Molecular Oncology
Volume 4, Issue 2 , Pages 98-118 , April 2010

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

  • Ivan O. Potapenko

      Affiliations

    • Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway
    • Faculty of Medicine, Oslo University, Norway
  • ,
  • Vilde D. Haakensen

      Affiliations

    • Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway
    • Faculty of Medicine, Oslo University, Norway
  • ,
  • Torben Lüders

      Affiliations

    • Institute for Clinical Epidemiology and Molecular Biology (Epi-Gen), Faculty Division Akershus University Hospital, Faculty of Medicine, Oslo, Norway
  • ,
  • Åslaug Helland

      Affiliations

    • Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway
    • Department of Oncology, Oslo University Hospital Radiumhospitalet, Oslo, Norway
  • ,
  • Ida Bukholm

      Affiliations

    • Institute for Clinical Epidemiology and Molecular Biology (Epi-Gen), Faculty Division Akershus University Hospital, Faculty of Medicine, Oslo, Norway
    • Department of Surgery, Akershus University Hospital, Oslo, Norway
  • ,
  • Therese Sørlie

      Affiliations

    • Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway
    • Institute for Informatics, Faculty of Natural Sciences and Mathematics, University of Oslo, Norway
  • ,
  • Vessela N. Kristensen

      Affiliations

    • Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway
    • Institute for Clinical Epidemiology and Molecular Biology (Epi-Gen), Faculty Division Akershus University Hospital, Faculty of Medicine, Oslo, Norway
  • ,
  • Ole C. Lingjærde

      Affiliations

    • Institute for Informatics, Faculty of Natural Sciences and Mathematics, University of Oslo, Norway
  • ,
  • Anne-Lise Børresen-Dale

      Affiliations

    • Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway
    • Faculty of Medicine, Oslo University, Norway
    • Corresponding Author InformationCorresponding author at: Department of Genetics, Institute for Cancer Research, Oslo University Hospital Radiumhospitalet, 0310 Oslo, Norway. Tel.: +47 22 78 13 33.

Received 20 October 2009 ,Revised 2 December 2009 ,Accepted 2 December 2009.

References 

  1. Ang LC, Zhang Y, Cao L, Yang BL, Young B, Kiani C, et al. Versican enhances locomotion of astrocytoma cells and reduces cell adhesion through its G1 domain. J. Neuropathol. Exp. Neurol. 1999;58:597–605
  2. Angulo J, Ojeda R, de Paz JL, Lucas R, Nieto PM, Lozano RM, et al. The activation of fibroblast growth factors (FGFs) by glycosaminoglycans: influence of the sulfation pattern on the biological activity of FGF-1. Chembiochem. 2004;5:55–61
  3. Barthel SR, Gavino JD, Descheny L, Dimitroff CJ. Targeting selectins and selectin ligands in inflammation and cancer. Expert. Opin. Ther. Targets. 2007;11:1473–1491
  4. Bennett EP, Hassan H, Hollingsworth MA, 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. 1999;460:226–230
  5. Bennett EP, Hassan H, Mandel U, Hollingsworth MA, Akisawa N, Ikematsu Y, et al. 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. 1999;274:25362–25370
  6. Bergelson LD. Gangliosides and antitumor immunity. Clin. Investig. 1993;71:590–594
  7. Berois N, Mazal D, Ubillos L, Trajtenberg F, Nicolas A, Sastre-Garau X, et al. UDP-N-acetyl-d-galactosamine: polypeptide N-acetylgalactosaminyltransferase-6 as a new immunohistochemical breast cancer marker. J. Histochem. Cytochem. 2006;54:317–328
  8. Bhaumik M, Harris T, Sundaram S, Johnson L, Guttenplan J, Rogler C, et al. 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. 1998;58:2881–2887
  9. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, et al Genes that mediate breast cancer metastasis to the brain. Nature. 2009;459:1005–1009
  10. Bosmann HB, Hall TC. Enzyme activity in invasive tumors of human breast and colon. Proc. Natl. Acad. Sci. U.S.A. 1974;71:1833–1837
  11. Braakhuis BJ, Tabor MP, Kummer JA, Leemans CR, Brakenhoff RH. A genetic explanation of slaughter's concept of field cancerization: evidence and clinical implications. Cancer Res. 2003;63:1727–1730
  12. Brinkman-Van der Linden EC, 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. 2000;275:8625–8632
  13. Brockhausen I. Pathways of O-glycan biosynthesis in cancer cells. Biochim. Biophys. Acta. 1999;1473:67–95
  14. Brockhausen I. Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep. 2006;7:599–604
  15. Bulow HE, Hobert O. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron. 2004;41:723–736
  16. Burchell J, Poulsom R, Hanby A, Whitehouse C, Cooper L, Clausen H, et al. An alpha2,3 sialyltransferase (ST3Gal I) is elevated in primary breast carcinomas. Glycobiology. 1999;9:1307–1311
  17. Carraway KL, Ramsauer VP, Haq B, Carothers Carraway CA. Cell signaling through membrane mucins. Bioessays. 2003;25:66–71
  18. Cebo C, Dambrouck T, Maes E, Laden C, Strecker G, Michalski JC, et al. 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. 2001;276:5685–5691
  19. Chen Q, Johnson DM, Haudenschild DR, Goetinck PF. Progression and recapitulation of the chondrocyte differentiation program: cartilage matrix protein is a marker for cartilage maturation. Dev. Biol. 1995;172:293–306
  20. Cho SH, Sahin A, Hortobagyi GN, Hittelman WN, Dhingra K. Sialyl-Tn antigen expression occurs early during human mammary carcinogenesis and is associated with high nuclear grade and aneuploidy. Cancer Res. 1994;54:6302–6305
  21. Dalziel M, Whitehouse C, McFarlane I, Brockhausen I, Gschmeissner S, Schwientek T, et al. 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. 2001;276:11007–11015
  22. Deepa SS, Umehara Y, Higashiyama S, Itoh N, 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. 2002;277:43707–43716
  23. Dube DH, Bertozzi CR. Glycans in cancer and inflammation – potential for therapeutics and diagnostics. Nat. Rev. Drug Discov. 2005;4:477–488
  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 MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 1998;95:14863–14868
  26. Elola MT, Capurro MI, Barrio MM, Coombs PJ, Taylor ME, Drickamer K, et al. 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. 2007;101:161–174
  27. Eshchenko TY, Rykova VI, Chernakov AE, Sidorov SV, Grigorieva EV. Expression of different proteoglycans in human breast tumors. Biochemistry (Mosc.). 2007;72:1016–1020
  28. Fukushi Y, Hakomori S, Nudelman E, 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. 1984;259:4681–4685
  29. Fukushi Y, Nudelman E, Levery SB, Hakomori S, Rauvala H. Novel fucolipids accumulating in human adenocarcinoma. III. A hybridoma antibody (FH6) defining a human cancer-associated difucoganglioside (VI3NeuAcV3III3Fuc2nLc6). J. Biol. Chem. 1984;259:10511–10517
  30. Fukushima K, Hirota M, Terasaki PI, Wakisaka A, Togashi H, Chia D, et al. Characterization of sialosylated Lewisx as a new tumor-associated antigen. Cancer Res. 1984;44:5279–5285
  31. Gandhi NS, Mancera RL. The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 2008;72:455–482
  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 BK, Thurmon LT, Marcus DM. Association of glycosphingolipids with intermediate filaments of mesenchymal, epithelial, glial, and muscle cells. Cell Motil. Cytoskeleton. 1992;21:255–271
  35. Goodarzi MT, Turner GA. Decreased branching, increased fucosylation and changed sialylation of alpha-1-proteinase inhibitor in breast and ovarian cancer. Clin. Chim. Acta. 1995;236:161–171
  36. Grose R, Dickson C. Fibroblast growth factor signaling in tumorigenesis. Cytokine Growth Factor Rev. 2005;16:179–186
  37. Gu J, Taniguchi N. Regulation of integrin functions by N-glycans. Glycoconj. J. 2004;21:9–15
  38. Gu J, Zhao Y, Isaji T, Shibukawa Y, Ihara H, Takahashi M, et al. 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. 2004;14:177–186
  39. Hakomori Si SI. Inaugural article: the glycosynapse. Proc. Natl. Acad. Sci. U.S.A. 2002;99:225–232
  40. Hakomori S, Zhang Y. Glycosphingolipid antigens and cancer therapy. Chem. Biol. 1997;4:97–104
  41. Hakomori SI, Murakami WT. Glycolipids of hamster fibroblasts and derived malignant-transformed cell lines. Proc. Natl. Acad. Sci. U.S.A. 1968;59:254–261
  42. Hayashi T, Takahashi T, Motoya S, Ishida T, Itoh F, Adachi M, et al. MUC1 mucin core protein binds to the domain 1 of ICAM-1. Digestion. 2001;63(Suppl. 1):87–92
  43. Hirose J, Kawashima H, Yoshie O, Tashiro K, Miyasaka M. Versican interacts with chemokines and modulates cellular responses. J. Biol. Chem. 2001;276:5228–5234
  44. Hollingsworth MA, Swanson BJ. Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer. 2004;4:45–60
  45. Iijima J, Zhao Y, Isaji T, Kameyama A, Nakaya S, Wang X, 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. 2006;281:13038–13046
  46. Iozzo RV. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 1998;67:609–652
  47. Iwaki J, Minamisawa T, Tateno H, Kominami J, Suzuki K, Nishi N, et al. Desulfated galactosaminoglycans are potential ligands for galectins: evidence from frontal affinity chromatography. Biochem. Biophys. Res. Commun. 2008;373:206–212
  48. Izumikawa T, Koike T, Shiozawa S, Sugahara K, Tamura J, 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. 2008;283:11396–11406
  49. Jepson S, Komatsu M, Haq B, Arango ME, Huang D, Carraway CA, et al. 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. 2002;21:7524–7532
  50. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat. Rev. Cancer. 2009;9:239–252
  51. Kakugawa Y, Wada T, Yamaguchi K, Yamanami H, Ouchi K, Sato I, et al. 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. 2002;99:10718–10723
  52. Kannagi R. Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj. J. 1997;14:577–584
  53. Kato T, Wang Y, Yamaguchi K, Milner CM, Shineha R, Satomi S, et al. Overexpression of lysosomal-type sialidase leads to suppression of metastasis associated with reversion of malignant phenotype in murine B16 melanoma cells. Int. J. Cancer. 2001;92:797–804
  54. Kawashima H, Atarashi K, Hirose M, Hirose J, Yamada S, Sugahara K, et al. Oversulfated chondroitin/dermatan sulfates containing GlcAbeta1/IdoAalpha1-3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. J. Biol. Chem. 2002;277:12921–12930
  55. Kawashima H, Hirose M, Hirose J, Nagakubo D, Plaas AH, Miyasaka M. Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. J. Biol. Chem. 2000;275:35448–35456
  56. KEGG Glycan Database. http://www.genome.jp/kegg/glycan/ (accessed 2008 Nov).
  57. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457:102–106
  58. Kim YJ, Borsig L, Han HL, Varki NM, Varki A. Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. Am. J. Pathol. 1999;155:461–472
  59. Kitagawa H, Izumikawa T, Uyama T, Sugahara K. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J. Biol. Chem. 2003;278:23666–23671
  60. Kitagawa H, Tsutsumi K, Tone Y, Sugahara K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem. 1997;272:31377–31381
  61. Kitagawa H, Uyama T, Sugahara K. Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 2001;276:38721–38726
  62. Kohlgraf KG, Gawron AJ, Higashi M, Meza JL, Burdick MD, Kitajima S, et al. Contribution of the MUC1 tandem repeat and cytoplasmic tail to invasive and metastatic properties of a pancreatic cancer cell line. Cancer Res. 2003;63:5011–5020
  63. Kusafuka K, Muramatsu K, Kasami M, Kuriki K, Hirobe K, Hayashi I, et al Cartilaginous features in matrix-producing carcinoma of the breast: four cases report with histochemical and immunohistochemical analysis of matrix molecules. Mod. Pathol. 2008;21:1282–1292
  64. Kusche-Gullberg M, Kjellen L. Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 2003;13:605–611
  65. Lagana A, Goetz JG, Cheung P, Raz A, Dennis JW, Nabi IR. Galectin binding to Mgat5-modified N-glycans regulates fibronectin matrix remodeling in tumor cells. Mol. Cell Biol. 2006;26:3181–3193
  66. Lau KS, Dennis JW. N-Glycans in cancer progression. Glycobiology. 2008;18:750–760
  67. Leygue E, Snell L, Dotzlaw H, Troup S, Hiller-Hitchcock T, Murphy LC, et al. Lumican and decorin are differentially expressed in human breast carcinoma. J. Pathol. 2000;192:313–320
  68. Liu FT, Rabinovich GA. Galectins as modulators of tumour progression. Nat. Rev. Cancer. 2005;5:29–41
  69. Loridon-Rosa B, Vielh P, Matsuura H, Clausen H, Cuadrado C, Burtin P. Distribution of oncofetal fibronectin in human mammary tumors: immunofluorescence study on histological sections. Cancer Res. 1990;50:1608–1612
  70. Matsuura N, Narita T, Hiraiwa N, Hiraiwa M, Murai H, Iwase T, et al. Gene expression of fucosyl- and sialyl-transferases which synthesize sialyl Lewisx, the carbohydrate ligands for E-selectin, in human breast cancer. Int. J. Oncol. 1998;12:1157–1164
  71. Mitsuzuka K, Handa K, Satoh M, Arai Y, 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. 2005;280:35545–35553
  72. Miura Y, Kainuma M, Jiang H, Velasco H, Vogt PK, Hakomori S. Reversion of the Jun-induced oncogenic phenotype by enhanced synthesis of sialosyllactosylceramide (GM3 ganglioside). Proc. Natl. Acad. Sci. U.S.A. 2004;101:16204–16209
  73. Miyagi T, Hata K, Konno K, Tsuiki S. Multiple forms of mammalian sialidase: altered expression in carcinogenesis. Tohoku J. Exp. Med. 1992;168:223–229
  74. Miyagi T, Konno K, Sagawa J, Tsuiki S. Neoplastic alteration of a membrane-associated sialidase of rat liver. Jpn. J. Cancer Res. 1990;81:915–919
  75. Miyagi T, Sato K, Hata K, Taniguchi S. Metastatic potential of transformed rat 3Y1 cell lines is inversely correlated with lysosomal-type sialidase activity. FEBS Lett. 1994;349:255–259
  76. Miyagi T, Wada T, Yamaguchi K, Hata K. Sialidase and malignancy: a minireview. Glycoconj. J. 2004;20:189–198
  77. Miyoshi E, Moriwaki K, Nakagawa T. Biological function of fucosylation in cancer biology. J. Biochem. 2008;143:725–729
  78. Mora PT, Brady RO, Bradley RM, McFarland VW. Gangliosides in DNA virus-transformed and spontaneously transformed tumorigenic mouse cell lines. Proc. Natl. Acad. Sci. U.S.A. 1969;63:1290–1296
  79. Nagase T, Ishikawa K, Suyama M, Kikuno R, Hirosawa M, Miyajima N, et al. 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. 1999;6:63–70
  80. Nath D, Hartnell A, Happerfield L, Miles DW, Burchell J, Taylor-Papadimitriou J, et al. Macrophage–tumour cell interactions: identification of MUC1 on breast cancer cells as a potential counter-receptor for the macrophage-restricted receptor, sialoadhesin. Immunology. 1999;98:213–219
  81. Nikitovic D, Katonis P, Tsatsakis A, Karamanos NK, Tzanakakis GN. Lumican, a small leucine-rich proteoglycan. IUBMB Life. 2008;60:818–823
  82. Pacheco B, Maccarana M, Goodlett DR, Malmstrom A, Malmstrom L. Identification of the active site of DS-epimerase 1 and requirement of N-glycosylation for enzyme function. J. Biol. Chem. 2009;284:1741–1747
  83. Partridge EA, Le RC, Di Guglielmo GM, Pawling J, Cheung P, Granovsky M, et al. Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science. 2004;306:120–124
  84. Pochec E, Litynska A, Amoresano A, Casbarra A. Glycosylation profile of integrin alpha 3 beta 1 changes with melanoma progression. Biochim. Biophys. Acta. 2003;1643:113–123
  85. Poola I, Abraham J, Marshalleck JJ, Yue Q, Lokeshwar VB, Bonney G, et al. Molecular risk assessment for breast cancer development in patients with ductal hyperplasias. Clin. Cancer Res. 2008;14:1274–1280
  86. Ricciardelli C, Rodgers RJ. Extracellular matrix of ovarian tumors. Semin. Reprod. Med. 2006;24:270–282
  87. Rothlein R, Dustin ML, Marlin SD, Springer TA. A human intercellular adhesion molecule (ICAM-1) distinct from LFA-1. J. Immunol. 1986;137:1270–1274
  88. Sawada M, Moriya S, Saito S, Shineha R, Satomi S, Yamori T, et al. Reduced sialidase expression in highly metastatic variants of mouse colon adenocarcinoma 26 and retardation of their metastatic ability by sialidase overexpression. Int. J. Cancer. 2002;97:180–185
  89. Schengrund CL, Lausch RN, Rosenberg A. Sialidase activity in transformed cells. J. Biol. Chem. 1973;248:4424–4428
  90. Shekhar MP, Werdell J, Santner SJ, Pauley RJ, Tait L. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: implications for tumor development and progression. Cancer Res. 2001;61:1320–1326
  91. Singh PK, Hollingsworth MA. Cell surface-associated mucins in signal transduction. Trends Cell Biol. 2006;16:467–476
  92. Slaughter DP, Southwick HW, Smejkal W. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer. 1953;6:963–968
  93. Soejima M, Koda Y. Molecular mechanisms of Lewis antigen expression. Leg. Med. (Tokyo). 2005;7:266–269
  94. Stern R. Hyaluronidases in cancer biology. Semin. Cancer Biol. 2008;18:275–280
  95. Sturm A, Lensch M, Andre S, Kaltner H, Wiedenmann B, Rosewicz S, et al. Human galectin-2: novel inducer of T cell apoptosis with distinct profile of caspase activation. J. Immunol. 2004;173:3825–3837
  96. Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 2003;13:612–620
  97. Tarp MA, Clausen H. Mucin-type O-glycosylation and its potential use in drug and vaccine development. Biochim. Biophys. Acta. 2008;1780:546–563
  98. Ten Hagen KG, Fritz TA, Tabak LA. All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology. 2003;13:1R–16R
  99. Thiery JP. Epithelial–mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 2003;15:740–746
  100. Tillack TW, Allietta M, Moran RE, Young WW. Localization of globoside and Forssman glycolipids on erythrocyte membranes. Biochim. Biophys. Acta. 1983;733:15–24
  101. Todeschini AR, Hakomori SI. Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim. Biophys. Acta. 2008;1780:421–433
  102. Tokuyama S, Moriya S, Taniguchi S, Yasui A, Miyazaki J, Orikasa S, et al. Suppression of pulmonary metastasis in murine B16 melanoma cells by transfection of a sialidase cDNA. Int. J. Cancer. 1997;73:410–415
  103. Tozeren A, Kleinman HK, Grant DS, Morales D, Mercurio AM, Byers SW. E-selectin-mediated dynamic interactions of breast- and colon-cancer cells with endothelial–cell monolayers. Int. J. Cancer. 1995;60:426–431
  104. Troup S, Njue C, Kliewer EV, Parisien M, Roskelley C, Chakravarti S, et al. 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. 2003;9:207–214
  105. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 2001;98:5116–5121
  106. Usuki S, Hoops P, Sweeley CC. Growth control of human foreskin fibroblasts and inhibition of extracellular sialidase activity by 2-deoxy-2,3-dehydro-N-acetylneuraminic acid. J. Biol. Chem. 1988;263:10595–10599
  107. Varki A, Angata T. Siglecs – the major subfamily of I-type lectins. Glycobiology. 2006;16:1R–27R
  108. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, et al. Essentials of Glycobiology. second ed.. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press; 2009;
  109. Wada J, Ota K, Kumar A, Wallner EI, Kanwar YS. Developmental regulation, expression, and apoptotic potential of galectin-9, a beta-galactoside binding lectin. J. Clin. Invest. 1997;99:2452–2461
  110. Wang X, Inoue S, Gu J, Miyoshi E, Noda K, Li W, 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. 2005;102:15791–15796
  111. Wight TN, Merrilees MJ. Proteoglycans in atherosclerosis and restenosis: key roles for versican. Circ. Res. 2004;94:1158–1167
  112. Yada T, Gotoh M, Sato T, Shionyu M, Go M, Kaseyama H, 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. 2003;278:30235–30247
  113. Yamagata M, Suzuki S, Akiyama SK, Yamada KM, Kimata K. Regulation of cell–substrate adhesion by proteoglycans immobilized on extracellular substrates. J. Biol. Chem. 1989;264:8012–8018
  114. Yamagata M, Yamada KM, Yoneda M, Suzuki S, Kimata K. Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin. J. Biol. Chem. 1986;261:13526–13535
  115. Yamaguchi Y. Lecticans: organizers of the brain extracellular matrix. Cell. Mol. Life Sci. 2000;57:276–289
  116. Yamashita K, Ohkura T, Tachibana Y, Takasaki S, Kobata A. Comparative study of the oligosaccharides released from baby hamster kidney cells and their polyoma transformant by hydrazinolysis. J. Biol. Chem. 1984;259:10834–10840
  117. Yang RY, Hsu DK, Yu L, Ni J, Liu FT. Cell cycle regulation by galectin-12, a new member of the galectin superfamily. J. Biol. Chem. 2001;276:20252–20260
  118. Yang RY, Rabinovich GA, Liu FT. Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 2008;10:e17
  119. Yee AJ, Akens M, Yang BL, Finkelstein J, Zheng PS, Deng Z, et al. The effect of versican G3 domain on local breast cancer invasiveness and bony metastasis. Breast Cancer Res. 2007;9:R47
  120. Yoshimura M, Ihara Y, Matsuzawa Y, Taniguchi N. Aberrant glycosylation of E-cadherin enhances cell–cell binding to suppress metastasis. J. Biol. Chem. 1996;271:13811–13815
  121. Zhao Y, Nakagawa T, Itoh S, Inamori K, Isaji T, Kariya Y, et al N-Acetylglucosaminyltransferase III antagonizes the effect of N-acetylglucosaminyltransferase V on alpha3beta1 integrin-mediated cell migration. J. Biol. Chem. 2006;281:32122–32130
  122. Zhao Y, Sato Y, Isaji T, Fukuda T, Matsumoto A, Miyoshi E, et al. Branched N-glycans regulate the biological functions of integrins and cadherins. FEBS J. 2008;275:1939–1948
  123. Zheng M, Fang H, 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. 1994;269:12325–12331
  124. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 2005;6:1245–1252
  125. Zimmermann DR, Ruoslahti E. Multiple domains of the large fibroblast proteoglycan, versican. EMBO J. 1989;8:2975–2981

PII: S1574-7891(09)00155-0

doi: 10.1016/j.molonc.2009.12.001

Molecular Oncology
Volume 4, Issue 2 , Pages 98-118 , April 2010