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Article ; Online: Effects of Drag-Reducing Polymers on Hemodynamics and Whole Blood-Endothelial Interactions in 3D-Printed Vascular Topologies.

Paone, Louis S / Szkolnicki, Matthew / DeOre, Brandon J / Tran, Kiet A / Goldman, Noah / Andrews, Allison M / Ramirez, Servio H / Galie, Peter A

ACS applied materials & interfaces

2024 Volume 16, Issue 12, Page(s) 14457–14466

Abstract: Most in vitro models use culture medium to apply fluid shear stress to endothelial cells, which does not capture the interaction between blood and endothelial cells. Here, we describe a new system to characterize whole blood flow through a 3D-printed, ... ...

Abstract	Most in vitro models use culture medium to apply fluid shear stress to endothelial cells, which does not capture the interaction between blood and endothelial cells. Here, we describe a new system to characterize whole blood flow through a 3D-printed, endothelialized vascular topology that induces flow separation at a bifurcation. Drag-reducing polymers, which have been previously studied as a potential therapy to reduce the pressure drop across the vascular bed, are evaluated for their effect on mitigating the disturbed flow. Polymer concentrations of 1000 ppm prevented recirculation and disturbed flow at the wall. Proteomic analysis of plasma collected from whole blood recirculated through the vascularized channel with and without drag-reducing polymers provides insight into the effects of flow regimes on levels of proteins indicative of the endothelial-blood interaction. The results indicate that blood flow alters proteins associated with coagulation, inflammation, and other processes. Overall, these proof-of-concept experiments demonstrate the importance of using whole blood flow to study the endothelial response to perfusion.
MeSH term(s)	Polymers/pharmacology ; Endothelial Cells ; Proteomics ; Hemodynamics/physiology ; Printing, Three-Dimensional ; Stress, Mechanical
Chemical Substances	Polymers
Language	English
Publishing date	2024-03-15
Publishing country	United States
Document type	Journal Article
ISSN	1944-8252
ISSN (online)	1944-8252
DOI	10.1021/acsami.3c17099
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Article ; Online: Implementation and characterization of a physiologically relevant flow waveform in a 3D microfluidic model of the blood-brain barrier.

Bouhrira, Nesrine / DeOre, Brandon J / Galie, Peter A

Biotechnology and bioengineering

2021 Volume 118, Issue 7, Page(s) 2411–2421

Abstract: Previous in vitro studies interrogating the endothelial response to physiologically relevant flow regimes require specialized pumps to deliver time-dependent waveforms that imitate in vivo blood flow. The aim of this study is to create a low-cost and ... ...

Abstract	Previous in vitro studies interrogating the endothelial response to physiologically relevant flow regimes require specialized pumps to deliver time-dependent waveforms that imitate in vivo blood flow. The aim of this study is to create a low-cost and broadly adaptable approach to mimic physiological flow, and then use this system to characterize the effect of flow separation on velocity and shear stress profiles in a three-dimensional (3D) topology. The flow apparatus incorporates a programmable linear actuator that superposes oscillations on a constant mean flow driven by a peristaltic pump to emulate flow in the carotid artery. The flow is perfused through a 3D in vitro model of the blood-brain barrier designed to induce separated flow. Experimental flow patterns measured by microparticle image velocimetry and modeled by computational fluid dynamics reveal periodic changes in the instantaneous shear stress along the channel wall. Moreover, the time-dependent flow causes periodic flow separation zones, resulting in variable reattachment points during the cycle. The effects of these complex flow regimes are assessed by evaluating the integrity of the in vitro blood-brain barrier model. Permeability assays and immunostaining for proteins associated with tight junctions reveal barrier breakdown in the region of disturbed flow. In conclusion, the flow system described here creates complex, physiologically relevant flow profiles that provide deeper insight into the fluid dynamics of separated flow and pave the way for future studies interrogating the cellular response to complex flow regimes.
MeSH term(s)	Blood-Brain Barrier/cytology ; Blood-Brain Barrier/metabolism ; Cell Culture Techniques ; Humans ; Lab-On-A-Chip Devices ; Microfluidic Analytical Techniques ; Models, Cardiovascular ; Tight Junctions/metabolism
Language	English
Publishing date	2021-04-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	280318-5
ISSN	1097-0290 ; 0006-3592
ISSN (online)	1097-0290
ISSN	0006-3592
DOI	10.1002/bit.27719
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Article ; Online: Transcriptomic analysis of a 3D blood-brain barrier model exposed to disturbed fluid flow.

Bouhrira, Nesrine / DeOre, Brandon J / Tran, Kiet A / Galie, Peter A

Fluids and barriers of the CNS

2022 Volume 19, Issue 1, Page(s) 94

Abstract: Cerebral aneurysms are more likely to form at bifurcations in the vasculature, where disturbed fluid is prevalent due to flow separation at sufficiently high Reynolds numbers. While previous studies have demonstrated that altered shear stress exerted by ... ...

Abstract	Cerebral aneurysms are more likely to form at bifurcations in the vasculature, where disturbed fluid is prevalent due to flow separation at sufficiently high Reynolds numbers. While previous studies have demonstrated that altered shear stress exerted by disturbed flow disrupts endothelial tight junctions, less is known about how these flow regimes alter gene expression in endothelial cells lining the blood-brain barrier. Specifically, the effect of disturbed flow on expression of genes associated with cell-cell and cell-matrix interaction, which likely mediate aneurysm formation, remains unclear. RNA sequencing of immortalized cerebral endothelial cells isolated from the lumen of a 3D blood-brain barrier model reveals distinct transcriptional changes in vessels exposed to fully developed and disturbed flow profiles applied by both steady and physiological waveforms. Differential gene expression, validated by qRT-PCR and western blotting, reveals that lumican, a small leucine-rich proteoglycan, is the most significantly downregulated gene in endothelial cells exposed to steady, disturbed flow. Knocking down lumican expression reduces barrier function in the presence of steady, fully developed flow. Moreover, adding purified lumican into the hydrogel of the 3D blood-brain barrier model recovers barrier function in the region exposed to fully developed flow. Overall, these findings emphasize the importance of flow regimes exhibiting spatial and temporal heterogeneous shear stress profiles on cell-matrix interaction in endothelial cells lining the blood-brain barrier, while also identifying lumican as a contributor to the formation and maintenance of an intact barrier.
MeSH term(s)	Blood-Brain Barrier ; Lumican ; Endothelial Cells ; Transcriptome ; Biological Transport
Chemical Substances	Lumican
Language	English
Publishing date	2022-11-24
Publishing country	England
Document type	Journal Article
ZDB-ID	2595406-4
ISSN	2045-8118 ; 2045-8118
ISSN (online)	2045-8118
ISSN	2045-8118
DOI	10.1186/s12987-022-00389-x
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Article ; Online: CD44 mediates shear stress mechanotransduction in an in vitro blood-brain barrier model through small GTPases RhoA and Rac1.

DeOre, Brandon J / Partyka, Paul P / Fan, Fan / Galie, Peter A

FASEB journal : official publication of the Federation of American Societies for Experimental Biology

2022 Volume 36, Issue 5, Page(s) e22278

Abstract: Fluid shear stress is an important mediator of vascular permeability, yet the molecular mechanisms underlying the effect of shear on the blood-brain barrier (BBB) have yet to be clarified in cerebral vasculature despite its importance for brain ... ...

Abstract	Fluid shear stress is an important mediator of vascular permeability, yet the molecular mechanisms underlying the effect of shear on the blood-brain barrier (BBB) have yet to be clarified in cerebral vasculature despite its importance for brain homeostasis. The goal of this study is to probe components of shear mechanotransduction within the BBB to gain a better understanding of pathologies associated with changes in cerebral perfusion including ischemic stroke. Interrogating the effects of shear stress in vivo is complicated by the complexity of factors in the brain parenchyma and the difficulty associated with modulating blood flow regimes. The in vitro model used in this study is compatible with real-time measurement of barrier function using a transendothelial electrical resistance as well as immunocytochemistry and dextran permeability assays. These experiments reveal that there is a threshold level of shear stress required for barrier formation and that the composition of the extracellular matrix, specifically the presence of high molecular weight hyaluronan, dictates the flow response. Gene editing to modulate the expression of CD44, a mechanosensitive receptor for hyaluronan, demonstrates that the receptor is required for the endothelial response to shear stress. Manipulation of small GTPase activity reveals CD44 activates Rac1 while inhibiting RhoA activation. Additionally, adducin-γ localizes to tight junctions in response to shear stress and RhoA inhibition and is required to maintain the barrier. This study identifies specific components of the mechanosensing complex associated with the BBB response to fluid shear stress and, therefore, illuminates potential targets for barrier manipulation in vivo.
MeSH term(s)	Blood-Brain Barrier/metabolism ; Capillary Permeability/physiology ; Hyaluronic Acid/metabolism ; Mechanotransduction, Cellular ; Monomeric GTP-Binding Proteins/metabolism
Chemical Substances	Hyaluronic Acid (9004-61-9) ; Monomeric GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2022-04-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	639186-2
ISSN	1530-6860 ; 0892-6638
ISSN (online)	1530-6860
ISSN	0892-6638
DOI	10.1096/fj.202100822RR
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Zs.A 2266: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Oxygen gradients dictate angiogenesis but not barriergenesis in a 3D brain microvascular model.

Tran, Kiet A / Baldwin-Leclair, Abigail / DeOre, Brandon J / Antisell, Morgan / Galie, Peter A

Journal of cellular physiology

2022 Volume 237, Issue 10, Page(s) 3872–3882

Abstract: A variety of biophysical properties are known to regulate angiogenic sprouting, and in vitro systems can parse the individual effects of these factors in a controlled setting. Here, a three-dimensional brain microvascular model interrogates how variables ...

Abstract	A variety of biophysical properties are known to regulate angiogenic sprouting, and in vitro systems can parse the individual effects of these factors in a controlled setting. Here, a three-dimensional brain microvascular model interrogates how variables including extracellular matrix composition, fluid shear stress, and radius of curvature affect angiogenic sprouting of cerebral endothelial cells. Tracking endothelial migration over several days reveals that application of fluid shear stress and enlarged vessel radius of curvature both attenuate sprouting. Computational modeling informed by oxygen consumption assays suggests that sprouting correlates to reduced oxygen concentration: both fluid shear stress and vessel geometry alter the local oxygen levels dictated by both ambient conditions and cellular respiration. Moreover, increasing cell density and consequently lowering the local oxygen levels yields significantly more sprouting. Further analysis reveals that the magnitude of oxygen concentration is not as important as its spatial concentration gradient: decreasing ambient oxygen concentration causes significantly less sprouting than applying an external oxygen gradient to the vessels. In contrast, barriergenesis is dictated by shear stress independent of local oxygen concentrations, suggesting that different mechanisms mediate angiogenesis and barrier formation and that angiogenic sprouting can occur without compromising the barrier. Overall, these results improve our understanding of how specific biophysical variables regulate the function and activation of cerebral vasculature, and identify spatial oxygen gradients as the driving factor of angiogenesis in the brain.
MeSH term(s)	Brain/metabolism ; Endothelial Cells ; Humans ; Neovascularization, Pathologic ; Neovascularization, Physiologic ; Oxygen/pharmacology ; Vascular Endothelial Growth Factor A/metabolism
Chemical Substances	Vascular Endothelial Growth Factor A ; Oxygen (S88TT14065)
Language	English
Publishing date	2022-07-28
Publishing country	United States
Document type	Journal Article
ZDB-ID	3116-1
ISSN	1097-4652 ; 0021-9541
ISSN (online)	1097-4652
ISSN	0021-9541
DOI	10.1002/jcp.30840
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Article ; Online: SARS-CoV-2 Spike Protein Disrupts Blood-Brain Barrier Integrity via RhoA Activation.

DeOre, Brandon J / Tran, Kiet A / Andrews, Allison M / Ramirez, Servio H / Galie, Peter A

Journal of neuroimmune pharmacology : the official journal of the Society on NeuroImmune Pharmacology

2021 Volume 16, Issue 4, Page(s) 722–728

Abstract: The SARS-CoV-2 spike protein has been shown to disrupt blood-brain barrier (BBB) function, but its pathogenic mechanism of action is unknown. Whether angiotensin converting enzyme 2 (ACE2), the viral binding site for SARS-CoV-2, contributes to the spike ... ...

Abstract	The SARS-CoV-2 spike protein has been shown to disrupt blood-brain barrier (BBB) function, but its pathogenic mechanism of action is unknown. Whether angiotensin converting enzyme 2 (ACE2), the viral binding site for SARS-CoV-2, contributes to the spike protein-induced barrier disruption also remains unclear. Here, a 3D-BBB microfluidic model was used to interrogate mechanisms by which the spike protein may facilitate barrier dysfunction. The spike protein upregulated the expression of ACE2 in response to laminar shear stress. Moreover, interrogating the role of ACE2 showed that knock-down affected endothelial barrier properties. These results identify a possible role of ACE2 in barrier homeostasis. Analysis of RhoA, a key molecule in regulating endothelial cytoskeleton and tight junction complex dynamics, reveals that the spike protein triggers RhoA activation. Inhibition of RhoA with C3 transferase rescues its effect on tight junction disassembly. Overall, these results indicate a possible means by which the engagement of SARS-CoV-2 with ACE2 facilitates disruption of the BBB via RhoA activation. Understanding how SARS-CoV-2 dysregulates the BBB may lead to strategies to prevent the neurological deficits seen in COVID-19 patients.
MeSH term(s)	Blood-Brain Barrier/metabolism ; COVID-19 ; Humans ; Protein Binding ; SARS-CoV-2 ; Spike Glycoprotein, Coronavirus ; rhoA GTP-Binding Protein
Chemical Substances	Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2 ; RHOA protein, human (124671-05-2) ; rhoA GTP-Binding Protein (EC 3.6.5.2)
Language	English
Publishing date	2021-10-23
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2227405-4
ISSN	1557-1904 ; 1557-1890
ISSN (online)	1557-1904
ISSN	1557-1890
DOI	10.1007/s11481-021-10029-0
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Article ; Online: Fluid flow rate dictates the efficacy of low-intensity anti-vascular ultrasound therapy in a microfluidic model.

DeOre, Brandon J / Galie, Peter A / Sehgal, Chandra M

Microcirculation (New York, N.Y. : 1994)

2019 Volume 26, Issue 7, Page(s) e12576

Abstract: Objective: Low-intensity anti-vascular ultrasound therapy is an effective means of disrupting the blood supply in the tumor microenvironment. Its diminished effect on the surrounding vasculature is thought to be due to higher blood flow rates outside ... ...

Abstract	Objective: Low-intensity anti-vascular ultrasound therapy is an effective means of disrupting the blood supply in the tumor microenvironment. Its diminished effect on the surrounding vasculature is thought to be due to higher blood flow rates outside the tumor that decreases the interaction time between the endothelial lining and the microbubbles, which transduce acoustic energy to thermal heat. However, investigating the effect of circulation rate on the response to low-intensity ultrasound is complicated by the heterogeneity of the in vivo vascular microenvironment. Here, a 3D microfluidic model is used to directly interrogate the dynamics of ultrasound stimulation. Methods: A 3D in vitro vessel consisting of LifeACT transfected endothelial cells facilitate real-time analysis of actin dynamics during ultrasound treatment. Using an integrated testing platform, both the flow rate of microbubbles within the vessel and the magnitude of insonation can be varied. Results: Morphological measurements and dextran transport assays indicate that lower flow rates exacerbate the effect of low-intensity ultrasound on vessel integrity. Additionally, immunostaining for VE-cadherin and transmission electron microscopy provide further insight into structural changes in cell-cell junctions following insonation. Conclusions: Overall, these results reveal that blood flow rate is an important parameter to consider during the refinement of anti-vascular low-intensity ultrasound therapies.
MeSH term(s)	Antigens, CD/metabolism ; Cadherins/metabolism ; Endothelial Cells/metabolism ; Endothelial Cells/pathology ; Humans ; Microfluidics ; Models, Cardiovascular ; Neoplasms/blood supply ; Neoplasms/metabolism ; Neoplasms/pathology ; Neoplasms/therapy ; Neovascularization, Pathologic/metabolism ; Neovascularization, Pathologic/pathology ; Neovascularization, Pathologic/therapy ; Tumor Microenvironment ; Ultrasonic Therapy
Chemical Substances	Antigens, CD ; Cadherins ; cadherin 5
Language	English
Publishing date	2019-08-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1217758-1
ISSN	1549-8719 ; 1073-9688
ISSN (online)	1549-8719
ISSN	1073-9688
DOI	10.1111/micc.12576
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Article ; Online: Magnetic alignment of injectable hydrogel scaffolds for spinal cord injury repair.

Tran, Kiet A / Jin, Ying / Bouyer, Julien / DeOre, Brandon J / Suprewicz, Łukasz / Figel, Ana / Walens, Hannah / Fischer, Itzhak / Galie, Peter A

Biomaterials science

2022 Volume 10, Issue 9, Page(s) 2237–2247

Abstract: Injectable hydrogels for cell delivery and tissue regeneration have several advantages over pre-fabricated scaffolds that require more invasive transplantation procedures, but lack the ability to implement tunable topologies. Here, we describe an ... ...

Abstract	Injectable hydrogels for cell delivery and tissue regeneration have several advantages over pre-fabricated scaffolds that require more invasive transplantation procedures, but lack the ability to implement tunable topologies. Here, we describe an approach to create patternable and injectable scaffolds using magnetically-responsive (MR) self-assembling peptide hydrogels, and validate their efficacy to promote and align axon infiltration at the site of a spinal cord injury.
MeSH term(s)	Humans ; Hydrogels/pharmacology ; Magnetic Phenomena ; Peptides ; Spinal Cord ; Spinal Cord Injuries/therapy ; Tissue Scaffolds
Chemical Substances	Hydrogels ; Peptides
Language	English
Publishing date	2022-05-04
Publishing country	England
Document type	Journal Article
ZDB-ID	2693928-9
ISSN	2047-4849 ; 2047-4830
ISSN (online)	2047-4849
ISSN	2047-4830
DOI	10.1039/d1bm01590g
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Article ; Online: Matching mechanical heterogeneity of the native spinal cord augments axon infiltration in 3D-printed scaffolds.

Tran, Kiet A / DeOre, Brandon J / Ikejiani, David / Means, Kristen / Paone, Louis S / De Marchi, Laura / Suprewicz, Łukasz / Koziol, Katarina / Bouyer, Julien / Byfield, Fitzroy J / Jin, Ying / Georges, Penelope / Fischer, Itzhak / Janmey, Paul A / Galie, Peter A

Biomaterials

2023 Volume 295, Page(s) 122061

Abstract: Scaffolds delivered to injured spinal cords to stimulate axon connectivity often match the anisotropy of native tissue using guidance cues along the rostral-caudal axis, but current approaches do not mimic the heterogeneity of host tissue mechanics. ... ...

Abstract	Scaffolds delivered to injured spinal cords to stimulate axon connectivity often match the anisotropy of native tissue using guidance cues along the rostral-caudal axis, but current approaches do not mimic the heterogeneity of host tissue mechanics. Although white and gray matter have different mechanical properties, it remains unclear whether tissue mechanics also vary along the length of the cord. Mechanical testing performed in this study indicates that bulk spinal cord mechanics do differ along anatomical level and that these differences are caused by variations in the ratio of white and gray matter. These results suggest that scaffolds recreating the heterogeneity of spinal cord tissue mechanics must account for the disparity between gray and white matter. Digital light processing (DLP) provides a means to mimic spinal cord topology, but has previously been limited to printing homogeneous mechanical properties. We describe a means to modify DLP to print scaffolds that mimic spinal cord mechanical heterogeneity caused by variation in the ratio of white and gray matter, which improves axon infiltration compared to controls exhibiting homogeneous mechanical properties. These results demonstrate that scaffolds matching the mechanical heterogeneity of white and gray matter improve the effectiveness of biomaterials transplanted within the injured spinal cord.
MeSH term(s)	Humans ; Spinal Cord Injuries ; Spinal Cord ; Axons ; Biocompatible Materials ; Printing, Three-Dimensional ; Tissue Scaffolds
Chemical Substances	Biocompatible Materials
Language	English
Publishing date	2023-02-16
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	603079-8
ISSN	1878-5905 ; 0142-9612
ISSN (online)	1878-5905
ISSN	0142-9612
DOI	10.1016/j.biomaterials.2023.122061
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Article ; Online: Microindentation of Fluid-Filled Cellular Domes Reveals the Contribution of RhoA-ROCK Signaling to Multicellular Mechanics.

DeOre, Brandon J / Baldwin-LeClair, Abigail / Tran, Kiet A / DaSilva, Angelica / Byfield, Fitzroy J / Janmey, Paul A / Galie, Peter A

Small (Weinheim an der Bergstrasse, Germany)

2022 Volume 18, Issue 21, Page(s) e2200883

Abstract: Cellular mechanics encompass both mechanical properties that resist forces applied by the external environment and internally generated forces applied at the location of cell-cell and cell-matrix junctions. Here, the authors demonstrate that ... ...

Abstract	Cellular mechanics encompass both mechanical properties that resist forces applied by the external environment and internally generated forces applied at the location of cell-cell and cell-matrix junctions. Here, the authors demonstrate that microindentation of cellular domes formed by cell monolayers that locally lift off the substrate provides insight into both aspects of cellular mechanics in multicellular structures. Using a modified Hertz contact equation, the force-displacement curves generated by a micro-tensiometer are used to measure an effective dome stiffness. The results indicate the domes are consistent with the Laplace-Young relationship for elastic membranes, regardless of biochemical modulation of the RhoA-ROCK signaling axis. In contrast, activating RhoA, and inhibiting ROCK both alter the relaxation dynamics of the domes deformed by the micro-tensiometer, revealing an approach to interrogate the role of RhoA-ROCK signaling in multicellular mechanics. A finite element model incorporating a Mooney-Rivlin hyperelastic constitutive equation to describe monolayer mechanics predicts effective stiffness values that are consistent with the micro-tensiometer measurements, verifying previous measurements of the response of cell monolayers to tension. Overall, these studies establish microindentation of fluid-filled domes as an avenue to investigate the contribution of cell-generated forces to the mechanics of multicellular structures.
MeSH term(s)	Signal Transduction
Language	English
Publishing date	2022-04-21
Publishing country	Germany
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2168935-0
ISSN	1613-6829 ; 1613-6810
ISSN (online)	1613-6829
ISSN	1613-6810
DOI	10.1002/smll.202200883
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