Penetration of anticancer drugs through tumour tissue as a function of cellular packing density and interstitial fluid pressure and its modification by bortezomib

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Grantab, Rama H ^a   Tannock, Ian F ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; DOXORUBICIN; FLUOROURACIL; GEMCITABINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER TISSUE; CELL DENSITY; CELL TYPE; CHEMOSENSITIVITY; COLON CARCINOMA; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG DISTRIBUTION; DRUG DOSE COMPARISON; DRUG PENETRATION; DRUG POTENTIATION; EPITHELIOID CELL; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; ROUND CELL; TISSUE PRESSURE; TUMOR XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; BORONIC ACIDS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR FLUID; HUMANS; MALE; MICE; MICE, NUDE; NEOPLASMS; PYRAZINES; TISSUE DISTRIBUTION; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84861804406     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-214     Document Type: Article

References (46)

1. Au JL, Jang SH, Zheng J, Chen CT, Song S, Hu L, Wientjes MG. Determinants of drug delivery and transport to solid tumors. J Control Release. 2001, 74(1-3):31-46.
2. Durand RE. Flow cytometry studies of intracellular adriamycin in multicell spheroids in vitro. Cancer Res 1981, 41(9 Pt 1):3495-3498.
3. Grantab R, Sivananthan S, Tannock IF. The penetration of anticancer drugs through tumor tissue as a function of cellular adhesion and packing density of tumor cells. Cancer Res 2006, 66(2):1033-1039. 10.1158/0008-5472.CAN-05-3077, 16424039.
4. Huxham LA, Kyle AH, Baker JH, Nykilchuk LK, Minchinton AI. Microregional effects of gemcitabine in HCT-116 xenografts. Cancer Res 2004, 64(18):6537-6541. 10.1158/0008-5472.CAN-04-0986, 15374965.
5. Kyle AH, Huxham LA, Chiam AS, Sim DH, Minchinton AI. Direct assessment of drug penetration into tissue using a novel application of three-dimensional cell culture. Cancer Res 2004, 64(17):6304-6309. 10.1158/0008-5472.CAN-04-1099, 15342419.
6. Kyle AH, Huxham LA, Yeoman DM, Minchinton AI. Limited tissue penetration of taxanes: a mechanism for resistance in solid tumors. Clin Cancer Res 2007, 13(9):2804-2810. 10.1158/1078-0432.CCR-06-1941, 17473214.
7. Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer 2006, 6(8):583-592. 10.1038/nrc1893, 16862189.
8. Primeau AJ, Rendon A, Hedley D, Lilge L, Tannock IF. The distribution of the anticancer drug Doxorubicin in relation to blood vessels in solid tumors. Clin Cancer Res 2005, 11(24 Pt 1):8782-8788.
9. Tannock IF, Lee CM, Tunggal JK, Cowan DS, Egorin MJ. Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy. Clin Cancer Res 2002, 8(3):878-884.
10. Tunggal JK, Cowan DS, Shaikh H, Tannock IF. Penetration of anticancer drugs through solid tissue: a factor that limits the effectiveness of chemotherapy for solid tumors. Clin Cancer Res 1999, 5(6):1583-1586.
11. Hicks KO, Ohms SJ, van Zijl PL, Denny WA, Hunter PJ, Wilson WR. An experimental and mathematical model for the extravascular transport of a DNA intercalator in tumours. Br J Cancer 1997, 76(7):894-903. 10.1038/bjc.1997.481, 2228074, 9328149.
12. Zheng JH, Chen CT, Au JL, Wientjes MG. Time- and concentration-dependent penetration of doxorubicin in prostate tumors. AAPS PharmSci. 2001, 3(2):E15. 2779556, 11741266.
13. Kuh HJ, Jang SH, Wientjes MG, Weaver JR, Au JL. Determinants of paclitaxel penetration and accumulation in human solid tumor. J Pharmacol Exp Ther 1999, 290(2):871-880.
14. Jang SH, Wientjes MG, Au JL. Enhancement of paclitaxel delivery to solid tumors by apoptosis-inducing pretreatment: effect of treatment schedule. J Pharmacol Exp Ther 2001, 296(3):1035-1042.
15. Croix BS, Rak JW, Kapitain S, Sheehan C, Graham CH, Kerbel RS. Reversal by hyaluronidase of adhesion-dependent multicellular drug resistance in mammary carcinoma cells. J Natl Cancer Inst. 1996, 88(18):1285-1296. 10.1093/jnci/88.18.1285, 8797768.
16. Green SK, Francia G, Isidoro C, Kerbel RS. Antiadhesive antibodies targeting E-cadherin sensitize multicellular tumor spheroids to chemotherapy in vitro. Mol Cancer Ther 2004, 3(2):149-159.
17. Denlinger CE, Rundall BK, Keller MD, Jones DR. Proteasome inhibition sensitizes non-small-cell lung cancer to gemcitabine-induced apoptosis. Ann Thorac Surg 2004, 78(4):1207-1214. discussion 1207-14, 10.1016/j.athoracsur.2004.04.029, 15464472.
18. Cusack JC, Liu R, Houston M, Abendroth K, Elliott PJ, Adams J, Baldwin AS. Enhanced chemosensitivity to CPT-11 with proteasome inhibitor PS-341: implications for systemic nuclear factor-kappaB inhibition. Cancer Res 2001, 61(9):3535-3540.
19. Nawrocki ST, Sweeney-Gotsch B, Takamori R, McConkey DJ. The proteasome inhibitor bortezomib enhances the activity of docetaxel in orthotopic human pancreatic tumor xenografts. Mol Cancer Ther 2004, 3(1):59-70.
20. Russo SM, Tepper JE, Baldwin AS, Liu R, Adams J, Elliott P, Cusack JC. Enhancement of radiosensitivity by proteasome inhibition: implications for a role of NF-kappaB. Int J Radiat Oncol Biol Phys 2001, 50(1):183-193. 10.1016/S0360-3016(01)01446-8, 11316563.
21. Mitsiades N, Mitsiades CS, Richardson PG, Poulaki V, Tai YT, Chauhan D, Fanourakis G, Gu X, Bailey C, Joseph M, Libermann TA, Schlossman R, Munshi NC, Hideshima T, Anderson KC. The proteasome inhibitor PS-341 potentiates sensitivity of multiple myeloma cells to conventional chemotherapeutic agents: therapeutic applications. Blood 2003, 101(6):2377-2380. 10.1182/blood-2002-06-1768, 12424198.
22. Aghajanian C, Dizon DS, Sabbatini P, Raizer JJ, Dupont J, Spriggs DR. Phase I trial of bortezomib and carboplatin in recurrent ovarian or primary peritoneal cancer. J Clin Oncol 2005, 23(25):5943-5949. 10.1200/JCO.2005.16.006, 16135465.
23. Dou QP, Goldfarb RH. Bortezomib (millennium pharmaceuticals). IDrugs. 2002, 5(8):828-834.
24. Frankel A, Man S, Elliott P, Adams J, Kerbel RS. Lack of multicellular drug resistance observed in human ovarian and prostate carcinoma treated with the proteasome inhibitor PS-341. Clin Cancer Res 2000, 6(9):3719-3728.
25. Williams S, Pettaway C, Song R, Papandreou C, Logothetis C, McConkey DJ. Differential effects of the proteasome inhibitor bortezomib on apoptosis and angiogenesis in human prostate tumor xenografts. Mol Cancer Ther 2003, 2(9):835-843.
26. Birle DC, Hedley DW. Suppression of the hypoxia-inducible factor-1 response in cervical carcinoma xenografts by proteasome inhibitors. Cancer Res 2007, 67(4):1735-1743. 10.1158/0008-5472.CAN-06-2722, 17308115.
27. Prujin FB, Patel K, Hay MP, Wilson WR, Hick KO. Prediction of tumour tissue diffusion coefficients of hypoxia activated prodrugs from physiochemical parameters. Aust J Chem 2008, 61(9):694-699.
28. Cowan DS, Hicks KO, Wilson WR. Multicellular membranes as an in vitro model for extravascular diffusion in tumours. Br J Cancer Suppl. 1996, 27:S28-S31. 2149990, 8763841.
29. Less JR, Posner MC, Boucher Y, Borochovitz D, Wolmark N, Jain RK. Interstitial hypertension in human breast and colorectal tumors. Cancer Res 1992, 52(22):6371-6374.
30. Netti PA, Berk DA, Swartz MA, Grodzinsky AJ, Jain RK. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000, 60(9):2497-2503.
31. Rintoul RC, Sethi T. The role of extracellular matrix in small-cell lung cancer. Lancet Oncol 2001, 2(7):437-442. 10.1016/S1470-2045(00)00421-6, 11905738.
32. Rintoul RC, Sethi T. Extracellular matrix regulation of drug resistance in small-cell lung cancer. Clin Sci (Lond). 2002, 102(4):417-424.
33. Sethi T, Rintoul RC, Moore SM, MacKinnon AC, Salter D, Choo C, Chilvers ER, Dransfield I, Donnelly SC, Strieter R, Haslett C. Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med. 1999, 5(6):662-668. 10.1038/9511, 10371505.
34. St Croix B, Man S, Kerbel RS. Reversal of intrinsic and acquired forms of drug resistance by hyaluronidase treatment of solid tumors. Cancer Lett 1998, 131(1):35-44. 10.1016/S0304-3835(98)00199-2, 9839618.
35. St Croix B, Sheehan C, Rak JW, Florenes VA, Slingerland JM, Kerbel RS. E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27(KIP1). J Cell Biol 1998, 142(2):557-571. 10.1083/jcb.142.2.557, 2133056, 9679152.
36. Akiyama M, Hideshima T, Hayashi T, Tai YT, Mitsiades CS, Mitsiades N, Chauhan D, Richardson P, Munshi NC, Anderson KC. Nuclear factor-kappaB p65 mediates tumor necrosis factor alpha-induced nuclear translocation of telomerase reverse transcriptase protein. Cancer Res 2003, 63(1):18-21.
37. Lorch JH, Thomas TO, Schmoll HJ. Bortezomib inhibits cell-cell adhesion and cell migration and enhances epidermal growth factor receptor inhibitor-induced cell death in squamous cell cancer. Cancer Res 2007, 67(2):727-734. 10.1158/0008-5472.CAN-06-2162, 17234784.
38. Teicher BA, Ara G, Herbst R, Palombella VJ, Adams J. The proteasome inhibitor PS-341 in cancer therapy. Clin Cancer Res 1999, 5(9):2638-2645.
39. Dreicer R, Petrylak D, Agus D, Webb I, Roth B. Phase I/II study of bortezomib plus docetaxel in patients with advanced androgen-independent prostate cancer. Clin Cancer Res 2007, 13(4):1208-1215. 10.1158/1078-0432.CCR-06-2046, 17317831.
40. Boucher Y, Kirkwood JM, Opacic D, Desantis M, Jain RK. Interstitial hypertension in superficial metastatic melanomas in humans. Cancer Res 1991, 51(24):6691-6694.
41. Boucher Y, Jain RK. Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse. Cancer Res 1992, 52(18):5110-5114.
42. Heldin CH, Rubin K, Pietras K, Ostman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer 2004, 4(10):806-813. 10.1038/nrc1456, 15510161.
43. Monsky WL, Fukumura D, Gohongi T, Ancukiewcz M, Weich HA, Torchilin VP, Yuan F, Jain RK. Augmentation of transvascular transport of macromolecules and nanoparticles in tumors using vascular endothelial growth factor. Cancer Res 1999, 59(16):4129-4135.
44. Pietras K, Ostman A, Sjoquist M, Buchdunger E, Reed RK, Heldin CH, Rubin K. Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors. Cancer Res 2001, 61(7):2929-2934.
45. Taghian AG, Abi-Raad R, Assaad SI, Casty A, Ancukiewicz M, Yeh E, Molokhia P, Attia K, Sullivan T, Kuter I, Boucher Y, Powell SN. Paclitaxel decreases the interstitial fluid pressure and improves oxygenation in breast cancers in patients treated with neoadjuvant chemotherapy: clinical implications. J Clin Oncol 2005, 23(9):1951-1961. 10.1200/JCO.2005.08.119, 15774788.
46. Eikenes L, Bruland OS, Brekken C, de Lange Davies C. Collagenase increases the transcapillary pressure gradient and improves the uptake and distribution of monoclonal antibodies in human osteosarcoma xenografts. Cancer Res 2004, 62(14):4768-4773.