Boron Delivery to Brain Cells via Cerebrospinal Fluid (CSF) Circulation in BNCT of Brain-Tumor-Model Rats—Ex Vivo Imaging of BPA Using MALDI Mass Spectrometry Imaging
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. B16F10 Melanoma Model Rats
2.3. Boron Compound
2.4. Boron CSF Administration to Brain Tumor Rats
2.5. Intravenous (IV) Administration to Brain Tumor Rats
2.6. Preparation of Samples for MALDI-MSI
2.7. MALDI-MSI
2.8. Ensuring Image Reliability
3. Results
4. Discussion
4.1. Previous Research and Progress of CSF Administration Method
4.2. Time-Course Study of BPA Biodistribution following CSF Administration
4.3. Confirmation of the Potential of CSF Microcirculation
4.4. BPA Biodistribution at the Cellular Level Based on MALDI-MSI
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Barth, R.F.; Vicente, H.M.; Harling, O.K.; Kiger, W.S., III; Riley, K.J.; Binns, P.J.; Wagner, F.M.; Suzuki, M.; Aihara, T.; Kato, I.; et al. Current status of boron neutron capture therapy of high grade gliomas and recurrent head and neck cancer. Radiat. Oncol. 2012, 7, 146. [Google Scholar] [CrossRef] [Green Version]
- Locher, G.L. Biological effects and therapeutic possibilities of neutron. Am. J. Roentgenol. 1936, 36, 1–13. [Google Scholar]
- Barth, R.F.; Mi, P.; Yang, W. Boron delivery agents for neutron capture therapy of cancer. Cancer Commun. 2018, 38, 1–15. [Google Scholar] [CrossRef] [Green Version]
- Nagamori, S.; Kanai, Y. Amino acid transporters in cancer. Biochemistry 2014, 86, 338–344. [Google Scholar]
- Pozzi, E.C.C.; Cardoso, J.E.; Colombo, L.L.; Thorp, S.; Hughes, A.M.; Molinari, A.J.; Garabalino, M.A.; Heber, E.M.; Miller, M.; Itoiz, M.E.; et al. Boron neutron capture therapy (BNCT) for liver metastasis: Therapeutic efficacy in an experimental model. Radiat. Environ. Biophys. 2012, 51, 331–339. [Google Scholar] [CrossRef]
- Steen, J.M.; Henry, H. Site-specific opening of the blood-brain barrier. Biophotonics 2010, 3, 356–367. [Google Scholar]
- Molly, S.S.; Shelley, R.W. Cell delivery to the central nervous system. Adv. Drug Deliv. Rev. 2000, 42, 81–102. [Google Scholar]
- Ching-Hsiang, F.; Chih-Kuang, Y. Microbubble-enhanced Focused Ultrasound-induced Blood–brain Barrier Opening for Local and Transient Drug Delivery in Central Nervous System Disease. J. Med. Ultrasound 2014, 22, 183–193. [Google Scholar]
- Gulyaev, A.E.; Gelperina, S.E.; Skidan, I.N.; Antropov, A.S.; Kivman, G.Y.; Kreuter, J. Significant transport of doxorubicin into the brain with polysorbate 80-coated nanoparticles. Pharm. Res. 1999, 16, 1564–1569. [Google Scholar] [CrossRef]
- Singh, M. Transferrin As A targeting ligand for liposomes and anticancer drugs. Curr. Pharm. Des. 1999, 5, 443–451. [Google Scholar]
- William, M.P.; Young-Sook, K.; Jody, L.B. Transport of Human Recombinant Brain-Derived Neurotrophic Factor (BDNF) Through the Rat Blood−Brain Barrier in Vivo Using Vector-Mediated Peptide Drug Delivery. Pharm. Res. 1994, 11, 738–746. [Google Scholar]
- Steven, R.S.; Alan, H.; Adamina, V.A.; Steven, F.D. In Vivo Protein Transduction: Delivery of a Biologically Active Protein into the Mouse. Science 1999, 285, 1569–1572. [Google Scholar]
- Guochen, H.; Kaiwen, B.; Xiaoyu, Y.; Chenhua, S.; Yi, J.; Jianping, Z.; Huaqing, Z.; Yang, D. “Drug-Carrier” Synergy Therapy for Amyloid-β Clearance and Inhibition of Tau Phosphorylation via Biomimetic Lipid Nanocomposite Assembly. Adv. Sci. 2022, 9, 2106072. [Google Scholar]
- Saito, R.; Tominaga, T. Convection-enhanced Delivery of Therapeutics for Malignant Gliomas. Neurol. Med. Chir. 2017, 57, 8–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kusaka, S.; Morizane, Y.; Tokumaru, Y.; Tamaki, S.; Indah, R.M.; Akiyama, Y.; Sato, F.; Murata, I. Boron Delivery to Brain Cells via Cerebrospinal Fluid (CSF) Circulation for BNCT in a Rat Melanoma Model. Biology 2022, 11, 397. [Google Scholar] [CrossRef]
- Kusaka, S.; Morizane, Y.; Tokumaru, Y.; Tamaki, S.; Indah, R.M.; Akiyama, Y.; Sato, F.; Murata, I. Cerebrospinal fluid-based boron delivery system may help increase the uptake boron for boron neutron capture therapy in veterinary medicine: A preliminary study with normal rat brain cells. Res. Vet. Sci. 2022, 148, 1–6. [Google Scholar]
- Nadia, A.J.; Anne, S.F.M.; Iben, L.; Maiken, N. The Glymphatic System: A Beginner’s Guide. Neurochem. Res. 2015, 40, 2583–2599. [Google Scholar]
- Xiaohui, L.; Jennifer, L.I.; Isaiah, N.; Mark, A.M.; Maritza, C.E.; Lan, Y.W.; Erin, D.; Claire, M.S.; Santosh, K.; Katherine, A.K.; et al. Molecular imaging of drug transit through the blood-brain barrier with MALDI mass spectrometry imaging. Sci. Rep. 2013, 3, 2859. [Google Scholar]
- Pardridge, W.M. Blood-Brain Barrier and Delivery of Protein and Gene Therapeutics to Brain. Front. Aging Neurosci. 2020, 11, 373. [Google Scholar]
- Ghazal, N.K.; Pankaj, K.; Susan, E.B.; Edward, B.R.; Didier, R.L. Biodistribution Analysis of an Anti-EGFR Antibody in the Rat Brain: Validation of CSF Microcirculation as a Viable Pathway to Circumvent the Blood-Brain Barrier for Drug Delivery. Pharmaceutics 2022, 14, 1441. [Google Scholar]
- Calias, P.; Banks, W.A.; Begley, D.; Scarpa, M.; Dickson, P. Intrathecal delivery of protein therapeutics to the brain: A critical reassessment. Pharmacol. Ther. 2014, 144, 114–122. [Google Scholar] [CrossRef] [PubMed]
- Rigo, F.; Chun, S.J.; Norris, D.A.; Hung, G.; Lee, S.; Matson, J.; Fey, R.A.; Gaus, H.; Hua, Y.; Grundy, J.S.; et al. Pharmacology of a Central Nervous System Delivered 20-O-Methoxyethyl–Modified Survival of Motor Neuron Splicing Oligonucleotide in Mice and Nonhuman Primates. J. Pharmacol. Exp. Ther. 2014, 350, 46–55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pardridge, W.M. The Blood-Brain Barrier: Bottleneck in Brain Drug Development. NeuroRX 2005, 2, 3–14. [Google Scholar] [CrossRef] [PubMed]
- Synnøve, N.A.; Heidi, E.; Tyagi, A.; Christopher, F.H.; Olivier, K.; Tine, V.K.; Olav, T.; Zaynah, M.; Hrvoje, M.; Tuyen, H.; et al. Improved Drug Delivery to Brain Metastases by Peptide-Mediated Permeabilization of the Blood–Brain Barrier. Molecular Cancer Therapeutics. Transl. Res. 2019, 18, 2171–2181. [Google Scholar]
- Ishikuro, M.; Wagatsuma, K. Determination of Trace Smounts of Boron in silicon and Germanium by Curcumin Spectrophotometry after Methyl Borate Distillation. Bunseki Kagaku 2009, 58, 373–377. [Google Scholar] [CrossRef]
- Amanda, E.S.; Andrea, M.H.; Marcela, A.G.; Gustavo, A.S.C.; Sara, J.G.; Juan, L.; Lucas, P.; Paulina, O.; Monica, R.; María, Á.C. Clinical Veterinary Boron Neutron Capture Therapy (BNCT) Studies in Dogs with Head and Neck Cancer: Bridging the Gap between Translational and Clinical Studies. Biology 2020, 9, 327. [Google Scholar]
- Miyake, Y.; Kusaka, S.; Murata, I.; Toyoda, M. Matrix-assisted laser desorption/ionization (MALDI) Mass Spectrometry Imaging (MSI) of L-4-phenylalanineboronic acid (BPA) in a Brain tumor model rat for Boron Neutron Capture Therapy (BNCT). Mass Spectrom. 2022, 11, A0105. [Google Scholar] [CrossRef]
- Yu-Chuan, L.; Yi-Jang, L.; Yi-Wei, C.; Shan-Ying, W.; Fong-In, C. Evaluation of the Key Advantages between Two Modalities of Boronophenylalanine Administration for Clinical Boron Neutron Capture Therapy Using an Animal Model. Cells 2022, 11, 2736. [Google Scholar]
- Yan, R.; Zhao, X.; Lei, J.; Zhou, Q. Structure of the human LAT1–4F2hc heteromeric amino acid transporter complex substances. Nature 2019, 568, 127–130. [Google Scholar] [CrossRef]
- 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.; et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987–996. [Google Scholar] [CrossRef] [Green Version]
- Jing, X.; Lin, M.; Zheng, G.; Hongjun, J.; Hongbin, Z.; Jianfei, T.; Tianjiao, L.; Juan, L.; Qiushi, R.; Qi, L. A Boronated Derivative of Temozolomide Showing Enhanced Efficacy in Boron Neutron Capture Therapy of Glioblastoma. Cells 2022, 11, 1173. [Google Scholar]
- Kouzehgarani, G.N.; Feldsien, T.; Engelhard, H.H.; Mirakhur, K.K.; Phipps, C.; Nimmrich, V.; Clausznitzer, D.; Lefevbre, D.R. Harnessing cerebrospinal fluid circulation for drug delivery to brain tissues. Adv. Drug Deliv. Rev. 2021, 173, 20–59. [Google Scholar] [CrossRef] [PubMed]
- Pardridge, W.M. CSF, blood-brain barrier, and brain drug delivery. Expert Opin. Drug Deliv. 2016, 13, 963–975. [Google Scholar] [CrossRef] [PubMed]
- Yankova, G.; Bogomyakova, O.; Tulupov, A. The glymphatic system and meningeal lymphatics of the brain: New understanding of brain clearance. Rev. Neurosci. 2021, 32, 693–705. [Google Scholar] [CrossRef] [PubMed]
- Mestre, H.; Mori, Y.; Nedergaard, M. The Brain’s Glymphatic System: Current Controversies. Trends Neurosci. 2020, 43, 458–466. [Google Scholar] [CrossRef] [PubMed]
- Abbott, N.J.; Pizzo, M.E.; Preston, J.E.; Janigro, D.; Thorne, R.G. The role of brain barriers in fluid movement in the CNS: Is there a ‘glymphatic’ system? Acta Neuropathol. 2018, 135, 387–407. [Google Scholar] [CrossRef] [Green Version]
- Pardridge, W.M. Drug transport in brain via the cerebrospinal fluid. Fluids Barriers CNS 2011, 8, 7. [Google Scholar] [CrossRef] [Green Version]
- Andrea, M.H.; Jessica, A.G.; Mónica, A.P.; Paula, R.; Iara, S.S.C.; Luciana, D.L.; Marcela, A.G.; Silvia, I.T.; Paula, C.; Emiliano, C.C.P.; et al. Boron Neutron Capture Therapy (BNCT) Mediated by Maleimide-Functionalized Closo-Dodecaborate Albumin Conjugates (MID:BSA) for Oral Cancer: Biodistribution Studies and In Vivo BNCT in the Hamster Cheek Pouch Oral Cancer Model. Life 2022, 12, 1082. [Google Scholar]
- Qi, D.; QiYao, Y.; Xiaoyan, B.; Jiejian, C.; Min, H.; Qichun, W. The Development of Boron Analysis and Imaging in Boron Neutron Capture Therapy (BNCT). Mol. Pharm. 2022, 19, 363–377. [Google Scholar]
- Amemiya, K.; Takahashi, H.; Kajimoto, Y.; Nakazawa, M.; Yanagie, H.; Hisa, T.; Eriguchi, M.; Nakagawa, Y.; Majima, T.; Kageji, T.; et al. High-resolution nuclear track mapping in detailed cellular histology using CR-39 with the contact microscopy technique. Radiat. Meas. 2005, 40, 283–288. [Google Scholar] [CrossRef]
- Chandra, S.; Ahmad, T.; Barth, R.F.; Kabalka, G.W. Quantitative evaluation of boron neutron capture therapy (BNCT) drugs for boron delivery and retention at subcellular-scale resolution in human glioblastoma cells with imaging secondary ion mass spectrometry (SIMS). J. Microsc. 2014, 254, 146–156. [Google Scholar] [CrossRef] [Green Version]
- Michel, J.; Sauerwein, W.; Wittig, A.; Balossier, G.; Zierold, K. Subcellular localization of boron in cultured melanoma cells by electron energy-loss spectroscopy of freeze-dried cryosections. J. Microsc. 2003, 210, 25–34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paul, M.; Mark, R.C.; Manuela, K.H.; Gurjeet, K.; Martin, K.O.; Oliver, M.S.; Michelle, P.; Stefan, K.; Sara, B.; Mark, D.M.; et al. Cancer Tissue Classification Using Supervised Machine Learning Applied to MALDI Mass Spectrometry Imaging. Cancers 2021, 13, 5388. [Google Scholar]
- Takeo, E.; Shimma, S. Development of quantitative imaging mass spectrometry (q-IMS) for drug visualization using animal tissues. Surf. Interface Anal. 2019, 51, 21–26. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kusaka, S.; Miyake, Y.; Tokumaru, Y.; Morizane, Y.; Tamaki, S.; Akiyama, Y.; Sato, F.; Murata, I. Boron Delivery to Brain Cells via Cerebrospinal Fluid (CSF) Circulation in BNCT of Brain-Tumor-Model Rats—Ex Vivo Imaging of BPA Using MALDI Mass Spectrometry Imaging. Life 2022, 12, 1786. https://doi.org/10.3390/life12111786
Kusaka S, Miyake Y, Tokumaru Y, Morizane Y, Tamaki S, Akiyama Y, Sato F, Murata I. Boron Delivery to Brain Cells via Cerebrospinal Fluid (CSF) Circulation in BNCT of Brain-Tumor-Model Rats—Ex Vivo Imaging of BPA Using MALDI Mass Spectrometry Imaging. Life. 2022; 12(11):1786. https://doi.org/10.3390/life12111786
Chicago/Turabian StyleKusaka, Sachie, Yumi Miyake, Yugo Tokumaru, Yuri Morizane, Shingo Tamaki, Yoko Akiyama, Fuminobu Sato, and Isao Murata. 2022. "Boron Delivery to Brain Cells via Cerebrospinal Fluid (CSF) Circulation in BNCT of Brain-Tumor-Model Rats—Ex Vivo Imaging of BPA Using MALDI Mass Spectrometry Imaging" Life 12, no. 11: 1786. https://doi.org/10.3390/life12111786