Non-vesicular trafficking by a ceramide-1-phosphate transfer protein regulates eicosanoids

Nature

Volumn 500, Issue 7463, 2013, Pages 463-467

  Simanshu, Dhirendra K ^a   Kamlekar, Ravi Kanth ^b   Wijesinghe, Dayanjan S ^c   Zou, Xianqiong ^b   Zhai, Xiuhong ^b   Mishra, Shrawan K ^b   Molotkovsky, Julian G ^d   Malinina, Lucy ^e   Hinchcliffe, Edward H ^b   Chalfant, Charles E ^c,f,g   Brown, Rhoderick E ^b   Patel, Dinshaw J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^e CIC BIOGUNE   (Spain)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CARRIER PROTEIN; CERAMIDE 1 PHOSPHATE; ICOSANOID; PHOSPHATIDIC ACID;

ASTHMA; CANCER; CELL ORGANELLE; CRYSTAL STRUCTURE; ENZYME; ENZYME ACTIVITY; GROWTH; MIGRATION; PHOSPHATE; PLASMA; PROTEIN; RNA; SURVIVAL; TRAFFICKING;

ARTICLE; CELL FRACTIONATION; CELL MEMBRANE; CHROMOSOME 1; CHROMOSOME 12; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOSOL; GOLGI COMPLEX; HYDROGEN BOND; HYDROPHOBICITY; MEMBRANE VESICLE; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPROTEINS; ARACHIDONIC ACID; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; CELL NUCLEUS; CERAMIDES; CRYSTALLOGRAPHY, X-RAY; CYTOSOL; EICOSANOIDS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MODELS, MOLECULAR; PHOSPHATIDIC ACIDS; PROTEIN CONFORMATION; PROTEIN FOLDING; SUBSTRATE SPECIFICITY; TRANS-GOLGI NETWORK;

EID: 84882924058     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12332     Document Type: Article

References (34)

1. Hannun, Y. A. & Obeid, L. M. Principles of bioactive lipid signalling: lessons from sphingolipids. Nature Rev. Mol. Cell Biol. 9, 139-150 (2008).
2. Chalfant, C. E.& Spiegel, S. Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling. J. Cell Sci. 118, 4605-4612 (2005).
3. Lamour, N. F. & Chalfant, C. E. Ceramide kinase and the ceramide-1-phosphate/cPLA2a interaction as a therapeutic target. Curr. Drug Targets 9, 674-682 (2008).
4. Gangoiti, P. et al. Control of metabolism and signaling of simple bioactive sphingolipids: Implications in disease. Prog. Lipid Res. 49, 316-334 (2010).
5. Maceyka, M., Harikumar, K. B., Milstien, S. & Spiegel, S. Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol. 22, 50-60 (2012).
6. Wymann, M. P. & Schneiter, R. Lipid signalling in disease. Nature Rev. Mol. Cell Biol. 9, 162-176 (2008).
7. Leslie, C. C., Gangelhoff, T. A. & Gelb, M. H. Localization and function of cytosolic phospholipase A2a at the Golgi. Biochimie 92, 620-626 (2010).
8. Bechler, M. E., de Figueiredo, P.&Brown, W. J. A. PLA1-2punch regulates the Golgi complex. Trends Cell Biol. 22, 116-124 (2012).
9. Harizi, H., Corcuff, J. B.&Gualde, N. Arachidonic-acid-derived eicosanoids: roles in biology and immunopathology. Trends Mol. Med. 14, 461-469 (2008).
10. Boath, A. et al. Regulation and traffic of ceramide 1-phosphate produced by ceramide kinase: comparative analysis to glucosylceramide and sphingomyelin. J. Biol. Chem. 283, 8517-8526 (2008).
11. Lev, S. Non-vesicular lipid transport by lipid-transfer proteins and beyond. Nature Rev. Mol. Cell Biol. 11, 739-750 (2010).
12. Prinz, W. A. Lipid trafficking sans vesicles: where, why, how? Cell 143, 870-874 (2010).
13. Malinina, L., Malakhova, M. L., Teplov, A., Brown, R. E. & Patel, D. J. Structural basis for glycosphingolipid transfer specificity. Nature 430, 1048-1053 (2004).
14. Malakhova, M. L. et al. Point mutational analysis of the liganding site in human glycolipid transfer protein. Functionality of the complex. J. Biol. Chem. 280, 26312-26320 (2005).
15. Hirsch, A. K., Fischer, F. R. & Diederich, F. Phosphate recognition in structural biology. Angew. Chem. Int. Ed. Engl. 46, 338-352 (2007).
16. Bourquin, F., Riezman, H., Capitani, G. & Grutter, M. G. Structure and function of sphingosine-1-phosphate lyase, a key enzyme of sphingolipid metabolism. Structure 18, 1054-1065 (2010).
17. Berna, A. et al. For whom the bell tolls? DING proteins in health and disease. Cell. Mol Life Sci. 66, 2205-2218 (2009).
18. Furuhashi, M. & Hotamisligil, G. S. Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nature Rev. Drug Discov. 7, 489-503 (2008).
19. Roderick, S. L. et al. Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nature Struct. Biol. 9, 507-511 (2002).
20. Hanada, K. et al. Molecular machinery for non-vesicular trafficking of ceramide. Nature 426, 803-809 (2003).
21. Kudo, N. et al. Structural basis for specific lipid recognition byCERTresponsible for nonvesicular trafficking of ceramide. Proc. Natl Acad. Sci. USA 105, 488-493 (2008).
22. Zou, X. et al. Human glycolipid transfer protein (GLTP) genes: organization, transcriptional status and evolution. BMC Genomics 9, 72 (2008).
23. Orengo, C. A. & Thornton, J. M. Protein families and their evolution-a structural perspective. Annu. Rev. Biochem. 74, 867-900 (2005).
24. Galperin, M. Y. & Koonin, E. V. Divergence and convergence in enzyme evolution. J. Biol. Chem. 287, 21-28 (2012).
25. Liberles, D. A. et al. The interface of protein structure, protein biophysics, and molecular evolution. Protein Sci. 21, 769-785 (2012).
26. Lamour, N. F. et al. Ceramide 1-phosphate is required for the translocation of group IVA cytosolic phospholipase A2 and prostaglandin synthesis. J. Biol. Chem. 284, 26897-26907 (2009).
27. Lamour, N. F. et al. Ceramide kinase uses ceramide provided by ceramide transport protein: localization to organelles of eicosanoid synthesis. J. Lipid Res. 48, 1293-1304 (2007).
28. Bornancin, F. Ceramide kinase: the first decade. Cell. Signal. 23, 999-1008(2011).
29. Durcan, T. M. et al. Tektin2is required for central spindle microtubule organization and the completion of cytokinesis. J. Cell Biol. 181, 595-603 (2008).
30. Samygina, V. R. et al. Enhanced selectivity for sulfatide by engineered human glycolipid transfer protein. Structure 19, 1644-1654 (2011).
31. Manders, E. M. M., Stap, J., Brakenhoff, G. J., van Driel, R. & Aten, J. A. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 103, 857-862 (1992).
32. Hornick, J. E. et al. Amphiastral mitotic spindle assembly in vertebrate cells lacking centrosomes. Curr. Biol. 21, 598-605 (2011).
33. Wijesinghe, D. S. et al. Use of high performance liquid chromatographyelectrospray ionization-tandemmass spectrometry for the analysis of ceramide-1-phosphate levels. J. Lipid Res. 51, 641-651 (2010).
34. Blaho, V. A., Buczynski, M. W., Brown, C. R. & Dennis, E. A. Lipidomic analysis of dynamic eicosanoid responses during the induction and resolution of Lyme arthritis. J. Biol. Chem. 284, 21599-21612 (2009).