The blood-brain barrier: Its influence in the treatment of brain tumor metastases

Current Cancer Drug Targets

Volumn 12, Issue 3, 2012, Pages 247-259

  Fortin, D ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Blood brain barrier; Blood brain barrier disruption; Brain metastases; Chemotherapy

Indexed keywords

BEVACIZUMAB; DAUNORUBICIN; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; ESTRAMUSTINE; ETOPOSIDE; FLUORESCEIN; IDARUBICIN; LAPATINIB; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR; RITUXIMAB; TEMOZOLOMIDE; TOPOTECAN; TRASTUZUMAB; VASCULOTROPIN; VINCRISTINE;

ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN ANGIOGRAPHY; BRAIN METASTASIS; BRAIN RADIATION; BRAIN TUMOR BARRIER; CANCER CHEMOTHERAPY; CANCER INCIDENCE; CANCER PALLIATIVE THERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SURVIVAL; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CEREBROSPINAL FLUID LEVEL; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG INHIBITION; DRUG PENETRATION; DRUG RESPONSE; DRUG TRANSPORT; FLUORESCENCE ANGIOGRAPHY; GLIOBLASTOMA; GLIOMA; HUMAN; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; MICROANGIOGRAPHY; MICROGLIA; MULTICENTER STUDY (TOPIC); NONHUMAN; PERMEABILITY BARRIER; PHASE 2 CLINICAL TRIAL (TOPIC); POST TREATMENT SURVIVAL; PROGRESSION FREE SURVIVAL; RADIATION DOSE; REVIEW; SEDENTARY LIFESTYLE; SYSTEMIC THERAPY; TUMOR MICROENVIRONMENT; UNITED STATES;

EID: 84857127841     PISSN: 15680096     EISSN: 18735576     Source Type: Journal    
DOI: 10.2174/156800912799277511     Document Type: Review

References (86)

1. Van Den Bent, M. J. The role of chemotherapy in brain metastases. Eur. J. Cancer 2003, 39 (15), 2114-2120.
2. Provenzale, J. M.; Mukundan, S.; Dewhirst, M. The role of blood-brain barrier permeability in brain tumor imaging and therapeutics. Am. J. Roentgenol. 2005, 185 (3), 763-767.
3. Rapoport, S. I.; Hori, M.; Klatzo I. Testing of a hypothesis for osmotic opening of the blood-brain barrier. Am. J. Physiol. 1972, 223 (2), 323-331.
4. Kroll, R. A.; Neuwelt, E. A. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery 1998, 42 (5), 1083-99; discussion 1099-1100.
5. Tosoni, A.; Ermani, M.; Brandes, A. A. The pathogenesis and treatment of brain metastases: a comprehensive review. Crit. Rev.Oncol. Hematol. 2004, 52, 199-215.
6. Sato, S.; Kawase, T.; Harada, S.; Takayama, H.; Suga, S. Effect of hyperosmotic solutions on human brain tumour vasculature. Acta Neurochir. 1998, 140 (11), 1135-1141, disc 1141-1142.
7. Bellavance, M. A.; Blanchette, M.; Fortin, D. Recent advances in blood-brain barrier disruption as a CNS delivery strategy. AAPS J. 2008, 10 (1), 166-177.
8. Lockman, P. R.; Mittapalli, R. K.; Taskar, K. S.; Rudraraju, V.; Gril, B.; Bohn, K. A.; Adkins, C. E.; Roberts, A.; Thorsheim, H. R.; Gaasch, J. A.; Huang, S.; Palmieri, D.; Steeg, P. S.; Smith, Q. R. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin. Cancer Res. 2010, 16 (23), 5664-5678.
9. Fortin, D.; Desjardins, A.; Benko, A.; Niyonsega, T.; Boudrias, M. Enhanced chemotherapy delivery by intraarterial infusion and blood-brain barrier disruption in malignant brain tumors. Cancer 2005, 103 (12), 2606-2615.
10. Weil, R. J.; Palmieri, D. C.; Bronder, J. L.; Stark, A. M.; Steeg, P. S. Breast cancer metastasis to the entral nervous system. Am J. Pathol. 2005, 167 (4), 913-920.
11. Patchell, R. A. The management of brain metastasis. Cancer Treat. Rev. 2003, 29 (6), 533-540.
12. Soffietti, R.; Ruda, R.; Mutani, R. Management of brain metastases. J. Neurol. 2002, 249 (10), 1357-1369.
13. Gavrilovic, I. T.; Posner, J. B. Brain metastases: epidemiology and pathophysiology. J. Neurooncol. 2005, 75 (1), 5-14.
14. Gril, B.; Evans, L.; Palmieri, D.; Steeg, P. S. Translational research in brain metastasis is identifying molecular pathways that may lead to the development of new therapeutic strategies. Eur. J. Cancer 2010, 46 (7), 1204-1210.
15. Smedby, K. E.; Brandt, L.; Bäcklund, M. L.; Blomqvist, P. Brain metastases admissions in sweden between 1987 and 2006. Br. J. Cancer 2009, 101 (11), 1919-1924.
16. Lin, A.; Rugo, H. S. The role of trastuzumab in early stage breast cancer: current data and treatment recommendations. Curr. Treat. Options Oncol. 2007, 8 (1), 47-60.
17. Omuro, A. M.; Kris, M. G.; Miller, V. A.; Franceschi, E.; Shah, N.; Milton, D. T.; Abrey, L. E. High incidence of disease recurrence in the brain and leptomeninges in patients with nonsmall cell lung carcinoma after response to gefitinib. Cancer 2005, 103 (11), 2344-2348.
18. Duffey, P.; Chari, G.; Cartlidge, N. E.; Shaw, P. J. Progressive deterioration of intellect and motor function occurring several decades after cranial irradiation: a new facet in the clinical spectrum of radiation encephalopathy. Arch. Neurol. 1996, 53, 814-818.
19. Tsao, M. N.; Sultamen, K.; Chiu, D.; Copps, F.; Dixon, P.; Easton, D.; Haddad, P.; Hayter, C.; Hoegler, D.; Wong, R. Supportive care management of brain metastases: what is known and what we need to know (NCIC). Clin. Oncol. 2003, 15, 429-434.
20. Metha, M. P.; Khuntia, D. Current strategies in whole-brain radiation therapy for brain metastases. Neurosurgery 2005, 57, s4-33-s4-44.
21. DeAngelis, L. M.; Delattre, J. Y.; Posner, J. B. Radiation-induced dementia in patients cured of brain metastases. Neurology 1989, 39, 789-796.
22. Pardridge, W. M. The blood-brain barrier: bottleneck in brain drug development. NeuroRx. 2005, 2, 3-14.
23. Stern, L.; Gautier, R. Rapports entre le liquide céphalo-rachidien et la circulation sanquine. Arch. Int. Physiol. 1921, 17, 138-192.
24. Brodie, B. B.; Kurz, H.; Schanker, L. S. The importance of dissociation constant and lipid-solubility in influencing the passage of drugs into the cerebrospinal fluid. J. Pharmacol. 1960, 130, 20-25.
25. Brightman, M. W.; Hori, M.; Rapoport, S. I.; Reese, T. S.; Westergaard, E. Osmotic opening of tight junctions in cerebral endothelium. J. Comp. Neurol. 1973, 152, 317-325.
26. Muldoon, L. L.; Nilaver, G.; Kroll, R. A.; Pagel, M. A.; Breakefield, X. O.; Chiocca, E. A.; Davidson, B. L.; Weissleder, R.; Neuwelt, E. A. Comparison of intracerebral inoculation and osmotic blood-brain barrier disruption for delivery of adenovirus, herpesvirus and iron oxide particles to normal rat brain. Am J. Pathol. 1995, 147, 1840-1851.
27. Rubin, L. L.; Staddon, J. M. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 1999, 22, 11-28.
28. Davson, H.; Oldendorf, W. H. Symposium on membrane transport. Transport in the central nervous system. Proc. R. Soc. Med. 1967, 60 (4), 326-329.
29. Cohen, Z.; Bonvento, G.; Lacombe, P.; Hamel, E. Serotonin in the regulation of brain microcirculation. Prog. Neurobiol. 1996, 50 (4), 335-362.
30. Cohen, Z.; Molinatti, G.; Hamel, E. Astroglial and vascular interactions of noradrenaline terminals in the rat cerebral cortex. J. Cereb. Blood Flow Metab. 1997, 17 (8), 894-904.
31. Fenstermacher, J.; Gross, P.; Sposito, N.; Acuff, V.; Pettersen, S.; Gruber, K. Structural and functional variations in capillary systems within the brain. Ann. N. Y. Acad. Sci. 1988, 529, 21-30.
32. Reese, T. S.; Karnovsky, M. J. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol. 1967, 34 (1), 207-217.
33. Wolburg, H.; Lippoldt, A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul. Pharmacol. 2002, 38 (6), 323-337.
34. Abbott, N. J.; Ronnback, L.; Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7 (1), 41-53.
35. Deeken, J. F.; Loscher, W. The blood-brain barrier and cancer: transporters, treatment, and trojan horses. Clin. Cancer Res. 2007, 13 (6), 1663-1674.
36. Smith, M. W.; Gumbleton, M. Endocytosis at the blood-brain barrier: from basic understanding to drug delivery strategies. J. Drug Target 2006, 14 (4), 191-214.
37. Hendry, S. H.; Jones, E. G.; Beinfeld, M. C. Cholecystokinin-immunoreactive neurons in rat and monkey cerebral cortex make symmetric synapses and have intimate associations with blood vessels. Proc. Natl. Acad. Sci. 1983, 80 (8), 2400-2404.
38. de Boer, A. G.; Gaillard, P. J. Drug targeting to the brain. Annu. Rev. Pharmacol. Toxicol. 2007, 47, 323-355.
39. Neuwelt, E. A. (ed.) Implications of the blood-brain barrier and its manipulation. Vol. 1 and 2, Plenum Press: New York, 1989.
40. Lockman, P. R.; Mittapalli, R. K.; Taskar, K. S.; Rudraraju, V.; Gril, B.; Bohn, K. A.; Adkins, C. E., Roberts, A.; Thorsheim, H. R.; Gaasch, J. A.; Huang, S.; Palmieri, D.; Steeg, P. S.; Smith, Q. R. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin. Cancer Res. 2010, 16 (23), 5664-5678.
41. Boyle, F. M.; Eller, S. L.; Grossman, S. A. Penetration of intra-arterially administered vincristine in experimental brain tumor. Neuro-oncology 2004, 6 (4), 3000-3005.
42. Blanchette, M.; Fortin, D. Blood-Brain barrier disruption in the treatment of brain tumors. Methods Mol. Biol. 2011, 686, 447-463.
43. Eichler, A. F.; Chung, E.; Kodack, D. P.; Loeffler, J. S.; Fukumura, D.; Jain, R. K. The biology of brain metastases-translation to new therapies. Nat. Rev. Clin. Onc. 2011, 6, 344-356.
44. de Boer, A. G.; van der Sandt, I. C.; Gaillard, P. J. The role of drug transporters at the blood-brain barrier. Annu. Rev. Pharmacol. Toxicol. 2003, 43, 629-656.
45. Lee, G.; Dallas, S.; Hong, M.; Bendayan, R. Drug transporters in the central nervous system: brain barriers and brain parenchyma considerations. Pharmacol. Rev. 2001, 53 (4), 569-596.
46. Loscher, W.; Potschka, H. Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog. Neurobiol. 2005, 1, 22-76.
47. Guo, Z.; Zhu, J.; Zhao, L.; Luo, Q.; Jin, X. Expression and clinical significance of multidrug resistance proteins in brain tumors. J. Exp. Clin. Canc. Res.: CR. 2010, 29-122.
48. Shen, F.; Chu, S.; Bence, A. K.; Bailey, B.; Xue, X.; Erickson, P. A.; Montrose, M. H.; Beck, W. T.; Erickson, L. C. Quantitation of doxorubicin uptake, efflux, and modulation of multidrug resistance (MDR) in MDR human cancer cells. J. Pharmacol. Exper. Ther. 2008, 324 (1), 95-102.
49. Arshad, F.; Wang, L.; Sy, C.; Avraham, S.; Avraham, H. K. Blood-Brain barrier integrity and breast cancer metastasis to the brain. Pathol. Res. Int. 2011.
50. Hu, Z.; Fan, C.; Livasy, C.; He, X.; Oh, D. S.; Ewend, M. G.; Carey, L. A.; Subramanian, S.; West, R.; Ikpatt, F.; Olopade, O. I.; van de Rijn, M.; Perou, C. M. A Compact VEGF signature associated with distant metastases and poor outcomes. BMC Med. 2009, 7, 9.
51. Huang, H.; Bhat, A.; Woodnutt, G.; Lappe, R. Targeting the ANGPT-TIE2 pathway in malignancy. Nat. Rev. Cancer 2010, 10 (8), 575-585.
52. Sfiligoi, C.; de Luca, A.; Cascone, I.; Sorbello, V.; Fuso, L.; Ponzone, R.; Biglia, N.; Audero, E.; Arisio, R.; Bussolino, F.; Sismondi, P.; de Bortoli, M. Angiopoietin-2 expression in breast cancer correlates with lymph node invasion and short survival. Int. J. Cancer 2003, 103 (4), 466-474.
53. H. Recent progress towards development of effective systemic chemotherapy for the treatment of malignant brain tumors. J. Transl. Med. 2009, 7, 77.
54. Platta, C. S.; Khuntia, D.; Mehta, M. P.; Suh, J. H. Current treatment strategies for brain metastasis and complications from therapeutic techniques: a review of current literature. Am. J. Clin.Oncol. 2010, 33 (4), 398-407.
55. Stupp, R.; Mason, W. P.; Van Den Bent, M. J.; Weller, M.; Fisher, B.; Taphoorn, M. J.; Belanger, K.; Brandes, A. A.; Marosi, C.; Bogdahn, U.; Curschmann, J.; Janzer, R. C.; Ludwin, S. K.; Gorlia, T.; Allgeier, A.; Lacombe, D.; Cairncross, J. G.; Eisenhauer, E.; Mirimanoff, R. O.; European organization for research and treatment of cancer brain tumor and radiotherapy groups; national cancer institute of Canada clinical trials group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl. J. Med. 2005, 352 (10), 987.
56. Agarwala, S. S.; Kirkwood, J. M.; Gore, M.; Dreno, B.; Thatcher, N.; Czarnetski, B.; Atkins, M.; Buzaid, A.; Skarlos, D.; Rankin, E. M. Temozolomide for the treatment of brain metastases associated with metastatic melanoma:a phase II study. J. Clin. Oncol. 2004, 22 (11), 2101-7.
57. Hofmann, M.; Kiecker, F.; Wurm, R.; Schlenger, L.; Budach, V.; Sterry, W.; Trefzer, U. Temozolomide with or without radiotherapy in melanoma with unresectable brain metastases. J. Neurooncol. 2006, 76 (1), 59-64.
58. Antonadou, D.; Paraskevaidis, M.; Sarris, G.; Coliarakis, N.; Economou, I.; Karageorgis, P.; Throuvalas, N. Phase II randomized trial of temozolomide and concurrent radiotherapy in patients with brain metastases. J. Clin. Oncol. 2002, 20 (17), 3644-50.
59. Korfel, A.; Oehm, C.; von Pawel, J.; Keppler, U.; Deppermann, M.; Kaubitsch, S.; Thiel, E. Response to topotecan of symptomatic brain metastases of small-cell lung cancer also after whole-brain irradiation. a multicentre phase II study. Eur. J. Cancer 2002, 38 (13), 1724-9.
60. Pitz, M. W.; Desai, A.; Grossman, S. A.; Blakeley, J. O. Tissue concentration of systemically administered antineoplastic agents in human brain tumors. J. Neuro-Oncology 2011, epub march.
61. Omuro, A. M.; Faivre, S.; Raymond, E. Lessons learned in the development of targeted therapy for malignant gliomas. Mol. Cancer Ther. 2007, 6 (7), 1909-19.
62. Lin, N. U.; Diéras, V.; Paul, D.; Lossignol, D.; Christodoulou, C.; Stemmler, H. J.; Roché, H.; Liu, M. C.; Greil, R.; Ciruelos, E.; Loibl, S.; Gori, S.; Wardley, A.; Yardley, D.; Brufsky, A.; Blum, J. L.; Rubin, S. D.; Dharan, B.; Steplewski, K.; Zembryki, D.; Oliva, C.; Roychowdhury, D.; Paoletti, P.; Winer, E. P. Multicenter phase II study of lapatinib in patients with brain metastases from her2-positive breast cancer. Clin. Cancer Res. 2009, 15 (4), 1452-9.
63. Clarke, J. L.; Pao, W.; Wu, N.; Miller, V. A.; Lassman, A. B. High dose weekly erlotinib achieves therapeutic concentrations in CSF and is effective in leptomeningeal metastases from epidermal growth factor receptor mutant lung cancer. J. Neurooncol. 2010, 99 (2), 283-6.
64. von Pawel, J.; Wagner, H.; Duell, T.; Poellinger, B. Erlotinib in patients with previously irradiated, recurrent brain metastases from non-small cell lung cancer: two case reports. Onkologie 2008, 31 (3), 123-6.
65. Kim, J. E.; Lee, D. H.; Choi, Y.; Yoon, D. H.; Kim, S. W.; Suh, C.; Lee, J. S. Epidermal growth factor receptor tyrosine kinase inhibitors as a first-line therapy for never-smokers with adenocarcinoma of the lung having asymptomatic synchronous brain metastasis. Lung Cancer 2009, 65 (3), 351-4.
66. Ehrlich, P. Uber die beziehungen von chemische constituion, vertheilung, und pharmakologischer wirkung. Collected studies in immunity. Repr. Transl. 1906, 567-595.
67. L. A. Monoclonal antibodies in neuro-oncology: getting past the blood-brain barrier. mAbs. 2011, 3, 2.
68. Reichel, A. Addressing central nervous system (CNS) penetration in drug discovery: basics and implications of the evolving new concept. Chem. Biodivers. 2009, 6 (11), 2030-49.
69. Roopenian, D. C.; Akilesh, S. FcRn: the neonatal fc receptor comes of age. Nat. Rev. Immunol. 2007, 7 (9), 715-25.
70. Newton, H. B.; Figg, G. M.; Slone, H. W.; Bourekas, E. Incidence of infusion plan alterations after angiography in patients undergoing intra-arterial chemotherapy for brain tumors. J. Neuro-Oncol. 2006, 78, 157-160.
71. Bradbury, M. W. B.; Suckling, A.; Rumsby, M.; Bradbury, M. Appraisal of the role of endothelial cells and glia in barrier breakdown. The Blood-Brain Barrier in Health and Disease 1986, 128-129.
72. W. M. Advances in cell biology of blood-brain barrier transport. Semin. Cell Biol. 1991, 2 (6), 419-426.
73. Smith, M. W.; Gumbleton, M. Endocytosis at the blood-brain barrier: from basic understanding to drug delivery strategies. J. Drug Target 2006,14 (4), 191-214.
74. Newton, H. B.; Slivka, M. A.; Volpi, C.; Bourekas, E. C; Christoforidis, G. A.; Baujan, M. A.; Slone, W.; Chakeres, D. W. Intra-arterial carboplatin and intravenous etoposide for the treatment of metastatic brain tumors. J. Neuro-Oncol. 2003, 61, 35-44.
75. Doolittle, N. D.; Miner, M. E. Safety and efficacy of a multicenter study using intra-arterial chemotherapy in conjunction with osmotic opening of the blood-brain barrier for the treatment of patients with malignant brain tumors. Cancer 2000, 88 (3), 637-647.
76. Fortin, D.; Gendron, C; Boudrias, M.; Garant, M, P. Enhanced chemotherapy delivery by intraarterial infusion and blood-brain barrier disruption in the treatment of cerebral metastasis. Cancer 2007, 109 (4), 751-760.
77. Blanchette, M.; Pellerin, M.; Tremblay, L.; Lepage, M.; Fortin, D. Real time monitoring of Gd-DTPA during osmotic blood brain barrier disruption using MRI in normal wistar rats. Neurosurgery 2009, 65, 344-351.
78. Hartz, A. M.; Bauer, B.; Fricker, G.; Miller, D. S. Rapid modulation of P-glycoprotein-mediated transport at the blood-brain barrier by TNF-{alpha} and LPS. Mol. Pharmacol. Epub 2005 Nov. 8.
79. Kraemer, D.; McAllister, L.; Fortin, D.; Doolittle, N.; Neuwelt, E. A. Association of drug delivery and clinical outcomes in human non-AIDS primary CNS lymphoma as a model to assess the impact of total dose intensity delivered to the CNS. Neurosurgery 2001, 48, 1033-1041.
80. Côté, J.; Savard, M.; Bovenzi, V.; Dubuc, C; Tremblay, L.; Tsanaclis, A. M.; Lepage, M.; Fortin, D.; Gobeil, F. Selective tumor blood-brain barrier opening with the kinin B2 receptor agonist [Phe8ψ(Ch2nh)Arg9]-BK in a F98 glioma rat model: an MRI study. Neuropeptides 2010, 44 (2), 177-185.
81. Charest, G.; Paquette, B.; Fortin, D.; Mathieu, D.; Sanche, L. Concomitant treatment of F98 glioma cells with new liposomal platinum compounds and ionizing radiation. J. Neurooncol. 2010, 97, 187-193.
82. Bellavance, M. A.; Poirier, M. B.; Fortin, D. Uptake and intracellular release kinetics of liposome formulations in glioma cells. Int. J. Pharm. 2010, 395, 251-259.
83. Rubin, P.; Gash, D. M.; Hansen, J. T.; Nelson, D. F.; Williams, J. P. Disruption of the blood-brain barrier as the primary effect of CNS irradiation. Radiother. Oncol. 1994, 31, 51-60.
84. Reinhold, H. S.; Calvo, W.; Hopewell, J. W.; van der Berg, A.P. Development of blood vessel-related radiation damage in the fimbria of the central nervous system. Int. J. Radiat. Oncol. Biol. Phys. 1990,18, 37-42.
85. Bart, J.; Nagengast, W. B.; Coppes, R. P.; Wegman, T. D.; van der Graaf, W. T. A.; Groen, H. J. M.; Vaalburg, W.; de Vries, E. G.; Hendrikse, N. H. Irradiation of rat brain reduces P-Glycoprotein expression and function. Brit. J. Cancer 2007, 97 (3), 322-326.
86. Mima, T.; Toyonaga, S.; Mori, K.; Taniguchi, T.; Ogawa, Y. Early decrease of P-Glycoprotein in the endothelium of the rat brain capillaries after moderate dose of irradiation. Neurol. Res. 1999, 21, 209.