RGD-coated polymeric microbubbles promote ultrasound-mediated drug delivery in an inflamed endothelium-pericyte co-culture model of the blood-brain barrier

Bhalerao A, Sivandzade F, Archie SR, Chowdhury EA, Noorani B, Cucullo L. In vitro modeling of the neurovascular unit: advances in the field, Fluids and Barriers of the CNS, 17 (2020).

Brown LS, Foster CG, Courtney J-M, King NE, Howells DW, Sutherland BA. Pericytes and neurovascular function in the healthy and diseased brain. Front Cell Neurosci, 13 (2019).

Banks WA. From blood-brain barrier to blood-brain interface: new opportunities for CNS drug delivery. Nat Rev Drug Discov. 2016;15:275–92.

PubMed  CAS  Google Scholar 

Stefan H, Feuerstein TJ. Novel anticonvulsant drugs. Pharmacol Ther. 2007;113:165–83.

PubMed  CAS  Google Scholar 

Gharbavi M, Amani J, Kheiri-Manjili H, Danafar H, Sharafi A. Niosome: A Promising Nanocarrier for Natural Drug Delivery through Blood-Brain Barrier, Advances in Pharmacological Sciences, 2018 (2018).

Rufino-Ramos D, Albuquerque PR, Carmona V, Perfeito R, Nobre RJ. Pereira De Almeida, Extracellular vesicles: novel promising delivery systems for therapy of brain diseases. J Control Release. 2017;262:247–58.

PubMed  CAS  Google Scholar 

Shi Y, van der Meel R, Chen X, Lammers T. The EPR effect and beyond: strategies to improve tumor targeting and cancer nanomedicine treatment efficacy. Theranostics. 2020;10:7921–4.

PubMed  PubMed Central  Google Scholar 

Zheng Y, Ma L, Sun Q. Clinically-relevant ABC transporter for Anti-cancer Drug Resistance. Front Pharmacol, 12 (2021).

de Maar JS, Rousou C, van Elburg B, Vos HJ, Lajoinie GPR, Bos C, Moonen CTW, Deckers R. Ultrasound-mediated drug delivery with a clinical Ultrasound System: in vitro evaluation. Front Pharmacol. 2021;12:768436.

PubMed  PubMed Central  Google Scholar 

Beekers I, Lattwein KR, Kouijzer JJP, Langeveld SAG, Vegter M, Beurskens R, Mastik F, Verduyn Lunel R, Verver E, van der Steen AFW, de Jong N. Kooiman, Combined Confocal Microscope and Brandaris 128 Ultra-high-speed Camera. Ultrasound Med Biol. 2019;45:2575–82.

PubMed  Google Scholar 

Beekers I, Mastik F, Beurskens R, Tang PY, Vegter M, Van Der Steen AFW, De Jong N, Verweij MD, Kooiman K. High-resolution imaging of intracellular calcium fluctuations caused by oscillating Microbubbles. Ultrasound Med Biol. 2020;46:2017–29.

PubMed  Google Scholar 

Beekers I, Vegter M, Lattwein KR, Mastik F, Beurskens R, Van Der Steen AFW, De Jong N, Verweij MD, Kooiman K. Opening of endothelial cell–cell contacts due to sonoporation. J Controlled Release. 2020;322:426–38.

CAS  Google Scholar 

Srinivasan B, Kolli AR, Esch MB, Abaci HE, Shuler ML, Hickman JJ. TEER Measurement Techniques for in Vitro Barrier Model systems. J Lab Autom. 2015;20:107–26.

PubMed  PubMed Central  CAS  Google Scholar 

Butt AM, Jones HC, Abbott NJ. Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study. J Physiol. 1990;429:47–62.

PubMed  PubMed Central  CAS  Google Scholar 

Berndt P, Winkler L, Cording J, Breitkreuz-Korff O, Rex A, Dithmer S, Rausch V, Blasig R, Richter M, Sporbert A, Wolburg H, Blasig IE, Haseloff RF. Tight junction proteins at the blood-brain barrier: far more than claudin-5. Cell Mol Life Sci. 2019;76:1987–2002.

PubMed  PubMed Central  CAS  Google Scholar 

Helms HC, Abbott NJ, Burek M, Cecchelli R, Couraud P-O, Deli MA, Förster C, Galla HJ, Romero IA, Shusta EV, Stebbins MJ, Vandenhaute E, Weksler B, Brodin B. In vitro models of the blood–brain barrier: an overview of commonly used brain endothelial cell culture models and guidelines for their use. J Cereb Blood Flow Metabolism. 2016;36:862–90.

CAS  Google Scholar 

Eigenmann DE, Xue G, Kim KS, Moses AV, Hamburger M, Oufir M. Comparative study of four immortalized human brain capillary endothelial cell lines, hCMEC/D3, hBMEC, TY10, and BB19, and optimization of culture conditions, for an in vitro blood-brain barrier model for drug permeability studies. Fluids Barriers CNS. 2013;10:33.

PubMed  PubMed Central  Google Scholar 

Gonzales-Aloy E, Ahmed-Cox A, Tsoli M, Ziegler DS, Kavallaris M. From cells to organoids: the evolution of blood-brain barrier technology for modelling drug delivery in brain cancer. Adv Drug Deliv Rev. 2023;196:114777.

PubMed  CAS  Google Scholar 

Pardridge WM. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab. 2012;32:1959–72.

PubMed  PubMed Central  CAS  Google Scholar 

de Vries HE, Blom-Roosemalen MCM, Oosten Mv, de Boer AG, van Berkel TJC, Breimer DD, Kuiper J. The influence of cytokines on the integrity of the blood-brain barrier in vitro. J Neuroimmunol. 1996;64:37–43.

PubMed  Google Scholar 

Muldoon LL, Alvarez JI, Begley DJ, Boado RJ, Del Zoppo GJ, Doolittle ND, Engelhardt B, Hallenbeck JM, Lonser RR, Ohlfest JR, Prat A, Scarpa M, Smeyne RJ, Drewes LR, Neuwelt EA. Immunologic privilege in the central nervous system and the blood-brain barrier. J Cereb Blood Flow Metab. 2013;33:13–21.

PubMed  CAS  Google Scholar 

Loh LC, Locke D, Melnychuk R, Laferté S. The RGD sequence in the cytomegalovirus DNA polymerase accessory protein can mediate cell adhesion. Virology. 2000;272:302–14.

PubMed  CAS  Google Scholar 

Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol. 1996;12:697–715.

PubMed  CAS  Google Scholar 

Ludwig BS, Kessler H, Kossatz S, Reuning U. RGD-Binding integrins revisited: how recently discovered functions and Novel Synthetic ligands (Re-)Shape an ever-evolving field. Cancers (Basel), 13 (2021).

Idriss HT, Naismith JH. TNF alpha and the TNF receptor superfamily: structure-function relationship(s). Microsc Res Tech. 2000;50:184–95.

PubMed  CAS  Google Scholar 

Horton MA. The αvβ3 integrin vitronectin receptor. Int J Biochem Cell Biol. 1997;29:721–5.

PubMed  CAS  Google Scholar 

Senger DR, Ledbetter SR, Claffey KP, Papadopoulos-Sergiou A, Peruzzi CA, Detmar M. Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the alphavbeta3 integrin, osteopontin, and thrombin. Am J Pathol. 1996;149:293–305.

PubMed  PubMed Central  CAS  Google Scholar 

Singh S, Drude N, Blank L, Desai PB, Königs H, Rütten S, Langen K-J, Möller M, Mottaghy FM, Morgenroth A. Protease responsive nanogels for transcytosis across the blood– brain barrier and intracellular delivery of Radiopharmaceuticals to Brain Tumor cells. Adv Healthc Mater. 2021;10:2100812.

CAS  Google Scholar 

Snipstad S, Sulheim E, de Lange Davies C, Moonen C, Storm G, Kiessling F, Schmid R, Lammers T. Sonopermeation to improve drug delivery to tumors: from fundamental understanding to clinical translation. Expert Opin Drug Deliv. 2018;15:1249–61.

PubMed  CAS  Google Scholar 

Koczera P, Appold L, Shi Y, Liu M, Dasgupta A, Pathak V, Ojha T, Fokong S, Wu Z, van Zandvoort M, Iranzo O, Kuehne AJC, Pich A, Kiessling F, Lammers T. PBCA-based polymeric microbubbles for molecular imaging and drug delivery. J Control Release. 2017;259:128–35.

PubMed  PubMed Central  CAS  Google Scholar 

Marty B, Larrat B, Van Landeghem M, Robic C, Robert P, Port M, Le Bihan D, Pernot M, Tanter M, Lethimonnier F, Mériaux S. Dynamic study of blood-brain barrier closure after its disruption using ultrasound: a quantitative analysis. J Cereb Blood Flow Metab. 2012;32:1948–58.

PubMed  PubMed Central  Google Scholar 

Skyba DM, Price RJ, Linka AZ, Skalak TC, Kaul S. Direct in vivo visualization of intravascular destruction of microbubbles by ultrasound and its local effects on tissue. Circulation. 1998;98:290–3.

PubMed  CAS  Google Scholar 

Sassaroli E, Hynynen K. Forced linear oscillations of microbubbles in blood capillaries. J Acoust Soc Am. 2004;115:3235–43.

PubMed  CAS  Google Scholar 

Nagy JA, Benjamin L, Zeng H, Dvorak AM, Dvorak HF. Vascular permeability, vascular hyperpermeability and angiogenesis. Volume 11. Angiogenesis; 2008. pp. 109–19.

May JN, Golombek SK, Baues M, Dasgupta A, Drude N, Rix A, Rommel D, von Stillfried S, Appold L, Pola R, Pechar M, van Bloois L, Storm G, Kuehne AJC, Gremse F, Theek B, Kiessling F, Lammers T. Multimodal and multiscale optical imaging of nanomedicine delivery across the blood-brain barrier upon sonopermeation. Theranostics. 2020;10:1948–59.

PubMed  PubMed Central  CAS  Google Scholar 

Shen Y, Guo J, Chen G, Chin CT, Chen X, Chen J, Wang F, Chen S, Dan G. Delivery of liposomes with different sizes to mice Brain after Sonication by Focused Ultrasound in the Presence of Microbubbles. Ultrasound Med Biol. 2016;42:1499–511.

PubMed  Google Scholar 

Wang S, Hossack JA, Klibanov AL. Targeting of microbubbles: contrast agents for ultrasound molecular imaging. J Drug Target. 2018;26:420–34.

PubMed  PubMed Central  Google Scholar 

Dasgupta A, Sun T, Rama E, Motta A, Zhang Y, Power C, Moeckel D, Fletcher S-M, Moosavifar M, Barmin R, Porte C, Buhl EM, Bastard C, Pallares RM, Kiessling F, McDannold N, Mitragotri S, Lammers T. Transferrin Receptor-Targeted Nonspherical Microbubbles for Blood–Brain Barrier Sonopermeation, Advanced Materials, n/a 2308150.

De Lorenzi F, Hansen N, Theek B, Daware R, Motta A, Breuel S, Nasehi R, Baumeister J, Schöneberg J, Stojanović N. Engineering Mesoscopic 3D tumor models with a Self-Organizing Vascularized Matrix. Adv Mater, (2023) 2303196.

De Lorenzi NHF, Theek B, Daware R, Motta A, Breuel S, Nasehi R, Baumeister J. Jan Schöneberg, Natalija Stojanović, Saskia Von Stillfried, Michael Vogt, Gerhard Müller-Newen, Jochen Maurer, Alexandros Marios Sofias, Twan Lammers, Horst Fischer, Fabian Kiessling, Engineering Mesoscopic 3D tumor models with a Self-Organizing Vascularized Matrix. Advanced Materials; 2023.

Boitsova EB, Morgun AV, Osipova ED, Pozhilenkova EA, Martinova GP, Frolova OV, Olovannikova RY, Tohidpour A, Gorina YV, Panina YA, Salmina AB. The inhibitory effect of LPS on the expression of GPR81 lactate receptor in blood-brain barrier model in vitro. J Neuroinflammation. 2018;15:196.

PubMed  PubMed Central  Google Scholar 

Hollmann EK, Bailey AK, Potharazu AV, Neely MD, Bowman AB, Lippmann ES. Accelerated differentiation of human induced pluripotent stem cells to blood–brain barrier endothelial cells. Fluids Barriers CNS. 2017;14:9.

PubMed  PubMed Central  Google Scholar 

Canfield SG, Stebbins MJ, Morales BS, Asai SW, Vatine GD, Svendsen CN, Palecek SP, Shusta EV. An isogenic blood–brain barrier model comprising brain endothelial cells, astrocytes, and neurons derived from human induced pluri

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