Inactivation of the Caenorhabditis elegans RNF-5 E3 ligase promotes IRE-1-independent ER functions

References

• Schröder M, Kaufman RJ, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74:739–789.
   PubMed Web of Science ®Google Scholar
• Ron D, Walter P. Walter P: signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8:519.
   PubMed Web of Science ®Google Scholar
• Vembar SS, Brodsky JL. One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol. 2008;9:944.
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89–102.
   PubMed Web of Science ®Google Scholar
• Calfon M, Zeng H, Urano F, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 2002;415:92.
   PubMed Web of Science ®Google Scholar
• Gardner BM. Walter P. Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science. 2011;333:1891–1894.
   PubMed Web of Science ®Google Scholar
• Shen X, Ellis RE, Sakaki K, Kaufman RJ. Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet. 2005;1:e37.
   PubMed Web of Science ®Google Scholar
• Richardson CE, Kinkel S, Kim DH. Physiological IRE-1-XBP-1 and PEK-1 signaling in caenorhabditis elegans larval development and immunity. PLoS Genet. 2011;7:e1002391.
   PubMed Web of Science ®Google Scholar
• Safra M, Ben-Hamo S, Kenyon C Henis-Korenblit S. The ire-1 ER stress-response pathway is required for normal secretory-protein metabolism in C. elegans. J Cell Sci. 2013;126:4136–4146.
   PubMed Web of Science ®Google Scholar
• Henis-Korenblit S, Zhang P, Hansen M, et al., Insulin/IGF-1 signaling mutants reprogram ER stress response regulators to promote longevity. Proc National Academy Sci 2010, 107:9730–9735.
   PubMed Web of Science ®Google Scholar
• Roux AE, Langhans K, Huynh W. Reversible age-related phenotypes induced during larval quiescence in C. elegans. Cell Metab. 2016;23:1113–1126.
   PubMed Web of Science ®Google Scholar
• Ohsumi Y. Historical landmarks of autophagy research. Cell Res. 2013;24:9.
   PubMed Web of Science ®Google Scholar
• Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6:463–477.
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Suzuki K, Kamada Y, et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–467.
   PubMed Web of Science ®Google Scholar
• Feng Y, He D, Yao Z, et al. The machinery of macroautophagy. Cell Res. 2014;24:24–41.
   PubMed Web of Science ®Google Scholar
• Palmisano NJ, Meléndez A, et al. Autophagy in C. elegans development. Dev Biol. 2019;447:103–125.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Komatsu M, et al. Autophagy: renovation of cells and tissues. Cell. 2011;147:728–741.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–293.
   PubMed Web of Science ®Google Scholar
• Kaur J, Debnath J. Autophagy at the crossroads of catabolism and anabolism. Nat Rev Mol Cell Biol. 2015;16:461–472.
   PubMed Web of Science ®Google Scholar
• Bachar-Wikstrom E, Wikstrom JD, Kaiser N, et al. Improvement of ER stress-induced diabetes by stimulating autophagy. Autophagy. 2013;9:626–628.
   PubMed Web of Science ®Google Scholar
• Ogata M, S-I H, Saito A, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 2006;26:9220–9231.
   PubMed Web of Science ®Google Scholar
• Rzymski T, Milani M, Pike L, et al. Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene. 2010;29:4424–4435.
   PubMed Web of Science ®Google Scholar
• Song S, Tan J, Miao Y, et al. Crosstalk of ER stress-mediated autophagy and ER-phagy: involvement of UPR and the core autophagy machinery. J Cell Physiol. 2018;233:3867–3874.
   PubMed Web of Science ®Google Scholar
• Yorimitsu T, Nair U, Yang Z, et al. Endoplasmic reticulum stress triggers autophagy. J Biol Chem. 2006;281:30299–30304.
   PubMed Web of Science ®Google Scholar
• Bernales S, McDonald KL, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 2006;4:e423.
   PubMed Web of Science ®Google Scholar
• Kouroku Y, Fujita E, Tanida I, et al. ER stress (PERK/eIF2α phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 2007;14:230–239.
   PubMed Web of Science ®Google Scholar
• Senft D, Ronai ZeA. UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem Sci. 2015;40:141–148.
   PubMed Web of Science ®Google Scholar
• Muscarella DE, Bloom SE. The contribution of c-Jun N-terminal kinase activation and subsequent Bcl-2 phosphorylation to apoptosis induction in human B-cells is dependent on the mode of action of specific stresses. Toxicol Appl Pharmacol. 2008;228:93–104.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Ichijo H, Korsmeyer SJ BCL-2 K. Is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G2/M. Mol Cell Biol. 1999;19:8469–8478.
   PubMed Web of Science ®Google Scholar
• Zalckvar E, Berissi H, Mizrachy L, et al. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 2009;10:285–292.
   PubMed Web of Science ®Google Scholar
• Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit beclin 1-dependent autophagy. Cell. 2005;122:927–939.
   PubMed Web of Science ®Google Scholar
• Pattingre S, Bauvy C, Carpentier S, et al. Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J Biol Chem. 2009;284:2719–2728.
   PubMed Web of Science ®Google Scholar
• Margariti A, Li H, Chen T, et al. XBP1 mRNA splicing triggers an autophagic response in endothelial cells through BECLIN-1 transcriptional activation. J Biol Chem. 2013;288:859–872.
   PubMed Web of Science ®Google Scholar
• Imanikia S, Özbey NP, Krueger C, et al. Neuronal XBP-1 activates intestinal lysosomes to improve proteostasis in C. elegans. Curr Biol. 2019;29:2322–2338.e2327.
   PubMed Web of Science ®Google Scholar
• B’chir W, Maurin A-C, Carraro V, et al. The eIF2α/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res. 2013;41:7683–7699.
   PubMed Web of Science ®Google Scholar
• Høyer-Hansen M, Bastholm L, Szyniarowski P, et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-β, and Bcl-2. Mol Cell. 2007;25:193–205.
   PubMed Web of Science ®Google Scholar
• Younger JM, Chen L, Ren H-Y, et al. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell. 2006;126:571–582.
   PubMed Web of Science ®Google Scholar
• Delaunay A, Bromberg KD, Hayashi Y, et al. The ER-bound ring finger protein 5 (RNF5/RMA1) causes degenerative myopathy in transgenic mice and is deregulated in inclusion body myositis. PLoS ONE. 2008;3:e1609.
   PubMed Web of Science ®Google Scholar
• Kuang E, Qi J, Ronai Z. Emerging roles of E3 ubiquitin ligases in autophagy. Trends Biochem Sci. 2013;38:453–460.
   PubMed Web of Science ®Google Scholar
• Tomati V, Sondo E, Armirotti A, et al. Genetic inhibition of the ubiquitin ligase Rnf5 attenuates phenotypes associated to F508del cystic fibrosis mutation. Sci Rep. 2015;5:12138.
   PubMed Web of Science ®Google Scholar
• Sondo E, Falchi F, Caci E, et al. Pharmacological Inhibition of the ubiquitin ligase RNF5 rescues F508del-CFTR in cystic fibrosis airway epithelia. Cell Chem Biol. 2018;25:891–905.e898.
   PubMed Web of Science ®Google Scholar
• Morito D, Hirao K, Oda Y, et al. Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRΔF508. Mol Biol Cell. 2008;19:1328–1336.
   PubMed Web of Science ®Google Scholar
• Jeon Young J, Khelifa S, Ratnikov B, et al. Regulation of glutamine carrier proteins by RNF5 determines breast cancer response to ER stress-inducing chemotherapies. Cancer Cell. 2015;27:354–369.
   PubMed Web of Science ®Google Scholar
• Zhong B, Zhang L, Lei C, et al. The ubiquitin ligase RNF5 regulates antiviral responses by mediating degradation of the adaptor protein MITA. Immunity. 2009;30:397–407.
   PubMed Web of Science ®Google Scholar
• Zhong B, Zhang Y, Tan B, et al. The E3 ubiquitin ligase RNF5 targets virus-induced signaling adaptor for ubiquitination and degradation. J Immunol. 2010;184:6249–6255.
   PubMed Web of Science ®Google Scholar
• Li Y, Tinoco R, Elmén L, et al. Gut microbiota dependent anti-tumor immunity restricts melanoma growth in Rnf5−/− mice. Nat Commun. 2019;10:1492.
   PubMed Web of Science ®Google Scholar
• Kuang E, Okumura CYM, Sheffy-Levin S, et al. Regulation of ATG4B stability by RNF5 limits basal levels of autophagy and influences susceptibility to bacterial infection. PLoS Genet. 2012;8:e1003007.
   PubMed Web of Science ®Google Scholar
• Broday L, Kolotuev I, Didier C, et al. The LIM domain protein UNC-95 is required for the assembly of muscle attachment structures and is regulated by the RING finger protein RNF-5 in C. elegans. J Cell Biol. 2004;165:857–867.
   PubMed Web of Science ®Google Scholar
• Zaidel-Bar R, Miller S, Kaminsky R, et al. Molting-specific downregulation of C. elegans body-wall muscle attachment sites: the role of RNF-5 E3 ligase. Biochem Biophys Res Commun. 2010;395:509–514.
   PubMed Web of Science ®Google Scholar
• Kovacevic I, Ho R, Cram EJ. CCDC-55 is required for larval development and distal tip cell migration in C. elegans. Mech Dev. 2012;128:548–559.
   PubMed Web of Science ®Google Scholar
• Didier C, Broday L, Bhoumik A, et al. RNF5, a RING finger protein that regulates cell motility by targeting paxillin ubiquitination and altered localization. Mol Cell Biol. 2003;23:5331–5345.
   PubMed Web of Science ®Google Scholar
• Baugh LR. To grow or not to grow: nutritional control of development during caenorhabditis elegans L1 arrest. Genetics. 2013;194:539–555.
   PubMed Web of Science ®Google Scholar
• Muñoz MJ, Riddle DL. Positive selection of caenorhabditis elegans mutants with increased stress resistance and longevity. Genetics. 2003;163:171–180.
   PubMed Web of Science ®Google Scholar
• Baugh LR, Sternberg PW. DAF-16/FOXO regulates transcription of cki-1/Cip/Kip and repression of lin-4 during C. elegans L1 arrest. Curr Biol. 2006;16:780–785.
   PubMed Web of Science ®Google Scholar
• Chang JT, Kumsta C, Hellman AB, et al. Spatiotemporal regulation of autophagy during caenorhabditis elegans aging. eLife. 2017;6:e18459.
   PubMed Web of Science ®Google Scholar
• Tian Y, Li Z, Hu W, et al. C. elegans screen identifies autophagy genes specific to multicellular organisms. Cell. 2010;141:1042–1055.
   PubMed Web of Science ®Google Scholar
• Ichimura Y, Kirisako T, Takao T, et al. A ubiquitin-like system mediates protein lipidation. Nature. 2000;408:488–492.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Yan L, Zhou Z, et al. SEPA-1 mediates the specific recognition and degradation of p granule components by autophagy in C. elegans. Cell. 2009;136:308–321.
   PubMed Web of Science ®Google Scholar
• Kang C, You Y-J, Avery L. Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation. Genes Dev. 2007;21:2161–2171.
   PubMed Web of Science ®Google Scholar
• Kao G, Nordenson C, Still M, et al. Positively regulates insulin secretion in C. elegans and mammalian cells. Cell. 2007;128:577–587.
   PubMed Web of Science ®Google Scholar
• Safra M, Henis-Korenblit S. A new tool in C. elegans reveals changes in secretory protein metabolism in ire-1-deficient animals. Worm. 2014;3:e27733.
   PubMedGoogle Scholar
• Safra M, Fickentscher R, Levi-Ferber M, et al. The FOXO transcription factor DAF-16 bypasses ire-1 requirement to promote endoplasmic reticulum homeostasis. Cell Metab. 2014;20:870–881.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Morris JH, Cook H, et al. The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–D368.
   PubMed Web of Science ®Google Scholar
• Levine B, Kroemer G. Biological functions of autophagy genes: a disease perspective. Cell. 2019;176:11–42.
   PubMed Web of Science ®Google Scholar
• Thorburn A. Autophagy and Its effects: making sense of double-edged swords. PLoS Biol. 2014;12:e1001967.
   PubMed Web of Science ®Google Scholar
• Levi-Ferber M, Salzberg Y, Safra M, et al. It’s all in your mind: determining germ cell fate by neuronal IRE-1 in C. elegans. PLoS Genet. 2014;10:e1004747.
   PubMed Web of Science ®Google Scholar
• Bohnert KA, Kenyon C. A lysosomal switch triggers proteostasis renewal in the immortal C. elegans germ lineage. Nature. 2017;551:629–633.
   PubMed Web of Science ®Google Scholar
• Hughes AL, Gottschling DE. An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature. 2012;492:261–265.
   PubMed Web of Science ®Google Scholar
• Gruidl ME, Smith PA, Kuznicki KA, et al., Multiple potential germ-line helicases are components of the germ-line-specific P granules of Caenorhabditis elegans. Proc National Academy Sci USA 1996; 93:13837–13842.
   PubMed Web of Science ®Google Scholar
• Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell. 2010;140:805–820.
   PubMed Web of Science ®Google Scholar
• Yunger E, Safra M, Levi-Ferber M, et al. Innate immunity mediated longevity and longevity induced by germ cell removal converge on the C-type lectin domain protein IRG-7. PLoS Genet. 2017;13:e1006577.
   PubMed Web of Science ®Google Scholar
• Zou Z, Yuan Z, Zhang Q, et al. Aurora kinase A inhibition-induced autophagy triggers drug resistance in breast cancer cells. Autophagy. 2012;8:1798–1810
   PubMed Web of Science ®Google Scholar
• Tsur A, Bening Abu-Shach U, Broday L. ULP-2 SUMO protease regulates E-Cadherin recruitment to adherens junctions. Dev Cell. 2015;35:63–77.
   PubMed Web of Science ®Google Scholar
• Yang J-S, Nam H-J, Seo M, et al. OASIS: online application for the survival analysis of lifespan assays performed in aging research. PLoS ONE. 2011;6:e23525.
   PubMed Web of Science ®Google Scholar
• Mitchell DH, Stiles JW, Santelli J, et al. Synchronous growth and aging of caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol. 1979;34:28–36.
   PubMedGoogle Scholar
• Krijgsveld J, Ketting RF, Mahmoudi T, et al. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat Biotechnol. 2003;21:927.
   PubMed Web of Science ®Google Scholar
• Dong M-Q, Venable JD, Au N, et al. Quantitative mass spectrometry identifies insulin signaling targets in C. elegans. Science. 2007;317:660–663.
   PubMed Web of Science ®Google Scholar
• Wu S, Zhu W, Nhan T, et al. CAND1 controls in vivo dynamics of the cullin 1-RING ubiquitin ligase repertoire. Nat Commun. 2013;4:1642.
   PubMed Web of Science ®Google Scholar
• Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2008;4:44.
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Gable AL, Lyon D, et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2018;47:D607–D613.
   Web of Science ®Google Scholar