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Published in: Digestive Diseases and Sciences 6/2011

01-06-2011 | Original Article

Myenteric Denervation Downregulates Galectin-1 and -3 Expression in Gastric Carcinogenesis

Authors: Cássia F. Estofolete, Sérgio Zucoloto, Sonia M. Oliani, Ana Cláudia Polli-Lopes, Cristiane D. Gil

Published in: Digestive Diseases and Sciences | Issue 6/2011

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Abstract

Background

This study evaluated the galectin-1 and -3 expression during N-methyl-N′-nitro-N-nitrosoguanidine (MNNG)-induced gastric carcinogenesis in denervated rat stomachs using benzalkonium chloride.

Method

Four experimental situations were evaluated: nondenervated and denervated stomachs without lesions and nondenervated and denervated stomachs with lesions. Sections of the pyloric region were stained with toluidine blue and incubated with mouse monoclonal anti-Gal-1 and rabbit polyclonal anti-Gal-3 for histopathological and immunohistochemical analysis, respectively.

Result

MNNG caused the development of benign and malignant epithelial lesions, which were more pronounced in nondenervated stomachs with lesions and accompanied by inflammatory cell-enriched stroma. By immunostaining, the epithelial cells, blood vessels, muscle layer, and myenteric plexus were Gal-1 and -3 positive. Gal-3 was also detected in the gastric crypts, mucus secretion, and fibroblasts of pyloric fragments. Development of lesions in denervated stomachs was associated with a significant decrease in Gal-1 and -3 expression in epithelial cells, mast cells, and neutrophil cytoplasm, compared with that of nondenervated stomach lesions (P < 0.01; P < 0.001; P < 0.001, respectively).

Conclusion

These results demonstrate that myenteric denervation downregulates endogenous Gal-1 and -3 expression, which might inhibit tumor development in this experimental model.
Literature
1.
go back to reference Rabinovich GA, Toscano MA. Turning ‘sweet’ on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol. 2009;9:338–352.PubMedCrossRef Rabinovich GA, Toscano MA. Turning ‘sweet’ on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol. 2009;9:338–352.PubMedCrossRef
2.
go back to reference Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer. 2005;5:29–41.PubMedCrossRef Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat Rev Cancer. 2005;5:29–41.PubMedCrossRef
3.
go back to reference Van Den Brule F, Califice S, Castronovo V. Expression of galectins in cancer: A critical review. Glycoconj J. 2004;19:537–542.PubMedCrossRef Van Den Brule F, Califice S, Castronovo V. Expression of galectins in cancer: A critical review. Glycoconj J. 2004;19:537–542.PubMedCrossRef
4.
go back to reference Lawrence T. Inflammation and cancer: A failure of resolution? Trends Pharmacol Sci. 2007;28:162–165.PubMedCrossRef Lawrence T. Inflammation and cancer: A failure of resolution? Trends Pharmacol Sci. 2007;28:162–165.PubMedCrossRef
5.
go back to reference Gil CD, Cooper D, Rosignoli G, Perretti M, Oliani SM. Inflammation-induced modulation of cellular galectin-1 and -3 expression in a model of rat peritonitis. Inflamm Res. 2006;55:99–107.PubMedCrossRef Gil CD, Cooper D, Rosignoli G, Perretti M, Oliani SM. Inflammation-induced modulation of cellular galectin-1 and -3 expression in a model of rat peritonitis. Inflamm Res. 2006;55:99–107.PubMedCrossRef
6.
go back to reference Pastrnak A, Jansa P, Kolar Z. Mastocytes in the process of cancerogenesis. I. Study of experimental model systems. Cesk Patol. 1986;22:210–213.PubMed Pastrnak A, Jansa P, Kolar Z. Mastocytes in the process of cancerogenesis. I. Study of experimental model systems. Cesk Patol. 1986;22:210–213.PubMed
7.
go back to reference Kondo K, Muramatsu M, Okamoto Y, et al. Expression of chymase-positive cells in gastric cancer and its correlation with the angiogenesis. J Surg Oncol. 2006;93:36–42.PubMedCrossRef Kondo K, Muramatsu M, Okamoto Y, et al. Expression of chymase-positive cells in gastric cancer and its correlation with the angiogenesis. J Surg Oncol. 2006;93:36–42.PubMedCrossRef
8.
go back to reference Estofolete CF, Botelho-Machado C, Taboga SR, Zucoloto S, Polli-Lopes AC, Gil CD. Effects of myenteric denervation on extracellular matrix fibers and mast cell distribution in normal stomach and gastric lesions. Cancer Cell Int. 2010;10:18.PubMedCrossRef Estofolete CF, Botelho-Machado C, Taboga SR, Zucoloto S, Polli-Lopes AC, Gil CD. Effects of myenteric denervation on extracellular matrix fibers and mast cell distribution in normal stomach and gastric lesions. Cancer Cell Int. 2010;10:18.PubMedCrossRef
9.
go back to reference Caruso RA, Ieni A, Fabiano V, Basile G, Inferrera C. Perivascular mast cells in advanced gastric adenocarcinomas: An electron microscopic study. Anticancer Res. 2004;24:2257–2263.PubMed Caruso RA, Ieni A, Fabiano V, Basile G, Inferrera C. Perivascular mast cells in advanced gastric adenocarcinomas: An electron microscopic study. Anticancer Res. 2004;24:2257–2263.PubMed
10.
go back to reference Caruso RA, Fedele F, Zuccalà V, Fracassi MG, Venuti A. Mast cell and eosinophil interaction in gastric carcinomas: Ultrastructural observations. Anticancer Res. 2007;27:391–394.PubMed Caruso RA, Fedele F, Zuccalà V, Fracassi MG, Venuti A. Mast cell and eosinophil interaction in gastric carcinomas: Ultrastructural observations. Anticancer Res. 2007;27:391–394.PubMed
11.
go back to reference Liang S, Hoskins M, Khanna P, Kunz RF, Dong C. Effects of the tumor-leukocyte microenvironment on melanoma-neutrophil adhesion to the endothelium in a shear flow. Cell Mol Bioeng. 2008;1:189–200.PubMedCrossRef Liang S, Hoskins M, Khanna P, Kunz RF, Dong C. Effects of the tumor-leukocyte microenvironment on melanoma-neutrophil adhesion to the endothelium in a shear flow. Cell Mol Bioeng. 2008;1:189–200.PubMedCrossRef
12.
go back to reference Souto JC, Vila L, Brú A. Polymorphonuclear neutrophils and cancer. Intense and sustained neutrophilia as a treatment against solid tumors. Med Res Rev. 2009; Dec 4 [Epub ahead of print]. Souto JC, Vila L, Brú A. Polymorphonuclear neutrophils and cancer. Intense and sustained neutrophilia as a treatment against solid tumors. Med Res Rev. 2009; Dec 4 [Epub ahead of print].
13.
go back to reference Polli-Lopes AC, Zucoloto S, Cunha FQ, Figueiredo LAS, Garcia SB. Myenteric denervation reduces the incidence of gastric tumors in rats. Cancer Lett. 2003;190:45–50.PubMedCrossRef Polli-Lopes AC, Zucoloto S, Cunha FQ, Figueiredo LAS, Garcia SB. Myenteric denervation reduces the incidence of gastric tumors in rats. Cancer Lett. 2003;190:45–50.PubMedCrossRef
14.
go back to reference Galinsky DS, Nechushtan H. Mast cells and cancer—No longer just basic science. Crit Rev Oncol Hematol. 2008;68:115–130.PubMedCrossRef Galinsky DS, Nechushtan H. Mast cells and cancer—No longer just basic science. Crit Rev Oncol Hematol. 2008;68:115–130.PubMedCrossRef
15.
go back to reference Van Der Zanden EP, Boeckxstaens GE, de Jonge WJ. The vagus nerve as a modulator of intestinal inflammation. Neurogastroenterol Motil. 2009;21:6–17.CrossRef Van Der Zanden EP, Boeckxstaens GE, de Jonge WJ. The vagus nerve as a modulator of intestinal inflammation. Neurogastroenterol Motil. 2009;21:6–17.CrossRef
16.
go back to reference Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458–462.PubMedCrossRef Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature. 2000;405:458–462.PubMedCrossRef
17.
go back to reference Galvis G, Lips KS, Kummer W. Expression of nicotinic acetylcholine receptors on murine alveolar macrophages. J Mol Neurosci. 2006;30:107–108.PubMedCrossRef Galvis G, Lips KS, Kummer W. Expression of nicotinic acetylcholine receptors on murine alveolar macrophages. J Mol Neurosci. 2006;30:107–108.PubMedCrossRef
18.
go back to reference Williams RM, Berthoud HR, Stead RH. Vagal afferent nerve fibres contact mast cells in rat small intestinal mucosa. Neuroimmunomodulation. 1997;4:266–270.PubMed Williams RM, Berthoud HR, Stead RH. Vagal afferent nerve fibres contact mast cells in rat small intestinal mucosa. Neuroimmunomodulation. 1997;4:266–270.PubMed
19.
go back to reference Wasano K, Hirakawa Y. Recombinant galectin-1 recognizes mucin and epithelial cell surface glycocalyces of gastrointestinal tract. J Histochem Cytochem. 1997;45:275–283.PubMedCrossRef Wasano K, Hirakawa Y. Recombinant galectin-1 recognizes mucin and epithelial cell surface glycocalyces of gastrointestinal tract. J Histochem Cytochem. 1997;45:275–283.PubMedCrossRef
20.
go back to reference Demetter P, Nagy N, Martin B, et al. The galectin family and digestive disease. J Pathol. 2008;215:1–12.PubMedCrossRef Demetter P, Nagy N, Martin B, et al. The galectin family and digestive disease. J Pathol. 2008;215:1–12.PubMedCrossRef
21.
go back to reference Lippert E, Gunckel M, Brenmoehl J, et al. Regulation of galectin-3 function in mucosal fibroblasts: Potential role in mucosal inflammation. Clin Exp Immunol. 2008;152:285–297.PubMedCrossRef Lippert E, Gunckel M, Brenmoehl J, et al. Regulation of galectin-3 function in mucosal fibroblasts: Potential role in mucosal inflammation. Clin Exp Immunol. 2008;152:285–297.PubMedCrossRef
22.
go back to reference Demydenko D, Berest I. Expression of galectin-1 in malignant tumors. Exp Oncol. 2009;31:74–79.PubMed Demydenko D, Berest I. Expression of galectin-1 in malignant tumors. Exp Oncol. 2009;31:74–79.PubMed
23.
go back to reference Rhodes JM, Campbell BJ, Yu LG. Lectin–epithelial interactions in the human colon. Biochem Soc Trans. 2008;36:1482–1486.PubMedCrossRef Rhodes JM, Campbell BJ, Yu LG. Lectin–epithelial interactions in the human colon. Biochem Soc Trans. 2008;36:1482–1486.PubMedCrossRef
24.
go back to reference Matarrese P, Tinari N, Semeraro ML, Natoli C, Iacobelli S, Malorni W. Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett. 2000;473:311–315.PubMedCrossRef Matarrese P, Tinari N, Semeraro ML, Natoli C, Iacobelli S, Malorni W. Galectin-3 overexpression protects from cell damage and death by influencing mitochondrial homeostasis. FEBS Lett. 2000;473:311–315.PubMedCrossRef
25.
go back to reference Yu F, Finley RL Jr, Raz A, Kim HR. Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome C release from the mitochondria. A role for synexin in galectin-3 translocation. J Biol Chem. 2002;277:15819–15827.PubMedCrossRef Yu F, Finley RL Jr, Raz A, Kim HR. Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome C release from the mitochondria. A role for synexin in galectin-3 translocation. J Biol Chem. 2002;277:15819–15827.PubMedCrossRef
26.
go back to reference Chen HY, Sharma BB, Yu L, et al. Role of galectin-3 in mast cell functions: galectin-3-deficient mast cells exhibit impaired mediator release and defective JNK expression. J Immunol. 2006;177:4991–4997.PubMed Chen HY, Sharma BB, Yu L, et al. Role of galectin-3 in mast cell functions: galectin-3-deficient mast cells exhibit impaired mediator release and defective JNK expression. J Immunol. 2006;177:4991–4997.PubMed
27.
go back to reference Patterson RJ, Wang W, Wang JL. Understanding the biochemical activities of galectin-1 and galectin-3 in the nucleus. Glycoconj J. 2004;19:499–506.PubMedCrossRef Patterson RJ, Wang W, Wang JL. Understanding the biochemical activities of galectin-1 and galectin-3 in the nucleus. Glycoconj J. 2004;19:499–506.PubMedCrossRef
28.
go back to reference Yamaoka A, Kuwabara I, Frigeri LG, Liu FT. A human lectin, galectin-3 (epsilon bp/Mac-2), stimulates superoxide production by neutrophils. J Immunol. 1995;154:3479–3487.PubMed Yamaoka A, Kuwabara I, Frigeri LG, Liu FT. A human lectin, galectin-3 (epsilon bp/Mac-2), stimulates superoxide production by neutrophils. J Immunol. 1995;154:3479–3487.PubMed
29.
go back to reference Feuk-Lagerstedt E, Jordan ET, Leffler H, Dahlgren C, Karlsson A. Identification of CD66a and CD66b as the major galectin-3 receptor candidates in human neutrophils. J Immunol. 1999;163:5592–5598.PubMed Feuk-Lagerstedt E, Jordan ET, Leffler H, Dahlgren C, Karlsson A. Identification of CD66a and CD66b as the major galectin-3 receptor candidates in human neutrophils. J Immunol. 1999;163:5592–5598.PubMed
30.
go back to reference Kuwabara I, Liu FT. Galectin-3 promotes adhesion of human neutrophils to laminin. J Immunol. 1996;156:3939–3944.PubMed Kuwabara I, Liu FT. Galectin-3 promotes adhesion of human neutrophils to laminin. J Immunol. 1996;156:3939–3944.PubMed
31.
go back to reference Truong MJ, Gruart V, Kusnierz JP, et al. Human neutrophils express immunoglobulin E (IgE)-binding proteins (Mac-2/epsilon BP) of the S-type lectin family: Role in IgE-dependent activation. J Exp Med. 1993;177:243–248.PubMedCrossRef Truong MJ, Gruart V, Kusnierz JP, et al. Human neutrophils express immunoglobulin E (IgE)-binding proteins (Mac-2/epsilon BP) of the S-type lectin family: Role in IgE-dependent activation. J Exp Med. 1993;177:243–248.PubMedCrossRef
32.
go back to reference Sato S, Ouellet N, Pelletier I, Simard M, Rancourt A, Bergeron MG. Role of galectin-3as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J Immunol. 2002;168:1813–1822.PubMed Sato S, Ouellet N, Pelletier I, Simard M, Rancourt A, Bergeron MG. Role of galectin-3as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J Immunol. 2002;168:1813–1822.PubMed
Metadata
Title
Myenteric Denervation Downregulates Galectin-1 and -3 Expression in Gastric Carcinogenesis
Authors
Cássia F. Estofolete
Sérgio Zucoloto
Sonia M. Oliani
Ana Cláudia Polli-Lopes
Cristiane D. Gil
Publication date
01-06-2011
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 6/2011
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-010-1516-7

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