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Review Article

TPR-containing proteins control protein organization and homeostasis for the endoplasmic reticulum

, &
Pages 103-118 | Received 22 Jan 2019, Accepted 01 Mar 2019, Published online: 26 Apr 2019

References

  • Alder NN, Shen Y, Brodsky JL, Hendershot LM, Johnson AE. 2005. The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum. J Cell Biol. 168:389–399.
  • Allan RK, Ratajczak T. 2011. Versatile TPR domains accommodate different modes of target protein recognition and function. Cell Stress Chaperones. 16:353–367.
  • Andresen CA, Smedegaard S, Sylvestersen KB, Svensson C, Iglesias-Gato D, Cazzamali G, Nielsen TK, Nielsen ML, Flores-Morales A. 2014. Protein interaction screening for the ankyrin repeats and suppressor of cytokine signaling (SOCS) box (ASB) family identify Asb11 as a novel endoplasmic reticulum resident ubiquitin ligase. J Biol Chem. 289:2043–2054.
  • Apweiler R, Hermjakob H, Sharon N. 1999. On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database11Dedicated to Prof. Akira Kobata and Prof. Harry Schachter on the occasion of their 65th birthdays. Biochimica et Biophysica Acta (BBA) - General Subjects. 1473:4–8.
  • Assimon VA, Southworth DR, Gestwicki JE. 2015. Specific binding of tetratricopeptide repeat proteins to heat shock protein 70 (Hsp70) and heat shock protein 90 (Hsp90) is regulated by affinity and phosphorylation. Biochemistry. 54:7120–7131.
  • Barlowe C. 1998. COPII and selective export from the endoplasmic reticulum. Biochim Biophys Acta. 1404:67–76.
  • Benyair R, Ogen-Shtern N, Lederkremer GZ. 2015. Glycan regulation of ER-associated degradation through compartmentalization. Semin Cell Dev Biol. 41:99–109.
  • Benyair R, Ogen-Shtern N, Mazkereth N, Shai B, Ehrlich M, Lederkremer GZ. 2015. Mammalian ER mannosidase I resides in quality control vesicles, where it encounters its glycoprotein substrates. Mol Biol Cell. 26:172–184.
  • Blobel G. 1980. Intracellular protein topogenesis. Proc Natl Acad Sci USA. 77:1496–1500.
  • Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH. 2003. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol. 5:1051–1061.
  • Brehme M, Voisine C, Rolland T, Wachi S, Soper JH, Zhu Y, Orton K, Villella A, Garza D, Vidal M. 2014. A chaperome subnetwork safeguards proteostasis in aging and neurodegenerative disease. Cell Rep. 9:1135–1150.
  • Budnik A, Stephens DJ. 2009. ER exit sites-localization and control of COPII vesicle formation. FEBS Lett. 583:3796–3803.
  • Bunney TD, Cole AR, Broncel M, Esposito D, Tate EW, Katan M. 2014. Crystal structure of the human, FIC-domain containing protein HYPE and implications for its functions. Structure. 22:1831–1843.
  • Bürkle A. 2001. Posttranslational Modification. In: Brenner S, Miller JH, editors. Encyclopedia of genetics [Internet]. New York, USA: Academic Press; p. 1533.
  • Caplan AJ. 2003. What is a co-chaperone? Cell Stress Chaperones. 8:105–107.
  • Caro LG. 1964. Protein synthesis, storage, and discharge in the pancreatic exocrine cell: an autoradiographic study. J Cell Biol. 20:473–495.
  • Chartron JW, Gonzalez GM, Clemons WM. 2011. A structural model of the Sgt2 protein and its interactions with chaperones and the Get4/Get5 complex. J Biol Chem. 286:34325–34334.
  • Chen W, Helenius J, Braakman I, Helenius A. 1995. Cotranslational folding and calnexin binding during glycoprotein synthesis. PNAS. 92:6229–6233.
  • Christianson JC, Shaler TA, Tyler RE, Kopito RR. 2008. OS-9 and GRP94 deliver mutant alpha1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat Cell Biol. 10:272–282.
  • D'Andrea LD, Regan L. 2003. TPR proteins: the versatile helix. Trends Biochem Sci. 28:655–662.
  • Daniels R, Kurowski B, Johnson AE, Hebert DN. 2003. N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell. 11:79–90.
  • Darby JF, Krysztofinska EM, Simpson PJ, Simon AC, Leznicki P, Sriskandarajah N, Bishop DS, Hale LR, Alfano C, Conte MR, et al. 2014. Solution structure of the SGTA dimerisation domain and investigation of its interactions with the ubiquitin-like domains of BAG6 and UBL4A. PLoS One. 9:e113281.
  • Dudek J, Benedix J, Cappel S, Greiner M, Jalal C, Müller L, Zimmermann R. 2009. Functions and pathologies of BiP and its interaction partners. Cell Mol Life Sci. 66:1556–1569.
  • Dutta S, Tan YJ. 2008. Structural and functional characterization of human SGT and its interaction with Vpu of the human immunodeficiency virus type 1. Biochemistry. 47:10123–10131.
  • Ecker M, Mrsa V, Hagen I, Deutzmann R, Strahl S, Tanner W. 2003. O-mannosylation precedes and potentially controls the N-glycosylation of a yeast cell wall glycoprotein. EMBO Rep. 4:628–632.
  • Ellgaard L, Helenius A. 2003. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol. 4:181–191.
  • Faber PW, Barnes GT, Srinidhi J, Chen J, Gusella JF, MacDonald ME. 1998. Huntingtin interacts with a family of WW domain proteins. Hum Mol Genet. 7:1463–1474.
  • Fan ACY, Bhangoo MK, Young JC. 2006. Hsp90 functions in the targeting and outer membrane translocation steps of Tom70-mediated mitochondrial import. J Biol Chem. 281:33313–33324.
  • Farhan SMK, Nixon KCJ, Everest M, Edwards TN, Long S, Segal D, Knip MJ, Arts HH, Chakrabarti R, Wang J, et al. 2017. Identification of a novel synaptic protein, TMTC3, involved in periventricular nodular heterotopia with intellectual disability and epilepsy. Hum Mol Genet. 26:4278–4289.
  • Garcia-Pino A, Zenkin N, Loris R. 2014. The many faces of Fic: structural and functional aspects of Fic enzymes. Trends Biochem Sci. 39:121–129.
  • Gardner RG, Swarbrick GM, Bays NW, Cronin SR, Wilhovsky S, Seelig L, Kim C, Hampton RY. 2000. Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p. J Cell Biol. 151:69–82.
  • 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.
  • Gilchrist A, Au CE, Hiding J, Bell AW, Fernandez-Rodriguez J, Lesimple S, Nagaya H, Roy L, Gosline SJC, Hallett M, et al. 2006. Quantitative proteomics analysis of the secretory pathway. Cell. 127:1265–1281.
  • Giorgi C, De Stefani D, Bononi A, Rizzuto R, Pinton P. 2009. Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int J Biochem Cell Biol. 41:1817–1827.
  • Glaser T, Arnaud Sampaio VF, Lameu C, Ulrich H. 2018. Calcium signalling: a common target in neurological disorders and neurogenesis. Semin Cell Develop Biol. https://doi.org/10.1016/j.semcdb.2018.12.002.
  • Good MC, Zalatan JG, Lim WA. 2011. Scaffold proteins: hubs for controlling the flow of cellular information. Science. 332:680–686.
  • Grove TZ, Cortajarena AL, Regan L. 2008. Ligand binding by repeat proteins: natural and designed. Curr Opin Struct Biol. 18:507–515.
  • Hales CN, Luzio JP, Chandler JA, Herman L. 1974. Localization of calcium in the smooth endoplasmic reticulum of rat isolated fat cells. J Cell Sci. 15:1–15.
  • Harada Y, Li H, Li H, Lennarz WJ. 2009. Oligosaccharyltransferase directly binds to ribosome at a location near the translocon-binding site. PNAS. 106:6945–6949.
  • Harkness TA, Nargang FE, Klei I, van der Neupert W, Lill R. 1994. A crucial role of the mitochondrial protein import receptor MOM19 for the biogenesis of mitochondria. J Cell Biol. 124:637–648.
  • Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature. 475:324–332.
  • Hayashi T, Rizzuto R, Hajnoczky G, Su T-P. 2009. MAM: more than just a housekeeper. Trends Cell Biol. 19:81–88.
  • Hebert DN, Lamriben L, Powers ET, Kelly JW. 2014. The intrinsic and extrinsic effects of N-linked glycans on glycoproteostasis. Nat Chem Biol. 10:902–910.
  • Hideaki I, Yohtalou T. 1991. The stress (heat shock) proteins. Int J Biochem. 23:1185–1191.
  • Itskanov S, Park E. 2019. Structure of the posttranslational Sec protein-translocation channel complex from yeast. Science. 363:84–87.
  • Iyer SPN, Hart GW. 2003. Roles of the tetratricopeptide repeat domain in O-GlcNAc transferase targeting and protein substrate specificity. J Biol Chem. 278:24608–24616.
  • Javadi Y, Main E. 2009. Exploring the folding energy landscape of a series of designed consensus tetratricopeptide repeat proteins. PNAS. 106:17383–17388.
  • Jensen D, Schekman R. 2011. COPII-mediated vesicle formation at a glance. J Cell Sci. 124:1–4.
  • Jeong H, Sim HJ, Song EK, Lee H, Ha SC, Jun Y, Park TJ, Lee C. 2016. Crystal structure of SEL1L: Insight into the roles of SLR motifs in ERAD pathway. Sci Rep. 6:20261.
  • Jerber J, Zaki MS, Al-Aama JY, Rosti RO, Ben-Omran T, Dikoglu E, Silhavy JL, Caglar C, Musaev D, Albrecht B, et al. 2016. Biallelic mutations in TMTC3, encoding a transmembrane and TPR-containing protein, lead to cobblestone lissencephaly. Am J Hum Genet. 99:1181–1189.
  • Jiménez B, Ugwu F, Zhao R, Ortí L, Makhnevych T, Pineda-Lucena A, Houry WA. 2012. Structure of minimal tetratricopeptide repeat domain protein Tah1 reveals mechanism of its interaction with Pih1 and Hsp90. J Biol Chem. 287:5698–5709.
  • Jínek M, Rehwinkel J, Lazarus BD, Izaurralde E, Hanover JA, Conti E. 2004. The superhelical TPR-repeat domain of O-linked GlcNAc transferase exhibits structural similarities to importin alpha. Nat Struct Mol Biol. 11:1001–1007.
  • Johnson AE, van Waes MA. 1999. The translocon: a dynamic gateway at the ER membrane. Annu Rev Cell Dev Biol. 15:799–842.
  • Kajander T, Cortajarena AL, Mochrie S, Regan L. 2007. Structure and stability of designed TPR protein superhelices: unusual crystal packing and implications for natural TPR proteins. Acta Crystallogr D Biol Crystallogr. 63:800–811.
  • Kalantari F, Bergeron JJM, Nilsson T. 2010. Biogenesis of lipid droplets – how cells get fatter. Mol Membr Biol. 27:462–468.
  • Kaneko M, Nomura Y. 2003. ER signaling in unfolded protein response. Life Sci. 74:199–205.
  • Klopfenstein DR, Klumperman J, Lustig A, Kammerer RA, Oorschot V, Hauri H-P. 2001. Subdomain-specific localization of Climp-63 (P63) in the endoplasmic reticulum is mediated by its luminal alpha-helical segment. J Cell Biol. 153:1287–1300.
  • Kopito RR, Sitia R. 2000. Aggresomes and Russell bodies. Symptoms of cellular indigestion? EMBO Rep. 1:225–231.
  • Lamriben L, Graham JB, Adams BM, Hebert DN. 2016. N-Glycan-based ER molecular chaperone and protein quality control system: the calnexin binding cycle. Traffic. 17:308–326.
  • Larsen ISB, Narimatsu Y, Joshi HJ, Siukstaite L, Harrison OJ, Brasch J, Goodman KM, Hansen L, Shapiro L, Honig B, et al. 2017. Discovery of an O-mannosylation pathway selectively serving cadherins and protocadherins. Proc Natl Acad Sci USA. 114:11163–11168.
  • Lazarus MB, Nam Y, Jiang J, Sliz P, Walker S. 2011. Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature. 469:564–567.
  • Letunic I, Bork P. 2018. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 46:D493–D496.
  • Leznicki P, Korac-Prlic J, Kliza K, Husnjak K, Nyathi Y, Dikic I, High S. 2015. Binding of SGTA to Rpn13 selectively modulates protein quality control. J Cell Sci. 128:3187–3196.
  • Li J, Akil O, Rouse SL, McLaughlin CW, Matthews IR, Lustig LR, Chan DK, Sherr EH. 2018. Deletion of Tmtc4 activates the unfolded protein response and causes postnatal hearing loss. J Clin Invest. 128:5150–5162.
  • Li S, Iakoucheva LM, Mooney SD, Radivojac P. 2010. Loss of post-translational modification sites in disease. Pac Symp Biocomput337–347.
  • Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M. 1991. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. PNAS. 88:2874–2878.
  • Lubas WA, Frank DW, Krause M, Hanover JA. 1997. O-Linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats. J Biol Chem. 272:9316–9324.
  • Lunz V, Romanin C, Frischauf I. 2019. STIM1 activation of Orai1. Cell Calcium. 77:29–38.
  • Lynes EM, Simmen T. 2011. Urban planning of the endoplasmic reticulum (ER): how diverse mechanisms segregate the many functions of the ER. Biochim Biophys Acta. 1813:1893–1905.
  • Madsen MB, Kogelman LJA, Kadarmideen HN, Rasmussen HB. 2018. Systems genetics analysis of pharmacogenomics variation during antidepressant treatment. Pharmacogenomics J. 18:144–152.
  • Magliery TJ, Regan L. 2005. Sequence variation in ligand binding sites in proteins. BMC Bioinformatics. 6:240.
  • Martínez-Lumbreras S, Krysztofinska EM, Thapaliya A, Spilotros A, Matak-Vinkovic D, Salvadori E, Roboti P, Nyathi Y, Muench JH, Roessler MM, et al. 2018. Structural complexity of the co-chaperone SGTA: a conserved C-terminal region is implicated in dimerization and substrate quality control. BMC Biol. 16:76.
  • Mast FD, Fagarasanu A, Knoblach B, Rachubinski RA. 2010. Peroxisome biogenesis: something old, something new, something borrowed. Physiology (Bethesda). 25:347–356.
  • Mazzarello P, Calligaro A, Vannini V, Muscatello U. 2003. The sarcoplasmic reticulum: its discovery and rediscovery. Nat Rev Mol Cell Biol. 4:69–74.
  • McGraw CF, Somlyo AV, Blaustein MP. 1980. Localization of calcium in presynaptic nerve terminals. An ultrastructural and electron microprobe analysis. J Cell Biol. 85:228–241.
  • Minami R, Hayakawa A, Kagawa H, Yanagi Y, Yokosawa H, Kawahara H. 2010. BAG-6 is essential for selective elimination of defective proteasomal substrates. J Cell Biol. 190:637–650.
  • Mittl PRE, Schneider-Brachert W. 2007. Sel1-like repeat proteins in signal transduction. Cellular Signalling.19:20–31.
  • Molinari M, Helenius A. 1999. Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature. 402:90–93.
  • Molinari M, Helenius A. 2000. Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science. 288:331–333.
  • Muto T, Obita T, Abe Y, Shodai T, Endo T, Kohda D. 2001. NMR identification of the Tom20 binding segment in mitochondrial presequences11Edited by M. F. Sumers. J Mol Biol. 306:137–143.
  • O’Connor SE, Imperiali B. 1996. Modulation of protein structure and function by asparagine-linked glycosylation. Chem Biol. 3:803–812.
  • Odunuga OO, Longshaw VM, Blatch GL. 2004. Hop: more than an Hsp70/Hsp90 adaptor protein. BioEssays. 26:1058–1068.
  • Palade GE, Porter KR. 1954. Studies on the endoplasmic reticulum. I. Its identification in cells in situ. J Exp Med. 100:641–656.
  • Palade GE, Siekevitz P. 1956. Liver microsomes: an integrated morphological and biochemical study. J Cell Biol. 2:171–200.
  • Park E, Rapoport TA. 2012. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys. 41:21–40.
  • Petrova K, Oyadomari S, Hendershot LM, Ron D. 2008. Regulated association of misfolded endoplasmic reticulum lumenal proteins with P58/DNAJc3. Embo J. 27:2862–2872.
  • Pichler H, Gaigg B, Hrastnik C, Achleitner G, Kohlwein SD, Zellnig G, Perktold A, Daum G. 2001. A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur J Biochem. 268:2351–2361.
  • Pobre KFR, Poet GJ, Hendershot LM. 2018. The endoplasmic reticulum (ER) chaperone BiP is a master regulator of ER functions: Getting by with a little help from ERdj friends. J Biol Chem. 2098–2108.
  • Preissler S, Rato C, Chen R, Antrobus R, Ding S, Fearnley IM, Ron D. 2015. AMPylation matches BiP activity to client protein load in the endoplasmic reticulum.Gilmore R, editor. eLife. 4:e12621.
  • Preissler S, Rato C, Perera LA, Saudek V, Ron D. 2017. FICD acts bifunctionally to AMPylate and de-AMPylate the endoplasmic reticulum chaperone BiP. Nat Struct Mol Biol. 24:23–29.
  • Preissler S, Rohland L, Yan Y, Chen R, Read RJ, Ron D. 2016. AMPylation targets the rate-limiting step of BiP’s ATPase cycle for its functional inactivation. eLife. 6:e29428.
  • Price JL, Culyba EK, Chen W, Murray AN, Hanson SR, Wong C-H, Powers ET, Kelly JW. 2012. N-glycosylation of enhanced aromatic sequons to increase glycoprotein stability. Biopolymers. 98:195–211.
  • Racapé M, Huyen J-P, Danger R, Giral M, Bleicher F, Foucher Y, Pallier A, Pilet P, Tafelmeyer P, Ashton-Chess J, et al. 2011. The involvement of SMILE/TMTC3 in endoplasmic reticulum stress response. PLoS One. 6:e19321.
  • Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 280:1763–1766.
  • Runge CL, Indap A, Zhou Y, Kent JW, King E, Erbe CB, Cole R, Littrell J, Merath K, James R, et al. 2016. Association of TMTC2 with human nonsyndromic sensorineural hearing loss. JAMA Otolaryngol Head Neck Surg. 142:866–872.
  • Rutkowski DT, Kang S-W, Goodman AG, Garrison JL, Taunton J, Katze MG, Kaufman RJ, Hegde RS. 2007. The role of p58IPK in protecting the stressed endoplasmic reticulum. Mol Biol Cell. 18:3681–3691.
  • Sanyal A, Chen AJ, Nakayasu ES, Lazar CS, Zbornik EA, Worby CA, Koller A, Mattoo S. 2015. A novel link between Fic (Filamentation induced by cAMP)-mediated adenylylation/AMPylation and the unfolded protein response. J Biol Chem. 290:8482–8499.
  • Satoh T, Ross CA, Villa A, Supattapone S, Pozzan T, Snyder SH, Meldolesi J. 1990. The inositol 1,4,5,-trisphosphate receptor in cerebellar Purkinje cells: quantitative immunogold labeling reveals concentration in an ER subcompartment. J Cell Biol. 111:615–624.
  • Sawyer N, Chen J, Regan L. 2013. All repeats are not equal: a module-based approach to guide repeat protein design. J Mol Biol. 425:1826–1838.
  • Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I. 2000. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell. 101:199–210.
  • Schjoldager KB, Clausen H. 2012. Site-specific protein O-glycosylation modulates proprotein processing — Deciphering specific functions of the large polypeptide GalNAc-transferase gene family. Biochimica et Biophysica Acta (BBA) - General Subjects. 1820:2079–2094.
  • Schnell DJ, Hebert DN. 2003. Protein translocons: multifunctional mediators of protein translocation across membranes. Cell. 112:491–505.
  • Shafi R, Iyer SP, Ellies LG, O-Donnel N, Marek KW, Chui D, Hart GW, Marth JD. 2000. The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc Natl Acad Sci USA. 97:5735–5739.
  • Shao S, Rodrigo-Brenni MC, Kivlen MH, Hegde RS. 2017. Mechanistic basis for a molecular triage reaction. Science. 355:298–302.
  • Shibata Y, Shemesh T, Prinz WA, Palazzo AF, Kozlov MM, Rapoport TA. 2010. Mechanisms determining the morphology of the peripheral ER. Cell. 143:774–788.
  • Shibatani T, David LL, McCormack AL, Frueh K, Skach WR. 2005. Proteomic analysis of mammalian oligosaccharyltransferase reveals multiple subcomplexes that contain Sec61, TRAP, and two potential new subunits. Biochemistry. 44:5982–5992.
  • Simmen T, Lynes EM, Gesson K, Thomas G. 2010. Oxidative protein folding in the endoplasmic reticulum: Tight links to the mitochondria-associated membrane (MAM). Biochimica et Biophysica Acta (BBA) - Biomembranes. 1798:1465–1473.
  • Simon AC, Simpson PJ, Goldstone RM, Krysztofinska EM, Murray JW, High S, Isaacson RL. 2013. Structure of the Sgt2/Get5 complex provides insights into GET-mediated targeting of tail-anchored membrane proteins. Proc Natl Acad Sci USA. 110:1327–1332.
  • Solá RJ, Griebenow K. 2009. Effects of glycosylation on the stability of protein pharmaceuticals. J Pharm Sci. 98:1223–1245.
  • Stein O, Stein Y. 1967. Lipid synthesis, intracellular transport, storage, and secretion. i. electron microscopic radioautographic study of liver after injection of tritiated palmitate or glycerol in fasted and ethanol-treated rats. J Cell Biol. 33:319–339.
  • Sun S, Shi G, Han X, Francisco AB, Ji Y, Mendonça N, Liu X, Locasale JW, Simpson KW, Duhamel GE, et al. 2014. Sel1L is indispensable for mammalian endoplasmic reticulum-associated degradation, endoplasmic reticulum homeostasis, and survival. Proc Natl Acad Sci USA. 111:E582–E591.
  • Sunryd JC, Cheon B, Graham JB, Giorda KM, Fissore RA, Hebert DN. 2014. TMTC1 and TMTC2 are novel endoplasmic reticulum TPR-containing adapter proteins involved in calcium homeostasis. J Biol Chem. 289:16085–16099.
  • Svärd M, Biterova EI, Bourhis J-M, Guy JE. 2011. The crystal structure of the human co-chaperone P58(IPK). PLoS One. 6:e22337.
  • Takei K, Stukenbrok H, Metcalf A, Mignery GA, Sudhof TC, Volpe P, Camilli PD. 1992. Ca2+ stores in Purkinje neurons: endoplasmic reticulum subcompartments demonstrated by the heterogeneous distribution of the InsP3 receptor, Ca(2+)-ATPase, and calsequestrin. J Neurosci. 12:489–505.
  • Tannous A, Patel N, Tamura T, Hebert DN. 2015. Reglucosylation by UDP-glucose:glycoprotein glucosyltransferase 1 delays glycoprotein secretion but not degradation.Brodsky JL, editor. Mol Biol Cell. 26:390–405.
  • Tao J, Petrova K, Ron D, Sha B. 2010. Crystal structure of P58(IPK) TPR fragment reveals the mechanism for its molecular chaperone activity in UPR. J Mol Biol. 397:1307–1315.
  • Thapaliya A, Nyathi Y, Martínez-Lumbreras S, Krysztofinska EM, Evans NJ, Terry IL, High S, Isaacson RL. 2016. SGTA interacts with the proteasomal ubiquitin receptor Rpn13 via a carboxylate clamp mechanism. Sci Rep. 6:36622.
  • 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. 292:8007–8018.
  • Truttmann MC, Ploegh HL. 2017. rAMPing up stress signaling: protein AMPylation in metazoans. Trends Cell Biol. 27:608–620.
  • Veratti E. 1961. Investigations on the fine structure of striated muscle fiber. J Cell Biol. 10:1–59.
  • Worby CA, Mattoo S, Kruger RP, Corbeil LB, Koller A, Mendez JC, Zekarias B, Lazar C, Dixon JE. 2009. The Fic domain: regulation of cell signaling by adenylylation. Mol Cell. 34:93–103.
  • Wu X, Cabanos C, Rapoport TA. 2019. Structure of the post-translational protein translocation machinery of the ER membrane. Nature. 566:136–139.
  • Wu Y, Sha B. 2006. Crystal structure of yeast mitochondrial outer membrane translocon member Tom70p. Nat Struct Mol Biol. 13:589–593.
  • Xu C, Ng D. 2015. O-mannosylation: The other glycan player of ER quality control. Semin Cell Dev Biol. 41:129–134.
  • Yan W, Frank CL, Korth MJ, Sopher BL, Novoa I, Ron D, Katze MG. 2002. Control of PERK eIF2α kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. PNAS. 99:15920–15925.
  • Yang X, Zhang F, Kudlow JE. 2002. Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: coupling protein O-GlcNAcylation to transcriptional repression. Cell. 110:69–80.
  • Yi F, Doudevski I, Regan L. 2010. HOP is a monomer: Investigation of the oligomeric state of the co-chaperone HOP. Protein Sci. 19:19–25.
  • Young JC, Hoogenraad NJ, Hartl FU. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell. 112:41–50.
  • Zeytuni N, Zarivach R. 2012. Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure. 20:397–405.
  • Zhang H, Hu J. 2016. Shaping the endoplasmic reticulum into a social network. Trends Cell Biol. 26:934–943.

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