Motor-driven marginal band coiling promotes cell shape change during platelet activation

Diagouraga, Boubou; Grichine, Alexeï; Fertin, Arnold; Wang, Jin; Khochbin, Saadi; Sadoul, Karin

doi:10.1083/jcb.201306085

Cited by 87 publications

(151 citation statements)

References 29 publications

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“…Microtubule coils in platelets at early stages of spreading were disrupted and spread platelet microtubule networks failed to form. Furthermore, the dynamics of microtubules were affected with observed microtubule coils failing to undergo the characteristic twisting of control platelets (as observed by Diagouraga et al) and appearing to depolymerize more rapidly than in controls. Thus, it would appear that there is an effect of SMIFH2 on microtubules in addition to the inhibition of actin polymerization.…”

Section: Discussionmentioning

confidence: 79%

SMIFH2 inhibition of platelets demonstrates a critical role for formin proteins in platelet cytoskeletal dynamics

Green

Zuidscherwoude

Alenazy

et al. 2020

Journal of Thrombosis and Haemostasis

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Background Reorganization of the actin cytoskeleton is required for proper functioning of platelets following activation in response to vascular damage. Formins are a family of proteins that regulate actin polymerization and cytoskeletal organization via a number of domains including the FH2 domain. However, the role of formins in platelet spreading has not been studied in detail. Objectives Several formin proteins are expressed in platelets so we used an inhibitor of FH2 domains (SMIFH2) to uncover the role of these proteins in platelet spreading and in maintenance of resting platelet shape. Methods Washed human and mouse platelets were treated with various concentrations of SMIFH2 and the effects on platelet spreading, platelet size, platelet cytoskeletal dynamics, and organization were analyzed using fluorescence and electron microscopy. Results Pretreatment with SMIFH2 completely blocks platelet spreading in both mouse and human platelets through effects on the organization and dynamics of actin and microtubules. However, platelet aggregation and secretion are unaffected. SMIFH2 also caused a decrease in resting platelet size and disrupted the balance of tubulin post‐translational modification. Conclusions These data therefore demonstrated an important role for formin‐mediated actin polymerization in platelet spreading and highlighted the importance of formins in cross‐talk between the actin and tubulin cytoskeletons.

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Section: Discussionmentioning

confidence: 79%

SMIFH2 inhibition of platelets demonstrates a critical role for formin proteins in platelet cytoskeletal dynamics

Green

Zuidscherwoude

Alenazy

et al. 2020

Journal of Thrombosis and Haemostasis

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“…The blood was collected in a BD Vacutainer tubes with 3.2% sodium citrate (Fisher Scientific). Prior to centrifugation, the whole blood collected was gently agitated at room temperature for 1 h to restore platelets partially activated during the withdrawal of blood back to the resting state . An anticoagulant, acid citrate dextrose (ACD), was then added to the blood at a ratio of 1:7 (ACD:blood).…”

Section: Methodsmentioning

confidence: 99%

Responses of endothelial cells, smooth muscle cells, and platelets dependent on the surface topography of polytetrafluoroethylene

Lamichhane

Anderson

Remund

et al. 2016

J Biomedical Materials Res

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In this study, the effect of different structures (flat, expanded, and electrospun) of polytetrafluoroethylene (PTFE) on the interactions of endothelial cells (ECs), smooth muscle cells (SMCs), and platelets was investigated. In addition, the mechanisms that govern the interactions between ECs, SMCs, and platelets with different structures of PTFE were discussed. The surface characterizations showed that the different structures of PTFE have the same surface chemistry, similar surface wettability and zeta potential, but uniquely different surface topography. The viability, proliferation, morphology, and phenotype of ECs and SMCs interacted with different structures of PTFE were investigated. Expanded PTFE (ePTFE) provided a relatively better surface for the growth of ECs. In case of SMC interactions, although all the different structures of PTFE inhibited SMC growth, a maximum inhibitory effect was observed for ePTFE. In case of platelet interactions, the electrospun PTFE provided a better surface for preventing the adhesion and activation of platelets. Thus, this study demonstrated that the responses of ECs, SMCs, and platelets strongly dependent on the surface topography of the PTFE. © 2016 Wiley Periodicals, Inc. J Biomed Mater Res Part A: 104A: 2291-2304, 2016.

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“…It was recently 26 shown that dynein slides microtubules apart to reorganize the marginal microtubule band of the resting platelet after activation. These forces extend the marginal band and induce coiling and are followed by actomyosin-mediated compression forces.…”

Section: Discussionmentioning

confidence: 99%

Microtubule sliding drives proplatelet elongation and is dependent on cytoplasmic dynein

Bender

Thon

Ehrlicher

et al. 2015

Blood

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Key Points• Dynein-dependent microtubule sliding drives proplatelet elongation under static and physiological shear stress conditions. • Proplatelet formation is a process that can be divided into repetitive phases: extension, pause, and retraction.Bone marrow megakaryocytes produce platelets by extending long cytoplasmic protrusions, designated proplatelets, into sinusoidal blood vessels. Although microtubules are known to regulate platelet production, the underlying mechanism of proplatelet elongation has yet to be resolved. Here we report that proplatelet formation is a process that can be divided into repetitive phases (extension, pause, and retraction), as revealed by differential interference contrast and fluorescence loss after photoconversion time-lapse microscopy. Furthermore, we show that microtubule sliding drives proplatelet elongation and is dependent on cytoplasmic dynein under static and physiological shear stress by using fluorescence recovery after photobleaching in proplatelets with fluorescence-tagged b1-tubulin. A refined understanding of the specific mechanisms regulating platelet production will yield strategies to treat patients with thrombocythemia or thrombocytopenia. (Blood. 2015;125(5):860-868)

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Motor-driven marginal band coiling promotes cell shape change during platelet activation

Abstract: During platelet activation, motor protein-induced coiling of the microtubule-based marginal band leads to the cells’ characteristic spherical shape, whereas actomyosin-mediated compression of the coil results in new microtubule polymerization in a smaller ring.

Cited by 87 publications

References 29 publications

SMIFH2 inhibition of platelets demonstrates a critical role for formin proteins in platelet cytoskeletal dynamics

SMIFH2 inhibition of platelets demonstrates a critical role for formin proteins in platelet cytoskeletal dynamics

Responses of endothelial cells, smooth muscle cells, and platelets dependent on the surface topography of polytetrafluoroethylene

Microtubule sliding drives proplatelet elongation and is dependent on cytoplasmic dynein

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