1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biochemistry
  4. Volume 89, 2020
  5. Article

Annual Review of Biochemistry

Volume 89, 2020

Double the Fun, Double the Trouble: Paralogs and Homologs Functioning in the Endoplasmic Reticulum

Abstract

The evolution of eukaryotic genomes has been propelled by a series of gene duplication events, leading to an expansion in new functions and pathways. While duplicate genes may retain some functional redundancy, it is clear that to survive selection they cannot simply serve as a backup but rather must acquire distinct functions required for cellular processes to work accurately and efficiently. Understanding these differences and characterizing gene-specific functions is complex. Here we explore different gene pairs and families within the context of the endoplasmic reticulum (ER), the main cellular hub of lipid biosynthesis and the entry site for the secretory pathway. Focusing on each of the ER functions, we highlight specificities of related proteins and the capabilities conferred to cells through their conservation. More generally, these examples suggest why related genes have been maintained by evolutionary forces and provide a conceptual framework to experimentally determine why they have survived selection.

Keyword(s): endoplasmic reticulum, gene families, homologs, ohnologs, paralogs
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-011520-104831
2020-06-20
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/biochem/89/1/annurev-biochem-011520-104831.html?itemId=/content/journals/10.1146/annurev-biochem-011520-104831&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ihmels J, Collins SR, Schuldiner M, Krogan NJ, Weissman JS 2007. Backup without redundancy: Genetic interactions reveal the cost of duplicate gene loss. Mol. Syst. Biol. 3:186
     [Google Scholar]
  2. 2. 
    Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A et al. 2003. Global analysis of protein expression in yeast. Nature 425:6959737–41
     [Google Scholar]
  3. 3. 
    Weill U, Yofe I, Sass E, Stynen B, Davidi D et al. 2018. Genome-wide SWAp-Tag yeast libraries for proteome exploration. Nat. Methods 15:617–22
     [Google Scholar]
  4. 4. 
    Aviram N, Schuldiner M. 2017. Targeting and translocation of proteins to the endoplasmic reticulum at a glance. J. Cell Sci. 130:244079–85
     [Google Scholar]
  5. 5. 
    Xing S, Mehlhorn DG, Wallmeroth N, Asseck LY, Kar R et al. 2017. Loss of GET pathway orthologs in Arabidopsis thaliana causes root hair growth defects and affects SNARE abundance. PNAS 114:8E1544–53
     [Google Scholar]
  6. 6. 
    Madeira F, Park YM, Lee J, Buso N, Gur T et al. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res 47:W1W636–41
     [Google Scholar]
  7. 7. 
    Chirico WJ, Waters MG, Blobel G 1988. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 332:6167805–10
     [Google Scholar]
  8. 8. 
    Becker J, Walter W, Yan W, Craig EA 1996. Functional interaction of cytosolic Hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol. Cell. Biol. 16:84378–86
     [Google Scholar]
  9. 9. 
    Ng DT. 1996. Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 134:2269–78
     [Google Scholar]
  10. 10. 
    Tripathi A, Mandon EC, Gilmore R, Rapoport TA 2017. Two alternative binding mechanisms connect the protein translocation Sec71-Sec72 complex with heat shock proteins. J. Biol. Chem. 292:198007–18
     [Google Scholar]
  11. 11. 
    Willmund F, del Alamo M, Pechmann S, Chen T, Albanèse V et al. 2013. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152:1–2196–209
     [Google Scholar]
  12. 12. 
    Craig EA. 2018. Hsp70 at the membrane: driving protein translocation. BMC Biol 16:111
     [Google Scholar]
  13. 13. 
    Cichocki BA, Krumpe K, Vitali DG, Rapaport D 2018. Pex19 is involved in importing dually targeted tail-anchored proteins to both mitochondria and peroxisomes. Traffic 19:10770–85
     [Google Scholar]
  14. 14. 
    Zimmermann R, Eyrisch S, Ahmad M, Helms V 2011. Protein translocation across the ER membrane. Biochim. Biophys. Acta 1808:3912–24
     [Google Scholar]
  15. 15. 
    Finke K, Plath K, Panzner S, Prehn S, Rapoport TA et al. 1996. A second trimeric complex containing homologs of the Sec61p complex functions in protein transport across the ER membrane of S. cerevisiae. EMBO J 15:71482–94
     [Google Scholar]
  16. 16. 
    Wilkinson BM, Tyson JR, Stirling CJ 2001. Ssh1p determines the translocation and dislocation capacities of the yeast endoplasmic reticulum. Dev. Cell 1:3401–9
     [Google Scholar]
  17. 17. 
    Jiang Y, Cheng Z, Mandon EC, Gilmore R 2008. An interaction between the SRP receptor and the translocon is critical during cotranslational protein translocation. J. Cell Biol. 180:61149–61
     [Google Scholar]
  18. 18. 
    Spiller MP, Stirling CJ. 2011. Preferential targeting of a signal recognition particle-dependent precursor to the Ssh1p translocon in yeast. J. Biol. Chem. 286:2521953–60
     [Google Scholar]
  19. 19. 
    Wittke S, Dünnwald M, Albertsen M, Johnsson N 2002. Recognition of a subset of signal sequences by Ssh1p, a Sec61p-related protein in the membrane of endoplasmic reticulum of yeast Saccharomyces cerevisiae. Mol. Biol. Cell 13:72223–32
     [Google Scholar]
  20. 20. 
    Laborenz J, Hansen K, Prescianotto-Baschong C, Spang A, Herrmann JM 2019. In vitro import experiments with semi-intact cells suggest a role of the Sec61 paralog Ssh1 in mitochondrial biogenesis. Biol. Chem. 400:91229–40
     [Google Scholar]
  21. 21. 
    Thul PJ, Åkesson L, Wiking M, Mahdessian D, Geladaki A et al. 2017. A subcellular map of the human proteome. Science 356:6340eaal3321
     [Google Scholar]
  22. 22. 
    Lang S, Benedix J, Fedeles SV, Schorr S, Schirra C et al. 2012. Different effects of Sec61α, Sec62 and Sec63 depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J. Cell Sci. 125:Pt. 81958–69
     [Google Scholar]
  23. 23. 
    Anghel SA, McGilvray PT, Hegde RS, Keenan RJ 2017. Identification of Oxa1 homologs operating in the eukaryotic endoplasmic reticulum. Cell Rep 21:133708–16
     [Google Scholar]
  24. 24. 
    Breitling J, Aebi M. 2013. N-linked protein glycosylation in the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 5:8a013359
     [Google Scholar]
  25. 25. 
    Spirig U, Bodmer D, Wacker M, Burda P, Aebi M 2005. The 3.4-kDa Ost4 protein is required for the assembly of two distinct oligosaccharyltransferase complexes in yeast. Glycobiology 15:121396–406
     [Google Scholar]
  26. 26. 
    Schwarz M, Knauer R, Lehle L 2005. Yeast oligosaccharyltransferase consists of two functionally distinct sub‐complexes, specified by either the Ost3p or Ost6p subunit. FEBS Lett 579:296564–68
     [Google Scholar]
  27. 27. 
    Yan A, Lennarz WJ. 2005. Two oligosaccharyl transferase complexes exist in yeast and associate with two different translocons. Glycobiology 15:121407–15
     [Google Scholar]
  28. 28. 
    Schulz BL, Aebi M. 2009. Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency. Mol. Cell. Proteom. 8:2357–64
     [Google Scholar]
  29. 29. 
    Kelleher DJ, Karaoglu D, Mandon EC, Gilmore R 2003. Oligosaccharyltransferase isoforms that contain different catalytic STT3 subunits have distinct enzymatic properties. Mol. Cell 12:1101–11
     [Google Scholar]
  30. 30. 
    Ruiz-Canada C, Kelleher DJ, Gilmore R 2009. Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian OST isoforms. Cell 136:2272–83
     [Google Scholar]
  31. 31. 
    Braunger K, Pfeffer S, Shrimal S, Gilmore R, Berninghausen O et al. 2018. Structural basis for coupling protein transport and N-glycosylation at the mammalian endoplasmic reticulum. Science 360:6385215–19
     [Google Scholar]
  32. 32. 
    Cherepanova NA, Shrimal S, Gilmore R 2014. Oxidoreductase activity is necessary for N-glycosylation of cysteine-proximal acceptor sites in glycoproteins. J. Cell Biol. 206:4525–39
     [Google Scholar]
  33. 33. 
    Cherepanova NA, Gilmore R. 2016. Mammalian cells lacking either the cotranslational or posttranslocational oligosaccharyltransferase complex display substrate-dependent defects in asparagine linked glycosylation. Sci. Rep. 6:20946
     [Google Scholar]
  34. 34. 
    Loibl M, Strahl S. 2013. Protein O-mannosylation: what we have learned from baker's yeast. Biochim. Biophys. Acta 1833:112438–46
     [Google Scholar]
  35. 35. 
    Blond-Elguindi S. 1993. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:4717–28
     [Google Scholar]
  36. 36. 
    Melnyk A, Rieger H, Zimmermann R 2015. Co-chaperones of the mammalian endoplasmic reticulum. The Networking of Chaperones by Co-chaperones: Control of Cellular Protein Homeostasis GL Blatch, AL Edkins 179–200 Cham, Switz.: Springer
     [Google Scholar]
  37. 37. 
    Shen Y, Hendershot LM. 2005. ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP's interactions with unfolded substrates. Mol. Biol. Cell 16:140–50
     [Google Scholar]
  38. 38. 
    Dudek J. 2002. A novel type of co-chaperone mediates transmembrane recruitment of DnaK-like chaperones to ribosomes. EMBO J 21:122958–67
     [Google Scholar]
  39. 39. 
    Dudek J, Greiner M, Müller A, Hendershot LM, Kopsch K et al. 2005. ERj1p has a basic role in protein biogenesis at the endoplasmic reticulum. Nat. Struct. Mol. Biol. 12:111008–14
     [Google Scholar]
  40. 40. 
    Haßdenteufel S, Johnson N, Paton AW, Paton JC, High S, Zimmermann R 2018. Chaperone-mediated Sec61 channel gating during ER import of small precursor proteins overcomes Sec61 inhibitor-reinforced energy barrier. Cell Rep 23:51373–86
     [Google Scholar]
  41. 41. 
    Wu X, Cabanos C, Rapoport TA 2019. Structure of the post-translational protein translocation machinery of the ER membrane. Nature 566:136–39
     [Google Scholar]
  42. 42. 
    Dong M, Bridges JP, Apsley K, Xu Y, Weaver TE 2008. ERdj4 and ERdj5 are required for endoplasmic reticulum-associated protein degradation of misfolded surfactant protein C. Mol. Biol. Cell 19:62620–30
     [Google Scholar]
  43. 43. 
    Petrova K, Oyadomari S, Hendershot LM, Ron D 2008. Regulated association of misfolded endoplasmic reticulum lumenal proteins with P58/DNAJc3. EMBO J 27:212862–72
     [Google Scholar]
  44. 44. 
    Ellgaard L, McCaul N, Chatsisvili A, Braakman I 2016. Co- and post-translational protein folding in the ER. Traffic 17:6615–38
     [Google Scholar]
  45. 45. 
    Barlowe C. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:6895–907
     [Google Scholar]
  46. 46. 
    Miller E, Antonny B, Hamamoto S, Schekman R 2002. Cargo selection into COPII vesicles is driven by the Sec24p subunit. EMBO J 21:226105–13
     [Google Scholar]
  47. 47. 
    Miller EA, Beilharz TH, Malkus PN, Lee MCS, Hamamoto S et al. 2003. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114:4497–509
     [Google Scholar]
  48. 48. 
    Geva Y, Schuldiner M. 2014. The back and forth of cargo exit from the endoplasmic reticulum. Curr. Biol. 24:3R130–36
     [Google Scholar]
  49. 49. 
    Roberg KJ, Crotwell M, Espenshade P, Gimeno R, Kaiser CA 1999. LST1 is a SEC24 homologue used for selective export of the plasma membrane ATPase from the endoplasmic reticulum. J. Cell Biol. 145:4659–72
     [Google Scholar]
  50. 50. 
    Shimoni Y, Kurihara T, Ravazzola M, Amherdt M, Orci L, Schekman R 2000. Lst1p and Sec24p cooperate in sorting of the plasma membrane ATPase into COPII vesicles in Saccharomyces cerevisiae. J. Cell Biol 151:5973–84
     [Google Scholar]
  51. 51. 
    Kurihara T, Hamamoto S, Gimeno RE, Kaiser CA, Schekman R, Yoshihisa T 2000. Sec24p and Iss1p function interchangeably in transport vesicle formation from the endoplasmic reticulum in Saccharomyces cerevisiae. Mol. Biol. Cell 11:3983–98
     [Google Scholar]
  52. 52. 
    Pagano A, Letourneur F, Garcia-Estefania D, Carpentier J-L, Orci L, Paccaud J-P 1999. Sec24 proteins and sorting at the endoplasmic reticulum. J. Biol. Chem. 274:127833–40
     [Google Scholar]
  53. 53. 
    Tang BL, Kausalya J, Low DYH, Lock ML, Hong W 1999. A family of mammalian proteins homologous to yeast Sec24p. Biochem. Biophys. Res. Commun. 258:3679–84
     [Google Scholar]
  54. 54. 
    Wendeler MW, Paccaud J-P, Hauri H-P 2007. Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep 8:3258–64
     [Google Scholar]
  55. 55. 
    Mancias JD, Goldberg J. 2007. The transport signal on Sec22 for packaging into COPII-coated vesicles is a conformational epitope. Mol. Cell 26:3403–14
     [Google Scholar]
  56. 56. 
    Mancias JD, Goldberg J. 2008. Structural basis of cargo membrane protein discrimination by the human COPII coat machinery. EMBO J 27:212918–28
     [Google Scholar]
  57. 57. 
    Adolf F, Rhiel M, Reckmann I, Wieland FT 2016. Sec24C/D-isoform-specific sorting of the preassembled ER-Golgi Q-SNARE complex. Mol. Biol. Cell 27:172697–707
     [Google Scholar]
  58. 58. 
    Cui Y, Parashar S, Zahoor M, Needham PG, Mari M et al. 2019. A COPII subunit acts with an autophagy receptor to target endoplasmic reticulum for degradation. Science 365:644853–60
     [Google Scholar]
  59. 59. 
    Boyadjiev SA, Fromme JC, Ben J, Chong SS, Nauta C et al. 2006. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat. Genet. 38:101192–97
     [Google Scholar]
  60. 60. 
    Garbes L, Kim K, Rieß A, Hoyer-Kuhn H, Beleggia F et al. 2015. Mutations in SEC24D, encoding a component of the COPII machinery, cause a syndromic form of osteogenesis imperfecta. Am. J. Hum. Genet. 96:3432–39
     [Google Scholar]
  61. 61. 
    Paccaud JP, Reith W, Carpentier JL, Ravazzola M, Amherdt M et al. 1996. Cloning and functional characterization of mammalian homologues of the COPII component Sec23. Mol. Biol. Cell 7:101535–46
     [Google Scholar]
  62. 62. 
    Takida S, Maeda Y, Kinoshita T 2008. Mammalian GPI-anchored proteins require p24 proteins for their efficient transport from the ER to the plasma membrane. Biochem. J. 409:2555–62
     [Google Scholar]
  63. 63. 
    Strating JRPM, Martens GJM. 2012. The p24 family and selective transport processes at the ER-Golgi interface. Biol. Cell 101:9495–509
     [Google Scholar]
  64. 64. 
    Springer S, Chen E, Duden R, Marzioch M, Rowley A et al. 2000. The p24 proteins are not essential for vesicular transport in Saccharomyces cerevisiae. PNAS 97:84034–39
     [Google Scholar]
  65. 65. 
    Karagöz GE, Acosta-Alvear D, Walter P 2019. The unfolded protein response: detecting and responding to fluctuations in the protein-folding capacity of the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 11:9a033886
     [Google Scholar]
  66. 66. 
    Walter P, Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:60591081–86
     [Google Scholar]
  67. 67. 
    Korennykh AV, Egea PF, Korostelev AA, Finer-Moore J, Zhang C et al. 2008. The unfolded protein response signals through high-order assembly of Ire1. Nature 457:7230687–93
     [Google Scholar]
  68. 68. 
    Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:7881–91
     [Google Scholar]
  69. 69. 
    Iwawaki T, Akai R, Yamanaka S, Kohno K 2009. Function of IRE1 alpha in the placenta is essential for placental development and embryonic viability. PNAS 106:3916657–62
     [Google Scholar]
  70. 70. 
    Ghosh R, Lipson KL, Sargent KE, Mercurio AM, Hunt JS et al. 2010. Transcriptional regulation of VEGF-A by the unfolded protein response pathway. PLOS ONE 5:3e9575
     [Google Scholar]
  71. 71. 
    Martino MB, Jones L, Brighton B, Ehre C, Abdulah L et al. 2013. The ER stress transducer IRE1β is required for airway epithelial mucin production. Mucosal Immunol 6:3639–54
     [Google Scholar]
  72. 72. 
    Bertolotti A, Wang X, Novoa I, Jungreis R, Schlessinger K et al. 2001. Increased sensitivity to dextran sodium sulfate colitis in IRE1β-deficient mice. J. Clin. Investig. 107:5585–93
     [Google Scholar]
  73. 73. 
    Iwawaki T, Hosoda A, Okuda T, Kamigori Y, Nomura-Furuwatari C et al. 2001. Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat. Cell Biol. 3:2158–64
     [Google Scholar]
  74. 74. 
    Imagawa Y, Hosoda A, Sasaka S-I, Tsuru A, Kohno K 2008. RNase domains determine the functional difference between IRE1α and IRE1β. FEBS Lett 582:5656–60
     [Google Scholar]
  75. 75. 
    Hollien J, Weissman JS. 2006. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313:5783104–7
     [Google Scholar]
  76. 76. 
    Han D, Lerner AG, Vande Walle L, Upton J-P, Xu W et al. 2009. IRE1α kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138:3562–75
     [Google Scholar]
  77. 77. 
    Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS 2009. Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186:3323–31
     [Google Scholar]
  78. 78. 
    Kimmig P, Diaz M, Zheng J, Williams CC, Lang A et al. 2012. The unfolded protein response in fission yeast modulates stability of select mRNAs to maintain protein homeostasis. eLife 1:e00048
     [Google Scholar]
  79. 79. 
    Maurel M, Chevet E, Tavernier J, Gerlo S 2014. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem. Sci. 39:5245–54
     [Google Scholar]
  80. 80. 
    Haze K, Yoshida H, Yanagi H, Yura T, Mori K 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10:113787–99
     [Google Scholar]
  81. 81. 
    Shoulders MD, Ryno LM, Genereux JC, Moresco JJ, Tu PG et al. 2013. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep 3:41279–92
     [Google Scholar]
  82. 82. 
    Haze K, Okada T, Yoshida H, Yanagi H, Yura T et al. 2001. Identification of the G13 (cAMP-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response. Biochem. J. 355:119–28
     [Google Scholar]
  83. 83. 
    Thuerauf DJ, Morrison L, Glembotski CC 2004. Opposing roles for ATF6α and ATF6β in endoplasmic reticulum stress response gene induction. J. Biol. Chem. 279:2021078–84
     [Google Scholar]
  84. 84. 
    Yamamoto K, Sato T, Matsui T, Sato M, Okada T et al. 2007. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1. Dev. Cell 13:3365–76
     [Google Scholar]
  85. 85. 
    Ishikawa T, Okada T, Ishikawa-Fujiwara T, Todo T, Kamei Y et al. 2013. ATF6α/β-mediated adjustment of ER chaperone levels is essential for development of the notochord in medaka fish. Mol. Biol. Cell 24:91387–95
     [Google Scholar]
  86. 86. 
    Olzmann JA, Kopito RR, Christianson JC 2013. The mammalian endoplasmic reticulum-associated degradation system. Cold Spring Harb. Perspect. Biol. 5:9a013185
     [Google Scholar]
  87. 87. 
    Carvalho P, Goder V, Rapoport TA 2006. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126:2361–73
     [Google Scholar]
  88. 88. 
    Ast T, Aviram N, Chuartzman SG, Schuldiner M 2014. A cytosolic degradation pathway, prERAD, monitors pre-inserted secretory pathway proteins. J. Cell Sci. 127:143017–23
     [Google Scholar]
  89. 89. 
    Swanson R, Locher M, Hochstrasser M 2001. A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matα2 repressor degradation. Genes Dev 15:202660–74
     [Google Scholar]
  90. 90. 
    Weber A, Cohen I, Popp O, Dittmar G, Reiss Y et al. 2016. Sequential poly-ubiquitylation by specialized conjugating enzymes expands the versatility of a quality control ubiquitin ligase. Mol. Cell 63:5827–39
     [Google Scholar]
  91. 91. 
    Bays NW, Gardner RG, Seelig LP, Joazeiro CA, Hampton RY 2001. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3:124–29
     [Google Scholar]
  92. 92. 
    Lester D, Farquharson C, Russell G, Houston B 2000. Identification of a family of noncanonical ubiquitin-conjugating enzymes structurally related to yeast UBC6. Biochem. Biophys. Res. Commun. 269:2474–80
     [Google Scholar]
  93. 93. 
    Oh RS, Bai X, Rommens JM 2006. Human homologs of Ubc6p ubiquitin-conjugating enzyme and phosphorylation of HsUbc6e in response to endoplasmic reticulum stress. J. Biol. Chem. 281:3021480–90
     [Google Scholar]
  94. 94. 
    Elangovan M, Chong HK, Park JH, Yeo EJ, Yoo YJ 2017. The role of ubiquitin-conjugating enzyme Ube2j1 phosphorylation and its degradation by proteasome during endoplasmic stress recovery. J. Cell Commun. Signal. 11:3265–73
     [Google Scholar]
  95. 95. 
    Younger JM, Chen L, Ren H-Y, Rosser MFN, Turnbull EL et al. 2006. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126:3571–82
     [Google Scholar]
  96. 96. 
    Burr ML, Cano F, Svobodova S, Boyle LH, Boname JM, Lehner PJ 2011. HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. PNAS 108:52034–39
     [Google Scholar]
  97. 97. 
    van de Weijer ML, Bassik MC, Luteijn RD, Voorburg CM, Lohuis MAM et al. 2014. A high-coverage shRNA screen identifies TMEM129 as an E3 ligase involved in ER-associated protein degradation. Nat. Commun. 5:3823
     [Google Scholar]
  98. 98. 
    Stefanovic-Barrett S, Dickson AS, Burr SP, Williamson JC, Lobb IT et al. 2018. MARCH6 and TRC8 facilitate the quality control of cytosolic and tail‐anchored proteins. EMBO Rep 19:5e45603
     [Google Scholar]
  99. 99. 
    Neutzner A, Neutzner M, Benischke A-S, Ryu S-W, Frank S et al. 2011. A systematic search for ER membrane-associated RING finger proteins identifies Nixin/ZNRF4 as a regulator of calnexin stability and ER homeostasis. J. Biol. Chem. 286:108633–43
     [Google Scholar]
  100. 100. 
    Maruyama Y, Yamada M, Takahashi K, Yamada M 2008. Ubiquitin ligase Kf-1 is involved in the endoplasmic reticulum-associated degradation pathway. Biochem. Biophys. Res. Commun. 374:4737–41
     [Google Scholar]
  101. 101. 
    Shmueli A, Tsai YC, Yang M, Braun MA, Weissman AM 2009. Targeting of gp78 for ubiquitin-mediated proteasomal degradation by Hrd1: cross-talk between E3s in the endoplasmic reticulum. Biochem. Biophys. Res. Commun. 390:3758–62
     [Google Scholar]
  102. 102. 
    Bernasconi R, Galli C, Calanca V, Nakajima T, Molinari M 2010. Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates. J. Cell Biol. 188:2223–35
     [Google Scholar]
  103. 103. 
    Sun S, Shi G, Sha H, Ji Y, Han X et al. 2015. IRE1α is an endogenous substrate of endoplasmic-reticulum-associated degradation. Nat. Cell Biol. 17:121546–55
     [Google Scholar]
  104. 104. 
    Tyler RE, Pearce MMP, Shaler TA, Olzmann JA, Greenblatt EJ, Kopito RR 2012. Unassembled CD147 is an endogenous endoplasmic reticulum-associated degradation substrate. Mol. Biol. Cell 23:244668–78
     [Google Scholar]
  105. 105. 
    Wang Q, Liu X, Cui Y, Tang Y, Chen W et al. 2014. The E3 ubiquitin ligase AMFR and INSIG1 bridge the activation of TBK1 kinase by modifying the adaptor STING. Immunity 41:6919–33
     [Google Scholar]
  106. 106. 
    Christianson JC, Olzmann JA, Shaler TA, Sowa ME, Bennett EJ et al. 2012. Defining human ERAD networks through an integrative mapping strategy. Nat. Cell Biol. 14:193–105
     [Google Scholar]
  107. 107. 
    Tcherpakov M, Delaunay A, Toth J, Kadoya T, Petroski MD, Ronai ZA 2009. Regulation of endoplasmic reticulum-associated degradation by RNF5-dependent ubiquitination of JNK-associated membrane protein (JAMP). J. Biol. Chem. 284:1812099–109
     [Google Scholar]
  108. 108. 
    Khouri El E, Le Pavec G, Toledano MB, Delaunay-Moisan A 2013. RNF185 is a novel E3 ligase of endoplasmic reticulum-associated degradation (ERAD) that targets cystic fibrosis transmembrane conductance regulator (CFTR). J. Biol. Chem. 288:4331177–91
     [Google Scholar]
  109. 109. 
    Zhong B, Zhang L, Lei C, Li Y, Mao A-P et al. 2009. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity 30:3397–407
     [Google Scholar]
  110. 110. 
    Wang Q, Huang L, Hong Z, Lv Z, Mao Z et al. 2017. The E3 ubiquitin ligase RNF185 facilitates the cGAS-mediated innate immune response. PLOS Pathog 13:3e1006264
     [Google Scholar]
  111. 111. 
    Christianson JC, Ye Y. 2014. Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat. Struct. Mol. Biol. 21:4325–35
     [Google Scholar]
  112. 112. 
    Foresti O, Rodriguez-Vaello V, Funaya C, Carvalho P 2014. Quality control of inner nuclear membrane proteins by the Asi complex. Science 346:6210751–55
     [Google Scholar]
  113. 113. 
    van Meer G, Voelker DR, Feigenson GW 2008. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9:2112–24
     [Google Scholar]
  114. 114. 
    Kuchler K, Daum G, Paltauf F 1986. Subcellular and submitochondrial localization of phospholipid-synthesizing enzymes in Saccharomyces cerevisiae. J. Bacteriol 165:3901–10
     [Google Scholar]
  115. 115. 
    Trotter PJ, Voelker DR. 1995. Identification of a non-mitochondrial phosphatidylserine decarboxylase activity (PSD2) in the yeast Saccharomyces cerevisiae. J. Biol. Chem 270:116062–70
     [Google Scholar]
  116. 116. 
    Gulshan K, Shahi P, Moye-Rowley WS 2010. Compartment-specific synthesis of phosphatidylethanolamine is required for normal heavy metal resistance. Mol. Biol. Cell 21:3443–55
     [Google Scholar]
  117. 117. 
    Chan EYL, McQuibban GA. 2012. Phosphatidylserine decarboxylase 1 (Psd1) promotes mitochondrial fusion by regulating the biophysical properties of the mitochondrial membrane and alternative topogenesis of mitochondrial genome maintenance protein 1 (Mgm1). J. Biol. Chem. 287:4840131–39
     [Google Scholar]
  118. 118. 
    Friedman JR, Kannan M, Toulmay A, Jan CH, Weissman JS et al. 2018. Lipid homeostasis is maintained by dual targeting of the mitochondrial PE biosynthesis enzyme to the ER. Dev. Cell 44:2261–66
     [Google Scholar]
  119. 119. 
    D'mello NP, Childress AM, Franklin DS, Kale SP, Pinswasdi C, Jazwinski SM 1994. Cloning and characterization of LAG1, a longevity-assurance gene in yeast. J. Biol. Chem. 269:2215451–59
     [Google Scholar]
  120. 120. 
    Jiang JC, Kirchman PA, Allen M, Jazwinski SM 2004. Suppressor analysis points to the subtle role of the LAG1 ceramide synthase gene in determining yeast longevity. Exp. Gerontol. 39:7999–1009
     [Google Scholar]
  121. 121. 
    Megyeri M, Prasad R, Volpert G, Sliwa-Gonzalez A, Haribowo AG et al. 2019. Yeast ceramide synthases, Lag1 and Lac1, have distinct substrate specificity. J. Cell Sci. 132:12jcs228411
     [Google Scholar]
  122. 122. 
    Levy M, Futerman AH. 2010. Mammalian ceramide synthases. IUBMB Life 62:5347–56
     [Google Scholar]
  123. 123. 
    Tidhar R, Zelnik ID, Volpert G, Ben-Dor S, Kelly S et al. 2018. Eleven residues determine the acyl chain specificity of ceramide synthases. J. Biol. Chem. 293:259912–21
     [Google Scholar]
  124. 124. 
    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. 109:41561–74
     [Google Scholar]
  125. 125. 
    Basson ME, Thorsness M, Rine J 1986. Saccharomyces cerevisiae contains two functional genes encoding 3-hydroxy-3-methylglutaryl-coenzyme A reductase. PNAS 83:155563–67
     [Google Scholar]
  126. 126. 
    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. 274:4431671–78
     [Google Scholar]
  127. 127. 
    Gardner R, Cronin S, Leader B, Rine J, Hampton R 1998. Sequence determinants for regulated degradation of yeast 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol. Biol. Cell 9:92611–26
     [Google Scholar]
  128. 128. 
    Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM et al. 2003. Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302:56532141–44
     [Google Scholar]
  129. 129. 
    Engfelt WH, Shackelford JE, Aboushadi N, Jessani N, Masuda K et al. 1997. Characterization of UT2 cells: the induction of peroxisomal 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 272:3924579–87
     [Google Scholar]
  130. 130. 
    Menzies SA, Volkmar N, van den Boomen DJ, Timms RT, Dickson AS et al. 2018. The sterol-responsive RNF145 E3 ubiquitin ligase mediates the degradation of HMG-CoA reductase together with gp78 and Hrd1. eLife 7:e40009
     [Google Scholar]
  131. 131. 
    Aboushadi N, Shackelford JE, Jessani N, Gentile A, Krisans SK 2000. Characterization of peroxisomal 3-hydroxy-3-methylglutaryl coenzyme A reductase in UT2* cells: sterol biosynthesis, phosphorylation, degradation, and statin inhibition. Biochemistry 39:1237–47
     [Google Scholar]
  132. 132. 
    Medina MW, Gao F, Ruan W, Rotter JI, Krauss RM 2008. Alternative splicing of 3-hydroxy-3-methylglutaryl coenzyme A reductase is associated with plasma low-density lipoprotein cholesterol response to simvastatin. Circulation 118:4355–62
     [Google Scholar]
  133. 133. 
    Kodaki T, Yamashita S. 1989. Characterization of the methyltransferases in the yeast phosphatidylethanolamine methylation pathway by selective gene disruption. Eur. J. Biochem. 185:2243–51
     [Google Scholar]
  134. 134. 
    Tomohiro S, Kawaguti A, Kawabe Y, Kitada S, Kuge O 2009. Purification and characterization of human phosphatidylserine synthases 1 and 2. Biochem. J. 418:2421–29
     [Google Scholar]
  135. 135. 
    Zaremberg V, McMaster CR. 2002. Differential partitioning of lipids metabolized by separate yeast glycerol-3-phosphate acyltransferases reveals that phospholipase D generation of phosphatidic acid mediates sensitivity to choline-containing lysolipids and drugs. J. Biol. Chem. 277:4139035–44
     [Google Scholar]
  136. 136. 
    Yu J, Loh K, Song Z-Y, Yang H-Q, Zhang Y, Lin S 2018. Update on glycerol-3-phosphate acyltransferases: the roles in the development of insulin resistance. Nutr. Diabetes 8:134
     [Google Scholar]
  137. 137. 
    Samtleben S, Jaepel J, Fecher C, Andreska T, Rehberg M, Blum R 2013. Direct imaging of ER calcium with targeted-esterase induced dye loading (TED). J. Vis. Exp. 7:75e50317
     [Google Scholar]
  138. 138. 
    Altshuler I, Vaillant JJ, Xu S, Cristescu ME 2012. The evolutionary history of sarco(endo)plasmic calcium ATPase (SERCA). PLOS ONE 7:12e52617
     [Google Scholar]
  139. 139. 
    Lytton J, Westlin M, Burk SE, Shull GE, MacLennan DH 1992. Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J. Biol. Chem. 267:2014483–89
     [Google Scholar]
  140. 140. 
    Toyofuku T, Kurzydlowski K, Tada M, MacLennan DH 1993. Identification of regions in the Ca2+-ATPase of sarcoplasmic reticulum that affect functional association with phospholamban. J. Biol. Chem. 268:42809–15
     [Google Scholar]
  141. 141. 
    Wootton LL, Michelangeli F. 2006. The effects of the phenylalanine 256 to valine mutation on the sensitivity of sarcoplasmic/endoplasmic reticulum Ca2+ ATPase (SERCA) Ca2+ pump isoforms 1, 2, and 3 to thapsigargin and other inhibitors. J. Biol. Chem. 281:116970–76
     [Google Scholar]
  142. 142. 
    Lanner JT, Georgiou DK, Joshi AD, Hamilton SL 2010. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb. Perspect. Biol. 2:11a003996
     [Google Scholar]
  143. 143. 
    Ivanova H, Vervliet T, Missiaen L, Parys JB, De Smedt H, Bultynck G 2014. Inositol 1,4,5-trisphosphate receptor-isoform diversity in cell death and survival. Biochim. Biophys. Acta 1843:102164–83
     [Google Scholar]
  144. 144. 
    Williams RT, Manji SSM, Parker NJ, Hancock MS, van Stekelenburg L et al. 2001. Identification and characterization of the STIM (stromal interaction molecule) gene family: coding for a novel class of transmembrane proteins. Biochem. J. 357:3673–85
     [Google Scholar]
  145. 145. 
    Brandman O, Liou J, Park WS, Meyer T 2007. STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:71327–39
     [Google Scholar]
  146. 146. 
    Scorrano L, De Matteis MA, Emr S, Giordano F, Hajnóczky G et al. 2019. Coming together to define membrane contact sites. Nat. Commun. 10:11287
     [Google Scholar]
  147. 147. 
    Valm AM, Cohen S, Legant WR, Melunis J, Hershberg U et al. 2017. Applying systems-level spectral imaging and analysis to reveal the organelle interactome. Nature 546:7656162–67
     [Google Scholar]
  148. 148. 
    Shai N, Yifrach E, van Roermund CWT, Cohen N, Bibi C et al. 2018. Systematic mapping of contact sites reveals tethers and a function for the peroxisome-mitochondria contact. Nat. Commun. 9:11761
     [Google Scholar]
  149. 149. 
    Gatta AT, Wong LH, Sere YY, Calderón-Noreña DM, Cockcroft S et al. 2015. A new family of StART domain proteins at membrane contact sites has a role in ER-PM sterol transport. eLife 4:e07253
     [Google Scholar]
  150. 150. 
    Weill U, Arakel EC, Goldmann O, Golan M, Chuartzman S et al. 2018. Toolbox: Creating a systematic database of secretory pathway proteins uncovers new cargo for COPI. Traffic 19:5370–79
     [Google Scholar]
  151. 151. 
    Elbaz-Alon Y, Eisenberg-Bord M, Shinder V, Stiller SB, Shimoni E et al. 2015. Lam6 regulates the extent of contacts between organelles. Cell Rep 12:17–14
     [Google Scholar]
  152. 152. 
    Murley A, Sarsam RD, Toulmay A, Yamada J, Prinz WA, Nunnari J 2015. Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts. J. Cell Biol. 209:4539–48
     [Google Scholar]
  153. 153. 
    Tong J, Manik MK, Im YJ 2018. Structural basis of sterol recognition and nonvesicular transport by lipid transfer proteins anchored at membrane contact sites. PNAS 115:5E856–65
     [Google Scholar]
  154. 154. 
    Sandhu J, Li S, Fairall L, Pfisterer SG, Gurnett JE et al. 2018. Aster proteins facilitate nonvesicular plasma membrane to ER cholesterol transport in mammalian cells. Cell 175:2514–20
     [Google Scholar]
  155. 155. 
    Horenkamp FA, Valverde DP, Nunnari J, Reinisch KM 2018. Molecular basis for sterol transport by StART‐like lipid transfer domains. EMBO J 37:6e98002
     [Google Scholar]
  156. 156. 
    Besprozvannaya M, Dickson E, Li H, Ginburg KS, Bers DM et al. 2018. GRAM domain proteins specialize functionally distinct ER-PM contact sites in human cells. eLife 7:e31019
     [Google Scholar]
  157. 157. 
    Hariri H, Ugrankar R, Liu Y, Henne WM 2016. Inter-organelle ER-endolysosomal contact sites in metabolism and disease across evolution. Commun. Integr. Biol. 9:3e1156278
     [Google Scholar]
  158. 158. 
    Shibata Y, Voeltz GK, Rapoport TA 2006. Rough sheets and smooth tubules. Cell 126:3435–39
     [Google Scholar]
  159. 159. 
    Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA 2006. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:3573–86
     [Google Scholar]
  160. 160. 
    Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA 2010. Mechanisms determining the morphology of the peripheral ER. Cell 143:5774–88
     [Google Scholar]
  161. 161. 
    Grumati P, Morozzi G, Hölper S, Mari M, Harwardt M-LIE et al. 2017. Full length RTN3 regulates turnover of tubular endoplasmic reticulum via selective autophagy. eLife 6:e25555
     [Google Scholar]
  162. 162. 
    Park SH, Zhu P-P, Parker RL, Blackstone C 2010. Hereditary spastic paraplegia proteins REEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J. Clin. Investig. 120:41097–110
     [Google Scholar]
  163. 163. 
    Hu J, Shibata Y, Zhu P-P, Voss C, Rismanchi N et al. 2009. A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell 138:3549–61
     [Google Scholar]
  164. 164. 
    Westrate LM, Lee JE, Prinz WA, Voeltz GK 2015. Form follows function: the importance of endoplasmic reticulum shape. Annu. Rev. Biochem. 84:791–811
     [Google Scholar]
  165. 165. 
    Joshi AS, Zhang H, Prinz WA 2017. Organelle biogenesis in the endoplasmic reticulum. Nat. Cell Biol. 19:8876–82
     [Google Scholar]
  166. 166. 
    Huh W-K, Falvo JV, Gerke LC, Carroll AS, Howson RW et al. 2003. Global analysis of protein localization in budding yeast. Nature 425:6959686–91
     [Google Scholar]
  167. 167. 
    Meurer M, Duan Y, Sass E, Kats I, Herbst K et al. 2018. Genome-wide C-SWAT library for high-throughput yeast genome tagging. Nat. Methods 15:8598–600
     [Google Scholar]
  168. 168. 
    Yofe I, Weill U, Meurer M, Chuartzman S, Zalckvar E et al. 2016. One library to make them all: streamlining the creation of yeast libraries via a SWAp-Tag strategy. Nat. Methods 13:4371–78
     [Google Scholar]
  169. 169. 
    Breker M, Gymrek M, Moldavski O, Schuldiner M 2013. LoQAtE—Localization and Quantitation ATlas of the yeast proteomE. A new tool for multiparametric dissection of single-protein behavior in response to biological perturbations in yeast. Nucleic Acids Res 42:D1D726–30
     [Google Scholar]
  170. 170. 
    Dubreuil B, Sass E, Nadav Y, Heidenreich M, Georgeson JM et al. 2018. YeastRGB: comparing the abundance and localization of yeast proteins across cells and libraries. Nucleic Acids Res 47:D1D1245–49
     [Google Scholar]
  171. 171. 
    Hibbs MA, Hess DC, Myers CL, Huttenhower C, Li K, Troyanskaya OG 2007. Exploring the functional landscape of gene expression: directed search of large microarray compendia. Bioinformatics 23:202692–99
     [Google Scholar]
  172. 172. 
    Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J et al. 2016. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44:D1D447–56
     [Google Scholar]
  173. 173. 
    Geiger T, Wehner A, Schaab C, Cox J, Mann M 2012. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol. Cell Proteom. 11:3M111.014050
     [Google Scholar]
  174. 174. 
    Geiger T, Velic A, Macek B, Lundberg E, Kampf C et al. 2013. Initial quantitative proteomic map of 28 mouse tissues using the SILAC mouse. Mol. Cell Proteom. 12:61709–22
     [Google Scholar]
  175. 175. 
    Larance M, Ahmad Y, Kirkwood KJ, Ly T, Lamond AI 2013. Global subcellular characterization of protein degradation using quantitative proteomics. Mol. Cell Proteom. 12:3638–50
     [Google Scholar]
  176. 176. 
    Nagana Gowda GA, Djukovic D, Bettcher LF, Gu H, Raftery D 2018. NMR-guided mass spectrometry for absolute quantitation of human blood metabolites. Anal. Chem. 90:32001–9
     [Google Scholar]
  177. 177. 
    Cajka T, Fiehn O. 2015. Toward merging untargeted and targeted methods in mass spectrometry-based metabolomics and lipidomics. Anal. Chem. 88:1524–45
     [Google Scholar]
  178. 178. 
    Kim W, Bennett EJ, Huttlin EL, Guo A, Li J et al. 2011. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44:2325–40
     [Google Scholar]
  179. 179. 
    Ordureau A, Münch C, Harper JW 2015. Quantifying ubiquitin signaling. Mol. Cell 58:4660–76
     [Google Scholar]
  180. 180. 
    Lebesgue N, Megyeri M, Cristobal A, Scholten A, Chuartzman SG et al. 2017. Combining deep sequencing, proteomics, phosphoproteomics, and functional screens to discover novel regulators of sphin-golipid homeostasis. J. Proteome Res. 16:2571–82
     [Google Scholar]
  181. 181. 
    Humphrey SJ, Karayel O, James DE, Mann M 2018. High-throughput and high-sensitivity phosphoproteomics with the EasyPhos platform. Nat. Protoc. 13:91897–916
     [Google Scholar]
  182. 182. 
    De Las Rivas J, Fontanillo C 2010. Protein–protein interactions essentials: key concepts to building and analyzing interactome networks. PLOS Comput. Biol. 6:6e1000807
     [Google Scholar]
  183. 183. 
    Krogan NJ, Cagney G, Yu H, Zhong G, Guo X et al. 2006. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:7084637–43
     [Google Scholar]
  184. 184. 
    Gavin A-C, Aloy P, Grandi P, Krause R, Boesche M et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature 440:7084631–36
     [Google Scholar]
  185. 185. 
    Tarassov K, Messier V, Landry CR, Radinovic S, Molina MMS et al. 2008. An in vivo map of the yeast protein interactome. Science 320:58821465–70
     [Google Scholar]
  186. 186. 
    Huttlin EL, Bruckner RJ, Paulo JA, Cannon JR, Ting L et al. 2017. Architecture of the human interactome defines protein communities and disease networks. Nature 545:7655505–9
     [Google Scholar]
  187. 187. 
    Kim DI, Jensen SC, Noble KA, Birendra KC, Roux KH et al. 2016. An improved smaller biotin ligase for BioID proximity labeling. Mol. Biol. Cell 27:81188–96
     [Google Scholar]
  188. 188. 
    Lam SS, Martell JD, Kamer KJ, Deerinck TJ, Ellisman MH et al. 2014. Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 12:151–54
     [Google Scholar]
  189. 189. 
    Branon TC, Bosch JA, Sanchez AD, Udeshi ND, Svinkina T et al. 2018. Efficient proximity labeling in living cells and organisms with TurboID. Nat. Biotechnol. 36:9880–87
     [Google Scholar]
  190. 190. 
    O'Connor HF, Lyon N, Leung JW, Agarwal P, Swaim CD et al. 2015. Ubiquitin-activated interaction traps (UBAITs) identify E3 ligase binding partners. EMBO Rep 16:121699–712
     [Google Scholar]
  191. 191. 
    Byrne KP, Wolfe KH. 2005. The Yeast Gene Order Browser: Combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15:101456–61
     [Google Scholar]
  192. 192. 
    Guan Y, Dunham MJ, Troyanskaya OG 2007. Functional analysis of gene duplications in Saccharomyces cerevisiae. Genetics 175:2933–43
     [Google Scholar]
  193. 193. 
    Jensen RA. 2001. Orthologs and paralogs—we need to get it right. Genome Biol 2:8 interactions1002.1
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-011520-104831
Loading
Double the Fun, Double the Trouble: Paralogs and Homologs Functioning in the Endoplasmic Reticulum
Annual Review of Biochemistry 89, 637 (2020); https://doi.org/10.1146/annurev-biochem-011520-104831
/content/journals/10.1146/annurev-biochem-011520-104831
/content/journals/10.1146/annurev-biochem-011520-104831
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error