Interleukin-6 trans signalling enhances photodynamic therapy by modulating cell cycling

British Journal of Cancer

Volumn 97, Issue 11, 2007, Pages 1513-1522

  Wei, L H ^a   Baumann, H ^b   Tracy, E ^b   Wang, Y ^b   Hutson, A ^b   Rose John, S ^c   Henderson, B W ^b  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

Cell cycle; Interleukin 6; Photodynamic therapy; Soluble interleukin 6 receptor

Indexed keywords

2 (1 HEXYLOXYETHYL) 2 DEVINYLPYROPHEOPHORBIDE A; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; GLYCOPROTEIN GP 130; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOTOSENSITIZING AGENT; PROTEIN TYROSINE PHOSPHATASE; RETINOBLASTOMA PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CONTROL; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR CELL;

ANIMALS; BLOTTING, WESTERN; CDC25 PHOSPHATASES; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CHLOROPHYLL; COLONIC NEOPLASMS; CULTURE MEDIA, CONDITIONED; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DOSE-RESPONSE RELATIONSHIP, DRUG; HELA CELLS; HUMANS; INTERLEUKIN-6; MACROPHAGES; MICE; MICE, INBRED BALB C; PHOTOCHEMOTHERAPY; RECEPTORS, INTERLEUKIN-6; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 36448991574     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6604073     Document Type: Article

References (45)

1. Ahmad N, Feyes DK, Agarwal R, Mukhtar H (1998) Photodynamic therapy results in induction of WAF1/CIP1/P21 leading to cell cycle arrest and apoptosis. Proc Natl Acad Sci USA 95: 6977-6982
2. Ahmad N, Gupta S, Mukhtar H (1999) Involvement of retinoblastoma (Rb) and E2F transcription factors during photodynamic therapy of human epidermoid carcinoma cells A431. Oncogene 18: 1891-1896
3. Barre B, Vigneron A, Coqueret O (2005) The STAT3 transcription factor is a target for the Myc and riboblastoma proteins on the Cdc25A promoter. J Biol Chem 280: 15673-15681
4. Bernardi R, Liebermann DA, Hoffman B (2000) Cdc25A stability is controlled by the ubiquitin-proteasome pathway during cell cycle progression and terminal differentiation. Oncogene 19: 2447-2454
5. (H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 8: 345-350
6. Chalaris A, Rabe B, Paliga K, Lange H, Laskay T, Fielding CA, Jones S, Rose-John S, Scheller J (2007) Apoptosis is a natural stimulus of IL6R shedding and contributes to the pro-inflammatory trans-signaling function of neutrophils. Blood 110: 1748-1755
7. Chattopadhyay S, Tracy E, Liang P, Robledo O, Rose-John S, Baumann H (2007) Interleukin-31 and oncostatin-M mediate distinct signaling reactions and response patterns in lung epithelial cells. J Biol Chem 282: 3014-3026
8. de Vree WJ, Essers MC, de Bruijn HS, Star WM, Koster JF, Sluiter W (1996) Evidence for an important role of neutrophils in the efficacy of photodynamic therapy in vivo. Cancer Res 56: 2908-2911
9. Fischer M, Goldschmitt J, Peschel C, Brakenhoff JP, Kallen KJ, Wollmer A, Grotzinger J, Rose-John S (1997) A bioactive designer cytokine for human hematopoietic progenitor cell expansion. Nat Biotechnol 15: 142-145
10. Girotti AW (2001) Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J Photochem Photobiol B 63: 103-113
11. Gollnick SO, Evans SS, Baumann H, Owczarczak B, Maier P, Vaughan L, Wang WC, Unger E, Henderson BW (2003) Role of cytokines in photodynamic therapy-induced local and systemic inflammation. Br J Cancer 88: 1772-1779
12. Gollnick SO, Liu X, Owczarczak B, Musser DA, Henderson BW (1997) Altered expression of interleukin 6 and interleukin 10 as a result of photodynamic therapy in vivo. Cancer Res 57: 3904-3909
13. Gollnick SO, Owczarczak B, Maier P (2006) Photodynamic therapy and anti-tumor immunity. Lasers Surg Med 38: 509-515
14. Gollnick SO, Vaughan L, Henderson BW (2002) Generation of effective antitumor vaccines using photodynamic therapy. Cancer Res 62: 1604-1608
15. Grant SL, Douglas AM, Goss GA, Begley CG (2001) Oncostatin M and leukemia inhibitory factor regulate the growth of normal human breast epithelial cells. Growth Factors 19: 153-162
16. Haywood-Small SL, Vernon DI, Griffiths J, Schofield J, Brown SB (2006) Phthalocyanine-mediated photodynamic therapy induces cell death and a G0/G1 cell cycle arrest in cervical cancer cells. Biochem Biophys Res Commun 339: 569-576
17. Henderson BW, Daroqui C, Tracy E, Vaughan L, Loewen GM, Cooper M, Baumann H (2007) Cross-linking of signal transducer and activator of transcription 3 (STAT3) - a molecular marker for the photodynamic reaction in cells and tumors. Clin Cancer Res 13: 3156-3163
18. Henderson BW, Gollnick SO (2003) Mechanistic principles of photodynamic therapy In Horspool W, Lenci F (eds) CRC Handbook of Organic Photochemistry and Photobiology, 2 edn. pp 145-1-145-25. Boca Raton, FL, USA: CRC Press
19. Henderson BW, Gollnick SO, Snyder JW, Busch TM, Kousis PC, Cheney RT, Morgan J (2004) Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors. Cancer Res 64: 2120-2126
20. Hibi M, Nakajima K, Hirano T (1996) IL-6 cytokine family and signal transduction: a model of the cytokine system. J Mol Med 74: 1-12
21. Hirano T, Ishihara K, Hibi M (2000) Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 19: 2548-2556
22. Jee SH, Shen SC, Chiu HC, Tsai WL, Kuo ML (2001) Overexpression of interleukin-6 in human basal cell carcinoma cell lines increases anti-apoptotic activity and tumorigenic potency. Oncogene 20: 198-208
23. Jones SA (2005) Directing transition from innate to acquired immunity: defining a role for IL-6. J Immunol 175: 3463-3468
24. Kick G, Messer G, Goetz A, Plewig G, Kind P (1995) Photodynamic therapy induces expression of interleukin 6 by activation of AP-1 but not NF-kappa B DNA binding. Cancer Res 55: 2373-2379
25. Kick G, Messer G, Plewig G, Kind P, Goetz AE (1996) Strong and prolonged induction of c-jun and c-fos proto-oncogenes by photodynamic therapy. Br J Cancer 74: 30-36
26. Kishimoto T, Akira S, Narazaki M, Taga T (1995) Interleukin-6 family of cytokines and gp130. Blood 86: 1243-1254
27. Klausen P, Pedersen L, Jurlander J, Baumann H (2000) Oncostatin M and interleukin 6 inhibit cell cycle progression by prevention of p27kip1 degradation in HepG2 cells. Oncogene 19: 3675-3683
28. Korbelik M (1996) Induction of tumor immunity by photodynamic therapy. J Clin Laser Med Surg 14: 329-334
29. Korbelik M, Krosl G, Krosl J, Dougherty GJ (1996a) Modulation of tumor response to photodynamic therapy in severe combined immunodeficient (SCID) mice by adoptively transferred lymphoid cells. SPIE 2675: 156-162
30. Korbelik M, Krosl G, Krosl J, Dougherty GJ (1996b) The role of host lymphoid populations in the response of mouse EMT6 tumor to photodynamic therapy. Cancer Res 56: 5647- 5652
31. Liu W, Oseroff AR, Baumann H (2004) Photodynamic therapy causes cross-linking of signal transducer and activator of transcription proteins and attenuation of interleukin-6 cytokine responsiveness in epithelial cells. Cancer Res 64: 6579-6587
32. Loewen GM, Tracy E, Blanchard F, Tan D, Yu J, Raza S, Matsui S, Baumann H (2005) Transformation of human bronchial epithelial cells alters responsiveness to inflammatory cytokines. BMC Cancer 5: 145
33. Luna MC, Wong S, Gomer CJ (1994) Photodynamic therapy mediated induction of early response genes. Cancer Res 54: 1374-1380
34. Minami M, Inoue M, Wei S, Takeda K, Matsumoto M, Kishimoto T, Akira S (1996) STAT3 activation is a critical step in gp130-mediated terminal differentiation and growth arrest of a myeloid cell line. Proc Natl Acad Sci USA 93: 3963-3966
35. Novick D, Shulman LM, Chen L, Revel M (1992) Enhancement of interleukin 6 cytostatic effect on human breast carcinoma cells by soluble IL-6 receptor from urine and reversion by monoclonal antibody. Cytokine 4: 6-11
36. Rakemann T, Niehof M, Kubicka S, Fischer M, Manns MP, Rose-John S, Trautwein C (1999) The designer cytokine hyper-interleukin-6 is a potent activator of STAT3-dependent gene transcription in vivo and in vitro. J Biol Chem 274: 1257-1266
37. Rose-John S, Heinrich PC (1994) Soluble receptors for cytokines and growth factors: generation and biological function. Biochem J 300: 281-290
38. Scheller J, Ohnesorge N, Rose-John S (2006) Interleukin-6 trans-signalling in chronic inflammation and cancer. Scand J Immunol 63: 321-329
39. Schwarze MM, Hawley RG (1995) Prevention of myeloma cell apoptosis by ectopic bcl-2 expression or interleukin 6-mediated up-regulation of bcl-xL. Cancer Res 55: 2262-2265
40. Taga T, Hibi M, Hirata Y, Yamasaki K, Yasukawa K, Matsuda T, Hirano T, Kishimoto T (1989) Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 58: 573-581
41. Usuda J, Okunaka T, Furukawa K, Tsuchida T, Kuroiwa Y, Ohe Y, Saijo N, Nishio K, Konaka C, Kato H (2001) Increased cytotoxic effects of photodynamic therapy in IL-6 gene transfected cells via enhanced apoptosis. Int J Cancer 93: 475 -480
42. Wei LH, Kuo ML, Chen CA, Chou CH, Lai KB, Lee CN, Hsieh CY (2003) Interleukin-6 promotes cervical tumor growth by VEGF-dependent angiogenesis via a STAT3 pathway. Oncogene 22: 1517-1527
43. Wong TW, Tracy E, Oseroff AR, Baumann H (2003) Photodynamic therapy mediates immediate loss of cellular responsiveness to cytokines and growth factors. Cancer Res 63: 3812-3818
44. Yom SS, Busch TM, Friedberg JS, Wileyto EP, Smith D, Glatstein E, Hahn SM (2003) Elevated serum cytokine levels in mesothelioma patients who have undergone pleurectomy or extrapleural pneumonectomy and adjuvant intraoperative photodynamic therapy. Photochem Photobiol 78: 75-81
45. Zhuang S, Ouedraogo GD, Kochevar IE (2003) Downregulation of epidermal growth factor receptor signaling by singlet oxygen through activation of caspase-3 and protein phosphatases. Oncogene 22: 4413-4424