Overcoming the blood-brain tumor barrier for effective glioblastoma treatment

Drug Resistance Updates

Volumn 19, Issue , 2015, Pages 1-12

  Van Tellingen, O ^c   Yetkin Arik, B ^a   De Gooijer, M C ^c   Wesseling, P ^a,d   Wurdinger, T ^a,b   De Vries, H E ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Blood brain barrier; Drug delivery; Glioma

Indexed keywords

ANTINEOPLASTIC AGENT;

ADULT; ANIMAL; BLOOD BRAIN BARRIER; BRAIN NEOPLASMS; DRUG DELIVERY SYSTEM; DRUG DESIGN; GLIOBLASTOMA; HUMAN; METABOLISM; PATHOLOGY; PROGNOSIS;

ADULT; ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; DRUG DELIVERY SYSTEMS; DRUG DESIGN; GLIOBLASTOMA; HUMANS; PROGNOSIS;

EID: 84939964233     PISSN: 13687646     EISSN: 15322084     Source Type: Journal    
DOI: 10.1016/j.drup.2015.02.002     Document Type: Review

References (158)

1. N.J. Abbott, A.A. Patabendige, D.E. Dolman, S.R. Yusof, and D.J. Begley Structure and function of the blood-brain barrier Neurobiol. Dis. 37 2010 13 25
2. N.J. Abbott, L. Ronnback, and E. Hansson Astrocyte-endothelial interactions at the blood-brain barrier Nat. Rev. Neurosci. 7 2006 41 53
3. S. Agarwal, R.K. Mittapalli, D.M. Zellmer, J.L. Gallardo, R. Donelson, C. Seiler, S.A. Decker, K.S. Santacruz, J.L. Pokorny, J.N. Sarkaria, W.F. Elmquist, and J.R. Ohlfest Active efflux of Dasatinib from the brain limits efficacy against murine glioblastoma: broad implications for the clinical use of molecularly targeted agents Mol. Cancer Ther. 11 2012 2183 2192
4. S. Agarwal, R. Sane, J.L. Gallardo, J.R. Ohlfest, and W.F. Elmquist Distribution of gefitinib to the brain is limited by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2)-mediated active efflux J. Pharmacol. Exp. Ther. 334 2010 147 155
5. C. Allen, M. Opyrchal, I. Aderca, M.A. Schroeder, J.N. Sarkaria, E. Domingo, M.J. Federspiel, and E. Galanis Oncolytic measles virus strains have significant antitumor activity against glioma stem cells Gene Ther. 20 2013 444 449
6. J.D. Allen, S.C. Van Dort, M. Buitelaar, O. van Tellingen, and A.H. Schinkel Mouse breast cancer resistance protein (Bcrp1/Abcg2) mediates etoposide resistance and transport, but etoposide oral availability is limited primarily by P-glycoprotein Cancer Res. 63 2003 1339 1344
7. D. Allhenn, M.A. Boushehri, and A. Lamprecht Drug delivery strategies for the treatment of malignant gliomas Int. J. Pharm. 436 2012 299 310
8. J.I. Alvarez, A. Dodelet-Devillers, H. Kebir, I. Ifergan, P.J. Fabre, S. Terouz, M. Sabbagh, K. Wosik, L. Bourbonniere, M. Bernard, J. van Horssen, H.E. de Vries, F. Charron, and A. Prat The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence Science 334 2011 1727 1731
9. J.I. Alvarez, T. Katayama, and A. Prat Glial influence on the blood-brain barrier Glia 61 2013 1939 1958
10. R.C. Anderson, B. Kennedy, C.L. Yanes, J. Garvin, M. Needle, P. Canoll, N.A. Feldstein, and J.N. Bruce Convection-enhanced delivery of topotecan into diffuse intrinsic brainstem tumors in children J. Neurosurg. Pediatr. 11 2013 289 295
11. L. Angelov, N.D. Doolittle, D.F. Kraemer, T. Siegal, G.H. Barnett, D.M. Peereboom, G. Stevens, J. McGregor, K. Jahnke, C.A. Lacy, N.A. Hedrick, E. Shalom, S. Ference, S. Bell, L. Sorenson, R.M. Tyson, M. Haluska, and E.A. Neuwelt Blood-brain barrier disruption and intra-arterial methotrexate-based therapy for newly diagnosed primary CNS lymphoma: a multi-institutional experience J. Clin. Oncol. 27 2009 3503 3509
12. E. Aronica, J.A. Gorter, S. Redeker, E.A. van Vliet, M. Ramkema, G.L. Scheffer, R.J. Scheper, P. van der Valk, S. Leenstra, J.C. Baayen, W.G. Spliet, and D. Troost Localization of breast cancer resistance protein (BCRP) in microvessel endothelium of human control and epileptic brain Epilepsia 46 2005 849 857
13. N.G. Avgeropoulos, and T.T. Batchelor New treatment strategies for malignant gliomas Oncologist 4 1999 209 224
14. N.U. Barua, S.S. Gill, and S. Love Convection-enhanced drug delivery to the brain: therapeutic potential and neuropathological considerations Brain Pathol. 24 2014 117 127
15. 11C]verapamil PET study J. Cereb. Blood Flow Metab. 2015 10.1038/jcbfm.2015.19 [Epub ahead of print]
16. 11C]verapamil and tariquidar at the human blood-brain barrier: a comparison with rat data Clin. Pharmacol. Ther. 91 2012 227 233
17. O.J. Becher, R. Mittapali, A.H. Chung, D. Crabtree, and W. Elmquist ABCG2 and MDR promote brainstem gliomagenesis and limit the efficacy of dasatinib in a diffuse intrinsic pontine glioma (DIPG) mouse model Neurooncology 16 Suppl. 3 2014 iii25
18. A. Ben-Zvi, B. Lacoste, E. Kur, B.J. Andreone, Y. Mayshar, H. Yan, and C. Gu Mfsd2a is critical for the formation and function of the blood-brain barrier Nature 509 2014 507 511
19. G.M. Bernal, M.J. LaRiviere, N. Mansour, P. Pytel, K.E. Cahill, D.J. Voce, S. Kang, R. Spretz, U. Welp, S.E. Noriega, L. Nunez, G. Larsen, R.R. Weichselbaum, and B. Yamini Convection-enhanced delivery and in vivo imaging of polymeric nanoparticles for the treatment of malignant glioma Nanomedicine 10 2014 149 157
20. D.S. Bidros, J.K. Liu, and M.A. Vogelbaum Future of convection-enhanced delivery in the treatment of brain tumors Future Oncol. 6 2010 117 125
21. D.S. Bidros, and M.A. Vogelbaum Novel drug delivery strategies in neuro-oncology Neurotherapeutics 6 2009 539 546
22. T. Birngruber, R. Raml, W. Gladdines, C. Gatschelhofer, E. Gander, A. Ghosh, T. Kroath, P.J. Gaillard, T.R. Pieber, and F. Sinner Enhanced doxorubicin delivery to the brain administered through glutathione PEGylated liposomal doxorubicin (2B3-101) as compared with generic Caelyx((R))/Doxil((R)) - a cerebral open flow microperfusion pilot study J. Pharm. Sci. 103 2014 1945 1948
23. R.G. Blasberg, H. Nakagawa, M.A. Bourdon, D.R. Groothuis, C.S. Patlak, and D.D. Bigner Regional localization of a glioma-associated antigen defined by monoclonal antibody 81C6 in vivo: kinetics and implications for diagnosis and therapy Cancer Res. 47 1987 4432 4443
24. U. Bogdahn, P. Hau, G. Stockhammer, N.K. Venkataramana, A.K. Mahapatra, A. Suri, A. Balasubramaniam, S. Nair, V. Oliushine, V. Parfenov, I. Poverennova, M. Zaaroor, P. Jachimczak, S. Ludwig, S. Schmaus, H. Heinrichs, K.H. Schlingensiepen, and Trabedersen Glioma Study Group Targeted therapy for high-grade glioma with the TGF-beta2 inhibitor trabedersen: results of a randomized and controlled phase IIb study Neurooncology 13 2011 132 142
25. C. Brandt, K. Bethmann, A.M. Gastens, and W. Loscher The multidrug transporter hypothesis of drug resistance in epilepsy: proof-of-principle in a rat model of temporal lobe epilepsy Neurobiol. Dis. 24 2006 202 211
26. H. Brem, S. Piantadosi, P.C. Burger, M. Walker, R. Selker, N.A. Vick, K. Black, M. Sisti, S. Brem, and G. Mohr Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The Polymer-Brain Tumor Treatment Group Lancet 345 1995 1008 1012
27. J.N. Bruce, R.L. Fine, P. Canoll, J. Yun, B.C. Kennedy, S.S. Rosenfeld, S.A. Sands, K. Surapaneni, R. Lai, C.L. Yanes, E. Bagiella, and R.L. DeLaPaz Regression of recurrent malignant gliomas with convection-enhanced delivery of topotecan Neurosurgery 69 2011 1272 1279
28. A.M.G. Bunt, and O. Van Tellingen Efflux Inhibitor Compositions and Methods of Treatment Using the Same 2014
29. C. Buonerba, G. Di Lorenzo, A. Marinelli, P. Federico, G. Palmieri, M. Imbimbo, P. Conti, G. Peluso, S. De Placido, and J.H. Sampson A comprehensive outlook on intracerebral therapy of malignant gliomas Crit. Rev. Oncol. Hematol. 80 2011 54 68
30. J.K. Burkhardt, H. Riina, B.J. Shin, P. Christos, K. Kesavabhotla, C.P. Hofstetter, A.J. Tsiouris, and J.A. Boockvar Intra-arterial delivery of bevacizumab after blood-brain barrier disruption for the treatment of recurrent glioblastoma: progression-free survival and overall survival World Neurosurg. 77 2012 130 134
31. X. Cao, and M.S. Schoichet Delivering neuroactive molecules from biodegradable microspheres for application in central nervous system disorders Biomaterials 20 1999 329 339
32. A. Carpentier, P. Metellus, R. Ursu, S. Zohar, F. Lafitte, M. Barrie, Y. Meng, M. Richard, C. Parizot, F. Laigle-Donadey, G. Gorochov, D. Psimaras, M. Sanson, A. Tibi, O. Chinot, and A.F. Carpentier Intracerebral administration of CpG oligonucleotide for patients with recurrent glioblastoma: a phase II study Neurooncology 12 2010 401 408
33. S.R. Chandana, S. Movva, M. Arora, and T. Singh Primary brain tumors in adults Am. Fam. Phys. 77 2008 1423 1430
34. C. Che, G. Yang, C. Thiot, M.C. Lacoste, J.C. Currie, M. Demeule, A. Regina, R. Beliveau, and J.P. Castaigne New Angiopep-modified doxorubicin (ANG1007) and etoposide (ANG1009) chemotherapeutics with increased brain penetration J. Med. Chem. 53 2010 2814 2824
35. P.Y. Chen, T. Ozawa, D.C. Drummond, A. Kalra, J.B. Fitzgerald, D.B. Kirpotin, K.C. Wei, N. Butowski, M.D. Prados, M.S. Berger, J.R. Forsayeth, K. Bankiewicz, and C.D. James Comparing routes of delivery for nanoliposomal irinotecan shows superior anti-tumor activity of local administration in treating intracranial glioblastoma xenografts Neurooncology 15 2013 189 197
36. E.A. Chiocca, K.M. Abbed, S. Tatter, D.N. Louis, F.H. Hochberg, F. Barker, J. Kracher, S.A. Grossman, J.D. Fisher, K. Carson, M. Rosenblum, T. Mikkelsen, J. Olson, J. Markert, S. Rosenfeld, L.B. Nabors, S. Brem, S. Phuphanich, S. Freeman, R. Kaplan, and J. Zwiebel A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting Mol. Ther. 10 2004 958 966
37. P. Chittiboina, J.D. Heiss, K.E. Warren, and R.R. Lonser Magnetic resonance imaging properties of convective delivery in diffuse intrinsic pontine gliomas J. Neurosurg. Pediatr. 13 2014 276 282
38. E.F. Choo, D. Kurnik, M. Muszkat, T. Ohkubo, S.D. Shay, J.N. Higginbotham, H. Glaeser, R.B. Kim, A.J. Wood, and G.R. Wilkinson Differential in vivo sensitivity to inhibition of P-glycoprotein located in lymphocytes, testes, and the blood-brain barrier J. Pharmacol. Exp. Ther. 317 2006 1012 1018
39. H.C. Cooray, C.G. Blackmore, L. Maskell, and M.A. Barrand Localisation of breast cancer resistance protein in microvessel endothelium of human brain Neuroreport 13 2002 2059 2063
40. C. Cordon-Cardo, J.P. O'Brien, D. Casals, L. Rittman-Grauer, J.L. Biedler, M.R. Melamed, and J.R. Bertino Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites Proc. Natl. Acad. Sci. U. S. A. 86 1989 695 698
41. R. Daneman, D. Agalliu, L. Zhou, F. Kuhnert, C.J. Kuo, and B.A. Barres Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis Proc. Natl. Acad. Sci. U. S. A. 106 2009 641 646
42. R. Daneman, L. Zhou, A.A. Kebede, and B.A. Barres Pericytes are required for blood-brain barrier integrity during embryogenesis Nature 468 2010 562 566
43. M. de Bruin, K. Miyake, T. Litman, R. Robey, and S.E. Bates Reversal of resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR Cancer Lett. 146 1999 117 126
44. H.E. de Vries, G. Kooij, D. Frenkel, S. Georgopoulos, A. Monsonego, and D. Janigro Inflammatory events at blood-brain barrier in neuroinflammatory and neurodegenerative disorders: implications for clinical disease Epilepsia 53 Suppl. 6 2012 45 52
45. N.A. de Vries, J. Zhao, E. Kroon, T. Buckle, J.H. Beijnen, and O. van Tellingen P-glycoprotein and breast cancer resistance protein: two dominant transporters working together in limiting the brain penetration of topotecan Clin. Cancer Res. 13 2007 6440 6449
46. M. Demeule, A. Regina, J. Jodoin, A. Laplante, C. Dagenais, F. Berthelet, A. Moghrabi, and R. Beliveau Drug transport to the brain: key roles for the efflux pump P-glycoprotein in the blood-brain barrier Vasc. Pharmacol. 38 2002 339 348
47. F.G. Dhermain, P. Hau, H. Lanfermann, A.H. Jacobs, and M.J. van den Bent Advanced MRI and PET imaging for assessment of treatment response in patients with gliomas Lancet Neurol. 9 2010 906 920
48. L.A. Doyle, W. Yang, L.V. Abruzzo, T. Krogmann, Y. Gao, A.K. Rishi, and D.D. Ross A multidrug resistance transporter from human MCF-7 breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 95 1998 15665 15670
49. J. Drappatz, A. Brenner, E.T. Wong, A. Eichler, D. Schiff, M.D. Groves, T. Mikkelsen, S. Rosenfeld, J. Sarantopoulos, C.A. Meyers, R.M. Fielding, K. Elian, X. Wang, B. Lawrence, M. Shing, S. Kelsey, J.P. Castaigne, and P.Y. Wen Phase I study of GRN1005 in recurrent malignant glioma Clin. Cancer Res. 19 2013 1567 1576
50. M. Duebgen, J. Martinez-Quintanilla, K. Tamura, S. Hingtgen, N. Redjal, H. Wakimoto, and K. Shah Stem cells loaded with multimechanistic oncolytic herpes simplex virus variants for brain tumor therapy J. Natl. Cancer Inst. 106 2014 dju090
51. S. Durmus, R.W. Sparidans, E. Wagenaar, J.H. Beijnen, and A.H. Schinkel Oral availability and brain penetration of the B-RAFV600E inhibitor vemurafenib can be enhanced by the P-GLYCOprotein (ABCB1) and breast cancer resistance protein (ABCG2) inhibitor elacridar Mol. Pharm. 9 2012 3236 3245
52. T. Eisenblatter, and H.J. Galla A new multidrug resistance protein at the blood-brain barrier Biochem. Biophys. Res. Commun. 293 2002 1273 1278
53. P.J. Elliott, N.J. Hayward, M.R. Huff, T.L. Nagle, K.L. Black, and R.T. Bartus Unlocking the blood-brain barrier: a role for RMP-7 in brain tumor therapy Exp. Neurol. 141 1996 214 224
54. D.F. Emerich, P. Snodgrass, R. Dean, M. Agostino, B. Hasler, M. Pink, H. Xiong, B.S. Kim, and R.T. Bartus Enhanced delivery of carboplatin into brain tumours with intravenous Cereport (RMP-7): dramatic differences and insight gained from dosing parameters Br. J. Cancer 80 1999 964 970
55. S.D. Ferguson Malignant gliomas: diagnosis and treatment Dis. Mon. 57 2011 558 569
56. P. Forsyth, G. Roldan, D. George, C. Wallace, C.A. Palmer, D. Morris, G. Cairncross, M.V. Matthews, J. Markert, Y. Gillespie, M. Coffey, B. Thompson, and M. Hamilton A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas Mol. Ther. 16 2008 627 632
57. D. Fortin, A. Desjardins, A. Benko, T. Niyonsega, and M. Boudrias Enhanced chemotherapy delivery by intraarterial infusion and blood-brain barrier disruption in malignant brain tumors: the Sherbrooke experience Cancer 103 2005 2606 2615
58. L.K. Fung, M.G. Ewend, A. Sills, E.P. Sipos, R. Thompson, M. Watts, O.M. Colvin, H. Brem, and W.M. Saltzman Pharmacokinetics of interstitial delivery of carmustine, 4-hydroperoxycyclophosphamide, and paclitaxel from a biodegradable polymer implant in the monkey brain Cancer Res. 58 1998 672 684
59. F.B. Furnari, T. Fenton, R.M. Bachoo, A. Mukasa, J.M. Stommel, A. Stegh, W.C. Hahn, K.L. Ligon, D.N. Louis, C. Brennan, L. Chin, R.A. DePinho, and W.K. Cavenee Malignant astrocytic glioma: genetics, biology, and paths to treatment Genes Dev. 21 2007 2683 2710
60. P.J. Gaillard, B.M. Kerklaan, P. Aftimos, S. Altintas, A. Jager, W. Gladdines, F. Lonnqvist, P. Soetekouw, H. Verheul, A. Awada, J. Schellens, and D. Brandsma Abstract CT216: phase I dose escalating study of 2B3-101, glutathione PEGylated liposomal doxorubicin, in patients with solid tumors and brain metastases or recurrent malignant glioma Cancer Res. 74 2014 CT216
61. K. Geletneky, J. Huesing, J. Rommelaere, J.R. Schlehofer, B. Leuchs, M. Dahm, O. Krebs, M. von Knebel Doeberitz, B. Huber, and J. Hajda Phase I/IIa study of intratumoral/intracerebral or intravenous/intracerebral administration of Parvovirus H-1 (ParvOryx) in patients with progressive primary or recurrent glioblastoma multiforme: ParvOryx01 protocol BMC Cancer 12 2012 99
62. D.R. Groothuis The blood-brain and blood-tumor barriers: a review of strategies for increasing drug delivery Neurooncology 2 2000 45 59
63. D.R. Groothuis, P. Molnar, and R.G. Blasberg Regional blood flow and blood-to-tissue transport in five brain tumor models: implications for chemotherapy Prog. Exp. Tumor Res. 27 1984 132 153
64. S. Hamm, B. Dehouck, J. Kraus, K. Wolburg-Buchholz, H. Wolburg, W. Risau, R. Cecchelli, B. Engelhardt, and M.P. Dehouck Astrocyte mediated modulation of blood-brain barrier permeability does not correlate with a loss of tight junction proteins from the cellular contacts Cell Tissue Res. 315 2004 157 166
65. M.E. Hardee, and D. Zagzag Mechanisms of glioma-associated neovascularization Am. J. Pathol. 181 2012 1126 1141
66. T. Huo, R.F. Barth, W. Yang, R.J. Nakkula, R. Koynova, B. Tenchov, A.R. Chaudhury, L. Agius, T. Boulikas, H. Elleaume, and R.J. Lee Preparation, biodistribution and neurotoxicity of liposomal cisplatin following convection enhanced delivery in normal and F98 glioma bearing rats PLoS ONE 7 2012 e48752
67. S. Idema, V. Caretti, M.L. Lamfers, V.W. van Beusechem, D.P. Noske, W.P. Vandertop, and C.M. Dirven Anatomical differences determine distribution of adenovirus after convection-enhanced delivery to the rat brain PLoS ONE 6 2011 e24396
68. T. Inamura, T. Nomura, R.T. Bartus, and K.L. Black Intracarotid infusion of RMP-7, a bradykinin analog: a method for selective drug delivery to brain tumors J. Neurosurg. 81 1994 752 758
69. A. Jacobs, P. Clifford, and H.E. Kay The Ommaya reservoir in chemotherapy for malignant disease in the CNS Clin. Oncol. 7 1981 123 129
70. A. Jordan, and K. Maier-Hauff Regional Therapy of Brain Tumors 2007 Human Press Inc. New Jersey
71. L. Juillerat-Jeanneret The targeted delivery of cancer drugs across the blood-brain barrier: chemical modifications of drugs or drug-nanoparticles? Drug Discov. Today 13 2008 1099 1106
72. R.L. Juliano, and V. Ling A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants Biochim. Biophys. Acta 455 1976 152 162
73. E.M. Kemper, A.E. Van Zandbergen, C. Cleypool, H.A. Mos, W. Boogerd, J.H. Beijnen, and O. van Tellingen Increased penetration of Paclitaxel into the brain by inhibition of P-glycoprotein Clin. Cancer Res. 9 2003 2849 2855
74. S. Kesari Understanding glioblastoma tumor biology: the potential to improve current diagnosis and treatments Semin. Oncol. 38 Suppl. 4 2011 S2 S10
75. K.P. Kicielinski, E.A. Chiocca, J.S. Yu, G.M. Gill, M. Coffey, and J.M. Markert Phase 1 clinical trial of intratumoral reovirus infusion for the treatment of recurrent malignant gliomas in adults Mol. Ther. 22 2014 1056 1062
76. J. Konig, F. Muller, and M.F. Fromm Transporters and drug-drug interactions: important determinants of drug disposition and effects Pharmacol. Rev. 65 2013 944 966
77. A. Korfel, and E. Thiel Targeted therapy and blood-brain barrier Recent Results Cancer Res. 176 2007 123 133
78. C. Kuntner, J.P. Bankstahl, M. Bankstahl, J. Stanek, T. Wanek, G. Stundner, R. Karch, R. Brauner, M. Meier, X. Ding, M. Muller, W. Loscher, and O. Langer Dose-response assessment of tariquidar and elacridar and regional quantification of P-glycoprotein inhibition at the rat blood-brain barrier using (R)-[(11)C]verapamil PET Eur. J. Nucl. Med. Mol. Imaging 37 2010 942 953
79. S. Kunwar, S. Chang, M. Westphal, M. Vogelbaum, J. Sampson, G. Barnett, M. Shaffrey, Z. Ram, J. Piepmeier, M. Prados, D. Croteau, C. Pedain, P. Leland, S.R. Husain, B.H. Joshi, R.K. Puri, and P.S. Group Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma Neurooncology 12 2010 871 881
80. I.E. Kuppens, E.O. Witteveen, R.C. Jewell, S.A. Radema, E.M. Paul, S.G. Mangum, J.H. Beijnen, E.E. Voest, and J.H. Schellens A phase I, randomized, open-label, parallel-cohort, dose-finding study of elacridar (GF120918) and oral topotecan in cancer patients Clin. Cancer Res. 13 2007 3276 3285
81. D. Kurnik, G.G. Sofowora, J.P. Donahue, U.B. Nair, G.R. Wilkinson, A.J. Wood, and M. Muszkat Tariquidar, a selective P-glycoprotein inhibitor, does not potentiate loperamide's opioid brain effects in humans despite full inhibition of lymphocyte P-glycoprotein Anesthesiology 109 2008 1092 1099
82. H. Kusuhara, and Y. Sugiyama Active efflux across the blood-brain barrier: role of the solute carrier family NeuroRx 2 2005 73 85
83. C. la Fougere, B. Suchorska, P. Bartenstein, F.W. Kreth, and J.C. Tonn Molecular imaging of gliomas with PET: opportunities and limitations Neurooncology 13 2011 806 819
84. J. Lachowicz, M. Demeule, A. Regina, E. Houle, S. Tripathy, and J.-P. Castaigne Abstract P6-11-05: ANG4043, a brain-penetrant anti-HER2 mAb increases survival in mice bearing intracranial BT-474 breast tumor cells Cancer Res. 73 2013 P6-11-05
85. J.S. Lagas, R.A. van Waterschoot, R.W. Sparidans, E. Wagenaar, J.H. Beijnen, and A.H. Schinkel Breast cancer resistance protein and P-glycoprotein limit sorafenib brain accumulation Mol. Cancer Ther. 9 2010 319 326
86. J.S. Lagas, R.A. van Waterschoot, T. van, V.M.J. Hillebrand, N. Lankheet, H. Rosing, J.H. Beijnen, and A.H. Schinkel Brain accumulation of dasatinib is restricted by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by elacridar treatment Clin. Cancer Res. 15 2009 2344 2351
87. Y.J. Lee, H. Kusuhara, J.W. Jonker, A.H. Schinkel, and Y. Sugiyama Investigation of efflux transport of dehydroepiandrosterone sulfate and mitoxantrone at the mouse blood-brain barrier: a minor role of breast cancer resistance protein J. Pharmacol. Exp. Ther. 312 2005 44 52
88. Z. Lidar, Y. Mardor, T. Jonas, R. Pfeffer, M. Faibel, D. Nass, M. Hadani, and Z. Ram Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study J. Neurosurg. 100 2004 472 479
89. S. Liebner, M. Corada, T. Bangsow, J. Babbage, A. Taddei, C.J. Czupalla, M. Reis, A. Felici, H. Wolburg, M. Fruttiger, M.M. Taketo, H. von Melchner, K.H. Plate, H. Gerhardt, and E. Dejana Wnt/beta-catenin signaling controls development of the blood-brain barrier J. Cell Biol. 183 2008 409 417
90. F. Lin, M.C. de Gooijer, D. Hanekamp, D. Brandsma, J.H. Beijnen, and O. van Tellingen Targeting core (mutated) pathways of high-grade gliomas: challenges of intrinsic resistance and drug efflux CNS Oncol. 2 2013 271 288
91. F. Lin, M.C. de Gooijer, E.M. Roig, L.C. Buil, S.M. Christner, J.H. Beumer, T. Wurdinger, J.H. Beijnen, and O. van Tellingen ABCB1, ABCG2, and PTEN determine the response of glioblastoma to temozolomide and ABT-888 therapy Clin. Cancer Res. 20 2014 2703 2713
92. F. Lin, S. Marchetti, D. Pluim, D. Iusuf, R. Mazzanti, J.H. Schellens, J.H. Beijnen, and O. van Tellingen Abcc4 together with abcb1 and abcg2 form a robust cooperative drug efflux system that restricts the brain entry of camptothecin analogues Clin. Cancer Res. 19 2013 2084 2095
93. R.R. Lonser, K.E. Warren, J.A. Butman, Z. Quezado, R.A. Robison, S. Walbridge, R. Schiffman, M. Merrill, M.L. Walker, D.M. Park, D. Croteau, R.O. Brady, and E.H. Oldfield Real-time image-guided direct convective perfusion of intrinsic brainstem lesions: technical note J. Neurosurg. 107 2007 190 197
94. D.N. Louis, H. Ohgaki, O.D. Wiestler, W.K. Cavenee, P.C. Burger, A. Jouvet, B.W. Scheithauer, and P. Kleihues The 2007 WHO classification of tumours of the central nervous system Acta Neuropathol. 114 2007 97 109
95. X. Lun, T. Alain, F.J. Zemp, H. Zhou, M.M. Rahman, M.G. Hamilton, G. McFadden, J. Bell, D.L. Senger, and P.A. Forsyth Myxoma virus virotherapy for glioma in immunocompetent animal models: optimizing administration routes and synergy with rapamycin Cancer Res. 70 2010 598 608
96. N. Luther, Z. Zhou, P. Zanzonico, N.K. Cheung, J. Humm, M.A. Edgar, and M.M. Souweidane The potential of theragnostic (1)(2)(4)I-8H9 convection-enhanced delivery in diffuse intrinsic pontine glioma Neurooncology 16 2014 800 806
97. M.R. Machein, J. Kullmer, B.L. Fiebich, K.H. Plate, and P.C. Warnke Vascular endothelial growth factor expression, vascular volume, and, capillary permeability in human brain tumors Neurosurgery 44 1999 732 740 discussion 740-741
98. J.M. Markert, S.N. Razdan, H.C. Kuo, A. Cantor, A. Knoll, M. Karrasch, L.B. Nabors, M. Markiewicz, B.S. Agee, J.M. Coleman, A.D. Lakeman, C.A. Palmer, J.N. Parker, R.J. Whitley, R.R. Weichselbaum, J.B. Fiveash, and G.Y. Gillespie A phase 1 trial of oncolytic HSV-1, G207, given in combination with radiation for recurrent GBM demonstrates safety and radiographic responses Mol. Ther. 22 2014 1048 1055
99. M.R. Mizee, and H.E. de Vries Blood-brain barrier regulation: environmental cues controlling the onset of barrier properties Tissue Barriers 1 2013 e26882
100. M.R. Mizee, D. Wooldrik, K.A. Lakeman, B. van het Hof, J.A. Drexhage, D. Geerts, M. Bugiani, E. Aronica, R.E. Mebius, A. Prat, H.E. de Vries, and A. Reijerkerk Retinoic acid induces blood-brain barrier development J. Neurosci. 33 2013 1660 1671
101. S. Mueller, M.Y. Polley, B. Lee, S. Kunwar, C. Pedain, E. Wembacher-Schroder, S. Mittermeyer, M. Westphal, J.H. Sampson, M.A. Vogelbaum, D. Croteau, and S.M. Chang Effect of imaging and catheter characteristics on clinical outcome for patients in the PRECISE study J. Neurooncol. 101 2011 267 277
102. A. Muik, L.J. Stubbert, R.Z. Jahedi, Y. Geibeta, J. Kimpel, C. Dold, R. Tober, A. Volk, S. Klein, U. Dietrich, B. Yadollahi, T. Falls, H. Miletic, D. Stojdl, J.C. Bell, and D. von Laer Re-engineering vesicular stomatitis virus to abrogate neurotoxicity, circumvent humoral immunity, and enhance oncolytic potency Cancer Res. 74 2014 3567 3578
103. N.S. Ningaraj, M. Rao, K. Hashizume, K. Asotra, and K.L. Black Regulation of blood-brain tumor barrier permeability by calcium-activated potassium channels J. Pharmacol. Exp. Ther. 301 2002 838 851
104. S. Nishio, M. Ohta, M. Abe, and K. Kitamura Microvascular abnormalities in ethylnitrosourea (ENU)-induced rat brain tumors: structural basis for altered blood-brain barrier function Acta Neuropathol. 59 1983 1 10
105. N.N. Nupponen, and H. Joensuu Molecular pathology of gliomas Curr. Diagn. Pathol. 12 2006 394 402
106. B. Obermeier, R. Daneman, and R.M. Ransohoff Development, maintenance and disruption of the blood-brain barrier Nat. Med. 19 2013 1584 1596
107. R.K. Oberoi, R.K. Mittapalli, and W.F. Elmquist Pharmacokinetic assessment of efflux transport in sunitinib distribution to the brain J. Pharmacol. Exp. Ther. 347 2013 755 764
108. H. Ohgaki, and P. Kleihues The definition of primary and secondary glioblastoma Clin. Cancer Res. 19 2013 764 772
109. H. Ohgaki, and P. Kleihues Genetic pathways to primary and secondary glioblastoma Am. J. Pathol. 170 2007 1445 1453
110. A. Ose, M. Ito, H. Kusuhara, K. Yamatsugu, M. Kanai, M. Shibasaki, M. Hosokawa, J.D. Schuetz, and Y. Sugiyama Limited brain distribution of [3R,4R,5S]-4-acetamido-5-amino-3-(1-ethylpropoxy)-1-cyclohexene-1-carboxylate phosphate (Ro 64-0802), a pharmacologically active form of oseltamivir, by active efflux across the blood-brain barrier mediated by organic anion transporter 3 (Oat3/Slc22a8) and multidrug resistance-associated protein 4 (Mrp4/Abcc4) Drug Metab. Dispos. 37 2009 315 321
111. W.M. Pardridge The blood-brain barrier: bottleneck in brain drug development NeuroRx 2 2005 3 14
112. W.M. Pardridge Drug transport across the blood-brain barrier J. Cereb. Blood Flow Metab. 32 2012 1959 1972
113. K.H. Plate, A. Scholz, and D.J. Dumont Tumor angiogenesis and anti-angiogenic therapy in malignant gliomas revisited Acta Neuropathol. 124 2012 763 775
114. H. Potschka, M. Fedrowitz, and W. Loscher Multidrug resistance protein MRP2 contributes to blood-brain barrier function and restricts antiepileptic drug activity J. Pharmacol. Exp. Ther. 306 2003 124 131
115. M.D. Prados, S.J.S. Schold, H.A. Fine, K. Jaeckle, F. Hochberg, L. Mechtler, M.R. Fetell, S. Phuphanich, L. Feun, T.J. Janus, K. Ford, and W. Graney A randomized, double-blind, placebo-controlled, phase 2 study of RMP-7 in combination with carboplatin administered intravenously for the treatment of recurrent malignant glioma Neurooncology 5 2003 96 103
116. N.G. Rainov, and V. Heidecke Long term survival in a patient with recurrent malignant glioma treated with intratumoral infusion of an IL4-targeted toxin (NBI-3001) J. Neurooncol. 66 2004 197 201
117. R.W. Rand, R.J. Kreitman, N. Patronas, F. Varricchio, I. Pastan, and R.K. Puri Intratumoral administration of recombinant circularly permuted interleukin-4-Pseudomonas exotoxin in patients with high-grade glioma Clin. Cancer Res. 6 2000 2157 2165
118. S.I. Rapoport Effect of concentrated solutions on blood-brain barrier Am. J. Physiol. 219 1970 270 274
119. S.I. Rapoport, M. Hori, and I. Klatzo Testing of a hypothesis for osmotic opening of the blood-brain barrier Am. J. Physiol. 223 1972 323 331
120. J.J. Raymond, D.M. Robertson, and H.B. Dinsdale Pharmacological modification of bradykinin induced breakdown of the blood-brain barrier, The Canadian journal of neurological sciences Le journal canadien des sciences neurologiques 13 1986 214 220
121. K.R. Robillard, G.N. Chan, G. Zhang, C. la Porte, W. Cameron, and R. Bendayan Role of P-glycoprotein in the distribution of the HIV protease inhibitor atazanavir in the brain and male genital tract Antimicrob. Agents Chemother. 58 2014 1713 1722
122. R. Saito, Y. Sonoda, T. Kumabe, K. Nagamatsu, M. Watanabe, and T. Tominaga Regression of recurrent glioblastoma infiltrating the brainstem after convection-enhanced delivery of nimustine hydrochloride J. Neurosurg. Pediatr. 7 2011 522 526
123. R. Saito, and T. Tominaga Convection-enhanced delivery: from mechanisms to clinical drug delivery for diseases of the central nervous system Neurol. Med. Chir. 52 2012 531 538
124. J.H. Sampson, G. Archer, C. Pedain, E. Wembacher-Schroder, M. Westphal, S. Kunwar, M.A. Vogelbaum, A. Coan, J.E. Herndon, R. Raghavan, M.L. Brady, D.A. Reardon, A.H. Friedman, H.S. Friedman, M.I. Rodriguez-Ponce, S.M. Chang, S. Mittermeyer, D. Croteau, and R.K. Puri Poor drug distribution as a possible explanation for the results of the PRECISE trial J. Neurosurg. 113 2010 301 309
125. J.H. Sampson, D.A. Reardon, A.H. Friedman, H.S. Friedman, R.E. Coleman, R.E. McLendon, I. Pastan, and D.D. Bigner Sustained radiographic and clinical response in patient with bifrontal recurrent glioblastoma multiforme with intracerebral infusion of the recombinant targeted toxin TP-38: case study Neurooncology 7 2005 90 96
126. N. Sanai, S. Chang, and M.S. Berger Low-grade gliomas in adults J. Neurosurg. 115 2011 948 965
127. R. Sane, R.K. Mittapalli, and W.F. Elmquist Development and evaluation of a novel microemulsion formulation of elacridar to improve its bioavailability J. Pharm. Sci. 102 2013 1343 1354
128. R. Sane, S.P. Wu, R. Zhang, and J.M. Gallo The effect of ABCG2 and ABCC4 on the pharmacokinetics of methotrexate in the brain Drug Metab. Dispos. 42 2014 537 540
129. A.H. Schinkel, J.J. Smit, O. van Tellingen, J.H. Beijnen, E. Wagenaar, L. van Deemter, C.A. Mol, M.A. van der Valk, E.C. Robanus-Maandag, H.P.J. te Riele, A.J.M. Berns, and P. Borst Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs Cell 77 1994 491 502
130. K.E. Schlageter, P. Molnar, G.D. Lapin, and D.R. Groothuis Microvessel organization and structure in experimental brain tumors: microvessel populations with distinctive structural and functional properties Microvasc. Res. 58 1999 312 328
131. A.C. Sewing, V. Caretti, T. Lagerweij, P. Schellen, M.H. Jansen, D.G. van Vuurden, S. Idema, C.F. Molthoff, W.P. Vandertop, G.J. Kaspers, D.P. Noske, and E. Hulleman Convection enhanced delivery of carmustine to the murine brainstem: a feasibility study J. Neurosci. Methods 238C 2014 88 94
132. T. Shimamura, S.R. Husain, and R.K. Puri The IL-4 and IL-13 Pseudomonas exotoxins: new hope for brain tumor therapy Neurosurg. Focus 20 2006 E11
133. Y. Shitara, K. Maeda, K. Ikejiri, K. Yoshida, T. Horie, and Y. Sugiyama Clinical significance of organic anion transporting polypeptides (OATPs) in drug disposition: their roles in hepatic clearance and intestinal absorption Biopharm. Drug Dispos. 34 2013 45 78
134. T. Siegal, R. Rubinstein, F. Bokstein, A. Schwartz, A. Lossos, E. Shalom, R. Chisin, and J.M. Gomori In vivo assessment of the window of barrier opening after osmotic blood-brain barrier disruption in humans J. Neurosurg. 92 2000 599 605
135. A.J. Slot, S.V. Molinski, and S.P. Cole Mammalian multidrug-resistance proteins (MRPs) Essays Biochem. 50 2011 179 207
136. A.M. Sonabend, A.S. Carminucci, B. Amendolara, M. Bansal, R. Leung, L. Lei, R. Realubit, H. Li, C. Karan, J. Yun, C. Showers, R. Rothcock, J.O.A. Califano, P. Canoll, and J.N. Bruce Convection-enhanced delivery of etoposide is effective against murine proneural glioblastoma Neurooncology 16 2014 1210 1219
137. A. Soontornmalai, M.L. Vlaming, and J.M. Fritschy Differential, strain-specific cellular and subcellular distribution of multidrug transporters in murine choroid plexus and blood-brain barrier Neuroscience 138 2006 159 169
138. W.D. Stein, S.E. Bates, and T. Fojo Intractable cancers: the many faces of multidrug resistance and the many targets it presents for therapeutic attack Curr. Drug Targets 5 2004 333 346
139. A. Suzuki, P. Leland, H. Kobayashi, P.L. Choyke, E.M. Jagoda, T. Inoue, B.H. Joshi, and R.K. Puri Analysis of biodistribution of intracranially infused radiolabeled interleukin-13 receptor-targeted immunotoxin IL-13PE by SPECT/CT in an orthotopic mouse model of human glioma J. Nucl. Med. 55 2014 1323 1329
140. Y. Takamiya, Y. Abe, Y. Tanaka, A. Tsugu, M. Kazuno, Y. Oshika, K. Maruo, Y. Ohnishi, O. Sato, H. Yamazaki, H. Kijima, Y. Ueyama, N. Tamaoki, and M. Nakamura Murine P-glycoprotein on stromal vessels mediates multidrug resistance in intracerebral human glioma xenografts Br. J. Cancer 76 1997 445 450
141. Y. Tanaka, Y. Abe, A. Tsugu, Y. Takamiya, A. Akatsuka, T. Tsuruo, H. Yamazaki, Y. Ueyama, O. Sato, and N. Tamaoki Ultrastructural localization of P-glycoprotein on capillary endothelial cells in human gliomas Virchows Archiv 425 1994 133 138
142. T. Tomita Interstitial chemotherapy for brain tumors: review J. Neurooncol. 10 1991 57 74
143. S. Valtonen, U. Timonen, P. Toivanen, H. Kalimo, L. Kivipelto, O. Heiskanen, G. Unsgaard, and T. Kuurne Interstitial chemotherapy with carmustine-loaded polymers for high-grade gliomas: a randomized double-blind study Neurosurgery 41 1997 44 48 discussion 48-49
144. E. van de Steeg, A. van Esch, E. Wagenaar, C.M. van der Kruijssen, O. van Tellingen, K.E. Kenworthy, and A.H. Schinkel High impact of Oatp1a/1b transporters on in vivo disposition of the hydrophobic anticancer drug paclitaxel Clin. Cancer Res. 17 2011 294 301
145. E.A. van Vliet, R. van Schaik, P.M. Edelbroek, R.A. Voskuyl, S. Redeker, E. Aronica, W.J. Wadman, and J.A. Gorter Region-specific overexpression of P-glycoprotein at the blood-brain barrier affects brain uptake of phenytoin in epileptic rats J. Pharmacol. Exp. Ther. 322 2007 141 147
146. D. Vecchio, A. Daga, E. Carra, D. Marubbi, A. Raso, S. Mascelli, P. Nozza, M.L. Garre, F. Pitto, J.L. Ravetti, S. Vagge, R. Corvo, A. Profumo, G. Baio, D. Marcello, and G. Frosina Pharmacokinetics, pharmacodynamics and efficacy on pediatric tumors of the glioma radiosensitizer KU60019 Int. J. Cancer 2014 10.1002/ijc.29121
147. M.H. Verheije, M.L. Lamfers, T. Wurdinger, G.C. Grinwis, W.R. Gerritsen, V.W. van Beusechem, and P.J. Rottier Coronavirus genetically redirected to the epidermal growth factor receptor exhibits effective antitumor activity against a malignant glioblastoma J. Virol. 83 2009 7507 7516
148. K. Warren, R. Jakacki, B. Widemann, A. Aikin, M. Libucha, R. Packer, G. Vezina, G. Reaman, D. Shaw, M. Krailo, C. Osborne, J. Cehelsky, D. Caldwell, J. Stanwood, S.M. Steinberg, and F.M. Balis Phase II trial of intravenous lobradimil and carboplatin in childhood brain tumors: a report from the Children's Oncology Group Cancer Chemother. Pharmacol. 58 2006 343 347
149. S. Watkins, S. Robel, I.F. Kimbrough, S.M. Robert, G. Ellis-Davies, and H. Sontheimer Disruption of astrocyte-vascular coupling and the blood-brain barrier by invading glioma cells Nat. Commun. 5 2014 4196
150. P.Y. Wen, and S. Kesari Malignant gliomas in adults N. Engl. J. Med. 359 2008 492 507
151. M. Westphal, D.C. Hilt, E. Bortey, P. Delavault, R. Olivares, P.C. Warnke, I.R. Whittle, J. Jaaskelainen, and Z. Ram A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma Neurooncology 5 2003 79 88
152. M. Westphal, and K. Lamszus The neurobiology of gliomas: from cell biology to the development of therapeutic approaches Nat. Rev. Neurosci. 12 2011 495 508
153. E. White, A. Bienemann, L. Megraw, C. Bunnun, and S. Gill Evaluation and optimization of the administration of a selectively replicating herpes simplex viral vector to the brain by convection-enhanced delivery Cancer Gene Ther. 18 2011 358 369
154. J. Wijnholds, E.C. deLange, G.L. Scheffer, D.J. van den Berg, C.A. Mol, M. van der Valk, A.H. Schinkel, R.J. Scheper, D.D. Breimer, and P. Borst Multidrug resistance protein 1 protects the choroid plexus epithelium and contributes to the blood-cerebrospinal fluid barrier J. Clin. Invest. 105 2000 279 285
155. H. Wolburg, and A. Lippoldt Tight junctions of the blood-brain barrier: development, composition and regulation Vasc. Pharmacol. 38 2002 323 337
156. Y. Yamashita, M.T. Krauze, T. Kawaguchi, C.O. Noble, D.C. Drummond, J.W. Park, and K.S. Bankiewicz Convection-enhanced delivery of a topoisomerase I inhibitor (nanoliposomal topotecan) and a topoisomerase II inhibitor (pegylated liposomal doxorubicin) in intracranial brain tumor xenografts Neurooncology 9 2007 20 28
157. W. Yang, R.F. Barth, T. Huo, R.J. Nakkula, M. Weldon, N. Gupta, L. Agius, and J.C. Grecula Radiation therapy combined with intracerebral administration of carboplatin for the treatment of brain tumors Radiat. Oncol. 9 2014 25
158. Y. Zhang, J.D. Schuetz, W.F. Elmquist, and D.W. Miller Plasma membrane localization of multidrug resistance-associated protein (MRP) homologues in brain capillary endothelial cells J. Pharmacol. Exp. Ther. 311 2004 449 455