Disruption of the vacuolar-type H⁺-ATPase complex in liver causes MTORC1-independent accumulation of autophagic vacuoles and lysosomes

References

• Feng Y, Yao Z, Klionsky DJ. How to control self-digestion: transcriptional, post-transcriptional, and post-translational regulation of autophagy. Trends Cell Biol 2015; 25:354-63; PMID:25759175; http://dx.doi.org/10.1016/j.tcb.2015.02.002
   PubMed Web of Science ®Google Scholar
• Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 1994; 369:756-8; PMID:8008069; http://dx.doi.org/10.1038/369756a0
   PubMed Web of Science ®Google Scholar
• Sabatini DM, Erdjument-Bromage H, Lui M, Tempst P, Snyder SH. RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 1994; 78:35-43; PMID:7518356; http://dx.doi.org/10.1016/0092-8674(94)90570-3
   PubMed Web of Science ®Google Scholar
• Sabers CJ, Martin MM, Brunn GJ, Williams JM, Dumont FJ, Wiederrecht G, Abraham RT. Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells. J Biol Chem 1995; 270:815-22; PMID:7822316; http://dx.doi.org/10.1074/jbc.270.2.815
   PubMed Web of Science ®Google Scholar
• Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149:274-93; PMID:22500797; http://dx.doi.org/10.1016/j.cell.2012.03.017
   PubMed Web of Science ®Google Scholar
• Dazert E, Hall MN. mTOR signaling in disease. Curr Opin Cell Biol 2011; 23:744-55; PMID:21963299; http://dx.doi.org/10.1016/j.ceb.2011.09.003
   PubMed Web of Science ®Google Scholar
• Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992-2003; PMID:19225151; http://dx.doi.org/10.1091/mbc.E08-12-1249
   PubMed Web of Science ®Google Scholar
• Ganley IG, Lam du H, Wang J, Ding X, Chen S, Jiang X. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284:12297-305; PMID:19258318; http://dx.doi.org/10.1074/jbc.M900573200
   PubMed Web of Science ®Google Scholar
• Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20:1981-91; PMID:19211835; http://dx.doi.org/10.1091/mbc.E08-12-1248
   PubMed Web of Science ®Google Scholar
• Dibble CC, Manning BD. Signal integration by mTORC1 coordinates nutrient input with biosynthetic output. Nat Cell Biol 2013; 15:555-64; PMID:23728461; http://dx.doi.org/10.1038/ncb2763
   PubMed Web of Science ®Google Scholar
• Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, Ballabio A. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 2011; 20:3852-66; PMID:21752829; http://dx.doi.org/10.1093/hmg/ddr306
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, et al. TFEB links autophagy to lysosomal biogenesis. Science 2011; 332:1429-33; PMID:21617040; http://dx.doi.org/10.1126/science.1204592
   PubMed Web of Science ®Google Scholar
• Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J 2012; 31:1095-108; PMID:22343943; http://dx.doi.org/10.1038/emboj.2012.32
   PubMed Web of Science ®Google Scholar
• Martina JA, Chen Y, Gucek M, Puertollano R. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy 2012; 8:903-14; PMID:22576015; http://dx.doi.org/10.4161/auto.19653
   PubMed Web of Science ®Google Scholar
• Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J, Angarola B, Walther TC, Ferguson SM. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 2012; 5:ra42; PMID:22692423; http://dx.doi.org/10.1126/scisignal.2002790
   PubMed Web of Science ®Google Scholar
• Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 2011; 334:678-83; PMID:22053050; http://dx.doi.org/10.1126/science.1207056
   PubMed Web of Science ®Google Scholar
• Jewell JL, Kim YC, Russell RC, Yu FX, Park HW, Plouffe SW, Tagliabracci VS, Guan KL. Metabolism. Differential regulation of mTORC1 by leucine and glutamine. Science 2015; 347:194-8.
   Google Scholar
• Rebsamen M, Pochini L, Stasyk T, de Araujo ME, Galluccio M, Kandasamy RK, Snijder B, Fauster A, Rudashevskaya EL, Bruckner M, et al. SLC38A9 is a component of the lysosomal amino acid sensing machinery that controls mTORC1. Nature 2015; 519:477-81; PMID:25561175; http://dx.doi.org/10.1038/nature14107
   PubMed Web of Science ®Google Scholar
• Wang S, Tsun ZY, Wolfson RL, Shen K, Wyant GA, Plovanich ME, Yuan ED, Jones TD, Chantranupong L, Comb W, et al. Metabolism. Lysosomal amino acid transporter SLC38A9 signals arginine sufficiency to mTORC1. Science 2015; 347:188-94.
   PubMed Web of Science ®Google Scholar
• Bar-Peled L, Sabatini DM. Regulation of mTORC1 by amino acids. Trends Cell Biol 2014; 24:400-6; PMID:24698685; http://dx.doi.org/10.1016/j.tcb.2014.03.003
   PubMed Web of Science ®Google Scholar
• Saucedo LJ, Gao X, Chiarelli DA, Li L, Pan D, Edgar BA. Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat Cell Biol 2003; 5:566-71; PMID:12766776; http://dx.doi.org/10.1038/ncb996
   PubMed Web of Science ®Google Scholar
• Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, Daram P, Breuer S, Thomas G, Hafen E. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat Cell Biol 2003; 5:559-65; PMID:12766775; http://dx.doi.org/10.1038/ncb995
   PubMed Web of Science ®Google Scholar
• Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. Rheb binds and regulates the mTOR kinase. Curr Biol 2005; 15:702-13; PMID:15854902; http://dx.doi.org/10.1016/j.cub.2005.02.053
   PubMed Web of Science ®Google Scholar
• Toei M, Saum R, Forgac M. Regulation and isoform function of the V-ATPases. Biochemistry 2010; 49:4715-23; PMID:20450191; http://dx.doi.org/10.1021/bi100397s
   PubMed Web of Science ®Google Scholar
• Cotter K, Stransky L, McGuire C, Forgac M. Recent Insights into the Structure, Regulation, and Function of the V-ATPases. Trends Biochem Sci 2015; 40:611-22; PMID:26410601; http://dx.doi.org/10.1016/j.tibs.2015.08.005
   PubMed Web of Science ®Google Scholar
• Kinouchi K, Ichihara A, Sano M, Sun-Wada GH, Wada Y, Kurauchi-Mito A, Bokuda K, Narita T, Oshima Y, Sakoda M, et al. The (pro)renin receptor/ATP6AP2 is essential for vacuolar H+-ATPase assembly in murine cardiomyocytes. Circ Res 2010; 107:30-4;PMID:20570919;http://dx.doi.org/10.1161/CIRCRESAHA.110.224667
   PubMed Web of Science ®Google Scholar
• Oshima Y, Kinouchi K, Ichihara A, Sakoda M, Kurauchi-Mito A, Bokuda K, Narita T, Kurosawa H, Sun-Wada GH, Wada Y, et al. Prorenin receptor is essential for normal podocyte structure and function. J Am Soc Nephrol 2011; 22:2203-12; PMID:22052048; http://dx.doi.org/10.1681/ASN.2011020202
   PubMed Web of Science ®Google Scholar
• Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V, et al. Prorenin receptor is essential for podocyte autophagy and survival. J Am Soc Nephrol 2011; 22:2193-202; PMID:22034640; http://dx.doi.org/10.1681/ASN.2011020200
   PubMed Web of Science ®Google Scholar
• Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 2010; 141:290-303; PMID:20381137; http://dx.doi.org/10.1016/j.cell.2010.02.024
   PubMed Web of Science ®Google Scholar
• Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, Wolff NC, Tran TA, Zou L, Xie XJ, Corey DR, Brugarolas J. Regulation of TFEB and V-ATPases by mTORC1. EMBO J 2011; 30:3242-58; PMID:21804531; http://dx.doi.org/10.1038/emboj.2011.257
   PubMed Web of Science ®Google Scholar
• Czaja MJ, Ding WX, Donohue TM, Jr., Friedman SL, Kim JS, Komatsu M, Lemasters JJ, Lemoine A, Lin JD, Ou JH, et al. Functions of autophagy in normal and diseased liver. Autophagy 2013; 9:1131-58; PMID:23774882; http://dx.doi.org/10.4161/auto.25063
   PubMed Web of Science ®Google Scholar
• Kissing S, Hermsen C, Repnik U, Nesset CK, von Bargen K, Griffiths G, Ichihara A, Lee BS, Schwake M, De Brabander J, et al. Vacuolar ATPase in phagosome-lysosome fusion. J Biol Chem 2015; 290:14166-80; PMID:25903133; http://dx.doi.org/10.1074/jbc.M114.628891
   PubMed Web of Science ®Google Scholar
• Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr SA, Sabatini DM. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 2007; 25:903-15; PMID:17386266; http://dx.doi.org/10.1016/j.molcel.2007.03.003
   PubMed Web of Science ®Google Scholar
• Liu Q, Chang JW, Wang J, Kang SA, Thoreen CC, Markhard A, Hur W, Zhang J, Sim T, Sabatini DM, et al. Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benz o[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J Med Chem 2010; 53:7146-55; PMID:20860370; http://dx.doi.org/10.1021/jm101144f
   PubMed Web of Science ®Google Scholar
• Settembre C, Ballabio A. TFEB regulates autophagy: an integrated coordination of cellular degradation and recycling processes. Autophagy 2011; 7:1379-81; PMID:21785263; http://dx.doi.org/10.4161/auto.7.11.17166
   PubMed Web of Science ®Google Scholar
• Bowman BJ, McCall ME, Baertsch R, Bowman EJ. A model for the proteolipid ring and bafilomycin/concanamycin-binding site in the vacuolar ATPase of Neurospora crassa. J Biol Chem 2006; 281:31885-93; PMID:16912037; http://dx.doi.org/10.1074/jbc.M605532200
   PubMed Web of Science ®Google Scholar
• Poea-Guyon S, Ammar MR, Erard M, Amar M, Moreau AW, Fossier P, Gleize V, Vitale N, Morel N. The V-ATPase membrane domain is a sensor of granular pH that controls the exocytotic machinery. J Cell Biol 2013; 203:283-98; PMID:24165939; http://dx.doi.org/10.1083/jcb.201303104
   PubMed Web of Science ®Google Scholar
• Wang D, Hiesinger PR. The vesicular ATPase: a missing link between acidification and exocytosis. J Cell Biol 2013; 203:171-3; PMID:24165933; http://dx.doi.org/10.1083/jcb.201309130
   PubMed Web of Science ®Google Scholar
• Xie XS, Padron D, Liao X, Wang J, Roth MG, De Brabander JK. Salicylihalamide A inhibits the V0 sector of the V-ATPase through a mechanism distinct from bafilomycin A1. J Biol Chem 2004; 279:19755-63; PMID:14998996; http://dx.doi.org/10.1074/jbc.M313796200
   PubMed Web of Science ®Google Scholar
• Dibble CC, Cantley LC. Regulation of mTORC1 by PI3K signaling. Trends Cell Biol 2015; 25:545-55; PMID:26159692; http://dx.doi.org/10.1016/j.tcb.2015.06.002
   PubMed Web of Science ®Google Scholar
• Inoki K, Li Y, Xu T, Guan KL. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 2003; 17:1829-34; PMID:12869586; http://dx.doi.org/10.1101/gad.1110003
   PubMed Web of Science ®Google Scholar
• Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003; 13:1259-68; PMID:12906785; http://dx.doi.org/10.1016/S0960-9822(03)00506-2
   PubMed Web of Science ®Google Scholar
• Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2007; 8:917-29; PMID:17912264; http://dx.doi.org/10.1038/nrm2272
   PubMed Web of Science ®Google Scholar
• Nishi T, Forgac M. The vacuolar (H+)-ATPases–nature's most versatile proton pumps. Nat Rev Mol Cell Biol 2002; 3:94-103; PMID:11836511; http://dx.doi.org/10.1038/nrm729
   PubMed Web of Science ®Google Scholar
• Vavassori S, Mayer A. A new life for an old pump: V-ATPase and neurotransmitter release. J Cell Biol 2014; 205:7-9; PMID:24733582; http://dx.doi.org/10.1083/jcb.201403040
   PubMed Web of Science ®Google Scholar
• Strasser B, Iwaszkiewicz J, Michielin O, Mayer A. The V-ATPase proteolipid cylinder promotes the lipid-mixing stage of SNARE-dependent fusion of yeast vacuoles. EMBO J 2011; 30:4126-41; PMID:21934648; http://dx.doi.org/10.1038/emboj.2011.335
   PubMed Web of Science ®Google Scholar
• Bayer MJ, Reese C, Buhler S, Peters C, Mayer A. Vacuole membrane fusion: V0 functions after trans-SNARE pairing and is coupled to the Ca2+-releasing channel. J Cell Biol 2003; 162:211-22; PMID:12876274; http://dx.doi.org/10.1083/jcb.200212004
   PubMed Web of Science ®Google Scholar
• Gu F, Gruenberg J. ARF1 regulates pH-dependent COP functions in the early endocytic pathway. J Biol Chem 2000; 275:8154-60; PMID:10713138; http://dx.doi.org/10.1074/jbc.275.11.8154
   PubMed Web of Science ®Google Scholar
• Vitavska O, Merzendorfer H, Wieczorek H. The V-ATPase subunit C binds to polymeric F-actin as well as to monomeric G-actin and induces cross-linking of actin filaments. J Biol Chem 2005; 280:1070-6; PMID:15525650; http://dx.doi.org/10.1074/jbc.M406797200
   PubMed Web of Science ®Google Scholar
• Chen SH, Bubb MR, Yarmola EG, Zuo J, Jiang J, Lee BS, Lu M, Gluck SL, Hurst IR, Holliday LS. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem 2004; 279:7988-98; PMID:14662773; http://dx.doi.org/10.1074/jbc.M305351200
   PubMed Web of Science ®Google Scholar
• Holliday LS, Lu M, Lee BS, Nelson RD, Solivan S, Zhang L, Gluck SL. The amino-terminal domain of the B subunit of vacuolar H+-ATPase contains a filamentous actin binding site. J Biol Chem 2000; 275:32331-7; PMID:10915794; http://dx.doi.org/10.1074/jbc.M004795200
   PubMed Web of Science ®Google Scholar
• Alers S, Loffler AS, Wesselborg S, Stork B. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 2012; 32:2-11; PMID:22025673; http://dx.doi.org/10.1128/MCB.06159-11
   PubMed Web of Science ®Google Scholar
• Settembre C, Medina DL. TFEB and the CLEAR network. Methods Cell Biol 2015; 126:45-62; PMID:25665440
   PubMed Web of Science ®Google Scholar
• Medina DL, Di Paola S, Peluso I, Armani A, De Stefani D, Venditti R, Montefusco S, Scotto-Rosato A, Prezioso C, Forrester A, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol 2015; 17:288-99; PMID:25720963; http://dx.doi.org/10.1038/ncb3114
   PubMed Web of Science ®Google Scholar
• Huck B, Duss S, Hausser A, Olayioye MA. Elevated protein kinase D3 (PKD3) expression supports proliferation of triple-negative breast cancer cells and contributes to mTORC1-S6K1 pathway activation. J Biol Chem 2014; 289:3138-47; PMID:24337579; http://dx.doi.org/10.1074/jbc.M113.502633
   PubMed Web of Science ®Google Scholar
• Moore SF, Hunter RW, Hers I. Protein kinase C and P2Y12 take center stage in thrombin-mediated activation of mammalian target of rapamycin complex 1 in human platelets. J Thromb Haemost 2014; 12:748-60; PMID:24612393; http://dx.doi.org/10.1111/jth.12552
   PubMed Web of Science ®Google Scholar
• Li Y, Xu M, Ding X, Yan C, Song Z, Chen L, Huang X, Wang X, Jian Y, Tang G, et al. Protein kinase C controls lysosome biogenesis independently of mTORC1. Nat Cell Biol 2016; 18:1065-77; PMID:27617930; http://dx.doi.org/10.1038/ncb3407
   PubMed Web of Science ®Google Scholar
• Dufner A, Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp Cell Res 1999; 253:100-9; PMID:10579915; http://dx.doi.org/10.1006/excr.1999.4683
   PubMed Web of Science ®Google Scholar
• Wolfson RL, Chantranupong L, Saxton RA, Shen K, Scaria SM, Cantor JR, Sabatini DM. Sestrin2 is a leucine sensor for the mTORC1 pathway. Science 2016; 351:43-8; PMID:26449471; http://dx.doi.org/10.1126/science.aab2674
   PubMed Web of Science ®Google Scholar
• Carroll B, Maetzel D, Maddocks OD, Otten G, Ratcliff M, Smith GR, Dunlop EA, Passos JF, Davies OR, Jaenisch R, et al. Control of TSC2-Rheb signaling axis by arginine regulates mTORC1 activity. Elife 2016; 5, e11058; http://dx.doi.org/10.7554/eLife.11058
   Web of Science ®Google Scholar
• Chantranupong L, Scaria SM, Saxton RA, Gygi MP, Shen K, Wyant GA, Wang T, Harper JW, Gygi SP, Sabatini DM. The CASTOR Proteins Are Arginine Sensors for the mTORC1 Pathway. Cell 2016; 165:153-64; PMID:26972053; http://dx.doi.org/10.1016/j.cell.2016.02.035
   PubMed Web of Science ®Google Scholar
• Efeyan A, Zoncu R, Chang S, Gumper I, Snitkin H, Wolfson RL, Kirak O, Sabatini DD, Sabatini DM. Regulation of mTORC1 by the Rag GTPases is necessary for neonatal autophagy and survival. Nature 2013; 493:679-83; PMID:23263183; http://dx.doi.org/10.1038/nature11745
   PubMed Web of Science ®Google Scholar
• Mahimainathan L, Das F, Venkatesan B, Choudhury GG. Mesangial cell hypertrophy by high glucose is mediated by downregulation of the tumor suppressor PTEN. Diabetes 2006; 55:2115-25; PMID:16804083; http://dx.doi.org/10.2337/db05-1326
   PubMed Web of Science ®Google Scholar
• Zheng X, Liang Y, He Q, Yao R, Bao W, Bao L, Wang Y, Wang Z. Current models of mammalian target of rapamycin complex 1 (mTORC1) activation by growth factors and amino acids. Int J Mol Sci 2014; 15:20753-69; PMID:25402640; http://dx.doi.org/10.3390/ijms151120753
   PubMed Web of Science ®Google Scholar
• Demetriades C, Plescher M, Teleman AA. Lysosomal recruitment of TSC2 is a universal response to cellular stress. Nat Commun 2016; 7:10662; PMID:26868506; http://dx.doi.org/10.1038/ncomms10662
   PubMed Web of Science ®Google Scholar
• Manolson MF, Yu H, Chen W, Yao Y, Li K, Lees RL, Heersche JN. The a3 isoform of the 100-kDa V-ATPase subunit is highly but differentially expressed in large (>or = 10 nuclei) and small (<or = nuclei) osteoclasts. J Biol Chem 2003; 278:49271-8; PMID:14504271; http://dx.doi.org/10.1074/jbc.M309914200
   PubMed Web of Science ®Google Scholar
• Mortensen RM, Zubiaur M, Neer EJ, Seidman JG. Embryonic stem cells lacking a functional inhibitory G-protein subunit (alpha i2) produced by gene targeting of both alleles. Proc Natl Acad Sci U S A 1991; 88:7036-40; PMID:1908087; http://dx.doi.org/10.1073/pnas.88.16.7036
   PubMed Web of Science ®Google Scholar
• Kowalewski B, Lubke T, Kollmann K, Braulke T, Reinheckel T, Dierks T, Damme M. Molecular characterization of arylsulfatase G: expression, processing, glycosylation, transport, and activity. J Biol Chem 2014; 289:27992-8005; PMID:25135642; http://dx.doi.org/10.1074/jbc.M114.584144
   PubMed Web of Science ®Google Scholar
• Wattiaux R, Wibo M, Baudhuin P. [Effect of the injection of Triton WR 1339 on the hepatic lysosomes of the rat]. Arch Int Physiol Biochim 1963; 71:140-2; PMID:13999241
   PubMedGoogle Scholar