The acid sphingomyelinase inhibitors block interferon-α-induced serotonin uptake via a COX-2/Akt/ERK/STAT-dependent pathway in T cells

International Immunopharmacology

Volumn 11, Issue 11, 2011, Pages 1823-1831

  Su, Hui Chen ^a   Ma, Ching Ting ^b,c   Lin, Chiou Feng ^b   Wu, Hung Tsung ^b   Chuang, Yeu Hui ^d   Chen, Li Jen ^b   Tsao, Chiung Wen ^c  

^a CHI MEI MEDICAL CENTER   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c CHUNG HWA UNIVERSITY OF MEDICAL TECHNOLOGY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Akt; Cyclooxygenase 2; Interferon ; Serotonin uptake; Sphingomyelinases

Indexed keywords

ALPHA INTERFERON; CELECOXIB; CYCLOOXYGENASE 2; FLUOXETINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; SEROTONIN; SPHINGOLACTONE 24; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; STAT1 PROTEIN; STAT3 PROTEIN; TRICYCLO[4.3.0.1]DECAN 9 YL XANTHOGENATE; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTONIN UPTAKE; T LYMPHOCYTE;

BLOTTING, WESTERN; CYCLOOXYGENASE 2; DEPRESSION; ENZYME INHIBITORS; HUMANS; INTERFERON-ALPHA; JURKAT CELLS; MAP KINASE SIGNALING SYSTEM; PROTO-ONCOGENE PROTEINS C-AKT; RECOMBINANT PROTEINS; SEROTONIN; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE; STAT TRANSCRIPTION FACTORS; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR;

EID: 80054975366     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2011.07.011     Document Type: Article

References (73)

1. R.A. Claus, M.J. Dorer, A.C. Bunck, and H.P. Deigner Inhibition of sphingomyelin hydrolysis: targeting the lipid mediator ceramide as a key regulator of cellular fate Curr Med Chem 16 2009 1978 2000
2. G.F. Nixon Sphingolipids in inflammation: pathological implications and potential therapeutic targets Br J Pharmacol 158 2009 982 993
3. M.W. Spence, J.K. Burgess, and E.R. Sperker Neutral and acid sphingomyelinases: somatotopographical distribution in Brain Res 168 1979 543 551
4. T. Mikami, T. Takahashi, A. Ishida, Y. Minamiya, H. Ida, and G. Takada Signaling pathway for radiation-induced apoptosis in the lymphoblasts from neuronopathic (type A) and non-neuronopathic (type B) forms of Niemann-Pick disease J Neurol Sci 199 2002 39 43 (Pubitemid 34663833)
5. J. Kornhuber, A. Medlin, S. Bleich, V. Jendrossek, A.W. Henkel, and J. Wiltfang High activity of acid sphingomyelinase in major depression J Neural Transm 112 2005 1583 1590 (Pubitemid 41504272)
6. J. Kornhuber, M. Reichel, P. Tripal, T.W. Groemer, A.W. Henkel, and C. Mühle The role of ceramide in major depressive disorder Eur Arch Psychiatry Clin Neurosci 259 Suppl 2 2009 S199 S204
7. M. Nikolova-Karakashian, A. Karakashian, and K. Rutkute Role of neutral sphingomyelinases in aging and inflammation Subcell Biochem 49 2008 469 486
8. W. Stoffel, B. Jenke, B. Block, M. Zumbansen, and J. Koebke Neutral sphingomyelinase 2 (smpd3) in the control of postnatal growth and development Proc Natl Acad Sci USA 102 2005 4554 4559 (Pubitemid 40397150)
9. M. aan het Rot, S.J. Mathew, and D.S. Charney Neurobiological mechanisms in major depressive disorder Cmaj 180 2009 305 313
10. S. Sockalingam, and S.E. Abbey Managing depression during hepatitis C treatment Can J Psychiatry 54 2009 614 625
11. A.M. Myint, M.J. Schwarz, H.W. Steinbusch, and B.E. Leonard Neuropsychiatric disorders related to interferon and interleukins treatment Metab Brain Dis 24 2009 55 68
12. C.L. Raison, M. Demetrashvili, L. Capuron, and A.H. Miller Neuropsychiatric adverse effects of interferon-alpha: recognition and management CNS Drugs 19 2005 105 123 (Pubitemid 40321763)
13. F.E. Lotrich, R.E. Ferrell, M. Rabinovitz, and B.G. Pollock Risk for depression during interferon-alpha treatment is affected by the serotonin transporter polymorphism Biol Psychiatry 65 2009 344 348
14. T.L. Awtry, J.G. Frank, and L.L. Werling In vitro regulation of serotonin transporter activity by protein kinase A and nicotinic acetylcholine receptors in the prefrontal cortex of rats Synapse 59 2006 342 349
15. S. Ramamoorthy, D.J. Samuvel, E.R. Buck, G. Rudnick, and L.D. Jayanthi Phosphorylation of threonine residue 276 is required for acute regulation of serotonin transporter by cyclic GMP J Biol Chem 282 2007 11639 11647 (Pubitemid 47100698)
16. L.D. Jayanthi, D.J. Samuvel, R.D. Blakely, and S. Ramamoorthy Evidence for biphasic effects of protein kinase C on serotonin transporter function, endocytosis, and phosphorylation Mol Pharmacol 67 2005 2077 2087 (Pubitemid 41007790)
17. M.A. Ciccone, M. Timmons, A. Phillips, and M.W. Quick Calcium/calmodulin-dependent kinase II regulates the interaction between the serotonin transporter and syntaxin 1A Neuropharmacology 55 2008 763 770
18. L.D. Jayanthi, S. Ramamoorthy, V.B. Mahesh, F.H. Leibach, and V. Ganapathy Calmodulin-dependent regulation of the catalytic function of the human serotonin transporter in placental choriocarcinoma cells J Biol Chem 269 1994 14424 14429 (Pubitemid 24193993)
19. C.W. Tsao, Y.S. Lin, J.T. Cheng, C.F. Lin, H.T. Wu, and S.R. Wu Interferon-alpha-induced serotonin uptake in Jurkat T cells via mitogen-activated protein kinase and transcriptional regulation of the serotonin transporter J Psychopharmacol 22 2008 753 760
20. D.J. Samuvel, L.D. Jayanthi, N.R. Bhat, and S. Ramamoorthy A role for p38 mitogen-activated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression J Neurosci 25 2005 29 41 (Pubitemid 40110763)
21. M. Caraglia, M. Marra, G. Pelaia, R. Maselli, M. Caputi, and S.A. Marsico Alpha-interferon and its effects on signal transduction pathways J Cell Physiol 202 2005 323 335 (Pubitemid 40041303)
22. A. Takaoka, and H. Yanai Interferon signalling network in innate defence Cell Microbiol 8 2006 907 922 (Pubitemid 43670834)
23. K.C. Goh, S.J. Haque, and B.R. Williams p38 MAP kinase is required for STAT1 serine phosphorylation and transcriptional activation induced by interferons EMBO J 18 1999 5601 5608 (Pubitemid 29486379)
24. V.C. Blank, C. Pena, and L.P. Roguin STAT1, STAT3 and p38MAPK are involved in the apoptotic effect induced by a chimeric cyclic interferon-alpha2b peptide Exp Cell Res 316 2009 603 614
25. K. Inamura, Y. Matsuzaki, N. Uematsu, A. Honda, N. Tanaka, and K. Uchida Rapid inhibition of MAPK signaling and anti-proliferation effect via JAK/STAT signaling by interferon-alpha in hepatocellular carcinoma cell lines Biochim Biophys Acta 30 2005 401 410 (Pubitemid 41330793)
26. 2+ and CaMKII for Stat1 Ser-727 phosphorylation in response to IFN-gamma Proc Natl Acad Sci USA 99 2002 5971 5976 (Pubitemid 34493249)
27. L. Wang, I. Tassiulas, K.H. Park-Min, A.C. Reid, H. Gil-Henn, and J. Schlessinger 'Tuning' of type I interferon-induced Jak-STAT1 signaling by calcium-dependent kinases in macrophages Nat Immunol 9 2008 186 193
28. E.L. Riddle, K.S. Rau, M.K. Topham, G.R. Hanson, and A.E. Fleckenstein Ceramide-induced alterations in dopamine transporter function Eur J Pharmacol 458 2003 31 36 (Pubitemid 36050698)
29. M. Jafurulla, T.J. Pucadyil, and A. Chattopadhyay Effect of sphingomyelinase treatment on ligand binding activity of human serotonin1A receptors Biochim Biophys Acta 10 2008 2022 2025
30. C. Maziere, M.A. Conte, and J.C. Maziere Activation of the JAK/STAT pathway by ceramide in cultured human fibroblasts FEBS Lett 507 2001 163 168 (Pubitemid 33001535)
31. N. Muller, and M.J. Schwarz The immune-mediated alteration of serotonin and glutamate: towards an integrated view of depression Mol Psychiatry 12 2007 988 1000 (Pubitemid 350006207)
32. R. De La Garza II, and G.M. Asnis The non-steroidal anti-inflammatory drug diclofenac sodium attenuates IFN-alpha induced alterations to monoamine turnover in prefrontal cortex and hippocampus Brain Res 977 2003 70 79 (Pubitemid 36638695)
33. M. Sandrini, G. Vitale, and L.A. Pini Effect of rofecoxib on nociception and the serotonin system in the rat brain Inflamm Res 51 2002 154 159 (Pubitemid 34297854)
34. K.P. Su, S.Y. Huang, C.Y. Peng, H.C. Lai, C.L. Huang, and Y.C. Chen Phospholipase A2 and cyclooxygenase 2 genes influence the risk of interferon-alpha-induced depression by regulating polyunsaturated fatty acids levels Biol Psychiatry 67 2010 550 557
35. K.K. Reddy, B. Lefkove, L.B. Chen, B. Govindarajan, A. Carracedo, and G. Velasco The antidepressant sertraline downregulates Akt and has activity against melanoma cells Pigment Cell Melanoma Res 21 2008 451 456 (Pubitemid 351990972)
36. S. Tanemura, H. Momose, N. Shimizu, D. Kitagawa, J. Seo, and T. Yamasaki Blockage by SP600125 of Fcepsilon receptor-induced degranulation and cytokine gene expression in mast cells is mediated through inhibition of phosphatidylinositol 3-kinase signalling pathway J Biochem 145 2009 345 354
37. J. Lee, H.H. Jung, Y.H. Im, J.H. Kim, J.O. Park, and K. Kin Interferon-alpha resistance can be reversed by inhibition of IFN-alpha-induced COX-2 expression potentially via STAT1 activation in A549 cells Oncol Rep 15 2006 1541 1549
38. L. Chen, Y. He, H. Huang, H. Liao, and W. Wei Selective COX-2 inhibitor celecoxib combined with EGFR-TKI ZD1839 on non-small cell lung cancer cell lines: in vitro toxicity and mechanism study Med Oncol 25 2008 161 171
39. S. Guruswamy, and C.V. Rao Synergistic effects of lovastatin and celecoxib on caveolin-1 and its down-stream signaling molecules: implications for colon cancer prevention Int J Oncol 35 2009 1037 1043
40. S. Ramamoorthy, A.L. Bauman, K.R. Moore, H. Han, T. Yang-Feng, and A.S. Chang Antidepressant- and cocaine-sensitive human serotonin transporter: molecular cloning, expression, and chromosomal localization Proc Natl Acad Sci USA 90 1993 2542 2546 (Pubitemid 23078664)
41. A. Gladkevich, H.F. Kauffman, and J. Korf Lymphocytes as a neural probe: potential for studying psychiatric disorders Prog Neuropsychopharmacol Biol Psychiatry 28 2004 559 576 (Pubitemid 38490769)
42. J.A. Steiner, A.M. Carneiro, and R.D. Blakely Going with the flow: trafficking-dependent and -independent regulation of serotonin transport Traffic 9 2008 1393 1402
43. J. Bergquist, A. Tarkowski, R. Ekman, and A. Ewing Discovery of endogenous catecholamines in lymphocytes and evidence for catecholamine regulation of lymphocyte function via an autocrine loop Proc Natl Acad Sci USA 91 1994 12912 12916
44. Z. Fisar, and J. Raboch Depression, antidepressants, and peripheral blood components Neuro Endocrinol Lett 29 2008 17 28
45. A.H. Miller Depression and immunity: a role for T cells? Brain Behav Immun 24 2009 1 8
46. C.L. Raison, A.S. Borisov, M. Majer, D.F. Drake, G. Pagnoni, and B.J. Woolwine Activation of central nervous system inflammatory pathways by interferon-alpha: relationship to monoamines and depression Biol Psychiatry 65 2009 296 303
47. C.W. Tsao, Y.S. Lin, C.C. Chen, C.H. Bai, and S.R. Wu Cytokines and serotonin transporter in patients with major depression Prog Neuropsychopharmacol Biol Psychiatry 30 2006 899 905
48. C.W. Tsao, Y.S. Lin, J.T. Cheng, W.W. Chang, C.L. Chen, and S.R. Wu Serotonin transporter mRNA expression is decreased by lamivudine and ribavirin and increased by interferon in immune cells Scand J Immunol 63 2006 106 115
49. S. Agarwal, C. Achari, D. Praveen, K.R. Roy, G.V. Reddy, and P. Reddanna Inhibition of 12-LOX and COX-2 reduces the proliferation of human epidermoid carcinoma cells (A431) by modulating the ERK and PI3K-Akt signalling pathways Exp Dermatol 18 2009 939 946
50. S. Shishodia, D. Koul, and B.B. Aggarwal Cyclooxygenase (COX)-2 inhibitor celecoxib abrogates TNF-induced NF-kappa B activation through inhibition of activation of I kappa B alpha kinase and Akt in human non-small cell lung carcinoma: correlation with suppression of COX-2 synthesis J Immunol 173 2004 2011 2022 (Pubitemid 38971638)
51. S.K. Kim, K.H. Ahn, J.E. Ji, J.M. Choi, H.J. Jeon, and S.Y. Jung Neutral sphingomyelinase 2 induces dopamine uptake through regulation of intracellular calcium Cell Signal 22 2010 865 870
52. J. Kornhuber, M. Reichel, P. Tripal, T.W. Groemer, A.W. Henkel, and C. Muhle The role of ceramide in major depressive disorder Eur Arch Psychiatry Clin Neurosci 259 2009 S199 S204
53. J. Kornhuber, P. Tripal, M. Reichel, C. Muhle, C. Rhein, and M. Muehlbacher Functional Inhibitors of Acid Sphingomyelinase (FIASMAs): a novel pharmacological group of drugs with broad clinical applications Cell Physiol Biochem 26 2010 9 20
54. P. Casolini, A. Catalani, A.R. Zuena, and L. Angelucci Inhibition of COX-2 reduces the age-dependent increase of hippocampal inflammatory markers, corticosterone secretion, and behavioral impairments in the rat J Neurosci Res 68 2002 337 343 (Pubitemid 34462539)
55. F. Hu, X. Wang, T.W. Pace, H. Wu, and A.H. Miller Inhibition of COX-2 by celecoxib enhances glucocorticoid receptor function Mol Psychiatry 10 2005 426 428
56. N. Muller, M.J. Schwarz, S. Dehning, A. Douhe, A. Cerovecki, and B. Goldstein-Muller (2006) The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine Mol Psychiatry 11 2006 680 684 (Pubitemid 43989814)
57. J. Mendlewicz, P. Kriwin, P. Oswald, D. Souery, S. Alboni, and N. Brunello Shortened onset of action of antidepressants in major depression using acetylsalicylic acid augmentation: a pilot open-label study Int Clin Psychopharmacol 21 2006 227 231 (Pubitemid 43740300)
58. R. Newton, L. Hart, K.F. Chung, and P.J. Barnes Ceramide induction of COX-2 and PGE(2) in pulmonary A549 cells does not involve activation of NF-kappaB Biochem Biophys Res Commun 277 2000 675 679
59. S. Schutze, K. Wiegmann, T. Machleidt, and M. Kronke TNF-induced activation of NF-kappa B Immunobiology 193 1995 193 203
60. K. Kuno, K. Sukegawa, Y. Ishikawa, T. Orii, and K. Matsushima Acid sphingomyelinase is not essential for the IL-1 and tumor necrosis factor receptor signaling pathway leading to NFkB activation Int Immunol 6 1994 1269 1272 (Pubitemid 24254132)
61. C.C. Chen, Y.T. Sun, J.J. Chen, and Y.J. Chang Tumor necrosis factor-alpha-induced cyclooxygenase-2 expression via sequential activation of ceramide-dependent mitogen-activated protein kinases, and IkappaB kinase 1/2 in human alveolar epithelial cells Mol Pharmacol 59 2001 493 500
62. B.C. Chen, H.M. Chang, M.J. Hsu, C.M. Shih, Y.H. Chiu, and W.T. Chiu Peptidoglycan induces cyclooxygenase-2 expression in macrophages by activating the neutral sphingomyelinase-ceramide pathway J Biol Chem 284 2009 20562 20573
63. M. Funakoshi-Tago, T. Shimizu, K. Tago, M. Nakamura, H. Itoh, and Y. Sonoda Celecoxib potently inhibits TNFalpha-induced nuclear translocation and activation of NF-kappaB Biochem Pharmacol 76 2008 662 671
64. M. David, E. Petricoin III, C. Benjamin, R. Pine, M.J. Weber, and A.C. Larner Requirement for MAP kinase (ERK2) activity in interferon alpha- and interferon beta-stimulated gene expression through STAT proteins Science 269 1995 1721 1723
65. S.A. Douglas, and S.J. Bunn Interferon-alpha signalling in bovine adrenal chromaffin cells: involvement of signal-transducer and activator of transcription 1 and 2, extracellular signal-regulated protein kinases 1/2 and serine 31 phosphorylation of tyrosine hydroxylase J Neuroendocrinol 21 2009 200 207
66. R. Iceta, J.E. Mesonero, and A.I. Alcalde Effect of long-term fluoxetine treatment on the human serotonin transporter in Caco-2 cells Life Sci 80 2007 1517 1524 (Pubitemid 46399752)
67. P. Schloss, and D.C. Williams The serotonin transporter: a primary target for antidepressant drugs J Psychopharmacol 12 1998 115 121 (Pubitemid 28312567)
68. S. Benmansour, M. Cecchi, D.A. Morilak, G.A. Gerhardt, M.A. Javors, and G.G. Gould Effects of chronic antidepressant treatments on serotonin transporter function, density, and mRNA level J Neurosci 19 1999 10494 10501 (Pubitemid 30228055)
69. S. Benmansour, W.A. Owens, M. Cecchi, D.A. Morilak, and A. Frazer Serotonin clearance in vivo is altered to a greater extent by antidepressant-induced downregulation of the serotonin transporter than by acute blockade of this transporter J Neurosci 22 2002 6766 6772 (Pubitemid 35386433)
70. D.A. Johnson, C.D. Ingram, E.J. Grant, M. Craighead, and S.E. Gartside Glucocorticoid receptor antagonism augments fluoxetine-induced downregulation of the 5-HT transporter Neuropsychopharmacology 34 2009 399 409
71. F. Fumagalli, R. Molteni, F. Calabrese, A. Frasca, G. Racagni, and M.A. Riva Chronic fluoxetine administration inhibits extracellular signal-regulated kinase 1/2 phosphorylation in rat brain J Neurochem 93 2005 1551 1560 (Pubitemid 40853278)
72. H. Einat, P. Yuan, T.D. Gould, J. Li, J. Du, and L. Zhang The role of the extracellular signal-regulated kinase signaling pathway in mood modulation J Neurosci 23 2003 7311 7316 (Pubitemid 36999520)
73. X. Li, W. Zhu, M.S. Roh, A.B. Friedman, K. Rosborough, and R.S. Jope In vivo regulation of glycogen synthase kinase-3beta (GSK3beta) by serotonergic activity in mouse brain Neuropsychopharmacology 29 2004 1426 1431 (Pubitemid 38982234)