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Article ; Online: High-throughput quantification of red blood cell deformability and oxygen saturation to probe mechanisms of sickle cell disease.

Williams, Dillon C / Wood, David K

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 48, Page(s) e2313755120

Abstract: The complex, systemic pathology of sickle cell disease is driven by multiple mechanisms including red blood cells (RBCs) stiffened by polymerized fibers of deoxygenated sickle hemoglobin. A critical step toward understanding the pathologic role of ... ...

Abstract	The complex, systemic pathology of sickle cell disease is driven by multiple mechanisms including red blood cells (RBCs) stiffened by polymerized fibers of deoxygenated sickle hemoglobin. A critical step toward understanding the pathologic role of polymer-containing RBCs is quantifying the biophysical changes in these cells in physiologically relevant oxygen environments. We have developed a microfluidic platform capable of simultaneously measuring single RBC deformability and oxygen saturation under controlled oxygen and shear stress. We found that RBCs with detectable amounts of polymer have decreased oxygen affinity and decreased deformability. Surprisingly, the deformability of the polymer-containing cells is oxygen-independent, while the fraction of these cells increases as oxygen decreases. We also find that some fraction of these cells is present at most physiologic oxygen tensions, suggesting a role for these cells in the systemic pathologies. Additionally, the ability to measure these pathological cells should provide clearer targets for evaluating therapies.
MeSH term(s)	Humans ; Oxygen Saturation ; Anemia, Sickle Cell ; Erythrocytes ; Erythrocyte Deformability ; Polymers ; Oxygen
Chemical Substances	Polymers ; Oxygen (S88TT14065)
Language	English
Publishing date	2023-11-20
Publishing country	United States
Document type	Journal Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2313755120
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Article ; Online: Simultaneous quantification of blood rheology and oxygen saturation to evaluate affinity-modifying therapies in sickle cell disease.

Hansen, Scott / Wood, David K

Lab on a chip

2022 Volume 22, Issue 21, Page(s) 4141–4150

Abstract: Sickle cell blood demonstrates oxygen-dependent flow behavior as a result of HbS polymerization during hypoxia, and these rheological changes provide a biophysical metric that can be used to quantify the pathological behavior of the blood. Relating these ...

Abstract	Sickle cell blood demonstrates oxygen-dependent flow behavior as a result of HbS polymerization during hypoxia, and these rheological changes provide a biophysical metric that can be used to quantify the pathological behavior of the blood. Relating these rheological changes directly to hemoglobin oxygen saturation would improve our understanding of SCD pathogenesis and the potential effects of therapeutic drugs. Towards this end, we have developed a microfluidic platform capable of spectrophotometric quantification of Hb-O
MeSH term(s)	Humans ; Oxygen Saturation ; Anemia, Sickle Cell/drug therapy ; Oxygen ; Rheology ; Hemoglobins ; Hemoglobin, Sickle/metabolism ; Hemoglobin, Sickle/therapeutic use
Chemical Substances	voxelotor (3ZO554A4Q8) ; Oxygen (S88TT14065) ; Hemoglobins ; Hemoglobin, Sickle
Language	English
Publishing date	2022-10-25
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	2056646-3
ISSN	1473-0189 ; 1473-0197
ISSN (online)	1473-0189
ISSN	1473-0197
DOI	10.1039/d2lc00623e
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Article ; Online: A scalable 3D tissue culture pipeline to enable functional therapeutic screening for pulmonary fibrosis.

Cummins, Katherine A / Bitterman, Peter B / Tschumperlin, Daniel J / Wood, David K

APL bioengineering

2021 Volume 5, Issue 4, Page(s) 46102

Abstract: Idiopathic pulmonary fibrosis (IPF) is a lethal lung disease targeting the alveolar gas exchange apparatus, leading to death by asphyxiation. IPF progresses on a tissue scale through aberrant matrix remodeling, enhanced cell contraction, and subsequent ... ...

Abstract	Idiopathic pulmonary fibrosis (IPF) is a lethal lung disease targeting the alveolar gas exchange apparatus, leading to death by asphyxiation. IPF progresses on a tissue scale through aberrant matrix remodeling, enhanced cell contraction, and subsequent microenvironment densification. Although two pharmaceuticals modestly slow progression, IPF patient survival averages less than 5 years. A major impediment to therapeutic development is the lack of high-fidelity models that account for the fibrotic microenvironment. Our goal is to create a three-dimensional (3D) platform to enable lung fibrosis studies and recapitulate IPF tissue features. We demonstrate that normal lung fibroblasts encapsulated in collagen microspheres can be pushed toward an activated phenotype, treated with FDA-approved therapies, and their fibrotic function quantified using imaging assays (extracellular matrix deposition, contractile protein expression, and microenvironment compaction). Highlighting the system's utility, we further show that fibroblasts isolated from IPF patient lungs maintain fibrotic phenotypes and manifest reduced fibrotic function when treated with epigenetic modifiers. Our system enables enhanced screening due to improved predictability and fidelity compared to 2D systems combined with superior tractability and throughput compared to 3D systems.
Language	English
Publishing date	2021-11-16
Publishing country	United States
Document type	Journal Article
ISSN	2473-2877
ISSN (online)	2473-2877
DOI	10.1063/5.0054967
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Article ; Online: Extracellular Vesicles Mediate the Intercellular Exchange of Nanoparticles.

Wu, Xian / Tang, Tang / Wei, Yushuang / Cummins, Katherine A / Wood, David K / Pang, Hong-Bo

Advanced science (Weinheim, Baden-Wurttemberg, Germany)

2022 Volume 9, Issue 7, Page(s) e2102441

Abstract: To exert their therapeutic effects, nanoparticles (NPs) often need to travel into the tissues composed of multilayered cells. Accumulative evidence has revealed the crucial role of transcellular transport route (entry into one cell, exocytosis, and re- ... ...

Abstract	To exert their therapeutic effects, nanoparticles (NPs) often need to travel into the tissues composed of multilayered cells. Accumulative evidence has revealed the crucial role of transcellular transport route (entry into one cell, exocytosis, and re-entry into another) in this process. While NP endocytosis and subcellular transport are intensively characterized, the exocytosis and re-entry steps are poorly understood, which becomes a barrier for NP delivery into complex tissues. Here, the authors term the exocytosis and re-entry steps together as intercellular exchange. A collagen-based three-dimension assay is developed to specifically quantify the intercellular exchange of NPs, and distinguish the contributions of several potential mechanisms. The authors show that NPs can be exocytosed freely or enclosed inside extracellular vesicles (EVs) for re-entry, while direct cell-cell contact is hardly involved. EVs account for a significant fraction of NP intercellular exchange, and its importance in NP transport is demonstrated in vitro and in vivo. While freely released NPs engage with the same receptors for re-entry, EV-enclosed ones bypass this dependence. These studies provide an easy and precise system to investigate the intercellular exchange stage of NP delivery, and shed the first light in the importance of EVs in NP transport between cells and into complex tissues.
MeSH term(s)	Endocytosis ; Exocytosis ; Extracellular Vesicles/metabolism ; Nanoparticles ; Transcytosis
Language	English
Publishing date	2022-01-17
Publishing country	Germany
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2808093-2
ISSN	2198-3844 ; 2198-3844
ISSN (online)	2198-3844
ISSN	2198-3844
DOI	10.1002/advs.202102441
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Article ; Online: Microfluidic methods to advance mechanistic understanding and translational research in sickle cell disease.

Azul, Melissa / Vital, Eudorah F / Lam, Wilbur A / Wood, David K / Beckman, Joan D

Translational research : the journal of laboratory and clinical medicine

2022 Volume 246, Page(s) 1–14

Abstract: Sickle cell disease (SCD) is caused by a single point mutation in the β-globin gene of hemoglobin, which produces an altered sickle hemoglobin (HbS). The ability of HbS to polymerize under deoxygenated conditions gives rise to chronic hemolysis, ... ...

Abstract	Sickle cell disease (SCD) is caused by a single point mutation in the β-globin gene of hemoglobin, which produces an altered sickle hemoglobin (HbS). The ability of HbS to polymerize under deoxygenated conditions gives rise to chronic hemolysis, oxidative stress, inflammation, and vaso-occlusion. Herein, we review recent findings using microfluidic technologies that have elucidated mechanisms of oxygen-dependent and -independent induction of HbS polymerization and how these mechanisms elicit the biophysical and inflammatory consequences in SCD pathophysiology. We also discuss how validation and use of microfluidics in SCD provides the opportunity to advance development of numerous therapeutic strategies, including curative gene therapies.
MeSH term(s)	Anemia, Sickle Cell/drug therapy ; Anemia, Sickle Cell/therapy ; Hemoglobin, Sickle ; Hemolysis ; Humans ; Microfluidics ; Translational Research, Biomedical
Chemical Substances	Hemoglobin, Sickle
Language	English
Publishing date	2022-03-27
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	2246684-8
ISSN	1878-1810 ; 1532-6543 ; 1931-5244
ISSN (online)	1878-1810 ; 1532-6543
ISSN	1931-5244
DOI	10.1016/j.trsl.2022.03.010
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Article ; Online: Rapid and inefficient kinetics of sickle hemoglobin fiber growth.

Castle, Brian T / Odde, David J / Wood, David K

Science advances

2019 Volume 5, Issue 3, Page(s) eaau1086

Abstract: In sickle cell disease, the aberrant assembly of hemoglobin fibers induces changes in red blood cell morphology and stiffness, which leads to downstream symptoms of the disease. Therefore, understanding of this assembly process will be important for the ... ...

Abstract	In sickle cell disease, the aberrant assembly of hemoglobin fibers induces changes in red blood cell morphology and stiffness, which leads to downstream symptoms of the disease. Therefore, understanding of this assembly process will be important for the treatment of sickle cell disease. By performing the highest spatiotemporal resolution measurements (55 nm at 1 Hz) of single sickle hemoglobin fiber assembly to date and combining them with a model that accounts for the multistranded structure of the fibers, we show that the rates of sickle hemoglobin addition and loss have been underestimated in the literature by at least an order of magnitude. These results reveal that the sickle hemoglobin self-assembly process is very rapid and inefficient (4% efficient versus 96% efficient based on previous analyses), where net growth is the small difference between over a million addition-loss events occurring every second.
MeSH term(s)	Anemia, Sickle Cell/blood ; Buffers ; Erythrocytes/chemistry ; Hemoglobin, Sickle/chemistry ; Hemoglobin, Sickle/ultrastructure ; Humans ; Image Processing, Computer-Assisted/statistics & numerical data ; Microscopy, Interference/methods ; Solutions ; Sulfites/chemistry
Chemical Substances	Buffers ; Hemoglobin, Sickle ; Solutions ; Sulfites ; sodium metabisulfite (4VON5FNS3C)
Language	English
Publishing date	2019-03-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2810933-8
ISSN	2375-2548 ; 2375-2548
ISSN (online)	2375-2548
ISSN	2375-2548
DOI	10.1126/sciadv.aau1086
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Article ; Online: 5-(Hydroxymethyl)furfural restores low-oxygen rheology of sickle trait blood in vitro.

Hansen, Scott / Wood, David K / Higgins, John M

British journal of haematology

2019 Volume 188, Issue 6, Page(s) 985–993

Abstract: Sickle cell trait (SCT) is the benign heterozygous carrier state for the sickle variant of the HBB gene. Most of the ~300 million people with SCT worldwide will not experience any significant complications. However, accumulating evidence finds SCT ... ...

Abstract	Sickle cell trait (SCT) is the benign heterozygous carrier state for the sickle variant of the HBB gene. Most of the ~300 million people with SCT worldwide will not experience any significant complications. However, accumulating evidence finds SCT associated with increased risk for the common conditions of chronic kidney disease and venous thromboembolism, and severe but rare renal medullary carcinoma and exercise-induced rhabdomyolysis. The mechanism is uncertain, but probably involves pathological rheology of SCT blood in regions of low oxygen tension, resulting from sickle haemoglobin polymerization in SCT red cells and leading to reduced blood flow and further tissue hypoxia and damage. Here, we used an in vitro microfluidic flow system to study the oxygen-dependent rheology of SCT blood and show that 5-(hydroxymethyl)furfural, a natural breakdown product of glucose and fructose-containing foods, such as fruit juices, can reduce the effects of hypoxia on SCT blood rheology in vitro, restoring near-normal flow velocities at very low oxygen. While opinions regarding the clinical significance of the risks associated with SCT are still evolving, these results suggest that a compound present in some food may provide a potential approach for managing risks that may be associated with SCT.
MeSH term(s)	Blood Viscosity ; Furaldehyde/analogs & derivatives ; Furaldehyde/pharmacology ; Furaldehyde/therapeutic use ; Humans ; Oxygen/blood ; Rheology ; Sickle Cell Trait/blood ; Sickle Cell Trait/drug therapy
Chemical Substances	5-hydroxymethylfurfural (70ETD81LF0) ; Furaldehyde (DJ1HGI319P) ; Oxygen (S88TT14065)
Language	English
Publishing date	2019-12-30
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80077-6
ISSN	1365-2141 ; 0007-1048
ISSN (online)	1365-2141
ISSN	0007-1048
DOI	10.1111/bjh.16251
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Article ; Online: Microscale Collagen and Fibroblast Interactions Enhance Primary Human Hepatocyte Functions in Three-Dimensional Models.

Kukla, David A / Crampton, Alexandra L / Wood, David K / Khetani, Salman R

Gene expression

2020 Volume 20, Issue 1, Page(s) 1–18

Abstract: Human liver models that are three-dimensional (3D) in architecture are indispensable for compound metabolism/toxicity screening, to model liver diseases for drug discovery, and for cell-based therapies; however, further development of such models is ... ...

Abstract	Human liver models that are three-dimensional (3D) in architecture are indispensable for compound metabolism/toxicity screening, to model liver diseases for drug discovery, and for cell-based therapies; however, further development of such models is needed to maintain high levels of primary human hepatocyte (PHH) functions for weeks to months. Therefore, here we determined how microscale 3D collagen I presentation and fibroblast interaction affect the longevity of PHHs. High-throughput droplet microfluidics was utilized to generate reproducibly sized (∼300-μm diameter) microtissues containing PHHs encapsulated in collagen I ± supportive fibroblasts, namely, 3T3-J2 murine embryonic fibroblasts or primary human hepatic stellate cells (HSCs); self-assembled spheroids and bulk collagen gels (macrogels) containing PHHs served as controls. Hepatic functions and gene expression were subsequently measured for up to 6 weeks. We found that microtissues placed within multiwell plates rescued PHH functions at 2- to 30-fold higher levels than spheroids or macrogels. Further coating of PHH microtissues with 3T3-J2s led to higher hepatic functions than when the two cell types were either coencapsulated together or when HSCs were used for the coating instead. Importantly, the 3T3-J2-coated PHH microtissues displayed 6+ weeks of relatively stable hepatic gene expression and function at levels similar to freshly thawed PHHs. Lastly, microtissues responded in a clinically relevant manner to drug-mediated cytochrome P450 induction or hepatotoxicity. In conclusion, fibroblast-coated collagen microtissues containing PHHs display high hepatic functions for 6+ weeks and are useful for assessing drug-mediated CYP induction and hepatotoxicity. Ultimately, microtissues may find utility for modeling liver diseases and as building blocks for cell-based therapies.
MeSH term(s)	3T3 Cells/cytology ; Animals ; Cell Encapsulation ; Cells, Cultured ; Coculture Techniques/methods ; Collagen Type I/chemistry ; Cytochrome P-450 Enzyme System/biosynthesis ; Enzyme Induction/drug effects ; Gels ; Gene Expression ; Hepatic Stellate Cells/cytology ; Hepatocytes/cytology ; Humans ; Lab-On-A-Chip Devices ; Mice ; Omeprazole/pharmacology ; Polymerization ; Rifampin/pharmacology ; Spheroids, Cellular ; Tissue Engineering/instrumentation ; Tissue Engineering/methods
Chemical Substances	Collagen Type I ; Gels ; Cytochrome P-450 Enzyme System (9035-51-2) ; Omeprazole (KG60484QX9) ; Rifampin (VJT6J7R4TR)
Language	English
Publishing date	2020-04-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1151108-4
ISSN	1555-3884 ; 1052-2116
ISSN (online)	1555-3884
ISSN	1052-2116
DOI	10.3727/105221620X15868728381608
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Article ; Online: An Experimental-Computational Approach to Quantify Blood Rheology in Sickle Cell Disease.

Bazzi, Marisa S / Valdez, José M / Barocas, Victor H / Wood, David K

Biophysical journal

2020 Volume 119, Issue 11, Page(s) 2307–2315

Abstract: In sickle cell disease, aberrant blood flow due to oxygen-dependent changes in red cell biomechanics is a key driver of pathology. Most studies to date have focused on the potential role of altered red cell deformability and blood rheology in ... ...

Abstract	In sickle cell disease, aberrant blood flow due to oxygen-dependent changes in red cell biomechanics is a key driver of pathology. Most studies to date have focused on the potential role of altered red cell deformability and blood rheology in precipitating vaso-occlusive crises. Numerous studies, however, have shown that sickle blood flow is affected even at high oxygen tensions, suggesting a potentially systemic role for altered blood flow in driving pathologies, including endothelial dysfunction, ischemia, and stroke. In this study, we applied a combined experimental-computation approach that leveraged an experimental platform that quantifies sickle blood velocity fields under a range of oxygen tensions and shear rates. We computationally fitted a continuum model to our experimental data to generate physics-based parameters that capture patient-specific rheological alterations. Our results suggest that sickle blood flow is altered systemically, from the arterial to the venous circulation. We also demonstrated the application of this approach as a tool to design patient-specific transfusion regimens. Finally, we demonstrated that patient-specific rheological parameters can be combined with patient-derived vascular models to identify patients who are at higher risk for cerebrovascular complications such as aneurysm and stroke. Overall, this study highlights that sickle blood flow is altered systemically, which can drive numerous pathologies, and this study demonstrates the potential utility of an experimentally parameterized continuum model as a predictive tool for patient-specific care.
MeSH term(s)	Anemia, Sickle Cell ; Erythrocyte Deformability ; Erythrocytes ; Humans ; Rheology
Language	English
Publishing date	2020-10-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	218078-9
ISSN	1542-0086 ; 0006-3495
ISSN (online)	1542-0086
ISSN	0006-3495
DOI	10.1016/j.bpj.2020.10.011
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Article ; Online: A high-throughput microtissue platform to probe endothelial function in vitro.

Crampton, Alexandra L / Cummins, Katherine A / Wood, David K

Integrative biology : quantitative biosciences from nano to macro

2018 Volume 10, Issue 9, Page(s) 555–565

Abstract: A critical role of vascular endothelium is as a semi-permeable barrier, dynamically regulating the flux of solutes between blood and the surrounding tissue. Existing platforms that quantify endothelial function in vitro are either significantly ... ...

Abstract	A critical role of vascular endothelium is as a semi-permeable barrier, dynamically regulating the flux of solutes between blood and the surrounding tissue. Existing platforms that quantify endothelial function in vitro are either significantly throughput limited or overlook physiologically relevant extracellular matrix (ECM) interactions and thus do not recapitulate in vivo function. Leveraging droplet microfluidics, we developed a scalable platform to measure endothelial function in nanoliter-volume, ECM-based microtissues. In this study, we describe our high-throughput method for fabricating endothelial-coated collagen microtissues that incorporate physiologically relevant cell-ECM interactions. We showed that the endothelial cells had characteristic morphology, expressed tight junction proteins, and remodeled the ECM via compaction and deposition of basement membrane. We also measured macromolecular permeability using two optical modalities, and found the cell layers: (1) had permeability values comparable to in vivo measurements and (2) were responsive to physiologically-relevant modulators of endothelial permeability (TNF-α and TGF-β). This is the first demonstration, to the authors' knowledge, of high-throughput assessment (n > 150) of endothelial permeability on natural ECM. Additionally, this technology is compatible with standard cell culture equipment (e.g. multi-well plates) and could be scaled up further to be integrated with automated liquid handling systems and automated imaging platforms. Overall, this platform recapitulates the functions of traditional transwell inserts, but extends application to high-throughput studies and introduces new possibilities for interrogating cell-cell and cell-matrix interactions.
MeSH term(s)	Animals ; Anisotropy ; Basement Membrane/physiology ; Cell Communication ; Cell Culture Techniques/methods ; Cells, Cultured ; Endothelial Cells/cytology ; Endothelium, Vascular/physiology ; Extracellular Matrix/physiology ; Macromolecular Substances ; Microfluidics ; Permeability ; Rats ; Transforming Growth Factor beta/metabolism ; Tumor Necrosis Factor-alpha/metabolism
Chemical Substances	Macromolecular Substances ; Transforming Growth Factor beta ; Tumor Necrosis Factor-alpha
Language	English
Publishing date	2018-08-23
Publishing country	England
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	2480063-6
ISSN	1757-9708 ; 1757-9694
ISSN (online)	1757-9708
ISSN	1757-9694
DOI	10.1039/c8ib00111a
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