Expression of the ORMDLS, modulators of serine palmitoyltransferase, is regulated by sphingolipids in mammalian cells

Journal of Biological Chemistry

Volumn 290, Issue 1, 2015, Pages 90-98

  Gupta, Sita D ^a   Gable, Kenneth ^a   Alexaki, Aikaterini ^b   Chandris, Panagiotis ^b   Proia, Richard L ^b   Dunn, Teresa M ^a   Harmon, Jeffrey M ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CHAINS; MAMMALS; PHYSIOLOGICAL MODELS;

FUSION PROTEINS; INDUCIBLE PROMOTER; MAMMALIAN CELLS; METABOLIC SIGNALS; OVER-EXPRESSION; PROTEIN EXPRESSIONS; SERINE PALMITOYLTRANSFERASES; TRANSFECTED CELLS;

PROTEINS;

CERAMIDE SYNTHASE; FUMONISIN; HYBRID PROTEIN; MESSENGER RNA; ORMDL PROTEIN; PROTEIN; SERINE PALMITOYLTRANSFERASE; SPHINGOLIPID; SYNTHETASE; THERMOZYMOCIDIN; UNCLASSIFIED DRUG; DIHYDROCERAMIDE DESATURASE; MEMBRANE PROTEIN; MONOUNSATURATED FATTY ACID; ORMDL1 PROTEIN, HUMAN; ORMDL2 PROTEIN, HUMAN; ORMDL3 PROTEIN, HUMAN; OXIDOREDUCTASE; PROTEIN SUBUNIT;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE MUTATION; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; HUMAN CELL; LIPOGENESIS; MAMMAL CELL; METABOLISM; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INDUCTION; ANTAGONISTS AND INHIBITORS; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; MUTATION; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION;

MAMMALIA; SPHINGOIDEA;

FATTY ACIDS, MONOUNSATURATED; FUMONISINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MUTATION; OXIDOREDUCTASES; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; SERINE C-PALMITOYLTRANSFERASE; SIGNAL TRANSDUCTION; SPHINGOLIPIDS; SUBSTRATE SPECIFICITY;

EID: 84920676629     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.588236     Document Type: Article

References (29)

1. Gururaj, C., Federman, R., and Chang, A. (2013) Orm proteins integrate multiple signals to maintain sphingolipid homeostasis. J. Biol. Chem. 288, 20453-20463
2. 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
3. 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
4. Sun, Y., Miao, Y., Yamane, Y., Zhang, C., Shokat, K. M., Takematsu, H., Kozutsumi, Y., and Drubin, D. G. (2012) Orm protein phosphoregulation mediates transient sphingolipid biosynthesis response to heat stress via the Pkh-Ypk and Cdc55-PP2A pathways. Mol. Biol. Cell 23, 2388-2398
5. 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
6. Siow, D. L., and Wattenberg, B. W. (2012) Mammalian ORMDL proteins mediate the feedback response in ceramide biosynthesis. J. Biol. Chem. 287, 40198-40204
7. 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
8. Zhuang, L. L., Jin, R., Zhu, L. H., Xu, H. G., Li, Y., Gao, S., Liu, J. Y., and Zhou, G. P. (2013) Promoter characterization and role of cAMP/PKA/CREB in the basal transcription of the mouse ORMDL3 gene. PLoS One 8, e60630
9. Taouji, S., Higa, A., Delom, F., Palcy, S., Mahon, F. X., Pasquet, J. M., Bosse, R., Ségui, B., and Chevet, E. (2013) Phosphorylation of serine palmitoyltransferase long chain-1 (SPTLC1) on tyrosine 164 inhibits its activity and promotes cell survival. J. Biol. Chem. 288, 17190-17201
10. Gable, K., Gupta, S. D., Han, G., Niranjanakumari, S., Harmon, J. M., and Dunn, T. M. (2010) A disease-causing mutation in the active site of serine palmitoyltransferase causes catalytic promiscuity. J. Biol. Chem. 285, 22846-22852
11. Han, G., Gupta, S. D., Gable, K., Niranjanakumari, S., Moitra, P., Eichler, F., Brown, R. H., Jr., Harmon, J. M., and Dunn, T. M. (2009) Identification of small subunits of mammalian serine palmitoyltransferase that confer distinct acyl-CoA substrate specificities. Proc. Natl. Acad. Sci. U.S.A. 106, 8186-8191
12. Han, G., Gable, K., Yan, L., Natarajan, M., Krishnamurthy, J., Gupta, S. D., Borovitskaya, A., Harmon, J. M., and Dunn, T. M. (2004) The topology of the Lcb1p subunit of yeast serine palmitoyltransferase. J. Biol. Chem. 279, 53707-53716
13. Harmon, J. M., Bacikova, D., Gable, K., Gupta, S. D., Han, G., Sengupta, N., Somashekarappa, N., and Dunn, T. M. (2013) Topological and functional characterization of the ssSPTs, small activating subunits of serine palmitoyltransferase. J. Biol. Chem. 288, 10144-10153
14. Tsegaye, Y., Richardson, C. G., Bravo, J. E., Mulcahy, B. J., Lynch, D. V., Markham, J. E., Jaworski, J. G., Chen, M., Cahoon, E. B., and Dunn, T. M. (2007) Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J. Biol. Chem. 282, 28195-28206
15. Hojjati, M. R., Li, Z., and Jiang, X. C. (2005) Serine palmitoyl-CoA transferase (SPT) deficiency and sphingolipid levels in mice. Biochim. Biophys. Acta 1737, 44-51
16. 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
17. Liu, M., Huang, C., Polu, S. R., Schneiter, R., and Chang, A. (2012) Regulation of sphingolipid synthesis through Orm1 and Orm2 in yeast. J. Cell Sci. 125, 2428-2435
18. Penno, A., Reilly, M. M., Houlden, H., Laurá, M., Rentsch, K., Niederkofler, V., Stoeckli, E. T., Nicholson, G., Eichler, F., Brown, R. H., Jr., von Eckardstein, A., and Hornemann, T. (2010) Hereditary sensory neuropathy type 1 is caused by the accumulation of two neurotoxic sphingolipids. J. Biol. Chem. 285, 11178-11187
19. Zitomer, N. C., Mitchell, T., Voss, K. A., Bondy, G. S., Pruett, S. T., Garnier-Amblard, E. C., Liebeskind, L. S., Park, H., Wang, E., Sullards, M. C., Merrill, A. H., Jr., and Riley, R. T. (2009) Ceramide synthase inhibition by fumonisin B1 causes accumulation of 1-deoxysphinganine: a novel category of bioactive 1-deoxysphingoid bases and 1-deoxydihydroceramides biosynthesized by mammalian cell lines and animals. J. Biol. Chem. 284, 4786-4795
20. Hanada, K., Hara, T., Fukasawa, M., Yamaji, A., Umeda, M., and Nishijima, M. (1998) Mammalian cell mutants resistant to a sphingomyelin-directed cytolysin. Genetic and biochemical evidence for complex formation of the LCB1 protein with the LCB2 protein for serine palmitoyltransferase. J. Biol. Chem. 273, 33787-33794
21. Wang, E., Norred, W. P., Bacon, C. W., Riley, R. T., and Merrill, A. H., Jr. (1991) Inhibition of sphingolipid biosynthesis by fumonisins. Implications for diseases associated with Fusarium moniliforme. J. Biol. Chem. 266, 14486-14490
22. Qiu, R., Yang, Y., Zhao, H., Li, J., Xin, Q., Shan, S., Liu, Y., Dang, J., Yu, X., Gong, Y., and Liu, Q. (2013) Signal transducer and activator of transcription 6 directly regulates human ORMDL3 expression. Febs J. 280, 2014-2026
23. Jin, R., Xu, H. G., Yuan, W. X., Zhuang, L. L., Liu, L. F., Jiang, L., Zhu, L. H., Liu, J. Y., and Zhou, G. P. (2012) Mechanisms elevating ORMDL3 expression in recurrent wheeze patients: role of Ets-1, p300 and CREB. Int. J. Biochem. Cell Biol. 44, 1174-1183
24. 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
25. Akhabir, L., and Sandford, A. J. (2011) Genome-wide association studies for discovery of genes involved in asthma. Respirology 16, 396-406
26. 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
27. Galanter, J., Choudhry, S., Eng, C., Nazario, S., Rodríguez-Santana, J. R., Casal, J., Torres-Palacios, A., Salas, J., Chapela, R., Watson, H. G., Meade, K., LeNoir, M., Rodriguez-Cintrón, W., Avila, P. C., and Burchard, E. G. (2008) ORMDL3 gene is associated with asthma in three ethnically diverse populations. Am. J. Respir. Crit. Care Med. 177, 1194-1200
28. Halapi, E., Gudbjartsson, D. F., Jonsdottir, G. M., Bjornsdottir, U. S., Thorleifsson, G., Helgadottir, H., Williams, C., Koppelman, G. H., Heinzmann, A., Boezen, H. M., Jonasdottir, A., Blondal, T., Gudjonsson, S. A., Jonasdottir, A., Thorlacius, T., Henry, A. P., Altmueller, J., Krueger, M., Shin, H. D., Uh, S. T., Cheong, H. S., Jonsdottir, B., Ludviksson, B. R., Ludviksdottir, D., Gislason, D., Park, C. S., Deichmann, K., Thompson, P. J., Wjst, M., Hall, I. P., Postma, D. S., Gislason, T., Kong, A., Jonsdottir, I., Thorsteinsdottir, U., and Stefansson, K. (2010) A sequence variant on 17q21 is associated with age at onset and severity of asthma. Eur. J. Hum. Genet. 18, 902-908
29. Worgall, T. S., Veerappan, A., Sung, B., Kim, B. I., Weiner, E., Bholah, R., Silver, R. B., Jiang, X. C., and Worgall, S. (2013) Impaired sphingolipid synthesis in the respiratory tract induces airway hyperreactivity. Sci. Transl. Med. 5, 186ra167