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BioMed Research International
Volume 2014, Article ID 921296, 10 pages
http://dx.doi.org/10.1155/2014/921296
Research Article

Enhanced Efficacy of Bleomycin in Bladder Cancer Cells by Photochemical Internalization

1Department of Cancer Research and Molecular Medicine, Faculty of Medicine, Norwegian University of Science and Technology, P.O. Box 8905, 7491 Trondheim, Norway
2PCI Biotech AS, Strandveien 55, 1366 Lysaker, Norway
3APIM Therapeutics AS, Sem Sælandsvei 14, 7084 Trondheim, Norway

Received 8 March 2014; Revised 29 May 2014; Accepted 29 May 2014; Published 30 June 2014

Academic Editor: Swaran J. S. Flora

Copyright © 2014 Yan Baglo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. C. Hall, S. S. Chang, G. Dalbagni et al., “Guideline for the management of nonmuscle invasive bladder cancer (stages Ta, T1, and Tis): 2007 update,” The Journal of Urology, vol. 178, no. 6, pp. 2314–2330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. T. R. L. Griffiths, “Current perspectives in bladder cancer management,” International Journal of Clinical Practice, vol. 67, no. 5, pp. 435–448, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. I. K. Larsen, B. Sæther, and B. Aagnes, “Cancer in Norway,” 2010, http://www.kreftregisteret.no/no/Generelt/Publikasjoner/Cancer-in-Norway/Cancer-in-Norway-2010/.
  4. National Cancer Institute, Bladder Cancer, 2014, http://www.cancer.gov/cancertopics/types/bladder.
  5. D. Ramotar and H. Wang, “Protective mechanisms against the antitumor agent bleomycin: lessons from Saccharomyces cerevisiae,” Current Genetics, vol. 43, no. 4, pp. 213–224, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. R. B. Bracken, D. E. Johnson, L. Rodriquez, M. L. Samuels, and A. Ayala, “Treatment of multiple superficial tumors of bladder with intravesical bleomycin,” Urology, vol. 9, no. 2, pp. 161–163, 1977. View at Publisher · View at Google Scholar · View at Scopus
  7. A. G. Turner, K. R. Durrant, and J. S. Malpas, “A trial of bleomycin versus adriamycin in advanced carcinoma of the bladder,” British Journal of Urology, vol. 51, no. 2, pp. 121–124, 1979. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Gad-el-Mawla, R. Hamsa, E. Chevlen, and J. L. Ziegler, “Phase II trial of bleomycin in bilharzial bladder cancer,” Cancer Treatment Reports, vol. 62, no. 7, pp. 1109–1110, 1978. View at Google Scholar · View at Scopus
  9. G. Pron, N. Mahrour, S. Orlowski et al., “Internalisation of the bleomycin molecules responsible for bleomycin toxicity: a receptor-mediated endocytosis mechanism,” Biochemical Pharmacology, vol. 57, no. 1, pp. 45–56, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Aouida, R. Poulin, and D. Ramotar, “The human carnitine transporter SLC22A16 mediates high affinity uptake of the anticancer polyamine analogue bleomycin-A5,” Journal of Biological Chemistry, vol. 285, no. 9, pp. 6275–6284, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. S. M. Sebti, J. P. Jani, S. Mistry, E. Gorelik, and J. S. Lazo, “Metabolic inactivation: a mechanism of human tumor resistance to bleomycin,” Cancer Research, vol. 51, no. 1, pp. 227–232, 1991. View at Google Scholar · View at Scopus
  12. D. R. Schwartz, G. E. Homanics, D. G. Hoyt, E. Klein, J. Abernethy, and J. S. Lazo, “The neutral cysteine protease bleomycin hydrolase is essential for epidermal integrity and bleomycin resistance,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 8, pp. 4680–4685, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. L. H. Einhorn, “Curing metastatic testicular cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 7, pp. 4592–4595, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Kubota, T. Nakada, H. Yanai, K. Itoh, I. Sasagawa, and K. Kawai, “Histological evaluation of the effects of electropermeabilization after administration of bleomycin on bladder cancer in the rat,” European Urology, vol. 34, no. 4, pp. 372–376, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Kubota, T. Nakada, H. Yanai, H. Kakizaki, I. Sasagawa, and M. Watanabe, “Electropermeabilization in bladder cancer chemotherapy,” Cancer Chemotherapy and Pharmacology, vol. 39, no. 1-2, pp. 67–70, 1996. View at Publisher · View at Google Scholar · View at Scopus
  16. T. J. Dougherty, “Photodynamic therapy,” Photochemistry and Photobiology, vol. 58, no. 6, pp. 895–900, 1993. View at Google Scholar · View at Scopus
  17. K. Berg, M. Folini, L. Prasmickaite et al., “Photochemical internalization: a new tool for drug delivery,” Current Pharmaceutical Biotechnology, vol. 8, no. 6, pp. 362–372, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Berg, P. K. Selbo, L. Prasmickaite et al., “Photochemical internalization: a novel technology for delivery of macromolecules into cytosol,” Cancer Research, vol. 59, no. 6, pp. 1180–1183, 1999. View at Google Scholar · View at Scopus
  19. K. Berg, S. Nordstrand, P. K. Selbo, D. T. T. Tran, E. Angell-Petersen, and A. Hogset, “Disulfonated tetraphenyl chlorin (TPCS 2a), a novel photosensitizer developed for clinical utilization of photochemical internalization,” Photochemical & Photobiological Sciences, vol. 10, no. 10, pp. 1637–1651, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. P. K. Selbo, G. Sivam, O. Fodstad, K. Sandvig, and K. Berg, “In vivo documentation of photochemical internalization, a novel approach to site specific cancer therapy,” International Journal of Cancer, vol. 92, pp. 761–766, 2001. View at Google Scholar
  21. M. Lilletvedt, H. H. Tønnesen, A. Høgset, L. Nardo, and S. Kristensen, “Physicochemical characterization of the photosensitizers TPCS2a and TPPS2a 1. Spectroscopic evaluation of drug—solvent interactions,” Die Pharmazie, vol. 65, no. 8, pp. 588–595, 2010. View at Google Scholar · View at Scopus
  22. K. Berg, A. Dietze, O. Kaalhus, and A. Høgset, “Site-specific drug delivery by photochemical internalization enhances the antitumor effect of bleomycin,” Clinical Cancer Research, vol. 11, no. 23, pp. 8476–8485, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Berg, P. K. Selbo, L. Prasmickaite, and A. Høgset, “Photochemical drug and gene delivery,” Current Opinion in Molecular Therapeutics, vol. 6, no. 3, pp. 279–287, 2004. View at Google Scholar · View at Scopus
  24. O. Norum, K. Giercksky, and K. Berg, “Photochemical internalization as an adjunct to marginal surgery in a human sarcoma model,” Photochemical and Photobiological Sciences, vol. 8, no. 6, pp. 758–762, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. O. J. Norum, J. V. Gaustad, E. Angell-Petersen et al., “Photochemical internalization of bleomycin is superior to photodynamic therapy due to the therapeutic effect in the tumor periphery,” Photochemistry and Photobiology, vol. 85, no. 3, pp. 740–749, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Berg, A. Weyergang, L. Prasmickaite et al., “Photochemical internalization (PCI): a technology for drug delivery,” Methods in Molecular Biology, vol. 635, pp. 133–145, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. “Study of Amphinex Based Photochemical Internalisation (PCI) of Bleomycin in Patients with Cutaneous Cancer,” http://clinicaltrials.gov/show/NCT00993512.
  28. H. C. Arentsen, J. Falke, A. Høgset, E. Oosterwijk, and J. A. Witjes, “The effect of photochemical internalization of bleomycin in the treatment of urothelial carcinoma of the bladder: an in vitro study,” Urologic Oncology, vol. 32, no. 1, pp. 49.e1–49.e6, 2014. View at Publisher · View at Google Scholar
  29. ClinicalTrials.gov, “A Study to Evaluate the Safety and Efficacy of PC-A11 in Patients with Recurrent Head and Neck Squamous Cell Carcinoma,” August 2013, http://clinicaltrials.gov/ct2/show/study/NCT01606566.
  30. J. Chen and J. Stubbe, “Bleomycins: towards better therapeutics,” Nature Reviews Cancer, vol. 5, no. 2, pp. 102–112, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. O. Tounekti, G. Pron, J. Belehradek Jr., and L. M. Mir, “Bleomycin, an apoptosis-mimetic drug that induces two types of cell death depending on the number of molecules internalized,” Cancer Research, vol. 53, no. 22, pp. 5462–5469, 1993. View at Google Scholar · View at Scopus
  32. O. Tounekti, A. Kenani, N. Foray, S. Orlowski, and L. M. Mir, “The ratio of single-to double-strand DNA breaks and their absolute values determine cell death pathway,” British Journal of Cancer, vol. 84, no. 9, pp. 1272–1279, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Müller, K. Misund, T. Holien et al., “Targeting proliferating cell nuclear antigen and its protein interactions induces apoptosis in multiple myeloma cells,” PLoS ONE, vol. 8, no. 7, Article ID e70430, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. K. M. Gilljam, E. Feyzi, P. A. Aas et al., “Identification of a novel, widespread, and functionally important PCNA-binding motif,” Journal of Cell Biology, vol. 186, no. 5, pp. 645–654, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. K. M. Gilljam, R. Müller, N. B. Liabakk, and M. Otterlei, “Nucleotide excision repair is associated with the replisome and its efficiency depends on a direct interaction between XPA and PCNA,” PLoS ONE, vol. 7, no. 11, Article ID e49199, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Ciccia, A. V. Nimonkar, Y. Hu et al., “Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress,” Molecular Cell, vol. 47, no. 3, pp. 396–409, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Bacquin, C. Pouvelle, N. Siaud et al., “The helicase FBH1 is tightly regulated by PCNA via CRL4(Cdt2)-mediated proteolysis in human cells,” Nucleic Acids Research, vol. 41, no. 13, pp. 6501–6513, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Prasmickaite, A. Høgset, P. K. Selbo, B. Ø. Engesæter, M. Helium, and K. Berg, “Photochemical disruption of endocytic vesicles before delivery of drugs: a new strategy for cancer therapy,” British Journal of Cancer, vol. 86, no. 4, pp. 652–657, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. M. B. Berstad, A. Weyergang, and K. Berg, “Photochemical internalization (PCI) of HER2-targeted toxins: synergy is dependent on the treatment sequence,” Biochimica et Biophysica Acta, vol. 1820, no. 12, pp. 1849–1858, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Weyergang, P. K. Selbo, and K. Berg, “Photochemically stimulated drug delivery increases the cytotoxicity and specificity of EGF-saporin,” Journal of Controlled Release, vol. 111, no. 1-2, pp. 165–173, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Baglo, M. M. L. Sousa, G. Slupphaug et al., “Photodynamic therapy with hexyl aminolevulinate induces carbonylation, posttranslational modifications and changed expression of proteins in cell survival and cell death pathways,” Photochemical and Photobiological Sciences, vol. 10, no. 7, pp. 1137–1145, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. S. K. Sreedharan, C. Verma, L. S. D. Caves et al., “Demonstration that 1-trans-epoxysuccinyl-L-leucylamido-(4-guanidino)butane (E-64) is one of the most effective low Mr inhibitors of trypsin-catalysed hydrolysis. Characterization by kinetic analysis and by energy minimization and molecular dynamics simulation of the E-64-β-trypsin complex,” The Biochemical Journal, vol. 316, part 3, pp. 777–786, 1996. View at Google Scholar · View at Scopus
  43. G. Morris, J. S. Mistry, J. P. Jani, S. M. Sebti, and J. S. Lazo, “Cysteine proteinase inhibitors and bleomycin-sensitive and -resistant cells,” Biochemical Pharmacology, vol. 41, no. 11, pp. 1559–1566, 1991. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Edward, “Red/far-red fluorescing dna-specific anthraquinones for nucl: cyto segmentation and viability reporting in cell-based assays,” Methods in Enzymology, vol. 505, pp. 23–45, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. J. T. Wang, K. Berg, A. Høgset, S. G. Bown, and A. J. MacRobert, “Photophysical and photobiological properties of a sulfonated chlorin photosensitiser TPCS2a for photochemical internalisation (PCI),” Photochemical & Photobiological Sciences, vol. 12, no. 3, pp. 519–526, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. N. P. Singh, M. T. McCoy, R. R. Tice, and E. L. Schneider, “A simple technique for quantitation of low levels of DNA damage in individual cells,” Experimental Cell Research, vol. 175, no. 1, pp. 184–191, 1988. View at Publisher · View at Google Scholar · View at Scopus
  47. P. L. Olive and J. P. Banáth, “The comet assay: a method to measure DNA damage in individual cells,” Nature Protocols, vol. 1, no. 1, pp. 23–29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Hanssen-Bauer, K. Solvang-Garten, K. M. Gilljam et al., “The region of XRCC1 which harbours the three most common nonsynonymous polymorphic variants, is essential for the scaffolding function of XRCC1,” DNA Repair, vol. 11, no. 4, pp. 357–366, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Mukherjee, R. N. Ghosh, and F. R. Maxfield, “Endocytosis,” Physiological Reviews, vol. 77, no. 3, pp. 759–803, 1997. View at Google Scholar · View at Scopus