A Missense Change in the ATG4D Gene Links Aberrant Autophagy to a Neurodegenerative Vacuolar Storage Disease

PLoS Genetics

Volumn 11, Issue 4, 2015, Pages

  Kyöstilä, Kaisa ^a,b   Syrjä, Pernilla ^a   Jagannathan, Vidhya ^c   Chandrasekar, Gayathri ^d   Jokinen, Tarja S ^a   Seppälä, Eija H ^a,b   Becker, Doreen ^c   Drögemüller, Michaela ^c   Dietschi, Elisabeth ^c   Drögemüller, Cord ^c   Lang, Johann ^c   Steffen, Frank ^e   Rohdin, Cecilia ^f   Jäderlund, Karin H ^g   Lappalainen, Anu K ^a   Hahn, Kerstin ^h   Wohlsein, Peter ^h   Baumgärtner, Wolfgang ^h   Henke, Diana ^c   Oevermann, Anna ^c   Kere, Juha ^a,b,d   Lohi, Hannes ^a,b   Leeb, Tosso ^c   more..

^a UNIVERSITY OF HELSINKI   (Finland)

^b FOLKHÄLSAN INSTITUTE OF GENETICS   (Finland)

^c UNIVERSITY OF BERN   (Switzerland)

^d KAROLINSKA INSTITUTE   (Sweden)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^g NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^h UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYSTEINE PROTEINASE; GUANINE; PROTEIN ATG4D; THYMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATG4D GENE; AUTOPHAGY; BEHAVIOR CHANGE; BREEDING; CELL AGGREGATION; CELL VACUOLE; CEREBELLAR ATAXIA; CHROMOSOME 20; CLINICAL EXAMINATION; CONTROLLED STUDY; CYTOPLASM; DEGENERATIVE DISEASE; DOG; EPITHELIUM; FEMALE; GENE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC CODE; GENETIC LINKAGE; HISTOPATHOLOGY; MACROAUTOPHAGY; MALE; MESENCHYME CELL; MISSENSE MUTATION; NERVOUS SYSTEM; NEURODEGENERATIVE VACUOLAR STORAGE DISEASE; NONHUMAN; NYSTAGMUS; PHENOTYPE; SPHEROID CELL; AMINO ACID SEQUENCE; ANIMAL; BRAIN; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; VETERINARY; ZEBRA FISH;

CANIS FAMILIARIS; DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; AUTOPHAGY; BASE SEQUENCE; BRAIN; CYSTEINE ENDOPEPTIDASES; DOGS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NEURODEGENERATIVE DISEASES; VACUOLES; ZEBRAFISH;

EID: 84930369233     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005169     Document Type: Article

References (49)

1. Jellinger KA, Basic mechanisms of neurodegeneration: A critical update. J Cell Mol Med. 2010;14(3): 457–487. doi: 10.1111/j.1582-4934.2010.01010.x 20070435
2. Murrow L, Debnath J, Autophagy as a stress-response and quality-control mechanism: Implications for cell injury and human disease. Annu Rev Pathol. 2013;8: 105–137. doi: 10.1146/annurev-pathol-020712-163918 23072311
3. Amm I, Sommer T, Wolf DH, Protein quality control and elimination of protein waste: The role of the ubiquitin-proteasome system. Biochim Biophys Acta. 2014;1843(1): 182–196. doi: 10.1016/j.bbamcr.2013.06.031 23850760
4. Korolchuk VI, Menzies FM, Rubinsztein DC, Mechanisms of cross-talk between the ubiquitin-proteasome and autophagy-lysosome systems. FEBS Lett. 2010;584(7): 1393–1398. doi: 10.1016/j.febslet.2009.12.047 20040365
5. Schreiber A, Peter M, Substrate recognition in selective autophagy and the ubiquitin-proteasome system. Biochim Biophys Acta. 2014;1843(1): 163–181. doi: 10.1016/j.bbamcr.2013.03.019 23545414
6. Tai HC, Schuman EM, Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat Rev Neurosci. 2008;9(11): 826–838. doi: 10.1038/nrn2499 18931696
7. Yang Y, Coleman M, Zhang L, Zheng X, Yue Z, Autophagy in axonal and dendritic degeneration. Trends Neurosci. 2013;36(7): 418–428. doi: 10.1016/j.tins.2013.04.001 23639383
8. Platt FM, Boland B, van der Spoel AC, The cell biology of disease: Lysosomal storage disorders: The cellular impact of lysosomal dysfunction. J Cell Biol. 2012;199(5): 723–734. doi: 10.1083/jcb.201208152 23185029
9. Boustany RM, Lysosomal storage diseases—the horizon expands. Nat Rev Neurol. 2013;9(10): 583–598. doi: 10.1038/nrneurol.2013.163 23938739
10. Schultz ML, Tecedor L, Chang M, Davidson BL, Clarifying lysosomal storage diseases. Trends Neurosci. 2011;34(8): 401–410. doi: 10.1016/j.tins.2011.05.006 21723623
11. Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T, et al. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature. 2000;406(6798): 906–910. 10972294
12. Wang D, Chan CC, Cherry S, Hiesinger PR, Membrane trafficking in neuronal maintenance and degeneration. Cell Mol Life Sci. 2013;70(16): 2919–2934. doi: 10.1007/s00018-012-1201-4 23132096
13. Lieberman AP, Puertollano R, Raben N, Slaugenhaupt S, Walkley SU, Ballabio A, Autophagy in lysosomal storage disorders. Autophagy. 2012;8(5): 719–730. doi: 10.4161/auto.19469 22647656
14. O'Brien DP, Leeb T, DNA testing in neurologic diseases. J Vet Intern Med. 2014;28(4): 1186–1198. doi: 10.1111/jvim.12383 24962505
15. Marino G, Uria JA, Puente XS, Quesada V, Bordallo J, Lopez-Otin C, Human autophagins, a family of cysteine proteinases potentially implicated in cell degradation by autophagy. J Biol Chem. 2003;278(6): 3671–3678. 12446702
16. Betin VM, Lane JD, Caspase cleavage of Atg4D stimulates GABARAP-L1 processing and triggers mitochondrial targeting and apoptosis. J Cell Sci. 2009;122(Pt 14): 2554–2566. doi: 10.1242/jcs.046250 19549685
17. Betin VM, MacVicar TD, Parsons SF, Anstee DJ, Lane JD, A cryptic mitochondrial targeting motif in Atg4D links caspase cleavage with mitochondrial import and oxidative stress. Autophagy. 2012;8(4): 664–676. doi: 10.4161/auto.19227 22441018
18. Bendl J, Stourac J, Salanda O, Pavelka A, Wieben ED, Zendulka J, et al. PredictSNP: Robust and accurate consensus classifier for prediction of disease-related mutations. PLoS Comput Biol. 2014;10(1): e1003440. doi: 10.1371/journal.pcbi.1003440 24453961
19. Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf DH, Thumm M, Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. Embo j. 1998;17(13): 3597–3607. 9649430
20. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol. 2000;151(2): 263–276. 11038174
21. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, et al. A ubiquitin-like system mediates protein lipidation. Nature. 2000;408(6811): 488–492. 11100732
22. Kim J, Huang WP, Klionsky DJ, Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J Cell Biol. 2001;152(1): 51–64. 11149920
23. Xie Z, Nair U, Klionsky DJ, Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell. 2008;19(8): 3290–3298. doi: 10.1091/mbc.E07-12-1292 18508918
24. Kaufmann A, Beier V, Franquelim HG, Wollert T, Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell. 2014;156(3): 469–481. doi: 10.1016/j.cell.2013.12.022 24485455
25. Kirisako T, Baba M, Ishihara N, Miyazawa K, Ohsumi M, Yoshimori T, et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J Cell Biol. 1999;147(2): 435–446. 10525546
26. Nakatogawa H, Ichimura Y, Ohsumi Y, Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell. 2007;130(1): 165–178. 17632063
27. Shpilka T, Weidberg H, Pietrokovski S, Elazar Z, Atg8: An autophagy-related ubiquitin-like protein family. Genome Biol. 2011;12(7): 226-2011-12-7-226. doi: 10.1186/gb-2011-12-7-226 21867568
28. Xin Y, Yu L, Chen Z, Zheng L, Fu Q, Jiang J, et al. Cloning, expression patterns, and chromosome localization of three human and two mouse homologues of GABA(A) receptor-associated protein. Genomics. 2001;74(3): 408–413. 11414770
29. He H, Dang Y, Dai F, Guo Z, Wu J, She X, et al. Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem. 2003;278(31): 29278–29287. 12740394
30. Nemos C, Mansuy V, Vernier-Magnin S, Fraichard A, Jouvenot M, Delage-Mourroux R, Expression of gec1/GABARAPL1 versus GABARAP mRNAs in human: Predominance of gec1/GABARAPL1 in the central nervous system. Brain Res Mol Brain Res. 2003;119(2): 216–219. 14625090
31. Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z, LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. Embo j. 2010;29(11): 1792–1802. doi: 10.1038/emboj.2010.74 20418806
32. Marino G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, Lopez-Otin C, Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J Biol Chem. 2007;282(25): 18573–18583. 17442669
33. Kabeya Y, Mizushima N, Yamamoto A, Oshitani-Okamoto S, Ohsumi Y, Yoshimori T, LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J Cell Sci. 2004;117(Pt 13): 2805–2812. 15169837
34. Li M, Hou Y, Wang J, Chen X, Shao ZM, Yin XM, Kinetics comparisons of mammalian Atg4 homologues indicate selective preferences toward diverse Atg8 substrates. J Biol Chem. 2011;286(9): 7327–7338. doi: 10.1074/jbc.M110.199059 21177865
35. Marino G, Fernandez AF, Cabrera S, Lundberg YW, Cabanillas R, Rodriguez F, et al. Autophagy is essential for mouse sense of balance. J Clin Invest. 2010;120(7): 2331–2344. doi: 10.1172/JCI42601 20577052
36. Read R, Savelieva K, Baker K, Hansen G, Vogel P, Histopathological and neurological features of Atg4b knockout mice. Vet Pathol. 2011;48(2): 486–494. doi: 10.1177/0300985810375810 20634410
37. Magdaleno S, Jensen P, Brumwell CL, Seal A, Lehman K, Asbury A, et al. BGEM: An in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol. 2006;4(4): e86. 16602821
38. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006;441(7095): 885–889. 16625204
39. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006;441(7095): 880–884. 16625205
40. Agler C, Nielsen DM, Urkasemsin G, Singleton A, Tonomura N, Sigurdsson S, et al. Canine hereditary ataxia in Old English Sheepdogs and Gordon Setters is associated with a defect in the autophagy gene encoding RAB24. PLoS Genet. 2014;10(2): e1003991. doi: 10.1371/journal.pgen.1003991 24516392
41. Deretic V, Jiang S, Dupont N, Autophagy intersections with conventional and unconventional secretion in tissue development, remodeling and inflammation. Trends Cell Biol. 2012;22(8): 397–406. doi: 10.1016/j.tcb.2012.04.008 22677446
42. Mizushima N, Yoshimori T, Levine B, Methods in mammalian autophagy research. Cell. 2010;140(3): 313–326. doi: 10.1016/j.cell.2010.01.028 20144757
43. Abecasis GR, Cherny SS, Cookson WO, Cardon LR, Merlin—rapid analysis of dense genetic maps using sparse gene flow trees. Nat Genet. 2002;30(1): 97–101. 11731797
44. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, et al. PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics. 2007;81(3): 559–575. 17701901
45. Drogemuller C, Becker D, Brunner A, Haase B, Kircher P, Seeliger F, et al. A missense mutation in the SERPINH1 gene in Dachshunds with osteogenesis imperfecta. PLoS Genet. 2009;5(7): e1000579. doi: 10.1371/journal.pgen.1000579 19629171
46. Li H, Durbin R, Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics. 2009;25(14): 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168
47. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20(9): 1297–1303. doi: 10.1101/gr.107524.110 20644199
48. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 2012;6(2): 80–92. doi: 10.4161/fly.19695 22728672
49. Bae YK, Kani S, Shimizu T, Tanabe K, Nojima H, Kimura Y, et al. Anatomy of zebrafish cerebellum and screen for mutations affecting its development. Dev Biol. 2009;330(2): 406–426. doi: 10.1016/j.ydbio.2009.04.013 19371731