Nerve growth factor-induced protein kinase C stimulation contribute to TrkA-dependent inhibition of p75 neurotrophin receptor sphingoliplid signaling

Journal of Neuroscience Research

Volumn 77, Issue 4, 2004, Pages 465-474

  Plo, Isabelle ^a,c   Bono, F ^b   Bezombes, C ^a   Alam, A ^b   Bruno, A ^a   Laurent, G ^a  

^a INSTITUT CLAUDIUS REGAUD   (France)

^b SANOFI   (France)

^c INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

Ceramide; NGF; PI3K; PKC; TrkA

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 2 MORPHOLINO 8 PHENYLCHROMONE; CERAMIDE; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR; PHORBOL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE C; PROTEIN P75; SPHINGOLIPID; SPHINGOMYELIN PHOSPHODIESTERASE;

APOPTOSIS; ARTICLE; CELL LABELING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL LINE, TUMOR; CERAMIDES; FEEDBACK, BIOCHEMICAL; HUMANS; NERVE GROWTH FACTOR; NEURONS; PHORBOL ESTERS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR; SIGNAL TRANSDUCTION; SPHINGOLIPIDS;

EID: 3442886198     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20189     Document Type: Article

References (49)

1. Altin JG, Bradshaw RA. 1990. Production of 1,2-diacylglycerol in PC12 cells by nerve growth factor and basic fibroblast growth factor. J Neurochem 54:1666-1676.
2. Bae YS, Candey LG, Chen CS, Kim SR, Kwon KS, Rhee SG. 1998. Activation of phospholipase C-gamma by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 273:4465-4469.
3. Barrett GL. 2000. The p75 neurotrophin receptor and neuronal apoptosis. Prog Neurobiol 61:205-229.
4. Bezombes C, Segui B, Cuvillier O, Bruno AP, Uro-Coste E, Gouaze V, Andrieu-Abadie N, Carpentier S, Laurent G, Salvayre R, Jaffrezou JP, Levade T. 2001a. Lysosomal sphingomyelinase is not solicited for apoptosis signaling. FASEB J 15:297-299.
5. Bezombes C, Plo I, Mansat-De Mas V, Quillet-Mary A, Negre-Salvayre A, Laurent, G, Jaffrezou JP. 2001b. Oxidative stress-induced activation of Lyn recruits sphingomyelinase and is requisite for its stimulation by Ara-C. FASEB J 15:1583-1585.
6. Bilderback TR, Gazula VR, Lisanti MP, Dobrowsky RT. 1999. Caveolin interacts with Trk A and p75(NTR) and regulates neurotrophin signaling pathways. J Biol Chem 274:257-263.
7. Bilderback TR, Gazula VR, Dobrowsky RT. 2001. Phosphoinositide 3-kinase regulates crosstalk between Trk A tyrosine kinase and p75(NTR)-dependent sphingolipid signaling pathways. J Neurochem 76:1540-1551.
8. NTR receptor in a cell cycle-dependent manner. FEBS Lett 457:93-97.
9. Bourbon NA, Sandirasegarane L, Kester M. 2002. Ceramide-induced inhibition of Akt is mediated through protein kinase C zeta: implications for growth arrest. J Biol Chem 277:3286-3292.
10. Bourteele S, Hausser A, Doppler H, Hom-Muller J, Ropke C, Schwarzmann G, Pfizenmaier K. 1998. Tumor necrosis factor induces ceramide oscillations and negatively controls sphingolipid synthases by caspases in apoptotic Kym-1 cells. J Biol Chem 273:31245-31251.
11. Brann AB, Tcherpakov M, Williams IM, Futerman AH, Fainzilber M. 2002. NGF-induced p75-mediated death of cultured hippocampal neurons is age-dependent and transduced through ceramide generated by neutral sphingomyelinase. J Biol Chem 277:9812-9818.
12. Chmura SJ, Nodzenski E, Weichselbaum RR, Quintans J. 1996. Protein kinase C inhibition induces apoptosis and ceramide production through activation of a neutral sphingomyelinase. Cancer Res 56:2711-2714.
13. Dobrowsky RT, Carter BD. 1998. Coupling of the p75 neurotrophin receptor to sphingolipid signaling. Ann N Y Acad Sci 845:32-45.
14. Dobrowsky RT, Carter BD. 2000. p75 Neurotrophin receptor signaling: mechanisms for neurotrophic modulation of cell stress? J Neurosci Res 61:237-243.
15. Dobrowsky RT, Werner MH, Castellino AM, Chao MV, Hannun YA. 1994. Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 265:1596-1599.
16. NTR with Trk receptors. J Biol Chem 270:22135-22142.
17. Hama T, Huang KP, Guroff G. 1986. Protein kinase C as a component of a nerve growth factor-sensitive phosphorylation system in PC12 cells. Proc Natl Acad Sci USA 83:2353-2357.
18. Heasley LE, Johnson GL. 1989. Regulation of protein kinase C by nerve growth factor, epidermal growth factor, and phorbol esters in PC12 pheochromocytoma cells. J Biol Chem 264:8646-8652.
19. Huwiler A, Fabbro D, Pfeilschifter J. 1998. Selective ceramide binding to protein kinase C-alpha and -delta isoenzymes in renal mesangial cells. Biochemistry 37:14556-14562.
20. Jackson TR, Blader IJ, Hammonds-Odie LP, Burga CR, Cooke F, Hawkins PT, Wolf AG, Heldman KA, Theibert AB. 1996. Initiation and maintenance of NGF-stimulated neurite outgrowth requires activation of a phosphoinositide 3-kinase. J Cell Sci 109:289-300.
21. Jaffrezou JP, Levade T, Bettaib A, Andrieu N, Bezombes C, Maestre N, Vermeersch S, Rousse A, Laurent G. 1996. Daunorubicin-induced apoptosis: triggering of ceramide generation through sphingomyelin hydrolysis. EMBO J 15:2417-2424.
22. Jarvis WD, Fornari FA Jr, Browning JL, Gewirtz DA, Kolesnick RN, Grant S. 1994. Attenuation of ceramide-induced apoptosis by diglyceride in human myeloid leukemia cells. J Biol Chem 269:31685-31692.
23. Jung KM, Tan S, Landman N, Petrova K, Murray S, Lewis R, Kim PK, Kim DS, Ryu SH, Chao MV, Kim TW. 2003. Regulated intramembrane proteolysis of the p75 neurotrophin receptor modulates its association with the TrkA receptor. J Biol Chem 278:42161-42169.
24. Kanning KC, Hudson M, Amieux PS, Wiley JC, Bothwell M, Schecterson LC. 2003. Proteolytic processing of the p75 neurotrophin receptor and two homologs generates C-terminal fragments with signaling capability. J Neurosci 23:5425-5436.
25. Kaszkin M, Huwiler A, Scholz K, van den Bosch H, Pfeitschifter J. 1998. Negative regulation of interleukin-1beta-activated neutral sphingomyelinase by protein kinase C in rat mesangial cells. FEBS Lett 440:163-166.
26. Kowalski-Chauvel A, Pradayrol L, Vaysse N, Seva C. 1997. Tyrosine phosphorylation of insulin receptor substrate-1 and activation of the PI-3-kinase pathway by glycine-extended gastrin precursors. Biochem Biophys Res Commun 236:687-692.
27. Lee JY, Hannun YA, Obeid LM. 1996. Ceramide inactivates cellular protein kinase C alpha. J Biol Chem 271:13169-13174.
28. Li J, Wurtman RJ. 1999. Mechanisms whereby nerve growth factor increases diacylglycerol levels in differentiating PC12 cells. Brain Res 818:252-259.
29. Lievremont JP, Sciorati C, Morandi E, Paolucci C, Bunone G, Della Valle G, Meldolesi J, Clementi E. 1999. The p75 (NTR)-induced apoptotic program develops through a ceramide-caspase pathway negatively regulated by nitric oxide. J Biol Chem 274:15466-15472.
30. Liu B, Andrieu-Abadie N, Levade T, Zhang P, Obeid LM, Hannun YA. 1998. Glutathione regulation of neutral sphingomyelinase in tumor necrosis factor-alpha-induced cell death. J Biol Chem 273:11313-11320.
31. MacPhee I, Barker PA. 1999. Extended ceramide exposure activates the trkA receptor by increasing receptor homodimer formation. J Neurochem 72:1423-1430.
32. Mansat V, Laurent G, Levade T, Bettaieb A, Jaffrezou JP. 1997. The protein kinase C activators phorbol esters and phosphatidylserine inhibit neutral sphingomyelinase activation, ceramide generation, and apoptosis triggered by daunorubicin. Cancer Res 57:5300-5304.
33. Mansat-De Mas V, Bezombes C, Quillet-Mary A, Bettaieb A, D'Orgeix A, Laurent G, Jaffrezou JP. 1999. Implication of radical oxygen species in ceramide generation, c-Jun N-terminal kinase activation and apoptosis induced by daunorubicin. Mol Pharmacol 56:867-874.
34. Ming G, Song H, Berninger B, Inagaki N, Tessier-Lavigne M, Poo M. 1999. Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23:139-148.
35. Neri LM, Martelli AM, Borgatti P, Colamussi ML, Marchisio M, Capitani S. 1999. Increase in nuclear phosphatidylinositol 3-kinase activity and phosphatidylinositol(3,4,5)trisphosphate synthesis precede PKC-zeta translocation to the nucleus of NGF-treated PC12 cells. FASEB J 13:2299-2310.
36. Ohmichi M, Zhu G, Saltiel AR. 1993. Nerve growth factor activates calcium-insensitive protein kinase C- epsilon in PC-12 rat pheochromocytoma cells. Biochem J 295:767-772.
37. Paris F, Fuks Z, Kang A, Capodieci P, Juan G, Ehleiter D, Haimovitz-Friedman A, Cordon-Cardo C, Kolesnick R. 2001. Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 293:293-297.
38. Plo I, Lautier D, Casteran N, Dubreuil P, Arock M, Laurent G. 2001. Kit activation inhibits daunorubicin-induced sphingomyelin cycle and apoptosis through a phospholipase Cγ and protein kinase C-dependent mechanism. Oncogene 20:6752-6763.
39. Soderholm H, Olsson A, Lavenius E, Ronnstrand L, Nanberg E. 2001. Activation of Ras, Raf-1 and protein kinase C in differentiating human neuroblastoma cells after treatment with phorbol ester and NGF. Cell Signal 13:95-104.
40. Toker A. 2000. Protein kinases as mediators of phosphoinositide 3-kinase signaling. Mol Pharmacol 57:652-658.
41. Toker A, Meyer M, Reddy KK, Falck JR, Aneja R, Aneja S, Parra A, Burns DJ, Ballas LM, Cantley LC. 1994. Activation of protein kinase C family members by the novel polyphosphoinositides PtdIns-3,4-P2 and PtdIns-3,4,5-P3. J Biol Chem 269:32358-32367.
42. Torres M, Bogenmann E. 1996. Nerve growth factor induces a multimeric TrkA receptor complex in neuronal cells that includes Crk, SHC and PLC-gamma 1 but excludes P130CAS. Oncogene 12:77-86.
43. Van der Zee CE, Ross GM, Riopelle RJ, Hagg T. 1996. Survival of cholinergic forebrain neurons in developing p75NGFR-deficient mice. Science 274:1729-1732.
44. Virdee K, Xue L, Hemmings BA, Goemans C, Heumann R, Tolkovsky AM. 1999. Nerve growth factor-induced PKB/Akt activity is sustained by phosphoinositide 3-kinase dependent and independent signals in sympathetic neurons. Brain Res 837:127-142.
45. Wooten MW, Seibenhener ML, Soh Y, Ewald SJ, White KR, Lloyd ED, Olivier A, Parker PJ. 1992. Characterization and differential expression of protein kinase C isoforms in PC12 cells. Differentiation parallels an increase in PKC beta II. FEBS Lett 298:74-78.
46. Wooten MW, Zhou G, Seibenhener ML, Coleman ES. 1994. A role for zeta protein kinase C in nerve growth factor-induced differentiation of PC12 cells. Cell Growth Differ 5:395-403.
47. Wooten MW, Zhou G, Wooten MC, Seibenhener ML. 1997. Transport of protein kinase C isoforms to the nucleus of PC12 cells by nerve growth factor: association of atypical zeta-PKC with the nuclear matrix. J Neurosci Res 49:393-403.
48. Wooten MW, Vandenplas ML, Seibenhener ML, Geetha T, Diaz-Meco MT. 2001. Nerve growth factor stimulates multisite tyrosine phosphorylation and activation of the atypical protein kinase C's via a src kinase pathway. Mol Cell Biol 21:8414-8427.
49. Yoon SO, Casaccia-Bonnefil P, Carter B, Chao MV. 1998. Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J Neurosci 18:3273-3281.