Coordinated regulation of the orosomucoid-like gene family expression controls de novo ceramide synthesis in mammalian cells

Journal of Biological Chemistry

Volumn 290, Issue 5, 2015, Pages 2822-2830

  Kiefer, Kerstin ^a   Carreras Sureda, Amado ^a   García López, Roberto ^a   Rubio Moscardó, Fanny ^a   Casas, Josefina ^b   Fabriàs, Gemma ^b   Vicente, Rubén ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOSYNTHESIS; CERAMIDES; ENERGY TRANSFER; FORSTER RESONANCE ENERGY TRANSFER; GENES; MAMMALS; PALMITIC ACID; PROTEINS; SUBSTRATES;

EXPRESSION CONTROLS; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOPRECIPITATIONS; OLIGOMERIC COMPLEXES; SERINE PALMITOYLTRANSFERASES; SINGLE NUCLEOTIDE POLYMORPHISMS; SYNTHESIS PATHWAYS; UNFOLDED PROTEIN RESPONSE;

COORDINATION REACTIONS;

CERAMIDE; OROSOMUCOID; OROSOMUCOID 1; OROSOMUCOID 2; OROSOMUCOID 3; SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID; UNCLASSIFIED DRUG; ISOPROTEIN; LIPOPOLYSACCHARIDE; PALMITIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME RELEASE; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE; GENE EXPRESSION; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MACROPHAGE; MACROPHAGE ACTIVATION; MAMMAL CELL; NONHUMAN; ORMDL GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; WESTERN BLOTTING; ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; LIPID METABOLISM; METABOLISM; MOUSE;

MAMMALIA;

ANIMALS; CELL LINE; CERAMIDES; HEK293 CELLS; HUMANS; LIPID METABOLISM; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; OROSOMUCOID; PALMITATES; PROTEIN ISOFORMS; SERINE C-PALMITOYLTRANSFERASE; SPHINGOLIPIDS;

EID: 84921932092     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.595116     Document Type: Article

References (24)

1. Hjelmqvist, L., Tuson, M., Marfany, G., Herrero, E., Balcells, S., and Gonzàlez-Duarte, R. (2002) ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins. Genome Biol. 3, RESEARCH0027
2. Moffatt, M. F., Kabesch, M., Liang, L., Dixon, A. L., Strachan, D., Heath, S., Depner, M., von Berg, A., Bufe, A., Rietschel, E., Heinzmann, A., Simma, B., Frischer, T., Willis-Owen, S. A., Wong, K. C., Illig, T., Vogelberg, C., Weiland, S. K., von Mutius, E., Abecasis, G. R., Farrall, M., Gut, I. G., Lathrop, G. M., and Cookson, W. O. (2007) Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 448, 470-473
3. McGovern, D. P., Gardet, A., Törkvist, L., Goyette, P., Essers, J., Taylor, K. D., Neale, B. M., Ong, R. T., Lagacé, C., Li, C., Green, T., Stevens, C. R., Beauchamp, C., Fleshner, P. R., Carlson, M., D'Amato, M., Halfvarson, J., Hibberd, M. L., Lördal, M., Padyukov, L., Andriulli, A., Colombo, E., Latiano, A., Palmieri, O., Bernard, E. J., Deslandres, C., Hommes, D. W., de Jong, D. J., Stokkers, P. C., Weersma, R. K., NIDDK IBD Genetics Consortium, Sharma, Y., Silverberg, M. S., Cho, J. H., Wu, J., Roeder, K., Brant, S. R., Schumm, L. P., Duerr, R. H., Dubinsky, M. C., Glazer, N. L., Haritunians, T., Ippoliti, A., Melmed, G. Y., Siscovick, D. S., Vasiliauskas, E. A., Targan, S. R., Annese, V., Wijmenga, C., Pettersson, S., Rotter, J. I., Xavier, R. J., Daly, M. J., Rioux, J. D., and Seielstad, M. (2010) Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat. Genet. 42, 332-337
4. Barrett, J. C., Hansoul, S., Nicolae, D. L., Cho, J. H., Duerr, R. H., Rioux, J. D., Brant, S. R., Silverberg, M. S., Taylor, K. D., Barmada, M. M., Bitton, A., Dassopoulos, T., Datta, L. W., Green, T., Griffiths, A. M., Kistner, E. O., Murtha, M. T., Regueiro, M. D., Rotter, J. I., Schumm, L. P., Steinhart, A. H., Targan, S. R., Xavier, R. J., NIDDK IBD Genetics Consortium, Libioulle, C., Sandor, C., Lathrop, M., Belaiche, J., Dewit, O., Gut, I., Heath, S., Laukens, D., Mni, M., Rutgeerts, P., Van Gossum, A., Zelenika, D., Franchimont, D., Hugot, J. P., de Vos, M., Vermeire, S., Louis, E., Belgian-French IBD Consortium, Wellcome Trust Case Control Consortium, Cardon, L. R., Anderson, C. A., Drummond, H., Nimmo, E., Ahmad, T., Prescott, N. J., Onnie, C. M., Fisher, S. A., Marchini, J., Ghori, J., Bumpstead, S., Gwilliam, R., Tremelling, M., Deloukas, P., Mansfield, J., Jewell, D., Satsangi, J., Mathew, C. G., Parkes, M., Georges, M., and Daly, M. J. (2008) Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 40, 955-962
5. Barrett, J. C., Clayton, D. G., Concannon, P., Akolkar, B., Cooper, J. D., Erlich, H. A., Julier, C., Morahan, G., Nerup, J., Nierras, C., Plagnol, V., Pociot, F., Schuilenburg, H., Smyth, D. J., Stevens, H., Todd, J. A., Walker, N. M., and Rich, S. S. (2009) Genome-wide association study and metaanalysis find that over 40 loci affect risk of type 1 diabetes. Nat. Genet. 41, 703-707
6. Kurreeman, F. A., Stahl, E. A., Okada, Y., Liao, K., Diogo, D., Raychaudhuri, S., Freudenberg, J., Kochi, Y., Patsopoulos, N. A., Gupta, N., CLEAR investigators, Sandor, C., Bang, S. Y., Lee, H. S., Padyukov, L., Suzuki, A., Siminovitch, K., Worthington, J., Gregersen, P. K., Hughes, L. B., Reynolds, R. J., Bridges, S. L., Jr., Bae, S. C., Yamamoto, K., and Plenge, R. M. (2012) Use of a multiethnic approach to identify rheumatoid-arthritissusceptibility loci, 1p36 and 17q12. Am. J. Hum. Genet. 90, 524-532
7. Cantero-Recasens, G., Fandos, C., Rubio-Moscardo, F., Valverde, M. A., and Vicente, R. (2010) The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Hum. Mol. Genet. 19, 111-121
8. Carreras-Sureda, A., Cantero-Recasens, G., Rubio-Moscardo, F., Kiefer, K., Peinelt, C., Niemeyer, B. A., Valverde, M. A., and Vicente, R. (2013) ORMDL3 modulates store-operated calcium entry and lymphocyte activation. Hum. Mol. Genet. 22, 519-530
9. Han, S., Lone, M. A., Schneiter, R., and Chang, A. (2010) Orm1 and Orm2 are conserved endoplasmic reticulum membrane proteins regulating lipid homeostasis and protein quality control. Proc. Natl. Acad. Sci. U.S.A. 107, 5851-5856
10. Breslow, D. K., Collins, S. R., Bodenmiller, B., Aebersold, R., Simons, K., Shevchenko, A., Ejsing, C. S., and Weissman, J. S. (2010) Orm family proteins mediate sphingolipid homeostasis. Nature 463, 1048-1053
11. Roelants, F. M., Breslow, D. K., Muir, A., Weissman, J. S., and Thorner, J. (2011) Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 108, 19222-19227
12. Munoz-Olaya, J. M., Matabosch, X., Bedia, C., Egido-Gabás, M., Casas, J., Llebaria, A., Delgado, A., and Fabriàs, G. (2008) Synthesis and biological activity of a novel inhibitor of dihydroceramide desaturase. ChemMed-Chem 3, 946-953
13. Canals, D., Mormeneo, D., Fabriàs, G., Llebaria, A., Casas, J., and Delgado, A. (2009) Synthesis and biological properties of pachastrissamine (jaspine B) and diastereoisomeric jaspines. Bioorg. Med. Chem. 17, 235-241
14. Garcia-Elias, A., Mrkonjic, S., Pardo-Pastor, C., Inada, H., Hellmich, U. A., Rubio-Moscardó, F., Plata, C., Gaudet, R., Vicente, R., and Valverde, M. A. (2013) Phosphatidylinositol-4,5-biphosphate-dependent rearrangement of TRPV4 cytosolic tails enables channel activation by physiological stimuli. Proc. Natl. Acad. Sci. U.S.A. 110, 9553-9558
15. Siow, D. L., and Wattenberg, B. W. (2012) Mammalian ORMDL proteins mediate the feedback response in ceramide biosynthesis. J. Biol. Chem. 287, 40198-40204
16. Schilling, J. D., Machkovech, H. M., He, L., Sidhu, R., Fujiwara, H., Weber, K., Ory, D. S., and Schaffer, J. E. (2013) Palmitate and lipopolysaccharide trigger synergistic ceramide production in primary macrophages. J. Biol. Chem. 288, 2923-2932
17. Andreyev, A. Y., Fahy, E., Guan, Z., Kelly, S., Li, X., McDonald, J. G., Milne, S., Myers, D., Park, H., Ryan, A., Thompson, B. M., Wang, E., Zhao, Y., Brown, H. A., Merrill, A. H., Raetz, C. R., Russell, D. W., Subramaniam, S., and Dennis, E. A. (2010) Subcellular organelle lipidomics in TLR-4-activated macrophages. J. Lipid Res. 51, 2785-2797
18. Chang, Z. Q., Lee, S. Y., Kim, H. J., Kim, J. R., Kim, S. J., Hong, I. K., Oh, B. C., Choi, C. S., Goldberg, I. J., and Park, T. S. (2011) Endotoxin activates de novo sphingolipid biosynthesis via nuclear factor κB-mediated upregulation of Sptlc2. Prostaglandins Other Lipid Mediat. 94, 44-52
19. Sims, K., Haynes, C. A., Kelly, S., Allegood, J. C., Wang, E., Momin, A., Leipelt, M., Reichart, D., Glass, C. K., Sullards, M. C., and Merrill, A. H., Jr. (2010) Kdo2-lipid A, a TLR4-specific agonist, induces de novo sphingolipid biosynthesis in RAW264.7 macrophages, which is essential for induction of autophagy. J. Biol. Chem. 285, 38568-38579
20. Yu, H., Valerio, M., and Bielawski, J. (2013) Fenretinide inhibited de novo ceramide synthesis and proinflammatory cytokines induced by Aggregatibacter actinomycetemcomitans. J. Lipid Res. 54, 189-201
21. Verlaan, D. J., Berlivet, S., Hunninghake, G. M., Madore, A. M., Larivière, M., Moussette, S., Grundberg, E., Kwan, T., Ouimet, M., Ge, B., Hoberman, R., Swiatek, M., Dias, J., Lam, K. C., Koka, V., Harmsen, E., Soto- Quiros, M., Avila, L., Celedón, J. C., Weiss, S. T., Dewar, K., Sinnett, D., Laprise, C., Raby, B. A., Pastinen, T., and Naumova, A. K. (2009) Allelespecific chromatin remodeling in the ZPBP2/GSDMB/ORMDL3 locus associated with the risk of asthma and autoimmune disease. Am. J. Hum. Genet. 85, 377-393
22. Shimobayashi, M., Oppliger, W., Moes, S., Jenö, P., and Hall, M. N. (2013) TORC1-regulated protein kinase Npr1 phosphorylates Orm to stimulate complex sphingolipid synthesis. Mol. Biol. Cell 24, 870-881
23. Miller, M., Tam, A. B., Cho, J. Y., Doherty, T. A., Pham, A., Khorram, N., Rosenthal, P., Mueller, J. L., Hoffman, H. M., Suzukawa, M., Niwa, M., and Broide, D. H. (2012) ORMDL3 is an inducible lung epithelial gene regulating metalloproteases, chemokines, OAS, and ATF6. Proc. Natl. Acad. Sci. U.S.A. 109, 16648-16653
24. Miller, M., Rosenthal, P., Beppu, A., Mueller, J. L., Hoffman, H. M., Tam, A. B., Doherty, T. A., McGeough, M. D., Pena, C. A., Suzukawa, M., Niwa, M., and Broide, D. H. (2014) ORMDL3 transgenic mice have increased airway remodeling and airway responsiveness characteristic of asthma. J. Immunol. 192, 3475-3487