Sphingosine 1-phosphate receptors are essential mediators of eyelid closure during embryonic development

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29882-29889

  Herr, Deron R ^a,b   Lee, Chang Wook ^a   Wang, Wei ^b   Ware, Adam ^a   Rivera, Richard ^a   Chun, Jerold ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PROCESS; EMBRYONIC DEVELOPMENT; EPIDERMAL GROWTH FACTORS; EPITHELIAL SHEETS; FETAL DEVELOPMENT; MOLECULAR SIGNALING; SIGNALING PATHWAYS; SPHINGOSINE 1 PHOSPHATES;

CELL CULTURE; GENE ENCODING; MAMMALS;

SPHINGOSINES;

EPIDERMAL GROWTH FACTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; SPHINGOSINE 1 PHOSPHATE RECEPTOR 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIZATION; EYE MALFORMATION; EYELID CLOSURE; FEMALE; FIBROBLAST; GENE DELETION; HISTOPATHOLOGY; HOMOZYGOTE; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

DEVELOPMENT; EPIDERMAL GROWTH FACTOR (EGF); ERK; EYE; G PROTEIN-COUPLED RECEPTORS (GPCRS); GENE KNOCKOUT; MAP KINASES (MAPKS); MOUSE; SPHINGOLIPID; SPHINGOSINE 1-PHOSPHATE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EPIDERMAL GROWTH FACTOR; EYE ABNORMALITIES; EYELIDS; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; PREGNANCY; RECEPTORS, LYSOSPHINGOLIPID; SPHINGOSINE;

EID: 84885598801     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.510099     Document Type: Article

References (64)

1. Findlater, G. S., McDougall, R. D., and Kaufman, M. H. (1993) Eyelid development, fusion and subsequent reopening in the mouse. J. Anat. 183, 121-129
2. Byun, T. H., Kim, J. T., Park, H. W., and Kim, W. K. (2011) Timetable for upper eyelid development in staged human embryos and fetuses. Anat Rec. 294, 789-796
3. Addison, W. H. F., and How, H. W. (1921) The development of the eyelids of the albino rat, until the completion of disjunction. Am. J. Anat. 29, 1-31
4. Xia, Y., and Kao, W. W. (2004) The signaling pathways in tissue morphogenesis: a lesson from mice with eye-open at birth phenotype. Biochem. Pharmacol. 68, 997-1001
5. Luetteke, N. C., Phillips, H. K., Qiu, T. H., Copeland, N. G., Earp, H. S., Jenkins, N. A., and Lee, D. C. (1994) The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev. 8, 399-413
6. Du, X., Tabeta, K., Hoebe, K., Liu, H., Mann, N., Mudd, S., Crozat, K., Sovath, S., Gong, X., and Beutler, B. (2004) Velvet, a dominant Egfr mutation that causes wavy hair and defective eyelid development in mice. Genetics 166, 331-340
7. Mine, N., Iwamoto, R., and Mekada, E. (2005) HB-EGF promotes epithelial cell migration in eyelid development. Development 132, 4317-4326
8. Mann, G. B., Fowler, K. J., Gabriel, A., Nice, E. C., Williams, R. L., and Dunn, A. R. (1993) Mice with a null mutation of the TGFα gene have abnormal skin architecture, wavy hair, and curly whiskers and often develop corneal inflammation. Cell 73, 249-261
9. Luetteke, N. C., Qiu, T. H., Peiffer, R. L., Oliver, P., Smithies, O., and Lee, D. C. (1993) TGFα deficiency results in hair follicle and eye abnormalities in targeted and waved-1 mice. Cell 73, 263-278
10. Tateossian, H., Hardisty-Hughes, R. E., Morse, S., Romero, M. R., Hilton, H., Dean, C., and Brown, S. D. (2009) Regulation of TGF-β signalling by Fbxo11, the gene mutated in the Jeff otitis media mouse mutant. Patho-Genetics 2, 5
11. Tao, H., Shimizu, M., Kusumoto, R., Ono, K., Noji, S., and Ohuchi, H. (2005) A dual role of FGF10 in proliferation and coordinated migration of epithelial leading edge cells during mouse eyelid development. Development 132, 3217-3230
12. Huang, J., Dattilo, L. K., Rajagopal, R., Liu, Y., Kaartinen, V., Mishina, Y., Deng, C. X., Umans, L., Zwijsen, A., Roberts, A. B., and Beebe, D. C. (2009) FGF-regulated BMP signaling is required for eyelid closure and to specify conjunctival epithelial cell fate. Development 136, 1741-1750
13. Jin, C., Yin, F., Lin, M., Li, H., Wang, Z., Weng, J., Liu, M., Da Dong, X., Qu, J., and Tu, L. (2008) GPR48 regulates epithelial cell proliferation and migration by activating EGFR during eyelid development. Invest. Ophthalmol. Vis. Sci. 49, 4245-4253
14. Wang, Z., Jin, C., Li, H., Li, C., Hou, Q., Liu, M., Dong Xda, E., and Tu, L. (2010) GPR48-induced keratinocyte proliferation occurs through HB-EGF mediated EGFR transactivation. FEBS Lett. 584, 4057-4062
15. Takatori, A., Geh, E., Chen, L., Zhang, L., Meller, J., and Xia, Y. (2008) Differential transmission of MEKK1 morphogenetic signals by JNK1 and JNK2. Development 135, 23-32
16. Zhang, L., Deng, M., Parthasarathy, R., Wang, L., Mongan, M., Molkentin, J. D., Zheng, Y., and Xia, Y. (2005) MEKK1 transduces activin signals in keratinocytes to induce actin stress fiber formation and migration. Mol. Cell. Biol. 25, 60-65
17. Zhang, L., Deng, M., Kao, C. W., Kao, W. W., and Xia, Y. (2003) MEK kinase 1 regulates c-Jun phosphorylation in the control of corneal morphogenesis. Mol. Vis. 9, 584-593
18. Yujiri, T., Ware, M., Widmann, C., Oyer, R., Russell, D., Chan, E., Zaitsu, Y., Clarke, P., Tyler, K., Oka, Y., Fanger, G. R., Henson, P., and Johnson, G. L. (2000) MEK kinase 1 gene disruption alters cell migration and c-Jun NH2-terminal kinase regulation but does not cause a measurable defect in NF-κB activation. Proc. Natl. Acad. Sci. U.S.A. 97, 7272-7277
19. Zenz, R., Scheuch, H., Martin, P., Frank, C., Eferl, R., Kenner, L., Sibilia, M., and Wagner, E. F. (2003) c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev. Cell 4, 879-889
20. Shimizu, Y., Thumkeo, D., Keel, J., Ishizaki, T., Oshima, H., Oshima, M., Noda, Y., Matsumura, F., Taketo, M. M., and Narumiya, S. (2005) ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J. Cell Biol. 168, 941-953
21. Chun, J., Hla, T., Lynch, K. R., Spiegel, S., and Moolenaar, W. H. (2010) International Union of Basic and Clinical Pharmacology. LXXVIII. Lysophospholipid receptor nomenclature. Pharmacol. Rev. 62, 579-587
22. Mutoh, T., Rivera, R., and Chun, J. (2012) Insights into the pharmacological relevance of lysophospholipid receptors. Br. J. Pharmacol. 165, 829-844
23. Choi, J. W., Lee, C. W., and Chun, J. (2008) Biological roles of lysophospholipid receptors revealed by genetic null mice: an update. Biochim. Biophys. Acta 1781, 531-539
24. Matloubian, M., Lo, C. G., Cinamon, G., Lesneski, M. J., Xu, Y., Brinkmann, V., Allende, M. L., Proia, R. L., and Cyster, J. G. (2004) Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427, 355-360
25. Allende, M. L., Yamashita, T., and Proia, R. L. (2003) G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102, 3665-3667
26. MacLennan, A. J., Carney, P. R., Zhu, W. J., Chaves, A. H., Garcia, J., Grimes, J. R., Anderson, K. J., Roper, S. N., and Lee, N. (2001) An essential role for the H218/AGR16/Edg-5/LPB2 sphingosine 1-phosphate receptor in neuronal excitability. Eur. J. Neurosci. 14, 203-209
27. Ishii, I., Ye, X., Friedman, B., Kawamura, S., Contos, J. J., Kingsbury, M. A., Yang, A. H., Zhang, G., Brown, J. H., and Chun, J. (2002) Marked perinatal lethality and cellular signaling deficits in mice null for the two sphingosine 1-phosphate (S1P) receptors, S1P2/LPB2/EDG-5 and S1P3/LPB3/EDG-3. J. Biol. Chem. 277, 25152-25159
28. Choi, J. W., Gardell, S. E., Herr, D. R., Rivera, R., Lee, C. W., Noguchi, K., Teo, S. T., Yung, Y. C., Lu, M., Kennedy, G., and Chun, J. (2011) 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, 751-756
29. Niessen, F., Schaffner, F., Furlan-Freguia, C., Pawlinski, R., Bhattacharjee, G., Chun, J., Derian, C. K., Andrade-Gordon, P., Rosen, H., and Ruf, W. (2008) Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation. Nature 452, 654-658
30. Herr, D. R., Grillet, N., Schwander, M., Rivera, R., Müller, U., and Chun, J. (2007) Sphingosine 1-phosphate (S1P) signaling is required for maintenance of hair cells mainly via activation of S1P2. J. Neurosci. 27, 1474-1478
31. 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, LPB3/EDG-3. J. Biol. Chem. 276, 33697-33704
32. 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
33. Herr, K. J., Herr, D. R., Lee, C. W., Noguchi, K., and Chun, J. (2011) Stereotyped fetal brain disorganization is induced by hypoxia and requires lysophosphatidic acid receptor 1 (LPA1) signaling. Proc. Natl. Acad. Sci. U.S.A. 108, 15444-15449
34. Sibilia, M., and Wagner, E. F. (1995) Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234-238
35. Wu, J., Bohanan, C. S., Neumann, J. C., and Lingrel, J. B. (2008) KLF2 transcription factor modulates blood vessel maturation through smooth muscle cell migration. J. Biol. Chem. 283, 3942-3950
36. Hait, N. C., Bellamy, A., Milstien, S., Kordula, T., and Spiegel, S. (2007) Sphingosine kinase type 2 activation by ERK-mediated phosphorylation. J. Biol. Chem. 282, 12058-12065
37. Johnstone, E. D., Mackova, M., Das, S., Payne, S. G., Lowen, B., Sibley, C. P., Chan, G., and Guilbert, L. J. (2005) Multiple anti-apoptotic pathways stimulated by EGF in cytotrophoblasts. Placenta 26, 548-555
38. Sukocheva, O., Wang, L., Verrier, E., Vadas, M. A., and Xia, P. (2009) Restoring endocrine response in breast cancer cells by inhibition of the sphingosine kinase-1 signaling pathway. Endocrinology 150, 4484-4492
39. Döll, F., Pfeilschifter, J., and Huwiler, A. (2005) The epidermal growth factor stimulates sphingosine kinase-1 expression and activity in the human mammary carcinoma cell line MCF7. Biochim. Biophys. Acta 1738, 72-81
40. Kamada, K., Arita, N., Tsubaki, T., Takubo, N., Fujino, T., Soga, Y., Miyazaki, T., Yamamoto, H., and Nose, M. (2009) Expression of sphingosine kinase 2 in synovial fibroblasts of rheumatoid arthritis contributing to apoptosis by a sphingosine analogue, FTY720. Pathol. Int. 59, 382-389
41. French, K. J., Schrecengost, R. S., Lee, B. D., Zhuang, Y., Smith, S. N., Eberly, J. L., Yun, J. K., and Smith, C. D. (2003) Discovery and evaluation of inhibitors of human sphingosine kinase. Cancer Res. 63, 5962-5969
42. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., and Ullrich, A. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402, 884-888
43. Lepley, D., Paik, J. H., Hla, T., and Ferrer, F. (2005) The G protein-coupled receptor S1P2 regulates Rho/Rho kinase pathway to inhibit tumor cell migration. Cancer Res. 65, 3788-3795
44. Salomone, S., Yoshimura, S., Reuter, U., Foley, M., Thomas, S. S., Moskowitz, M. A., and Waeber, C. (2003) S1P3 receptors mediate the potent constriction of cerebral arteries by sphingosine-1-phosphate. Eur. J. Pharmacol. 469, 125-134
45. Baudhuin, L. M., Cristina, K. L., Lu, J., and Xu, Y. (2002) Akt activation induced by lysophosphatidic acid and sphingosine-1-phosphate requires both mitogen-activated protein kinase kinase and p38 mitogen-activated protein kinase and is cell-line specific. Mol. Pharmacol. 62, 660-671
46. Hsieh, H. L., Sun, C. C., Wu, C. B., Wu, C. Y., Tung, W. H., Wang, H. H., and Yang, C. M. (2008) Sphingosine 1-phosphate induces EGFR expression via Akt/NF-κB and ERK/AP-1 pathways in rat vascular smooth muscle cells. J. Cell. Biochem. 103, 1732-1746
47. Usui, S., Sugimoto, N., Takuwa, N., Sakagami, S., Takata, S., Kaneko, S., and Takuwa, Y. (2004) Blood lipid mediator sphingosine 1-phosphate potently stimulates platelet-derived growth factor-A and -B chain expression through S1P1-Gi-Ras-MAPK-dependent induction of KrÜppel-like factor 5. J. Biol. Chem. 279, 12300-12311
48. 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
49. Rotstein, N. P., Miranda, G. E., Abrahan, C. E., and German, O. L. (2010) Regulating survival and development in the retina: key roles for simple sphingolipids. J. Lipid Res. 51, 1247-1262
50. Esche, M., Hirrlinger, P. G., Rillich, K., Yafai, Y., Pannicke, T., Reichenbach, A., and Weick, M. (2010) Signalling of sphingosine-1-phosphate in Müller glial cells via the S1P/EDG-family of G-protein-coupled receptors. Neurosci. Lett. 480, 101-105
51. Abrahan, C. E., Miranda, G. E., Agnolazza, D. L., Politi, L. E., and Rotstein, N. P. (2010) Synthesis of sphingosine is essential for oxidative stress-induced apoptosis of photoreceptors. Invest. Ophthalmol. Vis. Sci. 51, 1171-1180
52. Zhu, D., Sreekumar, P. G., Hinton, D. R., and Kannan, R. (2010) Expression and regulation of enzymes in the ceramide metabolic pathway in human retinal pigment epithelial cells and their relevance to retinal degeneration. Vis. Res. 50, 643-651
53. McGuire, P. G., Rangasamy, S., Maestas, J., and Das, A. (2011) Pericytederived sphingosine 1-phosphate induces the expression of adhesion proteins and modulates the retinal endothelial cell barrier. Arterioscler. Thromb. Vasc. Biol. 31, e107-e115
54. 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
55. Maines, L. W., French, K. J., Wolpert, E. B., Antonetti, D. A., and Smith, C. D. (2006) Pharmacologic manipulation of sphingosine kinase in retinal endothelial cells: implications for angiogenic ocular diseases. Invest. Ophthalmol. Vis. Sci. 47, 5022-5031
56. Sumida, G. M., and Stamer, W. D. (2011) S1P2 receptor regulation of sphingosine-1-phosphate effects on conventional outflow physiology. Am. J. Physiol. Cell Physiol. 300, C1164-C1171
57. Caballero, S., Swaney, J., Moreno, K., Afzal, A., Kielczewski, J., Stoller, G., Cavalli, A., Garland, W., Hansen, G., Sabbadini, R., and Grant, M. B. (2009) Anti-sphingosine-1-phosphate monoclonal antibodies inhibit angiogenesis and sub-retinal fibrosis in a murine model of laser-induced choroidal neovascularization. Exp. Eye Res. 88, 367-377
58. Xie, B., Shen, J., Dong, A., Rashid, A., Stoller, G., and Campochiaro, P. A. (2009) Blockade of sphingosine-1-phosphate reduces macrophage influx and retinal and choroidal neovascularization. J. Cell. Physiol. 218, 192-198
59. Groves, A., Kihara, Y., and Chun, J. (2013) Fingolimod: direct CNS effects of sphingosine 1-phosphate (S1P) receptor modulation and implications in multiple sclerosis therapy. J. Neurol. Sci. 328, 9-18
60. Copland, D. A., Liu, J., Schewitz-Bowers, L. P., Brinkmann, V., Anderson, K., Nicholson, L. B., and Dick, A. D. (2012) Therapeutic dosing of fingolimod (FTY720) prevents cell infiltration, rapidly suppresses ocular inflammation, and maintains the blood-ocular barrier. Am. J. Pathol. 180, 672-681
61. Raveney, B. J., Copland, D. A., Nicholson, L. B., and Dick, A. D. (2008) Fingolimod (FTY720) as an acute rescue therapy for intraocular inflammatory disease. Arch. Ophthalmol. 126, 1390-1395
62. Kurose, S., Ikeda, E., Tokiwa, M., Hikita, N., and Mochizuki, M. (2000) Effects of FTY720, a novel immunosuppressant, on experimental autoimmune uveoretinitis in rats. Exp. Eye Res. 70, 7-15
63. 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
64. 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