Acid sphingomyelinase-ceramide system mediates effects of antidepressant drugs

Nature Medicine

Volumn 19, Issue 7, 2013, Pages 934-938

  Gulbins, Erich ^a,b   Palmada, Monica ^a   Reichel, Martin ^c   Lüth, Anja ^d   Böhmer, Christoph ^a   Amato, Davide ^c   Müller, Christian P ^c   Tischbirek, Carsten H ^c   Groemer, Teja W ^c   Tabatabai, Ghazaleh ^e,f   Becker, Katrin A ^a   Tripal, Philipp ^c   Staedtler, Sven ^c   Ackermann, Teresa F ^g   Van Brederode, Johannes ^c   Alzheimer, Christian ^c   Weller, Michael ^e   Lang, Undine E ^h   Kleuser, Burkhard ^d   Grassmé, Heike ^a   Kornhuber, Johannes ^c   more..

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b UNIVERSITY OF CINCINNATI   (United States)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d UNIVERSITY OF POTSDAM   (Germany)

^e UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^f Neuroscience Center Zurich and Division of Neurosurgery   (Switzerland)

^g UNIVERSITY OF TÜBINGEN   (Germany)

^h UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMITRIPTYLINE; ANTIDEPRESSANT AGENT; CERAMIDE; FLUOXETINE; SPHINGOMYELIN PHOSPHODIESTERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN LEVEL; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; HIPPOCAMPUS; MOUSE; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIDEPRESSIVE AGENTS; CAENORHABDITIS ELEGANS; CELLS, CULTURED; CERAMIDES; DEPRESSIVE DISORDER, MAJOR; EMBRYO, MAMMALIAN; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE;

MUS;

EID: 84880269973     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3214     Document Type: Article

References (38)

1. Belmaker, R.H. & Agam, G. Major depressive disorder. N. Engl. J. Med. 358, 55-68 (2008).
2. Howren, M.B., Lamkin, D.M. & Suls, J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 71, 171-186 (2009).
3. Dowlati, Y. et al. A meta-analysis of cytokines in major depression. Biol. Psychiatry 67, 446-457 (2010).
4. Krishnan, V. & Nestler, E.J. The molecular neurobiology of depression. Nature 455, 894-902 (2008).
5. Brink, C.B., Harvey, B.H. & Brand, L. Tianeptine: a novel atypical antidepressant that may provide new insights into the biomolecular basis of depression. Recent Pat. CNS Drug Discov. 1, 29-41 (2006).
6. Santarelli, L. et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809 (2003).
7. Koo, J.W. & Duman, R.S. IL-1ß is an essential mediator of the antineurogenic and anhedonic effects of stress. Proc. Natl. Acad. Sci. USA 105, 751-756 (2008).
8. David, D.J. et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493 (2009).
9. Warner-Schmidt, J.L. & Duman, R.S. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16, 239-249 (2006).
10. Gulbins, E. & Kolesnick, R. Raft ceramide in molecular medicine. Oncogene 22, 7070-7077 (2003).
11. Grassmé, H. et al. CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 276, 20589-20596 (2001).
12. Perrotta, C. et al. Syntaxin 4 is required for acid sphingomyelinase activity and apoptotic function. J. Biol. Chem. 285, 40240-40251 (2010).
13. Grassmé, H. et al. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 9, 322-330 (2003).
14. Baumann, P. et al. The AGNP-TDM Expert Group Consensus Guidelines: focus on therapeutic monitoring of antidepressants. Dialogues Clin. Neurosci. 7, 231-247 (2005).
15. Kölzer, M., Werth, N. & Sandhoff, K. Interactions of acid sphingomyelinase and lipid bilayers in the presence of the tricyclic antidepressant desipramine. FEBS Lett. 559, 96-98 (2004).
16. Kornhuber, J. et al. Identification of new functional inhibitors of acid sphingomyelinase using a structure-property-activity relation model. J. Med. Chem. 51, 219-237 (2008).
17. Ranganathan, R., Sawin, E.R., Trent, C. & Horvitz, H.R. Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine. J. Neurosci. 21, 5871-5884 (2001).
18. Dempsey, C.M., Mackenzie, S.M., Gargus, A., Blanco, G. & Sze, J.Y. Serotonin (5HT), fluoxetine, imipramine and dopamine target distinct 5HT receptor signaling to modulate Caenorhabditis elegans egg-laying behavior. Genetics 169, 1425-1436 (2005).
19. De Stefanis, D. et al. Increase in ceramide level alters the lysosomal targeting of cathepsin D prior to onset of apoptosis in HT-29 colon cancer cells. Biol. Chem. 383, 989-999 (2002).
20. Hisaki, H. et al. In vivo influence of ceramide accumulation induced by treatment with a glucosylceramide synthase inhibitor on ischemic neuronal cell death. Brain Res. 1018, 73-77 (2004).
21. Peltier, J., O'Neill, A. & Schaffer, D.V. PI3K and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev. Neurobiol. 67, 1348-1361 (2007).
22. Zhang, Y., Li, X., Carpinteiro, A. & Gulbins, E. Acid sphingomyelinase amplifies redox signaling in Pseudomonas aeruginosa-induced macrophage apoptosis. J. Immunol. 181, 4247-4254 (2008).
23. Mathias, S. et al. Activation of the sphingomyelin signaling pathway in intact EL4 cells and in a cell-free system by IL-1 ß. Science 259, 519-522 (1993).
24. Wiegmann, K., Schütze, S., Machleidt, T., Witte, D. & Krönke, M. Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell 78, 1005-1015 (1994).
25. Kim, M.Y., Linardic, C., Obeid, L. & Hannun, Y. Identification of sphingomyelin turnover as an effector mechanism for the action of tumor necrosis factor a and -interferon. Specific role in cell differentiation. J. Biol. Chem. 266, 484-489 (1991).
26. Brenner, B. et al. Fas-or ceramide-induced apoptosis is mediated by a Rac1-regulated activation of Jun N-terminal kinase/p38 kinases and GADD153. J. Biol. Chem. 272, 22173-22181 (1997).
27. Lepple-Wienhues, A. et al. Stimulation of CD95 (Fas) blocks T lymphocyte calcium channels through sphingomyelinase and sphingolipids. Proc. Natl. Acad. Sci. USA 96, 13795-13800 (1999).
28. Müller, N. COX-2 inhibitors as antidepressants and antipsychotics: clinical evidence. Curr. Opin. Investig. Drugs 11, 31-42 (2010).
29. Walker, J.R. et al. Psychiatric disorders in patients with immune-mediated inflammatory diseases: prevalence, association with disease activity, and overall patient well-being. J. Rheumatol. Suppl. 88, 31-35 (2011).
30. Rudisch, B. & Nemeroff, C.B. Epidemiology of comorbid coronary artery disease and depression. Biol. Psychiatry 54, 227-240 (2003).
31. Kojima, M. et al. Depression, inflammation, and pain in patients with rheumatoid arthritis. Arthritis Rheum. 61, 1018-1024 (2009).
32. Tabas, I. Sphingolipids and atherosclerosis: a mechanistic connection? A therapeutic opportunity? Circulation 110, 3400-3401 (2004).
33. Kornhuber, J. et al. High activity of acid sphingomyelinase in major depression. J. Neural Transm. 112, 1583-1590 (2005).
34. Horinouchi, K. et al. Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10, 288-293 (1995).
35. Lozano, J. et al. Niemann-Pick disease versus acid sphingomyelinase deficiency. Cell Death Differ. 8, 100-103 (2001).
36. Lakso, M. et al. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc. Natl. Acad. Sci. USA 93, 5860-5865 (1996).
37. Amato, D., Müller, C.P. & Badiani, A. Increased drinking after intra-striatal injection of the dopamine D2/D3 receptor agonist quinpirole in the rat. Psychopharmacology (Berl.) 223, 457-463 (2012).
38. Franklin, K.B.J. & Paxinos, G. The Mouse Brain in Stereotaxic Coordinates 3rd edn., Figure 48 (Academic Press, San Diego, 2007).