Gangliosides and Cell Surface Ganglioside Glycohydrolases in the Nervous System

  • Massimo Aureli
  • Maura Samarani
  • Valentina Murdica
  • Laura Mauri
  • Nicoletta Loberto
  • Rosaria Bassi
  • Alessandro Prinetti
  • Sandro Sonnino
Chapter
Part of the Advances in Neurobiology book series (NEUROBIOL, volume 9)

Abstract

Gangliosides are a large group of complex lipids found predominantly on the outer layer of the plasma membranes of cells, and they are particularly concentrated in nerve endings. Their half-life in the nervous system is short, and their membrane composition and content are strictly connected to their metabolism. Their neobiosynthesis starts in the endoplasmic reticulum and is completed in the Golgi; catabolism occurs primarily in the lysosomes. However, the final content of gangliosides in the plasma membrane is affected by other cellular processes.

In this chapter structural changes in the oligosaccharide chains of gangliosides induced by the activity of glycohydrolases and in some cases by glycosyltransferases that are associated with plasma membranes are discussed. Some of the plasma membrane enzymes arise from fusion processes between intracellular fractions and the plasma membrane; however, other plasma membrane enzymes display a structure different from that of the intracellular enzymes. Several of these plasma membrane enzymes have been characterized and some of them seem to have a specific role in the nervous system.

Keywords

Ganglioside Glycosphingolipid Glycohydrolases Sphingolipid metabolism Central nervous system Neuronal differentiation Neurodegeneration 

References

  1. Acquotti D, Fronza G, Riboni L, Sonnino S, Tettamanti G. Ganglioside lactones:1H-NMR determination of the inner ester position of GD1b-ganglioside lactone naturally occurring in human brain or produced by chemical synthesis. Glycoconj J. 1987;V4:119–27.CrossRefGoogle Scholar
  2. Aureli M, Bassi R, Loberto N, Regis S, Prinetti A, Chigorno V, et al. Cell surface associated glycohydrolases in normal and Gaucher disease fibroblasts. J Inherit Metab Dis. 2012;35:1081–91.PubMedCrossRefGoogle Scholar
  3. Aureli M, Gritti A, Bassi R, Loberto N, Ricca A, Chigorno V, et al. Plasma membrane-associated glycohydrolases along differentiation of murine neural stem cells. Neurochem Res. 2011a;37:1344–54.CrossRefGoogle Scholar
  4. Aureli M, Loberto N, Chigorno V, Prinetti A, Sonnino S. Remodeling of sphingolipids by plasma membrane associated enzymes. Neurochem Res. 2011b;36:1636–44.PubMedCrossRefGoogle Scholar
  5. Aureli M, Loberto N, Lanteri P, Chigorno V, Prinetti A, Sonnino S. Cell surface sphingolipid glycohydrolases in neuronal differentiation and aging in culture. J Neurochem. 2011c;116:891–9.PubMedCrossRefGoogle Scholar
  6. Aureli M, Masilamani AP, Illuzzi G, Loberto N, Scandroglio F, Prinetti A, et al. Activity of plasma membrane beta-galactosidase and beta-glucosidase. FEBS Lett. 2009;583:2469–73.PubMedCrossRefGoogle Scholar
  7. Bassi R, Chigorno V, Fiorilli A, Sonnino S, Tettamanti G. Exogenous gangliosides GD1b and GD1b-lactone, stably associated to rat brain P2 subcellular fraction, modulate differently the process of protein phosphorylation. J Neurochem. 1991;57:1207–11.PubMedCrossRefGoogle Scholar
  8. Bassi R, Riboni L, Sonnino S, Tettamanti G. Lactonization of GD1b ganglioside under acidic conditions. Carbohydr Res. 1989;193:141–6.PubMedCrossRefGoogle Scholar
  9. Bassi R, Riboni L, Tettamanti G. Cultured cerebellar granule cells, but not astrocytes, produce an ester of ganglioside GD1b, presumably GD1b monolactone, from exogenous GD1b. Biochem J. 1994;302(Pt 3):937–42.PubMedCentralPubMedGoogle Scholar
  10. Bateman KS, Cherney MM, Mahuran DJ, Tropak M, James MN. Crystal structure of beta-hexosaminidase B in complex with pyrimethamine, a potential pharmacological chaperone. J Med Chem. 2011;54:1421–9.PubMedCentralPubMedCrossRefGoogle Scholar
  11. Bearpark TM, Stirling JL. A difference in the specificities of human liver N-acetyl-beta-hexosaminidases A and B detected by their activities towards glycosaminoglycan oligosaccharides. Biochem J. 1978;173:997–1000.PubMedCentralPubMedGoogle Scholar
  12. Brocca P, Sonnino S. Dynamic and spatial organization of surface gangliosides. Trends Glycosci Glycotech. 1997;9:433–45.CrossRefGoogle Scholar
  13. Chigorno V, Cardace G, Pitto M, Sonnino S, Ghidoni R, Tettamanti G. A radiometric assay for ganglioside sialidase applied to the determination of the enzyme subcellular location in cultured human fibroblasts. Anal Biochem. 1986;153:283–94.PubMedCrossRefGoogle Scholar
  14. Chigorno V, Giannotta C, Ottico E, Sciannamblo M, Mikulak J, Prinetti A, et al. Sphingolipid uptake by cultured cells: complex aggregates of cell sphingolipids with serum proteins and lipoproteins are rapidly catabolized. J Biol Chem. 2005;280:2668–75.PubMedCrossRefGoogle Scholar
  15. Chigorno V, Negroni E, Nicolini M, Sonnino S. Activity of 3-ketosphinganine synthase during differentiation and aging of neuronal cells in culture. J Lipid Res. 1997a;38:1163–9.PubMedGoogle Scholar
  16. Chigorno V, Riva C, Valsecchi M, Nicolini M, Brocca P, Sonnino S. Metabolic processing of gangliosides by human fibroblasts in culture–formation and recycling of separate pools of sphingosine. Eur J Biochem. 1997b;250:661–9.PubMedCrossRefGoogle Scholar
  17. Chigorno V, Sciannamblo M, Mikulak J, Prinetti A, Sonnino S. Efflux of sphingolipids metabolically labeled with [1–3H]sphingosine, l-[3–3H]serine and [9,10–3H]palmitic acid from normal cells in culture. Glycoconj J. 2006;23:159–65.PubMedCrossRefGoogle Scholar
  18. Coates PJ. Markers of senescence? J Pathol. 2002;196:371–3.PubMedCrossRefGoogle Scholar
  19. Crespo PM, Demichelis VT, Daniotti JL. Neobiosynthesis of glycosphingolipids by plasma membrane-associated glycosyltransferases. J Biol Chem. 2010;285:29179–90.PubMedCentralPubMedCrossRefGoogle Scholar
  20. Da Silva JS, Hasegawa T, Miyagi T, Dotti CG, Abad-Rodriguez J. Asymmetric membrane ganglioside sialidase activity specifies axonal fate. Nat Neurosci. 2005;8:606–15.PubMedCrossRefGoogle Scholar
  21. Daniels LB, Coyle PJ, Chiao YB, Glew RH, Labow RS. Purification and characterization of a cytosolic broad specificity beta-glucosidase from human liver. J Biol Chem. 1981;256:13004–13.PubMedGoogle Scholar
  22. Del Favero E, Brocca P, Motta S, Rondelli V, Sonnino S, Cantu L. Nanoscale structural response of ganglioside-containing aggregates to the interaction with sialidase. J Neurochem. 2011;116:833–9.PubMedCrossRefGoogle Scholar
  23. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995;92:9363–7.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Durrie R, Rosenberg A. Anabolic sialosylation of gangliosides in situ in rat brain cortical slices. J Lipid Res. 1989;30:1259–66.PubMedGoogle Scholar
  25. Durrie R, Saito M, Rosenberg A. Endogenous glycosphingolipid acceptor specificity of sialosyltransferase systems in intact Golgi membranes, synaptosomes, and synaptic plasma membranes from rat brain. Biochemistry. 1988;27:3759–64.PubMedCrossRefGoogle Scholar
  26. Evans MK, Robbins JH, Ganges MB, Tarone RE, Nairn RS, Bohr VA. Gene-specific DNA repair in xeroderma pigmentosum complementation groups A, C, D, and F. Relation to cellular survival and clinical features. J Biol Chem. 1993;268:4839–47.PubMedGoogle Scholar
  27. Ferreirinha F, Quattrini A, Pirozzi M, Valsecchi V, Dina G, Broccoli V, et al. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J Clin Invest. 2004;113:231–42.PubMedCentralPubMedCrossRefGoogle Scholar
  28. Geng YQ, Guan JT, Xu XH, Fu YC. Senescence-associated beta-galactosidase activity expression in aging hippocampal neurons. Biochem Biophys Res Commun. 2010;396:866–9.PubMedCrossRefGoogle Scholar
  29. Gulbins E, Grassme H. Ceramide and cell death receptor clustering. Biochim Biophys Acta. 2002;1585:139–45.PubMedCrossRefGoogle Scholar
  30. Hammer MB, Eleuch-Fayache G, Schottlaender LV, Nehdi H, Gibbs JR, Arepalli SK, et al. Mutations in GBA2 cause autosomal-recessive cerebellar ataxia with spasticity. Am J Hum Genet. 2013;92:245–51.PubMedCentralPubMedCrossRefGoogle Scholar
  31. Hasegawa T, Yamaguchi K, Wada T, Takeda A, Itoyama Y, Miyagi T. Molecular cloning of mouse ganglioside sialidase and its increased expression in neuro2a cell differentiation. J Biol Chem. 2000;275:14778.PubMedGoogle Scholar
  32. Hata K, Wada T, Hasegawa A, Kiso M, Miyagi T. Purification and characterization of a membrane-associated ganglioside sialidase from bovine brain. J Biochem (Tokyo). 1998;123:899–905.CrossRefGoogle Scholar
  33. Holopainen JM, Angelova MI, Kinnunen PK. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys J. 2000;78:830–8.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Huang Q, Shur BD, Begovac PC. Overexpressing cell surface beta 1.4-galactosyltransferase in PC12 cells increases neurite outgrowth on laminin. J Cell Sci. 1995;108(Pt 2):839–47.PubMedGoogle Scholar
  35. Iwamori M, Iwamori Y. Changes in the glycolipid composition and characteristic activation of GM3 synthase in the thymus of mouse after administration of dexamethasone. Glycoconj J. 2005;22:119–26.PubMedCrossRefGoogle Scholar
  36. Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi K, Sato I, et al. 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. 2002;99:10718–23.PubMedCentralPubMedCrossRefGoogle Scholar
  37. Kalka D, von Reitzenstein C, Kopitz J, Cantz M. The plasma membrane ganglioside sialidase cofractionates with markers of lipid rafts. Biochem Biophys Res Commun. 2001;283:989–93.PubMedCrossRefGoogle Scholar
  38. Kamerling JP, Vliegenthart JF. Identification of O-cetylated N-acylneuraminic acids by mass spectrometry. Carbohydr Res. 1975;41:7–17.PubMedCrossRefGoogle Scholar
  39. Kolter T, Sandhoff K. Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu Rev Cell Dev Biol. 2005;21:81–103.PubMedCrossRefGoogle Scholar
  40. Kolter T, Sandhoff K. Sphingolipid metabolism diseases. Biochim Biophys Acta. 2006;1758:2057–79.PubMedCrossRefGoogle Scholar
  41. Kopitz J, Muhl C, Ehemann V, Lehmann C, Cantz M. Effects of cell surface ganglioside sialidase inhibition on growth control and differentiation of human neuroblastoma cells. Eur J Cell Biol. 1997a;73:1–9.PubMedGoogle Scholar
  42. Kopitz J, Sinz K, Brossmer R, Cantz M. Partial characterization and enrichment of a membrane-bound sialidase specific for gangliosides from human brain tissue. Eur J Biochem. 1997b;248:527–34.PubMedCrossRefGoogle Scholar
  43. Kopitz J, von Reitzenstein C, Muhl C, Cantz M. Role of plasma membrane ganglioside sialidase of human neuroblastoma cells in growth control and differentiation. Biochem Biophys Res Commun. 1994;199:1188–93.PubMedCrossRefGoogle Scholar
  44. Korschen HG, Yildiz Y, Raju DN, Schonauer S, Bonigk W, Jansen V, et al. The non-lysosomal beta-glucosidase GBA2 is a non-integral membrane-associated protein at the endoplasmic reticulum (ER) and Golgi. J Biol Chem. 2012;288:3381–93.PubMedCentralPubMedCrossRefGoogle Scholar
  45. Kytzia HJ, Sandhoff K. Evidence for two different active sites on human beta-hexosaminidase A. Interaction of GM2 activator protein with beta-hexosaminidase A. J Biol Chem. 1985;260:7568–72.PubMedGoogle Scholar
  46. Li YT, Li SC. Enzymatic hydrolysis of glycosphingolipids. Anal Biochem. 1999;273:1–11.PubMedCrossRefGoogle Scholar
  47. Martin E, Schule R, Smets K, Rastetter A, Boukhris A, Loureiro JL, et al. Loss of function of glucocerebrosidase GBA2 is responsible for motor neuron defects in hereditary spastic paraplegia. Am J Hum Genet. 2013;92:238–44.PubMedCentralPubMedCrossRefGoogle Scholar
  48. Matern H, Boermans H, Lottspeich F, Matern S. Molecular cloning and expression of human bile acid beta-glucosidase. J Biol Chem. 2001;276:37929–33.PubMedGoogle Scholar
  49. Matsui Y, Lombard D, Massarelli R, Mandel P, Dreyfus H. Surface glycosyltransferase activities during development of neuronal cell cultures. J Neurochem. 1986;46:144–50.PubMedCrossRefGoogle Scholar
  50. Mazzulli JR, Xu YH, Sun Y, Knight AL, McLean PJ, Caldwell GA, et al. Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell. 2011;146:37–52.PubMedCentralPubMedCrossRefGoogle Scholar
  51. Mencarelli S, Cavalieri C, Magini A, Tancini B, Basso L, Lemansky P, et al. Identification of plasma membrane associated mature beta-hexosaminidase A, active towards GM2 ganglioside, in human fibroblasts. FEBS Lett. 2005;579:5501–6.PubMedCrossRefGoogle Scholar
  52. Miyagi T, Sagawa J, Konno K, Handa S, Tsuiki S. Biochemical and immunological studies on two distinct ganglioside-hydrolyzing sialidases from the particulate fraction of rat brain. J Biochem (Tokyo). 1990a;107:787–93.Google Scholar
  53. Miyagi T, Sagawa J, Konno K, Tsuiki S. Immunological discrimination of intralysosomal, cytosolic, and two membrane sialidases present in rat tissues. J Biochem (Tokyo). 1990b;107:794–8.Google Scholar
  54. Miyagi T, Wada T, Iwamatsu A, Hata K, Yoshikawa Y, Tokuyama S, et al. Molecular cloning and characterization of a plasma membrane-associated sialidase specific for gangliosides. J Biol Chem. 1999;274:5004–11.PubMedCrossRefGoogle Scholar
  55. Miyagi T, Wada T, Yamaguchi K. Roles of plasma membrane-associated sialidase NEU3 in human cancers. Biochim Biophys Acta. 2008a;1780:532–7.PubMedCrossRefGoogle Scholar
  56. Miyagi T, Wada T, Yamaguchi K, Shiozaki K, Sato I, Kakugawa Y, et al. Human sialidase as a cancer marker. Proteomics. 2008b;8:3303–11.PubMedCrossRefGoogle Scholar
  57. Monti E, Preti A, Venerando B, Borsani G. Recent development in mammalian sialidase molecular biology. Neurochem Res. 2002;27:649–63.PubMedCrossRefGoogle Scholar
  58. Neufeld EB, Cooney AM, Pitha J, Dawidowicz EA, Dwyer NK, Pentchev PG, et al. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J Biol Chem. 1996;271:21604–13.PubMedCrossRefGoogle Scholar
  59. Oehler C, Kopitz J, Cantz M. Substrate specificity and inhibitor studies of a membrane-bound ganglioside sialidase isolated from human brain tissue. Biol Chem. 2002;383:1735–42.PubMedGoogle Scholar
  60. Olayioye MA, Hausser A. Integration of non-vesicular and vesicular transport processes at the Golgi complex by the PKD-CERT network. Biochim Biophys Acta. 2012;1821:1096–103.PubMedCrossRefGoogle Scholar
  61. Papini N, Anastasia L, Tringali C, Croci G, Bresciani R, Yamaguchi K, et al. The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J Biol Chem. 2004;279:16989–95.PubMedCrossRefGoogle Scholar
  62. Preti A, Fiorilli A, Lombardo A, Caimi L, Tettamanti G. Occurrence of sialyltransferase activity in the synaptosomal membranes prepared from calf brain cortex. J Neurochem. 1980;35:281–96.PubMedCrossRefGoogle Scholar
  63. Prinetti A, Chigorno V, Prioni S, Loberto N, Marano N, Tettamanti G, et al. Changes in the lipid turnover, composition, and organization, as sphingolipid-enriched membrane domains, in rat cerebellar granule cells developing in vitro. J Biol Chem. 2001;276:21136–45.PubMedCrossRefGoogle Scholar
  64. Prinetti A, Chigorno V, Tettamanti G, Sonnino S. Sphingolipid-enriched membrane domains from rat cerebellar granule cells differentiated in culture. A compositional study. J Biol Chem. 2000a;275:11658–65.PubMedCrossRefGoogle Scholar
  65. Prinetti A, Marano N, Prioni S, Chigorno V, Mauri L, Casellato R, et al. Association of Src-family protein tyrosine kinases with sphingolipids in rat cerebellar granule cells differentiated in culture. Glycoconj J. 2000b;17:223–32.PubMedCrossRefGoogle Scholar
  66. Proshin S, Yamaguchi K, Wada T, Miyagi T. Modulation of neuritogenesis by ganglioside-specific sialidase (Neu 3) in human neuroblastoma NB-1 cells. Neurochem Res. 2002;27:841–6.PubMedCrossRefGoogle Scholar
  67. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell. 2001;106:157–69.PubMedCrossRefGoogle Scholar
  68. Riboni L, Prinetti A, Bassi R, Tettamanti G. Cerebellar granule cells in culture exhibit a ganglioside-sialidase presumably linked to the plasma membrane. FEBS Lett. 1991;287:42–6.PubMedCrossRefGoogle Scholar
  69. Riboni L, Sonnino S, Acquotti D, Malesci A, Ghidoni R, Egge H, et al. Natural occurrence of ganglioside lactones. Isolation and characterization of GD1b inner ester from adult human brain. J Biol Chem. 1986;261:8514–9.PubMedGoogle Scholar
  70. Rodriguez JA, Piddini E, Hasegawa T, Miyagi T, Dotti CG. Plasma membrane ganglioside sialidase regulates axonal growth and regeneration in hippocampal neurons in culture. J Neurosci. 2001;21:8387–95.PubMedGoogle Scholar
  71. Saqr HE, Pearl DK, Yates AJ. A review and predictive models of ganglioside uptake by biological membranes. J Neurochem. 1993;61:395–411.PubMedCrossRefGoogle Scholar
  72. Schengrund CL, Repman MA. Density-dependent changes in gangliosides and sialidase activity of murine neuroblastoma cells. J Neurochem. 1982;39:940–7.PubMedCrossRefGoogle Scholar
  73. Schengrund CL, Rosenberg A. Intracellular location and properties of bovine brain sialidase. J Biol Chem. 1970;245:6196–200.PubMedGoogle Scholar
  74. Schengrund CL, Rosenberg A, Repman MA. Ecto-ganglioside-sialidase activity of herpes simplex virus-transformed hamster embryo fibroblasts. J Cell Biol. 1976;70:555–61.PubMedCrossRefGoogle Scholar
  75. Schneider-Jakob HR, Cantz M. Lysosomal and plasma membrane ganglioside GM3 sialidases of cultured human fibroblasts. Differentiation by detergents and inhibitors. Biol Chem Hoppe Seyler. 1991;372:443–50.PubMedCrossRefGoogle Scholar
  76. Severino J, Allen RG, Balin S, Balin A, Cristofalo VJ. Is beta-galactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res. 2000;257:162–71.PubMedCrossRefGoogle Scholar
  77. Sidransky E, Nalls MA, Aasly JO, Aharon-Peretz J, Annesi G, Barbosa ER, et al. Multicenter analysis of glucocerebrosidase mutations in Parkinson’s disease. N Engl J Med. 2009;361:1651–61.PubMedCentralPubMedCrossRefGoogle Scholar
  78. Soderblom C, Stadler J, Jupille H, Blackstone C, Shupliakov O, Hanna MC. Targeted disruption of the Mast syndrome gene SPG21 in mice impairs hind limb function and alters axon branching in cultured cortical neurons. Neurogenetics. 2010;11:369–78.PubMedCrossRefGoogle Scholar
  79. Sonnino S, Cantu L, Corti M, Acquotti D, Venerando B. Aggregative properties of gangliosides in solution. Chem Phys Lipids. 1994;71:21–45.PubMedCrossRefGoogle Scholar
  80. Sonnino S, Chigorno V, Valsecchi M, Bassi R, Acquotti D, Cantu L, et al. Relationship between the regulation of membrane enzyme activities by gangliosides and a possible ganglioside segregation in membrane microdomains. Indian J Biochem Biophys. 1990;27:353–8.PubMedGoogle Scholar
  81. Sonnino S, Ghidoni R, Chigorno V, Masserini M, Tettamanti G. Recognition by two-dimensional thin-layer chromatography and densitometric quantification of alkali-labile gangliosides from the brain of different animals. Anal Biochem. 1983;128:104–14.PubMedCrossRefGoogle Scholar
  82. Sonnino S, Prinetti A, Mauri L, Chigorno V, Tettamanti G. Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chem Rev. 2006;106:2111–25.PubMedCrossRefGoogle Scholar
  83. Tettamanti G, Morgan IG, Gombos G, Vincendon G, Mandel P. Sub-synaptosomal localization of brain particulate neuraminidose. Brain Res. 1972;47:515–8.PubMedCrossRefGoogle Scholar
  84. Tettamanti G, Preti A, Lombardo A, Bonali F, Zambotti V. Parallelism of subcellular location of major particulate neuraminidase and gangliosides in rabbit brain cortex. Biochim Biophys Acta. 1973;306:466–77.PubMedCrossRefGoogle Scholar
  85. Tettamanti G, Preti A, Lombardo A, Suman T, Zambotti V. Membrane-bound neuraminidase in the brain of different animals: behaviour of the enzyme on endogenous sialo derivatives and rationale for its assay. J Neurochem. 1975;25:451–6.PubMedCrossRefGoogle Scholar
  86. Triggs-Raine B, Mahuran DJ, Gravel RA. Naturally occurring mutations in GM2 gangliosidosis: a compendium. Adv Genet. 2001;44:199–224.PubMedCrossRefGoogle Scholar
  87. Tringali C, Anastasia L, Papini N, Bianchi A, Ronzoni L, Cappellini MD, et al. Modification of sialidase levels and sialoglycoconjugate pattern during erythroid and erytroleukemic cell differentiation. Glycoconj J. 2007a;24:67–79.PubMedCrossRefGoogle Scholar
  88. Tringali C, Lupo B, Anastasia L, Papini N, Monti E, Bresciani R, et al. Expression of sialidase Neu2 in leukemic K562 cells induces apoptosis by impairing Bcr-Abl/Src kinases signaling. J Biol Chem. 2007b;282:14364–72.PubMedCrossRefGoogle Scholar
  89. Ueno S, Saito S, Wada T, Yamaguchi K, Satoh M, Arai Y, et al. Plasma membrane-associated sialidase is up-regulated in renal cell carcinoma and promotes interleukin-6-induced apoptosis suppression and cell motility. J Biol Chem. 2006;281:7756–64.PubMedCrossRefGoogle Scholar
  90. Valaperta R, Chigorno V, Basso L, Prinetti A, Bresciani R, Preti A, et al. Plasma membrane production of ceramide from ganglioside GM3 in human fibroblasts. FASEB J. 2006;20:1227–9.PubMedCrossRefGoogle Scholar
  91. Valaperta R, Valsecchi M, Rocchetta F, Aureli M, Prioni S, Prinetti A, et al. Induction of axonal differentiation by silencing plasma membrane-associated sialidase Neu3 in neuroblastoma cells. J Neurochem. 2007;100:708–19.PubMedCrossRefGoogle Scholar
  92. Valsecchi M, Palestini P, Chigorno V, Sonnino S. Age-related changes of the ganglioside long-chain base composition in rat cerebellum. Neurochem Int. 1996;28:183–7.PubMedCrossRefGoogle Scholar
  93. Valsecchi M, Palestini P, Chigorno V, Sonnino S, Tettamanti G. Changes in the ganglioside long-chain base composition of rat cerebellar granule cells during differentiation and aging in culture. J Neurochem. 1993;60(1):193–6.PubMedCrossRefGoogle Scholar
  94. van Weely S, Brandsma M, Strijland A, Tager JM, Aerts JM. Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease. Biochim Biophys Acta. 1993;1181:55–62.PubMedCrossRefGoogle Scholar
  95. Veldman RJ, Klappe K, Hinrichs J, Hummel I, van der Schaaf G, Sietsma H, et al. Altered sphingolipid metabolism in multidrug-resistant ovarian cancer cells is due to uncoupling of glycolipid biosynthesis in the Golgi apparatus. FASEB J. 2002;16:1111–3.PubMedGoogle Scholar
  96. Venable ME, Lee JY, Smyth MJ, Bielawska A, Obeid LM. Role of ceramide in cellular senescence. J Biol Chem. 1995;270:30701–8.PubMedCrossRefGoogle Scholar
  97. Venerando B, Fiorilli A, Croci G, Tringali C, Goi G, Mazzanti L, et al. Acidic and neutral sialidase in the erythrocyte membrane of type 2 diabetic patients. Blood. 2002;99:1064–70.PubMedCrossRefGoogle Scholar
  98. von Reitzenstein C, Kopitz J, Schuhmann V, Cantz M. Differential functional relevance of a plasma membrane ganglioside sialidase in cholinergic and adrenergic neuroblastoma cell lines. Eur J Biochem. 2001;268:326–33.CrossRefGoogle Scholar
  99. Wada T, Yoshikawa Y, Tokuyama S, Kuwabara M, Akita H, Miyagi T. Cloning, expression, and chromosomal mapping of a human ganglioside sialidase. Biochem Biophys Res Commun. 1999;261:21–7.PubMedCrossRefGoogle Scholar
  100. Xu YH, Barnes S, Sun Y, Grabowski GA. Multi-system disorders of glycosphingolipid and ganglioside metabolism. J Lipid Res. 2010;51:1643–75.PubMedCentralPubMedCrossRefGoogle Scholar
  101. Yildiz Y, Matern H, Thompson B, Allegood JC, Warren RL, Ramirez DM, et al. Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J Clin Invest. 2006;116:2985–94.PubMedCentralPubMedCrossRefGoogle Scholar
  102. Yu RK. Development regulation of ganglioside metabolism. Prog Brain Res. 1994;101:31–44.PubMedCrossRefGoogle Scholar
  103. Yu RK, Bieberich E, Xia T, Zeng G. Regulation of ganglioside biosynthesis in the nervous system. J Lipid Res. 2004;45:783–93.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Massimo Aureli
    • 1
  • Maura Samarani
    • 1
  • Valentina Murdica
    • 1
  • Laura Mauri
    • 1
  • Nicoletta Loberto
    • 1
  • Rosaria Bassi
    • 1
  • Alessandro Prinetti
    • 1
  • Sandro Sonnino
    • 1
  1. 1.Department of Medical Biotechnology and Translational MedicineUniversity of MilanoSegrate (MI)Italy

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