ALS-FTLD-linked mutations of SQSTM1/p62 disrupt selective autophagy and NFE2L2/NRF2 anti-oxidative stress pathway

References

• Achi EY, Rudnicki SA. ALS and frontotemporal dysfunction: a review. Neurol Res Int. 2012;2012:806306.
   PubMedGoogle Scholar
• Ling SC, Polymenidou M, Cleveland DW. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron. 2013;79(3):416–438.
   PubMed Web of Science ®Google Scholar
• Raffaele Ferrari DK, Huey ED, Momeni P. FTD and ALS a tale of two diseases. Curr Alzheimer Res. 2011;8(3):273–294.
   PubMed Web of Science ®Google Scholar
• Blokhuis AM, Groen EJN, Koppers M, et al. Protein aggregation in amyotrophic lateral sclerosis. Acta Neuropathol. 2013;125(6):777–794.
   PubMed Web of Science ®Google Scholar
• Li YR, King OD, Shorter J, et al. Stress granules as crucibles of ALS pathogenesis. J Cell Biol. 2013;201(3):361–372.
   PubMed Web of Science ®Google Scholar
• Lim J, Lachenmayer ML, Wu S, et al. Proteotoxic stress induces phosphorylation of SQSTM1/SQSTM1 by ULK1 to regulate selective autophagic clearance of protein aggregates. PLoS Genet. 2015;11(2):e1004987.
   PubMed Web of Science ®Google Scholar
• Wong YC, Holzbaur EL. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci U S A. 2014;111(42):E4439–E4448.
   PubMed Web of Science ®Google Scholar
• Wild P, Farhan H, McEwan DG, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science. 2011;333(6039):228–233.
   PubMed Web of Science ®Google Scholar
• Pilli M, Arko-Mensah J, Ponpuak M, et al. TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity. 2012;37(2):223–234.
   PubMed Web of Science ®Google Scholar
• Richter B, Sliter DA, Herhaus L, et al. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc Natl Acad Sci U S A. 2016;113(15):4039–4044.
   PubMed Web of Science ®Google Scholar
• Cirulli ET, Petrovski BNL,S, Sapp PC, et al. Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science. 2015;347:1436–1441.
   PubMed Web of Science ®Google Scholar
• Freischmidt A, Wieland T, Richter B, et al. Haploinsufficiency of TBK1 causes familial ALS and fronto-temporal dementia. Nat Neurosci. 2015;18(5):631–636.
   PubMed Web of Science ®Google Scholar
• Xu D, Jin T, Zhu H, et al. TBK1 suppresses RIPK1-driven apoptosis and inflammation during development and in aging. Cell. 2018;174(6):1477–1491.e19.
   PubMed Web of Science ®Google Scholar
• Moore AS, Holzbaur EL. Dynamic recruitment and activation of ALS-associated TBK1 with its target optineurin are required for efficient mitophagy. Proc Natl Acad Sci U S A. 2016;113(24):E3349–E3358.
   PubMed Web of Science ®Google Scholar
• Kang C, Xu Q, Martin TD, et al. The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. Science. 2015;349(6255):aaa5612.
   PubMed Web of Science ®Google Scholar
• Linares JF, Duran A, Reina-Campos M, et al. Amino acid activation of mTORC1 by a PB1-domain-driven kinase complex cascade. Cell Rep. 2015;12(8):1339–1352.
   PubMed Web of Science ®Google Scholar
• Matsumoto G, Wada K, Okuno M, et al. Serine 403 phosphorylation of SQSTM1/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell. 2011;44(2):279–289.
   PubMed Web of Science ®Google Scholar
• Mizuno Y, Amari M, Takatama M, et al. Immunoreactivities of SQSTM1, an ubiqutin-binding protein, in the spinal anterior horn cells of patients with amyotrophic lateral sclerosis. J Neurol Sci. 2006;249(1):13–18.
   PubMed Web of Science ®Google Scholar
• Arai T, Nonaka T, Hasegawa M, et al. Neuronal and glial inclusions in frontotemporal dementia with or without motor neuron disease are immunopositive for SQSTM1. Neurosci Lett. 2003;342(1–2):41–44.
   PubMed Web of Science ®Google Scholar
• Hiji M, Takahashi T, Fukuba H, et al. White matter lesions in the brain with frontotemporal lobar degeneration with motor neuron disease: TDP-43-immunopositive inclusions co-localize with SQSTM1, but not ubiquitin. Acta Neuropathol. 2008;116(2):183–191.
   PubMed Web of Science ®Google Scholar
• Lim J, Yue Z. Neuronal aggregates: formation, clearance, and spreading. Dev Cell. 2015;32(4):491–501.
   PubMed Web of Science ®Google Scholar
• Deng Z, Purtell K, Lachance V, et al. Autophagy receptors and neurodegenerative diseases. Trends Cell Biol. 2017;27:491–504.
   PubMed Web of Science ®Google Scholar
• Guo H, et al. Autophagy supports genomic stability by degrading retrotransposon RNA. Nat Commun. 2014;5:5276.
   PubMed Web of Science ®Google Scholar
• Chitiprolu M, Jagow C, Tremblay V, et al. A complex of C9ORF72 and SQSTM1 uses arginine methylation to eliminate stress granules by autophagy. Nat Commun. 2018;9(1):2794.
   PubMed Web of Science ®Google Scholar
• Lattante S, de Calbiac H, Le Ber I, et al. Sqstm1 knock-down causes a locomotor phenotype ameliorated by rapamycin in a zebrafish model of ALS/FTLD. Hum Mol Genet. 2015;24(6):1682–1690.
   PubMed Web of Science ®Google Scholar
• Goode A, Butler K, Long J, et al. Defective recognition of LC3B by mutant SQSTM1/SQSTM1 implicates impairment of autophagy as a pathogenic mechanism in ALS-FTLD. Autophagy. 2016;12(7):1094–1104.
   PubMed Web of Science ®Google Scholar
• Petri S, Korner S, Kiaei M. NFE2L2/ARE signaling pathway: key mediator in oxidative stress and potential therapeutic target in ALS. Neurol Res Int. 2012;2012:878030.
   PubMedGoogle Scholar
• Zhang DD. Mechanistic studies of the NFE2L2-Keap1 signaling pathway. Drug Metab Rev. 2006;38(4):769–789.
   PubMed Web of Science ®Google Scholar
• Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-NFE2L2 pathway in stress response and cancer evolution. Genes Cells. 2011;16(2):123–140.
   PubMed Web of Science ®Google Scholar
• Tong KI, Kobayashi A, Katsuoka F, et al. Two-site substrate recognition model for the Keap1-NFE2L2 system: a hinge and latch mechanism. Biol Chem. 2006;387(10–11):1311–1320.
   PubMed Web of Science ®Google Scholar
• Mimoto T, Miyazaki K, Morimoto N, et al. Impaired antioxydative Keap1/NFE2L2 system and the downstream stress protein responses in the motor neuron of ALS model mice. Brain Res. 2012;1446:109–118.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate SQSTM1 activates the stress responsive transcription factor NFE2L2 through inactivation of Keap1. Nat Cell Biol. 2010;12(3):213–223.
   PubMed Web of Science ®Google Scholar
• Goode A, Rea S, Sultana M, et al. ALS-FTLD associated mutations of SQSTM1 impact on Keap1-NFE2L2 signalling. Mol Cell Neurosci. 2016;76:52–58.
   PubMed Web of Science ®Google Scholar
• Zhan Z, Cao H, Xie X, et al. Phosphatase PP4 negatively regulates type I IFN production and antiviral innate immunity by dephosphorylating and deactivating TBK1. J Immunol. 2015;195(8):3849–3857.
   PubMed Web of Science ®Google Scholar
• Clark K, Plater L, Peggie M, et al. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J Biol Chem. 2009;284(21):14136–14146.
   PubMed Web of Science ®Google Scholar
• Rosen DR, Siddique T, Patterson D, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 1993;362:59.
   PubMed Web of Science ®Google Scholar
• Pottier C, Bieniek KF, Finch N, et al. Whole-genome sequencing reveals important role for TBK1 and OPTN mutations in frontotemporal lobar degeneration without motor neuron disease. Acta Neuropathol. 2015;130(1):77–92.
   PubMed Web of Science ®Google Scholar
• Chan EY, Longatti A, McKnight NC, et al. Kinase-inactivated ULK proteins inhibit autophagy via their conserved C-terminal domains using an Atg13-independent mechanism. Mol Cell Biol. 2009;29(1):157–171.
   PubMed Web of Science ®Google Scholar
• Garner TP, Long J, Layfield R, et al. Impact of SQSTM1/SQSTM1 UBA domain mutations linked to Paget’s disease of bone on ubiquitin recognition. Biochemistry. 2011;50(21):4665–4674.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Koike M, et al. Homeostatic levels of SQSTM1 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131(6):1149–1163.
   PubMed Web of Science ®Google Scholar
• Bai B, Tan H, Pagala VR, et al. Deep profiling of proteome and phosphoproteome by isobaric labeling, extensive liquid chromatography, and mass spectrometry. Methods Enzymol. 2017;585:377–395.
   PubMed Web of Science ®Google Scholar
• Riley BE, Kaiser SE, Shaler TA, et al. Ubiquitin accumulation in autophagy-deficient mice is dependent on the NFE2L2-mediated stress response pathway: a potential role for protein aggregation in autophagic substrate selection. J Cell Biol. 2010;191(3):537–552.
   PubMed Web of Science ®Google Scholar
• Ichimura Y, Waguri S, Sou Y-S, et al. Phosphorylation of SQSTM1 activates the Keap1-NFE2L2 pathway during selective autophagy. Mol Cell. 2013;51(5):618–631.
   PubMed Web of Science ®Google Scholar
• Colombrita C, Zennaro E, Fallini C, et al. TDP-43 is recruited to stress granules in conditions of oxidative insult. J Neurochem. 2009;111(4):1051–1061.
   PubMed Web of Science ®Google Scholar
• Tourriere H, Chebli K, Zekri L, et al. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J Cell Biol. 2003;160(6):823–831.
   PubMed Web of Science ®Google Scholar
• Kweon JH, Kim S, Lee SB. The cellular basis of dendrite pathology in neurodegenerative diseases. BMB Rep. 2017;50(1):5–11.
   PubMed Web of Science ®Google Scholar
• Kulkarni VA, Firestein BL. The dendritic tree and brain disorders. Mol Cell Neurosci. 2012;50(1):10–20.
   PubMed Web of Science ®Google Scholar
• Lee SB, Bagley JA, Lee HY, et al. Pathogenic polyglutamine proteins cause dendrite defects associated with specific actin cytoskeletal alterations in Drosophila. Proc Natl Acad Sci U S A. 2011;108(40):16795–16800.
   PubMed Web of Science ®Google Scholar
• Stolz A, Ernst A, Dikic I. Cargo recognition and trafficking in selective autophagy. Nat Cell Biol. 2014;16(6):495–501.
   PubMed Web of Science ®Google Scholar
• Loo YM, Gale M Jr. Immune signaling by RIG-I-like receptors. Immunity. 2011;34(5):680–692.
   PubMed Web of Science ®Google Scholar
• Matsumoto G, Shimogori T, Hattori N, et al. TBK1 controls autophagosomal engulfment of polyubiquitinated mitochondria through SQSTM1/SQSTM1 phosphorylation. Hum Mol Genet. 2015;24(15):4429–4442.
   PubMed Web of Science ®Google Scholar
• Cho C-S, Park HW, Ho A, et al. Lipotoxicity induces hepatic protein inclusions through TANK binding kinase 1–mediated SQSTM1/sequestosome 1 phosphorylation. Hepatology. 2018;68(4):1331-1346.
   Google Scholar
• Prabakaran T, Bodda C, Krapp C, et al. Attenuation of cGAS‐STING signaling is mediated by a SQSTM1/SQSTM1‐dependent autophagy pathway activated by TBK1. Embo J. 2018;37(8):e97858.
   PubMed Web of Science ®Google Scholar
• Korac J, Schaeffer V, Kovacevic I, et al. Ubiquitin-independent function of optineurin in autophagic clearance of protein aggregates. J Cell Sci. 2013;126(Pt 2):580–592.
   PubMed Web of Science ®Google Scholar
• Gal J, Ström A-L, Kwinter DM, et al. Sequestosome 1/SQSTM1 links familial ALS mutant SOD1 to LC3 via an ubiquitin-independent mechanism. J Neurochem. 2009;111(4):1062–1073.
   PubMed Web of Science ®Google Scholar
• Magrane J, Hervias I, Henning MS, et al. Mutant SOD1 in neuronal mitochondria causes toxicity and mitochondrial dynamics abnormalities. Hum Mol Genet. 2009;18(23):4552–4564.
   PubMed Web of Science ®Google Scholar
• Yamamoto A, Cremona ML, Rothman JE. Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway. J Cell Biol. 2006;172:719–731. PMID: 16505167.
   PubMed Web of Science ®Google Scholar
• Pan JA, Ullman E, Dou Z, et al. Inhibition of protein degradation induces apoptosis through a microtubule-associated protein 1 light chain 3-mediated activation of caspase-8 at intracellular membranes. Mol Cell Biol. 2011;31(15):3158–3170.
   PubMed Web of Science ®Google Scholar
• Wang H, Yang Y, Li Y, et al. Systematic optimization of long gradient chromatography mass spectrometry for deep analysis of brain proteome. J Proteome Res. 2015;14(2):829–838.
   PubMed Web of Science ®Google Scholar
• Wang X, Li Y, Wu Z, et al. JUMP: a tag-based database search tool for peptide identification with high sensitivity and accuracy. Mol Cell Proteomics. 2014;13(12):3663–3673.
   PubMed Web of Science ®Google Scholar
• Niu M, Cho J-H, Kodali K, et al. Extensive peptide fractionation and y(1) ion-based interference detection method for enabling accurate quantification by isobaric labeling and mass spectrometry. Anal Chem. 2017;89(5):2956–2963.
   PubMed Web of Science ®Google Scholar
• Ritchie ME, Phipson B, Wu D, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47.
   PubMed Web of Science ®Google Scholar
• Stewart E, McEvoy J, Wang H, et al. Identification of therapeutic targets in rhabdomyosarcoma through integrated genomic, epigenomic, and proteomic analyses. Cancer Cell. 2018;34(3):411–426.e19.
   PubMed Web of Science ®Google Scholar
• Ferreira TA, Blackman AV, Oyrer J, et al. Neuronal morphometry directly from bitmap images. Nat Methods. 2014;11(10):982–984.
   PubMed Web of Science ®Google Scholar