Lysophospholipids and their receptors in the central nervous system

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 1, 2013, Pages 20-32

  Choi, Ji Woong ^a,b   Chun, Jerold ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Gachon University College of Medicine   (South Korea)

Author keywords

Central nervous system; CNS disease; G protein coupled receptor; Lysophosphatidic acid; Sphingosine 1 phosphate

Indexed keywords

FINGOLIMOD; LYSOPHOSPHOLIPID; LYSOPHOSPHOLIPID RECEPTOR; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

ALZHEIMER DISEASE; APOPTOSIS; ASTROCYTE; BIOLOGICAL ACTIVITY; BRAIN; BRAIN ISCHEMIA; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; DRUG EFFICACY; DRUG TARGETING; FETUS HYPOXIA; HEARING IMPAIRMENT; HUMAN; HYDROCEPHALUS; MICROGLIA; MULTIPLE SCLEROSIS; NERVE CELL; NERVOUS SYSTEM INJURY; NEURAL PROGENITOR CELL; NEUROPATHIC PAIN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; SEIZURE; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD INJURY; STEM CELL; UPREGULATION;

CENTRAL NERVOUS SYSTEM; HUMANS; LYSOPHOSPHOLIPIDS; NERVOUS SYSTEM DISEASES; RECEPTORS, LYSOPHOSPHOLIPID; RECEPTORS, LYSOSPHINGOLIPID;

EID: 84868576848     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2012.07.015     Document Type: Review

References (206)

1. J.W. Choi, D.R. Herr, K. Noguchi, Y.C. Yung, C.W. Lee, T. Mutoh, M.E. Lin, S.T. Teo, K.E. Park, A.N. Mosley, and J. Chun LPA receptors: subtypes and biological actions Annu. Rev. Pharmacol. Toxicol. 50 2010 157 186
2. J. Chun, T. Hla, K.R. Lynch, S. Spiegel, and W.H. Moolenaar International Union of Basic and Clinical Pharmacology. LXXVIII. Lysophospholipid receptor nomenclature Pharmacol. Rev. 62 2010 579 587
3. I. Ishii, N. Fukushima, X. Ye, and J. Chun Lysophospholipid receptors: signaling and biology Annu. Rev. Biochem. 73 2004 321 354
4. T. Mutoh, R. Rivera, and J. Chun Insights into the pharmacological relevance of lysophospholipid receptors Br. J. Pharmacol. 165 2012 829 844
5. J.W. Choi, C.W. Lee, and J. Chun Biological roles of lysophospholipid receptors revealed by genetic null mice: an update Biochim. Biophys. Acta 1781 2008 531 539
6. C.A. Foster, L.M. Howard, A. Schweitzer, E. Persohn, P.C. Hiestand, B. Balatoni, R. Reuschel, C. Beerli, M. Schwartz, and A. Billich Brain penetration of the oral immunomodulatory drug FTY720 and its phosphorylation in the central nervous system during experimental autoimmune encephalomyelitis: consequences for mode of action in multiple sclerosis J. Pharmacol. Exp. Ther. 323 2007 469 475
7. N. Fukushima, I. Ishii, J.J. Contos, J.A. Weiner, and J. Chun Lysophospholipid receptors Annu. Rev. Pharmacol. Toxicol. 41 2001 507 534
8. K.K. Dev, F. Mullershausen, H. Mattes, R.R. Kuhn, G. Bilbe, D. Hoyer, and A. Mir Brain sphingosine-1-phosphate receptors: implication for FTY720 in the treatment of multiple sclerosis Pharmacol. Ther. 117 2008 77 93
9. D.R. Herr, and J. Chun Effects of LPA and S1P on the nervous system and implications for their involvement in disease Curr. Drug Targets 8 2007 155 167
10. K. Noguchi, and J. Chun Roles for lysophospholipid S1P receptors in multiple sclerosis Crit. Rev. Biochem. Mol. Biol. 46 2011 2 10
11. K. Noguchi, D. Herr, T. Mutoh, and J. Chun Lysophosphatidic acid (LPA) and its receptors Curr. Opin. Pharmacol. 9 2009 15 23
12. V. Brinkmann, A. Billich, T. Baumruker, P. Heining, R. Schmouder, G. Francis, S. Aradhye, and P. Burtin Fingolimod (FTY720): discovery and development of an oral drug to treat multiple sclerosis Nat. Rev. Drug Discov. 9 2010 883 897
13. J. Chun, and V. Brinkmann A mechanistically novel, first oral therapy for multiple sclerosis: the development of fingolimod (FTY720, Gilenya) Discov. Med. 12 2011 213 228
14. S.M. Harrison, C. Reavill, G. Brown, J.T. Brown, J.E. Cluderay, B. Crook, C.H. Davies, L.A. Dawson, E. Grau, C. Heidbreder, P. Hemmati, G. Hervieu, A. Howarth, Z.A. Hughes, A.J. Hunter, J. Latcham, S. Pickering, P. Pugh, D.C. Rogers, C.S. Shilliam, and P.R. Maycox LPA1 receptor-deficient mice have phenotypic changes observed in psychiatric disease Mol. Cell. Neurosci. 24 2003 1170 1179
15. K.J. Herr, D.R. Herr, C.W. Lee, K. Noguchi, and J. Chun Stereotyped fetal brain disorganization is induced by hypoxia and requires lysophosphatidic acid receptor 1 (LPA1) signaling Proc. Natl. Acad. Sci. U. S. A. 108 2011 15444 15449
16. Y.C. Yung, T. Mutoh, M.E. Lin, K. Noguchi, R.R. Rivera, J.W. Choi, M.A. Kingsbury, and J. Chun Lysophosphatidic acid signaling may initiate fetal hydrocephalus Sci. Transl. Med. 3 2011 99ra87
17. M. Inoue, M.H. Rashid, R. Fujita, J.J. Contos, J. Chun, and H. Ueda Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling Nat. Med. 10 2004 712 718
18. J. Nagai, H. Uchida, Y. Matsushita, R. Yano, M. Ueda, M. Niwa, J. Aoki, J. Chun, and H. Ueda Autotaxin and lysophosphatidic acid1 receptor-mediated demyelination of dorsal root fibers by sciatic nerve injury and intrathecal lysophosphatidylcholine Mol. Pain 6 2010 78
19. M.E. Lin, R.R. Rivera, and J. Chun Targeted deletion of LPA5 identifies novel roles for lysophosphatidic acid signaling in development of neuropathic pain J. Biol. Chem. 287 2012 17608 17617
20. Z.G. Li, Z.C. Yu, D.Z. Wang, W.P. Ju, X. Zhan, Q.Z. Wu, X.J. Wu, H.M. Cong, and H.H. Man Influence of acetylsalicylate on plasma lysophosphatidic acid level in patients with ischemic cerebral vascular diseases Neurol. Res. 30 2008 366 369
21. B. Czech, W. Pfeilschifter, N. Mazaheri-Omrani, M.A. Strobel, T. Kahles, T. Neumann-Haefelin, A. Rami, A. Huwiler, and J. Pfeilschifter The immunomodulatory sphingosine 1-phosphate analog FTY720 reduces lesion size and improves neurological outcome in a mouse model of cerebral ischemia Biochem. Biophys. Res. Commun. 389 2009 251 256
22. T. Frugier, D. Crombie, A. Conquest, F. Tjhong, C. Taylor, T. Kulkarni, C. McLean, and A. Pebay Modulation of LPA receptor expression in the human brain following neurotrauma Cell. Mol. Neurobiol. 31 2011 569 577
23. A.J. MacLennan, S.J. Benner, A. Andringa, A.H. Chaves, J.L. Rosing, R. Vesey, A.M. Karpman, S.A. Cronier, N. Lee, L.C. Erway, and M.L. Miller The S1P2 sphingosine 1-phosphate receptor is essential for auditory and vestibular function Hear. Res. 220 2006 38 48
24. D.R. Herr, N. Grillet, M. Schwander, R. Rivera, U. Muller, and J. Chun Sphingosine 1-phosphate (S1P) signaling is required for maintenance of hair cells mainly via activation of S1P2 J. Neurosci. 27 2007 1474 1478
25. M. Kono, I.A. Belyantseva, A. Skoura, G.I. Frolenkov, M.F. Starost, J.L. Dreier, D. Lidington, S.S. Bolz, T.B. Friedman, T. Hla, and R.L. Proia Deafness and stria vascularis defects in S1P2 receptor-null mice J. Biol. Chem. 282 2007 10690 10696
26. A.J. MacLennan, P.R. Carney, W.J. Zhu, A.H. Chaves, J. Garcia, J.R. Grimes, K.J. Anderson, S.N. Roper, and N. Lee An essential role for the H218/AGR16/Edg-5/LP(B2) sphingosine 1-phosphate receptor in neuronal excitability Eur. J. Neurosci. 14 2001 203 209
27. T. Trimbuch, P. Beed, J. Vogt, S. Schuchmann, N. Maier, M. Kintscher, J. Breustedt, M. Schuelke, N. Streu, O. Kieselmann, I. Brunk, G. Laube, U. Strauss, A. Battefeld, H. Wende, C. Birchmeier, S. Wiese, M. Sendtner, H. Kawabe, M. Kishimoto-Suga, N. Brose, J. Baumgart, B. Geist, J. Aoki, N.E. Savaskan, A.U. Brauer, J. Chun, O. Ninnemann, D. Schmitz, and R. Nitsch Synaptic PRG-1 modulates excitatory transmission via lipid phosphate-mediated signaling Cell 138 2009 1222 1235
28. N. Akahoshi, Y. Ishizaki, H. Yasuda, Y.L. Murashima, T. Shinba, K. Goto, T. Himi, J. Chun, and I. Ishii Frequent spontaneous seizures followed by spatial working memory/anxiety deficits in mice lacking sphingosine 1-phosphate receptor 2 Epilepsy Behav. 22 2011 659 665
29. Y.P. Wu, K. Mizugishi, M. Bektas, R. Sandhoff, and R.L. Proia Sphingosine kinase 1/S1P receptor signaling axis controls glial proliferation in mice with Sandhoff disease Hum. Mol. Genet. 17 2008 2257 2264
30. J.H. Hecht, J.A. Weiner, S.R. Post, and J. Chun Ventricular zone gene-1 (vzg-1) encodes a lysophosphatidic acid receptor expressed in neurogenic regions of the developing cerebral cortex J. Cell Biol. 135 1996 1071 1083
31. J. Chun How the lysophospholipid got its receptor The Scientist 21 2007 48 54
32. M. Lee, J. Van Brocklyn, S. Thangada, C. Liu, A. Hand, R. Menzeleev, S. Spiegel, and T. Hla Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1 Science 279 1998 1552 1555
33. G.C. Zondag, F.R. Postma, I.V. Etten, I. Verlaan, and W.H. Moolenaar Sphingosine 1-phosphate signalling through the G-protein-coupled receptor Edg-1 Biochem. J. 330 1998 605 609
34. S. An, T. Bleu, W. Huang, O.G. Hallmark, S.R. Coughlin, and E.J. Goetzl Identification of cDNAs encoding two G protein-coupled receptors for lysosphingolipids FEBS Lett. 417 1997 279 282
35. K. Bandoh, J. Aoki, H. Hosono, S. Kobayashi, T. Kobayashi, K. Murakami-Murofushi, M. Tsujimoto, H. Arai, and K. Inoue Molecular cloning and characterization of a novel human G-protein-coupled receptor, EDG7, for lysophosphatidic acid J. Biol. Chem. 274 1999 27776 27785
36. J.J. Contos, and J. Chun Genomic characterization of the lysophosphatidic acid receptor gene, lp(A2)/Edg4, and identification of a frameshift mutation in a previously characterized cDNA Genomics 64 2000 155 169
37. K. Kotarsky, A. Boketoft, J. Bristulf, N.E. Nilsson, A. Norberg, S. Hansson, C. Owman, R. Sillard, L.M. Leeb-Lundberg, and B. Olde Lysophosphatidic acid binds to and activates GPR92, a G protein-coupled receptor highly expressed in gastrointestinal lymphocytes J. Pharmacol. Exp. Ther. 318 2006 619 628
38. C.W. Lee, R. Rivera, A.E. Dubin, and J. Chun 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. 282 2007 4310 4317
39. C.W. Lee, R. Rivera, S. Gardell, A.E. Dubin, and J. Chun GPR92 as a new G12/13- and Gq-coupled lysophosphatidic acid receptor that increases cAMP, LPA5 J. Biol. Chem. 281 2006 23589 23597
40. K. Noguchi, S. Ishii, and T. Shimizu Identification of p2y9/GPR23 as a novel G protein-coupled receptor for Lysophosphatidic acid, structurally distant from the Edg family J. Biol. Chem. 278 2003 25600 25606
41. S.M. Pasternack, I. von Kugelgen, K.A. Aboud, Y.A. Lee, F. Ruschendorf, K. Voss, A.M. Hillmer, G.J. Molderings, T. Franz, A. Ramirez, P. Nurnberg, M.M. Nothen, and R.C. Betz G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth Nat. Genet. 40 2008 329 334
42. M.E. Lin, R.R. Rivera, and J. Chun Targeted deletion of LPA5 identifies novel roles for LPA signaling in the development of neuropathic pain J. Biol. Chem. 287 2012 17608 17617
43. J.J. Contos, I. Ishii, and J. Chun Lysophosphatidic acid receptors Mol. Pharmacol. 58 2000 1188 1196
44. H. Ohuchi, A. Hamada, H. Matsuda, A. Takagi, M. Tanaka, J. Aoki, H. Arai, and S. Noji Expression patterns of the lysophospholipid receptor genes during mouse early development Dev. Dyn. 237 2008 3280 3294
45. J.J. Contos, and J. Chun The mouse lp(A3)/Edg7 lysophosphatidic acid receptor gene: genomic structure, chromosomal localization, and expression pattern Gene 267 2001 243 253
46. J.A. Weiner, J.H. Hecht, and J. Chun Lysophosphatidic acid receptor gene vzg-1/lpA1/edg-2 is expressed by mature oligodendrocytes during myelination in the postnatal murine brain J. Comp. Neurol. 398 1998 587 598
47. Y. Goldshmit, K. Munro, S.Y. Leong, A. Pebay, and A.M. Turnley LPA receptor expression in the central nervous system in health and following injury Cell Tissue Res. 341 2010 23 32
48. S.I. Savitz, M.S. Dhallu, S. Malhotra, A. Mammis, L.C. Ocava, P.S. Rosenbaum, and D.M. Rosenbaum EDG receptors as a potential therapeutic target in retinal ischemia-reperfusion injury Brain Res. 1118 2006 168 175
49. A.E. Dubin, T. Bahnson, J.A. Weiner, N. Fukushima, and J. Chun Lysophosphatidic acid stimulates neurotransmitter-like conductance changes that precede GABA and l-glutamate in early, presumptive cortical neuroblasts J. Neurosci. 19 1999 1371 1381
50. A.E. Dubin, D.R. Herr, and J. Chun Diversity of lysophosphatidic acid receptor-mediated intracellular calcium signaling in early cortical neurogenesis J. Neurosci. 30 2010 7300 7309
51. N. Fukushima, J.A. Weiner, D. Kaushal, J.J. Contos, S.K. Rehen, M.A. Kingsbury, K.Y. Kim, and J. Chun Lysophosphatidic acid influences the morphology and motility of young, postmitotic cortical neurons Mol. Cell. Neurosci. 20 2002 271 282
52. T. Moller, J.J. Contos, D.B. Musante, J. Chun, and B.R. Ransom Expression and function of lysophosphatidic acid receptors in cultured rodent microglial cells J. Biol. Chem. 276 2001 25946 25952
53. C.S. Tham, F.F. Lin, T.S. Rao, N. Yu, and M. Webb Microglial activation state and lysophospholipid acid receptor expression Int. J. Dev. Neurosci. 21 2003 431 443
54. J. Allard, S. Barron, J. Diaz, C. Lubetzki, B. Zalc, J.C. Schwartz, and P. Sokoloff A rat G protein-coupled receptor selectively expressed in myelin-forming cells Eur. J. Neurosci. 10 1998 1045 1053
55. P. Cervera, M. Tirard, S. Barron, J. Allard, S. Trottier, J. Lacombe, C. Daumas-Duport, and P. Sokoloff Immunohistological localization of the myelinating cell-specific receptor LP(A1) Glia 38 2002 126 136
56. N. Yu, K.D. Lariosa-Willingham, F.F. Lin, M. Webb, and T.S. Rao Characterization of lysophosphatidic acid and sphingosine-1-phosphate-mediated signal transduction in rat cortical oligodendrocytes Glia 45 2004 17 27
57. V.E. Miron, J.A. Hall, T.E. Kennedy, B. Soliven, and J.P. Antel Cyclical and dose-dependent responses of adult human mature oligodendrocytes to fingolimod Am. J. Pathol. 173 2008 1143 1152
58. K. Terai, T. Soga, M. Takahashi, M. Kamohara, K. Ohno, S. Yatsugi, M. Okada, and T. Yamaguchi Edg-8 receptors are preferentially expressed in oligodendrocyte lineage cells of the rat CNS Neuroscience 116 2003 1053 1062
59. T.S. Rao, K.D. Lariosa-Willingham, F.F. Lin, N. Yu, C.S. Tham, J. Chun, and M. Webb Growth factor pre-treatment differentially regulates phosphoinositide turnover downstream of lysophospholipid receptor and metabotropic glutamate receptors in cultured rat cerebrocortical astrocytes Int. J. Dev. Neurosci. 22 2004 131 135
60. R. Van Doorn, J. Van Horssen, D. Verzijl, M. Witte, E. Ronken, B. Van Het Hof, K. Lakeman, C.D. Dijkstra, P. Van Der Valk, A. Reijerkerk, A.E. Alewijnse, S.L. Peters, and H.E. De Vries Sphingosine 1-phosphate receptor 1 and 3 are upregulated in multiple sclerosis lesions Glia 58 2010 1465 1476
61. C. McGiffert, J.J. Contos, B. Friedman, and J. Chun Embryonic brain expression analysis of lysophospholipid receptor genes suggests roles for s1p(1) in neurogenesis and s1p(1-3) in angiogenesis FEBS Lett. 531 2002 103 108
62. Z. Lee, C.T. Cheng, H. Zhang, M.A. Subler, J. Wu, A. Mukherjee, J.J. Windle, C.K. Chen, and X. Fang Role of LPA4/p2y9/GPR23 in negative regulation of cell motility Mol. Biol. Cell 19 2008 5435 5445
63. J.J. Contos, N. Fukushima, J.A. Weiner, D. Kaushal, and J. Chun Requirement for the lpA1 lysophosphatidic acid receptor gene in normal suckling behavior Proc. Natl. Acad. Sci. U. S. A. 97 2000 13384 13389
64. N. Fukushima, Y. Kimura, and J. Chun A single receptor encoded by vzg-1/lpA1/edg-2 couples to G proteins and mediates multiple cellular responses to lysophosphatidic acid Proc. Natl. Acad. Sci. U. S. A. 95 1998 6151 6156
65. N. Fukushima, S. Shano, R. Moriyama, and J. Chun Lysophosphatidic acid stimulates neuronal differentiation of cortical neuroblasts through the LPA1-G(i/o) pathway Neurochem. Int. 50 2007 302 307
66. M.A. Kingsbury, S.K. Rehen, J.J. Contos, C.M. Higgins, and J. Chun Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding Nat. Neurosci. 6 2003 1292 1299
67. S.I. Svetlov, T.N. Ignatova, K.K. Wang, R.L. Hayes, D. English, and V.G. Kukekov Lysophosphatidic acid induces clonal generation of mouse neurospheres via proliferation of Sca-1- and AC133-positive neural progenitors Stem Cells Dev. 13 2004 685 693
68. J.J. Contos, I. Ishii, N. Fukushima, M.A. Kingsbury, X. Ye, S. Kawamura, J.H. Brown, and J. Chun Characterization of lpa(2) (Edg4) and lpa(1)/lpa(2) (Edg2/Edg4) lysophosphatidic acid receptor knockout mice: signaling deficits without obvious phenotypic abnormality attributable to lpa(2) Mol. Cell. Biol. 22 2002 6921 6929
69. E. Blanco, A. Bilbao, M.J. Luque-Rojas, A. Palomino, F.J. Bermudez-Silva, J. Suarez, L.J. Santin, G. Estivill-Torrus, A. Gutierrez, J.A. Campos-Sandoval, F.J. Alonso-Carrion, J. Marquez, and F.R. de Fonseca Attenuation of cocaine-induced conditioned locomotion is associated with altered expression of hippocampal glutamate receptors in mice lacking LPA1 receptors Psychopharmacology (Berl) 220 2012 27 42
70. E. Castilla-Ortega, C. Hoyo-Becerra, C. Pedraza, J. Chun, F. Rodriguez De Fonseca, G. Estivill-Torrus, and L.J. Santin Aggravation of chronic stress effects on hippocampal neurogenesis and spatial memory in LPA receptor knockout mice PLoS One 6 2011 e25522
71. E. Castilla-Ortega, J. Sanchez-Lopez, C. Hoyo-Becerra, E. Matas-Rico, E. Zambrana-Infantes, J. Chun, F.R. De Fonseca, C. Pedraza, G. Estivill-Torrus, and L.J. Santin Exploratory, anxiety and spatial memory impairments are dissociated in mice lacking the LPA1 receptor Neurobiol. Learn. Mem. 94 2010 73 82
72. G. Estivill-Torrus, P. Llebrez-Zayas, E. Matas-Rico, L. Santin, C. Pedraza, I. De Diego, I. Del Arco, P. Fernandez-Llebrez, J. Chun, and F.R. De Fonseca Absence of LPA1 signaling results in defective cortical development Cereb. Cortex 18 2008 938 950
73. E. Matas-Rico, B. Garcia-Diaz, P. Llebrez-Zayas, D. Lopez-Barroso, L. Santin, C. Pedraza, A. Smith-Fernandez, P. Fernandez-Llebrez, T. Tellez, M. Redondo, J. Chun, F.R. De Fonseca, and G. Estivill-Torrus Deletion of lysophosphatidic acid receptor LPA1 reduces neurogenesis in the mouse dentate gyrus Mol. Cell. Neurosci. 39 2008 342 355
74. L.J. Santin, A. Bilbao, C. Pedraza, E. Matas-Rico, D. Lopez-Barroso, E. Castilla-Ortega, J. Sanchez-Lopez, R. Riquelme, I. Varela-Nieto, P. de la Villa, M. Suardiaz, J. Chun, F.R. De Fonseca, and G. Estivill-Torrus Behavioral phenotype of maLPA1-null mice: increased anxiety-like behavior and spatial memory deficits Genes Brain Behav. 8 2009 772 784
75. I. Ishii, J.J. Contos, N. Fukushima, and J. Chun Functional comparisons of the lysophosphatidic acid receptors, LP(A1)/VZG-1/EDG-2, LP(A2)/EDG-4, and LP(A3)/EDG-7 in neuronal cell lines using a retrovirus expression system Mol. Pharmacol. 58 2000 895 902
76. A. Kimura, T. Ohmori, Y. Kashiwakura, R. Ohkawa, S. Madoiwa, J. Mimuro, K. Shimazaki, Y. Hoshino, Y. Yatomi, and Y. Sakata Antagonism of sphingosine 1-phosphate receptor-2 enhances migration of neural progenitor cells toward an area of brain Stroke 39 2008 3411 3417
77. J. Harada, M. Foley, M.A. Moskowitz, and C. Waeber Sphingosine-1- phosphate induces proliferation and morphological changes of neural progenitor cells J. Neurochem. 88 2004 1026 1039
78. K. Mizugishi, T. Yamashita, A. Olivera, G.F. Miller, S. Spiegel, and R.L. Proia Essential role for sphingosine kinases in neural and vascular development Mol. Cell. Biol. 25 2005 11113 11121
79. S.K. Rehen, M.A. Kingsbury, B.S. Almeida, D.R. Herr, S. Peterson, and J. Chun A new method of embryonic culture for assessing global changes in brain organization J. Neurosci. Methods 158 2006 100 108
80. A. Kimura, T. Ohmori, R. Ohkawa, S. Madoiwa, J. Mimuro, T. Murakami, E. Kobayashi, Y. Hoshino, Y. Yatomi, and Y. Sakata 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 25 2007 115 124
81. J.W. Choi, S.E. Gardell, D.R. Herr, R. Rivera, C.W. Lee, K. Noguchi, S.T. Teo, Y.C. Yung, M. Lu, G. Kennedy, and J. Chun FTY720 (fingolimod) efficacy in an animal model of multiple sclerosis requires astrocyte sphingosine 1-phosphate receptor 1 (S1P1) modulation Proc. Natl. Acad. Sci. U. S. A. 108 2011 751 756
82. T. Eichholtz, K. Jalink, I. Fahrenfort, and W.H. Moolenaar The bioactive phospholipid lysophosphatidic acid is released from activated platelets Biochem. J. 291 1993 677 680
83. 1-3 are not required for the inhibitory effects of LPA on mouse retinal growth cones Eye Brain 2 2010 1 13
84. A.J. MacLennan, B.K. Devlin, L. Marks, A.A. Gaskin, K.L. Neitzel, and N. Lee Antisense studies in PC12 cells suggest a role for H218, a sphingosine 1-phosphate receptor, in growth-factor-induced cell-cell interaction and neurite outgrowth Dev. Neurosci. 22 2000 283 295
85. R.E. Toman, S.G. Payne, K.R. Watterson, M. Maceyka, N.H. Lee, S. Milstien, J.W. Bigbee, and S. Spiegel Differential transactivation of sphingosine-1-phosphate receptors modulates NGF-induced neurite extension J. Cell Biol. 166 2004 381 392
86. T. Kanno, T. Nishizaki, R.L. Proia, T. Kajimoto, S. Jahangeer, T. Okada, and S. Nakamura Regulation of synaptic strength by sphingosine 1-phosphate in the hippocampus Neuroscience 171 2010 973 980
87. Y. Pilpel, and M. Segal The role of LPA1 in formation of synapses among cultured hippocampal neurons J. Neurochem. 97 2006 1379 1392
88. H. Ueda Lysophosphatidic acid as the initiator of neuropathic pain Biol. Pharm. Bull. 34 2011 1154 1158
89. X.X. Chi, and G.D. Nicol The sphingosine 1-phosphate receptor, S1PR, plays a prominent but not exclusive role in enhancing the excitability of sensory neurons J. Neurophysiol. 104 2010 2741 2748
90. O. Coste, C. Brenneis, B. Linke, S. Pierre, C. Maeurer, W. Becker, H. Schmidt, W. Gao, G. Geisslinger, and K. Scholich Sphingosine 1-phosphate modulates spinal nociceptive processing J. Biol. Chem. 283 2008 32442 32451
91. S.J. Elmes, P.J. Millns, D. Smart, D.A. Kendall, and V. Chapman Evidence for biological effects of exogenous LPA on rat primary afferent and spinal cord neurons Brain Res. 1022 2004 205 213
92. E. Norman, R.G. Cutler, R. Flannery, Y. Wang, and M.P. Mattson Plasma membrane sphingomyelin hydrolysis increases hippocampal neuron excitability by sphingosine-1-phosphate mediated mechanisms J. Neurochem. 114 2010 430 439
93. L.J. Sim-Selley, P.B. Goforth, M.U. Mba, T.L. Macdonald, K.R. Lynch, S. Milstien, S. Spiegel, L.S. Satin, S.P. Welch, and D.E. Selley Sphingosine-1-phosphate receptors mediate neuromodulatory functions in the CNS J. Neurochem. 110 2009 1191 1202
94. T. Kajimoto, T. Okada, H. Yu, S.K. Goparaju, S. Jahangeer, and S. Nakamura Involvement of sphingosine-1-phosphate in glutamate secretion in hippocampal neurons Mol. Cell. Biol. 27 2007 3429 3440
95. T. Kanno, and T. Nishizaki Endogenous sphingosine 1-phosphate regulates spontaneous glutamate release from mossy fiber terminals via S1P(3) receptors Life Sci. 89 2011 137 140
96. C. Roberts, P. Winter, C.S. Shilliam, Z.A. Hughes, C. Langmead, P.R. Maycox, and L.A. Dawson Neurochemical changes in LPA1 receptor deficient mice - a putative model of schizophrenia Neurochem. Res. 30 2005 371 377
97. L. Musazzi, E. Di Daniel, P. Maycox, G. Racagni, and M. Popoli Abnormalities in alpha/beta-CaMKII and related mechanisms suggest synaptic dysfunction in hippocampus of LPA1 receptor knockout mice Int. J. Neuropsychopharmacol. 14 2011 941 953
98. S.D. Sorensen, O. Nicole, R.D. Peavy, L.M. Montoya, C.J. Lee, T.J. Murphy, S.F. Traynelis, and J.R. Hepler Common signaling pathways link activation of murine PAR-1, LPA, and S1P receptors to proliferation of astrocytes Mol. Pharmacol. 64 2003 1199 1209
99. T.C.S. e Spohr, J.W. Choi, S.E. Gardell, D.R. Herr, S.K. Rehen, F.C. Gomes, and J. Chun Lysophosphatidic acid receptor-dependent secondary effects via astrocytes promote neuronal differentiation J. Biol. Chem. 283 2008 7470 7479
100. T.C.S. e Spohr, R.S. Dezonne, S.K. Rehen, and F.C. Gomes Astrocytes treated by lysophosphatidic acid induce axonal outgrowth of cortical progenitors through extracellular matrix protein and epidermal growth factor signaling pathway J. Neurochem. 119 2011 113 123
101. S. Shano, R. Moriyama, J. Chun, and N. Fukushima Lysophosphatidic acid stimulates astrocyte proliferation through LPA(1) Neurochem. Int. 52 2008 216 220
102. V.E. Miron, S.K. Ludwin, P.J. Darlington, A.A. Jarjour, B. Soliven, T.E. Kennedy, and J.P. Antel Fingolimod (FTY720) enhances remyelination following demyelination of organotypic cerebellar slices Am. J. Pathol. 176 2010 2682 2694
103. V.E. Miron, C.G. Jung, H.J. Kim, T.E. Kennedy, B. Soliven, and J.P. Antel FTY720 modulates human oligodendrocyte progenitor process extension and survival Ann. Neurol. 63 2008 61 71
104. J.A. Cohen, F. Barkhof, G. Comi, H.P. Hartung, B.O. Khatri, X. Montalban, J. Pelletier, R. Capra, P. Gallo, G. Izquierdo, K. Tiel-Wilck, A. de Vera, J. Jin, T. Stites, S. Wu, S. Aradhye, and L. Kappos Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis N. Engl. J. Med. 362 2010 402 415
105. L. Kappos, E.W. Radue, P. O'Connor, C. Polman, R. Hohlfeld, P. Calabresi, K. Selmaj, C. Agoropoulou, M. Leyk, L. Zhang-Auberson, and P. Burtin A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis N. Engl. J. Med. 362 2010 387 401
106. B. Khatri, F. Barkhof, G. Comi, H.P. Hartung, L. Kappos, X. Montalban, J. Pelletier, T. Stites, S. Wu, F. Holdbrook, L. Zhang-Auberson, G. Francis, and J.A. Cohen Comparison of fingolimod with interferon beta-1a in relapsing-remitting multiple sclerosis: a randomised extension of the TRANSFORMS study Lancet Neurol. 10 2011 520 529
107. J.A. Cohen, and J. Chun Mechanisms of fingolimod's efficacy and adverse effects in multiple sclerosis Ann. Neurol. 69 2011 759 777
108. S. Tabuchi, K. Kume, M. Aihara, and T. Shimizu Expression of lysophosphatidic acid receptor in rat astrocytes: mitogenic effect and expression of neurotrophic genes Neurochem. Res. 25 2000 573 582
109. E. Malchinkhuu, K. Sato, T. Muraki, K. Ishikawa, A. Kuwabara, and F. Okajima Assessment of the role of sphingosine 1-phosphate and its receptors in high-density lipoprotein-induced stimulation of astroglial cell function Biochem. J. 370 2003 817 827
110. K. Sato, K. Ishikawa, M. Ui, and F. Okajima 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 Brain Res. Mol. Brain Res. 74 1999 182 189
111. K. Yamagata, M. Tagami, Y. Torii, F. Takenaga, S. Tsumagari, S. Itoh, Y. Yamori, and Y. Nara Sphingosine 1-phosphate induces the production of glial cell line-derived neurotrophic factor and cellular proliferation in astrocytes Glia 41 2003 199 206
112. C. Jaillard, S. Harrison, B. Stankoff, M.S. Aigrot, A.R. Calver, G. Duddy, F.S. Walsh, M.N. Pangalos, N. Arimura, K. Kaibuchi, B. Zalc, and C. Lubetzki Edg8/S1P5: an oligodendroglial receptor with dual function on process retraction and cell survival J. Neurosci. 25 2005 1459 1469
113. B. Anliker, and J. Chun Lysophospholipid G protein-coupled receptors J. Biol. Chem. 279 2004 20555 20558
114. H.J. Kim, V.E. Miron, D. Dukala, R.L. Proia, S.K. Ludwin, M. Traka, J.P. Antel, and B. Soliven Neurobiological effects of sphingosine 1-phosphate receptor modulation in the cuprizone model FASEB J. 25 2011 1509 1518
115. C.R. Rau, K. Hein, M.B. Sattler, B. Kretzschmar, C. Hillgruber, B.L. McRae, R. Diem, and M. Bahr Anti-inflammatory effects of FTY720 do not prevent neuronal cell loss in a rat model of optic neuritis Am. J. Pathol. 178 2011 1770 1781
116. + channels Neuroscience 109 2002 827 835
117. E. Bernhart, M. Kollroser, G. Rechberger, H. Reicher, A. Heinemann, P. Schratl, S. Hallstrom, A. Wintersperger, C. Nusshold, T. DeVaney, K. Zorn-Pauly, R. Malli, W. Graier, E. Malle, and W. Sattler Lysophosphatidic acid receptor activation affects the C13NJ microglia cell line proteome leading to alterations in glycolysis, motility, and cytoskeletal architecture Proteomics 10 2010 141 158
118. Y. Wei, M. Yemisci, H.H. Kim, L.M. Yung, H.K. Shin, S.K. Hwang, S. Guo, T. Qin, N. Alsharif, V. Brinkmann, J.K. Liao, E.H. Lo, and C. Waeber Fingolimod provides long-term protection in rodent models of cerebral ischemia Ann. Neurol. 69 2011 119 129
119. R. Fujita, Y. Ma, and H. Ueda Lysophosphatidic acid-induced membrane ruffling and brain-derived neurotrophic factor gene expression are mediated by ATP release in primary microglia J. Neurochem. 107 2008 152 160
120. + channels for lysophosphatidic acid-induced microglial migration Eur. J. Neurosci. 19 2004 1469 1474
121. H. Lin, N. Baby, J. Lu, C. Kaur, C. Zhang, J. Xu, E.A. Ling, and S.T. Dheen Expression of sphingosine kinase 1 in amoeboid microglial cells in the corpus callosum of postnatal rats J. Neuroinflammation 8 2011 13
122. D. Nayak, Y. Huo, W.X. Kwang, P.N. Pushparaj, S.D. Kumar, E.A. Ling, and S.T. Dheen Sphingosine kinase 1 regulates the expression of proinflammatory cytokines and nitric oxide in activated microglia Neuroscience 166 2010 132 144
123. L. Ma, J. Nagai, and H. Ueda Microglial activation mediates de novo lysophosphatidic acid production in a model of neuropathic pain J. Neurochem. 115 2010 643 653
124. L. Steinman Multiple sclerosis: a coordinated immunological attack against myelin in the central nervous system Cell 85 1996 299 302
125. E.M. Frohman, M.K. Racke, and C.S. Raine Multiple sclerosis - the plaque and its pathogenesis N. Engl. J. Med. 354 2006 942 955
126. S. Mandala, R. Hajdu, J. Bergstrom, E. Quackenbush, J. Xie, J. Milligan, R. Thornton, G.J. Shei, D. Card, C. Keohane, M. Rosenbach, J. Hale, C.L. Lynch, K. Rupprecht, W. Parsons, and H. Rosen Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists Science 296 2002 346 349
127. V. Brinkmann, M.D. Davis, C.E. Heise, R. Albert, S. Cottens, R. Hof, C. Bruns, E. Prieschl, T. Baumruker, P. Hiestand, C.A. Foster, M. Zollinger, and K.R. Lynch The immune modulator FTY720 targets sphingosine 1-phosphate receptors J. Biol. Chem. 277 2002 21453 21457
128. C.W. Lee, J.W. Choi, and J. Chun Neurological S1P signaling as an emerging mechanism of action of oral FTY720 (fingolimod) in multiple sclerosis Arch. Pharm. Res. 33 2010 1567 1574
129. C.A. Foster, D. Mechtcheriakova, M.K. Storch, B. Balatoni, L.M. Howard, F. Bornancin, A. Wlachos, J. Sobanov, A. Kinnunen, and T. Baumruker FTY720 rescue therapy in the dark agouti rat model of experimental autoimmune encephalomyelitis: expression of central nervous system genes and reversal of blood-brain-barrier damage Brain Pathol. 19 2009 254 266
130. N. Blondeau, Y. Lai, S. Tyndall, M. Popolo, K. Topalkara, J.K. Pru, L. Zhang, H. Kim, J.K. Liao, K. Ding, and C. Waeber Distribution of sphingosine kinase activity and mRNA in rodent brain J. Neurochem. 103 2007 509 517
131. B.K. Wacker, T.S. Park, and J.M. Gidday Hypoxic preconditioning-induced cerebral ischemic tolerance: role of microvascular sphingosine kinase 2 Stroke 40 2009 3342 3348
132. W. Pfeilschifter, B. Czech-Zechmeister, M. Sujak, A. Mirceska, A. Koch, A. Rami, H. Steinmetz, C. Foerch, A. Huwiler, and J. Pfeilschifter Activation of sphingosine kinase 2 is an endogenous protective mechanism in cerebral ischemia Biochem. Biophys. Res. Commun. 413 2011 212 217
133. C. Yang, J. Lafleur, B.R. Mwaikambo, T. Zhu, C. Gagnon, S. Chemtob, A. Di Polo, and P. Hardy The role of lysophosphatidic acid receptor (LPA1) in the oxygen-induced retinal ganglion cell degeneration Invest. Ophthalmol. Vis. Sci. 50 2009 1290 1298
134. T. Shichita, Y. Sugiyama, H. Ooboshi, H. Sugimori, R. Nakagawa, I. Takada, T. Iwaki, Y. Okada, M. Iida, D.J. Cua, Y. Iwakura, and A. Yoshimura Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury Nat. Med. 15 2009 946 950
135. D.E. Coyle Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior Glia 23 1998 75 83
136. T. Frugier, M.C. Morganti-Kossmann, D. O'Reilly, and C.A. McLean In situ detection of inflammatory mediators in post mortem human brain tissue after traumatic injury J. Neurotrauma 27 2010 497 507
137. M. Inoue, W. Xie, Y. Matsushita, J. Chun, J. Aoki, and H. Ueda Lysophosphatidylcholine induces neuropathic pain through an action of autotaxin to generate lysophosphatidic acid Neuroscience 152 2008 296 298
138. M. Inoue, A. Yamaguchi, M. Kawakami, J. Chun, and H. Ueda Loss of spinal substance P pain transmission under the condition of LPA1 receptor-mediated neuropathic pain Mol. Pain 2 2006 25
139. L. Ma, H. Uchida, J. Nagai, M. Inoue, J. Chun, J. Aoki, and H. Ueda Lysophosphatidic acid-3 receptor-mediated feed-forward production of lysophosphatidic acid: an initiator of nerve injury-induced neuropathic pain Mol. Pain 5 2009 64
140. W. Xie, M. Matsumoto, J. Chun, and H. Ueda Involvement of LPA1 receptor signaling in the reorganization of spinal input through Abeta-fibers in mice with partial sciatic nerve injury Mol. Pain 4 2008 46
141. M. Matloubian, C.G. Lo, G. Cinamon, M.J. Lesneski, Y. Xu, V. Brinkmann, M.L. Allende, R.L. Proia, and J.G. Cyster Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1 Nature 427 2004 355 360
142. M.O. Cunningham, J. Hunt, S. Middleton, F.E. LeBeau, M.J. Gillies, C.H. Davies, P.R. Maycox, M.A. Whittington, and C. Racca Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness J. Neurosci. 26 2006 2767 2776
143. N.A. Bowden, J. Weidenhofer, R.J. Scott, U. Schall, J. Todd, P.T. Michie, and P.A. Tooney Preliminary investigation of gene expression profiles in peripheral blood lymphocytes in schizophrenia Schizophr. Res. 82 2006 175 183
144. P.K. Dash, S.A. Orsi, M. Moody, and A.N. Moore A role for hippocampal Rho-ROCK pathway in long-term spatial memory Biochem. Biophys. Res. Commun. 322 2004 893 898
145. N. Takasugi, T. Sasaki, K. Suzuki, S. Osawa, H. Isshiki, Y. Hori, N. Shimada, T. Higo, S. Yokoshima, T. Fukuyama, V.M. Lee, J.Q. Trojanowski, T. Tomita, and T. Iwatsubo BACE1 activity is modulated by cell-associated sphingosine-1-phosphate J. Neurosci. 31 2011 6850 6857
146. K. Umemura, N. Yamashita, X. Yu, K. Arima, T. Asada, T. Makifuchi, S. Murayama, Y. Saito, K. Kanamaru, Y. Goto, S. Kohsaka, I. Kanazawa, and H. Kimura Autotaxin expression is enhanced in frontal cortex of Alzheimer-type dementia patients Neurosci. Lett. 400 2006 97 100
147. H. Yi, S.J. Lee, J. Lee, C.S. Myung, W.K. Park, H.J. Lim, G.H. Lee, J.Y. Kong, and H. Cho Sphingosylphosphorylcholine attenuated beta-amyloid production by reducing BACE1 expression and catalysis in PC12 cells Neurochem. Res. 36 2011 2083 2090
148. X. He, Y. Huang, B. Li, C.X. Gong, and E.H. Schuchman Deregulation of sphingolipid metabolism in Alzheimer's disease Neurobiol. Aging 31 2010 398 408
149. A. Gomez-Brouchet, D. Pchejetski, L. Brizuela, V. Garcia, M.F. Altie, M.L. Maddelein, M.B. Delisle, and O. Cuvillier Critical role for sphingosine kinase-1 in regulating survival of neuroblastoma cells exposed to amyloid-beta peptide Mol. Pharmacol. 72 2007 341 349
150. Z.Q. Zheng, X.J. Fang, Y. Zhang, and J.T. Qiao Neuroprotective effect of lysophosphatidic acid on AbetaP31-35-induced apoptosis in cultured cortical neurons Sheng Li Xue Bao 57 2005 289 294
151. F.V. Castelino, J. Seiders, G. Bain, S.F. Brooks, C.D. King, J.S. Swaney, D.S. Lorrain, J. Chun, A.D. Luster, and A.M. Tager Amelioration of dermal fibrosis by genetic deletion or pharmacologic antagonism of lysophosphatidic acid receptor 1 in a mouse model of scleroderma Arthritis Rheum. 63 2011 1405 1415
152. M. Funke, Z. Zhao, Y. Xu, J. Chun, and A.M. Tager The lysophosphatidic acid receptor LPA1 promotes epithelial cell apoptosis after lung injury Am. J. Respir. Cell Mol. Biol. 46 2012 355 364
153. J.P. Pradere, J. Klein, S. Gres, C. Guigne, E. Neau, P. Valet, D. Calise, J. Chun, J.L. Bascands, J.S. Saulnier-Blache, and J.P. Schanstra LPA1 receptor activation promotes renal interstitial fibrosis J. Am. Soc. Nephrol. 18 2007 3110 3118
154. A.M. Tager, P. Lacamera, B.S. Shea, G.S. Campanella, M. Selman, Z. Zhao, V. Polosukhin, J. Wain, B.A. Karimi-Shah, N.D. Kim, W.K. Hart, A. Pardo, T.S. Blackwell, Y. Xu, J. Chun, and A.D. Luster The lysophosphatidic acid receptor LPA(1) links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak Nat. Med. 14 2008 45 54
155. J. Zhao, D. He, Y. Su, E. Berdyshev, J. Chun, V. Natarajan, and Y. Zhao Lysophosphatidic acid receptor 1 modulates lipopolysaccharide-induced inflammation in alveolar epithelial cells and murine lungs Am. J. Physiol. Lung Cell. Mol. Physiol. 301 2011 L547 L556
156. K. Hama, J. Aoki, M. Fukaya, Y. Kishi, T. Sakai, R. Suzuki, H. Ohta, T. Yamori, M. Watanabe, J. Chun, and H. Arai Lysophosphatidic acid and autotaxin stimulate cell motility of neoplastic and non-neoplastic cells through LPA1 J. Biol. Chem. 279 2004 17634 17639
157. M.F. Simon, D. Daviaud, J.P. Pradere, S. Gres, C. Guigne, M. Wabitsch, J. Chun, P. Valet, and J.S. Saulnier-Blache Lysophosphatidic acid inhibits adipocyte differentiation via lysophosphatidic acid 1 receptor-dependent down-regulation of peroxisome proliferator-activated receptor gamma2 J. Biol. Chem. 280 2005 14656 14662
158. M. Panchatcharam, S. Miriyala, F. Yang, M. Rojas, C. End, C. Vallant, A. Dong, K. Lynch, J. Chun, A.J. Morris, and S.S. Smyth Lysophosphatidic acid receptors 1 and 2 play roles in regulation of vascular injury responses but not blood pressure Circ. Res. 103 2008 662 670
159. I. Gennero, S. Laurencin-Dalicieux, F. Conte-Auriol, F. Briand-Mesange, D. Laurencin, J. Rue, N. Beton, N. Malet, M. Mus, A. Tokumura, P. Bourin, L. Vico, G. Brunel, R.O. Oreffo, J. Chun, and J.P. Salles Absence of the lysophosphatidic acid receptor LPA1 results in abnormal bone development and decreased bone mass Bone 49 2011 395 403
160. H.Y. Cheng, A. Dong, M. Panchatcharam, P. Mueller, F. Yang, Z. Li, G. Mills, J. Chun, A.J. Morris, and S.S. Smyth Lysophosphatidic acid signaling protects pulmonary vasculature from hypoxia-induced remodeling Arterioscler. Thromb. Vasc. Biol. 32 2012 24 32
161. J.A. Weiner, N. Fukushima, J.J. Contos, S.S. Scherer, and J. Chun Regulation of Schwann cell morphology and adhesion by receptor-mediated lysophosphatidic acid signaling J. Neurosci. 21 2001 7069 7078
162. S. Lin, S.J. Lee, H. Shim, J. Chun, and C.C. Yun The absence of LPA receptor 2 reduces the tumorigenesis by ApcMin mutation in the intestine Am. J. Physiol. Gastrointest. Liver Physiol. 299 2010 G1128 G1138
163. 2 attenuates tumor formation in an experimental model of colitis-associated cancer Gastroenterology 136 2009 1711 1720
164. 2 in the development of allergic airway inflammation in a murine model of asthma Respir. Res. 10 2009 114
165. K. Hama, J. Aoki, A. Inoue, T. Endo, T. Amano, R. Motoki, M. Kanai, X. Ye, J. Chun, N. Matsuki, H. Suzuki, M. Shibasaki, and H. Arai Embryo spacing and implantation timing are differentially regulated by LPA3-mediated lysophosphatidic acid signaling in mice Biol. Reprod. 77 2007 954 959
166. X. Ye, H. Diao, and J. Chun 11-Deoxy prostaglandin F(2alpha), a thromboxane A2 receptor agonist, partially alleviates embryo crowding in Lpar3((-/-)) females Fertil. Steril. 97 2012 757 763
167. X. Ye, K. Hama, J.J. Contos, B. Anliker, A. Inoue, M.K. Skinner, H. Suzuki, T. Amano, G. Kennedy, H. Arai, J. Aoki, and J. Chun LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing Nature 435 2005 104 108
168. X. Ye, M.K. Skinner, G. Kennedy, and J. Chun Age-dependent loss of sperm production in mice via impaired lysophosphatidic acid signaling Biol. Reprod. 79 2008 328 336
169. H. Diao, J.D. Aplin, S. Xiao, J. Chun, Z. Li, S. Chen, and X. Ye Altered spatiotemporal expression of collagen types I, III, IV, and VI in Lpar3-deficient peri-implantation mouse uterus Biol. Reprod. 84 2011 255 265
170. L.C. Chan, W. Peters, Y. Xu, J. Chun, R.V. Farese Jr., and S. Cases LPA3 receptor mediates chemotaxis of immature murine dendritic cells to unsaturated lysophosphatidic acid (LPA) J. Leukoc. Biol. 82 2007 1193 1200
171. C. Zhao, A. Sardella, J. Chun, P.E. Poubelle, M.J. Fernandes, and S.G. Bourgoin TNF-alpha promotes LPA1- and LPA3-mediated recruitment of leukocytes in vivo through CXCR2 ligand chemokines J. Lipid Res. 52 2011 1307 1318
172. H. Sumida, K. Noguchi, Y. Kihara, M. Abe, K. Yanagida, F. Hamano, S. Sato, K. Tamaki, Y. Morishita, M.R. Kano, C. Iwata, K. Miyazono, K. Sakimura, T. Shimizu, and S. Ishii LPA4 regulates blood and lymphatic vessel formation during mouse embryogenesis Blood 116 2010 5060 5070
173. M.L. Allende, T. Yamashita, and R.L. Proia G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation Blood 102 2003 3665 3667
174. Y. Liu, R. Wada, T. Yamashita, Y. Mi, C.X. Deng, J.P. Hobson, H.M. Rosenfeldt, V.E. Nava, S.S. Chae, M.J. Lee, C.H. Liu, T. Hla, S. Spiegel, and R.L. Proia Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation J. Clin. Invest. 106 2000 951 961
175. J.P. Hobson, H.M. Rosenfeldt, L.S. Barak, A. Olivera, S. Poulton, M.G. Caron, S. Milstien, and S. Spiegel Role of the sphingosine-1-phosphate receptor EDG-1 in PDGF-induced cell motility Science 291 2001 1800 1803
176. B.S. Shea, S.F. Brooks, B.A. Fontaine, J. Chun, A.D. Luster, and A.M. Tager Prolonged exposure to sphingosine 1-phosphate receptor-1 agonists exacerbates vascular leak, fibrosis, and mortality after lung injury Am. J. Respir. Cell Mol. Biol. 43 2010 662 673
177. M.L. Allende, J.L. Dreier, S. Mandala, and R.L. Proia Expression of the sphingosine 1-phosphate receptor, S1P1, on T-cells controls thymic emigration J. Biol. Chem. 279 2004 15396 15401
178. K. Kabashima, N.M. Haynes, Y. Xu, S.L. Nutt, M.L. Allende, R.L. Proia, and J.G. Cyster Plasma cell S1P1 expression determines secondary lymphoid organ retention versus bone marrow tropism J. Exp. Med. 203 2006 2683 2690
179. I. Ishii, X. Ye, B. Friedman, S. Kawamura, J.J. Contos, M.A. Kingsbury, A.H. Yang, G. Zhang, J.H. Brown, and J. Chun Marked perinatal lethality and cellular signaling deficits in mice null for the two sphingosine 1-phosphate (S1P) receptors, S1P(2)/LP(B2)/EDG-5 and S1P(3)/LP(B3)/EDG-3 J. Biol. Chem. 277 2002 25152 25159
180. M. Kono, Y. Mi, Y. Liu, T. Sasaki, M.L. Allende, Y.P. Wu, T. Yamashita, and R.L. Proia The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis J. Biol. Chem. 279 2004 29367 29373
181. J.N. Lorenz, L.J. Arend, R. Robitz, R.J. Paul, and A.J. MacLennan Vascular dysfunction in S1P2 sphingosine 1-phosphate receptor knockout mice Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 2007 R440 R446
182. W.S. Szczepaniak, B.R. Pitt, and B.J. McVerry S1P2 receptor-dependent Rho-kinase activation mediates vasoconstriction in the murine pulmonary circulation induced by sphingosine 1-phosphate Am. J. Physiol. Lung Cell. Mol. Physiol. 299 2010 L137 L145
183. H. Ikeda, N. Watanabe, I. Ishii, T. Shimosawa, Y. Kume, T. Tomiya, Y. Inoue, T. Nishikawa, N. Ohtomo, Y. Tanoue, S. Iitsuka, R. Fujita, M. Omata, J. Chun, and Y. Yatomi Sphingosine 1-phosphate regulates regeneration and fibrosis after liver injury via sphingosine 1-phosphate receptor 2 J. Lipid Res. 50 2009 556 564
184. V. Serriere-Lanneau, F. Teixeira-Clerc, L. Li, M. Schippers, W. de Wries, B. Julien, J. Tran-Van-Nhieu, S. Manin, K. Poelstra, J. Chun, S. Carpentier, T. Levade, A. Mallat, and S. Lotersztajn The sphingosine 1-phosphate receptor S1P2 triggers hepatic wound healing FASEB J. 21 2007 2005 2013
185. S.K. Goparaju, P.S. Jolly, K.R. Watterson, M. Bektas, S. Alvarez, S. Sarkar, L. Mel, I. Ishii, J. Chun, S. Milstien, and S. Spiegel The S1P2 receptor negatively regulates platelet-derived growth factor-induced motility and proliferation Mol. Cell. Biol. 25 2005 4237 4249
186. A. Skoura, T. Sanchez, K. Claffey, S.M. Mandala, R.L. Proia, and T. Hla Essential role of sphingosine 1-phosphate receptor 2 in pathological angiogenesis of the mouse retina J. Clin. Invest. 117 2007 2506 2516
187. T. Imasawa, K. Koike, I. Ishii, J. Chun, and Y. Yatomi Blockade of sphingosine 1-phosphate receptor 2 signaling attenuates streptozotocin-induced apoptosis of pancreatic beta-cells Biochem. Biophys. Res. Commun. 392 2010 207 211
188. Y. Gon, M.R. Wood, W.B. Kiosses, E. Jo, M.G. Sanna, J. Chun, and H. Rosen S1P3 receptor-induced reorganization of epithelial tight junctions compromises lung barrier integrity and is potentiated by TNF Proc. Natl. Acad. Sci. U. S. A. 102 2005 9270 9275
189. L.M. Baudhuin, Y. Jiang, A. Zaslavsky, I. Ishii, J. Chun, and Y. Xu S1P3-mediated Akt activation and cross-talk with platelet-derived growth factor receptor (PDGFR) FASEB J. 18 2004 341 343
190. I. Ishii, B. Friedman, X. Ye, S. Kawamura, C. McGiffert, J.J. Contos, M.A. Kingsbury, G. Zhang, J.H. Brown, and J. Chun 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. 276 2001 33697 33704
191. I. Girkontaite, V. Sakk, M. Wagner, T. Borggrefe, K. Tedford, J. Chun, and K.D. Fischer The sphingosine-1-phosphate (S1P) lysophospholipid receptor S1P3 regulates MAdCAM-1 + endothelial cells in splenic marginal sinus organization J. Exp. Med. 200 2004 1491 1501
192. C.D. Keller, P. Rivera Gil, M. Tolle, M. van der Giet, J. Chun, H.H. Radeke, M. Schafer-Korting, and B. Kleuser Immunomodulator FTY720 induces myofibroblast differentiation via the lysophospholipid receptor S1P3 and Smad3 signaling Am. J. Pathol. 170 2007 281 292
193. D.H. Walter, U. Rochwalsky, J. Reinhold, F. Seeger, A. Aicher, C. Urbich, I. Spyridopoulos, J. Chun, V. Brinkmann, P. Keul, B. Levkau, A.M. Zeiher, S. Dimmeler, and J. Haendeler Sphingosine-1-phosphate stimulates the functional capacity of progenitor cells by activation of the CXCR4-dependent signaling pathway via the S1P3 receptor Arterioscler. Thromb. Vasc. Biol. 27 2007 275 282
194. B. Levkau, S. Hermann, G. Theilmeier, M. van der Giet, J. Chun, O. Schober, and M. Schafers High-density lipoprotein stimulates myocardial perfusion in vivo Circulation 110 2004 3355 3359
195. J.R. Nofer, M. van der Giet, M. Tolle, I. Wolinska, K. von Wnuck Lipinski, H.A. Baba, U.J. Tietge, A. Godecke, I. Ishii, B. Kleuser, M. Schafers, M. Fobker, W. Zidek, G. Assmann, J. Chun, and B. Levkau HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3 J. Clin. Invest. 113 2004 569 581
196. M. Tolle, B. Levkau, P. Keul, V. Brinkmann, G. Giebing, G. Schonfelder, M. Schafers, K. von Wnuck Lipinski, J. Jankowski, V. Jankowski, J. Chun, W. Zidek, and M. Van der Giet Immunomodulator FTY720 induces eNOS-dependent arterial vasodilatation via the lysophospholipid receptor S1P3 Circ. Res. 96 2005 913 920
197. S. Salomone, E.M. Potts, S. Tyndall, P.C. Ip, J. Chun, V. Brinkmann, and C. Waeber Analysis of sphingosine 1-phosphate receptors involved in constriction of isolated cerebral arteries with receptor null mice and pharmacological tools Br. J. Pharmacol. 153 2008 140 147
198. N. Takuwa, S. Ohkura, S. Takashima, K. Ohtani, Y. Okamoto, T. Tanaka, K. Hirano, S. Usui, F. Wang, W. Du, K. Yoshioka, Y. Banno, M. Sasaki, I. Ichi, M. Okamura, N. Sugimoto, K. Mizugishi, Y. Nakanuma, I. Ishii, M. Takamura, S. Kaneko, S. Kojo, K. Satouchi, K. Mitumori, J. Chun, and Y. Takuwa S1P3-mediated cardiac fibrosis in sphingosine kinase 1 transgenic mice involves reactive oxygen species Cardiovasc. Res. 85 2010 484 493
199. C. Herzog, M. Schmitz, B. Levkau, I. Herrgott, J. Mersmann, J. Larmann, K. Johanning, M. Winterhalter, J. Chun, F.U. Muller, F. Echtermeyer, R. Hildebrand, and G. Theilmeier Intravenous sphingosylphosphorylcholine protects ischemic and postischemic myocardial tissue in a mouse model of myocardial ischemia/reperfusion injury Mediators Inflamm. 2010 2010 425191
200. C.K. Means, C.Y. Xiao, Z. Li, T. Zhang, J.H. Omens, I. Ishii, J. Chun, and J.H. Brown Sphingosine 1-phosphate S1P2 and S1P3 receptor-mediated Akt activation protects against in vivo myocardial ischemia-reperfusion injury Am. J. Physiol. Heart Circ. Physiol. 292 2007 H2944 H2951
201. G. Theilmeier, C. Schmidt, J. Herrmann, P. Keul, M. Schafers, I. Herrgott, J. Mersmann, J. Larmann, S. Hermann, J. Stypmann, O. Schober, R. Hildebrand, R. Schulz, G. Heusch, M. Haude, K. von Wnuck Lipinski, C. Herzog, M. Schmitz, R. Erbel, J. Chun, and B. Levkau High-density lipoproteins and their constituent, sphingosine-1-phosphate, directly protect the heart against ischemia/reperfusion injury in vivo via the S1P3 lysophospholipid receptor Circulation 114 2006 1403 1409
202. F. Niessen, F. Schaffner, C. Furlan-Freguia, R. Pawlinski, G. Bhattacharjee, J. Chun, C.K. Derian, P. Andrade-Gordon, H. Rosen, and W. Ruf Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation Nature 452 2008 654 658
203. S. Golfier, S. Kondo, T. Schulze, T. Takeuchi, G. Vassileva, A.H. Achtman, M.H. Graler, S.J. Abbondanzo, M. Wiekowski, E. Kremmer, Y. Endo, S.A. Lira, K.B. Bacon, and M. Lipp Shaping of terminal megakaryocyte differentiation and proplatelet development by sphingosine-1-phosphate receptor S1P4 FASEB J. 24 2010 4701 4710
204. C.N. Jenne, A. Enders, R. Rivera, S.R. Watson, A.J. Bankovich, J.P. Pereira, Y. Xu, C.M. Roots, J.N. Beilke, A. Banerjee, S.L. Reiner, S.A. Miller, A.S. Weinmann, C.C. Goodnow, L.L. Lanier, J.G. Cyster, and J. Chun T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow J. Exp. Med. 206 2009 2469 2481
205. K. Mayol, V. Biajoux, J. Marvel, K. Balabanian, and T. Walzer Sequential desensitization of CXCR4 and S1P5 controls natural killer cell trafficking Blood 118 2011 4863 4871
206. T. Walzer, L. Chiossone, J. Chaix, A. Calver, C. Carozzo, L. Garrigue-Antar, Y. Jacques, M. Baratin, E. Tomasello, and E. Vivier Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor Nat. Immunol. 8 2007 1337 1344