Hyperosmolar blood–brain barrier opening using intra-arterial injection of hyperosmotic mannitol in mice under real-time MRI guidance

Chengyan Chu, Anna Jablonska, Yue Gao, Xiaoyan Lan, Wojciech G. Lesniak, Yajie Liang, Guanshu Liu, Shen Li, Tim Magnus, Monica Pearl, Miroslaw Janowski, Piotr Walczak

Published: 2021-12-12 DOI: 10.1038/s41596-021-00634-x

Blood–brain barrier

Mannitol

Interventional MRI

Therapeutic delivery

Mouse model

AI 解读

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The blood–nobreakbrain barrier (BBB) is the main obstacle to the effective delivery of therapeutic agents to the brain, compromising treatment efficacy for a variety of neurological disorders. Intra-arterial (IA) injection of hyperosmotic mannitol
Introduction
Materials
Procedure
Troubleshooting
Timing
Anticipated results
References
ACKNOWLEDGMENTS

Nduom, E. K., Yang, C., Merrill, M. J., Zhuang, Z. & Lonser, R. R. Characterization of the blood–brain barrier of metastatic and primary malignant neoplasms. J. Neurosurg. 119, 427–433 (2013).
Budde, M. D., Janes, L., Gold, E., Turtzo, L. C. & Frank, J. A. The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. Brain 134, 2248–2260 (2011).
Pardridge, W. M. The blood–brain barrier: bottleneck in brain drug development. NeuroRx 2, 3–14 (2005).
Goldstein, G. W. & Betz, A. L. The blood–brain barrier. Sci. Am. 255, 74–7 (1986).
Chakraborty, S. et al. Superselective intraarterial cerebral infusion of cetuximab after osmotic blood/brain barrier disruption for recurrent malignant glioma: phase I study. J. Neurooncol. 128, 405–415 (2016).
Gonzales-Portillo, G. S. et al. Mannitol-enhanced delivery of stem cells and their growth factors across the blood–brain barrier. Cell Transplant. 23, 531–539 (2014).
Brightman, M. W., Hori, M., Rapoport, S. I., Reese, T. S. & Westergaard, E. Osmotic opening of tight junctions in cerebral endothelium. J. Comp. Neurol. 152, 317–325 (1973).
Foley, C. P. et al. Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption. J. Control. Release 196, 71–78 (2014).
Burkhardt, J. K. et al. Intra-arterial delivery of bevacizumab after blood–brain barrier disruption for the treatment of recurrent glioblastoma: progression-free survival and overall survival. World Neurosurg. 77, 130–134 (2012).
Joshi, S. et al. Inconsistent blood brain barrier disruption by intraarterial mannitol in rabbits: implications for chemotherapy. J. Neurooncol. 104, 11–19 (2011).
Janowski, M., Walczak, P. & Pearl, M. S. Predicting and optimizing the territory of blood–brain barrier opening by superselective intra-arterial cerebral infusion under dynamic susceptibility contrast MRI guidance. J. Cereb. Blood Flow. Metab. 36, 569–575 (2016).
Kaya, M. et al. The effects of magnesium sulfate on blood–brain barrier disruption caused by intracarotid injection of hyperosmolar mannitol in rats. Life Sci. 76, 201–212 (2004).
Yang, W. L. et al. Evaluation of systemically administered radiolabeled epidermal growth factor as a brain tumor targeting agent. J. Neuro-Oncol. 55, 19–28 (2001).
Tajiri, N., Lee, J. Y., Acosta, S., Sanberg, P. R. & Borlongan, C. V. Breaking the blood–brain barrier with mannitol to aid stem cell therapeutics in the chronic stroke brain. Cell Transplant. 25, 1453–1460 (2016).
Seyfried, D. M. et al. Mannitol enhances delivery of marrow stromal cells to the brain after experimental intracerebral hemorrhage. Brain Res. 1224, 12–19 (2008).
Fu, H. et al. Self-complementary adeno-associated virus serotype 2 vector: global distribution and broad dispersion of AAV-mediated transgene expression in mouse brain. Mol. Ther. 8, 911–917 (2003).
Janowski, M. et al. Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J. Cereb. Blood Flow. Metab. 33, 921–927 (2013).
Walczak, P. et al. Real-time MRI for precise and predictable intra-arterial stem cell delivery to the central nervous system. J. Cereb. Blood Flow Metab. 37, 2346–2358 (2016).
Zawadzki, M. et al. Real-time MRI guidance for intra-arterial drug delivery in a patient with a brain tumor: technical note. BMJ Case Rep. 12, e014469 (2019).
Doyle, A., McGarry, M. P., Lee, N. A. & Lee, J. J. The construction of transgenic and gene knockout/knockin mouse models of human disease. Transgenic Res. 21, 327–349 (2012).
Rivera, J., Sobey, C. G., Walduck, A. K. & Drummond, G. R. Nox isoforms in vascular pathophysiology: insights from transgenic and knockout mouse models. Redox Rep. 15, 50–63 (2010).
Bartke, A. New findings in gene knockout, mutant and transgenic mice. Exp. Gerontol. 43, 11–14 (2008).
Chu, C. et al. Real-time MRI guidance for reproducible hyperosmolar opening of the blood–brain barrier in mice. Front. Neurol. 9, 921 (2018).
Chu, C. et al. Optimization of osmotic blood–brain barrier opening to enable intravital microscopy studies on drug delivery in mouse cortex. J. Control. Release 317, 312–321 (2020).
Lesniak, W. G. et al. PET imaging of distinct brain uptake of a nanobody and similarly-sized PAMAM dendrimers after intra-arterial administration. Eur. J. Nucl. Med. Mol. Imaging 46, 1940–1951 (2019).
Lesniak, W. G. et al. A distinct advantage to intraarterial delivery of (89)Zr-bevacizumab in PET imaging of mice with and without osmotic opening of the blood–brain barrier. J. Nucl. Med. 60, 617–622 (2019).
Liu, R., Martuza, R. L. & Rabkin, S. D. Intracarotid delivery of oncolytic HSV vector G47Delta to metastatic breast cancer in the brain. Gene Ther. 12, 647–654 (2005).
Choonara, Y. E., Kumar, P., Modi, G. & Pillay, V. Improving drug delivery technology for treating neurodegenerative diseases. Expert Opin. Drug Deliv. 13, 1029–1043 (2016).
Niu, X., Chen, J. & Gao, J. Nanocarriers as a powerful vehicle to overcome blood–brain barrier in treating neurodegenerative diseases: focus on recent advances. Asian J. Pharm. Sci. 14, 480–496 (2019).
Cerri, S. et al. Intracarotid infusion of mesenchymal stem cells in an animal model of parkinson’s disease, focusing on cell distribution and neuroprotective and behavioral effects. Stem Cells Transl. Med. 4, 1073–1085 (2015).
Kijima, N. & Kanemura, Y. Mouse models of glioblastoma. in Glioblastoma (ed. De Vleeschouwer, S.) Ch. 7 (Codon Publications, 2017).
Lan, X. et al. Modeling human pediatric and adult gliomas in immunocompetent mice through costimulatory blockade. Oncoimmunology 9, 1776577 (2020).
Hall, A. M. & Roberson, E. D. Mouse models of Alzheimer’s disease. Brain Res. Bull. 88, 3–12 (2012).
Schober, A. Classic toxin-induced animal models of Parkinson’s disease: 6-OHDA and MPTP. Cell Tissue Res. 318, 215–224 (2004).
Lipsman, N. et al. Blood–brain barrier opening in Alzheimer’s disease using MR-guided focused ultrasound. Nat. Commun. 9, 2336 (2018).
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, 321 (2019).
Meng, Y. et al. Safety and efficacy of focused ultrasound induced blood–brain barrier opening, an integrative review of animal and human studies. J. Control. Release 309, 25–36 (2019).
Silburt, J., Lipsman, N. & Aubert, I. Disrupting the blood–brain barrier with focused ultrasound: perspectives on inflammation and regeneration. Proc. Natl Acad. Sci. USA. 114, E6735–E6736 (2017).
Polycarpou, A. et al. Adaptation of the cerebrocortical circulation to carotid artery occlusion involves blood flow redistribution between cortical regions and is independent of eNOS. Am. J. Physiol. Heart Circ. Physiol. 311, H972–H980 (2016).
Yoshizaki, K. et al. Chronic cerebral hypoperfusion induced by right unilateral common carotid artery occlusion causes delayed white matter lesions and cognitive impairment in adult mice. Exp. Neurol. 210, 585–591 (2008).
Lacolley, P. et al. Occipital artery injections of 5-HT may directly activate the cell bodies of vagal and glossopharyngeal afferent cell bodies in the rat. Neuroscience 143, 289–308 (2006).
Gillilan, L. A. Potential collateral circulation to the human cerebral cortex. Neurology 24, 941–948 (1974).
Cuccione, E., Padovano, G., Versace, A., Ferrarese, C. & Beretta, S. Cerebral collateral circulation in experimental ischemic stroke. Exp. Transl. Stroke Med. 8, 2 (2016).
McGraw, C. P. & Howard, G. Effect of mannitol on increased intracranial pressure. Neurosurgery 13, 269–271 (1983).
Schwarz, S., Schwab, S., Bertram, M., Aschoff, A. & Hacke, W. Effects of hypertonic saline hydroxyethyl starch solution and mannitol in patients with increased intracranial pressure after stroke. Stroke 29, 1550–1555 (1998).
Cosolo, W. C., Martinello, P., Louis, W. J. & Christophidis, N. Blood–brain barrier disruption using mannitol: time course and electron microscopy studies. Am. J. Physiol. 256, R443–R447 (1989).
Fredericks, W. R. & Rapoport, S. I. Reversible osmotic opening of the blood–brain barrier in mice. Stroke 19, 266–268 (1988).
Doolittle, N. D., Muldoon, L. L., Culp, A. Y. & Neuwelt, E. A. Delivery of chemotherapeutics across the blood–brain barrier: challenges and advances. Adv. Pharmacol. 71, 203–243 (2014).
Guzman, R., Janowski, M. & Walczak, P. Intra-arterial delivery of cell therapies for stroke. Stroke 49, 1075–1082 (2018).
Golubczyk, D. et al. Endovascular model of ischemic stroke in swine guided by real-time MRI. Sci. Rep. 10, 17318 (2020).
Yang, W. et al. Enhanced survival of glioma bearing rats following boron neutron capture therapy with blood–brain barrier disruption and intracarotid injection of boronophenylalanine. J. Neurooncol. 33, 59–70 (1997).
Neuwelt, E. A. et al. Delivery of melanoma-associated immunoglobulin monoclonal antibody and Fab fragments to normal brain utilizing osmotic blood–brain barrier disruption. Cancer Res. 48, 4725–4729 (1988).
Kozler, P., Riljak, V., Jandova, K. & Pokorny, J. CT imaging and spontaneous behavior analysis after osmotic blood–brain barrier opening in Wistar rat. Physiol. Res. 63, S529–S534 (2014).
Chi, O. Z., Liu, X. & Weiss, H. R. Effects of mild hypothermia on blood–brain barrier disruption during isoflurane or pentobarbital anesthesia. Anesthesiology 95, 933–938 (2001).
Godinho, B. et al. Transvascular delivery of hydrophobically modified siRNAs: gene silencing in the rat brain upon disruption of the blood–brain barrier. Mol. Ther. 26, 2580–2591 (2018).
Martin, J. A.; Maris, A. S.; Ehtesham, M.; Singer, R. J., Rat model of blood–brain barrier disruption to allow targeted neurovascular therapeutics. J. Vis. Exp. 2012, e50019.
Bhattacharjee, A. K., Nagashima, T., Kondoh, T. & Tamaki, N. Quantification of early blood–brain barrier disruption by in situ brain perfusion technique. Brain Res. Brain Res. Protoc. 8, 126–131 (2001).
Ju, F. et al. Increased BBB permeability enhances activation of microglia and exacerbates loss of dendritic spines after transient global cerebral ischemia. Front. Cell Neurosci. 12, 236 (2018).

Hyperosmolar blood–brain barrier opening using intra-arterial injection of hyperosmotic mannitol in mice under real-time MRI guidance

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