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Citations to this article

Transcriptional activation of integrin β6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma
Richard C. Bates, … , Peter Oettgen, Arthur M. Mercurio
Richard C. Bates, … , Peter Oettgen, Arthur M. Mercurio
Published February 1, 2005
Citation Information: J Clin Invest. 2005;115(2):339-347. https://doi.org/10.1172/JCI23183.
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Transcriptional activation of integrin β6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma

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Abstract

We used a spheroid model of colon carcinoma to analyze integrin dynamics as a function of the epithelial-mesenchymal transition (EMT), a process that provides a paradigm for understanding how carcinoma cells acquire a more aggressive phenotype. This EMT involves transcriptional activation of the β6 integrin subunit and a consequent induction of αvβ6 expression. This integrin enhances the tumorigenic properties of colon carcinoma, including activation of autocrine TGF-β and migration on interstitial fibronectin. Importantly, this study validates the clinical relevance of the EMT. Kaplan-Meier analysis of β6 expression in 488 colorectal carcinomas revealed a striking reduction in median survival time of patients with high β6 expression. Elevated receptor expression did not simply reflect increasing tumor stage, since log-rank analysis showed a more significant impact on the survival of patients with early-stage, as opposed to late-stage, disease. Cox regression analysis confirmed that this integrin is an independent variable for these tumors. These findings define the αvβ6 integrin as an important risk factor for early-stage disease and a novel therapeutic candidate for colorectal cancer.

Authors

Richard C. Bates, David I. Bellovin, Courtney Brown, Elizabeth Maynard, Bingyan Wu, Hisaaki Kawakatsu, Dean Sheppard, Peter Oettgen, Arthur M. Mercurio

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Z Li, P Lin, C Gao, C Peng, S Liu, H Gao, B Wang, J Wang, J Niu, W Niu
Tumor Biology 2015
Fibroblast surface-associated FGF-2 promotes contact-dependent colorectal cancer cell migration and invasion through FGFR-SRC signaling and integrin αvβ5-mediated adhesion.
Knuchel S, Anderle P, Werfelli P, Diamantis E, Rüegg C
Oncotarget 2015
Therapeutic Targeting of Integrin αvβ6 in Breast Cancer
KM Moore, GJ Thomas, SW Duffy, J Warwick, R Gabe, P Chou, IO Ellis, AR Green, S Haider, K Brouilette, A Saha, S Vallath, R Bowen, C Chelala, D Eccles, WJ Tapper, AM Thompson, P Quinlan, L Jordan, C Gillett, A Brentnall, S Violette, PH Weinreb, J Kendrew, ST Barry, IR Hart, JL Jones, JF Marshall
JNCI Journal of the National Cancer Institute 2014
99m Tc-Labeled Cystine Knot Peptide Targeting Integrin α v β 6 for Tumor SPECT Imaging
X Zhu, J Li, Y Hong, RH Kimura, X Ma, H Liu, C Qin, X Hu, TR Hayes, P Benny, SS Gambhir, Z Cheng
Molecular Pharmaceutics 2014
Identification and Characterization of a Suite of Tumor Targeting Peptides for Non-Small Cell Lung Cancer
MJ McGuire, BP Gray, S Li, D Cupka, LA Byers, L Wu, S Rezaie, YH Liu, N Pattisapu, J Issac, T Oyama, L Diao, JV Heymach, XJ Xie, JD Minna, KC Brown
Scientific Reports 2014
Protein expression of eIF4E and integrin αvβ6 in colon cancer can predict clinical significance, reveal their correlation and imply possible mechanism of interaction
Z Niu, J Wang, S Muhammad, W Niu, E Liu, C Peng, B Liang, Q Sun, S Obo, Z He, S Liu, X Zou, J Niu
Cell & Bioscience 2014
Correlations between Integrin ανβ6 Expression and Clinico-Pathological Features in Stage B and Stage C Rectal Cancer
SB Ahn, A Mohamedali, C Chan, J Fletcher, SY Kwun, C Clarke, OF Dent, PH Chapuis, E Nice, MS Baker
PloS one 2014
Role of H-Ras/ERK signaling in carbon nanotube-induced neoplastic-like transformation of human mesothelial cells
W Lohcharoenkal, L Wang, TA Stueckle, J Park, W Tse, CZ Dinu, Y Rojanasakul
Frontiers in physiology 2014
Dimerization of a Phage-Display Selected Peptide for Imaging of αvβ6- Integrin: Two Approaches to the Multivalent Effect
AN Singh, MJ McGuire, S Li, G Hao, A Kumar, X Sun, KC Brown
Theranostics 2014
Pathophysiology of fistula formation in Crohn's disease
M Scharl, G Rogler
World journal of gastrointestinal pathophysiology 2014
Characterization and Evaluation of 64Cu-Labeled A20FMDV2 Conjugates for Imaging the Integrin αvβ6
LY Hu, N Bauer, LM Knight, Z Li, S Liu, CJ Anderson, PS Conti, JL Sutcliffe
Molecular Imaging and Biology 2014
Integrin αvβ6 and transcriptional factor Ets-1 act as prognostic indicators in colorectal cancer
C Peng, H Gao, Z Niu, B Wang, Z Tan, W Niu, E Liu, J Wang, J Sun, M Shahbaz, M Agrez, J Niu
Cell & Bioscience 2014
Targeting of the β6 gene to suppress degradation of ECM via inactivation of the MAPK pathway in breast adenocarcinoma cells
Y Zhang, L Wei, J Yu, G Li, X Zhang, A Wang, Y He, H Li, D Yin
Oncology reports 2014
Tumor Targeting via Integrin Ligands
UK Marelli, F Rechenmacher, TR Sobahi, C Mas-Moruno, H Kessler
Frontiers in Oncology 2013
Fibrosis of two: Epithelial cell-fibroblast interactions in pulmonary fibrosis
N Sakai, AM Tager
Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 2013
The role for dickkopf-homolog-1 in the pathogenesis of Crohn's disease-associated fistulae
SM Frei, C Hemsley, T Pesch, S Lang, A Weber, E Jehle, A Rühl, M Fried, G Rogler, M Scharl
PloS one 2013
Epithelial-mesenchymal plasticity in carcinoma metastasis
JH Tsai, J Yang
Genes & development 2013
A liposomal drug platform overrides peptide ligand targeting to a cancer biomarker, irrespective of ligand affinity or density
BP Gray, MJ McGuire, KC Brown
PloS one 2013
Binding of αvβ1 and αvβ6 integrins to tenascin-C induces epithelial-mesenchymal transition-like change of breast cancer cells
D Katoh, K Nagaharu, N Shimojo, N Hanamura, M Yamashita, Y Kozuka, K Imanaka-Yoshida, T Yoshida
Oncogenesis 2013
Structural guided scaffold phage display libraries as a source of bio-therapeutics
YK Man, D DiCara, N Chan, S Vessillier, SJ Mather, ML Rowe, MJ Howard, JF Marshall, A Nissim
PloS one 2013
18F-fluorobenzoate-labeled cystine knot peptides for PET imaging of integrin αvβ6
BJ Hackel, RH Kimura, Z Miao, H Liu, A Sathirachinda, Z Cheng, FT Chin, SS Gambhir
Journal of Nuclear Medicine 2013
Krüppel-like factor 5: a novel biomarker for lymph node metastasis and recurrence in supraglottic squamous cell laryngeal carcinoma
X Mao, S Miao, H He, S Miao, R Pei, X Yang, C Xiu, K Song, J Zhang, J Sun, S Jia, Q Guan
Tumor Biology 2013
Integrin-β5 and zyxin mediate formation of ventral stress fibers in response to transforming growth factor β
A Bianchi-Smiraglia, D Kunnev, M Limoge, A Lee, M Beckerle, A Bakin
Cell cycle (Georgetown, Tex.) 2013
From Phage Display to Nanoparticle Delivery: Functionalizing Liposomes with Multivalent Peptides Improves Targeting to a Cancer Biomarker
BP Gray, S Li, KC Brown
Bioconjugate Chemistry 2013
The role of the myofibroblast in tumor stroma remodeling
M Otranto, V Sarrazy, F Bonté, B Hinz, G Gabbiani, A Desmouliere
Cell adhesion & migration 2012
aV integrins and TGF-β-induced EMT: a circle of regulation
FA Mamuya, MK Duncan
Journal of Cellular and Molecular Medicine 2012
Integrin α9β1 promotes malignant tumor growth and metastasis by potentiating epithelial-mesenchymal transition
SK Gupta, S Oommen, MC Aubry, BP Williams, NE Vlahakis
Oncogene 2012
Integrin Trafficking and Tumor Progression
S Shin, L Wolgamott, SO Yoon
International Journal of Cell Biology 2012
Matched rabbit monoclonal antibodies against αv-series integrins reveal a novel αvβ3-LIBS epitope, and permit routine staining of archival paraffin samples of human tumors
SL Goodman, HJ Grote, C Wilm
Biology Open 2012
RGD-Binding Integrins in Prostate Cancer: Expression Patterns and Therapeutic Prospects against Bone Metastasis
M Sutherland, A Gordon, SD Shnyder, LH Patterson, HM Sheldrake
Cancers 2012
Elevated Preoperative Carcinoembryonic Antigen (CEA) and Ki67 Is Predictor of Decreased Survival in IIA Stage Colon Cancer
Y Peng, L Wang, J Gu
World Journal of Surgery 2012
C2-O-sLeX glycoproteins are E-selectin ligands that regulate invasion of human colon and hepatic carcinoma cells
CA st Hill, D Baharo-Hassan, M Farooqui
PloS one 2011
Tenascin C Induces Epithelial-Mesenchymal Transition–Like Change Accompanied by SRC Activation and Focal Adhesion Kinase Phosphorylation in Human Breast Cancer Cells
K Nagaharu, X Zhang, T Yoshida, D Katoh, N Hanamura, Y Kozuka, T Ogawa, T Shiraishi, K Imanaka-Yoshida
The American Journal of Pathology 2011
Chemically Programmed Antibodies Targeting Multiple Alpha(v) Integrins and Their Effects on Tumor-Related Functions in vitro
RK Goswami, KM Bajjuri, JS Forsyth, S Das, W Hassenpflug, ZZ Huang, RA Lerner, B Felding-Habermann, SC Sinha
Bioconjugate Chemistry 2011
The role of tumour stroma in colorectal cancer invasion and metastasis
J Conti, G Thomas
Cancers 2011
Pharmacokinetically stabilized cystine knot peptides that bind alpha-v-beta-6 integrin with single-digit nanomolar affinities for detection of pancreatic cancer
RH Kimura, R Teed, BJ Hackel, MA Pysz, CZ Chuang, A Sathirachinda, JK Willmann, SS Gambhir
Clinical cancer research 2011
Proteomics identification of ITGB3 as a key regulator in reactive oxygen species-induced migration and invasion of colorectal cancer cells
Y Lei, K Huang, C Gao, QC Lau, H Pan, K Xie, J Li, R Liu, T Zhang, N Xie, HS Nai, H Wu, Q Dong, X Zhao, EC Nice, C Huang, Y Wei
Molecular & cellular proteomics : MCP 2011
Synthesis and biological evaluation of a peptide–paclitaxel conjugate which targets the integrin αvβ6
S Li, BP Gray, MJ McGuire, KC Brown
Bioorganic & Medicinal Chemistry 2011
Why integrin as a primary target for imaging and therapy.
Niu G, Chen X
Theranostics 2011
Epithelial-Mesenchymal Transition Induced by Transforming Growth Factor-β1/Snail Activation Aggravates Invasive Growth of Cholangiocarcinoma
Y Sato, K Harada, K Itatsu, H Ikeda, Y Kakuda, S Shimomura, XS Ren, N Yoneda, M Sasaki, Y Nakanuma
The American Journal of Pathology 2010
Integrin–TGF-β crosstalk in fibrosis, cancer and wound healing
C Margadant, A Sonnenberg
EMBO reports 2010
Integrins in cancer: biological implications and therapeutic opportunities
JS Desgrosellier, DA Cheresh
Nature Reviews Cancer 2010
Tropism-Modification Strategies for Targeted Gene Delivery Using Adenoviral Vectors
L Coughlan, R Alba, AL Parker, AC Bradshaw, IA McNeish, SA Nicklin, AH Baker
Viruses 2010
Oxidative stress induced mechanisms in the progression of periodontal diseases and cancer: a common approach to redox homeostasis?
M Soory
Cancers 2010
Integrin signaling and lung cancer.
Caccavari F, Valdembri D, Sandri C, Bussolino F, Serini G
Cell adhesion & migration 2010
Biomarkers for epithelial-mesenchymal transitions
Michael Zeisberg1 and Eric G. Neilson2
Journal of Clinical Investigation 2009
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009
Mechanisms of the epithelial-mesenchymal transition by TGF-beta
MK Wendt, TM Allington, WP Schiemann
Future oncology (London, England) 2009
Revisiting the seed and soil in cancer metastasis
M Mendoza, C Khanna
The International Journal of Biochemistry & Cell Biology 2009
High-throughput in vivo screening of targeted molecular imaging agents
MK Gagnon, SH Hausner, J Marik, CK Abbey, JF Marshall, JL Sutcliffe
Proceedings of the National Academy of Sciences 2009
Norcantharidin induces HT-29 colon cancer cell apoptosis through the ��v��6���extracellular signal-related kinase signaling pathway
C Peng, X Liu, E Liu, K Xu, W Niu, R Chen, J Wang, Z Zhang, P Lin, J Wang, M Agrez, J Niu
Cancer Science 2009
MRI-Visible Micellar Nanomedicine for Targeted Drug Delivery to Lung Cancer Cells
JS Guthi, SG Yang, G Huang, S Li, C Khemtong, CW Kessinger, M Peyton, JD Minna, KC Brown, J Gao
Molecular Pharmaceutics 2009
Synthesis and characterization of a high-affinity α v β 6 -specific ligand for in vitro and in vivo applications
S Li, MJ McGuire, M Lin, YH Liu, T Oyama, X Sun, KC Brown
Molecular cancer therapeutics 2009
Targeted In vivo Imaging of Integrin α v β 6 with an Improved Radiotracer and Its Relevance in a Pancreatic Tumor Model
SH Hausner, CK Abbey, RJ Bold, MK Gagnon, J Marik, JF Marshall, CE Stanecki, JL Sutcliffe
Cancer research 2009
Defining the role of integrin alphavbeta6 in cancer.
Bandyopadhyay A, Raghavan S
Current drug targets 2009
Matrix metalloproteinase‐2 expression in stromal tissues is a consistent prognostic factor in stage II colon cancer
Inafuku Y, Furuhata T, Tayama M, Okita K, Nishidate T, Mizuguchi T, Kimura Y, Hirata K
Cancer Science 2009
Engineering a single-chain Fv antibody to alpha v beta 6 integrin using the specificity-determining loop of a foot-and-mouth disease virus
H Kogelberg, B Tolner, GJ Thomas, DD Cara, S Minogue, B Ramesh, S Sodha, D Marsh, MW Lowdell, T Meyer, RH Begent, I Hart, JF Marshall, K Chester
Journal of Molecular Biology 2008
PAI-1 and functional blockade of SNAI1 in breast cancer cell migration
E Fabre-Guillevin, M Malo, A Cartier-Michaud, H Peinado, G Moreno-Bueno, B Vallée, DA Lawrence, J Palacios, A Cano, G Barlovatz-Meimon, C Charrière-Bertrand
Breast Cancer Research 2008
Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front
OD Wever, P Pauwels, BD Craene, M Sabbah, S Emami, G Redeuilh, C Gespach, M Bracke, G Berx
Histochemistry and Cell Biology 2008
A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells
U Burk, J Schubert, U Wellner, O Schmalhofer, E Vincan, S Spaderna, T Brabletz
EMBO reports 2008
Intestinal adenomagenesis involves core molecular signatures of the epithelial–mesenchymal transition
X Chen, RB Halberg, RP Burch, WF Dove
Journal Of Molecular Histology 2008
Transforming Growth Factor β Controls the Directional Migration of Hepatocyte Cohorts by Modulating Their Adhesion to Fibronectin
F Binamé, P Lassus, U Hibner, CH Heldin
Molecular biology of the cell 2008
Peptide-Targeted Polyglutamic Acid Doxorubicin Conjugates for the Treatment of α v β 6 -Positive Cancers
H Guan, MJ McGuire, S Li, KC Brown
Bioconjugate Chemistry 2008
In Vivo Positron Emission Tomography (PET) Imaging with an α v β 6 Specific Peptide Radiolabeled using 18 F-“Click” Chemistry: Evaluation and Comparison with the Corresponding 4-[ 18 F]Fluorobenzoyl- and 2-[ 18 F]Fluoropropionyl-Peptides
SH Hausner, J Marik, MK Gagnon, JL Sutcliffe
Journal of Medicinal Chemistry 2008
Integrin alphavbeta6 mediates the potential for colon cancer cells to colonize in and metastasize to the liver
Yang G, Xu K, Pan Z, Zhang Z, Mi Y, Wang J, Chen R, Niu J
Cancer Science 2008
Constitutively Activated Stat3 Induces Tumorigenesis and Enhances Cell Motility of Prostate Epithelial Cells through Integrin β6
J Azare, K Leslie, H Al-Ahmadie, W Gerald, PH Weinreb, SM Violette, J Bromberg
Molecular and cellular biology 2007
Loss of TGFbeta signaling destabilizes homeostasis and promotes squamous cell carcinomas in stratified epithelia
G Guasch, M Schober, HA Pasolli, EB Conn, L Polak, E Fuchs
Cancer Cell 2007
Role of αvβ6 Integrin in Acute Biliary Fibrosis
B Wang, BM Dolinski, N Kikuchi, DR Leone, MG Peters, PH Weinreb, SM Violette, DM Bissell
Hepatology 2007
Signaling networks guiding epithelial–mesenchymal transitions during embryogenesis and cancer progression
Moustakas A, Heldin C
Cancer Science 2007
P-selectin activates integrin-mediated colon carcinoma cell adhesion to fibronectin
ME Reyes-Reyes, MD George, JD Roberts, SK Akiyama
Experimental Cell Research 2006

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