Spatial control of lipid droplet proteins by the ERAD ubiquitin ligase Doa10

EMBO Journal

Volumn 35, Issue 15, 2016, Pages 1644-1655

  Ruggiano, Annamaria ^a,b,c   Mora, Gabriel ^a,b   Buxó, Laura ^a,b   Carvalho, Pedro ^a,b  

^a BARCELONA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Doa10; endoplasmic reticulum; ERAD; lipid droplets; protein degradation

Indexed keywords

DGA1 PROTEIN; FAT DROPLET; LIPID DROPLET PROTEIN; PGC1 PROTEIN; PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE DOA10; UNCLASSIFIED DRUG; YEH1 PROTEIN;

ALLELE; ARTICLE; BLEACHING; CELL ORGANELLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME DEGRADATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UBIQUITINATION;

EID: 84980351850     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201593106     Document Type: Article

References (62)

1. Ammerer G, Hunter CP, Rothman JH, Saari GC, Valls LA, Stevens TH (1986) PEP4 gene of Saccharomyces cerevisiae encodes proteinase A, a vacuolar enzyme required for processing of vacuolar precursors. Mol Cell Biol 6: 2490–2499
2. Ast T, Aviram N, Chuartzman SG, Schuldiner M (2014) A cytosolic degradation pathway, prERAD, monitors pre-inserted secretory pathway proteins. J Cell Sci 127: 3017–3023
3. Bagnat M, Keranen S, Shevchenko A, Simons K (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 97: 3254–3259
4. Bays NW, Wilhovsky SK, Goradia A, Hodgkiss-Harlow K, Hampton RY (2001) HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol Biol Cell 12: 4114–4128
5. Beilharz T, Egan B, Silver PA, Hofmann K, Lithgow T (2003) Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J Biol Chem 278: 8219–8223
6. Boban M, Zargari A, Andreasson 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
7. Braakman I, Hebert DN (2013) Protein folding in the endoplasmic reticulum. Cold Spring Harb Perspect Biol 5: a013201
8. Braun S, Matuschewski K, Rape M, Thoms S, Jentsch S (2002) Role of the ubiquitin-selective CDC48(UFD1/NPL4)chaperone (segregase) in ERAD of OLE1 and other substrates. EMBO J 21: 615–621
9. Carvalho P, Goder V, Rapoport TA (2006) Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126: 361–373
10. Chen YC, Umanah GK, Dephoure N, Andrabi SA, Gygi SP, Dawson TM, Dawson VL, Rutter J (2014) Msp1/ATAD1 maintains mitochondrial function by facilitating the degradation of mislocalized tail-anchored proteins. EMBO J 33: 1548–1564
11. Choi K, Kim H, Kang H, Lee SY, Lee SJ, Back SH, Lee SH, Kim MS, Lee JE, Park JY, Kim J, Kim S, Song JH, Choi Y, Lee S, Lee HJ, Kim JH, Cho S (2014) Regulation of diacylglycerol acyltransferase 2 protein stability by gp78-associated endoplasmic-reticulum-associated degradation. FEBS J 281: 3048–3060
12. Christianson JC, Ye Y (2014) Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat Struct Mol Biol 21: 325–335
13. Currie E, Guo X, Christiano R, Chitraju C, Kory N, Harrison K, Haas J, Walther TC, Farese RV Jr (2014) High confidence proteomic analysis of yeast LDs identifies additional droplet proteins and reveals connections to dolichol synthesis and sterol acetylation. J Lipid Res 55: 1465–1477
14. Denic V, Quan EM, Weissman JS (2006) A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126: 349–359
15. Fei W, Shui G, Gaeta B, Du X, Kuerschner L, Li P, Brown AJ, Wenk MR, Parton RG, Yang H (2008) Fld1p, a functional homologue of human seipin, regulates the size of lipid droplets in yeast. J Cell Biol 180: 473–482
16. Fei W, Wang H, Fu X, Bielby C, Yang H (2009) Conditions of endoplasmic reticulum stress stimulate lipid droplet formation in Saccharomyces cerevisiae. Biochem J 424: 61–67
17. Fernandez-Murray JP, McMaster CR (2005) Glycerophosphocholine catabolism as a new route for choline formation for phosphatidylcholine synthesis by the Kennedy pathway. J Biol Chem 280: 38290–38296
18. Fisher E, Almaguer C, Holic R, Griac P, Patton-Vogt J (2005) Glycerophosphocholine-dependent growth requires Gde1p (YPL110c) and Git1p in Saccharomyces cerevisiae. J Biol Chem 280: 36110–36117
19. Foresti O, Rodriguez-Vaello V, Funaya C, Carvalho P (2014) Quality control of inner nuclear membrane proteins by the Asi complex. Science 346: 751–755
20. Foresti O, Ruggiano A, Hannibal-Bach HK, Ejsing CS, Carvalho P (2013) Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. eLife 2: e00953
21. Furth N, Gertman O, Shiber A, Alfassy OS, Cohen I, Rosenberg MM, Doron NK, Friedler A, Ravid T (2011) Exposure of bipartite hydrophobic signal triggers nuclear quality control of Ndc10 at the endoplasmic reticulum/nuclear envelope. Mol Biol Cell 22: 4726–4739
22. Gauss R, Jarosch E, Sommer T, Hirsch C (2006) A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery. Nat Cell Biol 8: 849–854
23. Grillitsch K, Connerth M, Kofeler H, Arrey TN, Rietschel B, Wagner B, Karas M, Daum G (2011) Lipid particles/droplets of the yeast Saccharomyces cerevisiae revisited: lipidome meets proteome. Biochim Biophys Acta 1811: 1165–1176
24. 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: 2029–2044
25. Heinemeyer W, Gruhler A, Mohrle V, Mahe Y, Wolf DH (1993) PRE2, highly homologous to the human major histocompatibility complex-linked RING10 gene, codes for a yeast proteasome subunit necessary for chrymotryptic activity and degradation of ubiquitinated proteins. J Biol Chem 268: 5115–5120
26. Hessa T, Sharma A, Mariappan M, Eshleman HD, Gutierrez E, Hegde RS (2011) Protein targeting and degradation are coupled for elimination of mislocalized proteins. Nature 475: 394–397
27. Ingelmo-Torres M, Gonzalez-Moreno E, Kassan A, Hanzal-Bayer M, Tebar F, Herms A, Grewal T, Hancock JF, Enrich C, Bosch M, Gross SP, Parton RG, Pol A (2009) Hydrophobic and basic domains target proteins to lipid droplets. Traffic 10: 1785–1801
28. Jacquier N, Choudhary V, Mari M, Toulmay A, Reggiori F, Schneiter R (2011) Lipid droplets are functionally connected to the endoplasmic reticulum in Saccharomyces cerevisiae. J Cell Sci 124: 2424–2437
29. Jarosch E, Taxis C, Volkwein C, Bordallo J, Finley D, Wolf DH, Sommer T (2002) Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol 4: 134–139
30. Jo Y, Hartman IZ, DeBose-Boyd RA (2013) Ancient ubiquitous protein-1 mediates sterol-induced ubiquitination of 3-hydroxy-3-methylglutaryl CoA reductase in lipid droplet-associated endoplasmic reticulum membranes. Mol Biol Cell 24: 169–183
31. Khmelinskii A, Blaszczak E, Pantazopoulou M, Fischer B, Omnus DJ, Le Dez G, Brossard A, Gunnarsson A, Barry JD, Meurer M, Kirrmaier D, Boone C, Huber W, Rabut G, Ljungdahl PO, Knop M (2014) Protein quality control at the inner nuclear membrane. Nature 516: 410–413
32. Klemm EJ, Spooner E, Ploegh HL (2011) Dual role of ancient ubiquitous protein 1 (AUP1) in lipid droplet accumulation and endoplasmic reticulum (ER) protein quality control. J Biol Chem 286: 37602–37614
33. Kushnirov VV (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857–860
34. Latterich M, Frohlich KU, Schekman R (1995) Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell 82: 885–893
35. Lian JP, Ferro-Novick S (1993) Bos1p, an integral membrane protein of the endoplasmic reticulum to Golgi transport vesicles, is required for their fusion competence. Cell 73: 735–745
36. Liu Q, Siloto RM, Snyder CL, Weselake RJ (2011) Functional and topological analysis of yeast acyl-CoA:diacylglycerol acyltransferase 2, an endoplasmic reticulum enzyme essential for triacylglycerol biosynthesis. J Biol Chem 286: 13115–13126
37. Loewen CJ, Young BP, Tavassoli S, Levine TP (2007) Inheritance of cortical ER in yeast is required for normal septin organization. J Cell Biol 179: 467–483
38. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961
39. Markgraf DF, Klemm RW, Junker M, Hannibal-Bach HK, Ejsing CS, Rapoport TA (2014) An ER protein functionally couples neutral lipid metabolism on lipid droplets to membrane lipid synthesis in the ER. Cell Rep 6: 44–55
40. McKinney SA, Murphy CS, Hazelwood KL, Davidson MW, Looger LL (2009) A bright and photostable photoconvertible fluorescent protein. Nat Methods 6: 131–133
41. Oelkers P, Cromley D, Padamsee M, Billheimer JT, Sturley SL (2002) The DGA1 gene determines a second triglyceride synthetic pathway in yeast. J Biol Chem 277: 8877–8881
42. Okreglak V, Walter P (2014) The conserved AAA-ATPase Msp1 confers organelle specificity to tail-anchored proteins. Proc Natl Acad Sci USA 111: 8019–8024
43. Olzmann JA, Richter CM, Kopito RR (2013) Spatial regulation of UBXD8 and p97/VCP controls ATGL-mediated lipid droplet turnover. Proc Natl Acad Sci USA 110: 1345–1350
44. Pol A, Gross SP, Parton RG (2014) Review: biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J Cell Biol 204: 635–646
45. Rabinovich E, Kerem A, Frohlich KU, Diamant N, Bar-Nun S (2002) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 22: 626–634
46. Rodrigo-Brenni MC, Gutierrez E, Hegde RS (2014) Cytosolic quality control of mislocalized proteins requires RNF126 recruitment to Bag6. Mol Cell 55: 227–237
47. Ruggiano A, Foresti O, Carvalho P (2014) Quality control: ER-associated degradation: protein quality control and beyond. J Cell Biol 204: 869–879
48. Sandager L, Gustavsson MH, Stahl U, Dahlqvist A, Wiberg E, Banas A, Lenman M, Ronne H, Stymne S (2002) Storage lipid synthesis is non-essential in yeast. J Biol Chem 277: 6478–6482
49. 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
50. Shibata Y, Voss C, Rist JM, Hu J, Rapoport TA, Prinz WA, Voeltz GK (2008) The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J Biol Chem 283: 18892–18904
51. Smith MH, Ploegh HL, Weissman JS (2011) Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086–1090
52. Sorger D, Athenstaedt K, Hrastnik C, Daum G (2004) A yeast strain lacking lipid particles bears a defect in ergosterol formation. J Biol Chem 279: 31190–31196
53. Sorger D, Daum G (2002) Synthesis of triacylglycerols by the acyl-coenzyme A:diacyl-glycerol acyltransferase Dga1p in lipid particles of the yeast Saccharomyces cerevisiae. J Bacteriol 184: 519–524
54. Spandl J, Lohmann D, Kuerschner L, Moessinger C, Thiele C (2011) Ancient ubiquitous protein 1 (AUP1) localizes to lipid droplets and binds the E2 ubiquitin conjugase G2 (Ube2g2) via its G2 binding region. J Biol Chem 286: 5599–5606
55. Stein A, Ruggiano A, Carvalho P, Rapoport TA (2014) Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158: 1375–1388
56. Stolz A, Besser S, Hottmann H, Wolf DH (2013) Previously unknown role for the ubiquitin ligase Ubr1 in endoplasmic reticulum-associated protein degradation. Proc Natl Acad Sci USA 110: 15271–15276
57. 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: 2660–2674
58. Thiam AR, Farese RV Jr, Walther TC (2013) The biophysics and cell biology of lipid droplets. Nat Rev Mol Cell Biol 14: 775–786
59. Tsirigos KD, Peters C, Shu N, Kall L, Elofsson A (2015) The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acids Res 43: W401–W407
60. Wang CW, Lee SC (2012) The ubiquitin-like (UBX)-domain-containing protein Ubx2/Ubxd8 regulates lipid droplet homeostasis. J Cell Sci 125: 2930–2939
61. Wilfling F, Wang H, Haas JT, Krahmer N, Gould TJ, Uchida A, Cheng JX, Graham M, Christiano R, Frohlich F, Liu X, Buhman KK, Coleman RA, Bewersdorf J, Farese RV Jr, Walther TC (2013) Triacylglycerol synthesis enzymes mediate lipid droplet growth by relocalizing from the ER to lipid droplets. Dev Cell 24: 384–399
62. 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: 652–656