Skip to main content
SpringerLink
Log in

Tumor Progression through Interaction of Mucins with Lectins and Subsequent Signal Transduction

  • Chapter
  • First Online:
Glycosignals in Cancer

  • 298 Accesses

Abstract

Glycans bearing on cell surface glycoproteins are often altered in tumor cells. A variety of aberrant glycans, tumor-associated carbohydrate antigens, are typically expressed on mucins. Some lectins recognizing these antigens have been identified mainly on immune cells and play a role as inhibitory receptors.

Binding of soluble lectins and/or membrane-bound lectins (lectin receptors) to membrane-bound mucins such as MUC1 triggers signaling in tumor cells. On the other hand, membrane-bound and/or soluble mucins play a role as ligands for lectin receptors, initiating signal transduction in immune cells. These mucin-lectin networks contribute to both tumor progression and immune suppression. In this chapter, first, we mainly describe our current data on MUC1-mediated signaling through interactions with galectin-3 and Siglec-9, and then review lectin receptor-mediated signaling triggered by binding of mucins and its biological significance.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Adams OJ, Stanczak MA, von Gunten S et al (2018) Targeting sialic acid-Siglec interactions to reverse immune suppression in cancer. Glycobiology 28:640–647

    CAS  PubMed  Google Scholar 

  • Ahmad N, Gabius HJ, André S et al (2004) Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J Biol Chem 279:10841–10847

    Article  CAS  PubMed  Google Scholar 

  • Ahmad R, Raina D, Trivedi V et al (2007) MUC1 oncoprotein activates the IkappaB kinase beta complex and constitutive NF-kappaB signalling. Nat Cell Biol 9:1419–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akita K, Tanaka M, Tanida S et al (2013) CA125/MUC16 interacts with Src family kinases, and over-expression of its C-terminal fragment in human epithelial cancer cells reduces cell-cell adhesion. Eur J Cell Biol 92:257–263

    Article  CAS  PubMed  Google Scholar 

  • Akita K, Yoshida S, Ikehara Y et al (2012) Different levels of sialyl-Tn antigen expressed on MUC16 in patients with endometriosis and ovarian cancer. Int J Gynecol Cancer 22:531–538

    Article  PubMed  Google Scholar 

  • Angata T (2018) Possible influences of endogenous and exogenous ligands on the evolution of human Siglecs. Front Immunol 9:2885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angata T, Varki A (2000) Cloning, characterization, and phylogenetic analysis of siglec-9, a new member of the CD33-related group of siglecs. Evidence for co-evolution with sialic acid synthesis pathways. J Biol Chem 275:22127–22135

    Article  CAS  PubMed  Google Scholar 

  • Apostolopoulos V, Stojanovska L, Gargosky SE (2015) MUC1 (CD227): a multi-tasked molecule. Cell Mol Life Sci 72:4475–4500

    Article  CAS  PubMed  Google Scholar 

  • Artigas G, Monteiro JT, Hinou H et al (2017) Glycopeptides as targets for dendritic cells: exploring MUC1 glycopeptides binding profile toward macrophage galactose-type lectin (MGL) orthologs. J Med Chem 60:9012–9021

    Article  CAS  PubMed  Google Scholar 

  • Bafna S, Kaur S, Batra SK (2010) Membrane-bound mucins: the mechanistic basis for alterations in the growth and survival of cancer cells. Oncogene 29:2893–2904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bast RC Jr, Xu FJ, Yu YH et al (1998) CA 125: the past and the future. Int J Biol Marker 13:179–187

    Article  CAS  Google Scholar 

  • Beatson R, Maurstad G, Picco G et al (2015) The breast cancer-associated glycoforms of MUC1, MUC1-Tn and sialyl-Tn, are expressed in COSMC wild-type cells and bind the C-type lectin MGL. PLoS One 10:e0125994

    Article  PubMed  PubMed Central  Google Scholar 

  • Beatson R, Tajadura-Ortega V, Achkova D et al (2016) The mucin MUC1 modulates the tumor immunological microenvironment through engagement of the lectin Siglec-9. Nat Immunol 17:1273–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker JW, Erickson HP, Hoffman S et al (1989) Topology of cell adhesion molecules. Proc Natl Acad Sci U S A 86:1088–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belisle JA, Horibata S, Jennifer GAA et al (2010) Identification of Siglec-9 as the receptor for MUC16 on human NK cells, B cells, and monocytes. Mol Cancer 9:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Bennett EP, Mandel U, Clausen H et al (2012) Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22:736–756

    Article  CAS  PubMed  Google Scholar 

  • Bian CF, Zhang Y, Sun H et al (2011) Structural basis for distinct binding properties of the human galectins to Thomsen-Friedenreich antigen. PLoS One 6:e25007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bitler BG, Goverdhan A, Schroeder JA (2010) MUC1 regulates nuclear localization and function of the epidermal growth factor receptor. J Cell Sci 123:1716–1723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blume SW, Snyder RC, Ray R et al (1991) Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J Clin Invest 88:1613–1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruney L, Conley KC, Moss NM et al (2014) Membrane-type I matrix metalloproteinase-dependent ectodomain shedding of mucin16/CA-125 on ovarian cancer cells modulates adhesion and invasion of peritoneal mesothelium. Biol Chem 395:1221–1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Büll C, Boltje TJ, Balneger N et al (2018) Sialic acid blockade suppresses tumor growth by enhancing T-cell-mediated tumor immunity. Cancer Res 78:3574–3588

    Article  PubMed  Google Scholar 

  • Cascio S, Zhang L, Finn OJ et al (2011) MUC1 protein expression in tumor cells regulates transcription of proinflammatory cytokines by forming a complex with nuclear factor-κB p65 and binding to cytokine promoters: importance of extracellular domain. J Biol Chem 286:42248–42256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cazet A, Julien S, Bobowski M et al (2010) Tumour-associated carbohydrate antigens in breast cancer. Breast Cancer Res 12:204

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaturvedi P, Singh AP, Chakraborty S et al (2008) MUC4 mucin interacts with and stabilizes the HER2 oncoprotein in human pancreatic cancer cells. Cancer Res 68:2065–2070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chauhan D, Li G, Podar K et al (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

    Article  CAS  PubMed  Google Scholar 

  • Chaux P, Favre N, Martin M et al (1997) Tumor-infiltrating dendritic cells are defective in their antigen-presenting function and inducible B7 expression in rats. Int J Cancer 72:619–624

    Article  CAS  PubMed  Google Scholar 

  • Chen SH, Dallas MR, Balzer EM et al (2012) Mucin 16 is a functional selectin ligand on pancreatic cancer cells. FASEB J 26:1349–1359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chugh S, Gnanapragassam VS, Jain M et al (2015) Pathobiological implications of mucin glycans in cancer: sweet poison and novel targets. Biochim Biophys Acta 1856:211–225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cicek M, Fukuyama R, Cicek MS et al (2009) BRMS1 contributes to the negative regulation of uPA gene expression through recruitment of HDAC1 to the NF-kappaB binding site of the uPA promoter. Clin Exp Metastasis 26:229–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper DN, Barondes SH (1999) God must love galectins; he made so many of them. Glycobiology 9:979–984

    Article  CAS  PubMed  Google Scholar 

  • Cornelissen LAM, Blanas A, Zaal A et al (2020) Tn antigen expression contributes to an immune suppressive microenvironment and drives tumor growth in colorectal cancer. Front Oncol 10:1622

    Article  PubMed  PubMed Central  Google Scholar 

  • Cubas R, Li M, Chen C et al (2009) Trop2: a possible therapeutic target for late stage epithelial carcinomas. Biochim Biophys Acta 1796:309–314

    CAS  PubMed  Google Scholar 

  • da Costa V, van Vliet SJ, Carasi P et al (2021) The Tn antigen promotes lung tumor growth by fostering immunosuppression and angiogenesis via interaction with macrophage galactose-type lectin 2 (MGL2). Cancer Lett 518:72–81

    Article  PubMed  Google Scholar 

  • Dahr W, Uhlenbruck G, Bird GW (1974) Cryptic A-like receptor sites in human erythrocyte glycoproteins: proposed nature of Tn-antigen. Vox Sang 27:29–42

    Article  CAS  PubMed  Google Scholar 

  • Dam TK, Gabius HJ, André S et al (2005) Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry 44:12564–12571

    Article  CAS  PubMed  Google Scholar 

  • Danø K, Behrendt N, Høyer-Hansen G et al (2005) Plasminogen activation and cancer. Thromb Haemost 93:676–681

    Article  PubMed  Google Scholar 

  • Das S, Rachagani S, Torres-Gonzalez MP et al (2015) Carboxyl-terminal domain of MUC16 imparts tumorigenic and metastatic functions through nuclear translocation of JAK2 to pancreatic cancer cells. Oncotarget 6:5772–5787

    Article  PubMed  PubMed Central  Google Scholar 

  • Delacour D, Cramm-Behrens CI, Drobecq H et al (2006) Requirement for galectin-3 in apical protein sorting. Curr Biol 16:408–414

    Article  CAS  PubMed  Google Scholar 

  • Ding D, Yao Y, Zhang S et al (2017) C-type lectins facilitate tumor metastasis. Oncol Lett 13:13–21

    Article  CAS  PubMed  Google Scholar 

  • Duraisamy S, Ramasamy S, Kharbanda S et al (2006) Distinct evolution of the human carcinoma-associated transmembrane mucins, MUC1, MUC4 AND MUC16. Gene 373:28–34

    Article  CAS  PubMed  Google Scholar 

  • Dusoswa SA, Verhoeff J, Abels E et al (2020) Glioblastomas exploit truncated O - linked glycans for local and distant immune modulation via the macrophage galactose-type lectin. Proc Natl Acad Sci U S A 117:3693–3703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elad-Sfadia G, Haklai R, Balan E et al (2004) Galectin-3 augments K-Ras activation and triggers a Ras signal that attenuates ERK but not phosphoinositide 3-kinase activity. J Biol Chem 279:34922–34930

    Article  CAS  PubMed  Google Scholar 

  • Freitas D, Campos D, Gomes J et al (2019) O-glycans truncation modulates gastric cancer cell signaling and transcription leading to a more aggressive phenotype. EBioMedicine 40:349–362

    Article  PubMed  PubMed Central  Google Scholar 

  • Fritsch K, Mernberger M, Nist A et al (2016) Galectin-3 interacts with components of the nuclear ribonucleoprotein complex. BMC Cancer 16:502

    Article  PubMed  PubMed Central  Google Scholar 

  • Funes M, Miller JK, Lai C et al (2006) The mucin Muc4 potentiates neuregulin signaling by increasing the cell-surface populations of ErbB2 and ErbB3. J Biol Chem 281:19310–19319

    Article  CAS  PubMed  Google Scholar 

  • Gabrilovich DI, Corak J, Ciernik IF et al (1997) Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin Cancer Res 3:483–490

    CAS  PubMed  Google Scholar 

  • Gao X, Balan V, Tai G et al (2014) Galectin-3 induces cell migration via a calcium-sensitive MAPK/ERK1/2 pathway. Oncotarget 5:2077–2084

    Article  PubMed  PubMed Central  Google Scholar 

  • García-Vallejo JJ, Ilarregui JM, Kalay H et al (2014) CNS myelin induces regulatory functions of DC-SIGN-expressing, antigen-presenting cells via cognate interaction with MOG. J Exp Med 211:1465–1483

    Article  PubMed  PubMed Central  Google Scholar 

  • Geijtenbeek TB, Torensma R, van Vliet SJ et al (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100:575–585

    Article  CAS  PubMed  Google Scholar 

  • Geijtenbeek TBH, van Vliet SJ, Engering A et al (2004) Self- and nonself-recognition by C-type lectins on dendritic cells. Annu Rev Immunol 22:33–54

    Article  CAS  PubMed  Google Scholar 

  • Gendler SJ, Spicer AP (1995) Epithelial mucin genes. Annu Rev Physiol 57:607–634

    Article  CAS  PubMed  Google Scholar 

  • Gendler SJ (2001) MUC1, the renaissance molecule. J Mammary Gland Biol Neoplasia 6:339–353

    Article  CAS  PubMed  Google Scholar 

  • Gendler S, Taylor-Papadimitriou J, Duhig T et al (1988) A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J Biol Chem 263:12820–12823

    Article  CAS  PubMed  Google Scholar 

  • Gill DJ, Chia J, Senewiratne J et al (2010) Regulation of O-glycosylation through Golgi-to-ER relocation of initiation enzymes. J Cell Biol 189:843–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill DJ, Clausen H, Bard F (2011) Location, location, location: new insights into O-GalNAc protein glycosylation. Trends Cell Biol 21:149–158

    Article  CAS  PubMed  Google Scholar 

  • Gringhuis SI, den Dunnen J, Litjens M et al (2007) C-type lectin DC-SIGN modulates toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26:605–616

    Article  CAS  PubMed  Google Scholar 

  • Gringhuis SI, den Dunnen J, Litjens M et al (2009) Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to mycobacterium tuberculosis, HIV-1 and helicobacter pylori. Nat Immunol 10:1081–1088

    Article  CAS  PubMed  Google Scholar 

  • Gringhuis SI, Kaptein TM, Wevers BA et al (2014a) Fucose-specific DC-SIGN signalling directs T helper cell type-2 responses via IKKε- and CYLD-dependent Bcl3 activation. Nat Commun 5:3898

    Article  CAS  PubMed  Google Scholar 

  • Gringhuis SI, Kaptein TM, Wevers BA et al (2014b) Fucose-based PAMPs prime dendritic cells for follicular T helper cell polarization via DC-SIGN-dependent IL-27 production. Nat Commun 5:5074

    Article  CAS  PubMed  Google Scholar 

  • Haas Q, Boligan KF, Jandus C et al (2019) Siglec-9 regulates an effector memory CD8 + T-cell subset that congregates in the melanoma tumor microenvironment. Cancer Immunol Res 7:707–718

    Article  CAS  PubMed  Google Scholar 

  • Hanson RL, Hollingsworth MA (2016) Functional consequences of differential O-glycosylation of MUC1, MUC4, and MUC16 (downstream effects on signaling). Biomol Ther 6:34

    Google Scholar 

  • Haridas D, Ponnusamy MP, Chugh S et al (2014) MUC16: molecular analysis and its functional implications in benign and malignant conditions. FASEB J 28:4183–4199

    Article  CAS  PubMed  Google Scholar 

  • Hattrup CL, Gendler SJ (2008) Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol 70:431–457

    Article  CAS  PubMed  Google Scholar 

  • Hawiger D, Inaba K, Dorsett Y et al (2001) Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 194:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132:344–362

    Article  CAS  PubMed  Google Scholar 

  • Higashi N, Fujioka K, Denda-Nagai K et al (2002) The macrophage C-type lectin specific for galactose/N-acetylgalactosamine is an endocytic receptor expressed on monocyte-derived immature dendritic cells. J Biol Chem 277:20686–20693

    Article  CAS  PubMed  Google Scholar 

  • Hirabayashi J, Hashidate T, Arata Y et al (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim Biophys Acta 1572:232–254

    Article  CAS  PubMed  Google Scholar 

  • Hofmann BT, Schlüter L, Lange P et al (2015) COSMC knockdown mediated aberrant O-glycosylation promotes oncogenic properties in pancreatic cancer. Mol Cancer 14:109

    Article  PubMed  PubMed Central  Google Scholar 

  • Holbro T, Hynes NE (2004) ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 44:195–217

    Article  CAS  PubMed  Google Scholar 

  • Hollingsworth MA, Swanson BJ (2004) Mucins in cancer: protection and control of the cell surface. Nat Rev Cancer 4:45–60

    Article  CAS  PubMed  Google Scholar 

  • Ho MK, Springer TA (1982) Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. Immunol 128:1221–1228

    Article  CAS  Google Scholar 

  • Hönig E, Ringer K, Dewes J et al (2018) Galectin-3 modulates the polarized surface delivery of β1-integrin in epithelial cells. J Cell Sci 131:jcs213199

    Article  PubMed  Google Scholar 

  • Hönig E, Schneider K, Jacob R (2015) Recycling of galectin-3 in epithelial cells. Eur J Cell Biol 94:309–315

    Article  PubMed  Google Scholar 

  • Huang L, Chen D, Liu D et al (2005) MUC1 oncoprotein blocks glycogen synthase kinase 3beta-mediated phosphorylation and degradation of beta-catenin. Cancer Res 65:10413–10422

    Article  CAS  PubMed  Google Scholar 

  • Irigoyen JP, Muñoz-Cánoves P, Montero L et al (1999) The plasminogen activator system: biology and regulation. Cell Mol Life Sci 56:104–132

    Article  CAS  PubMed  Google Scholar 

  • Iurisci I, Tinari N, Natoli C et al (2000) Concentrations of galectin-3 in the sera of normal controls and cancer patients. Clin Cancer Res 6:1389–1393

    CAS  PubMed  Google Scholar 

  • Iwai T, Inaba N, Naundorf A (2002) Molecular cloning and characterization of a novel UDP-GlcNAc:GalNAc-peptide beta1,3-N-acetylglucosaminyltransferase (beta 3Gn-T6), an enzyme synthesizing the core 3 structure of O-glycans. J Biol Chem 277:12802–12809

    Article  CAS  PubMed  Google Scholar 

  • Jandus C, Boligan KF, Chijioke O et al (2014) Interactions between Siglec-7/9 receptors and ligands influence NK cell-dependent tumor immunosurveillance. J Clin Invest 124:1810–1820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelman JA (2009) Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 9:550–562

    Article  CAS  PubMed  Google Scholar 

  • Jégouzo SAF, Quintero-Martínez A, Ouyang X et al (2013) Organization of the extracellular portion of the macrophage galactose receptor: a trimeric cluster of simple binding sites for N-acetylgalactosamine. Glycobiology 23:853–864

    Article  PubMed  PubMed Central  Google Scholar 

  • Julien S, Videira PA, Delannoy P (2012) Sialyl-tn in cancer: (how) did we miss the target? Biomol Ther 2:435–466

    CAS  Google Scholar 

  • Ju T, Brewer K, D’Souza A et al (2002) Cloning and expression of human core 1 beta1,3-galactosyltransferase. J Biol Chem 277:178–186

    Article  CAS  PubMed  Google Scholar 

  • Ju T, Cummings RD (2002) A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase. Proc Natl Acad Sci U S A 99:16613–16618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ju T, Lanneau GS, Gautam T et al (2008) Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res 68:1636–1646

    Article  CAS  PubMed  Google Scholar 

  • Karanikas V, Hwang LA, Pearson J et al (1997) Antibody and T cell responses of patients with adenocarcinoma immunized with mannan-MUC1 fusion protein. J Clin Invest 100:2783–2792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kharband A, Rajabi H, Jin C et al (2014) Targeting the oncogenic MUC1-C protein inhibits mutant EGFR-mediated signaling and survival in non-small cell lung cancer cells. Clin Cancer Res 20:5423–5434

    Article  Google Scholar 

  • Komatsu M, Carraway CA, Fregien NL et al (1997) Reversible disruption of cell-matrix and cell-cell interactions by overexpression of sialomucin complex. J Biol Chem 272:33245–33254

    Article  CAS  PubMed  Google Scholar 

  • Kominsky SL, Argani P, Korz D et al (2003) Loss of the tight junction protein claudin-7 correlates with histological grade in both ductal carcinoma in situ and invasive ductal carcinoma of the breast. Oncogene 22:2021–2033

    Article  CAS  PubMed  Google Scholar 

  • Kozloski GA, Carraway CAC, Carraway KL (2010) Mechanistic and signaling analysis of Muc4-ErbB2 signaling module: new insights into the mechanism of ligand-independent ErbB2 activity. J Cell Physiol 224:649–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kudelka MR, Ju T, Heimburg-Molinaro J et al (2015) Simple sugars to complex disease—mucin-type O-glycans in cancer. Adv Cancer Res 126:53–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kufe D, Inghirami G, Abe M et al (1984) Differential reactivity of a novel monoclonal antibody (DF3) with human malignant versus benign breast tumors. Hybridoma 3:223–332

    Article  CAS  PubMed  Google Scholar 

  • Kufe DW (2009) Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 9:874–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kufe DW (2013) MUC1-C oncoprotein as a target in breast cancer: activation of signaling pathways and therapeutic approaches. Oncogene 32:1073–1081

    Article  CAS  PubMed  Google Scholar 

  • Kwon DS, Gregorio G, Bitton N et al (2002) DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16:135–144

    Article  CAS  PubMed  Google Scholar 

  • Lakshmanan I, Seshacharyulu P, Haridas D et al (2015) Novel HER3/MUC4 oncogenic signaling aggravates the tumorigenic phenotypes of pancreatic cancer cells. Oncotarget 6:21085–21099

    Article  PubMed  PubMed Central  Google Scholar 

  • Lakshmanan I, Ponnusamy MP, Das S et al (2012) MUC16 induced rapid G2/M transition via interactions with JAK2 for increased proliferation and anti-apoptosis in breast cancer cells. Oncogene 31:805–817

    Article  CAS  PubMed  Google Scholar 

  • Läubli H, Pearce OMT, Schwarz F et al (2014) Engagement of myelomonocytic Siglecs by tumor-associated ligands modulates the innate immune response to cancer. Proc Natl Acad Sci U S A 111:14211–14216

    Article  PubMed  PubMed Central  Google Scholar 

  • Lei Z, Maeda T, Tamura A et al (2012) EpCAM contributes to formation of functional tight junction in the intestinal epithelium by recruiting claudin proteins. Dev Biol 371:136–145

    Article  CAS  PubMed  Google Scholar 

  • Leng Y, Cao C, Ren J (2007) Nuclear import of the MUC1-C oncoprotein is mediated by nucleoporin Nup62. J Biol Chem 282:19321–19330

    Article  CAS  PubMed  Google Scholar 

  • Levitin F, Stern O, Weiss M et al (2005) The MUC1 SEA module is a self-cleaving domain. J Biol Chem 280:33374–33386

    Article  CAS  PubMed  Google Scholar 

  • Li D, Romain G, Flamar AL (2012) Targeting self- and foreign antigens to dendritic cells via DC-ASGPR generates IL-10-producing suppressive CD4+ T cells. J Exp Med 209:109–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lillehoj EP, Kim H, Chun EY et al (2004) Pseudomonas aeruginosa stimulates phosphorylation of the airway epithelial membrane glycoprotein Muc1 and activates MAP kinase. Am J Physiol Lung Cell Mol Physiol 287:L809–L815

    Article  CAS  PubMed  Google Scholar 

  • Lin JC, Wu YY, Wu JY et al (2012) TROP2 is epigenetically inactivated and modulates IGF-1R signalling in lung adenocarcinoma. EMBO Mol Med 4:472–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipinski M, Parks DR, Rouse RV et al (1981) Human trophoblast cell-surface antigens defined by monoclonal antibodies. Proc Natl Acad Sci U S A 78:5147–5150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu FT, Patterson RJ, Wang JL (2002) Intracellular functions of galectins. Biochim Biophys Acta 1572:263–273

    Article  CAS  PubMed  Google Scholar 

  • Liu FT, Rabinovich GA (2005) Galectins as modulators of tumour progression. Nat Rev Cancer 5:29–41

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Liu D, Chen D et al (2003) Human DF3/MUC1 carcinoma-associated protein functions as an oncogene. Oncogene 22:6107–6110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ren J, Yu W et al (2001) The epidermal growth factor receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and beta-catenin. J Biol Chem 276:35239–35242

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Gu J (2015) Significance of β-galactoside α2,6 sialyltranferase 1 in cancers. Molecules 20:7509–7527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Z, Ding L, Hong H et al (2011) Claudin-7 inhibits human lung cancer cell migration and invasion through ERK/MAPK signaling pathway. Exp Cell Res 317:1935–1946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macao B, Johansson DGA, Hansson GC et al (2006) Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 13:71–76

    Article  CAS  PubMed  Google Scholar 

  • Macauley MS, Crocker PR, Paulson JC (2014) Siglec-mediated regulation of immune cell function in disease. Nat Rev Immunol 14:653–666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maeda T, Inoue M, Koshiba S et al (2004) Solution structure of the SEA domain from the murine homologue of ovarian cancer antigen CA125 (MUC16). Int J Biol Marker 13:179–187

    Google Scholar 

  • Mantovani A, Marchesi F, Malesci A et al (2017) Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol 14:399–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Masri AA, Gendler SJ (2005) Muc1 affects c-Src signaling in PyV MT-induced mammary tumorigenesis. Oncogene 24:5799–5808

    Article  PubMed  Google Scholar 

  • Mitchell DA, Fadden AJ, Drickamer K (2001) A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. J Biol Chem 276:28939–28945

    Article  CAS  PubMed  Google Scholar 

  • Moniaux N, Escande F, Porchet N et al (2001) Structural organization and classification of the human mucin genes. Front Biosci 6:D1192–D1206

    Article  CAS  PubMed  Google Scholar 

  • Monti P, Leone BE, Zerbi A et al (2004) Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10highIL-12low regulatory dendritic cell. J Immunol 172:7341–7349

    Article  CAS  PubMed  Google Scholar 

  • Mori Y, Akita K, Yashiro M et al (2015) Binding of galectin-3, a β-galactoside-binding lectin, to MUC1 protein enhances phosphorylation of extracellular signal-regulated kinase 1/2 (ERK1/2) and Akt, promoting tumor cell malignancy. J Biol Chem 290:26125–26140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori Y, Akita K, Tanida S et al (2014) MUC1 protein induces urokinase-type plasminogen activator (uPA) by forming a complex with NF-κB p65 transcription factor and binding to the uPA promoter, leading to enhanced invasiveness of cancer cells. J Biol Chem 289:35193–35204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori Y, Akita K, Ojima K et al (2019) Trophoblast cell surface antigen 2 (Trop-2) phosphorylation by protein kinase C α/δ (PKCα/δ) enhances cell motility. J Biol Chem 294:11513–11524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris S, Ahmad N, André S et al (2004) Quaternary solution structures of galectins-1, -3, and -7. Glycobiology 14:293–300

    Article  CAS  PubMed  Google Scholar 

  • Moustafa AEA, Alaoui-Jamali MA, Batist G et al (2002) Identification of genes associated with head and neck carcinogenesis by cDNA microarray comparison between matched primary normal epithelial and squamous carcinoma cells. Oncogene 21:2634–2640

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee P, Tinder TL, Basu GD et al (2005) MUC1 (CD227) interacts with lck tyrosine kinase in Jurkat lymphoma cells and normal T cells. J Leukoc Biol 77:90–99

    Article  CAS  PubMed  Google Scholar 

  • Munkley J (2016) The role of Sialyl-Tn in cancer. Int J Mol Sci 17:275

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagy P, Friedländer E, Tanner M et al (2005) Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 65:473–482

    Article  CAS  PubMed  Google Scholar 

  • Napoletano C, Zizzari IG, Rughetti A et al (2012) Targeting of macrophage galactose-type C-type lectin (MGL) induces DC signaling and activation. Eur J Immunol 42:936–945

    Article  CAS  PubMed  Google Scholar 

  • Nakatsukasa M, Kawasaki S, Yamasaki K et al (2010) Tumor-associated calcium signal transducer 2 is required for the proper subcellular localization of claudin 1 and 7: implications in the pathogenesis of gelatinous drop-like corneal dystrophy. Am J Pathol 177:1344–1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nath D, Hartnell A, Happerfield L et al (1999) Macrophage-tumour cell interactions: identification of MUC1 on breast cancer cells as a potential counter-receptor for the macrophage-restricted receptor, sialoadhesin. Immunology 98:213–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nath S, Mukherjee P (2014) MUC1: a multifaceted oncoprotein with a key role in cancer progression. Trends Mol Med 20:332–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nieminen J, Kuno A, Hirabayashi J et al (2007) Visualization of galectin-3 oligomerization on the surface of neutrophils and endothelial cells using fluorescence resonance energy transfer. J Biol Chem 282:1374–1383

    Article  CAS  PubMed  Google Scholar 

  • O’Brien TJ, Beard JB, Underwood LJ et al (2001) The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 22:348–366

    Article  PubMed  Google Scholar 

  • Ohta M, Ishida A, Toda M et al (2010) Immunomodulation of monocyte-derived dendritic cells through ligation of tumor-produced mucins to Siglec-9. Biochem Biophys Res Commun 402:663–669

    Article  CAS  PubMed  Google Scholar 

  • Orford K, Crockett C, Jensen JP et al (1997) Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J Biol Chem 272:24735–24738

    Article  CAS  PubMed  Google Scholar 

  • Ozaki K, Lee RT, Lee YC et al (1995) The differences in structural specificity for recognition and binding between asialoglycoprotein receptors of liver and macrophages. Glycoconj J 12:268–274

    Article  CAS  PubMed  Google Scholar 

  • Padler-Karavani V, Hurtado-Ziola N, Yung-Chi C et al (2014) Rapid evolution of binding specificities and expression patterns of inhibitory CD33-related Siglecs in primates. FASEB J 28:1280–12893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey P, Kharbanda S, Kufe D (1995) Association of the DF3/MUC1 breast cancer antigen with Grb2 and the Sos/Ras exchange protein. Cancer Res 55:4000–4003

    CAS  PubMed  Google Scholar 

  • Perdicchio M, Ilarregui JM, Verstege MI et al (2016a) Sialic acid-modified antigens impose tolerance via inhibition of T-cell proliferation and de novo induction of regulatory T cells. Proc Natl Acad Sci U S A 113:3329–3334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perdicchio M, Cornelissen LAM, Streng-Ouwehand I et al (2016b) Tumor sialylation impedes T cell mediated anti-tumor responses while promoting tumor associated-regulatory T cells. Oncotarget 7:8771–8782

    Article  PubMed  PubMed Central  Google Scholar 

  • Piyush T, Chacko AR, Sindrewicz P et al (2017) Interaction of galectin-3 with MUC1 on cell surface promotes EGFR dimerization and activation in human epithelial cancer cells. Cell Death Differ 24:1937–1947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponnusamy MP, Singh AP, Jain M et al (2008) MUC4 activates HER2 signalling and enhances the motility of human ovarian cancer cells. Br J Cancer 99:520–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pröpster JM, Yang F, Rabbani S et al (2016) Structural basis for sulfation-dependent self-glycan recognition by the human immune-inhibitory receptor Siglec-8. Proc Natl Acad Sci U S A 113:E4170–E4179

    Article  PubMed  PubMed Central  Google Scholar 

  • Qu CF, Li Y, Song YJ et al (2004) MUC1 expression in primary and metastatic pancreatic cancer cells for in vitro treatment by (213)Bi-C595 radioimmunoconjugate. Br J Cancer 91:2086–2093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahn JJ, Shen Q, Mah BK et al (2004) MUC1 initiates a calcium signal after ligation by intercellular adhesion molecule-1. J Biol Chem 279:29386–29390

    Article  CAS  PubMed  Google Scholar 

  • Raina D, Ahmad R, Rajabi H et al (2012) Targeting cysteine-mediated dimerization of the MUC1-C oncoprotein in human cancer cells. Int J Oncol 40:1643–1649

    CAS  PubMed  Google Scholar 

  • Ramasamy S, Duraisamy S, Barbashov S et al (2007) The MUC1 and galectin-3 oncoproteins function in a microRNA-dependent regulatory loop. Mol Cell 27:992–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao M, Atay SM, Shukla V et al (2016) Mithramycin depletes specificity protein 1 and activates p53 to mediate senescence and apoptosis of malignant pleural mesothelioma cells. Clin Cancer Res 22:1197–1210

    Article  CAS  PubMed  Google Scholar 

  • Rao TD, Tian H, Ma X et al (2015) Expression of the carboxy-terminal portion of MUC16/CA125 induces transformation and tumor invasion. PLoS One 10:e0126633

    Article  PubMed  PubMed Central  Google Scholar 

  • Ren J, Raina D, Wen C et al (2006) MUC1 oncoprotein functions in activation of fibroblast growth factor receptor signaling. Mol Cancer Res 4:873–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • RodrÍguez E, Schetters STT, van Kooyk Y (2018) The tumour glyco-code as a novel immune checkpoint for immunotherapy. Nat Rev Immunol 18:204–211

    Article  PubMed  Google Scholar 

  • Roy LD, Sahraei M, Subramani DB et al (2011) MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 30:1449–1459

    Article  CAS  PubMed  Google Scholar 

  • Ruvolo PP (2016) Galectin 3 as a guardian of the tumor microenvironment. Biochim Biophys Acta 1863:427–437

    Article  CAS  PubMed  Google Scholar 

  • Saeland E, van Vliet SJ, Bäckström M et al (2007) The C-type lectin MGL expressed by dendritic cells detects glycan changes on MUC1 in colon carcinoma. Cancer Immunol Immunother 56:1225–1236

    Article  CAS  PubMed  Google Scholar 

  • Sancho D, e Sousa CR (2012) Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 30:491–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato S, Hughes RC (1994) Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J Biol Chem 269:4424–4430

    Article  CAS  PubMed  Google Scholar 

  • Saussez S, Lorfevre F, Lequeux T et al (2008) The determination of the levels of circulating galectin-1 and -3 in HNSCC patients could be used to monitor tumor progression and/or responses to therapy. Oral Oncol 44:86–93

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JA, Masri AA, Adriance MC et al (2004) MUC1 overexpression results in mammary gland tumorigenesis and prolonged alveolar differentiation. Oncogene 23:5739–5747

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JA, Thompson MC, Gardner MM et al (2001) Transgenic MUC1 interacts with epidermal growth factor receptor and correlates with mitogen-activated protein kinase activation in the mouse mammary gland. J Biol Chem 276:13057–13064

    Article  CAS  PubMed  Google Scholar 

  • Sciacchitano S, Lavra L, Morgante A et al (2018) Galectin-3: one molecule for an alphabet of diseases from A to Z. Int J Mol Sci 19:379

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimura T, Takenaka Y, Tsutsumi S (2004) Galectin-3, a novel binding partner of beta-catenin. Cancer Res 64:6363–6367

    Article  CAS  PubMed  Google Scholar 

  • Shukla SK, Purohit V, Mehla K et al (2017) MUC1 and HIF-1alpha signaling crosstalk induces anabolic glucose metabolism to impart gemcitabine resistance to pancreatic cancer. Cancer Cell 32:71–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siddiqui J, Abe M, Hayes D et al (1988) Isolation and sequencing of a cDNA coding for the human DF3 breast carcinoma-associated antigen. Proc Natl Acad Sci U S A 85:2320–2323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sidenius N, Blasi F (2003) The urokinase plasminogen activator system in cancer: recent advances and implication for prognosis and therapy. Cancer Metastasis Rev 22:205–222

    Article  CAS  PubMed  Google Scholar 

  • Sindrewicz P, Lian LY, Yu LG (2016) Interaction of the oncofetal Thomsen-Friedenreich antigen with galectins in cancer progression and metastasis. Front Oncol 6:79

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh PK, Wen Y, Swanson BJ et al (2007) Platelet-derived growth factor receptor beta-mediated phosphorylation of MUC1 enhances invasiveness in pancreatic adenocarcinoma cells. Cancer Res 67:5201–5210

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Hollingsworth MA (2006) Cell surface-associated mucins in signal transduction. Trends Cell Biol 16:467–476

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Behrens ME, Eggers JP et al (2008) Phosphorylation of MUC1 by Met modulates interaction with p53 and MMP1 expression. J Biol Chem 283:26985–26995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh SK, Streng-Ouwehand I, Litjens M et al (2009) Characterization of murine MGL1 and MGL2 C-type lectins: distinct glycan specificities and tumor binding properties. Mol Immunol 46:1240–1249

    Article  CAS  PubMed  Google Scholar 

  • Stanczak MA, Siddiqui SS, Trefny MP et al (2018) Self-associated molecular patterns mediate cancer immune evasion by engaging Siglecs on T cells. J Clin Invest 128:4912–4923

    Article  PubMed  PubMed Central  Google Scholar 

  • Streetly MJ, Maharaj L, Joel S et al (2010) GCS-100, a novel galectin-3 antagonist, modulates MCL-1, NOXA, and cell cycle to induce myeloma cell death. Blood 115:3939–3948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strous GJ, Dekker J (1992) Mucin-type glycoproteins. Crit Rev Biochem Mol Biol 27:57–92

    Article  CAS  PubMed  Google Scholar 

  • Sun Q, Ju T, Cummings RD (2011) The transmembrane domain of the molecular chaperone Cosmc directs its localization to the endoplasmic reticulum. J Biol Chem 286:11529–11542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swanson BJ, McDermott KM, Singh PK et al (2007) MUC1 is a counter-receptor for myelin-associated glycoprotein (Siglec-4a) and their interaction contributes to adhesion in pancreatic cancer perineural invasion. Cancer Res 67:10222–10229

    Article  CAS  PubMed  Google Scholar 

  • Swindall AF, Londoño-Joshi AI, Schultz MJ et al (2013) ST6Gal-I protein expression is upregulated in human epithelial tumors and correlates with stem cell markers in normal tissues and colon cancer cell lines. Cancer Res 73:2368–2378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takaoka M, Nakamura T, Ban Y et al (2007) Phenotypic investigation of cell junction-related proteins in gelatinous drop-like corneal dystrophy. Invest Ophthalmol Vis Sci 48:1095–1101

    Article  PubMed  Google Scholar 

  • Tanida S, Mori Y, Ishida A et al (2014) Galectin-3 binds to MUC1-N-terminal domain and triggers recruitment of β-catenin in MUC1-expressing mouse 3T3 cells. Biochim Biophys Acta 1840:1790–1797

    Article  CAS  PubMed  Google Scholar 

  • Tanida S, Akita K, Ishida A et al (2013) Binding of the sialic acid-binding lectin, Siglec-9, to the membrane mucin, MUC1, induces recruitment of β-catenin and subsequent cell growth. J Biol Chem 288:31842–31852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanos B, Rodriguez-Boulan E (2008) The epithelial polarity program: machineries involved and their hijacking by cancer. Oncogene 27:6939–6957

    Article  CAS  PubMed  Google Scholar 

  • Thériault C, Pinard M, Comamala M et al (2011) MUC16 (CA125) regulates epithelial ovarian cancer cell growth, tumorigenesis and metastasis. Gynecol Oncol 121:434–443

    Article  PubMed  Google Scholar 

  • Thomas DB, Winzler RJ (1969) Structural studies on human erythrocyte glycoproteins. Alkali-labile oligosaccharides. J Biol Chem 244:5943–5946

    Article  CAS  PubMed  Google Scholar 

  • Toda M, Hisano R, Yurugi H et al (2009) Ligation of tumour-produced mucins to CD22 dramatically impairs splenic marginal zone B-cells. Biochem J 417:673–683

    Article  CAS  PubMed  Google Scholar 

  • Trerotola M, Cantanelli P, Guerra E et al (2013a) Upregulation of Trop-2 quantitatively stimulates human cancer growth. Oncogene 32:222–233

    Article  CAS  PubMed  Google Scholar 

  • Trerotola M, Jernigan DL, Qin L et al (2013b) Trop-2 promotes prostate cancer metastasis by modulating β(1) integrin functions. Cancer Res 73:3155–3167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unger WWJ, van Beelen AJ, Bruijns SC et al (2012) Glycan-modified liposomes boost CD4+ and CD8+ T-cell responses by targeting DC-SIGN on dendritic cells. J Control Release 160:88–95

    Article  CAS  PubMed  Google Scholar 

  • Usami Y, Chiba H, Nakayama F et al (2006) Reduced expression of claudin-7 correlates with invasion and metastasis in squamous cell carcinoma of the esophagus. Hum Pathol 37:569–577

    Article  CAS  PubMed  Google Scholar 

  • van de Wall S, Santegoets KCM, van Houtum EJH et al (2020) Sialoglycans and Siglecs can shape the tumor immune microenvironment. Trends Immunol 41:274–285

    Article  PubMed  Google Scholar 

  • van Gisbergen KP, Aarnoudse CA, Meijer GA et al (2005) Dendritic cells recognize tumor-specific glycosylation of carcinoembryonic antigen on colorectal cancer cells through dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin. Cancer Res 65:5935–5944

    Article  PubMed  Google Scholar 

  • van Kooyk Y, Ilarregui JM, van Vliet SJ et al (2015) Novel insights into the immunomodulatory role of the dendritic cell and macrophage-expressed C-type lectin MGL. Immunobiology 220:185–192

    Article  PubMed  Google Scholar 

  • van Vliet SJ, Bay S, Vuist IM et al (2013) MGL signaling augments TLR2-mediated responses for enhanced IL-10 and TNF-α secretion. J Leukoc Biol 94:315–323

    Article  PubMed  Google Scholar 

  • van Vliet SJ, van Liempt E, Saeland E et al (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int Immunol 17:661–669

    Article  PubMed  Google Scholar 

  • van Vliet SJ, Saeland E, van Kooyk Y (2008) Sweet preferences of MGL: carbohydrate specificity and function. Trends Immunol 29:83–90

    Article  PubMed  Google Scholar 

  • van Vliet SJ, Gringhuis SI, Geijtenbeek TBH et al (2006) Regulation of effector T cells by antigen-presenting cells via interaction of the C-type lectin MGL with CD45. Nat Immunol 7:1200–1208

    Article  PubMed  Google Scholar 

  • Varki A, Angata T (2006) Siglecs—the major subfamily of I-type lectins. Glycobiology 16:1R–27R

    Article  CAS  PubMed  Google Scholar 

  • Vermeer PD, Einwalter LA, Moninger TO et al (2003) Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422:322–326

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Ryan D, Yiyu D et al (2008) Identification of Trop-2 as an oncogene and an attractive therapeutic target in colon cancers. Mol Cancer 7:280–285

    Article  CAS  Google Scholar 

  • Wei X, Hai X, Kufe D (2006) MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell 21:295–305

    Article  CAS  PubMed  Google Scholar 

  • Wesseling J, van der Valk SW, Hilkens J (1996) A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol Biol Cell 7:565–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Workman HC, Sweeney C, Carraway KL 3rd (2009) The membrane mucin Muc4 inhibits apoptosis induced by multiple insults via ErbB2-dependent and ErbB2-independent mechanisms. Cancer Res 69:2845–2852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao H, Woods EC, Vukojicic P et al (2016) Precision glycocalyx editing as a strategy for cancer immunotherapy. Proc Natl Acad Sci U S A 85:2320–2323

    Google Scholar 

  • Xie J, Mølck C, Paquet-Fifield S et al (2016) High expression of TROP2 characterizes different cell subpopulations in androgen-sensitive and androgen-independent prostate cancer cells. Oncotarget 7:44492–44504

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamamoto M, Bharti A, Li Y et al (1997) Interaction of the DF3/MUC1 breast carcinoma-associated antigen and beta-catenin in cell adhesion. J Biol Chem 272:12492–12494

    Article  CAS  PubMed  Google Scholar 

  • Yamashita T, Mori Y, Alzaaqi SM et al (2019) Induction of Trop-2 expression through the binding of galectin-3 to MUC1. Biochem Biophys Res Commun 516:44–49

    Article  CAS  PubMed  Google Scholar 

  • Yang RY, Hill PN, Hsu DK et al (1998) Role of the carboxyl-terminal lectin domain in self-association of galectin-3. Biochemistry 37:4086–4092

    Article  CAS  PubMed  Google Scholar 

  • Yin BW, Lloyd KO (2001) Molecular cloning of the CA125 ovarian cancer antigen: identification as a new mucin, MUC16. J Biol Chem 276:27371–27375

    Article  CAS  PubMed  Google Scholar 

  • Yu LG, Andrews N, Zhao Q et al (2007) Galectin-3 interaction with Thomsen-Friedenreich disaccharide on cancer-associated MUC1 causes increased cancer cell endothelial adhesion. J Biol Chem 282:773–781

    Article  CAS  PubMed  Google Scholar 

  • Zeng P, Chen MB, Zhou LN et al (2016) Impact of TROP2 expression on prognosis in solid tumors: a systematic review and meta-analysis. Sci Rep 6:33658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Q, Guo X, Nash GB et al (2009) Circulating galectin-3 promotes metastasis by modifying MUC1 localization on cancer cell surface. Cancer Res 69:6799–6806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Q, Barclay M, Hilkens J et al (2010) Interaction between circulating galectin-3 and cancer-associated MUC1 enhances tumour cell homotypic aggregation and prevents anoikis. Mol Cancer 9:154

    Article  PubMed  PubMed Central  Google Scholar 

  • Zizzari IG, Martufi P, Battisti F et al (2015) The macrophage galactose-type C-type lectin (MGL) modulates regulatory T cell functions. PLoS One 10:e0132617

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Bioscience, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, Japan

    Shungo Iwamoto, Naoki Itano & Hiroshi Nakada

Authors
  1. Shungo Iwamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naoki Itano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroshi Nakada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroshi Nakada .

Editor information

Editors and Affiliations

  1. Department of Biomedical Sciences, Chubu University College of Life and Health Sciences, Kasugai, Aichi, Japan

    Koichi Furukawa

  2. Glycobiology Unit, Sanford-Burnham Medical Research Institute, La Jolla, CA, USA

    Minoru Fukuda

Rights and permissions

Reprints and permissions

Copyright information

© 2023 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Iwamoto, S., Itano, N., Nakada, H. (2023). Tumor Progression through Interaction of Mucins with Lectins and Subsequent Signal Transduction. In: Furukawa, K., Fukuda, M. (eds) Glycosignals in Cancer. Springer, Singapore. https://doi.org/10.1007/978-981-19-7732-9_9

Download citation

Publish with us

Policies and ethics

Search

Navigation