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Review Article

Platelet biomechanics, platelet bioenergetics, and applications to clinical practice and translational research

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Pages 431-439 | Received 04 Dec 2017, Accepted 01 Mar 2018, Published online: 26 Mar 2018

References

  • Kramer PA, Ravi S, Chacko B, Johnson MS, Darley-Usmar VM. A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: implications for their use as bioenergetic biomarkers. Redox Biol 2014;2:206–210. doi:10.1016/j.redox.2013.12.026
  • Paniccia R, Priora R, Liotta AA, Abbate R. Platelet function tests: a comparative review. Vasc Health Risk Manag 2015;11:133–148. doi:10.2147/VHRM.S44469
  • Born GV. Aggregation of blood platelets by adenosine diphosphate and its reversal. Nature 1962;194:927–929. doi:10.1038/194927b0
  • Hartert H. [Not Available]. Klin Wochenschr 1948;26(37–38):577–583. doi:10.1007/BF01697545
  • Doery JC, Hirsh J, Cooper I. Energy metabolism in human platelets: interrelationship between glycolysis and oxidative metabolism. Blood 1970;36(2):159–168.
  • Ravi S, Chacko B, Sawada H, Kramer PA, Johnson MS, Benavides GA, O’Donnell V, Marques MB, Darley-Usmar VM. Metabolic plasticity in resting and thrombin activated platelets. PLoS One 2015;10(4):e0123597. doi:10.1371/journal.pone.0123597
  • Akkerman JW, Holmsen H. Interrelationships among platelet responses: studies on the burst in proton liberation, lactate production, and oxygen uptake during platelet aggregation and Ca2+ secretion. Blood 1981;57(5):956–966.
  • Vasta V, Meacci E, Farnararo M, Bruni P. Glutamine transport and enzymatic activities involved in glutaminolysis in human platelets. Biochim Biophys Acta 1995;1243(1):43–48. doi:10.1016/0304-4165(94)00118-H
  • Cohen P, Derksen A, Van den Bosch H. Pathways of fatty acid metabolism in human platelets. J Clin Invest 1970;49(1):128–139. doi:10.1172/JCI106211
  • Chacko BK, Kramer PA, Ravi S, Johnson MS, Hardy RW, Ballinger SW, Darley-Usmar VM. Methods for defining distinct bioenergetic profiles in platelets, lymphocytes, monocytes, and neutrophils, and the oxidative burst from human blood. Lab Invest 2013;93(6):690–700. doi:10.1038/labinvest.2013.53
  • Rendu F, Brohard-Bohn B. The platelet release reaction: granules’ constituents, secretion and functions. Platelets 2001;12(5):261–273. doi:10.1080/09537100120068170
  • Qiu Y, Brown AC, Myers DR, Sakurai Y, Mannino RG, Tran R, Ahn B, Hardy ET, Kee MF, Kumar S, others. Platelet mechanosensing of substrate stiffness during clot formation mediates adhesion, spreading, and activation. Proc Natl Acad Sci U S A 2014;111(40):14430–14435. doi:10.1073/pnas.1322917111
  • Tobimatsu H, Nishibuchi Y, Sudo R, Goto S, Tanishita K. Adhesive forces between A1 domain of von willebrand factor and N-terminus domain of glycoprotein Ibalpha measured by atomic force microscopy. J Atheroscler Thromb 2015;22(10):1091–1099. doi:10.5551/jat.28423
  • Ruggeri ZM, Orje JN, Habermann R, Federici AB, Reininger AJ. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood 2006;108(6):1903–1910. doi:10.1182/blood-2006-04-011551
  • Nakamura F, Pudas R, Heikkinen O, Permi P, Kilpelainen I, Munday AD, Hartwig JH, Stossel TP, Ylanne J. The structure of the GPIb-filamin A complex. Blood 2006;107(5):1925–1932. doi:10.1182/blood-2005-10-3964
  • Zhang W, Deng W, Zhou L, Xu Y, Yang W, Liang X, Wang Y, Kulman JD, Zhang XF, Li R. Identification of a juxtamembrane mechanosensitive domain in the platelet mechanosensor glycoprotein Ib-IX complex. Blood 2015;125(3):562–569. doi:10.1182/blood-2014-07-589507
  • Deng W, Xu Y, Chen W, Paul DS, Syed AK, Dragovich MA, Liang X, Zakas P, Berndt MC, Di Paola J, others. Platelet clearance via shear-induced unfolding of a membrane mechanoreceptor. Nat Commun 2016;7:12863. doi:10.1038/ncomms12863
  • Ahamed J, Burg N, Yoshinaga K, Janczak CA, Rifkin DB, Coller BS. In vitro and in vivo evidence for shear-induced activation of latent transforming growth factor-beta1. Blood 2008;112(9):3650–3660. doi:10.1182/blood-2008-04-151753
  • Wu YP, De Groot PG, Sixma JJ. Shear-stress-induced detachment of blood platelets from various surfaces. Arterioscler Thromb Vasc Biol 1997;17(11):3202–3207. doi:10.1161/01.ATV.17.11.3202
  • Ugarova TP, Budzynski AZ, Shattil SJ, Ruggeri ZM, Ginsberg MH, Plow EF. Conformational changes in fibrinogen elicited by its interaction with platelet membrane glycoprotein GPIIb-IIIa. J Biol Chem 1993;268(28):21080–21087.
  • Smyth SS, Parise LV. Regulation of ligand binding to glycoprotein IIb-IIIa (integrin alpha IIb beta 3) in isolated platelet membranes. Biochem J 1993;292(Pt 3):749–758. doi:10.1042/bj2920749
  • Schwarz Henriques S, Sandmann R, Strate A, Koster S. Force field evolution during human blood platelet activation. J Cell Sci 2012;125(Pt 16):3914–3920. doi:10.1242/jcs.108126
  • Nguyen TH, Palankar R, Bui VC, Medvedev N, Greinacher A, Delcea M. Rupture forces among human blood platelets at different degrees of activation. Sci Rep 2016;6:25402. doi:10.1038/srep25402
  • Wheeler ME, Cox AC, Carroll RC. Retention of the glycoprotein IIb-IIIa complex in the isolated platelet cytoskeleton. Effects of separable assembly of platelet pseudopodal and contractile cytoskeletons. J Clin Invest 1984;74(3):1080–1089.
  • Lefebvre P, White JG, Krumwiede MD, Cohen I. Role of actin in platelet function. Eur J Cell Biol 1993;62(2):194–204.
  • Lam WA, Chaudhuri O, Crow A, Webster KD, Li TD, Kita A, Huang J, Fletcher DA. Mechanics and contraction dynamics of single platelets and implications for clot stiffening. Nat Mater 2011;10(1):61–66. doi:10.1038/nmat2903
  • Steinlechner B, Dworschak M, Birkenberg B, Duris M, Zeidler P, Fischer H, Milosevic L, Wieselthaler G, Wolner E, Quehenberger P, others. Platelet dysfunction in outpatients with left ventricular assist devices. Ann Thorac Surg 2009;87(1):131–137. doi:10.1016/j.athoracsur.2008.10.027
  • Misselwitz F, Leytin VL, Repin VS. Effect of metabolic inhibitors on platelet attachment, spreading and aggregation on collagen-coated surfaces. Thromb Res 1987;46(2):233–240. doi:10.1016/0049-3848(87)90285-4
  • Smith JB, Dangelmaier C, Selak MA, Daniel JL. Facile platelet adhesion to collagen requires metabolic energy and actin polymerization and evokes intracellular free calcium mobilization. J Cell Biochem 1991;47(1):54–61. doi:10.1002/(ISSN)1097-4644
  • Holmsen H, Setkowsky CA, Day HJ. Effects of antimycin and 2-deoxyglucose on adenine nucleotides in human platelets. Role of metabolic adenosine triphosphate in primary aggregation, secondary aggregation and shape change of platetets. Biochem J 1974;144(2):385–396. doi:10.1042/bj1440385
  • Vergun O, Han YY, Reynolds IJ. Glucose deprivation produces a prolonged increase in sensitivity to glutamate in cultured rat cortical neurons. Exp Neurol 2003;183(2):682–694. doi:10.1016/S0014-4886(03)00243-7
  • Murer EH, Hellem AJ, Rozenberg MC. Energy metabolism and platelet function. Scand J Clin Lab Invest 1967;19(3):280–282. doi:10.3109/00365516709090638
  • Chao FC, Shepro D, Tullis JL, Belamarich FA, Curby WA. Similarities between platelet contraction and cellular motility during mitosis: role of platelet microtubules in clot retraction. J Cell Sci 1976;20(3):569–588.
  • Radi R, Cassina A, Hodara R, Quijano C, Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 2002;33(11):1451–1464. doi:10.1016/S0891-5849(02)01111-5
  • Misztal T, Rusak T, Tomasiak M. Peroxynitrite may affect clot retraction in human blood through the inhibition of platelet mitochondrial energy production. Thromb Res 2014;133(3):402–411. doi:10.1016/j.thromres.2013.12.016
  • Brown AS, Moro MA, Masse JM, Cramer EM, Radomski M, Darley-Usmar V. Nitric oxide-dependent and independent effects on human platelets treated with peroxynitrite. Cardiovasc Res 1998;40(2):380–388. doi:10.1016/S0008-6363(98)00182-5
  • Merten M, Thiagarajan P. P-selectin expression on platelets determines size and stability of platelet aggregates. Circulation 2000;102(16):1931–1936. doi:10.1161/01.CIR.102.16.1931
  • Slatter DA, Aldrovandi M, O’Connor A, Allen SM, Brasher CJ, Murphy RC, Mecklemann S, Ravi S, Darley-Usmar V, O’Donnell VB. Mapping the human platelet lipidome reveals cytosolic phospholipase A2 as a regulator of mitochondrial bioenergetics during activation. Cell Metab 2016;23(5):930–944. doi:10.1016/j.cmet.2016.04.001
  • Sirajuddin S, Valdez C, DePalma L, Maluso P, Singhal R, Schroeder M, Sarani B. Inhibition of platelet function is common following even minor injury. J Trauma Acute Care Surg 2016;81(2):328–332. doi:10.1097/TA.0000000000001057
  • Favaloro EJ, Kershaw G, Bukuya M, Hertzberg M, Koutts J. Laboratory diagnosis of von Willebrand disorder (vWD) and monitoring of DDAVP therapy: efficacy of the PFA-100 and vWF:CBA as combined diagnostic strategies. Haemophilia 2001;7(2):180–189. doi:10.1046/j.1365-2516.2001.00487.x
  • Yin J, Zhao Z, Li Y, Wang J, Yao D, Zhang S, Yu W, Li N, Li J. Goal-directed transfusion protocol via thrombelastography in patients with abdominal trauma: a retrospective study. World J Emerg Surg 2014;9:28. doi:10.1186/1749-7922-9-28
  • Bochsen L, Wiinberg B, Kjelgaard-Hansen M, Steinbruchel DA, Johansson PI. Evaluation of the TEG platelet mapping assay in blood donors. Thromb J 2007;5:3. doi:10.1186/1477-9560-5-3
  • Solomon C, Ranucci M, Hochleitner G, Schochl H, Schlimp CJ. Assessing the methodology for calculating platelet contribution to clot strength (platelet component) in thromboelastometry and thrombelastography. Anesth Analg 2015;121(4):868–878. doi:10.1213/ANE.0000000000000859
  • White NJ, Newton JC, Martin EJ, Mohammed BM, Contaifer D Jr., Bostic JL, Brophy GM, Spiess BD, Pusateri AE, Ward KR, others. Clot formation is associated with fibrinogen and platelet forces in a cohort of severely injured emergency department trauma patients. Shock 2015;44(Suppl 1):39–44. doi:10.1097/SHK.0000000000000342
  • Kramer PA, Chacko BK, Ravi S, Johnson MS, Mitchell T, Darley-Usmar VM. Bioenergetics and the oxidative burst: protocols for the isolation and evaluation of human leukocytes and platelets. J Vis Exp 2014;(85). doi:10.3791/51301
  • Xu W, Cardenes N, Corey C, Erzurum SC, Shiva S. Platelets from asthmatic individuals show less reliance on glycolysis. PLoS One 2015;10(7):e0132007. doi:10.1371/journal.pone.0132007
  • Avila C, Huang RJ, Stevens MV, Aponte AM, Tripodi D, Kim KY, Sack MN. Platelet mitochondrial dysfunction is evident in type 2 diabetes in association with modifications of mitochondrial anti-oxidant stress proteins. Exp Clin Endocrinol Diabetes 2012;120(4):248–251. doi:10.1055/s-0031-1285833
  • Salabei JK, Gibb AA, Hill BG. Comprehensive measurement of respiratory activity in permeabilized cells using extracellular flux analysis. Nat Protoc 2014;9(2):421–438. doi:10.1038/nprot.2014.018
  • Myers DR, Qiu Y, Fay ME, Tennenbaum M, Chester D, Cuadrado J, Sakurai Y, Baek J, Tran R, Ciciliano JC, et al. Single-platelet nanomechanics measured by high-throughput cytometry. Nat Mater 2017;16:230–235.
  • Carr ME Jr. Development of platelet contractile force as a research and clinical measure of platelet function. Cell Biochem Biophys 2003;38(1):55–78. doi:10.1385/CBB:38:1:55
  • Devine DV, Serrano K. The platelet storage lesion. Clin Lab Med 2010;30(2):475–487. doi:10.1016/j.cll.2010.02.002
  • Ravi S, Chacko B, Kramer PA, Sawada H, Johnson MS, Zhi D, Marques MB, Darley-Usmar VM. Defining the effects of storage on platelet bioenergetics: the role of increased proton leak. Biochim Biophys Acta 2015;1852(11):2525–2534. doi:10.1016/j.bbadis.2015.08.026
  • Bynum JA, Meledeo MA, Getz TM, Rodriguez AC, Aden JK, Cap AP, Pidcoke HF. Bioenergetic profiling of platelet mitochondria during storage: 4 degrees C storage extends platelet mitochondrial function and viability. Transfusion 2016;56(Suppl 1):S76–S84. doi:10.1111/trf.13337
  • Harr JN, Moore EE, Chin TL, Ghasabyan A, Gonzalez E, Wohlauer MV, Banerjee A, Silliman CC, Sauaia A. Platelets are dominant contributors to hypercoagulability after injury. J Trauma Acute Care Surg 2013;74(3):756–762; discussion 762–765. doi:10.1097/TA.0b013e3182826d7e
  • Protti A, Fortunato F, Artoni A, Lecchi A, Motta G, Mistraletti G, Novembrino C, Comi GP, Gattinoni L. Platelet mitochondrial dysfunction in critically ill patients: comparison between sepsis and cardiogenic shock. Crit Care 2015;19:39. doi:10.1186/s13054-015-0762-7
  • Tutwiler V, Litvinov RI, Lozhkin AP, Peshkova AD, Lebedeva T, Ataullakhanov FI, Spiller KL, Cines DB, Weisel JW. Kinetics and mechanics of clot contraction are governed by the molecular and cellular composition of the blood. Blood 2016;127(1):149–159. doi:10.1182/blood-2015-05-647560
  • Tutwiler V, Peshkova AD, Andrianova IA, Khasanova DR, Weisel JW, Litvinov RI. Contraction of blood clots is impaired in acute ischemic stroke. Arterioscler Thromb Vasc Biol 2017;37(2):271–279. doi:10.1161/ATVBAHA.116.308622
  • Jurk K, Jahn UR, Van Aken H, Schriek C, Droste DW, Ritter MA, Bernd Ringelstein E, Kehrel BE. Platelets in patients with acute ischemic stroke are exhausted and refractory to thrombin, due to cleavage of the seven-transmembrane thrombin receptor (PAR-1). Thromb Haemost 2004;91(2):334–344.
  • Protti A, Fortunato F, Caspani ML, Pluderi M, Lucchini V, Grimoldi N, Solimeno LP, Fagiolari G, Ciscato P, Zella SM, others. Mitochondrial changes in platelets are not related to those in skeletal muscle during human septic shock. PLoS One 2014;9(5):e96205. doi:10.1371/journal.pone.0096205
  • Anderson EJ, Kypson AP, Rodriguez E, Anderson CA, Lehr EJ, Neufer PD. Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J Am Coll Cardiol 2009;54(20):1891–1898. doi:10.1016/j.jacc.2009.07.031
  • Montaigne D, Marechal X, Coisne A, Debry N, Modine T, Fayad G, Potelle C, El Arid JM, Mouton S, Sebti Y, others. Myocardial contractile dysfunction is associated with impaired mitochondrial function and dynamics in type 2 diabetic but not in obese patients. Circulation 2014;130(7):554–564. doi:10.1161/CIRCULATIONAHA.113.008476
  • Tyrrell DJ, Bharadwaj MS, Jorgensen MJ, Register TC, Molina AJ. Blood cell respirometry is associated with skeletal and cardiac muscle bioenergetics: implications for a minimally invasive biomarker of mitochondrial health. Redox Biol 2016;10:65–77. doi:10.1016/j.redox.2016.09.009
  • Zharikov S, Shiva S. Platelet mitochondrial function: from regulation of thrombosis to biomarker of disease. Biochem Soc Trans 2013;41(1):118–123. doi:10.1042/BST20120327
  • Cardenes N, Corey C, Geary L, Jain S, Zharikov S, Barge S, Novelli EM, Shiva S. Platelet bioenergetic screen in sickle cell patients reveals mitochondrial complex V inhibition, which contributes to platelet activation. Blood 2014;123(18):2864–2872. doi:10.1182/blood-2013-09-529420
  • Layios N, Delierneux C, Hego A, Huart J, Gosset C, Lecut C, Maes N, Geurts P, Joly A, Lancellotti P, others. Sepsis prediction in critically ill patients by platelet activation markers on ICU admission: a prospective pilot study. Intensive Care Med Exp 2017;5(1):32. doi:10.1186/s40635-017-0145-2
  • Blake CI, Spitz E, Leehey M, Hoffer BJ, Boyson SJ. Platelet mitochondrial respiratory chain function in Parkinson’s disease. Mov Disord 1997;12(1):3–8. doi:10.1002/(ISSN)1531-8257
  • Parker WD Jr., Filley CM, Parks JK. Cytochrome oxidase deficiency in Alzheimer’s disease. Neurology 1990;40(8):1302–1303. doi:10.1212/WNL.40.8.1302
  • Paglia G, Sigurjonsson OE, Rolfsson O, Valgeirsdottir S, Hansen MB, Brynjolfsson S, Gudmundsson S, Palsson BO. Comprehensive metabolomic study of platelets reveals the expression of discrete metabolic phenotypes during storage. Transfusion 2014;54(11):2911–2923. doi:10.1111/trf.12710

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