Distinctive alteration in the expression of autophagy genes in Drosophila models of amyloidopathy and tauopathy

References

• Hayashi SI, Sato N, Yamamoto A, Ikegame Y, Nakashima S, Ogihara T, et al Alzheimer disease-associated peptide, amyloid beta40, inhibits vascular regeneration with induction of endothelial autophagy. Arterioscler Thromb Vasc Biol. 2009;29:1909–15.
   PubMed Web of Science ®Google Scholar
• Caccamo A, Maldonado MA, Majumder S, Medina DX, Holbein W, Magrí A, et al Naturally secreted amyloid-beta increases mammalian target of rapamycin (mTOR) activity via a PRAS40-mediated mechanism. J Biol Chem. 2011;286:8924–32.
   PubMed Web of Science ®Google Scholar
• Esparza TJ, Gangolli M, Cairns NJ, Brody DL. Soluble amyloid-beta buffering by plaques in Alzheimer disease dementia versus high-pathology controls. PLoS One. 2018;13:e0200251.
   PubMed Web of Science ®Google Scholar
• Götz J, Ittner LM, Fändrich M, Schonrock N. Is tau aggregation toxic or protective: a sensible question in the absence of sensitive methods? J Alzheimers Dis. 2008;14:423–9.
   PubMed Web of Science ®Google Scholar
• Bendiske J, Bahr BA. Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis-an approach for slowing Alzheimer disease? J Neuropathol Exp Neurol. 2003;62:451–63.
   PubMed Web of Science ®Google Scholar
• Golpich M, Amini E, Mohamed Z, Azman Ali R, Mohamed Ibrahim N, Ahmadiani A. Mitochondrial dysfunction and biogenesis in neurodegenerative diseases: pathogenesis and treatment. CNS Neurosci Ther. 2017;23:5–22.
   PubMed Web of Science ®Google Scholar
• Schulz KL, Eckert A, Rhein V, Mai S, Haase W, Reichert AS, et al. A new link to mitochondrial impairment in tauopathies. Mol Neurobiol. 2012;46:205–16.
   PubMed Web of Science ®Google Scholar
• Uddin M, Stachowiak A, Mamun AA, Tzvetkov NT, Takeda S, Atanasov AG, et al. Autophagy and Alzheimer’s disease: from molecular mechanisms to therapeutic implications. Front Aging Neurosci 2018;10:4.
   PubMed Web of Science ®Google Scholar
• Chin LS, Olzmann JA, Li L. Aggresome formation and neurodegenerative diseases: therapeutic implications. Curr Med Chem. 2008;15:47–60.
   PubMed Web of Science ®Google Scholar
• Olenick MA, Tokito M, Boczkowska M, Dominguez R, Holzbaur EL. Hook adaptors induce unidirectional processive motility by enhancing the dynein-dynactin interaction. J Biol Chem. 2016;291:18239–51.
   PubMed Web of Science ®Google Scholar
• Hurley JH, Young LN. Mechanisms of autophagy initiation. Annu Rev Biochem. 2017;86:225–44.
   PubMed Web of Science ®Google Scholar
• Fitzwalter BE, Thorburn A. Recent insights into cell death and autophagy. Febs J. 2015;282:4279–88.
   PubMed Web of Science ®Google Scholar
• Shravage BV, Hill JH, Powers CM, Wu L, Baehrecke EH. Atg6 is required for multiple vesicle trafficking pathways and hematopoiesis in Drosophila. Development. 2013;140:1321–9.
   PubMed Web of Science ®Google Scholar
• Reggiori F, Ungermann C. Autophagosome maturation and fusion. J Mol Biol. 2017;429:486–96.
   PubMed Web of Science ®Google Scholar
• Badadani M. Autophagy mechanism, regulation, functions, and disorders. ISRN Cell Biol. 2012;2012:1–11.
   Google Scholar
• Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010;221:117–24.
   PubMed Web of Science ®Google Scholar
• Chai YL, Chong JR, Weng J, Howlett D, Halsey A, Lee JH, et al Lysosomal cathepsin D is upregulated in Alzheimer's disease neocortex and may be a marker for neurofibrillary degeneration. Brain Pathol. 2019;29:63–74.
   PubMed Web of Science ®Google Scholar
• Kuchitsu Y, Fukuda M. Revisiting Rab7 functions in mammalian autophagy: Rab7 knockout studies. Cells 2018;7:215.
   PubMed Web of Science ®Google Scholar
• Fujita N, Huang W, Lin TH, Groulx JF, Jean S, Nguyen J, et al. Genetic screen in Drosophila muscle identifies autophagy-mediated T-tubule remodeling and a Rab2 role in autophagy. Elife. 2017;6:e23367.
   PubMed Web of Science ®Google Scholar
• Lipinski MM, Zheng B, Lu T, Yan Z, Py BF, Ng A, et al Genome-wide analysis reveals mechanisms modulating autophagy in normal brain aging and in Alzheimer's disease. Proc Natl Acad Sci USA. 2010;107:14164–9.
   PubMed Web of Science ®Google Scholar
• Burgoyne JR. Oxidative stress impairs autophagy through oxidation of ATG3 and ATG7. Autophagy 2018;14:1092–3.
   PubMed Web of Science ®Google Scholar
• Kaur U, Banerjee P, Bir A, Sinha M, Biswas A, Chakrabarti S. Reactive oxygen species, redox signaling and neuroinflammation in Alzheimer's disease: the NF-κB connection. Curr Top Med Chem. 2015;15:446–57.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Korolchuk VI, Renna M, Imarisio S, Fleming A, Williams A, et al. Complex inhibitory effects of nitric oxide on autophagy. Mol Cell. 2011;43:19–32.
   PubMed Web of Science ®Google Scholar
• Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, et al. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science. 2001;293:711–4.
   PubMed Web of Science ®Google Scholar
• Tare M, Modi RM, Nainaparampil JJ, Puli OR, Bedi S, Fernandez-Funez P, et al. Activation of JNK signaling mediates amyloid-ss-dependent cell death. PLOS One. 2011;6:e24361.
   PubMed Web of Science ®Google Scholar
• Chouhan AK, Guo C, Hsieh YC, Ye H, Senturk M, Zuo Z, et al. Uncoupling neuronal death and dysfunction in Drosophila models of neurodegenerative disease. Acta Neuropathol Commun. 2016;4:62.
   PubMed Web of Science ®Google Scholar
• Finelli A, Kelkar A, Song HJ, Yang H, Konsolaki M. A model for studying Alzheimer's Abeta42-induced toxicity in Drosophila melanogaster. Mol Cell Neurosci. 2004;26:365–75.
   PubMed Web of Science ®Google Scholar
• Diez-Hermano S, Valero J, Rueda C, Ganfornina MD, Sanchez D. An automated image analysis method to measure regularity in biological patterns: a case study in a Drosophila neurodegenerative model. Mol Neurodegener. 2015;10:9.
   PubMed Web of Science ®Google Scholar
• Madabattula ST, Strautman JC, Bysice AM, O’Sullivan JA, Androschuk A, Rosenfelt C. Quantitative analysis of climbing defects in a Drosophila model of neurodegenerative disorders. J Vis Exp 2015;100:e52741.
   Google Scholar
• Ali YO, Escala W, Ruan K, Zhai RG. Assaying locomotor, learning, and memory deficits in Drosophila models of neurodegeneration. J Vis Exp 2011;49:2504.
   Google Scholar
• Koopmans M, Monroe SS, Coffield LM, Zaki SR. Optimization of extraction and PCR amplification of RNA extracts from paraffin-embedded tissue in different fixatives. J Virol Methods. 1993;43:189–204.
   PubMed Web of Science ®Google Scholar
• Fukatsu T. Acetone preservation: a practical technique for molecular analysis. Mol Ecol. 1999;8:1935–45.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25:402–8.
   PubMed Web of Science ®Google Scholar
• Austin PC, Brunner LJ, Hux JE. Bayeswatch: an overview of Bayesian statistics. J Eval Clin Pract. 2002;8:277–86.
   PubMed Web of Science ®Google Scholar
• Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, et al. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–76.
   PubMed Web of Science ®Google Scholar
• R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. Available at: http://www.R-project.org/.
   Google Scholar
• Szebenyi G, Hall B, Yu R, Hashim AI, Krämer H. Hook2 localizes to the centrosome, binds directly to centriolin/CEP110 and contributes to centrosomal function. Traffic. 2007;8:32–46.
   PubMed Web of Science ®Google Scholar
• Herrmann L, Wiegmann C, Arsalan-Werner A, Hilbrich I, Jäger C, Flach K, et al. Hook proteins: association with Alzheimer pathology and regulatory role of hook3 in amyloid beta generation. PLOS One. 2015;10:e0119423.
   PubMed Web of Science ®Google Scholar
• Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of autophagosome biogenesis. Curr Biol. 2012;22:R29–R34.
   PubMed Web of Science ®Google Scholar
• Simonsen A, Cumming RC, Brech A, Isakson P, Schubert DR, Finley KD. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy 2008;4:176–84.
   PubMed Web of Science ®Google Scholar
• Wu H, Wang MC, Bohmann D. JNK protects Drosophila from oxidative stress by trancriptionally activating autophagy. Mech Dev. 2009;126:624–37.
   PubMed Web of Science ®Google Scholar
• Shpilka T, Weidberg H, Pietrokovski S, Elazar Z. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol. 2011;12:226.
   PubMed Web of Science ®Google Scholar
• Di Domenico F, Tramutola A, Perluigi M. Cathepsin D as a therapeutic target in Alzheimer's disease. Expert Opin Ther Targets. 2016;20:1393–5.
   PubMed Web of Science ®Google Scholar
• Straface E, Matarrese P, Gambardella L, Vona R, Sgadari A, Silveri MC, et al. Oxidative imbalance and cathepsin D changes as peripheral blood biomarkers of Alzheimer disease: a pilot study. FEBS Lett. 2005;579:2759–66.
   PubMed Web of Science ®Google Scholar
• Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science. 1992;256:184–5.
   PubMed Web of Science ®Google Scholar
• Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, et al. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science. 2001;293:1487–91.
   PubMed Web of Science ®Google Scholar
• Rajmohan R, Reddy PH. Amyloid-beta and phosphorylated tau accumulations cause abnormalities at synapses of Alzheimer's disease neurons. J Alzheimers Dis. 2017;57:975–99.
   PubMed Web of Science ®Google Scholar
• Kametani F, Hasegawa M. Reconsideration of amyloid hypothesis and tau hypothesis in Alzheimer's Disease. Front Neurosci. 2018;12:25.
   PubMed Web of Science ®Google Scholar
• Belrose JC, Masoudi R, Michalski B, Fahnestock M. Increased pro-nerve growth factor and decreased brain-derived neurotrophic factor in non-Alzheimer's disease tauopathies. Neurobiol Aging. 2014;35:926–33.
   PubMed Web of Science ®Google Scholar
• Harrison JR, Owen MJ. Alzheimer’s disease: the amyloid hypothesis on trial. Br J Psychiatry 2016;208:1–3.
   PubMed Web of Science ®Google Scholar
• Bretteville A, Planel E. Tau aggregates: toxic, inert, or protective species? J Alzheimers Dis. 2008;14:431–6.
   PubMed Web of Science ®Google Scholar
• Nakamura M, Shiozawa S, Tsuboi D, Amano M, Watanabe H, Maeda S, et al. Pathological progression induced by the frontotemporal dementia-associated R406W tau mutation in patient-derived iPSCs. Stem Cell Reports. 2019;13:684–99.
   PubMed Web of Science ®Google Scholar
• Passarella D, Goedert M. Beta-sheet assembly of tau and neurodegeneration in Drosophila melanogaster. Neurobiol Aging. 2018;72:98–105.
   PubMed Web of Science ®Google Scholar
• Funderburk SF, Marcellino BK, Yue Z. Cell “‘self-eating’ (autophagy) mechanism in Alzheimer's disease”. Mt Sinai J Med. 2010;77:59–68.
   PubMedGoogle Scholar
• Lee JA, Gao FB. Regulation of Abeta pathology by beclin 1: a protective role for autophagy? J Clin Invest. 2008;118:2015–8.
   PubMed Web of Science ®Google Scholar
• Ihara Y, Morishima-Kawashima M, Nixon R. The ubiquitin–proteasome system and the autophagic–lysosomal system in Alzheimer disease. Cold Spring Harb Perspect Med. 2012;2:a006361.
   PubMed Web of Science ®Google Scholar
• Rajaguru P, Vaiphei K, Saikia B, Kochhar R. Increased accumulation of dendritic cells in celiac disease associates with increased expression of autophagy protein LC3. Indian J Pathol Microbiol. 2013;56:342.
   PubMed Web of Science ®Google Scholar
• Vidoni C, Follo C, Savino M, Melone MAB, Isidoro C. The role of cathepsin D in the pathogenesis of human neurodegenerative disorders. Med Res Rev. 2016;36:845–70.
   PubMed Web of Science ®Google Scholar
• Urbanelli L, Emiliani C, Massini C, Persichetti E, Orlacchio A, Pelicci G, et al Cathepsin D expression is decreased in Alzheimer's disease fibroblasts. Neurobiol Aging. 2008;29:12–22.
   PubMed Web of Science ®Google Scholar
• Cataldo AM, Barnett JL, Berman SA, Li J, Quarless S, Bursztajn S, et al Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system. Neuron 1995;14:671–80.
   PubMed Web of Science ®Google Scholar
• McGrath LT, McGleenon BM, Brennan S, McColl D, McIlroy S, Passmore AP. Increased oxidative stress in Alzheimer’s disease as assessed with 4‐hydroxynonenal but not malondialdehyde. QJM. 2001;94:485–90.
   PubMed Web of Science ®Google Scholar
• Christen Y. Oxidative stress and Alzheimer disease. Am J Clin Nutr. 2000;71:621S–9S.
   PubMed Web of Science ®Google Scholar