Sphingosine 1-phosphate receptor signaling regulates proper embryonic vascular patterning

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2143-2156

  Mendelson, Karen ^a   Zygmunt, Tomasz ^b   Torres Vázquez, Jesús ^b   Evans, Todd ^a   Hla, Timothy ^a  

^a Weill Cornell Medical College of Cornell University   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; AXIAL VESSELS; BIOINFORMATIC ANALYSIS; BLOOD CIRCULATION; CELL MIGRATION; CERAMIDES; DANIO RERIO; EXTRACELLULAR; G PROTEIN COUPLED RECEPTORS; HEART DEVELOPMENT; IMMUNE SYSTEMS; METABOLIC ENZYMES; ORTHOLOGS; PHYSIOLOGICAL EFFECTS; RECEPTOR SIGNALING; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATES; VASCULAR DEVELOPMENT; VASCULAR PATTERNING; VASCULAR SYSTEM; VASCULARIZATION; ZEBRAFISH;

AMIDES; BIOINFORMATICS; CARDIOVASCULAR SYSTEM; GENES;

DEFECTS;

CARRIER PROTEIN; CERAMIDE; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 1; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; SPINSTER 2; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; EMBRYO; EMBRYO PATTERN FORMATION; GENE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATOR GENE; SIGNAL TRANSDUCTION; SPHINGOSINE 1 PHOSPHATE RECEPTOR 1 GENE; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2 GENE; ZEBRA FISH;

ANIMALS; BIOLOGICAL TRANSPORT; BODY PATTERNING; CELL PROLIFERATION; CLONING, MOLECULAR; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; IN SITU HYBRIDIZATION; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; TISSUE DISTRIBUTION; ZEBRAFISH;

EID: 84873836098     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.427344     Document Type: Article

References (42)

1. Le Stunff, H., Milstien, S., and Spiegel, S. (2004) Generation and metabolism of bioactive sphingosine 1-phosphate. J. Cell. Biochem. 92, 882-899
2. Hla, T., and Maciag, T. (1990) An abundant transcript induced in differentiating human endothelial cells encodes a polypeptide with structural similarities to G-protein-coupled receptors. J. Biol. Chem. 265, 9308-9313
3. 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
4. Ishii, I., Friedman, B., Ye, X., Kawamura, S., McGiffert, C., Contos, J. J., Kingsbury, M. A., Zhang, G., Brown, J. H., and Chun, J. (2001) 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, 33697-33704
5. Liu, C. H., and Hla, T. (1997) The mouse gene for the inducible G-proteincoupled receptor edg-1. Genomics 43, 15-24
6. Gräler, M. H., Bernhardt, G., and Lipp, M. (1998) EDG6, a novel Gprotein- coupled receptor related to receptors for bioactive lysophospholipids, is specifically expressed in lymphoid tissue. Genomics 53, 164 -169
7. Im, D. S., Heise, C. E., Ancellin, N., O'Dowd, B. F., Shei, G. J., Heavens, R. P., Rigby, M. R., Hla, T., Mandala, S., McAllister, G., George, S. R., and Lynch, K. R. (2000) Characterization of a novel sphingosine 1-phosphate receptor, Edg-8. J. Biol. Chem. 275, 14281-14286
8. Malek, R. L., Toman, R. E., Edsall, L. C., Wong, S., Chiu, J., Letterle, C. A., Van Brocklyn, J. R., Milstien, S., Spiegel, S., and Lee, N. H. (2001) Nrg-1 belongs to the endothelial differentiation gene family of G protein-coupled sphingosine 1-phosphate receptors. J. Biol. Chem. 276, 5692-5699
9. Liu, Y., Wada, R., Yamashita, T., Mi, Y., Deng, C. X., Hobson, J. P., Rosenfeldt, H. M., Nava, V. E., Chae, S. S., Lee, M. J., Liu, C. H., Hla, T., Spiegel, S., and Proia, R. L. (2000) Edg-1, theGprotein-coupled receptor for sphingosine 1-phosphate, is essential for vascular maturation. J. Clin. Invest. 106, 951-961
10. Kono, M., Mi, Y., Liu, Y., Sasaki, T., Allende, M. L., Wu, Y. P., Yamashita, T., and Proia, R. L. (2004) The sphingosine 1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. J. Biol. Chem. 279, 29367-29373
11. Jung, B., Obinata, H., Galvani, S., Mendelson, K., Ding, B. S., Skoura, A., Kinzel, B., Brinkmann, V., Rafii, S., Evans, T., and Hla, T. (2012) Flowregulated endothelial S1P receptor-1 signaling sustains vascular development. Dev. Cell 23, 600-610
12. Skoura, A., Sanchez, T., Claffey, K., Mandala, S. M., Proia, R. L., and Hla, T. (2007) Essential role of sphingosine 1-phosphate receptor 2 in pathological angiogenesis of the mouse retina. J. Clin. Invest. 117, 2506-2516
13. Kono, M., Belyantseva, I. A., Skoura, A., Frolenkov, G. I., Starost, M. F., Dreier, J. L., Lidington, D., Bolz, S. S., Friedman, T. B., Hla, T., and Proia, R. L. (2007) Deafness and stria vascularis defects in S1P2 receptor-null mice. J. Biol. Chem. 282, 10690-10696
14. Hla, T. (2005) Genomic insights into mediator lipidomics. Prostaglandins Other Lipid Mediat. 77, 197-209
15. Kupperman, E., An, S., Osborne, N., Waldron, S., and Stainier, D. Y. (2000) A sphingosine 1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 406, 192-195
16. Kai, M., Heisenberg, C. P., and Tada, M. (2008) Sphingosine 1-phosphate receptors regulate individual cell behaviours underlying the directed migration of prechordal plate progenitor cells during zebrafish gastrulation. Development 135, 3043-3051
17. Kawahara, A., Nishi, T., Hisano, Y., Fukui, H., Yamaguchi, A., and Mochizuki, N. (2009) The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 323, 524-527
18. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995) Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310
19. Lawson, N. D., and Weinstein, B. M. (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318
20. Chi, N. C., Shaw, R. M., De Val, S., Kang, G., Jan, L. Y., Black, B. L., and Stainier, D. Y. (2008) Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. Genes Dev. 22, 734-739
21. Blum, Y., Belting, H. G., Ellertsdottir, E., Herwig, L., Lüders, F., and Affolter, M. (2008) Complex cell rearrangements during intersegmental ves-sel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322
22. Traver, D., Paw, B. H., Poss, K. D., Penberthy, W. T., Lin, S., and Zon, L. I. (2003) Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat. Immunol. 4, 1238-1246
23. Matsui, T., Raya, A., Callol-Massot, C., Kawakami, Y., Oishi, I., Rodriguez- Esteban, C., and Izpisúa Belmonte, J. C. (2007) Miles-apart-mediated regulation of cell-fibronectin interaction and myocardial migration in zebrafish. Nat. Clin. Pract. Cardiovasc. Med. 4, S77-S82
24. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A., and Ekker, S. C. (2007) p53 activation by knockdown technologies. PLoS Genet. 3, e78
25. Alexander, J., Stainier, D. Y., and Yelon, D. (1998) Screening mosaic F1 females for mutations affecting zebrafish heart induction and patterning. Dev. Genet. 22, 288-299
26. Pedroso, G. L., Hammes, T. O., Escobar, T. D., Fracasso, L. B., Forgiarini, L. F., and da Silveira, T. R. (2012) Blood collection for biochemical analysis in adult zebrafish. J. Vis. Exp. 63, e3865
27. Hisano, Y., Kobayashi, N., Yamaguchi, A., and Nishi, T. (2012) Mouse SPNS2 functions as a sphingosine 1-phosphate transporter in vascular endothelial cells. PLoS One 7, e38941
28. Kohno, M., Momoi, M., Oo, M. L., Paik, J. H., Lee, Y. M., Venkataraman, K., Ai, Y., Ristimaki, A. P., Fyrst, H., Sano, H., Rosenberg, D., Saba, J. D., Proia, R. L., and Hla, T. (2006) Intracellular role for sphingosine kinase 1 in intestinal adenoma cell proliferation. Mol. Cell. Biol. 26, 7211-7223
29. Langheinrich, U., Hennen, E., Stott, G., and Vacun, G. (2002) Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr. Biol. 12, 2023-2028
30. Choi, J., Mouillesseaux, K., Wang, Z., Fiji, H. D., Kinderman, S. S., Otto, G. W., Geisler, R., Kwon, O., and Chen, J. N. (2011) Aplexone targets the HMG-CoA reductase pathway and differentially regulates arteriovenous angiogenesis. Development 138, 1173-1181
31. Amores, A., Force, A., Yan, Y. L., Joly, L., Amemiya, C., Fritz, A., Ho, R. K., Langeland, J., Prince, V., Wang, Y. L., Westerfield, M., Ekker, M., and Postlethwait, J. H. (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282, 1711-1714
32. Meyer, A., and Van de Peer, Y. (2005) From 2R to 3R. Evidence for a fish-specific genome duplication (FSGD). BioEssays 27, 937-945
33. Taylor, J. S., Braasch, I., Frickey, T., Meyer, A., and Van de Peer, Y. (2003) Genome duplication, a trait shared by 22000 species of ray-finned fish. Genome Res. 13, 382-390
34. Schmelz, E. M., Crall, K. J., Larocque, R., Dillehay, D. L., and Merrill, A. H., Jr. (1994) Uptake and metabolism of sphingolipids in isolated intestinal loops of mice. J. Nutr. 124, 702-712
35. Im, D. S., Clemens, J., Macdonald, T. L., and Lynch, K. R. (2001) Characterization of the human and mouse sphingosine 1-phosphate receptor, S1P5 (Edg-8). Structure-activity relationship of sphingosine 1-phosphate receptors. Biochemistry 40, 14053-14060
36. Schwab, S. R., Pereira, J. P., Matloubian, M., Xu, Y., Huang, Y., and Cyster, J. G. (2005) Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309, 1735-1739
37. Hla, T., Venkataraman, K., and Michaud, J. (2008) The vascular S1P gradient- cellular sources and biological significance. Biochim. Biophys. Acta 1781, 477-482
38. Pappu, R., Schwab, S. R., Cornelissen, I., Pereira, J. P., Regard, J. B., Xu, Y., Camerer, E., Zheng, Y. W., Huang, Y., Cyster, J. G., and Coughlin, S. R. (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine 1-phosphate. Science 316, 295-298
39. Massberg, S., Schaerli, P., Knezevic-Maramica, I., Köllnberger, M., Tubo, N., Moseman, E. A., Huff, I. V., Junt, T., Wagers, A. J., Mazo, I. B., and von Andrian, U. H. (2007) Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131, 994-1008
40. Tobia, C., Chiodelli, P., Nicoli, S., Dell'era, P., Buraschi, S., Mitola, S., Foglia, E., van Loenen, P. B., Alewijnse, A. E., and Presta, M. (2012) Sphingosine 1-phosphate receptor-1 controls venous endothelial barrier integrity in zebrafish. Arterioscler. Thromb. Vasc. Biol. 32, e104-116
41. Paik, J. H., Skoura, A., Chae, S. S., Cowan, A. E., Han, D. K., Proia, R. L., and Hla, T. (2004) Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev. 18, 2392-2403
42. Gaengel, K., Niaudet, C., Hagikura, K., Siemsen, B. L., Muhl, L., Hofmann, J. J., Ebarasi, L., Nyström, S., Rymo, S., Chen, L. L., Pang, M. F., Jin, Y., Raschperger, E., Roswall, P., Schulte, D., Benedito, R., Larsson, J., Hellström, M., Fuxe, J., Uhlén, P., Adams, R., Jakobsson, L., Majumdar, A., Vestweber, D., Uv, A., and Betsholtz, C. (2012) The sphingosine 1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR2. Dev. Cell 23, 587-599