Lipid glycosylation: a primer for histochemists and cell biologists

Histochemistry and Cell Biology

Volumn 147, Issue 2, 2017, Pages 175-198

  Kopitz, Jürgen ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Ganglioside; Glycosphingolipid; Lectin; Lipid raft; Neuroblastoma

Indexed keywords

CERAMIDE DERIVATIVE; GLYCOLIPID; GLYCOSPHINGOLIPID; MONOGLYCOSYLCERAMIDE DERIVATIVE; UNCLASSIFIED DRUG; GLYCEROLGLYCOLIPIDS; LIPID;

BIOLOGICAL FUNCTIONS; CLASSIFICATION; CYTOLOGY; GLYCOSYLATION; HISTOCHEMISTRY; HUMAN; LIPID DEGRADATION; LIPOGENESIS; NEOPLASM; NEUROLOGIC DISEASE; NOMENCLATURE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPHINGOLIPID METABOLISM; STORAGE DISEASE; CELL ADHESION; CHEMISTRY; LIPID METABOLISM; METABOLISM;

CELL ADHESION; CELL BIOLOGY; GLYCOLIPIDS; GLYCOSYLATION; HUMANS; LIPID METABOLISM; LIPIDS;

EID: 85006790264     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-016-1518-4     Document Type: Review

References (238)

1. Abad-Rodríguez J, Díez-Revuelta N (2015) Axon glycoprotein routing in nerve polarity, function, and repair. Trends Biochem Sci 40:385–396
2. Adams CW, Bayliss OB (1963) Histochemical observations on the localisation and origin of sphingomyelin, cerebroside and cholesterol in the normal and atherosclerotic human artery. J Pathol Bacteriol 85:113–119
3. Ahmed M, Cheung NK (2014) Engineering anti-GD2 monoclonal antibodies for cancer immunotherapy. FEBS Lett 588:288–297
4. Akiyoshi K, Itaya A, Nomura S, Ono N, Yoshikawa K (2003) Induction of neuron-like tubes and liposome networks by cooperative effect of gangliosides and phospholipids. FEBS Lett 534:33–38
5. Alroy J, Ucci AA, Goyal V, Woods W (1986) Lectin histochemistry of glycolipid storage diseases on frozen and paraffin-embedded tissue sections. J Histochem Cytochem 34:501–505
6. INK4a: anoikis-favouring decrease in N/O-glycan/cell surface sialylation by down-regulation of enzymes in sialic acid biosynthesis in tandem in a pancreatic carcinoma model. FEBS J 279:4062–4080
7. André S, Kaltner H, Lensch M, Russwurm R, Siebert HC, Fallsehr C, Tajkhorshid E, Heck AJ, Knebel Doeberitz M, Gabius HJ, Kopitz J (2005) Determination of structural and functional overlap/divergence of five proto-type galectins by analysis of the growth-regulatory interaction with ganglioside GM1 in silico and in vitro on human neuroblastoma cells. Int J Cancer 114:46–57
8. INK4a: modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J 274:3233–3256
9. André S, Kopitz J, Kaltner H, Villalobo HA, Gabius HJ (2009) Glycans as functional markers in malignancy. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 419–432
10. André S, Kaltner H, Kayser K, Murphy PV, Gabius HJ (2016) Merging carbohydrate chemistry with lectin histochemistry to study inhibition of lectin binding by glycoclusters in the natural tissue context. Histochem Cell Biol 145:185–199
11. Ariga T, Kubota M, Nakane M, Oguro K, Yu RK, Ando S (2013) Anti-Chol-1 antigen, GQ1bα, antibodies are associated with Alzheimer’s disease. PLoS ONE 8:e63326
12. Asensio JL, Espinosa JF, Dietrich H, Cañada FJ, Schmidt RR, Martín-Lomas M, André S, Gabius H-J, Jiménez-Barbero J (1999) Bovine heart galectin-1 selects a distinct (syn) conformation of C-lactose, a flexible lactose analogue. J Am Chem Soc 121:8995–9000
13. Bhide GP, Colley KJ (2017) Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1520-x
14. Bhunia A, Vivekanandan S, Eckert T, Burg-Roderfeld M, Wechselberger R, Romanuka J, Bachle D, Kornilov AV, von der Lieth CW, Jimenez-Barbero J, Nifantiev NE, Schachner M, Sewald N, Lütteke T, Gabius HJ, Siebert HC (2010) Why structurally different cyclic peptides can be glycomimetics of the HNK-1 carbohydrate antigen. J Am Chem Soc 132:96–105
15. Binz T, Rummel A (2009) Cell entry strategy of clostridial neurotoxins. J Neurochem 109(6):1584–1595
16. Bleeke M, Fest S, Huebener N, Landgraf C, Schraven B, Gaedicke G, Volkmer R, Lode HN (2009) Systematic amino acid substitutions improved efficiency of GD2-peptide mimotope vaccination against neuroblastoma. Eur J Cancer 45:2915–2921
17. Bodian M, Lake BD (1963) The rectal approach to neuropathology. Br J Surg 50:702–714
18. Boukhris A, Schule R, Loureiro JL, Lourenco CM, Mundwiller E, Gonzalez MA, Charles P, Gauthier J, Rekik I, Acosta Lebrigio RF, Gaussen M, Speziani F, Ferbert A, Feki I, Caballero-Oteyza A, Dionne-Laporte A, Amri M, Noreau A, Forlani S, Cruz VT, Mochel F, Coutinho P, Dion P, Mhiri C, Schols L, Pouget J, Darios F, Rouleau GA, Marques W Jr, Brice A, Durr A, Zuchner S, Stevanin G (2013) Alteration of ganglioside biosynthesis responsible for complex hereditary spastic paraplegia. Am J Hum Genet 93:118–123
19. Bovin N (1997) Carbohydrate-carbohydrate interaction. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 277–290
20. Brady RO (2006) Enzyme replacement for lysosomal diseases. Annu Rev Med 57:283–296
21. Brockhausen I, Schachter H (1997) Glycosyltransferases involved in N- and O-glycan biosynthesis. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 79–114
22. Brown D (2002) Structure and function of membrane rafts. Int J Med Microbiol 291(6–7):433–437
23. Bucior I, Burger M, Fernandez-Busquets X (2009) Carbohydrate-carbohydrate interactions. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 347–362
24. Buddecke E (2009) Proteoglycans. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 199–216
25. Cacic M, Müthing J, Kracun I, Neumann U, Weber-Schurholz S (1994) Expression of neutral glycosphingolipids and gangliosides in human skeletal and heart muscle determined by indirect immunofluorescence staining. Glycoconj J 11:477–485
26. Cacic M, Sostaric K, Weber-Schurholz S, Müthing J (1995) Immunohistological analyses of neutral glycosphingolipids and gangliosides in normal mouse skeletal muscle and in mice with neuromuscular diseases. Glycoconj J 12:721–728
27. Caldwell S, Heitger A, Shen W, Liu Y, Taylor B, Ladisch S (2003) Mechanisms of ganglioside inhibition of APC function. J Immunol 171:1676–1683
28. Caselitz J (1987) Lectins and blood group substances as tumor markers. Curr Top Pathol 77:245–277
29. Chapman J, Sela BA, Wertman E, Michaelson DM (1988) Antibodies to ganglioside GM1 in patients with Alzheimer’s disease. Neurosci Lett 86:235–240
30. Cheng H, Wang M, Li JL, Cairns NJ, Han X (2013) Specific changes of sulfatide levels in individuals with pre-clinical Alzheimer’s disease: an early event in disease pathogenesis. J Neurochem 127:733–738
31. Chester MA (1998) IUPAC-IUB joint commission on biochemical nomenclature (JCBN). Nomenclature of glycolipids:recommendations 1997. Eur J Biochem 257:293–298
32. Corfield AP (2017) Protein glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1526-4
33. Corfield A, Berry M (2015) Glycan variation and evolution in the eukaryotes. Trends Biochem Sci 40:351–359
34. Dalakas MC (2015) Pathogenesis of immune-mediated neuropathies. Biochim Biophys Acta 1852:658–666
35. Danguy A, Akif F, Pajak B, Gabius HJ (1994) Contribution of carbohydrate histochemistry to glycobiology. Histol Histopathol 9:155–171
36. Danguy A, Camby I, Salmon I, Kiss R (1997) Modern glycohistochemistry: a major contribution to morphological changes. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 547–562
37. Daniotti JL, Lardone RD, Vilcaes AA (2015) Dysregulated expression of glycolipids in tumor cells: from negative modulator of anti-tumor immunity to promising targets for developing therapeutic agents. Front Oncol 5:300
38. Dawson H, André S, Karamitopoulou E, Zlobec I, Gabius HJ (2013) The growing galectin network in colon cancer and clinical relevance of cytoplasmic galectin-3 reactivity. Anticancer Res 33:3053–3059
39. Degroote S, Wolthoorn J, van Meer G (2004) The cell biology of glycosphingolipids. Semin Cell Dev Biol 15:375–387
40. Delacour D, Gouyer V, Zanetta JP, Drobecq H, Leteurtre E, Grard G, Moreau-Hannedouche O, Maes E, Pons A, André S, Le Bivic A, Gabius HJ, Manninen A, Simons K, Huet G (2005) Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 169:491–501
41. Denny CA, Desplats PA, Thomas EA, Seyfried TN (2010) Cerebellar lipid differences between R6/1 transgenic mice and humans with Huntington’s disease. J Neurochem 115:748–758
42. Desplats PA, Denny CA, Kass KE, Gilmartin T, Head SR, Sutcliffe JG, Seyfried Thomas EA (2007) Glycolipid and ganglioside metabolism imbalances in Huntington’s disease. Neurobiol Dis 27:265–277
43. Di Pardo A, Amico E, Maglione V (2016) Impaired levels of gangliosides in the Corpus Callosum of Huntington Disease animal models. Front Neurosci 10:457
44. Diaz-Rohrer B, Levental KR, Levental I (2014) Rafting through traffic: membrane domains in cellular logistics. Biochim Biophys Acta 1838:3003–3013
45. Dong Y, Ikeda K, Hamamura K, Zhang Q, Kondo Y, Matsumoto Y, Ohmi Y, Yamauchi Y, Furukawa K, Taguchi R, Furukawa K (2010) GM1/GD1b/GA1 synthase expression results in the reduced cancer phenotypes with modulation of composition and raft-localization of gangliosides in a melanoma cell line. Cancer Sci 101:2039–2047
46. Dong L, Liu Y, Colberg-Poley AM, Kaucic K, Ladisch S (2011) Induction of GM1a/GD1b synthase triggers complex ganglioside expression and alters neuroblastoma cell behavior; a new tumor cell model of ganglioside function. Glycoconj J 28:137–147
47. Eckert V, Gerold P, Schwarz R (1997) GPI-anchors: structure and functions. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 223–243
48. Ewers H, Helenius A (2011) Lipid-mediated endocytosis. Cold Spring Harb Perspect Biol 3:a004721
49. Fahie K, Zachara NE (2016) Molecular functions of glycoconjugates in autophagy. J Mol Biol 428:3305–3324
50. Fantini J, Maresca M, Hammache D, Yahi N, Delezay O (2000) Glycosphingolipid (GSL) microdomains as attachment platforms for host pathogens and their toxins on intestinal epithelial cells: activation of signal transduction pathways and perturbations of intestinal absorption and secretion. Glycoconj J 17:173–179
51. Farooqui AA (1981) Metabolism of sulfolipids in mammalian tissues. Adv Lipid Res 18:159–202
52. Fragaki K, Ait-El-Mkadem S, Chaussenot A, Gire C, Mengual R, Bonesso L, Beneteau M, Ricci JE, Desquiret-Dumas V, Procaccio V, Rotig A, Paquis-Flucklinger V (2013) Refractory epilepsy and mitochondrial dysfunction due to GM3 synthase deficiency. Eur J Hum Genet 21:528–534
53. Furukawa K, Hamamura K, Ohkawa Y, Ohmi Y, Furukawa K (2012) Disialyl gangliosides enhance tumor phenotypes with differential modalities. Glycoconj J 29:579–584
54. Furukawa K, Ohkawa Y, Matsumoto Y, Ohmi Y, Hashimoto N, Furukawa K (2016) Regulatory mechanisms of malignant properties of cancer cells with disialyl and monosialyl gangliosides. In: Furukawa K, Fukuda M (eds) Glycosignals in cancer: mechanisms of malignant phenotypes. Springer, Tokyo, pp 57–76
55. Gabius HJ (1997) Animal lectins. Eur J Biochem 243:543–576
56. Gabius H-J (1998) The how and why of protein–carbohydrate interaction: a primer to the theoretical concept and a guide to application in drug design. Pharm Res 15:23–30
57. Gabius HJ (2002) Animal lectins and life: a guided tour into the realm of the sugar code. Biochim Biophys Acta 1572:163–164
58. Gabius HJ (2009) Animal and human lectins. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 317–328
59. Gabius HJ (2015) The magic of the sugar code. Trends Biochem Sci 40:341
60. Gabius HJ, Kayser K (2014) Introduction to glycopathology: the concept, the tools and the perspectives. Diagn Pathol 9:4
61. Gabius H-J, Roth J (2017) An introduction to the sugar code. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1521-9
62. Gabius HJ, Wosgien B, Hendrys M, Bardosi A (1991) Lectin localization in human nerve by biochemically defined lectin-binding glycoproteins, neoglycoprotein and lectin-specific antibody. Histochemistry 95:269–277
63. Gabius HJ, André S, Kaltner H, Siebert HC (2002) The sugar code: functional lectinomics. Biochim Biophys Acta 1572:165–177
64. Gabius H-J, André S, Jiménez-Barbero J, Romero A, Solís D (2011) From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem Sci 36:298–313
65. Gabius HJ, Kaltner H, Kopitz J, André S (2015) The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci 40:360–376
66. Gabius HJ, Manning JC, Kopitz J, André S, Kaltner H (2016) Sweet complementarity: the functional pairing of glycans with lectins. Cell Mol Life Sci 73:1989–2016
67. García Caballero G, Kaltner H, Michalak M, Shilova N, Yegres M, André S, Ludwig AK, Manning JC, Schmidt S, Schnölzer M, Bovin NV, Reusch D, Kopitz J, Gabius HJ (2016) Chicken GRIFIN: a homodimeric member of the galectin network with canonical properties and a unique expression profile. Biochimie 128–129:34–47
68. Gebert J, Kloor M, Lee J, Lohr M, André S, Wagner R, Kopitz J, Gabius HJ (2012) Colonic carcinogenesis along different genetic routes: glycophenotyping of tumor cases separated by microsatellite instability/stability. Histochem Cell Biol 138:339–350
69. Goodfellow JA, Willison HJ (2016) Antiganglioside, antiganglioside-complex, and antiglycolipid-complex antibodies in immune-mediated neuropathies. Curr Opin Neurol 29:572–580
70. Grassi S, Prioni S, Cabitta L, Aureli M, Sonnino S, Prinetti A (2016) The role of 3-O-sulfogalactosylceramide, sulfatide, in the lateral organization of myelin membrane. Neurochem Res 41:130–143
71. 2+ channel complexes and EGFR signaling: novel targets to reduce tumor development by lipids? Biochim Biophys Acta 1848:2603–2620
72. Gupta G, Surolia A (2010) Glycosphingolipids in microdomain formation and their spatial organization. FEBS Lett 584:1634–1641
73. Hadaczek P, Wu G, Sharma N, Ciesielska A, Bankiewicz K, Davidow AL, Lu ZH, Forsayeth J, Ledeen RW (2015) GDNF signaling implemented by GM1 ganglioside: failure in Parkinson’s disease and GM1-deficient murine model. Exp Neurol 263:177–189
74. Hakomori SI (1998) Cancer-associated glycosphingolipid antigens: their structure, organization, and function. Acta Anat 161:79–90
75. Hakomori SI (2002) The glycosynapse. Proc Natl Acad Sci USA 99:225–232
76. Hakomori SI, Handa K (2016) Regulation of growth factor receptors by glycosphingolipids. In: Furukawa K, Fukuda M (eds) Glycosignals in cancer: mechanisms of malignant phenotypes. Springer, Tokyo, pp 77–94
77. Han X, McKeel DW, Kelley J, Morris JC (2002) Substantial sulfatide deficiency and ceramide elevation in very early Alzheimer’s disease: potential role in disease pathogenesis. J Neurochem 82:809–818
78. Harlalka GV, Lehman A, Chioza B, Baple EL, Maroofian R, Cross H, Sreekantan-Nair A, Priestman AD, Al-Turki S, McEntagart ME, Proukakis C, Royle L, Kozak RP, Bastaki L, Patton M, Wagner K, Coblentz R, Price J, Mezei M, Schlade-Bartusiak K, Platt FM, Hurles ME, Crosby AH (2013) Mutations in B4GALNT1 (GM2 synthase) underlie a new disorder of ganglioside biosynthesis. Brain 136:3618–3624
79. Helms JB, Zurzolo C (2004) Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic 5:247–254
80. Hennet T (2009) Diseases of glycosylation. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 365–384
81. Hennet T, Cabalzar J (2015) Congenital disorders of glycosylation: a concise chart of glycocalyx dysfunction. Trends Biochem Sci 40:377–384
82. Higuero AM, Díez-Revuelta N, Abad-Rodríguez J (2017) The sugar code in neuronal physiology. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1519-3
83. Hiraiwa N, Tsuyuoka K, Li YT, Tanaka M, Seno T, Okubo Y, Fukuda Y, Imura H, Kannagi R (1990) Gangliosides and sialoglycoproteins carrying a rare blood group antigen determinant, Cad, associated with human cancers as detected by specific monoclonal antibodies. Cancer Res 50:5497–5503
84. Holländer H (1963) A staining method for cerebroside-sulphuric esters in brain tissue. J Histochem Cytochem 11:112–118
85. Holzl G, Dormann P (2007) Structure and function of glycoglycerolipids in plants and bacteria. Prog Lipid Res 46:225–243
86. Honigmann A, Pralle A (2016) Compartmentalization of the cell membrane. J Mol Biol 428:4739
87. Horejsi V, Hrdinka M (2014) Membrane microdomains in immunoreceptor signaling. FEBS Lett 588:2392–2397
88. Hwang J, Lee S, Lee JT, Kwon TK, Kim DR, Kim H, Park HC, Suk K (2010) Gangliosides induce autophagic cell death in astrocytes. Br J Pharmacol 159:586–603
89. Iida N, Toida T, Kushi Y, Handa S, Fredman P, Svennerholm L, Ishizuka I (1989) A sulfated glucosylceramide from rat kidney. J Biol Chem 264:5974–5980
90. Ilyas AA, Quarles RH, Brady RO (1984) The monoclonal antibody HNK-1 reacts with a human peripheral nerve ganglioside. Biochem Biophys Res Commun 122:1206–1211
91. Ishizuka I (1997) Chemistry and functional distribution of sulfoglycolipids. Prog Lipid Res 36:245–319
92. Itokazu Y, Tsai YT, Yu RK (2016) Epigenetic regulation of ganglioside expression in neural stem cells and neuronal cells. Glycoconj J. doi:10.1007/s10719-016-9719-6
93. Jones M (2008) Lipids. In: Bancroft J, Gamble M (eds) Theory and practice of histological techniques. Elsevier, Amsterdam, pp 187–216
94. 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
95. Kaltner H, Gabius HJ (2012) A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol Histopathol 27:397–416
96. Kaltner H, Singh T, Manning JC, Raschta A-S, André S, Sinowatz F, Gabius H-J (2015) Network monitoring of adhesion/growth-regulatory galectins: localization of the five canonical chicken proteins in embryonic and maturing bone and cartilage and their introduction as histochemical tools. Anat Rec 298:2051–2070
97. Kaltner H, García Caballero G, Sinowatz F, Schmidt S, Manning JC, André S, Gabius HJ (2016) Galectin-related protein: an integral member of the network of chicken galectins. 2. From expression profiling to its immunocyto- and histochemical localization and application as tool for ligand detection. Biochim Biophys Acta 1860:2298–2312
98. Kaltner H, Toegel S, García Caballero G, Manning JC, Ledeen RW, Gabius HJ (2017) Galectins: their network and roles in immunity/tumor growth control. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1522-8
99. Kaneko T, Tsubakihara Y, Fushimi H, Yamaguchi S, Takabatake Y, Rakugi H, Kawakami H, Isaka Y (2015) Histochemical and immunoelectron microscopic analysis of ganglioside GM3 in human kidney. Clin Exp Nephrol 19:403–410
100. Karlsson KA (1989) Animal glycosphingolipids as membrane attachment sites for bacteria. Annu Rev Biochem 58:309–350
101. Kato K, Sasakawa H, Kamiya Y, Utsumi M, Nakano M, Takahashi N, Yamaguchi Y (2008) 920 MHz ultra-high field NMR approaches to structural glycobiology. Biochim Biophys Acta 1780:619–625
102. Katzenmaier EM, André S, Kopitz J, Gabius HJ (2014) Impact of sodium butyrate on the network of adhesion/growth-regulatory galectins in human colon cancer in vitro. Anticancer Res 34:5429–5438
103. Kawashima I, Tai T (1998) An immunocytochemical technique with monoclonal antibodies to glycosphingolipids in rat primary cerebellar cultures: influence of detergent permeabilization. Brain Res Protoc 2:299–305
104. Kawashima I, Ozawa H, Kotani M, Suzuki M, Kawano T, Gomibuchi M, Tai T (1993) Characterization of ganglioside expression in human melanoma cells: immunological and biochemical analysis. J Biochem 114:186–193
105. Kimata H, Yoshida A (1994) Differential effects of gangliosides on Ig production and proliferation by human B cells. Blood 84:1193–1200
106. Kopitz J (1997) Glycolipids: structure and function. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 163–180
107. Kopitz J (2009) Glycolipids. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 177–198
108. Kopitz J, von Reitzenstein C, Sinz K, Cantz M (1996) Selective ganglioside desialylation in the plasma membrane of human neuroblastoma cells. Glycobiology 6:367–376
109. Kopitz J, Mühl C, Ehemann V, Lehmann C, Cantz M (1997) Effects of cell surface ganglioside sialidase inhibition on growth control and differentiation of human neuroblastoma cells. Eur J Cell Biol 73:1–9
110. Kopitz J, Bergmann M, Gabius HJ (2010) How adhesion/growth-regulatory galectins-1 and -3 attain cell specificity: case study defining their target on neuroblastoma cells (SK-N-MC) and marked affinity regulation by affecting microdomain organization of the membrane. IUBMB Life 62:624–628
111. Kopitz J, von Reitzenstein C, Burchert M, Cantz M, Gabius HJ (1998) Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem 273:11205–11211
112. Kopitz J, von Reitzenstein C, André S, Kaltner H, Uhl J, Ehemann V, Cantz M, Gabius HJ (2001) Negative regulation of neuroblastoma cell growth by carbohydrate-dependent surface binding of galectin-1 and functional divergence from galectin-3. J Biol Chem 276:35917–35923
113. Kopitz J, André S, von Reitzenstein C, Versluis K, Kaltner H, Pieters RJ, Wasano K, Kuwabara I, Liu FT, Cantz M, Heck AJ, Gabius HJ (2003) Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene 18:6277–6288
114. Kopitz J, Ballikaya S, André S, Gabius HJ (2012) Ganglioside GM1/galectin-dependent growth regulation in human neuroblastoma cells: special properties of bivalent galectin-4 and significance of linker length for ligand selection. Neurochem Res 34:1267–1276
115. Kopitz J, Vértesy S, André S, Fiedler S, Schnölzer M, Gabius HJ (2014) Human chimera-type galectin-3: defining the critical tail length for high-affinity glycoprotein/cell surface binding and functional competition with galectin-1 in neuroblastoma cell growth regulation. Biochimie 104:90–99
116. Koscielak J, Miller-Podraza H, Krauze R, Piasek A (1976) Isolation and characterization of poly(glycosyl)ceramides (megaloglycolipids) with A, H and I blood-group activities. Eur J Biochem 71:9–18
117. Kotani M, Tai T (1997) An immunohistochemical technique with a series of monoclonal antibodies to gangliosides: their differential distribution in the rat cerebellum. Brain Res Brain Res Protoc 1:152–156
118. Kovacic N, Muthing J, Marusic A (2000) Immunohistological and flow cytometric analysis of glycosphingolipid expression in mouse lymphoid tissues. J Histochem Cytochem 48:1677–1690
119. Kozireski-Chuback D, Wu G, Ledeen RW (1999) Developmental appearance of nuclear GM1 in neurons of the central and peripheral nervous systems. Dev Brain Res 115:201–208
120. Kubo S, Hatano T, Hattori N (2015) Lipid rafts involvement in the pathogenesis of Parkinson’s disease. Front Biosci 20:263–279
121. Kusunoki S, Kaida K (2011) Antibodies against ganglioside complexes in Guillain–Barre syndrome and related disorders. J Neurochem 116:828–832
122. Lauc G, Heffer-Lauc M (2006) Shedding and uptake of gangliosides and glycosylphosphatidylinositol-anchored proteins. Biochim Biophys Acta 1760:584–602
123. Ledeen RW (1984) Biology of gangliosides: neuritogenic and neuronotrophic properties. J Neurosci Res 12:147–159
124. Ledeen RW (1987) The neuritogenic effect of gangliosides in cell cultures. In: Rahmann H (ed) Gangliosides and modulation of neuronal functions. Springer, Berlin, pp 491–500
125. Ledeen RW (1989) Biosynthesis, metabolism, and biological effects of gangliosides. In: Margolis RK, Margolis RU (eds) Neurobiology of glycoconjugates. Plenum Press, New York, pp 43–83
126. Ledeen RW, Wu G (2009) Neurobiology meets glycosciences. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 495–516
127. Ledeen RW, Wu G (2011) New findings on nuclear gangliosides: overview on metabolism and function. J Neurochem 116:714–720
128. Ledeen RW, Wu G (2015) The multi-tasked life of GM1 ganglioside, a true factotum of nature. Trends Biochem Sci 40:407–418
129. Ledeen RW, Yu RK (1982) Gangliosides: structure, isolation, and analysis. Methods Enzymol 83:139–191
130. Ledeen RW, Wu G, André Bleich D, Huet G, Kaltner H, Kopitz J, Gabius HJ (2012) Beyond glycoproteins as galectin counterreceptors: tumor-effector T cell growth control via ganglioside GM1. Ann N Y Acad Sci 1253:206–221
131. Legros N, S. Dusny S, Humpf HU, Pohlentz G, H. Karch H, Müthing J (2016) Shiga toxin glycosphingolipid receptors and their lipid membrane ensemble in primary human blood-brain barrier endothelial cells. Glycobiology. doi:10.1093/glycob/cww090
132. Levental I, Veatch SL (2016) The continuing mystery of lipid rafts. J Mol Biol. doi:10.1016/j.jmb.2016.08.022
133. Levery SB (2005) Glycosphingolipid structural analysis and glycosphingolipidomics. Methods Enzymol 405:300–369
134. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50
135. Lode HN, Schmidt M, Seidel D, Huebener N, Brackrock D, Bleeke M, Reker D, Brandt S, Mueller HP, Helm C, Siebert N (2013) Vaccination with anti-idiotype antibody ganglidiomab mediates a GD2-specific anti-neuroblastoma immune response. Cancer Immunol Immunother 62:999–1010
136. Lohr M, Kaltner H, Schwartz-Albiez R, Sinowatz F, Gabius HJ (2010) Towards functional glycomics by lectin histochemistry: strategic probe selection to monitor core and branch-end substitutions and detection of cell-type and regional selectivity in adult mouse testis and epididymis. Anat Histol Embryol 39:481–493
137. Ludwig AK, Vértesy S, Michalak M, Manning JC, André S, Kübler D, Kopitz J, Kaltner H, Gabius HJ (2016) Playing modular puzzle with adhesion/growth-regulatory galectins: design and testing of a hybrid to unravel structure–activity relationships. Protein Pept Lett 23:1003–1012
138. Maccioni HJ, Giraudo CG, Daniotti JL (2002) Understanding the stepwise synthesis of glycolipids. Neurochem Res 27:629–636
139. Majewski J, André S, Jones E, Chi E, Gabius HJ (2015) X-ray reflectivity and grazing incidence diffraction studies of interaction between human adhesion/growth-regulatory galectin-1 and DPPE-GM1 lipid monolayer at an air/water interface. Biochemistry (Moscow) 80:943–956
140. Manning JC, Romero A, Habermann F, García Caballero G, Kaltner H, Gabius HJ (2017) Lectins: a primer for histochemists and cell biologists. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1524-6
141. Marcus J, Popko B (2002) Galactolipids are molecular determinants of myelin development and axo-glial organization. Biochim Biophys Acta 1573:406–413
142. Martinez Z, Zhu M, Han S, Fink AL (2007) GM1 specifically interacts with α-synuclein and inhibits fibrillation. Biochemistry 46:1868–1877
143. Matarrese P, Garofalo T, Manganelli V, Gambardella L, Marconi M, Grasso M, Tinari A, Misasi R, Malorni W, Sorice M (2014) Evidence for the involvement of GD3 ganglioside in autophagosome formation and maturation. Autophagy 10:750–765
144. Matrosovich M, Herrler G, Klenk HD (2015) Sialic acid receptors of viruses. Top Curr Chem 367:1–28
145. Mayer S, Raulf MK, Lepenies B (2017) C-type lectins: their network and roles in immunity/pathogen recognition. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1523-7
146. Merrill AH Jr (2011) Sphingolipid and glycosphingolipid metabolic pathways in the era of sphingolipidomics. Chem Rev 111:6387–6422
147. Merrill AH Jr, Sullards MC, Allegood JC, Kelly S, Wang E (2005) Sphingolipidomics: high-throughput, structure-specific, and quantitative analysis of sphingolipids by liquid chromatography tandem mass spectrometry. Methods 36:207–224
148. Miura R, Ethell IM, Yamaguchi Y (2001) Carbohydrate-protein interactions between HNK-1-reactive sulfoglucuronyl glycolipids and the proteoglycan lectin domain mediate neuronal cell adhesion and neurite outgrowth. J Neurochem 76:413–424
149. Miyagi T, Takahashi K, Shiozaki K, Yamaguchi K, Hosono M (2015) Plasma membrane-associated sialidase confers cancer initiation, promotion and progression. Adv Exp Med Biol 842:139–145
150. Miyake M, Hashimoto K, Ito M, Ogawa O, Arai E, Hitomi S, Kannagi R (1990) The abnormal occurrence and the differentiation-dependent distribution of N-acetyl and N-glycolyl species of the ganglioside GM2 in human germ cell tumors. A study with specific monoclonal antibodies. Cancer 65:499–505
151. Morales A, Colell A, Mari M, Garcia-Ruiz C, Fernandez-Checa JC (2004) Glycosphingolipids and mitochondria: role in apoptosis and disease. Glycoconj J 20:579–588
152. Muanprasat C, Chatsudthipong V (2013) Cholera: pathophysiology and emerging therapeutic targets. Future Med Chem 5:781–798
153. Murphy PV, André S, Gabius H-J (2013) The third dimension of reading the sugar code by lectins: design of glycoclusters with cyclic scaffolds as tools with the aim to define correlations between spatial presentation and activity. Molecules 18:4026–4053
154. Müthing J (1996) High-resolution thin-layer chromatography of gangliosides. J Chromatogr A 720:3–25
155. Müthing J (2000) Analyses of glycosphingolipids by high-performance liquid chromatography. Methods Enzymol 312:45–64
156. Nadiri A, Polyak MJ, Jundi M, Alturaihi H, Reyes-Moreno C, Hassan GS, Mourad W (2011) CD40 translocation to lipid rafts: signaling requirements and downstream biological events. Eur J Immunol 41:2358–2367
157. Navid F, Sondel PM, Barfield R, Shulkin BL, Kaufman RA, Allay JA, Gan J, Hutson P, Seo S, Kim K, Goldberg J, Hank JA, Billups CA, Wu J, Furman WL, McGregor LM, Otto M, Gillies SD, Handgretinger R, Santana VM (2014) Phase I trial of a novel anti-GD2 monoclonal antibody, Hu14.18K322A, designed to decrease toxicity in children with refractory or recurrent neuroblastoma. J Clin Oncol 32:1445–1452
158. Nowycky MC, Wu G, Ledeen RW (2014) Glycobiology of ion transport in the nervous system. Adv Neurobiol 9:321–342
159. Patsos G, Corfield A (2009) O-Glycosylation: structural diversity and functions. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 111–138
160. Patsos G, André S, Roeckel N, Gromes R, Gebert J, Kopitz J, Gabius HJ (2009) Compensation of loss of protein function in microsatellite-unstable colon cancer cells (HCT116): a gene-dependent effect on the cell surface glycan profile. Glycobiology 19:726–734
161. Paulick MG, Bertozzi CR (2008) The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47:6991–7000
162. Peguet-Navarro J, Sportouch M, Popa I, Berthier O, Schmitt D, Portoukalian J (2003) Gangliosides from human melanoma tumors impair dendritic cell differentiation from monocytes and induce their apoptosis. J Immunol 170:3488–3494
163. Percec V, Leowanawat P, Sun HJ, Kulikov O, Nusbaum CD, Tran TM, Bertin A, Wilson DA, Peterca M, Zhang S, Kamat NP, Vargo K, Moock D, Johnston ED, Hammer DA, Pochan DJ, Chen Y, Chabre YM, Shiao TC, Bergeron-Brlek M, André S, Roy R, Gabius HJ, Heiney PA (2013) Modular synthesis of amphiphilic Janus glycodendrimers and their self-assembly into glycodendrimersomes and other complex architectures with bioactivity to biomedically relevant lectins. J Am Chem Soc 135:9055–9077
164. Platt FM (2014) Sphingolipid lysosomal storage disorders. Nature 510:68–75
165. Platt FM, Jeyakumar M (2008) Substrate reduction therapy. Acta Paediatr 97:88–93
166. Prinetti A, Loberto N, Chigorno V, Sonnino S (2009) Glycosphingolipid behaviour in complex membranes. Biochim Biophys Acta 1788:184–193
167. Regina-Todeschini A, Hakomori SI (2008) Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim Biophys Acta 1780:421–433
168. Reuter G, Gabius HJ (1996) Sialic acids structure: analysis-metabolism-occurrence-recognition. Biol Chem Hoppe Seyler 377:325–342
169. Reuter G, Gabius HJ (1999) Eukaryotic glycosylation: whim of nature or multipurpose tool? Cell Mol Life Sci 55:368–422
170. Reutter W, Stäsche S, Stehling P, Baum O (1997) The biology of sialic acids: insight into their structure, metabolism and function in particular during viral infection. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 245–260
171. Roots BI (1995) Locating lipids in the CNS: an historical perspective. Neurochem Res 20:1261–1268
172. Roth J (1983) Application of lectin: gold complexes for electron microscopic localization of glycoconjugates on thin sections. J Histochem Cytochem 31:987–999
173. Roth J (1993) Cellular sialoglycoconjugates: a histochemical perspective. Histochem J 25:687–710
174. Roth J (1996) Protein glycosylation in the endoplasmic reticulum and the Golgi apparatus and cell-type specificity of cell surface glycoconjugate expression: analysis by protein A-gold and lectin-gold techniques. Histochem Cell Biol 106:79–92
175. Roth J (2011) Lectins for histochemical demonstration of glycans. Histochem Cell Biol 136:117–130
176. Roth J, Zuber C (2017) Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1513-9
177. Roy R, Murphy PV, Gabius HJ (2016) Multivalent carbohydrate-lectin interactions: how synthetic chemistry enables insights into nanometric recognition. Molecules 21:629
178. Roy R, Cao Y, Kaltner H, Kottari N, Shiao TC, Belkhadem K, André S, Manning JC, Murphy PV, Gabius HJ (2017) Teaming up synthetic chemistry and histochemistry for activity screening in galectin-directed inhibitor design. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1525-5
179. Rüdiger H (1997) Structure and functions of plant lectins. In: Gabius HJ, Gabius S (eds) Glycosciences: status and perspectives. Chapman & Hall, Weinheim, pp 415–438
180. Rüdiger H, Gabius HJ (2001) Plant lectins: occurrence, biochemistry, functions and applications. Glycoconj J 18:589–613
181. Rüdiger H, Gabius HJ (2009) The biochemical basis and coding capacity of the sugar code. In: Gabius HJ (ed) the sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 3–14
182. Ruiz FM, Scholz BA, Buzamet E, Kopitz J, André S, Menendez M, Romero A, Solis D, Gabius HJ (2014) Natural single amino acid polymorphism (F19Y) in human galectin-8: detection of structural alterations and increased growth-regulatory activity on tumor cells. FEBS J 281:1446–1464
183. Saito T, Hakomori SI (1971) Quantitative isolation of total glycosphingolipids from animal cells. J Lipid Res 12:257–259
184. INK4a: downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J 277:3552–3563
185. Sandhoff K, Kolter T (2003) Biosynthesis and degradation of mammalian glycosphingolipids. Philos Trans R Soc Lond B 358:847–861
186. Sangiorgio V, Pitto M, Palestini P, Masserini M (2004) GPI-anchored proteins and lipid rafts. Ital J Biochem 53:98–111
187. Schengrund CL (2015) Gangliosides: glycosphingolipids essential for normal neural development and function. Trends Biochem Sci 40:397–406
188. Schnaar RL (2016) Gangliosides of the vertebrate nervous system. J Mol Biol 428:3325–3336
189. Schnaar RL, Needham LK (1994) Thin-layer chromatography of glycosphingolipids. Methods Enzymol 230:371–389
190. Schneider JS, Pope A, Simpson K, Taggart J, Smith MG, DiStefano L (1992) Recovery from experimental parkinsonism in primates with GM1 ganglioside treatment. Science 256:843–846
191. Schuette CG, Pierstorff B, Huettler S, Sandhoff K (2001) Sphingolipid activator proteins: proteins with complex functions in lipid degradation and skin biogenesis. Glycobiology 11:81R–90R
192. Schuller S (2011) Shiga toxin interaction with human intestinal epithelium. Toxins 3:626–639
193. Shams-Eldin H, Debierre-Grockiego F, Schwarz R (2009) Glycosylphosphatidylinositol anchors: structure, biosynthesis and functions. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 155–176
194. Shen W, Stone K, Jales A, Leitenberg D, Ladisch S (2008) Inhibition of TLR activation and up-regulation of IL-1R-associated kinase-M expression by exogenous gangliosides. J Immunol 180:4425–4432
195. Siebert HC, Jimenez-Barbero J, André S, Kaltner H, Gabius HJ (2003a) Describing topology of bound ligand by transferred nuclear Overhauser effect spectroscopy and molecular modeling. Methods Enzymol 362:417–434
196. Siebert HC, André S, Lu SY, Frank M, Kaltner H, van Kuik JA, Korchagina EY, Bovin N, Tajkhorshid E, Kaptein R, Vliegenthart JF, von der Lieth CW, Jiménez-Barbero J, Kopitz J, Gabius HJ (2003b) Unique conformer selection of human growth-regulatory lectin galectin-1 for ganglioside GM1 versus bacterial toxins. Biochemistry 42:14762–14773
197. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39
198. Simpson MA, Cross H, Proukakis C, Priestman DA, Neville DC, Reinkensmeier G, Wang H, Wiznitzer M, Gurtz K, Verganelaki A, Pryde A, Patton MA, Dwek RA, Butters TD, Platt FM, Crosby AH (2004) Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet 36:1225–1229
199. Skipski VP (1975) Thin-layer chromatography of neutral glycosphingolipids. Methods Enzymol 35:396–425
200. Solís D, Bovin NV, Davis AP, Jiménez-Barbero J, Romero A, Roy R, Smetana K Jr, Gabius H-J (2015) A guide into glycosciences: how chemistry, biochemistry and biology cooperate to crack the sugar code. Biochim Biophys Acta 1850:186–235
201. Spessott W, Crespo PM, Daniotti JL, Maccioni HJ (2012) Glycosyltransferase complexes improve glycolipid synthesis. FEBS Lett 586:2346–2350
202. Spicer SS, Schulte BA (1992) Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochem Cytochem 40:1–38
203. Stechly L, Morelle W, Dessein AF, André S, Grard G, Trinel D, Dejonghe MJ, Leteurtre E, Drobecq H, Trugnan G, Gabius HJ, Huet G (2009) Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10:438–450
204. Sullards MC, Allegood JC, Kelly S, Wang E, Haynes CA, Park H, Chen Y, Merrill AH Jr (2007) Structure-specific, quantitative methods for analysis of sphingolipids by liquid chromatography-tandem mass spectrometry: inside-out sphingolipidomics. Methods Enzymol 432:83–115
205. Surma MA, Klose C, Simons K (2012) Lipid-dependent protein sorting at the trans-Golgi network. Biochim Biophys Acta 1821:1059–1067
206. Suzuki KG (2015) New insights into the organization of plasma membrane and its role in signal transduction. Int Rev Cell Mol Biol 317:67–96
207. Suzuki M, Cheung NK (2015) Disialoganglioside GD2 as a therapeutic target for human diseases. Expert Opin Ther Targets 19:349–362
208. Suzuki K, Katzman R, Korey SR (1965) Chemical studies on Alzheimer’s disease. J Neuropathol Exp Neurol 24:211–224
209. Svennerholm L (1956) The quantitative estimation of cerebrosides in nervous tissue. J Neurochem 1:42–53
210. Svennerholm L (1957) Quantitative estimation of sialic acids. II. A colorimetric resorcinol-hydrochloric acid method. Biochim Biophys Acta 24:604–611
211. Tettamanti R, Anastasia L (2009) Chemistry, tissue and cellular distribution and developmental profiles of neural glycolipids. In: Tettamanti R, Goracci G (eds) Handbook of neurochemistry and molecular neurobiology: neural lipids. Springer, New York, pp 100–169
212. Thaxton C, Bhat M (2009) Myelination and regional domain differentiation of the axon. In: König E (ed) Cell biology of the axon. Springer, Heidelberg, pp 1–28
213. Tidhar R, Futerman AH (2013) The complexity of sphingolipid biosynthesis in the endoplasmic reticulum. Biochim Biophys Acta 1833:2511–2518
214. Toegel S, Bieder D, André S, Kayser K, Walzer SM, Hobusch G, Windhager R, Gabius HJ (2014) Human osteoarthritic knee cartilage: fingerprinting of adhesion/growth-regulatory galectins in vitro and in situ indicates differential upregulation in severe degeneration. Histochem Cell Biol 142:373–388
215. Toegel S, Weinmann D, André S, Walzer SM, Bilban M, Schmidt S, Chiari C, Windhager R, Krall C, Bennani-Baiti IM, Gabius H-J (2016) Galectin-1 couples glycobiology to inflammation in osteoarthritis through the activation of an NF-κB-regulated gene network. J Immunol 196:1910–1921
216. Tsai Y, Itokazu Y, Yu RK (2016) GM1 Ganglioside is involved in epigenetic activation loci of neuronal cells. Neurochem Res 41:107–115
217. Ullman MD, McCluer RH (1987) High-pressure liquid chromatography analysis of neutral glycosphingolipids: perbenzoylated mono-, di-, tri-, and tetraglycosylceramides. Methods Enzymol 138:117–125
218. Valentino L, Moss T, Olson E, Wang HJ, Elashoff R, Ladisch S (1990) Shed tumor gangliosides and progression of human neuroblastoma. Blood 75:1564–1567
219. van Echten-Deckert G (2000) Sphingolipid extraction and analysis by thin-layer chromatography. Methods Enzymol 312:64–79
220. van Echten-Deckert G, Walter J (2012) Sphingolipids: critical players in Alzheimer’s disease. Prog Lipid Res 51:378–393
221. Vartabedian VF, Savage PB, Teyton L (2016) The processing and presentation of lipids and glycolipids to the immune system. Immunol Rev 272:109–119
222. Velasco S, Díez-Revuelta N, Hernández-Iglesias T, Kaltner H, André S, Gabius HJ, Abad-Rodríguez J (2013) Neuronal Galectin-4 is required for axon growth and for the organization of axonal membrane L1 delivery and clustering. J Neurochem 125:49–62
223. Wang J, Lu ZH, Gabius HJ, Rohowsky-Kochan C, Ledeen RW, Wu G (2009) Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: possible role in suppressing experimental autoimmune encephalomyelitis. J Immunol 182:4036–4045
224. Wiegandt H (1992) Insect glycolipids. Biochim Biophys Acta 1123:117–126
225. Wilson IBH, Paschinger K, Rendic D (2009) Glycosylation of model and ‘lower’ organisms. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 139–154
226. Wondimu A, Liu Y, Su Y, Bobb D, Ma JS, Chakrabarti L, Radoja S, Ladisch S (2014) Gangliosides drive the tumor infiltration and function of myeloid-derived suppressor cells. Cancer Res 74:5449–5457
227. Wu G, Lu ZH, Obukhov AG, Nowycky MC, Ledeen RW (2007) Induction of calcium influx through TRPC5 channels by cross-linking of GM1 ganglioside associated with α5β1 integrin initiates neurite outgrowth. J Neurosci 27:7447–7458
228. Wu G, Lu ZH, Gabius HJ, Ledeen RW, Bleich D (2011) Ganglioside GM1 deficiency in effector T cells from NOD mice induces resistance to regulatory T-cell suppression. Diabetes 60:2341–2349
229. Wu G, Lu ZH, Kulkarni N, Ledeen RW (2012) Deficiency of ganglioside GM1 correlates with Parkinson’s disease in mice and humans. J Neurosci Res 90:1997–2008
230. 2+ influx. J Neurochem 136:550–563
231. Xiao Q, Zhang S, Wang Z, Sherman SE, Moussodia RO, Peterca M, Muncan A, Williams DR, Hammer DA, Vertésy S, André S, Gabius HJ, Klein ML, Percec V (2016) Onion-like glycodendrimersomes from sequence-defined Janus glycodendrimers and influence of architecture on reactivity to a lectin. Proc Natl Acad Sci USA 113:1162–1167
232. Yanagisawa K (2015) GM1 ganglioside and Alzheimer’s disease. Glycoconj J 32(3–4):87–91
233. Yu RK, Nakatani Y, Yanagisawa M (2009) The role of glycosphingolipid metabolism in the developing brain. J Lipid Res 50(Suppl):S440–S445
234. Yu RK, Tsai YT, Ariga T (2012) Functional roles of gangliosides in neurodevelopment: an overview of recent advances. Neurochem Res 37:1230–1244
235. Yuki N, Susuki K, Koga M, Nishimoto Y, Odaka M, Hirata K, Taguchi K, Miyatake T, Furukawa K, Kobata T, Yamada M (2004) Carbohydrate mimicry between human ganglioside GM1 and Campylobacter jejuni lipooligosaccharide causes Guillain–Barré syndrome. Proc Natl Acad Sci USA 101:11404–11409
236. Zeytin HE, Tripathi PK, Bhattacharya-Chatterjee M, Foon KA, Chatterjee SK (2000) Construction and characterization of DNA vaccines encoding the single-chain variable fragment of the anti-idiotype antibody 1A7 mimicking the tumor-associated antigen disialoganglioside GD2. Cancer Gene Ther 7:1426–1436
237. Zhang S, Moussodia RO, Murzeau C, Sun HJ, Klein ML, Vertésy S, André S, Roy R, Gabius HJ, Percec V (2015) Dissecting molecular aspects of cell interactions using glycodendrimersomes with programmable glycan presentation and engineered human lectins. Angew Chem Int Ed Engl 54:4036–4040
238. Zuber C, Roth J (2009) N-Glycosylation. In: Gabius HJ (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 87–110