Abstract
Mucins are high molecular weight epithelial proteins, strongly glycosylated, and are the main component of the mucus. Since mucus secretion can be altered in diseases, colon mucins can be regarded as a biomarker of chronic inflammatory bowel diseases or preneoplastic changes. Conventional histochemistry and lectin histochemistry combined with chemical treatment and enzymatic digestion were carried out to analyze the colon mucins in mice fed a high-fat diet for 25 weeks, a period sufficient to induce simple liver steatosis, to check whether the carbohydrate features of mucus can be altered by an inadequate diet. An increase in the sialo/sulfomucins ratio with respect to control mice, assessed by computerized image analysis, was observed in the colon, although differences in sialic acid acetylation between control and mice fed a high-fat diet were not found. High-fat diet was also associated with altered lectin-binding pattern of the mucus, with a probable shortening of oligosaccharide chains of glycoproteins. This pattern was leading to over-expression of Galβ1,3GalNAc terminal dimers (TF antigen) and GalNAc terminal residues (Tn antigen). This altered composition of mucins can be related to a defect in the process of glycosylation, or to incomplete maturation of goblet cells, and may be an early indication of preneoplastic and neoplastic changes. In conclusion, our findings confirm that a fatty-rich diet (Western-style diet) induces alteration of mucins and may be associated with colon diseases. Our investigation corroborates the usefulness of lectins histochemistry in the early diagnosis of prepathological states of the colon.
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References
Accili D, Menghi G, Gabrielli MG (2008) Lectin histochemistry for in situ profiling of rat colon sialoglycoconjugates. Histol Histopathol 23(7):863–875
Becker DJ, Lowe JB (2003) Fucose: biosynthesis and biological function in mammals. Glycobiology 13:41R–53R
Boland CR, Montgomery CK, Kim YS (1982) Alterations in human colonic mucin occurring with cellular differentiation and malignant transformation. Med Sci 79:2051–2055
Bonfrate L, Tack J, Grattagliano I, Cuomo R, Portincasa P (2013) Microbiota in health and irritable bowel syndrome: current knowledge, perspectives and therapeutic options. Scand J Gastroenterol 48:995–1009
Campbell BJ, Finnie IA, Hounsell EF, Rhodes JM (1995) Direct demonstration of increased expression of Thomsen-Friedenreich (TF) antigen in colonic adenocarcinoma and ulcerative colitis mucin and its concealment in normal mucin. J Clin Invest 95(2):571–576
Campbell BJ, Rowe GE, Leiper K, Rhodes JM (2001) Increasing the intra-Golgi pH of cultured LS174T goblet-differentiated cells mimics the decreased mucin sulfation and increased Thomsen-Friedenreich antigen (Galβ1-3GalNacα-) expression seen in colon cancer. Glycobiology 11(5):385–393
Croix JA, Carbonero F, Nava GM, Russell M, Greenberg E, Gaskins H (2011) On the relationship between sialomucin and sulfomucin expression and hydrogenotrophic microbes in the human colonic mucosa. PLoS ONE 6(9):e24447
Culling CF, Reid PE, Burton JD, Dunn WL (1975) A histochemical method of differentiating lower gastrointestinal tract mucin from other mucins in primary or metastatic tumours. J Clin Pathol 28:656–658
Dykstra NS, Hyde L, Adawi D, Kulik D, Ahrne S, Molin G et al (2011) Pulse probiotic administration induces repeated small intestinal Muc3 expression in rats. Pediatr Res 69(3):206–211
Erdely I, Levenkova N, Lin EY, Pinto JT, Lipkin M, Quimby FW et al (2009) Western-style diets induce oxidative stress and dysregulate immune responses in the colon in a mouse model of sporadic colon cancer. J Nutr 139(11):2072–2078
Greening DW, Ji H, Kapp EA, Simpson RJ (2013) Sulindac modulates secreted protein expression from LIM1215 colon carcinoma cells prior to apoptosis. Biochim Biophys Acta 1834(11):2293–2307
Grundy SM (2005) Metabolic syndrome: therapeutic considerations. Handb Exp Pharmacol 170:107–133
Hurd EA, Holmen JM, Hansson GC, Domino SE (2005) Gastrointestinal mucins of Fut2-null mice lack terminal fucosylation without affecting colonization by Candida albicans. Glycobiology 15:1002–1007
Ionilă SS, Mărgăritescu CL, Pirici D, Mogoantră SS (2011) Mucinous adenocarcinoma of the colon—a histochemical study. Rom J Morphol Embryol 52(3):783–790
Johansson ME, Larsson JM, Hansson GC (2011) The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci 108(Suppl. 1):4659–4665
Kim CH, Oh Y, Ha Y, Ahn Q, Kim SH, Cho KD et al (2010) Expression of mucins in the mucosal surface of small intestines in 1 week-old pigs. J Vet Med Sci 72(2):245–247
Larsson JM, Karlsson H, Sjovall H, Hansson GC (2009) A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn. Glycobiology 19:756–766
Liquori GE, Calamita G, Cascella D, Mastrodonato M, Portincasa P, Ferri D (2009) An innovative methodology for the automated morphometric and quantitative estimation of liver steatosis. Histol Histopathol 24:49–60
Liquori GE, Mastrodonato M, Mentino D, Scillitani G, Desantis S, Portincasa P et al (2012) In situ characterization of O-linked glycans of Muc2 in mouse colon. Acta Histochem 114:723–732
Martinez-Menarguez JA, Ballesta J, Aviles M, Madrid JF, Castells MT (1992) Influence of sulphate groups in the binding of peanut agglutinin. Histochemical demonstration with light- and electron-microscopy. Histochem J 24(4):207–216
Mastrodonato M, Calamita G, Rossi R, Scillitani G, Liquori GE, Ferri D (2009) Expression of H + , K + -ATPase and glycopattern analysis in the gastric glands of Rana esculenta. J Histochem Cytochem 57(3):215–225
Mastrodonato M, Calamita G, Rossi R, Mentino D, Bonfrate L, Portincasa P et al (2011) Altered distribution of caveolin-1 in early liversteatosis. Eur J Clin Invest 41(6):642–651
Mastrodonato M, Portincasa P, Mentino D, Rossi R, Resta L, Ferri D et al (2012) Caveolin-1 and mitochondrial alterations in regenerating rat liver. Microsc Res Tech 75(8):1026–1032
Mastrodonato M, Mentino D, Liquori GE, Ferri D (2013) Histochemical characterization of the sialic acid residues in mouse colon mucins. Microsc Res Tech 76:156–162
Milton JD, Eccleston D, Parker N, Raouf A, Cubbin C, Hoffman J et al (1993) Distribution of O-acetylated sialomucins in the normal and diseased gastrointestinal tract shown by a new monoclonal antibody. J Clin Pathol 46:323–329
Newmark HL, Yang K, Lipkin M, Kopelovich L, Liu Y, Fan K et al (2001) A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice. Carcinogenesis 11:1871–1875
Parillo F, Diverio S, Todini L, Fagioli O (2001) Histochemical detection of the lectin-binding carbohydrates in the zona pellucida during oocyte growth in the wild boar (Sus scrofa scrofa). Vet Res 32:581–590
Plendl J, Schönleber B, Schmahl W, Schumacher U (1989) Comparison of the unmasking of lectin receptors by neuraminidase and by enzyme-free buffer alone. J Histochem Cytochem 37:1743–1744
Rhodes JM, Gallimore R, Elias E, Allan RN, Kennedy JF (1985) Alimentary tract and pancreas Faecal mucus degrading glycosidases in ulcerative colitis and Crohn’s disease. Gut 26:761–765
Ryder SD, Smith JA, Rhodes JM (1992) Peanut lectin: a mitogen for normal human colonic epithelium and human HT29 colorectal cancer cells. J Natl Cancer Inst 84(18):1410–1416
Sharma R, Schumacher U (1995) The influence of diets and gut microflora on lectin binding patterns of intestinal mucins in rats. Lab Invest 73(4):558–564
Sharma R, Schumacher U, Adam E (1998) Lectin histochemistry reveals the appearance of M-cells in Peyer’s patches of SCID mice after syngeneic normal bone marrow transplantation. J Histochem Cytochem 46(2):143–148
Sheng YH, Hasnain SZ, Florin TH, McGuckin MA (2012) Mucins in inflammatory bowel diseases and colorectal cancer. J Gastroenterol Hepatol 27(1):28–38
Spicer SS, Leppi TJ, Stoward PJ (1965) Suggestions for a histochemical terminology of carbohydrate-rich tissue components. J Histochem Cytochem 13:599–603
Sugihara K, Jass JR (1986) Colorectal goblet cell sialomucin heterogeneity: its relation to malignant disease. J Clin Pathol 39:1088–1095
Tobisawa Y, Imai Y, Fukuda M, Kawashima H (2010) Sulfation of colonic mucins by N acetylglucosamine 6-O-sulfotransferase-2 and its protective function in experimental colitis in mice. J Biol Chem 285:6750–6760
Tsai HH, Dwarakanath AD, Hart CA, Milton JD, Rhodes JM (1995) Increased faecal mucin sulphatase activity in ulcerative colitis: a potential target for treatment. Gut 36:570–576
Willett WC (1998) Nutritional epidemiology, vol 30. Oxford University Press, New York
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Mastrodonato, M., Mentino, D., Portincasa, P. et al. High-fat diet alters the oligosaccharide chains of colon mucins in mice. Histochem Cell Biol 142, 449–459 (2014). https://doi.org/10.1007/s00418-014-1221-2
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DOI: https://doi.org/10.1007/s00418-014-1221-2