Dexamethasone protects human fibroblasts from apoptosis via an S1P3-receptor subtype dependent activation of PKB/Akt and BclXL

Pharmacological Research

Volumn 61, Issue 5, 2010, Pages 449-459

  Nieuwenhuis, Barbara ^a   Lüth, Anja ^a   Kleuser, Burkhard ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF POTSDAM   (Germany)

Author keywords

Akt signalling; Bcl 2 family; Glucocorticoids; Programmed cell death; S1P receptors; Sphingosine 1 phosphate

Indexed keywords

CASPASE 3; CASPASE 7; DEXAMETHASONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL XL; PROTEIN KINASE B; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

ADOLESCENT; APOPTOSIS; ARTICLE; CELL ISOLATION; CELL PROTECTION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; FIBROBLAST; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; JUVENILE; MITOCHONDRIAL MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; BCL-X PROTEIN; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CELLS, CULTURED; DEXAMETHASONE; FIBROBLASTS; HUMANS; MEMBRANE POTENTIALS; MITOCHONDRIAL MEMBRANES; ONCOGENE PROTEIN V-AKT; PROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, LYSOSPHINGOLIPID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77950629530     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2009.12.005     Document Type: Article

References (58)

1. Schoepe S., Schacke H., May E., Asadullah K. Glucocorticoid therapy-induced skin atrophy. Exp Dermatol 2006, 15:406-420.
2. Hammer S., Sauer B., Spika I., Schraut C., Kleuser B., Schafer-Korting M. Glucocorticoids mediate differential anti-apoptotic effects in human fibroblasts and keratinocytes via sphingosine-1-phosphate formation. J Cell Biochem 2004, 91:840-851.
3. Amsterdam A., Tajima K., Sasson R. Cell-specific regulation of apoptosis by glucocorticoids: implication to their anti-inflammatory action. Biochem Pharmacol 2002, 64:843-850.
4. Davis M.C., McColl K.S., Zhong F., Wang Z., Malone M.H., Distelhorst C.W. Dexamethasone-induced inositol 1,4,5-trisphosphate receptor elevation in murine lymphoma cells is not required for dexamethasone-mediated calcium elevation and apoptosis. J Biol Chem 2008, 283:10357-10365.
5. Schmidt M., Pauels H.G., Lugering N., Lugering L., Domschke W., Kucharzik T. Glucocorticoids induce apoptosis in human monocytes: potential role of IL-1 beta. J Immunol 1999, 163:3484-3490.
6. Bailly-Maitre B., de Sousa G., Zucchini N., Gugenheim J., Boulukos K.E., Rahmani R. Spontaneous apoptosis in primary cultures of human and rat hepatocytes: molecular mechanisms and regulation by dexamethasone. Cell Death Differ 2002, 9:945-955.
7. Herr I., Gassler N., Friess H., Buchler M.W. Regulation of differential pro- and anti-apoptotic signaling by glucocorticoids. Apoptosis 2007, 12:271-291.
8. Newton C.J., Xie Y.X., Burgoyne C.H., Adams I., Atkin S.L., Abidia A., et al. Fluvastatin induces apoptosis of vascular endothelial cells: blockade by glucocorticoids. Cardiovasc Surg 2003, 11:52-60.
9. Spiegel S., Milstien S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 2003, 4:397-407.
10. Japtok L., Kleuser B. The role of sphingosine-1-phosphate receptor modulators in the prevention of transplant rejection and autoimmune diseases. Curr Opin Investig Drugs 2009, 10:1183-1194.
11. Takabe K., Paugh S.W., Milstien S., Spiegel S. " Inside-out" signaling of sphingosine-1-phosphate: therapeutic targets. Pharmacol Rev 2008, 60:181-195.
12. Goetzl E.J., Wang W., McGiffert C., Liao J.J., Huang M.C. Sphingosine 1-phosphate as an intracellular messenger and extracellular mediator in immunity. Acta Paediatr Suppl 2007, 96:49-52.
13. Keller C.D., Rivera Gil P., Tolle M., van der Giet M., Chun J., Radeke H.H., et al. Immunomodulator FTY720 induces myofibroblast differentiation via the lysophospholipid receptor S1P3 and Smad3 signaling. Am J Pathol 2007, 170:281-292.
14. Nieuwenhuis B., Luth A., Chun J., Huwiler A., Pfeilschifter J., Schafer-Korting M., et al. Involvement of the ABC-transporter ABCC1 and the sphingosine 1-phosphate receptor subtype S1P(3) in the cytoprotection of human fibroblasts by the glucocorticoid dexamethasone. J Mol Med 2009, 87:645-657.
15. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2002, 2:489-501.
16. Wymann M.P., Zvelebil M., Laffargue M. Phosphoinositide 3-kinase signalling-which way to target?. Trends Pharmacol Sci 2003, 24:366-376.
17. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three Akts. Genes Dev 1999, 13:2905-2927.
18. Nicholson K.M., Anderson N.G. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 2002, 14:381-395.
19. Haake S.M., Dinh C.T., Chen S., Eshraghi A.A., Van De Water T.R. Dexamethasone protects auditory hair cells against TNFalpha-initiated apoptosis via activation of PI3K/Akt and NFkappaB signaling. Hear Res 2009, 255:22-32.
20. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997, 275:1132-1136.
21. Finucane D.M., Bossy-Wetzel E., Waterhouse N.J., Cotter T.G., Green D.R. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J Biol Chem 1999, 274:2225-2233.
22. Ishii I., Friedman B., Ye X., Kawamura S., McGiffert C., Contos J.J., et al. Selective loss of sphingosine 1-phosphate signaling with no obvious phenotypic abnormality in mice lacking its G protein-coupled receptor, LP(B3)/EDG-3. J Biol Chem 2001, 276:33697-33704.
23. Manggau M., Kim D.S., Ruwisch L., Vogler R., Korting H.C., Schafer-Korting M., et al. 1Alpha,25-dihydroxyvitamin D3 protects human keratinocytes from apoptosis by the formation of sphingosine-1-phosphate. J Invest Dermatol 2001, 117:1241-1249.
24. Baud V., Karin M. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 2001, 11:372-377.
25. Fraschini A., Bottone M.G., Scovassi A.I., Denegri M., Risueno M.C., Testillano P.S., et al. Changes in extranucleolar transcription during actinomycin D-induced apoptosis. Histol Histopathol 2005, 20:107-117.
26. Fieber C.B., Eldridge J., Taha T.A., Obeid L.M., Muise-Helmericks R.C. Modulation of total Akt kinase by increased expression of a single isoform: requirement of the sphingosine-1-phosphate receptor, Edg3/S1P3, for the VEGF-dependent expression of Akt3 in primary endothelial cells. Exp Cell Res 2006, 312:1164-1173.
27. Schutze S., Schneider-Brachert W. Impact of TNF-R1 and CD95 internalization on apoptotic and antiapoptotic signaling. Results Probl Cell Differ 2009, [epub ahead of print].
28. McNicol A., Jackson E.C. Inhibition of the MEK/ERK pathway has no effect on agonist-induced aggregation of human platelets. Biochem Pharmacol 2003, 65:1243-1250.
29. Parameswaran N., Spielman W.S., Brooks D.P., Nambi P. SB203580 reverses adrenomedullin's effect on proliferation and apoptosis in cultured mesangial cells. Eur J Pharmacol 1999, 371:75-82.
30. Bellis A., Castaldo D., Trimarco V., Monti, Chivasso P., Sadoshima J., et al. Cross-talk between PKA and Akt protects endothelial cells from apoptosis in the late ischemic preconditioning. Arterioscler Thromb Vasc Biol 2009, 29:1207-1212.
31. Bogoyevitch M.A., Arthur P.G. Inhibitors of c-Jun N-terminal kinases: JuNK no more?. Biochim Biophys Acta 2008, 1784:76-93.
32. Wanke I., Schwarz M., Buchmann A. Insulin and dexamethasone inhibit TGF-beta-induced apoptosis of hepatoma cells upstream of the caspase activation cascade. Toxicology 2004, 204:141-154.
33. Kizildag S., Ates H., Kizildag S. Treatment of K562 cells with 1,25-dihydroxyvitamin D(3) induces distinct alterations in the expression of apoptosis-related genes BCL2, BAX, BCL(XL), and p21. Ann Hematol 2009, [epub ahead of print].
34. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol 1998, 10:262-267.
35. Vogt P.K., Gymnopoulos M., Hart J.R. PI 3-kinase and cancer: changing accents. Curr Opin Genet Dev 2009, 19:12-17.
36. Burgering B.M., Coffer P.J. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 1995, 376:599-602.
37. Franke T.F., Yang S.I., Chan T.O., Datta K., Kazlauskas A., Morrison D.K., et al. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 1995, 81:727-736.
38. Carnero A., Blanco-Aparicio C., Renner O., Link W., Leal J.F. The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr Cancer Drug Targets 2008, 8:187-198.
39. Kok K., Geering B., Vanhaesebroeck B. Regulation of phosphoinositide 3-kinase expression in health and disease. Trends Biochem Sci 2009, 34:115-127.
40. Saffar A.S., Dragon S., Ezzati P., Shan L., Gounni A.S. Phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase regulate induction of Mcl-1 and survival in glucocorticoid-treated human neutrophils. J Allergy Clin Immunol 2008, 121:492-498.
41. Vanhaesebroeck B., Leevers S.J., Ahmadi K., Timms J., Katso R., Driscoll P.C., et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001, 70:535-602.
42. Buttgereit F., Scheffold A. Rapid glucocorticoid effects on immune cells. Steroids 2002, 67:529-534.
43. Merry W.H., Caplan R.H., Wickus G.G., Reynertson R.H., Kisken W.A., Cogbill T.A., et al. Postoperative acute adrenal failure caused by transient corticotropin deficiency. Surgery 1994, 116:1095-1100.
44. Buckingham J.C. Fifteenth Gaddum Memorial Lecture December 1994. Stress and the neuroendocrine-immune axis: the pivotal role of glucocorticoids and lipocortin 1. Br J Pharmacol 1996, 118:1-19.
45. Boldizsar F., Talaber G., Szabo M., Bartis D., Palinkas L., Nemeth P., et al. Emerging pathways of non-genomic glucocorticoid (GC) signalling in T cells. Immunobiology 2009, [epub ahead of print].
46. Kim J.H., Go H.Y., Jin D.H., Kim H.P., Hong M.H., Chung W.Y., et al. Inhibition of the PI3K-Akt/PKB survival pathway enhanced an ethanol extract of Rhus verniciflua Stokes-induced apoptosis via a mitochondrial pathway in AGS gastric cancer cell lines. Cancer Lett 2008, 265:197-205.
47. Zhao T., Adams M.H., Zou S.P., El-Hage N., Hauser K.F., Knapp P.E. Silencing the PTEN gene is protective against neuronal death induced by human immunodeficiency virus type 1 Tat. J Neurovirol 2007, 13:97-106.
48. Wang Y., Zhang B., Peng X., Perpetua M., Harbrecht B.G. Bcl-xL prevents staurosporine-induced hepatocyte apoptosis by restoring protein kinase B/mitogen-activated protein kinase activity and mitochondria integrity. J Cell Physiol 2008, 215:676-683.
49. Means C.K., Xiao C.Y., Li Z., Zhang T., Omens J.H., Ishii I., et al. Sphingosine 1-phosphate S1P2 and S1P3 receptor-mediated Akt activation protects against in vivo myocardial ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2007, 292:H2944-H2951.
50. Tran N.L., McDonough W.S., Savitch B.A., Sawyer T.F., Winkles J.A., Berens M.E. The tumor necrosis factor-like weak inducer of apoptosis (TWEAK)-fibroblast growth factor-inducible 14 (Fn14) signaling system regulates glioma cell survival via NFkappaB pathway activation and BCL-XL/BCL-W expression. J Biol Chem 2005, 280:3483-3492.
51. Spender L.C., O'Brien D.I., Simpson D., Dutt D., Gregory C.D., Allday M.J., et al. TGF-beta induces apoptosis in human B cells by transcriptional regulation of BIK and BCL-XL. Cell Death Differ 2009, 16:593-602.
52. Qian Y.H., Xiao Q., Chen H., Xu J. Dexamethasone inhibits camptothecin-induced apoptosis in C6-glioma via activation of Stat5/Bcl-xL pathway. Biochim Biophys Acta 2009, 1793:764-771.
53. Kim B.M., Choi Y.J., Han Y., Yun Y.S., Hong S.H. N,N-dimethyl phytosphingosine induces caspase-8-dependent cytochrome c release and apoptosis through ROS generation in human leukemia cells. Toxicol Appl Pharmacol 2009, 239:87-97.
54. Goetzl E.J., Kong Y., Mei B. Lysophosphatidic acid and sphingosine 1-phosphate protection of T cells from apoptosis in association with suppression of Bax. J Immunol 1999, 162:2049-2056.
55. Dykens J.A., Simpkins J.W., Wang J., Gordon K. Polycyclic phenols, estrogens and neuroprotection: a proposed mitochondrial mechanism. Exp Gerontol 2003, 38:101-107.
56. Tharakan B., Corprew R., Hunter F.A., Whaley J.G., Smythe W.R., Childs E.W. 17beta-estradiol mediates protection against microvascular endothelial cell hyperpermeability. Am J Surg 2009, 197:147-154.
57. Simpkins J.W., Yi K.D., Yang S., Dykens J.A. Mitochondrial mechanisms of estrogen neuroprotection. Biochim Biophys Acta 2009, [epub ahead of print].
58. Li Y., Wu H., Khardori R., Song Y.H., Lu Y.W., Geng Y.J. Insulin-like growth factor-1 receptor activation prevents high glucose-induced mitochondrial dysfunction, cytochrome-c release and apoptosis. Biochem Biophys Res Commun 2009, 384:259-264.