Regulation of stem cell pluripotency and neural differentiation by lysophospholipids

NeuroSignals

Volumn 17, Issue 4, 2009, Pages 242-254

  Pitson, Stuart M ^a,b   Pébay, Alice ^c  

^a CENTRE FOR CANCER BIOLOGY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Ceramide; G protein coupled receptors; Lysophosphatidic acid; Lysophospholipid; Neural differentiation; Progenitor cells; Signalling pathways; Sphingosine 1 phosphate; Stem cells, induced pluripotent

Indexed keywords

LYSOPHOSPHOLIPID; LYSOPHOSPHOLIPID RECEPTOR; MESSENGER RNA; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

BRAIN INJURY; CENTRAL NERVOUS SYSTEM; EMBRYONIC STEM CELL; HUMAN; LIPID METABOLISM; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; REVIEW;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MODELS, NEUROLOGICAL; NEUROGENESIS; NEURONS; OLIGODENDROGLIA; PLURIPOTENT STEM CELLS; SIGNAL TRANSDUCTION;

EID: 70350754356     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000231891     Document Type: Review

References (133)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM: Embryonic stem cell lines derived from human blastocysts. Science 1998; 282: 1145-1147.
2. Verfaillie CM, Pera MF, Lansdorp PM: Stem cells: hype and reality. Hematology 2002: 369-391.
3. Wong RC, Pebay A: Signaling pathways involved in the maintenance of human embryonic stem cells. J Stem Cells 2006; 1: 271-282.
4. Ohtsuka S, Dalton S: Molecular and biological properties of pluripotent embryonic stem cells. Gene Ther 2008; 15: 74-81.
5. Zhao C, Fancy SP, Magy L, Urwin JE, Franklin RJ: Stem cells, progenitors and myelin repair. J Anat 2005; 207: 251-258.
6. Picard-Riera N, Nait-Oumesmar B, Baron-Van Evercooren A: Endogenous adult neural stem cells: limits and potential to repair the injured central nervous system. J Neurosci Res 2004; 76: 223-231.
7. Van Meeteren LA, Ruurs P, Stortelers C, Bouwman P, van Rooijen MA, Pradere JP, Pettit TR, Wakelam MJ, Saulnier-Blache JS, Mummery CL, Moolenaar WH, Jonkers J: Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol Cell Biol 2006; 26: 5015-5022.
8. Aoki J: Mechanisms of lysophosphatidic acid production. Semin Cell Dev Biol 2004; 15: 477-489.
9. Bektas M, Payne SG, Liu H, Goparaju S, Milstien S, Spiegel S: A novel acylglycerol kinase that produces lysophosphatidic acid modulates cross talk with EGFR in prostate cancer cells. J Cell Biol 2005; 169: 801-811.
10. Dircks L, Sul HS: Acyltransferases of de novo glycerophospholipid biosynthesis. Prog Lipid Res 1999; 38: 461-479.
11. Pitson SM, Moretti PA, Zebol JR, Lynn HE, Xia P, Vadas MA, Wattenberg BW: Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J 2003; 22: 5491-5500.
12. Pitson SM, Xia P, Leclercq TM, Moretti PA, Zebol JR, Lynn HE, Wattenberg BW, Vadas MA: Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J Exp Med 2005; 201: 49-54.
13. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y, van Echten-Deckert G, Hajdu R, Rosenbach M, Keohane CA, Mandala S, Spiegel S, Proia RL: Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 2004; 279: 52487-52492.
14. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, Proia RL: Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 2005; 25: 11113-11121.
15. Yatomi Y, Ozaki Y, Ohmori T, Igarashi Y: Sphingosine 1-phosphate: synthesis and release. Prostaglandins Other Lipid Mediat 2001; 64: 107-122.
16. Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB, Xu Y, Camerer E, Zheng YW, Huang Y, Cyster JG, Coughlin SR: Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 2007; 316: 295-298.
17. Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y, Bonkovsky HL, Parikh NS, Habrukowich C, Hla T: Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 2008; 102: 669-676.
18. Mitra P, Oskeritzian CA, Payne SG, Beaven MA, Milstien S, Spiegel S: Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc Natl Acad Sci USA 2006; 103: 16394-16399.
19. Osborne N, Brand-Arzamendi K, Ober EA, Jin SW, Verkade H, Holtzman NG, Yelon D, Stainier DY: The spinster homolog, two of hearts, is required for sphingosine 1-phosphate signaling in zebrafish. Curr Biol 2008; 18: 1882-1888.
20. Kawahara A, Nishi T, Hisano Y, Fukui H, Yamaguchi A, Mochizuki N: The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 2009; 323: 524-527.
21. Ancellin N, Colmont C, Su J, Li Q, Mittereder N, Chae SS, Stefansson S, Liau G, Hla T: Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J Biol Chem 2002; 277: 6667-6675.
22. Waters C, Sambi B, Kong KC, Thompson D, Pitson SM, Pyne S, Pyne NJ: Sphingosine 1-phosphate and platelet-derived growth factor (PDGF) act via PDGF -receptor-sphingosine 1-phosphate receptor complexes in airway smooth muscle cells. J Biol Chem 2003; 278: 6282-6290.
23. Soldi R, Mandinova A, Venkataraman K, Hla T, Vadas M, Pitson S, Duarte M, Graziani I, Kolev V, Kacer D, Kirov A, Maciag T, Prudovsky I: Sphingosine kinase 1 is a critical component of the copper-dependent FGF1 export pathway. Exp Cell Res 2007; 313: 3308-3318.
24. Rosen H, Gonzalez-Cabrera PJ, Sanna MG, Brown S: Sphingosine 1-phosphate receptor signaling. Annu Rev Biochem 2009; 78: 743-768.
25. Shimomura Y, Wajid M, Ishii Y, Shapiro L, Petukhova L, Gordon D, Christiano AM: Disruption of p2ry5, an orphan G proteincoupled receptor, underlies autosomal recessive woolly hair. Nat Genet 2008; 40: 335-339.
26. Pasternack SM, von Kugelgen I, Aboud KA, Lee YA, Ruschendorf F, Voss K, Hillmer AM, Molderings GJ, Franz T, Ramirez A, Nurnberg P, Nothen MM, Betz RC: G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth. Nat Genet 2008; 40: 329-334.
27. Yanagida K, Masago K, Nakanishi H, Kihara Y, Hamano F, Tajima Y, Taguchi R, Shimizu T, Ishii S: Identification and characterization of a novel lysophosphatidic acid receptor, p2y5/LPA6. J Biol Chem 2009; 284: 17731-17741.
28. Tabata K, Baba K, Shiraishi A, Ito M, Fujita N: The orphan GPCR GPR87 was deorphanized and shown to be a lysophosphatidic acid receptor. Biochem Biophys Res Commun 2007; 363: 861-866.
29. Murakami M, Shiraishi A, Tabata K, Fujita N: Identification of the orphan GPCR, P2Y 10 receptor as the sphingosine-1-phosphate and lysophosphatidic acid receptor. Biochem Biophys Res Commun 2008; 371: 707-712.
30. Pebay A, Bonder CS, Pitson SM: Stem cell regulation by lysophospholipids. Prostaglandins Other Lipid Mediat 2007; 84: 83-97.
31. Meyer zu Heringdorf D, Jakobs KH: Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 2007; 1768: 923-940.
32. Tanimoto T, Lungu AO, Berk BC: Sphingosine 1-phosphate transactivates the plateletderived growth factor beta receptor and epidermal growth factor receptor in vascular smooth muscle cells. Circ Res 2004; 94: 1050-1058.
33. Sukocheva O, Wadham C, Holmes A, Albanese N, Verrier E, Feng F, Bernal A, Derian CK, Ullrich A, Vadas MA, Xia P: Estrogen transactivates EGFR via the sphingosine 1-phosphate receptor EDG-3: the role of sphingosine kinase-1. J Cell Biol 2006; 173: 301-310.
34. Shida D, Fang X, Kordula T, Takabe K, Lepine S, Alvarez SE, Milstien S, Spiegel S: Crosstalk between LPA1 and epidermal growth factor receptors mediates up-regulation of sphingosine kinase 1 to promote gastric cancer cell motility and invasion. Cancer Res 2008; 68: 6569-6577.
35. Lebman DA, Spiegel S: Cross-talk at the crossroads of sphingosine-1-phosphate, growth factors, and cytokine signaling. J Lipid Res 2008; 49: 1388-1394.
36. McIntyre TM, Pontsler AV, Silva AR, St Hilaire A, Xu Y, Hinshaw JC, Zimmerman GA, Hama K, Aoki J, Arai H, Prestwich GD: Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPAR -agonist. Proc Natl Acad Sci USA 2003; 100: 131-136. (Pubitemid 36078041)
37. Lehrke M, Lazar MA: The many faces of PPAR. Cell 2005; 123: 993-999.
38. Lee CW, Rivera R, Gardell S, Dubin AE, Chun J: Gpr92 as a new G 12/13 -and G q -coupled lysophosphatidic acid receptor that increases cAMP, LPA 5 . J Biol Chem 2006; 281: 23589-23597.
39. Kleger A, Busch T, Liebau S, Prelle K, Paschke S, Beil M, Rolletschek A, Wobus A, Wolf E, Adler G, Seufferlein T: The bioactive lipid sphingosylphosphorylcholine induces differentiation of mouse embryonic stem cells and human promyelocytic leukaemia cells. Cell Signal 2007; 19: 367-377.
40. Rodgers A, Mormeneo D, Long JS, Delgado A, Pyne NJ, Pyne S: Sphingosine 1-phosphate regulation of extracellular signal regulated kinase-1/2 in embyronic stem cells. Stem Cells Dev 2009; Epub ahead of print.
41. Todorova MG, Fuentes E, Soria B, Nadal A, Quesada I: Lysophosphatidic acid induces Ca2+ mobilization and c-Myc expression in mouse embryonic stem cells via the phospholipase C pathway. Cell Signal 2009; 21: 523-528.
42. Burdon T, Smith A, Savatier P: Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 2002; 12: 432-438.
43. Choi HJ, Lee JH, Park SY, Cho JH, Han JS: STAT3 is involved in phosphatidic acid-induced Bcl-2 expression in HeLa cells. Exp Mol Med 2009; 41: 94-101.
44. Frias MA, James RW, Gerber-Wicht C, Lang U: Native and reconstituted HDL activate Stat3 in ventricular cardiomyocytes via ERK1/2: role of sphingosine-1-phosphate. Cardiovasc Res 2009; 82: 313-323.
45. Schuck S, Soloaga A, Schratt G, Arthur JS, Nordheim A: The kinase MSK1 is required for induction of c-fos by lysophosphatidic acid in mouse embryonic stem cells. BMC Mol Biol 2003; 4: 6.
46. Burdon T, Stracey C, Chambers I, Nichols J, Smith A: Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev Biol 1999; 210: 30-43.
47. Sachinidis A, Gissel C, Nierhoff D, Hippler-Altenburg R, Sauer H, Wartenberg M, Hescheler J: Identification of platelet-derived growth factor-BB as cardiogenesis-inducing factor in mouse embryonic stem cells under serum-free conditions. Cell Physiol Biochem 2003; 13: 423-429.
48. Bieberich E, MacKinnon S, Silva J, Noggle S, Condie BG: Regulation of cell death in mitotic neural progenitor cells by asymmetric distribution of prostate apoptosis response 4 (PAR-4) and simultaneous elevation of endogenous ceramide. J Cell Biol 2003; 162: 469-479.
49. Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind S, Spiegel S: Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature 1996; 381: 800-803.
50. Bieberich E: Smart drugs for smarter stem cells: making sense (sphingolipid-enhanced neural stem cells) of ceramide. Neurosignals 2008; 16: 124-139.
51. Bieberich E, Silva J, Wang G, Krishnamurthy K, Condie BG: Selective apoptosis of pluripotent mouse and human stem cells by novel ceramide analogues prevents teratoma formation and enriches for neural precursors in ES cell-derived neural transplants. J Cell Biol 2004; 167: 723-734.
52. Brimble SN, Sherrer ES, Uhl EW, Wang E, Kelly S, Merrill AH Jr, Robins AJ, Schulz TC: The cell surface glycosphingolipids SSEA-3 and SSEA-4 are not essential for human ESC pluripotency. Stem Cells 2007; 25: 54-62.
53. Pebay A, Wong RC, Pitson SM, Wolvetang EJ, Peh GS, Filipczyk A, Koh KL, Tellis I, Nguyen LT, Pera MF: Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells 2005; 23: 1541-1548.
54. Inniss K, Moore H: Mediation of apoptosis and proliferation of human embryonic stem cells by sphingosine-1-phosphate. Stem Cells Dev 2006; 15: 789-796.
55. Dottori M, Leung J, Turnley AM, Pebay A: Lysophosphatidic acid inhibits neuronal differentiation of neural stem/progenitor cells derived from human embryonic stem cells. Stem Cells 2008; 26: 1146-1154.
56. Wong RC, Tellis I, Jamshidi P, Pera M, Pebay A: Anti-apoptotic effect of sphingosine-1-phosphate and platelet-derived growth factor in human embryonic stem cells. Stem Cells Dev 2007; 16: 989-1001.
57. Avery K, Avery S, Shepherd J, Heath PR, Moore H: Sphingosine-1-phosphate mediates transcriptional regulation of key targets associated with survival, proliferation, and pluripotency in human embryonic stem cells. Stem Cells Dev 2008; 17: 1195-1205.
58. James D, Levine AJ, Besser D, Hemmati-Brivanlou A: TGFbeta/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 2005; 132: 1273-1282.
59. Garcia-Gonzalo FR, Belmonte JC: Albuminassociated lipids regulate human embryonic stem cell self-renewal. PLoS One 2008; 3: e1384.
60. Salli U, Fox TE, Carkaci-Salli N, Sharma A, Robertson GP, Kester M, Vrana K: Propagation of undifferentiated human embryonic stem cells with nano-liposomal ceramide. Stem Cells Dev 2008; Epub ahead of print.
61. Takahashi K, Yamanaka S: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-676.
62. Okita K, Ichisaka T, Yamanaka S: Generation of germline-competent induced pluripotent stem cells. Nature 2007; 448: 313-317.
63. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ: Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008; 451: 141-146.
64. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
65. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA: Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-1920.
66. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S: Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008; 26: 101-106.
67. Harada J, Foley M, Moskowitz MA, Waeber C: Sphingosine-1-phosphate induces proliferation and morphological changes of neural progenitor cells. J Neurochem 2004; 88: 1026-1039.
68. Rhee HJ, Nam JS, Sun Y, Kim MJ, Choi HK, Han DH, Kim NH, Huh SO: Lysophosphatidic acid stimulates cAMP accumulation and cAMP response element-binding protein phosphorylation in immortalized hippocampal progenitor cells. Neuroreport 2006; 17: 523-526.
69. Kimura A, Ohmori T, Ohkawa R, Madoiwa S, Mimuro J, Murakami T, Kobayashi E, Hoshino Y, Yatomi Y, Sakata Y: Essential roles of sphingosine 1-phosphate/S1P1 receptor axis in the migration of neural stem cells toward a site of spinal cord injury. Stem Cells 2007; 25: 115-124.
70. Kimura A, Ohmori T, Kashiwakura Y, Ohkawa R, Madoiwa S, Mimuro J, Shimazaki K, Hoshino Y, Yatomi Y, Sakata Y: Antagonism of sphingosine 1-phosphate receptor-2 enhances migration of neural progenitor cells toward an area of brain. Stroke 2008; 39: 3411-3417.
71. Svetlov SI, Ignatova TN, Wang KK, Hayes RL, English D, Kukekov VG: Lysophosphatidic acid induces clonal generation of mouse neurospheres via proliferation of Sca-1-and AC133-positive neural progenitors. Stem Cells Dev 2004; 13: 685-693.
72. Shin S, Mitalipova M, Noggle S, Tibbitts D, Venable A, Rao R, Stice SL: Long-term proliferation of human embryonic stem cell-derived neuroepithelial cells using defined adherent culture conditions. Stem Cells 2006; 24: 125-138.
73. Hurst JH, Mumaw J, Machacek DW, Sturkie C, Callihan P, Stice SL, Hooks SB: Human neural progenitors express functional lysophospholipid receptors that regulate cell growth and morphology. BMC Neurosci 2008; 9: 118.
74. Lee CW, Rivera R, Dubin AE, Chun J: LPA 4 / GPR23 is a lysophosphatidic acid (LPA) receptor utilizing G s -, G q /G i -mediated calcium signaling and G 12/13 -mediated Rho activation. J Biol Chem 2007; 282: 4310-4317.
75. Noguchi K, Ishii S, Shimizu T: Identification of p2y9/GPR23 as a novel G protein-coupled receptor for lysophosphatidic acid, structurally distant from the Edg family. J Biol Chem 2003; 278: 25600-25606.
76. Dawson J, Hotchin N, Lax S, Rumsby M: Lysophosphatidic acid induces process retraction in CG-4 line oligodendrocytes and oligodendrocyte precursor cells but not in differentiated oligodendrocytes. J Neurochem 2003; 87: 947-957.
77. Jaillard C, Harrison S, Stankoff B, Aigrot MS, Calver AR, Duddy G, Walsh FS, Pangalos MN, Arimura N, Kaibuchi K, Zalc B, Lubetzki C: Edg8/S1P5: an oligodendroglial receptor with dual function on process retraction and cell survival. J Neurosci 2005; 25: 1459-1469.
78. Novgorodov AS, El-Alwani M, Bielawski J, Obeid LM, Gudz TI: Activation of sphingosine-1-phosphate receptor S1P5 inhibits oligodendrocyte progenitor migration. FASEB J 2007; 21: 1503-1514.
79. Terai K, Soga T, Takahashi M, Kamohara M, Ohno K, Yatsugi S, Okada M, Yamaguchi T: Edg-8 receptors are preferentially expressed in oligodendrocyte lineage cells of the rat CNS. Neuroscience 2003; 116: 1053-1062.
80. Miron VE, Jung CG, Kim HJ, Kennedy TE, Soliven B, Antel JP: FTY720 modulates human oligodendrocyte progenitor process extension and survival. Ann Neurol 2008; 63: 61-71.
81. Moller T, Contos JJ, Musante DB, Chun J, Ransom BR: Expression and function of lysophosphatidic acid receptors in cultured rodent microglial cells. J Biol Chem 2001; 276: 25946-25952.
82. Tham CS, Lin FF, Rao TS, Yu N, Webb M: Microglial activation state and lysophospholipid acid receptor expression. Int J Dev Neurosci 2003; 21: 431-443.
83. Pebay A, Torrens Y, Toutant M, Cordier J, Glowinski J, Tence M: Pleiotropic effects of lysophosphatidic acid on striatal astrocytes. Glia 1999; 28: 25-33.
84. Pebay A, Toutant M, Premont J, Calvo CF, Venance L, Cordier J, Glowinski J, Tence M: Sphingosine-1-phosphate induces proliferation of astrocytes: regulation by intracellular signalling cascades. Eur J Neurosci 2001; 13: 2067-2076.
85. Rouach N, Pebay A, Meme W, Cordier J, Ezan P, Etienne E, Giaume C, Tence M: S1P inhibits gap junctions in astrocytes: involvement of G and Rho GTPase/ROCK. Eur J Neurosci 2006; 23: 1453-1464.
86. Keller JN, Steiner MR, Mattson MP, Steiner SM: Lysophosphatidic acid decreases glutamate and glucose uptake by astrocytes. J Neurochem 1996; 67: 2300-2305.
87. Keller JN, Steiner MR, Holtsberg FW, Mattson MP, Steiner SM: Lysophosphatidic acidinduced proliferation-related signals in astrocytes. J Neurochem 1997; 69: 1073-1084.
88. Weiner JA, Hecht JH, Chun J: Lysophosphatidic acid receptor gene vzg-1/lpA1/edg-2 is expressed by mature oligodendrocytes during myelination in the postnatal murine brain. J Comp Neurol 1998; 398: 587-598.
89. Li Y, Gonzalez MI, Meinkoth JL, Field J, Kazanietz MG, Tennekoon GI: Lysophosphatidic acid promotes survival and differentiation of rat Schwann cells. J Biol Chem 2003; 278: 9585-9591.
90. Jalink K, Eichholtz T, Postma FR, van Corven EJ, Moolenaar WH: Lysophosphatidic acid induces neuronal shape changes via a novel, receptor-mediated signaling pathway: similarity to thrombin action. Cell Growth Differ 1993; 4: 247-255.
91. Fukushima N: LPA in neural cell development. J Cell Biochem 2004; 92: 993-1003.
92. Kingsbury MA, Rehen SK, Contos JJ, Higgins CM, Chun J: Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding. Nat Neurosci 2003; 6: 1292-1299.
93. Fukushima N, Shano S, Moriyama R, Chun J: Lysophosphatidic acid stimulates neuronal differentiation of cortical neuroblasts through the LPA1-G(i/o) pathway. Neurochem Int 2007; 50: 302-307.
94. Saini HS, Coelho RP, Goparaju SK, Jolly PS, Maceyka M, Spiegel S, Sato-Bigbee C: Novel role of sphingosine kinase 1 as a mediator of neurotrophin-3 action in oligodendrocyte progenitors. J Neurochem 2005; 95: 1298-1310.
95. Fukushima N, Weiner JA, Chun J: Lysophosphatidic acid (LPA) is a novel extracellular regulator of cortical neuroblast morphology. Dev Biol 2000; 228: 6-18.
96. Kingsbury MA, Rehen SK, Ye X, Chun J: Genetics and cell biology of lysophosphatidic acid receptor-mediated signaling during cortical neurogenesis. J Cell Biochem 2004; 92: 1004-1012.
97. Bassi R, Anelli V, Giussani P, Tettamanti G, Viani P, Riboni L: Sphingosine-1-phosphate is released by cerebellar astrocytes in response to bFGF and induces astrocyte proliferation through Gi-protein-coupled receptors. Glia 2006; 53: 621-630.
98. Contos JJ, Fukushima N, Weiner JA, Kaushal D, Chun J: Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior. Proc Natl Acad Sci USA 2000; 97: 13384-13389.
99. Hecht JH, Weiner JA, Post SR, Chun J: Ventricular zone gene-1 (vzg-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex. J Cell Biol 1996; 135: 1071-1083.
100. Dubin AE, Bahnson T, Weiner JA, Fukushima N, Chun J: Lysophosphatidic acid stimulates neurotransmitter-like conductance changes that precede GABA and L -glutamate in early, presumptive cortical neuroblasts. J Neurosci 1999; 19: 1371-1381.
101. Reynolds BA, Rietze RL: Neural stem cells and neurospheres -re-evaluating the relationship. Nat Methods 2005; 2: 333-336.
102. Reynolds BA, Weiss S: Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992; 255: 1707-1710.
103. Cui HL, Qiao JT: Promotive action of lysophosphatidic acid on proliferation of rat embryonic neural stem cells and their differentiation to cholinergic neurons in vitro. Sheng Li Xue Bao 2006; 58: 547-555.
104. Baumann N, Pham-Dinh D: Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 2001; 81: 871-927.
105. Miron VE, Hall JA, Kennedy TE, Soliven B, Antel JP: Cyclical and dose-dependent responses of adult human mature oligodendrocytes to fingolimod. Am J Pathol 2008; 173: 1143-1152.
106. Coelho RP, Payne SG, Bittman R, Spiegel S, Sato-Bigbee C: The immunomodulator FTY720 has a direct cytoprotective effect in oligodendrocyte progenitors. J Pharmacol Exp Ther 2007; 323: 626-635.
107. Saini HS, Gorse KM, Boxer LM, Sato-Bigbee C: Neurotrophin-3 and a CREB-mediated signaling pathway regulate Bcl-2 expression in oligodendrocyte progenitor cells. J Neurochem 2004; 89: 951-961.
108. Bieberich E, MacKinnon S, Silva J, Yu RK: Regulation of apoptosis during neuronal differentiation by ceramide and b-series complex gangliosides. J Biol Chem 2001; 276: 44396-44404.
109. Wang G, Krishnamurthy K, Chiang YW, Dasgupta S, Bieberich E: Regulation of neural progenitor cell motility by ceramide and potential implications for mouse brain development. J Neurochem 2008; 106: 718-733.
110. Bieberich E: Ceramide signaling in cancer and stem cells. Future Lipidol 2008; 3: 273-300.
111. Steiner MR, Urso JR, Klein J, Steiner SM: Multiple astrocyte responses to lysophosphatidic acids. Biochim Biophys Acta 2002; 1582: 154-160.
112. Eichholtz T, Jalink K, Fahrenfort I, Moolenaar WH: The bioactive phospholipid lysophosphatidic acid is released from activated platelets. Biochem J 1993; 291: 677-680.
113. Tigyi G, Hong L, Yakubu M, Parfenova H, Shibata M, Leffler CW: Lysophosphatidic acid alters cerebrovascular reactivity in piglets. Am J Physiol 1995; 268:H2048-H2055.
114. Savaskan NE, Rocha L, Kotter MR, Baer A, Lubec G, van Meeteren LA, Kishi Y, Aoki J, Moolenaar WH, Nitsch R, Brauer AU: Autotaxin (NPP-2) in the brain: Cell type-specific expression and regulation during development and after neurotrauma. Cell Mol Life Sci 2007; 64: 230-243.
115. Sorensen SD, Nicole O, Peavy RD, Montoya LM, Lee CJ, Murphy TJ, Traynelis SF, Hepler JR: Common signaling pathways link activation of murine PAR-1, LPA, and S1P receptors to proliferation of astrocytes. Mol Pharmacol 2003; 64: 1199-1209.
116. Elmes SJ, Millns PJ, Smart D, Kendall DA, Chapman V: Evidence for biological effects of exogenous LPA on rat primary afferent and spinal cord neurons. Brain Res 2004; 1022: 205-213.
117. Fujita R, Kiguchi N, Ueda H: LPA-mediated demyelination in ex vivo culture of dorsal root. Neurochem Int 2007; 50: 351-355.
118. Ueda H: Molecular mechanisms of neuropathic pain-phenotypic switch and initiation mechanisms. Pharmacol Ther 2006; 109: 57-77.
119. Renback K, Inoue M, Ueda H: Lysophosphatidic acid-induced, pertussis toxin-sensitive nociception through a substance P release from peripheral nerve endings in mice. Neurosci Lett 1999; 270: 59-61.
120. Renback K, Inoue M, Yoshida A, Nyberg F, Ueda H: Vzg-1/lysophosphatidic acid-receptor involved in peripheral pain transmission. Brain Res Mol Brain Res 2000; 75: 350-354.
121. Inoue M, Rashid MH, Fujita R, Contos JJ, Chun J, Ueda H: Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat Med 2004; 10: 712-718.
122. Holtsberg FW, Steiner MR, Keller JN, Mark RJ, Mattson MP, Steiner SM: Lysophosphatidic acid induces necrosis and apoptosis in hippocampal neurons. J Neurochem 1998; 70: 66-76.
123. Brault S, Gobeil F Jr, Fortier A, Honore JC, Joyal JS, Sapieha PS, Kooli A, Martin E, Hardy P, Ribeiro-Da-Silva A, Peri K, Lachapelle P, Varma D, Chemtob S: Lysophosphatidic acid induces endothelial cell death by modulating the redox environment. Am J Physiol Regul Integr Comp Physiol 2007; 292:R1174-R1183.
124. Edsall LC, Spiegel S: Enzymatic measurement of sphingosine 1-phosphate. Anal Biochem 1999; 272: 80-86.
125. Annabi B, Lachambre MP, Plouffe K, Sartelet H, Béliveau R: Modulation of invasive properties of CD133(+) glioblastoma stem cells: a role for MT1-mmp in bioactive lysophospholipid signaling. Mol Carcinog 2009; Epub ahead of print.
126. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS: Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006; 5: 67.
127. Van Brocklyn JR, Jackson CA, Pearl DK, Kotur MS, Snyder PJ, Prior TW: Sphingosine kinase-1 expression correlates with poor survival of patients with glioblastoma multiforme: roles of sphingosine kinase isoforms in growth of glioblastoma cell lines. J Neuropathol Exp Neurol 2005; 64: 695-705.
128. Hoelzinger DB, Mariani L, Weis J, Woyke T, Berens TJ, McDonough WS, Sloan A, Coons SW, Berens ME: Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets. Neoplasia 2005; 7: 7-16.
129. Kishi Y, Okudaira S, Tanaka M, Hama K, Shida D, Kitayama J, Yamori T, Aoki J, Fujimaki T, Arai H: Autotaxin is overexpressed in glioblastoma multiforme and contributes to cell motility of glioblastoma by converting lysophosphatidylcholine to lysophosphatidic acid. J Biol Chem 2006; 281: 17492-17500.
130. Li J, Guan HY, Gong LY, Song LB, Zhang N, Wu J, Yuan J, Zheng YJ, Huang ZS, Li M: Clinical significance of sphingosine kinase-1 expression in human astrocytomas progression and overall patient survival. Clin Cancer Res 2008; 14: 6996-7003.
131. Paugh BS, Bryan L, Paugh SW, Wilczynska KM, Alvarez SM, Singh SK, Kapitonov D, Rokita H, Wright S, Griswold-Prenner I, Milstien S, Spiegel S, Kordula T: Interleukin-1 regulates the expression of sphingosine kinase 1 in glioblastoma cells. J Biol Chem 2009; 284: 3408-3417.
132. Hoelzinger DB, Nakada M, Demuth T, Rosensteel T, Reavie LB, Berens ME: Autotaxin: a secreted autocrine/paracrine factor that promotes glioma invasion. J Neurooncol 2008; 86: 297-309.
133. Gaetano CG, Samadi N, Tomsig JL, Macdonald TL, Lynch KR, Brindley DN: Inhibition of autotaxin production or activity blocks lysophosphatidylcholine- induced migration of human breast cancer and melanoma cells. Mol Carcinog 2009; Epub ahead of print.