Latency of transcription factor Stp1 depends on a modular regulatory motif that functions as cytoplasmic retention determinant and nuclear degron

Molecular Biology of the Cell

Volumn 25, Issue 23, 2014, Pages 3823-3833

  Omnus, Deike J ^a,b   Ljungdahl, Per O ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASI PROTEIN; HISTONE; HISTONE HTB2; MEMBRANE PROTEIN; MUTANT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR STP1; UNCLASSIFIED DRUG; ASI1 PROTEIN, S CEREVISIAE; ASI2 PROTEIN, S CEREVISIAE; ASI3 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; RNA BINDING PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; STP1 PROTEIN, S CEREVISIAE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; LATENT PERIOD; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL MEMBRANE; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION, FUNGAL; MEMBRANE PROTEINS; MUTATION; NUCLEAR PROTEINS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84911399577     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-06-1140     Document Type: Article

References (34)

1. Abdel-Sater F, Jean C, Merhi A, Vissers S, André B (2011). Amino-acid signalling in yeast: activation of the Ssy5 protease is associated with its phosphorylation-induced ubiquitylation. J Biol Chem 286, 12006-12015.
2. Akhtar A, Gasser SM (2007). The nuclear envelope and transcriptional control. Nat Rev Genet 8, 507-517.
3. Andréasson C, Heessen S, Ljungdahl PO (2006). Regulation of transcription factor latency by receptor-activated proteolysis. Genes Dev 20, 1563-1568.
4. Andréasson C, Ljungdahl PO (2002). Receptor-mediated endoproteolytic activation of two transcription factors in yeast. Genes Dev 16, 3158-3172.
5. Andréasson C, Ljungdahl PO (2004). The N-terminal regulatory domain of Stp1p is modular and, fused to an artificial transcription factor, confers full Ssy1p-Ptr3p-Ssy5p sensor control. Mol Cell Biol 24, 7503-7513.
6. Antebi A, Fink GR (1992). The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol Biol Cell 3, 633-654.
7. Aronheim A, Zandi E, Hennemann H, Elledge SJ, Karin M (1997). Isolation of an AP-1 repressor by a novel method for detecting protein-protein interactions. Mol Cell Biol 17, 3094-3102.
8. Berndsen CE, Wolberger C (2014). New insights into ubiquitin E3 ligase mechanism. Nat Struct Biol Mol Biol 21, 301-307.
9. Boban M, Ljungdahl PO (2007). Dal81 enhances Stp1- and Stp2-dependent transcription necessitating negative modulation by inner nuclear membrane protein Asi1 in Saccharomyces cerevisiae. Genetics 176, 2087-2097.
10. Boban M, Zargari A, Andréasson C, Heessen S, Thyberg J, Ljungdahl PO (2006). Asi1 is an inner nuclear membrane protein that restricts promoter access of two latent transcription factors. J Cell Biol 173, 695-707.
11. Brivanlou AH, Darnell JE Jr (2002). Signal transduction and the control of gene expression. Science 295, 813-818.
12. Brown MS, Ye J, Rawson RB, Goldstein JL (2000). Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100, 391-398.
13. Budhidarmo R, Nakatani Y, Day CL (2012). RINGs hold the key to ubiquitin transfer. Trends Biol Sci 37, 58-65.
14. Chen P, Johnson P, Sommer T, Jentsch S, Hochstrasser M (1993). Multiple ubiquitin-conjugating enzymes participate in the in vivo degradation of the yeast MAT alpha 2 repressor. Cell 74, 357-369.
15. Delaunay A, Isnard AD, Toledano MB (2000). H2O2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19, 5157-5166.
16. Deng M, Hochstrasser M (2006). Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443, 827-831.
17. Forsberg H, Hammar M, Andréasson C, Moliner A, Ljungdahl PO (2001). Suppressors of ssy1 and ptr3 null mutations define novel amino acid sensor-independent genes in Saccharomyces cerevisiae. Genetics 158, 973-988.
18. Garnier J, Gibrat JF, Robson B (1996). GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol 266, 540-553.
19. Gulshan K, Thommandru B, Moye-Rowley WS (2012). Proteolytic degradation of the Yap1 transcription factor is regulated by subcellular localization and the E3 ubiquitin ligase Not4. J Biol Chem 287, 26796-26805.
20. Heessen S, Fornerod M (2007). The inner nuclear envelope as a transcription factor resting place. EMBO Rep 8, 914-919.
21. Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, Jentsch S (2000). Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102, 577-586.
22. Hoppe T, Rape M, Jentsch S (2001). Membrane-bound transcription factors: regulated release by RIP or RUP. Curr Opin Cell Biol 13, 344-348.
23. Jorgensen MU, Bruun MB, Didion T, Kielland-Brandt MC (1998). Mutations in five loci affecting GAP1-independent uptake of neutral amino acids in yeast. Yeast 14, 103-114.
24. Kippert F (1995). A rapid permeabilization procedure for accurate quantitative determination of beta-galactosidase activity in yeast cells. FEMS Microbiol Lett 128, 201-206.
25. Ljungdahl PO, Daignan-Fornier B (2012). Regulation of amino acid, nucleotide, and phosphate metabolism in Saccharomyces cerevisiae. Genetics 190, 885-929.
26. Malek S, Chen Y, Huxford T, Ghosh G (2001). IkappaBbeta, but not IkappaBalpha, functions as a classical cytoplasmic inhibitor of NF-kappaB dimers by masking both NF-kappaB nuclear localization sequences in resting cells. J Biol Chem 276, 45225-45235.
27. Morano KA, Grant CM, Moye-Rowley WS (2012). The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190, 1157-1195.
28. Omnus DJ, Ljungdahl PO (2013). Rts1-protein phosphatase 2A antagonizes Ptr3-mediated activation of the signaling protease Ssy5 by casein kinase I. Mol Biol Cell 24, 1480-1492.
29. Omnus DJ, Pfirrmann T, Andréasson C, Ljungdahl PO (2011). A phosphodegron controls nutrient-induced proteasomal activation of the signaling protease Ssy5. Mol Biol Cell 22, 2754-2765.
30. Pal B, Chan NC, Helfenbaum L, Tan K, Tansey WP, Gething MJ (2007). SCFCdc4-mediated degradation of the Hac1p transcription factor regulates the unfolded protein response in Saccharomyces cerevisiae. Mol Biol Cell 18, 426-440.
31. Rechsteiner M, Rogers SW (1996). PEST sequences and regulation by proteolysis. Trends Biochem Sci 21, 267-271.
32. Silve S, Volland C, Garnier C, Jund R, Chevallier MR, Haguenauer-Tsapis R (1991). Membrane insertion of uracil permease, a polytopic yeast plasma membrane protein. Mol Cell Biol 11, 1114-1124.
33. Tumusiime S, Zhang C, Overstreet MS, Liu Z (2010). Differential regulation of transcription factors Stp1 and Stp2 in the Ssy1-Ptr3-Ssy5 amino acid sensing pathway. J Biol Chem 286, 4620-4631.
34. Zargari A, Boban M, Heessen S, Andréasson C, Thyberg J, Ljungdahl PO (2007). Inner nuclear membrane proteins Asi1, Asi2, and Asi3 function in concert to maintain the latent properties of transcription factors Stp1 and Stp2. J Biol Chem 282, 594-605.