Structural biology of the macroautophagy machinery

doi:10.1007/s11515-014-1293-3

Front. Biol.

2014, Vol. 9

Issue (1) : 18-34 https://doi.org/10.1007/s11515-014-1293-3

REVIEW

Structural biology of the macroautophagy machinery

Leon H. CHEW,Calvin K. YIP(

)

Department of Biochemistry and Molecular Biology, The University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC V6T 1Z3, Canada

Download: PDF(452 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

Macroautophagy is a conserved degradative process mediated through formation of a unique double-membrane structure, the autophagosome. The discovery of autophagy-related (Atg) genes required for autophagosome formation has led to the characterization of approximately 20 genes mediating this process. Recent structural studies of the Atg proteins have provided the molecular basis for their function. Here we summarize the recent progress in elucidating the structural basis for autophagosome formation.

Keywords macroautophagy autophagy Atg proteins structural biology X-ray crystallography single-particle electron microscopy

Corresponding Author(s): Calvin K. YIP

Issue Date: 13 May 2014

Cite this article:

Leon H. CHEW,Calvin K. YIP. Structural biology of the macroautophagy machinery[J]. Front. Biol., 2014, 9(1): 18-34.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-014-1293-3
https://academic.hep.com.cn/fib/EN/Y2014/V9/I1/18

Fig.1 Overview of macroautophagy. Autophagosome formation begins at the preautophagosomal structure (PAS). Expansion of the PAS leads to formation of a cup-shaped membrane known as a phagophore. Elongation of the phagophore sequesters cytoplasmic content until the vesicle is sealed off, forming a complete mature autophagosome. The autophagosome is subsequently targeted to the lysosome where the inner membrane and its content would be degraded by hydrolytic enzymes. The overall contributions of each Atg functional group to the different steps of autophagosome biogenesis are depicted.

Functional group	Role in autophagosome formation	Yeast	Human	Structural biology reference	Technique	Species studied
Atg1 complex	Atg1 is a serine/threonine kinase with a role in tethering membranes. Atg17-Atg31-Atg29 acts a scaffold for assembling the Atg1 complex	Atg1	ULK1
		Atg13	ATG13	Jao et al., 2013	X-ray crystallography	Lachancea thermotolerans
		Atg17	FIP200	Ragusa et al., 2012	X-ray crystallography	Lachancea thermotolerans

				Chew et al., 2013	EM	Saccharomyces cerevisiae
		Atg29	N/A	Ragusa et al., 2012	X-ray crystallography	Lachancea thermotolerans

				Chew et al., 2013	EM	Saccharomyces cerevisiae
		Atg31	N/A	Ragusa et al., 2012	X-ray crystallography	Lachancea thermotolerans

				Chew et al., 2013	EM	Saccharomyces cerevisiae
			ATG101
PI(3)K complex	Produces Ptdins(3)P on autophagic membranes. Atg14 and Atg6 have shown membrane binding capabilities.	Vps34	VPS34	Miller et al., 2010	X-ray crystallography	Drosophila melanogaster
		Vps15	VPS15	Heenan et al., 2009	X-ray crystallography	Saccharomyces cerevisiae
		Atg14	ATG14L/BARKOR
		Vps30/Atg6	Beclin1	Oberstein et al., 2007	X-ray crystallography	Homo sapiens

				Feng et al., 2007	X-ray crystallography	Homo sapiens

				Huang et al., 2012	X-ray crystallography	Homo sapiens

				Li et al., 2012	X-ray crystallography	Rattus norvegicus

				Noda et al., 2012	X-ray crystallography	Saccharomyces cerevisiae
		Atg38
Atg9	Integral membrane protein. Provides early membrane source for PAS formation.	Atg9	Atg9
Atg18–Atg2 complex	Atg18 specifically binds PI(3)P . Recruits ubiquitin-like conjugation system.	Atg18	WIPI1-4	Krick et al., 2012	X-ray crystallography	Kluyveromyces lactis (Hsv2)

				Watanabe et al., 2012	X-ray crystallography	Kluyveromyces marxianus (Hsv2)

				Baskaran et al., 2012	X-ray crystallography	Kluyveromyces lactis (Hsv2)
		Atg2	Atg2
Atg12 conjugation	Atg12 is conjugated torAtg5 through a ubiquitin-like cascade. Atg12-Atg5 conjugates form a complex with Atg16. Atg5 can bind membranes and may tether membranes through dimerization of Atg16.	Atg12	ATG12	Suzuki et al., 2005	X-ray crystallography	Arabidopsis thaliana
		Atg7	ATG7	Taherbhoy et al., 2011	X-ray crystallography	Saccharomyces cerevisiae
				Noda et al., 2011	X-ray crystallography	Saccharomyces cerevisiae
				NMR
				Hong et al., 2011	X-ray crystallography	Saccharomyces cerevisiae

				Kaiser et al., 2012	X-ray crystallography	Saccharomyces cerevisiae

				Yamaguchi et al., 2012a	X-ray crystallography	Kluyveromyces marxianus
						Arabidopsis thaliana

		Atg10	ATG10	Yamaguchi et al., 2012a	X-ray crystallography	Kluyveromyces marxianus

				Kaiser et al., 2012	X-ray crystallography	Saccharomyces cerevisiae

				Hong et al., 2012	X-ray crystallography	Saccharomyces cerevisiae

				Yamaguchi et al., 2012b	X-ray crystallography	Kluyveromyces marxianus

		Atg5	ATG5	Matsushita et al., 2007	X-ray crystallography	Saccharomyces cerevisiae

				Otomo et al., 2013	X-ray crystallography	Homo sapiens

				Yamaguchi et al., 2012b	X-ray crystallography	Kluyveromyces marxianus
				NMR
				Noda et al., 2013	X-ray crystallography	Saccharomyces cerevisiae

				Metlagel et al., 2013	X-ray crystallography	Homo sapiens

		Atg16	ATG16L1/2	Fujioka et al., 2010	X-ray crystallography	Saccharomyces cerevisiae

Atg8 conjugation	Atg8 is lipidated to PE through an ubiquitin-like cascade. Atg4 proteolytically activates Atg8 followed by conjugation to the enzymes Atg7 (E1), Atg3 (E2).	Atg8	LC3A/B/C GABARAP GATE-16	Paz et al., 2000	X-ray crystallography	Bos taurus (GATE-16)

				Coyle et al., 2002	X-ray crystallography	Homo sapiens (GABARAP)

				Knight et al., 2002	X-ray crystallography	Homo sapiens (GABARAP)

				Sugawara et al., 2004	X-ray crystallography	Rattus norvegicus (LC3)

				Schwarten et al., 2010	NMR	Saccharomyces cerevisiae

				Kumeta et al., 2010	NMR	Saccharomyces cerevisiae
				Noda et al., 2011	X-ray crystallography	Saccharomyces cerevisiae

				Hong et al., 2011	X-ray crystallography, NMR	Saccharomyces cerevisiae

		Atg4	ATG4A-D	Sugawara et al., 2005	X-ray crystallography	Homo sapiens
				Kumanomidou et al., 2006	X-ray crystallography	Homo sapiens
				Satoo et al., 2009	X-ray Crystallography	Homo Sapiens
		Atg7	ATG7	see above
		Atg3	ATG3	Yamada et al., 2007	X-ray crystallography	Saccharomyces cerevisiae

Tab.1 Functional groups for autophagosome formation

Fig.2 Model of Atg1 kinase complex function. (A) Crystal structure of the Atg13-HORMA domain (PDB: 4J2G). Residues in red highlight the putative phosphate-sensing motif. (B) Model of vesicle tethering mediated by the Atg1 kinase complex. Atg17 (orange) and Atg31-Atg29 (blue) are constitutively formed during nutrient-rich conditions and are localized to the PAS. Upon autophagy induction, Atg17 recruits Atg9 vesicles through direct interaction with Atg9 and may function as a tether for these vesicles. Atg13 and Atg1 are recruited to the PAS where the C-terminal domain of Atg1 (Atg1-CTD) can function to bind the high-curved Atg9 vesicles. The dimerization of Atg1-CTD may promote fusion of Atg9 vesicles. PDB codes for structures depicted: 4HPQ (Atg17-Atg31-Atg29), 4J2G (Atg13 HORMA domain).

Fig.3 Components of the autophagy specific class III PI(3)K complex. (A) Structural organization of Beclin1. Beclin1 is a central hub for regulation of class III PI(3)K complex. Beclin1 can be subdivided into three functional domains; the N-terminal Bcl-2 homology (BH3) domain (PDB: 2P1L. residues 107-135), the central coiled-coil domain (CCD; PDB: 3Q8T, residues 144-269), and the evolutionarily conserved domain (ECD; PDB: 4DDP, residues 248-450). (B) Model of class III PI(3)K formation. This complex is composed of Vps34 (red), Vps15 (yellow), Atg6/Beclin1 (blue), Atg14 (orange) and Atg38 (brown). Complex formation occurs through interaction of Atg14 with Atg6/Beclin1 and Vps34 with Vps15, which is further stabilized by association with Atg38. The class III PI(3)K complex produces PtdIns(3)P at the autophagosome membrane through the catalytic activity of the PI(3) kinase Vps34. This complex is targeted and anchored to membranes by myristoylated Vps15 and the intrinsic membrane binding ability of Atg14 and Atg6/Beclin1. Following PtdIns(3)P production, Atg18 is recruited through two phosphoinositide binding sites. A small hydrophobic loop may facilitate its insertion into the membrane. Atg2 can be recruited in an Atg18 dependent or independent mechanism to interact with effectors. PDB codes for structures depicted: 3GRE (Vps15), 4DDP (Beclin1 ECD), 3Q8T (Beclin1 CCD), 2X6H (Vps34), 4EXV (Hsv2/Atg18).

Fig.4 Atg8-family of ubiquitin-like proteins. (A) NMR structure of yeast Atg8. Several interaction interfaces are labeled. (B) Comparison of Atg8-family protein structures exhibiting the ubiquitin-like fold. PDB Code for structure depicted: 2KQ7 (Atg8), 1UGM (LC3), 1GNU (GABARAP), 1EO6 (GATE-16), 1UBI (ubiquitin).

Fig.5 Model of Atg12-Atg5-Atg16 complex. (A) Dimer model of the Atg12-Atg5-Atg16 complex. Atg12 is covalently linked to Atg5. Atg16 is bridged through Atg5 and has a C terminus coiled-coil dimerization domain that mediates dimerization of this complex. Atg12 contains an Atg3 binding region highlighted in red. Atg5 has a membrane binding region highlighted in yellow. (B) Comparison of the Atg3 binding pocket of Atg12 to LC3-interacting region (LIR) peptides in complex with Atg8-family members. The peptide is depicted in magenta. Atg12 (4NAW), LC3 (2K6Q), Atg8 (2ZPN). C. A model for Atg12-Atg5-Atg16 membrane tethering. Membrane binding occurs through Atg5. This positioning of the complex allows for the freely exposed Atg3 binding region on Atg12. Structures were made from PDB files: 4GDK (Atg12-Atg5-Atg16) and 3A7O (Atg16 dimer).

1	AitaV M, LiangX H, MurtyV V, PincusD L, YuW, CayanisE, KalachikovS, GilliamT C, LevineB (1999). Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics, 59(1): 59–65 doi: 10.1006/geno.1999.5851 pmid: 10395800
2	ArakiY, KuW C, AkiokaM, MayA I, HayashiY, ArisakaF, IshihamaY, OhsumiY (2013). Atg38 is required for autophagy-specific phosphatidylinositol 3-kinase complex integrity. J Cell Biol, 203(2): 299–313 doi: 10.1083/jcb.201304123 pmid: 24165940
3	AshrafiG, SchwarzT L (2013). The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ, 20(1): 31–42 doi: 10.1038/cdd.2012.81 pmid: 22743996
4	AxeE L, WalkerS A, ManifavaM, ChandraP, RoderickH L, HabermannA, GriffithsG, KtistakisN T (2008). Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol, 182(4): 685–701 doi: 10.1083/jcb.200803137 pmid: 18725538
5	BaskaranS, RagusaM J, BouraE, HurleyJ H (2012). Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol Cell, 47(3): 339–348 doi: 10.1016/j.molcel.2012.05.027 pmid: 22704557
6	BirgisdottirA B, LamarkT, JohansenT (2013). The LIR motif- crucial for selective autophagy. J Cell Sci, 126(Pt 15): 3237–3247 pmid: 23908376
7	BurdaP, PadillaS M, SarkarS, EmrS D (2002). Retromer function in endosome-to-Golgi retrograde transport is regulated by the yeast Vps34 PtdIns 3-kinase. J Cell Sci, 115(Pt 20): 3889–3900 doi: 10.1242/jcs.00090 pmid: 12244127
8	ChanE Y W, LongattiA, McKnightN C, ToozeS A (2009). Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol, 29(1): 157–171 doi: 10.1128/MCB.01082-08 pmid: 18936157
9	CheongH, NairU, GengJ, KlionskyD J (2008). The Atg1 kinase complex is involved in the regulation of protein recruitment to initiate sequestering vesicle formation for nonspecific autophagy in Saccharomyces cerevisiae. Mol Biol Cell, 19(2): 668–681 doi: 10.1091/mbc.E07-08-0826 pmid: 18077553
10	CheongH, YorimitsuT, ReggioriF, LegakisJ E, WangC W, KlionskyD J (2005). Atg17 regulates the magnitude of the autophagic response. Mol Biol Cell, 16(7): 3438–3453 doi: 10.1091/mbc.E04-10-0894 pmid: 15901835
11	ChoiA M K, RyterS W, LevineB (2013). Autophagy in human health and disease. N Engl J Med, 368(7): 651–662 doi: 10.1056/NEJMra1205406 pmid: 23406030
12	CoyleJ E, QamarS, RajashankarK R, NikolovD B (2002). Structure of GABARAP in two conformations: implications for GABA(A) receptor localization and tubulin binding. Neuron, 33(1): 63–74 doi: 10.1016/S0896-6273(01)00558-X pmid: 11779480
13	DoveS K, PiperR C, McEwenR K, YuJ W, KingM C, HughesD C, ThuringJ, HolmesA B, CookeF T, MichellR H, ParkerP J, LemmonM A (2004). Svp1p defines a family of phosphatidylinositol 3,5-bisphosphate effectors. EMBO J, 23(9): 1922–1933 doi: 10.1038/sj.emboj.7600203 pmid: 15103325
14	FanW, NassiriA, ZhongQ (2011). Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc Natl Acad Sci USA, 108(19): 7769–7774 doi: 10.1073/pnas.1016472108 pmid: 21518905
15	FengW, HuangS, WuH, ZhangM (2007). Molecular basis of Bcl-xL’s target recognition versatility revealed by the structure of Bcl-xL in complex with the BH3 domain of Beclin-1. J Mol Biol, 372(1): 223–235 doi: 10.1016/j.jmb.2007.06.069 pmid: 17659302
16	FogelA I, DlouhyB J, WangC, RyuS W, NeutznerA, HassonS A, SiderisD P, AbeliovichH, YouleR J (2013). Role of membrane association and Atg14-dependent phosphorylation in beclin-1-mediated autophagy. Mol Cell Biol, 33(18): 3675–3688 doi: 10.1128/MCB.00079-13 pmid: 23878393
17	FujiokaY, NodaN N, NakatogawaH, OhsumiY, InagakiF (2010). Dimeric coiled-coil structure of Saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J Biol Chem, 285(2): 1508–1515 doi: 10.1074/jbc.M109.053520 pmid: 19889643
18	FuruyaN, YuJ, ByfieldM, PattingreS, LevineB (2005). The evolutionarily conserved domain of Beclin 1 is required for Vps34 binding, autophagy and tumor suppressor function. Autophagy, 1(1): 46–52 doi: 10.4161/auto.1.1.1542 pmid: 16874027
19	GammohN, FloreyO, OverholtzerM, JiangX (2013). Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and-independent autophagy. Nat Struct Mol Biol, 20(2): 144–149 doi: 10.1038/nsmb.2475 pmid: 23262492
20	GanleyI G, LamH, WangJ, DingX, ChenS, JiangX (2009). ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem, 284(18): 12297–12305 doi: 10.1074/jbc.M900573200 pmid: 19258318
21	GaugelA, BakulaD, HoffmannA, Proikas-CezanneT (2012). Defining regulatory and phosphoinositide-binding sites in the human WIPI-1 β-propeller responsible for autophagosomal membrane localization downstream of mTORC1 inhibition. J Mol Signal, 7(1): 16 doi: 10.1186/1750-2187-7-16 pmid: 23088497
22	HaileyD W, RamboldA S, Satpute-KrishnanP, MitraK, SougratR, KimP K, Lippincott-SchwartzJ (2010). Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell, 141(4): 656–667 doi: 10.1016/j.cell.2010.04.009 pmid: 20478256
23	HamasakiM, FurutaN, MatsudaA, NezuA, YamamotoA, FujitaN, OomoriH, NodaT, HaraguchiT, HiraokaY, AmanoA, YoshimoriT (2013). Autophagosomes form at ER-mitochondria contact sites. Nature, 495(7441): 389–393 doi: 10.1038/nature11910 pmid: 23455425
24	Hayashi-NishinoM, FujitaN, NodaT, YamaguchiA, YoshimoriT, YamamotoA (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol, 11(12): 1433–1437 doi: 10.1038/ncb1991 pmid: 19898463
25	HeenanE J, VanhookeJ L, TempleB R, BettsL, SondekJ E, DohlmanH G (2009). Structure and function of Vps15 in the endosomal G protein signaling pathway. Biochemistry, 48(27): 6390–6401 doi: 10.1021/bi900621w pmid: 19445518
26	HongS B, KimB W, KimJ H, SongH K (2012). Structure of the autophagic E2 enzyme Atg10. Acta Crystallogr D Biol Crystallogr, 68(Pt 10): 1409–1417 doi: 10.1107/S0907444912034166 pmid: 22993095
27	HongS B, KimB W, LeeK E, KimS W, JeonH, KimJ, SongH K (2011). Insights into noncanonical E1 enzyme activation from the structure of autophagic E1 Atg7 with Atg8. Nat Struct Mol Biol, 18(12): 1323–1330 doi: 10.1038/nsmb.2165 pmid: 22056771
28	HosokawaN, SasakiT, IemuraS, NatsumeT, HaraT, MizushimaN (2009). Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy, 5(7): 973–979 doi: 10.4161/auto.5.7.9296 pmid: 19597335
29	HuangW, ChoiW, HuW, MiN, GuoQ, MaM, LiuM, TianY, LuP, WangF L, DengH, LiuL, GaoN, YuL, ShiY (2012). Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein. Cell Res, 22(3): 473–489 doi: 10.1038/cr.2012.24 pmid: 22310240
30	IchimuraY, KirisakoT, TakaoT, SatomiY, ShimonishiY, IshiharaN, MizushimaN, TanidaI, KominamiE, OhsumiM, NodaT, OhsumiY (2000). A ubiquitin-like system mediates protein lipidation. Nature, 408(6811): 488–492 doi: 10.1038/35044114 pmid: 11100732
31	ItakuraE, KishiC, InoueK, MizushimaN (2008). Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell, 19(12): 5360–5372 doi: 10.1091/mbc.E08-01-0080 pmid: 18843052
32	JaoC C, RagusaM J, StanleyR E, HurleyJ H (2013). A HORMA domain in Atg13 mediates PI 3-kinase recruitment in autophagy. Proc Natl Acad Sci USA, 110(14): 5486–5491 doi: 10.1073/pnas.1220306110 pmid: 23509291
33	KabeyaY, KamadaY, BabaM, TakikawaH, SasakiM, OhsumiY (2005). Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy. Mol Biol Cell, 16(5): 2544–2553 doi: 10.1091/mbc.E04-08-0669 pmid: 15743910
34	KabeyaY, MizushimaN, YamamotoA, Oshitani-OkamotoS, OhsumiY, YoshimoriT (2004). LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci, 117(Pt 13): 2805–2812 doi: 10.1242/jcs.01131 pmid: 15169837
35	KabeyaY, NodaN N, FujiokaY, SuzukiK, InagakiF, OhsumiY (2009). Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae. Biochem Biophys Res Commun, 389(4): 612–615 doi: 10.1016/j.bbrc.2009.09.034 pmid: 19755117
36	KaiserS E, MaoK, TaherbhoyA M, YuS, OlszewskiJ L, DudaD M, KurinovI, DengA, FennT D, KlionskyD J, SchulmanB A (2012). Noncanonical E2 recruitment by the autophagy E1 revealed by Atg7-Atg3 and Atg7-Atg10 structures. Nat Struct Mol Biol, 19(12): 1242–1249 doi: 10.1038/nsmb.2415 pmid: 23142976
37	KakutaS, YamamotoH, NegishiL, Kondo-KakutaC, HayashiN, OhsumiY (2012). Atg9 vesicles recruit vesicle-tethering proteins Trs85 and Ypt1 to the autophagosome formation site. J Biol Chem, 287(53): 44261–44269 doi: 10.1074/jbc.M112.411454 pmid: 23129774
38	KamadaY, FunakoshiT, ShintaniT, NaganoK, OhsumiM, OhsumiY (2000). Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol, 150(6): 1507–1513 doi: 10.1083/jcb.150.6.1507 pmid: 10995454
39	KaranasiosE, StapletonE, ManifavaM, KaizukaT, MizushimaN, WalkerS A, KtistakisN T (2013). Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J Cell Sci, 126(Pt 22): 5224–5238 doi: 10.1242/jcs.132415 pmid: 24013547
40	KiharaA, NodaT, IshiharaN, OhsumiY (2001). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol, 152, 519–30
41	KijanskaM, DohnalI, ReiterW, KasparS, StoffelI, AmmererG, KraftC, PeterM (2010). Activation of Atg1 kinase in autophagy by regulated phosphorylation. Autophagy, 6(8): 1168–1178 doi: 10.4161/auto.6.8.13849 pmid: 20953146
42	KimJ, KunduM, ViolletB, GuanK L (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol, 13(2): 132–141 doi: 10.1038/ncb2152 pmid: 21258367
43	KnightD, HarrisR, McAlisterM S B, PhelanJ P, GeddesS, MossS J, DriscollP C, KeepN H (2002). The X-ray crystal structure and putative ligand-derived peptide binding properties of gamma-aminobutyric acid receptor type A receptor-associated protein. J Biol Chem, 277(7): 5556–5561 doi: 10.1074/jbc.M109753200 pmid: 11729197
44	KobayashiT, SuzukiK, OhsumiY (2012). Autophagosome formation can be achieved in the absence of Atg18 by expressing engineered PAS-targeted Atg2. FEBS Lett, 586(16): 2473–2478 doi: 10.1016/j.febslet.2012.06.008 pmid: 22728243
45	Kondo-OkamotoN, NodaN N, SuzukiS W, NakatogawaH, TakahashiI, MatsunamiM, HashimotoA, InagakiF, OhsumiY, OkamotoK (2012). Autophagy-related protein 32 acts as autophagic degron and directly initiates mitophagy. J Biol Chem, 287(13): 10631–10638 doi: 10.1074/jbc.M111.299917 pmid: 22308029
46	KraftC, DeplazesA, SohrmannM, PeterM (2008). Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol, 10(5): 602–610 doi: 10.1038/ncb1723 pmid: 18391941
47	KraftC, KijanskaM, KalieE, SiergiejukE, LeeS S, SemplicioG, StoffelI, BrezovichA, VermaM, HansmannI, AmmererG, HofmannK, ToozeS, PeterM (2012). Binding of the Atg1/ULK1 kinase to the ubiquitin-like protein Atg8 regulates autophagy. EMBO J, 31(18): 3691–3703 doi: 10.1038/emboj.2012.225 pmid: 22885598
48	KrickR, BusseR A, ScaciocA, StephanM, JanshoffA, ThummM, KühnelK (2012). Structural and functional characterization of the two phosphoinositide binding sites of PROPPINs, a β-propeller protein family. Proc Natl Acad Sci USA, 109(30): E2042–E2049 doi: 10.1073/pnas.1205128109 pmid: 22753491
49	KrickR, MueheY, PrickT, BremerS, SchlotterhoseP, EskelinenE L, MillenJ, GoldfarbD S, ThummM (2008). Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell, 19(10): 4492–4505 doi: 10.1091/mbc.E08-04-0363 pmid: 18701704
50	KuB, WooJ S, LiangC, LeeK H, HongH S, eX, KimK S, JungJ U, OhB H (2008). Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog, 4(2): e25 doi: 10.1371/journal.ppat.0040025 pmid: 18248095
51	KumaA, MizushimaN, IshiharaN, OhsumiY (2002). Formation of the approximately 350-kDa Apg12-Apg5.Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J Biol Chem, 277(21): 18619–18625 doi: 10.1074/jbc.M111889200 pmid: 11897782
52	KumanomidouT, MizushimaT, KomatsuM, SuzukiA, TanidaI, SouY S, UenoT, KominamiE, TanakaK, YamaneT (2006). The crystal structure of human Atg4b, a processing and de-conjugating enzyme for autophagosome-forming modifiers. J Mol Biol, 355(4): 612–618 doi: 10.1016/j.jmb.2005.11.018 pmid: 16325851
53	KumetaH, WatanabeM, NakatogawaH, YamaguchiM, OguraK, AdachiW, FujiokaY, NodaN N, OhsumiY, InagakiF (2010). The NMR structure of the autophagy-related protein Atg8. J Biomol NMR, 47(3): 237–241 doi: 10.1007/s10858-010-9420-1 pmid: 20428927
54	LambC A, YoshimoriT, ToozeS A (2013). The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol, 14(12): 759–774 doi: 10.1038/nrm3696 pmid: 24201109
55	LiX, HeL, CheK H, FunderburkS F, PanL, PanN, ZhangM, YueZ, ZhaoY (2012). Imperfect interface of Beclin1 coiled-coil domain regulates homodimer and heterodimer formation with Atg14L and UVRAG. Nat Commun, 3: 662 doi: 10.1038/ncomms1648 pmid: 22314358
56	LiangX H, JacksonS, SeamanM, BrownK, KempkesB, HibshooshH, LevineB (1999). Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature, 402(6762): 672–676 doi: 10.1038/45257 pmid: 10604474
57	LiangX H, KleemanL K, JiangH H, GordonG, GoldmanJ E, BerryG, HermanB, LevineB (1998). Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol, 72(11): 8586–8596 pmid: 9765397
58	LiuK, CzajaM J (2013). Regulation of lipid stores and metabolism by lipophagy. Cell Death Differ, 20(1): 3–11 doi: 10.1038/cdd.2012.63 pmid: 22595754
59	LiuX, DaiS, ZhuY, MarrackP, KapplerJ W (2003). The structure of a Bcl-xL/Bim fragment complex: implications for Bim function. Immunity, 19(3): 341–352 doi: 10.1016/S1074-7613(03)00234-6 pmid: 14499110
60	MaoK, ChewL H, Inoue-AonoY, CheongH, NairU, PopelkaH, YipC K, KlionskyD J (2013). Atg29 phosphorylation regulates coordination of the Atg17-Atg31-Atg29 complex with the Atg11 scaffold during autophagy initiation. Proc Natl Acad Sci USA, 110(31): E2875–E2884 doi: 10.1073/pnas.1300064110 pmid: 23858448
61	MatsunagaK, SaitohT, TabataK, OmoriH, SatohT, KurotoriN, MaejimaI, Shirahama-NodaK, IchimuraT, IsobeT, AkiraS, NodaT, YoshimoriT (2009). Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol, 11(4): 385–396 doi: 10.1038/ncb1846 pmid: 19270696
62	MatsushitaM, SuzukiN N, ObaraK, FujiokaY, OhsumiY, InagakiF (2007). Structure of Atg5.Atg16, a complex essential for autophagy. J Biol Chem, 282(9): 6763–6772 doi: 10.1074/jbc.M609876200 pmid: 17192262
63	MatsuuraA, TsukadaM, WadaY, OhsumiY (1997). Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene, 192, 245–250
64	MautheM, JacobA, FreibergerS, HentschelK, StierhofY D, CodognoP, Proikas-CezanneT (2011). Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy, 7(12): 1448–1461 doi: 10.4161/auto.7.12.17802 pmid: 22082875
65	Meiling-WesseK, BarthH, VossC, EskelinenE L, EppleU D, ThummM (2004). Atg21 is required for effective recruitment of Atg8 to the preautophagosomal structure during the Cvt pathway. J Biol Chem, 279(36): 37741–37750 doi: 10.1074/jbc.M401066200 pmid: 15194695
66	MercerC A, KaliappanA, DennisP B (2009). A novel, human Atg13 binding protein, Atg101, interacts with ULK1 and is essential for macroautophagy. Autophagy, 5(5): 649–662 doi: 10.4161/auto.5.5.8249 pmid: 19287211
67	MetlagelZ, OtomoC, TakaesuG, OtomoT (2013). Structural basis of ATG3 recognition by the autophagic ubiquitin-like protein ATG12. Proc Natl Acad Sci USA, 110(47): 18844–18849 doi: 10.1073/pnas.1314755110 pmid: 24191030
68	MillerS, TavshanjianB, OleksyA, PerisicO, HousemanB T, ShokatK M, WilliamsR L (2010). Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science, 327(5973): 1638–1642 doi: 10.1126/science.1184429 pmid: 20339072
69	MizushimaN, NodaT, YoshimoriT, TanakaY, IshiiT, GeorgeM D, KlionskyD J, OhsumiM, OhsumiY (1998). A protein conjugation system essential for autophagy. Nature, 395(6700): 395–398 doi: 10.1038/26506 pmid: 9759731
70	MizushimaN, YoshimoriT, OhsumiY (2011). The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol, 27(1): 107–132 doi: 10.1146/annurev-cellbio-092910-154005 pmid: 21801009
71	MoreauK, RavikumarB, RennaM, PuriC, RubinszteinD C (2011). Autophagosome precursor maturation requires homotypic fusion. Cell, 146(2): 303–317 doi: 10.1016/j.cell.2011.06.023 pmid: 21784250
72	MoreauK, RennaM, RubinszteinD C (2013). Connections between SNAREs and autophagy. Trends Biochem Sci, 38(2): 57–63 doi: 10.1016/j.tibs.2012.11.004 pmid: 23306003
73	NairU, JotwaniA, GengJ, GammohN, RichersonD, YenW L, GriffithJ, NagS, WangK, MossT, BabaM, McNewJ A, JiangX, ReggioriF, MeliaT J, KlionskyD J (2011). SNARE proteins are required for macroautophagy. Cell, 146(2): 290–302 doi: 10.1016/j.cell.2011.06.022 pmid: 21784249
74	NairU, YenW L, MariM, CaoY, XieZ, BabaM, ReggioriF, KlionskyD J (2012). A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy, 8(5): 780–793 doi: 10.4161/auto.19385 pmid: 22622160
75	NakatogawaH, IchimuraY, OhsumiY (2007). Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell, 130(1): 165–178 doi: 10.1016/j.cell.2007.05.021 pmid: 17632063
76	NakatogawaH, IshiiJ, AsaiE, OhsumiY (2012). Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy, 8(2): 1–10 doi: 10.4161/auto.8.2.18373 pmid: 22082964
77	NakatogawaH, SuzukiK, KamadaY, OhsumiY (2009). Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol, 10(7): 458–467 doi: 10.1038/nrm2708 pmid: 19491929
78	NishimuraT, KaizukaT, CadwellK, SahaniM H, SaitohT, AkiraS, VirginH W, MizushimaN (2013). FIP200 regulates targeting of Atg16L1 to the isolation membrane. EMBO Rep, 14(3): 284–291 doi: 10.1038/embor.2013.6 pmid: 23392225
79	NodaN N, FujiokaY, HanadaT, OhsumiY, InagakiF (2013). Structure of the Atg12-Atg5 conjugate reveals a platform for stimulating Atg8-PE conjugation. EMBO Rep, 14(2): 206–211 doi: 10.1038/embor.2012.208 pmid: 23238393
80	NodaN N, KobayashiT, AdachiW, FujiokaY, OhsumiY, InagakiF (2012). Structure of the novel C-terminal domain of vacuolar protein sorting 30/autophagy-related protein 6 and its specific role in autophagy. J Biol Chem, 287(20): 16256–16266 doi: 10.1074/jbc.M112.348250 pmid: 22437838
81	NodaN N, KumetaH, NakatogawaH, SatooK, AdachiW, IshiiJ, FujiokaY, OhsumiY, InagakiF (2008). Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells, 13(12): 1211–1218 doi: 10.1111/j.1365-2443.2008.01238.x pmid: 19021777
82	NodaN N, OhsumiY, InagakiF (2009). ATG systems from the protein structural point of view. Chem Rev, 109(4): 1587–1598 doi: 10.1021/cr800459r pmid: 19236009
83	NodaN N, SatooK, FujiokaY, KumetaH, OguraK, NakatogawaH, OhsumiY, InagakiF (2011). Structural basis of Atg8 activation by a homodimeric E1, Atg7. Mol Cell, 44(3): 462–475 doi: 10.1016/j.molcel.2011.08.035 pmid: 22055191
84	NodaT, KimJ, HuangW P, BabaM, TokunagaC, OhsumiY, KlionskyD J (2000). Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol, 148(3): 465–480 doi: 10.1083/jcb.148.3.465 pmid: 10662773
85	NodaT, MatsunagaK, Taguchi-AtarashiN, YoshimoriT (2010). Regulation of membrane biogenesis in autophagy via PI3P dynamics. Semin Cell Dev Biol, 21(7): 671–676 doi: 10.1016/j.semcdb.2010.04.002 pmid: 20403452
86	ObaraK, NodaT, NiimiK, OhsumiY (2008a). Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells, 13(6): 537–547 doi: 10.1111/j.1365-2443.2008.01188.x pmid: 18533003
87	ObaraK, SekitoT, NiimiK, OhsumiY (2008b). The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J Biol Chem, 283(35): 23972–23980 doi: 10.1074/jbc.M803180200 pmid: 18586673
88	ObaraK, SekitoT, OhsumiY (2006). Assortment of phosphatidylinositol 3-kinase complexes—Atg14p directs association of complex I to the pre-autophagosomal structure in Saccharomyces cerevisiae. Mol Biol Cell, 17(4): 1527–1539 doi: 10.1091/mbc.E05-09-0841 pmid: 16421251
89	ObersteinA, JeffreyP D, ShiY (2007). Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem, 282(17): 13123–13132 doi: 10.1074/jbc.M700492200 pmid: 17337444
90	OtomoC, MetlagelZ, TakaesuG, OtomoT (2013). Structure of the human ATG12~ATG5 conjugate required for LC3 lipidation in autophagy. Nat Struct Mol Biol, 20(1): 59–66 doi: 10.1038/nsmb.2431 pmid: 23202584
91	PanaretouC, DominJ, CockcroftS, WaterfieldM D (1997). Characterization of p150, an adaptor protein for the human phosphatidylinositol (PtdIns) 3-kinase.Substrate presentation by phosphatidylinositol transfer protein to the p150.Ptdins 3-kinase complex. J Biol Chem, 272(4): 2477–2485 doi: 10.1074/jbc.272.4.2477 pmid: 8999962
92	PazY, ElazarZ, FassD (2000). Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J Biol Chem, 275(33): 25445–25450 doi: 10.1074/jbc.C000307200 pmid: 10856287
93	PolsonH E J, de LartigueJ, RigdenD J, ReedijkM, UrbéS, ClagueM J, ToozeS A (2010). Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy, 6(4): 506–522 doi: 10.4161/auto.6.4.11863 pmid: 20505359
94	Proikas-CezanneT, WaddellS, GaugelA, FrickeyT, LupasA, NordheimA (2004). WIPI-1alpha (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene, 23(58): 9314–9325 doi: 10.1038/sj.onc.1208331 pmid: 15602573
95	PuriC, RennaM, BentoC F, MoreauK, RubinszteinD C (2013). Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell, 154(6): 1285–1299 doi: 10.1016/j.cell.2013.08.044 pmid: 24034251
96	RagusaM J, StanleyR E, HurleyJ H (2012). Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell, 151(7): 1501–1512 doi: 10.1016/j.cell.2012.11.028 pmid: 23219485
97	RavikumarB, MoreauK, JahreissL, PuriC, RubinszteinD C (2010). Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol, 12(8): 747–757 doi: 10.1038/ncb2078 pmid: 20639872
98	ReggioriF, KlionskyD J (2013). Autophagic processes in yeast: mechanism, machinery and regulation. Genetics, 194(2): 341–361 doi: 10.1534/genetics.112.149013 pmid: 23733851
99	ReggioriF, TuckerK A, StromhaugP E, KlionskyD J (2004). The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell, 6(1): 79–90 doi: 10.1016/S1534-5807(03)00402-7 pmid: 14723849
100	RennerL D, WeibelD B (2011). Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci USA, 108(15): 6264–6269 doi: 10.1073/pnas.1015757108 pmid: 21444798
101	RieterE, VinkeF, BakulaD, CebolleroE, UngermannC, Proikas-CezanneT, ReggioriF (2013). Atg18 function in autophagy is regulated by specific sites within its β-propeller. J Cell Sci, 126(Pt 2): 593–604 doi: 10.1242/jcs.115725 pmid: 23230146
102	SattlerM, LiangH, NettesheimD, MeadowsR P, HarlanJ E, EberstadtM, YoonH S, ShukerS B, ChangB S, MinnA J, ThompsonC B, FesikS W (1997). Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science, 275: 983–986
102	SatooK, NodaN N, KumetaH, FujiokaY, MizushimaN, OhsumiY, InagakiF (2009). The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy. EMBO J, 28(9): 1341–1350 doi: 10.1038/emboj.2009.80 pmid: 19322194
103	SchwartenM, StoldtM, MohrlüderJ, WillboldD (2010). Solution structure of Atg8 reveals conformational polymorphism of the N-terminal domain. Biochem Biophys Res Commun, 395(3): 426–431 doi: 10.1016/j.bbrc.2010.04.043 pmid: 20382112
104	SeglenP O, GordonP B (1982). 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA, 79(6): 1889–1892 doi: 10.1073/pnas.79.6.1889 pmid: 6952238
105	SekitoT, KawamataT, IchikawaR, SuzukiK, OhsumiY (2009). Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells, 14(5): 525–538 doi: 10.1111/j.1365-2443.2009.01299.x pmid: 19371383
106	SironiL, MapelliM, KnappS, De AntoniA, JeangK T, MusacchioA (2002). Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a ‘safety belt’ binding mechanism for the spindle checkpoint. EMBO J, 21(10): 2496–2506 doi: 10.1093/emboj/21.10.2496 pmid: 12006501
107	StrϕmhaugP E, ReggioriF, GuanJ, WangC W, KlionskyD J (2004). Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol Biol Cell, 15(8): 3553–3566 doi: 10.1091/mbc.E04-02-0147 pmid: 15155809
108	SugawaraK, SuzukiN N, FujiokaY, MizushimaN, OhsumiY, InagakiF (2004). The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8. Genes Cells, 9(7): 611–618 doi: 10.1111/j.1356-9597.2004.00750.x pmid: 15265004
109	SugawaraK, SuzukiN N, FujiokaY, MizushimaN, OhsumiY, InagakiF (2005). Structural basis for the specificity and catalysis of human Atg4B responsible for mammalian autophagy. J Biol Chem, 280(48): 40058–40065 doi: 10.1074/jbc.M509158200 pmid: 16183633
110	SunL L, LiM, SuoF, LiuX M, ShenE Z, YangB, DongM Q, HeW Z, DuL L (2013). Global analysis of fission yeast mating genes reveals new autophagy factors. PLoS Genet, 9(8): e1003715 doi: 10.1371/journal.pgen.1003715 pmid: 23950735
111	SuzukiK (2013). Selective autophagy in budding yeast. Cell Death Differ, 20(1): 43–48 doi: 10.1038/cdd.2012.73 pmid: 22705847
112	SuzukiK, KubotaY, SekitoT, OhsumiY (2007). Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells, 12(2): 209–218 doi: 10.1111/j.1365-2443.2007.01050.x pmid: 17295840
113	SuzukiK, OhsumiY (2007). Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett, 581(11): 2156–2161 doi: 10.1016/j.febslet.2007.01.096 pmid: 17382324
114	SuzukiN N, YoshimotoK, FujiokaY, OhsumiY, InagakiF (2005). The crystal structure of plant ATG12 and its biological implication in autophagy. Autophagy, 1(2): 119–126 doi: 10.4161/auto.1.2.1859 pmid: 16874047
115	TaherbhoyA M, TaitS W, KaiserS E, WilliamsA H, DengA, NourseA, HammelM, KurinovI, RockC O, GreenD R, SchulmanB A (2011). Atg8 transfer from Atg7 to Atg3: a distinctive E1-E2 architecture and mechanism in the autophagy pathway. Mol Cell, 44(3): 451–461 doi: 10.1016/j.molcel.2011.08.034 pmid: 22055190
116	TakeshigeK, BabaM, TsuboiS, NodaT, OhsumiY (1992). Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol, 119(2): 301–311 doi: 10.1083/jcb.119.2.301 pmid: 1400575
117	TsukadaM, OhsumiY (1993). Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett, 333(1-2): 169–174 doi: 10.1016/0014-5793(93)80398-E pmid: 8224160
118	WatanabeY, KobayashiT, YamamotoH, HoshidaH, AkadaR, InagakiF, OhsumiY, NodaN N (2012). Structure-based analyses reveal distinct binding sites for Atg2 and phosphoinositides in Atg18. J Biol Chem, 287(38): 31681–31690 doi: 10.1074/jbc.M112.397570 pmid: 22851171
119	WeidbergH, ShpilkaT, ShvetsE, AbadaA, ShimronF, ElazarZ (2011a). LC3 and GATE-16 N termini mediate membrane fusion processes required for autophagosome biogenesis. Dev Cell, 20(4): 444–454 doi: 10.1016/j.devcel.2011.02.006 pmid: 21497758
120	WeidbergH, ShvetsE, ElazarZ (2011b). Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem, 80(1): 125–156 doi: 10.1146/annurev-biochem-052709-094552 pmid: 21548784
121	WeidbergH, ShvetsE, ShpilkaT, ShimronF, ShinderV, ElazarZ (2010). LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J, 29(11): 1792–1802 doi: 10.1038/emboj.2010.74 pmid: 20418806
122	WuY T, TanH L, ShuiG, BauvyC, HuangQ, WenkM R, OngC N, CodognoP, ShenH M (2010). Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem, 285(14): 10850–10861 doi: 10.1074/jbc.M109.080796 pmid: 20123989
123	XieZ, NairU, KlionskyD J (2008). Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell, 19(8): 3290–3298 doi: 10.1091/mbc.E07-12-1292 pmid: 18508918
124	YamadaY, SuzukiN N, HanadaT, IchimuraY, KumetaH, FujiokaY, OhsumiY, InagakiF (2007). The crystal structure of Atg3, an autophagy-related ubiquitin carrier protein (E2) enzyme that mediates Atg8 lipidation. J Biol Chem, 282(11): 8036–8043 doi: 10.1074/jbc.M611473200 pmid: 17227760
125	YamaguchiM, MatobaK, SawadaR, FujiokaY, NakatogawaH, YamamotoH, KobashigawaY, HoshidaH, AkadaR, OhsumiY, NodaN N, InagakiF (2012a). Noncanonical recognition and UBL loading of distinct E2s by autophagy-essential Atg7. Nat Struct Mol Biol, 19(12): 1250–1256 doi: 10.1038/nsmb.2451 pmid: 23142983
126	YamaguchiM, NodaN N, NakatogawaH, KumetaH, OhsumiY, InagakiF (2010). Autophagy-related protein 8 (Atg8) family interacting motif in Atg3 mediates the Atg3-Atg8 interaction and is crucial for the cytoplasm-to-vacuole targeting pathway. J Biol Chem, 285(38): 29599–29607 doi: 10.1074/jbc.M110.113670 pmid: 20615880
127	YamaguchiM, NodaN N, YamamotoH, ShimaT, KumetaH, KobashigawaY, AkadaR, OhsumiY, InagakiF (2012b). Structural insights into Atg10-mediated formation of the autophagy-essential Atg12-Atg5 conjugate. Structure, 20(7): 1244–1254 doi: 10.1016/j.str.2012.04.018 pmid: 22682742
128	YamamotoH, KakutaS, WatanabeT M, KitamuraA, SekitoT, Kondo-KakutaC, IchikawaR, KinjoM, OhsumiY (2012). Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol, 198(2): 219–233 doi: 10.1083/jcb.201202061 pmid: 22826123
129	Ylä-AnttilaP, VihinenH, JokitaloE, EskelinenE L (2009). 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy, 5(8): 1180–1185 doi: 10.4161/auto.5.8.10274 pmid: 19855179
130	YuZ Q, NiT, HongB, WangH Y, JiangF J, ZouS, ChenY, ZhengX L, KlionskyD J, LiangY, XieZ (2012). Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy, 8(6): 1–10 doi: 10.4161/auto.19652 pmid: 22082964
131	ZhongY, WangQ J, LiX, YanY, BackerJ M, ChaitB T, HeintzN, YueZ (2009). Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol, 11(4): 468–476 doi: 10.1038/ncb1854 pmid: 19270693
132	ChewL H, SetiaputraD, KlionskyD J, YipC K (2013). Structural characterization of the Saccharomyces cerevisiae autophagy regulatory complex Atg17-Atg31-Atg29. Autophagy, 9: 1467–1474
133	KabeyaY, MizushimaN, UenoT, YamamotoA, KirisakoT, NodaT, KominamiE, OhsumiY, YoshimoriT (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J, 19: 5720–5728
134	LipatovaZ, BelogortsevaN, ZhangX Q, KimJ, TaussigD, SegevN (2012). Regulation of selective autophagy onset by a Ypt/Rab GTPase module. Proc Natl Acad Sci U S A, 109: 6981–6986
135	PetrosA M, NettesheimD G, WangY, OlejniczakE T, MeadowsR P, MackJ, SwiftK, MatayoshiE D, ZhangH, ThompsonC B, FesikS W (2010). Rationale for Bcl-xL/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci, 9: 2528–2534
136	RomanovJ, WalczakM, IbiricuI, SchüchnerS, OgrisE, KraftC, MartensS (2012). Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J, 31: 4304–4317 doi: 10.1038/emboj.2009.80 pmid: 19322194
138	YehY Y, ShahK H, ChouC C, HsiaoH H, WrasmanK M, StephanJ S, StamatakosD, KhooK H, HermanP K (2011). The identification and analysis of phosphorylation sites on the Atg1 protein kinase. Autophagy, 7: 716–726

[1]	Yanan Sun,Jie Yang,Zhenyi Ma. Functions of the adaptor protein p66^Shc in solid tumors[J]. Front. Biol., 2015, 10(6): 487-494.
[2]	Altea Rocchi,Congcong He. Emerging roles of autophagy in metabolism and metabolic disorders[J]. Front. Biol., 2015, 10(2): 154-164.
[3]	Noor GAMMOH,Simon WILKINSON. Autophagy in cancer biology and therapy[J]. Front. Biol., 2014, 9(1): 35-50.
[4]	Xiaoyan LIU, Jozsef GAL, Haining ZHU. Sequestosome 1/p62: a multi-domain protein with multi-faceted functions[J]. Front Biol, 2012, 7(3): 189-201.
[5]	Hongya HAN, Lishu ZHANG, Xinxian DAI, Yanpeng ZHENG. Cross-talking between autophagy and viral infection in mammalian cells[J]. Front Biol, 2010, 5(6): 507-515.

Viewed

Full text

Abstract

Cited

Shared

Discussed