Differential Cellular Expression of Galectin Family mRNAs in the Epithelial Cells of the Mouse Digestive Tract
Laboratory of Anatomy, Graduate School of Veterinary Medicine, Hokkaido University (JN,YK), and Laboratory of Cytology and Histology (TI), Hokkaido University Graduate School of Medicine, Sapporo, Japan
Correspondence to: Dr. Toshihiko Iwanaga, Laboratory of Cytology and Histology, Hokkaido University Graduate School of Medicine, Kita 15-Nishi 7, Kita-ku, Sapporo 060-8638, Japan. E-mail: tiwanaga{at}med.hokudai.ac.jp
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Summary |
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Key Words: lectin galectin digestive tract mouse in situ hybridization
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Introduction |
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It is generally noted that the galectin subtypes display cell- and tissue-specific distributions except for galectin-1, which is ubiquitously present as a stromal galectin in mammalian tissues (Poirier et al. 1992) and interacts with laminin (Cooper et al. 1991
; van den Brule et al. 1995
) and fibronectin (Ozeki et al. 1995
). The mammalian digestive tract is one of the organs rich in galectin, and six subtypes of galectin (galectin-2, -3, 4, -6, -7, and -9) have been detected by several assay systems. Oka et al. (1999)
showed an intense expression of rat galectin-2 mRNA in the stomach and small intestine and a less intense expression in the large intestine by Northern blot and reverse transcriptase polymerase chain reaction (RT-PCR) analyses. By immunostaining, they documented the presence of galectin-2 immunoreactivity only in the glandular epithelial cells of the rat stomach, possibly some population of parietal cells (Oka et al. 1999
). Galectin-3, formerly described as the Mac-2 antigen, carbohydrate-binding protein (CBP)-30/35, and IgE-binding protein, was identified in cell lineages of hematopoietic origin such as macrophages (Cherayil et al. 1989
; Woo et al. 1990
) and mast cells (Craig et al. 1995
). In the human and bovine intestine, immunostaining for galectin-3 detected the immunoreactivity in epithelia of the duodenum and colon (Sanjuan et al. 1997
; Kaltner et al. 2002
). Galectin-4 is a subtype unique to the gastrointestinal tract (Oda et al. 1993
; Gitt et al. 1998
). Northern blot analyses showed that the galectin-4 mRNA expression was intense in the small and large intestine but much less so in the stomach of the rat (Oda et al. 1993
) and mouse (Gitt et al. 1998
). Immunohistochemical studies for galectin-4 have provided fragmental information on cellular localization such as the stratified epithelium of the oral cavity and esophagus in pigs (Chiu et al. 1992
), the esophageal epithelium in rats (Wasano and Hirakawa 1995
), small intestinal epithelium in pigs (Danielsen and van Deurs 1997
), and the colonic epithelium in humans (Huflejt and Leffler 2004
). Galectin-6 is highly homologous to galectin-4 (83% in amino acid sequence, 93% in nucleotide sequence) but so far has only been found in mice and probably arose from a recent duplication during evolution. Because of this similarity, it is difficult to distinguish galectin-6 from galectin-4, and they are consequently detected together in most antibody-based and nucleotide hybridization assays (Leffler 1997
). Accordingly, their combined expression was briefly noted in the intestinal epithelium of mice by in situ hybridization analysis (Gitt et al. 1998
). Galectin-7 was originally cloned from the human epidermis as a molecular marker for keratinocyte differentiation (Madsen et al. 1995
; Magnaldo et al. 1995
). Immunohistochemically, human and mouse galectin-7 is distributed in stratified epithelial cells of the esophagus, tongue, and lip, as well as the epidermis (Magnaldo et al. 1998
; Sato et al. 2002a
). Galectin-9, previously described as ecalectin, possesses C-terminal CRD highly homologous (94% in cDNA) to that of galectin-5, which was found in rat erythrocytes (Gitt et al. 1995
) but is not present in the mouse (Wada and Kanwar 1997
). Wada and Kanwar (1997)
reported the expression of mouse galectin-9 mRNA in the small intestine, liver, thymus, and other tissues by Northern blot analysis, although the types of expressing cells have not been investigated.
The question therefore arises as to whether these family members show an overlapping or differential expression in the gastrointestinal tract or follow any rules in their combined expression. To answer this question, a systematic analysis of galectin expression is needed at cellular levels. In the present study, we identify the cell types of galectin-expressing cells in the mouse digestive tract by in situ hybridization using oligonucleotide probes specific for each of the predominant galectin subtypes (galectin-1 to galectin-7 except for galectin-5). The method used in this study has an advantage in its specific identification of subtypes with a higher homology and in its visual comparison of signal intensity. Furthermore, it is superior to immunohistochemistry when the proteins in question are highly water soluble (Huflejt et al. 1997) and tend to condense onto extracellular components after secretion (Wasano and Hirakawa 1995
,1999
).
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Materials and Methods |
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In Situ Hybridization
Two non-overlapping 45-mer antisense oligonucleotide probes specific for each of the mouse galectin mRNAs and for a proton pump (H+,K+-ATPase) and pepsinogen C were synthesized. The targeted nucleotide residues of probes used in this study are shown in Table 1. These oligonucleotides were labeled with 35S- or 33P-dATP using terminal deoxynucleotidyl transferase (TOYOBO; Osaka, Japan). Ten-µm-thick fresh frozen sections were prepared and mounted on glass slides precoated with 3-aminopropyltriethoxysilane. They were fixed with 4% paraformaldehyde in 0.1 M phosphate buffer for 15 min and then acetylated with 0.25% acetic anhydride in 0.1 M triethanolamine-HCl (pH 8.0) for 10 min. Hybridization was performed at 42C for 10 hr by adding 10,000 cpm/µl of 35S- or 33P-labeled oligonucleotide probes. Slides were rinsed at room temperature for 30 min in 2x SSC (1x SSC: 150 mM sodium chloride, 15 mM sodium citrate) containing 0.1% sarkosyl, twice at 55C for 40 min in 0.1x SSC containing 0.1% sarkosyl, dehydrated through a graded series of ethanol, and air dried. Sections were either exposed to BioMax MR films (Kodak; Rochester, NY) for a week or dipped into autoradiographic emulsion (NTB-2; Kodak) and exposed at 4C for 48 weeks. The hybridized sections were counterstained with hematoxylin after development. Some hybridized or non-hybridized sections adjacent to hybridized ones were stained with periodic acid/Schiff reaction (PAS) to identify mucous cells expressing galectin.
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Results |
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Observation of X-ray films revealed region-dependent expressions of galectin mRNAs in the mucosal layer from the lip to anus (Figure 1). Galectin-2 mRNA was expressed intensely in the glandular stomach and weakly in the pyloric antrum (Figure 1A). The small intestine from the duodenum to ileum showed an intense expression of galectin-2 mRNA, but the large intestine lacked the transcripts of this subtype (Figure 1A). In contrast, galectin-3 mRNA expression was intense in the large intestine including the cecum, colon, and rectum, whereas the stomach and small intestine had weak signals for galectin-3 that slightly increased in intensity toward the ileum (Figure 1B). Signals for galectin-3 mRNA were also observed in the stratified epithelium of the lip, tongue, esophagus, forestomach, and of the anus (Figure 1B), though much weaker than those of galectin-7. An intense expression of galectin-4/6 mRNAs was widely distributed from the glandular stomach to rectum, being especially intense in the large intestine (Figure 1C). Faint signals for galectin-4/6 were also found in the forestomach (Figure 1C). Galectin-7 mRNA expression was characterized by a restricted distribution in the stratified epithelia from the lip to forestomach, and of the anus (Figure 1D).
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Discussion |
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Tissue distribution of galectin-2 in the digestive tract has been roughly analyzed by the RT-PCR method in the rat (Oka et al. 1999). Namely, the galectin-2 mRNA expression at tissue levels was intense in the stomach and small intestine but much less so in the large intestine. The present in situ hybridization study confirmed the intense expression of mouse galectin-2 mRNA in the stomach and small intestine but could not detect any significant signals in the large intestine. Although Oka et al. (1999)
immunohistochemically identified galectin-2-expressing cells in the rat stomach as parietal cells, our galectin-2 mRNA-expressing cells were not identical to parietal cells characterized by expression of H+,K+-ATPase mRNA and instead corresponded to mucous cells distributed from gastric pits to the neck of gastric glands. The relation of galectin-2 to mucous secretion was also recognized in goblet cells of the small intestine. The lack of galectin-2 transcripts in goblet cells of the large intestine may be explained by differences in type or at least differences in the chemical component of mucus (More et al. 1987
). On the other hand, the expression sites of galectin-2 mRNA contained the proliferating zones, as clearly shown in the glandular stomach and small intestine where mitotic and undifferentiated epithelial cells reside. Although this unique expression pattern suggests the involvement of galectin-2 in the mitosis and differentiation of gut epithelial cells, no information is available for the relation between galectin-2 and cell proliferation. Other galectin subtypes, rather than galectin-2, are reported to be potent growth regulators, including galectin-1 and galectin-3, which play a role in cell proliferation as positive or negative regulators (Liu 2000
).
In contrast to the active production of galectin-3 by leukocytes and its crucial roles in infections and inflammation (Almkvist and Karlsson 2004; Sato and Nieminen 2004
), we could not detect any signals for galectin-3 in lamina propria cells including gastric mast cells and intestinal macrophages or in hepatic sinusoidal macrophages. Our failure to detect galectin-3 mRNA in leukocytes under normal conditions may be explained by the fact that infection and inflammation readily induce the galectin-3 expression in leukocytes (Sato et al. 2002b
; Almkvist and Karlsson 2004
). Instead, the analysis in the present study of normal mice demonstrated the broadest distribution of galectin-3 transcripts in epithelia from the lip to the anus. Previous immunohistochemical studies for galectin-3 briefly documented the positive reactivity in epithelial cells of the human colon (Sanjuan et al. 1997
) and of the bovine duodenum and colon (Kaltner et al. 2002
). In the present observation, the expression of galectin-3 mRNA in mice was characterized by an intensified expression on the luminal side of the gastric and intestinal mucosa. A similar tendency for galectin-3 expression was noted in immunostaining of galectin-3 in the human (Sanjuan et al. 1997
) and the bovine colons (Kaltner et al. 2002
). Interestingly, galectin-3 suppresses apoptosis in vitro through a cell death inhibition pathway that involves Bcl-2 (Yang et al. 1996
). The expression of galectin-3 has also been identified in various types of tumor cells both in vivo (Oda et al. 1991
; Woo et al. 2001
; Takenaka et al. 2003
) and in vitro (Cebo et al. 2002
), suggesting a possibility that it stimulates tumor cell proliferation by inhibiting cell death. It is well known that the major population of aged epithelial cells in the gut move to luminal sides and drop off into the lumen for epithelial renewal; therefore, galectin-3 may act to prevent epithelial cells from cell death at the terminal sites of maturation.
In adult mouse tissues, the expression of galectin-4/6 was assayed by Northern and Western blots only in gastrointestinal tissues (Gitt et al. 1998). An RNase protection assay, which permitted their separate detection, demonstrated a high expression of galectin-4 in the small intestine and colon but a lower level of expression in the stomach, whereas galectin-6 exhibited a relatively even distribution from the stomach to the colon (Gitt et al. 1998
). Because of the high sequence homology between galectin-4 and galectin-6, it is hard to distinguish their expression by the use of available histochemical techniques. A previous in situ hybridization study reported the combined expression of galectin-4/6 in the intestinal epithelium of mice (Gitt et al. 1998
); however, the precise cellular localization has not been described. We demonstrated here the intense and consistent expression of galectin-4/6 in the epithelium of the whole small intestine from crypts to villous tips. The transcripts of galectin-4/6 in enterocytes were maintained at equal or more intense levels in the large intestine, thus resulting in the finding that galectin-4/6 is the most dominant subtype in the large intestine. Recently, galectin-4 was immunohistochemically localized in the human colon epithelium and functionally related to the promotion of colon cancer growth and exacerbation of colitis (Hokama et al. 2004
; Huflejt and Leffler 2004
). Although stratified epithelial cells of the oral mucosa and esophagus contain immunoreactivity for galectin-4 in the pig (Chiu et al. 1992
) and the rat (Wasano and Hirakawa 1995
), we detected a faint expression of galectin-4/6 mRNA only in the forestomach among the stratified epithelia. Confining its description to the simple epithelium, galectin-4/6 is regarded as a subtype that is most intensely and consistently expressed from the glandular stomach to rectum, suggesting a fundamental function shared by gastric and intestinal epithelial cells. In accordance with this suggestion, it is reported that galectin-4 resides on the extracellular side of membrane in enterocytes and has roles in the stabilization of adhesion devices (Chiu et al. 1992
,1994
; Huflejt et al. 1997
) and membrane-associated molecules (Danielsen and van Deurs 1997
; Braccia et al. 2003
).
Galectin-7 displayed a limited expression in the stratified squamous epithelium of the lip, tongue, esophagus, forestomach, and of the anus. This finding was consistent with data from Western blot (Sato et al. 2002a) and immunohistochemical studies (Magnaldo et al. 1998
). However, there is a slight difference in the detailed cellular expression within the stratified epithelium. Intense labelings with a galectin-7 riboprobe and antibody were spread all over the thickness of the nucleated epithelium in the human epidermis (Magnaldo et al. 1995
,1998
), in contrast to the present study showing that signals for galectin-7 mRNA were restricted to the basal half of the stratified epithelium. Nevertheless, the specific expression of galectin-7 by keratinocytes is beyond doubt and further supported by the finding that the vaginal epithelium expresses galectin-7 mRNA, whereas the respiratory pseudostratified epithelium and urinary transitional epithelium do not (Nio J, et al., unpublished data).
Galectin-9 is distributed ubiquitously and is more abundantly expressed in the small intestine, liver, and thymus at a nucleotide level (Wada and Kanwar 1997). One of the unique features of galectin-9 is the presence of its alternate splicing isoform exclusively expressed in the small intestine, suggesting certain functions of the intestinal isoform that are related to the biology of intestinal epithelium but also shared by other galectin subtypes (Wada and Kanwar 1997
). When we hybridized sections of visceral organs using probes detecting both isoforms, significant signals were detected from the glandular stomach to the rectum as well as the liver (Nio J, et al., unpublished data). Galectin-9 in the gut was roughly identical to galectin-4/6 in distribution, although the intensity was much weaker than that of galectin-4/6 and remarkably so in the large intestine. Because of the existence of the isoforms, a further detailed investigation of galectin-9 is underway.
As summarized in Figure 7A, the digestive tract of mice expressed five subtypes of galectin mRNAs in the epithelium with region-dependent and cell-specific distributions. Their restricted expression in the epithelium suggests the involvement in the following: (a) digestion/absorption of food, (b) interaction with resident or pathogenic microorganisms, and (c) homeostasis of the epithelium including the regulation of cell kinetics. Although no studies have dealt with the direct relation of galectin in digestion and absorption, its interaction with digestive enzymes and mucin is proof enough to consider an indirect role in digestion. Danielsen and van Deurs (1997) have discussed how the porcine galectin-4 present in the intestinal brush border may keep digestive enzymes at the cell surface by preventing them from release into the gut lumen and also from undergoing endocytosis. One of the major ligands for galectin is mucin (Raz and Lotan 1987
; Wasano and Hirakawa 1997
), and especially galectin-3 modulates the expression of MUC2 mucin in human colon cancer cells (Bresalier et al. 1996
). The intense expression of galectin in the mucus-secreting goblet cells and gastric pits cells as shown in the present study suggests a role in the production and secretion of mucin and epithelial cell surface glycocalyces. As an example of the second function, the production of galectin (galectin-3 and possibly galectin-4) is upregulated in response to microbial infection and secreted to interact with microorganisms (Huflejt and Leffler 2004
; Sato and Nieminen 2004
). It has also been proposed that galectin-3, which is present in macrophages or the mucosal epithelium, can bind to ß-galactoside residues of lipopolysaccharide on pathogens to mediate the interaction between a pathogen and host cells (Mandrell et al. 1994
). To date, most studies have focused on the third function, namely, the regulation of cell growth, differentiation, apoptosis, adhesion, and malignant transformation. Taking into consideration the regulation of epithelial homeostasis, it is worth noting the changes in galectin subtypes expressed by the epithelium according to the maturation process. Namely, galectin-2 expressed at the proliferating zone of crypts changes, via galectin-4/6, to galectin-3 expressed in fully matured epithelial cells at villous tips (Figure 7B). The maturation-dependent expression of galectin subtypes was also found in the mucus-secreting cells of the stomach and in the epithelial cells of the large intestine. This phenomenon provides an example of a periodical shift of galectin subtype expressed by the same cell lineage (proto type
tandem repeat type
chimera type). Likewise, the maturation-dependent expression is important when taking into consideration interaction and switching among subtypes. Galectin-1, -3, or -1/3 null mutant mice appear healthy (Poirier and Robertson 1993
; Colnot et al. 1998
; Pugliese et al. 2001
), suggesting that their functions could be compensated for by other galectins with a similar carbohydrate specificity.
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Acknowledgments |
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Footnotes |
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Literature Cited |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
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Almkvist J, Karlsson A (2004) Galectins as inflammatory mediators. Glycoconj J 19:575581[CrossRef][Medline]
Barondes SH, Cooper DN, Gitt MA, Leffler H (1994) Galectins. Structure and function of a large family of animal lectins. J Biol Chem 269:2080720810
Braccia A, Villani M, Immerdal L, Niels-Christiansen LL, Nystrom BT, Hansen GH, Danielsen EM (2003) Microvillar membrane microdomains exist at physiological temperature. Role of galectin-4 as lipid raft stabilizer revealed by "superrafts". J Biol Chem 278:1567915684
Bresalier RS, Byrd JC, Wang L, Raz A (1996) Colon cancer mucin: a new ligand for the beta-galactoside-binding protein galectin-3. Cancer Res 56:43544357[Abstract]
Cebo C, Vergoten G, Zanetta JP (2002) Lectin activities of cytokines: functions and putative carbohydrate-recognition domains. Biochem Biophys Acta 1572:422434[Medline]
Cherayil BJ, Weiner SJ, Pillai S (1989) The Mac-2 antigen is a galactose-specific lectin that binds IgE. J Exp Med 170:19591972
Chiu ML, Jones JC, O'Keefe EJ (1992) Restricted tissue distribution of a 37-kD possible adherens junction protein. J Cell Biol 119:16891700[Abstract]
Chiu ML, Parry DA, Feldman SR, Klapper DG, O'Keefe EJ (1994) An adherens junction protein is a member of the family of lactose-binding lectins. J Biol Chem 269:3177031776
Colnot C, Fowlis D, Ripoche MA, Bouchaert I, Poirier F (1998) Embryonic implantation in galectin 1/galectin 3 double mutant mice. Dev Dyn 211:306313[CrossRef][Medline]
Cooper DN, Massa SM, Barondes SH (1991) Endogenous muscle lectin inhibits myoblast adhesion to laminin. J Cell Biol 115:14371448[Abstract]
Craig SS, Krishnaswamy P, Irani AM, Kepley CL, Liu FT, Schwartz LB (1995) Immunoelectron microscopic localization of galectin-3, an IgE binding protein, in human mast cells and basophils. Anat Rec 242:211219[CrossRef][Medline]
Danielsen EM, van Deurs B (1997) Galectin-4 and small intestinal brush border enzymes form clusters. Mol Biol Cell 8:22412251
Gitt MA, Wiser MF, Leffler H, Herrmann J, Xia YR, Massa SM, Cooper DN, et al. (1995) Sequence and mapping of galectin-5, a beta-galactoside-binding lectin, found in rat erythrocytes. J Biol Chem 270:50325038
Gitt MA, Colnot C, Poirier F, Nani KJ, Barondes SH, Leffler H (1998) Galectin-4 and galectin-6 are two closely related lectins expressed in mouse gastrointestinal tract. J Biol Chem 273:29542960
Hirabayashi J, Kasai K (1993) The family of metazoan metal-independent beta-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 3:297304[Abstract]
Hokama A, Mizoguchi E, Sugimoto K, Shimomura Y, Tanaka Y, Yoshida M, Rietdijk ST, et al. (2004) Induced reactivity of intestinal CD4(+) T cells with an epithelial cell lectin, galectin-4, contributes to exacerbation of intestinal inflammation. Immunity 20:681693[CrossRef][Medline]
Huflejt ME, Jordan ET, Gitt MA, Barondes SH, Leffler H (1997) Strikingly different localization of galectin-3 and galectin-4 in human colon adenocarcinoma T84 cells. Galectin-4 is localized at sites of cell adhesion. J Biol Chem 272:1429414303
Huflejt ME, Leffler H (2004) Galectin-4 in normal tissues and cancer. Glycoconj J 20:247255[CrossRef][Medline]
Kaltner H, Seyrek K, Heck A, Sinowatz F, Gabius HJ (2002) Galectin-1 and galectin-3 in fetal development of bovine respiratory and digestive tracts. Comparison of cell type-specific expression profiles and subcellular localization. Cell Tissue Res 307:3546[CrossRef][Medline]
Leffler H (1997) Introduction to galectins. Trends Glycosci Glycotech 9:919
Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F (2004) Introduction to galectins. Glycoconj J 19:433440[CrossRef]
Liu FT (2000) Galectins: a new family of regulators of inflammation. Clin Immunol 97:7988[CrossRef][Medline]
Madsen P, Rasmussen HH, Flint T, Gromov P, Kruse TA, Honore B, Vorum H, et al. (1995) Cloning, expression, and chromosome mapping of human galectin-7. J Biol Chem 270:58235829
Magnaldo T, Bernerd F, Darmon M (1995) Galectin-7, a human 14-kDa S-lectin, specifically expressed in keratinocytes and sensitive to retinoic acid. Dev Biol 168:259271[CrossRef][Medline]
Magnaldo T, Fowlis D, Darmon M (1998) Galectin-7, a marker of all types of stratified epithelia. Differentiation 63:159168[CrossRef][Medline]
Mandrell RE, Apicella MA, Lindstedt R, Leffler H (1994) Possible interaction between animal lectins and bacterial carbohydrates. Methods Enzymol 236:231254[Medline]
More J, Fioramonti J, Benazet F, Bueno L (1987) Histochemical characterization of glycoproteins present in jejunal and colonic goblet cells of pigs on different diets. A biopsy study using chemical methods and peroxidase-labelled lectins. Histochemistry 87:189194[CrossRef][Medline]
Oda Y, Leffler H, Sakakura Y, Kasai K, Barondes SH (1991) Human breast carcinoma cDNA encoding a galactoside-binding lectin homologous to mouse Mac-2 antigen. Gene 99:279283[CrossRef][Medline]
Oda Y, Herrmann J, Gitt MA, Turck CW, Burlingame AL, Barondes SH, Leffler H (1993) Soluble lactose-binding lectin from rat intestine with two different carbohydrate-binding domains in the same peptide chain. J Biol Chem 268:59295939
Oka T, Murakami S, Arata Y, Hirabayashi J, Kasai K, Wada Y, Futai M (1999) Identification and cloning of rat galectin-2: expression is predominantly in epithelial cells of the stomach. Arch Biochem Biophys 361:195201[CrossRef][Medline]
Ozeki Y, Matsui T, Yamamoto Y, Funahashi M, Hamako J, Titani K (1995) Tissue fibronectin is an endogenous ligand for galectin-1. Glycobiology 5:255261[Abstract]
Poirier F, Robertson EJ (1993) Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development 119:12291236
Poirier F, Timmons PM, Chan CT, Guenet JL, Rigby PW (1992) Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during pre- and post-implantation development. Development 115:143155
Pugliese G, Pricci F, Iacobini C, Leto G, Amadio L, Barsotti P, Frigeri L, et al. (2001) Accelerated diabetic glomerulopathy in galectin-3/AGE receptor 3 knockout mice. FASEB J 15:24712479
Rabinovich GA, Baum LG, Tinari N, Paganelli R, Natoli C, Liu FT, Iacobelli S (2002) Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol 23:313320[CrossRef][Medline]
Raz A, Lotan R (1987) Endogenous galactoside-binding lectins: a new class of functional tumor cell surface molecules related to metastasis. Cancer Metastasis Rev 6:433452[CrossRef][Medline]
Sanjuan X, Fernandez PL, Castells A, Castronovo V, van den Brule F, Liu FT, Cardesa A, et al. (1997) Differential expression of galectin 3 and galectin 1 in colorectal cancer progression. Gastroenterology 113:19061915[Medline]
Sato M, Nishi N, Shoji H, Kumagai M, Imaizumi T, Hata Y, Hirashima M, et al. (2002a) Quantification of galectin-7 and its localization in adult mouse tissues. J Biochem (Tokyo) 131:255260[Abstract]
Sato S, Nieminen J (2004) Seeing strangers or announcing "danger": galectin-3 in two models of innate immunity. Glycoconj J 19:583591[CrossRef][Medline]
Sato S, Ouellet N, Pelletier I, Simard M, Rancourt A, Bergeron MG (2002b) Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J Immunol 168:18131822
Shoji H, Nishi N, Hirashima M, Nakamura T (2003) Characterization of the Xenopus galectin family. Three structurally different types as in mammals and regulated expression during embryogenesis. J Biol Chem 278:1228512293
Takenaka Y, Inohara H, Yoshii T, Oshima K, Nakahara S, Akahani S, Honjo Y, et al. (2003) Malignant transformation of thyroid follicular cells by galectin-3. Cancer Lett 195:111119[CrossRef][Medline]
van den Brule FA, Buicu C, Baldet M, Sobel ME, Cooper DN, Marschal P, Castronovo V (1995) Galectin-1 modulates human melanoma cell adhesion to laminin. Biochem Biophys Res Commun 209:760767[CrossRef][Medline]
Wada J, Kanwar YS (1997) Identification and characterization of galectin-9, a novel beta-galactoside-binding mammalian lectin. J Biol Chem 272:60786086
Wasano K, Hirakawa Y (1995) Rat intestinal galactoside-binding lectin L-36 functions as a structural protein in the superficial squamous cells of the esophageal epithelium. Cell Tissue Res 281:7783[CrossRef][Medline]
Wasano K, Hirakawa Y (1997) Recombinant galectin-1 recognizes mucin and epithelial cell surface glycocalyces of gastrointestinal tract. J Histochem Cytochem 45:275283
Wasano K, Hirakawa Y (1999) Two domains of rat galectin-4 bind to distinct structures of the intercellular borders of colorectal epithelia. J Histochem Cytochem 47:7582
Woo HJ, Shaw LM, Messier JM, Mercurio AM (1990) The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2). J Biol Chem 265:70977099
Woo HJ, Joo HG, Song SW, Sohn YS, Chae C (2001) Immunohistochemical detection of galectin-3 in canine gastric carcinomas. J Comp Pathol 124:216218[CrossRef][Medline]
Yang RY, Hsu DK, Liu FT (1996) Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci USA 93:67376742
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