Serotonin-mediated tuning of human helper T cell responsiveness to the chemokine CXCL12

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Magrini, Elena ^a,d   Szabò, Ildikò ^b   Doni, Andrea ^a   Cibella, Javier ^a   Viola, Antonella ^a,c  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SEROTONIN; SEROTONIN 3 RECEPTOR; STROMAL CELL DERIVED FACTOR 1; ACTIN; CHEMOKINE RECEPTOR CXCR4; SEROTONIN RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE MIGRATION; MIGRATION INHIBITION; MOUSE; NONHUMAN; NORMAL HUMAN; PATCH CLAMP; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CHEMOTAXIS; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; POLYMERIZATION; PROTEIN BINDING; SECRETION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ACTINS; ANIMALS; CHEMOKINE CXCL12; CHEMOTAXIS; ENDOTHELIAL CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; POLYMERIZATION; PROTEIN BINDING; RECEPTORS, CXCR4; RECEPTORS, SEROTONIN; SEROTONIN; T-LYMPHOCYTES, HELPER-INDUCER; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 80051532788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022482     Document Type: Article

References (43)

1. Barnes NM, Gordon J, (2008) Harnessing serotonergic and dopaminergic pathways for lymphoma therapy: evidence and aspirations. Semin Cancer Biol 18: 218-225.
2. Walther DJ, Peter JU, Bashammakh S, Hortnagl H, Voits M, et al. (2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299: 76.
3. Gordon J, Barnes NM, (2003) Lymphocytes transport serotonin and dopamine: agony or ecstasy? Trends Immunol 24: 438-443.
4. Meredith EJ, Chamba A, Holder MJ, Barnes NM, Gordon J, (2005) Close encounters of the monoamine kind: immune cells betray their nervous disposition. Immunology 115: 289-295.
5. Cloez-Tayarani I, Changeux JP, (2007) Nicotine and serotonin in immune regulation and inflammatory processes: a perspective. J Leukoc Biol 81: 599-606.
6. Levite M, (2008) Neurotransmitters activate T-cells and elicit crucial functions via neurotransmitter receptors. Curr Opin Pharmacol 8: 460-471.
7. Khan WI, Ghia JE, Gut hormones: emerging role in immune activation and inflammation. Clin Exp Immunol 161: 19-27.
8. Muller T, Durk T, Blumenthal B, Grimm M, Cicko S, et al. (2009) 5-hydroxytryptamine modulates migration, cytokine and chemokine release and T-cell priming capacity of dendritic cells in vitro and in vivo. PLoS One 4: e6453.
9. Leon-Ponte M, Ahern GP, O'Connell PJ, (2007) Serotonin provides an accessory signal to enhance T-cell activation by signaling through the 5-HT7 receptor. Blood 109: 3139-3146.
10. O'Connell PJ, Wang X, Leon-Ponte M, Griffiths C, Pingle SC, et al. (2006) A novel form of immune signaling revealed by transmission of the inflammatory mediator serotonin between dendritic cells and T cells. Blood 107: 1010-1017.
11. Peters JA, Hales TG, Lambert JJ, (2005) Molecular determinants of single-channel conductance and ion selectivity in the Cys-loop family: insights from the 5-HT3 receptor. Trends Pharmacol Sci 26: 587-594.
12. Faerber L, Drechsler S, Ladenburger S, Gschaidmeier H, Fischer W, (2007) The neuronal 5-HT3 receptor network after 20 years of research-evolving concepts in management of pain and inflammation. Eur J Pharmacol 560: 1-8.
13. Davies PA, Pistis M, Hanna MC, Peters JA, Lambert JJ, et al. (1999) The 5-HT3B subunit is a major determinant of serotonin-receptor function. Nature 397: 359-363.
14. Dubin AE, Huvar R, D'Andrea MR, Pyati J, Zhu JY, et al. (1999) The pharmacological and functional characteristics of the serotonin 5-HT(3A) receptor are specifically modified by a 5-HT(3B) receptor subunit. J Biol Chem 274: 30799-30810.
15. Fiebich BL, Akundi RS, Seidel M, Geyer V, Haus U, et al. (2004) Expression of 5-HT3A receptors in cells of the immune system. Scand J Rheumatol Suppl pp. 9-11.
16. Cahalan MD, Chandy KG, (2009) The functional network of ion channels in T lymphocytes. Immunol Rev 231: 59-87.
17. Lai ZF, Chen YZ, Nishimura Y, Nishi K, (2000) An amiloride-sensitive and voltage-dependent Na+ channel in an HLA-DR-restricted human T cell clone. J Immunol 165: 83-90.
18. Yin J, Albert RH, Tretiakova AP, Jameson BA, (2006) 5-HT(1B) receptors play a prominent role in the proliferation of T-lymphocytes. J Neuroimmunol 181: 68-81.
19. Yao L, Salvucci O, Cardones AR, Hwang ST, Aoki Y, et al. (2003) Selective expression of stromal-derived factor-1 in the capillary vascular endothelium plays a role in Kaposi sarcoma pathogenesis. Blood 102: 3900-3905.
20. de Vreese K, Kofler-Mongold V, Leutgeb C, Weber V, Vermeire K, et al. (1996) The molecular target of bicyclams, potent inhibitors of human immunodeficiency virus replication. J Virol 70: 689-696.
21. Weyrich AS, Zimmerman GA, (2004) Platelets: signaling cells in the immune continuum. Trends Immunol 25: 489-495.
22. Mossner R, Lesch KP, (1998) Role of serotonin in the immune system and in neuroimmune interactions. Brain Behav Immun 12: 249-271.
23. Spiller R, (2008) Serotonin and GI clinical disorders. Neuropharmacology 55: 1072-1080.
24. Magro F, Fraga S, Azevedo I, Soares-da-Silva P, (2006) Intestinal 5-hydroxytryptamine and mast cell infiltration in rat experimental colitis. Dig Dis Sci 51: 495-501.
25. El-Nour H, Lundeberg L, Boman A, Abramowski D, Holst M, et al. (2007) The expression and functional significance of the serotonin(2C) receptor in murine contact allergy. Exp Dermatol 16: 644-650.
26. Lonne-Rahm SB, Rickberg H, El-Nour H, Marin P, Azmitia EC, et al. (2008) Neuroimmune mechanisms in patients with atopic dermatitis during chronic stress. J Eur Acad Dermatol Venereol 22: 11-18.
27. Thorslund K, Nordlind K, (2007) Serotonergic drugs-a possible role in the treatment of psoriasis? Drug News Perspect 20: 521-525.
28. Menard G, Turmel V, Bissonnette EY, (2007) Serotonin modulates the cytokine network in the lung: involvement of prostaglandin E2. Clin Exp Immunol 150: 340-348.
29. Iannacone M, Sitia G, Isogawa M, Marchese P, Castro MG, et al. (2005) Platelets mediate cytotoxic T lymphocyte-induced liver damage. Nat Med 11: 1167-1169.
30. Lang PA, Contaldo C, Georgiev P, El-Badry AM, Recher M, et al. (2008) Aggravation of viral hepatitis by platelet-derived serotonin. Nat Med 14: 756-761.
31. Khan NA, Poisson JP, (1999) 5-HT3 receptor-channels coupled with Na+ influx in human T cells: role in T cell activation. J Neuroimmunol 99: 53-60.
32. Schwab A, Nechyporuk-Zloy V, Fabian A, Stock C, (2007) Cells move when ions and water flow. Pflugers Arch 453: 421-432.
33. Simchowitz L, (1985) Chemotactic factor-induced activation of Na+/H+ exchange in human neutrophils. II. Intracellular pH changes. J Biol Chem 260: 13248-13255.
34. Simchowitz L, Cragoe EJ Jr, (1986) Regulation of human neutrophil chemotaxis by intracellular pH. J Biol Chem 261: 6492-6500.
35. Hayashi H, Aharonovitz O, Alexander RT, Touret N, Furuya W, et al. (2008) Na+/H+ exchange and pH regulation in the control of neutrophil chemokinesis and chemotaxis. Am J Physiol Cell Physiol 294: C526-534.
36. Mikami S, Nakase H, Yamamoto S, Takeda Y, Yoshino T, et al. (2008) Blockade of CXCL12/CXCR4 axis ameliorates murine experimental colitis. J Pharmacol Exp Ther 327: 383-392.
37. Nanki T, Hayashida K, El-Gabalawy HS, Suson S, Shi K, et al. (2000) Stromal cell-derived factor-1-CXC chemokine receptor 4 interactions play a central role in CD4+ T cell accumulation in rheumatoid arthritis synovium. J Immunol 165: 6590-6598.
38. Scimone ML, Felbinger TW, Mazo IB, Stein JV, Von Andrian UH, et al. (2004) CXCL12 mediates CCR7-independent homing of central memory cells, but not naive T cells, in peripheral lymph nodes. J Exp Med 199: 1113-1120.
39. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, et al. (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3: 687-694.
40. Levesque JP, Hendy J, Takamatsu Y, Simmons PJ, Bendall LJ, (2003) Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111: 187-196.
41. Rao RM, Betz TV, Lamont DJ, Kim MB, Shaw SK, et al. (2004) Elastase release by transmigrating neutrophils deactivates endothelial-bound SDF-1alpha and attenuates subsequent T lymphocyte transendothelial migration. J Exp Med 200: 713-724.
42. Bianchi G, Sironi M, Ghibaudi E, Selvaggini C, Elices M, et al. (1993) Migration of natural killer cells across endothelial cell monolayers. J Immunol 151: 5135-5144.
43. Szabo I, Bock J, Grassme H, Soddemann M, Wilker B, et al. (2008) Mitochondrial potassium channel Kv1.3 mediates Bax-induced apoptosis in lymphocytes. Proc Natl Acad Sci U S A 105: 14861-14866.