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Asymmetrical Forces Dictate the Distribution and Morphology of Platelets in Blood Clots

1
Center for Theoretical Problems of Physico-Chemical Pharmacology, Russian Academy of Sciences, 30 Srednyaya Kalitnikovskaya str., 109029 Moscow, Russia
2
Cardiology, Faculty of Science and Medicine, University of Fribourg, CH-1700 Fribourg, Switzerland
3
BPPS UMR-S 1255, EFS Grand Est, FMTS, INSERM, University of Strasbourg, F-67065 Strasbourg, France
4
Institute for Advanced Biosciences, University Grenoble Alpes, CNRS UMR 5309, INSERM U1209, F-38700 Grenoble, France
5
National Medical Research Centre of Pediatric Hematology, Oncology and Immunology Named after Dmitry Rogachev, 1 Samory Mashela St, 117198 Moscow, Russia
6
Surgical Research Unit, Faculty of Science and Medicine, University of Fribourg, CH-1700 Fribourg, Switzerland
*
Authors to whom correspondence should be addressed.
Equal contributions.
Academic Editor: Katya Ravid
Cells 2021, 10(3), 584; https://doi.org/10.3390/cells10030584
Received: 18 February 2021 / Accepted: 1 March 2021 / Published: 6 March 2021
Primary hemostasis consists in the activation of platelets, which spread on the exposed extracellular matrix at the injured vessel surface. Secondary hemostasis, the coagulation cascade, generates a fibrin clot in which activated platelets and other blood cells get trapped. Active platelet-dependent clot retraction reduces the clot volume by extruding the serum. Thus, the clot architecture changes with time of contraction, which may have an important impact on the healing process and the dissolution of the clot, but the precise physiological role of clot retraction is still not completely understood. Since platelets are the only actors to develop force for the retraction of the clot, their distribution within the clot should influence the final clot architecture. We analyzed platelet distributions in intracoronary thrombi and observed that platelets and fibrin co-accumulate in the periphery of retracting clots in vivo. A computational mechanical model suggests that asymmetric forces are responsible for a different contractile behavior of platelets in the periphery versus the clot center, which in turn leads to an uneven distribution of platelets and fibrin fibers within the clot. We developed an in vitro clot retraction assay that reproduces the in vivo observations and follows the prediction of the computational model. Our findings suggest a new active role of platelet contraction in forming a tight fibrin- and platelet-rich boundary layer on the free surface of fibrin clots. View Full-Text
Keywords: platelet; hemostasis; thrombosis; clot retraction; fibrin; computational modeling platelet; hemostasis; thrombosis; clot retraction; fibrin; computational modeling
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MDPI and ACS Style

Kovalenko, T.A.; Giraud, M.-N.; Eckly, A.; Ribba, A.-S.; Proamer, F.; Fraboulet, S.; Podoplelova, N.A.; Valentin, J.; Panteleev, M.A.; Gonelle-Gispert, C.; Cook, S.; Lafanechère, L.; Sveshnikova, A.N.; Sadoul, K. Asymmetrical Forces Dictate the Distribution and Morphology of Platelets in Blood Clots. Cells 2021, 10, 584. https://doi.org/10.3390/cells10030584

AMA Style

Kovalenko TA, Giraud M-N, Eckly A, Ribba A-S, Proamer F, Fraboulet S, Podoplelova NA, Valentin J, Panteleev MA, Gonelle-Gispert C, Cook S, Lafanechère L, Sveshnikova AN, Sadoul K. Asymmetrical Forces Dictate the Distribution and Morphology of Platelets in Blood Clots. Cells. 2021; 10(3):584. https://doi.org/10.3390/cells10030584

Chicago/Turabian Style

Kovalenko, Tatiana A., Marie-Noelle Giraud, Anita Eckly, Anne-Sophie Ribba, Fabienne Proamer, Sandrine Fraboulet, Nadezhda A. Podoplelova, Jeremy Valentin, Mikhail A. Panteleev, Carmen Gonelle-Gispert, Stéphane Cook, Laurence Lafanechère, Anastasia N. Sveshnikova, and Karin Sadoul. 2021. "Asymmetrical Forces Dictate the Distribution and Morphology of Platelets in Blood Clots" Cells 10, no. 3: 584. https://doi.org/10.3390/cells10030584

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