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Loss of a membrane trafficking protein αSNAP induces non-canonical autophagy in human epithelia

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Pages 4613-4625 | Published online: 27 Nov 2012

References

  • Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290:1717 - 21; http://dx.doi.org/10.1126/science.290.5497.1717; PMID: 11099404
  • Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102 - 9; http://dx.doi.org/10.1038/ncb1007-1102; PMID: 17909521
  • Denton D, Nicolson S, Kumar S. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ 2012; 19:87 - 95; http://dx.doi.org/10.1038/cdd.2011.146; PMID: 22052193
  • Dupont N, Jiang S, Pilli M, Ornatowski W, Bhattacharya D, Deretic V. Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. EMBO J 2011; 30:4701 - 11; http://dx.doi.org/10.1038/emboj.2011.398; PMID: 22068051
  • Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev 2010; 90:1383 - 435; http://dx.doi.org/10.1152/physrev.00030.2009; PMID: 20959619
  • Weidberg H, Shvets E, Elazar Z. Biogenesis and cargo selectivity of autophagosomes. Annu Rev Biochem 2011; 80:125 - 56; http://dx.doi.org/10.1146/annurev-biochem-052709-094552; PMID: 21548784
  • Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10:458 - 67; http://dx.doi.org/10.1038/nrm2708; PMID: 19491929
  • Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 2008; 90:313 - 23; http://dx.doi.org/10.1016/j.biochi.2007.08.014; PMID: 17928127
  • Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 2010; 12:747 - 57; http://dx.doi.org/10.1038/ncb2078; PMID: 20639872
  • Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 2008; 182:685 - 701; http://dx.doi.org/10.1083/jcb.200803137; PMID: 18725538
  • Chua CE, Gan BQ, Tang BL. Involvement of members of the Rab family and related small GTPases in autophagosome formation and maturation. Cell Mol Life Sci 2011; 68:3349 - 58; http://dx.doi.org/10.1007/s00018-011-0748-9; PMID: 21687989
  • Ohashi Y, Munro S. Membrane delivery to the yeast autophagosome from the Golgi-endosomal system. Mol Biol Cell 2010; 21:3998 - 4008; http://dx.doi.org/10.1091/mbc.E10-05-0457; PMID: 20861302
  • Orsi A, Polson HE, Tooze SA. Membrane trafficking events that partake in autophagy. Curr Opin Cell Biol 2010; 22:150 - 6; http://dx.doi.org/10.1016/j.ceb.2009.11.013; PMID: 20036114
  • Takahashi Y, Meyerkord CL, Hori T, Runkle K, Fox TE, Kester M, et al. Bif-1 regulates Atg9 trafficking by mediating the fission of Golgi membranes during autophagy. Autophagy 2011; 7:61 - 73; http://dx.doi.org/10.4161/auto.7.1.14015; PMID: 21068542
  • Tooze SA, Yoshimori T. The origin of the autophagosomal membrane. Nat Cell Biol 2010; 12:831 - 5; http://dx.doi.org/10.1038/ncb0910-831; PMID: 20811355
  • Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151 - 75; PMID: 18188003
  • Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007; 3:542 - 5; PMID: 17611390
  • Mari M, Tooze SA, Reggiori F. The puzzling origin of the autophagosomal membrane. F1000 Biol Rep 2011; 3:25; http://dx.doi.org/10.3410/B3-25; PMID: 22162728
  • Tooze SA, Jefferies HB, Kalie E, Longatti A, McAlpine FE, McKnight NC, et al. Trafficking and signaling in mammalian autophagy. IUBMB Life 2010; 62:503 - 8; http://dx.doi.org/10.1002/iub.334; PMID: 20552641
  • Hong W. SNAREs and traffic. Biochim Biophys Acta 2005; 1744:120 - 44; http://dx.doi.org/10.1016/j.bbamcr.2005.03.014; PMID: 15893389
  • Malsam J, Kreye S, Söllner TH. Membrane fusion: SNAREs and regulation. Cell Mol Life Sci 2008; 65:2814 - 32; http://dx.doi.org/10.1007/s00018-008-8352-3; PMID: 18726177
  • Ungar D, Hughson FM. SNARE protein structure and function. Annu Rev Cell Dev Biol 2003; 19:493 - 517; http://dx.doi.org/10.1146/annurev.cellbio.19.110701.155609; PMID: 14570579
  • Fader CM, Sánchez DG, Mestre MB, Colombo MI. TI-VAMP/VAMP7 and VAMP3/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim Biophys Acta 2009; 1793:1901 - 16; http://dx.doi.org/10.1016/j.bbamcr.2009.09.011; PMID: 19781582
  • Furuta N, Fujita N, Noda T, Yoshimori T, Amano A. Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes. Mol Biol Cell 2010; 21:1001 - 10; http://dx.doi.org/10.1091/mbc.E09-08-0693; PMID: 20089838
  • Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein DC. Autophagosome precursor maturation requires homotypic fusion. Cell 2011; 146:303 - 17; http://dx.doi.org/10.1016/j.cell.2011.06.023; PMID: 21784250
  • Renna M, Schaffner C, Winslow AR, Menzies FM, Peden AA, Floto RA, et al. Autophagic substrate clearance requires activity of the syntaxin-5 SNARE complex. J Cell Sci 2011; 124:469 - 82; http://dx.doi.org/10.1242/jcs.076489; PMID: 21242315
  • Andreeva AV, Kutuzov MA, Voyno-Yasenetskaya TA. A ubiquitous membrane fusion protein α SNAP: a potential therapeutic target for cancer, diabetes and neurological disorders?. Expert Opin Ther Targets 2006; 10:723 - 33; http://dx.doi.org/10.1517/14728222.10.5.723; PMID: 16981829
  • Burgoyne RD, Morgan A. Analysis of regulated exocytosis in adrenal chromaffin cells: insights into NSF/SNAP/SNARE function. Bioessays 1998; 20:328 - 35; http://dx.doi.org/10.1002/(SICI)1521-1878(199804)20:4<328::AID-BIES9>3.0.CO;2-L; PMID: 9619104
  • Whiteheart SW, Schraw T, Matveeva EA. N-ethylmaleimide sensitive factor (NSF) structure and function. Int Rev Cytol 2001; 207:71 - 112; http://dx.doi.org/10.1016/S0074-7696(01)07003-6; PMID: 11352269
  • Naydenov NG, Brown B, Harris G, Dohn MR, Morales VM, Baranwal S, et al. A membrane fusion protein αSNAP is a novel regulator of epithelial apical junctions. PLoS One 2012; 7:e34320; http://dx.doi.org/10.1371/journal.pone.0034320; PMID: 22485163
  • Naydenov NG, Harris G, Brown B, Schaefer KL, Das SK, Fisher PB, et al. Loss of soluble N-ethylmaleimide-sensitive factor attachment protein α (αSNAP) induces epithelial cell apoptosis via down-regulation of Bcl-2 expression and disruption of the Golgi. J Biol Chem 2012; 287:5928 - 41; http://dx.doi.org/10.1074/jbc.M111.278358; PMID: 22194596
  • Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, Yen WL, et al. SNARE proteins are required for macroautophagy. Cell 2011; 146:290 - 302; http://dx.doi.org/10.1016/j.cell.2011.06.022; PMID: 21784249
  • Le Bivic A, Real FX, Rodriguez-Boulan E. Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line. Proc Natl Acad Sci USA 1989; 86:9313 - 7; http://dx.doi.org/10.1073/pnas.86.23.9313; PMID: 2687880
  • Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452:181 - 97; http://dx.doi.org/10.1016/S0076-6879(08)03612-4; PMID: 19200883
  • He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67 - 93; http://dx.doi.org/10.1146/annurev-genet-102808-114910; PMID: 19653858
  • Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 2009; 461:654 - 8; http://dx.doi.org/10.1038/nature08455; PMID: 19794493
  • Geng J, Nair U, Yasumura-Yorimitsu K, Klionsky DJ. Post-Golgi Sec proteins are required for autophagy in Saccharomyces cerevisiae. Mol Biol Cell 2010; 21:2257 - 69; http://dx.doi.org/10.1091/mbc.E09-11-0969; PMID: 20444978
  • Guo Y, Chang C, Huang R, Liu B, Bao L, Liu W. AP1 is essential for generation of autophagosomes from the trans-Golgi network. J Cell Sci 2012; 125:1706 - 15; http://dx.doi.org/10.1242/jcs.093203; PMID: 22328508
  • van der Vaart A, Griffith J, Reggiori F. Exit from the Golgi is required for the expansion of the autophagosomal phagophore in yeast Saccharomyces cerevisiae. Mol Biol Cell 2010; 21:2270 - 84; http://dx.doi.org/10.1091/mbc.E09-04-0345; PMID: 20444982
  • Jackson CL. Brefeldin A revealing the fundamental principles governing membrane dynamics and protein transport. Subcell Biochem 2000; 34:233 - 72; http://dx.doi.org/10.1007/0-306-46824-7_6; PMID: 10808335
  • Sáenz JB, Sun WJ, Chang JW, Li J, Bursulaya B, Gray NS, et al. Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat Chem Biol 2009; 5:157 - 65; http://dx.doi.org/10.1038/nchembio.144; PMID: 19182783
  • Kawamoto K, Yoshida Y, Tamaki H, Torii S, Shinotsuka C, Yamashina S, et al. GBF1, a guanine nucleotide exchange factor for ADP-ribosylation factors, is localized to the cis-Golgi and involved in membrane association of the COPI coat. Traffic 2002; 3:483 - 95; http://dx.doi.org/10.1034/j.1600-0854.2002.30705.x; PMID: 12047556
  • Morinaga N, Tsai SC, Moss J, Vaughan M. Isolation of a brefeldin A-inhibited guanine nucleotide-exchange protein for ADP ribosylation factor (ARF) 1 and ARF3 that contains a Sec7-like domain. Proc Natl Acad Sci USA 1996; 93:12856 - 60; http://dx.doi.org/10.1073/pnas.93.23.12856; PMID: 8917509
  • Niu TK, Pfeifer AC, Lippincott-Schwartz J, Jackson CL. Dynamics of GBF1, a Brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol Biol Cell 2005; 16:1213 - 22; http://dx.doi.org/10.1091/mbc.E04-07-0599; PMID: 15616190
  • Nakajima K, Hirose H, Taniguchi M, Kurashina H, Arasaki K, Nagahama M, et al. Involvement of BNIP1 in apoptosis and endoplasmic reticulum membrane fusion. EMBO J 2004; 23:3216 - 26; http://dx.doi.org/10.1038/sj.emboj.7600333; PMID: 15272311
  • Verrier SE, Willmann M, Wenzel D, Winter U, von Mollard GF, Söling HD. Members of a mammalian SNARE complex interact in the endoplasmic reticulum in vivo and are found in COPI vesicles. Eur J Cell Biol 2008; 87:863 - 78; http://dx.doi.org/10.1016/j.ejcb.2008.07.003; PMID: 18834646
  • Tang F, Wang B, Li N, Wu Y, Jia J, Suo T, et al. RNF185, a novel mitochondrial ubiquitin E3 ligase, regulates autophagy through interaction with BNIP1. PLoS One 2011; 6:e24367; http://dx.doi.org/10.1371/journal.pone.0024367; PMID: 21931693
  • Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 2008; 9:1004 - 10; http://dx.doi.org/10.1038/nrm2529; PMID: 18971948
  • Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8:741 - 52; http://dx.doi.org/10.1038/nrm2239; PMID: 17717517
  • Hirota Y, Tanaka Y. A small GTPase, human Rab32, is required for the formation of autophagic vacuoles under basal conditions. Cell Mol Life Sci 2009; 66:2913 - 32; http://dx.doi.org/10.1007/s00018-009-0080-9; PMID: 19593531
  • Codogno P, Mehrpour M, Proikas-Cezanne T. Canonical and non-canonical autophagy: variations on a common theme of self-eating?. Nat Rev Mol Cell Biol 2012; 13:7 - 12; PMID: 22166994
  • Seo G, Kim SK, Byun YJ, Oh E, Jeong SW, Chae GT, et al. Hydrogen peroxide induces Beclin 1-independent autophagic cell death by suppressing the mTOR pathway via promoting the ubiquitination and degradation of Rheb in GSH-depleted RAW 264.7 cells. Free Radic Res 2011; 45:389 - 99; http://dx.doi.org/10.3109/10715762.2010.535530; PMID: 21067284
  • Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ 2008; 15:1318 - 29; http://dx.doi.org/10.1038/cdd.2008.51; PMID: 18421301
  • Zhu JH, Horbinski C, Guo F, Watkins S, Uchiyama Y, Chu CT. Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am J Pathol 2007; 170:75 - 86; http://dx.doi.org/10.2353/ajpath.2007.060524; PMID: 17200184
  • Mestre MB, Fader CM, Sola C, Colombo MI. α-hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus-infected cells. Autophagy 2010; 6:110 - 25; http://dx.doi.org/10.4161/auto.6.1.10698; PMID: 20110774
  • Yen WL, Shintani T, Nair U, Cao Y, Richardson BC, Li Z, et al. The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J Cell Biol 2010; 188:101 - 14; http://dx.doi.org/10.1083/jcb.200904075; PMID: 20065092
  • Zoppino FC, Militello RD, Slavin I, Alvarez C, Colombo MI. Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 2010; 11:1246 - 61; http://dx.doi.org/10.1111/j.1600-0854.2010.01086.x; PMID: 20545908
  • Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 2008; 19:2916 - 25; http://dx.doi.org/10.1091/mbc.E07-12-1231; PMID: 18448665
  • Young AR, Chan EY, Hu XW, Köchl R, Crawshaw SG, High S, et al. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006; 119:3888 - 900; http://dx.doi.org/10.1242/jcs.03172; PMID: 16940348
  • Martin HG, Henley JM, Meyer G. Novel putative targets of N-ethylmaleimide sensitive fusion protein (NSF) and α/β soluble NSF attachment proteins (SNAPs) include the Pak-binding nucleotide exchange factor betaPIX. J Cell Biochem 2006; 99:1203 - 15; http://dx.doi.org/10.1002/jcb.20998; PMID: 16795052
  • Rabouille C, Kondo H, Newman R, Hui N, Freemont P, Warren G. Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell 1998; 92:603 - 10; http://dx.doi.org/10.1016/S0092-8674(00)81128-9; PMID: 9506515
  • Aoki T, Kojima M, Tani K, Tagaya M. Sec22b-dependent assembly of endoplasmic reticulum Q-SNARE proteins. Biochem J 2008; 410:93 - 100; http://dx.doi.org/10.1042/BJ20071304; PMID: 17979832
  • Jahn R, Scheller RH. SNAREs--engines for membrane fusion. Nat Rev Mol Cell Biol 2006; 7:631 - 43; http://dx.doi.org/10.1038/nrm2002; PMID: 16912714
  • Donaldson JG, Honda A. Localization and function of Arf family GTPases. Biochem Soc Trans 2005; 33:639 - 42; http://dx.doi.org/10.1042/BST0330639; PMID: 16042562
  • Gillingham AK, Munro S. The small G proteins of the Arf family and their regulators. Annu Rev Cell Dev Biol 2007; 23:579 - 611; http://dx.doi.org/10.1146/annurev.cellbio.23.090506.123209; PMID: 17506703
  • Li L, Kim E, Yuan H, Inoki K, Goraksha-Hicks P, Schiesher RL, et al. Regulation of mTORC1 by the Rab and Arf GTPases. J Biol Chem 2010; 285:19705 - 9; http://dx.doi.org/10.1074/jbc.C110.102483; PMID: 20457610
  • Balakumaran BS, Porrello A, Hsu DS, Glover W, Foye A, Leung JY, et al. MYC activity mitigates response to rapamycin in prostate cancer through eukaryotic initiation factor 4E-binding protein 1-mediated inhibition of autophagy. Cancer Res 2009; 69:7803 - 10; http://dx.doi.org/10.1158/0008-5472.CAN-09-0910; PMID: 19773438
  • Ishihara N, Hamasaki M, Yokota S, Suzuki K, Kamada Y, Kihara A, et al. Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 2001; 12:3690 - 702; PMID: 11694599
  • Campoy E, Colombo MI. Autophagy in intracellular bacterial infection. Biochim Biophys Acta 2009; 1793:1465 - 77; http://dx.doi.org/10.1016/j.bbamcr.2009.03.003; PMID: 19303905
  • Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009; 5:527 - 49; http://dx.doi.org/10.1016/j.chom.2009.05.016; PMID: 19527881
  • Pierini R, Cottam E, Roberts R, Wileman T. Modulation of membrane traffic between endoplasmic reticulum, ERGIC and Golgi to generate compartments for the replication of bacteria and viruses. Semin Cell Dev Biol 2009; 20:828 - 33; http://dx.doi.org/10.1016/j.semcdb.2009.03.015; PMID: 19508853
  • Salcedo SP, Holden DW. Bacterial interactions with the eukaryotic secretory pathway. Curr Opin Microbiol 2005; 8:92 - 8; http://dx.doi.org/10.1016/j.mib.2004.12.007; PMID: 15694862
  • Chae TH, Kim S, Marz KE, Hanson PI, Walsh CA. The hyh mutation uncovers roles for α Snap in apical protein localization and control of neural cell fate. Nat Genet 2004; 36:264 - 70; http://dx.doi.org/10.1038/ng1302; PMID: 14758363
  • Ivanov AI, Bachar M, Babbin BA, Adelstein RS, Nusrat A, Parkos CA. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS One 2007; 2:e658; http://dx.doi.org/10.1371/journal.pone.0000658; PMID: 17668046
  • Ivanov AI, Young C, Den Beste K, Capaldo CT, Humbert PO, Brennwald P, et al. Tumor suppressor scribble regulates assembly of tight junctions in the intestinal epithelium. Am J Pathol 2010; 176:134 - 45; http://dx.doi.org/10.2353/ajpath.2010.090220; PMID: 19959811
  • Naydenov NG, Ivanov AI. Adducins regulate remodeling of apical junctions in human epithelial cells. Mol Biol Cell 2010; 21:3506 - 17; http://dx.doi.org/10.1091/mbc.E10-03-0259; PMID: 20810786

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