Design and validation of a reporter mouse to study the dynamic regulation of TFEB and TFE3 activity through in vivo imaging techniques

References

• Steingrímsson E, Copeland NG, Jenkins NA. Melanocytes and the microphthalmia transcription factor network. Ann Rev Genet. 2004;38(1):365–411. doi: 10.1146/annurev.genet.38.072902.092717 PubMed PMID: 15568981.
   PubMedGoogle Scholar
• Palmieri M, Impey S, Kang H, et al. Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet. 2011 Oct 1;20(19):3852–3866. doi:10.1093/hmg/ddr306 PubMed PMID: 21752829.
   PubMed Web of Science ®Google Scholar
• Sardiello M, Palmieri M, Di RA, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009, Jul 24;325(5939):473–477. doi: 10.1126/science.1174447 PubMed PMID: 19556463.
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011, Jun 17;332(6036):1429–1433. doi: 10.1126/science.1204592 PubMed PMID: 21617040.
   PubMed Web of Science ®Google Scholar
• Aksan I, Goding CR. Targeting the microphthalmia basic helix-loop-helix–leucine zipper transcription factor to a subset of E-box elements in vitro and in vivo. Mol Cell Biol. 1998 Dec;18(12):6930–6938. doi: 10.1128/MCB.18.12.6930 PubMed PMID: 9819381.
   PubMed Web of Science ®Google Scholar
• Mansueto G, Armani A, Viscomi C, et al. Transcription Factor EB Controls Metabolic Flexibility during Exercise. Cell Metab. 2017; 25(1):182–196. doi: 10.1016/j.cmet.2016.11.003 PubMed PMID: 28011087.
   PubMed Web of Science ®Google Scholar
• Martina JA, Diab HI, Lishu L, et al. The nutrient-responsive transcription factor TFE3 promotes autophagy, lysosomal biogenesis, and clearance of cellular debris. Sci Signal. 2014 Jan 21;7(309):ra9–ra9. doi: 10.1126/scisignal.2004754 PubMed PMID: 24448649.
   PubMed Web of Science ®Google Scholar
• Pastore N, Vainshtein A, Klisch TJ, et al. TFE 3 regulates whole‐body energy metabolism in cooperation with TFEB. EMBO Mol Med. 2017 May;9(5):605–621. doi: 10.15252/emmm.201607204 PubMed PMID: 28283651.
   PubMed Web of Science ®Google Scholar
• Puertollano R, Ferguson SM, Brugarolas J, et al. The complex relationship between TFEB transcription factor phosphorylation and subcellular localization. EMBO J. 2018 Jun; 1;37(11):e98804. doi: 10.15252/embj.201798804 PubMed PMID: 29764979.
   PubMed Web of Science ®Google Scholar
• Pastore N, Huynh T, Herz NJ, et al. TFEB regulates murine liver cell fate during development and regeneration. Nat Commun. 2020 18;11(1):2461. doi:10.1038/s41467-020-16300-x PubMed PMID: 32424153.
   PubMed Web of Science ®Google Scholar
• Settembre C, De Cegli R, Mansueto G, et al. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat Cell Biol. 2013 Jun 1;15(6):647–658. doi:10.1038/ncb2718. PubMed PMID: 23604321.
   PubMed Web of Science ®Google Scholar
• Yoneshima E, Okamoto K, Sakai E, et al. The transcription factor EB (TFEB) regulates osteoblast differentiation through ATF4/CHOP‐dependent pathway. J Cell Physiol. 2016 Jun;231(6):1321–1333. doi: 10.1002/jcp.25235 PubMed PMID: 26519689.
   PubMed Web of Science ®Google Scholar
• Pastore N, Brady OA, Diab HI, et al. TFEB and TFE3 cooperate in the regulation of the innate immune response in activated macrophages. Autophagy. 2016 Aug 2;12(8):1240–1258. doi:10.1080/15548627.2016.1179405. PubMed PMID: 27171064.
   PubMed Web of Science ®Google Scholar
• Orfali N, O’Donovan TR, Cahill MR, et al. All‐trans retinoic acid (ATRA)‐induced TFEB expression is required for myeloid differentiation in acute promyelocytic leukemia (APL). Eur J Haematol. 2020 Mar;104(3):236–250. doi: 10.1111/ejh.13367 PubMed PMID: 31811682.
   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 Oct 6;32(1):255. doi: 10.1146/annurev-cellbio-111315-125407 PubMed PMID: 27298091.
   PubMedGoogle Scholar
• Visvikis O, Ihuegbu N, Labed SA, et al. Innate host defense requires TFEB-mediated transcription of cytoprotective and antimicrobial genes. Immunity. 2014 Jun 19;40(6):896–909. doi: 10.1016/j.immuni.2014.05.002 PubMed PMID: 24882217.
   PubMed Web of Science ®Google Scholar
• Nezich CL, Wang C, Fogel AI, et al. MiT/TFE transcription factors are activated during mitophagy downstream of parkin and Atg5. J Cell Bio. 2015 Aug 3;210(3):435–450. doi: 10.1083/jcb.201501002 PubMed PMID: 26240184.
   PubMed Web of Science ®Google Scholar
• Martina JA, Diab HI, Brady OA, et al. TFEB and TFE 3 are novel components of the integrated stress response. EMBO J. 2016 Mar 1;35(5): 479–495. doi: 10.15252/embj.201593428 PubMed PMID: 26813791.
   PubMed Web of Science ®Google Scholar
• Cinque L, De Leonibus C, Iavazzo M, et al. MiT/ TFE factors control ER-phagy via transcriptional regulation of FAM 134B. EMBO J. 2020 Sep 1;39(17):e105696. doi: 10.15252/embj.2020105696 PubMed PMID: 32716134.
   PubMed Web of Science ®Google Scholar
• Napolitano G, Ballabio A. TFEB at a glance. J Cell Sci. 2016 Jul 1;129(13):2475–2481. doi: 10.1242/jcs.146365 PubMed PMID: 27252382.
   PubMed Web of Science ®Google Scholar
• Medina DL, Fraldi A, Bouche V, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell. 2011 Sep13;21(3):421–430. 10.1016/j.devcel.2011.07.016 PubMed PMID: 21889421.
   PubMed Web of Science ®Google Scholar
• Song W, Wang F, Savini M, et al. TFEB regulates lysosomal proteostasis. Hum Mol Genet. 2013 May 15;22(10):1994–2009. 10.1093/hmg/ddt052 PubMed PMID: 23393155.
   PubMed Web of Science ®Google Scholar
• Dehay B, Bové J, Rodríguez-Muela N, et al. Pathogenic lysosomal depletion in Parkinson’s disease. J Neurosci. 2010 Sep 15;30(37):12535–12544. doi: 10.1523/JNEUROSCI.1920-10.2010 PubMed PMID: 20844148.
   PubMed Web of Science ®Google Scholar
• Decressac M, Mattsson B, Weikop P, et al. TFEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity. Proc Natl Acad Sci. 2013 May 7;110(19):E1817–26. doi: 10.1073/pnas.1305623110 PubMed PMID: 23610405.
   PubMed Web of Science ®Google Scholar
• Kilpatrick K, Zeng Y, Hancock T, et al. Genetic and chemical activation of TFEB mediates clearance of aggregated α-synuclein. PloS One. 2015 Mar19;10(3):1–21. doi: 10.1371/journal.pone.0120819 PubMed PMID: 25790376.
   Web of Science ®Google Scholar
• Polito VA, Li H, Martini‐Stoica H, et al. Selective clearance of aberrant tau proteins and rescue of neurotoxicity by transcription factor EB. EMBO Mol Med. 2014 Sep;6(9):1142–1160. doi: 10.15252/emmm.201303671 PubMed PMID: 25069841.
   PubMed Web of Science ®Google Scholar
• Xiao Q, Yan P, Ma X, et al. Enhancing astrocytic lysosome biogenesis facilitates Aβ clearance and attenuates amyloid plaque pathogenesis. J Neurosci. 2014 Jul 16;34(29):9607–9620. doi:10.1523/JNEUROSCI.3788-13.2014. PubMed PMID: 25031402.
   PubMed Web of Science ®Google Scholar
• Chauhan S, Ahmed Z, Bradfute SB, et al. Pharmaceutical screen identifies novel target processes for activation of autophagy with a broad translational potential. Nat Commun. 2015 Oct 27;6(1):8620. 10.1038/ncomms9620 PubMed PMID: 26503418.
   PubMedGoogle Scholar
• Tsunemi T, Ashe TD, Morrison BE, et al. PGC-1α rescues Huntington’s disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci Transl Med. 2012 Jul 11;4(142):ra14297–ra14297. doi: 10.1126/scitranslmed.3003799 PubMed PMID: 22786682.
   Web of Science ®Google Scholar
• Rudnick DA, Perlmutter DH. α1‐Antitrypsin deficiency. Liver Biol Pathobiol. 2020 Jul 28;2:645–658. PubMed PMID: 27465791.
   Google Scholar
• Grunseich C, Fischbeck KH. Molecular pathogenesis of spinal bulbar muscular atrophy (Kennedy’s disease) and avenues for treatment. Curr Opin Neurol. 2020 Oct;33(5):629. doi: 10.1097/WCO.0000000000000856 PubMed PMID: 32773451.
   PubMed Web of Science ®Google Scholar
• Lang M, Schmidt LS, Wilson KM, et al. High-throughput and targeted drug screens identify pharmacological candidates against MiT-translocation renal cell carcinoma. J Exp Clin Cancer Res. 2023 Apr 25;42(1):99. doi: 10.1186/s13046-023-02667-4 PubMed PMID: 37095531.
   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 Sep;585(7826):597–602. doi: 10.1038/s41586-020-2444-0 PubMed PMID: 32612235.
   PubMed Web of Science ®Google Scholar
• Alesi N, Akl EW, Khabibullin D, et al. TSC2 regulates lysosome biogenesis via a non-canonical RAGC and TFEB-dependent mechanism. Nat Commun. 2021 Jul 12;12(1):4245. doi: 10.1038/s41467-021-24499-6 PubMed PMID: 34253722.
   PubMed Web of Science ®Google Scholar
• Asrani K, Woo J, Mendes AA, et al. An mTORC1-mediated negative feedback loop constrains amino acid-induced FLCN-Rag activation in renal cells with TSC2 loss. Nat Commun. 2022 Nov 10;13(1):6808. doi: 10.1038/s41467-022-34617-7 PubMed PMID: 36357396.
   PubMed Web of Science ®Google Scholar
• Garraway LA, Widlund HR, Rubin MA, et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature. 2005 Jul 7;436(7047):117–122. doi: 10.1038/nature03664 PubMed PMID: 16001072.
   PubMed Web of Science ®Google Scholar
• Song J-X, Liu J, Jiang Y, et al. Transcription factor EB: an emerging drug target for neurodegenerative disorders. Drug Discov Today. 2021 Jan;26(1):164–172. doi: 10.1016/j.drudis.2020.10.013 PubMed PMID: 33099023.
   PubMed Web of Science ®Google Scholar
• Kelkar M, De A. Bioluminescence based in vivo screening technologies. Curr Opin Pharmacol. 2012 Oct;12(5):592–600. doi: 10.1016/j.coph.2012.07.014 PubMed PMID: 22954534.
   PubMed Web of Science ®Google Scholar
• Pathmanathan S, Grozavu I, Lyakisheva A, et al. Drugging the undruggable proteins in cancer: a systems biology approach. Curr Opin Chem Biol. 2022 Feb;66:102079. doi: 10.1016/j.cbpa.2021.07.004 PubMed PMID: 34426091.
   PubMed Web of Science ®Google Scholar
• Biserni A, Giannessi F, Sciarroni AF, et al. In vivo imaging reveals selective peroxisome proliferator activated receptor modulator activity of the synthetic ligand 3-(1-(4-chlorobenzyl)-3-t-butylthio-5-isopropylindol-2-yl)-2, 2-dimethylpropanoic acid (MK-886). Mol Pharmacol. 2008 May;73(5):1434–1443. doi: 10.1124/mol.107.042689 PubMed PMID: 18292206.
   PubMed Web of Science ®Google Scholar
• Della Torre S, Biserni A, Rando G, et al. The conundrum of estrogen receptor oscillatory activity in the search for an appropriate hormone replacement therapy. Endocrinology. 2011 Jun;152(6):2256–2265. doi: 10.1210/en.2011-0173 PubMed PMID: 21505049.
   PubMed Web of Science ®Google Scholar
• Maggi A, Ciana P. Reporter mice and drug discovery and development. Nat Rev Drug Discov. 2005 Mar;4(3):249–255. doi: 10.1038/nrd1661 PubMed PMID: 15738979.
   PubMed Web of Science ®Google Scholar
• Maggi A, Ottobrini L, Biserni A, et al. Techniques: reporter mice–a new way to look at drug action. Trends Pharmacol Sci. 2004 Jun;25(6):337–342. doi: 10.1016/j.tips.2004.04.007 PubMed PMID: 15165750.
   PubMed Web of Science ®Google Scholar
• Fan F, Paguio A, Garvin D, et al. Using luciferase assays to study G-protein-coupled receptor pathways and screen for GPCR modulators. Lumin. 2005;10:1.
   Google Scholar
• Shaner NC, Campbell RE, Steinbach PA, et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol. 2004 Dec;22(12):1567–1572. doi: 10.1038/nbt1037 PubMed PMID: 15558047.
   PubMed Web of Science ®Google Scholar
• Trichas G, Begbie J, Srinivas S. Use of the viral 2A peptide for bicistronic expression in transgenic mice. BMC Biol. 2008 Sep 15;6(1):1–13. doi: 10.1186/1741-7007-6-40 PubMed PMID: 18793381.
   PubMedGoogle Scholar
• Cortes CJ, Miranda HC, Frankowski H, et al. Polyglutamine-expanded androgen receptor interferes with TFEB to elicit autophagy defects in SBMA. Nat Neurosci. 2014 Sep;17(9):1180–1189. doi: 10.1038/nn.3787 PubMed PMID: 25108912.
   PubMed Web of Science ®Google Scholar
• Hemesath TJ, Steingrímsson E, McGill G, et al. Microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes Dev. 1994 Nov15;8(22):2770–2780. doi: 10.1101/gad.8.22.2770 PubMed PMID: 7958932.
   PubMed Web of Science ®Google Scholar
• Pogenberg V, Ögmundsdóttir MH, Bergsteinsdóttir K, et al. Restricted leucine zipper dimerization and specificity of DNA recognition of the melanocyte master regulator MITF. Genes Dev. 2012 Dec 1;26(23):2647–2658. doi: 10.1101/gad.198192.112 PubMed PMID: 23207919.
   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 Jun 1;5(228):ra42–ra42. doi: 10.1126/scisignal.2002790 PubMed PMID: 22692423.
   PubMed Web of Science ®Google Scholar
• Rizzi N, Brunialti E, Cerri S, et al. In vivo imaging of early signs of dopaminergic neuronal death in an animal model of Parkinson’s disease. Neurobiol Dis. 2018 Jun 1;114:74–84. doi: 10.1016/j.nbd.2018.02.005 PubMed PMID: 29486298.
   PubMed Web of Science ®Google Scholar
• Palmieri M, Pal R, Sardiello M. AKT modulates the autophagy-lysosome pathway via TFEB. Cell Cycle. 2017 Jul 3;16(13):1237. doi: 10.1080/15384101.2017.1337968 PubMed PMID: 28636416.
   PubMed Web of Science ®Google Scholar
• McNeill A, Magalhaes J, Shen C, et al. Ambroxol improves lysosomal biochemistry in glucocerebrosidase mutation-linked parkinson disease cells. Brain. 2014 May;137(5):1481–1495. doi: 10.1093/brain/awu020 PubMed PMID: 24574503.
   PubMed Web of Science ®Google Scholar
• Rizzi N, Rebecchi M, Levandis G, et al. Identification of novel loci for the generation of reporter mice. Nucleic Acids Res. 2017 Apr 7;45(6):e37. 10.1093/nar/gkw1142 PubMed PMID: 27899606.
   PubMed Web of Science ®Google Scholar
• Sun F-L, Elgin SCR. Putting boundaries on silence. Cell. 1999 Nov 24;99(5):459–462. doi: 10.1016/S0092-8674(00)81534-2 PubMed PMID: 10589674.
   PubMed Web of Science ®Google Scholar
• Ciana P, Di Luccio G, Belcredito S, et al. Engineering of a mouse for the in vivo profiling of estrogen receptor activity. Mol Endocrinol. 2001 Jul 1;15(7):1104–1113. doi: 10.1210/mend.15.7.0658 PubMed PMID: 11435611.
   PubMedGoogle Scholar
• Schwenk F, Baron U, Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 1995 Dec25;23(24):5080. doi: 10.1093/nar/23.24.5080 PubMed PMID: 8559668.
   PubMed Web of Science ®Google Scholar
• Settembre C, Zoncu R, Medina DL, et al. A lysosome‐to‐nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 2012 Mar 7;31(5):1095–1108. doi: 10.1038/emboj.2012.32 PubMed PMID: 22343943.
   PubMed Web of Science ®Google Scholar
• Bonnet M-E, Erbacher P, Bolcato-Bellemin A-L. Systemic delivery of DNA or siRNA mediated by linear polyethylenimine (L-PEI) does not induce an inflammatory response. Pharm Res. 2008 Dec;25(12):2972–2982. doi: 10.1007/s11095-008-9693-1 PubMed PMID: 18709489.
   PubMed Web of Science ®Google Scholar
• Liu Q, Chang JW, Wang J, et al. Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl) phenyl)-9-(quinolin-3-yl) benzo [h][1, 6] naphthyridin-2 (1 H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J Med Chem. 2010 Oct 14;53(19):7146–7155. doi: 10.1021/jm101144f PubMed PMID: 20860370.
   PubMed Web of Science ®Google Scholar
• Medina DL, Settembre C, Ballabio A. Methods to monitor and manipulate TFEB activity during autophagy methods in enzymology. Elsevier. 2017 Jan 1;588:61–78. PubMed PMID: 28237119.
   Google Scholar
• Jiao F, Zhou B, Meng L. The regulatory mechanism and therapeutic potential of transcription factor EB in neurodegenerative diseases. CNS Neurosci Ther. 2023 Jan;29(1):37–59. doi: 10.1111/cns.13985 PubMed PMID: 36184826.
   PubMed Web of Science ®Google Scholar
• Lu H, Sun J, Hamblin MH, et al. Transcription factor EB regulates cardiovascular homeostasis. EBioMedicine. 2021 Jan 1;63:103207. doi: 10.1016/j.ebiom.2020.103207 PubMed PMID: 33418500.
   PubMed Web of Science ®Google Scholar
• Di Malta C, Zampelli A, Granieri L, et al. TFEB and TFE3 drive kidney cystogenesis and tumorigenesis. EMBO Mol Med. 2023 May 8;15(15):e16877. doi: 10.15252/emmm.202216877 PubMed PMID: 36987696.
   PubMedGoogle Scholar
• Lin Y, Shi Q, Yang G, et al. A small-molecule drug inhibits autophagy gene expression through the central regulator TFEB. Proc Natl Acad Sci. 2023 Feb 14;120(7): e2213670120. doi: 10.1073/pnas.2213670120 PubMed PMID: 36749723.
   PubMed Web of Science ®Google Scholar
• Zhao B, Dierichs L, Gu J-N, et al. TFEB-mediated lysosomal biogenesis and lysosomal drug sequestration confer resistance to MEK inhibition in pancreatic cancer. Cell Death Discov. 2020 Mar 11;6(1):12. doi: 10.1038/s41420-020-0246-7 PubMed PMID: 32194992.
   PubMed Web of Science ®Google Scholar
• Ciana P, Biserni A, Tatangelo L, et al. A novel peroxisome proliferator-activated receptor responsive element-luciferase reporter mouse reveals gender specificity of peroxisome proliferator-activated receptor activity in liver. Mol Endocrinol. 2007 Feb 1;21(2):388–400. doi: 10.1210/me.2006-0152 PubMed PMID: 17158222.
   PubMedGoogle Scholar
• Dehghani H, Guggenheim JA, Taylor SL, et al. Quantitative bioluminescence tomography using spectral derivative data. Biomed Opt Express. 2018 Sep 1;9(9):4163–74. doi: 10.1364/BOE.9.004163 PubMed PMID: 30615705.
   PubMed Web of Science ®Google Scholar
• Alencar GF, Owsiany KM, Karnewar S, et al. Stem cell pluripotency genes Klf4 and Oct4 regulate complex SMC phenotypic changes critical in late-stage atherosclerotic lesion pathogenesis. Circulation. 2020 Nov 24;142(21):2045–59. doi: 10.1161/CIRCULATIONAHA.120.046672 PubMed PMID: 32674599.
   PubMed Web of Science ®Google Scholar
• Martini-Stoica H, Xu Y, Ballabio A, et al. The autophagy-lysosomal pathway in neurodegeneration: a TFEB perspective. Trends Neurosci. 2016 Apr 1;39(4):221–234. doi: 10.1016/j.tins.2016.02.002 PubMed PMID: 26968346.
   PubMed Web of Science ®Google Scholar
• Silbereis JC, Pochareddy S, Zhu Y, et al. The cellular and molecular landscapes of the developing human central nervous system. Neuron. 2016 Jan 20;89(2):248–68. doi: 10.1016/j.neuron.2015.12.008 PubMed PMID: 26796689.
   PubMed Web of Science ®Google Scholar
• Brunialti E, Villa A, Mekhaeil M, et al. Inhibition of microglial β-glucocerebrosidase hampers the microglia-mediated antioxidant and protective response in neurons. J Neuroinflammation. 2021 Dec;18(1):1–8. doi: 10.1186/s12974-021-02272-2 PubMed PMID: 34551802.
   PubMed Web of Science ®Google Scholar