Autophagy in lysosomal storage disorders

Autophagy

Volumn 8, Issue 5, 2012, Pages 719-730

  Lieberman, Andrew P ^a   Puertollano, Rosa ^b,c   Raben, Nina ^b,d   Slaugenhaupt, Susan ^e   Walkley, Steven U ^f   Ballabio, Andrea ^g,h,i  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d Laboratory of Muscle Stem Cells and Gene Regulation   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^g TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^h TEXAS CHILDREN S HOSPITAL   (United States)

ⁱ UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Autophagy; Glycogenosis; Lysosomal storage disorders; Lysosomes; Mucolipidosis type IV; Mucopolysaccharidoses; Sphingolipidoses

Indexed keywords

CALCIUM; LIPID;

AUTOPHAGOSOME; AUTOPHAGY; CELL MEMBRANE; CELL MIGRATION; DANON DISEASE; GLYCOGEN STORAGE DISEASE TYPE 2; HOMEOSTASIS; HUMAN; LIPID DEGRADATION; LIPIDOSIS; LIPOGENESIS; LYSOSOME; LYSOSOME STORAGE DISEASE; MUCOLIPIDOSIS; MUCOPOLYSACCHARIDOSIS; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; REVIEW;

EID: 84862602473     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.4161/auto.19469     Document Type: Review

References (132)

1. Luzio JP, Pryor PR, Bright NA. Lysosomes: fusion and function. Nat Rev Mol Cell Biol 2007; 8:622-32; PMID:17637737; http://dx.doi.org/10.1038/nrm2217
2. Piper RC, Luzio JP. Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr Opin Cell Biol 2007; 19:459-65; PMID: 17689064; http://dx.doi.org/10.1016/j.ceb.2007.07.002
3. Yu L, McPhee CK, Zheng L, Mardones GA, Rong Y, Peng J, et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature 2010; 465:942-6; PMID:20526321; http://dx.doi.org/10.1038/nature09076
4. Hers HG. alpha-Glucosidase deficiency in generalized glycogenstorage disease (Pompe's disease). Biochem J 1963; 86:11-6; PMID:13954110
5. Platt FM, Walkley SU. Lysosomal Disorders of the Brain. Oxford University Press, 2004.
6. Ballabio A, Gieselmann V. Lysosomal disorders: from storage to cellular damage. Biochim Biophys Acta 2009; 1793:684-96; PMID:19111581; http://dx.doi.org/10.1016/j.bbamcr.2008.12.001
7. Walkley SU. Pathogenic cascades in lysosomal disease - Why so complex? J Inherit Metab Dis 2009; 32:181-9; PMID:19130290; http://dx.doi.org/10.1007/ s10545-008-1040-5
8. Sardiello M, Ballabio A. Lysosomal enhancement: a CLEAR answer to cellular degradative needs. Cell Cycle 2009; 8:4021-2; PMID:19949301; http://dx.doi.org/10.4161/cc.8.24.10263
9. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, et al. TFEB links autophagy to lysosomal biogenesis. Science 2011; 332:1429-33; PMID:21617040; http://dx.doi.org/10.1126/science.1204592
10. Settembre C, Fraldi A, Rubinsztein DC, Ballabio A. Lysosomal storage diseases as disorders of autophagy. Autophagy 2008; 4:113-4; PMID:18000397
11. Raben N, Hill V, Shea L, Takikita S, Baum R, Mizushima N, et al. Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease. Hum Mol Genet 2008; 17:3897-908; PMID:18782848; http://dx.doi.org/10. 1093/hmg/ddn292
12. Raben N, Schreiner C, Baum R, Takikita S, Xu S, Xie T, et al. Suppression of autophagy permits successful enzyme replacement therapy in a lysosomal storage disorder-murine Pompe disease. Autophagy 2010; 6:1078-89; PMID:20861693; http://dx.doi.org/10.4161/auto.6.8.13378
13. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, Lüllmann-Rauch R, et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000; 406:902-6; PMID: 10972293; http://dx.doi.org/10.1038/35022595
14. Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, et al. A block of autophagy in lysosomal storage disorders. Hum Mol Genet 2008; 17:119-29; PMID:17913701; http://dx.doi.org/10.1093/hmg/ddm289
15. Fraldi A, Annunziata F, Lombardi A, Kaiser HJ, Medina DL, Spampanato C, et al. Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J 2010; 29:3607-20; PMID:20871593; http://dx.doi.org/10.1038/emboj.2010.237
16. Tessitore A, Pirozzi M, Auricchio A. Abnormal autophagy, ubiquitination, inflammation and apoptosis are dependent upon lysosomal storage and are useful biomarkers of mucopolysaccharidosis VI. Pathogenetics 2009; 2:4; PMID:19531206; http://dx.doi.org/10.1186/1755-8417-2-4
17. Ko DC, Milenkovic L, Beier SM, Manuel H, Buchanan J, Scott MP. Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet 2005; 1:81-95; PMID:16103921
18. Pacheco CD, Elrick MJ, Lieberman AP. Tau deletion exacerbates the phenotype of Niemann-Pick type C mice and implicates autophagy in pathogenesis. Hum Mol Genet 2009; 18:956-65; PMID:19074461
19. Sun Y, Liou B, Ran H, Skelton MR, Williams MT, Vorhees CV, et al. Neuronopathic Gaucher disease in the mouse: viable combined selective saposin C deficiency and mutant glucocerebrosidase (V394L) mice with glucosylsphingosine and glucosylceramide accumulation and progressive neurological deficits. Hum Mol Genet 2010; 19:1088-97; PMID:20047948; http://dx.doi.org/10.1093/hmg/ddp580
20. Chévrier M, Brakch N, Céline L, Genty D, Ramdani Y, Moll S, et al. Autophagosome maturation is impaired in Fabry disease. Autophagy 2010; 6:589- 99; PMID:20431343; http://dx.doi.org/10.4161/auto.6.5.11943
21. Takamura A, Higaki K, Kajimaki K, Otsuka S, Ninomiya H, Matsuda J, et al. Enhanced autophagy and mitochondrial aberrations in murine G(M1)- gangliosidosis. Biochem Biophys Res Commun 2008;367:616-22; PMID:18190792; http://dx.doi.org/10.1016/j.bbrc.2007.12.187
22. Otomo T, Higaki K, Nanba E, Ozono K, Sakai N. Inhibition of autophagosome formation restores mitochondrial function in mucolipidosis II and III skin fibroblasts. Mol Genet Metab 2009; 98:393-9; PMID: 19656701; http://dx.doi.org/10.1016/j.ymgme.2009.07.002
23. Kobayashi H, Takahashi-Fujigasaki J, Fukuda T, Sakurai K, Shimada Y, Nomura K, et al. Pathology of the first autopsy case diagnosed as mucolipidosis type III α/β suggesting autophagic dysfunction. Mol Genet Metab 2011; 102:170-5; PMID:21051253; http://dx.doi.org/10.1016/j.ymgme.2010.09.014
24. Vergarajauregui S, Connelly PS, Daniels MP, Puertollano R. Autophagic dysfunction in mucolipidosis type IV patients. Hum Mol Genet 2008; 17:2723-37; PMID:18550655; http://dx.doi.org/10.1093/hmg/ddn174
25. Venugopal B, Mesires NT, Kennedy JC, Curcio-Morelli C, Laplante JM, Dice JF, et al. Chaperone-mediated autophagy is defective in mucolipidosis type IV. J Cell Physiol 2009; 219:344-53; PMID: 19117012; http://dx.doi.org/10.1002/jcp. 21676
26. Curcio-Morelli C, Charles FA, Micsenyi MC, Cao Y, Venugopal B, Browning MF, et al. Macroautophagy is defective in mucolipin-1-deficient mouse neurons. Neurobiol Dis 2010; 40:370-7; PMID:20600908; http://dx.doi.org/10.1016/j.nbd. 2010.06.010
27. Koike M, Shibata M, Waguri S, Yoshimura K, Tanida I, Kominami E, et al. Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease). Am J Pathol 2005; 167:1713-28; PMID:16314482; http://dx.doi.org/10.1016/S0002-9440(10)61253-9
28. Cao Y, Espinola JA, Fossale E, Massey AC, Cuervo AM, MacDonald ME, et al. Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J Biol Chem 2006; 281:20483-93; PMID:16714284; http://dx.doi.org/10.1074/jbc.M602180200
29. van der Ploeg AT, Reuser AJ. Pompe's disease. Lancet 2008; 372:1342-53; PMID:18929906; http://dx.doi.org/10.1016/S0140-6736(08)61555-X
30. Hirschhorn R, Reuser A. Glycogen storage disease type II: acid a-glucosidase (acid maltase) deficiency. In: Scriver C, Beaudet A, Sly W, Valle D, eds. The metabolic and molecular bases of inherited disease. New York, NY: McGraw-Hill; 2001:3389-420
31. Pompe JC. Over idiopatische hypertrophie van het hart. Ned Tijdschr Geneeskd 1932; 76:304.
32. Griffin JL. Infantile acid maltase deficiency. I. Muscle fiber destruction after lysosomal rupture. Virchows Arch B Cell Pathol Incl Mol Pathol 1984; 45:23-36; PMID: 6199885; http://dx.doi.org/10.1007/BF02889849
33. Thurberg BL, Lynch Maloney C, Vaccaro C, Afonso K, Tsai AC, Bossen E, et al. Characterization of pre- and post-treatment pathology after enzyme replacement therapy for Pompe disease. Lab Invest 2006; 86:1208-20; PMID:17075580; http://dx.doi.org/10.1038/labinvest.3700484
34. Raben N, Fukuda T, Gilbert AL, de Jong D, Thurberg BL, Mattaliano RJ, et al. Replacing acid alpha-glucosidase in Pompe disease: recombinant and transgenic enzymes are equipotent, but neither completely clears glycogen from type II muscle fibers. Mol Ther 2005; 11:48-56; PMID:15585405; http://dx.doi.org/10.1016/j.ymthe.2004.09.017
35. Xu S, Galperin M, Melvin G, Horowits R, Raben N, Plotz P, et al. Impaired organization and function of myofilaments in single muscle fibers from a mouse model of Pompe disease. J Appl Physiol 2010; 108:1383-8; PMID:20223998; http://dx.doi.org/10.1152/japplphysiol.01253.2009
36. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010; 140:313-26; PMID:20144757; http://dx.doi.org/10.1016/j. cell.2010.01.028
37. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, et al. 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; http://dx.doi.org/10.1083/jcb.200507002
38. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282:24131-45; PMID:17580304; http://dx.doi.org/10.1074/jbc.M702824200
39. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, Ueno T, et al. Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 2008; 283:22847-57; PMID:18524774; http://dx.doi.org/10.1074/jbc.M802182200
40. Berg TO, Fengsrud M, Strømhaug PE, Berg T, Seglen PO. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 1998; 273:21883-92; PMID:9705327; http://dx.doi.org/10.1074/jbc.273.34.21883
41. Fukuda T, Roberts A, Ahearn M, Zaal K, Ralston E, Plotz PH, et al. Autophagy and lysosomes in Pompe disease. Autophagy 2006; 2:318-20; PMID:16874053
42. Fukuda T, Ahearn M, Roberts A, Mattaliano RJ, Zaal K, Ralston E, et al. Autophagy and mistargeting of therapeutic enzyme in skeletal muscle in Pompe disease. Mol Ther 2006; 14:831-9; PMID:17008131; http://dx.doi.org/10.1016/j. ymthe.2006.08.009
43. Raben N, Wong A, Ralston E, Myerowitz R. Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am J Med Genet C Semin Med Genet 2012; 160:13-21; PMID: 22253254; http://dx.doi.org/10.1002/ ajmg.c.31317
44. Wu JJ, Quijano C, Chen E, Liu H, Cao L, Fergusson MM, et al. Mitochondrial dysfunction and oxidative stress mediate the physiological impairment induced by the disruption of autophagy. [AlbanyNY]. Aging (Albany NY) 2009; 1:425-37; PMID:20157526
45. Masiero E, Sandri M. Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles. Autophagy 2010; 6:307-9; PMID:20104028; http://dx.doi.org/10.4161/auto.6.2.11137
46. Raben N, Takikita S, Pittis MG, Bembi B, Marie SKN, Roberts A, et al. Deconstructing Pompe disease by analyzing single muscle fibers: to see a world in a grain of sand. Autophagy 2007; 3:546-52; PMID: 17592248
47. Raben N, Ralston E, Chien YH, Baum R, Schreiner C, Hwu WL, et al. Differences in the predominance of lysosomal and autophagic pathologies between infants and adults with Pompe disease: implications for therapy. Mol Genet Metab 2010; 101:324-31; PMID: 20801068; http://dx.doi.org/10.1016/j.ymgme.2010.08.001
48. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, et al. The role of autophagy during the early neonatal starvation period. Nature 2004; 432:1032-6; PMID:15525940; http://dx.doi.org/10.1038/nature03029
49. Schiaffino S, Hanzlíková V. Autophagic degradation of glycogen in skeletal muscles of the newborn rat. J Cell Biol 1972; 52:41-51; PMID:4331300; http://dx.doi.org/10.1083/jcb.52.1.41
50. Kondomerkos DJ, Kalamidas SA, Kotoulas OB, Hann AC. Glycogen autophagy in the liver and heart of newborn rats. The effects of glucagon, adrenalin or rapamycin. Histol Histopathol 2005; 20:689-96; PMID:15944916
51. Jiang S, Heller B, Tagliabracci VS, Zhai L, Irimia JM, DePaoli-Roach AA, et al. Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism. J Biol Chem 2010; 285:34960-71; PMID:20810658; http://dx.doi.org/10.1074/jbc.M110.150839
52. 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; 406:906-10; PMID:10972294; http://dx.doi.org/10.1038/ 35022604
53. Neufeld E, Muenzer J. The mucopolysaccharidoses New York: McGraw-Hill, 2001.
54. Cosma MP, Pepe S, Annunziata I, Newbold RF, Grompe M, Parenti G, et al. The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell 2003; 113:445-56; PMID:12757706; http://dx.doi.org/10.1016/S0092-8674(03)00348-9
55. Dierks T, Schmidt B, Borissenko LV, Peng J, Preusser A, Mariappan M, et al. Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme. Cell 2003; 113:435-44; PMID:12757705; http://dx.doi.org/10.1016/S0092-8674(03)00347-7
56. Hopwood JJ, Ballabio A. Multiple Sulfatase Deficiency and the Nature of the Sulfatase Family. In: Scriver CR, Beaudet AL, Valle D, Sly WS, Childs B, Kinzler KW, et al., eds. The Metabolic & Molecular Bases of Inherited Disease. New York: McGraw Hill, 2001: 3725-32.
57. Settembre C, Annunziata I, Spampanato C, Zarcone D, Cobellis G, Nusco E, et al. Systemic inflammation and neurodegeneration in a mouse model of multiple sulfatase deficiency. Proc Natl Acad Sci U S A 2007; 104:4506-11; PMID:17360554; http://dx.doi.org/10.1073/pnas.0700382104
58. Settembre C, Arteaga-Solis E, McKee MD, de Pablo R, Al Awqati Q, Ballabio A, et al. Proteoglycan desulfation determines the efficiency of chondrocyte autophagy and the extent of FGF signaling during endochondral ossification. Genes Dev 2008; 22:2645-50; PMID:18832069; http://dx.doi.org/10.1101/gad.1711308
59. Hopwood JJ, Morris CP. The mucopolysaccharidoses. Diagnosis, molecular genetics and treatment. Mol Biol Med 1990; 7:381-404; PMID:2128891
60. Walkley SU, Thrall MA, Haskins ME, Mitchell TW, Wenger DA, Brown DE, et al. Abnormal neuronal metabolism and storage in mucopolysaccharidosis type VI (Maroteaux-Lamy) disease. Neuropathol Appl Neurobiol 2005; 31:536-44; PMID:16150124; http://dx.doi.org/10.1111/j.1365-2990.2005.00675.x
61. Li Z, Yasuda Y, Li W, Bogyo M, Katz N, Gordon RE, et al. Regulation of collagenase activities of human cathepsins by glycosaminoglycans. J Biol Chem 2004; 279:5470-9; PMID:14645229; http://dx.doi.org/10.1074/jbc.M310349200
62. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 2008; 28:6926-37; PMID:18596167; http://dx.doi.org/10.1523/JNEUROSCI.0800-08.2008
63. Eckhardt M. Pathology and current treatment of neurodegenerative sphingolipidoses. Neuromolecular Med 2010; 12:362-82; PMID:20730629; http://dx.doi.org/10.1007/s12017-010-8133-7
64. Staretz-Chacham O, Lang TC, LaMarca ME, Krasnewich D, Sidransky E. Lysosomal storage disorders in the newborn. Pediatrics 2009; 123:1191-207; PMID:19336380; http://dx.doi.org/10.1542/peds.2008-0635
65. Tamboli IY, Hampel H, Tien NT, Tolksdorf K, Breiden B, Mathews PM, et al. Sphingolipid storage affects autophagic metabolism of the amyloid precursor protein and promotes Abeta generation. J Neurosci 2011; 31:1837-49; PMID:21289194; http://dx.doi.org/10.1523/JNEUROSCI.2954-10.2011
66. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997; 277:228-31; PMID: 9211849; http://dx.doi.org/10.1126/science.277. 5323.228
67. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, et al. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 2000; 290:2298-301; PMID:11125141; http://dx.doi.org/10.1126/science.290.5500. 2298
68. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, Brown MS, et al. Structure of N-terminal domain of NPC1 reveals distinct sub-domains for binding and transfer of cholesterol. Cell 2009; 137:1213-24; PMID:19563754; http://dx.doi.org/10.1016/j.cell.2009.03.049
69. Ioannou YA. Multidrug permeases and subcellular cholesterol transport. Nat Rev Mol Cell Biol 2001; 2:657-68; PMID:11533723; http://dx.doi.org/10.1038/ 35089558
70. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, Goldstein JL. NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc Natl Acad Sci U S A 2008; 105:15287-92; PMID:18772377; http://dx.doi.org/10.1073/pnas.0807328105
71. Scott C, Ioannou YA. The NPC1 protein: structure implies function. Biochim Biophys Acta 2004; 1685:8-13; PMID:15465421
72. Xu Z, Farver W, Kodukula S, Storch J. Regulation of sterol transport between membranes and NPC2. Biochemistry 2008; 47:11134-43; PMID:18823126; http://dx.doi.org/10.1021/bi801328u
73. Karten B, Peake KB, Vance JE. Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells. Biochim Biophys Acta 2009; 1791:659-70; PMID:19416638
74. Zhou S, Davidson C, McGlynn R, Stephney G, Dobrenis K, Vanier MT, et al. Endosomal/lysosomal processing of gangliosides affects neuronal cholesterol sequestration in Niemann-Pick disease type C. Am J Pathol 2011; 179:890-902; PMID:21708114; http://dx.doi.org/10.1016/j.ajpath.2011.04.017
75. Pacheco CD, Kunkel R, Lieberman AP. Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects. Hum Mol Genet 2007; 16:1495-503; PMID:17468177; http://dx.doi.org/10.1093/hmg/ddm100
76. Liao G, Yao Y, Liu J, Yu Z, Cheung S, Xie A, et al. Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1 -/- mouse brain. Am J Pathol 2007; 171:962-75; PMID: 17631520; http://dx.doi.org/10.2353/ajpath.2007.070052
77. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, et al. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat Cell Biol 2009; 11:468-76; PMID:19270693; http://dx.doi.org/10.1038/ncb1854
78. Higashi Y, Murayama S, Pentchev PG, Suzuki K. Cerebellar degeneration in the Niemann-Pick type C mouse. Acta Neuropathol 1993; 85:175-84; PMID: 8382896; http://dx.doi.org/10.1007/BF00227765
79. Vaccaro AM, Motta M, Tatti M, Scarpa S, Masuelli L, Bhat M, et al. Saposin C mutations in Gaucher disease patients resulting in lysosomal lipid accumulation, saposin C deficiency, but normal prosaposin processing and sorting. Hum Mol Genet 2010; 19:2987-97; PMID:20484222; http://dx.doi.org/10. 1093/hmg/ddq204
80. Mazzulli JR, Xu YH, Sun Y, Knight AL, McLean PJ, Caldwell GA, et al. Gaucher disease glucocerebrosidase and a-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 2011; 146:37-52; PMID: 21700325; http://dx.doi.org/10.1016/j.cell.2011.06.001
81. Altarescu G, Sun M, Moore DF, Smith JA, Wiggs EA, Solomon BI, et al. The neurogenetics of mucolipidosis type IV. Neurology 2002; 59:306-13; PMID:12182165
82. Bonavita S, Virta A, Jeffries N, Goldin E, Tedeschi G, Schiffmann R. Diffuse neuroaxonal involvement in mucolipidosis IV as assessed by proton magnetic resonance spectroscopic imaging. J Child Neurol 2003; 18:443-9; PMID:12940649; http://dx.doi.org/10.1177/08830738030180070701
83. Wakabayashi K, Gustafson AM, Sidransky E, Goldin E. Mucolipidosis type IV: an update. Mol Genet Metab 2011; 104:206-13; PMID:21763169; http://dx.doi.org/10.1016/j.ymgme.2011.06.006
84. Berman ER, Livni N, Shapira E, Merin S, Levij IS. Congenital corneal clouding with abnormal systemic storage bodies: a new variant of mucolipidosis. J Pediatr 1974; 84:519-26; PMID:4365943; http://dx.doi.org/10.1016/S0022- 3476(74)80671-2
85. Riedel KG, Zwaan J, Kenyon KR, Kolodny EH, Hanninen L, Albert DM. Ocular abnormalities in mucolipidosis IV. Am J Ophthalmol 1985; 99:125-36; PMID:3918453
86. Goldin E, Cooney A, Kaneski CR, Brady RO, Schiffmann R. Mucolipidosis IV consists of one complementation group. Proc Natl Acad Sci U S A 1999; 96:8562-6; PMID:10411915; http://dx.doi.org/10.1073/pnas.96.15.8562
87. Slaugenhaupt SA, Acierno JS, Jr., Helbling LA, Bove C, Goldin E, Bach G, et al. Mapping of the mucolipidosis type IV gene to chromosome 19p and definition of founder haplotypes. Am J Hum Genet 1999; 65:773-8; PMID:10441585; http://dx.doi.org/10.1086/302549
88. Bargal R, Avidan N, Ben-Asher E, Olender Z, Zeigler M, Frumkin A, et al. Identification of the gene causing mucolipidosis type IV. Nat Genet 2000; 26:118-23; PMID:10973263; http://dx.doi.org/10.1038/79095
89. Bassi MT, Manzoni M, Monti E, Pizzo MT, Ballabio A, Borsani G. Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am J Hum Genet 2000; 67:1110-20; PMID:11013137
90. Sun M, Goldin E, Stahl S, Falardeau JL, Kennedy JC, Acierno JS, Jr., et al. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet 2000; 9:2471-8; PMID:11030752; http://dx.doi.org/10.1093/hmg/9.17.2471
91. Dong XP, Cheng X, Mills E, Delling M, Wang F, Kurz T, et al. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature 2008; 455:992-6; PMID:18794901; http://dx.doi.org/10.1038/ nature07311
92. Puertollano R, Kiselyov K. TRPMLs: in sickness and in health. Am J Physiol Renal Physiol 2009; 296:F1245-54; PMID:19158345; http://dx.doi.org/10. 1152/ajprenal.90522.2008
93. Dong XP, Shen D, Wang X, Dawson T, Li X, Zhang Q, et al. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 2010; 1:38; PMID:20802798; http://dx.doi.org/10.1038/ncomms1037
94. Cheng X, Shen D, Samie M, Xu H. Mucolipins: Intracellular TRPML1-3 channels. FEBS Lett 2010; 584:2013-21; PMID:20074572; http://dx.doi.org/10.1016/ j.febslet.2009.12.056
95. Abe K, Puertollano R. Role of TRP channels in the regulation of the endosomal pathway. Physiology (Bethesda) 2011; 26:14-22; PMID:21357899; http://dx.doi.org/10.1152/physiol.00048.2010
96. Fares H, Greenwald I. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 2001; 28:64-8; PMID: 11326278; http://dx.doi.org/10.1038/ng0501-64
97. LaPlante JM, Sun M, Falardeau J, Dai D, Brown EM, Slaugenhaupt SA, et al. Lysosomal exocytosis is impaired in mucolipidosis type IV. Mol Genet Metab 2006; 89:339-48; PMID:16914343; http://dx.doi.org/10.1016/j.ymgme.2006.05.016
98. Thompson EG, Schaheen L, Dang H, Fares H. Lysosomal trafficking functions of mucolipin-1 in murine macrophages. BMC Cell Biol 2007; 8:54; PMID:18154673; http://dx.doi.org/10.1186/1471-2121-8-54
99. Medina DL, Fraldi A, Bouche V, Annunziata F, Mansueto G, Spampanato C, et al. Transcriptional activation of lysosomal exocytosis promotes cellular clearance. Dev Cell 2011; 21:421-30; PMID: 21889421; http://dx.doi.org/10.1016/ j.devcel.2011.07.016
100. Jennings JJ, Jr., Zhu JH, Rbaibi Y, Luo X, Chu CT, Kiselyov K. Mitochondrial aberrations in mucolipidosis Type IV. J Biol Chem 2006; 281:39041-50; PMID: 17056595; http://dx.doi.org/10.1074/jbc.M607982200
101. Curcio-Morelli C, Zhang P, Venugopal B, Charles FA, Browning MF, Cantiello HF, et al. Functional multimerization of mucolipin channel proteins. J Cell Physiol 2010; 222:328-35; PMID:19885840; http://dx.doi.org/10.1002/jcp. 21956
102. Zeevi DA, Lev S, Frumkin A, Minke B, Bach G. Heteromultimeric TRPML channel assemblies play a crucial role in the regulation of cell viability models and starvation-induced autophagy. J Cell Sci 2010; 123:3112-24; PMID:20736310; http://dx.doi.org/10.1242/jcs.067330
103. Kim HJ, Soyombo AA, Tjon-Kon-Sang S, So I, Muallem S. The Ca(2+) channel TRPML3 regulates membrane trafficking and autophagy. Traffic 2009; 10:1157-67; PMID:19522758; http://dx.doi.org/10.1111/j.1600-0854.2009.00924.x
104. Venugopal B, Browning MF, Curcio-Morelli C, Varro A, Michaud N, Nanthakumar N, et al. Neurologic, gastric, and opthalmologic pathologies in a murine model of mucolipidosis type IV. Am J Hum Genet 2007; 81:1070-83; PMID:17924347; http://dx.doi.org/10.1086/521954
105. Micsenyi MC, Dobrenis K, Stephney G, Pickel J, Vanier MT, Slaugenhaupt SA, et al. Neuropathology of the Mcoln1(-/-) knockout mouse model of mucolipidosis type IV. J Neuropathol Exp Neurol 2009; 68:125-35; PMID:19151629; http://dx.doi.org/10.1097/NEN.0b013e3181942cf0
106. Tiede S, Storch S, Lübke T, Henrissat B, Bargal R, Raas-Rothschild A, et al. Mucolipidosis II is caused by mutations in GNPTA encoding the alpha/beta GlcNAc-1-phosphotransferase. Nat Med 2005; 11:1109-12; PMID:16200072; http://dx.doi.org/10.1038/nm1305
107. Kudo M, Brem MS, Canfield WM. Mucolipidosis II (I-cell disease) and mucolipidosis IIIA (classical pseudo-hurler polydystrophy) are caused by mutations in the GlcNAc-phosphotransferase alpha / beta - subunits precursor gene. Am J Hum Genet 2006; 78:451-63; PMID:16465621; http://dx.doi.org/10.1086/ 500849
108. Hickman S, Neufeld EF. A hypothesis for I-cell disease: defective hydrolases that do not enter lysosomes. Biochem Biophys Res Commun 1972; 49:992-9; PMID:4345092; http://dx.doi.org/10.1016/0006-291X(72)90310-5
109. Vladutiu GD, Rattazzi MC. Abnormal lysosomal hydrolases excreted by cultured fibroblasts in I-cell disease (mucolipidosis II). Biochem Biophys Res Commun 1975; 67:956-64; PMID:1201084; http://dx.doi.org/10.1016/0006-291X(75) 90768-8
110. Kornfeld S, Sly WS. I-cell disease and pseudo-hurler polydystrophy: disorders of lysosomal enzyme phosphorylation and localization. In: Scriver CR, Beaudet AL, Sly WS, Valle D, eds. The Metabolic and Molecular Bases of Inherited Disease. New York: McGraw-Hill, 2001:3469-82.
111. Paik KH, Song SM, Ki CS, Yu HW, Kim JS, Min KH, et al. Identification of mutations in the GNPTA (MGC4170) gene coding for GlcNAc-phosphotransferase alpha/beta subunits in Korean patients with mucolipidosis type II or type IIIA. Hum Mutat 2005; 26:308-14; PMID:16116615; http://dx.doi.org/10.1002/humu.20205
112. Wisniewski KE, Zhong N, Philippart M. Pheno/genotypic correlations of neuronal ceroid lipofuscinoses. Neurology 2001; 57:576-81; PMID:11548735
113. The International Batten Disease Consortium. Isolation of a novel gene underlying Batten disease, CLN3. Cell 1995; 82:949-57; PMID:7553855; http://dx.doi.org/10.1016/0092-8674(95)90274-0
114. Siintola E, Partanen S, Strömme P, Haapanen A, Haltia M, Maehlen J, et al. Cathepsin D deficiency underlies congenital human neuronal ceroidlipofuscinosis. Brain 2006; 129:1438-45; PMID: 16670177; http://dx.doi.org/10.1093/brain/awl107
115. Schultz ML, Tecedor L, Chang M, Davidson BL. Clarifying lysosomal storage diseases. Trends Neurosci 2011; 34:401-10; PMID:21723623; http://dx.doi.org/10. 1016/j.tins.2011.05.006
116. 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; 441:885-9; PMID: 16625204; http://dx.doi.org/10. 1038/nature04724
117. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007; 131:1149-63; PMID: 18083104; http://dx.doi.org/10.1016/j.cell.2007.10.035
118. 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
119. Walkley SU, Suzuki K. Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim Biophys Acta 2004; 1685:48-62; PMID: 15465426
120. Ohmi K, Kudo LC, Ryazantsev S, Zhao HZ, Karsten SL, Neufeld EF. Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy. Proc Natl Acad Sci U S A 2009; 106:8332-7; PMID:19416848; http://dx.doi.org/10. 1073/pnas.0903223106
121. Auer IA, Schmidt ML, Lee VM, Curry B, Suzuki K, Shin RW, et al. Paired helical filament tau (PHFtau) in Niemann-Pick type C disease is similar to PHFtau in Alzheimer's disease. Acta Neuropathol 1995; 90:547-51; PMID:8615074; http://dx.doi.org/10.1007/BF00318566
122. Bu B, Li J, Davies P, Vincent I. Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J Neurosci 2002; 22:6515-25; PMID:12151531
123. Spillantini MG, Tolnay M, Love S, Goedert M. Microtubule-associated protein tau, heparan sulphate and alpha-synuclein in several neurodegenerative diseases with dementia. Acta Neuropathol 1999; 97:585-94; PMID:10378377; http://dx.doi.org/10.1007/s004010051034
124. Saito Y, Suzuki K, Hulette CM, Murayama S. Aberrant phosphorylation of alpha-synuclein in human Niemann-Pick type C1 disease. J Neuropathol Exp Neurol 2004; 63:323-8; PMID:15099022
125. Saito Y, Suzuki K, Nanba E, Yamamoto T, Ohno K, Murayama S. Niemann-Pick type C disease: accelerated neurofibrillary tangle formation and amyloid beta deposition associated with apolipoprotein E epsilon 4 homozygosity. Ann Neurol 2002; 52:351-5; PMID: 12205649; http://dx.doi.org/10.1002/ana.10266
126. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010; 141:1146-58; PMID:20541250; http://dx.doi.org/10.1016/j.cell.2010.05.008
127. Dehay B, Bové J, Rodríguez-Muela N, Perier C, Recasens A, Boya P, et al. Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci 2010; 30:12535-44; PMID:20844148; http://dx.doi.org/10.1523/JNEUROSCI.1920-10. 2010
128. Rubinsztein DC. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006; 443:780-6; PMID:17051204; http://dx.doi.org/10.1038/nature05291
129. Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36:585-95; PMID: 15146184; http://dx.doi.org/10.1038/ng1362
130. Ravikumar B, Duden R, Rubinsztein DC. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum Mol Genet 2002; 11:1107-17; PMID:11978769; http://dx.doi.org/10.1093/hmg/11.9.1107
131. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine- expanded huntingtin and related proteinopathies. Cell Death Differ 2009; 16:46-56; PMID:18636076; http://dx.doi.org/10.1038/cdd.2008.110
132. Davidson CD, Ali NF, Micsenyi MC, Stephney G, Renault S, Dobrenis K, et al. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 2009; 4:e6951; PMID:19750228; http://dx.doi.org/10.1371/journal.pone. 0006951