Temporary blood–brain barrier disruption by low intensity pulsed ultrasound increases carboplatin delivery and efficacy in preclinical models of glioblastoma
Introduction Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood–brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to...
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| Published in | Journal of neuro-oncology Vol. 144; no. 1; pp. 33 - 41 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Springer US
01.08.2019
Springer Nature B.V Springer Verlag |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0167-594X 1573-7373 1573-7373 |
| DOI | 10.1007/s11060-019-03204-0 |
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| Abstract | Introduction
Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood–brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models.
Methods
First, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival.
Results
Carboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity.
Conclusions
Carboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach. |
|---|---|
| AbstractList | Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood-brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models.INTRODUCTIONGlioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood-brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models.First, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival.METHODSFirst, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival.Carboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity.RESULTSCarboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity.Carboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach.CONCLUSIONSCarboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach. Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood-brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models. First, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival. Carboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity. Carboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach. INTRODUCTION: Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood-brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models.METHODS: First, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival.RESULTS: Carboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity.CONCLUSIONS: Carboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach. IntroductionGlioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood–brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models.MethodsFirst, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival.ResultsCarboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity.ConclusionsCarboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach. Introduction Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM, due in part to the presence of the blood–brain barrier (BBB), which reduces the penetration of chemotherapies from the blood to the brain. Ultrasound-induced BBB opening (US-BBB) has been shown to increase the penetration of multiple chemotherapeutic agents in the brain in animal models. In the current study, the anti-tumor activity of carboplatin chemotherapy with and without US-BBB was investigated in several GBM mouse models. Methods First, the IC50 of two commercial (U87 and U251) and six patient-derived GBM cell lines (PDCL) to carboplatin was measured. Next, U87 was subcutaneously grafted to a nude mouse model to test the in vivo response of the tumor to carboplatin in the absence of the BBB. Lastly, nude mice bearing orthotopically xenografted GBM cell lines (U87 or a PDCL) were randomized to four experimental groups: (i) untreated, (ii) US-BBB alone, (iii) carboplatin alone and, (iv) carboplatin + US-BBB. Mice were treated once weekly for 4 weeks and monitored for toxicity, tumor growth, and survival. Results Carboplatin plus US-BBB enhanced survival (p = 0.03) and delayed tumor growth (p < 0.05) of GBM-bearing mice compared to carboplatin alone, with a 4.2-fold increase of carboplatin penetration in the brain, without evidence of significant neurological or systemic toxicity. Conclusions Carboplatin efficacy was enhanced in GBM mouse models with US-BBB and appears to be a promising chemotherapy for this approach. |
| Author | Carpentier, Alexandre Canney, Michael Goli, Larissa Bouchoux, Guillaume Idbaih, Ahmed Schmitt, Charlotte Sottilini, Frédéric Bouzidi, Amira Sanson, Marc Guehennec, Jeremy Lemaire, Nolwenn Verreault, Maïté Delattre, Jean-Yves Mokhtari, Karima Goldwirt, Lauriane Dréan, Antonin |
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| Keywords | Carboplatin Ultrasound Glioblastoma Blood–brain barrier |
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| References | Sheikov, McDannold, Vykhodtseva (CR7) 2004; 30 Carpentier, Canney, Vignot (CR15) 2016 Yang, Horng (CR18) 2013; 04 Rosenberg, Verreault, Schmitt (CR20) 2016 Hynynen, McDannold, Vykhodtseva, Jolesz (CR5) 2001; 220 Prados, Warnick, Mack (CR24) 1996; 19 Horodyckid, Canney, Vignot (CR12) 2017; 126 Ostrom, Bauchet, Davis (CR1) 2014; 16 Raymond, Skoch, Hynynen, Bacskai (CR6) 2007; 27 Aryal, Vykhodtseva, Zhang (CR17) 2013; 169 McDannold, Arvanitis, Vykhodtseva, Livingstone (CR14) 2012; 72 Agarwal, Manchanda, Vogelbaum (CR21) 2013; 41 Treat, McDannold, Zhang (CR10) 2012; 38 Beccaria, Canney, Goldwirt (CR8) 2015 Shin, Kong, Cho (CR22) 2018; 44 Vanderbeek, Rahman, Fell (CR3) 2018; 20 Dréan, Goldwirt, Verreault (CR4) 2016 Goldwirt, Canney, Horodyckid (CR9) 2016; 77 Downs, Buch, Sierra (CR13) 2015; 10 Chen, Liu, Hua (CR11) 2010; 12 Stupp, Mason, van den Bent (CR2) 2005; 352 Idbaih, Canney, Belin (CR16) 2019 White, Bienemann, Taylor (CR23) 2012; 33 Kovacs, Werner, Rassi (CR19) 2014; 187 K Hynynen (3204_CR5) 2001; 220 R Stupp (3204_CR2) 2005; 352 A Idbaih (3204_CR16) 2019 F-Y Yang (3204_CR18) 2013; 04 J Shin (3204_CR22) 2018; 44 Z Kovacs (3204_CR19) 2014; 187 N Sheikov (3204_CR7) 2004; 30 A Carpentier (3204_CR15) 2016 S Rosenberg (3204_CR20) 2016 LH Treat (3204_CR10) 2012; 38 ME Downs (3204_CR13) 2015; 10 AM Vanderbeek (3204_CR3) 2018; 20 L Goldwirt (3204_CR9) 2016; 77 C Horodyckid (3204_CR12) 2017; 126 MD Prados (3204_CR24) 1996; 19 P-Y Chen (3204_CR11) 2010; 12 M Aryal (3204_CR17) 2013; 169 S Agarwal (3204_CR21) 2013; 41 QT Ostrom (3204_CR1) 2014; 16 A Dréan (3204_CR4) 2016 SB Raymond (3204_CR6) 2007; 27 K Beccaria (3204_CR8) 2015 E White (3204_CR23) 2012; 33 N McDannold (3204_CR14) 2012; 72 |
| References_xml | – volume: 220 start-page: 640 year: 2001 end-page: 646 ident: CR5 article-title: Noninvasive MR imaging-guided focal opening of the blood–brain barrier in rabbits publication-title: Radiology doi: 10.1148/radiol.2202001804 – volume: 41 start-page: 33 year: 2013 end-page: 39 ident: CR21 article-title: Function of the blood–brain barrier and restriction of drug delivery to invasive glioma cells: findings in an orthotopic rat xenograft model of glioma publication-title: Drug Metab Dispos Biol Fate Chem doi: 10.1124/dmd.112.048322 – volume: 77 start-page: 211 year: 2016 end-page: 216 ident: CR9 article-title: Enhanced brain distribution of carboplatin in a primate model after blood–brain barrier disruption using an implantable ultrasound device publication-title: Cancer Chemother Pharmacol doi: 10.1007/s00280-015-2930-5 – volume: 33 start-page: 320 year: 2012 end-page: 331 ident: CR23 article-title: A phase I trial of carboplatin administered by convection-enhanced delivery to patients with recurrent/progressive glioblastoma multiforme publication-title: Contemp Clin Trials doi: 10.1016/j.cct.2011.10.010 – volume: 44 start-page: E15 year: 2018 ident: CR22 article-title: Focused ultrasound–mediated noninvasive blood–brain barrier modulation: preclinical examination of efficacy and safety in various sonication parameters publication-title: Neurosurg Focus doi: 10.3171/2017.11.FOCUS17627 – volume: 187 start-page: 74 year: 2014 end-page: 82 ident: CR19 article-title: Prolonged survival upon ultrasound-enhanced doxorubicin delivery in two syngenic glioblastoma mouse models publication-title: J Control Release doi: 10.1016/j.jconrel.2014.05.033 – volume: 352 start-page: 987 year: 2005 end-page: 996 ident: CR2 article-title: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma publication-title: N Engl J Med doi: 10.1056/NEJMoa043330 – volume: 12 start-page: 1050 year: 2010 end-page: 1060 ident: CR11 article-title: Novel magnetic/ultrasound focusing system enhances nanoparticle drug delivery for glioma treatment publication-title: Neuro-Oncol doi: 10.1093/neuonc/noq054 – year: 2016 ident: CR15 article-title: Clinical trial of blood–brain barrier disruption by pulsed ultrasound publication-title: Sci Transl Med doi: 10.1126/scitranslmed.aaf6086 – volume: 19 start-page: 609 year: 1996 end-page: 612 ident: CR24 article-title: Intravenous carboplatin for recurrent gliomas. 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ultrasound in rat glioma publication-title: Ultrasound Med Biol doi: 10.1016/j.ultrasmedbio.2012.04.015 – volume: 169 start-page: 103 year: 2013 end-page: 111 ident: CR17 article-title: Multiple treatments with liposomal doxorubicin and ultrasound-induced disruption of blood-tumor and blood–brain barriers improve outcomes in a rat glioma model publication-title: J Control Release Off J Control Release Soc doi: 10.1016/j.jconrel.2013.04.007 – volume: 27 start-page: 393 year: 2007 end-page: 403 ident: CR6 article-title: Multiphoton imaging of ultrasound/optison mediated cerebrovascular effects in vivo publication-title: J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab doi: 10.1038/sj.jcbfm.9600336 – volume: 30 start-page: 979 year: 2004 end-page: 989 ident: CR7 article-title: Cellular mechanisms of the blood–brain barrier opening induced by ultrasound in presence of microbubbles publication-title: Ultrasound Med Biol doi: 10.1016/j.ultrasmedbio.2004.04.010 – volume: 72 start-page: 3652 year: 2012 end-page: 3663 ident: CR14 article-title: Temporary disruption of the blood–brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques publication-title: Cancer Res doi: 10.1158/0008-5472.CAN-12-0128 – volume: 16 start-page: 896 year: 2014 end-page: 913 ident: CR1 article-title: The epidemiology of glioma in adults: a “state of the science” review publication-title: Neuro-Oncol doi: 10.1093/neuonc/nou087 – year: 2016 ident: CR20 article-title: Multi-omics analysis of primary glioblastoma cell lines shows recapitulation of pivotal molecular features of parental tumors publication-title: Neuro-Oncol doi: 10.1093/neuonc/now160 – volume: 220 start-page: 640 year: 2001 ident: 3204_CR5 publication-title: Radiology doi: 10.1148/radiol.2202001804 – year: 2016 ident: 3204_CR4 publication-title: Expert Rev Neurother doi: 10.1080/14737175.2016.1202761 – volume: 16 start-page: 896 year: 2014 ident: 3204_CR1 publication-title: 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| Snippet | Introduction
Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective... Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective against GBM,... IntroductionGlioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective... INTRODUCTION: Glioblastoma (GBM) is the most common and aggressive primary brain cancer in adults. Few cytotoxic chemotherapies have been shown to be effective... |
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| SubjectTerms | Animal models Animals Antineoplastic Agents - pharmacokinetics Antineoplastic Agents - pharmacology Antitumor agents Apoptosis Blood-brain barrier Blood-Brain Barrier - drug effects Blood-Brain Barrier - metabolism Blood-Brain Barrier - radiation effects Brain cancer Brain Neoplasms - drug therapy Brain Neoplasms - metabolism Brain Neoplasms - pathology Cancer Carboplatin Carboplatin - pharmacokinetics Carboplatin - pharmacology Cell Proliferation Chemotherapy Cytotoxicity Disease Models, Animal Female Glioblastoma Glioblastoma - drug therapy Glioblastoma - metabolism Glioblastoma - pathology Humans Laboratory Investigation Life Sciences Medicine Medicine & Public Health Mice Mice, Nude Neurobiology Neurology Neurons and Cognition Oncology Pharmaceutical sciences Pharmacology Tissue Distribution Tumor Cells, Cultured Ultrasonic imaging Ultrasonic Waves Ultrasound Xenograft Model Antitumor Assays Xenografts |
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| Title | Temporary blood–brain barrier disruption by low intensity pulsed ultrasound increases carboplatin delivery and efficacy in preclinical models of glioblastoma |
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