Home LiteratureArticle Details
PMID: 12803923 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Review

Neurobiology and cellular pathogenesis of glycolipid storage diseases.

Walkley SU

Abstract

Disorders of lysosomal metabolism often involve the accumulation of specific types of glycolipid, particularly gangliosides, because of either degradative failure or other currently unknown mechanisms. Although the precise role of gangliosides in cells remains enigmatic, the presence of specific abnormalities secondary to ganglioside accumulation in lysosomal diseases has suggested important biological functions. Chief among these is the growth of new dendrites on particular classes of mature neurons secondary to an increase in GM2 ganglioside. That GM2 has also been shown to be elevated in normal immature neurons coincident with dendritic sprouting provides a compelling argument that this ganglioside plays a role in dendritic initiation. This discovery has led to the search for other regulators of dendritic differentiation that may in some way be linked to the expression and/or function of GM2 ganglioside. Principal candidates that have emerged include tyrosine kinase receptors, small GTPases and calcium/calmodulin-dependent protein kinase II. Understanding the mechanism underlying ectopic dendritogenesis in lysosomal diseases can be expected to generate significant insight into the control of dendritic plasticity in normal brain. The detrimental aspects of ganglioside accumulation in storage diseases as well as the potential link between gangliosides and dendritogenesis also provide a strong rationale for developing pharmacological means to manipulate ganglioside expression in neurons.

MeSH Terms
Animals Dendrites/metabolism,pathology Endosomes/metabolism,pathology Gangliosidoses/etiology,metabolism,pathology Glycolipids/metabolism Humans Lysosomes/metabolism,pathology
Chemicals
Glycolipids
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Walkley Steven U
Sidney Weisner Laboratory of Genetic Neurological Disease, Department of Neuroscience, Rose F. Kennedy Center for Research in Mental Retardation and Human Development, Albert Einstein College of Medicine, Bronx, NY 10461, USA. [email protected]
References (103)
103 references, click to expand
  1. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis.
    Neuron. 2000 Feb;25(2):307-16 PMID: 10719887
  2. Distribution of ectopic neurite growth and other geometrical distortions of CNS neurons in feline GM2 gangliosidosis.
    Brain Res. 1990 Feb 26;510(1):63-73 PMID: 2322847
  3. Lysosomal storage diseases of animals: an essay in comparative pathology.
    Vet Pathol. 1997 Nov;34(6):527-48 PMID: 9396134
  4. CaM-kinases: modulators of synaptic plasticity.
    Curr Opin Neurobiol. 2000 Jun;10(3):375-80 PMID: 10851169
  5. Molecular control of cortical dendrite development.
    Annu Rev Neurosci. 2002;25:127-49 PMID: 12052906
  6. Elevated GM2 ganglioside is associated with dendritic proliferation in normal developing neocortex.
    Brain Res Dev Brain Res. 1996 May 31;93(1-2):162-71 PMID: 8804703
  7. Depletion of rafts in late endocytic membranes is controlled by NPC1-dependent recycling of cholesterol to the plasma membrane.
    J Cell Sci. 2001 May;114(Pt 10):1893-900 PMID: 11329376
  8. New proteins from old diseases provide novel insights in cell biology.
    Curr Opin Neurol. 2001 Dec;14(6):805-10 PMID: 11723392
  9. Mucopolysaccharidosis types IH, IS, II, and IIIA: glycosaminoglycans and lipids of isolated brain cells and other fractions from autopsied tissues.
    J Neurochem. 1980 Jun;34(6):1399-411 PMID: 6770045
  10. GABAergic innervation of alpha type II calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala.
    J Comp Neurol. 2002 May 6;446(3):199-218 PMID: 11932937
  11. Accumulation of cholesterol and GM2 ganglioside in cells cultured in the presence of progesterone: an implication for the basic defect in Niemann-Pick disease type C.
    Brain Dev. 1998 Jan;20(1):50-2 PMID: 9533562
  12. Requirement for alpha-CaMKII in experience-dependent plasticity of the barrel cortex.
    Science. 1996 Apr 19;272(5260):421-3 PMID: 8602534
  13. Stabilization of dendritic arbor structure in vivo by CaMKII.
    Science. 1998 Jan 9;279(5348):222-6 PMID: 9422694
  14. Ferric ion-ferrocyanide staining in ganglioside storage disease establishes that meganeurites are of axon hillock origin and distinct from axonal spheroids.
    Brain Res. 1986 Sep 24;382(2):379-86 PMID: 2428446
  15. Neurotrophin regulation of cortical dendritic growth requires activity.
    Neuron. 1996 Dec;17(6):1057-64 PMID: 8982155
  16. Functions of lipid rafts in biological membranes.
    Annu Rev Cell Dev Biol. 1998;14:111-36 PMID: 9891780
  17. Gangliosides inhibit platelet-derived growth factor-stimulated growth, receptor phosphorylation, and dimerization in neuroblastoma SH-SY5Y cells.
    J Neurochem. 1995 Nov;65(5):2251-8 PMID: 7595514
  18. Cell adhesion/recognition and signal transduction through glycosphingolipid microdomain.
    Glycoconj J. 2000 Mar-Apr;17(3 -4):143-51 PMID: 11201785
  19. Formation of functional cell membrane domains: the interplay of lipid- and protein-mediated interactions.
    Philos Trans R Soc Lond B Biol Sci. 2003 May 29;358(1433):863-8 PMID: 12803918
  20. Neurotrophins regulate dendritic growth in developing visual cortex.
    Neuron. 1995 Oct;15(4):791-803 PMID: 7576629
  21. Developmental expression of the CaM kinase II isoforms: ubiquitous gamma- and delta-CaM kinase II are the early isoforms and most abundant in the developing nervous system.
    Brain Res Mol Brain Res. 1999 Jun 18;70(1):147-54 PMID: 10381553
  22. Neurons in Niemann-Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations.
    J Neuropathol Exp Neurol. 2001 Jan;60(1):49-64 PMID: 11202175
  23. In vivo blockade of neural activity alters dendritic development of neonatal CA1 pyramidal cells.
    Eur J Neurosci. 2002 Nov;16(10):1931-8 PMID: 12453057
  24. Nuclear Notch1 signaling and the regulation of dendritic development.
    Nat Neurosci. 2000 Jan;3(1):30-40 PMID: 10607392
  25. Growth of ectopic dendrites on cortical pyramidal neurons in neuronal storage diseases correlates with abnormal accumulation of GM2 ganglioside.
    J Neurochem. 1994 May;62(5):1852-62 PMID: 8158134
  26. Ferret pyramidal cell dendritogenesis: changes in morphology and ganglioside expression during cortical development.
    J Comp Neurol. 1999 Oct 25;413(3):429-48 PMID: 10502250
  27. Ectopic axon hillock-associated neurite growth is maintained in metabolically reversed swainsonine-induced neuronal storage disease.
    Brain Res. 1987 Apr 28;410(1):89-96 PMID: 3107757
  28. Regulation of Ca2+/calmodulin-dependent protein kinase II by brain gangliosides.
    J Neurochem. 1990 Jan;54(1):103-9 PMID: 2152790
  29. Alterations in neuron morphology in feline mannosidosis. A Golgi study.
    Acta Neuropathol. 1981;53(1):75-9 PMID: 7211201
  30. GABAergic neuroaxonal dystrophy and other cytopathological alterations in feline Niemann-Pick disease type C.
    Acta Neuropathol. 1997 Aug;94(2):164-72 PMID: 9255392
  31. Gangliosides: structure, isolation, and analysis.
    Methods Enzymol. 1982;83:139-91 PMID: 7047999
  32. Critical role for glycosphingolipids in Niemann-Pick disease type C.
    Curr Biol. 2001 Aug 21;11(16):1283-7 PMID: 11525744
  33. Signaling through sphingolipid microdomains of the plasma membrane: the concept of signaling platform.
    Glycoconj J. 2000 Mar-Apr;17(3 -4):191-7 PMID: 11201790
  34. Inhibition of leucocytic lysosomal enzymes by glycosaminoglycans in vitro.
    Biochem J. 1975 Oct;152(1):57-64 PMID: 2162
  35. Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth.
    Nat Neurosci. 2000 Apr;3(4):342-9 PMID: 10725923
  36. Lipid membrane domains in cell surface and vacuolar systems.
    Glycoconj J. 2000 Mar-Apr;17(3 -4):163-71 PMID: 11201787
  37. Actin-based plasticity in dendritic spines.
    Science. 2000 Oct 27;290(5492):754-8 PMID: 11052932
  38. BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus.
    Neuroscience. 2002;114(3):795-805 PMID: 12220579
  39. Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo.
    Nat Neurosci. 2000 Mar;3(3):217-25 PMID: 10700252
  40. Synaptic activity and the construction of cortical circuits.
    Science. 1996 Nov 15;274(5290):1133-8 PMID: 8895456
  41. Interaction between two adapter proteins, PAG and EBP50: a possible link between membrane rafts and actin cytoskeleton.
    FEBS Lett. 2001 Oct 26;507(2):133-6 PMID: 11684085
  42. Dynamic regulation of cpg15 during activity-dependent synaptic development in the mammalian visual system.
    J Neurosci. 1999 Sep 15;19(18):7999-8008 PMID: 10479700
  43. Development regulation of ganglioside metabolism.
    Prog Brain Res. 1994;101:31-44 PMID: 8029460
  44. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis.
    Science. 1997 Jul 11;277(5323):228-31 PMID: 9211849
  45. Precursor-product relationship between GM1 and GD1a biosynthesized from exogenous GM2 ganglioside in rat liver.
    J Biochem. 1990 Apr;107(4):619-23 PMID: 2358435
  46. Alterations in neuron morphology in mucopolysaccharidosis type I. A Golgi study.
    Acta Neuropathol. 1988;75(6):611-20 PMID: 2454013
  47. The NP-C gene: a key to pathways of intracellular cholesterol transport.
    Trends Cell Biol. 1994 Oct;4(10):365-9 PMID: 14731625
  48. Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42.
    Neuron. 1997 Sep;19(3):625-34 PMID: 9331353
  49. Functional roles of glycosphingolipids in signal transduction via lipid rafts.
    Glycoconj J. 2000 Mar-Apr;17(3 -4):153-62 PMID: 11201786
  50. Improved inhibitors of glucosylceramide synthase.
    J Biochem. 1992 Feb;111(2):191-6 PMID: 1533217
  51. Ultrastructure of neurites and meganeurites of cortical pyramidal neurons in feline gangliosidosis as revealed by the combined Golgi-EM technique.
    Brain Res. 1981 May 4;211(2):393-8 PMID: 6165433
  52. Inherited lysosomal storage disease associated with deficiencies of beta-galactosidase and alpha-neuraminidase in sheep.
    Am J Med Genet. 1988 Sep;31(1):39-56 PMID: 3146925
  53. Interaction of ganglioside with specific peptide sequences as a mechanism for the modulation of calmodulin-dependent enzymes.
    J Biochem. 1996 Jul;120(1):66-73 PMID: 8864846
  54. Abnormal fear response and aggressive behavior in mutant mice deficient for alpha-calcium-calmodulin kinase II.
    Science. 1994 Oct 14;266(5183):291-4 PMID: 7939668
  55. Biosynthesis and degradation of mammalian glycosphingolipids.
    Philos Trans R Soc Lond B Biol Sci. 2003 May 29;358(1433):847-61 PMID: 12803917
  56. GM2 gangliosidosis in a Japanese spaniel.
    Acta Neuropathol. 1985;67(3-4):247-53 PMID: 2931941
  57. Cellular pathology of lysosomal storage disorders.
    Brain Pathol. 1998 Jan;8(1):175-93 PMID: 9458175
  58. Limbic epilepsy in transgenic mice carrying a Ca2+/calmodulin-dependent kinase II alpha-subunit mutation.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):6852-5 PMID: 7624331
  59. Ganglioside GM1 binds to the Trk protein and regulates receptor function.
    Proc Natl Acad Sci U S A. 1995 May 23;92(11):5087-91 PMID: 7539142
  60. AB variant of infantile GM2 gangliosidosis: deficiency of a factor necessary for stimulation of hexosaminidase A-catalyzed degradation of ganglioside GM2 and glycolipid GA2.
    Proc Natl Acad Sci U S A. 1978 Aug;75(8):3979-83 PMID: 99746
  61. Influence of endogenous GM1 ganglioside on TrkB activity, in cultured neurons.
    FEBS Lett. 1998 Nov 13;439(1-2):93-6 PMID: 9849885
  62. Substrate reduction therapy in mouse models of the glycosphingolipidoses.
    Philos Trans R Soc Lond B Biol Sci. 2003 May 29;358(1433):947-54 PMID: 12803928
  63. Promotion of dendritic growth by CPG15, an activity-induced signaling molecule.
    Science. 1998 Sep 18;281(5384):1863-6 PMID: 9743502
  64. Segregation of gangliosides GM1 and GD3 on cell membranes, isolated membrane rafts, and defined supported lipid monolayers.
    Biol Chem. 2001 Feb;382(2):241-50 PMID: 11308022
  65. Rearing complexity affects branching of dendrites in the visual cortex of the rat.
    Science. 1972 Jun 30;176(4042):1445-7 PMID: 5033647
  66. GM2 ganglioside regulates the function of ciliary neurotrophic factor receptor in murine immortalized motor neuron-like cells (NSC-34).
    Neurochem Res. 2001 Apr;26(4):375-82 PMID: 11495348
  67. Small-molecule therapeutics for the treatment of glycolipid lysosomal storage disorders.
    Philos Trans R Soc Lond B Biol Sci. 2003 May 29;358(1433):927-45 PMID: 12803927
  68. Semaphorin 3A is a chemoattractant for cortical apical dendrites.
    Nature. 2000 Apr 6;404(6778):567-73 PMID: 10766232
  69. The molecular basis of CaMKII function in synaptic and behavioural memory.
    Nat Rev Neurosci. 2002 Mar;3(3):175-90 PMID: 11994750
  70. Decreased ganglioside neuraminidase activity in fibroblasts from mucopolysaccharidosis patients. Inhibition of the activity in vitro by sulfated glycosaminoglycans and other compounds.
    Biochim Biophys Acta. 1983 Dec 13;761(2):163-70 PMID: 6418214
  71. Inhibition of substrate synthesis as a strategy for glycolipid lysosomal storage disease therapy.
    J Inherit Metab Dis. 2001 Apr;24(2):275-90 PMID: 11405346
  72. Glycosphingolipid functions: insights from engineered mouse models.
    Philos Trans R Soc Lond B Biol Sci. 2003 May 29;358(1433):879-83 PMID: 12803921
  73. Gangliosides as modulators of dendritogenesis in normal and storage disease-affected pyramidal neurons.
    Cereb Cortex. 2000 Oct;10(10):1028-37 PMID: 11007553
  74. Alleviation of neuronal ganglioside storage does not improve the clinical course of the Niemann-Pick C disease mouse.
    Hum Mol Genet. 2000 Apr 12;9(7):1087-92 PMID: 10767333
  75. Cell- and lamina-specific expression and activity-dependent regulation of type II calcium/calmodulin-dependent protein kinase isoforms in monkey visual cortex.
    J Neurosci. 1998 Mar 15;18(6):2129-46 PMID: 9482799
  76. Ectopic dendritic growth in mature pyramidal neurones in human ganglioside storage disease.
    Nature. 1978 Nov 30;276(5687):520-1 PMID: 102998
  77. The pattern of mammalian brain gangliosides. 3. Regional and developmental differences.
    J Neurochem. 1965 Dec;12(12):969-79 PMID: 5892497
  78. Pathogenesis of brain dysfunction in Batten disease.
    Am J Med Genet. 1995 Jun 5;57(2):196-203 PMID: 7668330
  79. New therapeutic prospects for the glycosphingolipid lysosomal storage diseases.
    Biochem Pharmacol. 1998 Aug 15;56(4):421-30 PMID: 9763217
  80. The p75 receptor transduces the signal from myelin-associated glycoprotein to Rho.
    J Cell Biol. 2002 May 13;157(4):565-70 PMID: 12011108
  81. Ectopic dendritogenesis and associated synapse formation in swainsonine-induced neuronal storage disease.
    J Neurosci. 1988 Feb;8(2):445-57 PMID: 3123615
  82. Deficient plasticity in the primary visual cortex of alpha-calcium/calmodulin-dependent protein kinase II mutant mice.
    Neuron. 1996 Sep;17(3):491-9 PMID: 8816712
  83. Inhibition of sphingolipid synthesis: effects on glycosphingolipid-GPI-anchored protein microdomains.
    Trends Cell Biol. 1995 Oct;5(10):377-80 PMID: 14732053
  84. Regulation of glycosyltransferases in ganglioside biosynthesis by phosphorylation and dephosphorylation.
    Mol Cell Endocrinol. 2001 May 25;177(1-2):19-24 PMID: 11377816
  85. Pyramidal neurons with ectopic dendrites in storage diseases exhibit increased GM2 ganglioside immunoreactivity.
    Neuroscience. 1995 Oct;68(4):1027-35 PMID: 8544979
  86. Regulation of signal transduction by endocytosis.
    Curr Opin Cell Biol. 2000 Apr;12(2):204-10 PMID: 10712919
  87. Modulation of epidermal growth factor receptor phosphorylation by endogenously expressed gangliosides.
    Biochem J. 2001 Apr 15;355(Pt 2):465-72 PMID: 11284735
  88. Distortion of neuronal geometry and formation of aberrant synapses in neuronal storage disease.
    Brain Res. 1976 Oct 29;116(1):1-21 PMID: 824017
  89. Dendritic growth induced by BMP-7 requires Smad1 and proteasome activity.
    J Neurobiol. 2001 Aug;48(2):120-30 PMID: 11438941
  90. Cellular and molecular mechanisms of dendrite growth.
    Cereb Cortex. 2000 Oct;10(10):963-73 PMID: 11007547
  91. Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex.
    Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7332-6 PMID: 8692993
  92. Transmembrane molecular pump activity of Niemann-Pick C1 protein.
    Science. 2000 Dec 22;290(5500):2295-8 PMID: 11125140
  93. Membrane traffic in sphingolipid storage diseases.
    Traffic. 2000 Nov;1(11):807-15 PMID: 11208071
  94. Gangliosides are functional nerve cell ligands for myelin-associated glycoprotein (MAG), an inhibitor of nerve regeneration.
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8412-7 PMID: 12060784
  95. Intracellular trafficking of glycosphingolipids: role of sphingolipid activator proteins in the topology of endocytosis and lysosomal digestion.
    FEBS Lett. 1994 Jun 6;346(1):103-7 PMID: 8206147
  96. Gangliosides GM1, GM2 and GM3 inhibit the platelet-derived growth factor-induced signalling transduction pathway in vascular smooth muscle cells by different mechanisms.
    Eur J Cell Biol. 1996 Sep;71(1):79-88 PMID: 8884181
  97. The N-acetylgalactosamine residue of exogenous GM2 ganglioside is recycled for glycoconjugate biosynthesis in rat liver.
    Biochem J. 1990 Feb 15;266(1):103-6 PMID: 2310367
  98. Jamming the endosomal system: lipid rafts and lysosomal storage diseases.
    Trends Cell Biol. 2000 Nov;10(11):459-62 PMID: 11050411
  99. Sphingomyelin lipidosis in a cat: Golgi studies.
    Acta Neuropathol. 1984;65(2):138-44 PMID: 6441439
  100. The role of alpha-CaMKII autophosphorylation in neocortical experience-dependent plasticity.
    Nat Neurosci. 2000 Sep;3(9):911-8 PMID: 10966622
  101. Dendritic growth in the aged human brain and failure of growth in senile dementia.
    Science. 1979 Nov 16;206(4420):854-6 PMID: 493989
  102. Ganglioside modulation of the PDGF receptor. A model for ganglioside functions.
    J Neurooncol. 1995;24(1):65-73 PMID: 8523078
  103. Mucopolysaccharidosis: secondarily induced abnormal distribution of lysosomal isoenzymes.
    Science. 1973 Jul 27;181(4097):352-4 PMID: 4268963
Article Info
Journal
Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Abbr.
Philos Trans R Soc Lond B Biol Sci
ISSN
0962-8436
Published
2003-05-29
Pages
893-904
Language
English
Region
England
NLM ID
7503623
PMCID
PMC1693176
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]