Platelet Serotonin Aggravates Myocardial Ischemia/Reperfusion Injury via Neutrophil Degranulation

Circulation

Volumn 139, Issue 7, 2019, Pages 918-931

  Mauler, Maximilian ^a   Herr, Nadine ^b   Schoenichen, Claudia ^b   Witsch, Thilo ^b   Marchini, Timoteo ^b   Härdtner, Carmen ^b   Koentges, Christoph ^b,d   Kienle, Korbinian ^a,c   Ollivier, Véronique ^e,f   Schell, Maximilian ^b   Dorner, Ludwig ^b   Wippel, Christopher ^b   Stallmann, Daniela ^b   Normann, Claus ^b   Bugger, Heiko ^b   Walther, Paul ^g   Wolf, Dennis ^b   Ahrens, Ingo ^a   Lämmermann, Tim ^c   Ho Tin Noe, Benoît ^e,f   Ley, Klaus ^h   Bode, Christoph ^b   Hilgendorf, Ingo ^a   Duerschmied, Daniel ^a   more..

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e INSERM   (France)

^f Site Xavier Bichat and Département Hospitalo Universitaire Fibrosis Inflammation and Remodeling   (France)

^g UNIVERSITY OF ULM   (Germany)

^h LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

blood platelets; inflammation; integrins; neutrophils; reactive oxygen species; reperfusion injury; serotonin

Indexed keywords

ALPHA INTEGRIN; BUPRENORPHINE; CD11B ANTIGEN; ENOXAPARIN; FLUOXETINE; HYDROGEN PEROXIDE; INTEGRIN; KETAMINE; L SELECTIN; MYELOPEROXIDASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PADGEM PROTEIN; SELECTIN (GLYCOPROTEIN); SEROTONIN; SEROTONIN RECEPTOR; SEROTONIN UPTAKE INHIBITOR; TICAGRELOR; TRYPTOPHAN HYDROXYLASE; TUMOR NECROSIS FACTOR; XYLAZINE; ITGAM PROTEIN, MOUSE; PEROXIDASE; TPH1 PROTEIN, MOUSE;

ACUTE CORONARY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING RATE; CONTROLLED STUDY; CORONARY ARTERY LIGATION; DEGRANULATION; ECHOCARDIOGRAPHY; FLOW CYTOMETRY; GENE KNOCKDOWN; HEART FUNCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE ISCHEMIA; HEART RATE; HEART VENTRICLE SIZE; HUMAN; IN VITRO STUDY; INFLAMMATORY CELL; LEUKOCYTE ACTIVATION; MAXIMAL INSPIRATORY PRESSURE; MOUSE; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; MYOCARDITIS; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXYGEN SATURATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SEROTONIN BLOOD LEVEL; THORACOTOMY; THROMBOCYTE; THROMBOCYTE AGGREGATION; ANIMAL; BLOOD; C57BL MOUSE; CARDIAC MUSCLE; CASE CONTROL STUDY; DISEASE MODEL; GENETICS; HEART INFARCTION; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ACUTE CORONARY SYNDROME; ANIMALS; BLOOD PLATELETS; CASE-CONTROL STUDIES; CD11B ANTIGEN; CELL DEGRANULATION; DISEASE MODELS, ANIMAL; HUMANS; HYDROGEN PEROXIDE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NEUTROPHILS; PEROXIDASE; SEROTONIN; TRYPTOPHAN HYDROXYLASE;

EID: 85061352431     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.118.033942     Document Type: Article

References (50)

1. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121-1135. doi: 10.1056/NEJMra071667
2. Hausenloy DJ, Yellon DM. Myocardial ischemia-reperfusion injury: a neglected therapeutic target. J Clin Invest. 2013;123:92-100. doi: 10.1172/JCI62874
3. Hausenloy DJ, Botker HE, Engstrom T, Erlinge D, Heusch G, Ibanez B, Kloner RA, Ovize M, Yellon DM, Garcia-Dorado D. Targeting reperfusion injury in patients with ST-segment elevation myocardial infarction: trials and tribulations. Eur Heart J. 2017;38:935-941. doi: 10.1093/eurheartj/ehw145
4. Heusch G, Gersh BJ. The pathophysiology of acute myocardial infarction and strategies of protection beyond reperfusion: a continual challenge. Eur Heart J. 2017;38:774-784. doi: 10.1093/eurheartj/ehw224
5. Vinten-Johansen J. Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovasc Res. 2004;61:481-497. doi: 10.1016/j.cardiores.2003.10.011
6. Horckmans M, Ring L, Duchene J, Santovito D, Schloss MJ, Drechsler M, Weber C, Soehnlein O, Steffens S. Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype. Eur Heart J. 2017;38:187-197. doi: 10.1093/eurheartj/ehw002
7. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7:678-689. doi: 10.1038/nri2156
8. Diacovo TG, Roth SJ, Buccola JM, Bainton DF, Springer TA. Neutrophil rolling, arrest, and transmigration across activated, surface-adherent platelets via sequential action of P-selectin and the beta 2-integrin CD11b/CD18. Blood. 1996;88:146-157. https://www.ncbi.nlm.nih.gov/ pubmed/8704169. Accessed January 9, 2019.
9. Zarbock A, Ley K, McEver RP, Hidalgo A. Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood. 2011;118:6743-6751. doi: 10.1182/blood-2011-07-343566
10. Kempf T, Zarbock A, Widera C, Butz S, Stadtmann A, Rossaint J, Bolomini-Vittori M, Korf-Klingebiel M, Napp LC, Hansen B, Kanwischer A, Bavendiek U, Beutel G, Hapke M, Sauer MG, Laudanna C, Hogg N, Vestweber D, Wollert KC. GDF-15 is an inhibitor of leukocyte integrin activation required for survival after myocardial infarction in mice. Nat Med. 2011;17:581-588. doi: 10.1038/nm.2354
11. Duerschmied D, Suidan GL, Demers M, Herr N, Carbo C, Brill A, Cifuni SM, Mauler M, Cicko S, Bader M, Idzko M, Bode C, Wagner DD. Platelet serotonin promotes the recruitment of neutrophils to sites of acute inflammation in mice. Blood. 2013;121:1008-1015. doi: 10.1182/blood-2012-06-437392
12. Sauer WH, Berlin JA, Kimmel SE. Effect of antidepressants and their relative affinity for the serotonin transporter on the risk of myocardial infarction. Circulation. 2003;108:32-36. doi: 10.1161/01.CIR.0000079172.43229.CD
13. Ali M, Pulli B, Courties G, Tricot B, Sebas M, Iwamoto Y, Hilgendorf I, Schob S, Dong A, Zheng W, Skoura A, Kalgukar A, Cortes C, Ruggeri R, Swirski FK, Nahrendorf M, Buckbinder L, Chen JW. Myeloperoxidase inhibition improves ventricular function and remodeling after experimental myocardial infarction. JACC Basic Transl Sci. 2016;1:633-643. doi: 10.1016/j.jacbts.2016.09.004
14. Lindsey ML, Bolli R, Canty JM Jr, Du XJ, Frangogiannis NG, Frantz S, Gourdie RG, Holmes JW, Jones SP, Kloner RA, Lefer DJ, Liao R, Murphy E, Ping P, Przyklenk K, Recchia FA, Schwartz Longacre L, Ripplinger CM, Van Eyk JE, Heusch G. Guidelines for experimental models of myocardial ischemia and infarction. Am J Physiol Heart Circ Physiol. 2018;314:H812-H838. doi: 10.1152/ajpheart.00335.2017
15. Dürk T, Panther E, Müller T, Sorichter S, Ferrari D, Pizzirani C, Di Virgilio F, Myrtek D, Norgauer J, Idzko M. 5-Hydroxytryptamine modulates cytokine and chemokine production in LPS-primed human monocytes via stimulation of different 5-HTR subtypes. Int Immunol. 2005;17:599-606. doi: 10.1093/intimm/dxh242
16. Pracharová L, Okénková K, Lojek A, Cíz M. Serotonin and its 5-HT(2) receptor agonist DOI hydrochloride inhibit the oxidative burst in total leukocytes but not in isolated neutrophils. Life Sci. 2010;86:518-523. doi: 10.1016/j.lfs.2010.02.003
17. Patocka N, Sharma N, Rashid M, Ribeiro P. Serotonin signaling in Schistosoma mansoni: a serotonin-activated G protein-coupled receptor controls parasite movement. PLoS Pathog. 2014;10:e1003878. doi: 10.1371/journal.ppat.1003878
18. Okubo M, Satoh Y, Hirakawa M, Sasaki K, Masu K, J McHonde G, Ikeda-Kurosawa C, Kurosaka D, Saino T. Different effect of serotonin on intracellular calcium ion dynamics in the smooth muscle cells between rat posterior ciliary artery and vorticose vein. Biomed Res. 2016;37:101-115. doi: 10.2220/biomedres.37.101
19. Zarbock A, Polanowska-Grabowska RK, Ley K. Platelet-neutrophil-interactions: linking hemostasis and inflammation. Blood Rev. 2007;21:99-111. doi: 10.1016/j.blre.2006.06.001
20. Gros A, Ollivier V, Ho-Tin-Noé B. Platelets in inflammation: regulation of leukocyte activities and vascular repair. Front Immunol. 2014;5:678. doi: 10.3389/fimmu.2014.00678
21. Walther DJ, Peter JU, Bashammakh S, Hörtnagl H, Voits M, Fink H, Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science. 2003;299:76. doi: 10.1126/science.1078197
22. Jolly SR, Kane WJ, Hook BG, Abrams GD, Kunkel SL, Lucchesi BR. Reduction of myocardial infarct size by neutrophil depletion: effect of duration of occlusion. Am Heart J. 1986;112:682-690.
23. Page C, Pitchford S. Neutrophil and platelet complexes and their relevance to neutrophil recruitment and activation. Int Immunopharmacol. 2013;17:1176-1184. doi: 10.1016/j.intimp.2013.06.004
24. Mauler M, Seyfert J, Haenel D, Seeba H, Guenther J, Stallmann D, Schoenichen C, Hilgendorf I, Bode C, Ahrens I, Duerschmied D. Platelet-neutrophil complex formation-A detailed in vitro analysis of murine and human blood samples. J Leukoc Biol. 2016;99:781-789. doi: 10.1189/jlb.3TA0315-082R
25. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13:159-175. doi: 10.1038/nri3399
26. Vanags DM, Rodgers SE, Duncan EM, Lloyd JV, Bochner F. Potentiation of ADP-induced aggregation in human platelet-rich plasma by 5-hydroxytryptamine and adrenaline. Br J Pharmacol. 1992;106:917-923. doi: 10.1111/j.1476-5381.1992.tb14435.x
27. Borregaard N, Cowland JB. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood. 1997;89:3503-3521. https://www.ncbi. nlm.nih.gov/pubmed/9160655. Accessed January 9, 2019.
28. Ye Y, Birnbaum GD, Perez-Polo JR, Nanhwan MK, Nylander S, Birnbaum Y. Ticagrelor protects the heart against reperfusion injury and improves remodeling after myocardial infarction. Arterioscler Thromb Vasc Biol. 2015;35:1805-1814. doi: 10.1161/ATVBAHA.115.305655
29. Cohen MV, Yang XM, White J, Yellon DM, Bell RM, Downey JM. Cangrelor-mediated cardioprotection requires platelets and sphingosine phosphorylation. Cardiovasc Drugs Ther. 2016;30:229-232. doi: 10.1007/s10557-015-6633-2
30. Berger M, Gray JA, Roth BL. The expanded biology of serotonin. Annu Rev Med. 2009;60:355-366. doi: 10.1146/annurev.med.60.042307.110802
31. Duerschmied D, Bode C. [The role of serotonin in haemostasis]. Hamostaseologie. 2009;29:356-359. doi: 10.1055/s-0037-1617140
32. Watts SW. Oh, the places you'll go! My many colored serotonin (apologies to Dr. Seuss). Am J Physiol Heart Circ Physiol. 2016;311:H1225-H1233. doi: 10.1152/ajpheart.00538.2016
33. Shimizu Y, Minatoguchi S, Hashimoto K, Uno Y, Arai M, Wang N, Chen X, Lu C, Takemura G, Shimomura M, Fujiwara T, Fujiwara H. The role of serotonin in ischemic cellular damage and the infarct size-reducing effect of sarpogrelate, a 5-hydroxytryptamine-2 receptor blocker, in rabbit hearts. J Am Coll Cardiol. 2002;40:1347-1355. doi: 10.1016/S0735-1097(02)02158-7
34. Vikenes K, Farstad M, Nordrehaug JE. Serotonin is associated with coronary artery disease and cardiac events. Circulation. 1999;100:483-489.
35. Doggrell SA. The role of 5-HT on the cardiovascular and renal systems and the clinical potential of 5-HT modulation. Expert Opin Investig Drugs. 2003;12:805-823. doi: 10.1517/13543784.12.5.805
36. Nebigil CG, Etienne N, Messaddeq N, Maroteaux L. Serotonin is a novel survival factor of cardiomyocytes: mitochondria as a target of 5-HT2B receptor signaling. FASEB J. 2003;17:1373-1375. doi: 10.1096/fj.02-1122fje
37. Muto T, Usuda H, Yamamura A, Yoshida K, Ohashi A, Mitsui-Saitoh K, Sakai J, Sugimoto Y, Mizutani H, Nonogaki T, Hotta Y. Protective effects of fluvoxamine against ischemia/reperfusion injury in isolated, perfused guinea-pig hearts. Biol Pharm Bull. 2014;37:731-739. doi: 10.1248/bpb. b13-00552
38. Simpson PJ, Schelm JA, Jakubowski JA, Smallwood JK. The role of serotonin (5HT2) receptor blockade in myocardial reperfusion injury: effects of LY53857 in a canine model of myocardial infarction. J Pharmacol Exp Ther. 1991;258:979-985.
39. Hohlfeld T, Braun M, Strobach H, Schrör K. Protection of reperfused ischemic pig myocardium by nexopamil, a new combined Ca2+ and serotonin antagonist. J Cardiovasc Pharmacol. 1994;23:922-931.
40. Yang BC, Virmani R, Nichols WW, Mehta JL. Platelets protect against myocardial dysfunction and injury induced by ischemia and reperfusion in isolated rat hearts. Circ Res. 1993;72:1181-1190.
41. Grover GJ, Sargent CA, Dzwonczyk S, Normandin DE, Antonaccio MJ. Protective effect of serotonin (5-HT2) receptor antagonists in ischemic rat hearts. J Cardiovasc Pharmacol. 1993;22:664-672.
42. Cowland JB, Borregaard N. Granulopoiesis and granules of human neutrophils. Immunol Rev. 2016;273:11-28. doi: 10.1111/imr.12440
43. Dale DC, Boxer L, Liles WC. The phagocytes: neutrophils and monocytes. Blood. 2008;112:935-945. doi: 10.1182/blood-2007-12-077917
44. Faurschou M, Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 2003;5:1317-1327. doi: 10.1016/j. micinf.2003.09.008
45. Naegelen I, Beaume N, Plançon S, Schenten V, Tschirhart EJ, Bréchard S. Regulation of neutrophil degranulation and cytokine secretion: a novel model approach based on linear fitting. J Immunol Res. 2015;2015:817038. doi: 10.1155/2015/817038
46. Lacy P. Mechanisms of degranulation in neutrophils. Allergy Asthma Clin Immunol. 2006;2:98-108. doi: 10.1186/1710-1492-2-3-98
47. Wong DT, Perry KW, Bymaster FP. Case history: the discovery of fluoxetine hydrochloride (Prozac). Nat Rev Drug Discov. 2005;4:764-774. doi: 10.1038/nrd1821
48. Arai M, Lefer DJ, So T, DiPaula A, Aversano T, Becker LC. An anti-CD18 antibody limits infarct size and preserves left ventricular function in dogs with ischemia and 48-hour reperfusion. J Am Coll Cardiol. 1996;27:1278-1285. doi: 10.1016/0735-1097(95)00578-1
49. Lang PA, Contaldo C, Georgiev P, El-Badry AM, Recher M, Kurrer M, Cervantes-Barragan L, Ludewig B, Calzascia T, Bolinger B, Merkler D, Odermatt B, Bader M, Graf R, Clavien PA, Hegazy AN, Löhning M, Harris NL, Ohashi PS, Hengartner H, Zinkernagel RM, Lang KS. Aggravation of viral hepatitis by platelet-derived serotonin. Nat Med. 2008;14:756-761. doi: 10.1038/nm1780
50. Cloutier N, Paré A, Farndale RW, Schumacher HR, Nigrovic PA, Lacroix S, Boilard E. Platelets can enhance vascular permeability. Blood. 2012;120:1334-1343. doi: 10.1182/blood-2012-02-413047