Novel role of sphingosine kinase 1 as a mediator of neurotrophin-3 action in oligodendrocyte progenitors

Journal of Neurochemistry

Volumn 95, Issue 5, 2005, Pages 1298-1310

  Saini, Harsimran S ^a   Coelho, Rochelle P ^a   Goparaju, Sravan K ^a   Jolly, Puneet S ^a   Maceyka, Michael ^a   Spiegel, Sarah ^a   Sato Bigbee, Carmen ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cAMP response element binding protein; Cell survival; Neurotrophin 3; Oligodendrocytes; Sphingosine kinase 1; Sphingosine 1 phosphate

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GROWTH FACTOR; NEUROTROPHIN 3; NEUROTROPIN; SMALL INTERFERING RNA; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; IMMUNOCYTOCHEMISTRY; NERVE CELL CULTURE; NEURAL STEM CELL; NICK END LABELING; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DRUG INTERACTIONS; GENE EXPRESSION REGULATION; IN SITU NICK-END LABELING; LYSOPHOSPHOLIPIDS; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; NEUROTROPHIN 3; OLIGODENDROGLIA; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SPHINGOSINE; STEM CELLS; THIAZOLES; THIAZOLIDINEDIONES; THIONES; TIME FACTORS;

ANIMALIA;

EID: 28844457715     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03451.x     Document Type: Article

References (84)

1. Afshari F. S., Chu A. K. and Sato-Bigbee C. (2001) Effect of cyclic AMP on the expression of myelin basic protein species and myelin proteolipid protein in committed oligodendrocytes: differential involvement of the transcription factor CREB. J. Neurosci. Res. 66, 37-45.
2. Barbacid M. (1994) The Trk family of neurotrophin receptors. J. Neurobiol. 25, 1386-1403.
3. Barres B. A. and Raff M. C. (1994) Control of oligodendrocyte number in the developing rat optic nerve. Neuron 12, 935-942.
4. Barres B. A., Hart I. K., Coles H. S., Burne J. F., Voyvodic J. T., Richardson W. D. and Raff M. C. (1992) Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70, 31-46.
5. Barres B. A., Schmid R., Sendnter M. and Raff M. C. (1993) Multiple extracellular signals are required for long-term oligodendrocyte survival. Development 118, 283-295.
6. Barres B. A., Raff M. C., Gaese F., Bartke I., Dechant G. and Barde Y. A. (1994) A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367, 371-375.
7. Bonni A., Ginty D. D., Dudek H. and Greenberg M. E. (1995) Serine 133-phosphorylated CREB induces transcription via a cooperative mechanism that may confer specificity to neurotrophin signals. Mol. Cell Neurosci. 6, 168-183.
8. Brinkmann V., Cyster J. G. and Hla T. (2004) FTY720: sphingosine 1-phosphate receptor-1 in the control of lymphocyte egress and endothelial barrier function. Am. J. Transplant. 4, 1019-1025.
9. Casaccia-Bonnefil P., Aibel L. and Chao M. V. (1996a) Central glial and neuronal populations display differential sensitivity to ceramide-dependent cell death. J. Neurosci. Res. 43, 382-389.
10. Casaccia-Bonnefil P., Carter B. D., Dobrowsky R. T. and Chao M. V. (1996b) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383, 716-719.
11. Casaccia-Bonnefil P., Gu C. and Chao M. V. (1999) Neurotrophins in cell survival/death decisions. Adv. Exp. Med. Biol. 468, 275-282.
12. Cohen R. I., Marmur R., Norton W. T., Mehler M. F. and Kessler J. A. (1996) Nerve growth factor and neurotrophin-3 differentially regulate the proliferation and survival of developing rat brain oligodendrocytes. J. Neurosci. 16, 6433-6442.
13. Confort C., Charrasse S. and Clos J. (1991) Nerve growth factor enhances DNA synthesis in cultured cerebellar neuroblasts. Neuroreport 1, 566-568.
14. Coussin F., Scott R. H. and Nixon G. F. (2003) Sphingosine 1-phosphate induces CREB activation in rat cerebral artery via a protein kinase C-mediated inhibition of voltage-gated K+ channels. Biochem. Pharmacol. 66, 1861-1870.
15. Craighead M., Pole J. and Waters C. (2000) Caspases mediate C2-ceramide-induced apoptosis of the human oligodendroglial cell line, MO3.13. Neurosci. Lett. 278, 125-128.
16. Culmsee C., Gerling N., Lehmann M., Nikolova-Karakashian M., Prehn J. H., Mattson M. P. and Krieglstein J. (2002) Nerve growth factor survival signaling in cultured hippocampal neurons is mediated through TrkA and requires the common neurotrophin receptor P75. Neuroscience 115, 1089-1108.
17. Dobrowsky R. T., Werner M. H., Castellino A. M., Chao M. V. and Hannun Y. A. (1994) Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 265, 1596-1599.
18. Edsall L. C., Pirianov G. G. and Spiegel S. (1997) Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J. Neurosci. 17, 6952-6960.
19. Edsall L. C., Van Brocklyn J. R., Cuvillier O., Kleuser B. and Spiegel S. (1998) N,N-Dimethylsphingosine is a potent competitive inhibitor of sphingosine kinase but not of protein kinase C: modulation of cellular levels of sphingosine 1-phosphate and ceramide. Biochemistry 37, 12892-12898.
20. Edsall L. C., Cuvillier O., Twitty S., Spiegel S. and Milstien S. (2001) Sphingosine kinase expression regulates apoptosis and caspase activation in PC12 cells. J. Neurochem. 76, 1573-1584.
21. Pagan A. M., Zhang H., Landis S., Smeyne R. J., Silos-Santiago I. and Barbacid M. (1996) TrkA, but not TrkC, receptors are essential for survival of sympathetic neurons in vivo. J. Neurosci. 16, 6208-6218.
22. Fatatis A. and Miller R. J. (1997) Platelet-derived growth factor (PDGF)-induced Ca2+ signaling in the CG4 oligodendroglial cell line and in transformed oligodendrocytes expressing the beta-PDGF receptor. J. Biol. Chem. 272, 4351-4358.
23. Finkbeiner S. (2000) CREB couples neurotrophin signals to survival messages. Neuron 25, 11-14.
24. French K. J., Schrecengost R. S., Lee B. D., Zhuang Y., Smith S. N., Eberly J. L., Yun J. K. and Smith C. D. (2003) Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res. 63, 5962-5969.
25. Fressinaud C. (2005) Repeated injuries dramatically affect cells of the oligodendrocyte lineage: effects of PDGF and NT-3 in vitro. Glia 49, 555-566.
26. Fujino M., Funeshima N., Kitazawa Y., Kimura H., Amemiya H., Suzuki S. and Li X. K. (2003) Amelioration of experimental autoimmune encephalomyelitis in Lewis rats by FTY720 treatment. J. Pharmacol Exp. Ther. 305, 70-77.
27. Ginty D. D., Bonni A. and Greenberg M. E. (1994) Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell 77, 713-725.
28. Gonzalez G. A., Yamamoto K. K., Fischer W. H., Karr D., Menzel P., Biggs W., 3rd, Vale W. W. and Montminy M. R. (1989) A cluster of phosphorylation sites on the cyclic AMP-regulated nuclear factor CREB predicted by its sequence. Nature 337, 749-752.
29. Gotz R., Koster R., Winkler C., Raulf F., Lottspeich F., Schartl M. and Thoenen H. (1994) Neurotrophin-6 is a new member of the nerve growth factor family. Nature 372, 266-269.
30. Han J. S., Macarak E., Rosenbloom J., Chung K. C. and Chaqour B. (2003) Regulation of Cyr61/CCN1 gene expression through RhoA GTPase and p38MAPK signaling pathways. Eur. J. Biochem. 270, 3408-3421.
31. Hida H., Takeda M. and Soliven B. (1998) Ceramide inhibits inwardly rectifying K+ currents via a Ras- and Raf-1-dependent pathway in cultured oligodendrocytes. J. Neurosci. 18, 8712-8719.
32. Hida H., Nagano S., Takeda M. and Soliven B. (1999) Regulation of mitogen-activated protein kinases by sphingolipid products in oligodendrocytes. J. Neurosci. 19, 7458-7467.
33. Im D. S., Clemens J., Macdonald T. L. and Lynch K. R. (2001) Characterization of the human and mouse sphingosine 1-phosphate receptor, S1P5 (Edg-8): structure-activity relationship of sphingosinel-phosphate receptors. Biochemistry 40, 14 053-14 060.
34. Jaillard C., Harrison S., Stankoff B. et al. (2005) Edg8/S1P5: an oligodendroglial receptor with dual function on process retraction and cell survival. J. Neurosci. 25, 1459-1469.
35. Jatana M., Giri S. and Singh A. K. (2002) Apoptotic positive cells in Krabbe brain and induction of apoptosis in rat C6 glial cells by psychosine. Neurosci. Lett. 330, 183-187.
36. Jean I., Lavialle C., Barthelaix-Pouplard A. and Fressinaud C. (2003) Neurotrophin-3 specifically increases mature oligodendrocyte population and enhances remyelination after chemical demyelination of adult rat CNS. Brain Res. 972, 110-118.
37. Johnson J. R., Chu A. K. and Sato-Bigbee C. (2000) Possible role of CREB in the stimulation of oligodendrocyte precursor cell proliferation by neurotrophin-3. J. Neurochem. 74, 1409-1417.
38. Johnson K. R., Becker K. P., Facchinetti M. M., Hannun Y. A. and Obeid L. M. (2002) PKC-dependent activation of sphingosine kinase 1 and translocation to the plasma membrane. Extracellular release of sphingosine-1-phosphate induced by phorbol 12-myristate 13-acetate (PMA). J. Biol. Chem. 277, 35 257-35 262.
39. Jolly P. S., Bektas M., Olivera A., Gonzalez-Espinosa C., Proia R. L., Rivera J., Milstien S. and Spiegel S. (2004) Transactivation of sphingosine-1-phosphate receptors by FcepsilonRI triggering is required for normal mast cell degranulation and chemotaxis. J. Exp. Med. 199, 959-970.
40. Kahn M. A., Kumar S., Liebl D., Chang R., Parada L. F. and De Vellis J. (1999) Mice lacking NT-3, and its receptor TrkC, exhibit profound deficiencies in CNS glial cells. Glia 26, 153-165.
41. Kaplan D. R. and Miller F. D. (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
42. Kavanaugh B., Beesley J., Itoh T., Itoh A., Grinspan J. and Pleasure D. (2000) Neurotrophin-3 (NT-3) diminishes susceptibility of the oligodendroglial lineage to AMPA glutamate receptor-mediated excitotoxicity. J. Neurosci. Res. 60, 725-732.
43. Kumar S., Kahn M. A., Dinh L. and de Vellis J. (1998) NT-3-mediated TrkC receptor activation promotes proliferation and cell survival of rodent progenitor oligodendrocyte cells in vitro and in vivo. J. Neurosci. Res. 54, 754-765.
44. Larocca J. N., Farooq M. and Norton W. T. (1997) Induction of oligodendrocyte apoptosis by C2-ceramide. Neurochem. Res. 11, 529-534.
45. Limaye V., Li X., Hahn C., Xia P., Berndt M. C., Vadas M. A. and Gamble J. R. (2005) Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/ Akt and regulation of Bcl-2 family members. Blood 105, 3169-3177.
46. Liu H., Toman R. E., Goparaju S. K. et al. (2003) Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J. Biol. Chem. 278, 40 330-40 336.
47. Lucchinetti C. F., Bruck W. and Lassmann H. (2004) Evidence for pathogenic heterogeneity in multiple sclerosis. Ann. Neurol. 56, 308.
48. McDonald N. Q. and Chao M. V. (1995) Structural determinants of neurotrophin action. J. Biol. Chem. 270, 19 669-19 672.
49. McTigue D. M., Horner P. J., Stokes B. T. and Gage F. H. (1998) Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18, 5354-5365.
50. Meacci E., Nuti F., Catarzi S., Vasta V., Donati C., Bourgoin S., Bruni P., Moss J. and Vaughan M. (2003) Activation of phospholipase D by bradykinin and sphingosine 1-phosphate in A549 human lung adenocarcinoma cells via different GTP-binding proteins and protein kinase C delta signaling pathways. Biochemistry 42, 284-292.
51. Montminy M. R., Gonzalez G. A. and Yamamoto K. K. (1990) Characteristics of the cAMP response unit. Metabolism 39, 6-12.
52. Mutate T., Banno Y. K. T. K., Watanabe K. et al. (2001) Cell type-specific localization of Sphingosine kinase 1a in human tissues. J. Histochem. Cytochem. 49, 845-855.
53. Nilsson A. S., Fainzilber M., Falck P. and Ibanez C. F. (1998) Neurotrophin-7: a novel member of the neurotrophin family from the zebrafish. FEBS Lett. 424, 285-290.
54. Olivera A. and Spiegel S. (2001) Sphingosine kinase: a mediator of vital cellular functions. Prostaglandins 64, 123-134.
55. Olivera A., Kohama T., Edsall L., Nava V., Cuvillier O., Poulton S. and Spiegel S. (1999) Sphingosine kinase expression increases intracellular Sphingosine-1-phosphate and promotes cell growth and survival. J. Cell Biol. 147, 545-558.
56. Patapoutian A. and Reichardt L. F. (2001) Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 11, 272-280.
57. Pitson S. M., Moretti P. A., Zebol J. R., Lynn H. E., Xia P., Vadas M. A. and Wattenberg B. W. (2003) Activation of Sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J. 22, 5491-5500.
58. Pitson S. M., Xia P., Leclercq T. M., Moretti P. A., Zebol J. R., Lynn H. E., Wattenberg B. W. and Vadas M. A. (2005) Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J. Exp. Med. 201, 49-54.
59. Rabano M., Pena A., Brizuela L., Marino A., Macarulla J. M., Trueba M. and Gomez-Munoz A. (2003) Sphingosine-1-phosphate stimulates cortisol secretion. FEBS Lett. 535, 101-105.
60. Rausch M., Hiestand P., Foster C. A., Baumann D. R., Cannet C. and Rudin M. (2004) Predictability of FTY720 efficacy in experimental autoimmune encephalomyelitis by in vivo macrophage tracking: clinical implications for ultrasmall superparamagnetic iron oxide-enhanced magnetic resonance imaging. J. Magn. Reson. Imaging 20, 16-24.
61. Rius R. A., Edsall L. C. and Spiegel S. (1997) Activation of sphingosine kinase in pheochromocytoma PC12 neuronal cells in response to trophic factors. FEBS Lett. 417, 173-176.
62. de la Rosa E. J., Arribas A., Frade J. M. and Rodriguez-Tebar A. (1994) Role of neurotrophins in the control of neural development: neurotrophin-3 promotes both neuron differentiation and survival of cultured chick retinal cells. Neuroscience 58, 347-352.
63. Saini H. S., Gorse K. M., Boxer L. M. and Sato-Bigbee C. (2004) Neurotrophin-3 and a CREB-mediated signaling pathway regulate Bcl-2 expression in oligodendrocyte progenitor cells. J. Neurochem. 89, 951-961.
64. Sato-Bigbee C. and DeVries G. H. (1996) Treatment of oligodendrocytes with antisense deoxyoligonucleotide directed against CREB mRNA: effect on the cyclic AMP-dependent induction of myelin basic protein expression. J. Neurosci. Res. 46, 98-107.
65. Sato-Bigbee C., Pal S. and Chu A. K. (1999) Different neuroligands and signal transduction pathways stimulate CREB phosphorylation at specific developmental stages along oligodendrocyte differentiation. J. Neurochem. 72, 139-147.
66. Segal R. A., Pomeroy S. L. and Stiles C. D. (1995) Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J. Neurosci. 15, 4970-4981.
67. Shatrov V. A., Lehmann V. and Chouaib S. (1997) Sphingosine-1-phosphate mobilizes intracellular calcium and activates transcription factor NF-kappa B in U937 cells. Biochem. Biophys. Res. Commun. 234, 121-124.
68. Sheng M., Thompson M. A. and Greenberg M. E. (1991) CREB: a Ca (2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252, 1427-1430.
69. Singh I., Pahan K., Khan M. and Singh A. K. (1998) Cytokine-mediated induction of ceramide production is redox-sensitive. Implications to proinflammatory cytokine-mediated apoptosis in demyelinating diseases. J. Biol. Chem. 273, 20 354-20 362.
70. Soliven B., Ma L., Bae H., Attali B., Sobko A. and Iwase T. (2003) PDGF upregulates delayed rectifier via Src family kinases and sphingosine kinase in oligodendroglial progenitors. Am. J. Physiol. Cell Physiol. 284, C85-C93.
71. Spiegel S. and Milstien S. (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev. Mol. Cell Biol. 4, 397-407.
72. Spiegel S., English D. and Milstien S. (2002) Sphingosine 1-phosphate signaling: providing cells with a sense of direction. Trends Cell Biol. 12, 236-242.
73. Su Y., Rosenthal D., Smulson M. and Spiegel S. (1994) Sphingosine 1-phosphate, a novel signaling molecule, stimulates DNA binding activity of AP-I in quiescent Swiss 3T3 fibroblasts. J. Biol. Chem. 269, 16512-16517.
74. Takeshita A., Watanabe A., Takada Y. and Hanazawa S. (2000) Selective stimulation by ceramide of the expression of the alpha isoform of retinoic acid and retinoid X receptors in osteoblastic cells. A role of sphingosine 1-phosphate-mediated AP-1 in the ligand-dependent transcriptional activity of these receptors. J. Biol. Chem. 275, 32 220-32 226.
75. Terai K., Soga T., Takahashi M., Kamohara M., Ohno K., Yatsugi S., Okada M. and Yamaguchi T. (2003) Edg-8 receptors are preferentially expressed in oligodendrocyte lineage cells of the rat CNS. Neuroscience 116, 1053-1062.
76. Toman R. E., Payne S. G., Watterson K. R., Maceyka M., Lee N. H., Milstien S., Bigbee J. W. and Spiegel S. (2004) Differential transactivation of sphingosine-1-phosphate receptors modulates NGF-induced neurite extension. J. Cell Biol. 166, 381-392.
77. Wang F., Buckley N. E., Olivera A., Goodemote K. A., Su Y. and Spiegel S. (1996) Involvement of sphingolipids metabolites in cellular proliferation modulated by ganglioside GM1. Glycoconjugate J. 13, 937-945.
78. Watterson K., Sankala H., Milstien S. and Spiegel S. (2003) Pleiotropic actions of sphingosine-1-phosphate. Prog. Lipid Res. 42, 344-357.
79. Watterson K. R., Ratz P. H. and Spiegel S. (2005) The role of sphingosine-1-phosphate in smooth muscle contraction. Cell Signal. 17, 289-298.
80. Webb M., Tham C.-S., Lin F.-F., Lariosa-Willingham K., Yu N., Hale J., Mandala S., Chun J. and Rao T. S. (2004) Sphingosine 1-phosphate receptor agonists attenuate relapsing-remitting experimental autoimmune encephalitis in SJL mice. J. Neuroimmunol. 153, 108-121.
81. Wilson H. C., Onischke C. and Raine C. S. (2003) Human oligodendrocyte precursor cells in vitro: phenotypic analysis and differential response to growth factors. Glia 44, 153-165.
82. Xia P., Gamble J. R., Rye K. A., Wang L., Hu C. S., Cockerill P., Khew-Goodall Y, Bert A. G., Barter P. J. and Vadas M. A. (1998) Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl Acad. Sci. USA 95, 14196-14201.
83. Xing J., Ginty D. D. and Greenberg M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
84. Yu N., Lariosa-Willingham K. D., Lin F. F., Webb M. and Rao T. S. (2004) Characterization of lysophosphatidic acid and sphingosine-1-phosphate-mediated signal transduction in rat cortical oligodendrocytes. Glia 45, 17-27.