Summary
Insight on the function of gangliosides. can emerge from knowledge of their cellular distribution. In this paper we review the structure of ganglioside GD3 and recent information on its cellular distribution. GD3 appears to be enriched in a variety of neural cell types including: reactive glia, gliomas, undifferentiated neurons, Muller glia, and oligodendroglia. Because each of these cell types share an enhanced permeability to ions and metabolites or possess properties associated with enhanced permeability, we suggest that GD3 is associated with enhanced membrane permeability. A possible function for GD3 in membrane permeability has implications for other cellular events such as metabolism, growth and interactions.
Similar content being viewed by others
References
Kuhn R, Wiegandt H: Weitere Ganglioside im Menschenhirn, Z Naturforsch 19b:256, 1964.
Ledeen R, Salsman K, Cabrera M: Gangliosides in subacute sclerosing leukoencephalitis: isolation and fatty acid composition of nine fractions. J Lipid Res 9:129–136, 1968.
Hagberg B, Hultquist G, Ohman R, Svennerholm L: Congenital amaurotic diocy. Acta Pediat, Scand 54:116–130, 1965.
Ando S, Yu RK: Isolation and characterization of a novel trisialoganglioside, GTla, from human brain. J Bio Chem 252:6247–6250, 1977.
Das SK, McCullough MS: Gangliosides of bovine optic nerve. Lipids 15:932–936, 1980.
Chou KH, Ambers LSA, Jungalwala FB: Ganglioside composition of chemically induced rat neural tumors and characterization of hematoside from neurinomas. J Neurochem 33:863–873, 1979.
Seyfried T, Yu RK, Miyazawa N: Differential cellular enrichment of gangliosides in the mouse cerebellum: analysis using neurological mutants. J Neurochem 38:551–559, 1982.
Ando S, Yu RK: Fatty acid and long-chain base composition of gangliosides isolated from adult human brain. J Neurosci Res 12:205–211, 1984.
Vanier MT, Holm M, Mansson JE, Svennerholm L: The distribution of lipids in the human nervous system. V Gangliosides and allied neutral glycolipids of infant brain. J Neurochem 21:1375–1384, 1973.
Holm M, Mansson JE, Vanier MT, Svennerholm L: Gangliosides of human, bovine, and rabbit retina. Biochem Biophys Acta 280:356–364, 1972.
Holm M, Mansson JE: Differences in sphingosine and fatty acid patterns of the major gangliosides of bovine retina. FEBS Lett 38:261–262, 1974.
Kaufman B, Basu S, Roseman S: Enzymatic synthesis of disialogangliosides from monosialogangliosides by sialyltransferases from embryonic chicken brain. J Biol Chem 243:5804–5807, 1968.
Keenan TW, Morre DV, Basu S: Ganglioside biosynthesis: Concentration of glycosphingolipid glycosyltransferases in golgi apparatus from rat liver. J Biol Chem 249:310–315, 1974.
Pacuszka T, Duffard RO, Nishimura RN, Brady RO, Fishman PH: Biosynthesis of bovine thyroid gangliosides. J Biol Chem 253:5839–5846, 1978.
Basu S, Basu M, Kyle JW, Chon HC: Biosynthesis in vitro of gangliosides containing Gg- and Lc- cores. Adv Exp Med Biol 174:249–261, 1984.
Seyfried TN, Miyazawa N, Yu RK: Cellular localization of gangliosides in the developing mouse cerebellum: analysis using the weaver mutant. J Neurochem 41:491–505, 1983.
Seyfried, TN, Yu RK: Cellular localization of gangliosides in the mouse cerebellum: analysis using neurological mutants. Adv Exp Med Biol 174:169–182, 1984.
Seyfried TN, Bernard DJ, Yu RK: Cellular distribution of gangliosides in the developing mouse cerebellum: analysis using the staggerer mutant. J Neurochem 43:1152–1162, 1984.
Sax DS, Hirano A, Shofer RJ: Staggerer, a neurological murine mutant. Neurology 18:1093–1100, 1968.
Hirano A, Dembitzer HM: The fine structure of astrocytes in the adult staggerer. J Neurophthol Exp Neurol 34:1–11, 1976.
Mullen RJ, Eicher EM, Sidman RL: Purkinje cell degenration, a new neurological mutation in the mouse. Proc Natl Acad Sci USA 73:208–212, 1976.
Ghetti B, Truex L, Sawyer B, Strada S, Schmidt M: Exaggerated cyclic AMP accumulation and glial cell reaction in the cerebellum during Purkinje cell degeneration in pcd mutant mice. J Neurosci Res 6:789–801, 1981.
Yu RK, Ledeen R, Eng LF: Ganglioside abnormalities in multiple sclerosis. J Neurochem 23:169–174, 1974.
Yu RK, Ueno K, Glaser GH, Tourtellotte WW: Lipid and protein alterations in spinal cord and cord myelin of multiple sclerosis. J Neurochem 39:464–477, 1982.
Norton WT, Poduslo SE, Suzuki K: Subacute sclerosing leukoencephalitis. II Chemical studies including abnormal myelin and abnormal ganglioside pattern. J Neuropathol Exp Neurol 25:582–597, 1966.
Yu RK, Ledeen RW, Gajdusek DC, Gibbs CJ: Ganglioside changes in slow virus disease: analysis of chimpanzee brains infected with Kuru and Creutzfeldt-Jakob agents. Brain Res 70:103-112.
Suzuki K, Chen G: Chemical studies on Jakob-Creutzfeldt disease. J Neuropathol Exp Neurol 25:396–408, 1966.
Tamai Y, Kojima H, Ikuta F, Kumanishi T: Alterations in the composition of brain lipids in patients with Creutzfeldt-Jakob disease. J Neurol Sci 35:59–76, 1978.
Yu, RK, Manuelidis EE: Ganglioside alterations in guinea pig brains at end stages of experimental Creutzfeldt-Jakob disease. J Neurol Sci 35:15–23, 1978.
Bernheimer H, Sperk G, Price KS, Hornykiewicz O: Brain gangliosides in Huntington's disease. Adv Neurol 23:463–471, 1979.
Suzuki K: Ganglioside patterns of normal and pathological brains. In: Inborn Disorders of Sphingolipid Metabolism. Aronson SM and Volk BV (eds), pp 215–230, Oxford, Pergamon Press, London, 1967.
Svennerholm L, Vanier MT: Brain gangliosides in Krabbe disease. Adv Exp Med Biol 19:499–514, 1972.
Suzuki K, Tucker SH, Rorke LB, Suzuki K: Ultrastructural and biochemical sutides of Schilder's disease. J Neuropathol Exp Neurol 29:405–419, 1970.
Igarashi M, Belchis D, Suzuki K: Brain gangliosides in adrenoleukodystrophy. J Neurochem 27:327–328, 1976.
Stoolmiller AC, Dawson G, Kemp SF, Schachner M: Synthesis of glycolipids in mouse glial tumors. J Neurochem 32:637–641, 1979.
Yates AJ, Thompson DK, Boesel CP, Albrightson C, Hart RW: Lipid composition of human neural tumors. J Lipid Res 20:428–436, 1979.
Traylor DT, Hogan EL: Gangliosides of human cerebral astrocytomas. J Neurochem 34:126–131, 1980.
Manuelidis L, Yu RK, Manuelidis EE: Ganglioside content and pattern in human gliomas in culture. Acta Neuropath 38:129–135, 1977.
Pukel CS, Lloyd KO, Travassos LR, Dippold WR, Oettgen HF, Old LJ: GD3 — a prominent ganglioside of human melanoma: detection and characterization by mouse monoclonal antibody. J Exp Med 155:1133–1147, 1982.
Nudelman E, Hakomori SI, Kannagi R, Levery S, Yeh MY, Hellstrom KE, Hellstrom I: Characterization of a human melanoma — associated ganglioside antigen defined by a monoclonal antibody, 4.2. J Biol Chem 257:12752–12756, 1982.
Siddiqui B, Buehler J, DeGregorio MW, Macher B: Differential expression of ganglioside GD3 by human leukocytes and leukemic cells. Cancer Res 44:5262–5265, 1984.
Nakakuma H, Sanai Y, Shiroki K, Nagai Y: Gene regulated expression of glycolipids: appearance of GD3 ganglioside in rat cells on transfection with transforming gene El of human adremovirus type 12 DNA and its transcriptional subunits. J Biochem 96:1471–1480, 1984.
Duffard RO, Fishman PH, Bradley RM, Lauter CJ, Brady RO, Trams EG: Ganglioside composition and biosynthesis in cultured cells derived from CNS. J Neurochem 28:1161–1168, 1977.
Robert J, Rebel G, Mandel P: Glycosphingolipids from cultured astroblasts. J Lipid Res 18:517–522, 1977.
Dawson G, Stoolmiller AC: Comparison of the ganglioside composition of established mouse neuroblastoma cell strains grown in vivo and in tissue culture. J Neurochem 26:225–226, 1976.
Hamberger A, Svennerholm L: Composition of gangliosides and phospholipids of neuronal glial cell enriched fractions. J Neurochem 18:1821–1829, 1971.
Abe T, Norton WT: The characterization of sphingolipids from neurons and astrdglia of immature rat brain. J Neurochem 23:1025–1036, 1974.
Robert J, Freysz L, Sensenbrenner M, Mandel P, Rebel G: Gangliosides of glial cells: a comparative study of normal astroblasts in tissue culture and glial cells isolated on sucrose-ficoll gradients. FEBS Lett 50:144–146, 1975.
Urban PF, Harth S, Freysz L, Dreyfus H: Brain and retinal ganglioside composition from different species determined by TLC and HPTLC, Adv Exp Med Biol 125:149–157, 1980.
Ledeen RW, Skrivanek JA, Nunez J, Sclafani JR, Norton WT, Farooq M: Implications of the distribution and transport of gangliosides in the neuronal system. In: MM Raport and A Gorio (Eds). Gangliosides in Neurological and Neuromuscular Function, Development and Repair. Raven Press New York, 1981, pp 211–223.
Asou H, Brunngraber EG: Absence of ganglioside GM1 in astroglial cells from 21-day old rat brain: Immunohistochemical, histochemical and biochemical studies. Neurochem Res 8:1045–1057, 1983.
Asou H, Brunngraber EC: Absence of ganglioside GM1 in astroglial cells from newborn rat brain. Neurochem Int 6:81–89, 1984.
Berra B, Cestaro B, Sale FO, Venerando B, Beltrame D, Cantone A: Gangliosides and neuraminidase in foetal rat brain. Bull Molec Biol Med 3:86–97, 1978.
Engel ER, Wood JG, Byrd FI: Ganglioside patterns and cholera toxin-peroxidase labeling of aggregating cells from the chick optic tectum. J Neurobiol 10:429–440, 1979.
Irwin LN, Irwin CC: Developmental changes in ganglioside composition of hippocampus, retina, and optic tectum. Devel Neurosci 2:129–138, 1979.
Yavin E, Yavin Z: Ganglioside profiles during neural tissue development. Develop Neurosci 2:25–37, 1979.
Irwin LN, Michael DB, Irwin CC: Ganglioside patterns of fetal rat and mouse brain. J Neurochem 34:1527–1530, 1980.
Dreyfus H, Urban PF, Edel-Harth S, Mandel P: Developmental patterns of gangliosides and phospholipids in chick retina and brain. J Neurochem 25:245–250, 1975.
Dreyfus H, Louis VC, Harth S, Mandel P: Gangliosides in cultured neurons. Neurosci 5:1647–1655, 1980.
Rosner H: Ganglioside changes in the chicken optic lobes and cerebrum during embryonic development. Wilhelm Roux's Arch 188:205–213, 1980.
Rosner H: Ganglioside changes in the chicken optic lobes as biochemical indicators of brain development and maturation. Brain Res 236:49–61, 1982.
Hilbig R, Rosner H, Merz G, Segler-Stahl K, Rahmann H: Developmental profiles of gangliosides in mouse and rat cerebral cortex. Wilhelm Rouxs Arch 191:281–284, 1982.
Irwin LN: Phylogeny and ontogeny of vertebrate brain gangliosides. Adv Exp Med Biol 174:319–329, 1984.
Landa CA, Panzette P, Maccioni HJF: Biosynthesis of gangliosides in cultured retina from chick embryos. Develop Brain Res 14:83–92, 1984.
Maccioni HJF, Penzetta P, Arrieta D, Caputto R: Ganglioside glycosyltransferase activities in the cerebral hemispheres from developing rat embryos. Int J Develop Neurosci 2:13–19, 1984.
Wille W, Schaal H, Heinlein VAO: Molecular events during cerebellar development (Abstract). Soc Neurosci Abst 9:944, 1983.
Goldman JE, Hirano M, Yu RK, Seyfried TN: GD3 ganglioside is a glycolipid characteristic of immature neuroectodermal cells. J. Neuroimmunol 7:179–192, 1984.
Levine JM, Beasley L, Stallcup WB: The D1.1 antigen: a cell surface marker for germinal cells of the central nervous system. J Neurosci 4:820–831, 1984.
Cheresh DA, Varki AP, Varki NM, Stallcup WB, Levine J, Reisfeld RA: A monoclonal antibody recognizes an Oacylated sialic acid in a human melanoma — associated ganglioside. J Biol Chem 259:7453–7459, 1984.
Cheresh DA, Reisfeld RA, Varki AP: O-acetylation of disialoganglioside GD3 by human melanoma cells creates a unique antigenic determinant. Science 225:844–846, 1984.
Hatten ME, Messer A: Postnatal cerebellar cells from staggerer mutant mice express embryonic cell surface characteristic. Nature 276:504–506, 1978.
Trenkner E: Postnatal cerebellar cells of staggerer mutant mice express immature components on their surface. Nature 277:566–567, 1979.
Edelman GM, Chuong CM: Embryonic to adult conversion of neural cell adhesion molecules in normal and staggerer mice. Proc Natl Acad Sci 79:7036–7040, 1982.
Edel-Harth S, Dreyfus H, Bosch P, Rebel G, Urban PF, Mandel P: Gangliosides of whole retina and rod outer segments. FEBS Lett 35:284–288, 1973.
Dreyfus H, Urban PF, Bosch P, Edel-Harth S, Rebel G, Mandel P: Effect of light on gangliosides from calf retina and photoreceptors. J Neurochem 22:1073–1078, 1974.
Seyfried TN, Yu RK, Miyazawa N, Lai YK: Retinal gangliosides in RCS mutant rats. J Neurochem 39:277–279, 1982.
Caputo BL, Nores GA, Cemborain BN, Caputo R: The effect of light exposure following an intraocular injection of (3H)-N-acetylmannosamine on the labeling of gangliosides and glycoproteins of retina ganglion cells and optic tectum of singly caged chickens. Brain Res 245:231–238, 1982.
Holm M, Mansson JE: Gangliosides of the bovine optic nerve. FEBS Lett 45:159–161, 1974.
Holm M, Mansson JE: Differences in the incorporation of N-(acetyl-3H) monosamine into the sialic acid of the major retinal gangliosides, studies in vivo. FEBS Lett 46:200–202, 1974.
Holm M: Biodegradation of the major rabbit retinal gangliosides, studied in vivo. FEBS Lett 77:225–227, 1977.
Tractenberg MC, Packey DJ: Rapid isolation of mammalian Muller cells. Brain Res 261:43–52, 1983.
Kasai N, Yu RK: The monoclonal antibody A2B5 is specific to ganglioside GQ1C. Brain Res 277:155–158, 1983.
Eisenbarth GS, Walsh FS, Nirenberg M: Monoclonal antibody to a plasma membrane antigen of neurons. Proc Natl Acad Sci USA 76:4913–4917, 1979.
Hogan MJ, Alvarado JA, Weddell JE: Histology of the Human Eye. WB Saunders, New York, 1971.
Yu RK, Igbal K: Sialosylgalactosyl ceramide as a specific marker for human myelin and oligodendroglial perikarya: gangliosides of human myelin, oligodendroglia and neurons. J Neurochem 32:293–300, 1979.
Cochran FB, Yu RK, Ando S, Ledeen RW. Myelin gangliosides: an unusual pattern in the avian central nervous system. J Neurochem 36:696–702, 1981.
Mack SR, Szuchet S, Dawson G: Synthesis of gangliosides by cultured oligodendrocytes. J Neurosci Res 6:361–367, 1981.
Caputto R, Maccioni HV, Arce A: Biosynthesis of brain gangliosides. Molec Cell Biochem 4:97–106, 1974.
Maccioni HV, Landa C, Arce A, Caputto R: The biosynthesis of brain gangliosides-Evidence for a ‘transient pool’ and an ‘end product pool’ of gangliosides. Adv Exp Med Biol 83:267–281, 1977.
Yohe HC, Ueno K, Chang NC, Glaser GH, Yu RK: Incorporation of N-acetylmannosamine into rat brain subcellular gangliosides: effect of pentylenetetrazol-induced con vulsions on brain gangliosides. J Neurochem 34:560–568, 1980.
Landa CA, Maccioni HJF, Caputto R: The site of synthesis of gangliosides in the chick optic system. J Neurochem 33:825–838, 1979.
Miller-Podraza H, Bradley RM, Fishman PH: Biosynthesis and localization of gangliosides in cultured cells. Biochemistry 21:3260–3265, 1982.
Miller-Podraza H, Fishman PH: Soluble gangliosides in cultured neurotumor cells. J Neurochem 41:860–867, 1983.
Graus F, Cordon-Cardo C, Houghton AN, Melamed MR, Old LJ: Distribution of ganglioside GD3 in the human nervous system detected by R24 mouse monoclonal antibody. Brain Res 324:190–194, 1984.
Magalhaes MM, Coimbra A: Electron microscope radiographic study of glycogen synthesis in the rabbit retina. J Cell Biol 47:263–275, 1970.
Uga S, Smelser GK: Electron microscopic study of the development of retinal Mullerian cells. Invest Ophthalmol. 12:295–307, 1973.
Sarthy PV, Lam DMK: Biochemical studies of isolated glial (Muller) cells from turtle retina. J Cell Biol 78:675–684, 1978.
VanHarreveld A: Swelling of the Muller fibers in the chicken retina. J Neurobiol 13:519–536, 1982.
Newman EA, Frambach DA, Odette LL: Control of extracellular potassium by retinal glial cell K siphoning. Science 225:1174–1175, 1984.
Acosta-Vidrio E, Fedoroff S: Progress in Clinical and Biological Research, Vol 59A: Glial and Neuronal Cell Biology. Alan R Liss 1981.
Duffy PE: Astrocytes: normal, reactive and neoplastic. Raven Press New York, 1983.
Gordon PB, Rubin MS: Membrane transport during erythroid differentiation. J Memb Biol 64:11–21, 1982.
Isselbacher KJ: Increased uptake of amino acids and 2-deoxy-D-glucose by virus transformed cells in culture. Proc Natl Acad Sci USA 69:585–589, 1972.
Searls DB, Edidin M: Lipid composition and lateral diffusion in plasma membranes of teratocarcinoma-derived cell lines. Cell 24:511–517, 1981.
Wooley DW, Gommi BW: Serotonin receptors — VII. Activities of various pure gangliosides as the receptors. Proc Natl Acad Sci USA 53:959–963, 1965.
Gielen W: Uber die Funktion von Gangliosiden. Ein Serotonin und Ca++ Receptor. Z Naturforsch (B) 23b:117–118, 1968.
Price HC, Byard C, Sims W, Wilson R: Gangliosides and other lipid micelles. A study of amine binding by a dialysis/fluorescence method. Neurochem Res 4:63–72, 1979.
Tamir H, Brunner W, Casper D, Rapport MM: Enhancement by gangliosides of the binding of serotonin to Serotonin binding protein. J Neurochem 34:1719–1724, 1980.
Dippold WG, Knuth A, Buschenfeld KHM: Inhibition of human melanoma cell growth in vitro by monoclonal anti-GD3-ganglioside antibody. Cancer Res 44:806–810, 1984.
Houghton AN, Mintzer D, Cordon-Cardo C, Welt S, Fliegel B, Vadhan S, Carswell E, Melamed MR, Oettgen HF, Old LJ: Mouse monoclonal IgG3 antibody detecting GD3 ganglioside: a phase I trial in patients with malignant melanoma. Proc Natl Acad Sci USA 82:1242–1246, 1985.
Rosner H, Al-Agtum M, Henke-Fahle S: Developmental expression of GD3 and polysialogangliosides in embryonic chicken nervous tissue reacting with monoclonal antiganglioside antibodies. Develop Brain Res 18:85–95, 1985.
Cheresh DA, Harper JR, Shulz G, Resifeld RA: Localization of the gangliosides GD2 and GD3 in adhesion plaques and on the surface of human melanoma cells. Proc Natl Acad Sci USA 81:5767–5771, 1985.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Seyfrieda, T.N., Yu, R.K. Ganglioside GD3: structure, cellular distribution, and possible function. Mol Cell Biochem 68, 3–10 (1985). https://doi.org/10.1007/BF00219383
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00219383