Differentiation of cGMP-dependent and -independent nitric oxide effects on platelet apoptosis and reactive oxygen species production using platelets lacking soluble guanylyl cyclase

Thrombosis and Haemostasis

Volumn 106, Issue 5, 2011, Pages 922-933

  Rukoyatkina, Natalia ^a,b   Walter, Ulrich ^a   Friebe, Andreas ^a   Gambaryan, Stepan ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

Author keywords

Apoptosis; cGMP; NO; PKG; Platelet; sGC

Indexed keywords

CONVULXIN; CYCLIC GMP; GUANYLATE CYCLASE; NITRIC OXIDE; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; THROMBIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTE; THROMBOCYTE ACTIVATION;

ANIMALS; APOPTOSIS; BLOOD PLATELETS; CROTALID VENOMS; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GUANYLATE CYCLASE; HUMANS; LECTINS, C-TYPE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE DONORS; PHOSPHATIDYLSERINES; PLATELET ACTIVATION; REACTIVE OXYGEN SPECIES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; THROMBIN; UNCOUPLING AGENTS;

EID: 80155138053     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH11-05-0319     Document Type: Article

References (49)

1. Geddis AE. The regulation of proplatelet production. Haematologica 2009; 94: 756-759.
2. Li J, Xia Y, Bertino AM, et al. The mechanism of apoptosis in human platelets during storage. Transfusion 2000; 40: 1320-1329.
3. Perrotta PL, Perrotta CL, Snyder EL. Apoptotic activity in stored human platelets. Transfusion 2003; 43: 526-535.
4. Verhoeven AJ, Verhaar R, Gouwerok EG, et al. The mitochondrial membrane potential in human platelets: a sensitive parameter for platelet quality. Transfusion 2005; 45: 82-89.
5. Remenyi G, Szasz R, Friese P, et al. Role of mitochondrial permeability transition pore in coated-platelet formation. Arterioscler Thromb Vasc Biol 2005; 25: 467-471.
6. Gwozdz AM, Leung R, Wang H, et al. Calpain inhibition by calpeptin does not prevent APLT activity reduction in PS-exposing platelets, but calpeptin has independent pro-apoptotic effects. Thromb Haemost 2010; 103: 1218-1227.
7. Schoenwaelder SM, Yuan Y, Josefsson EC, et al. Two distinct pathways regulate platelet phosphatidylserine exposure and procoagulant function. Blood 2009; 114: 663-666.
8. Rukoyatkina N, Begonja AJ, Geiger J, et al. Phosphatidylserine surface expression and integrin alpha IIb beta 3 activity on thrombin/convulxin stimulated platelets/ particles of different sizes. Br J Haematol 2009; 144: 591-602.
9. Rand ML, Wang H, Bang KW, et al. Procoagulant surface exposure and apoptosis in rabbit platelets: association with shortened survival and steady-state senescence. J Thromb Haemost 2004; 2: 651-659.
10. Leung R, Gwozdz AM, Wang H, et al. Persistence of procoagulant surface expression on activated human platelets: involvement of apoptosis and aminophospholipid translocase activity. J Thromb Haemost 2007; 5: 560-570.
11. Garthwaite J, Boulton CL. Nitric oxide signaling in the central nervous system. Annu Rev Physiol 1995; 57: 683-706.
12. Friebe A, Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ Res 2003; 93: 96-105.
13. Ozuyaman B, Godecke A, Kusters S, et al. Endothelial nitric oxide synthase plays a minor role in inhibition of arterial thrombus formation. Thromb Haemost 2005; 93: 1161-1167.
14. Gambaryan S, Kobsar A, Hartmann S, et al. NO-synthase-/NO-independent regulation of human and murine platelet soluble guanylyl cyclase activity. J Thromb Haemost 2008; 6: 1376-1384.
15. Tymvios C, Moore C, Jones S, et al. Platelet aggregation responses are critically regulated in vivo by endogenous nitric oxide but not by endothelial nitric oxide synthase. Br J Pharmacol 2009; 158: 1735-1742.
16. Moore C, Tymvios C, Emerson M. Functional regulation of vascular and platelet activity during thrombosis by nitric oxide and endothelial nitric oxide synthase. Thromb Haemost 2010; 104: 342-349.
17. Cooper CE, Giulivi C. Nitric oxide regulation of mitochondrial oxygen consumption II: Molecular mechanism and tissue physiology. Am J Physiol Cell Physiol 2007; 292: C1993-2003.
18. Brown GC, Cooper CE. Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 1994; 356: 295-298.
19. Hall CN, Garthwaite J. What is the real physiological NO concentration in vivo? Nitric Oxide 2009; 21: 92-103.
20. Beltran B, Mathur A, Duchen MR, et al. The effect of nitric oxide on cell respiration: A key to understanding its role in cell survival or death. Proc Natl Acad Sci USA 2000; 97: 14602-14607.
21. Tsikas D, Ikic M, Tewes KS, et al. Inhibition of platelet aggregation by S-nitrosocysteine via cGMP-independent mechanisms: evidence of inhibition of thromboxane A2 synthesis in human blood platelets. FEBS Lett 1999; 442: 162-166.
22. Sogo N, Magid KS, Shaw CA, et al. Inhibition of human platelet aggregation by nitric oxide donor drugs: relative contribution of cGMP-independent mechanisms. Biochem Biophys Res Commun 2000; 279: 412-419.
23. Crane MS, Rossi AG, Megson IL. A potential role for extracellular nitric oxide generation in cGMP-independent inhibition of human platelet aggregation: biochemical and pharmacological considerations. B J Pharmacol 2005; 144: 849-859.
24. Marcondes S, Cardoso MH, Morganti RP, et al. Cyclic GMP-independent mechanisms contribute to the inhibition of platelet adhesion by nitric oxide donor: a role for alpha-actinin nitration. Proc Natl Acad Sci USA 2006; 103: 3434-3439.
25. Begonja AJ, Gambaryan S, Geiger J, et al. Platelet NAD(P)H-oxidase-generated ROS production regulates alphaIIbbeta3-integrin activation independent of the NO/cGMP pathway. Blood 2005; 106: 2757-2760.
26. Amer J, Fibach E. Oxidative status of platelets in normal and thalassemic blood. Thromb Haemost 2004; 92: 1052-1059.
27. Liaudet L, Vassalli G, Pacher P. Role of peroxynitrite in the redox regulation of cell signal transduction pathways. Front Biosci 2009; 14: 4809-4814.
28. Mergia E, Friebe A, Dangel O, et al. Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system. J Clin Invest 2006; 116: 1731-1737.
29. Friebe A, Mergia E, Dangel O, et al. Fatal gastrointestinal obstruction and hypertension in mice lacking nitric oxide-sensitive guanylyl cyclase. Proc Natl Acad Sci USA 2007; 104: 7699-7704.
30. Dangel O, Mergia E, Karlisch K, et al. Nitric oxide-sensitive guanylyl cyclase is the only nitric oxide receptor mediating platelet inhibition. J Thromb Haemost 2010; 8: 1343-1352.
31. Almeida A, Almeida J, Bolanos JP, et al. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci USA 2001; 98: 15294-15299.
32. Mitchell DA, Morton SU, Fernhoff NB, et al. Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc Natl Acad Sci USA 2007; 104: 11609-11614.
33. Groneberg D, Konig P, Wirth A, et al. Smooth muscle-specific deletion of nitric oxide-sensitive guanylyl cyclase is sufficient to induce hypertension in mice. Circulation 2010; 121: 401-409.
34. Tiedt R, Schomber T, Hao-Shen H, et al. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood 2007; 109: 1503-1506.
35. Gambaryan S, Kobsar A, Rukoyatkina N, et al. Thrombin and collagen induce a feedback inhibitory signaling pathway in platelets involving dissociation of the catalytic subunit of protein kinase A from an NFkappaB-IkappaB complex. J Biol Chem 2010; 285: 18352-18363.
36. Gruner S, Prostredna M, Aktas B, et al. Anti-glycoprotein VI treatment severely compromises hemostasis in mice with reduced alpha2beta1 levels or concomitant aspirin therapy. Circulation 2004; 110: 2946-2951.
37. Gambaryan S, Geiger J, Schwarz UR, et al. Potent inhibition of human platelets by cGMP analogs independent of cGMP-dependent protein kinase. Blood 2004; 103: 2593-2600.
38. Mergia E, Koesling D, Friebe A. Genetic mouse models of the NO receptor 'soluble' guanylyl cyclases. Handb Exp Pharmacol 2009: 33-46.
39. Haslam RJ, Dickinson NT, Jang EK. Cyclic nucleotides and phosphodiesterases in platelets. Thromb Haemost 1999; 82: 412-423.
40. Garthwaite J. New insight into the functioning of nitric oxide-receptive guanylyl cyclase: physiological and pharmacological implications. Mol Cell Biochem 2010; 334: 221-232.
41. Feelisch M. The use of nitric oxide donors in pharmacological studies. Naunyn- Schmiedeberg Arch Pharmacol 1998; 358: 113-122.
42. Thompson AJ, Mander PK, Brown GC. The NO donor DETA-NONOate reversibly activates an inward current in neurones and is not mediated by the released nitric oxide. Br J Pharmacol 2009; 158: 1338-1343.
43. Bellamy TC, Griffiths C, Garthwaite J. Differential sensitivity of guanylyl cyclase and mitochondrial respiration to nitric oxide measured using clamped concentrations. J Biol Chem 2002; 277: 31801-31807.
44. Rodriguez-Juarez F, Aguirre E, Cadenas S. Relative sensitivity of soluble guanylate cyclase and mitochondrial respiration to endogenous nitric oxide at physiological oxygen concentration. Biochem J 2007; 405: 223-231.
45. Echtay KS, Roussel D, St-Pierre J, et al. Superoxide activates mitochondrial uncoupling proteins. Nature 2002; 415: 96-99.
46. Begonja AJ, Teichmann L, Geiger J, et al. Platelet regulation by NO/cGMP signaling and NAD(P)H oxidase-generated ROS. Blood Cells Mol Dis 2006; 36: 166-170.
47. Brookes PS, Salinas EP, Darley-Usmar K, et al. Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J Biol Chem 2000; 275: 20474-20479.
48. Piantadosi CA. Regulation of mitochondrial processes by protein S-nitrosylation. Biochimica et biophysica acta 2011; in print.
49. Schrammel A, Behrends S, Schmidt K, et al. Characterization of 1H- [1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one as a heme-site inhibitor of nitric oxide-sensitive guanylyl cyclase. Mol Pharmacol 1996; 50: 1-5.