Synergistic enhancement of carboplatin efficacy with photodynamic therapy in a three-dimensional model for micrometastatic ovarian cancer

Cancer Research

Volumn 70, Issue 22, 2010, Pages 9319-9328

  Rizvi, Imran ^a,b   Celli, Jonathan P ^a   Evans, Conor L ^a   Abu Yousif, Adnan O ^a   Muzikansky, Alona ^a   Pogue, Brian W ^b   Finkelstein, Dianne ^a   Hasan, Tayyaba ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b DARTMOUTH COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOPLATIN; VERTEPORFIN;

ARTICLE; CANCER CHEMOTHERAPY; CANCER SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; FLUORESCENCE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MICROMETASTASIS; OVARY CANCER; OVARY METASTASIS; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; THREE DIMENSIONAL IMAGING; TREATMENT OUTCOME; TUMOR VOLUME;

ANTINEOPLASTIC AGENTS; CADHERINS; CARBOPLATIN; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FEMALE; FIBRONECTINS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MICROSCOPY, CONFOCAL; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; PORPHYRINS;

EID: 78549253203     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1783     Document Type: Article

References (50)

1. Bast RC, Jr., Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation. Nat Rev Cancer 2009;9:415-28.
2. Cho KR, Shih Ie M. Ovarian cancer. Annu Rev Pathol 2009;4:287-313.
3. Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat Rev Cancer 2005;5:355-66.
4. del Carmen MG, Rizvi I, Chang Y, et al. Synergism of epidermal growth factor receptor-targeted immunotherapy with photodynamic treatment of ovarian cancer in vivo. JNCI 2005;97:1516-24.
5. Chi DS, Eisenhauer EL, Zivanovic O, et al. Improved progression-free and overall survival in advanced ovarian cancer as a result of a change in surgical paradigm. Gynecol Oncol 2009;114:26-31.
6. Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer 2006;6:583-92.
7. Au JL, Jang SH, Zheng J, et al. Determinants of drug delivery and transport to solid tumors. J Control Release 2001;74:31-46.
8. Agarwal R, Kaye SB. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 2003;3:502-16.
9. Martin LP, Schilder RJ. Management of recurrent ovarian carcinoma: current status and future directions. Semin Oncol 2009;36:112-25.
10. Guarneri V, Piacentini F, Barbieri E, Conte PF. Achievements and unmet needs in the management of advanced ovarian cancer. Gynecol Oncol 2010;117:152-8.
11. Griffith LG, Swartz MA. Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 2006;7:211-24.
12. Sharma SV, Haber DA, Settleman J. Cell line-based platforms to evaluate the therapeutic efficacy of candidate anticancer agents. Nat Rev Cancer 2010;10:241-53.
13. Duska LR, Hamblin MR, Miller JL, Hasan T. Combination photoimmunotherapy and cisplatin: effects on human ovarian cancer ex vivo. J Natl Cancer Inst 1999;91:1557-63.
14. Hahn SM, Fraker DL, Mick R, et al. A phase II trial of intraperitoneal photodynamic therapy for patients with peritoneal carcinomatosis and sarcomatosis. Clin Cancer Res 2006;12:2517.
15. DeLaney TF, Sindelar WF, Tochner Z, et al. Phase I study of debulking surgery and photodynamic therapy for disseminated intraperitoneal tumors. Int J Radiat Oncol Biol Phys 1993;25:445-57.
16. Sindelar WF, DeLaney TF, Tochner Z, et al. Technique of photodynamic therapy for disseminated intraperitoneal malignant neoplasms. Phase I study. Arch Surg 1991;126:318-24.
17. Hendren SK, Hahn SM, Spitz FR, et al. Phase II trial of debulking surgery and photodynamic therapy for disseminated intraperitoneal tumors. Ann Surg Oncol 2001;8:65-71.
18. Kessel D, Reiners JJ, Jr. Apoptosis and autophagy after mitochondrial or endoplasmic reticulum photodamage. Photochem Photobiol 2007;83:1024-8.
19. Wierrani F, Fiedler D, Grin W, et al. Clinical effect of mesotetrahydroxyphenylchlorine based photodynamic therapy in recurrent carcinoma of the ovary: preliminary results. Br J Obstet Gynaecol 1997;104:376-8.
20. Gomer CJ, Ferrario A, Luna M, Rucker N, Wong S. Photodynamic therapy: combined modality approaches targeting the tumor microenvironment. Lasers Surg Med 2006;38:516-21.
21. Zuluaga MF, Lange N. Combination of photodynamic therapy with anti-cancer agents. Curr Med Chem 2008;15:1655-73.
22. Hongrapipat J, Kopeckova P, Liu J, Prakongpan S, Kopecek J. Combination chemotherapy and photodynamic therapy with fab' fragment targeted HPMA copolymer conjugates in human ovarian carcinoma cells. Mol Pharm 2008;5:696-709.
23. Markman M. Pharmaceutical management of ovarian cancer: current status. Drugs 2008;68:771-89.
24. Celli JP, Spring BQ, Rizvi I, et al. Imaging and photodynamic therapy: mechanisms, monitoring, and optimization. Chem Rev 2010;110:2795-838.
25. Dougherty TJ, Gomer CJ, Henderson BW, et al. Photodynamic therapy. J Natl Cancer Inst 1998;90:889-905.
26. Hasan T, Ortel B, Solban N, Pogue B. Photodynamic therapy of cancer. In: Kufe DW, Bast RCJ, Hait WN, et al, editors. Cancer Medicine. 7th ed Hamilton (Ontario): B.C. Decker, Inc; 2006, p. 537-48.
27. Kessel D, Castelli M. Evidence that bcl-2 is the target of three photosensitizers that induce a rapid apoptotic response. Photochem Photobiol 2001;74:318-22.
28. Wilson BC. Photodynamic therapy for cancer: principles. Can J Gastroenterol 2002;16:393-6.
29. Granville DJ, Jiang H, An MT, Levy JG, McManus BM, Hunt DW. Bcl-2 overexpression blocks caspase activation and downstream apoptotic events instigated by photodynamic therapy. Br J Cancer 1999;79:95-100.
30. Aveline B, Hasan T, Redmond RW. Photophysical and photosensitizing properties of benzoporphyrin derivative monoacid ring A (BPD-MA). Photochem Photobiol 1994;59:328-35.
31. Molpus KL, Kato D, Hamblin MR, Lilge L, Bamberg M, Hasan T. Intraperitoneal photodynamic therapy of human epithelial ovarian carcinomatosis in a xenograft murine model. Cancer Res 1996;56:1075-82.
32. NIH RePORT Expenditures and Results (RePORTER). Enhancing direct tumor cell cytotoxicity by manipulating growth factor signaling. 2010 [cited 2010 March 17]; Available from: http://projectreporter.nih.gov/reporter.cfm (Project 5PO1CA087971-08: 0005).
33. Lurje G, Lenz HJ. EGFR signaling and drug discovery. Oncology 2009;77:400-10.
34. Lewis R, Schuman L, Mickler M, et al. Preclinical evaluation of cetuximab and benzoporphyrin derivative-mediated intraperitoneal photodynamic therapy in a canine model. 35th Meeting of the American Society for Photobiology. Brown University, Providence (RI): American Society for Photobiology; 2010, p. 34.
35. Petersen OW, Ronnov-Jessen L, Howlett AR, Bissell MJ. Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells. Proc Natl Acad Sci U S A 1992;89:9064-8.
36. Debnath J, Muthuswamy SK, Brugge JS. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003;30:256-68.
37. Celli JP, Rizvi I, Evans CL, Abu-Yousif AO, 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;15:051603-10.
38. Evans CL, Rizvi I, Hasan T, de Boer JF. In vitro ovarian tumor growth and treatment response dynamics visualized with time-lapse OCT imaging. Opt Express 2009;17:8892-906.
39. Sundfeldt K. Cell-cell adhesion in the normal ovary and ovarian tumors of epithelial origin; an exception to the rule. Mol Cell Endocrinol 2003;202:89-96.
40. Demeter A, Sziller I, Csapo Z, et al. Molecular prognostic markers in recurrent and in non-recurrent epithelial ovarian cancer. Anticancer Res 2005;25:2885-9.
41. Franke FE, Von Georgi R, Zygmunt M, Munstedt K. Association between fibronectin expression and prognosis in ovarian carcinoma. Anticancer Res 2003;23:4261-7.
42. Fujiwara K. Can carboplatin replace cisplatin for intraperitoneal use? Int J Gynecol Cancer 2008;18 Suppl 1:29-32.
43. Ashkenazi A. Targeting the extrinsic apoptosis pathway in cancer. Cytokine Growth Factor Rev 2008;19:325-31.
44. Markman M. Intraperitoneal chemotherapy in the management of ovarian cancer: focus on carboplatin. Ther Clin Risk Manag 2009;5:161-8.
45. Ohmori T, Yang JL, Price JO, Arteaga CL. Blockade of tumor cell transforming growth factor-βs enhances cell cycle progression and sensitizes human breast carcinoma cells to cytotoxic chemotherapy. Exp Cell Res 1998;245:350-9.
46. Menon C, Kutney SN, Lehr SC, et al. Vascularity and uptake of photosensitizer in small human tumor nodules: implications for intraperitoneal photodynamic therapy. Clin Cancer Res 2001;7:3904-11.
47. Abu-Yousif AO, Rizvi I, Evans CL, Celli JP, Hasan T. PuraMatrix encapsulation of cancer cells. Journal of Visualized Experiments 2009 December 17 [cited 2010 July]; Available from: http://www.jove.com/index/details.stp?ID= 1692.
48. Kenny HA, Krausz T, Yamada SD, Lengyel E. Use of a novel 3D culture model to elucidate the role of mesothelial cells, fibroblasts and extra-cellular matrices on adhesion and invasion of ovarian cancer cells to the omentum. Int J Cancer 2007;121:1463-72.
49. Burleson KM, Boente MP, Pambuccian SE, Skubitz AP. Disaggregation and invasion of ovarian carcinoma ascites spheroids. J Transl Med 2006;4:6.
50. Pereira SP. Photodynamic therapy for pancreatic and biliary tract carcinoma. Optical Methods for Tumor Treatment and Detection: Mechanisms and Techniques in Photodynamic Therapy XVIII; 2009; San Jose CA, USA: SPIE; 2009. p. 71640J-10.