The possible functional role of neuronal gangliosides in temperature adaptation of vertebrates

Comparative studies on brain gangliosides of more than 60 vertebrate species show correlations between concentration and the level of evolutionary organization: poikilothermic lower vertebrates (fish, amphibs, reptiles) contain about 110 to 700 μg ganglioside bound NeuAc/g. fresh wt., homeothermic birds and mammals, on the other side, 500 to 1000 μg. The composition of brain gangliosides in poikilotherms is much more complex and variable (more multisialogangliosides) as compared with homeotherms (domination of less polar fractions). There are distinct correlations between brain ganglioside composition and state of thermal adaptation: Fishes being adapted to habitates with extreme temperatures (antarctic icefish — tropic fish) are characterized by quite opposite ganglioside patterns (domination of high versus less polar fractions). During seasonal acclimatization and experimental acclimation of fish to cold or during hibernation and early postnatal development of mammals poly-sialylations of brain gangliosides occur. With regard to this the individual brain structures react differently.

The results are taken for evidence that variations in the composion of synaptic membrane-bound gangliosides may induce long-term alterations in viscosity and permeability of the neuronal membrane by which the neuronal transmission might be kept on a constant level during the process of temperature adaptation.     

Variability in brain ganglioside composition: A further molecular mechanism beside serum antifreeze-glykoproteins for adaptation to cold in Antarctic and Arctic-boreal fishes

Summary Gangliosides and sialoglycoproteins from brain, liver and muscle have been isolated from 6 Antarctic fish species from the suborder Notothenoids and from 4 Arctic-boreal fish species. In addition freezing and melting points from serum of both groups were examined in order to determine the presence of protein antifreezes. In comparison with eurythermic fishes of temperate climates in both groups the phylogenetical adaptation to cold is correlated with a significantly higher concentration of gangliosides in the brain. The ganglioside concentration of liver in Antarctic fish, but not in Arctic species, is 3 to 5fold higher than in mammals (rat); in muscle the ganglioside content is increased only in red-blooded Antarctic fish as compared with mammals. The concentration of neuronal sialo-glycoproteins generally is lower in Antarctic fish than in other marine teleosts; in muscles the content is 2 to 3fold higher than in mammals. The molecular composition of brain gangliosides is characterized by an extreme high polarity which is due to an equipment with highly sialylated fractions (40 to 50% higher sialylated than tetrasialogangliosides). There are distinct differences between the freezing and melting point of blood serum, especially in the Antarctic species in favour of the existence of protein antifreezes. The results are discussed with regard to the fact that the extremely high polarity of brain gangliosides reflects a very efficient mechanism on molecular level to keep the neuronal membrane functional under low temperature conditions.     

Brain gangliosides in monotremes, marsupials and placentals: phylogenetic and thermoregulatory aspects

The concentration and composition of brain gangliosides of 17 mammalian species belonging to the subclasses of Prototheria (monotremes), Metatheria (marsupials), and Eutheria (placentals) were investigated. The mean concentration of brain gangliosides ranges from 525 to 610 micrograms NeuAc/g wet wt in monotremes, 445-900 micrograms in marsupials and from 630 to 1130 micrograms in the placentals. In the phylogenetic series of mammals, a decrease in the complexity of brain ganglioside composition becomes obvious: a drastic reduction in the number of individual ganglioside fractions particularly those of the c-pathway of biosynthesis, took place from the level of monotremes to that of the marsupials and placentals. In monotremes, marsupials and "lower" placentals (insectivores) the percentage of alkali-labile gangliosides is relatively low (between traces and 5%), whereas in the higher evolved mammals it amounts to about 20% of all gangliosides. The ratio of the contents of the two major mammalian ganglioside fractions GD1a and GT1b is generally in the range of 1.0 and even higher; in the heterothermic platypus from the monotremes and in hibernators among the placental mammals, however, it is much lower (about 0.8). These data support the hypothesis that the brain ganglioside composition not only depends on the phylogenetic level of nervous organization (cephalization) but is additionally correlated with the state of thermal adaptation.     

Brain gangliosides and cold-adaptation in high-antarctic fish

The concentration and composition of gangliosides from the brain of eight species of Antarctic Notothenioid fishes belonging to the class of perciformes and two species of boreal fishes (tropic cichlid fish Oreochromis mossambicus; Codfish Gadus morhua) were investigated. The concentration of whole brain gangliosides in Notothenioid fishes (between 1622 and 2183 μg NeuAc/g dry wt.) was slightly lower than that in the brains of fish species, which live in warm, temperate habitats (2483 μg NeuAc/g dry wt.). The composition of brain gangliosides was completely different from that of warm adapted fish species (e.g. the tropic cichlid fish Oreochromis mossambicus). The relative concentration of polysialogangliosides (GT1b-GH) is strongly increased in all the investigated Antarctic species. They were found to have the most complex and most polar brain ganglioside pattern (high degree of sialylation and alkali-lability) within the teleosts. This may be one of the mechanisms, beside antifreeze proteins, to keep the neuronal membranes functional even below the freezing point.     

FATTY ACIDS AND LONG CHAIN BASES OF VERTEBRATE BRAIN GANGLIOSIDES

Abstract— Fatty acid and long-chain base composition of gangliosides from brains of animals belonging to various vertebrate classes (fishes, amphibia, reptiles, birds and mammals) was studied by gas-liquid chromatography. Stearic acid was found to be the main fatty acid everywhere. Brain gangliosides of cold-blooded animals contain lesser amounts of stearic and higher amounts of palmitic and monoenoic acids as compared to those of mammals. Long-chain bases were separated as trimethylsilyl derivatives. Large amounts (23-48 per cent) of long chain bases with 20 carbon atoms were found in brain gangliosides of mammals while in those of cold-blooded animals they constitute 3-12 per cent of the total. The comparison of the composition of gangliosides with that of cerebrosides and sulphatides indicates, that the fatty acid and long chain base composition of gangliosides from mammalian brain differs from that of other glycosphingolipids, whereas in brains of cold-blooded animals they are much more similar.     

Systematic position of fish species and ganglioside composition and content

The ganglioside content in brain of cartilaginous and bony fishes studied varies from 110 to 581 and from 104 to 595 micrograms sialic acid per g of wet weight respectively. A high degree of alkali lability and the predominance of C18-sphingosine and N-acetylneuraminic acid are typical of fish brain gangliosides. A high content of oligosialogangliosides with four and more residues of sialic acid and the predominance of gangliosides with gangliotetraosyl carbohydrate chain are characteristic for teleost brain. No pronounced difference was revealed in ganglioside composition and content of clupeomorphs and percomorphs. Gangliosides with short (lactosyl and gangliotriaosyl) carbohydrate chain predominate in brain of all cartilaginous fishes studied. A statistically significant difference was found in ganglioside content, relative oligosialoganglioside content and ganglioside fatty acid composition of squalomorphs and rajiformes, on one hand, and dasyatiformes and galeomorphs, on the other hand.     

Intestinal microbiota composition in fishes is influenced by host ecology and environment

The digestive tracts of vertebrates are colonized by complex assemblages of micro-organisms, collectively called the gut microbiota. Recent studies have revealed important contributions of gut microbiota to vertebrate health and disease, stimulating intense interest in understanding how gut microbial communities are assembled and how they impact host fitness (Sekirov et al. 2010). Although all vertebrates harbour a gut microbiota, current information on microbiota composition and function has been derived primarily from mammals. Comparisons of different mammalian species have revealed intriguing associations between gut microbiota composition and host diet, anatomy and phylogeny (Ley et al. 2008b). However, mammals constitute <10% of all vertebrate species, and it remains unclear whether similar associations exist in more diverse and ancient vertebrate lineages such as fish. In this issue, Sullam et al. (2012) make an important contribution toward identifying factors determining gut microbiota composition in fishes. The authors conducted a detailed meta-analysis of 25 bacterial 16S rRNA gene sequence libraries derived from the intestines of different fish species. To provide a broader context for their analysis, they compared these data sets to a large collection of 16S rRNA gene sequence data sets from diverse free-living and host-associated bacterial communities. Their results suggest that variation in gut microbiota composition in fishes is strongly correlated with species habitat salinity, trophic level and possibly taxonomy. Comparison of data sets from fish intestines and other environments revealed that fish gut microbiota compositions are often similar to those of other animals and contain relatively few free-living environmental bacteria. These results suggest that the gut microbiota composition of fishes is not a simple reflection of the micro-organisms in their local habitat but may result from host-specific selective pressures within the gut (Bevins & Salzman 2011).     

Age-related changes in GM1, GD1a, GT1b components of gangliosides in Wistar albino rats

In this study, age-related changes of GM1, GD1a, GT1b fractions of gangliosides were investigated in whole brain of male Wistar albino rats. Insignificant increases were detected in GM1 values from the third to the 24th month, whereas GD1a and GT1b concentrations of ganglioside in 24-month-old rats decreased significantly as compared to 6-month-old rats. Although there were no significant differences in the GD1a/GT1b ratio of any groups, GM1/GD1a and GM1/GT1b ratios were significantly increased as compared to 6-month-old rats. The increase in the ratios of gangliosides are not due to an increase of GM1 fractions; they result from a decrease of GD1a and GT1b fractions of gangliosides. In conclusion, the concentration of ganglioside decreased with ageing.     

Age-Related Changes in the Ceramide Composition of the Major Gangliosides Present in Rat Brain Subcellular Fractions Enriched in Plasma Membranes of Neuronal and Myelin Origin

Abstract: Age-related changes of the ceramide composition of gangliosides were studied in the synaptosomal and myelin fractions from rat brain, carrying plasma membranes of neuronal and glial origin, respectively. The five major gangliosides (GM1, GD1 a, GD1 b, GT1 b, and GQ1 b) present in these fractions were separated and quantitated by normal-phase HPLC. Each ganglioside was then fractionated by reverse-phase HPLC into the molecular species carrying a single long-chain base (LCB). The largely preponderant LCBs in the synaptosomal and myelin fractions were the C18:1 and C20:1. The content of C20.1 LCB, generally low at 1 month, increased with age in all analyzed gangliosides and in all subcellular fractions and was greater in the "b series" than in the "a series" gangliosides. Remarkably, GM1 was the only ganglioside where the proportion of LCB 20:1 was higher in the synaptosomal fraction than in the myelin fraction. The fatty acid composition of the C18:1 or C20:1 LCB species of the different gangliosides in the synaptosomal and myelin fractions did not undergo appreciable changes with age. Stearic acid was largely predominant in all the gangliosides of the synaptosomal fraction, more in the C18:1 than in the C20:1 LCB species (80–90% vs. 60–70%). The gangliosides of the myelin fraction were characterized by a lower content of 18:0 and a much higher content of 16:0 and 18:1 fatty acids than those of the synaptosomal fraction. Thus, the ceramide composition is different in the gangliosides of neuronal and myelin origin and appears to be subjected to an age-related control.     

Mucopolysaccharidosis Types IH, IS, II and IIIA: Glycosaminoglycans and Lipids of Isolated Brain Cells and Other Fractions from Autopsied Tissues

Abstract: Brain cellular fractions were prepared in bulk from four non-neurological patients and from five patients with mucopolysaccharidosis (MPS). Glycosaminoglycans and lipids were isolated and chemically analyzed. Results of the present study: in the normal controls glycosaminoglycans as μg per mg protein (mean) were 2.2 in neuronal perikarya, 2.0 in astroglia, 2.1 in oligodendroglia, 3.3 in neuropile from gray matter and 3.2 in a mixed fraction from white matter. In the partially myelinated axons from gray and white matter of an 8-month-old infant, the concentration was 6.9 and 2.6 μg per mg protein, compared with 2.8 and 0.8 μg per mg protein, respectively, in the adult patients. It was estimated that chondroitin sulfates constituted more than one-half of the total glycosaminoglycan. Hyaluronic acid, heparan sulfate and dermatan sulfate were also present in all cell types and fractions. Cholesterol, phospholipids, cerebrosides, sulfatide and gangliosides were present in all cell types and fractions, but differed widely in concentration. There was a four- to sixfold increase in the concentration of total glycosaminoglycans in the neuronal perikarya of patients with MPS IH, II and IIIA. The increased glycosaminoglycans were heparan sulfate in MPS IIIA and dermatan sulfate plus heparan sulfate in MPS IH and II. Similar changes were found in the astroglia and in the other brain fractions of those patients. The concentration of the gangliosides G_{m 2}, G_{m 3}, G_{d 3} and ceramide dihexoside was markedly increased in the neurons and other brain fractions of the same patients. The quantities of G_{m 3}, G_{m 2} and G_{d 3} together amounted to 65% of the total gangliosides of the neurons, indicating changes of the same magnitude seen in the gangliosidoses. All these patients exhibited mental retardation. The concentration and composition of glycosaminoglycans, gangliosides and neutral hexosyl ceramides in the neuronal perikarya of the patient with MPS IS was normal. There was only a small increase of dermatan sulfate content in the neuropile, mixed fraction and myelinated axons from the white matter and some increase of ceramide dihexoside content in the myelinated axons. This patient was an adult of normal intelligence.     

Human brain gangliosides in development, aging and disease.

In this study, brain gangliosides in prenatal and postnatal human life and Alzheimer's disease were analyzed. Immunohistochemically, the presence of the "c"-series of gangliosides (GQ1c) was only registered in the embryonic brain at 5 weeks of gestation. Biochemical results indicated a two-fold increase in ganglioside concentration in the human cortex between 16 and 22 weeks of gestation. The increasing ganglioside concentration was based on an increasing GD1a ganglioside fraction in all regions analyzed except in the cerebellar cortex, which was characterized by increasing GT1b. During prenatal human development, regional differences in ganglioside composition could only be detected between the cerebrum ("a"-pathway) and the cerebellum ("b"-pathway). Between birth and 20-30 years of age, a cerebral neocortical difference of ganglioside composition occurred, characterized by the lowest GD1a in visual cortex. Analyzing the composition of gangliosides in cortical regions during aging, they were observed to follow region-specific alterations. In the frontal cortex, there was a greater decrease in GD1a and GM1 than in GT1b and GD1b, but in the occipital (visual) cortex there was no change in individual gangliosides. In hippocampus, GD1a moderately decreased, whereas other fractions were stable. In the cerebellar cortex, GD1b and GT1b fractions decreased with aging. In Alzheimer's disease, we found all ganglio-series gangliosides (GM1, GD1a, GD1b, GT1b) to be decreased in regions (temporal and frontal cortex and nucleus basalis of Meynert) involved in pathogenesis of disease. In addition, in Alzheimer's disease we found simple gangliosides (GN2, GM3) to be elevated in the frontal and parietal cortex, which might correlate accelerated lysosomal degradation of gangliosides and/or astrogliosis occurring during neuronal death.     

A new thin-layer chromatographic approach for separation of multisialogangliosides: Novel gangliosides fractions in the embryonic chicken brain

A novel thin-layer chromatographic procedure has been developed that permits rapid, high-resolution separation of complex ganglioside mixtures and direct densitometric quantification. A special advantage of the new procedure, performed by two different consecutive runs on high-performance thin-layer chromatography plates, is an excellent separation of multisialogangliosides containing more than three sialic acid residues. Using the new procedure, 10 unidentified fractions were detected in embryonic chick brains. These gangliosides were clearly distinguishable from the known gangliosides, GM1, GD3, GD1a, GD2, GD1b, GT1b, and GQ1b. Eight of these “additional” fractions were also found in the brains of rays. From published data on the cod fish brain, 6 of the novel fractions are suggested to correspond to GT3, GT2, GT1c, GQ1c, GP1c, and GP1b. Four fractions, moving on thin-layer chromatography plates below the suggested GP1c have not been reported previously in any vertebrate. Due to their very slow migration rates they may contain gangliosides with six, seven, or more sialic acid residues. During development of the chicken, the relative amounts of the newly detected fractions decrease in favor of GT1b and GD1a.     

Gangliosides in the human brain development and aging.

In this study, brain gangliosides in prenatal and postnatal human life were analyzed. Immunohistochemically, the presence of "c"-pathway of gangliosides (GQ1c) in embryonic brain was only recorded at 5 weeks of gestation. Biochemical results indicated a twofold increase in human cortex ganglioside concentration between 16 and 22 weeks of gestation. The increasing ganglioside concentration was based on an increasing GD1a ganglioside fraction in all regions analyzed except cerebellar cortex, which was characterized by increasing GT1b. In this developmental period, GD3 was found to be localized in the ventricular zone of the cortical wall. After birth, GD1b ganglioside in neuropil of granular cell layer corresponding to growing mossy fibers was expressed in cerebellar cortex. Between birth and 20/30 years of age, a cerebral neocortical difference of ganglioside composition was observed, characterized by lowest GD1a in visual cortex. Analyzing the composition of gangliosides in cortical regions during aging, they were observed to follow region-specific alterations. In frontal cortex, there was a greater decrease in GD1a and GM1 than in GT1b and GD1b, but in occipital (visual) cortex there was no change in individual gangliosides. In hippocampus, GD1a moderately decreased, whereas other fractions were stable. In cerebellar cortex, GD1b and GT1b fractions decreased with aging.     

The effect of cold stress on ganglioside fatty acid composition and ganglioside-bound sialic acid content of rat brain subcellular fractions

The effect of cold stress on the ganglioside fatty acid composition and sialic acid content of brain subcellular fractions and homogenate of rats was studied, the animals were kept in a cold room with 12h light-dark cycles at 3 and 10 degrees C for 2 weeks. (1) The rat brain homogenate, synaptosomes and myelin of rats exposed to 3 degrees C contained significantly higher amounts of ganglioside-bound sialic acid per mg of protein than these fractions of control rats kept at 23 degrees C; the differences were less pronounced in rats exposed to 10 degrees C. (2) A small, but significant, diminution of relative palmitic acid content and an increase of stearic acid content was found to take place in gangliosides from rat brain synaptosomes, synaptosomal plasma membranes and homogenate as a result of the exposure of animals to 3 degrees C and to a lesser extent to 10 degrees C. (3) The content of unsaturated fatty acids in gangliosides from brain subcellular fractions was approximately the same in cold exposed and control rats.     

Major and c-series gangliosides in lenticular tissues: mammals to molluscs

Gangliosides of eye lenses were examined in mammals (rat, rabbits, pig, cow), bird (chicken), reptile (terrapin), amphibian (bullfrog), bony fish (red sea bream, bluefin tuna, bonito, Pacific mackerel) and molluscs (common squid, Pacific octopus). Besides the fact that GM3 was the common ganglioside species, the composition of major gangliosides in mammalian eye lenses significantly differed from each other. While gangliotetraose gangliosides were abundant in rat eye lens, they did not constitute major components in porcine and bovine tissues. The c-series ganglioside GT3 was expressed in rat eye lenses but were practically absent in other mammalian tissues. The composition of major gangliosides in eye lenses of lower animals varied from species to species, whereas c-series gangliosides were consistently expressed, showing similar compositional profiles. Our results demonstrate the species-specific compositions of lenticular gangliosides. Evidence was also provided suggesting that eye lenses of common squid (Todarodes pacificus) and Pacific octopus (Octopus vulgaris) express gangliosides including gangliotetraose species and c-series gangliosides.     

Maternal alcohol consumption and undernutrition in the rat: Effects on gangliosides and their catabolizing enzymes in the CNS of the newborn

Consumption of fifteen percent alcohol, during gestation did not cause any decrease in the total calorie or fluid intake of the rats maintained on normal dietary regimen. However, the alcohol consumption by gestating mothers resulted in a decreased contents of both DNA and protein in the CNS of thein utero alcohol exposed pups at birth. DNA content was also found to be less in the undernourished pups compared to the normal pups. On the other hand an increase in the total gangliosides and a decrease in the ganglioside catabolizing enzymes was observed in the brain and spinal cord of alcoholic pups at birth. However undernutrition resulted in a decrease in the content of total gangliosides both in brain and spinal cord. Maternal alcohol consumption and undernutrition had also resulted in an altered proportions of the individual ganglioside fractions.     

Brain lipid biochemistry of the sturgeons Acipenseridae]

Brain lipids of 4 species of sturgeons-Acipenser güldenst?dti, A. stellatus, A. ruthenus and Huso huso-have been investigated. In whole brain homogenates the content of the basic phospholipid families, their fatty acid composition as well as the content of glycosphingolipids-gangliosides, cerebrosides and sulfatides were studied. The quantitative relations between different molecular ganglioside fractions and their fatty acid composition, as well as the relative content of hydroxycerebrosides and cerebrosides with normal fatty acids were determined. The brain lipids of Acipenseridae were compared to previously obtained data on the brain of Elasmobranch and Teleost fishes. The brain lipid pattern of the four sturgeon species is very similar, but it differs greatly from that of Elasmobranch and of Teleostean brain, being in some respect more like the type of bony fish brain, in others the kind of brain of sharks and rays, and frequently considerably differing from both these types. The conspicous peculiarity in the content and molecular characteristics of the brain lipids of Acipenseridae compels us to agree with the opinion expressed by the late A.N. Belozerski and his coworkers [26, 27], based on a detailed study of fish DNA nucleotides, that the Ganoid fish are to be regarded as an independent class.     

Developmental profiles of gangliosides in trisomy 19 mice

The ganglioside composition of the cerebrum, cerebellum, brainstem, liver, heart, and spleen was analyzed quantitatively in trisomy 19 (Ts19) mice aged 4 to 12 days postpartum. The developmental profiles of cerebral gangliosides were similar in Ts19 mice and control littermates: Total ganglioside-sialic acid as well as the proportions of the individual gangliosides GD1a and GM1 increased with age, while the percentages of GQ1b and GT1b decreased during development. Both the accretion of the total ganglioside content and the development of the individual ganglioside fractions were delayed by 2-3 days in the Ts19 telencephalon. Likewise, the shift from the b- to the a-pathway of ganglioside synthesis was retarded. Ganglioside development was equally delayed in the cerebellum and the brainstem of Ts19 mice. Since in Ts19 mice, morphogenesis of several brain regions is similarly delayed by 2 days, these results confirm the usefulness of gangliosides as biochemical markers for brain maturation. In contrast to brain gangliosides, the ganglioside composition of the Ts19 livers was clearly distinguished from that of control livers. Total ganglioside-bound sialic acid was increased by 35-50% in Ts19 livers. This elevation in ganglioside content not explicable by a simple delay in development was mainly due to an increase in GD3 and fraction 2, which is likely to contain GD1a and GD1b. In contrast, GM2 which increased considerably with age in control mice persisted on a low level in Ts19 livers. Comparable alterations of the ganglioside pattern were neither observed in the spleen nor in the heart of Ts19 mice. The data presented give additional evidence that ganglioside synthesis in the liver is under a different regulation mechanism than that in the brain, heart, and spleen.     

Seasonal variability of sialo-glycoconjugates in the brain of the Djungarian hamster (Phodopus sungorus)

The influence of season, photoperiod and ambient temperature on the content of proteins, sialo-glycoproteins and gangliosides and on the composition of gangliosides of three different brain regions (cortex, cerebellum and basalbrain) of the Djungarian dwarf hamster (Phodopus sungorus) had been investigated. Concomittantly changes in body wt and fur colouration were recorded. Dwarf hamsters living under natural photoperiod and ambient temperature conditions ("outside") showed a distinct annual cycle in body wt (summer: about 45 g; winter: about 25 g) and fur colouration (summer: dark grey; winter: whitish). Among the three brain regions the mean concentration of proteins ranged between 120 and 155 mg protein/g wet wt. The sialo-glycoprotein content varied between 260 and 410 micrograms NeuAc/g wet wt, and that of gangliosides between 800 and 1650 micrograms NeuAc/g wet wt. Seasonal fluctuations were not found. The composition of brain gangliosides remained uninfluenced throughout the year in the cerebellum, whereas seasonal variations were observed in cortex and basalbrain. Consequently the concentration ratio of the two major mammalian ganglioside fractions GD1a vs GT1b remained almost stable in cerebellum (0.3). In contrast to this the seasonal values of cortex and basalbrain changed from 0.6 and 0.8 in winter to 0.7 and 1.1 in summer. This indicated a higher polarity of the gangliosides in these brain regions during cold adaptation. The results are discussed with regard to modulatory functions of neuronal gangliosides for the process of synaptic transmission during seasonal adaptation.     

Brain ganglioside patterns of vertebrates

Abstract— The ganglioside content in brains of representatives of six vertebrate classes (lamprey, ray, sheat-fish, carp, frog, triton, tortoise, hen, pigeon, rabbit, rat and monkey) was determined. In most cases a correlation was found between the level of nervous organization and the ganglioside content of brain. In fish and amphibian brain ganglioside concentration is half to one third that in mammalian brain. Ganglioside composition of higher vertebrate brains (mammals, birds and reptiles) has many similar features. Four main gangliosides with 1-3 NANA residues in their molecules–G₁ * * Nomenclature of Korey and Gonatas (1963 ): G₁ trisialyl-hexosaminyl-trihexosyl-ceramide; G₂ and G₃, disialyl-hexosaminyl-trihexosyl-ceramides; G₄ monosialyl-hexosaminyl-trihexosyl-ceramide.
, G₂, G₃ and G₄–constitute 80-90 per cent of total ganglioside NANA. Fractions G_2a ? ? G_o, tetrasialyl-hexosaminyl-trihexosyl-ceramide; G_2a disialyl-hexosaminyl-dihexosyl-ceramide; G₅, monosialyl-hexosaminyl-dihexosyl-ceramide.
G_o and G₅ are present in much lesser amounts. Species peculiarities in distribution of NANA among different fractions were noted. The brain gangliosides of lower vertebrates–fish and amphibia–are unusual in having a high proportion of polysialogangliosides, containing 4 and 5 NANA residues, and a lower content of monosialogangliosides. In ray brain a considerable part of gangliosides has a reduced carbohydrate chain.