Retinoic acid worsens ATG10-dependent autophagy impairment in TBK1-mutant hiPSC-derived motoneurons through SQSTM1/p62 accumulation

References

• Pomerantz JL, Baltimore D. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK1, a novel IKK-related kinase. Embo J. 1999;18(23):6694–6704.
   PubMed Web of Science ®Google Scholar
• Xie X, Zhang D, Zhao B, et al. IkappaB kinase epsilon and TANK-binding kinase 1 activate AKT by direct phosphorylation. Proc Natl Acad Sci U S A. 2011;108(16):6474–6479.
   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
• Matsumoto G, Shimogori T, Hattori N, et al. TBK1 controls autophagosomal engulfment of polyubiquitinated mitochondria through p62/SQSTM1 phosphorylation. Hum Mol Genet. 2015;24(15):4429–4442.
   PubMed Web of Science ®Google Scholar
• Herman M, Ciancanelli M, Ou Y-H, et al. Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex encephalitis of childhood. J Exp Med. 2012;209(9):1567–1582.
   PubMed Web of Science ®Google Scholar
• Awadalla MS, Fingert JH, Roos BE, et al. Copy number variations of TBK1 in Australian patients with primary open-angle glaucoma. Am J Ophthalmol. 2015;159(1):124–130.
   PubMed Web of Science ®Google Scholar
• Cirulli ET, Lasseigne BN, Petrovski S, et al. Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science. 2015;347(6229):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
• Williams KL, McCann EP, Fifita JA, et al. Novel TBK1 truncating mutation in a familial amyotrophic lateral sclerosis patient of Chinese origin. Neurobiol Aging. 2015;36(12):3334.e1–3334.e5.
   Web of Science ®Google Scholar
• Gijselinck I, Van Mossevelde S, van der Zee J, et al. Loss of TBK1 is a frequent cause of frontotemporal dementia in a Belgian cohort. Neurology. 2015;85(24):2116–2125.
   PubMed Web of Science ®Google Scholar
• Van der Zee J, Gijselinck I, Van Mossevelde S, et al. TBK1 mutation spectrum in an extended european patient cohort with frontotemporal dementia and amyotrophic lateral sclerosis. Hum Mutat. 2017;38(3):297–309.
   PubMed Web of Science ®Google Scholar
• Pozzi L, Valenza F, Mosca L, et al. TBK1 mutations in Italian patients with amyotrophic lateral sclerosis: genetic and functional characterisation. J Neurol Neurosurg Psychiatry. 2017 Oct;88(10):869–875. doi:10.1136/jnnp-2017-316174. Epub 2017 Aug 19.
   Web of Science ®Google Scholar
• Larabi A, Devos JM, Ng SL, et al. Crystal structure and mechanism of activation of TANK-binding kinase 1. Cell Rep. 2013;3(3):734–746.
   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
• 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
• Mossevelde S, van der Zee J, Gijselinck I, et al. Clinical features of TBK1 carriers compared with C9orf72, GRN and non-mutation carriers in a Belgian cohort. Brain. 2016;139(Pt 2):452–467.
   PubMedGoogle 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
• Somers A, Jean JC, Sommer CA, et al. Generation of transgene-free lung disease-specific human iPS cells using a single excisable lentiviral stem cell cassette. Stem Cells. 2010;28(10):1728–1740.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–676.
   PubMed Web of Science ®Google Scholar
• Aasen T, Raya A, Barrero MJ, et al. Efficient and rapid generation of pluripotent stem cells from human keratinocytes. Nat Biotechnol. 2008;26:1276–1284.
   PubMed Web of Science ®Google Scholar
• Linta L, Stockmann M, Kleinhans KN, et al. Rat embryonic fibroblasts improve reprogramming of human keratinocytes into induced pluripotent stem cells. Stem Cells Dev. 2012;21(6):965–976.
   PubMed Web of Science ®Google Scholar
• Higelin J, Demestre M, Putz S, et al. FUS mislocalization and vulnerability to DNA damage in ALS patients derived hiPSCs and aging motoneurons. Front Cell Neurosci. 2016;10:290.
   PubMed Web of Science ®Google Scholar
• Shimojo D, Onodera K, Doi-Torii Y, et al. Rapid, efficient, and simple motor neuron differentiation from human pluripotent stem cells. Mol Brain. 2015;8(1):79.
   PubMedGoogle Scholar
• Cooper JM, Ou YH, McMillan EA, et al. TBK1 provides context-selective support of the activated AKT/mTOR pathway in lung cancer. Cancer Res. 2017;77(18):5077–5094.
   PubMed Web of Science ®Google Scholar
• Chen W, Luo K, Ke Z, et al. TBK1 promote bladder cancer cell proliferation and migration via Akt signaling. J Cancer. 2017;8(10):1892–1899.
   PubMed Web of Science ®Google Scholar
• Bjørkøy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005;171(4):603–614.
   PubMed Web of Science ®Google Scholar
• Taylor JP, Tanaka F, Robitschek J, et al. Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum Mol Genet. 2003;12(7):749–757.
   PubMed Web of Science ®Google Scholar
• Miller SB, Mogk A, Bukau B. Spatially organized aggregation of misfolded proteins as cellular stress defense strategy. J Mol Biol. 2015;427(7):1564–1574.
   PubMed Web of Science ®Google Scholar
• Hao Y, Lu Q, Yang G, et al. Lin28a protects against postinfarction myocardial remodeling and dysfunction through Sirt1 activation and autophagy enhancement. Biochem Biophys Res Commun. 2016;479(4):833–840.
   PubMed Web of Science ®Google Scholar
• Sigurdsson V, Takei H, Soboleva S, et al. Bile acids protect expanding hematopoietic stem cells from unfolded protein stress in fetal liver. Cell Stem Cell. 2016 Apr 7;18(4):522–532. doi:10.1016/j.stem.2016.01.002. Epub 2016 Jan 28.
   Web of Science ®Google Scholar
• Kalveram B, Schmidtke G, Groettrup M. The ubiquitin-like modifier FAT10 interacts with HDAC6 and localizes to aggresomes under proteasome inhibition. J Cell Sci. 2008;121:4079–4088.
   PubMed Web of Science ®Google Scholar
• Kawaguchi Y, Kovacs J, McLaurin A, et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell. 2003;115(6):727–738.
   PubMed Web of Science ®Google Scholar
• Evans RM, Mangelsdorf DJ. Nuclear receptors, RXR, and the big bang. Cell. 2014;157(1):255–266.
   PubMed Web of Science ®Google Scholar
• Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007;3(5):452–460.
   PubMed Web of Science ®Google Scholar
• Biazik J, Ylä-Anttila P, Vihinen H, et al. Ultrastractural relationship of the phagophore with surrounding organelles. Autophagy. 2015;11(3):439–451.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yamamoto A, Hatano M, et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol. 2001;152(4):657–668.
   PubMed Web of Science ®Google Scholar
• Lovat PE, Ranalli M, Annichiarrico-Petruzzelli M, et al. Effector mechanisms of fenretinide-induced apoptosis in neuroblastoma. Exp Cell Res. 2000;260(1):50–60.
   PubMed Web of Science ®Google Scholar
• Ulukaya E, Pirianov G, Kurt MA, et al. Fenretinide induces cytochrome c release, caspase 9 activation and apoptosis in the absence of mitochondrial membrane depolarisation. Cell Death Differ. 2003;10(7):856–859.
   PubMed Web of Science ®Google Scholar
• Shintani T, Mizushima N, Ogawa Y, et al. Apg10p, a novel protein-conjugating enzyme essential for autophagy in yeast. Embo J. 1999;8(19):5234–5241.
   Google Scholar
• Mizuno Y, Amari M, Takatama M, et al. Immunoreactivities of p62, an ubiquitin-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
• Sellier C, Campanari ML, Corbier C, et al. Loss of C9ORF72 impairs autophagy and synergizes with polyQ Ataxin-2 to induce motor neuron dysfunction and cell death. Embo J. 2016;35(12):1276–1297.
   PubMed Web of Science ®Google Scholar
• Cha-Molstad H, Lee SH, Kim JG, et al. Regulation of autophagic proteolysis by the N-recognin SQSTM1/p62 of the N-end rule pathway. Autophagy. 2018;14(2):359-361. doi: 10.1080/15548627.2017.1415190. Epub 2018 Jan 29.
   Web of Science ®Google Scholar
• Malm T, Mariani M, Donovan LJ, et al. Activation of the nuclear receptor PPARδ is neuroprotective in a transgenic mouse model of Alzheimer’s disease through inhibition of inflammation. J Neuroinflammation. 2015;12:7.
   PubMed Web of Science ®Google Scholar
• Lv Y, Zhang L, Li N, et al. Geraniol promotes functional recovery and attenuates neuropathic pain in rats with spinal cord injury. Can J Physiol Pharmacol. 2017;23:1–7.
   Google Scholar
• Bajbouj K, Shafarin J, Abdalla MY, et al. Estrogen-induced disruption of intracellular iron metabolism leads to oxidative stress, membrane damage, and cell cycle arrest in MCF-7 cells. Tumour Biol. 2017;39(10):1010428317726184.
   Google Scholar
• Cao H, Xie J, Guo L, et al. All-trans retinoic acid induces autophagic degradation of ubiquitin-like modifier activating enzyme 3 in acute promyelocytic leukemia cells. Leuk Lymphoma. 2017;29:1–9.
   Google Scholar
• Zhong C, Pu LY, Fang MM, et al. Retinoic acid receptor α promotes autophagy to alleviate liver ischemia and reperfusion injury. World J Gastroenterol. 2015;21(43):12381–12391.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdalla, FC, Abeliovich, H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(2):443.
   PubMed Web of Science ®Google Scholar
• Yoshii SR, Mizushima N. Monitoring and measuring autophagy. J Mol Sci. 2017;18(9).
   Google Scholar
• Trocoli A, Bensadoun P, Richard E, et al. p62/SQSTM1 upregulation constitutes a survival mechanism that occurs during granulocytic differentiation of acute myeloid leukemia cells. Cell Death Differ. 2014;21:1852–1861.
   PubMed Web of Science ®Google Scholar
• Trocoli A, Mathieu J, Priault M, et al. ATRA-induced upregulation of Beclin 1 prolongs the life span of differentiated acute promyelocytic leukemia cells. Autophagy. 2011;7:1108–1114.
   PubMed Web of Science ®Google Scholar
• Nemoto T, Tanida I, Tanida-Miyake E, et al. The mouse APG10 homologue, an E2-like enzyme for Apg12p conjugation, facilitates MAP-LC3 modification. J Biol Chem. 2003;278(41):39517–39526.
   PubMed Web of Science ®Google Scholar
• Rubinsztein D, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol. 2012;22(1):R29–R34.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol. 2010;12(3):213–223.
   PubMed Web of Science ®Google Scholar
• Pajares M, Jimenez-Morenoa N, Garcia-Yaguea AJ, et al. Transcription factor NFE2L2/NRF2 is a regulator of macroautophagy genes. Autophagy. 2016;12(10):1902–1916.
   PubMed Web of Science ®Google Scholar
• Matsumoto G, Wada K, Okuno M, et al. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell. 2011;44(2):279–289.
   PubMed Web of Science ®Google Scholar
• Zhou L, Wang H, Ren H, et al. Bcl-2-dependent upregulation of autophagy by sequestosome 1/p62 in vitro. Acta Pharmacol. 2013;34(5):651–656.
   Google Scholar
• Huang S, Okamoto K, Yu C, et al. p62/sequestosome-1 up-regulation promotes ABT-263-induced caspase-8 aggregation/activation on the autophagosome. J Biol Chem. 2013;288(47):33654–33666.
   PubMed Web of Science ®Google Scholar
• Zeng RX, Zhang YB, Fan Y, et al. p62/SQSTM1 is involved in caspase-8 associated cell death induced by proteasome inhibitor MG132 in U87MG cells. Cell Biol Int. 2014;38(10):1221–1226.
   PubMed Web of Science ®Google Scholar
• Teyssou E, Takeda T, Lebon V, et al. Mutations in SQSTM1 encoding p62 in amyotrophic lateral sclerosis: genetics an neuropathology. Acta Neuropathol. 2013;125(4):511–522.
   PubMed Web of Science ®Google Scholar
• Goode A, Rea S, Sultana M, et al. ALS-FTLD associated mutations of SQSTM1 impact on Keap1-Nrf2 signalling. Mol Cell Neurosci. 2016;76:52–58.
   PubMed Web of Science ®Google Scholar
• Maden M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci. 2007;8(10):755–765.
   PubMed Web of Science ®Google Scholar
• Riancho J, Ruiz-Soto M, Berciano MT, et al. Neuroprotective Effect of Bexarotene in the SOD1(G93A) Mouse Model of Amyotrophic Lateral Sclerosis. Front Cell Neurosci. 2015;9:250.
   PubMed Web of Science ®Google Scholar
• Crochemore CL, Virgili M, Bonamassa B, et al. Long-term dietary administration of valproic acid does not affect, while retinoic acid decreases, the lifespan of G93A mice, a model for amyotrophic lateral sclerosis. Muscle Nerve. 2009;39(4):548–552.
   PubMed Web of Science ®Google Scholar
• Cheng CW, Lin MJ, Shen CK. Rapamycin alleviates pathogenesis of a new Drosophila model of ALS-TDP. J Neurogenet. 2015;29(2–3):59–68.
   PubMed Web of Science ®Google Scholar
• Zhang X, Li L, Chen S, et al. Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Autophagy. 2011;7(4):412–425.
   PubMed Web of Science ®Google Scholar
• Saxena S, Roselli F, Singh K, et al. Neuroprotection through excitability and mTOR required in ALS motoneurons to delay disease and extend survival. Neuron. 2013;80(1):80–96.
   PubMed Web of Science ®Google Scholar
• Perera ND, Sheean RK, Lau CL, et al. Rilmenidine promotes MTOR-independent autophagy in the mutant SOD1 mouse model of amyotrophic lateral sclerosis without slowing disease progression. Autophagy. 2018;14(3):534-551. doi:10.1080/15548627.2017.1385674. Epub 2017 Dec 17.
   Web of Science ®Google Scholar
• Ching JK, Ju JS, Pittman SK, et al. Increased autophagy accelerates colchicine-induced muscle toxicity. Autophagy. 2013;9(12):2115–2125.
   PubMed Web of Science ®Google Scholar
• Shams Nooraei M, Noori-Zadeh A, Darabi S, et al. Low level of autophagy-related gene 10 (ATG10) Expression in the 6-Hydroxydopamine Rat Model of Parkinson’s Disease. Iran Biomed J. 2018;22(1):15–21.
   PubMedGoogle Scholar
• Imamura K, Izumi Y, Watanabe A, et al. The Src/c-Abl pathway is a potential therapeutic target in amyotrophic lateral sclerosis. Sci Transl Med. 2017;9(391).
   PubMed Web of Science ®Google Scholar
• Grabrucker AM, Schmeisser MJ, Udvardi PT, et al. Amyloid beta protein-induced zinc sequestration leads to synaptic loss via dysregulation of the ProSAP2/Shank3 scaffold. Mol Neurodegener. 2011;6:65.
   PubMed Web of Science ®Google Scholar
• Villinger C, Schauflinger M, Gregorius M, et al. Three-dimensional imaging of adherent cells using FIB/SEM and STEM. Methods Mol Biol. 2014;1117:617–638.
   PubMedGoogle Scholar
• Huber W, Carey VJ, Gentleman R, et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods. 2015;12:115.
   PubMed Web of Science ®Google Scholar
• Smyth GK. Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, et al., editors. Bioinformatics and computational biology solutions using R and Bioconductor. New York: Springer; 2005. p. 397–420.
   Google Scholar