyelitis. Science 263(5150), 1139-1143 (1994).
142. Gollnick SO, Vaughan L, Henderson BW. Generation of effective antitumor vaccines using photodynamic therapy. Cancer Res. 62(6), 1604-1608 (2002).
143. Sgambato A, Cittadini A. Inflammation and cancer: a multifaceted link. Eur. Rev. Med. Pharmacol. Sci. 14(4), 263-268 (2010).
144. Thong PS, Ong KW, Goh NS et al. Photodynamic-therapy-activated immune response against distant untreated tumours in recurrent angiosarcoma. Lancet Oncol. 8(10), 950-952 (2007).
145. Zitvogel L, Kepp O, Senovilla L, Menger L, Chaput N, Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clin. Cancer Res. 16(12), 3100-3104 (2010).
146. Spisek R, Dhodapkar MV. Towards a better way to die with chemotherapy: role of heat shock protein exposure on dying tumor cells. Cell Cycle 6(16), 1962-1965 (2007).
147. Tang D, Kang R, Zeh HJ 3rd, Lotze MT. High-mobility group box 1 and cancer. Biochim. Biophys. Acta 1799(1-2), 131-140 (2010).
148. Martins I, Tesniere A, Kepp O et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle 8(22), 3723-3728 (2009).
149. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr. Mol. Med. 7(8), 711-724 (2007).
150. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, Saito T. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat. Immunol. 9(10), 1179-1188 (2008).
151. Horino K, Nishiura H, Ohsako T et al. A monocyte chemotactic factor, S19 ribosomal protein dimer, in phagocytic clearance of apoptotic cells. Lab. Invest. 78(5), 603-617 (1998).
152. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425(6957), 516-521 (2003).
153. Uehara M, Sano K, Wang ZL, Sekine J, Ikeda H, Inokuchi T. Enhancement of the photodynamic antitumor effect by streptococcal preparation OK-432 in the mouse carcinoma. Cancer Immunol. Immunother. 49(8), 401-409 (2000).
154. Castano AP, Hamblin MR. Enhancing photodynamic therapy of a metastatic mouse breast cancer by immune stimulation. In: Biophotonics and Immune Responses. San Jose: The International Society for Optical Engineering, WA, USA (2006).
155. Korbelik M, Cecic I. Enhancement of tumour response to photodynamic therapy by adjuvant mycobacterium cell-wall treatment. J. Photochem. Photobiol. B. Biol. 44(2), 151-158 (1998).
156. Korbelik M, Sun J, Posakony JJ. Interaction between photodynamic therapy and BCG immunotherapy responsible for the reduced recurrence of treated mouse tumors. Photochem. Photobiol. 73(4), 403-409 (2001).
157. Myers RC, Lau BH, Kunihira DY, Torrey RR, Woolley JL, Tosk J. Modulation of hematoporphyrin derivative-sensitized phototherapy with corynebacterium parvum in murine transitional cell carcinoma. Urology 33(3), 230-235 (1989).
158. Winters U, Daayana S, Lear JT et al. Clinical and immunologic results of a Phase II trial of sequential imiquimod and photodynamic therapy for vulval intraepithelial neoplasia. Clin. Cancer Res. 14(16), 5292-5299 (2008).
159. Seshadri M, Bellnier DA. The vascular disrupting agent 5,6-dimethylxanthenone- 4-acetic acid improves the antitumor efficacy and shortens treatment time associated with Photochlor-sensitized photodynamic therapy in vivo. Photochem. Photobiol. 85(1), 50-56 (2009).
160. Krosl G, Korbelik M, Krosl J, Dougherty GJ. Potentiation of photodynamic therapy-elicited antitumor response by localized treatment with granulocyte-macrophage colony-stimulating factor. Cancer Res. 56(14), 3281-3286 (1996).
161. Castano AP, Mroz P, Wu MX, Hamblin MR. Photodynamic therapy plus low-dose cyclophosphamide generates antitumor immunity in a mouse model. Proc. Natl Acad. Sci. USA 105(14), 5495-5500 (2008).