Metabolic plasticity in resting and thrombin activated platelets

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Ravi, Saranya ^a,b   Chacko, Balu ^a,b   Sawada, Hirotaka ^a,b   Kramer, Philip A ^a,b   Johnson, Michelle S ^a,b   Benavides, Gloria A ^a,b   O'Donnell, Valerie ^c   Marques, Marisa B ^a   Darley Usmar, Victor M ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; FATTY ACID; GLUCOSE; GLUTAMINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); THROMBIN; HEMOSTATIC AGENT;

ADULT; ARTICLE; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; GLYCOLYSIS; HUMAN; HUMAN CELL; MALE; MITOCHONDRIAL RESPIRATION; NORMAL HUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; THROMBOCYTE AGGREGATION; THROMBOCYTE METABOLISM; BLOOD CLOTTING; DRUG EFFECTS; ENERGY METABOLISM; METABOLISM; MIDDLE AGED; PHYSIOLOGY; REST; THROMBOCYTE;

ADENOSINE TRIPHOSPHATE; ADULT; BLOOD COAGULATION; BLOOD PLATELETS; ENERGY METABOLISM; FEMALE; GLYCOLYSIS; HEMOSTATICS; HUMANS; MALE; MIDDLE AGED; OXIDATIVE PHOSPHORYLATION; PLATELET AGGREGATION; REST; THROMBIN;

EID: 84928920324     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0123597     Document Type: Article

References (56)

1. Thon JN, Italiano JE Platelets: production, morphology and ultrastructure. Handb Exp Pharmacol. 2012: 3-22. doi: 10.1007/978-3-642-30726-3-1 PMID: 23027443
2. Holmsen H, Kaplan KL, Dangelmaier CA Differential energy requirements for platelet responses. A simultaneous study of aggregation, three secretory processes, arachidonate liberation, phosphatidylinositol breakdown and phosphatidate production. Biochem J. 1982; 208: 9-18. PMID: 6218802
3. Misztal T, Przeslaw K, Rusak T, Tomasiak M Peroxynitrite-altered platelet mitochondria-a new link between inflammation and hemostasis. Thromb Res. 2013; 131: e17-25. doi: 10.1016/j.thromres. 2012.11.010 PMID: 23200902
4. Furie B, Furie BC Mechanisms of thrombus formation. N Engl J Med. 2008; 359: 938-949. doi: 10. 1056/NEJMra0801082 PMID: 18753650
5. 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 Biology. 2014; 2: 206-210. doi: 10.1016/j.redox.2013.12.026 PMID: 24494194
6. 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: 956-966. PMID: 6260270
7. Doery JC, Hirsh J, Cooper I Energy metabolism in human platelets: interrelationship between glycolysis and oxidative metabolism. Blood. 1970; 36: 159-168. PMID: 5427451
8. Fukami MH, Holmsen H, Salganicoff L Adenine nucleotide metabolism of blood platelets. IX. Time course of secretion and changes in energy metabolism in thrombin-treated platelets. Biochim Biophys Acta. 1976; 444: 633-643. PMID: 10970
9. Kattlove HE Platelet ATP in ADP-induced aggregation. Am J Physiol. 1974; 226: 325-329. PMID: 4811188
10. 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: 385-396. PMID: 4462589
11. Barile CJ, Herrmann PC, Tyvoll DA, Collman JP, Decreau RA, Bull BS Inhibiting platelet-stimulated blood coagulation by inhibition of mitochondrial respiration. Proc Natl Acad Sci U S A. 2012; 109: 2539-2543. doi: 10.1073/pnas.1120645109 PMID: 22308457
12. Rusak T, Tomasiak M, Ciborowski M Peroxynitrite can affect platelet responses by inhibiting energy production. Acta Biochim Pol. 2006; 53: 769-776. PMID: 17068635
13. Yamagishi SI, Edelstein D, Du XL, Brownlee M Hyperglycemia potentiates collagen-induced platelet activation through mitochondrial superoxide overproduction. Diabetes. 2001; 50: 1491-1494. PMID: 11375352
14. Misselwitz F, Leytin VL, Repin VS Effect of metabolic inhibitors on platelet attachment, spreading and aggregation on collagen-coated surfaces. Thromb Res. 1987; 46: 233-240. PMID: 3603423
15. Chaudhry AA, Sagone AL Jr, Metz EN, Balcerzak SP Relationship of glucose oxidation to aggregation of human platelets. Blood. 1973; 41: 249-258. PMID: 4707615
16. Leytin V, Allen DJ, Mykhaylov S, Lyubimov E, Freedman J Thrombin-triggered platelet apoptosis. J Thromb Haemost. 2006; 4: 2656-2663. PMID: 16961585
17. Remenyi G, Szasz R, Friese P, Dale GL Role of mitochondrial permeability transition pore in coatedplatelet formation. Arterioscler Thromb Vasc Biol. 2005; 25: 467-471. PMID: 15591217
18. Leytin V, Allen DJ, Mutlu A, Gyulkhandanyan AV, Mykhaylov S, Freedman J Mitochondrial control of platelet apoptosis: effect of cyclosporin A, an inhibitor of the mitochondrial permeability transition pore. Lab Invest. 2009; 89: 374-384. doi: 10.1038/labinvest.2009.13 PMID: 19238135
19. Liu F, Gamez G, Myers DR, Clemmons W, Lam WA, Jobe SM Mitochondrially mediated integrin alphaIIbbeta3 protein inactivation limits thrombus growth. J Biol Chem. 2013; 288: 30672-30681. doi: 10.1074/jbc.M113.472688 PMID: 24014035
20. Jobe SM, Wilson KM, Leo L, Raimondi A, Molkentin JD, Lentz SR, et al. Critical role for the mitochondrial permeability transition pore and cyclophilin D in platelet activation and thrombosis. Blood. 2008; 111: 1257-1265. PMID: 17989312
21. Donabedian R, Nemerson Y Fatty acid oxidation by human platelets and its stimulation by thrombin. Am J Physiol. 1971; 221: 1283-1286. PMID: 5124271
22. Cohen P, Derksen A, Van den Bosch H Pathways of fatty acid metabolism in human platelets. J Clin Invest. 1970; 49: 128-139. PMID: 5409801
23. Majerus PW, Smith MB, Clamon GH Lipid metabolism in human platelets. I. Evidence for a complete fatty acid synthesizing system. J Clin Invest. 1969; 48: 156-164. PMID: 5765018
24. Willoughby SR, Chirkov YY, Kennedy JA, Murphy GA, Chirkova LP, Horowitz JD Inhibition of longchain fatty acid metabolism does not affect platelet aggregation responses. Eur J Pharmacol. 1998; 356: 207-213. PMID: 9774251
25. Vasta V, Meacci E, Farnararo M, Bruni P Glutamine transport and enzymatic activities involved in glutaminolysis in human platelets. Biochim Biophys Acta. 1995; 1243: 43-48. PMID: 7827106
26. Vasta V, Meacci E, Farnararo M, Bruni P Glutamine utilization in resting and stimulated platelets. J Biochem. 1993; 114: 163-166. PMID: 7903295
27. 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.
28. Chacko BK, Kramer PA, Ravi S, Johnson MS, Hardy RW, Ballinger SW, et al. Methods for defining distinct bioenergetic profiles in platelets, lymphocytes, monocytes, and neutrophils, and the oxidative burst from human blood. Laboratory investigation; a journal of technical methods and pathology. 2013; 93: 690-700. doi: 10.1038/labinvest.2013.53 PMID: 23528848
29. Walkowiak B, Kesy A, Michalec L Microplate reader-a convenient tool in studies of blood coagulation. Thromb Res. 1997; 87: 95-103. PMID: 9253804
30. Chacko BK, Kramer PA, Ravi S, Johnson MS, Hardy RW, Ballinger SW, et al. Methods for defining distinct bioenergetic profiles in platelets, lymphocytes, monocytes, and neutrophils, and the oxidative burst from human blood. Lab Invest. 2013; 93: 690-700. doi: 10.1038/labinvest.2013.53 PMID: 23528848
31. Pike LS, Smift AL, Croteau NJ, Ferrick DA, Wu M Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Biochim Biophys Acta. 2011; 1807: 726-734. PMID: 21692241
32. Bednar B, Condra C, Gould RJ, Connolly TM Platelet aggregation monitored in a 96 well microplate reader is useful for evaluation of platelet agonists and antagonists. Thromb Res. 1995; 77: 453-463. PMID: 7778060
33. Salabei JK, Gibb AA, Hill BG Comprehensive measurement of respiratory activity in permeabilized cells using extracellular flux analysis. Nature protocols. 2014; 9: 421-438. doi: 10.1038/nprot.2014. 018 PMID: 24457333
34. Coolen EJ, Arts IC, Swennen EL, Bast A, Stuart MA, Dagnelie PC Simultaneous determination of adenosine triphosphate and its metabolites in human whole blood by RP-HPLC and UV-detection. J Chromatogr B Analyt Technol Biomed Life Sci. 2008; 864: 43-51. doi: 10.1016/j.jchromb.2008.01.033 PMID: 18282748
35. Perez J, Hill BG, Benavides GA, Dranka BP, Darley-Usmar VM Role of cellular bioenergetics in smooth muscle cell proliferation induced by platelet-derived growth factor. Biochem J. 2010; 428: 255-267. doi: 10.1042/BJ20100090 PMID: 20331438
36. Atkinson DE Regulation of enzyme function. Annu Rev Microbiol. 1969; 23: 47-68. PMID: 4900062
37. Reaven GM, Chang H, Hoffman BB Additive hypoglycemic effects of drugs that modify free-fatty acid metabolism by different mechanisms in rats with streptozocin-induced diabetes. Diabetes. 1988; 37: 28-32. PMID: 3275556
38. Kantor PF, Lucien A, Kozak R, Lopaschuk GD The antianginal drug trimetazidine shifts cardiac energy metabolism from fatty acid oxidation to glucose oxidation by inhibiting mitochondrial long-chain 3-ketoacyl coenzyme A thiolase. Circ Res. 2000; 86: 580-588. PMID: 10720420
39. Astarie-Dequeker C, Joulin Y, Devynck MA Inhibitory effect of trimetazidine on thrombin-induced aggregation and calcium entry into human platelets. J Cardiovasc Pharmacol. 1994; 23: 401-407. PMID: 7515983
40. Thangavelu K, Chong QY, Low BC, Sivaraman J Structural basis for the active site inhibition mechanism of human kidney-type glutaminase (KGA). Sci Rep. 2014; 4: 3827. doi: 10.1038/srep03827 PMID: 24451979
41. Siddiqui TI, Kumar KSA, Dikshit DK Platelets and atherothrombosis: causes, targets and treatments for thrombosis. Curr Med Chem. 2013; 20: 2779-2797. PMID: 23590713
42. Kim SJ, Bang OY Antiplatelet therapy for preventing stroke in patients with chronic kidney disease. Contrib Nephrol. 2013; 179: 119-129. doi: 10.1159/000346730 PMID: 23652455
43. Levi M, Schultz M, van der Poll T Sepsis and thrombosis. Semin Thromb Hemost. 2013; 39: 559-566. doi: 10.1055/s-0033-1343894 PMID: 23625756
44. Galbusera M, Remuzzi G, Boccardo P Treatment of bleeding in dialysis patients. Semin Dial. 2009; 22: 279-286. doi: 10.1111/j.1525-139X.2008.00556.x PMID: 19573008
45. Halestrap AP Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans. 2006; 34: 232-237. PMID: 16545083
46. Halestrap AP, Clarke SJ, Javadov SA Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res. 2004; 61: 372-385. PMID: 14962470
47. Niu X, Whisson ME, Guppy M Types and sources of fuels for platelets in a medium containing minimal added fuels and a low carryover plasma. Br J Haematol. 1997; 97: 908-916. PMID: 9217196
48. Derksen A, Cohen P Patterns of fatty acid release from endogenous substrates by human platelet homogenates and membranes. J Biol Chem. 1975; 250: 9342-9347. PMID: 394
49. Wanders RJ, Vreken P, Ferdinandusse S, Jansen GA, Waterham HR, van Roermund CW, et al. Peroxisomal fatty acid alpha- and beta-oxidation in humans: enzymology, peroxisomal metabolite transporters and peroxisomal diseases. Biochem Soc Trans. 2001; 29: 250-267. PMID: 11356164
50. Marnett LJ, Rowlinson SW, Goodwin DC, Kalgutkar AS, Lanzo CA Arachidonic acid oxygenation by COX-1 and COX-2. Mechanisms of catalysis and inhibition. J Biol Chem. 1999; 274: 22903-22906. PMID: 10438452
51. Borst P, Loos JA, Christ EJ, Slater EC Uncoupling activity of long-chain fatty acids. Biochim Biophys Acta. 1962; 62: 509-518. PMID: 13871487
52. Samartsev VN, Rybakova SR, Dubinin MV [Interaction of free fatty acids with mitochondria during uncoupling of oxidative phosphorylation]. Biofizika. 2013; 58: 481-487. PMID: 24159817
53. Rottenberg H, Steiner-Mordoch S Free fatty acids decouple oxidative phosphorylation by dissipating intramembranal protons without inhibiting ATP synthesis driven by the proton electrochemical gradient. FEBS Lett. 1986; 202: 314-318. PMID: 2873057
54. Bassit RA, Sawada LA, Bacurau RF, Navarro F, Martins E Jr., Santos RV, et al. Branched-chain amino acid supplementation and the immune response of long-distance athletes. Nutrition. 2002; 18: 376-379. PMID: 11985939
55. Newsholme P Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? J Nutr. 2001; 131: 2515S-2522S; discussion 2523S-2514S. PMID: 11533304
56. Mookerjee SA, Goncalves RL, Gerencser AA, Nicholls DG, Brand MD The contributions of respiration and glycolysis to extracellular acid production. Biochim Biophys Acta. 2015; 1847: 171- 181. doi: 10. 1016/j.bbabio.2014.10.005 PMID: 25449966