A Eukaryotic Sensor for Membrane Lipid Saturation

Molecular Cell

Volumn 63, Issue 1, 2016, Pages 49-59

  Covino, Roberto ^a   Ballweg, Stephanie ^b   Stordeur, Claudius ^b   Michaelis, Jonas B ^b   Puth, Kristina ^b   Wernig, Florian ^b   Bahrami, Amir ^a   Ernst, Andreas M ^c   Hummer, Gerhard ^a   Ernst, Robert ^b  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DESATURASE; LINOLEIC ACID; MEMBRANE LIPID; OLE1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MGA2; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; DELTA-9 FATTY ACID DESATURASE; FATTY ACID; MEMBRANE PROTEIN; MGA2 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOSENSOR; CELL DISRUPTION; CHEMICAL STRUCTURE; DIMERIZATION; ELECTRON SPIN RESONANCE; ENDOPLASMIC RETICULUM MEMBRANE; FATTY ACID DESATURATION; GENETIC CONSERVATION; HYDROPHOBICITY; INDEL MUTATION; LIPID BILAYER; LIPID COMPOSITION; LIPID METABOLISM; MEMBRANE FLUIDITY; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MUTAGENESIS; OLIGOMERIZATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROCESSING; UBIQUITINATION; ALPHA HELIX; CHEMISTRY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; MUTATION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION;

ELECTRON SPIN RESONANCE SPECTROSCOPY; ENDOPLASMIC RETICULUM; FATTY ACID DESATURASES; FATTY ACIDS; GENE EXPRESSION REGULATION, FUNGAL; INTRACELLULAR MEMBRANES; MEMBRANE FLUIDITY; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; MUTATION; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN STABILITY; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84992379395     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.015     Document Type: Article

References (41)

1. Auld, K.L., Brown, C.R., Casolari, J.M., Komili, S., Silver, P.A., Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates. Mol. Cell 21 (2006), 861–871.
2. Best, R.B., Zhu, X., Shim, J., Lopes, P.E.M., Mittal, J., Feig, M., Mackerell, A.D. Jr., Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, ψ and side-chain χ(1) and χ(2) dihedral angles. J. Chem. Theory Comput. 8 (2012), 3257–3273.
3. Bhattacharya, S., Shcherbik, N., Vasilescu, J., Smith, J.C., Figeys, D., Haines, D.S., Identification of lysines within membrane-anchored Mga2p120 that are targets of Rsp5p ubiquitination and mediate mobilization of tethered Mga2p90. J. Mol. Biol. 385 (2009), 718–725.
4. Bordignon, E., Steinhoff, H.-J., Membrane protein structure and dynamics studied by site-directed spin labeling ESR. Hemminga, M.A., Berline, L.J., (eds.) ESR Spectroscopy in Membrane Biophysics, 2007, Springer Science and Business Media, New York, 129–164.
5. Currie, E., Schulze, A., Zechner, R., Walther, T.C., Farese, R.V. Jr., Cellular fatty acid metabolism and cancer. Cell Metab. 18 (2013), 153–161.
6. Cybulski, L.E., Martín, M., Mansilla, M.C., Fernández, A., de Mendoza, D., Membrane thickness cue for cold sensing in a bacterium. Curr. Biol. 20 (2010), 1539–1544.
7. de Mendoza, D., Temperature sensing by membranes. Annu. Rev. Microbiol. 68 (2014), 101–116.
8. Deguil, J., Pineau, L., Rowland Snyder, E.C., Dupont, S., Beney, L., Gil, A., Frapper, G., Ferreira, T., Modulation of lipid-induced ER stress by fatty acid shape. Traffic 12 (2011), 349–362.
9. Eckel, R.H., Grundy, S.M., Zimmet, P.Z., The metabolic syndrome. Lancet 365 (2005), 1415–1428.
10. Holthuis, J.C., Menon, A.K., Lipid landscapes and pipelines in membrane homeostasis. Nature 510 (2014), 48–57.
11. Hoppe, T., Matuschewski, K., Rape, M., Schlenker, S., Ulrich, H.D., Jentsch, S., Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102 (2000), 577–586.
12. Hulko, M., Berndt, F., Gruber, M., Linder, J.U., Truffault, V., Schultz, A., Martin, J., Schultz, J.E., Lupas, A.N., Coles, M., The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126 (2006), 929–940.
13. Jiang, Y., Vasconcelles, M.J., Wretzel, S., Light, A., Gilooly, L., McDaid, K., Oh, C.S., Martin, C.E., Goldberg, M.A., Mga2p processing by hypoxia and unsaturated fatty acids in Saccharomyces cerevisiae: impact on LORE-dependent gene expression. Eukaryot. Cell 1 (2002), 481–490.
14. Kaiser, H.J., Lingwood, D., Levental, I., Sampaio, J.L., Kalvodova, L., Rajendran, L., Simons, K., Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. USA 106 (2009), 16645–16650.
15. Kaiser, H.J., Orłowski, A., Róg, T., Nyholm, T.K., Chai, W., Feizi, T., Lingwood, D., Vattulainen, I., Simons, K., Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching. Proc. Natl. Acad. Sci. USA 108 (2011), 16628–16633.
16. Kandasamy, P., Vemula, M., Oh, C.S., Chellappa, R., Martin, C.E., Regulation of unsaturated fatty acid biosynthesis in Saccharomyces: the endoplasmic reticulum membrane protein, Mga2p, a transcription activator of the OLE1 gene, regulates the stability of the OLE1 mRNA through exosome-mediated mechanisms. J. Biol. Chem. 279 (2004), 36586–36592.
17. Klauda, J.B., Venable, R.M., Freites, J.A., O'Connor, J.W., Tobias, D.J., Mondragon-Ramirez, C., Vorobyov, I., MacKerell, A.D. Jr., Pastor, R.W., Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J. Phys. Chem. B 114 (2010), 7830–7843.
18. Kolawa, N., Sweredoski, M.J., Graham, R.L.J., Oania, R., Hess, S., Deshaies, R.J., Perturbations to the ubiquitin conjugate proteome in yeast δubx mutants identify Ubx2 as a regulator of membrane lipid composition. Mol. Cell. Proteomics 12 (2013), 2791–2803.
19. Lande, M.B., Donovan, J.M., Zeidel, M.L., The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J. Gen. Physiol. 106 (1995), 67–84.
20. Marrink, S.J., Tieleman, D.P., Perspective on the Martini model. Chem. Soc. Rev. 42 (2013), 6801–6822.
21. Marrink, S.J., Risselada, H.J., Yefimov, S., Tieleman, D.P., de Vries, A.H., The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111 (2007), 7812–7824.
22. Marsh, D., Polarity and permeation profiles in lipid membranes. Proc. Natl. Acad. Sci. USA 98 (2001), 7777–7782.
23. Martin, C.E., Oh, C.S., Jiang, Y., Regulation of long chain unsaturated fatty acid synthesis in yeast. Biochim. Biophys. Acta 1771 (2007), 271–285.
24. Matthews, E.E., Zoonens, M., Engelman, D.M., Dynamic helix interactions in transmembrane signaling. Cell 127 (2006), 447–450.
25. Monticelli, L., Kandasamy, S.K., Periole, X., Larson, R.G., Tieleman, D.P., Marrink, S.-J., The MARTINI Coarse-Grained Force Field: Extension to Proteins. J. Chem. Theory Comput. 4 (2008), 819–834.
26. Neuber, O., Jarosch, E., Volkwein, C., Walter, J., Sommer, T., Ubx2 links the Cdc48 complex to ER-associated protein degradation. Nat. Cell Biol. 7 (2005), 993–998.
27. Puth, K., Hofbauer, H.F., Sáenz, J.P., Ernst, R., Homeostatic control of biological membranes by dedicated lipid and membrane packing sensors. Biol. Chem. 396 (2015), 1043–1058.
28. Rape, M., Hoppe, T., Gorr, I., Kalocay, M., Richly, H., Jentsch, S., Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 107 (2001), 667–677.
29. Schneiter, R., Brügger, B., Sandhoff, R., Zellnig, G., Leber, A., Lampl, M., Athenstaedt, K., Hrastnik, C., Eder, S., Daum, G., et al. Electrospray ionization tandem mass spectrometry (ESI-MS/MS) analysis of the lipid molecular species composition of yeast subcellular membranes reveals acyl chain-based sorting/remodeling of distinct molecular species en route to the plasma membrane. J. Cell Biol. 146 (1999), 741–754.
30. Sharpe, H.J., Stevens, T.J., Munro, S., A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142 (2010), 158–169.
31. Shcherbik, N., Zoladek, T., Nickels, J.T., Haines, D.S., Rsp5p is required for ER bound Mga2p120 polyubiquitination and release of the processed/tethered transactivator Mga2p90. Curr. Biol. 13 (2003), 1227–1233.
32. Shcherbik, N., Kee, Y., Lyon, N., Huibregtse, J.M., Haines, D.S., A single PXY motif located within the carboxyl terminus of Spt23p and Mga2p mediates a physical and functional interaction with ubiquitin ligase Rsp5p. J. Biol. Chem. 279 (2004), 53892–53898.
33. Siepe, D., Jentsch, S., Prolyl isomerase Pin1 acts as a switch to control the degree of substrate ubiquitylation. Nat. Cell Biol. 11 (2009), 967–972.
34. Sinensky, M., Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc. Natl. Acad. Sci. USA 71 (1974), 522–525.
35. Stordeur, C., Puth, K., Sáenz, J.P., Ernst, R., Crosstalk of lipid and protein homeostasis to maintain membrane function. Biol. Chem. 395 (2014), 313–326.
36. Stukey, J.E., McDonough, V.M., Martin, C.E., Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae. J. Biol. Chem. 264 (1989), 16537–16544.
37. Surma, M.A., Klose, C., Peng, D., Shales, M., Mrejen, C., Stefanko, A., Braberg, H., Gordon, D.E., Vorkel, D., Ejsing, C.S., et al. A lipid E-MAP identifies Ubx2 as a critical regulator of lipid saturation and lipid bilayer stress. Mol. Cell 51 (2013), 519–530.
38. Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., Mackerell, A.D. Jr., CHARMM general force field: a force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J. Comput. Chem. 31 (2010), 671–690.
39. Vembar, S.S., Brodsky, J.L., One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9 (2008), 944–957.
40. Volmer, R., van der Ploeg, K., Ron, D., Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc. Natl. Acad. Sci. USA 110 (2013), 4628–4633.
41. Zhang, S., Skalsky, Y., Garfinkel, D.J., MGA2 or SPT23 is required for transcription of the delta9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae. Genetics 151 (1999), 473–483.