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Human Nutrition and Metabolism

Human and Bovine Milk Gangliosides Differ in Their Fatty Acid Composition¹

Numico Research Germany, Bahnstrasse 14-30, D-61381 Friedrichsdorf, Germany

²To whom correspondence should be addressed. E-mail: Lbode{at}burnham.org.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Gangliosides are considered bioactive components in human infant nutrition, and their fatty acid composition alters their biological effects. We used matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) MS and GLC to analyze the fatty acid composition of the predominant gangliosides, the monosialoganglioside GM₃ [sialic acid (Sia) 2–3 galactose (Gal) ß1–4 glucose (Glc) ß1–1 ceramide] and the disialoganglioside GD₃ (Sia 2–8 Sia 2–3 Gal ß1–4 Glc ß1–1 ceramide), in pooled human and bovine milk, the latter being a source for gangliosides in infant formula. Compared with whole milk lipids, both human and bovine milk gangliosides were selectively enriched with certain fatty acids, and the fatty acid composition of milk gangliosides in the 2 species was significantly different. The amount of long-chain fatty acids (20 C atoms) was higher in bovine milk gangliosides (GM₃: 73.71 ± 3.39%; GD₃: 79.19 ± 2.79%) than in human milk gangliosides (GM₃: 51.25 ± 0.65%; GD₃: 34.04 ± 1.80%). Tricosanoic acid (23:0) dominated in bovine milk gangliosides (GM₃: 24.05 ± 1.37%; GD₃: 26.66 ± 1.24%), whereas it only played a minor role in human milk gangliosides (GM₃: 2.88 ± 0.10%; GD₃: 1.84 ± 0.29%). We hypothesized that the differences in the fatty acid composition of milk gangliosides result in physiological distinctions between breast-fed and formula-fed infants and therefore are of importance for human infant nutrition.

KEY WORDS: • human milk • bovine milk • gangliosides • fatty acid composition

Gangliosides in human milk and infant milk formula are considered to be bioactive components in human infant nutrition (1–4). However, ganglioside composition varies between human and bovine milk, and the latter is a major source for gangliosides in infant milk formula (5–8). Whether these structural differences alter biological effects in the infant is still unknown.

Gangliosides, sialic acid (Sia)⁴ -containing glycosphingolipids, consist of a hydrophobic ceramide moiety and a hydrophilic oligosaccharide chain. Ceramide itself is a chimera of a sphingoid base and a fatty acid joined in an amide bond. The oligosaccharide chain is linked to the sphingoid base and provides the basis for the traditional ganglioside nomenclature (9).

Milk gangliosides are part of the membrane fraction of the milk fat globule, which derives from the apical plasma membrane of the secretory cells in the lactating mammary gland (10). These gangliosides are considered to be bioactive components in human infant nutrition because they act as anti-adhesive (2) and prebiotic factors (3) in the infant’s gastrointestinal system. They inhibit the enterotoxic effects of Escherichia coli and Vibrio cholerae (1), reduce the adhesion of enterotoxigenic E. coli (ETEC) and enteropathogenic E. coli to human intestinal cells (2), and influence the composition of the fecal flora in preterm infants (3).

Human and bovine milk vary in the total amount and the composition of gangliosides (5–7). The total amount of gangliosides in human colostrum and mature human milk is 9.51 ± 1.16 mg lipid-bound Sia (LBSA)/L and 9.07 ± 1.15 mg LBSA/L, respectively (5). In contrast, the total amount of ganglioside in mature bovine milk is significantly lower (3.98 ± 0.25 mg LBSA/L, P < 0.01). As a consequence, the ganglioside content in bovine milk based infant formula is also significantly lower compared with human milk (5,8). In addition, not only the quantity but also the composition of bovine milk gangliosides differs from those in human milk. The monosialoganglioside [Sia 2–3 galactose (Gal) ß1–4 glucose (Glc) ß1–1 ceramide] (GM₃) is the main ganglioside in mature human milk (5,6), whereas the disialoganglioside GD₃ (Sia 2–8 Sia 2–3 Gal ß1–4 Glc ß1–1 ceramide) dominates in human colostrum and in mature bovine milk (5–7). Most of these studies compare the ganglioside composition in human milk, bovine milk, and infant milk formula according to the oligosaccharide-based nomenclature (5–8), but little is known about the fatty acid composition of milk gangliosides. However, their fatty acid composition might be of importance for human infant nutrition. Although there is no proof that dietary gangliosides are required for growth and survival of the neonate, it has been shown that exogenous gangliosides are taken up by cells and modulate cell function (11). The fatty acid composition of gangliosides influences membrane fluidity (12,13) and alters the formation of sphingolipid clusters in the cell membrane (14,15), which is important for cell–cell interactions, receptor–ligand interactions, and signaling pathways (15,16). In conclusion, not only the oligosaccharide structure but also the fatty acid composition determine the physiological effects of gangliosides.

In view of the potential biological importance and the putative impact for human infant nutrition, we analyzed the fatty acid compositions of the 2 main gangliosides GM₃ and GD₃ in pooled samples from mature human milk and compared them with the fatty acid composition of the respective gangliosides in pooled samples from mature bovine milk.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Preparation of human milk gangliosides. Mature human milk was provided by the milk bank of the Children Hospital of Chemnitz, Germany, and was collected according to the German recommendations of human milk banking (17). Milk samples were drawn after 10 d of lactation from breast feeding mothers of term infants (gestational age: 37–42 wk), after milk secretion exceeded the request of the infant. A 10-mL milk sample was collected and frozen at –80°C within 15 min after collection. Samples were stored at –80°C for <3 mo. For ganglioside extraction, samples from 21 donors were thawed on ice, pooled, and processed immediately.

We extracted total lipids from pooled human milk according to the method by Bligh and Dyer (18) and isolated the gangliosides with the partition method described by Ladisch and Gillard (19). Briefly, we dissolved dried total lipid extracts in 4 mL diisopropylether:1-butanol (60:40, v:v), added 2 mL water, and centrifuged the samples at 750 x g for 10 min at 4°C. To remove triacylglycerides and phospholipids, we discarded the upper organic layer and washed the lower aqueous layer twice with 4 mL diisopopylether:1-butanol (60:40, v:v). We dissolved dried crude ganglioside extracts in chloroform:methanol:0.1 mol/L potassium chloride (3:98:74, by vol) and further purified them using C18(EC) reversed-phase cartridges [Isolute C18(EC), Separtis GmbH] according to the method by Williams and McCluer (20). Briefly, we applied the samples to the cartridges, washed with chloroform:methanol:0.1 mol/L potassium chloride (3:98:74, by vol), water, and methanol:water (1:1, v:v), and subsequently eluted the gangliosides with methanol and chloroform:methanol (2:1, v:v).

We separated different ganglioside fractions on HPLC plates (precoated with silica gel 60; Merck Eurolab) with chloroform:methanol:20 mmol/L aqueous CaCl₂ (1:0.8:0.2, by vol) (21) as the mobile phase and detected the gangliosides with resorcinol HCl (22) or primuline (23) for analytical or preparative purposes, respectively. We scraped the silica gel from the glass plates, extracted the gangliosides with chloroform/methanol (1:1, v:v), and dried the fractions under a stream of nitrogen.

GM₃ and GD₃ standards from pooled samples of mature bovine milk were obtained from Matreya.

    Identification with matrix-assisted laser-desorption/ionization MS. To characterize the isolated fractions with matrix-assisted laser-desorption/ionization MS (MALDI-TOF-MS) (24), we dissolved the dried samples in methanol to a final concentration of 1 g/L, mixed 1 µL of these samples with 1 µL of 2,5-dihydroxybenzoic acid (20 g/L in water) on a stainless steel target, and dried the mixture under a gentle stream of cold air. MALDI-TOF-MS was performed on a Voyager-DE-STR system (PerSeptiveBiosystems) equipped with a nitrogen laser emitting at 337 nm wavelength. The instrument was operated in the linear ion mode with delayed extraction and an acceleration voltage of 20 kV. The achieved mass accuracy was better than ±0.1%.

    Fatty acid analysis. To analyze the fatty acid composition of milk gangliosides with GLC, we generated FAME according to the method by Lepage and Roy (25). Briefly, we dissolved the dried ganglioside fractions in 2 mL methanol:hexane (4:1, v:v), added pyrogallol as antioxidant, and carefully added 200 µL acetyl chloride. Afterward, we incubated the samples for 1 h at 100°C. After cooling the samples down to room temperature, we added 4.85 mL potassium carbonate to stop the reaction. After centrifugation for 10 min at 1600 x g, we removed the upper hexane layer containing the FAME. We analyzed the FAME with quantitative capillary GLC on a CP 9000 system (Chrompack GmbH) equipped with a minibore column DB 23 (J&W Scientific) and a flame ionization detector (26). We identified the fatty acids according to their retention times. In addition, we analyzed the FAME with a GC-MS system (ThermoQuest/Finnigan) and identified the fatty acids according to their mass spectra. The content of each fatty acid is given as the percentage of the total amount of fatty acids on a weight basis.

    Statistics. Results are given as means ± SD from 2 independent extractions and analyses. Differences in the fatty acid composition between GM₃ and GD₃ within the same species, as well as differences between human and bovine milk within the same ganglioside fraction (GM₃ or GD₃), were tested by two-tailed Student’s t test. P < 0.05 is considered significant.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
MALDI-TOF-MS analysis of the predominant ganglioside fractions isolated from human milk revealed mass distributions that we identified as different compositional variations of GM₃ (Fig. 1A) and GD₃ (data not shown). The mass distribution ascribed to GM₃ ranged from 1176 to 1326 Da, whereas the molecular masses of GD₃ were between 1523 and 1624 Da. Each of the mass peaks can be explained by MALDI-induced formation of ganglioside-alkali adduct ions, such as [M + Na]⁺ and [M + K]⁺. The 28 Da intervals within the peak cluster can be explained by chain-length variations in the sphingoid base or fatty acid with an even number of CH₂ groups. For example, the [M + Na]⁺ adduct of a GM₃ molecule containing a ceramide-residue with 36 C atoms, and one double bond (e.g., sphingosine and stearic-acid, d18:1-C18:0-GM₃) has a theoretical mass of 1204.48 Da. We found a respective peak at 1203.99 Da, which is within the mass accuracy of the MALDI-TOF-MS system. Because of the high salt content in the human ganglioside samples, we also detected double-sodium adduct ions of the different compositional variations of GM₃ ([M + 2Na-H]⁺) with a mass shift of +22 Da compared with their respective single-sodium adduct ions [M + Na]⁺.

View larger version (23K): [in this window] [in a new window]   FIGURE 1 MALDI-TOF mass spectra of human (A) and bovine (B) milk GM3. MALDI-induced loss of Sia results in a mass shift of –291 Da. Both [M + Na]+ and [M + 2Na-H]+ ions ([M + Na]+ + 22 Da) were detected in human GM3, whereas [M + Na]+ ions dominate the bovine GM3 spectrum. Heterogeneity in the ceramide composition results in 28 Da and 14 Da intervals in human and bovine GM3, respectively.

The MALDI-TOF-MS of the predominant ganglioside fractions from bovine milk were similar to the GM₃ and GD₃ fractions isolated from human milk. We mainly detected monosodium adduct ions [M + Na]⁺ and also found the 291 Da mass shifts, indicating a MALDI-induced loss of Sia residues (Fig. 1B). However, while detecting 28 Da intervals in the mass peak clusters when analyzing human milk gangliosides, we detected 14 Da intervals in the peak clusters of bovine milk gangliosides, which can be explained by chain-length variations in the sphingoid base or fatty acid with an even or odd number of CH₂ groups (Fig. 1B).

We further analyzed and compared the fatty acid compositions of the GM₃ and GD₃ fractions from both human and bovine milk (Table 1). In human milk, the main fatty acids of the GM₃ fraction were 22:0, 18:0, 16:0, and 24:0, whereas 18:0, 16:0, 19:0, and 22:0 dominated in the GD₃ fraction. In contrast, the fatty acid compositions of the 2 analyzed bovine milk gangliosides, GM₃ and GD₃, were dominated by 23:0, 22:0, and 24:0. Human and bovine milk gangliosides differ in the amount of fatty acids with 20 or more C atoms; these fatty acids account for 51.48 ± 0.90% and 34.04 ± 3.11% of total fatty acids in the ganglioside fraction of human milk GM₃ and GD₃, respectively. In contrast, the amount of these fatty acids was much higher in bovine milk gangliosides with 73.71 ± 4.53% in GM₃ and 79.19 ± 3.57% in GD₃. The amount of fatty acids with 19 C atoms and less was higher in human milk gangliosides compared with bovine milk gangliosides.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Glycosphingolipids are potent bioactive compounds and alterations in their fatty acid composition modify their physiological effects. Here, we show that milk gangliosides are selectively enriched with certain fatty acids and that the fatty acid composition differs significantly between human and bovine milk gangliosides. So far we can only speculate whether these differences alter the physiological effects of milk gangliosides.

Compared with the fatty acid composition of whole human milk lipids (27), the 2 analyzed human milk gangliosides contain more saturated and monounsaturated long-chain fatty acids with 20 or more C atoms; >50% of the gangliosides consist of these fatty acids, whereas they play only a minor role in whole human milk with <2%. On the other hand, long-chain PUFA, oleic acid, and fatty acids with 16 or less C atoms are more common in whole human milk lipids compared with the analyzed gangliosides. A similar selectivity could be found comparing the fatty acid composition of bovine milk gangliosides with whole bovine milk lipids (28). Why milk gangliosides are selectively enriched with certain fatty acids and whether this enrichment is of physiological importance is yet unknown.

The fatty acid composition of gangliosides from pooled samples of mature human and bovine milk differs significantly. The 14 Da mass shifts in the MALDI-TOF spectra of bovine milk gangliosides indicate the presence of odd numbered fatty acids, which was confirmed by GC-MS analysis. The odd numbered fatty acid 23:0 is the predominant fatty acid in bovine milk gangliosides (24.05 ± 1.37% in GM₃ and 26.66 ± 1.24% in GD₃), whereas its concentration in human milk gangliosides is only minor (2.88 ± 0.10% in GM₃ and 1.84 ± 0.29% in GD₃). Whether these significant differences between human and bovine milk gangliosides influence their physiological effects is unknown but may well be possible as speculated below.

In light of the wide variations in content and composition of milk gangliosides over the time of lactation, but also between individuals (5–7), the results from pooled samples have their limits. However, the amount of certain fatty acids, e.g., 23:0, differs significantly between the pooled samples from human and bovine milk gangliosides, providing a first insight into interspecies differences. With respect to the individual variations within one species and the changes over time of lactation (5–7), one could even speculate whether possible differences in the fatty acid composition also affect the physiological effects of milk gangliosides.

Although gangliosides are generally distinguished by their oligosaccharide chain, the ceramide moiety and its fatty acid composition become more and more important for the diverse biological effects exerted by gangliosides. Milk gangliosides reduce the adhesion of pathogens and promote the growth of bifidobacteria in the infant’s gastrointestinal system. Until recently, explanations for the underlying mechanisms had been based on their oligosaccharide structure (1–3). However, Martin et al. (29) reported that ETEC strains bind to gangliosides in a ceramide-dependent process. Adhesion of the ETEC strains changed with differences in the sphingoid base and fatty acid composition, whereas the oligosaccharide moiety remained unchanged (29). In another study, Ladisch et al. (30) reported an inverse relation between the fatty-acid chain length of the investigated gangliosides and their immunosuppressive activity. Monosialogangliosides with short and medium chain fatty acids (d18:1-C2:0-GM₃ and d18:1-C14:0-GM₃) were more immunosuppressive than those with long-chain fatty acids (d18:1-C18:0-GM₃ and d18:1-C24:0-GM₃). Both the oligosaccharide chain (GM₃) and the sphingoid base (d18:1) remained unchanged and only the fatty acid composition was modified (30). Although the latter study is independent of milk gangliosides, it corroborates the hypothesis that the physiological functions of gangliosides are not always determined only by the oligosaccharide structure but also by the sphingoid base and the fatty acid composition. Here, we report that the fatty acid compositions of gangliosides from mature human milk and mature bovine milk vary significantly and that the bovine milk is the major source for gangliosides in infant milk formula (5,8). Whether these differences result in physiological distinctions between breast-fed and formula-fed infants and therefore are of importance for human infant nutrition needs to be further elucidated.

	FOOTNOTES

 
¹ The authors confirm that all potential conflicts of interest, including patents they hold and the opportunity for their company to profit from this research, are disclosed.

³ Present address: The Burnham Institute, Glycobiology and Carbohydrate Chemistry Program, La Jolla, CA 92037.

⁴ Abbreviations used: ETEC, enterotoxigenic Escherichia coli; Gal, galactose; GD₃, disialoganglioside (Sia 2–8 Sia 2–3 Gal ß1–4 Glc ß1–1 ceramide); Glc, glucose; GM₃, monosialoganglioside (Sia 2–3 Gal ß1–4 Glc ß1–1 ceramide); LBSA, lipid-bound sialic acid; MALDI-TOF-MS, matrix-assisted laser desorption/ionization time of flight MS; Sia, sialic acid.

Manuscript received 2 April 2004. Initial review completed 27 April 2004. Revision accepted 26 August 2004.

	LITERATURE CITED

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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