Potent inhibition of human platelets by cGMP analogs independent of cGMP-dependent protein kinase
Abstract
Platelets play a key role in hemostasis through their ability to rapidly adhere to activated or injured endothelium, subendothelial matrix proteins, and other activated platelets. A strong equilibrium between activating and inhibiting processes is essential for normal platelet and vascular function, impairment of this equilibrium being associated with either thrombophilic or bleeding disorders. Both cyclic guanosine monophosphate (cGMP) and cyclic adenosine monophosphate (cAMP) have been established as crucial and synergistic intracellular messengers that mediate the effects of platelet inhibitors such as nitric oxide (NO) and prostacyclin (PG-I2). However, it was recently suggested that a rapid cGMP/cGMP-dependent protein kinase (cGK)–mediated extracellular signal-related kinase (ERK) phosphorylation promotes platelet activation. This hypothesis was examined here by evaluating established and proposed cGK activators/inhibitors with respect to their capacity to promote either platelet activation or inhibition. In particular, the regulatory role of cGK for ERK phosphorylation and thrombin-, thromboxane-, and VWF-induced platelet activation was investigated. The data obtained do not support the concept that cGK-mediated ERK phosphorylation promotes platelet activation but confirm the inhibitory role of cGK in platelet function. One explanation for these discrepancies is the novel finding that extracellular cGMP analogs potently and rapidly inhibit thrombin-, thromboxane-, and VWF-induced human platelet signaling and activation by a cGK-independent mechanism.
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NO is a potent inhibitor of PLT aggregation, acting via activation of soluble guanylyl cyclase in PLTs.
“NO is a potent inhibitor of PLT aggregation, acting via activation of soluble guanylyl cyclase in PLTs (64, 65).”
From Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism, Anemia (2017) · cites this paper as [64]
Cites
Atherosclerosis--an inflammatory disease
Ross, R. (1999) · New England Journal of Medicine · doi:10.1056/nejm199901143400207 · Cited by 21,725 · see citing works
Inflammation in atherosclerosis
Libby, P. (2002) · Nature · doi:10.1038/nature01323 · Cited by 8,315 · see citing works
Ruggeri, Z. M. (2002) · Nature Medicine · doi:10.1038/nm1102-1227 · Cited by 1,592 · see citing works
The specificities of protein kinase inhibitors: an update
BAIN, J., McLAUCHLAN, H., ELLIOTT, M., & COHEN, P. (2003) · Biochemical Journal · doi:10.1042/bj20021535 · Cited by 1,369 · see citing works
Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E
Huo, Y., Schober, A., Forlow, S. B., Smith, D. F., Hyman, M. C., Jung, S., Littman, D. R., Weber, C., & Ley, K. F. (2002) · Nature Medicine · doi:10.1038/nm810 · Cited by 1,008 · see citing works
A Critical Role of Platelet Adhesion in the Initiation of Atherosclerotic Lesion Formation
Maßberg, S., Brand, K., Grüner, S., Page, S., Müller, E., Müller, I. I., Bergmeier, W., Richter, T., Lorenz, M. C., Konrad, I., et al. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20012044 · Cited by 881 · see citing works
Scientific and therapeutic advances in antiplatelet therapy
Bhatt, D. L., & Topol, E. J. (2002) · Nature Reviews Drug Discovery · doi:10.1038/nrd985 · Cited by 409 · see citing works
Platelet P-selectin facilitates atherosclerotic lesion development
Burger, P. C., & Wagner, D. D. (2003) · Blood · doi:10.1182/blood-2002-07-2209 · Cited by 409 · see citing works
Distinct and specific functions of cGMP-dependent protein kinases
Lohmann, S. M., Vaandrager, A. B., Smolenski, A., Walter, U., & de Jonge, H. R. (1997) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(97)01086-4 · Cited by 383 · see citing works
Self-citationRising behind NO: cGMP-dependent protein kinases
Hofmann, F. B., Ammendola, A., & Schlossmann, J. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.10.1671 · Cited by 340 · see citing works
Smolenski, A., Bachmann, C., Reinhard, K., Hönig‐Liedl, P., Jarchau, T., Hoschuetzky, H., & Walter, U. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.32.20029 · Cited by 332 · see citing works
Self-citationSchwarz, U. R., Walter, U., & Eigenthaler, M. (2001) · Biochemical Pharmacology · doi:10.1016/s0006-2952(01)00760-2 · Cited by 329 · see citing works
Self-citationMünzel, T., Feil, R., Mülsch, A., Lohmann, S. M., Hofmann, F., & Walter, U. (2003) · Circulation · doi:10.1161/01.cir.0000094403.78467.c3 · Cited by 316 · see citing works
Self-citationA Stimulatory Role for cGMP-Dependent Protein Kinase in Platelet Activation
Li, Z., Xi, X., Gu, M., Feil, R., Ye, R. D., Eigenthaler, M., Hofmann, F. B., & Du, X. (2003) · Cell · doi:10.1016/s0092-8674(02)01254-0 · Cited by 264 · see citing works
Maßberg, S., Sausbier, M., Klatt, P., Bauer, M., Pfeifer, A., Siess, W., Fässler, R., Ruth, P., Krombach, F., & Hofmann, F. B. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.8.1255 · Cited by 224 · see citing works
Eigenthaler, M., NOLTE, C., Halbrügge, M., & Walter, U. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16803.x · Cited by 169 · see citing works
Self-citationCyclic Nucleotides and Phosphodiesterases in Platelets
Dickinson, N., Jang, E., & Haslam, R. (1999) · Thrombosis and Haemostasis · doi:10.1055/s-0037-1615861 · Cited by 164 · see citing works
Functional analysis of cGMP-dependent protein kinases I and II as mediators of NO/cGMP effects
Smolenski, A., Burkhardt, A. M., Eigenthaler, M., Butt, E., Gambaryan, S. P., Lohmann, S. M., & Walter, U. (1998) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/pl00005234 · Cited by 141 · see citing works
Self-citationLi, Z., Marjanovic, J., Eigenthaler, M., & Du, X. (2003) · Blood · doi:10.1182/blood-2002-10-3210 · Cited by 132 · see citing works
Smolenski, A., Poller, W. C., Walter, U., & Lohmann, S. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m909632199 · Cited by 132 · see citing works
Self-citationBurkhardt, M., Glazova, M. V., Gambaryan, S. P., Vollkommer, T., Butt, E., Bader, B., Heermeier, K., Lincoln, T., Walter, U., & Palmetshofer, A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m005670200 · Cited by 122 · see citing works
Self-citationLi, Z., Xi, X., & Du, X. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106129200 · Cited by 122 · see citing works
Aktas, B., Utz, A. L., Hönig‐Liedl, P., Walter, U., & Geiger, J. (2003) · Stroke · doi:10.1161/01.str.0000056527.34434.59 · Cited by 116 · see citing works
Self-citationShimizu‐Albergine, M., Rybalkin, S. D., Rybalkina, I. G., Feil, R., Wolfsgruber, W., Hofmann, F. B., & Beavo, J. A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-16-06452.2003 · Cited by 95 · see citing works
Tremblay, J., Gerzer, R., & Hamet, P. (1988) · PubMed · Cited by 91 · see citing works
Marshall, S. J., Senis, Y. A., Auger, J. M., Feil, R., Hofmann, F. B., Salmon, G. P., Peterson, J. T., Burslem, F., & Watson, S. P. (2003) · Blood · doi:10.1182/blood-2003-09-3319 · Cited by 81 · see citing works
Eigenthaler, M., Ullrich, H., Geiger, J., Horstrup, K., Hönig‐Liedl, P., Wiebecke, D., & Walter, U. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)38681-8 · Cited by 80 · see citing works
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Evgenov, O. V., Pacher, P., Schmidt, P. M., Haskó, G., Schmidt, H. H. H. W., & Stasch, J. (2006) · Nature Reviews Drug Discovery · doi:10.1038/nrd2038 · Cited by 748 · see citing works
Red Blood Cell Function and Dysfunction: Redox Regulation, Nitric Oxide Metabolism, Anemia
Kuhn, V., Diederich, L., Keller, T. C. S., Kramer, C. M., Lückstädt, W., Panknin, C., Suvorava, T., Isakson, B. E., Kelm, M., & Cortese-Krott, M. M. (2017) · Antioxidants & Redox Signaling · doi:10.1089/ars.2016.6954 · Cited by 469 · see citing works
Function of cGMP-Dependent Protein Kinases as Revealed by Gene Deletion
Hofmann, F. B., Feil, R., Kleppisch, T., & Schlossmann, J. (2005) · Physiological Reviews · doi:10.1152/physrev.00015.2005 · Cited by 395 · see citing works
Novel roles of cAMP/cGMP‐dependent signaling in platelets
Smolenski, A. (2011) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2011.04576.x · Cited by 312 · see citing works
The Biology of Cyclic GMP-dependent Protein Kinases
Hofmann, F. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.r400035200 · Cited by 245 · see citing works
Begonja, A. J., Gambaryan, S. P., Geiger, J., Aktas, B., Požgajová, M., Nieswandt, B., & Walter, U. (2005) · Blood · doi:10.1182/blood-2005-03-1047 · Cited by 225 · see citing works
Self-citationMechanisms of flavonoid protection against myocardial ischemia–reperfusion injury
Akhlaghi, M., & Bandy, B. (2008) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2008.12.003 · Cited by 212 · see citing works
NO/cGMP-Dependent Modulation of Synaptic Transmission
Feil, R., & Kleppisch, T. (2007) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-74805-2_16 · Cited by 190 · see citing works
Signalling through the platelet glycoprotein Ib-V–IX complex
Canobbio, I., Balduini, C., & Torti, M. (2004) · Cellular Signalling · doi:10.1016/j.cellsig.2004.05.008 · Cited by 151 · see citing works
Gambaryan, S. P., Kobsar, A. L., Rukoyatkina, N., Herterich, S., Geiger, J., Smolenski, A., Lohmann, S. M., & Walter, U. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.077602 · Cited by 150 · see citing works
Self-citationIRAG mediates NO/cGMP-dependent inhibition of platelet aggregation and thrombus formation
Antl, M., von Brühl, M.-L., Eiglsperger, C., Werner, M. E., Konrad, I., Köcher, T., Wilm, M. S., Hofmann, F. B., Maßberg, S., & Schlossmann, J. (2006) · Blood · doi:10.1182/blood-2005-10-026294 · Cited by 145 · see citing works
Aburima, A. A., Wraith, K. S., Raslan, Z., Law, R., Magwenzi, S., & Naseem, K. M. (2013) · Blood · doi:10.1182/blood-2013-03-487850 · Cited by 119 · see citing works
GAMBARYAN, S., KOBSAR, A., HARTMANN, S., BIRSCHMANN, I., KUHLENCORDT, P. J., MÜLLER‐ESTERL, W., LOHMANN, S. M., & WALTER, U. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.03014.x · Cited by 118 · see citing works
Self-citationBirschmann, I., & Walter, U. (2004) · Acta Biochimica Polonica · doi:10.18388/abp.2004_3579 · Cited by 115 · see citing works
Self-citationEffects of the NO/soluble guanylate cyclase/cGMP system on the functions of human platelets
Makhoul, S., Walter, E., Pagel, O., Walter, U., Sickmann, A., Gambaryan, S. P., Smolenski, A., Zahedi, R. P., & Jurk, K. (2018) · Nitric Oxide · doi:10.1016/j.niox.2018.03.008 · Cited by 102 · see citing works
Self-citationRap1GAP2 is a new GTPase-activating protein of Rap1 expressed in human platelets
Schultess, J., Danielewski, O., & Smolenski, A. (2005) · Blood · doi:10.1182/blood-2004-09-3605 · Cited by 101 · see citing works
Jkt, W., Pula, G., & Poole, A. W. (2005) · Biochemical Journal · doi:10.1042/bj20050796 · Cited by 98 · see citing works
cGMP and cGMP-Dependent Protein Kinase in Platelets and Blood Cells
Walter, U., & Gambaryan, S. P. (2008) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-68964-5_23 · Cited by 97 · see citing works
Self-citationFunction of cGMP-dependent Protein Kinases in the Nervous System
Feil, R., Hofmann, F. B., & Kleppisch, T. (2005) · Reviews in the Neurosciences · doi:10.1515/revneuro.2005.16.1.23 · Cited by 85 · see citing works
Marshall, S. J., Senis, Y. A., Auger, J. M., Feil, R., Hofmann, F. B., Salmon, G. P., Peterson, J. T., Burslem, F., & Watson, S. P. (2003) · Blood · doi:10.1182/blood-2003-09-3319 · Cited by 81 · see citing works
Akbar, H., Kim, J. J. Y. B., Funk, K. M., Cancelas, J. A., Shang, X., Chen, L., Johnson, J. F., Williams, D. A., & Zheng, Y. (2007) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2007.02646.x · Cited by 75 · see citing works
cGMP-binding Prepares PKG for Substrate Binding by Disclosing the C-terminal Domain
Alverdi, V., Mazon, H., Versluis, C., Hemrika, W., Esposito, G., van den Heuvel, R. H. H., Scholten, A., & Heck, A. J. R. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.11.053 · Cited by 73 · see citing works
Yang, S.-A., Carpenter, C. L., & Abrams, C. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404335200 · Cited by 72 · see citing works
Protein kinase A mediates inhibition of the thrombin-induced platelet shape change by nitric oxide
Jensen, B. O., Selheim, F., Døskeland, S. O., Gear, A. R. L., & Holmsen, H. (2004) · Blood · doi:10.1182/blood-2004-03-1058 · Cited by 70 · see citing works
Biphasic roles for soluble guanylyl cyclase (sGC) in platelet activation
Zhang, G., Xiang, B., Dong, A., Skoda, R. C., Daugherty, A., Smyth, S. S., Du, X., & Li, Z. (2011) · Blood · doi:10.1182/blood-2011-03-341107 · Cited by 69 · see citing works
cGMP-dependent protein kinases in drug discovery
Schlossmann, J., & Hofmann, F. B. (2005) · Drug Discovery Today · doi:10.1016/s1359-6446(05)03406-9 · Cited by 69 · see citing works
Gambaryan, S. P., & Tsikas, D. (2015) · Amino Acids · doi:10.1007/s00726-015-1986-1 · Cited by 67 · see citing works
Self-citationcGMP Signaling and Vascular Smooth Muscle Cell Plasticity
Lehners, M., Dobrowinski, H., Feil, S. C., & Feil, R. (2018) · Journal of Cardiovascular Development and Disease · doi:10.3390/jcdd5020020 · Cited by 67 · see citing works
Inhibitory effect of aqueous extracts of some herbs on human platelet aggregation in vitro
Pierre, S., Crosbie, L., & Duttaroy, A. K. (2005) · Platelets · doi:10.1080/09537100500129540 · Cited by 64 · see citing works
The NO/cGMP pathway inhibits Rap1 activation in human platelets via cGMP-dependent protein kinase I
Danielewski, O., Schultess, J., & Smolenski, A. (2005) · Thrombosis and Haemostasis · doi:10.1160/th04-09-0582 · Cited by 62 · see citing works
Tracking functions of cGMP-dependent protein kinases (cGK)
Suzanne, M. L. (2005) · Frontiers in bioscience · doi:10.2741/1621 · Cited by 62 · see citing works
Reduced Vascular NO Bioavailability in Diabetes Increases Platelet Activation In Vivo
Schäfer, A., Alp, N. J., Cai, S., Lygate, C. A., Neubauer, S., Eigenthaler, M., Bauersachs, J. K., & Channon, K. M. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000138072.76902.dd · Cited by 62 · see citing works
The Role of NO/sGC/cGMP/PKG Signaling Pathway in Regulation of Platelet Function
Gambaryan, S. P. (2022) · Cells · doi:10.3390/cells11223704 · Cited by 61 · see citing works
Self-citationVaiyapuri, S., Ali, M. S., Moraes, L. A., Sage, T., Lewis, K. R., Jones, C. I., & Gibbins, J. M. (2013) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.113.301988 · Cited by 60 · see citing works
Platelet regulation by NO/cGMP signaling and NAD(P)H oxidase-generated ROS
Begonja, A. J., Teichmann, L. L., Geiger, J., Gambaryan, S. P., & Walter, U. (2006) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.12.028 · Cited by 56 · see citing works
Self-citationUnresolved roles of platelet nitric oxide synthase
Naseem, K. M., & RIBA, R. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2007.02802.x · Cited by 53 · see citing works
Begonja, A. J., Geiger, J., Rukoyatkina, N., Rauchfuss, S., Gambaryan, S. P., & Walter, U. (2006) · Blood · doi:10.1182/blood-2006-07-038158 · Cited by 53 · see citing works
Self-citationRukoyatkina, N., Викторович, М. И., Walter, U., & Gambaryan, S. P. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.459 · Cited by 48 · see citing works
Self-citationRukoyatkina, N., Walter, U., Friebe, A., & Gambaryan, S. P. (2011) · Thrombosis and Haemostasis · doi:10.1160/th11-05-0319 · Cited by 48 · see citing works
Self-citationPhosphorylation of CalDAG‐GEFI by protein kinase A prevents Rap1b activation
Subramanian, H., Zahedi, R. P., Sickmann, A., Walter, U., & Gambaryan, S. P. (2013) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.12271 · Cited by 47 · see citing works
Self-citationBladowski, M., Gawryś, J., Gajecki, D., Szahidewicz-Krupska, E., Sawicz-Bladowska, A., & Doroszko, A. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/2979260 · Cited by 46 · see citing works
A heretical view on the role of NO and cGMP in vascular proliferative diseases
Feil, R., Feil, S. C., & Hofmann, F. B. (2005) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2004.12.001 · Cited by 45 · see citing works
Викторович, М. И., Gambaryan, S. P., Kehrer, L., Schuetz, C., Kobsar, A. L., Rukoyatkina, N., Nikolaev, V. O., Кривченко, А. И., Watson, S. P., Walter, U., et al. (2011) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2011.817 · Cited by 44 · see citing works
Self-citationValtcheva, N., Nestorov, P., Beck, A., Russwurm, M., Hillenbrand, M., Weinmeister, P., & Feil, R. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806161200 · Cited by 43 · see citing works
RIBA, R., Oberprieler, N. G., Roberts, W., & Naseem, K. M. (2006) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2006.02195.x · Cited by 42 · see citing works
Phosphoproteomics of human platelets: A quest for novel activation pathways
Zahedi, R. P., Begonja, A. J., Gambaryan, S. P., & Sickmann, A. (2006) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2006.08.017 · Cited by 41 · see citing works
Self-citationSun, Z., Lü, F., Cheng, J., Zhang, M., Zhang, Y., Xiong, W., Zhao, Y., & Qu, H. (2018) · Artificial Cells Nanomedicine and Biotechnology · doi:10.1080/21691401.2018.1492419 · Cited by 40 · see citing works
Yang, H., Jin, S., Jang, H., Kim, J., Lee, J., Kim, J., & Kim, H.-S. (2019) · Scientific Reports · doi:10.1038/s41598-019-44190-7 · Cited by 40 · see citing works
Aburima, A. A., Walladbegi, K., Wake, J. D., & Naseem, K. M. (2017) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.13738 · Cited by 39 · see citing works
The sGC stimulator riociguat inhibits platelet function in washed platelets but not in whole blood
Reiss, C., Викторович, М. И., Bischoff, V., Subramanian, H., Kehrer, L., Friebe, A., Stasch, J., Gambaryan, S. P., & Walter, U. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13286 · Cited by 35 · see citing works
Self-citationRoles of cGMP/cGMP-dependent protein kinase in platelet activation
Walter, U., & Gambaryan, S. P. (2004) · Blood · doi:10.1182/blood-2004-06-2389 · Cited by 33 · see citing works
Self-citationZHANG, S. H., Zhang, Y., Shen, J., Zhang, S., Chen, L., Gu, J., Mruk, J. S., Cheng, G., Zhu, L., Kunapuli, S. P., et al. (2013) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.12362 · Cited by 29 · see citing works
Rukoyatkina, N., Butt, E., Subramanian, H., Nikolaev, V. O., Викторович, М. И., Walter, U., Gambaryan, S. P., & Benz, P. M. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.290 · Cited by 29 · see citing works
Self-citationPediaditakis, P., Js, K., He, L., Zhang, X., Graves, L. M., & Lemasters, J. J. (2010) · Biochemical Journal · doi:10.1042/bj20091741 · Cited by 28 · see citing works
Rukoyatkina, N., Begonja, A. J., Geiger, J., Eigenthaler, M., Walter, U., & Gambaryan, S. P. (2008) · British Journal of Haematology · doi:10.1111/j.1365-2141.2008.07506.x · Cited by 27 · see citing works
Self-citationLauver, A. A., Driscoll, E. M., & Lucchesi, B. R. (2008) · Pharmacology · doi:10.1159/000132085 · Cited by 27 · see citing works
Gambaryan, S. P., Subramanian, H., Kehrer, L., Викторович, М. И., Sudnitsyna, J. S., Reiß, C., Rukoyatkina, N., Friebe, A., Sharina, I. G., Martin, E., et al. (2016) · Cell Communication and Signaling · doi:10.1186/s12964-016-0139-9 · Cited by 25 · see citing works
Self-citationDimerization of Nitric Oxide-sensitive Guanylyl Cyclase Requires the α1 N Terminus
Wagner, C., Russwurm, M., Jäger, R., Friebe, A., & Koesling, D. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412099200 · Cited by 25 · see citing works
Knowles, R., & Warner, T. D. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.08.004 · Cited by 24 · see citing works
Викторович, М. И., Fock, E. M., Dobrylko, I. A., Sudnitsyna, J. S., Gambaryan, S. P., & Panteleev, M. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810667 · Cited by 24 · see citing works
Self-citationFuentes, F., Alarcón, M. A., Badimón, L., Fuentes, M., Klotz, K., Vilahur, G., Kachler, S., Padró, T., Palomo, I. F., & Eduardo Fuentes, Q. (2017) · International Journal of Cardiology · doi:10.1016/j.ijcard.2017.08.006 · Cited by 23 · see citing works
Bilodeau, M. L., & Hamm, H. E. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.121830 · Cited by 23 · see citing works
Platelet nitric oxide signalling in heart failure: role of oxidative stress
Shah, A. M., Passacquale, G., Gkaliagkousi, Ε., Ritter, J. M., & Ferro, A. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr115 · Cited by 19 · see citing works
Burnley-Hall, N., Abdul, F. B., Androshchuk, V., Morris, K., Ossei‐Gerning, N., Anderson, R. A., Rees, A., & James, P. E. (2018) · Thrombosis and Haemostasis · doi:10.1160/th17-06-0394 · Cited by 19 · see citing works
Multifaceted effects of arachidonic acid and interaction with cyclic nucleotides in human platelets
Rukoyatkina, N., Shpakova, V., Panteleev, M., Kharazova, A., Gambaryan, S. P., & Geiger, J. (2018) · Thrombosis Research · doi:10.1016/j.thromres.2018.09.047 · Cited by 19 · see citing works
Self-citationSchweigel, H., Geiger, J., Beck, F., Buhs, S., Gerull, H., Walter, U., Sickmann, A., & Nollau, P. (2013) · PROTEOMICS · doi:10.1002/pmic.201200353 · Cited by 18 · see citing works
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RIBA, R., Patel, B., Aburima, A. A., & Naseem, K. M. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.03179.x · Cited by 18 · see citing works
Rauchfuss, S., Geiger, J., Walter, U., Renné, T., & Gambaryan, S. P. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.02925.x · Cited by 18 · see citing works
Self-citationLewis, G. D., Witzke, C. F., Colón-Hernández, P., Guerrero, J. L., Bloch, K. D., & Semigran, M. J. (2006) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2005.11.060 · Cited by 18 · see citing works
The oligopeptide DT‐2 is a specific PKG I inhibitor only in vitro, not in living cells
Gambaryan, S. P., Butt, E., Kobsar, A. L., Geiger, J., Rukoyatkina, N., Parnova, R. G., Nikolaev, V. O., & Walter, U. (2012) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2012.02044.x · Cited by 16 · see citing works
Self-citationCurcumin at Low Doses Potentiates and at High Doses Inhibits ABT-737-Induced Platelet Apoptosis
Rukoyatkina, N., Shpakova, V., Sudnitsyna, J. S., Panteleev, M., Makhoul, S., Gambaryan, S. P., & Jurk, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105405 · Cited by 14 · see citing works
Self-citationNavdaev, A., Subramanian, H., Petunin, A., Clemetson, K. J., Gambaryan, S. P., & Walter, U. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093569 · Cited by 13 · see citing works
Self-citationCyclic nucleotides inhibit MAP kinase activity in low-dose collagen-stimulated platelets
Jackson, E. C. G., & McNicol, A. (2009) · Thrombosis Research · doi:10.1016/j.thromres.2009.06.004 · Cited by 13 · see citing works
Koessler, J., Kehrer, L., Gambaryan, S. P., Walter, U., & Kobsar, A. L. (2012) · Thrombosis and Haemostasis · doi:10.1160/th11-07-0461 · Cited by 13 · see citing works
Self-citationRegulation of the renin-angiotensin-aldosterone system by cyclic nucleotides and phosphodiesterases
Gambaryan, S. P., Mohagaonkar, S., & Nikolaev, V. O. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1239492 · Cited by 12 · see citing works
Self-citationKim, J., Yang, H., Lee, J., Kim, B.-K., Jin, S., Lee, J., Park, K. W., Cho, H., Kwon, Y., Lee, H., et al. (2016) · Scientific Reports · doi:10.1038/srep36979 · Cited by 11 · see citing works
Brinkley, L. M., Brock, M. A., Stinson, G. P., Bilgili, A., Jacobs, J. P., Bleiweis, M. S., & Peek, G. J. (2024) · Perfusion · doi:10.1177/02676591241228169 · Cited by 9 · see citing works
Herfindal, L., Krakstad, C., Myhren, L. E., Hagland, H. R., Kopperud, R. K., Teigen, K., Schwede, F., Kleppe, R., & Døskeland, S. O. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094926 · Cited by 9 · see citing works
Lavõgina, D., Nickl, C. K., Enkvist, E., Raidaru, G., Lust, M., Vaasa, A., Uri, A., & Dostmann, W. R. (2010) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2010.04.007 · Cited by 8 · see citing works
Wen, L., Feil, S. C., & Feil, R. (2017) · Cardiac and vascular biology · doi:10.1007/978-3-319-66224-4_15 · Cited by 8 · see citing works
A modular systems biological modelling framework studies cyclic nucleotide signaling in platelets
Breitenbach, T., Englert, N., Osmanoğlu, Ö., Rukoyatkina, N., Wangorsch, G., Heinze, K. G., Friebe, A., Butt, E., Feil, R., Dittrich, M. T., et al. (2022) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2022.111222 · Cited by 7 · see citing works
Self-citationPark, J. Y., Oh, W. J., Kim, M., Kim, T., Cho, J. Y., Park, H.-J., Lee, I., Kim, S., Kim, G.-S., Kim, S., et al. (2012) · Platelets · doi:10.3109/09537104.2011.629309 · Cited by 7 · see citing works
Characterization of New Organic Nitrate Hybrid Drugs Covalently Bound to Valsartan and Cilostazol
Knorr, M., Hausding, M., Schulz, E., Oelze, M. W., Rümmler, R., Schuff, A., Daub, S., Schreiner, J., Kröller‐Schön, S., Wenzel, P., et al. (2012) · Pharmacology · doi:10.1159/000339861 · Cited by 7 · see citing works
On the roles of cGMP and glycoprotein Ib in platelet activation
Du, X., Marjanovic, J., & Li, Z. (2004) · Blood · doi:10.1182/blood-2004-02-0507 · Cited by 7 · see citing works
Yaylak, B., Altıntaş, B., Özcan, K. S., Akdeniz, E., Avcı, İ. İ., Zeren, G., Şimşek, B., & Karabay, C. Y. (2018) · Advances in Interventional Cardiology · doi:10.5114/aic.2018.79868 · Cited by 6 · see citing works
Nygaard, G., Herfindal, L., Kopperud, R., Aragay, A. M., Holmsen, H., Døskeland, S. O., Kleppe, R., & Selheim, F. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.05.032 · Cited by 6 · see citing works
Liu, Y., Zhao, Z., Huang, X., Xiao, Y., Li, N., Yang, W., Feng, R., Feng, W., Long, T., Wu, H., et al. (2025) · Journal of Thrombosis and Haemostasis · doi:10.1016/j.jtha.2025.02.027 · Cited by 4 · see citing works
Potential and limitations of PKA/ PKG inhibitors for platelet studies
Shpakova, V., Rukoyatkina, N., Walter, U., & Gambaryan, S. P. (2021) · Platelets · doi:10.1080/09537104.2021.2003316 · Cited by 4 · see citing works
Self-citationNO/cGMP and ROS Pathways in Regulation of Platelet Function and Megakaryocyte Maturation
Begonja, A. J. (2007) · Online Publication Service of Würzburg University (Würzburg University) · Cited by 4 · see citing works
Self-citationCyclic Nucleotide Specificity and Cross-Activation of Cyclic Nucleotide Receptors
Shabb, J. B. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374145-5.00190-x · Cited by 3 · see citing works
Dervaux, T., Porro, C., Kunzelmann, C., Freyssinet, J., & Martínez, M. C. (2006) · Biochimie · doi:10.1016/j.biochi.2006.04.003 · Cited by 3 · see citing works
NADPH oxidase 2 inhibitor GSK2795039 exerts antiplatelet and antithrombotic activity
Oh, E. B., Kong, Y. J., Kim, T. I., Jang, J., Yu, H., Park, J. W., Kim, S., Kim, T., Sohn, J., & Chang, T.-S. (2025) · Scientific Reports · doi:10.1038/s41598-025-20250-z · Cited by 2 · see citing works
Fock, E. M., Пронин, Н. А., Rukoyatkina, N., Whaley, A., Gambaryan, S. P., & Whaley, A. O. (2024) · Natural Product Research · doi:10.1080/14786419.2024.2334882 · Cited by 2 · see citing works
Self-citationLighting up kinase action in platelets
Smolenski, A. (2017) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.13725 · Cited by 2 · see citing works
Specific PKG inhibitors: do they really exist?
Gambaryan, S. P., Butt, E., Geiger, J., Lohmann, S. M., & Walter, U. (2011) · BMC Pharmacology · doi:10.1186/1471-2210-11-s1-p27 · Cited by 1 · see citing works
Self-citationResponse: yes, cGMP plays a stimulatory role in platelet activation
Li, Z., & Du, X. (2012) · Blood · doi:10.1182/blood-2012-02-410035 · Cited by 1 · see citing works
Peri-operative Decreased cAMP Levels in Long-term Alcoholic Patients
Schoenfeld, H., Franke, R., von Heymann, C., Döpfmer, U., Blaicher, A. M., Ziemer, S., & Spies, C. (2006) · Journal of International Medical Research · doi:10.1177/147323000603400501 · Cited by 1 · see citing works
cGMP and PKG Signaling in Platelets
Gambaryan, S. P., & Walter, U. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374145-5.00192-3 · Cited by 1 · see citing works
Self-citationRegulation von Plättchenfunktion durch Epac-Proteine
Börgermann, C., Schenck, M., Jakobs, K. H., Schmidt, M., Rubben, H., & Dorp, F. V. (2007) · Der Urologe · doi:10.1007/s00120-007-1427-1
Functional role of cGMP-dependent VASP phosphorylation in vascular cells
Walter, U. (2005) · BMC Pharmacology · doi:10.1186/1471-2210-5-s1-s24
Self-citation
- Authors
- Gambaryan, S., Geiger, J., Schwarz, U. R., Butt, E., Begonja, A., Obergfell, A., & Walter, U.
- Affiliations
- University of Würzburg (DE)
- From the Institute of Clinical Biochemistry and Pathobiochemistry, University of Wuerzburg, Germany.
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2004-04-01
- Volume
- 103
- Issue
- 7
- Pages
- 2593-2600
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W2095417890
- Cited by
- 107
- References
- 27
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 1 · 2022: 3 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 8 · 2017: 5 · 2016: 3 · 2015: 2 · 2014: 3 · 2013: 6 · 2012: 5
- FWCI
- 4.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Hematology › Platelet Disorders and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Health Sciences › Medicine › Hematology › Blood Coagulation and Thrombosis Mechanisms
- Keywords
- platelet activation, cGMP-dependent protein kinase, ERK1/2 phosphorylation, thrombin, thromboxane, von Willebrand factor, platelet aggregation inhibition, intracellular signaling, hemostasis, thrombosis
- MeSH terms
- Blood Platelets, Calcium, Cyclic GMP, Humans, Kinetics, Platelet Aggregation, Platelet Aggregation Inhibitors, von Willebrand Factor, 8-Bromo Cyclic Adenosine Monophosphate, Cyclic GMP-Dependent Protein Kinases, Nitric Oxide Donors, S-Nitroso-N-Acetylpenicillamine
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