SMURF1 controls the PPP3/calcineurin complex and TFEB at a regulatory node for lysosomal biogenesis

References

• Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008;451(7182):1069–1075. doi: 10.1038/nature06639
   PubMed Web of Science ®Google Scholar
• Medina DL, Di Paola S, Peluso I, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol. 2015;17(3):288–299. doi: 10.1038/ncb3114
   PubMed Web of Science ®Google Scholar
• Dong L, Liu L, Li Y, et al. E3 ligase Smurf1 protects against misfolded SOD1 in neuronal cells by promoting its K63 ubiquitylation and aggresome formation. Hum Mol Genet. 2022;31(12): 2035–2048. doi: 10.1093/hmg/ddac008
   PubMed Web of Science ®Google Scholar
• Franco LH, Nair VR, Scharn CR, et al. The ubiquitin ligase Smurf1 functions in selective autophagy of Mycobacterium tuberculosis and anti-tuberculous host defense. Cell Host Microbe. 2017;21:59–72. doi: 10.1016/j.chom.2016.11.002
   PubMed Web of Science ®Google Scholar
• Shariq M, Quadir N, Alam A, et al. The exploitation of host autophagy and ubiquitin machinery by Mycobacterium tuberculosis in shaping immune responses and host defense during infection. Autophagy. 2022;19:1–21. doi: 10.1080/15548627.2021.2021495
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332(6036):1429–1433. doi: 10.1126/science.1204592
   PubMed Web of Science ®Google Scholar
• Raben N, Puertollano R. TFEB and TFE3: linking lysosomes to cellular adaptation to stress. Annu Rev Cell Dev Biol. 2016;32:255–278. doi: 10.1146/annurev-cellbio-111315-125407
   PubMed Web of Science ®Google Scholar
• Zhou J, Li X-Y, Liu Y-J, et al. Full-coverage regulations of autophagy by ROS: from induction to maturation. Autophagy. 2022;18:1240–1255. doi: 10.1080/15548627.2021.1984656
   PubMed Web of Science ®Google Scholar
• Kim S, Lee J-Y, Shin SG, et al. ESRRA (estrogen related receptor alpha) is a critical regulator of intestinal homeostasis through activation of autophagic flux via gut microbiota. Autophagy. 2021;17:2856–2875. doi: 10.1080/15548627.2020.1847460
   PubMed Web of Science ®Google Scholar
• Najibi M, Honwad HH, Moreau JA, et al. A novel Nox/Phox-Cd38-naadp-tfeb axis important for macrophage activation during bacterial phagocytosis. Autophagy. 2022;18:124–141. doi: 10.1080/15548627.2021.1911548
   PubMed Web of Science ®Google Scholar
• Schuster EM, Epple MW, Glaser KM, et al. TFEB induces mitochondrial itaconate synthesis to suppress bacterial growth in macrophages. Nat Metab. 2022;4:856–866. doi: 10.1038/s42255-022-00605-w
   PubMedGoogle Scholar
• Perera RM, Stoykova S, Nicolay BN, et al. Transcriptional control of autophagy–lysosome function drives pancreatic cancer metabolism. Nature. 2015;524:361–365. doi: 10.1038/nature14587
   PubMed Web of Science ®Google Scholar
• Roczniak-Ferguson A, Petit CS, Froehlich F, et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal. 2012;5:ra42. doi: 10.1126/scisignal.2002790
   PubMed Web of Science ®Google Scholar
• Martina JA, Chen Y, Gucek M, et al. MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB. Autophagy. 2012;8:903–914. doi:10.4161/auto.19653
   PubMed Web of Science ®Google Scholar
• Jeong SJ, Stitham J, Evans TD, et al. Trehalose causes low-grade lysosomal stress to activate TFEB and the autophagy-lysosome biogenesis response. Autophagy. 2021;17:3740–3752. doi: 10.1080/15548627.2021.1896906
   PubMed Web of Science ®Google Scholar
• Kingsbury TJ, Cunningham KW. A conserved family of calcineurin regulators. Genes Dev. 2000;14(13):1595–1604. doi: 10.1101/gad.14.13.1595
   PubMed Web of Science ®Google Scholar
• Valdor R, Mocholi E, Botbol Y, et al. Chaperone-mediated autophagy regulates T cell responses through targeted degradation of negative regulators of T cell activation. Nat Immunol. 2014;15:1046–1054. doi: 10.1038/ni.3003
   PubMed Web of Science ®Google Scholar
• De Windt LJ, Lim HW, Bueno OF, et al. Targeted inhibition of calcineurin attenuates cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A. 2001;98:3322–3327. doi: 10.1073/pnas.031371998
   PubMed Web of Science ®Google Scholar
• Taigen T, De Windt LJ, Lim HW, et al. Targeted inhibition of calcineurin prevents agonist-induced cardiomyocyte hypertrophy. Proc Natl Acad Sci U S A. 2000;97:1196–1201. doi: 10.1073/pnas.97.3.1196
   PubMed Web of Science ®Google Scholar
• Kafadar KA, Zhu H, Snyder M, et al. Negative regulation of calcineurin signaling by Hrr25p, a yeast homolog of casein kinase I. Genes Dev. 2003;17:2698–2708. doi: 10.1101/gad.1140603
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu R-B, Cao Q, et al. USP16-mediated deubiquitination of calcineurin a controls peripheral T cell maintenance. J Clin Invest. 2019;129:2856–2871. doi: 10.1172/JCI123801
   PubMed Web of Science ®Google Scholar
• Xia Q, Zhang H, Zhang P, et al. Oncogenic Smurf1 promotes PTEN wild-type glioblastoma growth by mediating PTEN ubiquitylation. Oncogene. 2020;39:5902–5915. doi: 10.1038/s41388-020-01400-1
   PubMed Web of Science ®Google Scholar
• Jia J, Abudu YP, Claude-Taupin A, et al. Galectins control mTOR in response to endomembrane damage. Mol Cell. 2018;70:120–135 e128. doi: 10.1016/j.molcel.2018.03.009
   PubMed Web of Science ®Google Scholar
• Jia J, Claude-Taupin A, Gu Y, et al. Galectin-3 coordinates a cellular system for lysosomal repair and removal. Dev Cell. 2020;52:69–87 e68. doi: 10.1016/j.devcel.2019.10.025
   PubMed Web of Science ®Google Scholar
• Chauhan S, Kumar S, Jain A, et al. Trims and galectins Globally Cooperate and TRIM16 and galectin-3 Co-direct autophagy in endomembrane damage homeostasis. Dev Cell. 2016;39:13–27. doi: 10.1016/j.devcel.2016.08.003
   PubMed Web of Science ®Google Scholar
• Watson RO, Manzanillo PS, Cox JSE. Tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell. 2012;150:803–815. doi: 10.1016/j.cell.2012.06.040
   PubMed Web of Science ®Google Scholar
• Nakamura S, Shigeyama S, Minami S, et al. LC3 lipidation is essential for TFEB activation during the lysosomal damage response to kidney injury. Nat Cell Biol. 2020;22:1252–1263. doi: 10.1038/s41556-020-00583-9
   PubMed Web of Science ®Google Scholar
• Gatica D, Lahiri V, Klionsky DJ. Cargo recognition and degradation by selective autophagy. Nat Cell Biol. 2018;20:233–242. doi: 10.1038/s41556-018-0037-z
   PubMed Web of Science ®Google Scholar
• Orvedahl A, Sumpter R, Xiao G, et al. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature. 2011;480:113–117. doi: 10.1038/nature10546
   PubMed Web of Science ®Google Scholar
• Napolitano G, Di Malta C, Esposito A, et al. A substrate-specific mTORC1 pathway underlies Birt–Hogg–dubé syndrome. Nature. 2020;585:597–602. doi: 10.1038/s41586-020-2444-0
   PubMed Web of Science ®Google Scholar
• Stewart AA, Ingebritsen TS, Manalan A, et al. Discovery of a Ca2+- and calmodulin-dependent protein phosphatase: probable identity with calcineurin (CaM-BP80). FEBS Lett. 1982;137(1):80–4. doi: 10.1016/0014-5793(82)80319-0
   PubMed Web of Science ®Google Scholar
• Thurston TL, Wandel MP, von Muhlinen N, et al. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature. 2012;482:414–418. doi: 10.1038/nature10744
   PubMed Web of Science ®Google Scholar
• Kilka S, Erdmann F, Migdoll A, et al. The proline-rich N-terminal sequence of calcineurin abeta determines substrate binding. Biochemistry. 2009;48:1900–1910. doi: 10.1021/bi8019355
   PubMed Web of Science ®Google Scholar
• Gal M, Li S, Luna RE, et al. The LxVP and PxIxIT NFAT motifs bind jointly to overlapping epitopes on calcineurin’s catalytic domain distant to the regulatory domain. Structure. 2014;22:1016–1027. doi: 10.1016/j.str.2014.05.006
   PubMed Web of Science ®Google Scholar
• Klee CB, Crouch TH, Krinks MH. Calcineurin: a calcium- and calmodulin-binding protein of the nervous system. Proc Natl Acad Sci U S A. 1979;76:6270–6273. doi: 10.1073/pnas.76.12.6270
   PubMed Web of Science ®Google Scholar
• Hernandez GA, Perera RM. Autophagy in cancer cell remodeling and quality control. Molecular Cell. 2022;82:1514–1527. doi: 10.1016/j.molcel.2022.03.023
   PubMed Web of Science ®Google Scholar
• Sancak Y, Bar-Peled L, Zoncu R, et al. Ragulator-rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell. 2010;141:290–303. doi: 10.1016/j.cell.2010.02.024
   PubMed Web of Science ®Google Scholar
• Zoncu R, Bar-Peled L, Efeyan A, et al. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H+-ATPase. Science. 2011;334:678–683. doi: 10.1126/science.1207056
   PubMed Web of Science ®Google Scholar
• Liu GY, Sabatini D. M. mTOR at the nexus of nutrition, growth, ageing and disease. Nat Rev Mol Cell Biol. 2020;21:183–203. doi: 10.1038/s41580-019-0199-y
   PubMed Web of Science ®Google Scholar
• Xia Q, Li W, Ali S, et al. Smurf1 silencing restores PTEN expression that ameliorates progression of human glioblastoma and sensitizes tumor cells to mTORC1/C2 inhibitor Torin1. iScience. 2021;24:103528. doi: 10.1016/j.isci.2021.103528
   PubMed Web of Science ®Google Scholar
• Medina DL, Ballabio A. Lysosomal calcium regulates autophagy. Autophagy. 2015;11:970–971. doi: 10.1080/15548627.2015.1047130
   PubMed Web of Science ®Google Scholar
• Kissinger CR, Parge HE, Knighton DR, et al. Crystal structures of human calcineurin and the human FKBP12–FK506–calcineurin complex. Nature. 1995;378:641–644. doi: 10.1038/378641a0
   PubMed Web of Science ®Google Scholar
• Chapman NM, Boothby MR, Chi H. Metabolic coordination of T cell quiescence and activation. Nat Rev Immunol. 2020;20:55–70. doi: 10.1038/s41577-019-0203-y
   PubMed Web of Science ®Google Scholar
• Zhang X, Yu L, Xu H. Lysosome calcium in ROS regulation of autophagy. Autophagy. 2016;12:1954–1955. doi: 10.1080/15548627.2016.1212787
   PubMed Web of Science ®Google Scholar
• Kar P, Mirams GR, Christian HC, et al. Control of NFAT isoform activation and NFAT-Dependent gene expression through two coincident and spatially segregated intracellular Ca2+ signals. Molecular Cell. 2016;64:746–759. doi: 10.1016/j.molcel.2016.11.011
   PubMed Web of Science ®Google Scholar
• Goodwin JM, Walkup WG, Hooper K, et al. GABARAP sequesters the FLCN-FNIP tumor suppressor complex to couple autophagy with lysosomal biogenesis. Sci Adv. 2021;7:eabj2485. doi: 10.1126/sciadv.abj2485
   PubMed Web of Science ®Google Scholar