Loss of serotonin transporter function alters ADP-mediated glycoprotein αIIbβ3 Activation through dysregulation of the receptor

Journal of Biological Chemistry

Volumn 291, Issue 38, 2016, Pages 20210-20219

  Oliver, Kendra H ^a   Duvernay, Matthew T ^a   Hamm, Heidi E ^a   Carneiro, Ana M D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; MAMMALS; PLATELETS;

5-HYDROXYTRYPTAMINE (5-HT); PLATELET ACTIVATION; PLATELET AGGREGATION; RECEPTOR SURFACE; SELECTIVE SEROTONIN RE-UPTAKE INHIBITORS; SEROTONIN TRANSPORTERS; SURFACE EXPRESSION; SYNERGISTIC ACTIVATION;

CHEMICAL ACTIVATION;

ADENOSINE DIPHOSPHATE; CITALOPRAM; GLYCOPROTEIN; KETANSERIN; PADGEM PROTEIN; PROTEIN ALPHAIIBBETA3; SEROTONIN; SEROTONIN 2A ANTAGONIST; SEROTONIN 2A RECEPTOR; SEROTONIN TRANSPORTER; SEROTONIN UPTAKE INHIBITOR; SULFUR 35; TRITIUM; UNCLASSIFIED DRUG; FIBRINOGEN RECEPTOR; SLC6A4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLEEDING TIME; CONTROLLED STUDY; HEMOSTASIS; IN VIVO STUDY; ISOTOPE LABELING; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTONIN BLOOD LEVEL; SEROTONINERGIC TRANSMISSION; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOCYTE TRANSFUSION; WILD TYPE; ANIMAL; DEFICIENCY; FEMALE; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; THROMBOCYTE;

ADENOSINE DIPHOSPHATE; ANIMALS; BLOOD PLATELETS; CITALOPRAM; FEMALE; MALE; MICE; MICE, KNOCKOUT; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84987837352     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.736983     Document Type: Article

References (48)

1. Brenner, B., Harney, J. T., Ahmed, B. A., Jeffus, B. C., Unal, R., Mehta, J. L., and Kilic, F. (2007) Plasma serotonin levels and the platelet serotonin transporter. J. Neurochem. 102, 206-215
2. Matondo, R. B., Punt, C., Homberg, J., Toussaint, M. J., Kisjes, R., Korporaal, S. J., Akkerman, J. W., Cuppen, E., and de Bruin, A. (2009) Deletion of the serotonin transporter in rats disturbs serotonin homeostasis without impairing liver regeneration. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G963-G968
3. Beikmann, B. S., Tomlinson, I. D., Rosenthal, S. J., and Andrews, A. M. (2013) Serotonin uptake is largely mediated by platelets versus lymphocytes in peripheral blood cells. ACS Chem. Neurosci. 4, 161-170
4. Bismuth-Evenzal, Y., Gonopolsky, Y., Gurwitz, D., Iancu, I., Weizman, A., and Rehavi, M. (2012) Decreased serotonin content and reduced agonistinduced aggregation in platelets of patients chronically medicated with SSRI drugs. J. Affect. Disord. 136, 99-103
5. Carneiro, A. M., Cook, E. H., Murphy, D. L., and Blakely, R. D. (2008) Interactions between integrin αIIbβ3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans. J. Clin. Investig. 118, 1544-1552
6. Abdelmalik, N., Ruhé, H. G., Barwari, K., van den Dool, E.-J., Meijers, J. C., Middeldorp, S., Büller, H. R., Schene, A. H., and Kamphuisen, P. W. (2008) Effect of the selective serotonin reuptake inhibitor paroxetine on platelet function is modified by a SLC6A4 serotonin transporter polymorphism. J. Thromb. Haemost. 6, 2168-74
7. Namkung, J., Kim, H., and Park, S. (2015) Peripheral serotonin: a new player in systemic energy homeostasis. Mol. Cells 38, 1023-1028
8. Hranilovic, D., Blazevic, S., Ivica, N., Cicin-Sain, L., and Oreskovic, D. (2011) The effects of the perinatal treatment with 5-hydroxytryptophan or tranylcypromine on the peripheral and central serotonin homeostasis in adult rats. Neurochem. Int. 59, 202-207
9. Blazevic, S., Erjavec, I., Brizic, M., Vukicevic, S., and Hranilovic, D. (2015) Molecular background and physiological consequences of altered peripheral serotonin homeostasis in adult rats perinatally treated with tranylcypromine. J. Physiol. Pharmacol. 66, 529-537
10. Amireault, P., Sibon, D., and Côté, F. (2013) Life without peripheral serotonin: insights from tryptophan hydroxylase 1 knockout mice reveal the existence of paracrine/autocrine serotonergic networks. ACS Chem. Neurosci. 4, 64-71
11. Tseng, Y.-L., Chiang, M.-L., Huang, T.-F., Su, K.-P., Lane, H.-Y., and Lai, Y.-C. (2010) A selective serotonin reuptake inhibitor, citalopram, inhibits collagen-induced platelet aggregation and activation. Thromb. Res. 126, 517-523
12. Cerrito, F., Lazzaro, M. P., Gaudio, E., Arminio, P., and Aloisi, G. (1993) 5HT2-receptors and serotonin release: their role in human platelet aggregation. Life Sci. 53, 209-215
13. Thompson, N. T., Scrutton, M. C., and Wallis, R. B. (1986) Synergistic responses in human platelets. Comparison between aggregation, secretion and cytosolic Ca 2+concentration. Eur. J. Biochem. 161, 399-408
14. Mercado, C. P., Quintero, M. V., Li, Y., Singh, P., Byrd, A. K., Talabnin, K., Ishihara, M., Azadi, P., Rusch, N. J., Kuberan, B., Maroteaux, L., and Kilic, F. (2013) A serotonin-induced N-glycan switch regulates platelet aggregation. Sci. Rep. 3, 2795
15. Lin, O. A., Karim, Z. A., Vemana, H. P., Espinosa, E. V., and Khasawneh, F. T. (2014) The antidepressant 5-HT2A receptor antagonists pizotifen and cyproheptadine inhibit serotonin-enhanced platelet function. PLoS One 9, e87026
16. Adams, J. W., Ramirez, J., Shi, Y., Thomsen, W., Frazer, J., Morgan, M., Edwards, J. E., Chen, W., Teegarden, B. R., Xiong, Y., Al-Shamma, H., Behan, D. P., and Connolly, D. T. (2009) APD791, 3-methoxy-N-(3-(1-methyl-1H-pyrazol-5-yl)-4-(2-morpholinoethoxy)phenyl)benzamide, a novel 5-hydroxytryptamine 2A receptor antagonist: pharmacological profile, pharmacokinetics, platelet activity and vascular biology. J. Pharmacol. Exp. Ther. 331, 96-103
17. Przyklenk, K., Frelinger, A. L., 3rd, Linden, M. D., Whittaker, P., Li, Y., Barnard, M. R., Adams, J., Morgan, M., Al-Shamma, H., and Michelson, A. D. (2010) Targeted inhibition of the serotonin 5HT2A receptor im-proves coronary patency in an in vivo model of recurrent thrombosis. J. Thromb. Haemost. 8, 331-340
18. Li, N., Wallén, N. H., Ladjevardi, M., and Hjemdahl, P. (1997) Effects of serotonin on platelet activation in whole blood. Blood Coagul. Fibrinolysis 8, 517-523
19. Jirouskova, M., Shet, A. S., and Johnson, G. J. (2007) A guide to murine platelet structure, function, assays, and genetic alterations. J. Thromb. Haemost. 5, 661- 669
20. Walther, D. J., Peter, J.-U., Winter, S., Höltje, M., Paulmann, N., Grohmann, M., Vowinckel, J., Alamo-Bethencourt, V., Wilhelm, C. S., Ahnert-Hilger, G., and Bader, M. (2003) Serotonylation of small GTPases is a signal transduction pathway that triggers platelet ô-granule release. Cell 115, 851- 862
21. Hummerich, R., and Schloss, P. (2010) Serotonin-more than a neurotransmitter: transglutaminase-mediated serotonylation of C6 glioma cells and fibronectin. Neurochem. Int. 57, 67-75
22. Malyszko, J., Urano, T., Knofler, R., Taminato, A., Yoshimi, T., Takada, Y., and Takada, A. (1994) Daily variations of platelet aggregation in relation to blood and plasma serotonin in diabetes. Thromb. Res. 75, 569-576
23. Andrade, C., Sandarsh, S., Chethan, K. B., and Nagesh, K. S. (2010) Serotonin reuptake inhibitor antidepressants and abnormal bleeding: a review for clinicians and a reconsideration of mechanisms. J. Clin. Psychiatry 71, 1565-1575
24. Maurice, T., and Su, T.-P. (2009) The pharmacology of δ-1 receptors. Pharmacol. Ther. 124, 195-206
25. Ahmed, B. A., Jeffus, B. C., Bukhari, S. I., Harney, J. T., Unal, R., Lupashin, V. V., van der Sluijs, P., and Kilic, F. (2008) Serotonin transamidates Rab4 and facilitates its binding to the C terminus of serotonin transporter. J. Biol. Chem. 283, 9388-9398
26. Gartside, S. E., Umbers, V., Hajós, M., and Sharp, T. (1995) Interaction between a selective 5-HT1A receptor antagonist and an SSRI in vivo: effects on 5-HT cell firing and extracellular 5-HT. Br. J. Pharmacol. 115, 1064-1070
27. Artigas, F., Romero, L., de Montigny, C., and Blier, P. (1996) Acceleration of the effect of selected antidepressant drugs in major depression by 5-HT1A antagonists. Trends Neurosci. 19, 378-383
28. Schmid, C. L., Raehal, K. M., and Bohn, L. M. (2008) Agonist-directed signaling of the serotonin 2A receptor depends on β-arrestin-2 interactions in vivo. Proc. Natl. Acad. Sci. U.S.A. 105, 1079-1084
29. Bohn, L. M., and Schmid, C. L. (2010) Serotonin receptor signaling and regulation via β-arrestins. Crit. Rev. Biochem. Mol. Biol. 45, 555-566
30. Schaff, M., Receveur, N., Bourdon, C., Ohlmann, P., Lanza, F., Gachet, C., and Mangin, P. H. (2012) β-Arrestin-1 participates in thrombosis and regulates integrinαIIboβ3 signalling without affecting P2Y receptors desensitisation and function. Thromb. Haemost. 107, 735-748
31. Yamauchi, M., Miyara, T., Matsushima, T., and Imanishi, T. (2006) Desensitization of 5-HT2A receptor function by chronic administration of selective serotonin reuptake inhibitors. Brain Res. 1067, 164-169
32. Moore, T. C., and Eiseman, B. (1966) Serotonin metabolism in the isolated perfused canine liver. Surgery 59, 765-769
33. Anderson, G. M., Barr, C. S., Lindell, S., Durham, A. C., Shifrovich, I., and Higley, J. D. (2005) Time course of the effects of the serotoninselective reuptake inhibitor sertraline on central and peripheral serotonin neurochemistry in the rhesus monkey. Psychopharmacology 178, 339-346
34. Anderson, G. M., and Cook, E. H. (2016) Commentary on "platelet studies in autism spectrum disorder patients and first-degree relatives." Mol. Autism 7, 20
35. Lau, W. K., Chan-Yeung, M. M., Yip, B. H., Cheung, A. H., Ip, M. S., Mak, J. C., and COPD Study Group of the Hong Kong Thoracic Society (2012) The role of circulating serotonin in the development of chronic obstructive pulmonary disease. PLoS One 7, e31617
36. Jernej, B., Vladić, A., Cicin-Sain, L., Hranilović, D., Banović, M., Balija, M., Bilić, E., Sucić, Z., Vukadin, S., and Grgicević, D. (2002) Platelet serotonin measures in migraine. Headache 42, 588-595
37. Singh, P., Fletcher, T. W., Li, Y., Rusch, N. J., and Kilic, F. (2013) Serotonin uptake rates in platelets from angiotensin II-induced hypertensive mice. Health 5, 31-39
38. Walther, D. J., Peter, J. U., Bashammakh, S., Hörtnagl, H., Voits, M., Fink, H., and Bader, M. (2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299, 76-76
39. Berger, J. S., Becker, R. C., Kuhn, C., Helms, M. J., Ortel, T. L., and Williams, R. (2013) Hyperreactive platelet phenotypes: relationship to altered serotonin transporter number, transport kinetics and intrinsic response to adrenergic co-stimulation. Thromb. Haemost. 109, 85-92
40. Hirsh-Rokach, B., Spectre, G., Shai, E., Lotan, A., Ritter, A., Al-Aieshy, F., Malmström, R. E., Varon, D., and Alcalai, R. (2015) Differential impact of selective serotonin reuptake inhibitors on platelet response to clopidogrel: a randomized, double-blind, crossover trial. Pharmacotherapy 35, 140-147
41. Stahl, E. L., Zhou, L., Ehlert, F. J., and Bohn, L. M. (2015) A novel method for analyzing extremely biased agonism at G protein-coupled receptors. Mol. Pharmacol. 87, 866-877
42. Schmid, C. L., and Bohn, L. M. (2010) Serotonin, but not N-methyltryptamines, activates the serotonin 2A receptor via a β-arrestin2/Src/Akt signaling complex in vivo. J. Neurosci. 30, 13513-13524
43. Li, Z., Delaney, M. K., O'Brien, K. A., and Du, X. (2010) Signaling during platelet adhesion and activation. Arterioscler. Thromb. Vasc. Biol. 30, 2341-2349
44. Quinn, J. C., Johnson-Farley, N. N., Yoon, J., and Cowen, D. S. (2002) Activation of extracellular-regulated kinase by 5-hydroxytryptamine2A receptors in PC12 cells is protein kinase C-independent and requires calmodulin and tyrosine kinases. J. Pharmacol. Exp. Ther. 303, 746-752
45. Johnson-Farley, N. N., Kertesy, S. B., Dubyak, G. R., and Cowen, D. S. (2005) Enhanced activation of Akt and extracellular-regulated kinase pathways by simultaneous occupancy of Gq-coupled 5-HT2A receptors and Gs-coupled 5-HT7A receptors in PC12 cells. J. Neurochem. 92, 72-82
46. Göoz, M., Göoz, P., Luttrell, L. M., and Raymond, J. R. (2006) 5-HT2A receptor induces ERK phosphorylation and proliferation through ADAM-17 tumor necrosis factor-α-converting enzyme (TACE) activation and heparinbound epidermal growth factor-like growth factor (HB-EGF) shedding in mesangial cells. J. Biol. Chem. 281, 21004-21012
47. Miller, K. J., Mariano, C. L., and Cruz, W. R. (1997) Serotonin 5HT2A receptor activation inhibits inducible nitric oxide synthase activity in C6 glioma cells. Life Sci. 61, 1819-1827
48. Oliver, K. H., Jessen, T., Crawford, E. L., Chung, C. Y., Sutcliffe, J. S., and Carneiro, A. M. (2014) Pro32Pro33 mutations in the integrinβ3 PSI domain result inαIIboβ3 priming and enhanced adhesion: reversal of the hypercoagulability phenotype by the Src inhibitor SKI-606. Mol. Pharmacol. 85, 921-931