Skip to main content

Advertisement

Log in

Photochemical internalization of bleomycin and temozolomide — in vitro studies on the glioma cell line F98

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Here we evaluate the photosensitizer meso-tetraphenyl chlorin disulphonate (TPCS2a) in survival studies of rat glioma cancer cells in combination with the novel photochemical internalization (PCI) technique. The tested anticancer drugs were bleomycin (BLM) and temozolomide (TMZ). Glioma cells were incubated with TPCS2a (0.2 μg ml−1, 18 h, 37 °C) before BLM or TMZ stimulation (4 h) prior to red light illumination (652 nm, 50 mW cm−2). The cell survival after BLM (0.5 μm)-PCI (40 s light) quantified using the MTT assay was reduced to about 25% after 24 h relative to controls, and to 31% after TMZ-PCI. The supplementing quantification by clonogenic assays, using BLM (0.1 μm), indicated a long-term cytotoxic effect: the surviving fraction of clonogenic cells was reduced to 5% after light exposure (80 s) with PCI, compared to 70% in the case of PDT. In parallel, structural and morphological changes within the cells upon light treatment were examined using fluorescence microscopy techniques. The present study demonstrates that PCI of BLM is an effective method for killing F98 glioma cells, but smaller effects were observed using TMZ following the “light after” strategy. The results are the basis for further in vivo studies on our rat glioma cancer model using PDT and PCI.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Notes and references

  1. K. Hynynen, N. McDannold, N. A. Sheikov, F. A. Jolesz, N. Vykhodtseva, Neuroimage, 2005, 24, 12–20.

    Article  PubMed  Google Scholar 

  2. M. Jamal, B. H. Rath, P. S. Tsang, K. Camphausen, P. J. Tofilon, Neoplasia, 2012, 14, 150–158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. L. Paszat, N. Laperriere, P. Groome, K. Schulze, W. Mackillop, E. Holowaty, Int. J. Radiat. Oncol., Biol., Phys., 2001, 51, 100–107.

    Article  CAS  Google Scholar 

  4. R. Helseth, E. Helseth, T. B. Johannesen, C. W. Langberg, K. Lote, P. Rønning, D. Scheie, A. Vik, T. R. Meling, Acta Neurol. Scand., 2010, 122, 159–167.

    Article  CAS  PubMed  Google Scholar 

  5. K. Berg, A. Dietze, O. Kaalhus, A. Høgset, Clin. Cancer Res., 2005, 11, 8476–8485.

    Article  CAS  PubMed  Google Scholar 

  6. O.-J. Norum, P. K. Selbo, A. Weyergang, K.-E. Giercksky, K. Berg, J. Photochem. Photobiol., B, 2009, 96, 83–92.

    Article  CAS  Google Scholar 

  7. O.-J. Norum, J.-V. Gaustad, E. Angell-Petersen, E. K. Rofstad, Q. Peng, K.-E. Giercksky, K. Berg, Photochem. Photobiol., 2009, 85, 740–749.

    Article  CAS  PubMed  Google Scholar 

  8. Y. Baglo, Q. Peng, L. Hagen, K. Berg, A. Høgset, F. Drabløs, O. A. Gederaas, Photodiagn. Photodyn. Ther., 2015, 12, 58–66.

    Article  CAS  Google Scholar 

  9. P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, J. Golab, CA-Cancer J. Clin., 2011, 61, 250–281.

    Article  PubMed  PubMed Central  Google Scholar 

  10. K. Berg, M. Folini, L. Prasmickaite, P. Selbo, A. Bonsted, B. Engesaeter, N. Zaffaroni, A. Weyergang, A. Dietzea, G. Maelandsmo, E. Wagner, O.-J. Norum, A. Hogset, Curr. Pharm. Biotechnol., 2007, 8, 362–372.

    Article  CAS  PubMed  Google Scholar 

  11. H. Mojzisova, S. Bonneau, P. Maillard, K. Berg, D. Brault, Photochem. Photobiol. Sci., 2009, 8, 778–787.

    Article  CAS  PubMed  Google Scholar 

  12. K. Berg, D. Tran, P. K. Selbo and C. Rimington, Compound PCT WO, 03/020309, 2001.

    Google Scholar 

  13. PCI Biotech AS, Safety study of Amphinex based photochemical internalisation (PCI) of bleomycin in patients with cutaneous cancer, http://clinicaltrials.gov/show/NCT00993512, NLM identifier NCT00993512, 2009.

  14. Y.-E. K. Lee, R. Kopelman, Methods Mol. Biol., 2011, 726, 151–178.

    Article  CAS  PubMed  Google Scholar 

  15. C. Cepraga, T. Gallavardin, S. Marotte, P.-H. Lanoe, J.-C. Mulatier, F. Lerouge, S. Parola, M. Lindgren, P. L. Baldeck, J. Marvel, O. Maury, C. Monnereau, A. Favier, C. Andraud, Y. Leverrier, M.-T. Charreyre, Polym. Chem., 2013, 4, 61–67.

    Article  CAS  Google Scholar 

  16. S.-H. Cheng, L.-W. Lo, Curr. Drug Discovery Technol., 2011, 8, 250–268.

    Article  Google Scholar 

  17. C. Wang, L. Cheng, Z. Liu, Theranostics, 2013, 3, 317–330.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. K. Ogawa, Y. Kobuke, BioMed Res. Int., 2013, 2013, 125658.

    Article  PubMed  CAS  Google Scholar 

  19. D. Gao, R. R. Agayan, H. Xu, M. A. Philbert, R. Kopelman, Nano Lett., 2006, 6, 2383–2386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. T. Gallavardin, M. Maurin, S. Marotte, T. Simon, A.-M. Gabudean, Y. Bretonniere, M. Lindgren, F. Lerouge, P. L. Baldeck, O. Stephan, Y. Leverrier, J. Marvel, S. Parola, O. Maury, C. Andraud, Photochem. Photobiol. Sci., 2011, 10, 1216–1225.

    Article  CAS  PubMed  Google Scholar 

  21. T. Gallavardin, C. Armagnat, O. Maury, P. L. Baldeck, M. Lindgren, C. Monnereau, C. Andraud, Chem. Commun., 2012, 48, 1689–1691.

    Article  CAS  Google Scholar 

  22. M. S. Mathews, J. W. Blickenstaff, E. Shih, G. Zamora, V. Vo, C. Sun, H. Hirschberg, S. J. Madsen, J. Biomed. Opt., 2012, 17, 1–8.

    Article  CAS  Google Scholar 

  23. J. L. Villano, T. E. Seery, L. R. Bressler, Cancer Chemother. Pharmacol., 2009, 64, 647–655.

    Article  CAS  PubMed  Google Scholar 

  24. A. Weyergang, O. Kaalhus, K. Berg, Mol. Cancer Ther., 2008, 7, 1740–1750.

    Article  CAS  PubMed  Google Scholar 

  25. M. Lilletvedt, H. H. Tønnesen, A. Høgset, L. Nardo, S. Kristensen, Pharmazie, 2010, 65, 588–595.

    CAS  PubMed  Google Scholar 

  26. M. Lilletvedt, S. Kristensen, H. H. Tønnesen, A. Høgset, L. Nardo, J. Photochem. Photobiol., A, 2010, 214, 40–47.

    Article  CAS  Google Scholar 

  27. E. Glimsdal, M. Carlsson, B. Eliasson, B. Minaev, M. Lindgren, J. Phys. Chem. A, 2007, 111, 244–250.

    Article  CAS  PubMed  Google Scholar 

  28. B. Minaev, M. Lindgren, Sensors, 2009, 9, 1937–1966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. R. Vestberg, A. Nyström, M. Lindgren, E. Malmström, A. Hult, Chem. Mater., 2004, 16, 2794–2804.

    Article  CAS  Google Scholar 

  30. B. Minaev and M. Lindgren, Vibration and Fluorescence Spectra of Porphyrin-Cored 2,2-Bis(methylol)-propionic Acid Dendrimers, 2009, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3345821&tool=pmcentrez&rendertype=abstract.

    Google Scholar 

  31. A. (LGC Standards), Product information: F98 (CRL-2397), https://www.lgcstandards-atcc.org/Products/Cells_and_Microorganisms/By_Tissue/Brain/CRL-2397.

  32. M. R. Hamblin, E. L. Newman, J. Photochem. Photobiol., B, 1994, 23, 3–8.

    Article  CAS  Google Scholar 

  33. Y. Baglo, L. Hagen, A. Høgset, F. Drabløs, M. Otterlei, O. A. Gederaas, BioMed. Res. Int., 2014, 2014, 921296.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. V. L. Bull, M. J. Tisdale, Biochem. Pharmacol., 1987, 36, 3215–3220.

    Article  CAS  PubMed  Google Scholar 

  35. L. D. Rhines, P. Sampath, M. E. Dolan, B. M. Tyler, H. Brem, J. Weingart, Cancer Res., 2000, 60, 6307–6310.

    CAS  PubMed  Google Scholar 

  36. M. E. Hegi, A.-C. Diserens, T. Gorlia, M.-F. Hamou, N. de Tribolet, M. Weller, J. M. Kros, J. A. Hainfellner, W. Mason, L. Mariani, J. E. C. Bromberg, P. Hau, R. O. Mirimanoff, J. G. Cairncross, R. C. Janzer, R. Stupp, N. Engl. J. Med., 2005, 352, 997–1003.

    Article  CAS  PubMed  Google Scholar 

  37. R. Stupp, W. P. Mason, M. J. van den Bent, M. Weller, B. Fisher, M. J. B. Taphoorn, K. Belanger, A. A. Brandes, C. Marosi, U. Bogdahn, J. Curschmann, R. C. Janzer, S. K. Ludwin, T. Gorlia, A. Allgeier, D. Lacombe, J. G. Cairncross, E. Eisenhauer, R. O. Mirimanoff, N. Engl. J. Med., 2005, 352, 987–996.

    Article  CAS  PubMed  Google Scholar 

  38. P. A. Rønning, E. Helseth, T. R. Meling, T. B. Johannesen, Neuro-Oncol., 2012, 14, 1178–1184.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. M. S. Mathews, Enhancing the efficacy of phototherapy for malignant gliomas, Doctoral thesis, UiO, 2013.

    Google Scholar 

  40. B. Poddevin, S. Orlowski, J. Belehradek Jr., L. M. Mir, Biochem. Pharmacol., 1991, 42, S67–S75.

    Article  CAS  PubMed  Google Scholar 

  41. K. Berg, S. Nordstrand, P. K. Selbo, D. T. T. Tran, E. Angell-Petersen, A. Høgset, Photochem. Photobiol. Sci., 2011, 10, 1637–1651.

    Article  CAS  PubMed  Google Scholar 

  42. M. E. B. Berstad, M.Sc. thesis, UiB, Radiumhospitalet, Oslo, 2009.

    Google Scholar 

  43. I. K. Ekroll, M.Sc. thesis, NTNU, 2009.

  44. P. K. Selbo, M. G. Rosenblum, L. H. Cheung, W. Zhang, K. Berg, PLoS One, 2009, 4, e6691.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. J. Carmichael, W. G. DeGraff, A. F. Gazdar, J. D. Minna, J. B. Mitchell, Cancer Res., 1987, 47, 936–942.

    CAS  PubMed  Google Scholar 

  46. O. A. Gederaas, S. A. Schønberg, S. l. Ramstad, K. Berg, A. Johnsson, H. E. Krokan, Photochem. Photobiol. Sci., 2005, 4, 383–389.

    Article  CAS  PubMed  Google Scholar 

  47. E. Ulukaya, M. Colakogullari, E. J. Wood, Chemotherapy, 2004, 50, 43–50.

    Article  CAS  PubMed  Google Scholar 

  48. R. M. Hoffman, J. Clin. Lab. Anal., 1991, 5, 133–143.

    Article  CAS  PubMed  Google Scholar 

  49. M. Stevens, J. Hickman, S. Langdon, Cancer Res., 1987, 47, 5846–5852.

    CAS  PubMed  Google Scholar 

  50. J. Berlanda, T. Kiesslich, C. B. Oberdanner, F. J. Obermair, B. Krammer, K. Plaetzer, J. Environ. Pathol., Toxicol. Oncol., 2006, 25, 173–188.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Odrun A. Gederaas.

Additional information

Electronic supplementary information (ESI) available. See DOI: 10.1039/c5pp00144g

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gederaas, O.A., Hauge, A., Ellingsen, P.G. et al. Photochemical internalization of bleomycin and temozolomide — in vitro studies on the glioma cell line F98. Photochem Photobiol Sci 14, 1357–1366 (2015). https://doi.org/10.1039/c5pp00144g

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c5pp00144g

Navigation