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Article: Integrating Shear Flow and Trypsin Treatment to Assess Cell Adhesion Strength.

Patel, Antra / Bhavanam, Bhavana / Keenan, Trevor / Maruthamuthu, Venkat

bioRxiv : the preprint server for biology

2023

Abstract: Cell adhesion is of fundamental importance in cell and tissue organization, and for designing cell-laden constructs for tissue engineering. Prior methods to assess cell adhesion strength for strongly adherent cells using hydrodynamic shear flow either ... ...

Abstract	Cell adhesion is of fundamental importance in cell and tissue organization, and for designing cell-laden constructs for tissue engineering. Prior methods to assess cell adhesion strength for strongly adherent cells using hydrodynamic shear flow either involved the use of specialized flow devices to generate high shear stress or used simpler implementations like larger height parallel plate chambers that enable multi-hour cell culture but generate low shear stress and are hence more applicable for weakly adherent cells. Here, we propose a shear flow assay for adhesion strength assessment of strongly adherent cells that employs off-the-shelf parallel plate chambers for shear flow as well as simultaneous trypsin treatment to tune down the adhesion strength of cells. We implement the assay with a strongly adherent cell type and show that shear stress in the 0.07 to 7 Pa range is sufficient to dislodge the cells with simultaneous trypsin treatment. Imaging of cells over a square centimeter area allows cell morphological analysis of hundreds of cells. We show that the cell area of cells that are dislodged, on average, does not monotonically increase with shear stress at the higher end of shear stresses used and suggest that this can be explained by the likely higher resistance of high circularity cells to trypsin digestion. The adhesion strength assay proposed can be easily adapted by labs to assess the adhesion strength of both weakly and strongly adherent cell types and has the potential to be adapted for substrate stiffness-dependent adhesion strength assessment in mechanobiology studies.
Language	English
Publishing date	2023-09-28
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.26.559598
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Article ; Online: Integrating shear flow and trypsin treatment to assess cell adhesion strength.

Patel, Antra / Bhavanam, Bhavana / Keenan, Trevor / Maruthamuthu, Venkat

Biointerphases

2023 Volume 18, Issue 6

Abstract: Cell adhesion is of fundamental importance in cell and tissue organization and for designing cell-laden constructs for tissue engineering. Prior methods to assess cell adhesion strength for strongly adherent cells using hydrodynamic shear flow either ... ...

Abstract	Cell adhesion is of fundamental importance in cell and tissue organization and for designing cell-laden constructs for tissue engineering. Prior methods to assess cell adhesion strength for strongly adherent cells using hydrodynamic shear flow either involved the use of specialized flow devices to generate high shear stress or used simpler implementations like larger height parallel plate chambers that enable multihour cell culture but generate low wall shear stress and are, hence, more applicable for weakly adherent cells. Here, we propose a shear flow assay for adhesion strength assessment of strongly adherent cells that employs off-the-shelf parallel plate chambers for shear flow as well as simultaneous trypsin treatment to tune down the adhesion strength of cells. We implement the assay with a strongly adherent cell type and show that wall shear stress in the 0.07-7 Pa range is sufficient to dislodge the cells with simultaneous trypsin treatment. Imaging of cells over a square centimeter area allows cell morphological analysis of hundreds of cells. We show that the cell area of cells that are dislodged, on average, does not monotonically increase with wall shear stress at the higher end of wall shear stresses used and suggest that this can be explained by the likely higher resistance of high circularity cells to trypsin digestion. The adhesion strength assay proposed can be used to assess the adhesion strength of both weakly and strongly adherent cell types and has the potential to be adapted for substrate stiffness-dependent adhesion strength assessment in mechanobiology studies.
MeSH term(s)	Cell Adhesion ; Trypsin ; Stress, Mechanical
Chemical Substances	Trypsin (EC 3.4.21.4)
Language	English
Publishing date	2023-12-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	2234510-3
ISSN	1559-4106 ; 1559-4106
ISSN (online)	1559-4106
ISSN	1559-4106
DOI	10.1116/6.0003028
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Article: α-Catenin Dependent E-cadherin Adhesion Dynamics as Revealed by an Accelerated Force Ramp.

Bush, Joshua / Cabe, Jolene I / Conway, Daniel / Maruthamuthu, Venkat

bioRxiv : the preprint server for biology

2023

Abstract: Tissue remodeling and shape changes often rely on force-induced cell rearrangements occurring via cell-cell contact dynamics. Epithelial cell-cell contact shape changes are particularly dependent upon E-cadherin adhesion dynamics which are directly ... ...

Abstract	Tissue remodeling and shape changes often rely on force-induced cell rearrangements occurring via cell-cell contact dynamics. Epithelial cell-cell contact shape changes are particularly dependent upon E-cadherin adhesion dynamics which are directly influenced by cell-generated and external forces. While both the mobility of E-cadherin adhesions and their adhesion strength have been reported before, it is not clear how these two aspects of E-cadherin adhesion dynamics are related. Here, using magnetic pulling cytometry, we applied an accelerated force ramp on the E-cadherin adhesion between an E-cadherin-coated magnetic microbead and an epithelial cell to ascertain this relationship. Our approach enables the determination of the adhesion strength and force-dependent mobility of individual adhesions, which revealed a direct correlation between these key characteristics. Since α-catenin has previously been reported to play a role in both E-cadherin mobility and adhesion strength when studied independently, we also probed epithelial cells in which α-catenin has been knocked out. We found that, in the absence of α-catenin, E-cadherin adhesions not only had lower adhesion strength, as expected, but were also more mobile. We observed that α-catenin was required for the recovery of strained cell-cell contacts and propose that the adhesion strength and force-dependent mobility of E-cadherin adhesions act in tandem to regulate cell-cell contact homeostasis. Our approach introduces a method which relates the force-dependent adhesion mobility to adhesion strength and highlights the morphological role played by α-catenin in E-cadherin adhesion dynamics.
Language	English
Publishing date	2023-08-19
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.28.550975
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Article ; Online: E-cadherin adhesion dynamics as revealed by an accelerated force ramp are dependent upon the presence of α-catenin.

Bush, Joshua / Cabe, Jolene I / Conway, Daniel / Maruthamuthu, Venkat

Biochemical and biophysical research communications

2023 Volume 682, Page(s) 308–315

Abstract	Tissue remodeling and shape changes often rely on force-induced cell rearrangements occurring via cell-cell contact dynamics. Epithelial cell-cell contact shape changes are particularly dependent upon E-cadherin adhesion dynamics which are directly influenced by cell-generated and external forces. While both the mobility of E-cadherin adhesions and their adhesion strength have been reported before, it is not clear how these two aspects of E-cadherin adhesion dynamics are related. Here, using magnetic pulling cytometry, we applied an accelerated force ramp on the E-cadherin adhesion between an E-cadherin-coated magnetic microbead and an epithelial cell to ascertain this relationship. Our approach enables the determination of the adhesion strength and force-dependent mobility of individual adhesions, which revealed a direct correlation between these key characteristics. Since α-catenin has previously been reported to play a role in both E-cadherin mobility and adhesion strength when studied independently, we also probed epithelial cells in which α-catenin has been knocked out. We found that, in the absence of α-catenin, E-cadherin adhesions not only had lower adhesion strength, as expected, but were also more mobile. We observed that α-catenin was required for the recovery of strained cell-cell contacts and propose that the adhesion strength and force-dependent mobility of E-cadherin adhesions act in tandem to regulate cell-cell contact homeostasis. Our approach introduces a method which relates the force-dependent adhesion mobility to adhesion strength and highlights the morphological role played by α-catenin in E-cadherin adhesion dynamics.
MeSH term(s)	alpha Catenin/metabolism ; Cell Adhesion/physiology ; Cadherins/metabolism ; Epithelial Cells/metabolism
Chemical Substances	alpha Catenin ; Cadherins
Language	English
Publishing date	2023-10-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	205723-2
ISSN	1090-2104 ; 0006-291X ; 0006-291X
ISSN (online)	1090-2104 ; 0006-291X
ISSN	0006-291X
DOI	10.1016/j.bbrc.2023.09.077
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Article ; Online: Epithelial Cell-Like Elasticity Modulates Actin-Dependent E-Cadherin Adhesion Organization.

Eftekharjoo, Mohamad / Mezher, Mazen / Chatterji, Siddharth / Maruthamuthu, Venkat

ACS biomaterials science & engineering

2022 Volume 8, Issue 6, Page(s) 2455–2462

Abstract: E-cadherin adhesions are essential for cell-to-cell cohesion and mechanical coupling between epithelial cells and reside in a microenvironment that comprises the adjoining epithelial cells. While E-cadherin has been shown to be a mechanosensor, it is ... ...

Abstract	E-cadherin adhesions are essential for cell-to-cell cohesion and mechanical coupling between epithelial cells and reside in a microenvironment that comprises the adjoining epithelial cells. While E-cadherin has been shown to be a mechanosensor, it is unknown if E-cadherin adhesions can differentially sense stiffness within the range of that of epithelial cells. A survey of literature shows that epithelial cells' Young's moduli of elasticity lie predominantly in the sub-kPa to few-kPa range, with cancer cells often being softer than noncancerous ones. Here, we devised oriented E-cadherin-coated soft silicone substrates with sub-kPa or few-kPa elasticity but with similar viscous moduli and found that E-cadherin adhesions differentially organize depending on the magnitude of epithelial cell-like elasticity. Our results show that the actin cytoskeleton organizes E-cadherin adhesions in two ways─by supporting irregularly shaped adhesions at localized regions of high actin density and linear shaped adhesions at the end of linear actin bundles. Linearly shaped E-cadherin adhesions associated with radially oriented actin─but not irregularly shaped E-cadherin adhesions associated with circumferential actin foci─were much more numerous on 2.4 kPa E-cadherin substrates compared to 0.3 kPa E-cadherin substrates. However, the total amount of E-cadherin in both types of adhesions taken together was similar on the 0.3 and 2.4 kPa E-cadherin substrates across many cells. Our results show how the distribution of E-cadherin adhesions, supported by actin density and architecture, is modulated by epithelial cell-like elasticity and have significant implications for disease states like carcinomas characterized by altered epithelial cell elasticity.
MeSH term(s)	Actins ; Cadherins ; Cell Adhesion ; Elasticity ; Epithelial Cells/pathology
Chemical Substances	Actins ; Cadherins
Language	English
Publishing date	2022-05-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	2373-9878
ISSN (online)	2373-9878
DOI	10.1021/acsbiomaterials.2c00253
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Article: In situ

Bush, Joshua / Maruthamuthu, Venkat

AIP advances

2019 Volume 9, Issue 3, Page(s) 35221

Abstract: Localized application of exogenous forces on soft biomaterials and cells is often essential for the study of their response to external mechanical stimuli. Magnetic means of applying forces, particularly those based on permanent magnets and magnetic ... ...

Abstract	Localized application of exogenous forces on soft biomaterials and cells is often essential for the study of their response to external mechanical stimuli. Magnetic means of applying forces, particularly those based on permanent magnets and magnetic beads coupled to substrates or cells provide an accessible means of exerting forces of appropriate magnitude. The amount of force exerted, however, is often inferred from calibration performed
Language	English
Publishing date	2019-03-14
Publishing country	United States
Document type	Journal Article
ZDB-ID	2583909-3
ISSN	2158-3226
ISSN	2158-3226
DOI	10.1063/1.5084261
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Article ; Online: Low-Cost Flexible Glass-Based pH Sensor via Cold Atmospheric Plasma Deposition.

Kasi, Venkat / Sedaghat, Sotoudeh / Alcaraz, Alejandro M / Maruthamuthu, Murali Kannan / Heredia-Rivera, Ulisses / Nejati, Sina / Nguyen, Juliane / Rahimi, Rahim

ACS applied materials & interfaces

2022 Volume 14, Issue 7, Page(s) 9697–9710

Abstract: Many commercially available pH sensors are fabricated with a glass membrane as the sensing component because of several advantages of glass-based electrodes such as versatility, high accuracy, and excellent stability in various conditions. However, ... ...

Abstract	Many commercially available pH sensors are fabricated with a glass membrane as the sensing component because of several advantages of glass-based electrodes such as versatility, high accuracy, and excellent stability in various conditions. However, because of their bulkiness and poor mechanical properties, conventional glass-based sensors are not ideal for wearable or flexible applications. Here, we report for the first time the fabrication of a flexible glass-based pH sensor suitable for biomedical and environmental applications where flexibility and stability of the sensor are critical for long-term and real-time monitoring. The sensor was fabricated via a simple and facile approach using the cold atmospheric plasma technique in which a pH sensitive silica coating was deposited from a siloxane precursor onto a carbon electrode. In order to increase the sensitivity and stability of the sensor, we employed a postprocessing step which involves annealing of the silica coated electrode at elevated temperatures. This process was optimized to ensure that the crucial properties such as porosity and hydration functionality were balanced to obtain the best and most reliable sensitivity of the sensor. Our sensitivity test results indicated that these sensors exhibit excellent and stable sensitivity with a slope of about 48 mV/pH (
Language	English
Publishing date	2022-02-10
Publishing country	United States
Document type	Journal Article
ISSN	1944-8252
ISSN (online)	1944-8252
DOI	10.1021/acsami.1c19805
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Article ; Online: α-Catenin-dependent vinculin recruitment to adherens junctions is antagonistic to focal adhesions.

Bejar-Padilla, Vidal / Cabe, Jolene I / Lopez, Santiago / Narayanan, Vani / Mezher, Mazen / Maruthamuthu, Venkat / Conway, Daniel E

Molecular biology of the cell

2022 Volume 33, Issue 11, Page(s) ar93

Abstract: Vinculin is a protein found in both focal adhesions (FAs) and adherens junctions (AJs) which regulates actin connectivity to these structures. Many studies have demonstrated that mechanical perturbations of cells result in enhanced recruitment of ... ...

Abstract	Vinculin is a protein found in both focal adhesions (FAs) and adherens junctions (AJs) which regulates actin connectivity to these structures. Many studies have demonstrated that mechanical perturbations of cells result in enhanced recruitment of vinculin to FAs and/or AJs. Likewise, many other studies have shown "cross-talk" between FAs and AJs. Vinculin itself has been suggested to be a probable regulator of this adhesion cross-talk. In this study we used MDCK as a model system of epithelia, developing cell lines in which vinculin recruitment was reduced or enhanced at AJs. Careful analysis of these cells revealed that perturbing vinculin recruitment to AJs resulted in a reduction of detectable FAs. Interestingly the cross-talk between these two structures was not due to a limited pool of vinculin, as increasing expression of vinculin did not rescue FA formation. Instead, we demonstrate that vinculin translocation between AJs and FAs is necessary for actin cytoskeleton rearrangements that occur during cell migration, which is necessary for large, well-formed FAs. Last, we show using a wound assay that collective cell migration is similarly hindered when vinculin recruitment is reduced or enhanced at AJs, highlighting that vinculin translocation between each compartment is necessary for efficient collective migration.
MeSH term(s)	Adherens Junctions/metabolism ; Catenins/metabolism ; Cell Adhesion ; Focal Adhesions/metabolism ; Vinculin/metabolism ; alpha Catenin/metabolism
Chemical Substances	Catenins ; alpha Catenin ; Vinculin (125361-02-6)
Language	English
Publishing date	2022-08-03
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	1098979-1
ISSN	1939-4586 ; 1059-1524
ISSN (online)	1939-4586
ISSN	1059-1524
DOI	10.1091/mbc.E22-02-0071
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Zs.A 2853: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article: Mechanical response of an epithelial island subject to uniaxial stretch on a hybrid silicone substrate.

Bashirzadeh, Yashar / Dumbali, Sandeep / Qian, Shizhi / Maruthamuthu, Venkat

Cellular and molecular bioengineering

2018 Volume 12, Issue 1, Page(s) 33–40

Abstract: Introduction: The mechanical response of large multi-cellular collectives to external stretch has remained largely unexplored, despite its relevance to normal function and to external challenges faced by some tissues. Here, we introduced a simple hybrid ...

Abstract	Introduction: The mechanical response of large multi-cellular collectives to external stretch has remained largely unexplored, despite its relevance to normal function and to external challenges faced by some tissues. Here, we introduced a simple hybrid silicone substrate to enable external stretch while providing a physiologically relevant physical micro-environment for cells. Methods: We micropatterned epithelial islands on the substrate using a stencil to allow for a circular island shape without restraining island edges. We then used traction force microscopy to determine the strain energy and the inter-cellular sheet tension within the island as a function of time after stretch. Results: While the strain energy stored in the substrate for unstretched cell islands stayed constant over time, a uniaxial 10% stretch resulted in an abrupt increase, followed by sustained increase in the strain energy of the islands over tens of minutes, indicating slower dynamics than for single cells reported previously. The sheet tension at the island mid-line perpendicular to the stretch direction also more than doubled compared to unstretched islands. Interestingly, the sheet tension at the island mid-line parallel to the stretch direction also reached similar levels over tens of minutes indicating the tendency of the island to homogenize its internal stress. Conclusions: We found that the sheet tension within large epithelial islands depends on its direction relative to that of the stretch initially, but not at longer times. We suggest that the hybrid silicone substrate provides for an accessible substrate for studying the mechanobiology of large epithelial cell islands.
Language	English
Publishing date	2018-10-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	2416037-4
ISSN	1865-5033 ; 1865-5025
ISSN (online)	1865-5033
ISSN	1865-5025
DOI	10.1007/s12195-018-00560-1
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Article ; Online: Effect of pharmacological modulation of actin and myosin on collective cell electrotaxis.

Bashirzadeh, Yashar / Poole, Jonathan / Qian, Shizhi / Maruthamuthu, Venkat

Bioelectromagnetics

2018 Volume 39, Issue 4, Page(s) 289–298

Abstract: Electrotaxis-the directional migration of cells in response to an electric field-is most evident in multicellular collectives and plays an important role in physiological contexts. While most cell types respond to applied electric fields of the order of ... ...

Abstract	Electrotaxis-the directional migration of cells in response to an electric field-is most evident in multicellular collectives and plays an important role in physiological contexts. While most cell types respond to applied electric fields of the order of a Volt per centimeter, our knowledge of the factors influencing this response is limited. This is especially true for collective cell electrotaxis, in which the subcellular migration response within a cell has to be coordinated with coupled neighboring cells. Here, we investigated the effect of the level of actin cytoskeleton polymerization and myosin activity on collective cell electrotaxis of Madin-Darby Canine Kidney (MDCK) cells in response to a weak electric field of physiologically relevant magnitude. We modulated the polymerization state of the actin cytoskeleton using the depolymerizing agent cytochalasin D or the polymerizing agent jasplakinolide. We also modulated the contractility of the cell using the myosin motor inhibitor blebbistatin or the phosphatase inhibitor calyculin A. While all the above pharmacological treatments altered cell speed to various extents, we found that only increasing the contractility and a high level of increase/stabilization of polymerized actin had a strong inhibitory effect specifically on the directedness of collective cell electrotaxis. On the other hand, even as the effect of the actin modulators on collective cell migration was varied, most conditions of actin and myosin pharmacological modulation-except for high level of actin polymerization/stabilization-resulted in cell speeds that were similar in the absence or presence of the electric field. Our results led us to speculate that the applied electric field may largely impact the cellular apparatus specifying the polarity of collective cell migration, rather than the functioning of the migratory apparatus. Bioelectromagnetics. 39:289-298, 2018. © 2018 Wiley Periodicals, Inc.
MeSH term(s)	Actins/chemistry ; Actins/metabolism ; Animals ; Cell Movement ; Cytoskeleton/metabolism ; Dogs ; Electricity ; Madin Darby Canine Kidney Cells ; Myosins/metabolism ; Protein Multimerization ; Protein Structure, Quaternary
Chemical Substances	Actins ; Myosins (EC 3.6.4.1)
Language	English
Publishing date	2018-04-17
Publishing country	United States
Document type	Journal Article
ZDB-ID	760683-7
ISSN	1521-186X ; 0197-8462
ISSN (online)	1521-186X
ISSN	0197-8462
DOI	10.1002/bem.22119
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