Partially defective store operated calcium entry and hem(ITAM) signaling in platelets of serotonin transporter deficient mice

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Wolf, Karen ^a   Braun, Attila ^a   Haining, Elizabeth J ^a   Tseng, Yu Lun ^c   Kraft, Peter ^a   Schuhmann, Michael K ^a   Gotru, Sanjeev K ^a   Chen, Wenchun ^a   Hermanns, Heike M ^a   Stoll, Guido ^a   Lesch, Klaus Peter ^a   Nieswandt, Bernhard ^a,b  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c TAIPEI TZU CHI HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2B BETA3 INTEGRIN; C TYPE LECTIN LIKE RECEPTOR 2; CALCIUM CHANNEL; COLLAGEN; FIBRINOGEN; INTEGRIN; LECTIN RECEPTOR; MELATONIN; PADGEM PROTEIN; SEROTONIN; SEROTONIN 2A RECEPTOR; SEROTONIN TRANSPORTER; STORE OPERATED CALCIUM CHANNEL; UNCLASSIFIED DRUG; 5 HYDROXYINDOLEACETIC ACID; CALCIUM; MYO-INOSITOL-1 (OR 4)-MONOPHOSPHATASE; PHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING TIME; BLOOD CLOTTING DISORDER; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL SPREADING; CONTROLLED STUDY; DEGRANULATION; EX VIVO STUDY; IN VIVO STUDY; MOUSE; NEUROPATHOLOGY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SEROTONIN BLOOD LEVEL; SEROTONIN RELEASE; SEROTONIN UPTAKE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; ANIMAL; BLOOD; CEREBROVASCULAR ACCIDENT; DEFICIENCY; DISEASE MODEL; HEMOSTASIS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOSIS; URINE;

ANIMALS; BLOOD PLATELETS; CALCIUM; DISEASE MODELS, ANIMAL; FIBRINOGEN; HEMOSTASIS; HYDROXYINDOLEACETIC ACID; MELATONIN; MICE; MICE, KNOCKOUT; PHOSPHORIC MONOESTER HYDROLASES; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SIGNAL TRANSDUCTION; STROKE; THROMBOSIS;

EID: 84958078162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0147664     Document Type: Article

References (69)

1. Walther DJ, Bader M. A unique central tryptophan hydroxylase isoform. Biochemical pharmacology. 2003;66(9):1673-80. Epub 2003/10/18. PMID: 14563478.
2. Bischoff SC, Mailer R, Pabst O, Weier G, Sedlik W, Li Z, et al. Role of serotonin in intestinal inflammation: knockout of serotonin reuptake transporter exacerbates 2, 4, 6-trinitrobenzene sulfonic acid colitis in mice. American journal of physiology Gastrointestinal and liver physiology. 2009;296(3):G685-95. Epub 2008/12/20. doi: 10.1152/ajpgi.90685.2008 PMID: 19095763.
3. Ghia JE, Li N, Wang H, Collins M, Deng Y, El-Sharkawy RT, et al. Serotonin has a key role in pathogenesis of experimental colitis. Gastroenterology. 2009;137(5):1649-60. Epub 2009/08/27. doi: 10.1053/j. gastro.2009.08.041 PMID: 19706294.
4. Ahern GP. 5-HT and the immune system. Current opinion in pharmacology. 2011;11(1):29-33. Epub 2011/03/12. doi: 10.1016/j.coph.2011.02.004 PMID: 21393060; PubMed Central PMCID: PMC3144148.
5. Cloez-Tayarani I, Changeux JP. Nicotine and serotonin in immune regulation and inflammatory processes: a perspective. Journal of leukocyte biology. 2007;81(3):599-606. Epub 2006/11/17. doi: 10. 1189/jlb.0906544 PMID: 17108054.
6. Duerschmied D, Suidan GL, Demers M, Herr N, Carbo C, Brill A, et al. Platelet serotonin promotes the recruitment of neutrophils to sites of acute inflammation in mice. Blood. 2013;121(6):1008-15. Epub 2012/12/18. doi: 10.1182/blood-2012-06-437392 PMID: 23243271; PubMed Central PMCID: PMC3567335.
7. Gobin V, Van Steendam K, Denys D, Deforce D. Selective serotonin reuptake inhibitors as a novel class of immunosuppressants. International immunopharmacology. 2014;20(1):148-56. Epub 2014/03/13. doi: 10.1016/j.intimp. 2014.02.030 PMID: 24613205.
8. Zucker MB, Borrelli J. A Survey of Some Platelet Enzymes and Functions-the Platelets as the Source of Normal Serum Acid Glycerophosphatase. Annals of the New York Academy of Sciences. 1958;75(1):203-13. doi: 10.1111/j.1749-6632.1958.tb36867.x PMID: ISI:A1958WQ46400024.
9. Born GV, Gillson RE. Studies on the uptake of 5-hydroxytryptamine by blood platelets. The Journal of physiology. 1959;146(3):472-91. Epub 1959/06/11. PMID: 13665673; PubMed Central PMCID: PMC1357045.
10. Tranzer JP, Da Prada M, Pletscher A. Ultrastructural localization of 5-hydroxytryptamine in blood platelets. Nature. 1966;212(5070):1574-5. Epub 1966/12/31. PMID: 21105508.
11. Zucker MB, Borrelli J. Relationship of some blood clotting factors to serotonin release from washed platelets. Journal of applied physiology. 1955;7(4):432-42. Epub 1955/01/01. PMID: 13233135.
12. Varga-Szabo D, Braun A, Nieswandt B. Calcium signaling in platelets. J Thromb Haemost. 2009;7(7):1057-66. Epub 2009/05/09. doi: 10.1111/j.1538-7836.2009.03455.x PMID: 19422456.
13. Baumgartner HR, Born GV. Effects of 5-hydroxytryptamine on platelet aggregation. Nature. 1968;218(5137):137-41. Epub 1968/04/13. PMID: 5645287.
14. Blakely RD, Berson HE, Fremeau RT Jr., Caron MG, Peek MM, Prince HK, et al. Cloning and expression of a functional serotonin transporter from rat brain. Nature. 1991;354(6348):66-70. Epub 1991/11/17. doi: 10.1038/354066a0 PMID: 1944572.
15. Lesch KP, Balling U, Gross J, Strauss K, Wolozin BL, Murphy DL, et al. Organization of the human serotonin transporter gene. Journal of neural transmission General section. 1994;95(2):157-62. Epub 1994/01/01. PMID: 7865169.
16. Zarpellon A, Donella-Deana A, Folda A, Turetta L, Pavanetto M, Deana R. Serotonin (5-HT) transport in human platelets is modulated by Src-catalysed Tyr-phosphorylation of the plasma membrane transporter SERT. Cellular Physiology and Biochemistry. 2008;21(1-3):87-94. doi: 10.1159/000113750 PMID: ISI:000252589900009.
17. Pavanetto M, Zarpellon A, Borgo C, Donella-Deana A, Deana R. Regulation of Serotonin Transport in Human Platelets by Tyrosine Kinase Syk. Cellular Physiology and Biochemistry. 2011;27(2):139-48. PMID: ISI:000288585100004. doi: 10.1159/000325216
18. Tseng YL, Chiang ML, Huang TF, Su KP, Lane HY, Lai YC. A selective serotonin reuptake inhibitor, citalopram, inhibits collagen-induced platelet aggregation and activation. Thromb Res. 2010;126(6):517-23. Epub 2010/10/22. doi: 10.1016/j.thromres.2010.09.017 PMID: 20961601.
19. Hyttel J. Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). International clinical psychopharmacology. 1994;9 Suppl 1:19-26. Epub 1994/03/01. PMID: 8021435.
20. Tuomisto J, Tukiainen E. Decreased uptake of 5-hydroxytryptamine in blood platelets from depressed patients. Nature. 1976;262(5569):596-8. Epub 1976/08/12. PMID: 958421.
21. Sauer WH, Berlin JA, Kimmel SE. Selective serotonin reuptake inhibitors and myocardial infarction. Circulation. 2001;104(16):1894-8. Epub 2001/10/17. PMID: 11602490.
22. Serebruany VL. Selective serotonin reuptake inhibitors and increased bleeding risk: are we missing something? The American journal of medicine. 2006;119(2):113-6. Epub 2006/01/31. doi: 10.1016/j. amjmed.2005.03.044 PMID: 16443409.
23. Meijer WE, Heerdink ER, Nolen WA, Herings RM, Leufkens HG, Egberts AC. Association of risk of abnormal bleeding with degree of serotonin reuptake inhibition by antidepressants. Archives of internal medicine. 2004;164(21):2367-70. Epub 2004/11/24. doi: 10.1001/archinte.164.21.2367 PMID: 15557417.
24. Eddahibi S, Hanoun N, Lanfumey L, Lesch KP, Raffestin B, Hamon M, et al. Attenuated hypoxic pulmonary hypertension in mice lacking the 5-hydroxytryptamine transporter gene. The Journal of clinical investigation. 2000;105(11):1555-62. Epub 2000/06/07. doi: 10.1172/JCI8678 PMID: 10841514; PubMed Central PMCID: PMC300850.
25. Mercado CP, Quintero MV, Li Y, Singh P, Byrd AK, Talabnin K, et al. A serotonin-induced N-glycan switch regulates platelet aggregation. Scientific reports. 2013;3:2795. Epub 2013/10/01. doi: 10.1038/srep02795 PMID: 24077408; PubMed Central PMCID: PMC3786303.
26. Ziu E, Mercado CP, Li Y, Singh P, Ahmed BA, Freyaldenhoven S, et al. Down-regulation of the serotonin transporter in hyperreactive platelets counteracts the pro-thrombotic effect of serotonin. Journal of molecular and cellular cardiology. 2012;52(5):1112-21. Epub 2012/03/01. doi: 10.1016/j.yjmcc.2012. 02.004 PMID: 22366712; PubMed Central PMCID: PMC3327821.
27. Golino P, Piscione F, Willerson JT, Cappelli-Bigazzi M, Focaccio A, Villari B, et al. Divergent effects of serotonin on coronary-artery dimensions and blood flow in patients with coronary atherosclerosis and control patients. The New England journal of medicine. 1991;324(10):641-8. Epub 1991/03/07. doi: 10.1056/NEJM199103073241001 PMID: 1994246.
28. Golino P, Ashton JH, Buja LM, Rosolowsky M, Taylor AL, McNatt J, et al. Local platelet activation causes vasoconstriction of large epicardial canine coronary arteries in vivo. Thromboxane A2 and serotonin are possible mediators. Circulation. 1989;79(1):154-66. Epub 1989/01/01. PMID: 2910540.
29. Selim MH, Molina CA. Poststroke Treatment With Selective Serotonin Reuptake Inhibitors A Journey From Sadness to Motor Recovery. Stroke. 2012;43(11):3154-5. doi: 10.1161/Strokeaha.112.657635 PMID: ISI:000310432800320.
30. McCann SK, Irvine C, Mead GE, Sena ES, Currie GL, Egan KE, et al. Efficacy of Antidepressants in Animal Models of Ischemic Stroke A Systematic Review and Meta-Analysis. Stroke. 2014;45(10):3055-63. doi: 10.1161/Strokeaha.114.006304 PMID: ISI:000342794700044.
31. Persico AM, Baldi A, Dell'Acqua ML, Moessner R, Murphy DL, Lesch KP, et al. Reduced programmed cell death in brains of serotonin transporter knockout mice. Neuroreport. 2003;14(3):341-4. doi: 10. 1097/01.wnr.0000058244.21747.83 PMID: ISI:000181641800009.
32. Lesch KP, Gutknecht L. Pharmacogenetics of the serotonin transporter. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29(6):1062-73. Epub 2005/06/14. doi: 10.1016/j.pnpbp. 2005.03.012 PMID: 15951088.
33. Murphy DL, Lerner A, Rudnick G, Lesch KP. Serotonin transporter: gene, genetic disorders, and pharmacogenetics. Mol Interv. 2004;4(2):109-23. Epub 2004/04/17. doi: 10.1124/mi.4.2.8 PMID: 15087484.
34. Murphy DL, Lesch KP. Targeting the murine serotonin transporter: insights into human neurobiology. Nat Rev Neurosci. 2008;9(2):85-96. Epub 2008/01/23. doi: 10.1038/nrn2284 PMID: 18209729.
35. Knight CG, Morton LF, Onley DJ, Peachey AR, Ichinohe T, Okuma M, et al. Collagen-platelet interaction: Gly-Pro-Hyp is uniquely specific for platelet Gp VI and mediates platelet activation by collagen. Cardiovasc Res. 1999;41(2):450-7. Epub 1999/05/26. PMID: 10341844.
36. Stegner D, Deppermann C, Kraft P, Morowski M, Kleinschnitz C, Stoll G, et al. Munc13-4-mediated secretion is essential for infarct progression but not intracranial hemostasis in acute stroke. Journal of thrombosis and haemostasis: JTH. 2013;11(7):1430-3. Epub 2013/05/11. doi: 10.1111/jth.12293 PMID: 23659589.
37. Bengel D, Murphy DL, Andrews AM, Wichems CH, Feltner D, Heils A, et al. Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ("Ecstasy") in serotonin transporter-deficient mice. Molecular pharmacology. 1998;53(4):649-55. Epub 1998/05/09. PMID: 9547354.
38. Deppermann C, Cherpokova D, Nurden P, Schulz JN, Thielmann I, Kraft P, et al. Gray platelet syndrome and defective thrombo-inflammation in Nbeal2-deficient mice. The Journal of clinical investigation. 2013. Epub 2013/07/19. doi: 10.1172/JCI69210 PMID: 23863626; PubMed Central PMCID: PMC4011026.
39. Schuhmann MK, Kraft P, Stoll G, Lorenz K, Meuth SG, Wiendl H, et al. CD28 superagonist-mediated boost of regulatory T cells increases thrombo-inflammation and ischemic neurodegeneration during the acute phase of experimental stroke. Journal of Cerebral Blood Flow and Metabolism. 2015;35(1):6-10. doi: 10.1038/jcbfm.2014.175 PMID: ISI:000347392200002.
40. Kraft P, Gob E, Schuhmann MK, Gobel K, Deppermann C, Thielmann I, et al. FTY720 Ameliorates Acute Ischemic Stroke in Mice by Reducing Thrombo-Inflammation but Not by Direct Neuroprotection. Stroke. 2013;44(11):3202-10. doi: 10.1161/Strokeaha.113.002880 PMID: ISI:000325987300054.
41. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke. 1986;17(3):472-6. Epub 1986/05/01. PMID: 3715945.
42. Moran PM, Higgins LS, Cordell B, Moser PC. Age-Related Learning-Deficits in Transgenic Mice Expressing the 751-Amino Acid Isoform of Human Beta-Amyloid Precursor Protein. Proceedings of the National Academy of Sciences of the United States of America. 1995;92(12):5341-5. doi: 10.1073/pnas.92.12.5341 PMID: ISI:A1995RB80400018.
43. Kristensen AS, Andersen J, Jørgensen TN, Sørensen L, Eriksen J, Loland CJ, et al. SLC6 Neurotransmitter Transporters: Structure, Function, and Regulation. Pharmacological Reviews. 2011;63(3):585-640. doi: 10.1124/pr.108.000869 PMID: 21752877
44. Qi R, Ozaki Y, Satoh K, Kurota K, Asazuma N, Yatomi Y, et al. Quantitative measurement of various 5-HT receptor antagonists on platelet activation induced by serotonin. Thromb Res. 1996;81(1):43-54. Epub 1996/01/01. PMID: 8747519.
45. Carneiro AM, Cook EH, Murphy DL, Blakely RD. Interactions between integrin alphaIIbbeta3 and the serotonin transporter regulate serotonin transport and platelet aggregation in mice and humans. J Clin Invest. 2008;118(4):1544-52. doi: 10.1172/JCI33374 PMID: 18317590; PubMed Central PMCID: PMC2260909.
46. Braun A, Vogtle T, Varga-Szabo D, Nieswandt B. STIM and Orai in hemostasis and thrombosis. Front Biosci (Landmark Ed). 2011;16:2144-60. PMID: 21622167.
47. Dale GL, Friese P, Batar P, Hamilton SF, Reed GL, Jackson KW, et al. Stimulated platelets use serotonin to enhance their retention of procoagulant proteins on the cell surface. Nature. 2002;415(6868):175-9. Epub 2002/01/24. doi: 10.1038/415175a PMID: 11805836.
48. Dale GL. Coated-platelets: an emerging component of the procoagulant response. J Thromb Haemost. 2005;3(10):2185-92. Epub 2005/10/01. doi: 10.1111/j.1538-7836.2005.01274.x PMID: 16194197.
49. Alberio LJ, Clemetson KJ. All platelets are not equal: COAT platelets. Curr Hematol Rep. 2004;3(5):338-43. Epub 2004/09/03. PMID: 15341700.
50. Mazepa M, Hoffman M, Monroe D. Superactivated platelets: thrombus regulators, thrombin generators, and potential clinical targets. Arterioscler Thromb Vasc Biol. 2013;33(8):1747-52. Epub 2013/07/19. doi: 10.1161/atvbaha.113.301790 PMID: 23864724.
51. Szasz R, Dale GL. COAT platelets. Curr Opin Hematol. 2003;10(5):351-5. Epub 2003/08/13. PMID: 12913789.
52. Espinera AR, Ogle ME, Gu X, Wei L. Citalopram enhances neurovascular regeneration and sensorimotor functional recovery after ischemic stroke in mice. Neuroscience. 2013;247:1-11. Epub 2013/04/18. doi: 10.1016/j.neuroscience.2013.04.011 PMID: 23590907; PubMed Central PMCID: PMCPmc3916088.
53. McFarlane A, Kamath MV, Fallen EL, Malcolm V, Cherian F, Norman G. Effect of sertraline on the recovery rate of cardiac autonomic function in depressed patients after acute myocardial infarction. American heart journal. 2001;142(4):617-23. Epub 2001/10/02. doi: 10.1067/mhj.2001.116766 PMID: 11579351.
54. Mead GE, Hsieh CF, Lee R, Kutlubaev MA, Claxton A, Hankey GJ, et al. Selective serotonin reuptake inhibitors (SSRIs) for stroke recovery. Cochrane Database Syst Rev. 2012;11:Cd009286. Epub 2012/11/16. doi: 10.1002/14651858. CD009286.pub2 PMID: 23152272.
55. Frankhauser P, Grimmer Y, Bugert P, Deuschle M, Schmidt M, Schloss P. Characterization of the neuronal dopamine transporter DAT in human blood platelets. Neurosci Lett. 2006;399(3):197-201. Epub 2006/02/24. doi: 10.1016/j.neulet.2006.01.062 PMID: 16490314.
56. Nishio H, Nezasa K, Nakata Y. Role of calcium ion in platelet serotonin uptake regulation. Eur J Pharmacol. 1995;288(2):149-55. PMID: 7720776.
57. Turetta L, Bazzan E, Bertagno K, Musacchio E, Deana R. Role of Ca (2+) and protein kinase C in the serotonin (5-HT) transport in human platelets. Cell calcium. 2002;31(5):235-44. Epub 2002/07/06. doi: 10.1016/s0143-4160 (02) 00052-0 PMID: 12098226.
58. Watts SW. Serotonin-induced contraction in mesenteric resistance arteries: signaling and changes in deoxycorticosterone acetate-salt hypertension. Hypertension. 2002;39(3):825-9. PMID: 11897772.
59. Watts SW, Morrison SF, Davis RP, Barman SM. Serotonin and blood pressure regulation. Pharmacol Rev. 2012;64(2):359-88. Epub 2012/03/13. doi: 10.1124/pr.111.004697 PMID: 22407614; PubMed Central PMCID: PMCPmc3310484.
60. Canan F, Ataoglu A. The effect of escitalopram on platelet activity. Thromb Res. 2011;127(1):57. Epub 2010/08/17. doi: 10.1016/j.thromres.2010.07.017 PMID: 20709365.
61. Hallback I, Hagg S, Eriksson AC, Whiss PA. In vitro effects of serotonin and noradrenaline reuptake inhibitors on human platelet adhesion and coagulation. Pharmacol Rep. 2012;64(4):979-83. Epub 2012/10/23. PMID: 23087151.
62. Schmitt A, Benninghoff J, Moessner R, Rizzi M, Paizanis E, Doenitz C, et al. Adult neurogenesis in serotonin transporter deficient mice. Journal of neural transmission. 2007;114(9):1107-19. Epub 2007/05/19. doi: 10.1007/s00702-007-0724-6 PMID: 17510734.
63. Wester P, Dietrich WD, Prado R, Watson BD, Globus MY. Serotonin release into plasma during common carotid artery thrombosis in rats. Stroke. 1992;23(6):870-5. Epub 1992/06/01. PMID: 1595108.
64. Walther DJ, Peter JU, Winter S, Holtje M, Paulmann N, Grohmann M, et al. Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release. Cell. 2003;115(7):851-62. Epub 2003/12/31. PMID: 14697203.
65. Asada M, Ebihara S, Yamanda S, Niu K, Okazaki T, Sora I, et al. Depletion of serotonin and selective inhibition of 2B receptor suppressed tumor angiogenesis by inhibiting endothelial nitric oxide synthase and extracellular signal-regulated kinase 1/2 phosphorylation. Neoplasia. 2009;11(4):408-17. Epub 2009/03/25. PMID: 19308295; PubMed Central PMCID: PMCPmc2657884.
66. Anglin R, Yuan Y, Moayyedi P, Tse F, Armstrong D, Leontiadis GI. Risk of upper gastrointestinal bleeding with selective serotonin reuptake inhibitors with or without concurrent nonsteroidal anti-inflammatory use: a systematic review and meta-analysis. Am J Gastroenterol. 2014;109(6):811-9. doi: 10. 1038/ajg.2014.82 PMID: 24777151.
67. Hankey GJ. Selective serotonin reuptake inhibitors and risk of cerebral bleeding. Stroke. 2014;45(7):1917-8. doi: 10.1161/STROKEAHA.114.005844 PMID: 24876088.
68. Jiang HY, Chen HZ, Hu XJ, Yu ZH, Yang W, Deng M, et al. Use of selective serotonin reuptake inhibitors and risk of upper gastrointestinal bleeding: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2015;13(1):42-50 e3. doi: 10.1016/j.cgh.2014.06.021 PMID: 24993365.
69. Sander K. SD. Depression and psychological distress as risk factors for stroke and worse stroke recovery: clinical implications and therapeutic options. EMJ Neurol. 2014;1:53-8.