Differential regulation of autophagy during metabolic stress in astrocytes and neurons

References

• Yin Z, Pascual C, Klionsky DJ. Autophagy: machinery and regulation. Microb Cell. 2016;3:588–596.
   PubMed Web of Science ®Google Scholar
• Dikic I, Elazar Z. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol. 2018;19:349–364.
   PubMed Web of Science ®Google Scholar
• Schneider JL, Cuervo AM. Autophagy and human disease: emerging themes. Curr Opin Genet Dev. 2014;26:16–23.
   PubMed Web of Science ®Google Scholar
• Yamamoto A, Yue Z. Autophagy and its normal and pathogenic states in the brain. Annu Rev Neurosci. 2014;37:55–78.
   PubMed Web of Science ®Google Scholar
• Maday S. Mechanisms of neuronal homeostasis: autophagy in the axon. Brain Res. 2016;1649:143–150.
   PubMed Web of Science ®Google Scholar
• Jiang P, Mizushima N. Autophagy and human diseases. Cell Res. 2014;24:69–79.
   PubMed Web of Science ®Google Scholar
• Kulkarni VV, Maday S. Compartment-specific dynamics and functions of autophagy in neurons. Dev Neurobiol. 2018;78:298–310.
   PubMed Web of Science ®Google Scholar
• Kulkarni A, Chen J, Maday S. Neuronal autophagy and intercellular regulation of homeostasis in the brain. Curr Opin Neurobiol. 2018;51:29–36.
   PubMed Web of Science ®Google Scholar
• Ariosa AR, Klionsky DJ. Autophagy core machinery: overcoming spatial barriers in neurons. J Mol Med (Berl). 2016;94:1217–1227.
   PubMed Web of Science ®Google Scholar
• Fuger P, Hefendehl JK, Veeraraghavalu K, et al. Microglia turnover with aging and in an Alzheimer’s model via long-term in vivo single-cell imaging. Nat Neurosci. 2017;20:1371–1376.
   PubMed Web of Science ®Google Scholar
• Harris JJ, Attwell D. The energetics of CNS white matter. J Neurosci. 2012;32:356–371.
   PubMed Web of Science ®Google Scholar
• Cajigas IJ, Will T, Schuman EM. Protein homeostasis and synaptic plasticity. Embo J. 2010;29:2746–2752.
   PubMed Web of Science ®Google Scholar
• Vijayan V, Verstreken P. Autophagy in the presynaptic compartment in health and disease. J Cell Biol. 2017;216:1895–1906.
   PubMed Web of Science ®Google Scholar
• Stavoe AK, Hill SE, Hall DH, et al. KIF1A/UNC-104 transports ATG-9 to regulate neurodevelopment and autophagy at synapses. Dev Cell. 2016;38:171–185.
   PubMed Web of Science ®Google Scholar
• Dragich JM, Kuwajima T, Hirose-Ikeda M, et al. Autophagy linked FYVE (Alfy/WDFY3) is required for establishing neuronal connectivity in the mammalian brain. ELife. 2016;5: e14810.
   PubMed Web of Science ®Google Scholar
• Shen W, Ganetzky B. Autophagy promotes synapse development in Drosophila. J Cell Biol. 2009;187:71–79.
   PubMed Web of Science ®Google Scholar
• Tang G, Gudsnuk K, Kuo SH, et al. Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron. 2014;83:1131–1143.
   PubMed Web of Science ®Google Scholar
• Wang S, Li B, Qiao H, et al. Autophagy-related gene Atg5 is essential for astrocyte differentiation in the developing mouse cortex. EMBO Rep. 2014;15:1053–1061.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Cho MH, Shim WH, et al. Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects. Mol Psychiatry. 2017;22:1576–1584.
   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;441:880–884.
   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;441:885–889.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Wang QJ, Holstein GR, et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci U S A. 2007;104:14489–14494.
   PubMed Web of Science ®Google Scholar
• Nishiyama J, Miura E, Mizushima N, et al. Aberrant membranes and double-membrane structures accumulate in the axons of Atg5-null Purkinje cells before neuronal death. Autophagy. 2007;3:591–596.
   PubMed Web of Science ®Google Scholar
• Rudnick ND, Griffey CJ, Guarnieri P, et al. Distinct roles for motor neuron autophagy early and late in the SOD1G93A mouse model of ALS. Proc Natl Acad Sci U S A. 2017;114:E8294–E303.
   PubMed Web of Science ®Google Scholar
• Hernandez D, Torres CA, Setlik W, et al. Regulation of presynaptic neurotransmission by macroautophagy. Neuron. 2012;74:277–284.
   PubMed Web of Science ®Google Scholar
• Glatigny M, Moriceau S, Rivagorda M, et al. Autophagy is required for memory formation and reverses age-related memory decline. Curr Biol. 2019;29:435–48 e8.
   PubMed Web of Science ®Google Scholar
• Gomez-Sanchez JA, Carty L, Iruarrizaga-Lejarreta M, et al. Schwann cell autophagy, myelinophagy, initiates myelin clearance from injured nerves. J Cell Biol. 2015;210:153–168.
   PubMed Web of Science ®Google Scholar
• Jang SY, Shin YK, Park SY, et al. Autophagic myelin destruction by schwann cells during wallerian degeneration and segmental demyelination. Glia. 2016;64:730–742.
   PubMed Web of Science ®Google Scholar
• Ries M, Sastre M. Mechanisms of abeta clearance and degradation by glial cells. Front Aging Neurosci. 2016;8:160.
   PubMed Web of Science ®Google Scholar
• Lucin KM, O’Brien CE, Bieri G, et al. Microglial beclin 1 regulates retromer trafficking and phagocytosis and is impaired in Alzheimer’s disease. Neuron. 2013;79:873–886.
   PubMed Web of Science ®Google Scholar
• Cho MH, Cho K, Kang HJ, et al. Autophagy in microglia degrades extracellular beta-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy. 2014;10:1761–1775.
   PubMed Web of Science ®Google Scholar
• Maday S, Wallace KE, Holzbaur EL. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol. 2012;196:407–417.
   PubMed Web of Science ®Google Scholar
• Maday S, Holzbaur EL. Autophagosome biogenesis in primary neurons follows an ordered and spatially regulated pathway. Dev Cell. 2014;30:71–85.
   PubMed Web of Science ®Google Scholar
• Maday S, Holzbaur EL. Compartment-specific regulation of autophagy in primary neurons. J Neurosci. 2016;36:5933–5945.
   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;15:1101–1111.
   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;19:5720–5728.
   PubMed Web of Science ®Google Scholar
• Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010;119:7–35.
   PubMed Web of Science ®Google Scholar
• Thoreen CC, Kang SA, Chang JW, et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem. 2009;284:8023–8032.
   PubMed Web of Science ®Google Scholar
• Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282:24131–24145.
   PubMed Web of Science ®Google Scholar
• Laplante M, Sabatini DM. mTOR signaling at a glance. J Cell Sci. 2009;122:3589–3594.
   PubMed Web of Science ®Google Scholar
• Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;168:960–976.
   PubMed Web of Science ®Google Scholar
• Kochl R, Hu XW, Chan EY, et al. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic. 2006;7:129–145.
   PubMed Web of Science ®Google Scholar
• Sahani MH, Itakura E, Mizushima N. Expression of the autophagy substrate SQSTM1/p62 is restored during prolonged starvation depending on transcriptional upregulation and autophagy-derived amino acids. Autophagy. 2014;10:431–441.
   PubMed Web of Science ®Google Scholar
• Yu L, Chen Y, Tooze SA. Autophagy pathway: cellular and molecular mechanisms. Autophagy. 2018;14:207–215.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–141.
   PubMed Web of Science ®Google Scholar
• Hare WA, Owen WG. Effects of bicarbonate versus HEPES buffering on measured properties of neurons in the salamander retina. Vis Neurosci. 1998;15:263–271.
   PubMed Web of Science ®Google Scholar
• Walton ZE, Patel CH, Brooks RC, et al. Acid suspends the circadian clock in hypoxia through inhibition of mTOR. Cell. 2018;174:72–87 e32.
   PubMed Web of Science ®Google Scholar
• Xu T, Su H, Ganapathy S, et al. Modulation of autophagic activity by extracellular pH. Autophagy. 2011;7:1316–1322.
   PubMed Web of Science ®Google Scholar
• Mejlvang J, Olsvik H, Svenning S, et al. Starvation induces rapid degradation of selective autophagy receptors by endosomal microautophagy. J Cell Biol. 2018;217:3640–3655.
   PubMed Web of Science ®Google Scholar
• Zheng X, Boyer L, Jin M, et al. Metabolic reprogramming during neuronal differentiation from aerobic glycolysis to neuronal oxidative phosphorylation. ELife. 2016;5: e13374.
   PubMed Web of Science ®Google Scholar
• Saab AS, Tzvetanova ID, Nave KA. The role of myelin and oligodendrocytes in axonal energy metabolism. Curr Opin Neurobiol. 2013;23:1065–1072.
   PubMed Web of Science ®Google Scholar
• Belanger M, Allaman I, Magistretti PJ. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 2011;14:724–738.
   PubMed Web of Science ®Google Scholar
• Lee Y, Morrison BM, Li Y, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature. 2012;487:443–448.
   PubMed Web of Science ®Google Scholar
• Dorrbaum AR, Kochen L, Langer JD, et al. Local and global influences on protein turnover in neurons and glia. ELife. 2018;7:e34202.
   PubMed Web of Science ®Google Scholar
• Nikoletopoulou V, Sidiropoulou K, Kallergi E, et al. Modulation of autophagy by BDNF underlies synaptic plasticity. Cell Metab. 2017;26:230–42 e5.
   PubMed Web of Science ®Google Scholar
• Pamenter ME, Perkins GA, McGinness AK, et al. Autophagy and apoptosis are differentially induced in neurons and astrocytes treated with an in vitro mimic of the ischemic penumbra. PLoS One. 2012;7:e51469.
   PubMed Web of Science ®Google Scholar
• Pla A, Pascual M, Guerri C. Autophagy constitutes a protective mechanism against ethanol toxicity in mouse astrocytes and neurons. PLoS One. 2016;11:e0153097.
   PubMed Web of Science ®Google Scholar
• Bordi M, Berg MJ, Mohan PS, et al. Autophagy flux in CA1 neurons of Alzheimer hippocampus: increased induction overburdens failing lysosomes to propel neuritic dystrophy. Autophagy. 2016;12:2467–2483.
   PubMed Web of Science ®Google Scholar
• Ferguson CJ, Lenk GM, Meisler MH. Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2. Hum Mol Genet. 2009;18:4868–4878.
   PubMed Web of Science ®Google Scholar
• Moruno-Manchon JF, Uzor NE, Ambati CR, et al. Sphingosine kinase 1-associated autophagy differs between neurons and astrocytes. Cell Death Dis. 2018;9:521.
   PubMed Web of Science ®Google Scholar
• Tydlacka S, Wang CE, Wang X, et al. Differential activities of the ubiquitin-proteasome system in neurons versus glia may account for the preferential accumulation of misfolded proteins in neurons. J Neurosci. 2008;28:13285–13295.
   PubMed Web of Science ®Google Scholar
• Davis CH, Kim KY, Bushong EA, et al. Transcellular degradation of axonal mitochondria. Proc Natl Acad Sci U S A. 2014;111:9633–9638.
   PubMed Web of Science ®Google Scholar
• Spiller KJ, Restrepo CR, Khan T, et al. Microglia-mediated recovery from ALS-relevant motor neuron degeneration in a mouse model of TDP-43 proteinopathy. Nat Neurosci. 2018;21:329–340.
   PubMed Web of Science ®Google Scholar
• Barmada SJ, Serio A, Arjun A, et al. Autophagy induction enhances TDP43 turnover and survival in neuronal ALS models. Nat Chem Biol. 2014;10:677–685.
   PubMed Web of Science ®Google Scholar
• Dong A, Kulkarni VV, Maday S. Methods for imaging autophagosome dynamics in primary neurons. Methods Mol Biol. 2019;1880:243–256.
   PubMedGoogle Scholar