The Glycosphingolipid Hydrolases in the Central Nervous System

Molecular Neurobiology

Volumn 50, Issue 1, 2014, Pages 76-87

  Aureli, Massimo ^a   Samarani, Maura ^a   Loberto, Nicoletta ^a   Bassi, Rosaria ^a   Murdica, Valentina ^a   Prioni, Simona ^a   Prinetti, Alessandro ^a   Sonnino, Sandro ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

GBA2; Glycohydrolases; Glycosphingolipids; Neu3; Neuronal differentiation and aging

Indexed keywords

BETA GALACTOSIDASE; BETA GLUCOSYLCERAMIDASE; BETA N ACETYLHEXOSAMINIDASE; GLUCOSYLCERAMIDASE; GLYCOSPHINGOLIPID; HYDROLASE; SIALIDASE; UNCLASSIFIED DRUG;

CENTRAL NERVOUS SYSTEM; ENZYME ACTIVITY; HUMAN; LIPOGENESIS; LIPOLYSIS; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; ANIMAL; CELL MEMBRANE; METABOLISM; NERVE CELL;

ANIMALS; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; GLYCOSPHINGOLIPIDS; HYDROLASES; NEURONS;

EID: 84911005598     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8592-6     Document Type: Review

References (103)

1. Sonnino S, Mauri L, Chigorno V, Prinetti A (2007) Gangliosides as components of lipid membrane domains. Glycobiology 17:1–13
2. Sonnino S, Prinetti A, Mauri L, Chigorno V, Tettamanti G (2006) Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chem Rev 106:2111–2125
3. Del Favero E, Brocca P, Motta S, Rondelli V, Sonnino S, Cantu L (2011) Nanoscale structural response of ganglioside-containing aggregates to the interaction with sialidase. J Neurochem 116:833–839
4. Ira, Johnston LJ (2008) Sphingomyelinase generation of ceramide promotes clustering of nanoscale domains in supported bilayer membranes. Biochim Biophys Acta 1778:185–197
5. Svennerholm L, Bostrom K, Fredman P, Mansson JE, Rosengren B, Rynmark BM (1989) Human brain gangliosides: developmental changes from early fetal stage to advanced age. Biochim Biophys Acta 1005:109–117
6. Yu RK, Macala LJ, Taki T, Weinfield HM, Yu FS (1988) Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J Neurochem 50:1825–1829
7. Irwin LN, Irwin CC (1982) Development changes and regional variation in the ganglioside composition of the rat hippocampus. Brain Res 256:481–485
8. Kotani M, Terashima T, Tai T (1995) Developmental changes of ganglioside expressions in postnatal rat cerebellar cortex. Brain Res 700:40–58
9. Kracun I, Rosner H, Drnovsek V, Vukelic Z, Cosovic C, Trbojevic-Cepe M, Kubat M (1992) Gangliosides in the human brain development and aging. Neurochem Int 20:421–431
10. Dreyfus H, Louis JC, Harth S, Mandel P (1980) Gangliosides in cultured neurons. Neuroscience 5:1647–1655
11. Ngamukote S, Yanagisawa M, Ariga T, Ando S, Yu RK (2007) Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J Neurochem 103:2327–2341
12. Facci L, Leon A, Toffano G, Sonnino S, Ghidoni R, Tettamanti G (1984) Promotion of neuritogenesis in mouse neuroblastoma cells by exogenous gangliosides. Relationship between the effect and the cell association of ganglioside GM1. J Neurochem 42:299–305
13. Walkley SU, Siegel DA, Dobrenis K, Zervas M (1998) GM2 ganglioside as a regulator of pyramidal neuron dendritogenesis. Ann N Y Acad Sci 845:188–199
14. Hakomori S (1990) Bifunctional role of glycosphingolipids. Modulators for transmembrane signaling and mediators for cellular interactions. J Biol Chem 265:18713–18716
15. Schnaar RL (1991) Glycosphingolipids in cell surface recognition. Glycobiology 1:477–485
16. Yu RK, Nakatani Y, Yanagisawa M (2009) The role of glycosphingolipid metabolism in the developing brain. J Lipid Res 50(Suppl):S440–S445
17. Roseman S (1970) The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion. Chem Phys Lipids 5:270–297
18. Preti A, Fiorilli A, Lombardo A, Caimi L, Tettamanti G (1980) Occurrence of sialyltransferase activity in the synaptosomal membranes prepared from calf brain cortex. J Neurochem 35:281–296
19. Miyagi T, Wada T, Iwamatsu A, Hata K, Yoshikawa Y, Tokuyama S, Sawada M (1999) Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J Biol Chem 274:5004–5011
20. Mencarelli S, Cavalieri C, Magini A, Tancini B, Basso L, Lemansky P, Hasilik A, Li YT, Chigorno V, Orlacchio A, Emiliani C, Sonnino S (2005) Identification of plasma membrane associated mature beta-hexosaminidase A, active towards GM2 ganglioside, in human fibroblasts. FEBS Lett 579:5501–5506
21. Aureli M, Masilamani AP, Illuzzi G, Loberto N, Scandroglio F, Prinetti A, Chigorno V, Sonnino S (2009) Activity of plasma membrane beta-galactosidase and beta-glucosidase. FEBS Lett 583:2469–2473
22. Schengrund CL, Rosenberg A (1970) Intracellular location and properties of bovine brain sialidase. J Biol Chem 245:6196–6200
23. Tettamanti G, Morgan IG, Gombos G, Vincendon G, Mandel P (1972) Sub-synaptosomal localization of brain particulate neuraminidose. Brain Res 47:515–518
24. Tettamanti G, Preti A, Lombardo A, Suman T, Zambotti V (1975) Membrane-bound neuraminidase in the brain of different animals: behaviour of the enzyme on endogenous sialo derivatives and rationale for its assay. J Neurochem 25:451–456
25. Tettamanti G, Preti A, Lombardo A, Bonali F, Zambotti V (1973) Parallelism of subcellular location of major particulate neuraminidase and gangliosides in rabbit brain cortex. Biochim Biophys Acta 306:466–477
26. Triggs-Raine B, Mahuran DJ, Gravel RA (2001) Naturally occurring mutations in GM2 gangliosidosis: a compendium. Adv Genet 44:199–224
27. Bearpark TM, Stirling JL (1978) A difference in the specificities of human liver N-acetyl-beta-hexosaminidases A and B detected by their activities towards glycosaminoglycan oligosaccharides. Biochem J 173:997–1000
28. Kytzia HJ, Sandhoff K (1985) Evidence for two different active sites on human beta-hexosaminidase A. Interaction of GM2 activator protein with beta-hexosaminidase A. J Biol Chem 260:7568–7572
29. Kolter T, Sandhoff K (2006) Sphingolipid metabolism diseases. Biochim Biophys Acta 1758:2057–2079
30. Bateman KS, Cherney MM, Mahuran DJ, Tropak M, James MN (2011) Crystal structure of beta-hexosaminidase B in complex with pyrimethamine, a potential pharmacological chaperone. J Med Chem 54:1421–1429
31. Reddy A, Caler EV, Andrews NW (2001) Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106:157–169
32. Mellon PL, Windle JJ, Goldsmith PC, Padula CA, Roberts JL, Weiner RI (1990) Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5:1–10
33. Radovick S, Wray S, Lee E, Nicols DK, Nakayama Y, Weintraub BD, Westphal H, Cutler GB Jr, Wondisford FE (1991) Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proc Natl Acad Sci U S A 88:3402–3406
34. Aureli M, Bassi R, Loberto N, Regis S, Prinetti A, Chigorno V, Aerts JM, Boot RG, Filocamo M, Sonnino S (2012) Cell surface associated glycohydrolases in normal and Gaucher disease fibroblasts. J Inherit Metab Dis 35:1081–1091
35. Hatten ME (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100:384–396
36. Agholme L, Lindstrom T, Kagedal K, Marcusson J, Hallbeck M (2010) An in vitro model for neuroscience: differentiation of SH-SY5Y cells into cells with morphological and biochemical characteristics of mature neurons. J Alzheimers Dis 20:1069–1082
37. Aureli M, Gritti A, Bassi R, Loberto N, Ricca A, Chigorno V, Prinetti A, Sonnino S (2011) Plasma membrane-associated glycohydrolases along differentiation of murine neural stem cells. Neurochem Res 37:1344–1354
38. Miyagi T, Sagawa J, Konno K, Handa S, Tsuiki S (1990) Biochemical and immunological studies on two distinct ganglioside-hydrolyzing sialidases from the particulate fraction of rat brain. J Biochem (Tokyo) 107:787–793
39. Miyagi T, Sagawa J, Konno K, Tsuiki S (1990) Immunological discrimination of intralysosomal, cytosolic, and two membrane sialidases present in rat tissues. J Biochem (Tokyo) 107:794–798
40. Miyagi T, Tsuiki S (1986) Evidence for sialidase hydrolyzing gangliosides GM2 and GM1 in rat liver plasma membrane. FEBS Lett 206:223–228
41. D'Azzo A, Hoogeveen A, Reuser AJ, Robinson D, Galjaard H (1982) Molecular defect in combined beta-galactosidase and neuraminidase deficiency in man. Proc Natl Acad Sci U S A 79:4535–4539
42. Fanzani A, Colombo F, Giuliani R, Preti A, Marchesini S (2004) Cytosolic sialidase Neu2 upregulation during PC12 cells differentiation. FEBS Lett 566:178–182
43. Kopitz J, von Reitzenstein C, Muhl C, Cantz M (1994) Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation. Biochem Biophys Res Commun 199:1188–1193
44. Monti E, Preti A, Venerando B, Borsani G (2002) Recent development in mammalian sialidase molecular biology. Neurochem Res 27:649–663
45. Miyagi T, Wada T, Yamaguchi K (2008) Roles of plasma membrane-associated sialidase NEU3 in human cancers. Biochim Biophys Acta 1780:532–537
46. Miyagi T, Wada T, Yamaguchi K, Hata K, Shiozaki K (2008) Plasma membrane-associated sialidase as a crucial regulator of transmembrane signalling. J Biochem 144:279–285
47. Ueno S, Saito S, Wada T, Yamaguchi K, Satoh M, Arai Y, Miyagi T (2006) Plasma membrane-associated sialidase is up-regulated in renal cell carcinoma and promotes interleukin-6-induced apoptosis suppression and cell motility. J Biol Chem 281:7756–7764
48. Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi K, Sato I, Miyagi T (2002) Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression. Proc Natl Acad Sci U S A 99:10718–10723
49. Venerando B, Fiorilli A, Croci G, Tringali C, Goi G, Mazzanti L, Curatola G, Segalini G, Massaccesi L, Lombardo A, Tettamanti G (2002) Acidic and neutral sialidase in the erythrocyte membrane of type 2 diabetic patients. Blood 99:1064–1070
50. Tringali C, Anastasia L, Papini N, Bianchi A, Ronzoni L, Cappellini MD, Monti E, Tettamanti G, Venerando B (2007) Modification of sialidase levels and sialoglycoconjugate pattern during erythroid and erytroleukemic cell differentiation. Glycoconj J 24:67–79
51. Tringali C, Lupo B, Anastasia L, Papini N, Monti E, Bresciani R, Tettamanti G, Venerando B (2007) Expression of sialidase Neu2 in leukemic K562 cells induces apoptosis by impairing Bcr-Abl/Src kinases signaling. J Biol Chem 282:14364–14372
52. Chigorno V, Cardace G, Pitto M, Sonnino S, Ghidoni R, Tettamanti G (1986) A radiometric assay for ganglioside sialidase applied to the determination of the enzyme subcellular location in cultured human fibroblasts. Anal Biochem 153:283–294
53. Schengrund CL, Repman MA (1982) Density-dependent changes in gangliosides and sialidase activity of murine neuroblastoma cells. J Neurochem 39:940–947
54. Valaperta R, Chigorno V, Basso L, Prinetti A, Bresciani R, Preti A, Miyagi T, Sonnino S (2006) Plasma membrane production of ceramide from ganglioside GM3 in human fibroblasts. FASEB J 20:1227–1229
55. Valaperta R, Valsecchi M, Rocchetta F, Aureli M, Prioni S, Prinetti A, Chigorno V, Sonnino S (2007) Induction of axonal differentiation by silencing plasma membrane-associated sialidase Neu3 in neuroblastoma cells. J Neurochem 100:708–719
56. Proshin S, Yamaguchi K, Wada T, Miyagi T (2002) Modulation of neuritogenesis by ganglioside-specific sialidase (Neu 3) in human neuroblastoma NB-1 cells. Neurochem Res 27:841–846
57. Hasegawa T, Yamaguchi K, Wada T, Takeda A, Itoyama Y, Miyagi T (2000) Molecular cloning of mouse ganglioside sialidase and its increased expression in neuro2a cell differentiation. J Biol Chem 275:14778
58. von Reitzenstein C, Kopitz J, Schuhmann V, Cantz M (2001) Differential functional relevance of a plasma membrane ganglioside sialidase in cholinergic and adrenergic neuroblastoma cell lines. Eur J Biochem 268:326–333
59. Aureli M, Loberto N, Lanteri P, Chigorno V, Prinetti A, Sonnino S (2011) Cell surface sphingolipid glycohydrolases in neuronal differentiation and aging in culture. J Neurochem 116:891–899
60. Rodriguez JA, Piddini E, Hasegawa T, Miyagi T, Dotti CG (2001) Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture. J Neurosci 21:8387–8395
61. Da Silva JS, Hasegawa T, Miyagi T, Dotti CG, Abad-Rodriguez J (2005) Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci 8:606–615
62. Kalka D, von Reitzenstein C, Kopitz J, Cantz M (2001) The plasma membrane ganglioside sialidase cofractionates with markers of lipid rafts. Biochem Biophys Res Commun 283:989–993
63. Papini N, Anastasia L, Tringali C, Croci G, Bresciani R, Yamaguchi K, Miyagi T, Preti A, Prinetti A, Prioni S, Sonnino S, Tettamanti G, Venerando B, Monti E (2004) The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J Biol Chem 279:16989–16995
64. Yamaguchi K, Hata K, Koseki K, Shiozaki K, Akita H, Wada T, Moriya S, Miyagi T (2005) Evidence for mitochondrial localization of a novel human sialidase (NEU4). Biochem J 390:85–93
65. Comelli EM, Amado M, Lustig SR, Paulson JC (2003) Identification and expression of Neu4, a novel murine sialidase. Gene 321:155–161
66. Shiozaki K, Koseki K, Yamaguchi K, Shiozaki M, Narimatsu H, Miyagi T (2009) Developmental change of sialidase neu4 expression in murine brain and its involvement in the regulation of neuronal cell differentiation. J Biol Chem 284:21157–21164
67. Seyrantepe V, Canuel M, Carpentier S, Landry K, Durand S, Liang F, Zeng J, Caqueret A, Gravel RA, Marchesini S, Zwingmann C, Michaud J, Morales CR, Levade T, Pshezhetsky AV (2008) Mice deficient in Neu4 sialidase exhibit abnormal ganglioside catabolism and lysosomal storage. Hum Mol Genet 17:1556–1568
68. Seyrantepe V, Lema P, Caqueret A, Dridi L, Bel Hadj S, Carpentier S, Boucher F, Levade T, Carmant L, Gravel RA, Hamel E, Vachon P, Di Cristo G, Michaud JL, Morales CR, Pshezhetsky AV (2010) Mice doubly-deficient in lysosomal hexosaminidase A and neuraminidase 4 show epileptic crises and rapid neuronal loss. PLoS Genet 6:e1001118
69. Li YT, Li SC (1999) Enzymatic hydrolysis of glycosphingolipids. Anal Biochem 273:1–11
70. Xu YH, Barnes S, Sun Y, Grabowski GA (2010) Multi-system disorders of glycosphingolipid and ganglioside metabolism. J Lipid Res 51:1643–1675
71. Coates PJ (2002) Markers of senescence? J Pathol 196:371–373
72. Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ (2000) Is beta-galactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res 257:162–171
73. Geng YQ, Guan JT, Xu XH, Fu YC (2010) Senescence-associated beta-galactosidase activity expression in aging hippocampal neurons. Biochem Biophys Res Commun 396:866–869
74. Evans MK, Taffe BG, Harris CC, Bohr VA (1993) DNA strand bias in the repair of the p53 gene in normal human and xeroderma pigmentosum group C fibroblasts. Cancer Res 53:5377–5381
75. Huang Q, Shur BD, Begovac PC (1995) Overexpressing cell surface beta 1.4-galactosyltransferase in PC12 cells increases neurite outgrowth on laminin. J Cell Sci 108(Pt 2):839–847
76. Neufeld EB, Cooney AM, Pitha J, Dawidowicz EA, Dwyer NK, Pentchev PG, Blanchette-Mackie EJ (1996) Intracellular trafficking of cholesterol monitored with a cyclodextrin. J Biol Chem 271:21604–21613
77. van Weely S, Brandsma M, Strijland A, Tager JM, Aerts JM (1993) Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease. Biochim Biophys Acta 1181:55–62
78. Daniels LB, Coyle PJ, Chiao YB, Glew RH, Labow RS (1981) Purification and characterization of a cytosolic broad specificity beta-glucosidase from human liver. J Biol Chem 256:13004–13013
79. Dekker N, Voorn-Brouwer T, Verhoek M, Wennekes T, Narayan RS, Speijer D, Hollak CE, Overkleeft HS, Boot RG, Aerts JM (2011) The cytosolic beta-glucosidase GBA3 does not influence type 1 Gaucher disease manifestation. Blood Cells Mol Dis 46:19–26
80. Nilsson O, Svennerholm L (1982) Accumulation of glucosylceramide and glucosylsphingosine (psychosine) in cerebrum and cerebellum in infantile and juvenile Gaucher disease. J Neurochem 39:709–718
81. de Fost M, Aerts JM, Hollak CE (2003) Gaucher disease: from fundamental research to effective therapeutic interventions. Neth J Med 61:3–8
82. Sidransky E (2005) Gaucher disease and parkinsonism. Mol Genet Metab 84:302–304
83. Sidransky E, Nalls MA, Aasly JO, Aharon-Peretz J, Annesi G, Barbosa ER, Bar-Shira A, Berg D, Bras J, Brice A, Chen CM, Clark LN, Condroyer C, De Marco EV, Durr A, Eblan MJ, Fahn S, Farrer MJ, Fung HC, Gan-Or Z, Gasser T, Gershoni-Baruch R, Giladi N, Griffith A, Gurevich T, Januario C, Kropp P, Lang AE, Lee-Chen GJ, Lesage S, Marder K, Mata IF, Mirelman A, Mitsui J, Mizuta I, Nicoletti G, Oliveira C, Ottman R, Orr-Urtreger A, Pereira LV, Quattrone A, Rogaeva E, Rolfs A, Rosenbaum H, Rozenberg R, Samii A, Samaddar T, Schulte C, Sharma M, Singleton A, Spitz M, Tan EK, Tayebi N, Toda T, Troiano AR, Tsuji S, Wittstock M, Wolfsberg TG, Wu YR, Zabetian CP, Zhao Y, Ziegler SG (2009) Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N Engl J Med 361:1651–1661
84. Mazzulli JR, Xu YH, Sun Y, Knight AL, McLean PJ, Caldwell GA, Sidransky E, Grabowski GA, Krainc D (2011) Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 146:37–52
85. Yap TL, Velayati A, Sidransky E, Lee JC (2013) Membrane-bound alpha-synuclein interacts with glucocerebrosidase and inhibits enzyme activity. Mol Genet Metab 108:56–64
86. Martin E, Schule R, Smets K, Rastetter A, Boukhris A, Loureiro JL, Gonzalez MA, Mundwiller E, Deconinck T, Wessner M, Jornea L, Oteyza AC, Durr A, Martin JJ, Schols L, Mhiri C, Lamari F, Zuchner S, De Jonghe P, Kabashi E, Brice A, Stevanin G (2013) Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia. Am J Hum Genet 92:238–244
87. Korschen HG, Yildiz Y, Raju DN, Schonauer S, Bonigk W, Jansen V, Kremmer E, Kaupp UB, Wachten D (2012) The non-lysosomal beta-glucosidase GBA2 is a non-integral membrane-associated protein at the endoplasmic reticulum (ER) and Golgi. J Biol Chem 288:3381–3393
88. Boot RG, Verhoek M, Donker-Koopman W, Strijland A, van Marle J, Overkleeft HS, Wennekes T, Aerts JM (2007) Identification of the non-lysosomal glucosylceramidase as beta-glucosidase 2. J Biol Chem 282:1305–1312
89. Matern H, Boermans H, Lottspeich F, Matern S (2001) Molecular cloning and expression of human bile acid beta-glucosidase. J Biol Chem 276:37929–37933
90. Yildiz Y, Matern H, Thompson B, Allegood JC, Warren RL, Ramirez DM, Hammer RE, Hamra FK, Matern S, Russell DW (2006) Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J Clin Invest 116:2985–2994
91. Hammer MB, Eleuch-Fayache G, Schottlaender LV, Nehdi H, Gibbs JR, Arepalli SK, Chong SB, Hernandez DG, Sailer A, Liu G, Mistry PK, Cai H, Shrader G, Sassi C, Bouhlal Y, Houlden H, Hentati F, Amouri R, Singleton AB (2013) Mutations in GBA2 cause autosomal-recessive cerebellar ataxia with spasticity. Am J Hum Genet 92:245–251
92. Ferreirinha F, Quattrini A, Pirozzi M, Valsecchi V, Dina G, Broccoli V, Auricchio A, Piemonte F, Tozzi G, Gaeta L, Casari G, Ballabio A, Rugarli EI (2004) Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J Clin Invest 113:231–242
93. Soderblom C, Stadler J, Jupille H, Blackstone C, Shupliakov O, Hanna MC (2010) Targeted disruption of the Mast syndrome gene SPG21 in mice impairs hind limb function and alters axon branching in cultured cortical neurons. Neurogenetics 11:369–378
94. Scandroglio F, Loberto N, Valsecchi M, Chigorno V, Prinetti A, Sonnino S (2009) Thin layer chromatography of gangliosides. Glycoconj J 26:961–973
95. Loberto N, Prioni S, Bettiga A, Chigorno V, Prinetti A, Sonnino S (2005) The membrane environment of endogenous cellular prion protein in primary rat cerebellar neurons. J Neurochem 95:771–783
96. Prinetti A, Bassi R, Riboni L, Tettamanti G (1997) Involvement of a ceramide activated protein phosphatase in the differentiation of neuroblastoma Neuro2a cells. FEBS Lett 414:475–479
97. Yu RK (1994) Development regulation of ganglioside metabolism. Prog Brain Res 101:31–44
98. Yu RK, Bieberich E, Xia T, Zeng G (2004) Regulation of ganglioside biosynthesis in the nervous system. J Lipid Res 45:783–793
99. Prinetti A, Chigorno V, Prioni S, Loberto N, Marano N, Tettamanti G, Sonnino S (2001) Changes in the lipid turnover, composition, and organization, as sphingolipid-enriched membrane domains, in rat cerebellar granule cells developing in vitro. J Biol Chem 276:21136–21145
100. Sonnino S, Cantu L, Corti M, Acquotti D, Venerando B (1994) Aggregative properties of gangliosides in solution. Chem Phys Lipids 71:21–45
101. Brocca P, Sonnino S (1997) Dynamic and spatial organization of surface gangliosides. Trends Glycosci Glyc 9:433–445
102. Prinetti A, Chigorno V, Tettamanti G, Sonnino S (2000) Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J Biol Chem 275:11658–11665
103. Venable ME, Lee JY, Smyth MJ, Bielawska A, Obeid LM (1995) Role of ceramide in cellular senescence. J Biol Chem 270:30701–30708