Low or No Inhibitory Potency of the Canonical Galectin Carbohydrate-binding Site by Pectins and Galactomannans

Journal of Biological Chemistry

Volumn 291, Issue 25, 2016, Pages 13318-13334

  Stegmayr, John ^a,b   Lepur, Adriana ^a,f   Kahl Knutson, Barbro ^a   Aguilar Moncayo, Matilde ^c   Klyosov, Anatole A ^d   Field, Robert A ^e   Oredsson, Stina ^c   Nilsson, Ulf J ^b   Leffler, Hakon ^a,e  

^a LUND UNIVERSITY   (Sweden)

^b Department of Biology ^*  (Sweden)

^c NORWICH RESEARCH PARK   (United Kingdom)

^d Galectin Therapeutics   (United States)

^e LUND UNIVERSITY   (Sweden)

^f RUDER BO KOVI INSTITUTE   (Croatia)

Author keywords

[No Author keywords available]

Indexed keywords

ASSAYS; BINDING SITES; BINS; CHAINS; INTEGRATED CIRCUITS; PHYSIOLOGY;

ANTI-INFLAMMATORIES; CARBOHYDRATE BINDING; DIRECT INTERACTIONS; FLUORESCENCE ANISOTROPY; NO INHIBITORY ACTIVITIES; PHYSIOLOGICAL CONCENTRATIONS; PHYSIOLOGICAL EFFECTS; PLANT POLYSACCHARIDES;

POLYSACCHARIDES;

GALACTAN; GALACTOMANNAN; GALECTIN; GALECTIN 3; MANNOSIDE; OLIGOSACCHARIDE; PECTIN; ANTINEOPLASTIC AGENT; DAVANAT; GALACTOSE; POLYSACCHARIDE; PROTEIN BINDING;

ANISOTROPY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; BREAST CANCER CELL LINE; CARBOHYDRATE ANALYSIS; CELL ASSAY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; HUMAN; HUMAN CELL; IC50; INHIBITION KINETICS; MINIMUM INHIBITORY CONCENTRATION; PRIORITY JOURNAL; PROTEIN INTERACTION; RECEPTOR BINDING; ANALOGS AND DERIVATIVES; CHEMISTRY; DRUG SCREENING; FLUORESCENCE POLARIZATION; HEMAGGLUTINATION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BINDING SITES; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; FLUORESCENCE POLARIZATION; GALACTOSE; GALECTINS; HEMAGGLUTINATION; HUMANS; INHIBITORY CONCENTRATION 50; PECTINS; POLYSACCHARIDES; PROTEIN BINDING;

EID: 84975077039     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.721464     Document Type: Article

References (77)

1. Platt, D., and Raz, A. (1992) Modulation of the lung colonization of B16-F1 melanoma cells by citrus pectin. J. Natl. Cancer Inst. 84, 438-442
2. Inohara, H., and Raz, A. (1994) Effects of natural complex carbohydrate (citrus pectin) on murine melanoma cell properties related to galectin-3 functions. Glycoconj. J. 11, 527-532
3. Pienta, K. J., Naik, H., Akhtar, A., Yamazaki, K., Replogle, T. S., Lehr, J., Donat, T. L., Tait, L., Hogan, V., and Raz, A. (1995) Inhibition of spontaneous metastasis in a rat prostate cancer model by oral administration of modified citrus pectin. J. Natl. Cancer Inst. 87, 348-353
4. Nangia-Makker, P., Honjo, Y., Sarvis, R., Akahani, S., Hogan, V., Pienta, K. J., and Raz, A. (2000) Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am. J. Pathol. 156, 899-909
5. Nangia-Makker, P., Hogan, V., Honjo, Y., Baccarini, S., Tait, L., Bresalier, R., and Raz, A. (2002) Inhibition of human cancer cell growth and metastasis in nude mice by oral intake of modified citrus pectin. J. Natl. Cancer Inst. 94, 1854-1862
6. Chauhan, D., Li, G., Podar, K., Hideshima, T., Neri, P., He, D., Mitsiades, N., Richardson, P., Chang, Y., Schindler, J., Carver, B., and Anderson, K. C. (2005) A novel carbohydrate-based therapeutic GCS-100 overcomes bortezomib resistance and enhances dexamethasone-induced apoptosis in multiple myeloma cells. Cancer Res. 65, 8350-8358
7. Glinskii, O. V., Huxley, V. H., Glinsky, G. V., Pienta, K. J., Raz, A., and Glinsky, V. V. (2005) Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia 7, 522-527
8. Jackson, C. L., Dreaden, T. M., Theobald, L. K., Tran, N. M., Beal, T. L., Eid, M., Gao, M. Y., Shirley, R. B., Stoffel, M. T., Kumar, M. V., and Mohnen, D. (2007) Pectin induces apoptosis in human prostate cancer cells: correlation of apoptotic function with pectin structure. Glycobiology 17, 805-819
9. Johnson, K. D., Glinskii, O. V., Mossine, V. V., Turk, J. R., Mawhinney, T. P., Anthony, D. C., Henry, C. J., Huxley, V. H., Glinsky, G. V., Pienta, K. J., Raz, A., and Glinsky, V. V. (2007) Galectin-3 as a potential therapeutic target in tumors arising from malignant endothelia. Neoplasia 9, 662- 670
10. Glinsky, V. V., and Raz, A. (2009) Modified citrus pectin anti-metastatic properties: one bullet, multiple targets. Carbohydr. Res. 344, 1788-1791
11. Demotte, N., Wieërs, G., Van Der Smissen, P., Moser, M., Schmidt, C., Thielemans, K., Squifflet, J. L., Weynand, B., Carrasco, J., Lurquin, C., Courtoy, P. J., and van der Bruggen, P. (2010) A galectin-3 ligand corrects the impaired function of human CD4 and CD8 tumor-infiltrating lymphocytes and favors tumor rejection in mice. Cancer Res. 70, 7476-7488
12. Yan, J., and Katz, A. (2010) PectaSol-C modified citrus pectin induces apoptosis and inhibition of proliferation in human and mouse androgendependent and -independent prostate cancer cells. Integr. Cancer Ther. 9, 197-203
13. Streetly, M. J., Maharaj, L., Joel, S., Schey, S. A., Gribben, J. G., and Cotter, F. E. (2010) GCS-100, a novel galectin-3 antagonist, modulates MCL-1, NOXA, and cell cycle to induce myeloma cell death. Blood 115, 3939-3948
14. Vayssade, M., Sengkhamparn, N., Verhoef, R., Delaigue, C., Goundiam, O., Vigneron, P., Voragen, A. G., Schols, H. A., and Nagel, M. D. (2010) Antiproliferative and proapoptotic actions of okra pectin on B16F10 melanoma cells. Phytother. Res. 24, 982-989
15. Kolatsi-Joannou, M., Price, K. L., Winyard, P. J., and Long, D. A. (2011) Modified citrus pectin reduces galectin-3 expression and disease severity in experimental acute kidney injury. PLoS ONE 6, e18683
16. Yamamoto-Sugitani, M., Kuroda, J., Ashihara, E., Nagoshi, H., Kobayashi, T., Matsumoto, Y., Sasaki, N., Shimura, Y., Kiyota, M., Nakayama, R., Akaji, K., Taki, T., Uoshima, N., Kobayashi, Y., Horiike, S., et al. (2011) Galectin-3 (Gal-3) induced by leukemia microenvironment promotes drug resistance and bone marrow lodgment in chronic myelogenous leukemia. Proc. Natl. Acad. Sci. U.S.A. 108, 17468-17473
17. Gao, X., Zhi, Y., Zhang, T., Xue, H., Wang, X., Foday, A. D., Tai, G., and Zhou, Y. (2012) Analysis of the neutral polysaccharide fraction of MCP and its inhibitory activity on galectin-3. Glycoconj. J. 29, 159-165
18. Clark, M. C., Pang, M., Hsu, D. K., Liu, F. T., de Vos, S., Gascoyne, R. D., Said, J., and Baum, L. G. (2012) Galectin-3 binds to CD45 on diffuse large B-cell lymphoma cells to regulate susceptibility to cell death. Blood 120, 4635- 4644
19. Jiang, J., Eliaz, I., and Sliva, D. (2013) Synergistic and additive effects of modified citrus pectin with two polybotanical compounds, in the suppression of invasive behavior of human breast and prostate cancer cells. Integr Cancer Ther. 12, 145-152
20. MacKinnon, A. C., Liu, X., Hadoke, P. W., Miller, M. R., Newby, D. E., and Sethi, T. (2013) Inhibition of galectin-3 reduces atherosclerosis in apolipoprotein E-deficient mice. Glycobiology 23, 654-663
21. Gao, X., Zhi, Y., Sun, L., Peng, X., Zhang, T., Xue, H., Tai, G., and Zhou, Y. (2013) The inhibitory effects of a rhamnogalacturonan I (RG-I) domain from ginseng pectin on galectin-3 and its structure-activity relationship. J. Biol. Chem. 288, 33953-33965
22. Martínez-Martínez, E., López-Ándres, N., Jurado-López, R., Rousseau, E., Bartolomé, M. V., Fernández-Celis, A., Rossignol, P., Islas, F., Antequera, A., Prieto, S., Luaces, M., and Cachofeiro, V. (2015) Galectin-3 participates in cardiovascular remodeling associated with obesity. Hypertension 66, 961-969
23. Martinez-Martinez, E., Calvier, L., Rossignol, P., Rousseau, E., Fernandez-Celis, A., Jurado-Lopez, R., Laville, M., Cachofeiro, V., and Lopez-Andres, N. (2016) Galectin-3 inhibition prevents adipose tissue remodelling in obesity. Int. J. Obes. 10.1038/ijo.2016.19
24. Ma, Z., Han, Q., Wang, X., Ai, Z., and Zheng, Y. (2016) Galectin-3 inhibition is associated with neuropathic pain attenuation after peripheral nerve injury. PLoS ONE 11, e0148792
25. Ridley, B. L., O'Neill, M. A., and Mohnen, D. (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57, 929-967
26. Caffall, K. H., and Mohnen, D. (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res. 344, 1879-1900
27. Maxwell, E. G., Belshaw, N. J., Waldron, K. W., and Morris, V. J. (2012) Pectin-an emerging new bioactive food polysaccharide. Trends Food Sci. Technol. 24, 64-73
28. Thibault, J. F., Renard, C. M., Axelos, M. A., Roger, P., and Crepeau, M. J. (1993) Studies of the length of homogalacturonic regions in pectins by acid-hydrolysis. Carbohydr. Res. 238, 271-286
29. Gunning, A. P., Bongaerts, R. J., and Morris, V. J. (2009) Recognition of galactan components of pectin by galectin-3. FASEB J. 23, 415- 424
30. Yu, L., Zhang, X., Li, S. S., Liu, X. Y., Sun, L., Liu, H. B., Iteku, J., Zhou, Y. F., and Tai, G. H. (2010) Rhamnogalacturonan I domains from ginseng pectin. Carbohydr. Polym. 79, 811-817
31. Klyosov, A. A., Platt, D., and Zomer, E. (2003) Preclinical studies of anticancer efficacy of 5-fluorouracil when co-administered with the 1,4-β-Dgalactomannan. Preclinica 1, 175-184
32. Klyosov, A. A., Zomer, E., and Platt, D. (2006) in Carbohydrate Drug Design (Klyosov, A. A., Witczak, Z. J., and Platt, D., eds) pp. 67-104, American Chemical Society, Washington, D. C.
33. Miller, M. C., Klyosov, A., Platt, D., and Mayo, K. H. (2009) Using pulse field gradient NMR diffusion measurements to define molecular size distributions in glycan preparations. Carbohydr. Res. 344, 1205-1212
34. Miller, M. C., Klyosov, A., and Mayo, K. H. (2009) The α-galactomannan Davanat binds galectin-1 at a site different from the conventional galectin carbohydrate binding domain. Glycobiology 19, 1034-1045
35. Leffler, H., Carlsson, S., Hedlund, M., Qian, Y., and Poirier, F. (2004) Introduction to galectins. Glycoconj. J. 19, 433- 440
36. Di Lella, S., Sundblad, V., Cerliani, J. P., Guardia, C. M., Estrin, D. A., Vasta, G. R., and Rabinovich, G. A. (2011) When galectins recognize glycans: from biochemistry to physiology and back again. Biochemistry 50, 7842-7857
37. Newlaczyl, A. U., and Yu, L. G. (2011) Galectin-3-a jack-of-all-trades in cancer. Cancer Lett. 313, 123-128
38. Sathisha, U. V., Jayaram, S., Harish Nayaka, M. A., and Dharmesh, S. M. (2007) Inhibition of galectin-3 mediated cellular interactions by pectic polysaccharides from dietary sources. Glycoconj. J. 24, 497-507
39. Miller, M. C., Klyosov, A. A., and Mayo, K. H. (2012) Structural features for α-galactomannan binding to galectin-1. Glycobiology 22, 543-551
40. Miller, M. C., Ippel, H., Suylen, D., Klyosov, A. A., Traber, P. G., Hackeng, T., and Mayo, K. H. (2016) Binding of polysaccharides to human galectin-3 at a noncanonical site in its carbohydrate recognition domain. Glycobiology 26, 88-99
41. Sörme, P., Kahl-Knutsson, B., Huflejt, M., Nilsson, U. J., and Leffler, H. (2004) Fluorescence polarization as an analytical tool to evaluate galectinligand interactions. Anal. Biochem. 334, 36-47
42. Cumpstey, I., Carlsson, S., Leffler, H., and Nilsson, U. J. (2005) Synthesis of a phenyl thio-β-D-galactopyranoside library from 1,5-difluoro-2,4-dinitrobenzene: discovery of efficient and selective monosaccharide inhibitors of galectin-7. Org. Biomol. Chem. 3, 1922-1932
43. Salomonsson, E., Carlsson, M. C., Osla, V., Hendus-Altenburger, R., Kahl-Knutson, B., Oberg, C. T., Sundin, A., Nilsson, R., Nordberg-Karlsson, E., Nilsson, U. J., Karlsson, A., Rini, J. M., and Leffler, H. (2010) Mutational tuning of galectin-3 specificity and biological function. J. Biol. Chem. 285, 35079-35091
44. Mandal, S., Rajput, V. K., Sundin, A. P., Leffler, H., Mukhopadhyay, B., and Nilsson, U. J. (2016) Galactose-amidine derivatives as selective antagonists of galectin-9. Can. J. Chem. 10.1139/cjc-2015-0598
45. Li, S., Wandel, M. P., Li, F., Liu, Z., He, C., Wu, J., Shi, Y., and Randow, F. (2013) Sterical hindrance promotes selectivity of the autophagy cargo receptor NDP52 for the danger receptor galectin-8 in antibacterial autophagy. Sci. Signal. 6, ra9
46. Kim, B. W., Hong, S. B., Kim, J. H., Kwon do, H., and Song, H. K. (2013) Structural basis for recognition of autophagic receptor NDP52 by the sugar receptor galectin-8. Nat. Commun. 4, 1613
47. Nowak, T. P., Haywood, P. L., and Barondes, S. H. (1976) Developmentally regulated lectin in embryonic chick muscle and a myogenic cell line. Biochem. Biophys. Res. Commun. 68, 650-657
48. Lapierre, Y., Rigal, D., Adam, J., Josef, D., Meyer, F., Greber, S., and Drot, C. (1990) The gel test: a new way to detect red cell antigen-antibody reactions. Transfusion 30, 109-113
49. Springer, T. A. (1981) Monoclonal antibody analysis of complex biological systems. Combination of cell hybridization and immunoadsorbents in a novel cascade procedure and its application to the macrophage cell surface. J. Biol. Chem. 256, 3833-3839
50. Ho, M. K., and Springer, T. A. (1982) Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. J. Immunol. 128, 1221-1228
51. Salomonsson, E., Larumbe, A., Tejler, J., Tullberg, E., Rydberg, H., Sundin, A., Khabut, A., Frejd, T., Lobsanov, Y. D., Rini, J. M., Nilsson, U. J., and Leffler, H. (2010) Monovalent interactions of galectin-1. Biochemistry 49, 9518-9532
52. Lepur, A., Salomonsson, E., Nilsson, U. J., and Leffler, H. (2012) Ligand induced galectin-3 protein self-association. J. Biol. Chem. 287, 21751-21756
53. Butler, W. T. (1963) Hemagglutination studies with formalinized erythrocytes. Effect of bis-diazo-benzidine and tannic acid treatment on sensitization by soluble antigen. J. Immunol. 90, 663-671
54. John, C. M., Leffler, H., Kahl-Knutsson, B., Svensson, I., and Jarvis, G. A. (2003) Truncated galectin-3 inhibits tumor growth and metastasis in orthotopic nude mouse model of human breast cancer. Clin. Cancer Res. 9, 2374-2383
55. Mackinnon, A. C., Gibbons, M. A., Farnworth, S. L., Leffler, H., Nilsson, U. J., Delaine, T., Simpson, A. J., Forbes, S. J., Hirani, N., Gauldie, J., and Sethi, T. (2012) Regulation of transforming growth factor-β1-driven lung fibrosis by galectin-3. Am. J. Respir. Crit. Care Med. 185, 537-546
56. Hayashi, A., Gillen, A. C., and Lott, J. R. (2000) Effects of daily oral administration of quercetin chalcone and modified citrus pectin on implanted colon-25 tumor growth in Balb-c mice. Altern. Med. Rev. 5, 546-552
57. Paz, I., Sachse, M., Dupont, N., Mounier, J., Cederfur, C., Enninga, J., Leffler, H., Poirier, F., Prevost, M. C., Lafont, F., and Sansonetti, P. (2010) Galectin-3, a marker for vacuole lysis by invasive pathogens. Cell. Microbiol. 12, 530-544
58. Thurston, T. L., Wandel, M. P., von Muhlinen, N., Foeglein, A., and Randow, F. (2012) Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482, 414- 418
59. Aits, S., Kricker, J., Liu, B., Ellegaard, A. M., Hämälistö, S., Tvingsholm, S., Corcelle-Termeau, E., Høgh, S., Farkas, T., Holm Jonassen, A., Gromova, I., Mortensen, M., and Jäättelä, M. (2015) Sensitive detection of lysosomal membrane permeabilization by lysosomal galectin puncta assay. Autophagy 11, 1408-1424
60. Jadot, M., Colmant, C., Wattiaux-De Coninck, S., and Wattiaux, R. (1984) Intralysosomal hydrolysis of glycyl-L-phenylalanine 2-naphthylamide. Biochem. J. 219, 965-970
61. Berg, T. O., Strømhaug, E., Løvdal, T., Seglen, O., and Berg, T. (1994) Use of glycyl-L-phenylalanine 2-naphthylamide, a lysosome-disrupting cathepsin C substrate, to distinguish between lysosomes and prelysosomal endocytic vacuoles. Biochem. J. 300, 229-236
62. Nishi, N., Abe, A., Iwaki, J., Yoshida, H., Itoh, A., Shoji, H., Kamitori, S., Hirabayashi, J., and Nakamura, T. (2008) Functional and structural bases of a cysteine-less mutant as a long-lasting substitute for galectin-1. Glycobiology 18, 1065-1073
63. Stowell, S. R., Cho, M., Feasley, C. L., Arthur, C. M., Song, X., Colucci, J. K., Karmakar, S., Mehta, P., Dias-Baruffi, M., McEver, R. P., and Cummings, R. D. (2009) Ligand reduces galectin-1 sensitivity to oxidative inactivation by enhancing dimer formation. J. Biol. Chem. 284, 4989-4999
64. Thijssen, V. L., Postel, R., Brandwijk, R. J., Dings, R. P., Nesmelova, I., Satijn, S., Verhofstad, N., Nakabeppu, Y., Baum, L. G., Bakkers, J., Mayo, K. H., Poirier, F., and Griffioen, A. W. (2006) Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc. Natl. Acad. Sci. U.S.A. 103, 15975-15980
65. Salomonsson, E., Thijssen, V. L., Griffioen, A. W., Nilsson, U. J., and Leffler, H. (2011) The anti-angiogenic peptide anginex greatly enhances galectin-1 binding affinity for glycoproteins. J. Biol. Chem. 286, 13801-13804
66. Dings, R. P., Miller, M. C., Nesmelova, I., Astorgues-Xerri, L., Kumar, N., Serova, M., Chen, X., Raymond, E., Hoye, T. R., and Mayo, K. H. (2012) Antitumor agent calixarene 0118 targets human galectin-1 as an allosteric inhibitor of carbohydrate binding. J. Med. Chem. 55, 5121-5129
67. Dings, R. P., Kumar, N., Miller, M. C., Loren, M., Rangwala, H., Hoye, T. R., and Mayo, K. H. (2013) Structure-based optimization of angiostatic agent 6DBF7, an allosteric antagonist of galectin-1. J. Pharmacol. Exp. Ther. 344, 589-599
68. Bian, C. F., Zhang, Y., Sun, H., Li, D. F., and Wang, D. C. (2011) Structural basis for distinct binding properties of the human galectins to Thomsen-Friedenreich antigen. PLoS ONE 6, e25007
69. Sato, S., and Hughes, R. C. (1994) Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem. 269, 4424-4430
70. Dabelic, S., Novak, R., Goreta, S. S., and Dumic, J. (2012) Galectin-3 expression in response to LPS, immunomodulatory drugs and exogenously added galectin-3 in monocyte-like THP-1 cells. In Vitro Cell. Dev. Biol. Anim. 48, 518-527
71. Schneider, D., Greb, C., Koch, A., Straube, T., Elli, A., Delacour, D., and Jacob, R. (2010) Trafficking of galectin-3 through endosomal organelles of polarized and non-polarized cells. Eur. J. Cell Biol. 89, 788-798
72. Boscher, C., Dennis, J. W., and Nabi, I. R. (2011) Glycosylation, galectins and cellular signaling. Curr. Opin. Cell Biol. 23, 383-392
73. Li, L., Wan, T., Wan, M., Liu, B., Cheng, R., and Zhang, R. (2015) The effect of the size of fluorescent dextran on its endocytic pathway. Cell Biol. Int. 39, 531-539
74. Leclere, L., Fransolet, M., Cote, F., Cambier, P., Arnould, T., Van Cutsem, P., and Michiels, C. (2015) Heat-modified citrus pectin induces apoptosislike cell death and autophagy in HepG2 and A549 cancer cells. PLoS ONE 10, e0115831
75. Leclere, L., Fransolet, M., Cambier, P., El Bkassiny, S., Tikad, A., Dieu, M., Vincent, S. P., Van Cutsem, P., and Michiels, C. (2016) Identification of a cytotoxic molecule in heat-modified citrus pectin. Carbohydr. Polym. 137, 39-51
76. Bohne, A., Lang, E., and von der Lieth, C. W. (1999) SWEET-WWWbased rapid 3D construction of oligo- and polysaccharides. Bioinformatics 15, 767-768
77. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612