Lipid phosphate phosphatase 3 enables efficient thymic egress

Journal of Experimental Medicine

Volumn 208, Issue 6, 2011, Pages 1267-1278

  Bréart, Béatrice ^a   Ramos Perez, Willy D ^a   Mendoza, Alejandra ^a   Salous, Abdelghaffar K ^b   Gobert, Michael ^a   Huang, Yong ^c   Adams, Ralf H ^d,e   Lafaille, Juan J ^a   Escalante Alcalde, Diana ^f   Morris, Andrew J ^b   Schwab, Susan R ^a  

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

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^e UNIVERSITY OF MÜNSTER   (Germany)

^f INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID PHOSPHATE PHOSPHATASE 3; PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CIRCULATION; ENDOTHELIUM CELL; ENZYME DEGRADATION; EPITHELIUM CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; THYMUS;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ENDOTHELIAL CELLS; EPITHELIAL CELLS; GENE DELETION; GREEN FLUORESCENT PROTEINS; LECTINS, C-TYPE; LYSOPHOSPHOLIPIDS; MASS SPECTROMETRY; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PHOSPHATIDATE PHOSPHATASE; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE; T-LYMPHOCYTES; THYMUS GLAND;

EID: 79958257954     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20102551     Document Type: Article

References (60)

1. Alfonso, C., M.G. McHeyzer-Williams, and H. Rosen. 2006. CD69 down-modulation and inhibition of thymic egress by short- and long-term selective chemical agonism of sphingosine 1-phosphate receptors. Eur. J. Immunol. 36:149-159.
2. Allende, M.L., J.L. Dreier, S. Mandala, and R.L. Proia. 2004. Expression of the sphingosine 1-phosphate receptor, S1P1, on T-cells controls thymic emigration. J. Biol. Chem. 279:15396-15401.
3. Alvarez, S.E., K.B. Harikumar, N.C. Hait, J. Allegood, G.M. Strub, E.Y. Kim, M. Maceyka, H. Jiang, C. Luo, T. Kordula, et al. 2010. Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature. 465:1084-1088.
4. Barilà, D., M. Plateroti, F. Nobili, A.O. Muda, Y. Xie, T. Morimoto, and G. Perozzi. 1996. The Dri 42 gene, whose expression is up-regulated during epithelial differentiation, encodes a novel endoplasmic reticulum resident transmembrane protein. J. Biol. Chem. 271:29928-29936.
5. Blair-Handon, R., K. Mueller, and S. Hoogstraten-Miller. 2010. An alternative method for intrathymic injections in mice. Lab Anim. (NY). 39:248-252.
6. Boursalian, T.E., J. Golob, D.M. Soper, C.J. Cooper, and P.J. Fink. 2004. Continued maturation of thymic emigrants in the periphery. Nat. Immunol. 5:418-425.
7. Brindley, D.N., J. Xu, R. Jasinska, and D.W. Waggoner. 2000. Analysis of ceramide 1-phosphate and sphingosine-1-phosphate phosphatase activities. Methods Enzymol. 311:233-244.
8. Brinkmann, V., A. Billich, T. Baumruker, P. Heining, R. Schmouder, G. Francis, S. Aradhye, and P. Burtin. 2010. Fingolimod (FTY720): discovery anddevelopment of an oral drug to treat multiple sclerosis. Nat. Rev. Drug Discov. 9:883-897.
9. Camerer, E., J.B. Regard, I. Cornelissen, Y. Srinivasan, D.N. Duong, D. Palmer, T.H. Pham, J.S. Wong, R. Pappu, and S.R. Coughlin. 2009. Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. J. Clin. Invest. 119:1871-1879.
10. Carroll, W.M. 2010. Oral therapy for multiple sclerosis-sea change or incremental step? N. Engl. J. Med. 362:456-458.
11. Dassule, H.R., P. Lewis, M. Bei, R. Maas, and A.P. McMahon. 2000. Sonic hedgehog regulates growth and morphogenesis of the tooth. Development. 127:4775-4785.
12. Egerton, M., R. Scollay, and K. Shortman. 1990. Kinetics of mature T-cell development in the thymus. Proc. Natl. Acad. Sci. USA. 87:2579-2582.
13. Escalante-Alcalde, D., L. Hernandez, H. Le Stunff, R. Maeda, H.S. Lee, Jr-Gang-Cheng, V.A. Sciorra, I. Daar, S. Spiegel, A.J. Morris, and C.L. Stewart. 2003. The lipid phosphatase LPP3 regulates extra-embryonic vasculogenesis and axis patterning. Development. 130:4623-4637.
14. Escalante-Alcalde, D., R. Sánchez-Sánchez, and C.L. Stewart. 2007. Generation of a conditional Ppap2b/Lpp3 null allele. Genesis. 45:465-469. oi:10.1002/dvg.20314
15. Gordon, J., S. Xiao, B. Hughes III, D.M. Su, S.P. Navarre, B.G. Condie, and N.R. Manley. 2007. Specific expression of lacZ and cre recombinase in fetal thymic epithelial cells by multiplex gene targeting at the Foxn1 locus. BMC Dev. Biol. 7:69.
16. Gray, D.H., A.P. Chidgey, and R.L. Boyd. 2002. Analysis of thymic stromal cell populations using flow cytometry. J. Immunol. Methods. 260:15-28.
17. Hafner, M., J. Wenk, A. Nenci, M. Pasparakis, K. Scharffetter-Kochanek, N. Smyth, T. Peters, D. Kess, O. Holtkötter, P. Shephard, et al. 2004. Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis. 38:176-181.
18. Hait, N.C., J. Allegood, M. Maceyka, G.M. Strub, K.B. Harikumar, S.K. Singh, C. Luo, R. Marmorstein, T. Kordula, S. Milstien, and S. Spiegel. 2009. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science. 325:1254-1257.
19. Hannun, Y.A., and L.M. Obeid. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9:139-150. oi:10.1038/nrm2329
20. Hla, T. 2004. Physiological and pathological actions of sphingosine 1-phosphate. Semin. Cell Dev. Biol. 15:513-520.
21. Hla, T., K. Venkataraman, and J. Michaud. 2008. The vascular S1P gradient-cellular sources and biological significance. Biochim. Biophys. Acta. 781:477-482.
22. Humtsoe, J.O., S. Feng, G.D. Thakker, J. Yang, J. Hong, and K.K. Wary. 2003. Regulation of cell-cell interactions by phosphatidic acid phosphatase 2b/VCIP. EMBO J. 22:1539-1554.
23. Jia, Y.J., M. Kai, I. Wada, F. Sakane, and H. Kanoh. 2003. Differential localization of lipid phosphate phosphatases 1 and 3 to cell surface subdomains in polarized MDCK cells. FEBS Lett. 552:240-246.
24. Kai, M., I. Wada, S. Imai, F. Sakane, and H. Kanoh. 1997. Cloning and characterization of two human isozymes of Mg2+-independent phosphatidic acid phosphatase. J. Biol. Chem. 272:24572-24578.
25. Kato, S. 1997. Thymic microvascular system. Microsc. Res. Tech. 38:287-299.
26. Kisanuki, Y.Y., R.E. Hammer, J. Miyazaki, S.C. Williams, J.A. Richardson, and M. Yanagisawa. 2001. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230:230-242.
27. Kono, M., M.L. Allende, and R.L. Proia. 2008. Sphingosine-1-phosphate regulation of mammalian development. Biochim. Biophys. Acta. 1781:435-41.
28. Kühn, R., F. Schwenk, M. Aguet, and K. Rajewsky. 1995. Inducible gene targeting in mice. Science. 269:1427-1429.
29. Lee, M.J., S. Thangada, K.P. Claffey, N. Ancellin, C.H. Liu, M. Kluk, M. Volpi, R.I. Sha'afi, and T. Hla. 1999. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell. 99:301-312.
30. Liu, C.H., S. Thangada, M.J. Lee, J.R. Van Brocklyn, S. Spiegel, and T. Hla. 1999. Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. Mol. Biol. Cell. 10:1179-1190.
31. Liu, G., S. Burns, G. Huang, K. Boyd, R.L. Proia, R.A. Flavell, and H. Chi. 2009. The receptor S1P1 overrides regulatory T cell-mediated immune suppression through Akt-mTOR. Nat. Immunol. 10:769-777.
32. Liu, G., K. Yang, S. Burns, S. Shrestha, and H. Chi. 2010. The S1P(1)-mTOR axis directs the reciprocal differentiation of T(H)1 and T(reg) cells. Nat. Immunol. 11:1047-1056.
33. Lo, C.G., Y. Xu, R.L. Proia, and J.G. Cyster. 2005. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 201:291-301.
34. López-Juárez, A., S. Morales-Lázaro, R. Sánchez-Sánchez, M. Sunkara, H. Lomelí, I. Velasco, A.J. Morris, and D. Escalante-Alcalde. 2011. Expression of LPP3 in Bergmann glia is required for proper cerebellar sphingosine-1-phosphate metabolism/signaling and development. Glia. 59:577-589.
35. Matloubian, M., C.G. Lo, G. Cinamon, M.J. Lesneski, Y. Xu, V. Brinkmann, M.L. Allende, R.L. Proia, and J.G. Cyster. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 427:355-360.
36. McCaughtry, T.M., M.S. Wilken, and K.A. Hogquist. 2007. Thymic emigration revisited. J. Exp. Med. 204:2513-2520.
37. Mizugishi, K., T. Yamashita, A. Olivera, G.F. Miller, S. Spiegel, and R.L. Proia. 2005. Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol. 25:11113-11121.
38. Mori, K., M. Itoi, N. Tsukamoto, H. Kubo, and T. Amagai. 2007. The perivascular space as a path of hematopoietic progenitor cells and mature T cells between the blood circulation and the thymic parenchyma. Int. Immunol. 19:745-753.
39. Pappu, R., S.R. Schwab, I. Cornelissen, J.P. Pereira, J.B. Regard, Y. Xu, E. Camerer, Y.W. Zheng, Y. Huang, J.G. Cyster, and S.R. Coughlin. 2007. Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science. 316:295-298.
40. Pham, T.H., P. Baluk, Y. Xu, I. Grigorova, A.J. Bankovich, R. Pappu, S.R. Coughlin, D.M. McDonald, S.R. Schwab, and J.G. Cyster. 2010. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207:17-27. oi:10.1084/jem.20091619
41. Puneet, P., C.T. Yap, L. Wong, Y. Lam, D.R. Koh, S. Moochhala, J. Pfeilschifter, A. Huwiler, and A.J. Melendez. 2010. SphK1 regulates proinflammatory responses associated with endotoxin and polymicrobial sepsis. Science. 328:1290-1294.
42. Pyne, S., K.C. Kong, and P.I. Darroch. 2004. Lysophosphatidic acid and sphingosine 1-phosphate biology: the role of lipid phosphate phosphatases. Semin. Cell Dev. Biol. 15:491-501.
43. Renault, A.D., and R. Lehmann. 2006. Follow the fatty brick road: lipid signaling in cell migration. Curr. Opin. Genet. Dev. 16:348-354.
44. Rivera, J., R.L. Proia, and A. Olivera. 2008. The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat. Rev. Immunol. 8:753-763.
45. Roberts, R., V.A. Sciorra, and A.J. Morris. 1998. Human type 2 phosphatidic acid phosphohydrolases. Substrate specificity of the type 2a, 2b, and 2c enzymes and cell surface activity of the 2a isoform. J. Biol. Chem. 273:22059-22067.
46. Rosen, H., C. Alfonso, C.D. Surh, and M.G. McHeyzer-Williams. 2003. Rapid induction of medullary thymocyte phenotypic maturation and egress inhibition by nanomolar sphingosine 1-phosphate receptor agonist. Proc. Natl. Acad. Sci. USA. 100:10907-10912.
47. Saba, J.D., and T. Hla. 2004. Point-counterpoint of sphingosine 1-phosphate metabolism. Circ. Res. 94:724-734.
48. Schwab, S.R., and J.G. Cyster. 2007. Finding a way out: lymphocyte egress from lymphoid organs. Nat. Immunol. 8:1295-1301.
49. Schwab, S.R., J.P. Pereira, M. Matloubian, Y. Xu, Y. Huang, and J.G. Cyster. 2005. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science. 309:1735-1739.
50. Senda, K., K. Koizumi, O. Prangsaengtong, T. Minami, S. Suzuki, I. Takasaki, Y. Tabuchi, H. Sakurai, Y. Doki, T. Misaki, and I. Saiki. 2009. Inducible capillary formation in lymphatic endothelial cells by blocking lipid phosphate phosphatase-3 activity. Lymphat. Res. Biol. 7:69-74.
51. Shiow, L.R., D.B. Rosen, N. Brdicková, Y. Xu, J. An, L.L. Lanier, J.G. Cyster, and M. Matloubian. 2006. CD69 acts downstream of interferon-alpha/ beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature. 440:540-544.
52. Srinivas, S., T. Watanabe, C.S. Lin, C.M. William, Y. Tanabe, T.M. Jessell, and F. Costantini. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1:4.
53. Ushiki, T. 1986. A scanning electron-microscopic study of the rat thymus with special reference to cell types and migration of lymphocytes into the general circulation. Cell Tissue Res. 244:285-298.
54. Ushiki, T., and M. Takeda. 1997. Three-dimensional ultrastructure of the perivascular space in the rat thymus. Arch. Histol. Cytol. 60:89-99.
55. Venkataraman, K., Y.M. Lee, J. Michaud, S. Thangada, Y. Ai, H.L. Bonkovsky, N.S. Parikh, C. Habrukowich, and T. Hla. 2008. Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ. Res. 102:669-676.
56. Wang, Y., M. Nakayama, M.E. Pitulescu, T.S. Schmidt, M.L. Bochenek, A. Sakakibara, S. Adams, A. Davy, U. Deutsch, U. Lüthi, et al. 2010. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature. 465:483-486.
57. Wary, K.K., and J.O. Humtsoe. 2005. Anti-lipid phosphate phosphohydrolase-3 (LPP3) antibody inhibits bFGF- and VEGF-induced capillary morphogenesis of endothelial cells. Cell Commun. Signal. 3:9.
58. Weinreich, M.A., and K.A. Hogquist. 2008. Thymic emigration: when and how T cells leave home. J. Immunol. 181:2265-2270.
59. Yu, W., H. Nagaoka, M. Jankovic, Z. Misulovin, H. Suh, A. Rolink, F. Melchers, E. Meffre, and M.C. Nussenzweig. 1999. Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature. 400:682-687.
60. Zachariah, M.A., and J.G. Cyster. 2010. Neural crest-derived pericytes promote egress of mature thymocytes at the corticomedullary junction. Science. 328:1129-1135.