Inhibition of NF-κB in tumor cells exacerbates immune cell activation following photodynamic therapy

International Journal of Molecular Sciences

Volumn 16, Issue 8, 2015, Pages 19960-19977

  Broekgaarden, Mans ^a   Kos, Milan ^a   Jurg, Freek A ^a   van Beek, Adriaan A ^b   van Gulik, Thomas M ^a   Heger, Michal ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Anti tumor immunity; Inflammation; Interferon gamma; Interleukin 12p70; Interleukin 6; Monocyte chemotactic protein 1 interleukin 10; Phototherapy; siRNA; Tumor necrosis factor alpha

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOSOME; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; PHTHALOCYANINE ZINC; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; CONDITIONED MEDIUM; CYTOKINE; INDOLE DERIVATIVE; ORGANOMETALLIC COMPOUND; PHOTOSENSITIZING AGENT; ZN(II)-PHTHALOCYANINE;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ACTIVATION; CELL VIABILITY; GENETIC TRANSFECTION; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PROTEIN SYNTHESIS INHIBITION; TUMOR CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL SURVIVAL; CONDITIONED MEDIUM; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE SILENCING; IMMUNOLOGY; METABOLISM; PHARMACOLOGY; PHOTOCHEMOTHERAPY; PROCEDURES; TUMOR CELL LINE;

MURINAE;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; CULTURE MEDIA, CONDITIONED; CYTOKINES; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; INDOLES; MACROPHAGES; MICE; NF-KAPPA B; ORGANOMETALLIC COMPOUNDS; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; RNA, SMALL INTERFERING;

EID: 84939856901     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160819960     Document Type: Article

References (68)

1. Dolmans, D.E.J.G.J.; Fukumura, D.; Jain, R.K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3, 380–387
2. Broekgaarden, M.; Weijer, R.; van Gulik, T.M.; Hamblin, M.R.; Heger, M. Tumor cell survival pathways activated by photodynamic therapy: A molecular basis for pharmacological inhibition strategies. Cancer Metastasis Rev.2015, in press.
3. Khan, S.A.; Thomas, H.C.; Davidson, B.R.; Taylor-Robinson, S.D. Cholangiocarcinoma. Lancet 2005, 366, 1303–1314
4. O’Connor, A.E.; Gallagher, W.M.; Byrne, A.T. Porphyrin and nonporphyrin photosensitizers in oncology: Preclinical and clinical advances in photodynamic therapy. Photochem. Photobiol. 2009, 85, 1053–1074
5. Weijer, R.; Broekgaarden, M.; Kos, M.; Vught, R.; Rauws, E.; van Gulik, T.M.; Heger, M. Enhancing photodynamic therapy of refractory solid cancers: Combining second generation photosensitizers with multi-targeted drug delivery. J. Photochem. Photobiol. C Photochem. Rev.2015, 23, 103–131
6. Broekgaarden, M.; de Kroon, A.I.P.M.; van Gulik, T.M.; Heger, M. Development and in vitro proof-of-concept of interstitially targeted zinc-phthalocyanine liposomes for photodynamic therapy. Curr. Med. Chem. 2013, 21, 377–391
7. Rizvi, I.; Celli, J.P.; Evans, C.L.; Abu-Yousif, A.O.; Muzikansky, A.; Pogue, B.W.; Finkelstein, D.; Hasan, T. Synergistic enhancement of carboplatin efficacy with photodynamic therapy in a three-dimensional model for micrometastatic ovarian cancer. Cancer Res. 2010, 70, 9319–9328
8. Broekgaarden, M.; Weijer, R.; van Wijk, A.C.; Cox, R.C.; Egmond, M.R.; Hoebe, R.; van Gulik, T.M.; Heger, M. Photodynamic therapy with liposomal zinc phthalocyanine and tirapazamine increases tumor cell death via DNA damage. J. Biomed. Nanotechnol. 2015, submitted.
9. Coupienne, I.; Bontems, S.B.; Dewaele, M.; Rubio, N.; Habraken, Y.; Fulda, S.; Agostinis, P.; Piette, J. NF-κB inhibition improves the sensitivity of human glioblastoma cells to 5-aminolevulinic acid-based photodynamic therapy. Biochem. Pharmacol. 2011, 81, 606–616
10. Matroule, J.Y.; Hellin, A.C.; Morliere, P.; Fabiano, A.S.; Santus, R.; Merville, M.P.; Piette, J. Role of nuclear factor-κB in colon cancer cell apoptosis mediated by aminopyropheophorbide photosensitization. Photochem. Photobiol. 1999, 70, 540–548
11. Chen, H.M.; Liu, C.M.; Yang, H.; Chou, H.Y.; Chiang, C.P.; Kuo, M.Y. 5-Aminolevulinic acid induce apoptosis via NF-κB/JNK pathway in human oral cancer Ca9–22 cells. J. Oral Pathol. Med. 2011, 40, 483–489
12. Taylor, C.T.; Cummins, E.P. The role of NF-κB in hypoxia-induced gene expression. Ann. N. Y. Acad. Sci. 2009, 1177, 178–184
13. Karin, M.; Cao, Y.; Greten, F.R.; Li, Z.-W. NF-κB in cancer: From innocent bystander to major culprit. Nat. Rev. Cancer 2002, 2, 301–310
14. Guttridge, D.C.; Albanese, C.; Reuther, J.Y.; Pestell, R.G.; Baldwin, A.S., Jr. NF-κB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol. Cell. Biol. 1999, 19, 5785–5799
15. Schoonbroodt, S.; Piette, J. Oxidative stress interference with the nuclear factor-κB activation pathways. Biochem. Pharmacol. 2000, 60, 1075–1083
16. Matroule, J.-Y.; Volanti, C.; Piette, J. NF-κB in photodynamic therapy: Discrepancies of a master regulator. Photochem. Photobiol. 2006, 82, 1241–1246
17. Korbelik, M.; Cecic, I. Contribution of myeloid and lymphoid host cells to the curative outcome of mouse sarcoma treatment by photodynamic therapy. Cancer Lett.1999, 137, 91–98
18. 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, 5647–5652
19. Thong, P.S.-P.; Ong, K.W.; Goh, N.S.G.; 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, 950–952
20. 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, 1839–1848
21. Matroule, J.Y.; Piette, J. Photosensitization and redox signaling. Antioxid. Redox Signal. 2000, 2, 301–315
22. Piva, R.; Belardo, G.; Santoro, M.G. NF-κB: A stress-regulated switch for cell survival. Antioxid. Redox Signal. 2006, 8, 478–486
23. Castano, A.P.; Mroz, P.; Hamblin, M.R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 2006, 6, 535–545
24. Broekgaarden, M.; Weijer, R.; van Golen, R.F.; Maas, M.A.; van Wijk, A.C.; Furse, S.; van Gulik, T.M.; Heger, M. Development of tumor vascular endothelium targeted liposomes containing zinc phthalocyanine for application in photodynamic therapy. ACS Nano 2015, in preparation.
25. Broekgaarden, M.; Weijer, R.; Krekorian, M.; van den IJssel, B.; Kos, M.; Alles, L.K.; van Wijk, A.C.; Bikadi, Z.; Hazai, E.; van Gulik, T.M., et al. Inhibition of hypoxia inducible factor 1 with acriflavine sensitizes tumor cells to photodynamic therapy with zinc phthalocyanine-encapsulating cationic liposomes. Nano Res. 2015, submitted.
26. Kloek, J.J.; Marechal, X.; Roelofsen, J.; Houtkooper, R.H.; van Kuilenburg, A.B.; Kulik, W.; Bezemer, R.; Neviere, R.; van Gulik, T.M.; Heger, M. Cholestasis is associated with hepatic microvascular dysfunction and aberrant energy metabolism before and during ischemia-reperfusion. Antioxid. Redox Signal. 2012, 17, 1109–1123
27. Lyons, C.R.; Orloff, G.J.; Cunningham, J.M. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J. Biol. Chem.1992, 267, 6370–6374
28. 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, 670–680
29. Korbelik, M.; Hamblin, M.R. The impact of macrophage-cancer cell interaction on the efficacy of photodynamic therapy. Photochem. Photobiol. Sci. 2015, 14, 1403–1409
30. Beg, A.A.; Baltimore, D. An essential role for NF-κB in preventing TNF-α-induced cell death. Science 1996, 274, 782–784
31. Kundu, S.D.; Lee, C.; Billips, B.K.; Habermacher, G.M.; Zhang, Q.; Liu, V.; Wong, L.Y.; Klumpp, D.J.; Thumbikat, P. The toll-like receptor pathway: A novel mechanism of infection-induced carcinogenesis of prostate epithelial cells. Prostate 2008, 68, 223–229
32. Wijayanti, N.; Huber, S.; Samoylenko, A.; Kietzmann, T.; Immenschuh, S. Role of NF-κB and p38 MAP kinase signaling pathways in the lipopolysaccharide-dependent activation of heme oxygenase-1 gene expression. Antioxid. Redox Signal. 2004, 6, 802–810
33. Cohen, P. The TLR and IL-1 signaling network at a glance. J. Cell Sci.2014, 127, 2383–2390
34. Eigenbrod, T.; Park, J.H.; Harder, J.; Iwakura, Y.; Núñez, G. Cutting edge: Critical role for mesothelial cells in necrosis-induced inflammation through the recognition of IL-1α released from dying cells. J. Immunol. 2008, 181, 8194–8198
35. Carr, M.W.; Roth, S.J.; Luther, E.; Rose, S.S.; Springer, T.A. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Sci. USA 1994, 91, 3652–3656
36. Chu, W.M. Tumor necrosis factor. Cancer Lett.2012, 328, 222–225
37. Cecic, I.; Korbelik, M. Mediators of peripheral blood neutrophilia induced by photodynamic therapy of solid tumors. Cancer Lett.2002, 183, 43–51
38. Byun, J.Y.; Choi, H.Y.; Myung, K.B.; Choi, Y.W. Expression of IL-10, TGF-β1 and TNF-α in cultured keratinocytes (HaCaT cells) after IPL treatment or ALA-IPL photodynamic treatment. Ann. Dermatol. 2009, 21, 12–17
39. Shixiang, Y.; Xi, S.; Junliang, L.; Shanyi, Z.; Xingke, X.; Meiguang, Z.; Kai, W.; Fangcheng, L. Antitumor efficacy of a photodynamic therapy-generated dendritic cell glioma vaccine. Med. Oncol. 2011, 28, 453–461
40. Balkwill, F. Tumour necrosis factor and cancer. Nat. Rev. Cancer 2009, 9, 361–371
41. Han, D.; Ybanez, M.D.; Ahmadi, S.; Yeh, K.; Kaplowitz, N. Redox regulation of tumor necrosis factor signaling. Antioxid. Redox Signal. 2009, 11, 2245–2263
42. Kawczyk-Krupka, A.; Bugaj, A.M.; Latos, W.; Wawrzyniec, K.; Oles, P.; Mertas, A.; Czuba, Z.; Krol, W.; Sieron-Stoltny, K.; Sieron, A. ALA-mediated photodynamic effect on apoptosis induction and secretion of macrophage migration inhibitory factor (MIF) and of monocyte chemotactic protein (MCP-1) by colon cancer cells in normoxia and in hypoxia-like conditions in vitro. Photodiagn. Photodyn. Ther. 2015, 12, 27–35
43. Zaidi, M.R.; Merlino, G. The two faces of interferon-γ in cancer. Clin. Cancer Res.2011, 17, 6118–6124
44. Li, F.; Cheng, Y.; Lu, J.; Hu, R.; Wan, Q.; Feng, H. Photodynamic therapy boosts anti-glioma immunity in mice: A dependence on the activities of T cells and complement C3. J. Cell. Biochem 2011, 112, 3035–3043
45. Trinchieri, G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 2003, 3, 133–146
46. Gollnick, S.O.; Liu, X.; Owczarczak, B.; Musser, D.A.; Henderson, B.W. Altered expression of interleukin 6 and interleukin 10 as a result of photodynamic therapy in vivo. Cancer Res. 1997, 57, 3904–3909
47. Lin, W.W.; Karin, M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Investig. 2007, 117, 1175–1183
48. Panzarini, E.; Inguscio, V.; Tenuzzo, B.A.; Dini, L. In vitro and in vivo clearance of rose bengal acetate-photodynamic therapy-induced autophagic and apoptotic cells. Exp. Biol. Med.2013, 238, 765–778
49. Garg, A.D.; Krysko, D.V.; Verfaillie, T.; Kaczmarek, A.; Ferreira, G.B.; Marysael, T.; Rubio, N.; Firczuk, M.; Mathieu, C.; Roebroek, A.J.M., et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J. 2012, 31, 1062–1079
50. Kick, G.; Messer, G.; Goetz, A.; Plewig, G.; Kind, P. Photodynamic therapy induces expression of interleukin 6 by activation of AP-1 but not NF-κB DNA binding. Cancer Res. 1995, 55, 2373–2379
51. 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 2004, 23, 8649–8658
52. 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, 1772–1779
53. De Vree, W.J.A.; 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, 2908–2911
54. De Vree, W.J.A.; Essers, M.C.; Koster, J.F.; Sluiter, W. Role of interleukin 1 and granulocyte colony-stimulating factor in photofrin-based photodynamic therapy of rat rhabdomyosarcoma tumors. Cancer Res. 1997, 57, 2555–2558
55. Du, H.; Bay, B.-H.; Mahendran, R.; Olivo, M. Hypericin-mediated photodynamic therapy elicits differential interleukin-6 response in nasopharyngeal cancer. Cancer Lett. 2006, 235, 202–208
56. Heger, M.; van der Wal, A.C.; Storm, G.; van Gemert, M.J. Potential therapeutic benefits stemming from the thermal nature of irreversible electroporation of solid cancers. Hepatobiliary Pancreat. Dis. Int. 2015, 14, 331–333
57. Wei, L.H.; Baumann, H.; Tracy, E.; Wang, Y.; Hutson, A.; Rose-John, S.; Henderson, B.W. Interleukin-6 trans signalling enhances photodynamic therapy by modulating cell cycling. Br. J. Cancer 2007, 97, 1513–1522
58. Kushibiki, T.; Tajiri, T.; Tomioka, Y.; Awazu, K. Photodynamic therapy induces interleukin secretion from dendritic cells. Int. J. Clin. Exp. Med. 2010, 3, 110–114
59. Kim, R.; Emi, M.; Tanabe, K. Functional roles of immature dendritic cells in impaired immunity of solid tumour and their targeted strategies for provoking tumour immunity. Clin. Exp. Immunol. 2006, 146, 189–196
60. Demaria, S.; Santori, F.R.; Ng, B.; Liebes, L.; Formenti, S.C.; Vukmanovic, S. Select forms of tumor cell apoptosis induce dendritic cell maturation. J. Leukoc. Biol. 2005, 77, 361–368
61. Feng, F.; Wang, Y.-C.; Hu, X.-B.; Liu, X.-W.; Ji, G.; Chen, Y.-R.; Wang, L.; He, F.; Dou, G.-R.; Liang, L., et al. The transcription factor RBP-J-mediated signaling is essential for dendritic cells to evoke efficient anti-tumor immune responses in mice. Mol. Cancer 2010, 9, 90–90
62. Brackett, C.M.; Owczarczak, B.; Ramsey, K.; Maier, P.G.; Gollnick, S.O. IL-6 potentiates tumor resistance to photodynamic therapy (PDT). Lasers Surg. Med. 2011, 43, 676–685
63. Yu, H.; Pardoll, D.; Jove, R. STATs in cancer inflammation and immunity: A leading role for STAT3. Nat. Rev. Cancer 2009, 9, 798–809
64. Hatzi, E.; Murphy, C.; Zoephel, A.; Rasmussen, H.; Morbidelli, L.; Ahorn, H.; Kunisada, K.; Tontsch, U.; Klenk, M.; Yamauchi-Takihara, K., et al. N-myc oncogene overexpression down-regulates IL-6; evidence that IL-6 inhibits angiogenesis and suppresses neuroblastoma tumor growth. Oncogene 2002, 21, 3552–3561
65. Usuda, J.; Okunaka, T.; Furukawa, K.; Tsuchida, T.; Kuroiwa, Y.; Ohe, Y.; Saijo, N.; Nishio, K.; Konaka, C.; Kato, H. Increased cytotoxic effects of photodynamic therapy in IL-6 gene transfected cells via enhanced apoptosis. Int. J. Cancer 2001, 93, 475–480
66. Thurston, G.; McLean, J.W.; Rizen, M.; Baluk, P.; Haskell, A.; Murphy, T.J.; Hanahan, D.; McDonald, D.M. Cationic liposomes target angiogenic endothelial cells in tumors and chronic inflammation in mice. J. Clin. Investig. 1998, 101, 1401–1413
67. Fingar, V.H. Vascular effects of photodynamic therapy. J. Clin. Laser Med. Surg. 1996, 14, 323–328
68. De Vries, E.M.; Kwakkel, J.; Eggels, L.; Kalsbeek, A.; Barrett, P.; Fliers, E.; Boelen, A. NFκB signaling is sssential for the lipopolysaccharide-induced increase of type 2 seiodinase in tanycytes. Endocrinology 2014, 155, 2000–2008.