Skip to main content
Top
Published in: Clinical & Experimental Metastasis 4/2015

01-04-2015 | Review

MUC1-mediated motility in breast cancer: a review highlighting the role of the MUC1/ICAM-1/Src signaling triad

Authors: Lacey Haddon, Judith Hugh

Published in: Clinical & Experimental Metastasis | Issue 4/2015

Login to get access

Abstract

Breast cancer is the most common cancer in women with the leading cause of death being metastasis, the spread of cancer to distant organs. For those patients with high-risk estrogen receptor positive (ER+) breast cancer, an increased expression of the glycoprotein MUC1 is associated with resistance to anti-hormonal therapy, metastasis and death. Tumor cells may use MUC1 to metastasize by exploiting the vascular adhesion pathways used by leukocytes during the inflammatory response. MUC1 is a type 1 transmembrane protein whose cytoplasmic tail acts as a scaffold for several signaling pathways including the non-receptor kinase Src, a signaling molecule involved in cell differentiation, proliferation, adhesion and motility. This review will highlight our current knowledge of how MUC1/ICAM-1 binding can lead to the recruitment and activation of Src and propose a novel role for lipid raft microdomains in this promigratory signaling. Improved understanding of the mechanism of metastases and the underlying signaling cascade is a prerequisite to the discovery of therapeutic targets to prevent metastasis and death in ER+ breast cancer patients.
Literature
1.
go back to reference Gruvberger S, Ringner M, Chen Y et al (2001) Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res 61:5979–5984PubMed Gruvberger S, Ringner M, Chen Y et al (2001) Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res 61:5979–5984PubMed
2.
go back to reference Perou CM, Sorlie T, Eisen MB et al (2000) Molecular portraits of human breast tumours. Nature 406:747–752PubMed Perou CM, Sorlie T, Eisen MB et al (2000) Molecular portraits of human breast tumours. Nature 406:747–752PubMed
4.
go back to reference Jumppanen M, Gruvberger-Saal S, Kauraniemi P et al (2007) Basal-like phenotype is not associated with patient survival in estrogen-receptor-negative breast cancers. Breast Cancer Res. 9:R16PubMedCentralPubMed Jumppanen M, Gruvberger-Saal S, Kauraniemi P et al (2007) Basal-like phenotype is not associated with patient survival in estrogen-receptor-negative breast cancers. Breast Cancer Res. 9:R16PubMedCentralPubMed
9.
go back to reference Pitroda SP, Khodarev NN, Beckett MA, Kufe DW, Weichselbaum RR (2009) MUC1-induced alterations in a lipid metabolic gene network predict response of human breast cancers to tamoxifen treatment. Proc Natl Acad Sci USA 106:5837–5841PubMedCentralPubMed Pitroda SP, Khodarev NN, Beckett MA, Kufe DW, Weichselbaum RR (2009) MUC1-induced alterations in a lipid metabolic gene network predict response of human breast cancers to tamoxifen treatment. Proc Natl Acad Sci USA 106:5837–5841PubMedCentralPubMed
10.
go back to reference Rahn JJ, Dabbagh L, Pasdar M, Hugh JC (2001) The importance of MUC1 cellular localization in patients with breast carcinoma: an immunohistologic study of 71 patients and review of the literature. Cancer 91:1973–1982PubMed Rahn JJ, Dabbagh L, Pasdar M, Hugh JC (2001) The importance of MUC1 cellular localization in patients with breast carcinoma: an immunohistologic study of 71 patients and review of the literature. Cancer 91:1973–1982PubMed
11.
go back to reference Rakha E, Boyce R, Abd El-Rehim D et al (2005) Expression of mucins (MUC1, MUC2, MUC3, MUC4, MUC5AC and MUC6) and their prognostic significance in human breast cancer. Mod Pathol 18:1295–1304. doi:10.1038/modpathol.3800445 PubMed Rakha E, Boyce R, Abd El-Rehim D et al (2005) Expression of mucins (MUC1, MUC2, MUC3, MUC4, MUC5AC and MUC6) and their prognostic significance in human breast cancer. Mod Pathol 18:1295–1304. doi:10.​1038/​modpathol.​3800445 PubMed
13.
go back to reference Shen Q, Rahn JJ, Zhang J et al (2008) MUC1 initiates Src-CrkL-Rac1/Cdc42-mediated actin cytoskeletal protrusive motility after ligating intercellular adhesion molecule-1. Mol Cancer Res 6:555–567PubMed Shen Q, Rahn JJ, Zhang J et al (2008) MUC1 initiates Src-CrkL-Rac1/Cdc42-mediated actin cytoskeletal protrusive motility after ligating intercellular adhesion molecule-1. Mol Cancer Res 6:555–567PubMed
14.
17.
go back to reference Shimizu M, Yamauchi K (1982) Isolation and characterization of mucin-like glycoprotein in human milk fat globule membrane. J Biochem 91:515–524PubMed Shimizu M, Yamauchi K (1982) Isolation and characterization of mucin-like glycoprotein in human milk fat globule membrane. J Biochem 91:515–524PubMed
18.
go back to reference Gendler S, Taylor-Papadimitriou J, Duhig T, Rothbard J, Burchell J (1988) A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J Biol Chem 263:12820–12823PubMed Gendler S, Taylor-Papadimitriou J, Duhig T, Rothbard J, Burchell J (1988) A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J Biol Chem 263:12820–12823PubMed
19.
go back to reference Hilkens J, Buijs F (1988) Biosynthesis of Mam-6, an epithelial sialomucin—evidence for involvement of a rare proteolytic cleavage step in the endoplasmic-reticulum. J Biol Chem 263:4215–4222PubMed Hilkens J, Buijs F (1988) Biosynthesis of Mam-6, an epithelial sialomucin—evidence for involvement of a rare proteolytic cleavage step in the endoplasmic-reticulum. J Biol Chem 263:4215–4222PubMed
20.
go back to reference Gendler SJ, Lancaster CA, Taylor-Papadimitriou J et al (1990) Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem 265:15286–15293PubMed Gendler SJ, Lancaster CA, Taylor-Papadimitriou J et al (1990) Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem 265:15286–15293PubMed
24.
go back to reference Ligtenberg M, Kruijshaar L, Buijs F, Vanmeijer M, Litvinov S, Hilkens J (1992) Cell-associated episialin is a complex containing 2 proteins derived from a common precursor. J Biol Chem 267:6171–6177PubMed Ligtenberg M, Kruijshaar L, Buijs F, Vanmeijer M, Litvinov S, Hilkens J (1992) Cell-associated episialin is a complex containing 2 proteins derived from a common precursor. J Biol Chem 267:6171–6177PubMed
25.
go back to reference Bork P, Patthy L (1995) The sea module—a new extracellular domain associated with O-glycosylation. Protein Sci 4:1421–1425PubMedCentralPubMed Bork P, Patthy L (1995) The sea module—a new extracellular domain associated with O-glycosylation. Protein Sci 4:1421–1425PubMedCentralPubMed
26.
go back to reference Macao B, Johansson D, Hansson G, Hard T (2006) Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 13:71–76. doi:10.1038/nsmb1035 PubMed Macao B, Johansson D, Hansson G, Hard T (2006) Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 13:71–76. doi:10.​1038/​nsmb1035 PubMed
27.
go back to reference Gendler SJ, Spicer AP (1995) Epithelial mucin genes. Annu Rev Physiol 57:607–634PubMed Gendler SJ, Spicer AP (1995) Epithelial mucin genes. Annu Rev Physiol 57:607–634PubMed
28.
go back to reference Litvinov S, Hilkens J (1993) The epithelial sialomucin, episialin, is sialylated during recycling. J Biol Chem 268:21364–21371PubMed Litvinov S, Hilkens J (1993) The epithelial sialomucin, episialin, is sialylated during recycling. J Biol Chem 268:21364–21371PubMed
30.
go back to reference Burchell J, Mungul A, Taylor-Papadimitriou J (2001) O-linked glycosylation in the mammary gland: changes that occur during malignancy. J Mammary Gland Biol Neoplasia 6:355–364. doi:10.1023/A:1011331809881 PubMed Burchell J, Mungul A, Taylor-Papadimitriou J (2001) O-linked glycosylation in the mammary gland: changes that occur during malignancy. J Mammary Gland Biol Neoplasia 6:355–364. doi:10.​1023/​A:​1011331809881 PubMed
33.
go back to reference Zhang K, Baeckstrom D, Brevinge H, Hansson G (1997) Comparison of sialyl-Lewis a carrying CD43 and MUC1 mucins secreted from a colon carcinoma cell line for E-selectin binding and inhibition of leukocyte adhesion. Tumour Biol 18:175–187PubMed Zhang K, Baeckstrom D, Brevinge H, Hansson G (1997) Comparison of sialyl-Lewis a carrying CD43 and MUC1 mucins secreted from a colon carcinoma cell line for E-selectin binding and inhibition of leukocyte adhesion. Tumour Biol 18:175–187PubMed
34.
go back to reference Geng Y, Yeh K, Takatani T, King MR (2012) Three to tango: muc1 as a ligand for both E-selectin and ICAM-1 in the breast cancer metastatic cascade. Front Oncol 2:76PubMedCentralPubMed Geng Y, Yeh K, Takatani T, King MR (2012) Three to tango: muc1 as a ligand for both E-selectin and ICAM-1 in the breast cancer metastatic cascade. Front Oncol 2:76PubMedCentralPubMed
37.
go back to reference Yu L, 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. doi:10.1074/jbc.M606862200 PubMed Yu L, 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. doi:10.​1074/​jbc.​M606862200 PubMed
38.
go back to reference Tanida S, Mori Y, Ishida A, Akita K, Nakada H (2014) Galectin-3 binds to MUC1-N-terminal domain and triggers recruitment of β-catenin in MUC1-expressing mouse 3T3 cells. Biochim Biophys Acta 1840:1790–1797PubMed Tanida S, Mori Y, Ishida A, Akita K, Nakada H (2014) Galectin-3 binds to MUC1-N-terminal domain and triggers recruitment of β-catenin in MUC1-expressing mouse 3T3 cells. Biochim Biophys Acta 1840:1790–1797PubMed
39.
go back to reference 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 276:35239–35242PubMed 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 276:35239–35242PubMed
41.
go back to reference Fontenot J, Tjandra N, Bu D, Ho C, Montelaro R, Finn O (1993) Biophysical characterization of One-tandem, 2-tandem, and 3-tandem repeats of human mucin (Muc-1) protein core. Cancer Res 53:5386–5394PubMed Fontenot J, Tjandra N, Bu D, Ho C, Montelaro R, Finn O (1993) Biophysical characterization of One-tandem, 2-tandem, and 3-tandem repeats of human mucin (Muc-1) protein core. Cancer Res 53:5386–5394PubMed
42.
go back to reference Patton S, Gendler SJ, Spicer AP (1995) The epithelial mucin, MUC1, of milk, mammary gland and other tissues. Biochim Biophys Acta 1241:407–423PubMed Patton S, Gendler SJ, Spicer AP (1995) The epithelial mucin, MUC1, of milk, mammary gland and other tissues. Biochim Biophys Acta 1241:407–423PubMed
43.
go back to reference Fontenot J, Mariappan S, Catasti P, Domenech N, Finn O, Gupta G (1995) Structure of a tumor-associated antigen containing a tandemly repeated immunodominant epitope. J Biomol Struct Dyn 13:245–260PubMed Fontenot J, Mariappan S, Catasti P, Domenech N, Finn O, Gupta G (1995) Structure of a tumor-associated antigen containing a tandemly repeated immunodominant epitope. J Biomol Struct Dyn 13:245–260PubMed
44.
go back to reference Kam JL, Regimbald LH, Hilgers JH et al (1998) MUC1 synthetic peptide inhibition of intercellular adhesion molecule-1 and MUC1 binding requires six tandem repeats. Cancer Res 58:5577–5581PubMed Kam JL, Regimbald LH, Hilgers JH et al (1998) MUC1 synthetic peptide inhibition of intercellular adhesion molecule-1 and MUC1 binding requires six tandem repeats. Cancer Res 58:5577–5581PubMed
46.
go back to reference Staubach S, Razawi H, Hanisch FG (2009) Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 9:2820–2835PubMed Staubach S, Razawi H, Hanisch FG (2009) Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 9:2820–2835PubMed
49.
go back to reference Casadio R, Fariselli P, Taroni C, Compiani M (1996) A predictor of transmembrane alpha-helix domains of proteins based on neural networks. Eur Biophys J 24:165–178PubMed Casadio R, Fariselli P, Taroni C, Compiani M (1996) A predictor of transmembrane alpha-helix domains of proteins based on neural networks. Eur Biophys J 24:165–178PubMed
50.
go back to reference Spicer AP, Parry G, Patton S, Gendler SJ (1991) Molecular cloning and analysis of the mouse homologue of the tumor-associated mucin, MUC1, reveals conservation of potential O-glycosylation sites, transmembrane, and cytoplasmic domains and a loss of minisatellite-like polymorphism. J Biol Chem 266:15099–15109PubMed Spicer AP, Parry G, Patton S, Gendler SJ (1991) Molecular cloning and analysis of the mouse homologue of the tumor-associated mucin, MUC1, reveals conservation of potential O-glycosylation sites, transmembrane, and cytoplasmic domains and a loss of minisatellite-like polymorphism. J Biol Chem 266:15099–15109PubMed
51.
go back to reference Handa K, Jacobs F, Longenecker B, Hakomori S (2001) Association of MUC-1 and PSGL-1 with low-density microdomain in T-lymphocytes: a preliminary note. Biochem Biophys Res Commun 285:788–794. doi:10.1006/bbrc.2001.5225 PubMed Handa K, Jacobs F, Longenecker B, Hakomori S (2001) Association of MUC-1 and PSGL-1 with low-density microdomain in T-lymphocytes: a preliminary note. Biochem Biophys Res Commun 285:788–794. doi:10.​1006/​bbrc.​2001.​5225 PubMed
54.
go back to reference Kinlough CL, McMahan RJ, Poland PA et al (2006) Recycling of MUC1 is dependent on its palmitoylation. J Biol Chem 281:12112–12122PubMed Kinlough CL, McMahan RJ, Poland PA et al (2006) Recycling of MUC1 is dependent on its palmitoylation. J Biol Chem 281:12112–12122PubMed
55.
go back to reference Pemberton L, Rughetti A, TaylorPapadimitriou J, Gendler S (1996) The epithelial mucin MUC1 contains at least two discrete signals specifying membrane localization in cells. J Biol Chem 271:2332–2340PubMed Pemberton L, Rughetti A, TaylorPapadimitriou J, Gendler S (1996) The epithelial mucin MUC1 contains at least two discrete signals specifying membrane localization in cells. J Biol Chem 271:2332–2340PubMed
56.
go back to reference Levental I, Lingwood D, Grzybek M, Coskun U, Simons K (2010) Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci USA 107:22050–22054PubMedCentralPubMed Levental I, Lingwood D, Grzybek M, Coskun U, Simons K (2010) Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci USA 107:22050–22054PubMedCentralPubMed
59.
go back to reference Raina D, Ahmad R, Rajabi H, Panchamoorthy G, Kharbanda S, Kufe D (2012) Targeting cysteine-mediated dimerization of the MUC1-C oncoprotein in human cancer cells. Int J Oncol 40:1643–1649PubMedCentralPubMed Raina D, Ahmad R, Rajabi H, Panchamoorthy G, Kharbanda S, Kufe D (2012) Targeting cysteine-mediated dimerization of the MUC1-C oncoprotein in human cancer cells. Int J Oncol 40:1643–1649PubMedCentralPubMed
60.
go back to reference Bernier AJ, Zhang J, Lillehoj E, Shaw AR, Gunasekara N, Hugh JC (2011) Non-cysteine linked MUC1 cytoplasmic dimers are required for Src recruitment and ICAM-1 binding induced cell invasion. Mol Cancer 10:93PubMedCentralPubMed Bernier AJ, Zhang J, Lillehoj E, Shaw AR, Gunasekara N, Hugh JC (2011) Non-cysteine linked MUC1 cytoplasmic dimers are required for Src recruitment and ICAM-1 binding induced cell invasion. Mol Cancer 10:93PubMedCentralPubMed
63.
go back to reference Li Y, Kuwahara H, Ren J, Wen G, Kufe D (2001) The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3 beta and beta-catenin. J Biol Chem 276:6061–6064. doi:10.1074/jbc.C000754200 PubMed Li Y, Kuwahara H, Ren J, Wen G, Kufe D (2001) The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3 beta and beta-catenin. J Biol Chem 276:6061–6064. doi:10.​1074/​jbc.​C000754200 PubMed
65.
go back to reference Gunasekara N, Sykes B, Hugh J (2012) Characterization of a novel weak interaction between MUC1 and Src-SH3 using nuclear magnetic resonance spectroscopy. Biochem Biophys Res Commun 421:832–836PubMed Gunasekara N, Sykes B, Hugh J (2012) Characterization of a novel weak interaction between MUC1 and Src-SH3 using nuclear magnetic resonance spectroscopy. Biochem Biophys Res Commun 421:832–836PubMed
66.
go back to reference Dustin M, Rothlein R, Bhan A, Dinarello C, Springer T (1986) Induction by Il-1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (Icam-1). J Immunol 137:245–254PubMed Dustin M, Rothlein R, Bhan A, Dinarello C, Springer T (1986) Induction by Il-1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (Icam-1). J Immunol 137:245–254PubMed
67.
go back to reference Wyble C, Desai T, Clark E, Hynes K, Gewertz B (1996) Physiologic concentrations of TNF alpha and IL-1 beta released from reperfused human intestine upregulate E-selectin and ICAM-1. J Surg Res 63:333–338. doi:10.1006/jsre.1996.0271 PubMed Wyble C, Desai T, Clark E, Hynes K, Gewertz B (1996) Physiologic concentrations of TNF alpha and IL-1 beta released from reperfused human intestine upregulate E-selectin and ICAM-1. J Surg Res 63:333–338. doi:10.​1006/​jsre.​1996.​0271 PubMed
68.
go back to reference Staunton D, Marlin S, Stratowa C, Dustin M, Springer T (1988) Primary structure of Icam-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell 52:925–933. doi:10.1016/0092-8674(88)90434-5 PubMed Staunton D, Marlin S, Stratowa C, Dustin M, Springer T (1988) Primary structure of Icam-1 demonstrates interaction between members of the immunoglobulin and integrin supergene families. Cell 52:925–933. doi:10.​1016/​0092-8674(88)90434-5 PubMed
69.
70.
go back to reference Miller J, Knorr R, Ferrone M, Houdei R, Carron C, Dustin M (1995) Intercellular-adhesion molecule-1 dimerization and its consequences for adhesion mediated by lymphocyte function associated-1. J Exp Med 182:1231–1241. doi:10.1084/jem.182.5.1231 PubMed Miller J, Knorr R, Ferrone M, Houdei R, Carron C, Dustin M (1995) Intercellular-adhesion molecule-1 dimerization and its consequences for adhesion mediated by lymphocyte function associated-1. J Exp Med 182:1231–1241. doi:10.​1084/​jem.​182.​5.​1231 PubMed
72.
go back to reference Jun C, Carman C, Redick S, Shimaoka M, Erickson H, Springer T (2001) Ultrastructure and function of dimeric, soluble intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 276:29019–29027. doi:10.1074/jbc.M103394200 PubMed Jun C, Carman C, Redick S, Shimaoka M, Erickson H, Springer T (2001) Ultrastructure and function of dimeric, soluble intercellular adhesion molecule-1 (ICAM-1). J Biol Chem 276:29019–29027. doi:10.​1074/​jbc.​M103394200 PubMed
74.
go back to reference Oh H, Lee S, Na B et al (2007) RKIKK motif in the intracellular domain is critical for spatial and dynamic organization of ICAM-1: functional implication for the leukocyte adhesion and transmigration. Mol Biol Cell 18:2322–2335. doi:10.1091/mbc.E06-08-0744 PubMedCentralPubMed Oh H, Lee S, Na B et al (2007) RKIKK motif in the intracellular domain is critical for spatial and dynamic organization of ICAM-1: functional implication for the leukocyte adhesion and transmigration. Mol Biol Cell 18:2322–2335. doi:10.​1091/​mbc.​E06-08-0744 PubMedCentralPubMed
75.
go back to reference Heiska L, Alfthan K, Gronholm M, Vilja P, Vaheri A, Carpen O (1998) Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2)—regulation by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 273:21893–21900. doi:10.1074/jbc.273.34.21893 PubMed Heiska L, Alfthan K, Gronholm M, Vilja P, Vaheri A, Carpen O (1998) Association of ezrin with intercellular adhesion molecule-1 and -2 (ICAM-1 and ICAM-2)—regulation by phosphatidylinositol 4,5-bisphosphate. J Biol Chem 273:21893–21900. doi:10.​1074/​jbc.​273.​34.​21893 PubMed
76.
go back to reference Regimbald LH, Pilarski LM, Longenecker BM, Reddish MA, Zimmermann G, Hugh JC (1996) The breast mucin MUC1 as a novel adhesion ligand for endothelial intercellular adhesion molecule 1 in breast cancer. Cancer Res 56:4244–4249PubMed Regimbald LH, Pilarski LM, Longenecker BM, Reddish MA, Zimmermann G, Hugh JC (1996) The breast mucin MUC1 as a novel adhesion ligand for endothelial intercellular adhesion molecule 1 in breast cancer. Cancer Res 56:4244–4249PubMed
77.
go back to reference Hayashi T, Takahashi T, Motoya S et al (2001) MUC1 mucin core protein binds to the domain 1 of ICAM-1. Digestion 63:87–92PubMed Hayashi T, Takahashi T, Motoya S et al (2001) MUC1 mucin core protein binds to the domain 1 of ICAM-1. Digestion 63:87–92PubMed
78.
go back to reference Etienne-Manneville S, Manneville J, Adamson P, Wilbourn B, Greenwood J, Couraud P (2000) ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 165:3375–3383PubMed Etienne-Manneville S, Manneville J, Adamson P, Wilbourn B, Greenwood J, Couraud P (2000) ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 165:3375–3383PubMed
87.
go back to reference Rossy J, Owen DM, Williamson DJ, Yang Z, Gaus K (2013) Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat Immunol 14:82–89. doi:10.1038/ni.2488 PubMed Rossy J, Owen DM, Williamson DJ, Yang Z, Gaus K (2013) Conformational states of the kinase Lck regulate clustering in early T cell signaling. Nat Immunol 14:82–89. doi:10.​1038/​ni.​2488 PubMed
89.
91.
go back to reference Glinskii O, Huxley V, Glinsky G, Pienta K, Raz A, Glinsky V (2005) Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia 7:522–527. doi:10.1593/neo.04646 PubMedCentralPubMed Glinskii O, Huxley V, Glinsky G, Pienta K, Raz A, Glinsky V (2005) Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia 7:522–527. doi:10.​1593/​neo.​04646 PubMedCentralPubMed
93.
go back to reference Somers W, Tang J, Shaw G, Camphausen R (2000) Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell 103:467–479. doi:10.1016/S0092-8674(00)00138-0 PubMed Somers W, Tang J, Shaw G, Camphausen R (2000) Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell 103:467–479. doi:10.​1016/​S0092-8674(00)00138-0 PubMed
95.
101.
go back to reference Bennett R, Jarvela T, Engelhardt P et al (2001) Mucin MUC1 is seen in cell surface protrusions together with ezrin in immunoelectron tomography and is concentrated at tips of filopodial protrusions in MCF-7 breast carcinoma cells. J Histochem Cytochem 49:67–77PubMed Bennett R, Jarvela T, Engelhardt P et al (2001) Mucin MUC1 is seen in cell surface protrusions together with ezrin in immunoelectron tomography and is concentrated at tips of filopodial protrusions in MCF-7 breast carcinoma cells. J Histochem Cytochem 49:67–77PubMed
102.
go back to reference Bretscher A, Edwards K, Fehon R (2002) ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3:586–599. doi:10.1038/nrm882 PubMed Bretscher A, Edwards K, Fehon R (2002) ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 3:586–599. doi:10.​1038/​nrm882 PubMed
104.
go back to reference Hitosugi T, Sato M, Sasaki K, Urnezawa Y (2007) Lipid raft-specific knockdown of src family kinase activity inhibits cell adhesion and cell cycle progression of breast cancer cells. Cancer Res 67:8139–8148. doi:10.1158/0008-5472.CAN-06-4539 PubMed Hitosugi T, Sato M, Sasaki K, Urnezawa Y (2007) Lipid raft-specific knockdown of src family kinase activity inhibits cell adhesion and cell cycle progression of breast cancer cells. Cancer Res 67:8139–8148. doi:10.​1158/​0008-5472.​CAN-06-4539 PubMed
107.
go back to reference Resh MD (2006) Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci STKE 359:re14 Resh MD (2006) Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci STKE 359:re14
109.
go back to reference Sezgin E, Kaiser H, Baumgart T, Schwille P, Simons K, Levental I (2012) Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc 7:1042–1051. doi:10.1038/nprot.2012.059 PubMed Sezgin E, Kaiser H, Baumgart T, Schwille P, Simons K, Levental I (2012) Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc 7:1042–1051. doi:10.​1038/​nprot.​2012.​059 PubMed
Metadata
Title
MUC1-mediated motility in breast cancer: a review highlighting the role of the MUC1/ICAM-1/Src signaling triad
Authors
Lacey Haddon
Judith Hugh
Publication date
01-04-2015
Publisher
Springer Netherlands
Published in
Clinical & Experimental Metastasis / Issue 4/2015
Print ISSN: 0262-0898
Electronic ISSN: 1573-7276
DOI
https://doi.org/10.1007/s10585-015-9711-8

Other articles of this Issue 4/2015

Clinical & Experimental Metastasis 4/2015 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine