Structures, biosynthesis, and functions of gangliosides-an overview

Journal of Oleo Science

Volumn 60, Issue 10, 2011, Pages 537-544

  Yu, Robert K ^a   Tsai, Yi Tzang ^a   Ariga, Toshio ^a   Yanagisawa, Makoto ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Glycosphingolipid; Glycosyltransferase; Knockout mouse; Neural stem cell; Stem cell

Indexed keywords

CARBOHYDRATE CHAINS; CELL SURFACES; EXPRESSION LEVELS; GLYCOSPHINGOLIPIDS; GLYCOSYLTRANSFERASE; INTEGRAL COMPONENTS; KNOCKOUT MOUSE; MICRO-DOMAINS; NEURAL STEM CELL; SPHINGOMYELIN; STRUCTURAL COMPLEXITY;

ADHESION; BIOCHEMISTRY; CARBOHYDRATES; CARBOXYLIC ACIDS; CELL MEMBRANES; PHOSPHOLIPIDS; SIGNAL TRANSDUCTION;

STEM CELLS;

GANGLIOSIDE;

ANIMAL; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; HUMAN; METABOLISM; REVIEW;

ANIMALS; CARBOHYDRATE CONFORMATION; GANGLIOSIDES; HUMANS;

EID: 80053060999     PISSN: 13458957     EISSN: 13473352     Source Type: Journal    
DOI: 10.5650/jos.60.537     Document Type: Review

References (55)

1. Yu, R. K.; Yanagisawa, M.; Ariga, T. Glycosphingolipid structures. in Comprehensive Glycoscienc (Kamer-ling, J. P. ed.) Elsevier. Oxford, UK, pp.73-12 (2007).
2. Nakamura, K.; Inagaki, F.; Tamai, Y. A novel ganglio-side in dogfish brain. Occurrence of a trisialoganglio- side with a sialic acid linked to N-acetylgalactosamine. J. Biol. Chem. 263, 9896-990 (1988).
3. Maccioni, H. J. Glycosylation of glycolipids in the Golgi complex. J. Neurochem. 103 Suppl 1, 81-9 (2007).
4. Ngamukote, S.; Yanagisawa, M.; Ariga, T.; Ando, S.; Yu, R. K. Developmental changes of glycosphingolipids and expression of glycogenes in mouse brains. J. Neu- rochem. 103, 2327-234 (2007).
5. Yu, R. K.; Macala, L. J.; Taki, T.; Weinfield, H. M.; Yu, F.S. Developmental changes in ganglioside composition and synthesis in embryonic rat brain. J. Neurochem. 50, 1825-182 (1988).
6. Ishii, A.; Ikeda, T.; Hitoshi, S.; Fujimoto, I.; Torii, T.; Sakuma, K.; Nakakita, S.; Hase, S.; Ikenaka, K. Devel- opmental changes in the expression of glycogenes and the content of N-glycans in the mouse cerebral cortex. Glycobiology 17, 261-27 (2007).
7. Yu, R. K.; Ariga, T.; Yanagisawa, M.; Zeng, G. Ganglio-sides in the nervous system: Biosynthesis and degra-dation. in Glycoscienc (Fraser-Reid, B.; Tatsuka, K.; Thiem, J. ed.) Springer-Verlag. Berlin-Heiderberg, Ger-many. pp.1671-169 (2008).
8. Suzuki, Y.; Yanagisawa, M.; Ariga, T.; Yu, R. K. Histone acetylation-mediated glycosyltransferase gene regula-tion in mouse brain during development. J. Neuro-chem. 116, 874-88 (2011).
9. Yu, R. K.; Nakatani, Y.; Yanagisawa, M. The role of gly-cosphingolipid metabolism in the developing brain. J. Lipid Res. 50 Suppl, S440-44 (2009).
10. Anderson, R. G. The caveolae membrane system. Ann. Rev. Biochem. 67, 199-22 (1998).
11. Simons, K.; Toomre, D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-3 (2000).
12. Hakomori, S.; Handa, K.; Iwabuchi, K.; Yamamura, S.; Prinetti, A. New insights in glycosphingolipid function: glycosignaling domain, a cell surface assembly of gly-cosphingolipids with signal transducer molecules, in-volved in cell adhesion coupled with signaling. Glyco-biology 8, xi-xi (1998).
13. Ledeen, R. W.; Wu, G. Nuclear sphingolipids: metabolism and signaling. J. Lipid Res. 49, 1176-118 (2008).
14. Yoshikawa, M.; Go, S.; Takasaki, K.; Kakazu, Y.; Ohashi, M.; Nagafuku, M.; Kabayama, K.; Sekimoto, J.; Suzuki, S.; Takaiwa, K.; Kimitsuki, T.; Matsumoto, N.; Komune, S.; Kamei, D.; Saito, M.; Fujiwara, M.; Iwasaki, K.; In-okuchi, J. Mice lacking ganglioside GM3 synthase ex-hibit complete hearing loss due to selective degenera-tion of the organ of Corti. Proc. Natl. Acad. Sci. USA 106, 9483-948 (2009).
15. Niimi, K.; Nishioka, C.; Miyamoto, T.; Takahashi, E.; Miyoshi, I.; Itakura, C.; Yamashita, T. Impairment of neuropsychological behaviors in ganglioside GM3-knockout mice. Biochem. Biophys. Res. Commun. 406, 524-52 (2011).
16. Okada, M.; Itoh Mi, M.; Haraguchi, M.; Okajima, T.; In-oue, M.; Oishi, H.; Matsuda, Y.; Iwamoto, T.; Kawano, T.; Fukumoto, S.; Miyazaki, H.; Furukawa, K.; Aizawa, S. b-series Ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apoptosis but impairs regeneration of the le-sioned hypoglossal nerve. J. Biol. Chem. 277, 1633-163 (2002).
17. Takamiya, K.; Yamamoto, A.; Furukawa, K.; Yamashiro, S.; Shin, M.; Okada, M.; Fukumoto, S.; Haraguchi, M.; Takeda, N.; Fujimura, K.; Sakae, M.; Kishikawa, M.; Shiku, H.; Aizawa, S. Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system. Proc. Natl. Acad. Sci. USA 93, 10662-1066 (1996).
18. Chiavegatto, S.; Sun, J.; Nelson, R.J.; Schnaar, R.L. A functional role for complex gangliosides: motor deficits in GM2/GD2 synthase knockout mice. Exp. Neu-rol. 166, 227-23 (2000).
19. Sheikh, K. A.; Sun, J.; Liu, Y.; Kawai, H.; Crawford, T. O.; Proia, R. L.; Griffin, J. W.; Schnaar, R. L. Mice lacking complex gangliosides develop Wallerian degeneration and myelination defects. Proc. Natl. Acad. Sci. USA 96, 7532-753 (1999).
20. Sugiura, Y.; Furukawa, K.; Tajima, O.; Mii, S.; Honda, T. Sensory nerve-dominant nerve degeneration and re-modeling in the mutant mice lacking complex ganglio-sides. Neuroscience 135, 1167-117 (2005).
21. Tajima, O.; Egashira, N.; Ohmi, Y.; Fukue, Y.; Mishima, K.; Iwasaki, K.; Fujiwara, M.; Inokuchi, J.; Sugiura, Y.; Furukawa, K. Reduced motor and sensory functions and emotional response in GM3-only mice: emergence from early stage of life and exacerbation with aging. Behav. Brain Res. 198, 74-8 (2009).
22. Tajima, O.; Egashira, N.; Ohmi, Y.; Fukue, Y.; Mishima, K.; Iwasaki, K.; Fujiwara, M.; Sugiura, Y.; Furukawa, K. Dysfunction of muscarinic acetylcholine receptors as a substantial basis for progressive neurological deterio-ration in GM3-only mice. Behav. Brain Res. 206, 101-10 (2010).
23. Ohmi, Y.; Tajima, O.; Ohkawa, Y.; Yamauchi, Y.; Sugiura, Y.; Furukawa, K. Gangliosides are essential in the pro-tection of inflammation and neurodegeneration via maintenance of lipid rafts: elucidation by a series of ganglioside-deficient mutant mice. J. Neurochem. 116, 926-93 (2011).
24. Ohmi, Y.; Tajima, O.; Ohkawa, Y.; Mori, A.; Sugiura, Y.; Furukawa, K. Gangliosides play pivotal roles in the regulation of complement systems and in the mainte-nance of integrity in nerve tissues. Proc. Natl. Acad. Sci. USA 106, 22405-2241 (2009).
25. Kawai, H.; Allende, M. L.; Wada, R.; Kono, M.; Sango, K.; Deng, C.; Miyakawa, T.; Crawley, J. N.; Werth, N.; Bier-freund, U.; Sandhoff, K.; Proia, R. L. Mice expressing only monosialoganglioside GM3 exhibit lethal audio-genic seizures. J. Biol. Chem. 276, 6885-688 (2001).
26. Yamashita, T.; Wu, Y. P.; Sandhoff, R.; Werth, N.; Mizu-kami, H.; Ellis, J. M.; Dupree, J. L.; Geyer, R.; Sandhoff, K.; Proia, R. L. Interruption of ganglioside synthesis produces central nervous system degeneration and al-tered axon-glial interactions. Proc. Natl. Acad. Sci. USA 102, 2725-273 (2005).
27. Yanagisawa, M. Stem cell glycolipids. Neurochem. Res. (2011) in press.
28. Yu, R. K.; Suzuki, Y.; Yanagisawa, M. Membrane glyco-lipids in stem cells. FEBS Lett. 584, 1694-169 (2010).
29. Kannagi, R.; Cochran, N. A.; Ishigami, F.; Hakomori, S.; Andrews, P. W.; Knowles, B. B.; Solter, D. Stage-specif-ic embryonic antigen (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J. 2, 2355-236 (1983).
30. Thomson, J. A.; Itskovitz-Eldor, J.; Shapiro, S. S.; Waknitz, M. A.; Swiergiel, J. J.; Marshall, V. S.; Jones, J. M. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-114 (1998).
31. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichi-saka, T.; Tomoda, K.; Yamanaka, S. Induction of plurip-otent stem cells from adult human fibroblasts by de-fined factors. Cell 131, 861-87 (2007).
32. Yu, J.; Vodyanik, M. A.; Smuga-Otto, K.; Antosiewicz-Bourget, J.; Frane, J. L.; Tian, S.; Nie, J.; Jonsdottir, G. A.; Ruotti, V.; Stewart, R.; Slukvin, II; Thomson, J. A. Induced pluripotent stem cell lines derived from hu-man somatic cells. Science 318, 1917-192 (2007).
33. Nakatani, Y.; Yanagisawa, M.; Suzuki, Y.; Yu, R.K. Char-acterization of GD3 ganglioside as a novel biomarker of mouse neural stem cells. Glycobiology 20, 78-86 (2010).
34. Yanagisawa, M.; Yoshimura, S.; Yu, R. K. Expression of GD2 and GD3 gangliosides in human embryonic neural stem cells. ASN Neuro. 3, e0005 (2011).
35. Martinez, C.; Hofmann, T. J.; Marino, R.; Dominici, M.; Horwitz, E. M. Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood 109, 4245-424 (2007).
36. Gang, E. J.; Bosnakovski, D.; Figueiredo, C. A.; Visser, J. W.; Perlingeiro, R. C. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 109, 1743-1751 (2007).
37. Ogden, A. T.; Waziri, A. E.; Lochhead, R. A.; Fusco, D.; Lopez, K.; Ellis, J. A.; Kang, J.; Assanah, M.; McKhann, G. M.; Sisti, M. B.; McCormick, P. C.; Canoll, P.; Bruce, J. N. Identification of A2B5+CD133- tumor-initiating cells in adult human gliomas. Neurosurgery 62, 505-51 (2008).
38. Tchoghandjian, A.; Baeza, N.; Colin, C.; Cayre, M.; Me-tellus, P.; Beclin, C.; Ouafik, L.; Figarella-Branger, D. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol. 20, 211-22 (2010).
39. Kaida, K.; Ariga, T.; Yu, R.K. Antiganglioside antibod-ies and their pathophysiological effects on Guillain-Barre syndrome and related disorders-a review. Gly-cobiology 19, 676-69 (2009).
40. Suzuki, Y. Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull. 28, 399-40 (2005).
41. Simpson, M. A.; Cross, H.; Proukakis, C.; Priestman, D. A.; Neville, D. C.; Reinkensmeier, G.; Wang, H.; Wiz-nitzer, M.; Gurtz, K.; Verganelaki, A.; Pryde, A.; Patton, M. A.; Dwek, R. A.; Butters, T. D.; Platt, F. M.; Crosby, A.H. Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat. Genet. 36, 1225-122 (2004).
42. Inokuchi, J. Membrane microdomains and insulin resistance. FEBS Lett. 584, 1864-187 (2010).
43. Bernardo, A.; Harrison, F. E.; McCord, M.; Zhao, J.; Bruchey, A.; Davies, S. S.; Jackson Roberts, L., 2nd; Mathews, P. M.; Matsuoka, Y.; Ariga, T.; Yu, R.K.; Thompson, R.; McDonald, M. P. Elimination of GD3 synthase improves memory and reduces amyloid-beta plaque load in transgenic mice. Neurobiol. Aging 30, 1777-179 (2009).
44. Matsuzaki, K.; Kato, K.; Yanagisawa, K. Aß polymeriza-tion through interaction with membrane gangliosides. Biochim. Biophys. Acta 1801, 868-87 (2010).
45. Ando, S.; Hirabayashi, Y.; Kon, K.; Inagaki, F.; Tate, S.; Whittaker, V. P. A trisialoganglioside containing a sialyl alpha 2-6 N-acetylgalactosamine residue is a choliner-gic-specific antigen, Chol-1 alpha. J. Biochem (To-kyo) 111, 287-29 (1992).
46. Hirabayashi, Y.; Nakao, T.; Irie, F.; Whittaker, V. P.; Kon, K.; Ando, S. Structural characterization of a novel cholinergic neuron-specific ganglioside in bovine brain. J. Biol. Chem. 267, 12973-1297 (1992).
47. Ariga, T.; Yanagisawa, M.; Wakade, C.; Ando, S.; Bucca-fusco, J. J.; McDonald, M.; Yu, R. K. Ganglioside me-tabolism in a transgenic mouse model of Alzheimer's disease: expression of Chol-1α antigens in the brain. ASN Neuro. 2, e0004 (2010).
48. Mukherjee, P.; Faber, A. C.; Shelton, L. M.; Baek, R. C.; Chiles, T. C.; Seyfried, T. N. Ganglioside GM3 sup-presses the pro-angiogenic effects of vascular endo-thelial growth factor and ganglioside GD1A. J. Lipid Res. 49, 929-93 (2008).
49. Kanda, T.; Yoshino, H.; Ariga, T.; Yamawaki, M.; Yu, R. K. Glycosphingolipid antigens in cultured microvascular bovine brain endothelial cells: Sulfglucuronosyl para- globoside as a target of monoclonal IgM in demyelin-ative neuropathy. J. Cell Biol. 126, 235-24 (1994).
50. Svennerholm, L.; Brane, G.; Karlsson, I.; Lekman, A.; Ramstrom, I.; Wikkelso, C. Alzheimer disease-effect of continuous intracerebroventricular treatment with GM1 ganglioside and a systematic activation programme. Dement. Geriatr. Cogn. Disord. 14, 128-136 (2002).
51. Klenk, E. Über die Ganglioside, eine neue Gruppe von zuckerhaltigen Gehirnlipoiden. Hoppe-Seyler's Z. Physiol. Chem. 273, 76-8 (1942).
52. Yamakawa, T. A reflection on the early history of glycosphingolipids. Glycoconj. J. 13, 123-12 (1996).
53. Svennerholm, L. Chromatographic separation of hu-man brain gangliosides. J. Neurochem. 10, 613-623 (1963).
54. IUPAC-IUBMB Joint Commission on Biochemical Nomenclature. Nomenclature of glycolipids. Pure Appl. Chem. 69, 2475-248 (1997).
55. Wu, G; Lu, Z.-H., Kulkarni, N.; Amin, R.; Ledeen, R. W. Mice lacking major brain gangliosides develop Parkin-sonism. Neurochem. Res. 36, 1706-1714 (2011).