Glycan gene expression signatures in normal and malignant breast tissue; possible role in diagnosis and progression

Molecular Oncology

Volumn 4, Issue 2, 2010, Pages 98-118

  Potapenko, Ivan O ^a,b   Haakensen, Vilde D ^a,b   Lüders, Torben ^c   Helland, Åslaug ^a   Bukholm, Ida ^c   Sørlie, Therese ^a,d   Kristensen, Vessela N ^a,c   Lingjærde, Ole C ^d   Børresen Dale, Anne Lise ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c AKERSHUS UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

Breast cancer; Expression profiling; Glycosaminoglycans; Glycosphingolipids; Glycosylation; N O linked glycans

Indexed keywords

CHONDROITIN; GLYCAN DERIVATIVE; GLYCOSAMINOGLYCAN; GROWTH FACTOR; GROWTH FACTOR RECEPTOR; HEPARIN; HYALURONIC ACID; KERATAN SULFATE; MESSENGER RNA;

BREAST CANCER; BREAST CARCINOGENESIS; CANCER DIAGNOSIS; CANCER GROWTH; CELL ADHESION; CELL MOTILITY; GENE EXPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; REVIEW;

EID: 77949272116     PISSN: 15747891     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molonc.2009.12.001     Document Type: Review

References (125)

1. Ang L.C., Zhang Y., Cao L., Yang B.L., Young B., Kiani C., Lee V., Allan K., and Yang B.B. Versican enhances locomotion of astrocytoma cells and reduces cell adhesion through its G1 domain. J. Neuropathol. Exp. Neurol. 58 (1999) 597-605
2. Angulo J., Ojeda R., de Paz J.L., Lucas R., Nieto P.M., Lozano R.M., Redondo-Horcajo M., Gimenez-Gallego G., and Martin-Lomas M. The activation of fibroblast growth factors (FGFs) by glycosaminoglycans: influence of the sulfation pattern on the biological activity of FGF-1. Chembiochem 5 (2004) 55-61
3. Barthel S.R., Gavino J.D., Descheny L., and Dimitroff C.J. Targeting selectins and selectin ligands in inflammation and cancer. Expert. Opin. Ther. Targets 11 (2007) 1473-1491
4. Bennett E.P., Hassan H., Hollingsworth M.A., and Clausen H. A novel human UDP-N-acetyl-d-galactosamine:polypeptide N-acetylgalactosaminyltransferase, GalNAc-T7, with specificity for partial GalNAc-glycosylated acceptor substrates. FEBS Lett. 460 (1999) 226-230
5. Bennett E.P., Hassan H., Mandel U., Hollingsworth M.A., Akisawa N., Ikematsu Y., Merkx G., van Kessel A.G., Olofsson S., and Clausen H. Cloning and characterization of a close homologue of human UDP-N-acetyl-alpha-d-galactosamine:polypeptide N-acetylgalactosaminyltransferase-T3, designated GalNAc-T6. Evidence for genetic but not functional redundancy. J. Biol. Chem. 274 (1999) 25362-25370
6. Bergelson L.D. Gangliosides and antitumor immunity. Clin. Investig. 71 (1993) 590-594
7. Berois N., Mazal D., Ubillos L., Trajtenberg F., Nicolas A., Sastre-Garau X., Magdelenat H., and Osinaga E. UDP-N-acetyl-d-galactosamine: polypeptide N-acetylgalactosaminyltransferase-6 as a new immunohistochemical breast cancer marker. J. Histochem. Cytochem. 54 (2006) 317-328
8. Bhaumik M., Harris T., Sundaram S., Johnson L., Guttenplan J., Rogler C., and Stanley P. Progression of hepatic neoplasms is severely retarded in mice lacking the bisecting N-acetylglucosamine on N-glycans: evidence for a glycoprotein factor that facilitates hepatic tumor progression. Cancer Res. 58 (1998) 2881-2887
9. Bos P.D., Zhang X.H., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., van de Vijver M.J., Gerald W.L., Foekens J.A., et al. Genes that mediate breast cancer metastasis to the brain. Nature 459 (2009) 1005-1009
10. Bosmann H.B., and Hall T.C. Enzyme activity in invasive tumors of human breast and colon. Proc. Natl. Acad. Sci. U.S.A. 71 (1974) 1833-1837
11. Braakhuis B.J., Tabor M.P., Kummer J.A., Leemans C.R., and Brakenhoff R.H. A genetic explanation of slaughter's concept of field cancerization: evidence and clinical implications. Cancer Res. 63 (2003) 1727-1730
12. Brinkman-Van der Linden E.C., and Varki A. New aspects of siglec binding specificities, including the significance of fucosylation and of the sialyl-Tn epitope. Sialic acid-binding immunoglobulin superfamily lectins. J. Biol. Chem. 275 (2000) 8625-8632
13. Brockhausen I. Pathways of O-glycan biosynthesis in cancer cells. Biochim. Biophys. Acta 1473 (1999) 67-95
14. Brockhausen I. Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep. 7 (2006) 599-604
15. Bulow H.E., and Hobert O. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron 41 (2004) 723-736
16. Burchell J., Poulsom R., Hanby A., Whitehouse C., Cooper L., Clausen H., Miles D., and Taylor-Papadimitriou J. An alpha2,3 sialyltransferase (ST3Gal I) is elevated in primary breast carcinomas. Glycobiology 9 (1999) 1307-1311
17. Carraway K.L., Ramsauer V.P., Haq B., and Carothers Carraway C.A. Cell signaling through membrane mucins. Bioessays 25 (2003) 66-71
18. Cebo C., Dambrouck T., Maes E., Laden C., Strecker G., Michalski J.C., and Zanetta J.P. Recombinant human interleukins IL-1alpha, IL-1beta, IL-4, IL-6, and IL-7 show different and specific calcium-independent carbohydrate-binding properties. J. Biol. Chem. 276 (2001) 5685-5691
19. Chen Q., Johnson D.M., Haudenschild D.R., and Goetinck P.F. Progression and recapitulation of the chondrocyte differentiation program: cartilage matrix protein is a marker for cartilage maturation. Dev. Biol. 172 (1995) 293-306
20. Cho S.H., Sahin A., Hortobagyi G.N., Hittelman W.N., and Dhingra K. Sialyl-Tn antigen expression occurs early during human mammary carcinogenesis and is associated with high nuclear grade and aneuploidy. Cancer Res. 54 (1994) 6302-6305
21. Dalziel M., Whitehouse C., McFarlane I., Brockhausen I., Gschmeissner S., Schwientek T., Clausen H., Burchell J.M., and Taylor-Papadimitriou J. The relative activities of the C2GnT1 and ST3Gal-I glycosyltransferases determine O-glycan structure and expression of a tumor-associated epitope on MUC1. J. Biol. Chem. 276 (2001) 11007-11015
22. Deepa S.S., Umehara Y., Higashiyama S., Itoh N., and Sugahara K. Specific molecular interactions of oversulfated chondroitin sulfate E with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J. Biol. Chem. 277 (2002) 43707-43716
23. Dube D.H., and Bertozzi C.R. Glycans in cancer and inflammation - potential for therapeutics and diagnostics. Nat. Rev. Drug Discov. 4 (2005) 477-488
24. Dublin M. Sweet Time for Informatics. Genome Technology. Available from URL: (2008). http://cdnwww.genomeweb.com/sweet-time-informatics (accessed 2009 Jan)
25. Eisen M.B., Spellman P.T., Brown P.O., and Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 14863-14868
26. Elola M.T., Capurro M.I., Barrio M.M., Coombs P.J., Taylor M.E., Drickamer K., and Mordoh J. Lewis x antigen mediates adhesion of human breast carcinoma cells to activated endothelium. Possible involvement of the endothelial scavenger receptor C-type lectin. Breast Cancer Res. Treat. 101 (2007) 161-174
27. Eshchenko T.Y., Rykova V.I., Chernakov A.E., Sidorov S.V., and Grigorieva E.V. Expression of different proteoglycans in human breast tumors. Biochemistry (Mosc.) 72 (2007) 1016-1020
28. Fukushi Y., Hakomori S., Nudelman E., and Cochran N. Novel fucolipids accumulating in human adenocarcinoma. II. Selective isolation of hybridoma antibodies that differentially recognize mono-, di-, and trifucosylated type 2 chain. J. Biol. Chem. 259 (1984) 4681-4685
29. Fukushi Y., Nudelman E., Levery S.B., Hakomori S., and Rauvala H. Novel fucolipids accumulating in human adenocarcinoma. III. A hybridoma antibody (FH6) defining a human cancer-associated difucoganglioside (VI3NeuAcV3III3Fuc2nLc6). J. Biol. Chem. 259 (1984) 10511-10517
30. Fukushima K., Hirota M., Terasaki P.I., Wakisaka A., Togashi H., Chia D., Suyama N., Fukushi Y., Nudelman E., and Hakomori S. Characterization of sialosylated Lewisx as a new tumor-associated antigen. Cancer Res. 44 (1984) 5279-5285
31. Gandhi N.S., and Mancera R.L. The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 72 (2008) 455-482
32. Gene Ontology AmiGO. http://amigo.geneontology.org/cgi-bin/amigo/search.cgi (accessed 2008 Nov).
33. GGDB Glycan Gene Database. http://riodb.ibase.aist.go.jp/rcmg/ggdb/ (accessed 2008 Aug).
34. Gillard B.K., Thurmon L.T., and Marcus D.M. Association of glycosphingolipids with intermediate filaments of mesenchymal, epithelial, glial, and muscle cells. Cell Motil. Cytoskeleton 21 (1992) 255-271
35. Goodarzi M.T., and Turner G.A. Decreased branching, increased fucosylation and changed sialylation of alpha-1-proteinase inhibitor in breast and ovarian cancer. Clin. Chim. Acta 236 (1995) 161-171
36. Grose R., and Dickson C. Fibroblast growth factor signaling in tumorigenesis. Cytokine Growth Factor Rev. 16 (2005) 179-186
37. Gu J., and Taniguchi N. Regulation of integrin functions by N-glycans. Glycoconj. J. 21 (2004) 9-15
38. Gu J., Zhao Y., Isaji T., Shibukawa Y., Ihara H., Takahashi M., Ikeda Y., Miyoshi E., Honke K., and Taniguchi N. Beta1,4-N-acetylglucosaminyltransferase III down-regulates neurite outgrowth induced by costimulation of epidermal growth factor and integrins through the Ras/ERK signaling pathway in PC12 cells. Glycobiology 14 (2004) 177-186
39. Hakomori Si S.I. Inaugural article: the glycosynapse. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 225-232
40. Hakomori S., and Zhang Y. Glycosphingolipid antigens and cancer therapy. Chem. Biol. 4 (1997) 97-104
41. Hakomori S.I., and Murakami W.T. Glycolipids of hamster fibroblasts and derived malignant-transformed cell lines. Proc. Natl. Acad. Sci. U.S.A. 59 (1968) 254-261
42. Hayashi T., Takahashi T., Motoya S., Ishida T., Itoh F., Adachi M., Hinoda Y., and Imai K. MUC1 mucin core protein binds to the domain 1 of ICAM-1. Digestion 63 Suppl. 1 (2001) 87-92
43. Hirose J., Kawashima H., Yoshie O., Tashiro K., and Miyasaka M. Versican interacts with chemokines and modulates cellular responses. J. Biol. Chem. 276 (2001) 5228-5234
44. Hollingsworth M.A., and Swanson B.J. Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 4 (2004) 45-60
45. Iijima J., Zhao Y., Isaji T., Kameyama A., Nakaya S., Wang X., Ihara H., Cheng X., Nakagawa T., Miyoshi E., et al. Cell-cell interaction-dependent regulation of N-acetylglucosaminyltransferase III and the bisected N-glycans in GE11 epithelial cells. Involvement of E-cadherin-mediated cell adhesion. J. Biol. Chem. 281 (2006) 13038-13046
46. Iozzo R.V. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67 (1998) 609-652
47. Iwaki J., Minamisawa T., Tateno H., Kominami J., Suzuki K., Nishi N., Nakamura T., and Hirabayashi J. Desulfated galactosaminoglycans are potential ligands for galectins: evidence from frontal affinity chromatography. Biochem. Biophys. Res. Commun. 373 (2008) 206-212
48. Izumikawa T., Koike T., Shiozawa S., Sugahara K., Tamura J., and Kitagawa H. Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization: chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members. J. Biol. Chem. 283 (2008) 11396-11406
49. Jepson S., Komatsu M., Haq B., Arango M.E., Huang D., Carraway C.A., and Carraway K.L. Muc4/sialomucin complex, the intramembrane ErbB2 ligand, induces specific phosphorylation of ErbB2 and enhances expression of p27(kip), but does not activate mitogen-activated kinase or protein kinaseB/Akt pathways. Oncogene 21 (2002) 7524-7532
50. Joyce J.A., and Pollard J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9 (2009) 239-252
51. Kakugawa Y., Wada T., Yamaguchi K., Yamanami H., Ouchi K., Sato I., and Miyagi T. Up-regulation of plasma membrane-associated ganglioside sialidase (Neu3) in human colon cancer and its involvement in apoptosis suppression. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 10718-10723
52. Kannagi R. Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj. J. 14 (1997) 577-584
53. Kato T., Wang Y., Yamaguchi K., Milner C.M., Shineha R., Satomi S., and Miyagi T. Overexpression of lysosomal-type sialidase leads to suppression of metastasis associated with reversion of malignant phenotype in murine B16 melanoma cells. Int. J. Cancer 92 (2001) 797-804
54. Kawashima H., Atarashi K., Hirose M., Hirose J., Yamada S., Sugahara K., and Miyasaka M. Oversulfated chondroitin/dermatan sulfates containing GlcAbeta1/IdoAalpha1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J. Biol. Chem. 277 (2002) 12921-12930
55. Kawashima H., Hirose M., Hirose J., Nagakubo D., Plaas A.H., and Miyasaka M. Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. J. Biol. Chem. 275 (2000) 35448-35456
56. KEGG Glycan Database. http://www.genome.jp/kegg/glycan/ (accessed 2008 Nov).
57. Kim S., Takahashi H., Lin W.W., Descargues P., Grivennikov S., Kim Y., Luo J.L., and Karin M. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457 (2009) 102-106
58. Kim Y.J., Borsig L., Han H.L., Varki N.M., and Varki A. Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. Am. J. Pathol. 155 (1999) 461-472
59. Kitagawa H., Izumikawa T., Uyama T., and Sugahara K. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J. Biol. Chem. 278 (2003) 23666-23671
60. Kitagawa H., Tsutsumi K., Tone Y., and Sugahara K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 272 (1997) 31377-31381
61. Kitagawa H., Uyama T., and Sugahara K. Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276 (2001) 38721-38726
62. Kohlgraf K.G., Gawron A.J., Higashi M., Meza J.L., Burdick M.D., Kitajima S., Kelly D.L., Caffrey T.C., and Hollingsworth M.A. Contribution of the MUC1 tandem repeat and cytoplasmic tail to invasive and metastatic properties of a pancreatic cancer cell line. Cancer Res. 63 (2003) 5011-5020
63. Kusafuka K., Muramatsu K., Kasami M., Kuriki K., Hirobe K., Hayashi I., Watanabe H., Hiraki Y., Shukunami C., Mochizuki T., et al. Cartilaginous features in matrix-producing carcinoma of the breast: four cases report with histochemical and immunohistochemical analysis of matrix molecules. Mod. Pathol. 21 (2008) 1282-1292
64. Kusche-Gullberg M., and Kjellen L. Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13 (2003) 605-611
65. Lagana A., Goetz J.G., Cheung P., Raz A., Dennis J.W., and Nabi I.R. Galectin binding to Mgat5-modified N-glycans regulates fibronectin matrix remodeling in tumor cells. Mol. Cell Biol. 26 (2006) 3181-3193
66. Lau K.S., and Dennis J.W. N-Glycans in cancer progression. Glycobiology 18 (2008) 750-760
67. Leygue E., Snell L., Dotzlaw H., Troup S., Hiller-Hitchcock T., Murphy L.C., Roughley P.J., and Watson P.H. Lumican and decorin are differentially expressed in human breast carcinoma. J. Pathol. 192 (2000) 313-320
68. Liu F.T., and Rabinovich G.A. Galectins as modulators of tumour progression. Nat. Rev. Cancer 5 (2005) 29-41
69. Loridon-Rosa B., Vielh P., Matsuura H., Clausen H., Cuadrado C., and Burtin P. Distribution of oncofetal fibronectin in human mammary tumors: immunofluorescence study on histological sections. Cancer Res. 50 (1990) 1608-1612
70. Matsuura N., Narita T., Hiraiwa N., Hiraiwa M., Murai H., Iwase T., Funahashi H., Imai T., Takagi H., and Kannagi R. Gene expression of fucosyl- and sialyl-transferases which synthesize sialyl Lewisx, the carbohydrate ligands for E-selectin, in human breast cancer. Int. J. Oncol. 12 (1998) 1157-1164
71. Mitsuzuka K., Handa K., Satoh M., Arai Y., and Hakomori S. A specific microdomain ("glycosynapse 3") controls phenotypic conversion and reversion of bladder cancer cells through GM3-mediated interaction of alpha3beta1 integrin with CD9. J. Biol. Chem. 280 (2005) 35545-35553
72. Miura Y., Kainuma M., Jiang H., Velasco H., Vogt P.K., and Hakomori S. Reversion of the Jun-induced oncogenic phenotype by enhanced synthesis of sialosyllactosylceramide (GM3 ganglioside). Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 16204-16209
73. Miyagi T., Hata K., Konno K., and Tsuiki S. Multiple forms of mammalian sialidase: altered expression in carcinogenesis. Tohoku J. Exp. Med. 168 (1992) 223-229
74. Miyagi T., Konno K., Sagawa J., and Tsuiki S. Neoplastic alteration of a membrane-associated sialidase of rat liver. Jpn. J. Cancer Res. 81 (1990) 915-919
75. Miyagi T., Sato K., Hata K., and Taniguchi S. Metastatic potential of transformed rat 3Y1 cell lines is inversely correlated with lysosomal-type sialidase activity. FEBS Lett. 349 (1994) 255-259
76. Miyagi T., Wada T., Yamaguchi K., and Hata K. Sialidase and malignancy: a minireview. Glycoconj. J. 20 (2004) 189-198
77. Miyoshi E., Moriwaki K., and Nakagawa T. Biological function of fucosylation in cancer biology. J. Biochem. 143 (2008) 725-729
78. Mora P.T., Brady R.O., Bradley R.M., and McFarland V.W. Gangliosides in DNA virus-transformed and spontaneously transformed tumorigenic mouse cell lines. Proc. Natl. Acad. Sci. U.S.A. 63 (1969) 1290-1296
79. Nagase T., Ishikawa K., Suyama M., Kikuno R., Hirosawa M., Miyajima N., Tanaka A., Kotani H., Nomura N., and Ohara O. Prediction of the coding sequences of unidentified human genes. XIII. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 6 (1999) 63-70
80. Nath D., Hartnell A., Happerfield L., Miles D.W., Burchell J., Taylor-Papadimitriou J., and Crocker P.R. Macrophage-tumour cell interactions: identification of MUC1 on breast cancer cells as a potential counter-receptor for the macrophage-restricted receptor, sialoadhesin. Immunology 98 (1999) 213-219
81. Nikitovic D., Katonis P., Tsatsakis A., Karamanos N.K., and Tzanakakis G.N. Lumican, a small leucine-rich proteoglycan. IUBMB Life 60 (2008) 818-823
82. Pacheco B., Maccarana M., Goodlett D.R., Malmstrom A., and Malmstrom L. Identification of the active site of DS-epimerase 1 and requirement of N-glycosylation for enzyme function. J. Biol. Chem. 284 (2009) 1741-1747
83. Partridge E.A., Le R.C., Di Guglielmo G.M., Pawling J., Cheung P., Granovsky M., Nabi I.R., Wrana J.L., and Dennis J.W. Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306 (2004) 120-124
84. Pochec E., Litynska A., Amoresano A., and Casbarra A. Glycosylation profile of integrin alpha 3 beta 1 changes with melanoma progression. Biochim. Biophys. Acta 1643 (2003) 113-123
85. Poola I., Abraham J., Marshalleck J.J., Yue Q., Lokeshwar V.B., Bonney G., and Dewitty R.L. Molecular risk assessment for breast cancer development in patients with ductal hyperplasias. Clin. Cancer Res. 14 (2008) 1274-1280
86. Ricciardelli C., and Rodgers R.J. Extracellular matrix of ovarian tumors. Semin. Reprod. Med. 24 (2006) 270-282
87. Rothlein R., Dustin M.L., Marlin S.D., and Springer T.A. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J. Immunol. 137 (1986) 1270-1274
88. Sawada M., Moriya S., Saito S., Shineha R., Satomi S., Yamori T., Tsuruo T., Kannagi R., and Miyagi T. Reduced sialidase expression in highly metastatic variants of mouse colon adenocarcinoma 26 and retardation of their metastatic ability by sialidase overexpression. Int. J. Cancer 97 (2002) 180-185
89. Schengrund C.L., Lausch R.N., and Rosenberg A. Sialidase activity in transformed cells. J. Biol. Chem. 248 (1973) 4424-4428
90. Shekhar M.P., Werdell J., Santner S.J., Pauley R.J., and Tait L. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: implications for tumor development and progression. Cancer Res. 61 (2001) 1320-1326
91. Singh P.K., and Hollingsworth M.A. Cell surface-associated mucins in signal transduction. Trends Cell Biol. 16 (2006) 467-476
92. Slaughter D.P., Southwick H.W., and Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 6 (1953) 963-968
93. Soejima M., and Koda Y. Molecular mechanisms of Lewis antigen expression. Leg. Med. (Tokyo) 7 (2005) 266-269
94. Stern R. Hyaluronidases in cancer biology. Semin. Cancer Biol. 18 (2008) 275-280
95. Sturm A., Lensch M., Andre S., Kaltner H., Wiedenmann B., Rosewicz S., Dignass A.U., and Gabius H.J. Human galectin-2: novel inducer of T cell apoptosis with distinct profile of caspase activation. J. Immunol. 173 (2004) 3825-3837
96. Sugahara K., Mikami T., Uyama T., Mizuguchi S., Nomura K., and Kitagawa H. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13 (2003) 612-620
97. Tarp M.A., and Clausen H. Mucin-type O-glycosylation and its potential use in drug and vaccine development. Biochim. Biophys. Acta 1780 (2008) 546-563
98. Ten Hagen K.G., Fritz T.A., and Tabak L.A. All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13 (2003) 1R-16R
99. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15 (2003) 740-746
100. Tillack T.W., Allietta M., Moran R.E., and Young Jr. W.W. Localization of globoside and Forssman glycolipids on erythrocyte membranes. Biochim. Biophys. Acta 733 (1983) 15-24
101. Todeschini A.R., and Hakomori S.I. Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim. Biophys. Acta 1780 (2008) 421-433
102. Tokuyama S., Moriya S., Taniguchi S., Yasui A., Miyazaki J., Orikasa S., and Miyagi T. Suppression of pulmonary metastasis in murine B16 melanoma cells by transfection of a sialidase cDNA. Int. J. Cancer 73 (1997) 410-415
103. Tozeren A., Kleinman H.K., Grant D.S., Morales D., Mercurio A.M., and Byers S.W. E-selectin-mediated dynamic interactions of breast- and colon-cancer cells with endothelial-cell monolayers. Int. J. Cancer 60 (1995) 426-431
104. Troup S., Njue C., Kliewer E.V., Parisien M., Roskelley C., Chakravarti S., Roughley P.J., Murphy L.C., and Watson P.H. Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer. Clin. Cancer Res. 9 (2003) 207-214
105. Tusher V.G., Tibshirani R., and Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 5116-5121
106. Usuki S., Hoops P., and Sweeley C.C. Growth control of human foreskin fibroblasts and inhibition of extracellular sialidase activity by 2-deoxy-2,3-dehydro-N-acetylneuraminic acid. J. Biol. Chem. 263 (1988) 10595-10599
107. Varki A., and Angata T. Siglecs - the major subfamily of I-type lectins. Glycobiology 16 (2006) 1R-27R
108. Varki A., Cummings R.D., Esko J.D., Freeze H.H., Stanley P., Bertozzi C.R., Hart G.W., and Etzler M.E. Essentials of Glycobiology. second ed. (2009), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
109. Wada J., Ota K., Kumar A., Wallner E.I., and Kanwar Y.S. Developmental regulation, expression, and apoptotic potential of galectin-9, a beta-galactoside binding lectin. J. Clin. Invest. 99 (1997) 2452-2461
110. Wang X., Inoue S., Gu J., Miyoshi E., Noda K., Li W., Mizuno-Horikawa Y., Nakano M., Asahi M., Takahashi M., et al. Dysregulation of TGF-beta1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 15791-15796
111. Wight T.N., and Merrilees M.J. Proteoglycans in atherosclerosis and restenosis: key roles for versican. Circ. Res. 94 (2004) 1158-1167
112. Yada T., Gotoh M., Sato T., Shionyu M., Go M., Kaseyama H., Iwasaki H., Kikuchi N., Kwon Y.D., Togayachi A., et al. Chondroitin sulfate synthase-2. Molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. J. Biol. Chem. 278 (2003) 30235-30247
113. Yamagata M., Suzuki S., Akiyama S.K., Yamada K.M., and Kimata K. Regulation of cell-substrate adhesion by proteoglycans immobilized on extracellular substrates. J. Biol. Chem. 264 (1989) 8012-8018
114. Yamagata M., Yamada K.M., Yoneda M., Suzuki S., and Kimata K. Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin. J. Biol. Chem. 261 (1986) 13526-13535
115. Yamaguchi Y. Lecticans: organizers of the brain extracellular matrix. Cell. Mol. Life Sci. 57 (2000) 276-289
116. Yamashita K., Ohkura T., Tachibana Y., Takasaki S., and Kobata A. Comparative study of the oligosaccharides released from baby hamster kidney cells and their polyoma transformant by hydrazinolysis. J. Biol. Chem. 259 (1984) 10834-10840
117. Yang R.Y., Hsu D.K., Yu L., Ni J., and Liu F.T. Cell cycle regulation by galectin-12, a new member of the galectin superfamily. J. Biol. Chem. 276 (2001) 20252-20260
118. Yang R.Y., Rabinovich G.A., and Liu F.T. Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 10 (2008) e17
119. Yee A.J., Akens M., Yang B.L., Finkelstein J., Zheng P.S., Deng Z., and Yang B. The effect of versican G3 domain on local breast cancer invasiveness and bony metastasis. Breast Cancer Res. 9 (2007) R47
120. Yoshimura M., Ihara Y., Matsuzawa Y., and Taniguchi N. Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J. Biol. Chem. 271 (1996) 13811-13815
121. Zhao Y., Nakagawa T., Itoh S., Inamori K., Isaji T., Kariya Y., Kondo A., Miyoshi E., Miyazaki K., Kawasaki N., et al. N-Acetylglucosaminyltransferase III antagonizes the effect of N-acetylglucosaminyltransferase V on alpha3beta1 integrin-mediated cell migration. J. Biol. Chem. 281 (2006) 32122-32130
122. Zhao Y., Sato Y., Isaji T., Fukuda T., Matsumoto A., Miyoshi E., Gu J., and Taniguchi N. Branched N-glycans regulate the biological functions of integrins and cadherins. FEBS J. 275 (2008) 1939-1948
123. Zheng M., Fang H., and Hakomori S. Functional role of N-glycosylation in alpha 5 beta 1 integrin receptor. De-N-glycosylation induces dissociation or altered association of alpha 5 and beta 1 subunits and concomitant loss of fibronectin binding activity. J. Biol. Chem. 269 (1994) 12325-12331
124. Zhu C., Anderson A.C., Schubart A., Xiong H., Imitola J., Khoury S.J., Zheng X.X., Strom T.B., and Kuchroo V.K. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6 (2005) 1245-1252
125. Zimmermann D.R., and Ruoslahti E. Multiple domains of the large fibroblast proteoglycan, versican. EMBO J. 8 (1989) 2975-2981