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Review

Degradation-mediated protein quality control at the inner nuclear membrane

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Pages 41-49 | Received 02 Dec 2015, Accepted 04 Jan 2016, Published online: 31 Mar 2016

References

  • Wolff S, Weissman JS, Dillin A. Differential scales of protein quality control. Cell 2014; 157:52-64; PMID:24679526; http://dx.doi.org/10.1016/j.cell.2014.03.007
  • Ciechanover A. Intracellular protein degradation from a vague idea through the lysosome and the ubiquitin-proteasome system and on to human diseases and drug targeting: Nobel Lecture, December 8, 2004. Ann N Y Acad Sci 2007; 1116:1-28; PMID:18083918
  • Kriegenburg F, Ellgaard L, Hartmann-Petersen R. Molecular chaperones in targeting misfolded proteins for ubiquitin-dependent degradation. FEBS J 2012; 279:532-42; PMID:22177318; http://dx.doi.org/10.1111/j.1742-4658.2011.08456.x
  • Knaevelsrud H, Simonsen A. Fighting disease by selective autophagy of aggregate-prone proteins. FEBS Lett 2010; 584:2635-45; PMID:20412801; http://dx.doi.org/10.1016/j.febslet.2010.04.041
  • Klionsky DJ. The molecular machinery of autophagy: unanswered questions. J Cell Sci 2005; 118:7-18; PMID:15615779; http://dx.doi.org/10.1242/jcs.01620
  • Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol 2001; 2:211-6; PMID:11265251; http://dx.doi.org/10.1038/35056522
  • Mijaljica D, Prescott M, Devenish RJ. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy 2011; 7:673-82; PMID:21646866; http://dx.doi.org/10.4161/auto.7.7.14733
  • Buchberger A, Bukau B, Sommer T. Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol Cell 2010; 40:238-52; PMID:20965419; http://dx.doi.org/10.1016/j.molcel.2010.10.001
  • Nielsen SV, Poulsen EG, Rebula CA, Hartmann-Petersen R. Protein quality control in the nucleus. Biomolecules 2014; 4:646-61; PMID:25010148; http://dx.doi.org/10.3390/biom4030646
  • Chowdhury M, Enenkel C. Intracellular Dynamics of the Ubiquitin-Proteasome-System. F1000Research 2015; 4:367; PMID:26339477
  • Gardner RG, Nelson ZW, Gottschling DE. Degradation-mediated protein quality control in the nucleus. Cell 2005; 120:803-15; PMID:15797381; http://dx.doi.org/10.1016/j.cell.2005.01.016
  • Hegde RS, Ploegh HL. Quality and quantity control at the endoplasmic reticulum. Curr Opin Cell Biol 2010; 22:1-10; PMID:20102790; http://dx.doi.org/10.1016/j.ceb.2010.05.005
  • Vembar SS, Brodsky JL. One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 2008; 9:944-57; PMID:19002207; http://dx.doi.org/10.1038/nrm2546
  • Deng M, Hochstrasser M. Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 2006; 443:827-31; PMID:17051211; http://dx.doi.org/10.1038/nature05170
  • Boban M, Pantazopoulou M, Schick A, Ljungdahl PO, Foisner R. A nuclear ubiquitin-proteasome pathway targets the inner nuclear membrane protein Asi2 for degradation. J Cell Sci 2014; 127:3603-13; PMID:24928896; http://dx.doi.org/10.1242/jcs.153163
  • Furth N, Gertman O, Shiber A, Alfassy OS, Cohen I, Rosenberg MM, Doron NK, Friedler A, Ravid T. Exposure of bipartite hydrophobic signal triggers nuclear quality control of Ndc10 at the endoplasmic reticulum/nuclear envelope. Mol Biol Cell 2011; 22:4726-39; PMID:21998200; http://dx.doi.org/10.1091/mbc.E11-05-0463
  • Foresti O, Rodriguez-Vaello V, Funaya C, Carvalho P. Quality control of inner nuclear membrane proteins by the Asi complex. Science 2014; 346:751-5; PMID:25236469; http://dx.doi.org/10.1126/science.1255638
  • Khmelinskii A, Blaszczak E, Pantazopoulou M, Fischer B, Omnus DJ, Le Dez G, Brossard A, Gunnarsson A, Barry JD, Meurer M, et al. Protein quality control at the inner nuclear membrane. Nature 2014; 516:410-3; PMID:25519137; http://dx.doi.org/10.1038/nature14096
  • Mijaljica D, Devenish RJ. Nucleophagy at a glance. J Cell Sci 2013; 126:4325-30; PMID:24013549; http://dx.doi.org/10.1242/jcs.133090
  • Hetzer MW. The nuclear envelope. Cold Spring Harb Perspect Biol 2010; 2:a000539; PMID:20300205; http://dx.doi.org/10.1101/cshperspect.a000539
  • Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD. Nuclear lamins. Cold Spring Harb Perspect Biol 2010; 2:a000547; PMID:20826548; http://dx.doi.org/10.1101/cshperspect.a000547
  • Gruenbaum Y, Foisner R. Lamins: nuclear intermediate filament proteins with fundamental functions in nuclear mechanics and genome regulation. Annu Rev Biochem 2015; 84:131-64; PMID:25747401; http://dx.doi.org/10.1146/annurev-biochem-060614-034115
  • Schirmer EC, Foisner R. Proteins that associate with lamins: many faces, many functions. Exp Cell Res 2007; 313:2167-79; PMID:17451680; http://dx.doi.org/10.1016/j.yexcr.2007.03.012
  • Wilson KL, Berk JM. The nuclear envelope at a glance. J Cell Sci 2010; 123:1973-8; PMID:20519579; http://dx.doi.org/10.1242/jcs.019042
  • Amsterdam A, Pitzer F, Baumeister W. Changes in intracellular localization of proteasomes in immortalized ovarian granulosa cells during mitosis associated with a role in cell cycle control. Proceedings of the National Academy of Sciences of the United States of America 1993; 90:99-103; PMID:8380501; http://dx.doi.org/10.1073/pnas.90.1.99
  • Enenkel C, Lehmann A, Kloetzel PM. Subcellular distribution of proteasomes implicates a major location of protein degradation in the nuclear envelope-ER network in yeast. EMBO J 1998; 17:6144-54; PMID:9799224; http://dx.doi.org/10.1093/emboj/17.21.6144
  • Hugle B, Kleinschmidt JA, Franke WW. The 22 S cylinder particles of Xenopus laevis. II. Immunological characterization and localization of their proteins in tissues and cultured cells. Eur J Cell Biol 1983; 32:157-63; PMID:6667692
  • McDonald HB, Byers B. A proteasome cap subunit required for spindle pole body duplication in yeast. J Cell Biol 1997; 137:539-53; PMID:9151663; http://dx.doi.org/10.1083/jcb.137.3.539
  • Peters JM, Franke WW, Kleinschmidt JA. Distinct 19 S and 20 S subcomplexes of the 26 S proteasome and their distribution in the nucleus and the cytoplasm. J Biol Chem 1994; 269:7709-18; PMID:8125997
  • Russell SJ, Steger KA, Johnston SA. Subcellular localization, stoichiometry, and protein levels of 26 S proteasome subunits in yeast. J Biol Chem 1999; 274:21943-52; PMID:10419517; http://dx.doi.org/10.1074/jbc.274.31.21943
  • Wojcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol 2003; 35:579-89; PMID:12672451; http://dx.doi.org/10.1016/S1357-2725(02)00380-1
  • Fredrickson EK, Rosenbaum JC, Locke MN, Milac TI, Gardner RG. Exposed hydrophobicity is a key determinant of nuclear quality control degradation. Mol Biol Cell 2011; 22:2384-95; PMID:21551067; http://dx.doi.org/10.1091/mbc.E11-03-0256
  • Rosenbaum JC, Fredrickson EK, Oeser ML, Garrett-Engele CM, Locke MN, Richardson LA, Nelson ZW, Hetrick ED, Milac TI, Gottschling DE, et al. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol Cell 2011; 41:93-106; PMID:21211726; http://dx.doi.org/10.1016/j.molcel.2010.12.004
  • Roberts P, Moshitch-Moshkovitz S, Kvam E, O'Toole E, Winey M, Goldfarb DS. Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol Biol Cell 2003; 14:129-41; PMID:12529432; http://dx.doi.org/10.1091/mbc.E02-08-0483
  • Mijaljica D, Prescott M, Devenish RJ. A late form of nucleophagy in Saccharomyces cerevisiae. PLoS One 2012; 7:e40013; PMID:22768199; http://dx.doi.org/10.1371/journal.pone.0040013
  • Mochida K, Oikawa Y, Kimura Y, Kirisako H, Hirano H, Ohsumi Y, Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 2015; 522:359-62; PMID:26040717; http://dx.doi.org/10.1038/nature14506
  • Cao K, Graziotto JJ, Blair CD, Mazzulli JR, Erdos MR, Krainc D, Collins FS. Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Sci Transl Med 2011; 3:89ra58
  • Cenni V, Capanni C, Columbaro M, Ortolani M, D'Apice MR, Novelli G, Fini M, Marmiroli S, Scarano E, Maraldi NM, et al. Autophagic degradation of farnesylated prelamin A as a therapeutic approach to lamin-linked progeria. Eur J Histochem 2011; 55:e36; PMID:22297442; http://dx.doi.org/10.4081/ejh.2011.e36
  • Dou Z, Xu C, Donahue G, Shimi T, Pan JA, Zhu J, Ivanov A, Capell BC, Drake AM, Shah PP, et al. Autophagy mediates degradation of nuclear lamina. Nature 2015; 527(7576):105-9; PMID: 26524528
  • Miller SB, Ho CT, Winkler J, Khokhrina M, Neuner A, Mohamed MY, Guilbride DL, Richter K, Lisby M, Schiebel E, et al. Compartment-specific aggregases direct distinct nuclear and cytoplasmic aggregate deposition. EMBO J 2015; 34:778-97; PMID:25672362; http://dx.doi.org/10.15252/embj.201489524
  • Forsberg H, Hammar M, Andréasson C, Moliner A, Ljungdahl PO. Suppressors of ssy1 and ptr3 null mutations define novel amino acid sensor-independent genes in Saccharomyces cerevisiae. Genetics 2001; 158:973-88; PMID:11454748
  • Ljungdahl PO, Daignan-Fornier B. Regulation of amino acid, nucleotide, and phosphate metabolism in Saccharomyces cerevisiae. Genetics 2012; 190:885-929; PMID:22419079; http://dx.doi.org/10.1534/genetics.111.133306
  • Zargari A, Boban M, Heessen S, Andréasson C, Thyberg J, Ljungdahl PO. Inner nuclear membrane proteins Asi1, Asi2, and Asi3 function in concert to maintain the latent properties of transcription factors Stp1 and Stp2. J Biol Chem 2007; 282:594-605; PMID:17085444; http://dx.doi.org/10.1074/jbc.M609201200
  • Boban M, Ljungdahl PO. Dal81 enhances Stp1- and Stp2-dependent transcription necessitating negative modulation by inner nuclear membrane protein Asi1 in Saccharomyces cerevisiae. Genetics 2007; 176:2087-97; PMID:17603098; http://dx.doi.org/10.1534/genetics.107.075077
  • Boban M, Zargari A, Andréasson C, Heessen S, Thyberg J, Ljungdahl PO. Asi1 is an inner nuclear membrane protein that restricts promoter access of two latent transcription factors. J Cell Biol 2006; 173:695-707; PMID:16735580; http://dx.doi.org/10.1083/jcb.200601011
  • Omnus DJ, Ljungdahl PO. Latency of transcription factor Stp1 depends on a modular regulatory motif that functions as cytoplasmic retention determinant and nuclear degron. Mol Biol Cell 2014; 25:3823-33; PMID:25253722; http://dx.doi.org/10.1091/mbc.E14-06-1140
  • Boban M, Ljungdahl PO, Foisner R. Atypical ubiquitylation in yeast targets lysine-less Asi2 for proteasomal degradation. J Biol Chem 2015; 290:2489-95; PMID:25492870; http://dx.doi.org/10.1074/jbc.M114.600593
  • Cadwell K, Coscoy L. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 2005; 309:127-30; PMID:15994556; http://dx.doi.org/10.1126/science.1110340
  • Carvalho AF, Pinto MP, Grou CP, Alencastre IS, Fransen M, Sa-Miranda C, Azevedo JE. Ubiquitination of mammalian Pex5p, the peroxisomal import receptor. J Biol Chem 2007; 282:31267-72; PMID:17726030; http://dx.doi.org/10.1074/jbc.M706325200
  • Domingues C, Ryoo HD. Drosophila BRUCE inhibits apoptosis through non-lysine ubiquitination of the IAP-antagonist REAPER. Cell Death Differ 2012; 19:470-7; PMID:21886178; http://dx.doi.org/10.1038/cdd.2011.116
  • Ishikura S, Weissman AM, Bonifacino JS. Serine residues in the cytosolic tail of the T-cell antigen receptor alpha-chain mediate ubiquitination and endoplasmic reticulum-associated degradation of the unassembled protein. J Biol Chem 2010; 285:23916-24; PMID:20519503; http://dx.doi.org/10.1074/jbc.M110.127936
  • Kravtsova-Ivantsiv Y, Ciechanover A. Non-canonical ubiquitin-based signals for proteasomal degradation. J Cell Sci 2012; 125:539-48; PMID:22389393; http://dx.doi.org/10.1242/jcs.093567
  • Shimizu Y, Okuda-Shimizu Y, Hendershot LM. Ubiquitylation of an ERAD substrate occurs on multiple types of amino acids. Mol Cell 2010; 40:917-26; PMID:21172657; http://dx.doi.org/10.1016/j.molcel.2010.11.033
  • Wang X, Herr RA, Chua WJ, Lybarger L, Wiertz EJ, Hansen TH. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J Cell Biol 2007; 177:613-24; PMID:17502423; http://dx.doi.org/10.1083/jcb.200611063
  • Williams C, van den Berg M, Sprenger RR, Distel B. A conserved cysteine is essential for Pex4p-dependent ubiquitination of the peroxisomal import receptor Pex5p. J Biol Chem 2007; 282:22534-43; PMID:17550898; http://dx.doi.org/10.1074/jbc.M702038200
  • Johnson PR, Swanson R, Rakhilina L, Hochstrasser M. Degradation signal masking by heterodimerization of MATalpha2 and MATa1 blocks their mutual destruction by the ubiquitin-proteasome pathway. Cell 1998; 94:217-27; PMID:9695950; http://dx.doi.org/10.1016/S0092-8674(00)81421-X
  • Ravid T, Kreft SG, Hochstrasser M. Membrane and soluble substrates of the Doa10 ubiquitin ligase are degraded by distinct pathways. EMBO J 2006; 25:533-43; PMID:16437165; http://dx.doi.org/10.1038/sj.emboj.7600946
  • Park YE, Hayashi YK, Bonne G, Arimura T, Noguchi S, Nonaka I, Nishino I. Autophagic degradation of nuclear components in mammalian cells. Autophagy 2009; 5:795-804; PMID:19550147; http://dx.doi.org/10.4161/auto.8901
  • Candelario J, Borrego S, Reddy S, Comai L. Accumulation of distinct prelamin A variants in human diploid fibroblasts differentially affects cell homeostasis. Exp Cell Res 2011; 317:319-29; PMID:20974128; http://dx.doi.org/10.1016/j.yexcr.2010.10.014
  • Capanni C, Del Coco R, Squarzoni S, Columbaro M, Mattioli E, Camozzi D, Rocchi A, Scotlandi K, Maraldi N, Foisner R, et al. Prelamin A is involved in early steps of muscle differentiation. Exp Cell Res 2008; 314:3628-37; PMID:18951892; http://dx.doi.org/10.1016/j.yexcr.2008.09.026
  • Dechat T, Shimi T, Adam SA, Rusinol AE, Andres DA, Spielmann HP, Sinensky MS, Goldman RD. Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proceedings of the National Academy of Sciences of the United States of America 2007; 104:4955-60; PMID:17360326; http://dx.doi.org/10.1073/pnas.0700854104
  • Prokocimer M, Barkan R, Gruenbaum Y. Hutchinson-Gilford progeria syndrome through the lens of transcription. Aging Cell 2013; 12:533-43; PMID:23496208; http://dx.doi.org/10.1111/acel.12070
  • Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 1998; 273:3963-6; PMID:9461583; http://dx.doi.org/10.1074/jbc.273.7.3963
  • Cutler NS, Heitman J, Cardenas ME. TOR kinase homologs function in a signal transduction pathway that is conserved from yeast to mammals. Mol Cell Endocrinol 1999; 155:135-42; PMID:10580846; http://dx.doi.org/10.1016/S0303-7207(99)00121-5
  • Chen Y, Klionsky DJ. The regulation of autophagy - unanswered questions. J Cell Sci 2011; 124:161-70; PMID:21187343; http://dx.doi.org/10.1242/jcs.064576
  • Klionsky DJ, Baehrecke EH, Brumell JH, Chu CT, Codogno P, Cuervo AM, Debnath J, Deretic V, Elazar Z, Eskelinen EL, et al. A comprehensive glossary of autophagy-related molecules and processes (2nd edition). Autophagy 2011; 7:1273-94; PMID:21997368; http://dx.doi.org/10.4161/auto.7.11.17661
  • Rose A, Schlieker C. Alternative nuclear transport for cellular protein quality control. Trends Cell Biol 2012; 22:509-14; PMID:22858153; http://dx.doi.org/10.1016/j.tcb.2012.07.003
  • Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y, Ataman B, Koon A, Chang YT, Li Q, et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 2012; 149:832-46; PMID:22579286; http://dx.doi.org/10.1016/j.cell.2012.03.032
  • Mettenleiter TC, Muller F, Granzow H, Klupp BG. The way out: what we know and do not know about herpesvirus nuclear egress. Cell Microbiol 2013; 15:170-8; PMID:23057731; http://dx.doi.org/10.1111/cmi.12044
  • Stolz A, Ernst A, Dikic I. Cargo recognition and trafficking in selective autophagy. Nat Cell Biol 2014; 16:495-501; PMID:24875736; http://dx.doi.org/10.1038/ncb2979
  • Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 2011; 27:107-32; PMID:21801009; http://dx.doi.org/10.1146/annurev-cellbio-092910-154005
  • English L, Chemali M, Desjardins M. Nuclear membrane-derived autophagy, a novel process that participates in the presentation of endogenous viral antigens during HSV-1 infection. Autophagy 2009; 5:1026-9; PMID:19556870; http://dx.doi.org/10.4161/auto.5.7.9163
  • Radtke K, English L, Rondeau C, Leib D, Lippe R, Desjardins M. Inhibition of the host translation shutoff response by herpes simplex virus 1 triggers nuclear envelope-derived autophagy. J Virol 2013; 87:3990-7; PMID:23365427; http://dx.doi.org/10.1128/JVI.02974-12
  • Heck JW, Cheung SK, Hampton RY. Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1. Proceedings of the National Academy of Sciences of the United States of America 2010; 107:1106-11; PMID:20080635; http://dx.doi.org/10.1073/pnas.0910591107
  • Prasad R, Kawaguchi S, Ng DT. A nucleus-based quality control mechanism for cytosolic proteins. Mol Biol Cell 2010; 21:2117-27; PMID:20462951; http://dx.doi.org/10.1091/mbc.E10-02-0111
  • Guerriero CJ, Weiberth KF, Brodsky JL. Hsp70 targets a cytoplasmic quality control substrate to the San1p ubiquitin ligase. J Biol Chem 2013; 288:18506-20; PMID:23653356; http://dx.doi.org/10.1074/jbc.M113.475905
  • Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, Clark HB, Zoghbi HY, Orr HT. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 1998; 95:41-53; PMID:9778246; http://dx.doi.org/10.1016/S0092-8674(00)81781-X
  • Davies SW, Turmaine M, Cozens BA, DiFiglia M, Sharp AH, Ross CA, Scherzinger E, Wanker EE, Mangiarini L, Bates GP. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997; 90:537-48; PMID:9267033; http://dx.doi.org/10.1016/S0092-8674(00)80513-9
  • Woulfe JM. Abnormalities of the nucleus and nuclear inclusions in neurodegenerative disease: a work in progress. Neuropathol Appl Neurobiol 2007; 33:2-42; PMID:17239006