Sphingosine-1-phosphate induces proliferation and morphological changes of neural progenitor cells

Journal of Neurochemistry

Volumn 88, Issue 4, 2004, Pages 1026-1039

  Harada, Jun ^a,b   Foley, Melissa ^a   Moskowitz, Michael A ^a   Waeber, Christian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b DAIICHI SANKYO CO   (Japan)

Author keywords

MAP kinase; Neural progenitor cells; Neurogenesis; Rho associated kinase; Sphingolipids; Telomerase

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; BETA3 TUBULIN, MOUSE; BROXURIDINE; DNA ENZYME ED5; DRUG DERIVATIVE; ENZYME INHIBITOR; FIBROBLAST GROWTH FACTOR 2; G PROTEIN COUPLED RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); INTERMEDIATE FILAMENT PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NESTIN PROTEIN; O ANTIGEN; O4 ANTIGEN, STENOTROPHOMONAS; RECEPTOR SUBTYPE; RHO KINASE; SINGLE STRANDED DNA; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR 1; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; SPHINGOSINE 1 PHOSPHATE RECEPTOR 3; SPHINGOSINE 1 PHOSPHATE RECEPTOR 5; SPHINGOSINE 1-PHOSPHATE; SULFUR; TELOMERASE; TUBULIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BIOSYNTHESIS; BRAIN; BRAIN TISSUE; CELL CULTURE; CELL DIVISION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; EMBRYO; EMBRYOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; NERVE CELL; NERVE CELL CULTURE; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; RAT STRAIN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEM CELL; WESTERN BLOTTING;

ANIMALIA; STENOTROPHOMONAS;

EID: 1042278008     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02219.x     Document Type: Article

References (67)

1. Amoureux M.-C., Cunningham B. A., Edelman G. M. and Crossin K. L. (2000) N-CAM binding inhibits the proliferation of hippocampal progenitor cells and promotes their differentiation to a neuronal phenotype. J. Neurosci. 20, 3631-3640.
2. Arsenijevic Y., Weiss S., Schneider B. and Aebischer P. (2001) Insulin-like growth factor-1 is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J. Neurosci. 21, 7194-7202.
3. Biesiada E., Razandi M. and Levin E. R. (1996) Egr-1 activates basic fibroblast growth factor transcription. Mechanistic implications for astrocyte proliferation. J. Biol. Chem. 271, 18576-18581.
4. Cameron H. A. and Gould E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61, 203-209.
5. Chun J., Goetzl E. J., Hla T., Igarashi Y., Lynch K. R., Moolenaar W., Pyne S. and Tigyi G. (2002) International Union of Pharmacology. XXXIV. Lysophospholipid receptor nomenclature. Pharmacol. Rev. 54, 265-269.
6. Collins K. and Mitchell J. R. (2002) Telomerase in the human organism. Oncogene 21, 564-579.
7. Davies S. P., Reddy H., Caivano M. and Cohen P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105.
8. Donovan P. and Gearhart J. (2001) The end of the beginning for pluripotent stem cells. Nature 414, 92-97.
9. English D., Brindley D. N., Spiegel S. and Carcia J. G. N. (2002) Lipid mediators of angiogenesis and the signaling pathways they initiate. Biochim. Biophys. Acta 1582, 228-239.
10. Eriksson P. S., Perfilieva E., Bjork-Eriksson T., Alborn A. M., Nordborg C., Peterson D. A. and Gage F. H. (1998) Neurogenesis in the adult human hippocampus. Nature Med. 4, 1313-1317.
11. Erlandsson A., Enarsson M. and Forsberg-Nilsson K. J. (2001) Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor. J. Neurosci. 21, 3483-3491.
12. Fahmy R. G., Dass C. R., Sun L.-Q., Chesterman C. N. and Khachigian L. M. (2003) Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med. 9, 1026-1032.
13. Favata M. F., Horiuchi K. Y., Manos E. J. et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase. J. Biol. Chem. 273, 18623-18632.
14. Fu W., Begley J. G., Killen M. W. and Mattson M. P. (1999) Antiapoptotic role of telomerase in pheochromocytoma cells. J. Biol. Chem. 274, 7264-7271.
15. Fukushima N., Weiner J. A. and Chun J. (2000) Lysophosphatidic acid (LPA) is a novel extracellular regulator of cortical neuroblast morphology. Dev. Biol. 228, 6-18.
16. Fukushima N., Weiner J. A., Kaushal D., Contos J. J., Rehen S. K., Kingsbury M. A., Kim K. Y. and Chun J. (2002) Lysophosphatidic acid influences the morphology and motility of young, postmitotic cortical neurons. Mol. Cell Neurosci. 20, 271-282.
17. Gage F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438.
18. Gould E. and Gross C. G. (2002) Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22, 619-623.
19. Gritti A., Parati E. A., Cova L. et al. (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16, 1091-1100.
20. Haik S., Gauthier L. R., Granotier C., Peyrin J.-M., Lages C. S., Dormont D. and Boussin F. D. (2000) Fibroblast growth factor 2 up regulates telomerase activity in neural precursor cells. Oncogene 19, 2957-2966.
21. 35S]GTPgammaS autoradiography: optimization for high sensitivity. Eur. J. Pharmacol. 422, 1-13.
22. Hecht J. H., Weiner J. A., Post S. R. and Chun J. (1996) Ventricular zone gene-1 (vzg-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex. J. Cell. Biol. 135, 1071-1083.
23. Hirose M., Ishizaki T., Watanabe N., Uehata M., Kranenburg O., Moolenaar W. H., Matsumura F., Maekawa M., Bito H. and Narumiya S. (1998) Molecular dissection of Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625-1636.
24. Hobson J. P., Rosenfeldt H. M., Barak L. S., Olivera A., Poulton S., Caron M. G., Milstien S. and Spiegel S. (2001) Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility. Science 291, 1800-1803.
25. Ii M., Yoshida H., Aramaki Y., Masuya H., Hada T., Terada M., Hatanaka I. and Ichimori Y. (1993) Improved enzyme immunoassay for human basic fibroblast growth factor using a new enhanced chemiluminescence system. Biochem. Biophys. Res. Commun. 193, 540-545.
26. Inui T., Shinomiya N., Fukasawa M., Kobayashi M., Kuranaga N., Ohkura S. and Seki S. (2002) Growth-related signaling regulates activation of telomerase in regenerating hepatocytes. Exp. Cell Res. 273, 147-156.
27. Jin K., Mao X. O., Sun Y., Xie L., Jin L., Nishi E., Klagsbrun M. and Greenberg D. A. (2002) Heparin-binding epidermal growth factor-like growth factor: hypoxia-induced expression in vivo and stimulation of neurogenesis in vitro and in vivo. J. Neurosci. 22, 5365-5373.
28. Kim N. W., Piatyszek M. A., Prowse K. R., Harley C. B., West M. D., Ho P. L. C., Coviello G. M., Wright W. E., Weinrich S. L. and Shay J. W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015.
29. Klapper W., Shin T. and Mattson M. P. (2001) Differential regulation of telomerase activity and TERT expression during brain development in mice. J. Neurosci. Res. 64, 252-260.
30. Kluk M. J. and Hla T. (2002) Signaling of sphingosine 1-phosphate via the S1P/EDG-family of G-protein-coupled receptors. Biochim. Biophys. Acta. 1582, 72-80.
31. 35S]guanosine 5′-(γ-thio) triphosphate autoradiography. Neuroscience 90, 1265-1279.
32. Learish R. D., Bruss M. D. and Haak-Frendscho M. (2000) Inhibition of mitogen-activated protein kinase kinase blocks proliferation of neural progenitor cells. Dev. Brain Res. 122, 97-109.
33. Lee M.-J., Van Brocklyn J. R., Thangada S., Liu C. H., Hand A. R., Menzeleev R., Spiegel S. and Hla T. (1998) Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279, 1552-1555.
34. Lee M.-J., Thangada S., Claffey K. P., Ancellin N., Liu C. H., Kluk M., Volpi M., Sha'afi R. I. and Hla T. (1999) Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99, 301-312.
35. Li B. S., Ma W., Zhang L., Barker J. L., Stenger D. A. and Pant H. C. (2001) Activation of phosphatidylinositol-3 kinase (PI-3K) and extracellular regulated kinase (ERK1/2) is involved in muscarinic receptor-mediated DNA synthesis in neural progenitor cells. J. Neurosci. 21, 1569-1579.
36. Liu J.-P. (1999) Studies of the molecular mechanisms in the regulation of telomerase activity. FASEB J. 13, 2091-2104.
37. Liu Y., Wada R., Yamashita T. et al. (2000) Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Invest. 106, 951-961.
38. Ma W., Maric D., Li B.-S. et al. (2000) Acetylcholine stimulates cortical cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur. J. Neurosci. 12, 1227-1240.
39. B2 sphingosine I-phosphate receptor in neuronal excitability. Eur. J. Neurosci. 14, 203-209.
40. Mattson M. P. and Klapper W. (2001) Emerging roles for telomerase in neuronal development and apoptosis. J. Neurosci. Res. 63, 1-9.
41. McGiffert C., Contos J. J. A., Friedman B. and Chun J. (2002) Embryonic brain expression analysis of lysophospholipid receptor genes suggests roles for s1p(1) in neurogenesis and s1p(1-3) in angiogenesis. FEBS Lett. 531, 103-108.
42. Niedemberg A., Tunaru S., Blaukat A., Ardati A. and Kostenis E. (2003) Sphingosine 1-phosphate and dioleoylphosphatidic acid are low affinity agonists for the orphan receptor GPR63. Cell Signal. 15, 435-446.
43. Oh H., Taffet G. E., Youker K. A., Entman M. L., Overbeek P. A., Michael L. H. and Schneider M. D. (2001) Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy, and survival. Proc. Natl Acad. Sci. USA 98, 10308-10313.
44. Palmer T. D., Willhoite A. R. and Gage F. H. (2000) Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425, 479-494.
45. Pébay A., Toutant M., Prémont J., Calvo C. F., Venance L., Cordier J., Glowinski J. and Tencé M. (2001) Sphingosine-1-phosphate induces proliferation of astrocytes: regulation by intracellular signalling cascades. Eur. J. Neurosci. 13, 2067-2076.
46. Perez-Juste G. and Aranda A. (1999) The cyclin-dependent kinase inhibitor p27 (Kip1) is involved in thyroid hormone-mediated neuronal differentiation. J. Biol. Chem. 274, 5026-5031.
47. Pyne S. and Pyne N. J. (2000) Sphingosine 1-phosphate signaling in mammalian cells. Biochem. J. 349, 385-402.
48. Ray J., Peterson D. A., Schinstine M. and Gage F. H. (1993) Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl Acad. Sci. USA 90, 3602-3606.
49. Santiago F. S., Lowe H. C., Day F. L., Chesterman C. N. and Khachigian L. M. (1999) Early growth response factor-1 induction by injury is triggered by release and paracrine activation by fibroblast growth factor-2. Am. J. Pathol. 154, 937-944.
50. kip1 in neuronal differentiation of embryonal carcinoma cells. Mol. Brain Res. 77, 209-221.
51. Sato K., Ishikawa K., Ui M. and Okajima F. (1999) Sphingosine 1-phosphate induces expression of early growth response-1 and fibroblast growth factor-2 through mechanism involving extracellular signal-regulated kinase in astroglial cells. Mol. Brain Res. 74, 182-189.
52. Shimazaki T., Shingo T. and Weiss S. (2001) The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J. Neurosci. 21, 7642-7653.
53. Smith L. L., Coller H. A. and Roberts J. M. (2003) Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nature Cell Biol. 5, 474-479.
54. Spiegel S. and Milstien S. (2000) Functions of new family of sphingosine-1-phoaphate receptors. Biochim. Biophys. Acta 1484, 107-116.
55. Spiegel S. and Milstien S. (2002) Sphingosine 1-phosphate, a key cell signaling molecule. J. Biol. Chem. 277, 25851-25854.
56. Tanimoto T., Jin Z.-G. and Berk B. C. (2002) Transactivation of vascular endothelial growth factor (VEGF) receptor Flk-1/KDR is involved in sphingosine 1-phosphate-stimulated phosphorylation of Akt and endothelial nitric-oxide synthase (eNOS). J. Biol. Chem. 277, 42997-43001.
57. Uhlenbrock K., Gassenhuber H. and Kostenis E. (2002) Sphingosine 1-phosphate is a ligand of the human gpr3, gpr6 and gpr12 family of constitutively active G protein-coupled receptors. Cell Signal. 14, 941-953.
58. 35S]thio) triphosphate binding stimulated by sphingosine 1-phosphate and lysophosphatidic acid. J. Neurochem. 73, 1212-1221.
59. 35S]guanosine-5′-O-(3-thio) triphosphate binding to rodent brain sections as visualized by in vitro autoradiography. Mol. Pharmacol. 52, 623-631.
60. Wang D., Mayo M. W. and Baldwin A. S. (1997) Basic fibroblast growth factor transcriptional autoregulation requires EGR-1. Oncogene 15, 2291-2299.
61. i-coupled cell surface receptor. J. Biol. Chem. 274, 35343-35350.
62. Waters C., Sambi B., Kong K.-C., Thompson D., Pitson S. M., Pyne S. and Pyne N. J. (2003) Sphingosine 1-phosphate and platelet-derived growth factor (PDGF) act via PDGF β receptor-sphingosine 1-phosphate receptor complexes in airway smooth muscle cells. J. Biol. Chem. 278, 6282-6290.
63. Weiss S., Dunne C., Hewson J., Mohl C., Wheatley M., Peterson A. C. and Reynolds B. A. (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J. Neurosci. 16, 7599-7609.
64. Windh R. T., Lee M.-J., Hla T., An S., Barr A. J. and Manning D. R. (1999) Differential coupling of the sphingosine 1-phosphate receptors Edg-1, Edg-3, and H218/Edg-5 to the G(i), G(q), and G(12) families of heterotrimeric G proteins. J. Biol. Chem. 274, 27351-27358.
65. Yatomi Y., Igarashi Y., Yang L., Hisano N., Qi R., Asazuma N., Satoh K., Ozaki Y. and Kume S. (1997) Sphingosine 1-phosphate, a bioactive sphingolipid abundantly stored in platelets, is a normal constituent of human plasma and serum. J. Biochem. 121, 969-973.
66. Yatomi Y., Ozaki Y., Ohmori T. and Igarashi Y. (2001) Sphingosine 1-phosphate: synthesis and release. Prostaglandins Other Lipid Med. 64, 107-112.
67. Yoshimura S., Takagi Y., Harada J., Teramoto T., Thomas S. S., Waeber C., Baskowska J., Breakefield X. O. and Moskowitz. M. A. (2001) FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc. Natl Acad. Sci. USA 98, 5874-5879.