Abstract
Ubiquitination has long been recognised as a key determinator of protein fate by tagging proteins for proteasomal degradation. Most recently, the ability of conjugated ubiquitin chains to confer selectivity to autophagy was demonstrated. Although autophagy was first believed to be a bulk, non-selective ‘self-eating’ degradative process, the molecular mechanisms of selectivity are now starting to emerge. With the discovery of autophagy receptors – which bind both ubiquitinated substrates and autophagy specific light chain 3 (LC3) modifier on the inner sheath of autophagosomes – a new pathway of selective autophagy is being unravelled. In this review, we focus on the special role of ubiquitin signals and selective autophagy receptors in sorting a variety of autophagic cargos.
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Abbreviations
- ATG:
-
autophagy-related gene
- BAG:
-
BCL-2-associated athanogene
- BECN1:
-
Beclin1
- c-CBL:
-
c-Casitas B-lineage lymphoma
- CHIP:
-
carboxyl terminus of HSC70-interacting protein
- CMA:
-
chaperone-mediated autophagy
- Dvl2:
-
dishevelled 2
- ER:
-
endoplasmatic reticulum
- FIP200:
-
FAK family kinase-interacting protein of 200 kDa
- FUNDC1:
-
FUN14 domain containing 1
- GABARAP:
-
gamma-aminobutyric acid receptor-associated protein
- GATE-16:
-
golgi-associated ATPase enhancer of 16 kDa
- HDAC6:
-
histone deacetylase 6
- Hsp:
-
heat-shock protein
- Hsc70:
-
heat-shock cognate70
- K:
-
lysine
- LC3:
-
light chain 3
- LIR:
-
LC3-interacting region
- M:
-
methionine
- MO:
-
membranous organelle
- MAP1LC3:
-
microtubule-associated protein 1 light chain 3
- NBR1:
-
neighbour of breast cancer 1
- NDP52:
-
nuclear domain 10 protein 52
- NF-kB:
-
nuclear factor of kappa light polypeptide gene enhancer in B-cells 1
- OPTN:
-
optineurin
- p97/VCP:
-
protein 97/valosin-containing protein
- PB1:
-
Phox and Bem1p domain
- PE:
-
phosphatidylethanolamine
- PI3K:
-
1-phosphatidylinositol 3-kinase
- ROS:
-
reactive oxygen species
- src:
-
sarcoma viral oncogene homologue
- SMURF1:
-
SMAD-specific E3 ubiquitin protein ligase 1
- p62/SQSTM1:
-
sequestosome 1
- TBK1:
-
TANK binding kinase 1
- Tecpr:
-
Tachylectin-II-like beta-propeller domain
- UBA:
-
ubiquitin-associated
- UBL:
-
ubiquitin-like system
- UBD:
-
ubiquitin binding domain
- Ubp3:
-
ubiquitin carboxyl-terminal hydrolase 3
- ULK:
-
Unc-51-like kinase
- UPS:
-
ubiquitin–proteasomal system
- UPR:
-
unfolded protein response
- USP9x:
-
ubiquitin-specific peptidase 9, X-linked
- VDAC1:
-
voltage-dependent anion channel 1
- VPS34:
-
vacuolar protein sorting 34
References
Hershko A, Ciechanover A . The ubiquitin system. Annu Rev Biochem 1998; 67: 425–479.
Ohsumi Y, Mizushima N . Two ubiquitin-like conjugation systems essential for autophagy. Semin Cell Dev Biol 2004; 15: 231–236.
De Duve C, Wattiaux R . Functions of lysosomes. Annu Rev Physiol 1966; 28: 435–492.
Levine B, Mizushima N, Virgin HW . Autophagy in immunity and inflammation. Nature 2011; 469: 323–335.
Mizushima N, Levine B, Cuervo AM, Klionsky DJ . Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069–1075.
Bjorkoy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171: 603–614.
Kirkin V, Lamark T, Sou YS, Bjorkoy G, Nunn JL, Bruun JA et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009; 33: 505–516.
Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y et al. Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 2008; 453: 481–488.
Weidberg H, Shvets E, Elazar Z . Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 2011; 80: 125–156.
Goldberg AL . Protein degradation and protection against misfolded or damaged proteins. Nature 2003; 426: 895–899.
Kubota H . Quality control against misfolded proteins in the cytosol: a network for cell survival. J Biochem 2009; 146: 609–616.
Ikeda F, Dikic I . Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep 2008; 9: 536–542.
Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, Kanie M et al. A ubiquitin ligase complex assembles linear polyubiquitin chains. Embo J 2006; 25: 4877–4887.
Haglund K, Dikic I . Ubiquitylation and cell signaling. Embo J 2005; 24: 3353–3359.
Behrends C, Harper JW . Constructing and decoding unconventional ubiquitin chains. Nat Struct Mol Biol 2011; 18: 520–528.
Walczak H . TNF and ubiquitin at the crossroads of gene activation, cell death, inflammation, and cancer. Immunol Rev 2011; 244: 9–28.
Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J et al. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009; 137: 133–145.
Tan JM, Wong ES, Kirkpatrick DS, Pletnikova O, Ko HS, Tay SP et al. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet 2008; 17: 431–439.
Kopito RR . Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000; 10: 524–530.
Bence NF, Sampat RM, Kopito RR . Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292: 1552–1555.
Johnston JA, Ward CL, Kopito RR . Aggresomes: a cellular response to misfolded proteins. J Cell Biol 1998; 143: 1883–1898.
Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007; 6: 458–471.
Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6: 472–483.
Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007; 447: 859–863.
Korolchuk VI, Mansilla A, Menzies FM, Rubinsztein DC . Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell 2009; 33: 517–527.
Kettern N, Dreiseidler M, Tawo R, Hohfeld J . Chaperone-assisted degradation: multiple paths to destruction. Biol Chem 2010; 391: 481–489.
Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C . Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. Embo J 2009; 28: 889–901.
Wojcik C, Yano M, DeMartino GN . RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. J Cell Sci 2004; 117: 281–292.
Richly H, Rape M, Braun S, Rumpf S, Hoege C, Jentsch S . A series of ubiquitin binding factors connects CDC48/p97 to substrate multiubiquitylation and proteasomal targeting. Cell 2005; 120: 73–84.
Mizuno Y, Hori S, Kakizuka A, Okamoto K . Vacuole-creating protein in neurodegenerative diseases in humans. Neurosci Lett 2003; 343: 77–80.
Hirabayashi M, Inoue K, Tanaka K, Nakadate K, Ohsawa Y, Kamei Y et al. VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ 2001; 8: 977–984.
Ju JS, Weihl CC . Inclusion body myopathy, Paget's disease of the bone and fronto-temporal dementia: a disorder of autophagy. Hum Mol Genet 2010; 19: R38–R45.
Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, Prodromou C et al. Chaperoned ubiquitylation--crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 2005; 20: 525–538.
Shin Y, Klucken J, Patterson C, Hyman BT, McLean PJ . The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J Biol Chem 2005; 280: 23727–23734.
Hattori N, Mizuno Y . Pathogenetic mechanisms of parkin in Parkinson's disease. Lancet 2004; 364: 722–724.
Olzmann JA, Li L, Chudaev MV, Chen J, Perez FA, Palmiter RD et al. Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J Cell Biol 2007; 178: 1025–1038.
Narendra D, Tanaka A, Suen DF, Youle RJ . Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183: 795–803.
Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8: e1000298.
Mizushima N, Kuma A, Kobayashi Y, Yamamoto A, Matsubae M, Takao T et al. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 2003; 116: 1679–1688.
Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152: 657–668.
Sou YS, Waguri S, Iwata J, Ueno T, Fujimura T, Hara T et al. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol Biol Cell 2008; 19: 4762–4775.
Noda NN, Ohsumi Y, Inagaki F . ATG systems from the protein structural point of view. Chem Rev 2009; 109: 1587–1598.
Klionsky DJ, Cregg JM, Dunn WA, Emr SD, Sakai Y, Sandoval IV et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell 2003; 5: 539–545.
Paz Y, Elazar Z, Fass D . Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J Biol Chem 2000; 275: 25445–25450.
Suzuki NN, Yoshimoto K, Fujioka Y, Ohsumi Y, Inagaki F . The crystal structure of plant ATG12 and its biological implication in autophagy. Autophagy 2005; 1: 119–126.
Geng J, Klionsky DJ . The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep 2008; 9: 859–864.
Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z . Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. Embo J 2007; 26: 1749–1760.
Nakatogawa H, Ichimura Y, Ohsumi Y . Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 2007; 130: 165–178.
Xie Z, Nair U, Klionsky DJ . Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 2008; 19: 3290–3298.
Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T . LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci 2004; 117: 2805–2812.
Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z . LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. Embo J 2010; 29: 1792–1802.
Dikic I, Wakatsuki S, Walters KJ . Ubiquitin-binding domains - from structures to functions. Nat Rev Mol Cell Biol 2009; 10: 659–671.
Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282: 24131–24145.
Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T et al. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 2008; 283: 22847–22857.
Kirkin V, McEwan DG, Novak I, Dikic I . A role for ubiquitin in selective autophagy. Mol Cell 2009; 34: 259–269.
Strnad P, Zatloukal K, Stumptner C, Kulaksiz H, Denk H . Mallory-Denk-bodies: lessons from keratin-containing hepatic inclusion bodies. Biochim Biophys Acta 2008; 1782: 764–774.
Moscat J, Diaz-Meco MT, Wooten MW . Signal integration and diversification through the p62 scaffold protein. Trends Biochem Sci 2007; 32: 95–100.
Wilson MI, Gill DJ, Perisic O, Quinn MT, Williams RL . PB1 domain-mediated heterodimerization in NADPH oxidase and signaling complexes of atypical protein kinase C with Par6 and p62. Mol Cell 2003; 12: 39–50.
Nakamura K, Kimple AJ, Siderovski DP, Johnson GL . PB1 domain interaction of p62/sequestosome 1 and MEKK3 regulates NF-kappaB activation. J Biol Chem 2010; 285: 2077–2089.
Lamark T, Perander M, Outzen H, Kristiansen K, Overvatn A, Michaelsen E et al. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem 2003; 278: 34568–34581.
Vadlamudi RK, Joung I, Strominger JL, Shin J . p62, a phosphotyrosine-independent ligand of the SH2 domain of p56lck, belongs to a new class of ubiquitin-binding proteins. J Biol Chem 1996; 271: 20235–20237.
Seibenhener ML, Babu JR, Geetha T, Wong HC, Krishna NR, Wooten MW . Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 2004; 24: 8055–8068.
Goode A, Layfield R . Recent advances in understanding the molecular basis of Paget disease of bone. J Clin Pathol 2010; 63: 199–203.
Cavey JR, Ralston SH, Hocking LJ, Sheppard PW, Ciani B, Searle MS et al. Loss of ubiquitin-binding associated with Paget’s disease of bone p62 (SQSTM1) mutations. J Bone Miner Res 2005; 20: 619–624.
Matsumoto G, Wada K, Okuno M, Kurosawa M, Nukina N . Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell 2011; 44: 279–289.
Gao C, Cao W, Bao L, Zuo W, Xie G, Cai T et al. Autophagy negatively regulates Wnt signalling by promoting Dishevelled degradation. Nat Cell Biol 2010; 12: 781–790.
Kuo TC, Chen CT, Baron D, Onder TT, Loewer S, Almeida S et al. Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity. Nat Cell Biol 2011; 13: 1214–1223.
Pohl C, Jentsch S . Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat Cell Biol 2009; 11: 65–70.
Waters S, Marchbank K, Solomon E, Whitehouse CA . Autophagic receptors Nbr1 and p62 coregulate skeletal remodeling. Autophagy 2010; 6: 981–983.
D’Agostino C, Nogalska A, Cacciottolo M, Engel WK, Askanas V . Abnormalities of NBR1, a novel autophagy-associated protein, in muscle fibers of sporadic inclusion-body myositis. Acta Neuropathol 2011; 122: 627–636.
Novak I, Kirkin V, McEwan DG, Zhang J, Wild P, Rozenknop A et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep 2010; 11: 45–51.
Schweers RL, Zhang J, Randall MS, Loyd MR, Li W, Dorsey FC et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc Natl Acad Sci USA 2007; 104: 19500–19505.
Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G . Ubiquitin tag for sperm mitochondria. Nature 1999; 402: 371–372.
Al Rawi S, Louvet-Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C et al. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 2011; 334: 1144–1147.
Sato M, Sato K . Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 2011; 334: 1141–1144.
Gomes LC, Di Benedetto G, Scorrano L . During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat Cell Biol 2011; 13: 589–598.
Kim I, Rodriguez-Enriquez S, Lemasters JJ . Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 2007; 462: 245–253.
Geisler S, Holmstrom KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12: 119–131.
Narendra D, Kane LA, Hauser DN, Fearnley IM, Youle RJ . p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy 2010; 6: 1090–1106.
Polson HE, de Lartigue J, Rigden DJ, Reedijk M, Urbe S, Clague MJ et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 2010; 6 e-pub ahead of print 16 May 2010.
Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 2010; 189: 211–221.
Lee JY, Nagano Y, Taylor JP, Lim KL, Yao TP . Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J Cell Biol 2010; 189: 671–679.
Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW . Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 2010; 19: 4861–4870.
Tanaka A, Cleland MM, Xu S, Narendra DP, Suen DF, Karbowski M et al. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol 2010; 191: 1367–1380.
Ding WX, Ni HM, Li M, Liao Y, Chen X, Stolz DB et al. Nix is critical to two distinct phases of mitophagy, reactive oxygen species-mediated autophagy induction and Parkin-ubiquitin-p62-mediated mitochondrial priming. J Biol Chem 2010; 285: 27879–27890.
Liu L, Feng D, Chen G, Chen M, Zheng Q, Song P et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol 2012; 14: 177–185.
Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH . Recognition of bacteria in the cytosol of Mammalian cells by the ubiquitin system. Curr Biol 2004; 14: 806–811.
Virgin HW, Levine B . Autophagy genes in immunity. Nat Immunol 2009; 10: 461–470.
Shahnazari S, Brumell JH . Mechanisms and consequences of bacterial targeting by the autophagy pathway. Curr Opin Microbiol 2011; 14: 68–75.
Zheng YT, Shahnazari S, Brech A, Lamark T, Johansen T, Brumell JH . The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J Immunol 2009; 183: 5909–5916.
Thurston TL, Ryzhakov G, Bloor S, von Muhlinen N, Randow F . The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat Immunol 2009; 10: 1215–1221.
Wild P, Farhan H, McEwan DG, Wagner S, Rogov VV, Brady NR et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 2011; 333: 228–233.
Cemma M, Kim PK, Brumell JH . The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway. Autophagy 2011; 7: 341–345.
Ponpuak M, Davis AS, Roberts EA, Delgado MA, Dinkins C, Zhao Z et al. Delivery of cytosolic components by autophagic adaptor protein p62 endows autophagosomes with unique antimicrobial properties. Immunity 2010; 32: 329–341.
Thurston TL, Wandel MP, von Muhlinen N, Foeglein A, Randow F . Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 2012; 482: 414–418.
Kim PK, Hailey DW, Mullen RT, Lippincott-Schwartz J . Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes. Proc Natl Acad Sci USA 2008; 105: 20567–20574.
Kraft C, Deplazes A, Sohrmann M, Peter M . Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 2008; 10: 602–610.
Grasso D, Ropolo A, Lo Re A, Boggio V, Molejon MI, Iovanna JL et al. Zymophagy, a novel selective autophagy pathway mediated by VMP1-USP9x-p62, prevents pancreatic cell death. J Biol Chem 2011; 286: 8308–8324.
Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 2006; 26: 9220–9231.
Bernales S, McDonald KL, Walter P . Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 2006; 4: 2311–2324.
Sandilands E, Serrels B, McEwan DG, Morton JP, Macagno JP, McLeod K et al. Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling. Nat Cell Biol 2011; 14: 51–60.
Orvedahl A, Sumpter R, Xiao G, Ng A, Zou Z, Tang Y et al. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011; 480: 113–117.
Behrends C, Sowa ME, Gygi SP, Harper JW . Network organization of the human autophagy system. Nature 2010; 466: 68–76.
Ogawa M, Yoshikawa Y, Kobayashi T, Mimuro H, Fukumatsu M, Kiga K et al. A Tecpr1-dependent selective autophagy pathway targets bacterial pathogens. Cell Host Microbe 2011; 9: 376–389.
Chen D, Fan W, Lu Y, Ding X, Chen S, Zhong QA . Mammalian autophagosome maturation mechanism mediated by TECPR1 and the Atg12-Atg5 Conjugate. Mol Cell 2012; 45: 629–641.
McEwan DG, Dikic I . The three musketeers of autophagy: phosphorylation, ubiquitylation and acetylation. Trends Cell Biol 2011; 21: 195–201.
Acknowledgements
We apologize to scientists whose important contribution was not referenced in this review owing to space limitations. We would like to thank Ligia Gomes and Christian Behrends for critical reading of the manuscript and also to Philipp Wild and Evgenij Fiškin for comments and discussions. Research in the I.D. laboratory is supported by the Deutsche Forschungsgemeinschaft, the Cluster of Excellence ‘Macromolecular Complexes’ of the Goethe University Frankfurt (EXC115), LOEWE OSF and a European Research Council Advanced Grant and in the C.B. laboratory through a LOEWE Cell and Gene Therapy (CGT) grant, SFB834 funding, LOEWE OSF and Frankfurt Autophagy Network (FAN) funding. S.S. is the recipient of a fellowship from the Faculty of Medicine of the Goethe University, Frankfurt am Main.
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Shaid, S., Brandts, C., Serve, H. et al. Ubiquitination and selective autophagy. Cell Death Differ 20, 21–30 (2013). https://doi.org/10.1038/cdd.2012.72
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