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Research Article

Role of the NO-GC/cGMP signaling pathway in platelet biomechanics

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Article: 2313359 | Received 05 Jul 2023, Accepted 26 Jan 2024, Published online: 14 Feb 2024

References

  • Thomas SG. The structure of resting and activated platelets. In: Michelson A. editor. Platelets 4th ed. Cambridge, Massachusetts: Academic Press (Elsevier);2019. p. 47–9.
  • Cooper JN, Evans RW, Mori Brooks M, Fried L, Holmes C, Barinas-Mitchell E, Sutton-Tyrrell K. Associations between arterial stiffness and platelet activation in normotensive overweight and obese young adults. Clin Exp Hypertens. 2014;36(3):115–22. doi:10.3109/10641963.2013.789045.
  • Kaiser R, Anjum A, Kammerer L, Loew Q, Akhalkatsi A, Rossaro D, Escaig R, Droste Zu Senden A, Raude B, Lorenz M, et al. Mechanosensing via a GpIIb/Src/14-3-3ζ axis critically regulates platelet migration in vascular inflammation. Blood. 2023 doi:10.1182/blood.2022019210. Epub ahead of print. PMID: 37018659.
  • Qiu Y, Brown AC, Myers DR, Sakurai Y, Mannino RG, Tran R, Ahn B, Hardy ET, Kee MF, Kumar S, et al. Platelet mechanosensing of substrate stiffness during clot formation mediates adhesion, spreading, and activation. Proc Natl Acad Sci USA. 2014;111(40):14430–5. doi:10.1073/pnas.1322917111.
  • Denninger JW, Marletta MA. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim Biophys Acta Bioenerg. 1999;1411(2–3):334–50. doi:10.1016/S0005-2728(99)00024-9.
  • Emerson M, Momi S, Paul W, Alberti F. Endogenous nitric oxide acts as a natural antithrombotic agent in vivo by inhibiting platelet aggregation in the pulmonary vasculature. Thromb Haemost. 1999;81(6):961–6. doi:10.1055/s-0037-1614607.
  • Wen L, Feil S, Feil R. cGMP signaling in platelets. In: Zirlik A, Bode C, Gawaz M, editors. Platelets, Haemostasis, and Inflammation. Cham: Springer; 2017. p. 231–252.
  • Pan J, Zhong F, Tan X. Soluble guanylate cyclase in NO signaling transduction. Rev Inorg Chem. 2013;33(4):193–206. doi:10.1515/revic-2013-0011.
  • Schmidt H, Schmidt PM, Stasch JP. NO- and haem-independent soluble guanylate cyclase activators. In: Schmidt H, Hofmann F, and Stasch J. editors. cGMP: generators, effectors and therapeutic implications. Berlin, Heidelberg: Springer; 2009. p. 309–39.
  • Stasch JP, Schlossmann J, Hocher B. Renal effects of soluble guanylate cyclase stimulators and activators: a review of the preclinical evidence. Curr Opin Pharmacol. 2015;21:95–104. doi:10.1016/j.coph.2014.12.014.
  • Reiss C, Mindukshev I, Bischoff V, Subramanian H, Kehrer L, Friebe A, Stasch JP, Gambaryan S, Walter U. The sGC stimulator riociguat inhibits platelet function in washed platelets but not in whole blood. Br J Pharmacol. 2015;172(21):5199–210. doi:10.1111/bph.13286.
  • Németh BT, Mátyás C, Oláh A, Lux Á, Hidi L, Ruppert M, Kellermayer D, Kökény G, Szabó G, Merkely B, et al. Cinaciguat prevents the development of pathologic hypertrophy in a rat model of left ventricular pressure overload. Sci Rep Nature. 2016;6:37166. doi:10.1038/srep37166.
  • Rheinlaender J, Schäffer TE. Mapping the mechanical stiffness of live cell with the scanning ion conductance microscopy. Soft Matter. 2013;9(12):561–74. doi:10.1039/c2sm27412d.
  • Schäffer TE. Nanomechanics of molecules and living cells with scanning ion conductance microscopy. Anal Chem. 2013;85(15):6988–94. doi:10.1021/ac400686k.
  • Seifert J, Rheinlaender J, von Eysmondt H, Schäffer TE. Mechanics of migrating platelets investigated with scanning ion conductance microscopy. Nanoscale. 2022;14(22):8192–9. doi:10.1039/D2NR01187E.
  • Baumann J, Sachs L, Otto O, Schoen I, Nestler P, Zaninetti C, Kenny M, Kranz R, von Eysmondt H, Rodriguez J, et al. Reduced platelet forces underlie impaired hemostasis in mouse models of MYH9-related disease. Sci Adv. 2022;8(20):eabn2627. doi:10.1126/sciadv.abn2627.
  • Zaninetti C, Sachs L, Palankar R. Role of platelet cytoskeleton in platelet biomechanics: Current and emerging methodologies and their potential relevance for the investigation of inherited platelet disorders. Hamostaseologie. 2020;40(3):337–47. doi:10.1055/a-1175-6783.
  • Seifert J, von Eysmondt H, Chatterjee M, Gawaz M, Schäffer TE. Effect of oxidized LDL on platelet shape, spreading, and migration investigated with deep learning platelet morphometry. Cells. 2021;10(11):2932. doi:10.3390/cells10112932.
  • Taylor KA, Smyth E, Rauzi F, Cerrone M, Khawaja AA, Gazzard B, Nelson M, Boffito M, Emerson M. Pharmacological impact of antiretroviral therapy on platelet function to investigate human immunodeficiency virus-associated cardiovascular risk. Br J Pharmacol. 2019;176(7):879–89. doi:10.1111/bph.14589.
  • Rukoyatkina N, Walter U, Friebe A, Gambaryan S. Differentiation of cGMP-dependent and -independent nitric oxide effects on platelet apoptosis and reactive oxygen species production using platelets lacking soluble guanylyl cyclase. Thromb Haemost. 2011;106(5):922–33. doi:10.1160/TH11-05-0319.
  • Tiedt R, Schomber T, Hao-Shen H, Skoda RC. Pf4-cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood. 2007;109(4):1503–6. doi:10.1182/blood-2006-04-020362.
  • Friebe A, Mergia E, Dangel O, Lange A, Koesling D, Beavo JA. Fatal gastrointestinal obstruction and hypertension in mice lacking nitric oxide-sensitive guanylyl cyclase. PNAS. 2007;104(18):7699–704. doi:10.1073/pnas.0609778104.
  • Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the arrive guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412. doi:10.1371/journal.pbio.1000412.
  • Seifert J, Rheinlaender J, Lang F, Gawaz M, Schäffer TE. Thrombin-induced cytoskeleton dynamics in spread human platelets observed with fast scanning ion conductance microscopy. Sci Rep. 2017;7(1):1–11. doi:10.1038/s41598-017-04999-6.
  • Rheinlaender J, Schäffer TE. Mapping the mechanical stiffness of live cells with the scanning ion conductance microscope. Soft Matter. 2013;9(12):3230–6. doi:10.1039/c2sm27412d.
  • Li Z, Zhang G, Marjanovic JA, Ruan C, Du X. A platelet secretion pathway mediated by cGMP-dependent protein kinase. J Biol Chem. 2004;279(41):42469–75. doi:10.1074/jbc.M401532200.
  • Libersan D, Rousseau G, Merhi Y. Differential regulation of P-selectin expression by protein kinase a and protein kinase G in thrombin-stimulated human platelets. Thromb Haemost. 2003;89(2):310–7. doi:10.1055/s-0037-1613448.
  • Hiratsuka T, Sano T, Kato H, Komatsu N, Imajo M, Kamioka Y, Sumiyama K, Banno F, Miyata T, Matsuda M, et al. Live imaging of extracellular signal-regulated kinase and protein kinase a activities during thrombus formation in mice expressing biosensors based on Förster resonance energy transfer. J Thromb Haemostasis. 2017;15(7):1487–99. doi:10.1111/jth.13723.
  • Moskalensky AE, Litvinenko AL. The platelet shape change: biophysical basis and physiological consequences. Platelets. 2019;30(5):543–548. doi:10.1080/09537104.2018.1514109.
  • Bearer EL, Prakash JM, Li Z. Actin dynamics in platelets. Int Rev Cytol. 2002;217:137–82.
  • Shin EK, Park H, Noh JY, Lim KM, Chung JH. Platelet shape changes and cytoskeleton dynamics as novel therapeutic targets for anti-thrombotic drugs. Biomol Ther. 2017;25(3):223–30. doi:10.4062/biomolther.2016.138.
  • Pike JA, Simms VA, Smith CW, Morgan NV, Khan AO, Poulter NS, Styles IB, Thomas SG. An adaptable analysis workflow for characterization of platelet spreading and morphology. Platelets. 2021;32(1):54–8. doi:10.1080/09537104.2020.1748588.
  • Sabin CA, Worm SW, Weber R, Reiss P, El-Sadr W, Dabis F, de Wit S, Law M, D’Arminio Monforte A, Friis-Møller N, et al. Use of nucleoside reverse transcriptase inhibitors and risk of myocardial infarction in HIV-infected patients enrolled in the D: A: D study: a multi-cohort collaboration. Lancet. 2008;371(9622):1417–26.
  • Yamasaki F, Furuno T, Sato K, Zhang D, Nishinaga M, Sato T, Doi Y, Sugiura T. Association between arterial stiffness and platelet activation. J Hum Hypertens. 2005;19(7):527–33. doi:10.1038/sj.jhh.1001861.
  • Lyle AN, Raaz U. Killing me un-softly: causes and mechanisms of arterial stiffness recent highlights of ATVB: early career committee contribution. Arterioscler Thromb Vasc Biol. 2018;37(2):1–11. doi:10.1161/ATVBAHA.116.308563.