Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD)

Lecarpentier, Yves; Kindler, Vincent; Krokidis, Xénophon; Bochaton-Piallat, Marie-Luce; Claes, Victor; Hébert, Jean-Louis; Vallée, Alexandre; Schussler, Olivier

doi:10.3390/cells9061510

Open AccessArticle

Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD)

by

Yves Lecarpentier

^1,*,

Vincent Kindler

²,

Xénophon Krokidis

¹,

Marie-Luce Bochaton-Piallat

³,

Victor Claes

⁴,

Jean-Louis Hébert

⁵,

Alexandre Vallée

⁶

and

Olivier Schussler

^7,8

¹

Centre de Recherche Clinique, Grand Hôpital de l’Est Francilien, 77104 Meaux, France

²

Department of Specialties in Medicine, Hematology Service, Geneva University Hospital, Faculty of Medicine, 1200 Geneva, Switzerland

³

Department of Pathology and Immunology, Geneva University Hospital, Faculty of Medicine, 1200 Geneva, Switzerland

⁴

Department of Pharmaceutical Sciences, University of Antwerp, 2000 Wilrijk, Belgium

⁵

Institut de Cardiologie, Hôpital de la Pitié-Salpêtrière, 75013 Paris, France

⁶

Diagnosis and Therapeutic Center, Hypertension and Cardiovascular Prevention Unit, Hôtel-Dieu Hospital, AP-HP, Paris-Descartes University, 75004 Paris, France

⁷

Department of Cardiovascular Surgery, Research Laboratory, Geneva University Hospital, Faculty of Medicine, 1200 Geneva, Switzerland

⁸

Department of Thoracic surgery, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, 67000 Strasbourg, France

^*

Author to whom correspondence should be addressed.

Cells 2020, 9(6), 1510; https://doi.org/10.3390/cells9061510

Submission received: 1 May 2020 / Revised: 18 June 2020 / Accepted: 19 June 2020 / Published: 21 June 2020

(This article belongs to the Special Issue Mesenchymal Stem Cells, Niche and Tissue Homeostasis: Applications to Organoids)

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Abstract

Mesenchymal stromal cells (MSCs) were obtained from human bone marrow and amplified in cultures supplemented with human platelet lysate. Once semi-confluent, cells were seeded in solid collagen scaffolds that were rapidly colonized by the cells generating a 3D cell scaffold. Here, they acquired a myofibroblast phenotype and when exposed to appropriate chemical stimulus, developed tension and cell shortening, similar to those of striated and smooth muscle cells. Myofibroblasts contained a molecular motor—the non-muscle myosin type IIA (NMMIIA) whose crossbridge (CB) kinetics are dramatically slow compared with striated and smooth muscle myosins. Huxley’s equations were used to determine the molecular mechanical properties of NMMIIA. Thank to the great number of NMMIIA molecules, we determined the statistical mechanics (SM) of MSCs, using the grand canonical ensemble which made it possible to calculate various thermodynamic entities such as the chemical affinity, statistical entropy, internal energy, thermodynamic flow, thermodynamic force, and entropy production rate. The linear relationship observed between the thermodynamic force and the thermodynamic flow allowed to establish that MSC-laden in collagen scaffolds were in a near-equilibrium stationary state (affinity ≪ RT), MSCs were also seeded in solid collagen scaffolds functionalized with the tripeptide Arg-Gly-Asp (RGD). This induced major changes in NMMIIA SM particularly by increasing the rate of entropy production. In conclusion, collagen scaffolds laden with MSCs can be viewed as a non-muscle contractile bioengineered tissue operating in a near-equilibrium linear regime, whose SM could be substantially modified by the RGD peptide.

Keywords: myofibroblast; mesenchymal stromal cell; RGD; collagen scaffold; tissue engineering; bone marrow; non-muscle myosin NMMIIA; statistical mechanics; entropy production rate; chemical affinity; thermodynamic force; thermodynamic flow; near-equilibrium thermodynamics; linear stationary state

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MDPI and ACS Style

Lecarpentier, Y.; Kindler, V.; Krokidis, X.; Bochaton-Piallat, M.-L.; Claes, V.; Hébert, J.-L.; Vallée, A.; Schussler, O. Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD). Cells 2020, 9, 1510. https://doi.org/10.3390/cells9061510

AMA Style

Lecarpentier Y, Kindler V, Krokidis X, Bochaton-Piallat M-L, Claes V, Hébert J-L, Vallée A, Schussler O. Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD). Cells. 2020; 9(6):1510. https://doi.org/10.3390/cells9061510

Chicago/Turabian Style

Lecarpentier, Yves, Vincent Kindler, Xénophon Krokidis, Marie-Luce Bochaton-Piallat, Victor Claes, Jean-Louis Hébert, Alexandre Vallée, and Olivier Schussler. 2020. "Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD)" Cells 9, no. 6: 1510. https://doi.org/10.3390/cells9061510

APA Style

Lecarpentier, Y., Kindler, V., Krokidis, X., Bochaton-Piallat, M.-L., Claes, V., Hébert, J.-L., Vallée, A., & Schussler, O. (2020). Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD). Cells, 9(6), 1510. https://doi.org/10.3390/cells9061510

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Statistical Mechanics of Non-Muscle Myosin IIA in Human Bone Marrow-Derived Mesenchymal Stromal Cells Seeded in a Collagen Scaffold: A Thermodynamic Near-Equilibrium Linear System Modified by the Tripeptide Arg-Gly-Asp (RGD)

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