Fol. Biol. 2014, 60, 95-107

https://doi.org/10.14712/fb2014060030095

Rho GTPase Rac1: Molecular Switch within the Galectin Network and for N-Glycan α2,6-Sialylation/O-Glycan Core 1 Sialylation in Colon Cancer in Vitro

S. André1, T. Singh1, J. C. Lacal2, K. Smetana, Jr3, Hans-Joachim Gabius1

1Ludwig-Maximilians-University Munich, Faculty of Veterinary Medicine, Institute of Physiological Chemistry, Munich, Germany
2Instituto de Investigaciones Biomédicas, CSIC, Madrid, Spain
3Institute of Anatomy, First Faculty of Medicine, Charles University in Prague, Czech Republic

Received February 2014
Accepted February 2014

References

1. Ahmad, N., Gabius, H.-J., Sabesan, S., Oscarson, S., Brewer, C. F. (2004) Thermodynamic binding studies of bivalent oligosaccharides to galectin-1, galectin-3, and the carbohydrate recognition domain of galectin-3. Glycobiology 14, 817-825. <https://doi.org/10.1093/glycob/cwh095>
2. Amado, M., Yan, Q., Comelli, E. M., Collins, B. E., Paulson, J. C. (2004) Peanut agglutinin high phenotype of activated CD8+ T cells results from de novo synthesis of CD45 glycans. J. Biol. Chem. 279, 36689-36697. <https://doi.org/10.1074/jbc.M405629200>
3. Amano, M., Eriksson, H., Manning, J. C., Detjen, K. M., André, S., Nishimura, S.-I., Lehtiö, J., Gabius, H.-J. (2012) Tumour suppressor p16INK4a: anoikis-favouring decrease in N/O-glycan/cell surface sialylation by down-regulation of enzymes in sialic acid biosynthesis in tandem in a pancreatic carcinoma model. FEBS J. 279, 4062-4080. <https://doi.org/10.1111/febs.12001>
4. André, S., Kojima, S., Yamazaki, N., Fink, C., Kaltner, H., Kayser, K., Gabius, H.-J. (1999) Galectins-1 and -3 and their ligands in tumor biology. J. Cancer Res. Clin. Oncol. 125, 461-474.
5. André, S., Liu, B., Gabius, H.-J., Roy, R. (2003) First demonstration of differential inhibition of lectin binding by synthetic triand tetravalent glycoclusters from cross-coupling of rigidified 2-propynyl lactoside. Org. Biomol. Chem. 1, 3909-3916. <https://doi.org/10.1039/B307802G>
6. 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 Doeberitz, M., Gress, T. M., Nishimura, S.-I., Rosewicz, S., Gabius, H.-J. (2007) 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. <https://doi.org/10.1111/j.1742-4658.2007.05851.x>
7. André, S., Renaudet, O., Bossu, I., Dumy, P., Gabius, H.-J. (2011) Cyclic neoglycodecapeptides: how to increase their inhibitory activity and selectivity on lectin/toxin binding to a glycoprotein and cells. J. Pept. Sci. 17, 427-437. <https://doi.org/10.1002/psc.1338>
8. Avellana-Adalid, V., Joubert-Caron, R., Caron, M., Bladier, D. (1992) Electrophoretic study of conformational changes of a human soluble β-D-galactoside-binding lectin upon storage. Electrophoresis 13, 416-421. <https://doi.org/10.1002/elps.1150130188>
9. Barkan,B.,Cox,A.D.,Kloog,Y.(2013)Rasinhibitionboosts galectin-7 at the expense of galectin-1 to sensitize cells to apoptosis. Oncotarget 4, 256-268. <https://doi.org/10.18632/oncotarget.844>
10. Bolscher, J. G. M., van der Bijl, M. M. M., Neefjes, J. J., Hall, A., Smets, L. A., Ploegh, H. L. (1988) Ras (proto)oncogene induces N-linked carbohydrate modification: temporal relationship with induction of invasive potential. EMBO J. 7, 3361-3368. <https://doi.org/10.1002/j.1460-2075.1988.tb03208.x>
11. Burridge, K., Wennerberg, K. (2004) Rho and Rac take center stage. Cell 116, 167-179. <https://doi.org/10.1016/S0092-8674(04)00003-0>
12. Čada, Z., Smetana, K. Jr., Lacina, L., Plzáková, Z., Štork, J., Kaltner, H., Russwurm, R., Lensch, M., André, S., Gabius, H.-J. (2009) Immunohistochemical fingerprinting of the network of seven adhesion/growth-regulatory lectins in human skin and detection of distinct tumour-associated alterations. Folia Biol. (Praha) 55, 145-152.
13. Camby, I., Belot, N., Lefranc, F., Sadeghi, N., de Launoit, Y., Kaltner, H., Musette, S., Darro, F., Danguy, A., Salmon, I., Gabius, H.-J., Kiss, R. (2002) Galectin-1 modulates human glioblastoma cell migration into the brain through modifications to the actin cytoskeleton and levels of expression of small GTPases. J. Neuropathol. Exp. Neurol. 61, 585-596. <https://doi.org/10.1093/jnen/61.7.585>
14. Chokhawala, H. A., Huang, S., Lau, K., Yu, H., Cheng, J., Thon, V., Hurtado-Ziola, N., Guerrero, J. A., Varki, A., Chen, X. (2008) Combinatorial chemoenzymatic synthesis and high-throughput screening of sialosides. ACS Chem. Biol. 3, 567-576. <https://doi.org/10.1021/cb800127n>
15. Cludts, S., Decaestecker, C., Mahillon, V., Chevalier, D., Kaltner, H., André, S., Remmelink, M., Leroy, X., Gabius, H.-J., Saussez, S. (2009) Galectin-8 up-regulation during hypopharyngeal and laryngeal tumor progression and comparison with galectins-1, -3 and -7. Anticancer Res. 29, 4933-4940.
16. Coso, O. A., Chiariello, M., Yu, J.-C., Teramoto, H., Crespo, P., Xu, N., Miki, T., Gutkind, J. S. (1995) The small GTPbinding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146. <https://doi.org/10.1016/S0092-8674(05)80018-2>
17. Dall'Olio, F., Malagolini, N., Di Stefano, G., Ciambella, M., Serafini-Cessi, F. (1991) α2,6-Sialylation of N-acetyllactosaminic sequences in human colorectal cancer cell lines. Relationship with non-adherent growth. Int. J. Cancer 47, 291-297. <https://doi.org/10.1002/ijc.2910470220>
18. Dall'Olio, F., Chiricolo, M., Lau, J. T. Y. (1999) Differential expression of the hepatic transcript of β-galactoside α2,6sialyltransferase in human colon cancer cell lines. Int. J. Cancer 81, 243-247. <https://doi.org/10.1002/(SICI)1097-0215(19990412)81:2<243::AID-IJC13>3.0.CO;2-O>
19. Dalziel, M., Dall‘Olio, F., Mungul, A., Piller, V., Piller, F. (2004) Ras oncogene induces β-galactoside α2,6sialyltransferase (ST6Gal-I) via a RalGEF-mediated signal to its housekeeping promoter. Eur. J. Biochem. 271, 3623-3634. <https://doi.org/10.1111/j.1432-1033.2004.04284.x>
20. Dawson, H., André, S., Karamitopoulou, E., Zlobec, I., Gabius, H.-J. (2013) The growing galectin network in colon cancer and clinical relevance of cytoplasmic galectin-3 reactivity. Anticancer Res. 33, 3053-3059.
21. Díez-Revuelta, N., Velasco, S., André, S., Kaltner, H., Kübler, D., Gabius, H.-J., Abad-Rodríguez, J. (2010) Phosphorylation of adhesion-/growth-regulatory human galectin-3 leads to the induction of axonal branching by local membrane L1 and ERM redistribution. J. Cell Sci. 123, 671-681. <https://doi.org/10.1242/jcs.058198>
22. Dvořánková, B., Szabo, P., Lacina, L., Gál, P., Uhrova, J., Zima, T., Kaltner, H., André, S., Gabius, H.-J., Sykova, E., Smetana, K. Jr. (2011) Human galectins induce conversion of dermal fibroblasts into myofibroblasts and production of extracellular matrix: potential application in tissue engineering and wound repair. Cells Tissues Organs 194, 469-480. <https://doi.org/10.1159/000324864>
23. Elad-Sfadia, G., Haklai, R., Ballan, E., Gabius, H.-J., Kloog, Y. (2002) Galectin-1 augments Ras activation and diverts Ras signals to Raf-1 at the expense of phosphoinositide 3-kinase. J. Biol. Chem. 277, 37169-37175. <https://doi.org/10.1074/jbc.M205698200>
24. Espina, C., Céspedes, M. V., García-Cabezas, M. A., Gómez del Pulgar, M. T., Boluda, A., Oroz, L. G., Cejas, P., Nistal, M., Mangues, R., Lacal, J. C. (2008) A critical role for Rac1 in tumor progression of human colorectal adenocarcinoma cells. Am. J. Pathol. 172, 156-166. <https://doi.org/10.2353/ajpath.2008.070561>
25. Fík, Z., Valach, J., Chovanec, M., Mazánek, J., Kodet, R., Kodet, O., Tachezy, R., Foltynová, E., André, S., Kaltner, H., Gabius, H.-J., Smetana, K. Jr. (2013) Loss of adhesion/ growth-regulatory galectin-9 from squamous cell epithelium in head and neck carcinomas. J. Oral Pathol. Med. 42, 166-173. <https://doi.org/10.1111/j.1600-0714.2012.01185.x>
26. Fischer, C., Sanchez-Ruderisch, H., Welzel, M., Wiedenmann, B., Sakai, T., André, S., Gabius, H.-J., Khachigian, L., Detjen, K. M., Rosewicz, S. (2005) Galectin-1 interacts with the α5β1 fibronectin receptor to restrict carcinoma cell growth via induction of p21 and p27. J. Biol. Chem. 280, 37266-37277. <https://doi.org/10.1074/jbc.M411580200>
27. Gabius, H.-J. (ed.) (2009) The Sugar Code. Fundamentals of Glycosciences. Wiley-VCH, Weinheim, Germany.
28. Gabius, H.-J., Kayser, K. (2014) Introduction to glycopathology: the concept, the tools and the perspectives. Diagn. Pathol. 9, 4. <https://doi.org/10.1186/1746-1596-9-4>
29. Gabius, H.-J., André, S., Jiménez-Barbero, J., Romero, A., Solís, D. (2011) From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem. Sci. 36, 298-313. <https://doi.org/10.1016/j.tibs.2011.01.005>
30. Gabius, H.-J., van de Wouwer, M., André, S., Villalobo, A. (2012) Down-regulation of the epidermal growth factor receptor by altering N-glycosylation: emerging role of β1,4galactosyltransferases. Anticancer Res. 32, 1565-1572.
31. Gál, P., Vasilenko, T., Kostelníková, M., Jakubčo, J., Kováč, I., Sabol, F., André, S., Kaltner, H., Gabius, H.-J., Smetana, K. Jr. (2011) Open wound healing in vivo: monitoring binding and presence of adhesion/growth-regulatory galectins in rat skin during the course of complete re-epithelialization. Acta Histochem. Cytochem. 44, 191-199. <https://doi.org/10.1267/ahc.11014>
32. Gebert, J., Kloor, M., Lee, J., Lohr, M., André, S., Wagner, R., Kopitz, J., Gabius, H.-J. (2012) Colonic carcinogenesis along different genetic routes: glycophenotyping of tumor cases separated by microsatellite instability/stability. Histochem. Cell Biol. 138, 339-350. <https://doi.org/10.1007/s00418-012-0957-9>
33. Gómez del Pulgar, T., Benitah, S. A., Valerón, P. F., Espina, C., Lacal, J. C. (2005) Rho GTPase expression in tumourigenesis: evidence for a significant link. BioEssays 27, 602-613. <https://doi.org/10.1002/bies.20238>
34. Gómez del Pulgar, T., Bandrés, E., Espina, C., Valdés-Mora, F., Pérez-Palacios, R., Garciá-Amigot, F., Garciá-Foncillas, J., Lacal, J. C. (2007) Differential expression of Rac1 identifies its target genes and its contribution to progression of colorectal cancer. Int. J. Biochem. Cell Biol. 39, 2289-2302. <https://doi.org/10.1016/j.biocel.2007.06.014>
35. Grendel, T., Sokolský, J., Vaščáková, A., Hudák, V., Chovanec, M., Sabol, F., André, S., Kaltner, H., Gabius, H.-J., Frankovičová, M., Lenčeš, P., Betka, J., Smetana, K. Jr., Gál, P. (2012) Early stages of trachea healing process: (immuno/lectin) histochemical monitoring of selected markers and adhesion/growth-regulatory endogenous lectins. Folia Biol. (Praha) 58, 135-143.
36. Gu, J., Isaji, T., Sato, Y., Kariya, Y., Fukuda, T. (2009) Importance of N-glycosylation on α5β1-integrin for its biological functions. Biol. Pharm. Bull. 32, 780-785. <https://doi.org/10.1248/bpb.32.780>
37. Habermann, F. A., André, S., Kaltner, H., Kübler, D., Sinowatz, F., Gabius, H.-J. (2011) Galectins as tools for glycan mapping in histology: comparison of their binding profiles to the bovine zona pellucida by confocal laser scanning microscopy. Histochem. Cell Biol. 135, 539-552. <https://doi.org/10.1007/s00418-011-0814-2>
38. Hamann, K. K., Cowles, E. A., Wang, J. L., Anderson, R. L. (1991) Expression of carbohydrate binding protein 35 in human fibroblasts: variations in the levels of mRNA, protein, and isoelectric species as a function of replicative competence. Exp. Cell Res. 196, 82-91. <https://doi.org/10.1016/0014-4827(91)90458-7>
39. Haudek, K. C., Spronk, K. J., Voss, P. G., Patterson, R. J., Wang, J. L., Arnoys, E. J. (2010) Dynamics of galectin-3 in the nucleus and cytoplasm. Biochim. Biophys. Acta 1800, 181-189. <https://doi.org/10.1016/j.bbagen.2009.07.005>
40. Heasman, S. J., Ridley, A. J. (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701. <https://doi.org/10.1038/nrm2476>
41. Hittelet, A., Legendre, H., Nagy, N., Bronckart, Y., Pector, J.-C., Salmon, I., Yeaton, P., Gabius, H.-J., Kiss, R., Camby, I. (2003) Upregulation of galectins-1 and -3 in human colon cancer and their role in regulating cell migration. Int. J. Cancer 103, 370-379. <https://doi.org/10.1002/ijc.10843>
42. Hodis, E., Watson, I. R., Kryukov, G. V., Arold, S. T., Imielinski, M., Theurillat, J.-P., Nickerson, E., Auclair, D., Li, L., Place, C., Dicara, D., Ramos, A. H., Lawrence, M. S., Cibulskis, K., Sivachenko, A., Voet, D., Saksena, G., Stransky, N., Onofrio, R. C., Winckler, W., Ardlie, K., Wagle, N., Wargo, J., Chong, K., Morton, D. L., StemkeHale, K., Chen, G., Noble, M., Meyerson, M., Ladbury, J. E., Davies, M. A., Gershenwald, J. E., Wagner, S. N., Hoon, D. S. B., Schadendorf, D., Lander, E. S., Gabriel, S. B., Getz, G., Garraway, L. A., Chin, L. (2012) A landscape of driver mutations in melanoma. Cell 150, 251-263. <https://doi.org/10.1016/j.cell.2012.06.024>
43. Jaffe, A. B., Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269. <https://doi.org/10.1146/annurev.cellbio.21.020604.150721>
44. Kaltner, H., Gabius, H.-J. (2012) A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol. Histopathol. 27, 397-416.
45. Knibbs, R. N., Goldstein, I. J., Ratcliffe, R. M., Shibuya, N. (1991) Characterization of the carbohydrate-binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J. Biol. Chem. 266, 83-88. <https://doi.org/10.1016/S0021-9258(18)52405-4>
46. Kodet, O., Dvořánková, B., Lacina, L., André, S., Kaltner, H., Gabius, H.-J., Smetana, K. Jr. (2011) Comparative analysis of the nuclear presence of adhesion/growth-regulatory galectins and reactivity in the nuclei of interphasic and mitotic cells. Folia Biol. (Praha) 57, 125-132.
47. Kopitz, J., von Reitzenstein, C., Burchert, M., Cantz, M., Gabius, H.-J. (1998) Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J. Biol. Chem. 273, 11205-11211. <https://doi.org/10.1074/jbc.273.18.11205>
48. Kopitz, J., von Reitzenstein, C., André, S., Kaltner, H., Uhl, J., Ehemann, V., Cantz, M., Gabius, H.-J. (2001) Negative regulation of neuroblastoma cell growth by carbohydratedependent surface binding of galectin-1 and functional divergence from galectin-3. J. Biol. Chem. 276, 35917-35923. <https://doi.org/10.1074/jbc.M105135200>
49. Kopitz, J., Fík, Z., André, S., Smetana, K. Jr., Gabius, H.-J. (2013) Single-site mutational engineering and following monoPEGylation of the human lectin galectin-2: effects on ligand binding, functional aspects, and clearance from serum. Mol. Pharmaceut. 10, 2054-2061. <https://doi.org/10.1021/mp4000629>
50. Krauthammer, M., Kong, Y., Ha, B. H., Evans, P., Bacchiocchi, A., McCusker, J. P., Cheng, E., Davis, M. J., Goh, G., Choi, M., Ariyan, S., Narayan, D., Dutton-Regester, K., Capatana, A., Holman, E. C., Bosenberg, M., Sznol, M., Kluger, H. M., Brash, D. E., Stern, D. F., Materin, M. A., Lo, R. S., Mane, S., Ma, S., Kidd, K. K., Hayward, N. K., Lifton, R. P., Schlessinger, J., Boggon, T. J., Halaban, R. (2012) Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat. Genet. 44, 1006-1014. <https://doi.org/10.1038/ng.2359>
51. Krzeminski, M., Singh, T., André, S., Lensch, M., Wu, A. M., Bonvin, A. M. J. J., Gabius, H.-J. (2011) Human galectin-3 (Mac-2 antigen): defining molecular switches of affinity to natural glycoproteins, structural and dynamic aspects of glycan binding by flexible ligand docking and putative regulatory sequences in the proximal promoter region. Biochim. Biophys. Acta 1810, 150-161. <https://doi.org/10.1016/j.bbagen.2010.11.001>
52. Kübler, D., Seidler, J., André, S., Kumar, S., Schwartz-Albiez, R., Lehmann, W.-D., Gabius, H.-J. (2014) Phosphorylation of multifunctional galectins by protein kinases CK1, CK2, and PKA. Anal. Biochem. 449, 109-117. <https://doi.org/10.1016/j.ab.2013.12.006>
53. Lahm, H., André, S., Hoeflich, A., Fischer, J. R., Sordat, B., Kaltner, H., Wolf, E., Gabius, H.-J. (2001) Comprehensive galectin fingerprinting in a panel of 61 human tumor cell lines by RT-PCR and its implications for diagnostic and therapeutic procedures. J. Cancer Res. Clin. Oncol. 127, 375-386. <https://doi.org/10.1007/s004320000207>
54. Le Marer, N., Laudet, V., Svensson, E. C., Cazlaris, H., van Hille, B., Lagrou, C., Stehelin, D., Montreuil, J., Verbert, A., Delannoy, P. (1992) The c-Ha-ras oncogene induces increased expression of β-galactoside α2,6-sialyltransferase in rat fibroblast (FR3T3) cells. Glycobiology 2, 49-56. <https://doi.org/10.1093/glycob/2.1.49>
55. Ledeen, R. W., Wu, G., André, S., Bleich, D., Huet, G., Kaltner, H., Kopitz, J., Gabius, H.-J. (2012) Beyond glycoproteins as galectin counterreceptors: tumor-effector T cell growth control via ganglioside GM1. Ann. NY Acad. Sci. 1253, 206-221. <https://doi.org/10.1111/j.1749-6632.2012.06479.x>
56. Liu, S., Kapoor, M., Leask, A. (2009) Rac1 expression by fibroblasts is required for tissue repair in vivo. Am. J. Pathol. 174, 1847-1856. <https://doi.org/10.2353/ajpath.2009.080779>
57. Lohr, M., Lensch, M., André, S., Kaltner, H., Siebert, H.-C., Smetana, K. Jr., Sinowatz, F., 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.
58. Machesky, L. M., Sansom, O. J. (2012) Rac1 in the driver's seat for melanoma. Pigment Cell Melanoma Res. 25, 762-764. <https://doi.org/10.1111/pcmr.12004>
59. Montaner, S., Perona, R., Saniger, L., Lacal, J. C. (1998) Multiple signalling pathways lead to the activation of the nuclear factor κB by the Rho family of GTPases. J. Biol. Chem. 273, 12779-12785. <https://doi.org/10.1074/jbc.273.21.12779>
60. 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., Gabius, H.-J. (2002) Galectin-8 expression decreases in cancer compared with normal and dysplastic human colon tissue and acts significantly on human colon cancer cell migration as a suppressor. Gut 50, 392-401. <https://doi.org/10.1136/gut.50.3.392>
61. Nagy, N., Legendré, H., Engels, O., André, S., Kaltner, H., Wasano, K., Zick, Y., Pector, J.-C., Decaestecker, C., Gabius, H.-J., Salmon, I., Kiss, R. (2003) Refined prognostic evaluation in colon carcinoma using immunohistochemical galectin fingerprinting. Cancer 97, 1849-1858. <https://doi.org/10.1002/cncr.11268>
62. Patsos, G., Corfield, A. (2009) O-Glycosylation: structural diversity and functions. In: The Sugar Code. Fundamentals of Glycosciences, ed. Gabius, H.-J., pp. 111-137, Wiley-VCH, Weinheim, Germany.
63. Patsos, G., André, S., Roeckel, N., Gromes, R., Gebert, J., Kopitz, J., Gabius, H.-J. (2009) Compensation of loss of protein function in microsatellite-unstable colon cancer cells (HCT116): a gene-dependent effect on the cell surface glycan profile. Glycobiology 19, 726-734. <https://doi.org/10.1093/glycob/cwp040>
64. Perona, R., Montaner, S., Saniger, L., Sánchez-Pérez, I., Bravo, R., Lacal, J. C. (1997) Activation of the nuclear factor-κB by Rho, CDC42, and Rac-1 proteins. Genes Dev. 11, 463-475. <https://doi.org/10.1101/gad.11.4.463>
65. Plzák, J., Betka, J., Smetana, K. Jr., Chovanec, M., Kaltner, H., André, S., Kodet, R., Gabius, H.-J. (2004) Galectin-3: an emerging prognostic indicator in advanced head and neck carcinoma. Eur. J. Cancer 40, 2324-2330. <https://doi.org/10.1016/j.ejca.2004.06.025>
66. Polyak, K., Xia, Y., Zweier, J. L., Kinzler, K. W., Vogelstein, B. (1997) A model for p53-induced apoptosis. Nature 389, 300-305. <https://doi.org/10.1038/38525>
67. Purkrábková, T., Smetana, K. Jr., Dvořánková, B., Holíková, Z., Böck, C., Lensch, M., André, S., Pytlík, R., Liu, F.-T., Klíma, J., Smetana, K., Motlík, J., 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. <https://doi.org/10.1016/j.biolcel.2003.08.002>
68. Remmelink, M., de Leval, L., Decaestecker, C., Duray, A., Crompot, E., Sirtaine, N., André, S., Kaltner, H., Leroy, X., Gabius, H.-J., Saussez, S. (2011) Quantitative immunohistochemical fingerprinting of adhesion/growth-regulatory galectins in salivary gland tumours: divergent profiles with diagnostic potential. Histopathology 58, 543-556. <https://doi.org/10.1111/j.1365-2559.2011.03776.x>
69. Roda, O., Ortiz-Zapater, E., Martínez-Bosch, N., GutiérrezGallego, R., Vila-Perelló, M., Ampurdanés, C., Gabius, H.J., André, S., Andreu, D., Real, F. X., Navarro, P. (2009) Galectin-1 is a novel functional receptor for tissue plasminogen activator in pancreatic cancer. Gastroenterology 136, 1379-1390. <https://doi.org/10.1053/j.gastro.2008.12.039>
70. Rotblat, B., Niv, H., André, S., Kaltner, H., Gabius, H.-J., Kloog, Y. (2004) Galectin-1(L11A) predicted from a computed galectin-1 farnesyl-binding pocket selectively inhibits Ras-GTP. Cancer Res. 64, 3112-3118. <https://doi.org/10.1158/0008-5472.CAN-04-0026>
71. Saal, I., Nagy, N., Lensch, M., Lohr, M., Manning, J. C., Decaestecker, C., André, S., Kiss, R., Salmon, I., Gabius, H.-J. (2005) Human galectin-2: expression profiling by RTPCR/immunohistochemistry and its introduction as a histochemical tool for ligand localization. Histol. Histopathol. 20, 1191-1208.
72. Sanchez-Ruderisch, H., Fischer, C., Detjen, K. M., Welzel, M., Wimmel, A., Manning, J. C., André, S., Gabius, H.-J. (2010) Tumor suppressor p16INK4a: downregulation of galectin-3, an endogenous competitor of the pro-anoikis effector galectin-1, in a pancreatic carcinoma model. FEBS J. 277, 3552-3563. <https://doi.org/10.1111/j.1742-4658.2010.07764.x>
73. Sanchez-Ruderisch, H., Detjen, K. M., Welzel, M., André, S., Fischer, C., Gabius, H.-J., Rosewicz, S. (2011) Galectin-1 sensitizes carcinoma cells to anoikis via the fibronectin receptor α5β1-integrin. Cell Death Differ. 18, 806-816. <https://doi.org/10.1038/cdd.2010.148>
74. Saussez, S., Cludts, S., Capouillez, A., Mortuaire, G., Smetana, K. Jr., Kaltner, H., André, S., Leroy, X., Gabius, H.-J., Decaestecker, C. (2009) Identification of matrix metalloproteinase-9 as an independent prognostic marker in laryngeal and hypopharyngeal cancer with opposite correlations to adhesion/growth-regulatory galectins-1 and -7. Int. J. Oncol. 34, 433-439.
75. Schlötzer-Schrehardt, U., André, S., Janko, C., Kaltner, H., Kopitz, J., Gabius, H.-J., Herrmann, M. (2012) Adhesion/ growth-regulatory galectins in the human eye: localization profiles and tissue reactivities as a standard to detect disease-associated alterations. Graefe's Arch. Clin. Exp. Ophthalmol. 250, 1169-1180. <https://doi.org/10.1007/s00417-012-2021-9>
76. Seales, E. C., Jurado, G. A., Singhal, A., Bellis, S. L. (2003) Ras oncogene directs expression of a differentially sialylated, functionally altered β1-integrin. Oncogene 22, 7137-7145. <https://doi.org/10.1038/sj.onc.1206834>
77. Seales, E. C., Gustavo, A. J., Brunson, B. A., Wakefield, J. K., Frost, A. R., Bellis, S. L. (2005) Hypersialylation of β1integrins, observed in colon adenocarcinoma, may contribute to cancer progression by up-regulating cell motility. Cancer Res. 65, 4645-4652. <https://doi.org/10.1158/0008-5472.CAN-04-3117>
78. Sengupta, P. K., Bouchie, M. P., Kukuruzinska, M. A. (2010) N-Glycosylation gene DPAGT1 is a target of the Wnt/βcatenin signaling pathway. J. Biol. Chem. 285, 31164-31173. <https://doi.org/10.1074/jbc.M110.149195>
79. Shaikh, F. M., Seales, E. C., Clem, W. C., Hennessy, K. M., Zhuo, Y., Bellis, S. L. (2008) Tumor cell migration and invasion are regulated by expression of variant integrin glycoforms. Exp. Cell Res. 314, 2941-2950. <https://doi.org/10.1016/j.yexcr.2008.07.021>
80. Smetana, K. Jr., André, S., Kaltner, H., Kopitz, J., Gabius, H.J. (2013) Context-dependent multifunctionality of galectin-1: a challenge for defining the lectin as therapeutic target. Exp. Opin. Ther. Targets 17, 379-392. <https://doi.org/10.1517/14728222.2013.750651>
81. Uemura, T., Shiozaki, K., Yamaguchi, K., Miyazaki, S., Satomi, S., Kato, K., Sakuraba, H., Miyagi, T. (2009) Contribution of sialidase NEU1 to suppression of metastasis of human colon cancer cells through desialylation of integrin β4. Oncogene 28, 1218-1229. <https://doi.org/10.1038/onc.2008.471>
82. Valach, J., Fík, Z., Strnad, H., Chovanec, M., Plzák, J., Čada, Z., Szabo, P., Šáchová, J., Hroudová, M., Urbanová, M., Šteffl, M., Pačes, J., Mazánek, J., Vlček, Č., Betka, J., Kaltner, H., André, S., Gabius, H.-J., Kodet, R., Smetana, K. Jr., Gál, P., Kolář, M. (2012) Smooth muscle actin-expressing stromal fibroblasts in head and neck squamous cell carcinoma: increased expression of galectin-1 and induction of poor prognosis factors. Int. J. Cancer 131, 2499-2508. <https://doi.org/10.1002/ijc.27550>
83. Vandamme, V., Cazlaris, H., Le Marer, N., Laudet, V., Lagrou, C., Verbert, A., Delannoy, P. (1992) Comparison of sialyland α1,3-galactosyltransferase activity in NIH3T3 cells transformed with ras oncogene: increased β-galactoside α2,6-sialyltransferase. Biochimie 74, 89-99. <https://doi.org/10.1016/0300-9084(92)90188-K>
84. Villalobo, A., Nogales-González, A., Gabius, H.-J. (2006) A guide to signaling pathways connecting protein-glycan interaction with the emerging versatile effector functionality of mammalian lectins. Trends Glycosci. Glycotechnol. 18, 1-37. <https://doi.org/10.4052/tigg.18.1>
85. Wang, J., Lu, Z.-H., Gabius, H.-J., Rohowsky-Kochan, C., Ledeen, R. W., Wu, G. (2009) Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T cell activity involving TRPC5 channel activation: possible role in suppressing experimental autoimmune encephalomyelitis. J. Immunol. 182, 4036-4045. <https://doi.org/10.4049/jimmunol.0802981>
86. Wasano, K., Hirakawa, Y. (1997) Recombinant galectin-1 recognizes mucin and epithelial cell surface glycocalyces of gastrointestinal tract. J. Histochem. Cytochem. 45, 275-283. <https://doi.org/10.1177/002215549704500212>
87. Wherlock, M., Mellor, H. (2002) The Rho GTPase family: a Racs to Wrchs story. J. Cell Sci. 115, 239-240. <https://doi.org/10.1242/jcs.115.2.239>
88. Wu, G., Lu, Z.-H., Gabius, H.-J., Ledeen, R. W., Bleich, D. (2011) Ganglioside GM1 deficiency in effector T cells from NOD mice induces resistance to regulatory T-cell suppression. Diabetes 60, 2341-2349. <https://doi.org/10.2337/db10-1309>
89. Yu, S., Zhang, L., Li, N., Fan, J., Liu, L., Zhang, J., Wang, S. (2012) Caveolin-1 up-regulates ST6Gal-I to promote the adhesive capability of mouse hepatocarcinoma cells to fibronectin via FAK-mediated adhesion signaling. Biochem. Biophys. Res. Commun. 427, 506-512. <https://doi.org/10.1016/j.bbrc.2012.09.086>
90. Zhu, Y., Srivatana, U., Ullah, A., Gagneja, H., Berenson, C. S., Lance, P. (2001) Suppression of a sialyltransferase by antisense DNA reduces invasiveness of human colon cancer cells in vitro. Biochim. Biophys. Acta 1536, 148-160. <https://doi.org/10.1016/S0925-4439(01)00044-8>
91. Zuber, C., Roth, J. (2009) N-Glycosylation. In: The Sugar Code. Fundamentals of Glycosciences, ed. Gabius, H.-J., pp. 87-110, Wiley-VCH, Weinheim, Germany.
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive