3,492
Views
63
CrossRef citations to date
0
Altmetric
Research Paper - Basic Science

Atg9a deficiency causes axon-specific lesions including neuronal circuit dysgenesis

, , , , , , , , ORCID Icon, , , & show all
Pages 764-777 | Received 08 Feb 2016, Accepted 29 Mar 2017, Published online: 06 Mar 2018

References

  • Uchiyama Y, Shibata M, Koike M, Yoshimura K, Sasaki M. Autophagy-physiology and pathophysiology. Histochem Cell Biol 2008; 129:407-20; PMID:18320203; https://doi.org/10.1007/s00418-008-0406-y
  • Mochida K, Oikawa Y, Kimura Y, Kirisako H, Hirano H, Ohsumi Y, Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 2015; 522:359-62; PMID:26040717; https://doi.org/10.1038/nature14506
  • Okamoto K. Organellophagy: eliminating cellular building blocks via selective autophagy. J Cell Biol 2014; 205:435-45; PMID:24862571; https://doi.org/10.1083/jcb.201402054
  • Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; https://doi.org/10.1038/nature06639
  • Khaminets A, Heinrich T, Mari M, Grumati P, Huebner AK, Akutsu M, Liebmann L, Stolz A, Nietzsche S, Koch N, et al. Regulation of endoplasmic reticulum turnover by selective autophagy. Nature 2015; 522:354-8; PMID:26040720; https://doi.org/10.1038/nature14498
  • Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10:458-67; PMID:19491929; https://doi.org/10.1038/nrm2708
  • Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008; 456:264-8; PMID:18849965; https://doi.org/10.1038/nature07383
  • Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169:425-34; PMID:15866887; https://doi.org/10.1083/jcb.200412022
  • Sou YS, Waguri S, Iwata J, Ueno T, Fujimura T, Hara T, Sawada N, Yamada A, Mizushima N, Uchiyama Y, et al. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol Biol Cell 2008; 19:4762-75; PMID:18768753; https://doi.org/10.1091/mbc.E08-03-0309
  • Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. The role of autophagy during the early neonatal starvation period. Nature 2004; 432:1032-6; PMID:15525940; https://doi.org/10.1038/nature03029
  • Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:1149-63; PMID:18083104; https://doi.org/10.1016/j.cell.2007.10.035
  • Birgisdottir Å, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci 2013; 126:3237-47; PMID:23908376
  • Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441:880-4; PMID:16625205; https://doi.org/10.1038/nature04723
  • Komatsu M, Wang QJ, Holstein GR, Friedrich VL, Iwata J, Kominami E, Chait BT, Tanaka K, Yue Z. 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; 104:14489-94; PMID:17726112; https://doi.org/10.1073/pnas.0701311104
  • Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006; 441:885-9; PMID:16625204; https://doi.org/10.1038/nature04724
  • Nishiyama J, Miura E, Mizushima N, Watanabe M, Yuzaki M. Aberrant membranes and double-membrane structures accumulate in the axons of Atg5-null Purkinje cells before neuronal death. Autophagy 2007; 3:591-6; PMID:17912025; https://doi.org/10.4161/auto.4964
  • Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, Kondo-Kakuta C, Ichikawa R, Kinjo M, Ohsumi Y. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 2012; 198:219-33; PMID:22826123; https://doi.org/10.1083/jcb.201202061
  • Yamada T, Carson AR, Caniggia I, Umebayashi K, Yoshimori T, Nakabayashi K, Scherer SW. Endothelial nitric-oxide synthase antisense (NOS3AS) gene encodes an autophagy-related protein (APG9-like2) highly expressed in trophoblast. J Biol Chem 2005; 280:18283-90; PMID:15755735; https://doi.org/10.1074/jbc.M413957200
  • Saitoh T, Fujita N, Hayashi T, Takahara K, Satoh T, Lee H, Matsunaga K, Kageyama S, Omori H, Noda T, et al. Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A 2009; 106:20842-6; PMID:19926846; https://doi.org/10.1073/pnas.0911267106
  • Kojima T, Yamada T, Akaishi R, Furuta I, Saitoh T, Nakabayashi K, Nakayama KI, Nakayama K, Akira S, Minakami H. Role of the Atg9a gene in intrauterine growth and survival of fetal mice. Reprod Biol 2015; 15:131-8; PMID:26370455; https://doi.org/10.1016/j.repbio.2015.05.001
  • Young AR, Chan EY, Hu XW, Köchl R, Crawshaw SG, High S, Hailey DW, Lippincott-Schwartz J, Tooze SA. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J Cell Sci 2006; 119:3888-900; PMID:16940348; https://doi.org/10.1242/jcs.03172
  • Webber JL, Young AR, Tooze SA. Atg9 trafficking in Mammalian cells. Autophagy 2007; 3:54-6; PMID:17102588; https://doi.org/10.4161/auto.3419
  • Longatti A, Tooze SA. Recycling endosomes contribute to autophagosome formation. Autophagy 2012; 8:1682-3; PMID:22874560; https://doi.org/10.4161/auto.21486
  • Takahashi Y, Meyerkord CL, Hori T, Runkle K, Fox TE, Kester M, Loughran TP, Wang HG. Bif-1 regulates Atg9 trafficking by mediating the fission of Golgi membranes during autophagy. Autophagy 2011; 7:61-73; PMID:21068542; https://doi.org/10.4161/auto.7.1.14015
  • Orsi A, Razi M, Dooley HC, Robinson D, Weston AE, Collinson LM, Tooze SA. Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol Biol Cell 2012; 23:1860-73; PMID:22456507; https://doi.org/10.1091/mbc.E11-09-0746
  • Suzuki SW, Yamamoto H, Oikawa Y, Kondo-Kakuta C, Kimura Y, Hirano H, Ohsumi Y. Atg13 HORMA domain recruits Atg9 vesicles during autophagosome formation. Proc Natl Acad Sci U S A 2015; 112:3350-5; PMID:25737544; https://doi.org/10.1073/pnas.1421092112
  • Noda T, Kim J, Huang WP, Baba M, Tokunaga C, Ohsumi Y, Klionsky DJ. Apg9p/Cvt7p is an integral membrane protein required for transport vesicle formation in the Cvt and autophagy pathways. J Cell Biol 2000; 148:465-80; PMID:10662773; https://doi.org/10.1083/jcb.148.3.465
  • Tamura H, Shibata M, Koike M, Sasaki M, Uchiyama Y. Atg9A protein, an autophagy-related membrane protein, is localized in the neurons of mouse brains. J Histochem Cytochem 2010; 58:443-53; PMID:20124090; https://doi.org/10.1369/jhc.2010.955690
  • Yue Z, Wang QJ, Komatsu M. Neuronal autophagy: going the distance to the axon. Autophagy 2008; 4:94-6; PMID:18000396; https://doi.org/10.4161/auto.5202
  • Liang CC, Wang C, Peng X, Gan B, Guan JL. Neural-specific deletion of FIP200 leads to cerebellar degeneration caused by increased neuronal death and axon degeneration. J Biol Chem 2010; 285:3499-509; PMID:19940130; https://doi.org/10.1074/jbc.M109.072389
  • Zhao YG, Sun L, Miao G, Ji C, Zhao H, Sun H, Miao L, Yoshii SR, Mizushima N, Wang X, et al. The autophagy gene Wdr45/Wipi4 regulates learning and memory function and axonal homeostasis. Autophagy 2015; 11:881-90; PMID:26000824; https://doi.org/10.1080/15548627.2015.1047127
  • Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 2009; 20:1981-91; PMID:19211835; https://doi.org/10.1091/mbc.E08-12-1248
  • Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005; 171:603-14; PMID:16286508; https://doi.org/10.1083/jcb.200507002
  • Kirkin V, Lamark T, Sou YS, Bjørkøy G, Nunn JL, Bruun JA, Shvets E, McEwan DG, Clausen TH, Wild P, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009; 33:505-16; PMID:19250911; https://doi.org/10.1016/j.molcel.2009.01.020
  • Seibenhener ML, Babu JR, Geetha T, Wong HC, Krishna NR, Wooten MW. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 2004; 24:8055-68; PMID:15340068; https://doi.org/10.1128/MCB.24.18.8055-8068.2004
  • Meixner A, Haverkamp S, Wässle H, Führer S, Thalhammer J, Kropf N, Bittner RE, Lassmann H, Wiche G, Propst F. MAP1B is required for axon guidance and Is involved in the development of the central and peripheral nervous system. J Cell Biol 2000; 151:1169-78; PMID:11121433; https://doi.org/10.1083/jcb.151.6.1169
  • Kelkar N, Delmotte MH, Weston CR, Barrett T, Sheppard BJ, Flavell RA, Davis RJ. Morphogenesis of the telencephalic commissure requires scaffold protein JNK-interacting protein 3 (JIP3). Proc Natl Acad Sci U S A 2003; 100:9843-8; PMID:12897243; https://doi.org/10.1073/pnas.1733944100
  • Ha HY, Cho IH, Lee KW, Song JY, Kim KS, Yu YM, Lee JK, Song JS, Yang SD, Shin HS, et al. The axon guidance defect of the telencephalic commissures of the JSAP1-deficient brain was partially rescued by the transgenic expression of JIP1. Dev Biol 2005; 277:184-99; PMID:15572149; https://doi.org/10.1016/j.ydbio.2004.09.019
  • Zhou X, Babu JR, da Silva S, Shu Q, Graef IA, Oliver T, Tomoda T, Tani T, Wooten MW, Wang F. Unc-51-like kinase 1/2-mediated endocytic processes regulate filopodia extension and branching of sensory axons. Proc Natl Acad Sci U S A 2007; 104:5842-7; PMID:17389358; https://doi.org/10.1073/pnas.0701402104
  • Oyama G, Yoshimi K, Natori S, Chikaoka Y, Ren YR, Funayama M, Shimo Y, Takahashi R, Nakazato T, Kitazawa S, et al. Impaired in vivo dopamine release in parkin knockout mice. Brain Res 2010; 1352:214-22; PMID:20620130; https://doi.org/10.1016/j.brainres.2010.06.065
  • Nanao T, Koike M, Yamaguchi J, Sasaki M, Uchiyama Y. Cellular localization and tissue distribution of endogenous DFCP1 protein. Biomed Res 2015; 36:121-33; PMID:25876663; https://doi.org/10.2220/biomedres.36.121
  • Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, et al. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008; 172:454-69; PMID:18187572; https://doi.org/10.2353/ajpath.2008.070876
  • Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 1995; 15:1001-11; PMID:7869078
  • Kamagata K, Hatano T, Okuzumi A, Motoi Y, Abe O, Shimoji K, Kamiya K, Suzuki M, Hori M, Kumamaru KK, et al. Neurite orientation dispersion and density imaging in the substantia nigra in idiopathic Parkinson disease. Eur Radiol 2015; 26(8):2567-77
  • Kerever A, Kamagata K, Yokosawa S, Otake Y, Ochi H, Yamada T, Hori M, Kamiya K, Nishikori A, Aoki S, et al. See-through Brains and Diffusion Tensor MRI Clarified Fiber Connections: A Preliminary Microstructural Study in a Mouse with Callosal Agenesis. Magn Reson Med Sci 2015; 14:159-62; PMID:25833270; https://doi.org/10.2463/mrms.2014-0142
  • Mori Y, Shiota T, Jones M, Wanitkun S, Irvine T, Li X, Delabays A, Pandian NG, Sahn DJ. Three-dimensional reconstruction of the color Doppler-imaged vena contracta for quantifying aortic regurgitation: studies in a chronic animal model. Circulation 1999; 99:1611-7; PMID:10096939; https://doi.org/10.1161/01.CIR.99.12.1611