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Mechanical Forces in the Cell
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Mechanical Forces in the Cell

A special issue of Life (ISSN 2075-1729). This special issue belongs to the section "Biochemistry, Biophysics and Computational Biology".

Deadline for manuscript submissions: closed (22 April 2021) | Viewed by 27989

Special Issue Editors

Dr. Pietro Mascheroni

E-Mail Website
Guest Editor
Department Systems Immunology (SIMM), Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany
Interests: cancer modeling; continuum mechanics; contact inhibition; biophysics of the immune system
Dr. Haralampos Hatzikirou

E-Mail Website
Guest Editor
1. Centre for Information Services and High Performance Computing, Technische Universität Dresden, Nöthnitzer Straße 46, 01062 Dresden, Germany
2. Mathematics Department, Khalifa University, Abu Dhabi P.O. Box 127788, United Arab Emirates
Interests: mathematical biology; systems medicine/biology; cell decision-making; multi-scale modeling; non-equilibrium dynamics
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Animal and plant cells perform a complex sequence of actions to carry out life processes and maintain homeostasis in living organisms. For many years, researchers focused on identifying molecular and chemical players that mediate cell response to internal and external signals. However, evidence has recently emerged suggesting that physical factors play a dramatic role in cellular functions. For example, leukocytes sense the mechanical environment in which they live and modify their phenotype and immune activity as a response. Plant development, as another example, is the result of expansive growth, division, and differentiation of cells, all involving mechanical aspects. In addition, the ability of cells to crawl on substrates and move in porous matrices depends on the non-linear rheological properties of cellular assemblies. The rich amount of experimental data has promoted numerous attempts to generate theoretical models to test biological hypotheses and mechanisms. In this Special Issue, we will cover the most recent advances in cellular biomechanics, including both experimental and theoretical work.

Dr. Pietro Mascheroni
Dr. Haralambos Hatzikirou
Guest Editors

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Keywords

  • cell mechanics
  • mechanobiology
  • mechanotransduction
  • geometrical constraints
  • biomechanics of active matter
  • mathematical modeling

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Published Papers (7 papers)

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Research

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13 pages, 1859 KiB  
Article
Effect of HIT Components on the Development of Breast Cancer Cells
by Li-Yu Chen, Gurunath Apte, Annerose Lindenbauer, Marion Frant and Thi-Huong Nguyen
Life 2021, 11(8), 832; https://doi.org/10.3390/life11080832 - 13 Aug 2021
Cited by 3 | Viewed by 2805
Abstract
Cancer cells circulating in blood vessels activate platelets, forming a cancer cell encircling platelet cloak which facilitates cancer metastasis. Heparin (H) is frequently used as an anticoagulant in cancer patients but up to 5% of patients have a side effect, heparin-induced thrombocytopenia (HIT) [...] Read more.
Cancer cells circulating in blood vessels activate platelets, forming a cancer cell encircling platelet cloak which facilitates cancer metastasis. Heparin (H) is frequently used as an anticoagulant in cancer patients but up to 5% of patients have a side effect, heparin-induced thrombocytopenia (HIT) that can be life-threatening. HIT is developed due to a complex interaction among multiple components including heparin, platelet factor 4 (PF4), HIT antibodies, and platelets. However, available information regarding the effect of HIT components on cancers is limited. Here, we investigated the effect of these materials on the mechanical property of breast cancer cells using atomic force microscopy (AFM) while cell spreading was quantified by confocal laser scanning microscopy (CLSM), and cell proliferation rate was determined. Over time, we found a clear effect of each component on cell elasticity and cell spreading. In the absence of platelets, HIT antibodies inhibited cell proliferation but they promoted cell proliferation in the presence of platelets. Our results indicate that HIT complexes influenced the development of breast cancer cells. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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15 pages, 3699 KiB  
Article
An Improved Scalable Hydrogel Dish for Spheroid Culture
by Jonard Corpuz Valdoz, Dallin J. Jacobs, Collin G. Cribbs, Benjamin C. Johnson, Brandon M. Hemeyer, Ethan L. Dodson, Jordan A. Saunooke, Nicholas A. Franks, Peter Daniel Poulson, Seth R. Garfield, Connor J. Knight and Pam M. Van Ry
Life 2021, 11(6), 517; https://doi.org/10.3390/life11060517 - 3 Jun 2021
Cited by 7 | Viewed by 5024
Abstract
Research in fields studying cellular response to surface tension and mechanical forces necessitate cell culture tools with tunability of substrate stiffness. We created a scalable hydrogel dish design to facilitate scaffold-free formation of multiple spheroids in a single dish. Our novel design features [...] Read more.
Research in fields studying cellular response to surface tension and mechanical forces necessitate cell culture tools with tunability of substrate stiffness. We created a scalable hydrogel dish design to facilitate scaffold-free formation of multiple spheroids in a single dish. Our novel design features inner and outer walls, allowing efficient media changes and downstream experiments. The design is easily scalable, accommodating varying numbers of microwells per plate. We report that non-adherent hydrogel stiffness affects spheroid morphology and compaction. We found that spheroid morphology and viability in our hydrogel dishes were comparable to commercially available Aggrewell™800 plates, with improved tunability of surface stiffness and imaging area. Device function was demonstrated with a migration assay using two investigational inhibitors against EMT. We successfully maintained primary-derived spheroids from murine and porcine lungs in the hydrogel dish. These features increase the ability to produce highly consistent cell aggregates for biological research. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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15 pages, 1629 KiB  
Article
Emergence of Mechano-Sensitive Contraction Autoregulation in Cardiomyocytes
by Leighton Izu, Rafael Shimkunas, Zhong Jian, Bence Hegyi, Mohammad Kazemi-Lari, Anthony Baker, John Shaw, Tamas Banyasz and Ye Chen-Izu
Life 2021, 11(6), 503; https://doi.org/10.3390/life11060503 - 29 May 2021
Cited by 3 | Viewed by 2683
Abstract
The heart has two intrinsic mechanisms to enhance contractile strength that compensate for increased mechanical load to help maintain cardiac output. When vascular resistance increases the ventricular chamber initially expands causing an immediate length-dependent increase of contraction force via the Frank-Starling mechanism. Additionally, [...] Read more.
The heart has two intrinsic mechanisms to enhance contractile strength that compensate for increased mechanical load to help maintain cardiac output. When vascular resistance increases the ventricular chamber initially expands causing an immediate length-dependent increase of contraction force via the Frank-Starling mechanism. Additionally, the stress-dependent Anrep effect slowly increases contraction force that results in the recovery of the chamber volume towards its initial state. The Anrep effect poses a paradox: how can the cardiomyocyte maintain higher contractility even after the cell length has recovered its initial length? Here we propose a surface mechanosensor model that enables the cardiomyocyte to sense different mechanical stresses at the same mechanical strain. The cell-surface mechanosensor is coupled to a mechano-chemo-transduction feedback mechanism involving three elements: surface mechanosensor strain, intracellular Ca2+ transient, and cell strain. We show that in this simple yet general system, contractility autoregulation naturally emerges, enabling the cardiomyocyte to maintain contraction amplitude despite changes in a range of afterloads. These nontrivial model predictions have been experimentally confirmed. Hence, this model provides a new conceptual framework for understanding the contractility autoregulation in cardiomyocytes, which contributes to the heart’s intrinsic adaptivity to mechanical load changes in health and diseases. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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20 pages, 6012 KiB  
Article
Dectin-1-Mediated DC-SIGN Recruitment to Candida albicans Contact Sites
by Rohan P. Choraghe and Aaron K. Neumann
Life 2021, 11(2), 108; https://doi.org/10.3390/life11020108 - 31 Jan 2021
Cited by 2 | Viewed by 3675
Abstract
At host–pathogen contact sites with Candida albicans, Dectin-1 activates pro-inflammatory signaling, while DC-SIGN promotes adhesion to the fungal surface. We observed that Dectin-1 and DC-SIGN collaborate to enhance capture/retention of C. albicans under fluid shear culture conditions. Therefore, we devised a cellular [...] Read more.
At host–pathogen contact sites with Candida albicans, Dectin-1 activates pro-inflammatory signaling, while DC-SIGN promotes adhesion to the fungal surface. We observed that Dectin-1 and DC-SIGN collaborate to enhance capture/retention of C. albicans under fluid shear culture conditions. Therefore, we devised a cellular model system wherein we could investigate the interaction between these two receptors during the earliest stages of host–pathogen interaction. In cells expressing both receptors, DC-SIGN was quickly recruited to contact sites (103.15% increase) but Dectin-1 did not similarly accumulate. Once inside the contact site, FRAP studies revealed a strong reduction in lateral mobility of DC-SIGN (but not Dectin-1), consistent with DC-SIGN engaging in multivalent adhesive binding interactions with cell wall mannoprotein ligands. Interestingly, in the absence of Dectin-1 co-expression, DC-SIGN recruitment to the contact was much poorer—only 35.04%. These data suggested that Dectin-1 promotes the active recruitment of DC-SIGN to the contact site. We proposed that Dectin-1 signaling activates the RHOA pathway, leading to actomyosin contractility that promotes DC-SIGN recruitment, perhaps via the formation of a centripetal actomyosin flow (AMF) directed into the contact site. Indeed, RHOA pathway inhibitors significantly reduced Dectin-1-associated DC-SIGN recruitment to the contact site. We used agent-based modeling to predict DC-SIGN transport kinetics with (“Directed + Brownian”) and without (“Brownian”) the hypothesized actomyosin flow-mediated transport. The Directed + Brownian transport model predicted a DC-SIGN contact site recruitment (106.64%), similar to that we observed experimentally under receptor co-expression. Brownian diffusive transport alone predicted contact site DC-SIGN recruitment of only 55.60%. However, this value was similar to experimentally observed DC-SIGN recruitment in cells without Dectin-1 or expressing Dectin-1 but treated with RHOA inhibitor, suggesting that it accurately predicted DC-SIGN recruitment when a contact site AMF would not be generated. TIRF microscopy of nascent cell contacts on glucan-coated glass revealed Dectin-1-dependent DC-SIGN and F-actin (LifeAct) recruitment kinetics to early stage contact site membranes. DC-SIGN entry followed F-actin with a temporal lag of 8.35 ± 4.57 s, but this correlation was disrupted by treatment with RHOA inhibitor. Thus, computational and experimental evidence provides support for the existence of a Dectin-1/RHOA-dependent AMF that produces a force to drive DC-SIGN recruitment to pathogen contact sites, resulting in improved pathogen capture and retention by immunocytes. These data suggest that the rapid collaborative response of Dectin-1 and DC-SIGN in early contact sties might be important for the efficient acquisition of yeast under flow conditions, such as those that prevail in circulation or mucocutaneous sites of infection. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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Review

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18 pages, 2557 KiB  
Review
In Vitro Measurements of Cellular Forces and their Importance in the Lung—From the Sub- to the Multicellular Scale
by Peter Kolb, Annika Schundner, Manfred Frick and Kay-E. Gottschalk
Life 2021, 11(7), 691; https://doi.org/10.3390/life11070691 - 14 Jul 2021
Cited by 4 | Viewed by 3307
Abstract
Throughout life, the body is subjected to various mechanical forces on the organ, tissue, and cellular level. Mechanical stimuli are essential for organ development and function. One organ whose function depends on the tightly connected interplay between mechanical cell properties, biochemical signaling, and [...] Read more.
Throughout life, the body is subjected to various mechanical forces on the organ, tissue, and cellular level. Mechanical stimuli are essential for organ development and function. One organ whose function depends on the tightly connected interplay between mechanical cell properties, biochemical signaling, and external forces is the lung. However, altered mechanical properties or excessive mechanical forces can also drive the onset and progression of severe pulmonary diseases. Characterizing the mechanical properties and forces that affect cell and tissue function is therefore necessary for understanding physiological and pathophysiological mechanisms. In recent years, multiple methods have been developed for cellular force measurements at multiple length scales, from subcellular forces to measuring the collective behavior of heterogeneous cellular networks. In this short review, we give a brief overview of the mechanical forces at play on the cellular level in the lung. We then focus on the technological aspects of measuring cellular forces at many length scales. We describe tools with a subcellular resolution and elaborate measurement techniques for collective multicellular units. Many of the technologies described are by no means restricted to lung research and have already been applied successfully to cells from various other tissues. However, integrating the knowledge gained from these multi-scale measurements in a unifying framework is still a major future challenge. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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17 pages, 3061 KiB  
Review
Mechanically Induced Cavitation in Biological Systems
by Chunghwan Kim, Won June Choi, Yisha Ng and Wonmo Kang
Life 2021, 11(6), 546; https://doi.org/10.3390/life11060546 - 10 Jun 2021
Cited by 14 | Viewed by 4181
Abstract
Cavitation bubbles form in soft biological systems when subjected to a negative pressure above a critical threshold, and dynamically change their size and shape in a violent manner. The critical threshold and dynamic response of these bubbles are known to be sensitive to [...] Read more.
Cavitation bubbles form in soft biological systems when subjected to a negative pressure above a critical threshold, and dynamically change their size and shape in a violent manner. The critical threshold and dynamic response of these bubbles are known to be sensitive to the mechanical characteristics of highly compliant biological systems. Several recent studies have demonstrated different biological implications of cavitation events in biological systems, from therapeutic drug delivery and microsurgery to blunt injury mechanisms. Due to the rapidly increasing relevance of cavitation in biological and biomedical communities, it is necessary to review the current state-of-the-art theoretical framework, experimental techniques, and research trends with an emphasis on cavitation behavior in biologically relevant systems (e.g., tissue simulant and organs). In this review, we first introduce several theoretical models that predict bubble response in different types of biological systems and discuss the use of each model with physical interpretations. Then, we review the experimental techniques that allow the characterization of cavitation in biologically relevant systems with in-depth discussions of their unique advantages and disadvantages. Finally, we highlight key biological studies and findings, through the direct use of live cells or organs, for each experimental approach. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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22 pages, 3046 KiB  
Review
Biomechanics of Neutrophil Tethers
by Andrea Cugno, Alex Marki and Klaus Ley
Life 2021, 11(6), 515; https://doi.org/10.3390/life11060515 - 31 May 2021
Cited by 7 | Viewed by 3773
Abstract
Leukocytes, including neutrophils, propelled by blood flow, can roll on inflamed endothelium using transient bonds between selectins and their ligands, and integrins and their ligands. When such receptor–ligand bonds last long enough, the leukocyte microvilli become extended and eventually form thin, 20 µm [...] Read more.
Leukocytes, including neutrophils, propelled by blood flow, can roll on inflamed endothelium using transient bonds between selectins and their ligands, and integrins and their ligands. When such receptor–ligand bonds last long enough, the leukocyte microvilli become extended and eventually form thin, 20 µm long tethers. Tether formation can be observed in blood vessels in vivo and in microfluidic flow chambers. Tethers can also be extracted using micropipette aspiration, biomembrane force probe, optical trap, or atomic force microscopy approaches. Here, we review the biomechanical properties of leukocyte tethers as gleaned from such measurements and discuss the advantages and disadvantages of each approach. We also review and discuss viscoelastic models that describe the dependence of tether formation on time, force, rate of loading, and cell activation. We close by emphasizing the need to combine experimental observations with quantitative models and computer simulations to understand how tether formation is affected by membrane tension, membrane reservoir, and interactions of the membrane with the cytoskeleton. Full article
(This article belongs to the Special Issue Mechanical Forces in the Cell)
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