Developmental changes in the level of free and conjugated sialic acids, Neu5Ac, Neu5Gc and KDN in different organs of pig: a LC-MS/MS quantitative analyses
Recent studies have shown a relationship between the level of the sialic acid (Sia), N-glycolylneuraminic acid (Neu5Gc) in red meat and its risk in cancer, cardiovascular and inflammatory diseases. Unresolved is the Sia concentration in different organs of piglets during development. Our aim was to determine the level of free and conjugated forms of Neu5Gc, N-acetylneuraminic acid (Neu5Ac) and ketodeoxynonulsonic acid (Kdn) in fresh and cooked spleen, kidney, lung, heart, liver, and skeletal muscle from 3-days-old (n = 4–8), 38-days-old (n = 10) and adult piglets (n = 4) by LC-MS/MS. Our findings show: (1) Lung tissue from 3 days-old piglets contained the highest level of total Sia (14.6 μmol/g protein) compared with other organs or age groups; (2) Unexpectedly, Neu5Gc was the major Sia in spleen (67–79 %) and adult lung (36–49 %) while free Kdn was the major Sia in skeletal muscle. Conjugated Neu5Ac was the highest Sia in other organs (61–84 %); (3) Skeletal muscle contained the lowest concentration of Neu5Gc in fresh and cooked meat; (4) Kdn accounted for <5 % of the total Sia in most organs; (5) During development, the total Sia concentration showed a 44–79 % decrease in all organs; (6) In adult piglets, the high to low rank order of total Sia was lung, heart, spleen, kidney, liver and skeletal muscle. In conclusion, the high level of Neu5Gc in all organs compared to skeletal muscle is a potential risk factor suggesting that dietary consumption of organ meats should be discouraged in favor of muscle to protect against cancer, cardiovascular and other inflammatory diseases.
KeywordsSialic acids Neu5Gc LC-MS/MS Development Pig
2-keto-3-deoxy-D-glycero- D-galacto-nononic acid (Ketodeoxynonulosonic acid)
Liquid chromatography-tandem mass spectrometry
This study was funded by research grants from the School of Medicine, Xiamen University.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
This article does not contain any studies with human participants performed by any of the authors.
- 8.Diaz S.L., Padler-Karavani V., Ghaderi D., Hurtado-Ziola N., Yu H., Chen X., Brinkman-Van der Linden E.C.M., Varki A., Varki N.M.: Sensitive and Specific Detection of the Non-Human Sialic Acid N-Glycolylneuraminic Acid In Human Tissues and Biotherapeutic Products. PLoS ONE. 4(1), e4241 (2009). doi: 10.1371/journal.pone.0004241 CrossRefPubMedPubMedCentralGoogle Scholar
- 9.Inoue S., Lin S.L., Chang T., Wu S.H., Yao C.W., Chu T.Y., Troy 2nd F.A., Inoue Y.: Identification of free deaminated sialic acid (2-keto-3-deoxy-D-glycero-D-galacto- nononic acid) in human red blood cells and its elevated expression in fetal cord red blood cells and ovarian cancer cells. J. Biol. Chem. 273(42), 27199–27204 (1998)CrossRefPubMedGoogle Scholar
- 11.Morimoto N., Nakano M., Kinoshita M., Kawabata A., Morita M., Oda Y., Kuroda R., Kakehi K.: Specific distribution of sialic acids in animal tissues as examined by LC-ESI-MS after derivatization with 1, 2-diamino-4, 5-methylenedioxybenzene. Anal. Chem. 73(22), 5422–5428 (2001)CrossRefPubMedGoogle Scholar
- 14.Karunanithi, D., Radhakrishna, A., Biju, V.: Quantitative determination of sialic acid in Indian milk and milk products. International Journal of Applied Biology and P (2013)Google Scholar
- 20.Stasche R., Hinderlich S., Weise C., Effertz K., Lucka L., Moormann P., Reutter W.: A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver - Molecular cloning and functional expression of UDP-N-acetyl-glucosamine 2-epimerase/N-acetylmannosamine kinase. J. Biol. Chem. 272(39), 24319–24324 (1997). doi: 10.1074/jbc.272.39.24319 CrossRefPubMedGoogle Scholar
- 21.Hinderlich S., Stasche R., Zeitler R., Reutter W.: A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver - Purification and characterization of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase. J. Biol. Chem. 272(39), 24313–24318 (1997). doi: 10.1074/jbc.272.39.24313 CrossRefPubMedGoogle Scholar
- 25.Drake P.M., Nathan J.K., Stock C.M., Chang P.V., Muench M.O., Nakata D., Reader J.R., Gip P., Golden K.P., Weinhold B., Gerardy-Schanh R., Troy II F.A., Bertozzi C.R.: Polysialic acid, a glycan with highly restricted expression, is found on human and murine leukocytes and modulates immune responses. J. Immunol. 181(10), 6850–6858 (2008)CrossRefPubMedPubMedCentralGoogle Scholar
- 28.Samraj A.N., Pearce O.M., Laubli H., Crittenden A.N., Bergfeld A.K., Banda K., Gregg C.J., Bingman A.E., Secrest P., Diaz S.L., Varki N.M., Varki A.: A red meat-derived glycan promotes inflammation and cancer progression. Proc.Natl. Acad. Sci. U. S. A. 112(2), 542–547 (2015). doi: 10.1073/pnas.1417508112 CrossRefPubMedGoogle Scholar
- 29.Hedlund M., Tangvoranuntakul P., Takematsu H., Long J.M., Housley G.D., Kozutsumi Y., Suzuki A., Wynshaw-Boris A., Ryan A.F., Gallo R.L., Varki N., Varki A.: N-glycolylneuraminic acid deficiency in mice: implications for human biology and evolution. Mol. Cell. Biol. 27(12), 4340–4346 (2007). doi: 10.1128/MCB.00379-07 CrossRefPubMedPubMedCentralGoogle Scholar
- 33.Larsen J.: Meat consumption in China now double that in the United States. Earth Policy Institute. 24, (2012)Google Scholar
- 37.Cheng Y.: Chinese dietary reference intake. 2013 revision introduction. Acta Nutrimenta Sinica. 36, 313–315 (2014)Google Scholar
- 38.Chen Y., Pan L.L., Liu N., Troy F.A., Wang B.: LC-MS/MS quantification of N-acetylneuraminic acid, N-glycolylneuraminic acid and ketodeoxynonulosonic acid levels in the urine and potential relationship with dietary sialic acid intake and disease in 3- to 5-year-old children. Brit J Nutr. 111(2), 332–341 (2014). doi: 10.1017/S0007114513002468 CrossRefPubMedGoogle Scholar