Proteolytic regulation of metabolic enzymes by E3 ubiquitin ligase complexes: Lessons from yeast

Critical Reviews in Biochemistry and Molecular Biology

Volumn 50, Issue 6, 2015, Pages 489-502

  Nakatsukasa, Kunio ^a   Okumura, Fumihiko ^a   Kamura, Takumi ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

Doa10; ER associated degradation; F box protein; Hrd1; metabolic pathway; SCF complex; ubiquitin proteasome system

Indexed keywords

UBIQUITIN PROTEIN LIGASE E3; F BOX PROTEIN; HRD1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SKP1 PROTEIN, S CEREVISIAE; SSM4 PROTEIN, S CEREVISIAE; UBIQUITIN PROTEIN LIGASE;

ACCLIMATIZATION; ARTICLE; CARBON METABOLISM; CARBON SOURCE; CELL CYCLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENVIRONMENTAL CHANGE; ENZYME STABILITY; METABOLIC RATE; METABOLIC REGULATION; METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; STEROL SYNTHESIS; YEAST; CHEMISTRY; CYTOLOGY;

ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; F-BOX PROTEINS; METABOLIC NETWORKS AND PATHWAYS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASES;

EID: 84948567055     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2015.1081869     Document Type: Article

References (156)

1. Alibhoy AA, Giardina BJ, Dunton DD, Chiang HL. (2012). Vid30 is required for the association of Vid vesicles and actin patches in the vacuole import and degradation pathway. Autophagy 8: 29-46
2. Andreasson C, Heessen S, Ljungdahl PO. (2006). Regulation of transcription factor latency by receptor-Activated proteolysis. Genes Dev 20: 1563-8
3. Andreasson C, Ljungdahl PO. (2002). Receptor-mediated endoproteolytic activation of two transcription factors in yeast. Genes Dev 16: 3158-72
4. Andreasson 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: 7503-13
5. Araki K, Nagata K. (2011). Protein folding and quality control in the ER. Cold Spring Harb Perspect Biol 3: a007526
6. Bays NW, Wilhovsky SK, Goradia A, et al. (2001). HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol Biol Cell 12: 4114-28
7. Bazirgan OA, Hampton RY. (2008). Cue1p is an activator of Ubc7p E2 activity in vitro and in vivo. J Biol Chem 283: 12797-810
8. Benanti JA, Cheung SK, Brady MC, Toczyski DP. (2007). A proteomic screen reveals SCFGrr1 targets that regulate the glycolytic-gluconeogenic switch. Nat Cell Biol 9: 1184-91
9. Bhamidipati A, Denic V, Quan EM, Weissman JS. (2005). Exploration of the topological requirements of ERAD identifies Yos9p as a lectin sensor of misfolded glycoproteins in the ER lumen. Mol Cell 19: 741-51
10. Biederer T, Volkwein C, Sommer T. (1997). Role of Cue1p in ubiquitination and degradation at the ER surface. Science 278: 1806-9
11. Bordallo J, Plemper RK, Finger A, Wolf DH. (1998). Der3p/Hrd1p is required for endoplasmic reticulum-Associated degradation of misfolded lumenal and integral membrane proteins. Mol Biol Cell 9: 209-22
12. Brodsky JL. (2012). Cleaning up: ER-Associated degradation to the rescue. Cell 151: 1163-7
13. Brown MS, Goldstein JL. (1980). Multivalent feedback regulation of HMG CoA reductase, a control mechanism coordinating isoprenoid synthesis and cell growth. J Lipid Res 21: 505-17
14. Burgess RJ, Zhou H, Han J, et al. (2012). The SCFDia2 ubiquitin E3 ligase ubiquitylates Sir4 and functions in transcriptional silencing. PLoS Genet 8: e1002846
15. Buschhorn BA, Kostova Z, Medicherla B, Wolf DH. (2004). A genome-wide screen identifies Yos9p as essential for ER-Associated degradation of glycoproteins. FEBS Lett 577: 422-6
16. Carroll SM, Hampton RY. (2010). Usa1p is required for optimal function and regulation of the Hrd1p endoplasmic reticulum-Associated degradation ubiquitin ligase. J Biol Chem 285: 5146-56
17. Carvalho P, Goder V, Rapoport TA. (2006). Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126: 361-73
18. Carvalho P, Stanley AM, Rapoport TA. (2010). Retrotranslocation of a misfolded luminal ER protein by the ubiquitin-ligase Hrd1p. Cell 143: 579-91
19. Chen SH, Chen S, Tokarev AA, et al. (2005). Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol Biol Cell 16: 178-92
20. Chiang HL, Schekman R. (1991). Regulated import and degradation of a cytosolic protein in the yeast vacuole. Nature 350: 313-18
21. Chin JW, Cropp TA, Anderson JC, et al. (2003). An expanded eukaryotic genetic code. Science 301: 964-7
22. Christiano R, Nagaraj N, Frohlich F, Walther TC. (2014). Global proteome turnover analyses of the Yeasts S. cerevisiae and S. pombe. Cell Rep 9: 1959-65
23. Christianson JC, Ye Y. (2014). Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat Struct Mol Biol 21: 325-35
24. Claessen JH, Kundrat L, Ploegh HL. (2012). Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 22: 22-32
25. Clerc S, Hirsch C, Oggier DM, et al. (2009). Htm1 protein generates the N-glycan signal for glycoprotein degradation in the endoplasmic reticulum. J Cell Biol 184: 159-72
26. Daran-lapujade P, Jansen ML, Daran JM, et al. (2004). Role of transcriptional regulation in controlling fluxes in central carbon metabolism of Saccharomyces cerevisiae. A chemostat culture study. J Biol Chem 279: 9125-38
27. Deak PM, Wolf DH. (2001). Membrane topology and function of Der3/Hrd1p as a ubiquitin-protein ligase (E3) involved in endoplasmic reticulum degradation. J Biol Chem 276: 10663-9
28. Deng M, Hochstrasser M. (2006). Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443: 827-31
29. Denic V, Quan EM, Weissman JS. (2006). A luminal surveillance complex that selects misfolded glycoproteins for ER-Associated degradation. Cell 126: 349-59
30. Deshaies RJ, Joazeiro CA. (2009). RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434
31. Duda DM, Borg LA, Scott DC, et al. (2008). Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134: 995-1006
32. Escusa S, Camblong J, Galan JM, et al. (2006). Proteasome- and SCF-dependent degradation of yeast adenine deaminase upon transition from proliferation to quiescence requires a new F-box protein named Saf1p. Mol Microbiol 60: 1014-25
33. Fang L, Wang X, Yamoah K, et al. (2008). Characterization of the human COP9 signalosome complex using affinity purification and mass spectrometry. J Proteome Res 7: 4914-25
34. Feldman RM, Correll CC, Kaplan KB, Deshaies RJ. (1997). A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91: 221-30
35. Finger A, Knop M, Wolf DH. (1993). Analysis of two mutated vacuolar proteins reveals a degradation pathway in the endoplasmic reticulum or a related compartment of yeast. Eur J Biochem 218: 565-74
36. Flury I, Garza R, Shearer A, et al. (2005). INSIG: a broadly conserved transmembrane chaperone for sterol-sensing domain proteins. EMBO J 24: 3917-26
37. Foresti O, Rodriguez-vaello V, Funaya C, Carvalho P. (2014). Quality control of inner nuclear membrane proteins by the Asi complex. Science 346: 751-5
38. Foresti O, Ruggiano A, Hannibal-bach HK, et al. (2013). Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. Elife 2: e00953
39. Forsberg H, Ljungdahl PO. (2001). Genetic and biochemical analysis of the yeast plasma membrane Ssy1p-Ptr3p-Ssy5p sensor of extracellular amino acids. Mol Cell Biol 21: 814-26
40. Furuta N, Fujimura-kamada K, Saito K, et al. (2007). Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol Biol Cell 18: 295-312
41. Galan JM, Wiederkehr A, Seol JH, et al. (2001). Skp1p and the F-box protein Rcy1p form a non-SCF complex involved in recycling of the SNARE Snc1p in yeast. Mol Cell Biol 21: 3105-17
42. Gardner RG, Hampton RY. (1999). A highly conserved signal controls degradation of 3-hydroxy-3-methylglutaryl-coenzyme A (HMG-CoA) reductase in eukaryotes. J Biol Chem 274: 31671-8
43. Gardner RG, Swarbrick GM, Bays NW, et al. (2000). Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p. J Cell Biol 151: 69-82
44. Garza RM, Sato BK, Hampton RY. (2009a). In vitro analysis of Hrd1p-mediated retrotranslocation of its multispanning membrane substrate 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase. J Biol Chem 284: 14710-22
45. Garza RM, Tran PN, Hampton RY. (2009b). Geranylgeranyl pyrophosphate is a potent regulator of HRD-dependent 3-Hydroxy-3-methylglutaryl-CoA reductase degradation in yeast. J Biol Chem 284: 35368-80
46. Gasch AP, Spellman PT, Kao CM, et al. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-57
47. Gauss R, Jarosch E, Sommer T, Hirsch C. (2006a). A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 8: 849-54
48. Gauss R, Kanehara K, Carvalho P, et al. (2011). A complex of Pdi1p and the mannosidase Htm1p initiates clearance of unfolded glycoproteins from the endoplasmic reticulum. Mol Cell 42: 782-93
49. Gauss R, Sommer T, Jarosch E. (2006b). The Hrd1p ligase complex forms a linchpin between ER-lumenal substrate selection and Cdc48p recruitment. EMBO J 25: 1827-35
50. Giardina BJ, Chiang HL. (2013). The key gluconeogenic enzyme fructose-1,6-bisphosphatase is secreted during prolonged glucose starvation and is internalized following glucose re-feeding via the non-classical secretory and internalizing pathways in Saccharomyces cerevisiae. Plant Signal Behav 8: e24936
51. Giardina BJ, Dunton D, Chiang HL. (2013). Vid28 protein is required for the association of vacuole import and degradation (Vid) vesicles with actin patches and the retention of Vid vesicle proteins in the intracellular fraction. J Biol Chem 288: 11636-48
52. Gill S, Stevenson J, Kristiana I, Brown AJ. (2011). Cholesterol-dependent degradation of squalene monooxygenase, a control point in cholesterol synthesis beyond HMG-CoA reductase. Cell Metab 13: 260-73
53. Goldstein JL, Debose-boyd RA, Brown MS. (2006). Protein sensors for membrane sterols. Cell 124: 35-46
54. Graham IA. (2008). Seed storage oil mobilization. Annu Rev Plant Biol 59: 115-42
55. Habeck G, Ebner FA, Shimada-kreft H, Kreft SG. (2015). The yeast ERAD-C ubiquitin ligase Doa10 recognizes an intramembrane degron. J Cell Biol 209: 261-73
56. Hampton RY. (2002). Proteolysis and sterol regulation. Annu Rev Cell Dev Biol 18: 345-78
57. Hampton RY, Gardner RG, Rine J. (1996). Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol Biol Cell 7: 2029-44
58. Hampton RY, Garza RM. (2009). Protein quality control as a strategy for cellular regulation: lessons from ubiquitin-mediated regulation of the sterol pathway. Chem Rev 109: 1561-74
59. Hampton RY, Rine J. (1994). Regulated degradation of HMG-CoA reductase, an integral membrane protein of the endoplasmic reticulum, in yeast. J Cell Biol 125: 299-312
60. Hampton RY, Sommer T. (2012). Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 24: 460-6
61. Harper JW, Tan MK. (2012). Understanding cullin-RING E3 biology through proteomics-based substrate identification. Mol Cell Proteomics 11: 1541-50
62. Helenius A, Aebi M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73: 1019-49
63. Hirsch C, Gauss R, Horn SC, et al. (2009). The ubiquitylation machinery of the endoplasmic reticulum. Nature 458: 453-60
64. Horn SC, Hanna J, Hirsch C, et al. (2009). Usa1 functions as a scaffold of the HRD-ubiquitin ligase. Mol Cell 36: 782-93
65. Hung GC, Brown CR, Wolfe AB, et al. (2004). Degradation of the gluconeogenic enzymes fructose-1,6-bisphosphatase and malate dehydrogenase is mediated by distinct proteolytic pathways and signaling events. J Biol Chem 279: 49138-50
66. Hwang CS, Shemorry A, Varshavsky A. (2010). N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327: 973-7
67. Jakob CA, Bodmer D, Spirig U, et al. (2001). Htm1p, a mannosidase-like protein, is involved in glycoprotein degradation in yeast. EMBO Rep 2: 423-30
68. Jarosch E, Taxis C, Volkwein C, et al. (2002). Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol 4: 134-9
69. Jo Y, Debose-boyd RA. (2010). Control of cholesterol synthesis through regulated ER-Associated degradation of HMG CoA reductase. Crit Rev Biochem Mol Biol 45: 185-98
70. Jonkers W, Rep M. (2009). Lessons from fungal F-box proteins. Eukaryot Cell 8: 677-95
71. Kawakami T, Chiba T, Suzuki T, et al. (2001). NEDD8 recruits E2-ubiquitin to SCF E3 ligase. EMBO J 20: 4003-12
72. Khmelinskii A, Blaszczak E, Pantazopoulou M, et al. (2014). Protein quality control at the inner nuclear membrane. Nature 516: 410-13
73. Kim I, Li Y, Muniz P, Rao H. (2009). Usa1 protein facilitates substrate ubiquitylation through two separate domains. PLoS One 4: e7604
74. Kim W, Spear ED, Ng DT. (2005). Yos9p detects and targets misfolded glycoproteins for ER-Associated degradation. Mol Cell 19: 753-64
75. Knop M, Finger A, Braun T, et al. (1996). Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J 15: 753-63
76. Kornberg HL, Madsen NB. (1958). The metabolism of C2 compounds in microorganisms. 3. Synthesis of malate from acetate via the glyoxylate cycle. Biochem J 68: 549-57
77. Kostova Z, Mariano J, Scholz S, et al. (2009). A Ubc7p-binding domain in Cue1p activates ER-Associated protein degradation. J Cell Sci 122: 1374-81
78. Krebs HA. (1942). The effect of inorganic salts on the ketone decomposition of oxaloacetic acid. Biochem J 36: 303-5
79. Kreft SG, Wang L, Hochstrasser M. (2006). Membrane topology of the yeast endoplasmic reticulum-localized ubiquitin ligase Doa10 and comparison with its human ortholog TEB4 (MARCH-VI). J Biol Chem 281: 4646-53
80. Kunze M, Hartig A. (2013). Permeability of the peroxisomal membrane: lessons from the glyoxylate cycle. Front Physiol 4: 204
81. Kunze M, Pracharoenwattana I, Smith SM, Hartig A. (2006). A central role for the peroxisomal membrane in glyoxylate cycle function. Biochim Biophys Acta 1763: 1441-52
82. La Rue J, Tokarz S, Lanker S. (2005). SCFGrr1-mediated ubiquitination of Gis4 modulates glucose response in yeast. J Mol Biol 349: 685-98
83. Lammer D, Mathias N, Laplaza JM, et al. (1998). Modification of yeast Cdc53p by the ubiquitin-related protein rub1p affects function of the SCFCdc4 complex. Genes Dev 12: 914-26
84. Lechner E, Achard P, Vansiri A, et al. (2006). F-box proteins everywhere. Curr Opin Plant Biol 9: 631-8
85. Liakopoulos D, Busgen T, Brychzy A, et al. (1999). Conjugation of the ubiquitin-like protein NEDD8 to cullin-2 is linked to von Hippel-Lindau tumor suppressor function. Proc Natl Acad Sci USA 96: 5510-15
86. Liu J, Furukawa M, Matsumoto T, Xiong Y. (2002). NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol Cell 10: 1511-18
87. Liu Y, Mimura S, Kishi T, Kamura T. (2009). A longevity protein, Lag2, interacts with SCF complex and regulates SCF function. EMBO J 28: 3366-77
88. Liu Y, Nakatsukasa K, Kotera M, et al. (2011). Non-SCF-type F-box protein Roy1/Ymr258c interacts with a Rab5-like GTPase Ypt52 and inhibits Ypt52 function. Mol Biol Cell 22: 1575-84
89. Loayza D, Tam A, Schmidt WK, Michaelis S. (1998). Ste6p mutants defective in exit from the endoplasmic reticulum (ER) reveal aspects of an ER quality control pathway in Saccharomyces cerevisiae. Mol Biol Cell 9: 2767-84
90. Maric M, Maculins T, De Piccoli G, Labib K. (2014). Cdc48 and a ubiquitin ligase drive disassembly of the CMG helicase at the end of DNA replication. Science 346: 1253596
91. Mark KG, Simonetta M, Maiolica A, et al. (2014). Ubiquitin ligase trapping identifies an SCF(Saf1) pathway targeting unprocessed vacuolar/lysosomal proteins. Mol Cell 53: 148-61
92. Martinez MJ, Roy S, Archuletta AB, et al. (2004). Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol Biol Cell 15: 5295-305
93. Mazon MJ, Gancedo JM, Gancedo C. (1982). Inactivation of yeast fructose-1,6-bisphosphatase. In vivo phosphorylation of the enzyme. J Biol Chem 257: 1128-30
94. Mehnert M, Sommer T, Jarosch E. (2014). Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane. Nat Cell Biol 16: 77-86
95. Mehnert M, Sommermeyer F, Berger M, et al. (2015). The interplay of Hrd3 and the molecular chaperone system ensures efficient degradation of malfolded secretory proteins. Mol Biol Cell 26: 185-94
96. Menssen R, Schweiggert J, Schreiner J, et al. (2012). Exploring the topology of the Gid complex, the E3 ubiquitin ligase involved in catabolite-induced degradation of gluconeogenic enzymes. J Biol Chem 287: 25602-14
97. Mimura S, Komata M, Kishi T, et al. (2009). SCF(Dia2) regulates DNA replication forks during S-phase in budding yeast. EMBO J 28: 3693-705
98. Moriya H, Johnston M. (2004). Glucose sensing and signaling in Saccharomyces cerevisiae through the Rgt2 glucose sensor and casein kinase I. Proc Natl Acad Sci USA 101: 1572-7
99. Morohashi H, Maculins T, Labib K. (2009). The amino-terminal TPR domain of Dia2 tethers SCF(Dia2) to the replisome progression complex. Curr Biol 19: 1943-9
100. Muller M, Muller H, Holzer H. (1981). Immunochemical studies on catabolite inactivation of phosphoenolpyruvate carboxykinase in Saccharomyces cerevisiae. J Biol Chem 256: 723-7
101. Muratani M, Kung C, Shokat KM, Tansey WP. (2005). The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing. Cell 120: 887-99
102. Nakatsukasa K, Brodsky JL. (2008). The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 9: 861-70
103. Nakatsukasa K, Brodsky JL, Kamura T. (2013). A stalled retrotranslocation complex reveals physical linkage between substrate recognition and proteasomal degradation during ER-Associated degradation. Mol Biol Cell 24: 1765-75, S1-8
104. Nakatsukasa K, Huyer G, Michaelis S, Brodsky JL. (2008). Dissecting the ER-Associated degradation of a misfolded polytopic membrane protein. Cell 132: 101-12
105. Nakatsukasa K, Kamura T, Brodsky JL. (2014). Recent technical developments in the study of ER-Associated degradation. Curr Opin Cell Biol 29: 82-91
106. Nakatsukasa K, Nishimura T, Byrne SD, et al. (2015). The ubiquitin ligase SCF acts as a metabolic switch for the glyoxylate cycle. Mol Cell 59: 22-34
107. Nakatsukasa K, Nishikawa S, Hosokawa N, et al. (2001). Mnl1p, an alpha-mannosidase-like protein in yeast Saccharomyces cerevisiae, is required for endoplasmic reticulum-Associated degradation of glycoproteins. J Biol Chem 276: 8635-8
108. Neuber O, Jarosch E, Volkwein C, et al. (2005). Ubx2 links the Cdc48 complex to ER-Associated protein degradation. Nat Cell Biol 7: 993-8
109. Nishikawa SI, Fewell SW, Kato Y, et al. (2001). Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J Cell Biol 153: 1061-70
110. Omnus DJ, Pfirrmann T, Andreasson C, Ljungdahl PO. (2011). A phosphodegron controls nutrient-induced proteasomal activation of the signaling protease Ssy5. Mol Biol Cell 22: 2754-65
111. Osborne TF, Espenshade PJ. (2009). Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it's been. Genes Dev 23: 2578-91
112. Plaxton WC. (2004). Principles of metabolic control. In: Storey KB, ed. Functional metabolism: regulation and adaptation. Hoboken (NJ): John Wiley & Sons, 1-24
113. Plemper RK, Bohmler S, Bordallo J, et al. (1997). Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature 388: 891-5
114. Plemper RK, Egner R, Kuchler K, Wolf DH. (1998). Endoplasmic reticulum degradation of a mutated ATP-binding cassette transporter Pdr5 proceeds in a concerted action of Sec61 and the proteasome. J Biol Chem 273: 32848-56
115. Poulsen P, Lo Leggio L, Kielland-Brandt MC. (2006). Mapping of an internal protease cleavage site in the Ssy5p component of the amino acid sensor of Saccharomyces cerevisiae and functional characterization of the resulting pro- and protease domains by gain-of-function genetics. Eukaryot Cell 5: 601-8
116. Quan EM, Kamiya Y, Kamiya D, et al. (2008). Defining the glycan destruction signal for endoplasmic reticulum-Associated degradation. Mol Cell 32: 870-7
117. Rabinovich E, Kerem A, Fröhlich KU, et al. (2002). AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-Associated protein degradation. Mol Cell Biol 22: 626-34
118. Radonjic M, Andrau JC, Lijnzaad P, et al. (2005). Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol Cell 18: 171-83
119. Ravid T, Kreft SG, Hochstrasser M. (2006). Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J 25: 533-43
120. Raychaudhuri S, Espenshade PJ. (2015). Endoplasmic reticulum exit of golgi-resident defective for SREBP cleavage (Dsc) E3 ligase complex requires its activity. J Biol Chem 290: 14430-40
121. Regelmann J, Schule T, Josupeit FS, et al. (2003). Catabolite degradation of fructose-1,6-bisphosphatase in the yeast Saccharomyces cerevisiae: a genome-wide screen identifies eight novel GID genes and indicates the existence of two degradation pathways. Mol Biol Cell 14: 1652-63
122. Romisch K. (2005). Endoplasmic reticulum-Associated degradation. Annu Rev Cell Dev Biol 21: 435-56
123. Rouillon A, Barbey R, Patton EE, et al. (2000). Feedback-regulated degradation of the transcriptional activator Met4 is triggered by the SCF(Met30)complex. EMBO J 19: 282-94
124. Rubenstein EM, Kreft SG, Greenblatt W, et al. (2012). Aberrant substrate engagement of the ER translocon triggers degradation by the Hrd1 ubiquitin ligase. J Cell Biol 197: 761-73
125. Ruggiano A, Foresti O, Carvalho P. (2014). Quality control: ER-Associated degradation: protein quality control and beyond. J Cell Biol 204: 869-79
126. Saha A, Deshaies RJ. (2008). Multimodal activation of the ubiquitin ligase SCF by Nedd8 conjugation. Mol Cell 32: 21-31
127. Santt O, Pfirrmann T, Braun B, et al. (2008). The yeast GID complex, a novel ubiquitin ligase (E3) involved in the regulation of carbohydrate metabolism. Mol Biol Cell 19: 3323-33
128. Sato BK, Schulz D, Do PH, Hampton RY. (2009). Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol Cell 34: 212-22
129. Schork SM, Bee G, Thumm M, Wolf DH. (1994). Site of catabolite inactivation. Nature 369: 283-4
130. Schuberth C, Buchberger A. (2005). Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-Associated protein degradation. Nat Cell Biol 7: 999-1006
131. Siergiejuk E, Scott DC, Schulman BA, et al. (2009). Cullin neddylation and substrate-Adaptors counteract SCF inhibition by the CAND1-like protein Lag2 in Saccharomyces cerevisiae. EMBO J 28: 3845-56
132. Smothers DB, Kozubowski L, Dixon C, et al. (2000). The abundance of Met30p limits SCF(Met30p) complex activity and is regulated by methionine availability. Mol Cell Biol 20: 7845-52
133. Sommer T, Jentsch S. (1993). A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature 365: 176-9
134. Sommer T, Wolf DH. (2014). The ubiquitin-proteasome-system. Biochim Biophys Acta 1843: 1
135. Song BL, Sever N, Debose-boyd RA. (2005). Gp78, a membrane-Anchored ubiquitin ligase, associates with Insig-1 and couples sterol-regulated ubiquitination to degradation of HMG CoA reductase. Mol Cell 19: 829-40
136. Spielewoy N, Flick K, Kalashnikova TI, et al. (2004). Regulation and recognition of SCFGrr1 targets in the glucose and amino acid signaling pathways. Mol Cell Biol 24: 8994-9005
137. Spielewoy N, Guaderrama M, Wohlschlegel JA, et al. (2010). Npr2, yeast homolog of the human tumor suppressor NPRL2, is a target of Grr1 required for adaptation to growth on diverse nitrogen sources. Eukaryot Cell 9: 592-601
138. Stein A, Ruggiano A, Carvalho P, Rapoport TA. (2014). Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158: 1375-88
139. Stewart EV, Lloyd SJ, Burg JS, et al. (2012). Yeast sterol regulatory element-binding protein (SREBP) cleavage requires Cdc48 and Dsc5, a ubiquitin regulatory X domain-containing subunit of the Golgi Dsc E3 ligase. J Biol Chem 287: 672-81
140. Stewart EV, Nwosu CC, Tong Z, et al. (2011). Yeast SREBP cleavage activation requires the Golgi Dsc E3 ligase complex. Mol Cell 42: 160-71
141. Strijbis K, Distel B. (2010). Intracellular acetyl unit transport in fungal carbon metabolism. Eukaryot Cell 9: 1809-15
142. Swanson R, Locher M, Hochstrasser M. (2001). A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-Associated and Matalpha2 repressor degradation. Genes Dev 15: 2660-74
143. Szathmary R, Bielmann R, Nita-Lazar M, et al. (2005). Yos9 protein is essential for degradation of misfolded glycoproteins and may function as lectin in ERAD. Mol Cell 19: 765-75
144. Theesfeld CL, Hampton RY. (2013). Insulin-induced gene protein (INSIG)-dependent sterol regulation of Hmg2 endoplasmic reticulum-Associated degradation (ERAD) in yeast. J Biol Chem 288: 8519-30
145. Thibault G, Ng DT. (2012). The endoplasmic reticulum-Associated degradation pathways of budding yeast. Cold Spring Harb Perspect Biol 4: a013193
146. Tumusiime S, Zhang C, Overstreet MS, Liu Z. (2011). Differential regulation of transcription factors Stp1 and Stp2 in the Ssy1-Ptr3-Ssy5 amino acid sensing pathway. J Biol Chem 286: 4620-31
147. Vashist S, Ng DT. (2004). Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J Cell Biol 165: 41-52
148. Wang Z, Liu P, Inuzuka H, Wei W. (2014). Roles of F-box proteins in cancer. Nat Rev Cancer 14: 233-47
149. Wiegand G, Remington SJ. (1986). Citrate synthase: structure, control, and mechanism. Annu Rev Biophys Biophys Chem 15: 97-117
150. Wielemans K, Jean C, Vissers S, Andre B. (2010). Amino acid signaling in yeast: post-genome duplication divergence of the Stp1 and Stp2 transcription factors. J Biol Chem 285: 855-65
151. Willems AR, Schwab M, Tyers M. (2004). A hitchhikers guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695: 133-70
152. Ye Y, Meyer HH, Rapoport TA. (2001). The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414: 652-6
153. Ye Y, Meyer HH, Rapoport TA. (2003). Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J Cell Biol 162: 71-84\
154. Zattas D, Adle DJ, Rubenstein EM, Hochstrasser M. (2013). N-terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Mol Biol Cell 24: 890-900
155. Zattas D, Hochstrasser M. (2015). Ubiquitin-dependent protein degradation at the yeast endoplasmic reticulum and nuclear envelope. Crit Rev Biochem Mol Biol 50: 1-17
156. Zheng N, Schulman BA, Song L, et al. (2002). Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416: 703-9