Strategies to improve delivery of anticancer drugs across the blood-brain barrier to treat glioblastoma

Neuro-Oncology

Volumn 18, Issue 1, 2016, Pages 27-36

  Oberoi, Rajneet K ^a   Parrish, Karen E ^a   Sio, Terence T ^b   Mittapalli, Rajendar K ^a   Elmquist, William F ^a   Sarkaria, Jann N ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MAYO CLINIC   (United States)

Author keywords

blood brain barrier; drug delivery; efflux transporters; glioma

Indexed keywords

ANTINEOPLASTIC AGENT; NANOCARRIER; NANOPARTICLE; PEPTIDE;

BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; CANCER CHEMOTHERAPY; CONVECTION ENHANCED DELIVERY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG TRANSPORT; DRUG TREATMENT FAILURE; ECHOGRAPHY; GLIOBLASTOMA; GLIOMA CELL; HUMAN; MEMBRANE DAMAGE; MEMBRANE TRANSPORT; MOLECULARLY TARGETED THERAPY; NONHUMAN; OSMOSIS; PHYSICAL CHEMISTRY; REVIEW; STRUCTURE ACTIVITY RELATION; SYSTEMIC CIRCULATION; THERMODYNAMICS; TIGHT JUNCTION; TREATMENT RESPONSE; TUMOR INVASION; ANIMAL; BRAIN NEOPLASMS; DEVICES; METABOLISM; PROCEDURES;

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

EID: 84960433266     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nov164     Document Type: Review

References (84)

1. Furnari FB, Fenton T, Bachoo RM, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007; 21(21):2683-2710.
2. Ostrom QT, Gittleman H, Liao P, et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007-2011. Neurooncol. 2014;16(Suppl 4): iv1-iv63.
3. Vartanian A, Singh SK, Agnihotri S, et al. GBM?s multifaceted landscape: highlighting regional and microenvironmental heterogeneity. Neuro Oncol. 2014;16(9):1167-1175.
4. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis. 2004;16(1):1-13.
5. Agarwal S, Sane R, Oberoi R, et al. Delivery of molecularly targeted therapy to malignant glioma, a disease of the whole brain. Expert Rev Mol Med. 2011;13:e17.
6. Tamai I, Tsuji A. Transporter-mediated permeation of drugs across the blood-brain barrier. J Pharm Sci. 2000;89(11):1371-1388.
7. Vick NA, Khandekar JD, Bigner DD. Chemotherapy of brain tumors. Arch Neurol. 1977;34(9):523-526.
8. Hou LC, Veeravagu A, Hsu AR, Tse VC. Recurrent glioblastoma multiforme: a review of natural history and management options. Neurosurg Focus. 2006;20(4):E5.
9. Pafundi DH, Laack NN, Youland RS, et al. Biopsy validation of 18F-DOPA PET and biodistribution in gliomas for neurosurgical planning and radiotherapy target delineation: results of a prospective pilot study. Neuro Oncol. 2013;15(8):1058-1067.
10. Onda K, Tanaka R, Takahashi H, et al. Cerebral glioblastoma with cerebrospinal fluid dissemination: a clinicopathological study of 14 cases examined by complete autopsy. Neurosurgery. 1989; 25(4):533-540.
11. Rapoport SI. Effect of concentrated solutions on blood-brain barrier. Am J Physiol. 1970;219(1):270-274.
12. Rapoport SI, HoriM, Klatzo I. Testingofahypothesis forosmoticopening of the blood-brain barrier. Am J Physiol. 1972;223(2):323-331.
13. Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery. 1998;42(5):1083-1099; discussion 1099-1100.
14. Neuwelt EA, Howieson J, Frenkel EP, et al. Therapeutic efficacy of multiagent chemotherapy with drug delivery enhancement by blood-brain barrier modification in glioblastoma. Neurosurgery. 1986;19(4):573-582.
15. Kraemer DF, Fortin D, Neuwelt EA. Chemotherapeutic dose intensification for treatment of malignant brain tumors: recent developments and future directions. Curr Neurol Neurosci Rep. 2002;2(3):216-224.
16. Seto A, Murakami M, Fukuyama H, et al. Ventricular tachycardia caused by hyperkalemia after administration of hypertonic mannitol. Anesthesiology. 2000;93(5):1359-1361.
17. Kemper EM, Boogerd W, Thuis I, et al. Modulation of the blood-brain barrier in oncology: therapeutic opportunities for the treatment of brain tumours?. Cancer Treat Rev. 2004;30(5):415-423.
18. Hynynen K, McDannold N, Vykhodtseva N, et al. Focal disruption of the blood-brain barrier due to 260-kHz ultrasound bursts: a method for molecular imaging and targeted drug delivery. J Neurosurg. 2006;105(3):445-454.
19. Etame AB, Diaz RJ, Smith CA, et al. Focused ultrasound disruption of the blood-brain barrier: a new frontier for therapeutic delivery in molecular neurooncology. Neurosurg Focus. 2012;32(1):E3.
20. Aryal M, Arvanitis CD, Alexander PM, McDannold N. Ultrasound-mediated blood-brain barrier disruption for targeted drug delivery in the central nervous system. Adv Drug Deliv Rev. 2014;72C:94-109.
21. McDannold N, King RL, Hynynen K. MRI monitoring of heating produced by ultrasound absorption in the skull: in vivo study in pigs. Magn Reson Med. 2004;51(5):1061-1065.
22. Ting CY, Fan CH, Liu HL, et al. Concurrent blood-brain barrier opening and local drug delivery using drug-carrying microbubbles and focused ultrasound for brain glioma treatment. Biomaterials. 2012;33(2):704-712.
23. Liu HL, Hua MY, Chen PY, et al. Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment. Radiology. 2010;255(2):415-425.
24. Liu H-L, Huang C-Y, Chen J-Y, et al. Pharmacodynamic and therapeutic investigation of focused ultrasound-induced blood-brain barrier opening for enhanced temozolomide delivery in glioma treatment. PLoS One. 2014;9(12):e114311-E114311.
25. Fan CH, Liu HL, Huang CY, et al. Detection of intracerebral hemorrhage and transient blood-supply shortage in focusedultrasound-induced blood-brain barrier disruption by ultrasound imaging. Ultrasound Med Biol. 2012;38(8):1372-1382.
26. Fan C-H, Ting C-Y, Chang Y-C, et al. Acta Biomaterialia Drug-loaded bubbles with matched focused ultrasound excitation for concurrent blood-brain barrier opening and brain-Tumor drug delivery. Acta Biomater. 2015;15:89-101.
27. Nakano S, Matsukado K, Black KL. Increased brain tumor microvessel permeability after intracarotid bradykinin infusion is mediated by nitric oxide. Cancer Res. 1996;56(17):4027-4031.
28. Inamura T, Black KL. Bradykinin selectively opens blood-Tumor barrier in experimental brain tumors. J Cereb Blood Flow Metab. 1994;14(5):862-870.
29. Kroll RA, Pagel MA, Muldoon LL, et al. Improving drug delivery to intracerebral tumor and surrounding brain in a rodent model: a comparison of osmotic versus bradykinin modification of the blood-brain and/or blood-Tumor barriers. Neurosurgery. 1998; 43(4):879-886; discussion 886-889.
30. Doctrow SR, Abelleira SM, Curry LA, et al. The bradykinin analog RMP-7 increases intracellular free calcium levels in rat brain microvascular endothelial cells. J Pharmacol Exp Ther. 1994; 271(1):229-237.
31. Borlongan CV, Emerich DF. Facilitation of drug entry into the CNS via transient permeation of blood brain barrier: laboratory and preliminary clinical evidence from bradykinin receptor agonist, Cereport. Brain Res Bull. 2003;60(3):297-306.
32. Elliott PJ, Hayward NJ, Dean RL, et al. Intravenous RMP-7 selectively increases uptake of carboplatin into rat brain tumors. Cancer Res. 1996;56(17):3998-4005.
33. Prados MD, Schold SJS, Fine HA, et al. 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. Neuro Oncol. 2003;5(2):96-103.
34. Argaw AT, Gurfein BT, Zhang Y, et al. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci U S A. 2009;106(6):1977-1982.
35. Wang W, Dentler WL, Borchardt RT. VEGF increases BMEC monolayer permeability by affecting occludin expression and tight junction assembly. Am J Physiol Heart Circ Physiol. 2001; 280(1):H434-H440.
36. Alvarez JI, Dodelet-Devillers A, Kebir H, et al. The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science. 2011;334(6063):1727-1731.
37. Agarwal S, Hartz AM, Elmquist WF, Bauer B. Breast cancer resistance protein and P-glycoprotein in brain cancer: two gatekeepers team up. Curr Pharm Des. 2011;17(26):2793-2802.
38. Vlieghe P, Khrestchatisky M. Medicinal chemistry based approaches and nanotechnology-based systems to improve CNS drug targeting and delivery. Med Res Rev. 2013;33(3):457-516.
39. Takasato Y, Rapoport SI, Smith QR. An in situ brain perfusion technique to study cerebrovascular transport in the rat. Am J Physiol. 1984;247(3 Pt 2):H484-H493.
40. Heffron TP, Salphati L, Alicke B, et al. The design and identification of brain penetrant inhibitors of phosphoinositide 3-kinase alpha. J Med Chem. 2012;55(18):8007-8020.
41. Drappatz J, Brenner A, Wong ET, et al. Phase I study of GRN1005 in recurrent malignant glioma. Clin Cancer Res. 2013;19(6): 1567-1576.
42. Wen PY, Lee EQ, Reardon DA, et al. Current clinical development of PI3K pathway inhibitors in glioblastoma. Neuro Oncol. 2012;14(7): 819-829.
43. Demeule M, Shedid D, Beaulieu E, et al. Expression of multidrug-resistance P-glycoprotein (MDR1) in human brain tumors. Int J Cancer. 2001;93(1):62-66.
44. Agarwal S, Sane R, Gallardo JL, et al. 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. 2010;334(1):147-155.
45. Minocha M, Khurana V, Qin B, et al. Co-Administration strategy to enhance brain accumulation of vandetanib by modulating P-glycoprotein (P-gp/Abcb1) and breast cancer resistance protein (Bcrp1/Abcg2) mediated efflux with m-TOR inhibitors. Int J Pharm. 2012;434(1-2):306-314.
46. Agarwal S, Manchanda P, Vogelbaum MA, et al. Function of the blood-brain barrier and restriction of drug delivery to invasive glioma cells: findings in an orthotopic rat xenograft model of glioma. Drug Metab Dispos. 2013;41(1):33-39.
47. Sasongko L, Link JM, Muzi M, et al. Imaging P-glycoprotein transport activity at the human blood-brain barrier with positron emission tomography. Clin Pharmacol Ther. 2005;77(6):503-514.
48. Wagner CC, Bauer M, Karch R, et al. A pilot study to assess the efficacy of tariquidar to inhibit P-glycoprotein at the human blood-brain barrier with (R)-11C-verapamil and PET. J Nucl Med. 2009;50(12):1954-1961.
49. Planting AS, Sonneveld P, van der Gaast A, et al. A phase I and pharmacologic study of the MDR converter GF120918 in combination with doxorubicin in patients with advanced solid tumors. Cancer Chemother Pharmacol. 2005;55:91-99.
50. Kuppens IELM, Witteveen EO, Jewell RC, et al. A phase I, randomized, open-label, parallel-cohort, dose-finding study of elacridar (GF120918) and oral topotecan in cancer patients. Clin Cancer Res. 2007;13(11):3276-3285.
51. Groothuis DR, Ward S, Itskovich AC, et al. Comparison of 14Csucrose delivery to the brain by intravenous, intraventricular, and convection-Enhanced intracerebral infusion. J Neurosurg. 1999;90(2):321-331.
52. Bobo RH, Laske DW, Akbasak A, et al. Convection-Enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci U S A. 1994;91(6):2076-2080.
53. Ding D, Kanaly CW, Bigner DD, et al. Convection-Enhanced delivery of free gadolinium with the recombinant immunotoxin MR1-1. J Neurooncol. 2010;98(1):1-7.
54. Serwer LP, James CD. Challenges in drug delivery to tumors of the central nervous system: an overview of pharmacological and surgical considerations. Adv Drug Deliv Rev. 2012;64(7):590-597.
55. Bogdahn U, Hau P, Stockhammer G, et al. Targeted therapy for high-grade glioma with the TGF-beta2 inhibitor trabedersen: results of a randomized and controlled phase IIb study. Neuro Oncol. 2011;13(1):132-142.
56. Groothuis DR. The blood-brain and blood-Tumor barriers: a review of strategies for increasing drug delivery. Neuro Oncol. 2000;2(1):45-59.
57. Duntze J, Litre CF, Eap C, et al. Implanted carmustinewafers followed by concomitant radiochemotherapy to treat newly diagnosed malignant gliomas: prospective, observational, multicenter study on 92 cases. Ann Surg Oncol. 2013;20(6):2065-2072.
58. Bhatia G, Lau ME, Gulur P, Koury KM. Intrathecal drug delivery (ITDD) systems for cancer pain. F1000 Res. 2013;2:96.
59. Herve F, Ghinea N, Scherrmann JM. CNS delivery via adsorptive transcytosis. AAPS J. 2008;10(3):455-472.
60. Blasi P, Giovagnoli S, Schoubben A, et al. Solid lipid nanoparticles for targeted brain drug delivery. Adv Drug Deliv Rev. 2007;59(6): 454-477.
61. Cirpanli Y, Allard E, Passirani C, et al. Antitumoral activity of camptothecin-loaded nanoparticles in 9L rat glioma model. Int J Pharm. 2011;403(1-2):201-206.
62. Battaglia L, Gallarate M, Peira E, et al. Solid lipid nanoparticles for potential doxorubicin delivery in glioblastoma treatment: preliminary in vitro studies. J Pharm Sci. 2014;103(7):2157-2165.
63. Scherrmann JM. Drug delivery to brain via the blood-brain barrier. Vascul Pharmacol. 2002;38(6):349-354.
64. Rousselle C, Clair P, Lefauconnier JM, et al. New advances in the transport of doxorubicin through the blood-brain barrier by a peptide vector-mediated strategy. Mol Pharmacol. 2000;57(4):679-686.
65. Agarwal S, Sane R, Ohlfest JR, Elmquist WF. The role of the breast cancer resistance protein (ABCG2) in the distribution of sorafenib to the brain. J Pharmacol Exp Ther. 2011;336(1):223-233.
66. Lagas JS, van Waterschoot RA, Sparidans RW, Wagenaar E, Beijnen JH, Schinkel AH. Breast cancer resistance protein and Pglycoprotein limit sorafenib brain accumulation. Mol Cancer Ther. 2010;9(2):319-326.
67. Minocha M, Khurana V, Qin B, Pal D, Mitra AK. Enhanced brain accumulation of pazopanib by modulating P-gp and Bcrp1 mediated efflux with canertinib or erlotinib. Int J Pharm. 2012; 436(1-2):127-134.
68. Lagas JS, van Waterschoot RA, van Tilburg VA, et al. 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. 2009; 15(7):2344-2351.
69. Tang SC, Lagas JS, Lankheet NA, et al. Brain accumulation of sunitinib is restricted by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by oral elacridar and sunitinib coadministration. Int J Cancer J Int Cancer. 2012;130(1):223-233.
70. Oberoi RK, Mittapalli RK, Elmquist WF. Pharmacokinetic assessment of efflux transport in sunitinib distribution to the brain. J Pharmacol Exp Ther. 2013;347(3):755-764.
71. Dai H, Marbach P, Lemaire M, Hayes M, ElmquistWF. Distribution of STI-571 to the brain is limited by P-glycoprotein-mediated efflux. J Pharmacol Exp Ther. 2003;304(3):1085-1092.
72. Breedveld P, Pluim D, Cipriani G, et al. The effect of Bcrp1 (Abcg2) on the in vivo pharmacokinetics and brain penetration of imatinib mesylate (Gleevec): implications for the use of breast cancer resistance protein and P-glycoprotein inhibitors to enable the brain penetration of imatinib in patients. Cancer Res. 2005;65(7): 2577-2582.
73. Bihorel S, Camenisch G, Lemaire M, Scherrmann JM. Influence of breast cancer resistance protein (Abcg2) and p-glycoprotein (Abcbla) on the transport of imatinib mesylate (Gleevec) across the mouse blood-brain barrier. J Neurochem. 2007;102(6): 1749-1757.
74. Polli JW, Olson KL, Chism JP, et al. An unexpected synergist role of P- glycoprotein and breast cancer resistance protein on the central nervous system penetration of the tyrosine kinase inhibitor lapatinib (N-{3-chloro-4-[(3- fluorobenzyl)oxy]phenyl}-6-[5-({[2-(methylsulfonyl)ethyl]amino }methyl)-2- furyl]-4-quinazolinamine; GW572016). Drug Metab Dispos. 2009;37(2):439-442.
75. Chu C, Abbara C, Noel-Hudson MS, et al. Disposition of everolimus in mdrla-/1b- mice and after a pre-Treatment of lapatinib in Swiss mice. Biochem Pharmacol. 2009;77(10):1629-1634.
76. Salphati L, Pang J, Plise EG, et al. Preclinical assessment of the absorption and disposition of the phosphatidylinositol 3-kinase/ mammalian target of rapamycin inhibitor GDC-0980 and prediction of its pharmacokinetics and efficacy in human. Drug Metab Dispos. 2012;40(9):1785-1796.
77. Salphati L, Lee LB, Pang J, Plise EG, Zhang X. Role of P-glycoprotein and breast cancer resistance protein-1 in the brain penetration and brain pharmacodynamic activity of the novel phosphatidylinositol 3-kinase inhibitor GDC-0941. Drug Metab Dispos. 2010; 38(9):1422-1426.
78. Poller B, Iusuf D, Sparidans RW, Wagenaar E, Beijnen JH, Schinkel AH. Differential impact of P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) on axitinib brain accumulation and oral plasma pharmacokinetics. Drug Metab Dispos. 2011; 39(5):729-735.
79. Wang F, Zhou F, Kruh GD, Gallo JM. Influence of blood-brain barrier efflux pumps on the distribution of vincristine in brain and brain tumors. Neuro Oncol. 2010;12(10):1043-1049.
80. Pawlowski KM, Mucha J, Majchrzak K, Motyl T, Krol M. Expression and role of PGP, BCRP, MRP1 and MRP3 in multidrug resistance of canine mammary cancer cells. BMC Vet Res. 2013;9:119-119.
81. van Asperen J, van Tellingen O, Tijssen F, Schinkel aH, Beijnen JH. Increased accumulation of doxorubicin and doxorubicinol in cardiac tissue of mice lacking mdrla P-glycoprotein. Br J Cancer. 1999;79:108-113.
82. Kemper EM, Van Zandbergen aE, Cleypool C, et al. Increased penetration of paclitaxel into the brain by inhibition of Pglycoprotein. Clin Cancer Res. 2003;9(July):2849-2855.
83. Goldwirt L, Beccaria K, Carpentier A, Farinotti R, Fernandez C. Irinotecan and temozolomide brain distribution: a focus on ABCB1. Cancer Chemother Pharmacol. 2014;74:185-193.
84. DeVries Na, Zhao J, Kroon E, Buckle T, Beijnen JH, Van Tellingen O. P-glycoprotein and breast cancer resistance protein: Two dominant transporters working together in limiting the brain penetration of topotecan. Clin Cancer Res. 2007;13(11): 6440-6449.