Dynamics of calcium spiking, mitochondrial collapse and phosphatidylserine exposure in platelet subpopulations during activation

Journal of Thrombosis and Haemostasis

Volumn 14, Issue 9, 2016, Pages 1867-1881

  Obydennyy, S I ^a,b   Sveshnikova, A N ^a,b,c,d   Ataullakhanov, F I ^a,b,c   Panteleev, M A ^a,b,c,e  

^a Federal Research and Clinical Center of Pediatric Hematology   (Russian Federation)

^b CENTER FOR THEORETICAL PROBLEMS OF PHYSICOCHEMICAL PHARMACOLOGY   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d PIROGOV RUSSIAN NATIONAL RESEARCH MEDICAL UNIVERSITY   (Russian Federation)

^e MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

Author keywords

blood platelets; calcium signaling; mitochondria; platelet activation; protease activated receptors

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM; DYE; FIBRINOGEN; FLUORESCENT DYE; PADGEM PROTEIN; PHOSPHATIDYLSERINE; PROTEASE ACTIVATED RECEPTOR 1 AGONIST; PROTEINASE ACTIVATED RECEPTOR 1; RHOD 2; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SENSITIVE; CALCIUM SIGNALING; CALCIUM SPIKING; CALCIUM TRANSPORT; CELL LOSS; CELL SUBPOPULATION; COMPUTER SIMULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSOL; DESENSITIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DYNAMICS; FLUORESCENCE; FURA RED FLUORESCENCE; INNER MEMBRANE; INNER MEMBRANE POTENTIAL; MATHEMATICAL MODEL; MITOCHONDRIAL CALCIUM ENTRY; MITOCHONDRIAL COLLAPSE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; PRIORITY JOURNAL; SPIKE; STOCHASTIC MODEL; THROMBOCYTE; THROMBOCYTE ACTIVATION;

EID: 84988493403     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.13395     Document Type: Article

References (33)

1. Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005; 62: 971–88.
2. Podoplelova NA, Sveshnikova AN, Kurasawa JH, Sarafanov AG, Chambost H, Vasil'ev SA, Demina IA, Ataullakhanov FI, Alessi MC, Panteleev MA. Hysteresis-like binding of coagulation factors X/Xa to procoagulant activated platelets and phospholipids results from multistep association and membrane-dependent multimerization. Biochim Biophys Acta 2016; 1858: 1216–27.
3. Li Z, Delaney MK, O'Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010; 30: 2341–9.
4. Lenoci L, Duvernay M, Satchell S, DiBenedetto E, Hamm HE. Mathematical model of PAR1-mediated activation of human platelets. Mol BioSyst 2011; 7: 1129–37.
5. Stalker TJ, Newman DK, Ma P, Wannemacher KM, Brass LF. Platelet signaling. Handb Exp Pharmacol 2012; 210: 59–85.
6. Varga-Szabo D, Braun A, Nieswandt B. Calcium signaling in platelets. J Thromb Haemost 2009; 7: 1057–66.
7. Munnix IC, Cosemans JM, Auger JM, Heemskerk JW. Platelet response heterogeneity in thrombus formation. Thromb Haemost 2009; 102: 1149–56.
8. Dale GL. Coated-platelets: an emerging component of the procoagulant response. J Thromb Haemost 2005; 3: 2185–92.
9. Heemskerk JW, Mattheij NJ, Cosemans JM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost 2013; 11: 2–16.
10. Jackson SP, Schoenwaelder SM. Procoagulant platelets: are they necrotic? Blood 2010; 116: 2011–18.
11. Abaeva AA, Canault M, Kotova YN, Obydennyy SI, Yakimenko AO, Podoplelova NA, Kolyadko VN, Chambost H, Mazurov AV, Ataullakhanov FI, Nurden AT, Alessi MC, Panteleev MA. Procoagulant platelets form an alpha-granule protein-covered ‘cap’ on their surface that promotes their attachment to aggregates. J Biol Chem 2013; 288: 29621–32.
12. Kempton CL, Hoffman M, Roberts HR, Monroe DM. Platelet heterogeneity: variation in coagulation complexes on platelet subpopulations. Arterioscler Thromb Vasc Biol 2005; 25: 861–6.
13. Panteleev MA, Ananyeva NM, Greco NJ, Ataullakhanov FI, Saenko EL. Two subpopulations of thrombin-activated platelets differ in their binding of the components of the intrinsic factor X-activating complex. J Thromb Haemost 2005; 3: 2545–53.
14. Yakimenko AO, Verholomova FY, Kotova YN, Ataullakhanov FI, Panteleev MA. Identification of different proaggregatory abilities of activated platelet subpopulations. Biophys J 2012; 102: 2261–9.
15. Artemenko EO, Yakimenko AO, Pichugin AV, Ataullakhanov FI, Panteleev MA. Calpain-controlled detachment of major glycoproteins from the cytoskeleton regulates adhesive properties of activated phosphatidylserine-positive platelets. Biochem J 2016; 473: 435–48.
16. Kotova YN, Ataullakhanov FI, Panteleev MA. Formation of coated platelets is regulated by the dense granule secretion of adenosine 5′diphosphate acting via the P2Y12 receptor. J Thromb Haemost 2008; 6: 1603–5.
17. Ramstrom S, O'Neill S, Dunne E, Kenny D. Annexin V binding to platelets is agonist, time and temperature dependent. Platelets 2010; 21: 289–96.
18. Topalov NN, Kotova YN, Vasil'ev SA, Panteleev MA. Identification of signal transduction pathways involved in the formation of platelet subpopulations upon activation. Br J Haematol 2012; 157: 105–15.
19. London FS, Marcinkiewicz M, Walsh PN. PAR-1-stimulated factor IXa binding to a small platelet subpopulation requires a pronounced and sustained increase of cytoplasmic calcium. Biochemistry 2006; 45: 7289–98.
20. 2+ responses. Blood 1997; 90: 2615–25.
21. Remenyi G, Szasz R, Friese P, Dale GL. Role of mitochondrial permeability transition pore in coated-platelet formation. Arterioscler Thromb Vasc Biol 2005; 25: 467–71.
22. Jobe SM, Wilson KM, Leo L, Raimondi A, Molkentin JD, Lentz SR, Di Paola J. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood 2008; 111: 1257–65.
23. Choo HJ, Saafir TB, Mkumba L, Wagner MB, Jobe SM. Mitochondrial calcium and reactive oxygen species regulate agonist-initiated platelet phosphatidylserine exposure. Arterioscler Thromb Vasc Biol 2012; 32: 2946–55.
24. Arachiche A, Kerbiriou-Nabias D, Garcin I, Letellier T, Dachary-Prigent J. Rapid procoagulant phosphatidylserine exposure relies on high cytosolic calcium rather than on mitochondrial depolarization. Arterioscler Thromb Vasc Biol 2009; 29: 1883–9.
25. Sveshnikova AN, Ataullakhanov FI, Panteleev MA. Compartmentalized calcium signaling triggers subpopulation formation upon platelet activation through PAR1. Mol BioSyst 2015; 11: 1052–60.
26. Balabin FA, Sveshnikova AN. Computational biology analysis of platelet signaling reveals roles of feedbacks through phospholipase C and inositol 1,4,5-trisphosphate 3-kinase in controlling amplitude and duration of calcium oscillations. Math Biosci 2016; 276: 67–74.
27. Shakhidzhanov SS, Shaturny VI, Panteleev MA, Sveshnikova AN. Modulation and pre-amplification of PAR1 signaling by ADP acting via the P2Y12 receptor during platelet subpopulation formation. Biochim Biophys Acta 2015; 1850: 2518–29.
28. Mazurov AV, Pevzner DV, Antonova OA, Byzova TV, Khaspekova SG, Semenov AV, Vlasik TN, Samko AN, Staroverov II, Ruda MY. Safety, inhibition of platelet aggregation and pharmacokinetics of Fab′2 fragments of the anti-glycoprotein IIb–IIIa monoclonal antibody FRaMon in high-risk coronary angioplasty. Platelets 2002; 13: 465–77.
29. Topalov NN, Yakimenko AO, Canault M, Artemenko EO, Zakharova NV, Abaeva AA, Loosveld M, Ataullakhanov FI, Nurden AT, Alessi MC, Panteleev MA. Two types of procoagulant platelets are formed upon physiological activation and are controlled by integrin alpha(IIb)beta(3). Arterioscler Thromb Vasc Biol 2012; 32: 2475–83.
30. Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques 2011; 50: 98–115.
31. Magnus G, Keizer J. Model of beta-cell mitochondrial calcium handling and electrical activity. I. Cytoplasmic variables. Am J Physiol 1998; 274: C1158–73.
32. Alberio L, Safa O, Clemetson KJ, Esmon CT, Dale GL. Surface expression and functional characterization of alpha-granule factor V in human platelets: effects of ionophore A23187, thrombin, collagen, and convulxin. Blood 2000; 95: 1694–702.
33. Ramstrom S, Oberg KV, Akerstrom F, Enstrom C, Lindahl TL. Platelet PAR1 receptor density – correlation to platelet activation response and changes in exposure after platelet activation. Thromb Res 2008; 121: 681–8.