In vitro optimization of EtNBS-PDT against hypoxic tumor environments with a tiered, high-content, 3D model optical screening platform

Molecular Pharmaceutics

Volumn 9, Issue 11, 2012, Pages 3171-3182

  Klein, Oliver J ^a   Bhayana, Brijesh ^a   Park, Yong Jin ^b   Evans, Conor L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

3D cancer culture models; acidosis; high content screening; hypoxia; microscopy; photodynamic therapy

Indexed keywords

5 ETHYLAMINO 9 DIETHYL AMINOBENZO[A]PHENOTHIAZINIUM CHLORIDE; ANTINEOPLASTIC AGENT; PHOTOSENSITIZING AGENT; UNCLASSIFIED DRUG; VERTEPORFIN;

ARTICLE; CELL KILLING; CELL VIABILITY; CHEMICAL STRUCTURE; CLINICAL EFFECTIVENESS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DRUG UPTAKE; ENDOPLASMIC RETICULUM; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; OVARY CANCER; PHOTOCHEMISTRY; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; TREATMENT OUTCOME; TUMOR LOCALIZATION; TUMOR MICROENVIRONMENT;

ANOXIA; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; OVARIAN NEOPLASMS; PHOTOCHEMOTHERAPY; THIAZINES; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84868521712     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp300262x     Document Type: Article

References (50)

1. Hanahan, D.; Weinberg, R. A. The hallmarks of cancer Cell 2000, 100 (1) 57-70
2. Berek, J. S.; Bast, R. C. J. Ovarian Cancer. In Cancer Medicine; Kufe, D. W.; Pollack, R. E.; Weichselbaum, R. R.; Bast, R. C. J.; Gansler, T. S.; Holland, J. F.; Frei, E. I., Eds.; BC Decker Inc.: Hamilton, 2003; pp 1831-1861.
3. Cannistra, S. A. Cancer of the Ovary N. Engl. J. Med. 2004, 351 (24) 2519-2529
4. Höckel, M.; Vaupel, P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects J. Natl. Cancer Inst. 2001, 93 (4) 266-76
5. Shannon, A. M.; Bouchier-Hayes, D. J.; Condron, C. M.; Toomey, D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies Cancer Treat. Rev. 2003, 29 (4) 297-307
6. Xu, R.-H.; Pelicano, H.; Zhou, Y.; Carew, J. S.; Feng, L.; Bhalla, K. N.; Keating, M. J.; Huang, P. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia Cancer Res. 2005, 65 (2) 613-21
7. Song, X.; Liu, X.; Chi, W.; Liu, Y.; Wei, L.; Wang, X.; Yu, J. Hypoxia-induced resistance to cisplatin and doxorubicin in non-small cell lung cancer is inhibited by silencing of HIF-1alpha gene Cancer Chemother Pharmacol 2006, 58 (6) 776-784
8. Wang, Y.; Saad, M.; Pakunlu, R. I.; Khandare, J. J.; Garbuzenko, O. B.; Vetcher, A. A.; Soldatenkov, V. A.; Pozharov, V. P.; Minko, T. Nonviral nanoscale-based delivery of antisense oligonucleotides targeted to hypoxia-inducible factor 1 alpha enhances the efficacy of chemotherapy in drug-resistant tumor Clin. Cancer Res. 2008, 14, 3607-3616
9. Koch, S.; Mayer, F.; Honecker, F.; Schittenhelm, M.; Bokemeyer, C. Efficacy of cytotoxic agents used in the treatment of testicular germ cell tumours under normoxic and hypoxic conditions in vitro Br. J. Cancer 2003, 89 (11) 2133-2139
10. Gillies, R. J.; Schornack, P. A.; Secomb, T. W.; Raghunand, N. Causes and effects of heterogeneous perfusion in tumors Neoplasia 1999, 1 (3) 197-207
11. Mahoney, B. P.; Raghunand, N.; Baggett, B.; Gillies, R. J. Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro Biochem. Pharmacol. 2003, 66 (7) 1207-1218
12. Raghunand, N.; Mahoney, B. P.; Gillies, R. J. Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents Biochem. Pharmacol. 2003, 66 (7) 1219-1229
13. Reichert, M.; Steinbach, J. P.; Supra, P.; Weller, M. Modulation of growth and radiochemosensitivity of human malignant glioma cells by acidosis Cancer 2002, 95, 1113-1119
14. Thews, O.; Gassner, B.; Kelleher, D. K.; Schwerdt, G.; Gekle, M. Impact of extracellular acidity on the activity of P-glycoprotein and the cytotoxicity of chemotherapeutic drugs Neoplasia 2006, 8 (2) 143-152
15. Major, a. L.; Rose, G. S.; Chapman, C. F.; Hiserodt, J. C.; Tromberg, B. J.; Krasieva, T. B.; Tadir, Y.; Haller, U.; DiSaia, P. J.; Berns, M. W. In vivo fluorescence detection of ovarian cancer in the NuTu-19 epithelial ovarian cancer animal model using 5-aminolevulinic acid (ALA) Gynecol. Oncol. 1997, 66, 122-132
16. Zhong, W.; Celli, J. P.; Rizvi, I.; Mai, Z.; Spring, B. Q.; Yun, S. H.; Hasan, T. In Vivo High-Resolution Fluorescence Microendoscopy for Ovarian Cancer Detection and Treatment Monitoring Br. J. Cancer 2009, 101, 2015-2022
17. Friedrich, J.; Seidel, C.; Ebner, R.; Kunz-Schughart, L. A. Spheroid-based drug screen: considerations and practical approach Nat. Protoc. 2009, 4, 309-324
18. Evans, C. L.; Rizvi, I.; Hasan, T.; de Boer, J. F. In vitro ovarian tumor growth and treatment response dynamics visualized with time-lapse OCT imaging Opt. Express 2009, 17 (11) 8892-8906
19. Celli, J.; Rizvi, I.; Evans, C. L.; Abu-Yousift, A.; Hasan, T. Quantitative imaging reveals heterogeneous growth dynamics and treatment-dependent residual tumor distributions in a three-dimensional ovarian cancer model J Biomed. Opt. 2010, 15, 051603
20. 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 (22) 9319-9328
21. Tannock, I. F.; Lee, C. M.; Tunggal, J. K.; Cowan, D. S. M.; Egorin, M. J. Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy Clin. Cancer Res. 2002, 8, 878-884
22. Jain, R. K.; Munn, L. L.; Fukumura, D. Dissection Tumor Pathophysiology Using Intravital Microscopy Nat. Rev. Cancer 2002, 2, 266-276
23. Evans, C. L.; Rizvi, I.; Celli, J.; Abu-Yousift, A.; de Boer, J. F.; Hasan, T. Visualizing Photodynamic Therapy Response with Time-Lapse OCT in an in vitro Model of Metastatic Ovarian Cancer Proc. SPIE 2010, 7551
24. Evans, C. L.; Abu-Yousif, A. O.; Park, Y. J.; Klein, O. J.; Celli, J. P.; Rizvi, I.; Zheng, X.; Hasan, T. Killing Hypoxic Cell Populations in a 3D Tumor Model with EtNBS-PDT PLoS One 2011, 6 (8) e23434
25. Dougherty, T. J.; Gomer, C. J.; Henderson, B. W.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic therapy J. Natl. Cancer Inst. 1998, 90 (12) 889-905
26. Duska, L. R.; Hamblin, M. R.; Miller, J. L.; Hasan, T. Combination Photoimmunotherapy and Cisplatin: Effects on Human Ovarian Cancer Ex Vivo J. Natl. Cancer Inst. 1999, 91 (18) 1557-1563
27. Canti, G.; Lattuada, D.; Morelli, S.; Nicolin, A.; Cubeddu, R.; Taroni, P.; Valentini, G. Efficacy of photodynamic therapy against doxorubicin-resistant murine tumors Cancer Lett 1995, 93 (2) 255-259
28. Teiten, M. H.; Bezdetnaya, L.; Merlin, J. L.; Bour-Dill, C.; Pauly, M. E.; Dicato, M.; Guillemin, F. Effect of meta-tetra (hydroxyphenyl) chlorin (mTHPC)-mediated photodynamic therapy on sensitive and multidrug-resistant human breast cancer cells J. Photochem. Photobiol., B 2001, 62 (3) 146-152
29. Cincotta, L.; Foley, J. W.; Cincotta, A. H. Phototoxicity, redox behavior, and pharmacokinetics of benzophenoxazine analogues in EMT-6 murine sarcoma cells Cancer Res. 1993, 53 (11) 2571-2580
30. Cincotta, L.; Foley, J. W.; MacEachern, T.; Lampros, E.; Cincotta, A. H. Novel photodynamic effects of a benzophenothiazine on two different murine sarcomas Cancer Res. 1994, 54 (5) 1249-1258
31. Frimberger, A. E.; Moore, A. S.; Cincotta, L.; Cotter, S. M.; Foley, J. W. Photodynamic therapy of naturally occurring tumors in animals using a novel benzophenothiazine photosensitizer Clin. Cancer Res. 1998, 4 (9) 2207-2218
32. Verma, S.; Sallum, U. W.; Athar, H.; Rosenblum, L.; Foley, J. W.; Hasan, T. Antimicrobial photodynamic efficacy of side-chain functionalized benzo[ a ]phenothiazinium dyes Photochem. Photobiol. 2009, 85 (1) 111-118
33. Carmichael, J.; DeGraff, W.; Gazdar, A. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing Cancer Res. 1987, 47, 936-942
34. Kawada, K.; Yonei, T.; Ueoka, H.; Kiura, K.; Tabata, M.; Takigawa, M.; Harada, M.; Tanimoto, M. Comparison of Chemisensitivity Tests: Clonogentic Assays versus MTT Assay Acta Med. Okayama 2002, 56, 129-134
35. Buch, K.; Peters, T.; Nawroth, T.; Sänger, M.; Schmidberger, H.; Langguth, P. Determination of cell survival after irradiation via clonogenic assay versus multiple MTT Assay - a comparative study Radiat. Oncol. 2012, 7, 1
36. Crescenzi, E.; Varriale, L. Photodynamic therapy with indocyanine green complements and enhances low-dose cisplatin cytotoxicity in MCF-7 breast cancer cells Mol. Cancer Ther. 2004, 3, 537-544
37. Tsai, T.; Hong, R.-L.; Tsai, J.-C.; Lou, P.-J.; Ling, I.-F.; Chen, C.-T. Effect of 5-aminolevulinic acid-mediated photodynamic therapy on MCF-7 and MCF-7/ADR cells Lasers Surg. Med. 2004, 34, 62-72
38. Goff, B. A.; Blake, J.; Bamberg, M. P.; Hasan, T. Treatment of ovarian cancer with photodynamic therapy and immunoconjugates in a murine ovarian cancer model Br. J. Cancer 1996, 74, 1194-1198
39. Hamblin, M. R.; Miller, J. L.; Rizvi, I.; Loew, H. G.; Hasan, T. Pegylation of charged polymer-photosensitiser conjugates: effects on photodynamic efficacy Br. J. Cancer 2003, 89, 937-943
40. Debnath, J.; Mills, K.; Collins, N.; Reginato, M.; Muthuswamy, S.; Brugge, J. S. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini Cell 2002, 111 (1) 29-40
41. Choi, H. S.; Nasr, K.; Alyabyev, S.; Feith, D.; Lee, J. H.; Kim, S. H.; Ashitate, Y.; Hyun, H.; Patonay, G.; Strekowski, L.; Henary, M.; Frangioni, J. V. Synthesis and in vivo fate of zwitterionic near-infrared fluorophores Angew. Chem. 2011, 50, 6258-6263
42. Georgakoudi, I.; Foster, T. H. Effects of the Subcellular Redistribution of Two Nile Blue Derivatives on Photodynamic Oxygen Consumption Photochem. Photobiol. 1998, 68 (1) 115-122
43. Molpus, K. L.; Koelliker, D.; Atkins, L.; Kato, D. T.; Buczek-Thomas, J.; Fuller, A. F., Jr.; Hasan, T. Characterization of a xenograft model of human ovarian carcinoma which produces intraperitoneal carcinomatosis and metastases in mice Int. J. Cancer 1996, 68 (5) 588-595
44. Sharma, S. V.; Haber, D. A.; Settleman, J. Cell line-based platforms to evaluate the therapeutic efficacy of candidate anticancer agents Nat. Rev. Cancer 2010, 10, 241-253
45. Loessner, D.; Stok, K. S.; Lutolf, M. P.; Hutmacher, D. W.; Clements, J. A.; Rizzi, S. C. Bioengineered 3D platform to explore cell-ECM interactions and drug resistance of epithelial ovarian cancer cells Biomaterials 2010, 31, 8494-8506
46. Zahir, N.; Weaver, V. M. Death in the third dimension: apoptosis regulation and tissue architecture Curr. Opin. Genet. Dev. 2004, 14, 71-80
47. Benz, R. Structural requirement for the rapid movement of charged molecules across membranes. Experiments with tetraphenylborate analogues Biophys. J. 1988, 54, 25-33
48. Gros, P.; Talbot, F.; Tang-Wai, D.; Bibi, E.; Kaback, H. R. Lipophilic cations: a group of model substrates for the multidrug-resistance transporter Biochemistry 1992, 31, 1992-1998
49. Walker, I.; Gorman, S. A.; Cox, R. D.; Vernon, D. I.; Griffiths, J.; Brown, S. B. A comparative analysis of phenothiazinium salts for the photosensitisation of murine fibrosarcoma (RIF-1) cells in vitro Photochem. Photobiol. Sci. 2004, 3, 653-659
50. Dapson, R. W. Dye-tissue interactions: mechanisms, quantification and bonding parameters for dyes used in biological staining Biotech. Histochem. 2005, 80, 49-72