Selective serotonin reuptake inhibitors as a novel class of immunosuppressants

International Immunopharmacology

Volumn 20, Issue 1, 2014, Pages 148-156

  Gobin, Veerle ^a   Van Steendam, Katleen ^a   Denys, Damiaan ^b,c   Deforce, Dieter ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Autoimmune diseases; Graft versus host disease; Immunosuppression; Lymphocytes; Selective serotonin reuptake inhibitors

Indexed keywords

CITALOPRAM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE A; FLUOXETINE; FLUVOXAMINE; GAMMA INTERFERON; IMMUNOSUPPRESSIVE AGENT; INOSITOL PHOSPHATE; INTERLEUKIN 10; PAROXETINE; PROTEIN KINASE C; SEROTONIN; SEROTONIN TRANSPORTER; SEROTONIN UPTAKE INHIBITOR; SERTRALINE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; AUTOIMMUNE DISEASE; CELL FUNCTION; CELL VIABILITY; CONTACT ALLERGY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG ACETYLATION; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG MECHANISM; GRAFT VERSUS HOST REACTION; IC 50; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOPHARMACOLOGY; IMMUNOREGULATION; INFLAMMATORY BOWEL DISEASE; ISOMERIZATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MULTIPLE SCLEROSIS; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SEPTIC SHOCK; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; HUMAN;

ANIMALS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; SEROTONIN UPTAKE INHIBITORS;

EID: 84896347680     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2014.02.030     Document Type: Review

References (85)

1. S. Preskorn et al. Antidepressants: past, present, and future 2004 Springer Berlin; New York
2. S.C. Stanford Selective serotonin reuptake inhibitors (SSRIs). Past, present and future 1999 R.G. Landes Company Austin, Texas, U.S.A.
3. M. Vaswani, F.K. Linda, and S. Ramesh Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review Prog Neuropsychopharmacol Biol Psychiatry 27 2003 85 102
4. L.J. Brandes, R.J. Arron, R.P. Bogdanovic, J. Tong, C.L. Zaborniak, and G.R. Hogg et al. Stimulation of malignant growth in rodents by antidepressant drugs at clinically relevant doses Cancer Res 52 1992 3796 3800
5. M. Taler, I. Gil-Ad, L. Lomnitski, I. Korov, E. Baharav, and M. Bar et al. Immunomodulatory effect of selective serotonin reuptake inhibitors (SSRIs) on human T lymphocyte function and gene expression Eur Neuropsychopharmacol 17 2007 774 780
6. S.M. Reed, and J.W. Glick Fluoxetine and reactivation of the herpes simplex virus Am J Psychiatry 148 1991 949 950
7. M. Maes, C. Song, A.H. Lin, S. Bonaccorso, G. Kenis, and R. De Jongh et al. Negative immunoregulatory effects of antidepressants: inhibition of interferon-gamma and stimulation of interleukin-10 secretion Neuropsychopharmacology 20 1999 370 379
8. E. Baharav, M. Bar, M. Taler, I. Gil-Ad, L. Karp, and A. Weinberger et al. Immunomodulatory effect of sertraline in a rat model of rheumatoid arthritis Neuroimmunomodulation 19 2012 309 318
9. S.J. Koh, J.M. Kim, I.K. Kim, N. Kim, H.C. Jung, and I.S. Song et al. Fluoxetine inhibits NF-kappaB signaling in intestinal epithelial cells and ameliorates experimental colitis and colitis-associated colon cancer in mice Am J Physiol Gastrointest Liver Physiol 301 2011 G9 G19
10. M. Kubera, K. Curzytek, M. Majewska-Szczepanik, M. Szczepanik, K. Marcinska, and W. Ptak et al. Inhibitory effect of antidepressant drugs on contact hypersensitivity reaction Pharmacol Rep 64 2012 714 722
11. C. Roumestan, A. Michel, F. Bichon, K. Portet, M. Detoc, and C. Henriquet et al. Anti-inflammatory properties of desipramine and fluoxetine Respir Res 8 2007 35
12. S. Sacre, M. Medghalchi, B. Gregory, F. Brennan, and R. Williams Fluoxetine and citalopram exhibit potent antiinflammatory activity in human and murine models of rheumatoid arthritis and inhibit toll-like receptors Arthritis Rheum 62 2010 683 693
13. M. Taler, I. Gil-Ad, I. Korob, and A. Weizman The immunomodulatory effect of the antidepressant sertraline in an experimental autoimmune encephalomyelitis mouse model of multiple sclerosis Neuroimmunomodulation 18 2011 117 122
14. V. Gobin, K. Van Steendam, S. Fevery, K. Tilleman, A.D. Billiau, and D. Denys et al. Fluoxetine reduces murine graft-versus-host disease by induction of T cell immunosuppression J Neuroimmune Pharmacol 8 2013 934 943
15. V.A. Edgar, A.M. Genaro, G. Cremaschi, and L. Sterin-Borda Fluoxetine action on murine T-lymphocyte proliferation: participation of PKC activation and calcium mobilisation Cell Signal 10 1998 721 726
16. V.A. Edgar, L. Sterin-Borda, G.A. Cremaschi, and A.M. Genaro Role of protein kinase C and cAMP in fluoxetine effects on human T-cell proliferation Eur J Pharmacol 372 1999 65 73
17. L.R. Frick, M. Rapanelli, M.L. Arcos, G.A. Cremaschi, and A.M. Genaro Oral administration of fluoxetine alters the proliferation/apoptosis balance of lymphoma cells and up-regulates T cell immunity in tumor-bearing mice Eur J Pharmacol 659 2011 265 272
18. L.R. Frick, M.L. Palumbo, M.P. Zappia, M.A. Brocco, G.A. Cremaschi, and A.M. Genaro Inhibitory effect of fluoxetine on lymphoma growth through the modulation of antitumor T-cell response by serotonin-dependent and independent mechanisms Biochem Pharmacol 75 2008 1817 1826
19. L.R. Frick, and M. Rapanelli Antidepressants: influence on cancer and immunity? Life Sci 92 2013 525 532
20. L.R. Frick, M. Rapanelli, G.A. Cremaschi, and A.M. Genaro Fluoxetine directly counteracts the adverse effects of chronic stress on T cell immunity by compensatory and specific mechanisms Brain Behav Immun 23 2009 36 40
21. N. Abdul, C.J. Logothetis, and N.M. Hoosein Growth-inhibitory effects of serotonin uptake inhibitors on human prostate carcinoma cell-lines J Urol 154 1995 247 250
22. A. Serafeim, M.J. Holder, G. Grafton, A. Chamba, M.T. Drayson, and Q.T. Luong et al. Selective serotonin reuptake inhibitors directly signal for apoptosis in biopsy-like Burkitt lymphoma cells Blood 101 2003 3212 3219
23. I. Gil-Ad, A. Zolokov, L. Lomnitski, M. Taler, M. Bar, and D. Luria et al. Evaluation of the potential anti-cancer activity of the antidepressant sertraline in human colon cancer cell lines and in colorectal cancer-xenografted mice Int J Oncol 33 2008 277 286
24. D. Duerschmied, G.L. Suidan, M. Demers, N. Herr, C. Carbo, and A. Brill et al. Platelet serotonin promotes the recruitment of neutrophils to sites of acute inflammation in mice Blood 121 2012 1008 1015
25. M.B. Berkeley, S. Daussin, M.C. Hernandez, and B.M. Bayer In vitro effects of cocaine, lidocaine and monoamine uptake inhibitors on lymphocyte proliferative responses Immunopharmacol Immunotoxicol 16 1994 165 178
26. F. Fazzino, C. Montes, M. Urbina, I. Carreira, and L. Lima Serotonin transporter is differentially localized in subpopulations of lymphocytes of major depression patients. Effect of fluoxetine on proliferation J Neuroimmunol 196 2008 173 180
27. M. Taler, M. Bar, I. Korob, L. Lomnitski, E. Baharav, and N. Grunbaum-Novak et al. Evidence for an inhibitory immunomodulatory effect of selected antidepressants on rat splenocytes: possible relevance to depression and hyperactive-immune disorders Int Immunopharmacol 8 2008 526 533
28. B.H. Amit, I. Gil-Ad, M. Taler, M. Bar, A. Zolokov, and A. Weizman Proapoptotic and chemosensitizing effects of selective serotonin reuptake inhibitors on T cell lymphoma/leukemia (Jurkat) in vitro Eur Neuropsychopharmacol 19 2009 726 734
29. T.C. Pellegrino, and B.M. Bayer Specific serotonin reuptake inhibitor-induced decreases in lymphocyte activity require endogenous serotonin release Neuroimmunomodulation 8 2000 179 187
30. T.C. Pellegrino, and B.M. Bayer Modulation of immune cell function following fluoxetine administration in rats Pharmacol Biochem Behav 59 1998 151 157
31. Z. Xia, J.W. DePierre, and L. Nassberger Tricyclic antidepressants inhibit IL-6, IL-1 beta and TNF-alpha release in human blood monocytes and IL-2 and interferon-gamma in T cells Immunopharmacology 34 1996 27 37
32. M. Kubera, A.H. Lin, G. Kenis, E. Bosmans, D. van Bockstaele, and M. Maes Anti-inflammatory effects of antidepressants through suppression of the interferon-gamma/interleukin-10 production ratio J Clin Psychopharmacol 21 2001 199 206
33. A.R. Shenoy, T. Dehmel, M. Stettner, D. Kremer, B.C. Kieseier, and H.P. Hartung et al. Citalopram suppresses thymocyte cytokine production J Neuroimmunol 262 2013 46 52
34. Z. Xia, H. Karlsson, J.W. DePierre, and L. Nassberger Tricyclic antidepressants induce apoptosis in human T lymphocytes Int J Immunopharmacol 19 1997 645 654
35. C. Schuster, N. Fernbach, U. Rix, G. Superti-Furga, M. Holy, and M. Freissmuth et al. Selective serotonin reuptake inhibitors - a new modality for the treatment of lymphoma/leukaemia? Biochem Pharmacol 74 2007 1424 1435
36. A. Chamba, M.J. Holder, R.F. Jarrett, L. Shield, K.M. Toellner, and M.T. Drayson et al. SLC6A4 expression and anti-proliferative responses to serotonin transporter ligands chlomipramine and fluoxetine in primary B-cell malignancies Leuk Res 34 2010 1103 1106
37. T. Barkan, D. Gurwitz, G. Levy, A. Weizman, and M. Rehavi Biochemical and pharmacological characterization of the serotonin transporter in human peripheral blood lymphocytes Eur Neuropsychopharmacol 14 2004 237 243
38. A. Serafeim, G. Grafton, A. Chamba, C.D. Gregory, R.D. Blakely, and N.G. Bowery et al. 5-Hydroxytryptamine drives apoptosis in biopsylike Burkitt lymphoma cells: reversal by selective serotonin reuptake inhibitors Blood 99 2002 2545 2553
39. T.M. Aune, H.W. Golden, and K.M. McGrath Inhibitors of serotonin synthesis and antagonists of serotonin 1A receptors inhibit T lymphocyte function in vitro and cell-mediated immunity in vivo J Immunol 153 1994 489 498
40. J. Yin, R.H. Albert, A.P. Tretiakova, and B.A. Jameson 5-HT(1B) receptors play a prominent role in the proliferation of T-lymphocytes J Neuroimmunol 181 2006 68 81
41. M. Leon-Ponte, G.P. Ahern, and P.J. O'Connell Serotonin provides an accessory signal to enhance T-cell activation by signaling through the 5-HT7 receptor Blood 109 2007 3139 3146
42. P.J. O'Connell, X. Wang, M. Leon-Ponte, C. Griffiths, S.C. Pingle, and G.P. Ahern A novel form of immune signaling revealed by transmission of the inflammatory mediator serotonin between dendritic cells and T cells Blood 107 2006 1010 1017
43. B.L. Fanburg, and S.L. Lee A new role for an old molecule: serotonin as a mitogen Am J Physiol 272 1997 L795 L806
44. R. Mossner, and K.P. Lesch Role of serotonin in the immune system and in neuroimmune interactions Brain Behav Immun 12 1998 249 271
45. G.P. Ahern 5-HT and the immune system Curr Opin Pharmacol 11 2011 29 33
46. N.L. Baganz, and R.D. Blakely A dialogue between the immune system and brain, spoken in the language of serotonin ACS Chem Neurosci 4 2012 48 63
47. G. Miolo, S. Caffieri, L. Levorato, M. Imbesi, P. Giusti, and T. Uz et al. Photoisomerization of fluvoxamine generates an isomer that has reduced activity on the 5-hydroxytryptamine transporter and does not affect cell proliferation Eur J Pharmacol 450 2002 223 229
48. F. Ferriere, N.A. Khan, J.P. Meyniel, and P. Deschaux Characterisation of serotonin transport mechanisms in rainbow trout peripheral blood lymphocytes: role in PHA-induced lymphoproliferation Dev Comp Immunol 23 1999 37 50
49. A. Chamba, M.J. Holder, N.M. Barnes, and J. Gordon Characterisation of the endogenous human peripheral serotonin transporter SLC6A4 reveals surface expression without N-glycosylation J Neuroimmunol 204 2008 75 84
50. S.M. Cloonan, A. Drozgowska, D. Fayne, and D.C. Williams The antidepressants maprotiline and fluoxetine have potent selective antiproliferative effects against Burkitt lymphoma independently of the norepinephrine and serotonin transporters Leuk Lymphoma 51 2010 523 539
51. M. Diamond, J.P. Kelly, and T.J. Connor Antidepressants suppress production of the Th1 cytokine interferon-gamma, independent of monoamine transporter blockade Eur Neuropsychopharmacol 16 2006 481 490
52. D.J. Walther, J.U. Peter, S. Winter, M. Holtje, N. Paulmann, and M. Grohmann et al. Serotonylation of small GTPases is a signal transduction pathway that triggers platelet alpha-granule release Cell 115 2003 851 862
53. B.J. Thompson, T. Jessen, L.K. Henry, J.R. Field, K.L. Gamble, and P.J. Gresch et al. Transgenic elimination of high-affinity antidepressant and cocaine sensitivity in the presynaptic serotonin transporter Proc Natl Acad Sci U S A 108 2011 3785 3790
54. I.H. Heijink, H.F. Kauffman, D.S. Postma, J.G. de Monchy, and E. Vellenga Sensitivity of IL-5 production to the cAMP-dependent pathway in human T cells is reduced by exogenous IL-2 in a phosphoinositide 3-kinase-dependent way Eur J Immunol 33 2003 2206 2215
55. G. Kenis, H. Steinbusch, M. De Baets, and M. Maes Influence of antidepressants on intracellular levels of cyclic adenosine monophosphate in human peripheral blood mononuclear cells Eur Neuropsychopharmacol 13 2003 53 56
56. M. Maes, G. Kenis, M. Kubera, M. De Baets, H. Steinbusch, and E. Bosmans The negative immunoregulatory effects of fluoxetine in relation to the cAMP-dependent PKA pathway Int Immunopharmacol 5 2005 609 618
57. S. Feske, E.Y. Skolnik, and M. Prakriya Ion channels and transporters in lymphocyte function and immunity Nat Rev Immunol 12 2012 532 547
58. Z. Xia, J.W. DePierre, and L. Nassberger Dysregulation of bcl-2, c-myc, and Fas expression during tricyclic antidepressant-induced apoptosis in human peripheral lymphocytes J Biochem Toxicol 11 1996 203 204
59. Z. Xia, A. Bergstrand, J.W. DePierre, and L. Nassberger The antidepressants imipramine, clomipramine, and citalopram induce apoptosis in human acute myeloid leukemia HL-60 cells via caspase-3 activation J Biochem Mol Toxicol 13 1999 338 347
60. Z. Xia, B. Lundgren, A. Bergstrand, J.W. DePierre, and L. Nassberger Changes in the generation of reactive oxygen species and in mitochondrial membrane potential during apoptosis induced by the antidepressants imipramine, clomipramine, and citalopram and the effects on these changes by Bcl-2 and Bcl-X(L) Biochem Pharmacol 57 1999 1199 1208
61. E.J. Meredith, M.J. Holder, A. Chamba, A. Challa, A. Drake-Lee, and C.M. Bunce et al. The serotonin transporter (SLC6A4) is present in B-cell clones of diverse malignant origin: probing a potential anti-tumor target for psychotropics FASEB J 19 2005 1187 1189
62. E. Daley, D. Wilkie, A. Loesch, I.P. Hargreaves, D.A. Kendall, and G.J. Pilkington et al. Chlorimipramine: a novel anticancer agent with a mitochondrial target Biochem Biophys Res Commun 328 2005 623 632
63. B. Eisensamer, M. Uhr, S. Meyr, G. Gimpl, T. Deiml, and G. Rammes et al. Antidepressants and antipsychotic drugs colocalize with 5-HT3 receptors in raft-like domains J Neurosci 25 2005 10198 10206
64. R.J. Donati, and M.M. Rasenick Chronic antidepressant treatment prevents accumulation of gsalpha in cholesterol-rich, cytoskeletal-associated, plasma membrane domains (lipid rafts) Neuropsychopharm 30 2005 1238 1245
65. P.A. van der Merwe, and O. Dushek Mechanisms for T cell receptor triggering Nat Rev Immunol 11 2011 47 55
66. C.M. Pariante, A. Makoff, S. Lovestone, S. Feroli, A. Heyden, and A.H. Miller et al. Antidepressants enhance glucocorticoid receptor function in vitro by modulating the membrane steroid transporters Br J Pharmacol 134 2001 1335 1343
67. M. Antonioli, J. Rybka, and L.A. Carvalho Neuroimmune endocrine effects of antidepressants Neuropsychiatr Dis Treat 8 2012 65 83
68. P. Vollmar, S. Nessler, S.R. Kalluri, H.P. Hartung, and B. Hemmer The antidepressant venlafaxine ameliorates murine experimental autoimmune encephalomyelitis by suppression of pro-inflammatory cytokines Int J Neuropsychopharmacol 12 2009 525 536
69. X.Q. Yuan, G. Qiu, X.J. Liu, S. Liu, Y.M. Wu, and X.Y. Wang et al. Fluoxetine promotes remission in acute experimental autoimmune encephalomyelitis in rats Neuroimmunomodulation 19 2012 201 208
70. A.A. Guemei, N.M. El Din, A.M. Baraka, and Darwish I. El Said Do desipramine [10,11-dihydro-5-[3-(methylamino) propyl]-5H-dibenz[b, f]azepine monohydrochloride] and fluoxetine [N-methyl-3-phenyl-3-[4-(trifluoromethyl) phenoxy]-propan-1-amine] ameliorate the extent of colonic damage induced by acetic acid in rats? J Pharmacol Exp Ther 327 2008 846 850
71. K.F. Foley, and R.E. Kast Review of evidence that posttransplantation psychiatric treatment commonly affects prolactin levels and thereby influences graft fate Gen Hosp Psychiatry 28 2006 230 233
72. J.L. Ferrara, J.E. Levine, P. Reddy, and E. Holler Graft-versus-host disease Lancet 373 2009 1550 1561
73. M.L. MacMillan, D.J. Weisdorf, J.E. Wagner, T.E. DeFor, L.J. Burns, and N.K. Ramsay et al. Response of 443 patients to steroids as primary therapy for acute graft-versus-host disease: comparison of grading systems Biol Blood Marrow Transplant 8 2002 387 394
74. F.R. Appelbaum Haematopoietic cell transplantation as immunotherapy Nature 411 2001 385 389
75. J.P. Mostert, F. Admiraal-Behloul, J.M. Hoogduin, J. Luyendijk, D.J. Heersema, and M.A. van Buchem et al. Effects of fluoxetine on disease activity in relapsing multiple sclerosis: a double-blind, placebo-controlled, exploratory study J Neurol Neurosurg Psychiatry 79 2008 1027 1031
76. H. Bird, and M. Broggini Paroxetine versus amitriptyline for treatment of depression associated with rheumatoid arthritis: a randomized, double blind, parallel group study J Rheumatol 27 2000 2791 2797
77. S.M. Wille, S.G. Cooreman, H.M. Neels, and W.E. Lambert Relevant issues in the monitoring and the toxicology of antidepressants Crit Rev Clin Lab Sci 45 2008 25 89
78. C.L. DeVane Metabolism and pharmacokinetics of selective serotonin reuptake inhibitors Cell Mol Neurobiol 19 1999 443 466
79. M. Uhr, M.T. Grauer, and F. Holsboer Differential enhancement of antidepressant penetration into the brain in mice with abcb1ab (mdr1ab) P-glycoprotein gene disruption Biol Psychiatry 54 2003 840 846
80. D. Denys, A. Kavelaars, C.J. Heijnen, and H. Westenberg A case of venlafaxine-induced inhibition of T-lymphocyte proliferation Psychopharmacology (Berl) 164 2002 432
81. S.C. Dulawa, K.A. Holick, B. Gundersen, and R. Hen Effects of chronic fluoxetine in animal models of anxiety and depression Neuropsychopharmacology 29 2004 1321 1330
82. J.T. Barbey, and S.P. Roose SSRI safety in overdose J Clin Psychiatry 59 Suppl. 15 1998 42 48
83. E.H. Decloedt, and D.J. Stein Current trends in drug treatment of obsessive-compulsive disorder Neuropsychiatr Dis Treat 6 2010 233 242
84. R. Krishnadas, and J. Cavanagh Sustained remission of rheumatoid arthritis with a specific serotonin reuptake inhibitor antidepressant: a case report and review of the literature J Med Case Reports 5 2011 112
85. P. Vollmar, S. Nessler, SR. Kalluri, HP. Hartung, and B. Hemmer The antidepressant venlafaxine ameliorates murine experimental autoimmune encephalomyelitis by suppression of pro-inflammatory cytokines Int J Neuropsychopharmacol 12 2009 525 536