A novel transgenic zebrafish line allows for in vivo quantification of autophagic activity in neurons

References

• Lee J-A. Neuronal autophagy: a housekeeper or a fighter in neuronal cell survival? Exp Neurobiol. 2012;21(1):1–8.
   PubMedGoogle Scholar
• Jh S, Shim JH, Kim K-H, et al. Neuronal autophagy and neurodegenerative diseases. Exp Mol Med. 2012;44(2):89–98.
   PubMed Web of Science ®Google Scholar
• Maday S. Mechanisms of neuronal homeostasis: autophagy in the axon. Brain Res. 2016 Oct;1649(Pt B):143–150.
   PubMedGoogle Scholar
• Shen W, Ganetzky B. Autophagy promotes synapse development in Drosophila. J Cell Biol. 2009 Oct;187(1):71–79.
   PubMed Web of Science ®Google Scholar
• Hara T, Nakamura K, Matsui M, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006 Apr;441(7095):885–889.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Chiba T, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006 Apr;441(7095):880–884.
   PubMed Web of Science ®Google Scholar
• Boland B, Kumar A, Lee S, et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer’s disease. J Neurosci. 2008 Jul;28(27):6926–6937.
   PubMed Web of Science ®Google Scholar
• Lynch-Day MA, Mao K, Wang K, et al. The role of autophagy in parkinson’s disease. Cold Spring Harb Perspect Med. 2012 Apr;2(4):a009357–a009357.
   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;39(4):221–234.
   PubMed Web of Science ®Google Scholar
• Robak LA, Jansen IE, van Rooij J, et al. International Parkinson’s Disease Genomics Consortium (IPDGC), Heutink P, Shulman JM, IPDGC consortium members. Excessive burden of lysosomal storage disorder gene variants in Parkinson’s disease. Brain. 2017 Nov;140(12):3191–3203.
   PubMed Web of Science ®Google Scholar
• Vogiatzi T, Xilouri M, Vekrellis K, et al. Wild type α-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem. 2008;283(35):23542–23556.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Ohsumi Y. The role of atg proteins in autophagosome formation. Annu Rev Cell Dev Biol. 2011 Nov;27:107–132.
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000;19(21):5720–5728.
   PubMed Web of Science ®Google Scholar
• Yu L, Chen Y, Tooze SA. Autophagy pathway: cellular and molecular mechanisms. Autophagy. 2018;14(2):207–215.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yamamoto A, Matsui M, et al. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004 Mar;15(3):1101–1111.
   PubMed Web of Science ®Google Scholar
• Rusten TE, Lindmo K, Juhász G, et al. Programmed autophagy in the drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell. 2004 Aug;7(2):179–192.
   PubMed Web of Science ®Google Scholar
• Scott RC, Schuldiner O, Neufeld TP. Role and regulation of starvation-induced autophagy in the drosophila fat body. Dev Cell. 2004 Aug;7(2):167–178.
   PubMed Web of Science ®Google Scholar
• He C, Bartholomew CR, Zhou W, et al. Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy. 2009 May;5(4):520–526.
   PubMed Web of Science ®Google Scholar
• Kozol RA, Abrams AJ, James DM, et al. Function over form: modeling groups of inherited neurological conditions in zebrafish. Front Mol Neurosci. 2016;9:55.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008 Feb;451(7182):1069–1075.
   PubMed Web of Science ®Google Scholar
• Kim C-H, Ueshima E, Muraoka O, et al. Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci Lett. 1996;216(2):109–112.
   PubMed Web of Science ®Google Scholar
• Park H-C, Kim C-H, Bae Y-K, et al. Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev Biol. 2000 Nov;227(2):279–293.
   PubMed Web of Science ®Google Scholar
• Zhang L, Yu J, Pan H, et al. Small molecule regulators of autophagy identified by an image-based high-throughput screen. Proc Nat Acad Sci. 2007;104(48):19023–19028.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Perlstein EO, Imarisio S, et al. Small molecules enhance autophagy and reduce toxicity in Huntington’s disease models. Nat Chem Biol. 2007 Jun;3(6):331–338.
   PubMed Web of Science ®Google Scholar
• Balgi AD, Fonseca BD, Donohue E, et al. Screen for chemical modulators of autophagy reveals novel therapeutic inhibitors of mTORC1 signaling. PLoS ONE. 2009 Sep 22;4(9):e7124.
   PubMed Web of Science ®Google Scholar
• Farkas T, Høyer-Hansen M, Jäättelä M. Identification of novel autophagy regulators by a luciferase-based assay for the kinetics of autophagic flux. Autophagy. 2009 Oct;5(7):1018–1025.
   PubMed Web of Science ®Google Scholar
• Kudoh T. A gene expression screen in zebrafish embryogenesis. Genome Res. 2001 Dec;11(12):1979–1987.
   PubMed Web of Science ®Google Scholar
• Ito Y, Tanaka H, Okamoto H, et al. Characterization of neural stem cells and their progeny in the adult zebrafish optic tectum. Dev Biol. 2010 Jun;342(1):26–38.
   PubMed Web of Science ®Google Scholar
• Kamada Y, Funakoshi T, Shintani T, et al. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol. 2000 Sep 18;150(6):1507–1513.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2016 Jan;12(1):1–222. 3rd edition.
   PubMed Web of Science ®Google Scholar
• Wu Y-T, Tan H-L, Shui G, et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem. 2010 Apr 2;285(4):10850–10861.
   PubMedGoogle Scholar
• Heras-Sandoval D, Pérez-Rojas JM, Hernández-Damián J, et al. The role of PI3K/AKT/mTOR pathway in the modulation of autophagy and the clearance of protein aggregates in neurodegeneration. Cell Signal. 2014 Dec 26;26(12):2694.
   PubMed Web of Science ®Google Scholar
• Mauvezin C, Neufeld TP. Bafilomycin A1 disrupts autophagic flux by inhibiting both V-ATPase-dependent acidification and Ca-P60A/SERCA-dependent autophagosome-lysosome fusion. Autophagy. 2015 Jun;11(8):1437–1438.
   PubMed Web of Science ®Google Scholar
• Scarlatti F, Maffei R, Beau I, et al. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ. 2008 Aug;15(8):1318–1329.
   PubMed Web of Science ®Google Scholar
• Spillantini MG, Schmidt ML, Lee VMY, et al. α-Synuclein in Lewy bodies. Nature. 1997 Aug 28;388(6645):839–840.
   PubMed Web of Science ®Google Scholar
• Braak H, Braak E. Pathoanatomy of Parkinson’s disease. J Neurol. 2000 Apr;247(Suppl 2):II3–II10.
   PubMed Web of Science ®Google Scholar
• Stefanis L. α-synuclein in parkinson’s disease. Cold Spring Harb Perspect Med. 2012 Feb;2(2):a009399.
   PubMed Web of Science ®Google Scholar
• Nah J, Yuan J, Jung Y-K. Autophagy in neurodegenerative diseases: from mechanism to therapeutic approach. Mol Cells. 2015 May;38(5):381–389.
   PubMed Web of Science ®Google Scholar
• Biglan KM, Oakes D, Lang AE, et al. A novel design of a Phase III trial of isradipine in early Parkinson disease (STEADY-PD III). Ann Clin Transl Neurol. 2017 May 9;4(6):360–368.
   PubMed Web of Science ®Google Scholar
• Chan CS, Guzman JN, Ilijic E, et al. “Rejuvenation” protects neurons in mouse models of Parkinson’s disease. Nature. 2007 Jun 28;447(7148):1081–1086.
   PubMed Web of Science ®Google Scholar
• Anekonda TS, Quinn JF. Calcium channel blocking as a therapeutic strategy for Alzheimer’s disease: the case for isradipine. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2011 Dec;1812(12):1584–1590.
   PubMed Web of Science ®Google Scholar
• Williams A, Sarkar S, Cuddon P, et al. Novel targets for Huntington’s disease in an mTOR-independent autophagy pathway. Nat Chem Biol. 2008 Mar;4(5):295.
   PubMed Web of Science ®Google Scholar
• Shaker ME, Ghani A, Shiha GE, et al. Nilotinib induces apoptosis and autophagic cell death of activated hepatic stellate cells via inhibition of histone deacetylases. Biochim Biophys Acta, Mol Cell Res. 2013 Aug;1833(8):1992–1993.
   Web of Science ®Google Scholar
• Yu H-C, Lin C-S, Tai W-T, et al. Nilotinib induces autophagy in hepatocellular carcinoma through AMPK activation. J Biol Chem. 2013 Jun 21;288(25):18249–18259.
   PubMed Web of Science ®Google Scholar
• Hebron ML, Lonskaya I, Moussa CEH. Nilotinib reverses loss of dopamine neurons and improves motor behavior via autophagic degradation of α-synuclein in Parkinson’s disease models. Hum Mol Genet. 2013 Aug 14;22(16):3315–3328.
   PubMed Web of Science ®Google Scholar
• Karuppagounder SS, Brahmachari S, Lee Y, et al. The c-Abl inhibitor, nilotinib, protects dopaminergic neurons in a preclinical animal model of Parkinson’s disease. Sci Rep. 2014 May;2(4):4874.
   Google Scholar
• Menzies FM, Fleming A, Rubinsztein DC. Compromised autophagy and neurodegenerative diseases. Nat Rev Neurosci. 2015 Jun;16(6):345–357.
   PubMed Web of Science ®Google Scholar
• Xi Y, Noble S, Ekker M. Modeling neurodegeneration in Zebrafish. Curr Neurol Neurosci Rep. 2011 Jun;11(3):274–282.
   PubMed Web of Science ®Google Scholar
• Prabhudesai S, Sinha S, Attar A, et al. “Molecular Tweezer” inhibitor of α-synuclein neurotoxicity in vitro and in vivo. Neurotherapeutics. 2012 Apr;9(2):464–476.
   PubMed Web of Science ®Google Scholar
• Bai Q, Burton EA. Zebrafish models of tauopathy. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2011 Mar;1812(3):353–363.
   PubMed Web of Science ®Google Scholar
• Lopez A, Lee SE, Wojta K, et al. A152T tau allele causes neurodegeneration that can be ameliorated in a zebrafish model by autophagy induction. Brain. 2017 Apr 1;140(4):1128–1146.
   PubMedGoogle Scholar
• Bandmann O, Burton EA. Genetic zebrafish models of neurodegenerative diseases. Neurobiol Dis. 2010 Oct;40(1):58–65.
   PubMed Web of Science ®Google Scholar
• Paquet D, Bhat R, Sydow A, et al. A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest. 2009 May;119(5):1382–1395.
   PubMed Web of Science ®Google Scholar
• Fleming A, Rubinsztein DC. Zebrafish as a model to understand autophagy and its role in neurological disease. Biochim Biophys Acta (BBA) - Mol Basis Dis. 2011 Apr;1812(4):520–526.
   PubMed Web of Science ®Google Scholar
• Varga M, Fodor E, Vellai T. Autophagy in zebrafish. Methods. 2015 Mar;75:172–180.
   PubMed Web of Science ®Google Scholar
• Mathai BJ, Meijer AH, Simonsen A. Studying autophagy in Zebrafish. Cells. 2017 Jul 9;6(3).
   PubMed Web of Science ®Google Scholar
• Hu Z-Y, Chen B, Zhang J-P, et al. Up-regulation of autophagy-related gene 5 (ATG5) protects dopaminergic neurons in a zebrafish model of Parkinson’s disease. J Biol Chem. 2017 Nov 3;292(44):18062–18074.
   PubMed Web of Science ®Google Scholar
• Watchon M, Yuan KC, Mackovski N, et al. Calpain inhibition is protective in machado–joseph disease zebrafish due to induction of autophagy. J Neurosci. 2017 Aug 9;37(32):7782–7794.
   PubMed Web of Science ®Google Scholar
• Swart C, Khoza A, Khan K, et al. Investigating basal autophagic activity in brain regions associated with neurodegeneration using in vivo and ex vivo models. J Alzheimer’s Dis Parkinsonism. 2017;07(4).
   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 Sep-Oct;3(5):452–460.
   PubMed Web of Science ®Google Scholar
• Kwan KM, Fujimoto E, Grabher C, et al. The Tol2kit: A multisite gateway-based construction kit forTol2 transposon transgenesis constructs. Dev Dyn. 2007 Nov;236(11):3088–3099.
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012 Jun 28;9(7):676–682.
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012 Jul;9(7):671–675.
   PubMed Web of Science ®Google Scholar
• Asi YT, Simpson JE, Heath PR, et al. Alpha-synuclein mRNA expression in oligodendrocytes in MSA. Glia. 2014 Jun;62(6):964–970.
   PubMed Web of Science ®Google Scholar
• Chiou W-F. Effect of Aβ exposure on the mRNA expression patterns of voltage-sensitive calcium channel α1 subunits (α1A–α1D) in human SK-N-SH neuroblastoma. Neurochem Int. 2006 Aug;49(3):256–261.
   PubMed Web of Science ®Google Scholar
• Sousa SR, Vetter I, Ragnarsson L, et al. Expression and pharmacology of endogenous cav channels in SH-SY5Y human neuroblastoma cells. PLoS ONE. 2013 Mar 25;8(3):e59293–11. Dryer SE, editor.
   PubMed Web of Science ®Google Scholar