MALT-1 shortens lifespan by inhibiting autophagy in the intestine of C. elegans

References

• Meininger I, Krappmann D. Lymphocyte signaling and activation by the CARMA1-BCL10-MALT1 signalosome. Biol Chem. 2016;397(12):1315-1333.
   PubMed Web of Science ®Google Scholar
• Gomez Solsona B, Schmitt A, Schulze-Osthoff K, et al. The Paracaspase MALT1 in Cancer. Biomedicines. 2022;10(2):344.
   PubMed Web of Science ®Google Scholar
• Ruland J, Hartjes L. CARD-BCL-10-MALT1 signalling in protective and pathological immunity. Nat Rev Immunol. 2019 Feb;19(2):118-134.
   PubMed Web of Science ®Google Scholar
• Lork M, Staal J, Beyaert R. Ubiquitination and phosphorylation of the CARD11-BCL10-MALT1 signalosome in T cells. Cell Immunol. 2019;340:103877.
   PubMedGoogle Scholar
• Juilland M, Thome M. Holding All the CARDs: How MALT1 Controls CARMA/CARD-Dependent Signaling. Front Immunol. 2018;9:1927.
   PubMedGoogle Scholar
• Sun L, Deng L, Ea CK, et al. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol Cell. 2004 May 7;14(3):289-301.
   Web of Science ®Google Scholar
• Dubois SM, Alexia C, Wu Y, et al. A catalytic-independent role for the LUBAC in NF-kappaB activation upon antigen receptor engagement and in lymphoma cells. Blood. 2014;123(14):2199-203.
   PubMed Web of Science ®Google Scholar
• Yu JW, Jeffrey PD, Ha JY, et al. Crystal structure of the mucosa-associated lymphoid tissue lymphoma translocation 1 (MALT1) paracaspase region. Proc Natl Acad Sci U S A. 2011;108(52):21004-9.
   Web of Science ®Google Scholar
• Wiesmann C, Leder L, Blank J, et al. Structural determinants of MALT1 protease activity. J Mol Biol. 2012 May 25;419(1–2):4-21.
   PubMed Web of Science ®Google Scholar
• Rebeaud F, Hailfinger S, Posevitz-Fejfar A, et al. The proteolytic activity of the paracaspase MALT1 is key in T cell activation. Nat Immunol. 2008;9(3):272-81.
   PubMed Web of Science ®Google Scholar
• Klei LR, Hu D, Panek R, et al. MALT1 Protease Activation Triggers Acute Disruption of Endothelial Barrier Integrity via CYLD Cleavage. Cell Rep. 2016;17(1):221-232.
   PubMed Web of Science ®Google Scholar
• Uren AG, O’Rourke K, Aravind LA, et al. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell. 2000;6(4):961-7.
   Web of Science ®Google Scholar
• Staal J, Driege Y, Haegman M, et al. Ancient Origin of the CARD-Coiled Coil/Bcl10/MALT1-Like Paracaspase Signaling Complex Indicates Unknown Critical Functions. Front Immunol. 2018;9:1136.
   Google Scholar
• Flynn SM, Chen C, Artan M, et al. MALT-1 mediates IL-17 neural signaling to regulate C. elegans behavior, immunity and longevity. Nat Commun. 2020 Apr 29;11(1):2099.
   Web of Science ®Google Scholar
• Uno M, Nishida E. Lifespan-regulating genes in C. elegans. NPJ Aging Mech Dis. 2016;2:16010.
   PubMedGoogle Scholar
• Kapahi P, Kaeberlein M, Hansen M. Dietary restriction and lifespan: Lessons from invertebrate models. Ageing Res Rev. 2017;39:3-14.
   PubMed Web of Science ®Google Scholar
• Aman Y, Schmauck-Medina T, Hansen M, et al. Autophagy in healthy aging and disease. Nat Aging. 2021;1(8):634-650.
   PubMedGoogle Scholar
• Hansen M, Rubinsztein DC, Walker DW. Autophagy as a promoter of longevity: insights from model organisms. Nat Rev Mol Cell Biol. 2018 Sep;19(9):579-593.
   Web of Science ®Google Scholar
• Toth ML, Sigmond T, Borsos E, et al. Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy. 2008;4(3):330-8.
   Web of Science ®Google Scholar
• Dall KB, Faergeman NJ. Metabolic regulation of lifespan from a C. elegans perspective. Genes Nutr. 2019;14:25.
   PubMedGoogle Scholar
• Ashley N, Holgado A. The autophagy gene product BEC-1 supports normal aging and neurodevelopment in Caenorhabditis elegans I. MicroPubl Biol. 2019 Jun 14;2019:17912.
   Google Scholar
• Hashimoto Y, Ookuma S, Nishida E. Lifespan extension by suppression of autophagy genes in Caenorhabditis elegans. Genes Cells. 2009;14(6):717-26.
   Web of Science ®Google Scholar
• Robida-Stubbs S, Glover-Cutter K, Lamming DW, et al. TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab. 2012;15(5):713-24.
   PubMed Web of Science ®Google Scholar
• Lapierre LR, Silvestrini MJ, Nunez L, et al. Autophagy genes are required for normal lipid levels in C. elegans. Autophagy. 2013;9(3):278-86.
   PubMed Web of Science ®Google Scholar
• Madeo F, Eisenberg T, Pietrocola F, et al. Spermidine in health and disease. Science. 2018;359(6374):eaan2788.
   PubMed Web of Science ®Google Scholar
• O’Rourke EJ, Ruvkun G. MXL-3 and HLH-30 transcriptionally link lipolysis and autophagy to nutrient availability. Nat Cell Biol. 2013;15(6):668-76.
   PubMed Web of Science ®Google Scholar
• Hermann GJ, Schroeder LK, Hieb CA, et al. Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol Biol Cell. 2005;16(7):3273-88.
   PubMed Web of Science ®Google Scholar
• So S, Tokumaru T, Miyahara K, et al. Control of lifespan by food bacteria, nutrient limitation and pathogenicity of food in C. elegans. Mech Ageing Dev. 2011;132(4):210-2.
   PubMed Web of Science ®Google Scholar
• Mallo GV, Kurz CL, Couillault C, et al. Inducible antibacterial defense system in C. elegans. Curr Biol. 2002;12(14):1209-14.
   PubMed Web of Science ®Google Scholar
• Kaeberlein TL, Smith ED, Tsuchiya M, et al. Lifespan extension in Caenorhabditis elegans by complete removal of food. Aging Cell. 2006;5(6):487-94.
   Web of Science ®Google Scholar
• Lee GD, Wilson MA, Zhu M, et al. Dietary deprivation extends lifespan in Caenorhabditis elegans. Aging Cell. 2006;5(6):515-24.
   Web of Science ®Google Scholar
• Greer EL, Brunet A. Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell. 2009;8(2):113-27.
   PubMed Web of Science ®Google Scholar
• Hosono R, Nishimoto S, Kuno S. Alterations of life span in the nematode Caenorhabditis elegans under monoxenic culture conditions. Exp Gerontol. 1989;24(3):251-64.
   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.
   Web of Science ®Google Scholar
• Baxi K, de Carvalho CE. Assessing Lysosomal Alkalinization in the Intestine of Live Caenorhabditis elegans. J Vis Exp. 2018;134:57414.
   Google Scholar
• Alberti A, Michelet X, Djeddi A, et al. The autophagosomal protein LGG-2 acts synergistically with LGG-1 in dauer formation and longevity in C. elegans. Autophagy. 2010;6(5):622-33.
   PubMed Web of Science ®Google Scholar
• Melendez A, Talloczy Z, Seaman M, et al. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science. 2003 Sep 5;301(5638):1387–28.
   PubMed Web of Science ®Google Scholar
• Tian E, Wang F, Han J, et al. epg-1 functions in autophagy-regulated processes and may encode a highly divergent Atg13 homolog in C. elegans. Autophagy. 2009;5(5):608-15.
   Web of Science ®Google Scholar
• Ganley IG, Lam du H, Wang J, et al. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem. 2009;284(18):12297-305.
   PubMed Web of Science ®Google Scholar
• Takacs-Vellai K, Vellai T, Puoti A, et al. Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Curr Biol. 2005;15(16):1513-7.
   PubMed Web of Science ®Google Scholar
• Manil-Segalen M, Lefebvre C, Jenzer C, et al. The C. elegans LC3 acts downstream of GABARAP to degrade autophagosomes by interacting with the HOPS subunit VPS39. Dev Cell. 2014;28(1):43-55.
   PubMed Web of Science ®Google Scholar
• Jenzer C, Manil-Segalen M, Lefebvre C, et al. Human GABARAP can restore autophagosome biogenesis in a C. elegans lgg-1 mutant. Autophagy. 2014;10(10):1868-72.
   PubMed Web of Science ®Google Scholar
• Morselli E, Maiuri MC, Markaki M, et al. Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis. 2010;1:e10.
   PubMed Web of Science ®Google Scholar
• Manifava M KN. Chapter 24 - Autophagy on the road to longevity and aging. Autophagy in Health and Disease (Second Edition). 2022:347–360.
   Google Scholar
• Pan KZ, Palter JE, Rogers AN, et al. Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell. 2007;6(1):111-9.
   Web of Science ®Google Scholar
• Hansen M, Taubert S, Crawford D, et al. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell. 2007;6(1):95-110.
   PubMed Web of Science ®Google Scholar
• Vellai T, Takacs-Vellai K, Zhang Y, et al. Genetics: influence of TOR kinase on lifespan in C. elegans. Nature. 2003;426(6967):620.
   PubMed Web of Science ®Google Scholar
• Jia K, Chen D, Riddle DL. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development. 2004;131(16):3897-906.
   PubMed Web of Science ®Google Scholar
• Sun X, Chen WD, Wang YD. DAF-16/FOXO Transcription Factor in Aging and Longevity. Front Pharmacol. 2017;8:548.
   Google Scholar
• Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332(6036):1429–33.
   PubMed Web of Science ®Google Scholar
• Kumsta C, Chang JT, Lee R, et al. The autophagy receptor p62/SQST-1 promotes proteostasis and longevity in C. elegans by inducing autophagy. Nat Commun. 2019 Dec 11;10(1):5648.
   PubMedGoogle Scholar
• Nakamura S, Oba M, Suzuki M, et al. Suppression of autophagic activity by Rubicon is a signature of aging. Nat Commun. 2019;10(1):847.
   Google Scholar
• Kang C, You YJ, Avery L. Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation. Genes Dev. 2007;21(17):2161-71.
   PubMed Web of Science ®Google Scholar
• Jia K, Levine B. Autophagy is required for dietary restriction-mediated life span extension in C. elegans. Autophagy. 2007;3(6):597-9.
   Web of Science ®Google Scholar
• Gelino S, Chang JT, Kumsta C, et al. Intestinal Autophagy Improves Healthspan and Longevity in C. elegans during Dietary Restriction. PLoS Genet. 2016;12(7):e1006135.
   Web of Science ®Google Scholar
• Hansen M, Chandra A, Mitic LL, et al. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 2008;4(2):e24.
   Web of Science ®Google Scholar
• Paul S, Kashyap AK, Jia W, et al. Selective autophagy of the adaptor protein Bcl10 modulates T cell receptor activation of NF-kappaB. Immunity. 2012;36(6):947-58.
   PubMed Web of Science ®Google Scholar
• Yang CS, Rodgers M, Min CK, et al. The autophagy regulator Rubicon is a feedback inhibitor of CARD9-mediated host innate immunity. Cell Host Microbe. 2012;11(3):277-89.
   Web of Science ®Google Scholar
• Jacobs KA, Andre-Gregoire G, Maghe C, et al. Paracaspase MALT1 regulates glioma cell survival by controlling endo-lysosome homeostasis. EMBO J. 2020;39(1):e102030.
   PubMed Web of Science ®Google Scholar
• Habacher C, Guo Y, Venz R, et al. Ribonuclease-Mediated Control of Body Fat. Dev Cell. 2016;39(3):359-369.
   PubMed Web of Science ®Google Scholar
• Schaefer JS, Klein JR. Roquin--a multifunctional regulator of immune homeostasis. Genes Immun. 2016;17(2):79-84.
   PubMed Web of Science ®Google Scholar
• Hadweh P, Chaitoglou I, Gravato-Nobre MJ, et al. Functional analysis of the C. elegans cyld-1 gene reveals extensive similarity with its human homolog. PLoS One. 2018;13(2):e0191864.
   PubMed Web of Science ®Google Scholar
• Li W, Gao B, Lee SM, et al. RLE-1, an E3 ubiquitin ligase, regulates C. elegans aging by catalyzing DAF-16 polyubiquitination. Dev Cell. 2007;12(2):235-46.
   Web of Science ®Google Scholar
• Colombo E, Horta G, Roesler MK, et al. The K63 deubiquitinase CYLD modulates autism-like behaviors and hippocampal plasticity by regulating autophagy and mTOR signaling. Proc Natl Acad Sci U S A. 2021;118(47):e2110755118.
   Web of Science ®Google Scholar
• Younce C, Kolattukudy P. MCP-1 induced protein promotes adipogenesis via oxidative stress, endoplasmic reticulum stress and autophagy. Cell Physiol Biochem. 2012;30(2):307-20.
   PubMedGoogle Scholar
• Pelzer C, Cabalzar K, Wolf A, et al. The protease activity of the paracaspase MALT1 is controlled by monoubiquitination. Nat Immunol. 2013;14(4):337-45.
   PubMed Web of Science ®Google Scholar
• Schairer R, Hall G, Zhang M, et al. Allosteric activation of MALT1 by its ubiquitin-binding Ig3 domain. Proc Natl Acad Sci U S A. 2020;117(6):3093-3102.
   PubMed Web of Science ®Google Scholar
• Stiernagle T. Maintenance of C. elegans. WormBook. 2006:1–11.
   Google Scholar
• Wang C, Liu Z, Huang X. Rab32 is important for autophagy and lipid storage in Drosophila. PLoS One. 2012;7(2):e32086.
   PubMed Web of Science ®Google Scholar
• 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(17):2913-32.
   PubMed Web of Science ®Google Scholar
• Zhou Q, Li H, Xue D. Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Res. 2011;21(12):1662-9.
   Web of Science ®Google Scholar
• McDonald KL, Webb RI. Freeze substitution in 3 hours or less. J Microsc. 2011;243(3):227-33.
   PubMed Web of Science ®Google Scholar
• Low IIC, Williams CR, Chong MK, et al. Morphogenesis of neurons and glia within an epithelium. Development. 2019;146(4):dev171124.
   Web of Science ®Google Scholar
• Kolotuev I. Positional correlative anatomy of invertebrate model organisms increases efficiency of TEM data production. Microsc Microanal. 2014;20(5):1392-403.
   PubMed Web of Science ®Google Scholar
• Burel A, Lavault MT, Chevalier C, et al. A targeted 3D EM and correlative microscopy method using SEM array tomography. Development. 2018;145(12):dev160879.
   PubMed Web of Science ®Google Scholar
• Kremer JR, Mastronarde DN, McIntosh JR. Computer visualization of three-dimensional image data using IMOD. J Struct Biol. 1996;116(1):71-6.
   PubMed Web of Science ®Google Scholar