Beta-propeller protein-associated neurodegeneration (BPAN) as a genetically simple model of multifaceted neuropathology resulting from defects in autophagy

References

Abidi, A., Mignon-Ravix, C., Cacciagli, P., Girard, N., Milh, M., and Villard, L. (2016). Early-onset epileptic encephalopathy as the initial clinical presentation of WDR45 deletion in a male patient. Eur. J. Hum. Genet. 24, 615–618.10.1038/ejhg.2015.159Search in Google Scholar PubMed PubMed Central

Akizu, N., Cantagrel, V., Zaki, M.S., Al-Gazali, L., Wang, X., Rosti, R.O., Dikoglu, E., Gelot, A.B., Rosti, B., Vaux, K.K., et al. (2015). Biallelic mutations in SNX14 cause a syndromic form of cerebellar atrophy and lysosome-autophagosome dysfunction. Nat. Genet. 47, 528–534.10.1038/ng.3256Search in Google Scholar PubMed PubMed Central

Alegre-Abarrategui, J., Christian, H., Lufino, M.M.P., Mutihac, R., Venda, L.L., Ansorge, O., and Wade-Martins, R. (2009). LRRK2 regulates autophagic activity and localizes to specific membrane microdomains in a novel human genomic reporter cellular model. Hum. Mol. Genet. 18, 4022–4034.10.1093/hmg/ddp346Search in Google Scholar PubMed PubMed Central

Aminkeng, F. (2013). WDR45 mutations define a novel disease entity – static encephalopathy of childhood with neurodegeneration in adulthood. Clin. Genet. 84, 209.10.1111/cge.12183Search in Google Scholar PubMed

Araújo, R., Garabal, A., Baptista, M., Carvalho, S., Pinho, C., de Sá, J., and Vasconcelos, M. (2017). Novel WDR45 mutation causing β-propeller protein associated neurodegeneration (BPAN) in two monozygotic twins. J. Neurol. 264, 1020–1022.10.1007/s00415-017-8475-2Search in Google Scholar PubMed

Arico, S., Petiot, A., Bauvy, C., Dubbelhuis, P.F., Meijer, A.J., Codogno, P., and Ogier-Denis, E. (2001). The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 276, 35243–35246.10.1074/jbc.C100319200Search in Google Scholar PubMed

Arosio, P., Elia, L., and Poli, M. (2017). Ferritin, cellular iron storage and regulation. IUBMB Life 69, 414–422.10.1002/iub.1621Search in Google Scholar PubMed

Bakula, D., Müller, A.J., Zuleger, T., Takacs, Z., Franz-Wachtel, M., Thost, A.K., Brigger, D., Tschan, M.P., Frickey, T., Robenek, H., et al. (2017). WIPI3 and WIPI4 β-propellers are scaffolds for LKB1-AMPK-TSC signalling circuits in the control of autophagy. Nat. Commun. 8, 15637.10.1038/ncomms15637Search in Google Scholar PubMed PubMed Central

Bakula, D., Mueller, A.J., and Proikas-Cezanne, T. (2018). WIPI β-propellers function as scaffolds for STK11/LKB1-AMPK and AMPK-related kinase signaling in autophagy. Autophagy 14, 1082–1083.10.1080/15548627.2017.1382784Search in Google Scholar PubMed PubMed Central

Baskaran, S., Ragusa, M.J., Boura, E., and Hurley, J.H. (2012). Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol. Cell. 47, 339–348.10.1016/j.molcel.2012.05.027Search in Google Scholar PubMed PubMed Central

Bejarano, E. and Rodríguez-Navarro, J.A. (2015). Autophagy and amino acid metabolism in the brain: implications for epilepsy. Amino Acids 47, 2113–2126.10.1007/s00726-014-1822-zSearch in Google Scholar PubMed

Biasiotto, G., Di Lorenzo, D., Archetti, S., and Zanella, I. (2016). Iron and neurodegeneration: is ferritinophagy the link? Mol. Neurobiol. 53, 5542–5574.10.1007/s12035-015-9473-ySearch in Google Scholar PubMed

Bravo-San Pedro, J.M., Gómez-Sánchez, R., Niso-Santano, M., Pizarro-Estrella, E., González-Polo, R.A., and Fuentes, J.M. (2012). Possible involvement of the relationship of LRRK2 and autophagy in Parkinson’s disease. Biochem. Soc. Trans. 40, 1129–1133.10.1042/BST20120095Search in Google Scholar PubMed

Burger, B.J., Rose, S., Bennuri, S.C., Gill, P.S., Tippett, M.L., Delhey, L., Melnyk, S., and Frye, R.E. (2017). Autistic siblings with novel mutations in two different genes: insight for genetic workups of autistic siblings and connection to mitochondrial dysfunction. Front. Pediatr. 5, 219.10.3389/fped.2017.00219Search in Google Scholar PubMed PubMed Central

Butler, M.G., Dasouki, M.J., Zhou, X.P., Talebizadeh, Z., Brown, M., Takahashi, T.N., Miles, J.H., Wang, C.H., Stratton, R., Pilarski, R., et al. (2005). Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J. Med. Genet. 42, 318–321.10.1136/jmg.2004.024646Search in Google Scholar PubMed PubMed Central

Byrne, S., Jansen, L., U-King-Im, J.M., Siddiqui, A., Lidov, H.G.W., Bodi, I., Smith, L., Mein, R., Cullup, T., Dionisi-Vici, C., et al. (2016). EPG5-related Vici syndrome: a paradigm of neurodevelopmental disorders with defective autophagy. Brain 139, 765–781.10.1093/brain/awv393Search in Google Scholar PubMed PubMed Central

Caccamo, A., Magrì, A., Medina, D.X., Wisely, E.V., López-Aranda, M.F., Silva, A.J., and Oddo, S. (2013). mTOR regulates tau phosphorylation and degradation: implications for Alzheimer’s disease and other tauopathies. Aging Cell 12, 370–380.10.1111/acel.12057Search in Google Scholar PubMed PubMed Central

Carvill, G.L., Liu, A., Mandelstam, S., Schneider, A., Lacroix, A., Zemel, M., McMahon, J.M., Bello-Espinosa, L., Mackay, M., Wallace, G., et al. (2018). Severe infantile onset developmental and epileptic encephalopathy caused by mutations in autophagy gene WDR45. Epilepsia 59, e5–e13.10.1111/epi.13957Search in Google Scholar PubMed PubMed Central

Chen, L., Wang, H., Vicini, S., and Olsen, R.W. (2000). The γ-aminobutyric acid type A (GABA_A) receptor-associated protein (GABARAP) promotes GABA_A receptor clustering and modulates the channel kinetics. Proc. Natl. Acad. Sci. USA 97, 11557–11562.10.1073/pnas.190133497Search in Google Scholar PubMed PubMed Central

Chen, J.S., Dagdas, Y.S., Kleinstiver, B.P., Welch, M.M., Sousa, A.A., Harrington, L.B., Sternberg, S.H., Joung, J.K., Yildiz, A., and Doudna, J.A. (2017). Enhanced proofreading governs CRISPR-Cas9 targeting accuracy. Nature 550, 407–410.10.1038/nature24268Search in Google Scholar PubMed PubMed Central

Chia, R., Chiò, A., and Traynor, B.J. (2018). Novel genes associated with amyotrophic lateral sclerosis: diagnostic and clinical implications. Lancet Neurol. 17, 94–102.10.1016/S1474-4422(17)30401-5Search in Google Scholar PubMed

Ciura, S., Sellier, C., Campanari, M.L., Charlet-Berguerand, N., and Kabashi, E. (2016). The most prevalent genetic cause of ALS-FTD, C9orf72 synergizes the toxicity of ATXN2 intermediate polyglutamine repeats through the autophagy pathway. Autophagy 12, 1406–1408.10.1080/15548627.2016.1189070Search in Google Scholar PubMed

Correia, S.C., Resende, R., Moreira, P.I., and Pereira, C.M. (2015). Alzheimer’s disease-related misfolded proteins and dysfunctional organelles on autophagy menu. DNA Cell. Biol. 34, 261–273.10.1089/dna.2014.2757Search in Google Scholar PubMed

Crino, P.B. (2015). mTOR signaling in epilepsy: insights from malformations of cortical development. Cold Spring Harb. Perspect. Med. 5, pii: a022442. doi: 10.1101/cshperspect.a022442.10.1101/cshperspect.a022442Search in Google Scholar

Crino, P.B., Miyata, H., and Vinters, H.V. (2002). Neurodevelopmental disorders as a cause of seizures: neuropathologic, genetic, and mechanistic considerations. Brain Pathol. 12, 212–233.10.1111/j.1750-3639.2002.tb00437.xSearch in Google Scholar PubMed

Cuervo, A.M., Stefanis, L., Fredenburg, R., Lansbury, P.T., and Sulzer, D. (2004). Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science 305, 1292–1295.10.1126/science.1101738Search in Google Scholar PubMed

Cullup, T., Kho, A.L., Dionisi-Vici, C., Brandmeier, B., Smith, F., Urry, Z., Simpson, M.A., Yau, S., Bertini, E., McClelland, V., et al. (2013). Recessive mutations in EPG5 cause Vici syndrome, a multisystem disorder with defective autophagy. Nat. Genet. 45, 83–87.10.1038/ng.2497Search in Google Scholar PubMed

Curatolo, P., Moavero, R., and de Vries, P.J. (2015). Neurological and neuropsychiatric aspects of tuberous sclerosis complex. Lancet Neurol. 14, 733–745.10.1016/S1474-4422(15)00069-1Search in Google Scholar PubMed

Curatolo, P., Moavero, R., van Scheppingen, J., and Aronica, E. (2018). mTOR dysregulation and tuberous sclerosis-related epilepsy. Expert Rev. Neurother. 18, 185–201.10.1080/14737175.2018.1428562Search in Google Scholar PubMed

Decressac, M., Mattsson, B., Weikop, P., Lundblad, M., Jakobsson, J., and Björklund, A. (2013). TFEB-mediated autophagy rescues midbrain dopamine neurons from α-synuclein toxicity. Proc. Natl. Acad. Sci. USA 110, E1817–E1826.10.1073/pnas.1305623110Search in Google Scholar PubMed PubMed Central

DeJesus-Hernandez, M., Mackenzie, I.R., Boeve, B.F., Boxer, A.L., Baker, M., Rutherford, N.J., Nicholson, A.M., Finch, N.A., Flynn, H., Adamson, J., et al. (2011). Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 72, 245–256.10.1016/j.neuron.2011.09.011Search in Google Scholar PubMed PubMed Central

Deng, Z., Sheehan, P., Chen, S., and Yue, Z. (2017). Is amyotrophic lateral sclerosis/frontotemporal dementia an autophagy disease? Mol. Neurodegener. 12, 90.10.1186/s13024-017-0232-6Search in Google Scholar PubMed PubMed Central

Dere, E., Dahm, L., Lu, D., Hammerschmidt, K., Ju, A., Tantra, M., Kästner, A., Chowdhury, K., and Ehrenreich, H. (2014). Heterozygous ambra1 deficiency in mice: a genetic trait with autism-like behavior restricted to the female gender. Front Behav. Neurosci. 8, 181.10.3389/fnbeh.2014.00181Search in Google Scholar PubMed PubMed Central

Devenney, E., Vucic, S., Hodges, J.R., and Kiernan, M.C. (2015). Motor neuron disease-frontotemporal dementia: a clinical continuum. Expert Rev. Neurother. 15, 509–522.10.1586/14737175.2015.1034108Search in Google Scholar PubMed

Di Nardo, A., Wertz, M.H., Kwiatkowski, E., Tsai, P.T., Leech, J.D., Greene-Colozzi, E., Goto, J., Dilsiz, P., Talos, D.M., Clish, C.B., et al. (2014). Neuronal Tsc1/2 complex controls autophagy through AMPK-dependent regulation of ULK1. Hum. Mol. Genet. 23, 3865–3874.10.1093/hmg/ddu101Search in Google Scholar PubMed PubMed Central

Dooley, H.C., Razi, M., Polson, H.E.J., Girardin, S.E., Wilson, M.I., and Tooze, S.A. (2014). WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol. Cell. 55, 238–252.10.1016/j.molcel.2014.05.021Search in Google Scholar PubMed PubMed Central

Doorn, J.M., and Kruer, M.C. (2013). Newly characterized forms of neurodegeneration with brain iron accumulation. Curr. Neurol. Neurosci. Rep. 13, 413.10.1007/s11910-013-0413-9Search in Google Scholar PubMed PubMed Central

Dove, S.K., Dong, K., Kobayashi, T., Williams, F.K., and Michell, R.H. (2009). Phosphatidylinositol 3,5-bisphosphate and Fab1p/PIKfyve underPPIn endo-lysosome function. Biochem. J. 419, 1–13.10.1042/BJ20081950Search in Google Scholar PubMed

Ebrahimi-Fakhari, D., Saffari, A., Wahlster, L., Lu, J., Byrne, S., Hoffmann, G.F., Jungbluth, H., and Sahin, M. (2016). Congenital disorders of autophagy: an emerging novel class of inborn errors of neuro-metabolism. Brain 139, 317–337.10.1093/brain/awv371Search in Google Scholar PubMed PubMed Central

Edvardson, S., Cinnamon, Y., Jalas, C., Shaag, A., Maayan, C., Axelrod, F.B., and Elpeleg, O. (2012). Hereditary sensory autonomic neuropathy caused by a mutation in dystonin. Ann. Neurol. 71, 569–572.10.1002/ana.23524Search in Google Scholar PubMed

Egan, D.F., Shackelford, D.B., Mihaylova, M.M., Gelino, S., Kohnz, R.A., Mair, W., Vasquez, D.S., Joshi, A., Gwinn, D.M., Taylor, R., et al. (2011). Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456–461.10.1126/science.1196371Search in Google Scholar PubMed PubMed Central

Elrick, M.J., Yu, T., Chung, C., and Lieberman, A.P. (2012). Impaired proteolysis underlies autophagic dysfunction in Niemann-Pick type C disease. Hum. Mol. Genet. 21, 4876–4887.10.1093/hmg/dds324Search in Google Scholar PubMed PubMed Central

Esteves, A.R., and Cardoso, S.M. (2017). LRRK2 at the crossroad between autophagy and microtubule trafficking: insights into Parkinson’s disease. Neuroscientist 23, 16–26.10.1177/1073858415616558Search in Google Scholar PubMed

Feng, Y., He, D., Yao, Z., and Klionsky, D.J. (2014). The machinery of macroautophagy. Cell Res. 24, 24–41.10.1038/cr.2013.168Search in Google Scholar PubMed PubMed Central

Ferrier, A., De Repentigny, Y., Lynch-Godrei, A., Gibeault, S., Eid, W., Kuo, D., Zha, X., and Kothary, R. (2015). Disruption in the autophagic process underlies the sensory neuropathy in dystonia musculorum mice. Autophagy 11, 1025–1036.10.1080/15548627.2015.1052207Search in Google Scholar PubMed PubMed Central

Fimia, G.M., Stoykova, A., Romagnoli, A., Giunta, L., Di Bartolomeo, S., Nardacci, R., Corazzari, M., Fuoco, C., Ucar, A., Schwartz, P., et al. (2007). Ambra1 regulates autophagy and development of the nervous system. Nature 447, 1121–1125.10.1038/nature05925Search in Google Scholar PubMed

Fonderico, M., Laudisi, M., Andreasi, N.G., Bigoni, S., Lamperti, C., Panteghini, C., Garavaglia, B., Carecchio, M., Emanuele, E.A., Forni, G.L., et al. (2017). Patient affected by beta-propeller protein-associated neurodegeneration: a therapeutic attempt with iron chelation therapy. Front Neurol. 8, 385.10.3389/fneur.2017.00385Search in Google Scholar PubMed PubMed Central

Fujita, N., Itoh, T., Omori, H., Fukuda, M., Noda, T., and Yoshimori, T. (2008). The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell. 19, 2092–2100.10.1091/mbc.e07-12-1257Search in Google Scholar PubMed PubMed Central

Giaime, E., Tong, Y., Wagner, L.K., Yuan, Y., Huang, G., and Shen, J. (2017). Age-dependent dopaminergic neurodegeneration and impairment of the autophagy-lysosomal pathway in LRRK-deficient Mice. Neuron 96, 796–807.e6.10.1016/j.neuron.2017.09.036Search in Google Scholar PubMed PubMed Central

Giles, L.M., Chen, J., Li, L., and Chin, L.S. (2008). Dystonia-associated mutations cause premature degradation of torsinA protein and cell-type-specific mislocalization to the nuclear envelope. Hum. Mol. Genet. 17, 2712–2722.10.1093/hmg/ddn173Search in Google Scholar PubMed PubMed Central

Giorgi, F.S., Biagioni, F., Lenzi, P., Frati, A., and Fornai, F. (2015). The role of autophagy in epileptogenesis and in epilepsy-induced neuronal alterations. J. Neural. Transm. 122, 849–862.10.1007/s00702-014-1312-1Search in Google Scholar PubMed

Gregory, A., and Hayflick, S.J. (2011). Genetics of neurodegeneration with brain iron accumulation. Curr. Neurol. Neurosci. Rep. 11, 254–261.10.1007/s11910-011-0181-3Search in Google Scholar PubMed PubMed Central

Gregory, A., Hayflick, S., Adam, M., Ardinger, H., Pagon, R., and Wallace, S., eds. (2014). GeneReviews^®: Neurodegeneration with Brain Iron Accumulation Disorders Overview (Seattle, USA: University of Washington).Search in Google Scholar

Gregory, A., Kurian, M., Haack, T., Hayflick, S., Hogarth, P., Adam, M., Ardinger, H., Pagon, R., and Wallace, S., eds. (2017). GeneReviews^®: Beta-Propeller Protein-Associated Neurodegeneration (Seattle, USA: University of Washington).Search in Google Scholar

Guiney, S.J., Adlard, P.A., Bush, A.I., Finkelstein, D.I., and Ayton, S. (2017). Ferroptosis and cell death mechanisms in Parkinson’s disease. Neurochem. Int. 104, 34–48.10.1016/j.neuint.2017.01.004Search in Google Scholar PubMed

Haack, T.B., Hogarth, P., Kruer, M.C., Gregory, A., Wieland, T., Schwarzmayr, T., Graf, E., Sanford, L., Meyer, E., Kara, E., et al. (2012). Exome sequencing reveals de novo WDR45 mutations causing a phenotypically distinct, X-linked dominant form of NBIA. Am. J. Hum. Genet. 91, 1144–1149.10.1016/j.ajhg.2012.10.019Search in Google Scholar PubMed PubMed Central

Haack, T.B., Hogarth, P., Gregory, A., Prokisch, H., and Hayflick, S.J. (2013). BPAN: the only X-linked dominant NBIA disorder. Int Rev Neurobiol. 110, 85–90.10.1016/B978-0-12-410502-7.00005-3Search in Google Scholar PubMed

Haack, T.B., Ignatius, E., Calvo-Garrido, J., Iuso, A., Isohanni, P., Maffezzini, C., Lönnqvist, T., Suomalainen, A., Gorza, M., Kremer, L.S., et al. (2016). Absence of the autophagy adaptor SQSTM1/p62 causes childhood-onset neurodegeneration with ataxia, dystonia, and gaze palsy. Am. J. Hum. Genet. 99, 735–743.10.1016/j.ajhg.2016.06.026Search in Google Scholar PubMed PubMed Central

Haidar, M., and Timmerman, V. (2017). Autophagy as an emerging common pathomechanism in inherited peripheral neuropathies. Front Mol. Neurosci. 10, 143.10.3389/fnmol.2017.00143Search in Google Scholar PubMed PubMed Central

Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., et al. (2013). Autophagosomes form at ER-mitochondria contact sites. Nature 495, 389–393.10.1038/nature11910Search in Google Scholar PubMed

Hanein, S., Martin, E., Boukhris, A., Byrne, P., Goizet, C., Hamri, A., Benomar, A., Lossos, A., Denora, P., Fernandez, J., et al. (2008). Identification of the SPG15 gene, encoding spastizin, as a frequent cause of complicated autosomal-recessive spastic paraplegia, including Kjellin syndrome. Am. J. Hum. Genet. 82, 992–1002.10.1016/j.ajhg.2008.03.004Search in Google Scholar PubMed PubMed Central

Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., et al. (2006). Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885–889.10.1038/nature04724Search in Google Scholar PubMed

Hare, D.J., and Double, K.L. (2016). Iron and dopamine: a toxic couple. Brain 139, 1026–1035.10.1093/brain/aww022Search in Google Scholar PubMed

Hartley, B.J., and Brennand, K.J. (2017). Neural organoids for disease phenotyping, drug screening and developmental biology studies. Neurochem. Int. 106, 85–93.10.1016/j.neuint.2016.10.004Search in Google Scholar PubMed PubMed Central

Hattingen, E., Handke, N., Cremer, K., Hoffjan, S., and Kukuk, G.M. (2017). Clinical and imaging presentation of a patient with beta-propeller protein-associated neurodegeneration, a rare and sporadic form of neurodegeneration with brain iron accumulation (NBIA). Clin. Neuroradiol. 27, 481–483.10.1007/s00062-017-0605-9Search in Google Scholar PubMed

Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., and Yamamoto, A. (2009). A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell. Biol. 11, 1433–1437.10.1038/ncb1991Search in Google Scholar PubMed

Hayflick, S.J., Kruer, M.C., Gregory, A., Haack, T.B., Kurian, M.A., Houlden, H.H., Anderson, J., Boddaert, N., Sanford, L., Harik, S.I., et al. (2013). β-propeller protein-associated neurodegeneration: a new X-linked dominant disorder with brain iron accumulation. Brain 136, 1708–1717.10.1093/brain/awt095Search in Google Scholar PubMed PubMed Central

Hayflick, S.J., Kurian, M.A., and Hogarth, P. (2018). Neurodegeneration with brain iron accumulation. Handb. Clin. Neurol. 147, 293–305.10.1016/B978-0-444-63233-3.00019-1Search in Google Scholar PubMed PubMed Central

Hermann, A., Kitzler, H.H., Pollack, T., Biskup, S., Krüger, S., Funke, C., Terrile, C., and Haack, T.B. (2017). A case of beta-propeller protein-associated neurodegeneration due to a heterozygous deletion of WDR45. Tremor. Other Hyperkinet. Mov. (NY). 7, 465.10.5334/tohm.360Search in Google Scholar

Hoffjan, S., Ibisler, A., Tschentscher, A., Dekomien, G., Bidinost, C., and Rosa, A.L. (2016). WDR45 mutations in Rett (-like) syndrome and developmental delay: case report and an appraisal of the literature. Mol. Cell. Probes 30, 44–49.10.1016/j.mcp.2016.01.003Search in Google Scholar PubMed

Hori, I., Otomo, T., Nakashima, M., Miya, F., Negishi, Y., Shiraishi, H., Nonoda, Y., Magara, S., Tohyama, J., Okamoto, N., et al. (2017). Defects in autophagosome-lysosome fusion underlie Vici syndrome, a neurodevelopmental disorder with multisystem involvement. Sci. Rep. 7, 3552.10.1038/s41598-017-02840-8Search in Google Scholar PubMed PubMed Central

Huber, K.M., Klann, E., Costa-Mattioli, M., and Zukin, R.S. (2015). Dysregulation of mammalian target of rapamycin signaling in mouse models of autism. J. Neurosci. 35, 13836–13842.10.1523/JNEUROSCI.2656-15.2015Search in Google Scholar PubMed PubMed Central

Hutsler, J.J., and Zhang, H. (2010). Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res. 1309, 83–94.10.1016/j.brainres.2009.09.120Search in Google Scholar PubMed

Ichinose, Y., Miwa, M., Onohara, A., Obi, K., Shindo, K., Saitsu, H., Matsumoto, N., and Takiyama, Y. (2014). Characteristic MRI findings in beta-propeller protein-associated neurodegeneration (BPAN). Neurology. Clin. Pract 4, 175–177.10.1212/01.CPJ.0000437694.17888.9bSearch in Google Scholar

Ingrassia, R., Memo, M., and Garavaglia, B. (2017). Ferrous iron up-regulation in fibroblasts of patients with beta propeller protein-associated neurodegeneration (BPAN). Front Genet. 8, 18.10.3389/fgene.2017.00018Search in Google Scholar PubMed

Jansen, L.A., Uhlmann, E.J., Crino, P.B., Gutmann, D.H., and Wong, M. (2005). Epileptogenesis and reduced inward rectifier potassium current in tuberous sclerosis complex-1-deficient astrocytes. Epilepsia 46, 1871–1880.10.1111/j.1528-1167.2005.00289.xSearch in Google Scholar PubMed

Jo, J., Xiao, Y., Sun, A.X., Cukuroglu, E., Tran, H.D., Göke, J., Tan, Z.Y., Saw, T.Y., Tan, C.P., Lokman, H., et al. (2016). Midbrain-like organoids from human pluripotent stem cells contain functional dopaminergic and neuromelanin-producing neurons. Cell Stem Cell 19, 248–257.10.1016/j.stem.2016.07.005Search in Google Scholar PubMed

Joachim, J., and Tooze, S.A. (2018). Control of GABARAP-mediated autophagy by the Golgi complex, centrosome and centriolar satellites. Biol. Cell. 110, 1–5.10.1111/boc.201700046Search in Google Scholar PubMed

Kalia, L.V., and Lang, A.E. (2015). Parkinson’s disease. Lancet 386, 896–912.10.1016/S0140-6736(14)61393-3Search in Google Scholar PubMed

Kaliszewski, M., Knott, A.B., and Bossy-Wetzel, E. (2015). Primary cilia and autophagic dysfunction in Huntington’s disease. Cell Death Differ. 22, 1413–1424.10.1038/cdd.2015.80Search in Google Scholar PubMed PubMed Central

Kamm, C. (2006). Early onset torsion dystonia (Oppenheim’s dystonia). Orphanet. J. Rare Dis. 1, 48.10.1186/1750-1172-1-48Search in Google Scholar PubMed PubMed Central

Kane, L.A., Lazarou, M., Fogel, A.I., Li, Y., Yamano, K., Sarraf, S.A., Banerjee, S., and Youle, R.J. (2014). PINK1 phosphorylates ubiquitin to activate Parkin E3 ubiquitin ligase activity. J. Cell. Biol. 205, 143–153.10.1083/jcb.201402104Search in Google Scholar PubMed PubMed Central

Karabiyik, C., Lee, M.J., and Rubinsztein, D.C. (2017). Autophagy impairment in Parkinson’s disease. Essays Biochem. 61, 711–720.10.1042/EBC20170023Search in Google Scholar PubMed

Kerr, J.S., Adriaanse, B.A., Greig, N.H., Mattson, M.P., Cader, M.Z., Bohr, V.A., and Fang, E.F. (2017). Mitophagy and Alzheimer’s disease: cellular and molecular mechanisms. Trends Neurosci. 40, 151–166.10.1016/j.tins.2017.01.002Search in Google Scholar PubMed PubMed Central

Khalifa, M., and Naffaa, L. (2015). Exome sequencing reveals a novel WDR45 frameshift mutation and inherited POLR3A heterozygous variants in a female with a complex phenotype and mixed brain MRI findings. Eur. J. Med. Genet. 58, 381–386.10.1016/j.ejmg.2015.05.009Search in Google Scholar PubMed

Kim, J., Kundu, M., Viollet, B., and Guan, K.L. (2011). AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell. Biol. 13, 132–141.10.1038/ncb2152Search in Google Scholar PubMed PubMed Central

Kim, H.J., Cho, M.H., Shim, W.H., Kim, J.K., Jeon, E.Y., Kim, D.H., and Yoon, S.Y. (2017a). Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects. Mol. Psychiatry 22, 1576–1584.10.1038/mp.2016.103Search in Google Scholar PubMed PubMed Central

Kim, Y.D., Jeong, E.I., Nah, J., Yoo, S.M., Lee, W.J., Kim, Y., Moon, S., Hong, S.H., and Jung, Y.K. (2017b). Pimozide reduces toxic forms of tau in TauC3 mice via 5’ adenosine monophosphate-activated protein kinase-mediated autophagy. J. Neurochem. 142, 734–746.10.1111/jnc.14109Search in Google Scholar PubMed

Kimura, Y., Sato, N., Sugai, K., Maruyama, S., Ota, M., Kamiya, K., Ito, K., Nakata, Y., Sasaki, M., and Sugimoto, H. (2013). MRI, MR spectroscopy, and diffusion tensor imaging findings in patient with static encephalopathy of childhood with neurodegeneration in adulthood (SENDA). Brain Dev. 35, 458–461.10.1016/j.braindev.2012.07.008Search in Google Scholar PubMed

Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., and Shimizu, N. (1998). Mutations in the parkin gene cause autosomal recessive juvenile Parkinsonism. Nature 392, 605–608.10.1038/33416Search in Google Scholar PubMed

Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J.I., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., et al. (2006). Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880–884.10.1038/nature04723Search in Google Scholar PubMed

Koyano, F., Okatsu, K., Kosako, H., Tamura, Y., Go, E., Kimura, M., Kimura, Y., Tsuchiya, H., Yoshihara, H., Hirokawa, T., et al. (2014). Ubiquitin is phosphorylated by PINK1 to activate parkin. Nature 510, 162–166.10.1038/nature13392Search in Google Scholar PubMed

Ktistakis, N.T. and Tooze, S.A. (2016). Digesting the expanding mechanisms of autophagy. Trends Cell Biol. 26, 624–635.10.1016/j.tcb.2016.03.006Search in Google Scholar PubMed

Kulikovskaja, L., Sarajlija, A., Savic-Pavicevic, D., Dobricic, V., Klein, C., and Westenberger, A. (2018). WDR45 mutations may cause a MECP2 mutation-negative Rett syndrome phenotype. Neurol. Genet. 4, e227.10.1212/NXG.0000000000000227Search in Google Scholar PubMed PubMed Central

Kwon, C.H., Luikart, B.W., Powell, C.M., Zhou, J., Matheny, S.A., Zhang, W., Li, Y., Baker, S.J., and Parada, L.F. (2006). Pten regulates neuronal arborization and social interaction in mice. Neuron 50, 377–388.10.1016/j.neuron.2006.03.023Search in Google Scholar PubMed PubMed Central

Lalonde, R., and Strazielle, C. (2007). Spontaneous and induced mouse mutations with cerebellar dysfunctions: behavior and neurochemistry. Brain Res. 1140, 51–74.10.1016/j.brainres.2006.01.031Search in Google Scholar PubMed

Lancaster, M.A., Renner, M., Martin, C.A., Wenzel, D., Bicknell, L.S., Hurles, M.E., Homfray, T., Penninger, J.M., Jackson, A.P., and Knoblich, J.A. (2013). Cerebral organoids model human brain development and microcephaly. Nature 501, 373–379.10.1038/nature12517Search in Google Scholar PubMed PubMed Central

Leonard, H., Cobb, S., and Downs, J. (2017). Clinical and biological progress over 50 years in Rett syndrome. Nat. Rev. Neurol. 13, 37–51.10.1038/nrneurol.2016.186Search in Google Scholar PubMed

Levi, S., and Finazzi, D. (2014). Neurodegeneration with brain iron accumulation: update on pathogenic mechanisms. Front Pharmacol. 5, 99.10.3389/fphar.2014.00099Search in Google Scholar PubMed PubMed Central

Li, K., and Reichmann, H. (2016). Role of iron in neurodegenerative diseases. J. Neural. Transm. 123, 389–399.10.1007/s00702-016-1508-7Search in Google Scholar PubMed

Liu, J., Wang, X., Lu, Y., Duan, C., Gao, G., Lu, L., and Yang, H. (2017). Pink1 interacts with α-synuclein and abrogates α-synuclein-induced neurotoxicity by activating autophagy. Cell Death Dis. 8, e3056.10.1038/cddis.2017.427Search in Google Scholar PubMed PubMed Central

Long, M., Abdeen, N., Geraghty, M.T., Hogarth, P., Hayflick, S., and Venkateswaran, S. (2015). Novel WDR45 mutation and pathognomonic BPAN imaging in a young female with mild cognitive delay. Pediatrics 136, e714–e717.10.1542/peds.2015-0750Search in Google Scholar PubMed

Loy, C.T., Schofield, P.R., Turner, A.M., and Kwok, J.B.J. (2014). Genetics of dementia. Lancet 383, 828–840.10.1016/S0140-6736(13)60630-3Search in Google Scholar PubMed

Lynch-Day, M.A., Mao, K., Wang, K., Zhao, M., and Klionsky, D.J. (2012). The role of autophagy in Parkinson’s disease. Cold Spring Harb. Perspect. Med. 2, a009357.10.1101/cshperspect.a009357Search in Google Scholar PubMed PubMed Central

Mancias, J.D., Wang, X., Gygi, S.P., Harper, J.W., and Kimmelman, A.C. (2014). Quantitative proteomics identifies NCOA4 as the cargo receptor mediating ferritinophagy. Nature 509, 105–109.10.1038/nature13148Search in Google Scholar PubMed PubMed Central

Manzoni, C., and Lewis, P.A. (2017). LRRK2 and autophagy. Adv. Neurobiol. 14, 89–105.10.1007/978-3-319-49969-7_5Search in Google Scholar PubMed

Marton, R.M., and Paşca, S.P. (2016). Neural differentiation in the third dimension: Generating a human midbrain. Cell Stem Cell 19, 145–146.10.1016/j.stem.2016.07.017Search in Google Scholar PubMed

McMahon, J., Huang, X., Yang, J., Komatsu, M., Yue, Z., Qian, J., Zhu, X., and Huang, Y. (2012). Impaired autophagy in neurons after disinhibition of mammalian target of rapamycin and its contribution to epileptogenesis. J. Neurosci. 32, 15704–15714.10.1523/JNEUROSCI.2392-12.2012Search in Google Scholar PubMed PubMed Central

Menzies, F.M., Fleming, A., Caricasole, A., Bento, C.F., Andrews, S.P., Ashkenazi, A., Füllgrabe, J., Jackson, A., Jimenez Sanchez, M., Karabiyik, C., et al. (2017). Autophagy and neurodegeneration: pathogenic mechanisms and therapeutic opportunities. Neuron 93, 1015–1034.10.1016/j.neuron.2017.01.022Search in Google Scholar PubMed

Michiorri, S., Gelmetti, V., Giarda, E., Lombardi, F., Romano, F., Marongiu, R., Nerini-Molteni, S., Sale, P., Vago, R., Arena, G., et al. (2010). The Parkinson-associated protein PINK1 interacts with Beclin1 and promotes autophagy. Cell Death Differ. 17, 962–974.10.1038/cdd.2009.200Search in Google Scholar PubMed

Morikawa, M., Takano, K., Motobayashi, M., Shiba, N., Kosho, T., Nakazawa, Y., and Inaba, Y. (2017). Clinical features of a female with WDR45 mutation complicated by infantile spasms: a case report and literature review. Brain Dev. 39, 804–807.10.1016/j.braindev.2017.05.003Search in Google Scholar PubMed

Morisada, N., Tsuneishi, S., Taguchi, K., Yagi, R., Nishiyama, M., Toyoshima, D., Nakagawa, T., Takeshima, Y., Takada, S., and Iijima, K. (2016). A woman with β-propeller protein-associated neurodegeneration identified by the WDR45 mutation presenting as Rett-like syndrome in childhood. No To Hattatsu 48, 209–212.Search in Google Scholar PubMed

Mouton-Liger, F., Jacoupy, M., Corvol, J.C., and Corti, O. (2017). PINK1/Parkin-dependent mitochondrial surveillance: from pleiotropy to Parkinson’s disease. Front. Mol. Neurosci. 10, 120.10.3389/fnmol.2017.00120Search in Google Scholar PubMed PubMed Central

Nakashima, M., Takano, K., Tsuyusaki, Y., Yoshitomi, S., Shimono, M., Aoki, Y., Kato, M., Aida, N., Mizuguchi, T., Miyatake, S., et al. (2016). WDR45 mutations in three male patients with West syndrome. J. Hum. Genet. 61, 653–661.10.1038/jhg.2016.27Search in Google Scholar PubMed

Nash, Y., Schmukler, E., Trudler, D., Pinkas-Kramarski, R., and Frenkel, D. (2017). DJ-1 deficiency impairs autophagy and reduces alpha-synuclein phagocytosis by microglia. J. Neurochem. 143, 584–594.10.1111/jnc.14222Search in Google Scholar PubMed

Nassif, M., Woehlbier, U., and Manque, P.A. (2017). The enigmatic role of C9ORF72 in autophagy. Front. Neurosci. 11, 442.10.3389/fnins.2017.00442Search in Google Scholar PubMed PubMed Central

Nishioka, K., Oyama, G., Yoshino, H., Li, Y., Matsushima, T., Takeuchi, C., Mochizuki, Y., Mori-Yoshimura, M., Murata, M., Yamasita, C., et al. (2015). High frequency of beta-propeller protein-associated neurodegeneration (BPAN) among patients with intellectual disability and young-onset Parkinsonism. Neurobiol. Aging 36, 2004.e9–2004.e15.10.1016/j.neurobiolaging.2015.01.020Search in Google Scholar PubMed

Obara, K., Sekito, T., Niimi, K., and Ohsumi, Y. (2008). The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J. Biol. Chem. 283, 23972–23980.10.1074/jbc.M803180200Search in Google Scholar PubMed PubMed Central

Ohba, C., Nabatame, S., Iijima, Y., Nishiyama, K., Tsurusaki, Y., Nakashima, M., Miyake, N., Tanaka, F., Ozono, K., Saitsu, H., et al. (2014). De novo WDR45 mutation in a patient showing clinically Rett syndrome with childhood iron deposition in brain. J. Hum. Genet. 59, 292–295.10.1038/jhg.2014.18Search in Google Scholar PubMed

Orenstein, S.J., Kuo, S.H., Tasset, I., Arias, E., Koga, H., Fernandez-Carasa, I., Cortes, E., Honig, L.S., Dauer, W., Consiglio, A., et al. (2013). Interplay of LRRK2 with chaperone-mediated autophagy. Nat. Neurosci. 16, 394–406.10.1038/nn.3350Search in Google Scholar PubMed PubMed Central

Oz-Levi, D., Ben-Zeev, B., Ruzzo, E.K., Hitomi, Y., Gelman, A., Pelak, K., Anikster, Y., Reznik-Wolf, H., Bar-Joseph, I., Olender, T., et al. (2012). Mutation in TECPR2 reveals a role for autophagy in hereditary spastic paraparesis. Am. J. Hum. Genet. 91, 1065–1072.10.1016/j.ajhg.2012.09.015Search in Google Scholar PubMed PubMed Central

Paudel, R., Li, A., Wiethoff, S., Bandopadhyay, R., Bhatia, K., de Silva, R., Houlden, H., and Holton, J.L. (2015). Neuropathology of beta-propeller protein associated neurodegeneration (BPAN): a new tauopathy. Acta Neuropathol. Commun. 3, 39.10.1186/s40478-015-0221-3Search in Google Scholar PubMed PubMed Central

Piano Mortari, E., Folgiero, V., Marcellini, V., Romania, P., Bellacchio, E., D’Alicandro, V., Bocci, C., Carrozzo, R., Martinelli, D., Petrini, S., et al. (2018). The Vici syndrome protein EPG5 regulates intracellular nucleic acid trafficking linking autophagy to innate and adaptive immunity. Autophagy 14, 22–37.10.1080/15548627.2017.1389356Search in Google Scholar PubMed PubMed Central

Polson, H.E.J., de Lartigue, J., Rigden, D.J., Reedijk, M., Urbé, S., Clague, M.J., and Tooze, S.A. (2010). Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6, 506–522.10.4161/auto.6.4.11863Search in Google Scholar PubMed

Proikas-Cezanne, T., Takacs, Z., Dönnes, P., and Kohlbacher, O. (2015). WIPI proteins: essential PtdIns3P effectors at the nascent autophagosome. J. Cell. Sci. 128, 207–217.10.1242/jcs.146258Search in Google Scholar PubMed

Puri, C., Vicinanza, M., Ashkenazi, A., Gratian, M.J., Zhang, Q., Bento, C.F., Renna, M., Menzies, F.M., and Rubinsztein, D.C. (2018). The RAB11A-positive compartment is a primary platform for autophagosome assembly mediated by WIPI2 recognition of PI3P-RAB11A. Dev. Cell. 45, 114–131.e8.10.1016/j.devcel.2018.03.008Search in Google Scholar PubMed PubMed Central

Raab-Graham, K.F., Haddick, P.C.G., Jan, Y.N., and Jan, L.Y. (2006). Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314, 144–148.10.1126/science.1131693Search in Google Scholar PubMed

Rabanal-Ruiz, Y., Otten, E.G., and Korolchuk, V.I. (2017). mTORC1 as the main gateway to autophagy. Essays Biochem. 61, 565–584.10.1042/EBC20170027Search in Google Scholar PubMed PubMed Central

Ramachandran, N., Girard, J.M., Turnbull, J., and Minassian, B.A. (2009). The autosomal recessively inherited progressive myoclonus epilepsies and their genes. Epilepsia 50(suppl 5), 29–36.10.1111/j.1528-1167.2009.02117.xSearch in Google Scholar PubMed

Ramesh, N. and Pandey, U.B. (2017). Autophagy dysregulation in ALS: when protein aggregates get out of hand. Front. Mol. Neurosci. 10, 263.10.3389/fnmol.2017.00263Search in Google Scholar PubMed PubMed Central

Rathore, G.S., Schaaf, C.P., and Stocco, A.J. (2014). Novel mutation of the WDR45 gene causing beta-propeller protein-associated neurodegeneration. Mov. Disord. 29, 574–575.10.1002/mds.25868Search in Google Scholar PubMed

Recalcati, S., Gammella, E., Buratti, P., and Cairo, G. (2017). Molecular regulation of cellular iron balance. IUBMB Life 69, 389–398.10.1002/iub.1628Search in Google Scholar PubMed

Redon, S., Benech, C., Schutz, S., Despres, A., Gueguen, P., Le Berre, P., Le Marechal, C., Peudenier, S., Meriot, P., Parent, P., et al. (2017). Intragenic deletion of the WDR45 gene in a male with encephalopathy, severe psychomotor disability, and epilepsy. Am. J. Med. Genet A. 173, 1444–1446.10.1002/ajmg.a.38180Search in Google Scholar PubMed

Renton, A.E., Majounie, E., Waite, A., Simón-Sánchez, J., Rollinson, S., Gibbs, J.R., Schymick, J.C., Laaksovirta, H., van Swieten, J.C., Myllykangas, L., et al. (2011). A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72, 257–268.10.1016/j.neuron.2011.09.010Search in Google Scholar PubMed

Ross, C.A., and Tabrizi, S.J. (2011). Huntington’s disease: from molecular pathogenesis to clinical treatment. Lancet Neurol. 10, 83–98.10.1016/S1474-4422(10)70245-3Search in Google Scholar PubMed

Russell, R.C., Tian, Y., Yuan, H., Park, H.W., Chang, Y.Y., Kim, J., Kim, H., Neufeld, T.P., Dillin, A., and Guan, K.L. (2013). ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat. Cell. Biol. 15, 741–750.10.1038/ncb2757Search in Google Scholar PubMed

Saitsu, H., Nishimura, T., Muramatsu, K., Kodera, H., Kumada, S., Sugai, K., Kasai-Yoshida, E., Sawaura, N., Nishida, H., Hoshino, A., et al. (2013). De novo mutations in the autophagy gene WDR45 cause static encephalopathy of childhood with neurodegeneration in adulthood. Nat. Genet. 45, 445–449.e1.10.1038/ng.2562Search in Google Scholar PubMed

Sarkar, S., Carroll, B., Buganim, Y., Maetzel, D., Ng, A.H.M., Cassady, J.P., Cohen, M.A., Chakraborty, S., Wang, H., Spooner, E., et al. (2013). Impaired autophagy in the lipid-storage disorder Niemann-Pick type C1 disease. Cell Rep. 5, 1302–1315.10.1016/j.celrep.2013.10.042Search in Google Scholar PubMed

Sbardella, D., Tundo, G.R., Campagnolo, L., Valacchi, G., Orlandi, A., Curatolo, P., Borsellino, G., D’Esposito, M., Ciaccio, C., Cesare, S.D., et al. (2017). Retention of mitochondria in mature human red blood cells as the result of autophagy impairment in Rett syndrome. Sci. Rep. 7, 12297.10.1038/s41598-017-12069-0Search in Google Scholar PubMed

Scheltens, P., Blennow, K., Breteler, M.M.B., de Strooper, B., Frisoni, G.B., Salloway, S., and Van der Flier, W.M. (2016). Alzheimer’s disease. Lancet 388, 505–517.10.1016/S0140-6736(15)01124-1Search in Google Scholar PubMed

Schneider, S.A., and Bhatia, K.P. (2012). Syndromes of neurodegeneration with brain iron accumulation. Semin. Pediatr. Neurol. 19, 57–66.10.1016/j.spen.2012.03.005Search in Google Scholar PubMed

Sellier, C., Campanari, M.L., Julie Corbier, C., Gaucherot, A., Kolb-Cheynel, I., Oulad-Abdelghani, M., Ruffenach, F., Page, A., Ciura, S., Kabashi, E., et al. (2016). Loss of C9ORF72 impairs autophagy and synergizes with polyQ Ataxin-2 to induce motor neuron dysfunction and cell death. EMBO J. 35, 1276–1297.10.15252/embj.201593350Search in Google Scholar PubMed PubMed Central

Shah, R.R., and Bird, A.P. (2017). MeCP2 mutations: progress towards understanding and treating Rett syndrome. Genome Med. 9, 17.10.1186/s13073-017-0411-7Search in Google Scholar PubMed PubMed Central

Shiba-Fukushima, K., Arano, T., Matsumoto, G., Inoshita, T., Yoshida, S., Ishihama, Y., Ryu, K.Y., Nukina, N., Hattori, N., and Imai, Y. (2014). Phosphorylation of mitochondrial polyubiquitin by PINK1 promotes Parkin mitochondrial tethering. PLoS Genet. 10, e1004861.10.1371/journal.pgen.1004861Search in Google Scholar PubMed

Sisodiya, S.M., Fauser, S., Cross, J.H., and Thom, M. (2009). Focal cortical dysplasia type II: biological features and clinical perspectives. Lancet Neurol. 8, 830–843.10.1016/S1474-4422(09)70201-7Search in Google Scholar PubMed

Smith, T.F., Gaitatzes, C., Saxena, K., and Neer, E.J. (1999). The WD repeat: a common architecture for diverse functions. Trends Biochem Sci. 24, 181–185.10.1016/S0968-0004(99)01384-5Search in Google Scholar PubMed

Spiegel, R., Shalev, S., Bercovich, D., Rabinovich, D., Khayat, M., Shaag, A., and Elpeleg, O. (2016). Severe infantile male encephalopathy is a result of early post-zygotic WDR45 somatic mutation. Clin. Genet. 90, 560–562.10.1111/cge.12849Search in Google Scholar PubMed

Spillantini, M.G. and Goedert, M. (2013). Tau pathology and neurodegeneration. Lancet Neurol. 12, 609–622.10.1016/S1474-4422(13)70090-5Search in Google Scholar PubMed

Srivastava, S., Desai, S., Cohen, J., Smith-Hicks, C., Barañano, K., Fatemi, A., and Naidu, S. (2018). Monogenic disorders that mimic the phenotype of Rett syndrome. Neurogenetics 19, 41–47.10.1007/s10048-017-0535-3Search in Google Scholar PubMed PubMed Central

Stevanin, G., Santorelli, F.M., Azzedine, H., Coutinho, P., Chomilier, J., Denora, P.S., Martin, E., Ouvrard-Hernandez, A.M., Tessa, A., Bouslam, N., et al. (2007). Mutations in SPG11, encoding spatacsin, are a major cause of spastic paraplegia with thin corpus callosum. Nat. Genet. 39, 366–372.10.1038/ng1980Search in Google Scholar PubMed

Takano, K., Shiba, N., Wakui, K., Yamaguchi, T., Aida, N., Inaba, Y., Fukushima, Y., and Kosho, T. (2016). Elevation of neuron specific enolase and brain iron deposition on susceptibility-weighted imaging as diagnostic clues for beta-propeller protein-associated neurodegeneration in early childhood: additional case report and review of the literature. Am. J. Med. Genet A. 170A, 322–328.10.1002/ajmg.a.37432Search in Google Scholar PubMed

Takano, K., Goto, K., Motobayashi, M., Wakui, K., Kawamura, R., Yamaguchi, T., Fukushima, Y., and Kosho, T. (2017). Early manifestations of epileptic encephalopathy, brain atrophy, and elevation of serum neuron specific enolase in a boy with β-propeller protein-associated neurodegeneration. Eur. J. Med. Genet. 60, 521–526.10.1016/j.ejmg.2017.07.008Search in Google Scholar PubMed

Tang, B.L. (2016). C9orf72’s interaction with Rab GTPases-Modulation of membrane traffic and autophagy. Front. Cell. Neurosci. 10, 228.10.3389/fncel.2016.00228Search in Google Scholar PubMed PubMed Central

Tang, G., Gudsnuk, K., Kuo, S.H., Cotrina, M.L., Rosoklija, G., Sosunov, A., Sonders, M.S., Kanter, E., Castagna, C., Yamamoto, A., et al. (2014). Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron 83, 1131–1143.10.1016/j.neuron.2014.07.040Search in Google Scholar PubMed

Tello, C., Darling, A., Lupo, V., Pérez-Dueñas, B., and Espinós, C. (2018). On the complexity of clinical and molecular bases of neurodegeneration with brain iron accumulation. Clin. Genet. 93, 731–740.10.1111/cge.13057Search in Google Scholar PubMed

Thomas, A.C., Williams, H., Setó-Salvia, N., Bacchelli, C., Jenkins, D., O’Sullivan, M., Mengrelis, K., Ishida, M., Ocaka, L., Chanudet, E., et al. (2014). Mutations in SNX14 cause a distinctive autosomal-recessive cerebellar ataxia and intellectual disability syndrome. Am. J. Hum. Genet. 95, 611–621.10.1016/j.ajhg.2014.10.007Search in Google Scholar

Tomaskovic-Crook, E. and Crook, J.M. (2017). Clinically amendable, defined, and rapid induction of human brain organoids from induced pluripotent stem cells. Methods Mol Biol. Doi: 10.1007/7651_2017_95.10.1007/7651_2017_95Search in Google Scholar PubMed

Tomoda, T., Bhatt, R.S., Kuroyanagi, H., Shirasawa, T., and Hatten, M.E. (1999). A mouse serine/threonine kinase homologous to C. elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 24, 833–846.10.1016/S0896-6273(00)81031-4Search in Google Scholar

Truban, D., Hou, X., Caulfield, T.R., Fiesel, F.C., and Springer, W. (2017). PINK1, Parkin, and mitochondrial quality control: What can we learn about Parkinson’s disease pathobiology? J. Parkinson’s Dis. 7, 13–29.10.3233/JPD-160989Search in Google Scholar PubMed PubMed Central

Tschentscher, A., Dekomien, G., Ross, S., Cremer, K., Kukuk, G.M., Epplen, J.T., and Hoffjan, S. (2015). Analysis of the C19orf12 and WDR45 genes in patients with neurodegeneration with brain iron accumulation. J. Neurol. Sci. 349, 105–109.10.1016/j.jns.2014.12.036Search in Google Scholar PubMed

Tsukamoto, S., Kuma, A., Murakami, M., Kishi, C., Yamamoto, A., and Mizushima, N. (2008). Autophagy is essential for preimplantation development of mouse embryos. Science 321, 117–120.10.1126/science.1154822Search in Google Scholar PubMed

Valente, E.M., Abou-Sleiman, P.M., Caputo, V., Muqit, M.M.K., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A.R., Healy, D.G., et al. (2004). Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 304, 1158–1160.10.1126/science.1096284Search in Google Scholar PubMed

Velikkakath, A.K.G., Nishimura, T., Oita, E., Ishihara, N., and Mizushima, N. (2012). Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol. Biol. Cell. 23, 896–909.10.1091/mbc.e11-09-0785Search in Google Scholar PubMed PubMed Central

Wang, R.C., Wei, Y., An, Z., Zou, Z., Xiao, G., Bhagat, G., White, M., Reichelt, J., and Levine, B. (2012). Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 338, 956–959.10.1126/science.1225967Search in Google Scholar PubMed PubMed Central

Wang, H., Bedford, F.K., Brandon, N.J., Moss, S.J., and Olsen, R.W. (1999). GABA_A-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397, 69–72.10.1038/16264Search in Google Scholar PubMed

Wang, B., Iyengar, R., Li-Harms, X., Joo, J.H., Wright, C., Lavado, A., Horner, L., Yang, M., Guan, J.L., Frase, S., et al. (2017). The autophagy-inducing kinases, ULK1 and ULK2, regulate axon guidance in the developing mouse forebrain via a noncanonical pathway. Autophagy 14, 796–811.10.1080/15548627.2017.1386820Search in Google Scholar PubMed PubMed Central

Wauer, T., Simicek, M., Schubert, A., and Komander, D. (2015). Mechanism of phospho-ubiquitin-induced PARKIN activation. Nature 524, 370–374.10.1038/nature14879Search in Google Scholar PubMed PubMed Central

Webster, C.P., Smith, E.F., Bauer, C.S., Moller, A., Hautbergue, G.M., Ferraiuolo, L., Myszczynska, M.A., Higginbottom, A., Walsh, M.J., Whitworth, A.J., et al. (2016). The C9orf72 protein interacts with Rab1a and the ULK1 complex to regulate initiation of autophagy. EMBO J. 35, 1656–1676.10.15252/embj.201694401Search in Google Scholar PubMed PubMed Central

Weidberg, H., Shvets, E., Shpilka, T., Shimron, F., Shinder, V., and Elazar, Z. (2010). LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 29, 1792–1802.10.1038/emboj.2010.74Search in Google Scholar PubMed PubMed Central

Weishaupt, J.H., Hyman, T., and Dikic, I. (2016). Common molecular pathways in amyotrophic lateral sclerosis and frontotemporal dementia. Trends Mol. Med. 22, 769–783.10.1016/j.molmed.2016.07.005Search in Google Scholar PubMed

Xiao, Y., Chen, X., Huang, S., Li, G., Mo, M., Zhang, L., Chen, C., Guo, W., Zhou, M., Wu, Z., et al. (2018). Iron promotes α-synuclein aggregation and transmission by inhibiting TFEB-mediated autophagosome-lysosome fusion. J. Neurochem. 145, 34–50.10.1111/jnc.14312Search in Google Scholar PubMed

Xilouri, M., Brekk, O.R., and Stefanis, L. (2016). Autophagy and alpha-synuclein: relevance to Parkinson’s disease and related synucleopathies. Mov. Disord. 31, 178–192.10.1002/mds.26477Search in Google Scholar PubMed

Xixis, K.I., and Mikati, M.A. (2016). Epileptic spasms: a previously unreported manifestation of WDR45 gene mutation. Epileptic Disord. 18, 336.10.1684/epd.2016.0840Search in Google Scholar PubMed

Xu, C.Y., Kang, W.Y., Chen, Y.M., Jiang, T.F., Zhang, J., Zhang, L.N., Ding, J.Q., Liu, J., and Chen, S.D. (2017). DJ-1 inhibits α-Synuclein aggregation by regulating chaperone-mediated autophagy. Front. Aging Neurosci. 9, 308.10.3389/fnagi.2017.00308Search in Google Scholar PubMed PubMed Central

Yang, M., Liang, C., Swaminathan, K., Herrlinger, S., Lai, F., Shiekhattar, R., and Chen, J.F. (2016). A C9ORF72/SMCR8-containing complex regulates ULK1 and plays a dual role in autophagy. Sci. Adv. 2, e1601167.10.1126/sciadv.1601167Search in Google Scholar PubMed PubMed Central

Yazdankhah, M., Farioli-Vecchioli, S., Tonchev, A.B., Stoykova, A., and Cecconi, F. (2014). The autophagy regulators Ambra1 and Beclin 1 are required for adult neurogenesis in the brain subventricular zone. Cell Death Dis. 5, e1403.10.1038/cddis.2014.358Search in Google Scholar PubMed PubMed Central

Yu, L., Chen, Y., and Tooze, S.A. (2017). Autophagy pathway: cellular and molecular mechanisms. Autophagy 14, 207–215.10.1080/15548627.2017.1378838Search in Google Scholar PubMed PubMed Central

Zarate, Y.A., Jones, J.R., Jones, M.A., Millan, F., Juusola, J., Vertino-Bell, A., Schaefer, G.B., and Kruer, M.C. (2016). Lessons from a pair of siblings with BPAN. Eur. J. Hum. Genet. 24, 1080–1083.10.1038/ejhg.2015.242Search in Google Scholar PubMed PubMed Central

Zhang, Y., Mikhael, M., Xu, D., Li, Y., Soe-Lin, S., Ning, B., Li, W., Nie, G., Zhao, Y., and Ponka, P. (2010). Lysosomal proteolysis is the primary degradation pathway for cytosolic ferritin and cytosolic ferritin degradation is necessary for iron exit. Antioxid. Redox Signal. 13, 999–1009.10.1089/ars.2010.3129Search in Google Scholar PubMed

Zhao, H., Zhao, Y.G., Wang, X., Xu, L., Miao, L., Feng, D., Chen, Q., Kovács, A.L., Fan, D., and Zhang, H. (2013). Mice deficient in Epg5 exhibit selective neuronal vulnerability to degeneration. J. Cell. Biol. 200, 731–741.10.1083/jcb.201211014Search in Google Scholar PubMed PubMed Central

Zhao, Y.G., Sun, L., Miao, G., Ji, C., Zhao, H., Sun, H., Miao, L., Yoshii, S.R., Mizushima, N., Wang, X., et al. (2015). The autophagy gene Wdr45/Wipi4 regulates learning and memory function and axonal homeostasis. Autophagy 11, 881–890.10.1080/15548627.2015.1047127Search in Google Scholar PubMed PubMed Central

Zheng, J.X., Li, Y., Ding, Y.H., Liu, J.J., Zhang, M.J., Dong, M.Q., Wang, H.W., and Yu, L. (2017). Architecture of the ATG2B-WDR45 complex and an aromatic Y/HF motif crucial for complex formation. Autophagy 13, 1870–1883.10.1080/15548627.2017.1359381Search in Google Scholar PubMed PubMed Central

Zimprich, A., Biskup, S., Leitner, P., Lichtner, P., Farrer, M., Lincoln, S., Kachergus, J., Hulihan, M., Uitti, R.J., Calne, D.B., et al. (2004). Mutations in LRRK2 cause autosomal-dominant Parkinsonism with pleomorphic pathology. Neuron 44, 601–607.10.1016/j.neuron.2004.11.005Search in Google Scholar PubMed

Zoghbi, H.Y., and Bear, M.F. (2012). Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol. 4, pii: a009886.10.1101/cshperspect.a009886Search in Google Scholar PubMed PubMed Central