Production of serotonin by tryptophan hydroxylase 1 and release via platelets contribute to allergic airway inflammation

American Journal of Respiratory and Critical Care Medicine

Volumn 187, Issue 5, 2013, Pages 476-485

  Dürk, Thorsten ^a   Duerschmied, Daniel ^b   Müller, Tobias ^a   Grimm, Melanie ^a   Reuter, Sebastian ^c   Vieira, Rodolfo Paula ^a   Ayata, Korcan ^a   Cicko, Sanja ^a   Sorichter, Stephan ^a   Walther, Diego J ^d   Virchow, J Christian ^e   Taube, Christian ^f   Idzko, Marco ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^e University Medical Center Rostock   (Germany)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Asthma; Dendritic cells; Platelets; Serotonin; Tryptophan hydroxylase 1

Indexed keywords

SEROTONIN; TRYPTOPHAN HYDROXYLASE; TRYPTOPHAN HYDROXYLASE 1; UNCLASSIFIED DRUG;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DERMATOPHAGOIDES; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG LAVAGE; MAST CELL; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROVOCATION TEST; TH2 CELL; THROMBOCYTE; THROMBOCYTE TRANSFUSION;

ANIMALS; ASTHMA; BLOOD PLATELETS; BRONCHOALVEOLAR LAVAGE FLUID; DENDRITIC CELLS; HUMANS; MAST CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; PYROGLYPHIDAE; SEROTONIN; TRYPTOPHAN HYDROXYLASE;

EID: 84875191476     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201208-1440OC     Document Type: Article

References (60)

1. Fanta CH. Asthma. N Engl J Med 2009;360:1002-1014.
2. Mossner R, Lesch KP. Role of serotonin in the immune system and in neuroimmune interactions. Brain Behav Immun 1998;12:249-271.
3. Gordon J, Barnes NM. Lymphocytes transport serotonin and dopamine: agony or ecstasy? Trends Immunol 2003;24:438-443.
4. Meredith EJ, Chamba A, Holder MJ, Barnes NM, Gordon J. Close encounters of the monoamine kind: immune cells betray their nervous disposition. Immunology 2005;115:289-295.
5. Cloez-Tayarani I, Changeux JP. Nicotine and serotonin in immune regulation and inflammatory processes: a perspective. J Leukoc Biol 2007;81:599-606.
6. Boehme SA, Lio FM, Sikora L, Pandit TS, Lavrador K, Rao SP, Sriramarao P. Cutting edge: serotonin is a chemotactic factor for eosinophils and functions additively with eotaxin. J Immunol 2004;173:3599-3603.
7. Kushnir-Sukhov NM, Gilfillan AM, Coleman JW, Brown JM, Bruening S, Toth M, Metcalfe DD. 5-Hydroxytryptamine induces mast cell adhesion and migration. J Immunol 2006;177:6422-6432.
8. Sato E, Haniuda M, Numanami H, Ushiyama T, Tsukadaira A, Takashi S, Okubo Y, Koyama S. Histamine and serotonin stimulate eotaxin production by a human lung fibroblast cell line. Int Arch Allergy Immunol 2002;128:12-17.
9. Durk T, Panther E, Muller 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.
10. Idzko M, Panther E, Stratz C, Muller T, Bayer H, Zissel G, Durk T, Sorichter S, Di Virgilio F, Geissler M, et al. The serotoninergic receptors of human dendritic cells: identification and coupling to cytokine release. J Immunol 2004;172:6011-6019.
11. Bayer H, Muller T, Myrtek D, Sorichter S, Ziegenhagen M, Norgauer J, Zissel G, Idzko M. Serotoninergic receptors on human airway epithelial cells. Am J Respir Cell Mol Biol 2007;36:85-93.
12. Muller T, Durk T, Blumenthal B, Grimm M, Cicko S, Panther E, Sorichter S, Herouy Y, Di Virgilio F, Ferrari D, et al. 5-Hydroxytryptamine modulates migration, cytokine and chemokine release and T-cell priming capacity of dendritic cells in vitro and in vivo. PLoS ONE 2009;4:e6453.
13. Leon-Ponte M, Ahern GP, O'Connell PJ. Serotonin provides an accessory signal to enhance T-cell activation by signaling through the 5-HT7 receptor. Blood 2007;109:3139-3146.
14. O'Connell PJ, Wang X, Leon-Ponte M, Griffiths C, Pingle SC, Ahern GP. A novel form of immune signaling revealed by transmission of the inflammatory mediator serotonin between dendritic cells and T cells. Blood 2006;107:1010-1017.
15. Berger M, Gray JA, Roth BL. The expanded biology of serotonin. Annu Rev Med 2009;60:355-366.
16. Walther DJ, Peter J-U, Bashammakh S, Hortnagl H, Voits M, Fink H, Bader M. Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 2003;299:76.
17. Kushnir-Sukhov NM, Brown JM, Wu YL, Kirshenbaum A, Metcalfe DD. Human mast cells are capable of serotonin synthesis and release. J Allergy Clin Immunol 2007;119:498-499.
18. McNicol A, Israels SJ. Platelet dense granules: structure, function and implications for haemostasis. Thromb Res 1999;95:1-18.
19. Toh CC. Release of 5-hydroxytryptamine (serotonin) and histamine from platelets by tissue extracts. J Physiol 1956;133:402-411.
20. Yoshida A, Ohba M, Wu X, Sasano T, Nakamura M, Endo Y. Accumulation of platelets in the lung and liver and their degranulation following antigen-challenge in sensitized mice. Br J Pharmacol 2002;137:146-152.
21. Lechin F, van der Dijs B, Orozco B, Lechin M, Lechin AE. Increased levels of free serotonin in plasma of symptomatic asthmatic patients. Ann Allergy Asthma Immunol 1996;77:245-253.
22. Lechin F, van der Dijs B, Orozco B, Jara H, Rada I, Lechin ME, Lechin AE. The serotonin uptake-enhancing drug tianeptine suppresses asthmatic symptoms in children: a double-blind, crossover, placebo-controlled study. J Clin Pharmacol 1998;38:918-925.
23. Lechin F, van der Dijs B, Orozco B, Jara H, Rada I, Lechin ME, Lechin AE. Neuropharmacologic treatment of bronchial asthma with the antidepressant tianeptine: a double-blind, crossover placebo-controlled study. Clin Pharmacol Ther 1998;64:223-232.
24. Lechin F, van der Dijs B, Lechin AE. Treatment of bronchial asthma with tianeptine. Methods Find Exp Clin Pharmacol 2004;26:697-701.
25. Lima C, Souza VM, Soares AL,MacedoMS, Tavares-de-LimaW, Vargaftig BB. Interference of methysergide, a specific 5-hydroxytryptamine receptor antagonist, with airway chronic allergic inflammation and remodelling in a murine model of asthma. Clin Exp Allergy 2007;37:723-734.
26. De Bie JJ, Henricks PA, Cruikshank WW, Hofman G, Jonker EH, Nijkamp FP, Van Oosterhout AJ. Modulation of airway hyper-responsiveness and eosinophilia by selective histamine and 5-HT receptor antagonists in a mouse model of allergic asthma. Br J Pharmacol 1998;124:857-864.
27. Reuter S, Heinz A, Sieren M, Wiewrodt R, Gelfand EW, Stassen M, Buhl R, Taube C. Mast cell-derived tumour necrosis factor is essential for allergic airway disease. Eur Respir J 2008;31:773-782.
28. Muller T, Vieira RP, Grimm M, Durk T, Cicko S, Zeiser R, Jakob T, Martin SF, Blumenthal B, Sorichter S, et al. A potential role for p2 × 7r in allergic airway inflammation in mice and humans. Am J Respir Cell Mol Biol 2011;44:456-464.
29. Idzko M, Hammad H, van Nimwegen M, Kool M, Willart MA, Muskens F, Hoogsteden HC, Luttmann W, Ferrari D, Di Virgilio F, et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nat Med 2007;13:913-919.
30. Julius P, Lommatzsch M, Kuepper M, Bratke K, Faehndrich S, Luttmann W, Virchow JC. Safety of segmental allergen challenge in human allergic asthma. J Allergy Clin Immunol 2008;121:712-717.
31. Idzko M, Hammad H, van Nimwegen M, Kool M, Muller T, Soullie T, Willart MA, Hijdra D, Hoogsteden HC, Lambrecht BN. Local application of FTY720 to the lung abrogates experimental asthma by altering dendritic cell function. J Clin Invest 2006;116:2935-2944.
32. Lommatzsch M, Julius P, Kuepper M, Garn H, Bratke K, Irmscher S, Luttmann W, Renz H, Braun A, Virchow JC. The course of allergen-induced leukocyte infiltration in human and experimental asthma. J Allergy Clin Immunol 2006;118:91-97.
33. van Rijt LS, Vos N, Willart M, Kleinjan A, Coyle AJ, Hoogsteden HC, Lambrecht BN. Essential role of dendritic cell CD80/CD86 costimulation in the induction, but not reactivation, of Th2 effector responses in a mouse model of asthma. J Allergy Clin Immunol 2004;114:166-173.
34. Finocchiaro LM, Arzt ES, Fernandez-Castelo S, Criscuolo M, Finkielman S, Nahmod VE. Serotonin and melatonin synthesis in peripheral blood mononuclear cells: stimulation by interferon-gamma as part of an immuno-modulatory pathway. J Interferon Res 1988;8:705-716.
35. Carrillo-Vico A, Calvo JR, Abreu P, Lardone PJ, Garcia-Maurino S, Reiter RJ,Guerrero JM. Evidence of melatonin synthesis by human lymphocytes and its physiological significance: possible role as intracrine, autocrine, and/or paracrine substance. FASEB J 2004;18:537-539.
36. Duerschmied D, Canault M, Lievens D, Brill A, Cifuni SM, Bader M, Wagner DD. Serotonin stimulates platelet receptor shedding by tumor necrosis factor-alpha-converting enzyme (adam17). J Thromb Haemost 2009;7:1163-1171.
37. Benedict CR, Mathew B, Rex KA, Cartwright J Jr., Sordahl LA. Correlation of plasma serotonin changes with platelet aggregation in an in vivo dog model of spontaneous occlusive coronary thrombus formation. Circ Res 1986;58:58-67.
38. Lederer DJ, Horn EM, Rosenzweig EB, Karmally W, Jahnes M, Barst RJ, Kawut SM. Plasma serotonin levels are normal in pulmonary arterial hypertension. Pulm Pharmacol Ther 2008;21:112-114.
39. Liu Y, Wei L, Laskin DL, Fanburg BL. Role of protein transamidation in serotonin-induced proliferation and migration of pulmonary artery smooth muscle cells. Am J Respir Cell Mol Biol 2011;44:548-555.
40. Eddahibi S, Humbert M, Fadel E, Raffestin B, Darmon M, Capron F, Simonneau G, Dartevelle P, Hamon M, Adnot S. Serotonin transporter overexpression is responsible for pulmonary artery smooth muscle hyperplasia in primary pulmonary hypertension. J Clin Invest 2001; 108:1141-1150.
41. Eddahibi S, Raffestin B, Pham I, Launay JM, Aegerter P, Sitbon M, Adnot S. Treatment with 5-HT potentiates development of pulmonary hypertension in chronically hypoxic rats. Am J Physiol 1997;272:H1173-H1181.
42. Kereveur A, Callebert J, Humbert M, Herve P, Simonneau G, Launay JM, Drouet L. High plasma serotonin levels in primary pulmonary hypertension. Effect of long-term epoprostenol (prostacyclin) therapy. Arterioscler Thromb Vasc Biol 2000;20:2233-2239.
43. Taube C, Stassen M. Mast cells and mast cell-derived factors in the regulation of allergic sensitization. Chem Immunol Allergy 2008;94:58-66.
44. Becker M, Reuter S, Friedrich P, Doener F, Michel A, Bopp T, Klein M, Schmitt E, Schild H, Radsak MP, et al. Genetic variation determines mast cell functions in experimental asthma. J Immunol 2011;186: 7225-7231.
45. Takeda K, Hamelmann E, Joetham A, Shultz LD, Larsen GL, Irvin CG, Gelfand EW. Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J Exp Med 1997;186:449-454.
46. Kowal K, Pampuch A, Kowal-Bielecka O, DuBuske LM, Bodzenta-Lukaszyk A. Platelet activation in allergic asthma patients during allergen challenge with dermatophagoides pteronyssinus. Clin Exp Allergy 2006;36:426-432.
47. Gresele P, Dottorini M, Selli ML, Iannacci L, Canino S, Todisco T, Romano S, Crook P, Page CP, Nenci GG. Altered platelet function associated with the bronchial hyperresponsiveness accompanying nocturnal asthma. J Allergy Clin Immunol 1993;91:894-902.
48. Pitchford SC, Riffo-Vasquez Y, Sousa A, Momi S, Gresele P, Spina D, Page CP. Platelets are necessary for airway wall remodeling in a murine model of chronic allergic inflammation. Blood 2004;103:639-647.
49. Pitchford SC, Momi S, Giannini S, Casali L, Spina D, Page CP, Gresele P. Platelet P-selectin is required for pulmonary eosinophil and lymphocyte recruitment in a murine model of allergic inflammation. Blood 2005; 105:2074-2081.
50. Pitchford SC, Momi S, Baglioni S, Casali L, Giannini S, Rossi R, Page CP, Gresele P. Allergen induces the migration of platelets to lung tissue in allergic asthma. Am J Respir Crit Care Med 2008;177:604-612.
51. Johansson MW, Han ST, Gunderson KA, Busse WW, Jarjour NN, Mosher DF. Platelet activation, P-selectin, and eosinophil beta1-integrin activation in asthma. Am J Respir Crit Care Med 2012;185: 498-507.
52. Lambrecht BN, Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu Rev Immunol 2012;30:243-270.
53. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med 2012;18:673-683.
54. Huh JC, Strickland DH, Jahnsen FL, Turner DJ, Thomas JA, Napoli S, Tobagus I, Stumbles PA, Sly PD, Holt PG. Bidirectional interactions between antigen-bearing respiratory tract dendritic cells (DCS) and T cells precede the late phase reaction in experimental asthma: DC activation occurs in the airway mucosa but not in the lung parenchyma. J Exp Med 2003;198:19-30.
55. Zinser E, Lechmann M, Golka A, Lutz MB, Steinkasserer A. Prevention and treatment of experimental autoimmune encephalomyelitis by soluble CD83. J Exp Med 2004;200:345-351.
56. Xu JF, Huang BJ, Yin H, Xiong P, Feng W, Xu Y, Fang M, Zheng F, Wang CY, Gong FL. A limited course of soluble CD83 delays acute cellular rejection of MHC-mismatched mouse skin allografts. Transpl Int 2007;20:266-276.
57. Ge W, Arp J, Lian D, LiuW, Baroja ML, Jiang J, Ramcharran S, Eldeen FZ, Zinser E, Steinkasserer A, et al. Immunosuppression involving soluble CD83 induces tolerogenic dendritic cells that prevent cardiac allograft rejection. Transplantation 2010;90:1145-1156.
58. Lundell AC, Andersson K, Josefsson E, Steinkasserer A, Rudin A. Soluble CD14 and CD83 from human neonatal antigen-presenting cells are inducible by commensal bacteria and suppress allergen-induced human neonatal Th2 differentiation. Infect Immun 2007;75: 4097-4104.
59. Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, Panther E, Di Virgilio F. The p2 × 7 receptor: a key player in IL-1 processing and release. J Immunol 2006;176:3877-3883.
60. Li N, Ghia JE, Wang H, McClemens J, Cote F, Suehiro Y, Mallet J, Khan WI. Serotonin activates dendritic cell function in the context of gut inflammation. Am J Pathol 2011;178:662-671.