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PMID: 22647656 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't Review

Autophagy in lysosomal storage disorders.

Autophagy ·Vol. 8 ·No. 5 ·2012-05-01 ·Pages 719-30

Lieberman AP, Puertollano R, Raben N, Slaugenhaupt S, Walkley SU, Ballabio A

Abstract

Lysosomes are ubiquitous intracellular organelles that have an acidic internal pH, and play crucial roles in cellular clearance. Numerous functions depend on normal lysosomes, including the turnover of cellular constituents, cholesterol homeostasis, downregulation of surface receptors, inactivation of pathogenic organisms, repair of the plasma membrane and bone remodeling. Lysosomal storage disorders (LSDs) are characterized by progressive accumulation of undigested macromolecules within the cell due to lysosomal dysfunction. As a consequence, many tissues and organ systems are affected, including brain, viscera, bone and cartilage. The progressive nature of phenotype development is one of the hallmarks of LSDs. In recent years biochemical and cell biology studies of LSDs have revealed an ample spectrum of abnormalities in a variety of cellular functions. These include defects in signaling pathways, calcium homeostasis, lipid biosynthesis and degradation and intracellular trafficking. Lysosomes also play a fundamental role in the autophagic pathway by fusing with autophagosomes and digesting their content. Considering the highly integrated function of lysosomes and autophagosomes it was reasonable to expect that lysosomal storage in LSDs would have an impact upon autophagy. The goal of this review is to provide readers with an overview of recent findings that have been obtained through analysis of the autophagic pathway in several types of LSDs, supporting the idea that LSDs could be seen primarily as "autophagy disorders."

MeSH Terms
Animals Autophagy Humans Lysosomal Storage Diseases/etiology,pathology Models, Biological Muscles/pathology,ultrastructure
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lieberman Andrew P
Department of Pathology, University of Michigan Medical School, Ann Arbor, MI USA.
Puertollano Rosa
Raben Nina
Slaugenhaupt Susan
Walkley Steven U
Ballabio Andrea
References (126)
126 references, click to expand
  1. Endosomal/lysosomal processing of gangliosides affects neuronal cholesterol sequestration in Niemann-Pick disease type C.
    Am J Pathol. 2011 Aug;179(2):890-902 PMID: 21708114
  2. Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease.
    PLoS Genet. 2005 Jul;1(1):81-95 PMID: 16103921
  3. The neurogenetics of mucolipidosis type IV.
    Neurology. 2002 Aug 13;59(3):306-13 PMID: 12182165
  4. Functional multimerization of mucolipin channel proteins.
    J Cell Physiol. 2010 Feb;222(2):328-35 PMID: 19885840
  5. Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects.
    Hum Mol Genet. 2007 Jun 15;16(12):1495-503 PMID: 17468177
  6. Mucolipidosis IV consists of one complementation group.
    Proc Natl Acad Sci U S A. 1999 Jul 20;96(15):8562-6 PMID: 10411915
  7. 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 Jan;11(1):48-56 PMID: 15585405
  8. Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells.
    Biochim Biophys Acta. 2009 Jul;1791(7):659-70 PMID: 19416638
  9. Lysosomal trafficking functions of mucolipin-1 in murine macrophages.
    BMC Cell Biol. 2007 Dec 21;8:54 PMID: 18154673
  10. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog.
    Nat Genet. 2001 May;28(1):64-8 PMID: 11326278
  11. Sanfilippo syndrome type B, a lysosomal storage disease, is also a tauopathy.
    Proc Natl Acad Sci U S A. 2009 May 19;106(20):8332-7 PMID: 19416848
  12. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel.
    Hum Mol Genet. 2000 Oct 12;9(17):2471-8 PMID: 11030752
  13. Neurologic, gastric, and opthalmologic pathologies in a murine model of mucolipidosis type IV.
    Am J Hum Genet. 2007 Nov;81(5):1070-83 PMID: 17924347
  14. Lysosomal exocytosis is impaired in mucolipidosis type IV.
    Mol Genet Metab. 2006 Dec;89(4):339-48 PMID: 16914343
  15. Heteromultimeric TRPML channel assemblies play a crucial role in the regulation of cell viability models and starvation-induced autophagy.
    J Cell Sci. 2010 Sep 15;123(Pt 18):3112-24 PMID: 20736310
  16. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease.
    J Neurosci. 2008 Jul 2;28(27):6926-37 PMID: 18596167
  17. Pathogenic lysosomal depletion in Parkinson's disease.
    J Neurosci. 2010 Sep 15;30(37):12535-44 PMID: 20844148
  18. Differences in the predominance of lysosomal and autophagic pathologies between infants and adults with Pompe disease: implications for therapy.
    Mol Genet Metab. 2010 Dec;101(4):324-31 PMID: 20801068
  19. Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis.
    J Biol Chem. 2006 Jul 21;281(29):20483-93 PMID: 16714284
  20. Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders.
    EMBO J. 2010 Nov 3;29(21):3607-20 PMID: 20871593
  21. Lysosomal storage diseases as disorders of autophagy.
    Autophagy. 2008 Jan;4(1):113-4 PMID: 18000397
  22. Gaucher disease glucocerebrosidase and α-synuclein form a bidirectional pathogenic loop in synucleinopathies.
    Cell. 2011 Jul 8;146(1):37-52 PMID: 21700325
  23. The role of autophagy during the early neonatal starvation period.
    Nature. 2004 Dec 23;432(7020):1032-6 PMID: 15525940
  24. 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 Mar 15;19(6):1088-97 PMID: 20047948
  25. 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 Aug 1;19(15):2987-97 PMID: 20484222
  26. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol.
    Cell. 2009 Jun 26;137(7):1213-24 PMID: 19563754
  27. The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases.
    Cell. 2003 May 16;113(4):445-56 PMID: 12757706
  28. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.
    Cell. 2007 Dec 14;131(6):1149-63 PMID: 18083104
  29. Neuropathology of the Mcoln1(-/-) knockout mouse model of mucolipidosis type IV.
    J Neuropathol Exp Neurol. 2009 Feb;68(2):125-35 PMID: 19151629
  30. The NPC1 protein: structure implies function.
    Biochim Biophys Acta. 2004 Oct 11;1685(1-3):8-13 PMID: 15465421
  31. alpha-Glucosidase deficiency in generalized glycogenstorage disease (Pompe's disease).
    Biochem J. 1963 Jan;86:11-6 PMID: 13954110
  32. The roles of intracellular protein-degradation pathways in neurodegeneration.
    Nature. 2006 Oct 19;443(7113):780-6 PMID: 17051204
  33. Mucolipins: Intracellular TRPML1-3 channels.
    FEBS Lett. 2010 May 17;584(10):2013-21 PMID: 20074572
  34. Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1 -/- mouse brain.
    Am J Pathol. 2007 Sep;171(3):962-75 PMID: 17631520
  35. Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme.
    Cell. 2003 May 16;113(4):435-44 PMID: 12757705
  36. Identification of the gene causing mucolipidosis type IV.
    Nat Genet. 2000 Sep;26(1):118-23 PMID: 10973263
  37. Consequences of NPC1 and NPC2 loss of function in mammalian neurons.
    Biochim Biophys Acta. 2004 Oct 11;1685(1-3):48-62 PMID: 15465426
  38. Pathogenic cascades in lysosomal disease-Why so complex?
    J Inherit Metab Dis. 2009 Apr;32(2):181-9 PMID: 19130290
  39. Aberrant membranes and double-membrane structures accumulate in the axons of Atg5-null Purkinje cells before neuronal death.
    Autophagy. 2007 Nov-Dec;3(6):591-6 PMID: 17912025
  40. Pathology and current treatment of neurodegenerative sphingolipidoses.
    Neuromolecular Med. 2010 Dec;12(4):362-82 PMID: 20730629
  41. Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model.
    J Neurosci. 2002 Aug 1;22(15):6515-25 PMID: 12151531
  42. Transcriptional activation of lysosomal exocytosis promotes cellular clearance.
    Dev Cell. 2011 Sep 13;21(3):421-30 PMID: 21889421
  43. 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 Mar;78(3):451-63 PMID: 16465621
  44. Niemann-Pick type C disease: accelerated neurofibrillary tangle formation and amyloid beta deposition associated with apolipoprotein E epsilon 4 homozygosity.
    Ann Neurol. 2002 Sep;52(3):351-5 PMID: 12205649
  45. Mapping of the mucolipidosis type IV gene to chromosome 19p and definition of founder haplotypes.
    Am J Hum Genet. 1999 Sep;65(3):773-8 PMID: 10441585
  46. Clarifying lysosomal storage diseases.
    Trends Neurosci. 2011 Aug;34(8):401-10 PMID: 21723623
  47. Impaired organization and function of myofilaments in single muscle fibers from a mouse model of Pompe disease.
    J Appl Physiol (1985). 2010 May;108(5):1383-8 PMID: 20223998
  48. Glycogen autophagy in the liver and heart of newborn rats. The effects of glucagon, adrenalin or rapamycin.
    Histol Histopathol. 2005 Jul;20(3):689-96 PMID: 15944916
  49. Lysosomal enhancement: a CLEAR answer to cellular degradative needs.
    Cell Cycle. 2009 Dec 15;8(24):4021-2 PMID: 19949301
  50. Lysosomal storage disorders in the newborn.
    Pediatrics. 2009 Apr;123(4):1191-207 PMID: 19336380
  51. 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 Feb 15;160C(1):13-21 PMID: 22253254
  52. A hypothesis for I-cell disease: defective hydrolases that do not enter lysosomes.
    Biochem Biophys Res Commun. 1972 Nov 15;49(4):992-9 PMID: 4345092
  53. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice.
    Nature. 2006 Jun 15;441(7095):885-9 PMID: 16625204
  54. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease).
    Nature. 2000 Aug 24;406(6798):906-10 PMID: 10972294
  55. Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease).
    Am J Pathol. 2005 Dec;167(6):1713-28 PMID: 16314482
  56. Macroautophagy is defective in mucolipin-1-deficient mouse neurons.
    Neurobiol Dis. 2010 Nov;40(2):370-7 PMID: 20600908
  57. Methods in mammalian autophagy research.
    Cell. 2010 Feb 5;140(3):313-26 PMID: 20144757
  58. Proteoglycan desulfation determines the efficiency of chondrocyte autophagy and the extent of FGF signaling during endochondral ossification.
    Genes Dev. 2008 Oct 1;22(19):2645-50 PMID: 18832069
  59. Pathology of the first autopsy case diagnosed as mucolipidosis type III α/β suggesting autophagic dysfunction.
    Mol Genet Metab. 2011 Feb;102(2):170-5 PMID: 21051253
  60. Microtubule-associated protein tau, heparan sulphate and alpha-synuclein in several neurodegenerative diseases with dementia.
    Acta Neuropathol. 1999 Jun;97(6):585-94 PMID: 10378377
  61. Pheno/genotypic correlations of neuronal ceroid lipofuscinoses.
    Neurology. 2001 Aug 28;57(4):576-81 PMID: 11548735
  62. Autophagic degradation of glycogen in skeletal muscles of the newborn rat.
    J Cell Biol. 1972 Jan;52(1):41-51 PMID: 4331300
  63. Suppression of autophagy permits successful enzyme replacement therapy in a lysosomal storage disorder--murine Pompe disease.
    Autophagy. 2010 Nov;6(8):1078-89 PMID: 20861693
  64. 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 Dec 15;17(24):3897-908 PMID: 18782848
  65. Termination of autophagy and reformation of lysosomes regulated by mTOR.
    Nature. 2010 Jun 17;465(7300):942-6 PMID: 20526321
  66. Isolation of a novel gene underlying Batten disease, CLN3. The International Batten Disease Consortium.
    Cell. 1995 Sep 22;82(6):949-57 PMID: 7553855
  67. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease.
    Nat Genet. 2004 Jun;36(6):585-95 PMID: 15146184
  68. Abnormal autophagy, ubiquitination, inflammation and apoptosis are dependent upon lysosomal storage and are useful biomarkers of mucopolysaccharidosis VI.
    Pathogenetics. 2009 Jun 16;2(1):4 PMID: 19531206
  69. Systemic inflammation and neurodegeneration in a mouse model of multiple sulfatase deficiency.
    Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4506-11 PMID: 17360554
  70. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy.
    J Biol Chem. 2007 Aug 17;282(33):24131-45 PMID: 17580304
  71. Autophagic dysfunction in mucolipidosis type IV patients.
    Hum Mol Genet. 2008 Sep 1;17(17):2723-37 PMID: 18550655
  72. Sphingolipid storage affects autophagic metabolism of the amyloid precursor protein and promotes Abeta generation.
    J Neurosci. 2011 Feb 2;31(5):1837-49 PMID: 21289194
  73. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression.
    PLoS One. 2009 Sep 11;4(9):e6951 PMID: 19750228
  74. Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes.
    Curr Opin Cell Biol. 2007 Aug;19(4):459-65 PMID: 17689064
  75. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death.
    J Cell Biol. 2005 Nov 21;171(4):603-14 PMID: 16286508
  76. Chaperone-mediated autophagy is defective in mucolipidosis type IV.
    J Cell Physiol. 2009 May;219(2):344-53 PMID: 19117012
  77. The Ca(2+) channel TRPML3 regulates membrane trafficking and autophagy.
    Traffic. 2009 Aug;10(8):1157-67 PMID: 19522758
  78. Starch binding domain-containing protein 1/genethonin 1 is a novel participant in glycogen metabolism.
    J Biol Chem. 2010 Nov 5;285(45):34960-71 PMID: 20810658
  79. Mucolipidosis type IV: an update.
    Mol Genet Metab. 2011 Nov;104(3):206-13 PMID: 21763169
  80. Autophagy and lysosomes in Pompe disease.
    Autophagy. 2006 Oct-Dec;2(4):318-20 PMID: 16874053
  81. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy.
    Hum Mol Genet. 2002 May 1;11(9):1107-17 PMID: 11978769
  82. Cathepsin D deficiency underlies congenital human neuronal ceroid-lipofuscinosis.
    Brain. 2006 Jun;129(Pt 6):1438-45 PMID: 16670177
  83. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine-expanded huntingtin and related proteinopathies.
    Cell Death Differ. 2009 Jan;16(1):46-56 PMID: 18636076
  84. Autophagy and mistargeting of therapeutic enzyme in skeletal muscle in Pompe disease.
    Mol Ther. 2006 Dec;14(6):831-9 PMID: 17008131
  85. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel.
    Nature. 2008 Oct 16;455(7215):992-6 PMID: 18794901
  86. Paired helical filament tau (PHFtau) in Niemann-Pick type C disease is similar to PHFtau in Alzheimer's disease.
    Acta Neuropathol. 1995;90(6):547-51 PMID: 8615074
  87. Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex.
    Nat Cell Biol. 2009 Apr;11(4):468-76 PMID: 19270693
  88. Enhanced autophagy and mitochondrial aberrations in murine G(M1)-gangliosidosis.
    Biochem Biophys Res Commun. 2008 Mar 14;367(3):616-22 PMID: 18190792
  89. Role of TRP channels in the regulation of the endosomal pathway.
    Physiology (Bethesda). 2011 Feb;26(1):14-22 PMID: 21357899
  90. Abnormal lysosomal hydrolases excreted by cultured fibroblasts in I-cell disease (mucolipidosis II).
    Biochem Biophys Res Commun. 1975 Dec 1;67(3):956-64 PMID: 1201084
  91. Identification of HE1 as the second gene of Niemann-Pick C disease.
    Science. 2000 Dec 22;290(5500):2298-301 PMID: 11125141
  92. TRPMLs: in sickness and in health.
    Am J Physiol Renal Physiol. 2009 Jun;296(6):F1245-54 PMID: 19158345
  93. Structural basis for sorting mechanism of p62 in selective autophagy.
    J Biol Chem. 2008 Aug 15;283(33):22847-57 PMID: 18524774
  94. Mucolipidosis II is caused by mutations in GNPTA encoding the alpha/beta GlcNAc-1-phosphotransferase.
    Nat Med. 2005 Oct;11(10):1109-12 PMID: 16200072
  95. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice.
    Nature. 2000 Aug 24;406(6798):902-6 PMID: 10972293
  96. TFEB links autophagy to lysosomal biogenesis.
    Science. 2011 Jun 17;332(6036):1429-33 PMID: 21617040
  97. Tau deletion exacerbates the phenotype of Niemann-Pick type C mice and implicates autophagy in pathogenesis.
    Hum Mol Genet. 2009 Mar 1;18(5):956-65 PMID: 19074461
  98. Regulation of collagenase activities of human cathepsins by glycosaminoglycans.
    J Biol Chem. 2004 Feb 13;279(7):5470-9 PMID: 14645229
  99. Autophagosome maturation is impaired in Fabry disease.
    Autophagy. 2010 Jul;6(5):589-99 PMID: 20431343
  100. Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles.
    Autophagy. 2010 Feb;6(2):307-9 PMID: 20104028
  101. Mitochondrial dysfunction and oxidative stress mediate the physiological impairment induced by the disruption of autophagy.
    Aging (Albany NY). 2009 Apr 09;1(4):425-37 PMID: 20157526
  102. Lysosomes: fusion and function.
    Nat Rev Mol Cell Biol. 2007 Aug;8(8):622-32 PMID: 17637737
  103. Deconstructing Pompe disease by analyzing single muscle fibers: to see a world in a grain of sand...
    Autophagy. 2007 Nov-Dec;3(6):546-52 PMID: 17592248
  104. Pompe's disease.
    Lancet. 2008 Oct 11;372(9646):1342-53 PMID: 18929906
  105. Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes.
    J Biol Chem. 1998 Aug 21;273(34):21883-92 PMID: 9705327
  106. Infantile acid maltase deficiency. I. Muscle fiber destruction after lysosomal rupture.
    Virchows Arch B Cell Pathol Incl Mol Pathol. 1984;45(1):23-36 PMID: 6199885
  107. Multidrug permeases and subcellular cholesterol transport.
    Nat Rev Mol Cell Biol. 2001 Sep;2(9):657-68 PMID: 11533723
  108. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome.
    Nat Commun. 2010 Jul 13;1:38 PMID: 20802798
  109. Lysosomal disorders: from storage to cellular damage.
    Biochim Biophys Acta. 2009 Apr;1793(4):684-96 PMID: 19111581
  110. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations.
    Cell. 2010 Jun 25;141(7):1146-58 PMID: 20541250
  111. The mucopolysaccharidoses. Diagnosis, molecular genetics and treatment.
    Mol Biol Med. 1990 Oct;7(5):381-404 PMID: 2128891
  112. Inhibition of autophagosome formation restores mitochondrial function in mucolipidosis II and III skin fibroblasts.
    Mol Genet Metab. 2009 Dec;98(4):393-9 PMID: 19656701
  113. Regulation of sterol transport between membranes and NPC2.
    Biochemistry. 2008 Oct 21;47(42):11134-43 PMID: 18823126
  114. 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 Oct 7;105(40):15287-92 PMID: 18772377
  115. Cerebellar degeneration in the Niemann-Pick type C mouse.
    Acta Neuropathol. 1993;85(2):175-84 PMID: 8382896
  116. 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 Nov;67(5):1110-20 PMID: 11013137
  117. Characterization of pre- and post-treatment pathology after enzyme replacement therapy for Pompe disease.
    Lab Invest. 2006 Dec;86(12):1208-20 PMID: 17075580
  118. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis.
    Science. 1997 Jul 11;277(5323):228-31 PMID: 9211849
  119. 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 Oct;26(4):308-14 PMID: 16116615
  120. Aberrant phosphorylation of alpha-synuclein in human Niemann-Pick type C1 disease.
    J Neuropathol Exp Neurol. 2004 Apr;63(4):323-8 PMID: 15099022
  121. Ocular abnormalities in mucolipidosis IV.
    Am J Ophthalmol. 1985 Feb 15;99(2):125-36 PMID: 3918453
  122. Congenital corneal clouding with abnormal systemic storage bodies: a new variant of mucolipidosis.
    J Pediatr. 1974 Apr;84(4):519-26 PMID: 4365943
  123. Diffuse neuroaxonal involvement in mucolipidosis IV as assessed by proton magnetic resonance spectroscopic imaging.
    J Child Neurol. 2003 Jul;18(7):443-9 PMID: 12940649
  124. Abnormal neuronal metabolism and storage in mucopolysaccharidosis type VI (Maroteaux-Lamy) disease.
    Neuropathol Appl Neurobiol. 2005 Oct;31(5):536-44 PMID: 16150124
  125. Mitochondrial aberrations in mucolipidosis Type IV.
    J Biol Chem. 2006 Dec 22;281(51):39041-50 PMID: 17056595
  126. A block of autophagy in lysosomal storage disorders.
    Hum Mol Genet. 2008 Jan 1;17(1):119-29 PMID: 17913701
Article Info
Journal
Autophagy
Abbr.
Autophagy
ISSN
1554-8635
DOI
10.4161/auto.19469
Published
2012-05-01
Epub
2012-00-01
Pages
719-30
Language
English
Region
United States
NLM ID
101265188
PMCID
PMC3378416
Subset
IM
Grants
NICHD NIH HHS · HD045561 · United States
Telethon · TGM11CB6 · Italy
Intramural NIH HHS · United States
NINDS NIH HHS · R01 NS063967 · United States
European Research Council · 250154 · International
NICHD NIH HHS · R01 HD045561 · United States
External Links
PubMed source DOI: 10.4161/auto.19469 PMC Full Text View journal details
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