Pharmacokinetic strategies to improve drug penetration and entrapment within solid tumors

Journal of Controlled Release

Volumn 219, Issue , 2015, Pages 269-277

  Al Abd, Ahmed M ^a,b,c   Aljehani, Zekra K ^c   Gazzaz, Rana W ^c   Fakhri, Sarah H ^c   Jabbad, Aisha H ^c   Alahdal, Abdulrahman M ^c   Torchilin, Vladimir P ^b,c  

^a NATIONAL RESEARCH CENTRE   (Egypt)

^b NORTHEASTERN UNIVERSITY   (United States)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Angiogenesis inhibitors; Chemoembolization; Extracellular matrix dissolving agents; Intratumoral pharmacokinetics; Metronomic therapy; P glycoprotein inhibitors; Tumor priming; Vascular disrupting agent

Indexed keywords

DISSOLUTION; GLYCOPROTEINS; PHARMACOKINETICS;

ANGIOGENESIS INHIBITORS; CHEMOEMBOLIZATION; EXTRACELLULAR MATRICES; METRONOMIC THERAPY; P-GLYCOPROTEIN; VASCULAR DISRUPTING AGENTS;

TUMORS;

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; VASCULAR TARGETING AGENT; CARRIER PROTEIN;

ANTIANGIOGENIC ACTIVITY; ARTICLE; BLOOD VESSEL OCCLUSION; CANCER RESISTANCE; CHEMOEMBOLIZATION; DRUG PENETRATION; EXTRACELLULAR MATRIX; HUMAN; PRIORITY JOURNAL; SOLID TUMOR; TUMOR MICROENVIRONMENT; ANIMAL; DRUG EFFECTS; METABOLISM; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

ANIMALS; ANTINEOPLASTIC AGENTS; CHEMOEMBOLIZATION, THERAPEUTIC; HUMANS; MEMBRANE TRANSPORT PROTEINS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR MICROENVIRONMENT;

EID: 84947494942     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.08.055     Document Type: Article

References (188)

1. World Health Organization The Global Burden of Disease: 2004 Update 2008 WHO Geneva (available at www.who.int/evidence/bod)
2. D.M. Parkin, P. Pisani, and J. Ferlay Global cancer statistics CA Cancer J. Clin. 49 1 1999 33 64 (31)
3. D.M. Parkin Global cancer statistics in the year 2000 Lancet Oncol. 2 9 2001 533 543
4. C.D. Mathers, K. Shibuya, C. Boschi-Pinto, A.D. Lopez, and C.J. Murray Global and regional estimates of cancer mortality and incidence by site: I. Application of regional cancer survival model to estimate cancer mortality distribution by site BMC Cancer 2 2002 36
5. D.M. Parkin, F. Bray, J. Ferlay, and P. Pisani Global cancer statistics, 2002 CA Cancer J. Clin. 55 2 2005 74 108
6. A. Jemal, F. Bray, M.M. Center, J. Ferlay, E. Ward, and D. Forman Global cancer statistics CA Cancer J. Clin. 61 2 2011 69 90
7. L.S. Goodman Goodman and Gilman's the Pharmacological Basis of Therapeutics 1996 McGraw-Hill New York
8. H. Derendorf Drug Actions: Basic Principles and Therapeutic Aspects 1995 CRC Press
9. O. Tredan, C.M. Galmarini, K. Patel, and I.F. Tannock Drug resistance and the solid tumor microenvironment J. Natl. Cancer Inst. 99 19 2007 1441 1454
10. R.K. Jain, R.T. Tong, and L.L. Munn Effect of vascular normalization by antiangiogenic therapy on interstitial hypertension, peritumor edema, and lymphatic metastasis: insights from a mathematical model Cancer Res. 67 6 2007 2729 2735
11. R.S. Kerbel Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science (New York, N.Y.) 312 5777 2006 1171 1175
12. A.I. Minchinton, and I.F. Tannock Drug penetration in solid tumours Nat. Rev. Cancer 6 8 2006 583 592
13. R.K. Jain, L.L. Munn, and D. Fukumura Measuring vascular permeability in mice Cold Spring Harb. Protoc. 2013 5 2013 444 446
14. U. Prabhakar, H. Maeda, R.K. Jain, E.M. Sevick-Muraca, W. Zamboni, O.C. Farokhzad, S.T. Barry, A. Gabizon, P. Grodzinski, and D.C. Blakey Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology Cancer Res. 73 8 2013 2412 2417
15. H.L. Wong, Z. Shen, Z. Lu, M.G. Wientjes, and J.L.-S. Au Paclitaxel tumor-priming enhances siRNA delivery and transfection in 3-dimensional tumor cultures Mol. Pharm. 8 3 2011 833 840
16. D. Lu, M.G. Wientjes, Z. Lu, and J.L.-S. Au Tumor priming enhances delivery and efficacy of nanomedicines J. Pharmacol. Exp. Ther. 322 1 2007 80 88
17. R. Grantab, S. Sivananthan, and I.F. Tannock The penetration of anticancer drugs through tumor tissue as a function of cellular adhesion and packing density of tumor cells Cancer Res. 66 2 2006 1033 1039
18. R.K. Jain, L.L. Munn, and D. Fukumura Measuring interstitial diffusion, convection, and binding parameters in mouse tumors Cold Spring Harb. Protoc. 2013 7 2013 678 680
19. A.M. Al-Abd, F.A. Al-Abbasi, G.F. Asaad, and A.B. Abdel-Naim Didox potentiates the cytotoxic profile of doxorubicin and protects from its cardiotoxicity Eur. J. Pharmacol. 718 1-3 2013 361 369
20. A.M. Mahmoud, A.M. Al-Abd, D.A. Lightfoot, and H.A. El-Shemy Anti-cancer characteristics of mevinolin against three different solid tumor cell lines was not solely p53-dependent J. Enzyme Inhib. Med. Chem. 27 5 2012 673 679
21. A.M. Al-Abd, K.Y. Hong, S.C. Song, and H.J. Kuh Pharmacokinetics of doxorubicin after intratumoral injection using a thermosensitive hydrogel in tumor-bearing mice J. Control. Release 142 1 2010 101 107
22. A.M. Al-Abd, F.A. Al-Abbasi, and V.P. Torchilin Intratumoral pharmacokinetics: challenges to nanobiomaterials Curr. Pharm. Des. 21 22 2015 3208 3214
23. M.I. Koukourakis, A. Giatromanolaki, E. Sivridis, and I. Fezoulidis Cancer vascularization: implications in radiotherapy? International Journal of Radiation Oncology∗Biology∗Physics 48 2 2000 545 553
24. J. Folkman Is angiogenesis an organizing principle in biology and medicine? J. Pediatr. Surg. 42 1 2007 1 11
25. M.P. Barr, D.J. Bouchier-Hayes, and J.J. Harmey Vascular endothelial growth factor is an autocrine survival factor for breast tumour cells under hypoxia Int. J. Oncol. 32 1 2008 41 48
26. J. Folkman Tumor angiogenesis: therapeutic implications N. Engl. J. Med. 285 21 1971 1182 1186
27. J. Folkman Angiogenesis: an organizing principle for drug discovery? Nat. Rev. 6 4 2007 273 286
28. D. Fukumura, and R.K. Jain Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize J. Cell. Biochem. 101 4 2007 937 949
29. D. Fukumura, and R.K. Jain Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization Microvasc. Res. 74 2-3 2007 72 84
30. R.K. Jain Molecular regulation of vessel maturation Nat. Med. 9 6 2003 685 693
31. R.K. Jain Delivery of molecular medicine to solid tumors: lessons from in vivo imaging of gene expression and function J. Control. Release 74 1-3 2001 7 25
32. R.K. Jain Delivery of molecular and cellular medicine to solid tumors Adv. Drug Deliv. Rev. 46 1-3 2001 149 168
33. R.K. Jain Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy Nat. Med. 7 9 2001 987 989
34. Y. Huang, S. Goel, D.G. Duda, D. Fukumura, and R.K. Jain Vascular normalization as an emerging strategy to enhance cancer immunotherapy Cancer Res. 73 10 2013 2943 2948
35. J. Segers, V. Di Fazio, R. Ansiaux, P. Martinive, O. Feron, P. Wallemacq, and B. Gallez Potentiation of cyclophosphamide chemotherapy using the anti-angiogenic drug thalidomide: importance of optimal scheduling to exploit the 'normalization' window of the tumor vasculature Cancer Lett. 244 1 2006 129 135
36. Y. Huang, T. Stylianopoulos, D.G. Duda, D. Fukumura, and R.K. Jain Benefits of vascular normalization are dose and time dependent - letter Cancer Res. 73 23 2013 7144 7146
37. S. Goel, D.G. Duda, L. Xu, L.L. Munn, Y. Boucher, D. Fukumura, and R.K. Jain Normalization of the vasculature for treatment of cancer and other diseases Physiol. Rev. 91 3 2011 1071 1121
38. R.T. Tong, Y. Boucher, S.V. Kozin, F. Winkler, D.J. Hicklin, and R.K. Jain Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors Cancer Res. 64 11 2004 3731 3736
39. N. Hansen-Algenstaedt, B.R. Stoll, T.P. Padera, D.E. Dolmans, D.J. Hicklin, D. Fukumura, and R.K. Jain Tumor oxygenation in hormone-dependent tumors during vascular endothelial growth factor receptor-2 blockade, hormone ablation, and chemotherapy Cancer Res. 60 16 2000 4556 4560
40. T.Y. Juan, S.R. Roffler, H.S. Hou, S.M. Huang, K.C. Chen, Y.L. Leu, Z.M. Prijovich, C.P. Yu, C.C. Wu, G.H. Sun, and T.L. Cha Antiangiogenesis targeting tumor microenvironment synergizes glucuronide prodrug antitumor activity Clin. Cancer Res. 15 14 2009 4600 4611
41. R.K. Jain Normalizing tumor microenvironment to treat cancer: bench to bedside to biomarkers J. Clin. Oncol. 31 17 2013 2205 2218
42. V.P. Chauhan, T. Stylianopoulos, J.D. Martin, Z. Popovic, O. Chen, W.S. Kamoun, M.G. Bawendi, D. Fukumura, and R.K. Jain Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner Nat. Nanotechnol. 7 6 2012 383 388
43. F. Winkler, S.V. Kozin, R.T. Tong, S.S. Chae, M.F. Booth, I. Garkavtsev, L. Xu, D.J. Hicklin, D. Fukumura, E. di Tomaso, L.L. Munn, and R.K. Jain Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases Cancer Cell 6 6 2004 553 563
44. P. Oliva, A. Decio, V. Castiglioni, A. Bassi, E. Pesenti, M. Cesca, E. Scanziani, D. Belotti, and R. Giavazzi Cisplatin plus paclitaxel and maintenance of bevacizumab on tumour progression, dissemination, and survival of ovarian carcinoma xenograft models Br. J. Cancer 107 2 2012 360 369
45. M. Cesca, F. Bizzaro, M. Zucchetti, and R. Giavazzi Tumor delivery of chemotherapy combined with inhibitors of angiogenesis and vascular targeting agents Front. Oncol. 3 2013 259
46. Q. Zhou, P. Guo, and J.M. Gallo Impact of angiogenesis inhibition by sunitinib on tumor distribution of temozolomide Clin. Cancer Res. 14 5 2008 1540 1549
47. J. Tabernero, T. Yoshino, A.L. Cohn, R. Obermannova, G. Bodoky, R. Garcia-Carbonero, T.E. Ciuleanu, D.C. Portnoy, E. Van Cutsem, A. Grothey, J. Prausova, P. Garcia-Alfonso, K. Yamazaki, P.R. Clingan, S. Lonardi, T.W. Kim, L. Simms, S.C. Chang, F. Nasroulah, and R.S. Investigators Ramucirumab versus placebo in combination with second-line FOLFIRI in patients with metastatic colorectal carcinoma that progressed during or after first-line therapy with bevacizumab, oxaliplatin, and a fluoropyrimidine (RAISE): a randomised, double-blind, multicentre, phase 3 study Lancet Oncol. 16 5 2015 499 508
48. D.P. Petrylak, N.J. Vogelzang, N. Budnik, P.J. Wiechno, C.N. Sternberg, K. Doner, J. Bellmunt, J.M. Burke, M.O. de Olza, A. Choudhury, J.E. Gschwend, E. Kopyltsov, A. Flechon, N. Van As, N. Houede, D. Barton, A. Fandi, U. Jungnelius, S. Li, R. de Wit, and K. Fizazi Docetaxel and prednisone with or without lenalidomide in chemotherapy-naive patients with metastatic castration-resistant prostate cancer (MAINSAIL): a randomised, double-blind, placebo-controlled phase 3 trial Lancet Oncol. 16 4 2015 417 425
49. I. Kumler, O.G. Christiansen, and D.L. Nielsen A systematic review of bevacizumab efficacy in breast cancer Cancer Treat. Rev. 40 8 2014 960 973
50. C.P. Raut, Y. Boucher, D.G. Duda, J.A. Morgan, R. Quek, M. Ancukiewicz, J. Lahdenranta, J.P. Eder, G.D. Demetri, and R.K. Jain Effects of sorafenib on intra-tumoral interstitial fluid pressure and circulating biomarkers in patients with refractory sarcomas (NCI protocol 6948) PLoS One 7 2 2012 e26331
51. A.G. Sorensen, K.E. Emblem, P. Polaskova, D. Jennings, H. Kim, M. Ancukiewicz, M. Wang, P.Y. Wen, P. Ivy, T.T. Batchelor, and R.K. Jain Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion Cancer Res. 72 2 2012 402 407
52. R.N. Gacche, and R.J. Meshram Angiogenic factors as potential drug target: efficacy and limitations of anti-angiogenic therapy Biochim. Biophys. Acta 1846 1 2014 161 179
53. T. Browder, C.E. Butterfield, B.M. Kraling, B. Shi, B. Marshall, M.S. O'Reilly, and J. Folkman Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer Cancer Res. 60 7 2000 1878 1886
54. S. Man, G. Bocci, G. Francia, S.K. Green, S. Jothy, D. Hanahan, P. Bohlen, D.J. Hicklin, G. Bergers, and R.S. Kerbel Antitumor effects in mice of low-dose (metronomic) cyclophosphamide administered continuously through the drinking water Cancer Res. 62 10 2002 2731 2735
55. U. Emmenegger, Y. Shaked, S. Man, G. Bocci, I. Spasojevic, G. Francia, A. Kouri, R. Coke, W. Cruz-Munoz, S.M. Ludeman, O.M. Colvin, and R.S. Kerbel Pharmacodynamic and pharmacokinetic study of chronic low-dose metronomic cyclophosphamide therapy in mice Mol. Cancer Ther. 6 8 2007 2280 2289
56. C.S. Chen, J.C. Doloff, and D.J. Waxman Intermittent metronomic drug schedule is essential for activating antitumor innate immunity and tumor xenograft regression Neoplasia 16 1 2014 84 96
57. G. Bocci, G. Francia, S. Man, J. Lawler, and R.S. Kerbel Thrombospondin 1, a mediator of the antiangiogenic effects of low-dose metronomic chemotherapy Proc. Natl. Acad. Sci. U. S. A. 100 22 2003 12917 12922
58. J.E. Damber, C. Vallbo, P. Albertsson, B. Lennernas, and K. Norrby The anti-tumour effect of low-dose continuous chemotherapy may partly be mediated by thrombospondin Cancer Chemother. Pharmacol. 58 3 2006 354 360
59. M.W. Kieran, C.D. Turner, J.B. Rubin, S.N. Chi, M.A. Zimmerman, C. Chordas, G. Klement, A. Laforme, A. Gordon, A. Thomas, D. Neuberg, T. Browder, and J. Folkman A feasibility trial of antiangiogenic (metronomic) chemotherapy in pediatric patients with recurrent or progressive cancer J. Pediatr. Hematol. Oncol. 27 11 2005 573 581
60. B. Lennernas, P. Albertsson, J.E. Damber, and K. Norrby Antiangiogenic effect of metronomic paclitaxel treatment in prostate cancer and non-tumor tissue in the same animals: a quantitative study APMIS 112 3 2004 201 209
61. D.W. Siemann, M.C. Bibby, G.G. Dark, A.P. Dicker, F.A. Eskens, M.R. Horsman, D. Marme, and P.M. Lorusso Differentiation and definition of vascular-targeted therapies Clin. Cancer Res. 11 2 Pt 1 2005 416 420
62. M. Taylor, F. Billiot, V. Marty, V. Rouffiac, P. Cohen, E. Tournay, P. Opolon, F. Louache, G. Vassal, C. Laplace-Builhe, P. Vielh, J.C. Soria, and F. Farace Reversing resistance to vascular-disrupting agents by blocking late mobilization of circulating endothelial progenitor cells Cancer Discov. 2 5 2012 434 449
63. P. Nathan, M. Zweifel, A.R. Padhani, D.M. Koh, M. Ng, D.J. Collins, A. Harris, C. Carden, J. Smythe, N. Fisher, N.J. Taylor, J.J. Stirling, S.P. Lu, M.O. Leach, G.J. Rustin, and I. Judson Phase I trial of combretastatin A4 phosphate (CA4P) in combination with bevacizumab in patients with advanced cancer Clin. Cancer Res. 18 12 2012 3428 3439
64. R. Giavazzi, M.R. Bani, and G. Taraboletti Tumor-host interaction in the optimization of paclitaxel-based combination therapies with vascular targeting compounds Cancer Metastasis Rev. 26 3-4 2007 481 488
65. M. Martinelli, K. Bonezzi, E. Riccardi, E. Kuhn, R. Frapolli, M. Zucchetti, A.J. Ryan, G. Taraboletti, and R. Giavazzi Sequence dependent antitumour efficacy of the vascular disrupting agent ZD6126 in combination with paclitaxel Br. J. Cancer 97 7 2007 888 894
66. C. Sessa, P. Lorusso, A. Tolcher, F. Farace, N. Lassau, A. Delmonte, A. Braghetti, R. Bahleda, P. Cohen, M. Hospitel, C. Veyrat-Follet, and J.C. Soria Phase I safety, pharmacokinetic and pharmacodynamic evaluation of the vascular disrupting agent ombrabulin (AVE8062) in patients with advanced solid tumors Clin. Cancer Res. 19 17 2013 4832 4842
67. T. Kusumoto, Y. Maehara, Y. Sakaguchi, M. Saku, and K. Sugimachi Hypoxia enhances the lethality of mitomycin C and carboquone against human malignant tumor cells in vitro Eur. Surg. Res. 21 3-4 1989 224 231
68. B.G. Siim, D.R. Menke, M.J. Dorie, and J.M. Brown Tirapazamine-induced cytotoxicity and DNA damage in transplanted tumors: relationship to tumor hypoxia Cancer Res. 57 14 1997 2922 2928
69. A.S. Lalani, S.E. Alters, A. Wong, M.R. Albertella, J.L. Cleland, and W.D. Henner Selective tumor targeting by the hypoxia-activated prodrug AQ4N blocks tumor growth and metastasis in preclinical models of pancreatic cancer Clin. Cancer Res. 13 7 2007 2216 2225
70. C.K. Luk, L. Veinot-Drebot, E. Tjan, and I.F. Tannock Effect of transient hypoxia on sensitivity to doxorubicin in human and murine cell lines J. Natl. Cancer Inst. 82 8 1990 684 692
71. H. Sasano, T. Suzuki, J. Takeyama, H. Utsunomiya, K. Ito, N. Ariga, and T. Moriya 17-Beta-hydroxysteroid dehydrogenase in human breast and endometrial carcinoma. A new development in intracrinology Oncology 59 Suppl. 1 2000 5 12
72. L. Chen, and D.J. Waxman Cytochrome P450 gene-directed enzyme prodrug therapy (GDEPT) for cancer Curr. Pharm. Des. 8 15 2002 1405 1416
73. H. Utsunomiya, K. Ito, T. Suzuki, T. Kitamura, C. Kaneko, T. Nakata, H. Niikura, K. Okamura, N. Yaegashi, and H. Sasano Steroid sulfatase and estrogen sulfotransferase in human endometrial carcinoma Clin. Cancer Res. 10 17 2004 5850 5856
74. C.N. Habib, A.M. Al-Abd, M.F. Tolba, A.E. Khalifa, A. Khedr, H.A. Mosli, and A.B. Abdel-Naim Leptin influences estrogen metabolism and accelerates prostate cell proliferation Life Sci. 121 2015 10 15
75. A. el-Tahtawy, and W. Wolf In vivo measurements of intratumoral metabolism, modulation, and pharmacokinetics of 5-fluorouracil, using 19F nuclear magnetic resonance spectroscopy Cancer Res. 51 21 1991 5806 5812
76. R. Bahleda, C. Sessa, G. Del Conte, L. Gianni, G. Capri, A. Varga, C. Oprea, B. Daglish, M. Hospitel, and J.C. Soria Phase I clinical and pharmacokinetic study of ombrabulin (AVE8062) combined with cisplatin/docetaxel or carboplatin/paclitaxel in patients with advanced solid tumors Investig. New Drugs 32 6 2014 1188 1196
77. M. Millward, P. Mainwaring, A. Mita, K. Federico, G.K. Lloyd, N. Reddinger, S. Nawrocki, M. Mita, and M.A. Spear Phase 1 study of the novel vascular disrupting agent plinabulin (NPI-2358) and docetaxel Investig. New Drugs 30 3 2012 1065 1073
78. W. Song, Z. Tang, D. Zhang, H. Yu, and X. Chen Coadministration of vascular disrupting agents and nanomedicines to eradicate tumors from peripheral and central regions Small 2015
79. R.K. Jain Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia Cancer Cell 26 5 2014 605 622
80. E.R. Gerstner, X. Ye, D.G. Duda, M.A. Levine, T. Mikkelsen, T.J. Kaley, J.J. Olson, B.L. Nabors, M.S. Ahluwalia, P.Y. Wen, R.K. Jain, T.T. Batchelor, and S. Grossman A phase I study of cediranib in combination with cilengitide in patients with recurrent glioblastoma Neuro-Oncology 2015
81. Q.S. Ng, H. Mandeville, V. Goh, R. Alonzi, J. Milner, D. Carnell, K. Meer, A.R. Padhani, M.I. Saunders, and P.J. Hoskin Phase Ib trial of radiotherapy in combination with combretastatin-A4-phosphate in patients with non-small-cell lung cancer, prostate adenocarcinoma, and squamous cell carcinoma of the head and neck Ann. Oncol. 23 1 2012 231 237
82. C. Lu-Emerson, D.G. Duda, K.E. Emblem, J.W. Taylor, E.R. Gerstner, J.S. Loeffler, T.T. Batchelor, and R.K. Jain Lessons from anti-vascular endothelial growth factor and anti-vascular endothelial growth factor receptor trials in patients with glioblastoma J. Clin. Oncol. 33 10 2015 1197 1213
83. P.M. Lorusso, S.A. Boerner, and S. Hunsberger Clinical development of vascular disrupting agents: what lessons can we learn from ASA404? J. Clin. Oncol. 29 22 2011 2952 2955
84. E.S. Wang, R. Pili, and M. Seshadri Modulation of chemotherapeutic efficacy by vascular disrupting agents: optimizing the sequence and schedule J. Clin. Oncol. 30 7 2012 760 761 (author reply 761-763)
85. R.S. Heist, D.G. Duda, D.V. Sahani, M. Ancukiewicz, P. Fidias, L.V. Sequist, J.S. Temel, A.T. Shaw, N.A. Pennell, J.W. Neal, L. Gandhi, T.J. Lynch, J.A. Engelman, and R.K. Jain Improved tumor vascularization after anti-VEGF therapy with carboplatin and nab-paclitaxel associates with survival in lung cancer Proc. Natl. Acad. Sci. U. S. A. 112 5 2015 1547 1552
86. K.E. Emblem, K. Mouridsen, A. Bjornerud, C.T. Farrar, D. Jennings, R.J. Borra, P.Y. Wen, P. Ivy, T.T. Batchelor, B.R. Rosen, R.K. Jain, and A.G. Sorensen Vessel architectural imaging identifies cancer patient responders to anti-angiogenic therapy Nat. Med. 19 9 2013 1178 1183
87. M. Datta, L.E. Via, W.S. Kamoun, C. Liu, W. Chen, G. Seano, D.M. Weiner, D. Schimel, K. England, J.D. Martin, X. Gao, L. Xu, C.E. Barry III, and R.K. Jain Anti-vascular endothelial growth factor treatment normalizes tuberculosis granuloma vasculature and improves small molecule delivery Proc. Natl. Acad. Sci. U. S. A. 112 6 2015 1827 1832
88. S. Goel, A.H. Wong, and R.K. Jain Vascular normalization as a therapeutic strategy for malignant and nonmalignant disease Cold Spring Harb. Perspect. Med. 2 3 2012 a006486
89. L. Eikenes, O.S. Bruland, C. Brekken, and L. Davies Cde Collagenase increases the transcapillary pressure gradient and improves the uptake and distribution of monoclonal antibodies in human osteosarcoma xenografts Cancer Res. 64 14 2004 4768 4773
90. P.A. Netti, D.A. Berk, M.A. Swartz, A.J. Grodzinsky, and R.K. Jain Role of extracellular matrix assembly in interstitial transport in solid tumors Cancer Res. 60 9 2000 2497 2503
91. I.K. Choi, R. Strauss, M. Richter, C.O. Yun, and A. Lieber Strategies to increase drug penetration in solid tumors Front. Oncol. 3 2013 193
92. S. Guedan, J.J. Rojas, A. Gros, E. Mercade, M. Cascallo, and R. Alemany Hyaluronidase expression by an oncolytic adenovirus enhances its intratumoral spread and suppresses tumor growth Mol. Ther. 18 7 2010 1275 1283
93. S. Ganesh, M. Gonzalez-Edick, D. Gibbons, M. Van Roey, and K. Jooss Intratumoral coadministration of hyaluronidase enzyme and oncolytic adenoviruses enhances virus potency in metastatic tumor models Clin. Cancer Res. 14 12 2008 3933 3941
94. L. Eikenes, M. Tari, I. Tufto, O.S. Bruland, and C. de Lange Davies Hyaluronidase induces a transcapillary pressure gradient and improves the distribution and uptake of liposomal doxorubicin (Caelyx) in human osteosarcoma xenografts Br. J. Cancer 93 1 2005 81 88
95. J.S. Blackburn, C.H. Rhodes, C.I. Coon, and C.E. Brinckerhoff RNA interference inhibition of matrix metalloproteinase-1 prevents melanoma metastasis by reducing tumor collagenase activity and angiogenesis Cancer Res. 67 22 2007 10849 10858
96. J.L. Kovar, M.A. Johnson, W.M. Volcheck, J. Chen, and M.A. Simpson Hyaluronidase expression induces prostate tumor metastasis in an orthotopic mouse model Am. J. Pathol. 169 4 2006 1415 1426
97. W.G. Stetler-Stevenson Type IV collagenases in tumor invasion and metastasis Cancer Metastasis Rev. 9 4 1990 289 303
98. R.K. Jain, D. Fukumura, and D.G. Duda Lessons from 30 years of teaching about the microenvironment of tumors Cancer J. 21 3 2015 137
99. R.K. Jain, D. Fukumura, and D.G. Duda From the guest editors: role of tumor microenvironment in tumor progression and treatment response: a 30 years' journey Cancer J. 21 4 2015 235 236
100. T. Stylianopoulos, B. Diop-Frimpong, L.L. Munn, and R.K. Jain Diffusion anisotropy in collagen gels and tumors: the effect of fiber network orientation Biophys. J. 99 10 2010 3119 3128
101. P.P. Provenzano, C. Cuevas, A.E. Chang, V.K. Goel, D.D. Von Hoff, and S.R. Hingorani Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma Cancer Cell 21 3 2012 418 429
102. K.E. DelGiorno, M.A. Carlson, R. Osgood, P.P. Provenzano, J.S. Brockenbough, C.B. Thompson, H.M. Shepard, G.I. Frost, J.D. Potter, and S.R. Hingorani Response to Chauhan et al.: interstitial pressure and vascular collapse in pancreas cancer-fluids and solids, measurement and meaning Cancer Cell 26 1 2014 16 17
103. P.P. Provenzano, and S.R. Hingorani Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer Br. J. Cancer 108 1 2013 1 8
104. I.M. Stromnes, K.E. DelGiorno, P.D. Greenberg, and S.R. Hingorani Stromal reengineering to treat pancreas cancer Carcinogenesis 35 7 2014 1451 1460
105. I.K. Choi, Y.S. Lee, J.Y. Yoo, A.R. Yoon, H. Kim, D.S. Kim, D.G. Seidler, J.H. Kim, and C.O. Yun Effect of decorin on overcoming the extracellular matrix barrier for oncolytic virotherapy Gene Ther. 17 2 2010 190 201
106. W. Mok, Y. Boucher, and R.K. Jain Matrix metalloproteinases-1 and -8 improve the distribution and efficacy of an oncolytic virus Cancer Res. 67 22 2007 10664 10668
107. E.I. Ager, S.V. Kozin, N.D. Kirkpatrick, G. Seano, D.P. Kodack, V. Askoxylakis, Y. Huang, S. Goel, M. Snuderl, A. Muzikansky, D.M. Finkelstein, D.T. Dransfield, L. Devy, Y. Boucher, D. Fukumura, and R.K. Jain Blockade of MMP14 activity in murine breast carcinomas: implications for macrophages, vessels, and radiotherapy J. Natl. Cancer Inst. 107 4 2015
108. I. Beyer, Z. Li, J. Persson, Y. Liu, R. van Rensburg, R. Yumul, X.B. Zhang, M.C. Hung, and A. Lieber Controlled extracellular matrix degradation in breast cancer tumors improves therapy by trastuzumab Mol. Ther. 19 3 2011 479 489
109. V.P. Chauhan, J.D. Martin, H. Liu, D.A. Lacorre, S.R. Jain, S.V. Kozin, T. Stylianopoulos, A.S. Mousa, X. Han, P. Adstamongkonkul, Z. Popovic, P. Huang, M.G. Bawendi, Y. Boucher, and R.K. Jain Angiotensin inhibition enhances drug delivery and potentiates chemotherapy by decompressing tumour blood vessels Nat. Commun. 4 2013 2516
110. B. Diop-Frimpong, V.P. Chauhan, S. Krane, Y. Boucher, and R.K. Jain Losartan inhibits collagen I synthesis and improves the distribution and efficacy of nanotherapeutics in tumors Proc. Natl. Acad. Sci. U. S. A. 108 7 2011 2909 2914
111. J. Liu, S. Liao, B. Diop-Frimpong, W. Chen, S. Goel, K. Naxerova, M. Ancukiewicz, Y. Boucher, R.K. Jain, and L. Xu TGF-beta blockade improves the distribution and efficacy of therapeutics in breast carcinoma by normalizing the tumor stroma Proc. Natl. Acad. Sci. U. S. A. 109 41 2012 16618 16623
112. K.B. Neeves, A.J. Sawyer, C.P. Foley, W.M. Saltzman, and W.L. Olbricht Dilation and degradation of the brain extracellular matrix enhances penetration of infused polymer nanoparticles Brain Res. 1180 2007 121 132
113. T. Stylianopoulos, and R.K. Jain Combining two strategies to improve perfusion and drug delivery in solid tumors Proc. Natl. Acad. Sci. U. S. A. 110 46 2013 18632 18637
114. J.K. Tunggal, J.R. Ballinger, and I.F. Tannock Influence of cell concentration in limiting the therapeutic benefit of P-glycoprotein reversal agents Int. J. Cancer 81 5 1999 741 747
115. J. Wang, Z. Lu, Y. Gao, M.G. Wientjes, and J.L. Au Improving delivery and efficacy of nanomedicines in solid tumors: role of tumor priming Nanomedicine (London) 6 9 2011 1605 1620
116. Z. Lu, M. Tsai, D. Lu, J. Wang, M.G. Wientjes, and J.L. Au Tumor-penetrating microparticles for intraperitoneal therapy of ovarian cancer J. Pharmacol. Exp. Ther. 327 3 2008 673 682
117. T. Stylianopoulos, J.D. Martin, V.P. Chauhan, S.R. Jain, B. Diop-Frimpong, N. Bardeesy, B.L. Smith, C.R. Ferrone, F.J. Hornicek, Y. Boucher, L.L. Munn, and R.K. Jain Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors Proc. Natl. Acad. Sci. U. S. A. 109 38 2012 15101 15108
118. T. Stylianopoulos, J.D. Martin, M. Snuderl, F. Mpekris, S.R. Jain, and R.K. Jain Coevolution of solid stress and interstitial fluid pressure in tumors during progression: implications for vascular collapse Cancer Res. 73 13 2013 3833 3841
119. V.P. Chauhan, Y. Boucher, C.R. Ferrone, S. Roberge, J.D. Martin, T. Stylianopoulos, N. Bardeesy, R.A. DePinho, T.P. Padera, L.L. Munn, and R.K. Jain Compression of pancreatic tumor blood vessels by hyaluronan is caused by solid stress and not interstitial fluid pressure Cancer Cell 26 1 2014 14 15
120. A. Batista, L. Riedemann, T. Vardam, and R.K. Jain Targeting the tumor microenvironment to enhance pediatric brain cancer treatment Cancer J. 21 4 2015 307 313
121. J.J. Longacre, C. Benton, and R.A. Unterthiner Treatment of facial hemangioma by intravascular embolization with silicone spheres. Case report Plast. Reconstr. Surg. 50 6 1972 618 621
122. G.H. Roberson, H. Biller, D.G. Sessions, and J.H. Ogura Presurgical internal maxillary artery embolization in juvenile angiofibroma Laryngoscope 82 8 1972 1524 1532
123. G.G. Hartnell, J. Gates, K. Stuart, J. Underhill, and D.P. Brophy Hepatic chemoembolization: effect of intraarterial lidocaine on pain and postprocedure recovery Cardiovasc. Intervent. Radiol. 22 4 1999 293 297
124. M. Varela, M.I. Real, M. Burrel, A. Forner, M. Sala, M. Brunet, C. Ayuso, L. Castells, X. Montana, J.M. Llovet, and J. Bruix Chemoembolization of hepatocellular carcinoma with drug eluting beads: efficacy and doxorubicin pharmacokinetics J. Hepatol. 46 3 2007 474 481
125. K. Ahrar, and S. Gupta Hepatic artery embolization for hepatocellular carcinoma: technique, patient selection, and outcomes Surg. Oncol. Clin. N. Am. 12 1 2003 105 126
126. S.W. Shin The current practice of transarterial chemoembolization for the treatment of hepatocellular carcinoma Korean J. Radiol. 10 5 2009 425 434
127. K. Hong, H. Kobeiter, C.S. Georgiades, M.S. Torbenson, and J.F. Geschwind Effects of the type of embolization particles on carboplatin concentration in liver tumors after transcatheter arterial chemoembolization in a rabbit model of liver cancer J. Vasc. Interv. Radiol. 16 12 2005 1711 1717
128. M. Grosso, C. Vignali, P. Quaretti, A. Nicolini, F. Melchiorre, G. Gallarato, I. Bargellini, P. Petruzzi, C. Massa Saluzzo, S. Crespi, and I. Sarti Transarterial chemoembolization for hepatocellular carcinoma with drug-eluting microspheres: preliminary results from an Italian multicentre study Cardiovasc. Intervent. Radiol. 31 6 2008 1141 1149
129. W.Y. Lau, and E.C. Lai Hepatocellular carcinoma: current management and recent advances Hepatobiliary Pancreat. Dis. Int. 7 3 2008 237 257
130. S.C. Yu, T.W. Leung, W.Y. Lau, N. Lee, E.P. Hui, W. Yeo, P.B. Lai, and T.S. Mok A comparison of three transarterial lipiodol-based formulations for hepatocellular carcinoma: in vivo biodistribution study in humans Cardiovasc. Intervent. Radiol. 31 2 2008 289 298
131. H.C. Spangenberg, I. Zuber-Jerger, R. Thimme, H.E. Blum, and F. Von Weizsacker Systemic treatment for hepatocellular carcinoma Zentralbl. Chir. 128 11 2003 906 910
132. J.M. Llovet, and J. Bruix Systematic review of randomized trials for unresectable hepatocellular carcinoma: chemoembolization improves survival Hepatology 37 2 2003 429 442
133. J. Tu, Z. Jia, and G. Jiang Re: safety and efficacy of 70-150 microm and 100-300 microm drug-eluting bead transarterial chemoembolization for hepatocellular carcinoma J. Vasc. Interv. Radiol. 26 8 2015 1251
134. J.H. Kim Re: "Comparison of transarterial chemoembolization and hepatic resection for large solitary hepatocellular carcinoma: a propensity score analysis" J. Vasc. Interv. Radiol. 26 8 2015 1249 1250
135. H. Kitade, H. Yanagida, N. Yokoigawa, M. Yamada, T. Hijikawa, M. Kaibori, K. Matsui, M. Ishizaki, K. Yoshioka, and M. Kon Two patients with recurrence of hepatocellular carcinoma after liver resection who achieved long-term stable disease with small doses of sorafenib therapy Gan To Kagaku Ryoho 42 7 2015 863 865
136. Y.R. Huo, and G.D. Eslick Transcatheter arterial chemoembolization plus radiotherapy compared with chemoembolization alone for hepatocellular carcinoma: a systematic review and meta-analysis JAMA Oncol. 2015
137. C.Y. Hsu, P.H. Liu, Y.H. Lee, C.Y. Hsia, Y.H. Huang, Y.Y. Chiou, H.C. Lin, and T.I. Huo Hepatocellular carcinoma patients with performance status 1 deserve new classification and treatment algorithm in the BCLC system Medicine 94 29 2015 e1223
138. M. Horio, E. Lovelace, I. Pastan, and M.M. Gottesman Agents which reverse multidrug-resistance are inhibitors of [3H]vinblastine transport by isolated vesicles Biochim. Biophys. Acta 1061 1 1991 106 110
139. M. Horio, K.V. Chin, S.J. Currier, S. Goldenberg, C. Williams, I. Pastan, M.M. Gottesman, and J. Handler Transepithelial transport of drugs by the multidrug transporter in cultured Madin-Darby canine kidney cell epithelia J. Biol. Chem. 264 25 1989 14880 14884
140. M.M. Cornwell, A.R. Safa, R.L. Felsted, M.M. Gottesman, and I. Pastan Membrane vesicles from multidrug-resistant human cancer cells contain a specific 150- to 170-kDa protein detected by photoaffinity labeling Proc. Natl. Acad. Sci. U. S. A. 83 11 1986 3847 3850
141. K. Kawai, I. Kusano, M. Ido, M. Sakurai, T. Shiraishi, and R. Yatani Identification of a P-glycoprotein-related protein (mini-P-glycoprotein) which is overexpressed in multidrug resistant cells Biochem. Biophys. Res. Commun. 198 2 1994 804 810
142. R. Krishna, and L.D. Mayer Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs Eur. J. Pharm. Sci. 11 4 2000 265 283
143. L.C. Young, B.G. Campling, S.P. Cole, R.G. Deeley, and J.H. Gerlach Multidrug resistance proteins MRP3, MRP1, and MRP2 in lung cancer: correlation of protein levels with drug response and messenger RNA levels Clin. Cancer Res. 7 6 2001 1798 1804
144. H. Zeng, L.J. Bain, M.G. Belinsky, and G.D. Kruh Expression of multidrug resistance protein-3 (multispecific organic anion transporter-D) in human embryonic kidney 293 cells confers resistance to anticancer agents Cancer Res. 59 23 1999 5964 5967
145. J.W. Jonker, J.W. Smit, R.F. Brinkhuis, M. Maliepaard, J.H. Beijnen, J.H. Schellens, and A.H. Schinkel Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan J. Natl. Cancer Inst. 92 20 2000 1651 1656
146. D.D. Ross, J.E. Karp, T.T. Chen, and L.A. Doyle Expression of breast cancer resistance protein in blast cells from patients with acute leukemia Blood 96 1 2000 365 368
147. M. Maliepaard, M.A. van Gastelen, L.A. de Jong, D. Pluim, R.C. van Waardenburg, M.C. Ruevekamp-Helmers, B.G. Floot, and J.H. Schellens Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line Cancer Res. 59 18 1999 4559 4563
148. L. Campos, D. Guyotat, E. Archimbaud, P. Calmard-Oriol, T. Tsuruo, J. Troncy, D. Treille, and D. Fiere Clinical significance of multidrug resistance P-glycoprotein expression on acute nonlymphoblastic leukemia cells at diagnosis Blood 79 2 1992 473 476
149. G.A. Niehans, W. Jaszcz, V. Brunetto, R.T. Perri, K. Gajl-Peczalska, M.R. Wick, T. Tsuruo, and C.D. Bloomfield Immunohistochemical identification of P-glycoprotein in previously untreated, diffuse large cell and immunoblastic lymphomas Cancer Res. 52 13 1992 3768 3775
150. A.T. Fojo, K. Ueda, D.J. Slamon, D.G. Poplack, M.M. Gottesman, and I. Pastan Expression of a multidrug-resistance gene in human tumors and tissues Proc. Natl. Acad. Sci. U. S. A. 84 1 1987 265 269
151. H.M. Abdallah, A.M. Al-Abd, R.S. El-Dine, and A.M. El-Halawany P-glycoprotein inhibitors of natural origin as potential tumor chemo-sensitizers: a review J. Adv. Res. 6 1 2015 45 62
152. T. Tsuruo, H. Iida, S. Tsukagoshi, and Y. Sakurai Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil Cancer Res. 41 5 1981 1967 1972
153. T. Tsuruo, H. Iida, S. Tsukagoshi, and Y. Sakurai Increased accumulation of vincristine and adriamycin in drug-resistant P388 tumor cells following incubation with calcium antagonists and calmodulin inhibitors Cancer Res. 42 11 1982 4730 4733
154. G.J. Schuurhuis, H.J. Broxterman, J.J. van der Hoeven, H.M. Pinedo, and J. Lankelma Potentiation of doxorubicin cytotoxicity by the calcium antagonist bepridil in anthracycline-resistant and -sensitive cell lines. A comparison with verapamil Cancer Chemother. Pharmacol. 20 4 1987 285 290
155. V. Hollt, M. Kouba, M. Dietel, and G. Vogt Stereoisomers of calcium antagonists which differ markedly in their potencies as calcium blockers are equally effective in modulating drug transport by P-glycoprotein Biochem. Pharmacol. 43 12 1992 2601 2608
156. M. Sehested, P.B. Jensen, T. Skovsgaard, N. Bindslev, E.J. Demant, E. Friche, and L. Vindelov Inhibition of vincristine binding to plasma membrane vesicles from daunorubicin-resistant Ehrlich ascites cells by multidrug resistance modulators Br. J. Cancer 60 6 1989 809 814
157. M.J. Newman, J.C. Rodarte, K.D. Benbatoul, S.J. Romano, C. Zhang, S. Krane, E.J. Moran, R.T. Uyeda, R. Dixon, E.S. Guns, and L.D. Mayer Discovery and characterization of OC144-093, a novel inhibitor of P-glycoprotein-mediated multidrug resistance Cancer Res. 60 11 2000 2964 2972
158. E.C. Spoelstra, H. Dekker, G.J. Schuurhuis, H.J. Broxterman, and J. Lankelma P-glycoprotein drug efflux pump involved in the mechanisms of intrinsic drug resistance in various colon cancer cell lines. Evidence for a saturation of active daunorubicin transport Biochem. Pharmacol. 41 3 1991 349 359
159. N.J. Chao, M. Aihara, K.G. Blume, and B.I. Sikic Modulation of etoposide (VP-16) cytotoxicity by verapamil or cyclosporine in multidrug-resistant human leukemic cell lines and normal bone marrow Exp. Hematol. 18 11 1990 1193 1198
160. H. Nawrath, and M. Raschack Effects of (-)-desmethoxyverapamil on heart and vascular smooth muscle J. Pharmacol. Exp. Ther. 242 3 1987 1090 1097
161. R. Pirker, G. Keilhauer, M. Raschack, C. Lechner, and H. Ludwig Reversal of multi-drug resistance in human KB cell lines by structural analogs of verapamil Int. J. Cancer 45 5 1990 916 919
162. D. Kessel, and C. Wilberding Promotion of daunorubicin uptake and toxicity by the calcium antagonist tiapamil and its analogs Cancer Treat. Rep. 69 6 1985 673 676
163. M.A. Alaoui-Jamali, R.L. Schecter, Y.M. Rustum, M.G. Centurioni, S. Lehnert, and G. Batist In vivo reversal of doxorubicin resistance by a new tiapamil analog Ro11-2933 J. Pharmacol. Exp. Ther. 264 3 1993 1299 1304
164. D. Boesch, C. Gaveriaux, B. Jachez, A. Pourtier-Manzanedo, P. Bollinger, and F. Loor In vivo circumvention of P-glycoprotein-mediated multidrug resistance of tumor cells with SDZ PSC 833 Cancer Res. 51 16 1991 4226 4233
165. B. Jonsson, K. Nilsson, P. Nygren, and R. Larsson SDZ PSC-833 - a novel potent in vitro chemosensitizer in multiple myeloma Anti-Cancer Drugs 3 6 1992 641 646
166. A.H. Dantzig, R.L. Shepard, J. Cao, K.L. Law, W.J. Ehlhardt, T.M. Baughman, T.F. Bumol, and J.J. Starling Reversal of P-glycoprotein-mediated multidrug resistance by a potent cyclopropyldibenzosuberane modulator, LY335979 Cancer Res. 56 18 1996 4171 4179
167. F. Hyafil, C. Vergely, P.D. Vignaud, and T. Grand-Perret In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative Cancer Res. 53 19 1993 4595 4602
168. I.L. Dale, W. Tuffley, R. Callaghan, J.A. Holmes, K. Martin, M. Luscombe, P. Mistry, H. Ryder, A.J. Stewart, P. Charlton, P.R. Twentyman, and P. Bevan Reversal of P-glycoprotein-mediated multidrug resistance by XR9051, a novel diketopiperazine derivative Br. J. Cancer 78 7 1998 885 892
169. S. Mullin, N. Mani, and T.H. Grossman Inhibition of antibiotic efflux in bacteria by the novel multidrug resistance inhibitors biricodar (VX-710) and timcodar (VX-853) Antimicrob. Agents Chemother. 48 11 2004 4171 4176
170. P. Kannan, S. Telu, S. Shukla, S.V. Ambudkar, V.W. Pike, C. Halldin, M.M. Gottesman, R.B. Innis, and M.D. Hall The "specific" P-glycoprotein inhibitor Tariquidar is also a substrate and an inhibitor for breast cancer resistance protein (BCRP/ABCG2) ACS Chem. Neurosci. 2 2 2011 82 89
171. V. Ling, and L.H. Thompson Reduced permeability in CHO cells as a mechanism of resistance to colchicine J. Cell. Physiol. 83 1 1974 103 116
172. S. Gollapudi, F. Thadepalli, C.H. Kim, and S. Gupta Difloxacin reverses multidrug resistance in HL-60/AR cells that overexpress the multidrug resistance-related protein (MRP) gene Oncol. Res. 7 5 1995 213 225
173. M. Louisa, T.M. Soediro, and F.D. Suyatna In vitro modulation of P-glycoprotein, MRP-1 and BCRP expression by mangiferin in doxorubicin-treated MCF-7 cells Asian Pac. J. Cancer Prev. 15 4 2014 1639 1642
174. S. Kawabata, M. Oka, K. Shiozawa, K. Tsukamoto, K. Nakatomi, H. Soda, M. Fukuda, Y. Ikegami, K. Sugahara, Y. Yamada, S. Kamihira, L.A. Doyle, D.D. Ross, and S. Kohno Breast cancer resistance protein directly confers SN-38 resistance of lung cancer cells Biochem. Biophys. Res. Commun. 280 5 2001 1216 1223
175. N. Xie, L. Mou, J. Yuan, W. Liu, T. Deng, Z. Li, Y. Jin, and Z. Hu Modulating drug resistance by targeting BCRP/ABCG2 using retrovirus-mediated RNA interference PLoS One 9 7 2014 e103463
176. B. Goldman Multidrug resistance: can new drugs help chemotherapy score against cancer? J. Natl. Cancer Inst. 95 4 2003 255 257
177. A.H. Kyle, L.A. Huxham, A.S. Chiam, D.H. Sim, and A.I. Minchinton Direct assessment of drug penetration into tissue using a novel application of three-dimensional cell culture Cancer Res. 64 17 2004 6304 6309
178. J.K. Tunggal, D.S. Cowan, H. Shaikh, and I.F. Tannock Penetration of anticancer drugs through solid tissue: a factor that limits the effectiveness of chemotherapy for solid tumors Clin. Cancer Res. 5 6 1999 1583 1586
179. I.F. Tannock, C.M. Lee, J.K. Tunggal, D.S. Cowan, and M.J. Egorin Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy Clin. Cancer Res. 8 3 2002 878 884
180. H.R. Mellor, S. Snelling, M.D. Hall, S. Modok, M. Jaffar, T.W. Hambley, and R. Callaghan The influence of tumour microenvironmental factors on the efficacy of cisplatin and novel platinum(IV) complexes Biochem. Pharmacol. 70 8 2005 1137 1146
181. S. Modok, P. Hyde, H.R. Mellor, T. Roose, and R. Callaghan Diffusivity and distribution of vinblastine in three-dimensional tumour tissue: experimental and mathematical modelling Eur. J. Cancer 42 14 2006 2404 2413
182. S. Modok, H.R. Mellor, and R. Callaghan Modulation of multidrug resistance efflux pump activity to overcome chemoresistance in cancer Curr. Opin. Pharmacol. 6 4 2006 350 354
183. J. Walker, C. Martin, and R. Callaghan Inhibition of P-glycoprotein function by XR9576 in a solid tumour model can restore anticancer drug efficacy Eur. J. Cancer 40 4 2004 594 605
184. J.K. Tunggal, T. Melo, J.R. Ballinger, and I.F. Tannock The influence of expression of P-glycoprotein on the penetration of anticancer drugs through multicellular layers Int. J. Cancer 86 1 2000 101 107
185. M.F. Flessner, and R.L. Dedrick Tissue-level transport mechanisms of intraperitoneally-administered monoclonal antibodies J. Control. Release 53 1-3 1998 69 75
186. G. Fracasso, and M. Colombatti Effect of therapeutic macromolecules in spheroids Crit. Rev. Oncol. Hematol. 36 2-3 2000 159 178
187. T. Nakajima, K. Sano, P.L. Choyke, and H. Kobayashi Improving the efficacy of photoimmunotherapy (PIT) using a cocktail of antibody conjugates in a multiple antigen tumor model Theranostics 3 6 2013 357 365
188. A.K. Larsen, A.E. Escargueil, and A. Skladanowski Resistance mechanisms associated with altered intracellular distribution of anticancer agents Pharmacol. Ther. 85 3 2000 217 229