Immunohistochemical localization of galectins-1 and -3 and monitoring of tissue galectin-binding sites during tubular regeneration after renal ischemia reperfusion in the rat

Histology and Histopathology

Volumn 25, Issue 11, 2010, Pages 1417-1429

  Vansthertem, David ^a   Cludts, Stéphanie ^a   Nonclercq, Denis ^a   Gossiaux, Annabel ^a   Saussez, Sven ^a   Legrand, Alexandre ^a   Gabius, Hans Joachim ^b   Toubeau, Gérard ^a  

^a UNIVERSITY OF MONS   (Belgium)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Acute renal failure; Kidney regeneration; Renal interstitium; Tubular necrosis

Indexed keywords

RATTUS;

GALECTIN 1; GALECTIN 3;

ANIMAL; ARTICLE; BINDING SITE; IMMUNOHISTOCHEMISTRY; KIDNEY TUBULE; MALE; METABOLISM; PATHOPHYSIOLOGY; RAT; REGENERATION; REPERFUSION INJURY; WISTAR RAT;

ANIMALS; BINDING SITES; GALECTIN 1; GALECTIN 3; IMMUNOHISTOCHEMISTRY; KIDNEY TUBULES; MALE; RATS; RATS, WISTAR; REGENERATION; REPERFUSION INJURY;

EID: 79952108143     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. Ahmad N., Gabius H.J., Sabesan S., Oscarson S. and Brewer C.F. (2004a). Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3, and the carbohydrate recognition domain of galectin-3. Glycobiology 14, 817-825.
2. Ahmad N., Gabius H.J., Andre S., Kaltner H., Sabesan S., Roy R., Liu B., Macaluso F. and Brewer C.F. (2004b). Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J. Biol. Chem. 279, 10841-10847.
3. Al-Awqati Q. (2008). 2007 Homer W. Smith award: control of terminal differentiation in epithelia. J. Am. Soc. Nephrol. 19, 443-449.
4. Al Awqati Q. and Oliver J.A. (2002). Stem cells in the kidney. Kidney Int. 61, 387-395.
5. André S., Kojima S., Yamazaki N., Fink C., Kaltner H., Kayser K. and Gabius H.J. (1999). Galectins-1 and -3 and their ligands in tumor biology. J. Cancer Res. Clin. Oncol. 125, 461-474.
6. André S., Pieters R.J., Vrasidas I., Kaltner H., Kuwabara I., Liu F.T., Liskamp R.M. and Gabius H.J. (2001). Wedgelike glycodendrimers as inhibitors of binding of mammalian galectins to glycoproteins, lactose maxiclusters, and cell surface glycoconjugates. Chembiochem. 2, 822-830.
7. André S., Unverzagt C., Kojima S., Frank M., Seifert J., Fink C., Kayser K., von der Lieth C.W. and Gabius H.J. (2004). Determination of modulation of ligand properties of synthetic complex-type biantennary N-glycans by introduction of bisecting GlcNAc in silico, in vitro and in vivo. Eur. J. Biochem. 271, 118-134.
8. André S., Pei Z., Siebert H.C., Ramström O. and Gabius H.J. (2006). Glycosyldisulfides from dynamic combinatorial libraries as Oglycoside mimetics for plant and mammalian lectins: their reactivities in solid-phase and cell assays and conformational analysis by molecular dynamics simulations. Bioorg. Med. Chem. 14, 6314-6323.
9. André S., Kozár T., Schuberth R., Unverzagt C., Kojima S. and Gabius H.J. (2007a). Substitutions in the N-glycan core as regulators of biorecognition: the case of core-fucose and bisecting GlcNAc moieties. Biochemistry 46, 6984-6995.
10. André S., Sanchez-Ruderisch H., Nakagawa H., Buchholz M., Kopitz J., Forberich P., Kemmner W., Böck C., Deguchi K., Detjen K.M., Wiedenmann B., von Knebel-Döberitz M., Gress T.M., Nishimura S.I., Rosewicz S. and Gabius H.J. (2007b). Tumor suppressor p16INK4a: modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J. 274, 3233-3256.
11. André S., Sansone F., Kaltner H., Casnati A., Kopitz J., Gabius H.J. and Ungaro R. (2008). Calix[n]arene-based glycoclusters: bioactivity of thiourea-linked galactose/lactose moieties as inhibitors of binding of medically relevant lectins to a glycoprotein and cell-surface glycoconjugates and selectivity among human adhesion/growthregulatory galectins. Chembiochem. 9, 1649-1661.
12. Bao Q. and Hughes R.C. (1995). Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J. Cell. Sci. 108, 2791-2800.
13. Barondes S.H., Cooper D., Gitt M. and Leffler H. (1994). Galectins. Structure and function of a large family of animal lectins. J. Biol. Chem. 269, 20807-20810.
14. Bichara M., Attmane-Elakeb A., Brown D., Essig M., Karim Z., Muffat-Joly M., Micheli L., Eude-Le Parco I., Cluzeaud F., Peuchmaur M., Bonvalet J.P., Poirier F. and Farman N. (2006). Exploring the role of galectin 3 in kidney function: a genetic approach. Glycobiology 16, 36-45.
15. Bonventre J.V. (2003). Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J. Am. Soc. Nephrol. 14, 55-61.
16. Bullock S.L., Johnson T.M., Bao Q., Hughes R.C., Winyard P.J. and Woolf A.S. (2001). Galectin-3 modulates ureteric bud branching in organ culture of the developing mouse kidney. J. Am. Soc. Nephrol. 12, 515-523.
17. Chan J., O'Donoghue K., Gavina M., Torrente Y., Kennea N., Mehmet H., Stewart H., Watt D.J., Morgan J.E. and Fisk N.M. (2006). Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells 24, 1879-1891.
18. Chiu M.G., Johnson T.M., Woolf A.S., Dahm-Vicker E.M., Long D.A., Guay-Woodford L., Hillman K.A., Bawumia S., Venner K., Hughes R.C., Poirier F. and Winyard P.J. (2006). Galectin-3 associates with the primary cilium and modulates cyst growth in congenital polycystic kidney disease. Am. J. Pathol. 169, 1925-1938.
19. Chou Y.H., Khuon Sherrmann H. and Goldman R.D. (2003). Nestin promotes the phosphorylation-dependent disassembly of vimentin intermediate filaments during mitosis. Mol. Biol. Cell 14, 1468-1478.
20. Dam T.K., Gabius H.J., André S., Kaltner H., Lensch M. and Brewer C.F. (2005). Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry 44, 12564-12571.
21. Duffield J.S. and Bonventre J.V. (2005). Kidney tubular epithelium is restored without replacement with bone marrow-derived cells during repair after ischemic injury. Kidney Int. 68, 1956-1961.
22. Dumic J., Dabelic S. and Flögel M. (2006). Galectin-3: an open-ended story. Biochim. Biophys. Acta 1760, 616-635.
23. Fernandes Bertocchi A.P., Campanhole G., Wang P.H., Gonçalves G.M., Damião M.J., Cenedeze M.A., Beraldo F.C., de Paula Antunes Teixeira V., Dos Reis M.A., Mazzali M., Pacheco-Silva A. and Câmara N.O. (2008). A Role for galectin-3 in renal tissue damage triggered by ischemia and reperfusion injury. Transpl. Int. 21, 999-1007.
24. Friedrichs J., Manninen A., Muller D.J. and Helenius J. (2008). Galectin- 3 regulates integrin ·2'1-mediated adhesion to collagen-I and -IV. J. Biol. Chem. 283, 32264-32272.
25. Gabius H.J. (2006). Cell surface glycans: the why and how of their functionality as biochemical signals in lectin-mediated information transfer. Crit. Rev. Immunol. 26, 43-80.
26. Gabius H.J. (2008). Glycans: bioactive signals decoded by lectins. Biochem. Soc. Trans. 36, 1491-1496.
27. Gabius H.J. (2009). The Sugar Code. Fundamentals of glycosciences. Wiley-Blackwell. Weinheim. Germany.
28. Gabius H.J., Wosgien B., Hendrys M. and Bardosi A. (1991). Lectin localization in human nerve by biochemically defined lectin-binding glycoproteins, neoglycoprotein and lectin-specific antibody. Histochemistry 95, 269-277.
29. Goldring K., Jones G.E., Thiagarajah R. and Watt D.J. (2002). The effect of galectin-1 on the differentiation of fibroblasts and myoblasts in vitro. J. Cell Sci. 115, 355-366.
30. Henderson N.C., Mackinnon A.C., Farnworth S.L., Kipari T., Haslett C., Iredale J.P., Liu F.T., Hughes J. and Sethi T. (2008). Galectin-3 expression and secretion links macrophages to the promotion of renal fibrosis. Am. J. Pathol. 172, 288-298.
31. Hikita C., Vijayakumar S., Takito J., Erdjument-Bromage H., Tempst P. and Al-Awqati Q. (2000). Induction of terminal differentiation in epithelial cells requires polymerization of hensin by galectin 3. J. Cell Biol. 151, 1235-1246.
32. Horie H. and Kadoya T. (2004). Galectin-1 plays essential roles in adult mammalian nervous tissues. Roles of oxidized galectin-1. Glycoconj. J. 19, 479-489.
33. Hughes C.R. (2004). Galectins in kidney development. Glycoconj. J. 19, 621-629.
34. Humphreys B.D., Duffield J.S. and Bonventre J.V. (2006). Renal stem cells in recovery from acute kidney injury. Minerva Urol. Nefrol. 58, 329-337.
35. Kaltner H. and Stierstorfer B. (1998). Animal lectins as cell adhesion molecules. Acta Anat. (Basel) 161, 162-79.
36. Kaltner H., Seyrek K., Heck A., Sinowatz F. and Gabius H.J. (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, 35-46.
37. Kikuchi Y., Kobayashi S., Hemmi N., Ikee R., Hyodo N., Saigusa T., Namikoshi T., Yamada M., Suzuki S. and Miura S. (2004). Galectin- 3-positive cell infiltration in human diabetic nephropathy. Nephrol. Dial. Transplant. 19, 602-607.
38. Kim H., Lee J., Hyun J.W., Park J.W., Joo H.G. and Shin T. (2007). Expression and immunohistochemical localization of galectin-3 in various mouse tissues. Cell Biol. Int. 31, 655-662.
39. Kopitz J., André S., von Reitzenstein C., Versluis K., Kaltner H., Pieters R.J., Wasano K., Kuwabara I., Liu F.T., Cantz M., Heck A.J.R. and Gabius H.J. (2003). Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene 22, 6277-6288.
40. Lahm H., André S., Hoeflich A., Kaltner H., Siebert H.C., Sordat B., von der Lieth C.W., Wolf E. and Gabius H.J. (2004). Tumor galectinology: insights into the complex network of a family of endogenous lectins. Glycoconj. J. 20, 227-238.
41. Langbein S., Brade J., Badawi J.K., Hatzinger M., Kaltner H., Lensch M., Specht K., André S., Brinck U., Alken P. and Gabius H.J. (2007). Gene-expression signature of adhesion/growth-regulatory tissue lectins (galectins) in transitional cell cancer and its prognostic relevance. Histopathology 51, 681-690.
42. Lee M.Y. and Han H.J. (2008). Galectin-1 upregulates glucose transporter-1 expression level via protein kinase C, phosphoinositol- 3 kinase, and mammalian target of rapamycin pathways in mouse embryonic stem cells. Int. J. Biochem. Cell Biol. 40, 2421-2430.
43. Lee M.Y., Lee S.H., Park J.H. and Han H.J. (2009). Interaction of galectin-1 with caveolae induces mouse embryonic stem cell proliferation through the Src, ERas, Akt and mTOR signaling pathways. Cell Mol. Life Sci. 66, 1467-1478.
44. Lensch M., Lohr M., Russwurm R., Vidal M., Kaltner H., André S. and Gabius H.J. (2006). Unique sequence and expression profiles of rat galectins-5 and -9 as a result of species-specific gene divergence. Int. J. Biochem. Cell Biol. 38, 1741-1758.
45. Liu F.T. (2000). Galectins: a new family of regulators of inflammation. Clin. Immunol. 97, 79-88.
46. Liu Y.H., D'Ambrosio M., Liao T.D., Peng H., Rhaleb N.E., Sharma U.C., André S., Gabius H.J. and Carretero O.A. (2009). N-Acetyl-serylaspartyl- lysyl-proline prevents cardiac remodeling and dysfunction induced by galectin-3, a mammalian adhesion/growth-regulatory lectin. Am. J. Physiol. Heart Circ. Physiol. 296, H404-H412.
47. Lohr M., Lensch M., André S., Kaltner H., Siebert H.C., Smetana K. Jr, Sinowatz F. and Gabius H.J. (2007). Murine homodimeric adhesion/growth-regulatory galectins-1, -2 and -7: comparative profiling of gene/promoter sequences by database mining, of expression by RT-PCR/immunohistochemistry and of contact sites for carbohydrate ligands by computational chemistry. Folia Biol. (Praha) 53, 109-128.
48. Lohr M., Kaltner H., Lensch M., André S., Sinowatz F. and Gabius H.J. (2008). Cell-type-specific expression of murine multifunctional galectin-3 and its association with follicular atresia/luteolysis in contrast to pro-apoptotic galectins-1 and -7. Histochem. Cell Biol. 130, 567-581.
49. Manning J.C., Seyrek K., Kaltner H., Andre S., Sinowatz F. and Gabius H.J. (2004). Glycomic profiling of developmental changes in bovine testis by lectin histochemistry and further analysis of the most prominent alteration on the level of the glycoproteome by lectin blotting and lectin affinity chromatography. Histol. Histopathol. 19, 1043-1060.
50. Morris S., Ahmad N., André S., Kaltner H., Gabius H.J., Brenowitz M. and Brewer F. (2004). Quaternary solution structures of galectins-1, -3, and -7. Glycobiology 14, 293-300.
51. Nagy N., Bronckart Y., Camby I., Legendre H., Lahm H., Kaltner H., Hadari Y., Van Ham P., Yeaton P., Pector J.C., Zick Y., Salmon I., Danguy A., Kiss R. and Gabius H.J. (2002). Galectin-8 expression decreases in cancer as compared to normal and dysplastic human colon tissue and acts significantly on human colon cancer cell migration. Gut 50, 392-401.
52. Nagy N., Legendre H., Engels O., André S., Kaltner H., Wasano K., Zick Y., Pector J.C., Decaestecker C., Gabius H.J., Salmon I. and Kiss R. (2003). Refined prognostic evaluation in colon carcinoma using immunohistochemical galectin fingerprinting. Cancer 97, 1849-1858.
53. Nio J., Takahashi-Iwanaga H, Morimatsu M, Kon Y. and Iwanaga T. (2006). Immunohistochemical and in situ hybridization analysis of galectin-3, a ß-galactoside binding lectin, in the urinary system of adult mice. Histochem. Cell Biol. 126, 45-56.
54. Nishiyama J., Kobayashi S., Ishida A., Nakabayashi I., Tajima O., Miura S., Katayama M. and Nogami H. (2000). Up- regulation of galectin- 3 in acute renal failure of the rat. Am. J. Pathol. 157, 815-823.
55. Ochieng J., Leite-Browning M.L. and Warfield P. (1998). Regulation of cellular adhesion to extracellular matrix proteins by galectin-3. Biochem. Biophys. Res. Commun.246, 788-791.
56. Ochieng J., Furtak V. and Lukyanov P. (2004). Extracellular functions of galectin-3. Glycoconj. J. 19, 527-535.
57. Purkrábková T., Smetana K. Jr., Dvoránková B., Holíková Z., Böck C., Lensch M., André S., Pytlík R., Liu F.T., Klíma J., Smetana K., Motlík J. and Gabius H.J. (2003). New aspects of galectin functionality in nuclei of cultured bone marrow stromal and epidermal cells: biotinylated galectins as tool to detect specific binding sites. Biol. Cell 95, 535-545.
58. Rao S.P., Wang Z., Zuberi R.I., Sikora L., Bahaie N.S., Zuraw B.L., Liu F.T. and Sriramarao P. (2007). Galectin-3 functions as an adhesion molecule to support eosinophil rolling and adhesion under conditions of flow. J. Immunol. 179, 7800-7807.
59. Romagnani P. (2009). Toward the identification of a renopoietic system? Stem Cells 27, 2247-2253.
60. Saal I., Nagy N., Lensch M., Lohr M., Manning J.C., Decaestecker C., André S., Kiss R., Salmon I. and Gabius H.J. (2005). Human galectin-2: expression profiling by RT-PCR/immunohistochemistry and its introduction as histochemical tool for ligand localization. Histol. Histopathol. 20, 1191-1208.
61. Sakaguchi M., Imaizumi Y. and Okano H. (2007). Expression and function of galectin-1 in adult neural stem cells. Cell Mol. Life Sci. 64, 1254-1258.
62. Sakairi T., Hiromura K., Yamashita S., Takeuchi S., Tomioka M., Ideura H., Maeshima A., Kaneko Y., Kuroiwa T., Nangaku M., Takeuchi T. and Nojima Y. (2007). Nestin expression in the kidney with an obstructed ureter. Kidney Int. 72, 307-318.
63. Sato S., Ouellet N., Pelletier I., Simard M., Rancourt A. and Bergeron M.G. (2002). Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia. J. Immunol. 168, 1813-1822.
64. Saussez S., Nonclercq D., Laurent G., Wattiez R., André S., Kaltner H., Gabius H.J., Kiss R. and Toubeau G. (2005). Toward functional glycomics by localization of tissue lectins: immunohistochemical galectin fingerprinting during diethylstilbestrol-induced kidney tumorigenesis in male Syrian hamster. Histochem. Cell Biol. 123, 29-41.
65. Saussez S., Lorfevre F., Nonclercq D., Laurent G., André S., Journé F., Kiss R., Toubeau G. and Gabius H.J. (2006). Towards functional glycomics by localization of binding sites for tissue lectins: lectin histochemical reactivity for galectins during diethylstilbestrol-induced kidney tumorigenesis in male Syrian hamster. Histochem. Cell Biol. 126, 57-69.
66. Schaudies P., Nonclercq D., Nelson L., Toubeau G., Zanen J., Heuson- Stiennon J.A. and Laurent G. (1993). Endogenous EGF as a potential renotrophic factor in ischemia-induced acute renal failure. Am. J. Physiol. 265, 425-434.
67. Schwaderer A.L, Vijayakumar S., Al-Awqati Q. and Schwartz G.J. (2006). Galectin-3 expression is induced in renal ß-intercalated cells during metabolic acidosis. Am. J. Physiol. Renal Physiol. 290, F148-F158.
68. Scott K. and Weinberg C. (2004). Galectin-1: a bifunctional regulator of cellular proliferation. Glycoconj. J. 19, 467-477.
69. Shimizu M., Khoshnoodi J., Akimoto Y., Kawakami H., Hirano H., Higashihara E., Hosoyamada M., Sekine Y., Kurayama R., Kurayama H., Joh K., Hirabayashi J., Kasai K., Tryggvason K., Ito N. and Yan K. (2009). Expression of galectin-1, a new component of slit diaphragm, is altered in minimal change nephrotic syndrome. Lab. Invest. 89, 178-195.
70. Silva W.A. Jr, Covas D.T., Panepucci R.A., Proto-Siqueira R., Siufi J.L., Zanette D.L., Santos A.R. and Zago M.A. (2003). The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 21, 661-669.
71. Smetana K. Jr, Dvoránková B., Chovanec M., Boucek J., Klíma J., Motlík J., Lensch M., Kaltner H., André S. and Gabius H.J. (2006). Nuclear presence of adhesion/growth-regulatory galectins in normal/malignant cells of squamous epithelial origin. Histochem. Cell Biol. 125, 171-182.
72. Toubeau G., Nonclercq D., Zanen J., Laurent G., Schaudies P. and Heuson-Stiennon J.A. (1994). Renal tissue expression of EGF and EGF-receptor after ischemic tubular injury: an immunohistochemical study. Exp. Nephrol. 2, 229-239.
73. Van den Brûle F.A., Fernandez P.L., Buicu C., Liu F.T., Jackers P., Lambotte R. and Castronovo V. (1997). Differential expression of galectin-1 and galectin-3 during first trimester human embryogenesis. Dev. Dyn. 209, 399-405.
74. Vansthertem D., Caron N., Declèves A.E, Cludts S., Gossiaux A., Nonclercq D., Flamion B., Legrand A. and Toubeau G. (2008). Label-retaining cells and tubular regeneration in postischaemic kidney. Nephrol. Dial. Transplant. 23, 3786-3797.
75. Vrasidas I., André S., Valentini P., Böck C., Lensch M., Kaltner H., Liskamp R.M., Gabius H.J. and Pieters R.J. (2003). Rigidified multivalent lactose molecules and their interactions with mammalian galectins: a route to selective inhibitors. Org. Biomol. Chem. 1, 803-810.
76. Wasano K., Hirakawa Y. and Yamamoto T. (1990). Immunohistochemical localization of 14 kDa beta-galactoside-binding lectin in various organs of rat. Cell Tissue Res. 259, 43-49.
77. Williams P., Lopez H., Britt D., Chan C., Ezrin A. and Hottendorf R. (1997). Characterization of renal ischemia-reperfusion injury in rats. J. Pharmacol. Toxicol. 37, 1-7.
78. Winyard P.J., Bao Q., Hughes R.C. and Woolf A.S. (1997). Epithelial galectin-3 during human nephrogenesis and childhood cystic diseases. J. Am. Soc. Nephrol. 8, 1647-1657.
79. Yu L.G., Andrews N., Zhao Q., McKean D., Williams J.F., Connor L.J., Gerasimenko O.V., Hilkens J., Hirabayashi J., Kasai K. and Rhodes J.M. (2007). Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J. Biol. Chem. 282, 773-781.
80. Zhu H., Mitsuhashi N., Klein A., Barsky L.W., Weinberg K., Barr M.L., Demetriou A. and Wu G.D. (2006). The role of hyaluronan receptor CD44 in mesenchymal stem cell migration in the extracellular matrix. Stem Cells 24, 928-935.
81. Zuk A., Bonventre J.V., Brown D. and Matlin K.S. (1998). Polarity, integrin, and extracellular matrix dynamics in the postischemic rat kidney. Am. J. Physiol. 275, 711-731.