Magnetic resonance imaging analysis predicts nanoparticle concentration delivered to the brain parenchyma.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
15 09 2022
15 09 2022
Historique:
received:
21
02
2022
accepted:
23
08
2022
entrez:
15
9
2022
pubmed:
16
9
2022
medline:
20
9
2022
Statut:
epublish
Résumé
Ultrasound in combination with the introduction of microbubbles into the vasculature effectively opens the blood brain barrier (BBB) to allow the passage of therapeutic agents. Increased permeability of the BBB is typically demonstrated with small-molecule agents (e.g., 1-nm gadolinium salts). Permeability to small-molecule agents, however, cannot reliably predict the transfer of remarkably larger molecules (e.g., monoclonal antibodies) required by numerous therapies. To overcome this issue, we developed a magnetic resonance imaging analysis based on the ΔR
Identifiants
pubmed: 36109574
doi: 10.1038/s42003-022-03881-0
pii: 10.1038/s42003-022-03881-0
pmc: PMC9477799
doi:
Substances chimiques
Antibodies, Monoclonal
0
Liposomes
0
Salts
0
Gadolinium
AU0V1LM3JT
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
964Informations de copyright
© 2022. The Author(s).
Références
Sukovich, J. R. et al. In vivo histotripsy brain treatment. J. Neurosurg. 131, 1331–1338 (2018).
doi: 10.3171/2018.4.JNS172652
Naor, O., Krupa, S. & Shoham, S. Ultrasonic neuromodulation. J. Neural Eng. 13, 031003 (2016).
pubmed: 27153566
doi: 10.1088/1741-2560/13/3/031003
Plaksin, M., Shoham, S. & Kimmel, E. Intramembrane cavitation as a predictive bio-piezoelectric mechanism for ultrasonic brain stimulation. Phys. Rev. X 4, 011004 (2014).
Plaksin, M., Kimmel, E. & Shoham, S. Cell-type-selective effects of intramembrane cavitation as a unifying theoretical framework for ultrasonic neuromodulation. eNeuro 3, ENEURO.0136–15.2016 (2016).
Aryal, M., Vykhodtseva, N., Zhang, Y.-Z. & McDannold, N. Multiple sessions of liposomal doxorubicin delivery via focused ultrasound mediated blood–brain barrier disruption: a safety study. J. Control. Release 204, 60–69 (2015).
pubmed: 25724272
pmcid: 4385501
doi: 10.1016/j.jconrel.2015.02.033
Meng, Y. et al. MR-guided focused ultrasound enhances delivery of trastuzumab to Her2-positive brain metastases. Sci. Transl. Med. 13, eabj4011 (2021).
pubmed: 34644145
doi: 10.1126/scitranslmed.abj4011
Kinoshita, M., McDannold, N., Jolesz, F. A. & Hynynen, K. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood–brain barrier disruption. Proc. Natl. Acad. Sci. USA 103, 11719–11723 (2006).
pubmed: 16868082
pmcid: 1544236
doi: 10.1073/pnas.0604318103
Pardridge, W. M. The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2, 3–14 (2005).
pubmed: 15717053
pmcid: 539316
doi: 10.1602/neurorx.2.1.3
Tung, Y.-S., Vlachos, F., Feshitan, J. A., Borden, M. A. & Konofagou, E. E. The mechanism of interaction between focused ultrasound and microbubbles in blood-brain barrier opening in mice. J. Acoust. Soc. Am. 130, 3059–3067 (2011).
pubmed: 22087933
pmcid: 3248062
doi: 10.1121/1.3646905
Konofagou, E. E. Optimization of the ultrasound-induced blood-brain barrier opening. Theranostics 2, 1223 (2012).
pubmed: 23382778
pmcid: 3563154
doi: 10.7150/thno.5576
Jahangiri, A. et al. Convection-enhanced delivery in glioblastoma: a review of preclinical and clinical studies. J. Neurosurg. 126, 191–200 (2017).
pubmed: 27035164
doi: 10.3171/2016.1.JNS151591
Yang, W. et al. Radiation therapy combined with intracerebral administration of carboplatin for the treatment of brain tumors. Radiat. Oncol. 9, 1–9 (2014).
doi: 10.1186/1748-717X-9-25
Lidar, Z. et al. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study. J. Neurosurg. 100, 472–479 (2004).
pubmed: 15035283
doi: 10.3171/jns.2004.100.3.0472
Bruinsmann, F. A. et al. Nasal drug delivery of anticancer drugs for the treatment of glioblastoma: preclinical and clinical trials. Molecules 24, 4312 (2019).
pmcid: 6930669
doi: 10.3390/molecules24234312
Da Fonseca, C. O. et al. Preliminary results from a phase I/II study of perillyl alcohol intranasal administration in adults with recurrent malignant gliomas. Surg. Neurol. 70, 259–266 (2008).
pubmed: 18295834
doi: 10.1016/j.surneu.2007.07.040
Da Fonseca, C. O. et al. Efficacy of monoterpene perillyl alcohol upon survival rate of patients with recurrent glioblastoma. J. Cancer Res. Clin. Oncol. 137, 287–293 (2011).
pubmed: 20401670
doi: 10.1007/s00432-010-0873-0
Bradley, M. O. et al. Tumor targeting by covalent conjugation of a natural fatty acid to paclitaxel. Clin. Cancer Res. 7, 3229–3238 (2001).
pubmed: 11595719
Agarwal, S., Hartz, A. M. S., Elmquist, W. F. & Bauer, B. Breast cancer resistance protein and P-glycoprotein in brain cancer: two gatekeepers team up. Curr. Pharm. Des. 17, 2793–2802 (2011).
pubmed: 21827403
pmcid: 3269897
doi: 10.2174/138161211797440186
Bankstahl, J. P. et al. Tariquidar and elacridar are dose-dependently transported by P-glycoprotein and Bcrp at the blood-brain barrier: a small-animal positron emission tomography and in vitro study. Drug Metab. Dispos. 41, 754–762 (2013).
pubmed: 23305710
doi: 10.1124/dmd.112.049148
Wang, D., Wang, C., Wang, L. & Chen, Y. A comprehensive review in improving delivery of small-molecule chemotherapeutic agents overcoming the blood-brain/brain tumor barriers for glioblastoma treatment. Drug Deliv. 26, 551–565 (2019).
pubmed: 31928355
pmcid: 6534214
doi: 10.1080/10717544.2019.1616235
Siegal, T. et al. In vivo assessment of the window of barrier opening after osmotic blood–brain barrier disruption in humans. J. Neurosurg. 92, 599–605 (2000).
pubmed: 10761648
doi: 10.3171/jns.2000.92.4.0599
Patel, N. V. et al. Laser interstitial thermal therapy technology, physics of magnetic resonance imaging thermometry, and technical considerations for proper catheter placement during magnetic resonance imaging-guided laser interstitial thermal therapy. Neurosurgery 79, S8–S16 (2016).
pubmed: 27861321
doi: 10.1227/NEU.0000000000001440
Hawasli, A. H., Bandt, S. K., Hogan, R. E., Werner, N. & Leuthardt, E. C. Laser ablation as treatment strategy for medically refractory dominant insular epilepsy: therapeutic and functional considerations. Stereotact. Funct. Neurosurg. 92, 397–404 (2014).
pubmed: 25359500
doi: 10.1159/000366001
Choi, J. J. et al. Noninvasive and transient blood-brain barrier opening in the hippocampus of Alzheimer’s double transgenic mice using focused ultrasound. Ultrason. Imaging 30, 189–200 (2008).
pubmed: 19149463
pmcid: 3919133
doi: 10.1177/016173460803000304
Hynynen, K., McDannold, N., Sheikov, N. A., Jolesz, F. A. & Vykhodtseva, N. Local and reversible blood–brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 24, 12–20 (2005).
pubmed: 15588592
doi: 10.1016/j.neuroimage.2004.06.046
Choi, J. J., Pernot, M., Small, S. A. & Konofagou, E. E. Noninvasive, transcranial and localized opening of the blood-brain barrier using focused ultrasound in mice. Ultrasound Med. Biol. 33, 95–104 (2007).
pubmed: 17189051
doi: 10.1016/j.ultrasmedbio.2006.07.018
McDannold, N. et al. Acoustic feedback enables safe and reliable carboplatin delivery across the blood-brain barrier with a clinical focused ultrasound system and improves survival in a rat glioma model. Theranostics 9, 6284 (2019).
pubmed: 31534551
pmcid: 6735504
doi: 10.7150/thno.35892
Marty, B. et al. Dynamic study of blood–brain barrier closure after its disruption using ultrasound: a quantitative analysis. J. Cereb. Blood Flow. Metab. 32, 1948–1958 (2012).
pubmed: 22805875
pmcid: 3463875
doi: 10.1038/jcbfm.2012.100
Yemane, P. T. et al. Effect of ultrasound on the vasculature and extravasation of nanoscale particles imaged in real time. Ultrasound Med. Biol. 45, 3028–3041 (2019).
pubmed: 31474384
doi: 10.1016/j.ultrasmedbio.2019.07.683
Choi, J. J., Wang, S., Tung, Y.-S., Morrison, B. III & Konofagou, E. E. Molecules of various pharmacologically-relevant sizes can cross the ultrasound-induced blood-brain barrier opening in vivo. Ultrasound Med. Biol. 36, 58–67 (2010).
pubmed: 19900750
pmcid: 2997717
doi: 10.1016/j.ultrasmedbio.2009.08.006
Yang, Y. et al. Cavitation dose painting for focused ultrasound-induced blood-brain barrier disruption. Sci. Rep. 9, 1–10 (2019).
Hsu, P.-H. et al. Noninvasive and targeted gene delivery into the brain using microbubble-facilitated focused ultrasound. PLoS ONE 8, e57682 (2013).
pubmed: 23460893
pmcid: 3584045
doi: 10.1371/journal.pone.0057682
Burgess, A. et al. Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS ONE 6, e27877 (2011).
pubmed: 22114718
pmcid: 3218061
doi: 10.1371/journal.pone.0027877
Anastasiadis, P. et al. Localized blood–brain barrier opening in infiltrating gliomas with MRI-guided acoustic emissions-controlled focused ultrasound. Proc. Natl. Acad. Sci. USA 118, e2103280118 (2021).
Christen, T. et al. Is T2* enough to assess oxygenation? quantitative blood oxygen level–dependent analysis in brain tumor. Radiology 262, 495–502 (2012).
pubmed: 22156990
pmcid: 3267079
doi: 10.1148/radiol.11110518
Russo, R. et al. Hemoglobin is present as a canonical α2β2 tetramer in dopaminergic neurons. Biochim. Biophys. Acta BBA Proteins Proteom. 1834, 1939–1943 (2013).
doi: 10.1016/j.bbapap.2013.05.005
Tani, K., Imura, M., Koyama, D. & Watanabe, Y. Quantitative evaluation of hemolysis in bovine red blood cells caused by acoustic cavitation under pulsed ultrasound. Acoust. Sci. Technol. 38, 161–164 (2017).
doi: 10.1250/ast.38.161
Le Duc, G. et al. Advantages of gadolinium based ultrasmall nanoparticles vs molecular gadolinium chelates for radiotherapy guided by MRI for glioma treatment. Cancer Nanotechnol. 5, 1–14 (2014).
Laurent, S., Elst, L. V. & Muller, R. N. Comparative study of the physicochemical properties of six clinical low molecular weight gadolinium contrast agents. Contrast Media Mol. Imaging 1, 128–137 (2006).
pubmed: 17193689
doi: 10.1002/cmmi.100
Marty, B. et al. Hindered diffusion of MRI contrast agents in rat brain extracellular micro‐environment assessed by acquisition of dynamic T1 and T2 maps. Contrast Media Mol. Imaging 8, 12–19 (2013).
pubmed: 23109388
doi: 10.1002/cmmi.1489
Stewart, S. & Harrington, K. J. The biodistribution and pharmacokinetics of stealth liposomes in patients with solid tumors. Oncology 11, 33–37 (1997).
Chavhan, G. B., Babyn, P. S., Thomas, B., Shroff, M. M. & Haacke, E. M. Principles, techniques, and applications of T2*-based MR imaging and its special applications. Radiographics 29, 1433–1449 (2009).
pubmed: 19755604
pmcid: 2799958
doi: 10.1148/rg.295095034
Vieira, D. B. & Gamarra, L. F. Getting into the brain: liposome-based strategies for effective drug delivery across the blood–brain barrier. Int. J. Nanomed. 11, 5381 (2016).
doi: 10.2147/IJN.S117210
Gea, Z. Abstract–interim results of a phase II multicenter study of the conditionally replicative oncolytic adenovirus DNX-2401 with pembrolizumab (Keytruda) for recurrent glioblastoma; CAPTIVE STUDY (LEYNOTE-192). Neuro-Oncology 20, vi6 (2018).
doi: 10.1093/neuonc/noy148.019
Ahlawat, J. et al. Nanocarriers as potential drug delivery candidates for overcoming the blood–brain barrier: challenges and possibilities. ACS Omega 5, 12583–12595 (2020).
pubmed: 32548442
pmcid: 7288355
doi: 10.1021/acsomega.0c01592
Aryal, M. et al. MRI monitoring and quantification of ultrasound-mediated delivery of liposomes dually labeled with gadolinium and fluorophore through the blood-brain barrier. Ultrasound Med. Biol. 45, 1733–1742 (2019).
pubmed: 31010598
pmcid: 6555669
doi: 10.1016/j.ultrasmedbio.2019.02.024
Rusu, L., Lumma, D. & Rädler, J. O. Charge and size dependence of liposome diffusion in semidilute biopolymer solutions. Macromol. Biosci. 10, 1465–1472 (2010).
pubmed: 20602414
doi: 10.1002/mabi.201000033
O’Reilly, M. A. et al. Investigation of the safety of focused ultrasound-induced blood-brain barrier opening in a natural canine model of aging. Theranostics 7, 3573 (2017).
pubmed: 28912896
pmcid: 5596444
doi: 10.7150/thno.20621
Conti, A. et al. Empirical and theoretical characterization of the diffusion process of different gadolinium-based nanoparticles within the brain tissue after ultrasound-induced permeabilization of the blood-brain barrier. Contrast Media Mol. Imaging 2019, 6341545 (2019).
Gasca-Salas, C. et al. Blood-brain barrier opening with focused ultrasound in Parkinson’s disease dementia. Nat. Commun. 12, 1–7 (2021).
doi: 10.1038/s41467-021-21022-9
Chu, P.-C. et al. Focused ultrasound-induced blood-brain barrier opening: association with mechanical index and cavitation index analyzed by dynamic contrast-enhanced magnetic-resonance imaging. Sci. Rep. 6, 1–13 (2016).
doi: 10.1038/srep33264
Park, J., Zhang, Y., Vykhodtseva, N., Jolesz, F. A. & McDannold, N. J. The kinetics of blood brain barrier permeability and targeted doxorubicin delivery into brain induced by focused ultrasound. J. Control. Release 162, 134–142 (2012).
pubmed: 22709590
pmcid: 3520430
doi: 10.1016/j.jconrel.2012.06.012
Heye, A. K. et al. Assessment of blood–brain barrier disruption using dynamic contrast-enhanced MRI. a systematic review. NeuroImage Clin. 6, 262–274 (2014).
pubmed: 25379439
pmcid: 4215461
doi: 10.1016/j.nicl.2014.09.002
Sun, T. et al. Closed-loop control of targeted ultrasound drug delivery across the blood–brain/tumor barriers in a rat glioma model. Proc. Natl Acad. Sci. USA 114, E10281–E10290 (2017).
pubmed: 29133392
pmcid: 5715774
doi: 10.1073/pnas.1713328114
Cheng, B., Bing, C. & Chopra, R. The effect of transcranial focused ultrasound target location on the acoustic feedback control performance during blood-brain barrier opening with nanobubbles. Sci. Rep. 9, 1–10 (2019).
doi: 10.1038/s41598-019-55629-2
O’Reilly, M. A. & Hynynen, K. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology 263, 96–106 (2012).
pubmed: 22332065
pmcid: 3309801
doi: 10.1148/radiol.11111417
Rao, M. R., Norquay, G., Stewart, N. J. & Wild, J. M. Measuring 129Xe transfer across the blood‐brain barrier using MR spectroscopy. Magn. Reson. Med. 85, 2939–2949 (2021).
pubmed: 33458859
pmcid: 7986241
doi: 10.1002/mrm.28646
Molotkov, A. et al. Real-time positron emission tomography evaluation of topotecan brain kinetics after ultrasound-mediated blood–brain barrier permeability. Pharmaceutics 13, 405 (2021).
pubmed: 33803856
pmcid: 8003157
doi: 10.3390/pharmaceutics13030405
Arif, W. M. et al. Focused ultrasound for opening blood-brain barrier and drug delivery monitored with positron emission tomography. J. Control. Release 324, 303–316 (2020).
pubmed: 32428519
doi: 10.1016/j.jconrel.2020.05.020
Wong, E. T. et al. Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J. Clin. Oncol. 17, 2572–2572 (1999).
pubmed: 10561324
doi: 10.1200/JCO.1999.17.8.2572
Lacroix, M. et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J. Neurosurg. 95, 190–198 (2001).
pubmed: 11780887
doi: 10.3171/jns.2001.95.2.0190
Adamson, C. et al. Glioblastoma multiforme: a review of where we have been and where we are going. Expert Opin. Investig. Drugs 18, 1061–1083 (2009).
pubmed: 19555299
doi: 10.1517/13543780903052764
Kroeger, K. M. et al. Gene therapy and virotherapy: novel therapeutic approaches for brain tumors. Discov. Med. 10, 293 (2010).
pubmed: 21034670
pmcid: 3059086
Westphal, M. et al. Adenovirus-mediated gene therapy with sitimagene ceradenovec followed by intravenous ganciclovir for patients with operable high-grade glioma (ASPECT): a randomised, open-label, phase 3 trial. Lancet Oncol. 14, 823–833 (2013).
pubmed: 23850491
doi: 10.1016/S1470-2045(13)70274-2
Sampson, J. H. et al. Poor drug distribution as a possible explanation for the results of the PRECISE trial. J. Neurosurg. 113, 301–309 (2010).
pubmed: 20020841
doi: 10.3171/2009.11.JNS091052
Kim, M. J. et al. Technical and operative factors affecting magnetic resonance imaging–guided focused ultrasound thalamotomy for essential tremor: experience from 250 treatments. J. Neurosurg. 1, 1–9 (2021).
Mainprize, T. et al. Blood-brain barrier opening in primary brain tumors with non-invasive MR-guided focused ultrasound: a clinical safety and feasibility study. Sci. Rep. 9, 1–7 (2019).
doi: 10.1038/s41598-018-36340-0
Chen, K.-T. et al. Neuronavigation-guided focused ultrasound for transcranial blood-brain barrier opening and immunostimulation in brain tumors. Sci. Adv. 7, eabd0772 (2021).
pubmed: 33547073
pmcid: 7864566
doi: 10.1126/sciadv.abd0772
Carpentier, A. et al. Clinical trial of blood-brain barrier disruption by pulsed ultrasound. Sci. Transl. Med. 8, 343re2–343re2 (2016).
pubmed: 27306666
doi: 10.1126/scitranslmed.aaf6086
Cohen, Z. R. et al. Localized RNAi therapeutics of chemoresistant grade IV glioma using hyaluronan-grafted lipid-based nanoparticles. ACS Nano 9, 1581–1591 (2015).
pubmed: 25558928
doi: 10.1021/nn506248s
Gutkin, A., Cohen, Z. R. & Peer, D. Harnessing nanomedicine for therapeutic intervention in glioblastoma. Expert Opin. Drug Deliv. 13, 1573–1582 (2016).
pubmed: 27292970
doi: 10.1080/17425247.2016.1200557
Rosenblum, D. et al. CRISPR-Cas9 genome editing using targeted lipid nanoparticles for cancer therapy. Sci. Adv. 6, eabc9450 (2020).
pubmed: 33208369
pmcid: 7673804
doi: 10.1126/sciadv.abc9450
Marstal, K., Berendsen, F., Staring, M. & Klein, S. SimpleElastix: a user-friendly, multi-lingual library for medical image registration. In Proc. of the IEEE Conference on Computer Vision and Pattern Recognition Workshops (CVPRW) 574–582 (IEEE, 2016).
Carugo, D., Bottaro, E., Owen, J., Stride, E. & Nastruzzi, C. Liposome production by microfluidics: potential and limiting factors. Sci. Rep. 6, 1–15 (2016).
doi: 10.1038/srep25876
Langeveld, S. A. et al. Ligand distribution and lipid phase behavior in phospholipid-coated microbubbles and monolayers. Langmuir 36, 3221–3233 (2020).
pubmed: 32109064
pmcid: 7279639
doi: 10.1021/acs.langmuir.9b03912