دورية أكاديمية
An extensional strain sensing mechanosome drives adhesion-independent platelet activation at supraphysiological hemodynamic gradients.
العنوان: | An extensional strain sensing mechanosome drives adhesion-independent platelet activation at supraphysiological hemodynamic gradients. |
---|---|
المؤلفون: | Zainal Abidin NA; The Australian Centre for Blood Diseases, Monash University, Melbourne, VIC, 3004, Australia., Poon EKW; Department of Medicine, St Vincent's Hospital, Melbourne Medical School, Faculty of Medicine, Dentistry & Health Sciences, The University of Melbourne, Fitzroy, VIC, 3065, Australia., Szydzik C; The Australian Centre for Blood Diseases, Monash University, Melbourne, VIC, 3004, Australia.; School of Engineering, RMIT University, La Trobe Street, Melbourne, VIC, 3004, Australia., Timofeeva M; Department of Mechanical Engineering, Faculty of Engineering and Information Technology, The University of Melbourne, Melbourne, VIC, 3010, Australia., Akbaridoust F; Department of Mechanical Engineering, Faculty of Engineering and Information Technology, The University of Melbourne, Melbourne, VIC, 3010, Australia., Brazilek RJ; The Australian Centre for Blood Diseases, Monash University, Melbourne, VIC, 3004, Australia., Tovar Lopez FJ; School of Engineering, RMIT University, La Trobe Street, Melbourne, VIC, 3004, Australia., Ma X; Medicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash University, Parkville, VIC, 3052, Australia., Lav C; Department of Mechanical Engineering, Faculty of Engineering and Information Technology, The University of Melbourne, Melbourne, VIC, 3010, Australia.; CFD Methodology Group, Scuderia AlphaTauri F1, Bicester, OX26 4LD, UK., Marusic I; Department of Mechanical Engineering, Faculty of Engineering and Information Technology, The University of Melbourne, Melbourne, VIC, 3010, Australia., Thompson PE; Medicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash University, Parkville, VIC, 3052, Australia., Mitchell A; School of Engineering, RMIT University, La Trobe Street, Melbourne, VIC, 3004, Australia., Ooi ASH; Department of Mechanical Engineering, Faculty of Engineering and Information Technology, The University of Melbourne, Melbourne, VIC, 3010, Australia., Hamilton JR; The Australian Centre for Blood Diseases, Monash University, Melbourne, VIC, 3004, Australia., Nesbitt WS; The Australian Centre for Blood Diseases, Monash University, Melbourne, VIC, 3004, Australia. warwick.nesbitt@monash.edu. |
المصدر: | BMC biology [BMC Biol] 2022 Mar 24; Vol. 20 (1), pp. 73. Date of Electronic Publication: 2022 Mar 24. |
نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
اللغة: | English |
بيانات الدورية: | Publisher: BioMed Central Country of Publication: England NLM ID: 101190720 Publication Model: Electronic Cited Medium: Internet ISSN: 1741-7007 (Electronic) Linking ISSN: 17417007 NLM ISO Abbreviation: BMC Biol Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: [London] : BioMed Central, c2003- |
مواضيع طبية MeSH: | Platelet Activation* , Thrombosis*, Blood Platelets/metabolism ; Hemodynamics ; Humans ; Ion Channels ; Stress, Mechanical ; von Willebrand Factor/metabolism |
مستخلص: | Background: Supraphysiological hemodynamics are a recognized driver of platelet activation and thrombosis at high-grade stenosis and in blood contacting circulatory support devices. However, whether platelets mechano-sense hemodynamic parameters directly in free flow (in the absence of adhesion receptor engagement), the specific hemodynamic parameters at play, the precise timing of activation, and the signaling mechanism(s) involved remain poorly elucidated. Results: Using a generalized Newtonian computational model in combination with microfluidic models of flow acceleration and quasi-homogenous extensional strain, we demonstrate that platelets directly mechano-sense acute changes in free-flow extensional strain independent of shear strain, platelet amplification loops, von Willebrand factor, and canonical adhesion receptor engagement. We define an extensional strain sensing "mechanosome" in platelets involving cooperative Ca 2+ signaling driven by the mechanosensitive channel Piezo1 (as the primary strain sensor) and the fast ATP gated channel P2X1 (as the secondary signal amplifier). We demonstrate that type II PI3 kinase C2α activity (acting as a "clutch") couples extensional strain to the mechanosome. Conclusions: Our findings suggest that platelets are adapted to rapidly respond to supraphysiological extensional strain dynamics, rather than the peak magnitude of imposed wall shear stress. In the context of overall platelet activation and thrombosis, we posit that "extensional strain sensing" acts as a priming mechanism in response to threshold levels of extensional strain allowing platelets to form downstream adhesive interactions more rapidly under the limiting effects of supraphysiological hemodynamics. (© 2022. The Author(s).) |
References: | Biophys J. 1993 Jul;65(1):344-53. (PMID: 8369442) Blood. 2002 Jan 1;99(1):151-8. (PMID: 11756165) Biophys J. 2010 May 19;98(9):L35-7. (PMID: 20441731) Nat Commun. 2015 Mar 17;6:6535. (PMID: 25779105) Biophys J. 2005 Feb;88(2):1432-43. (PMID: 15533923) Methods Mol Biol. 2012;788:73-89. (PMID: 22130701) Nat Med. 2009 Jun;15(6):665-73. (PMID: 19465929) J Biol Chem. 2014 Jun 6;289(23):16565-75. (PMID: 24759099) Biophys J. 2017 Jan 10;112(1):31-45. (PMID: 28076814) Blood. 2002 Jan 1;99(1):159-67. (PMID: 11756166) Blood. 2012 Oct 11;120(15):e73-82. (PMID: 22869793) Blood. 1996 Sep 1;88(5):1525-41. (PMID: 8781407) Microcirculation. 2009 Jan;16(1):58-83. (PMID: 19191170) FEBS Lett. 2019 Jan;593(1):88-96. (PMID: 30421419) Lab Chip. 2017 Jul 25;17(15):2595-2608. (PMID: 28660968) Biophys J. 2020 Oct 20;119(8):1683-1697. (PMID: 32949489) Biorheology. 1991;28(5):355-67. (PMID: 1782391) Elife. 2017 Dec 12;6:. (PMID: 29231809) Nat Commun. 2019 Oct 3;10(1):4503. (PMID: 31582801) J Exp Med. 2003 Aug 18;198(4):661-7. (PMID: 12913094) J Thromb Haemost. 2014 Jun;12(6):987-98. (PMID: 24655807) Cell Rep. 2017 Nov 28;21(9):2357-2366. (PMID: 29186675) Arterioscler Thromb Vasc Biol. 2013 Jan;33(1):105-13. (PMID: 23104847) Blood. 2012 Jan 19;119(3):e22-34. (PMID: 22123846) J Biol Chem. 2002 Jan 25;277(4):2965-72. (PMID: 11713259) Nat Commun. 2019 Mar 13;10(1):1200. (PMID: 30867417) Ann Biomed Eng. 1997 Mar-Apr;25(2):344-56. (PMID: 9084839) Elife. 2015 May 22;4:. (PMID: 26001275) Thromb Haemost. 1993 Jul 1;70(1):119-23. (PMID: 8236086) Eur Heart J. 2019 Nov 1;40(41):3421-3433. (PMID: 31566246) Biophys J. 2009 Mar 18;96(6):2313-20. (PMID: 19289057) Science. 2010 Oct 1;330(6000):55-60. (PMID: 20813920) Stem Cells. 2020 Mar;38(3):410-421. (PMID: 31746084) J Cell Sci. 2003 Aug 1;116(Pt 15):3037-40. (PMID: 12829733) J Physiol. 2001 Sep 15;535(Pt 3):625-35. (PMID: 11559762) Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):10986-91. (PMID: 21690355) Blood. 2015 Aug 27;126(9):1128-37. (PMID: 26109204) J Biomech. 2010 Nov 16;43(15):2970-7. (PMID: 20728892) Thromb Haemost. 1993 Dec 20;70(6):884-93. (PMID: 8165606) Proc Natl Acad Sci U S A. 2007 May 8;104(19):7899-903. (PMID: 17470810) Sci Transl Med. 2020 Jul 22;12(553):. (PMID: 32718993) J Biol Chem. 2017 Jun 2;292(22):9204-9217. (PMID: 28416610) Lab Chip. 2020 Jul 14;20(14):2539-2548. (PMID: 32567621) J Clin Invest. 2016 Dec 1;126(12):4527-4536. (PMID: 27797339) Biochem Soc Trans. 2019 Dec 20;47(6):1833-1842. (PMID: 31754715) PLoS One. 2013 Oct 23;8(10):e74123. (PMID: 24194822) Nat Commun. 2018 Mar 14;9(1):1087. (PMID: 29540687) Blood. 2002 Oct 15;100(8):2801-11. (PMID: 12351388) Thromb Haemost. 2001 Feb;85(2):303-8. (PMID: 11246552) J Biomech Eng. 2018 May 1;140(5):. (PMID: 29450473) Am J Physiol. 1993 Nov;265(5 Pt 2):H1787-96. (PMID: 8238592) |
فهرسة مساهمة: | Keywords: Extensional strain; Hemodynamics; Mechanotransduction; Platelet |
المشرفين على المادة: | 0 (Ion Channels) 0 (PIEZO1 protein, human) 0 (von Willebrand Factor) |
تواريخ الأحداث: | Date Created: 20220325 Date Completed: 20220414 Latest Revision: 20220414 |
رمز التحديث: | 20240628 |
مُعرف محوري في PubMed: | PMC8944166 |
DOI: | 10.1186/s12915-022-01274-7 |
PMID: | 35331224 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1741-7007 |
---|---|
DOI: | 10.1186/s12915-022-01274-7 |