Abstract
In the digestive tract of mice (HR-1, 5 months old, ♀), asialo GM1 (GA1) exhibiting receptor activity toward several intestinal bacteria was preferentially expressed in the small intestine. Also, less than 10% of GA1 in the small intestine was converted into fucosylated and sulfated derivatives, but it was completely converted to fucosyl GA1 (FGA1) in the stomach, cecum and colon. Among the lipid components in these tissues, glycolipids other than Forssman antigen and cholesterol sulfate (CS) were present in the digestive tract contents. However, sulfated GA1, sulfatide and fucosyl GM1 in the gastro-intestinal contents were not present in the cecal and colonic contents, in which the major glycolipids were ceramide monohexoside (CMH), GA1 and FGA1. The total amount of GA1 in the whole contents was 20% of that in the tissues. Thus, glycolipids were stable during the process of digestion, and excreted from the body together with cholesterol and CS. On the other hand, Lactobacillus johnsonii (LJ), whose receptor is GA1, was detected in the cecal and colonic contents on sequential analysis of 16S-ribosomal RNA and TLC-immunostaining of antigenic glycolipids with anti-LJ antiserum. LJ was found to comprise 20% of the total bacteria cultured in the lactobacillus medium under aerobic conditions, and to be present in the cecal and colonic contents, 9.8 × 107 cells versus 37 μg GA1 and 1.4 × 108 cells versus 49 μg GA1, respectively. Thus, GA1 in the contents might facilitate the discharge of intestinal bacteria by becoming attached them to prevent their irregular diffusion.
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Abbreviations
- CMH:
-
ceramide monohexoside
- CS:
-
cholesterol sulfate
- 18t:0:
-
phytosphingosine
- 18d:1:
-
sphingosine
- 24h:0:
-
α-hydroxylignoceric acid
- GA1:
-
asialo GM1
- FGA1:
-
fucosyl GA1
- FGM1:
-
fucosyl GM1
- SGA1:
-
sulfated GA1
- LJ:
-
Lactobacillus johnsonii
References
IUPAC-IUB Commission on Biochemical Nomenclature: The Nomenclature of Lipids. Eur. J. Biochem. 179, 11–21 (1977)
Karlsson, K.A.: Animal glycosphingolipids as membrane attachment sites for bacteria. Annu. Rev. Biochem. 58, 309–350 (1989)
Yamamoto, K., Miwa, T., Taniguchi, H., Nagano, T., Shimamura, K., Tanaka, T., Kumagai, H.: Binding specificity of Lactobacillus to glycolipids. Biochem. Biophys. Res. Commun. 228, 148–152 (1996)
Neeser, J.R., Granato, D., Rouvet, M., Servin, A., Teneberg, S., Karlsson, K.A.: Lactobacillus johnsonii La1 shares carbohydrate-binding specificities with several enteropathogenic bacteria. Glycobiology 10, 1193–1199 (2000)
Iwamori, M., Shibagaki, T., Nakata, Y., Adachi, S., Nomura, T.: Distribution of receptor glycolipids for lactobacilli in the murine digestive tract and production of antibodies cross-reactive with them by immunization of rabbits with lactobacilli. J. Biochem. 146, 185–191 (2009)
Lin, B., Hayashi, Y., Saito, M., Sakakibara, Y., Yanagisawa, M., Iwamori, M.: GDP-fucose: beta-galactoside alpha1, 2-fucosyltransferase, MFUT-II, and not MFUT-I or -III, is induced in a restricted region of the digestive tract of germ-free mice by host-microbe interactions and cycloheximide. Biochim. Biophys. Acta 1487, 275–285 (2000)
Bry, L., Falk, P.G., Midtvedt, T., Gordon, J.I.: A model of host-microbial interactions in an open mammalian ecosystem. Science 273, 1380–1383 (1996)
Iwamori, M., Domino, S.E.: Tissue-specific loss of fucosylated glycolipids in mice with targeted deletion of α(1, 2)fucosyltransferase genes. Biochem. J. 380, 75–81 (2004)
Yoneshige, A., Sasaki, A., Miyazaki, M., Kojima, N., Suzuki, A., Matsuda, J.: Developmental changes in glycolipids and synchronized expression of nutrient transporters in the mouse small intestine. J. Nutr. Biochem. 21, 214–226 (2010)
Gustafsson, B.E., Karlsson, K.A., Larson, G., Midtvedt, T., Strömberg, N., Teneberg, S., Thurin, J.: Glycosphingolipid patterns of the gastrointestinal tract and feces of germ-free and conventional rats. J. Biol. Chem. 261, 15294–15300 (1986)
Larson, G., Watsfeldt, P., Falk, P., Leffler, H., Koprowski, H.: Fecal excretion of intestinal glycosphingolipids by newborns and young children. FEBS Lett. 214, 41–44 (1987)
Larson, G., Falk, P., Hoskins, L.C.: Degradation of human intestinal glycosphingolipids by extracellular glycosidases from mucin-degrading bacteria of the human fecal flora. J. Biol. Chem. 263, 10790–10798 (1988)
Manual of microbiological culture media, Difco & BBL Manual, Becton, Dickinson and Company, Sparks, MD, USA (2003)
Iwamori, M., Ohta, Y., Uchida, Y., Tsukada, Y.: Arthrobacter ureafaciens sialidase isoenzymes, L, M1 and M2, cleave fucosyl GM1. Glycoconj. J. 14, 67–73 (1997)
Iwamori, M., Kaido, T., Iwamori, Y., Ohta, Y., Tsukamoto, K., Kozaki, S.: Involvement of the C-terminal tail of Arthrobacter ureafaciens sialidase isoenzyme M in cleavage of the internal sialic acid of ganglioside GM1. J. Biochem. 138, 327–334 (2005)
Iwamori, M., Takamizawa, K., Momoeda, M., Iwamori, Y., Taketani, Y.: Gangliosides in human, cow and goat milk, and their abilities as to neutralization of cholera toxin and botulinum type A neurotoxin. Glycoconj. J. 25, 675–683 (2008)
Woese, C.R., Kandler, O., Wheelis, M.L.: Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990)
Leffler, H., Hansson, G.C., Strömberg, N.: A novel sulfoglycosphingolipid of mouse small intestine, IV3-sulfogangliotetraosylceramide, demonstrated by negative ion fast atom bombardment mass spectrometry. J. Biol. Chem. 261, 1440–1444 (1986)
Shaw, N.: Bacterial glycolipids. Bacteriol. Rev. 34, 365–377 (1970)
Shaw, N., Baddiley, J.: Structure and distribution of glycosyl diglycerides in bacteria. Nature 217, 142–144 (1970)
Suzuki, A., Yamakawa, T.: The different distributions of asialo GM1 and Forssman antigen in the small intestine of mouse demonstrated by immunofluorescence staining. J. Biochem. 90, 1541–1544 (1981)
Kono, M., Dreier, J.L., Ellis, J.M., Allende, M.L., Kalkofen, D.N., Sanders, K.M., Bielawski, J., Bielawska, A., Hannun, Y.A., Proia, R.L.: Neutral ceramidase encoded by the Asah2 gene is essential for the intestinal degradation of sphingolipids. J. Biol. Chem. 281, 7324–7331 (2006)
Cui, Y., Iwamori, M.: Distribution of cholesterol sulfate and its anabolic and catabolic enzymes in various rabbit tissues. Lipids 32, 599–604 (1997)
Sugiyama, T., Smith, P.F., Langworthy, T.A., Mayberry, W.R.: Immunological analysis of glycolipids and lipopolysaccharides derived from various mycoplasmas. Infect. Immun. 10, 1273–1279 (1974)
Alving, C.R., Fowble, J.W., Joseph, K.C.: Comparative properties of four galactosyl lipids as antigens in liposomes. Immunochemistry 11, 475–481 (1974)
Hirsch, H.E., Parks, M.E.: Serological reactions against glycolipid-sensitized liposomes in multiple sclerosis. Nature 264, 785–787 (1976)
Jacobs, B.C., Rothbarth, P.H., van der Meché, F.G., Herbrink, P., Schmitz, P.I., de Klerk, M.A., van Doorn, P.A.: The spectrum of antecedent infections in Guillain-Barré syndrome: a case-control study. Neurology 51, 1110–1115 (1998)
Houliston, R.S., Yuki, N., Hirama, T., Khieu, N.H., Brisson, J.R., Gilbert, M., Jarrell, H.C.: Recognition characteristics of monoclonal antibodies that are cross-reactive with gangliosides and lipooligosaccharide from Campylobacter jejuni strains associated with Guillain-Barré and Fisher syndromes. Biochemistry 46, 36–44 (2007)
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Iwamori, M., Iwamori, Y., Adachi, S. et al. Excretion into feces of asialo GM1 in the murine digestive tract and Lactobacillus johnsonii exhibiting binding ability toward asialo GM1. A possible role of epithelial glycolipids in the discharge of intestinal bacteria. Glycoconj J 28, 21–30 (2011). https://doi.org/10.1007/s10719-010-9320-3
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DOI: https://doi.org/10.1007/s10719-010-9320-3