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LM Milstone, L Hough-Monroe, LC Kugelman, JR Bender, JG Haggerty (1994)
Epican, a heparan/chondroitin sulfate proteoglycan form of CD44, mediates cell–cell adhesionJ Cell Sci, 107
N Aceto, A Bardia, DT Miyamoto, MC Donaldson, BS Wittner, JA Spencer, M Yu, A Pely, A Engstrom, H Zhu (2014)
Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasisCell, 158
J Yamaguchi (2008)
382Am J Clin Pathol, 130
P Friedl (2012)
777Nat Cell Biol, 14
O Wever De (2003)
429J Pathol, 200
MH Chui (2013)
1487Int J Cancer, 132
D Jiang, J Liang, PW Noble (2011)
Hyaluronan as an immune regulator in human diseasesPhysiol Rev, 91
O Ilina (2009)
3203J Cell Sci, 122
P Johnson, B Ruffell (2009)
CD44 and its role in inflammation and inflammatory diseasesInflamm Allergy Drug Targets, 8
DC Zaha (2014)
Significance of immunohistochemistry in breast cancerWorld J Clin Oncol, 5
P Bronsert (2014)
410J Pathol, 234
N Kirschner, M Haftek, CM Niessen, MJ Behne, M Furuse, I Moll, JM Brandner (2011)
CD44 regulates tight-junction assembly and barrier functionJ Invest Dermatol, 131
KJ Cheung, E Gabrielson, Z Werb, AJ Ewald (2013)
Collective invasion in breast cancer requires a conserved basal epithelial programCell, 155
DC Zaha (2014)
382World J Clin Oncol, 5
P Johnson (2009)
208Inflamm Allergy Drug Targets, 8
D Jiang (2011)
221Physiol Rev, 91
P Auvinen, R Tammi, J Parkkinen, M Tammi, U Agren, R Johansson, P Hirvikoski, M Eskelinen, VM Kosma (2000)
Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survivalAm J Pathol, 156
KM Nieman (2013)
1533Biochim Biophys Acta, 1831
KM Nieman, IL Romero, B Houten, E Lengyel (2013)
Adipose tissue and adipocytes support tumorigenesis and metastasisBiochim Biophys Acta, 1831
K Wolf, YI Wu, Y Liu, J Geiger, E Tam, C Overall, MS Stack, P Friedl (2007)
Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasionNat Cell Biol, 9
AA Khalil, P Friedl (2010)
Determinants of leader cells in collective cell migrationIntegr Biol, 2
I Kimijima (2000)
25Int Soc Cell, 59
WJ Leeuw De (1997)
404J Pathol, 183
M Reffay (2014)
217Nat Cell Biol, 16
T Schlange (2007)
R63Breast Cancer Res, 9
O Ilina, P Friedl (2009)
Mechanisms of collective cell migration at a glanceJ Cell Sci, 122
MH Chui (2013)
Insights into cancer metastasis from a clinicopathologic perspective: epithelial–mesenchymal transition is not a necessary stepInt J Cancer, 132
K Wolf (2007)
893Nat Cell Biol, 9
PN Span, G Pollakis, WA Paxton, FC Sweep, JA Foekens, JW Martens, AM Sieuwerts, HW Laarhoven (2015)
Improved metastasis-free survival in nonadjuvantly treated postmenopausal breast cancer patients with chemokine receptor 5 del32 frameshift mutationsInt J Cancer, 136
P Friedl, D Gilmour (2009)
Collective cell migration in morphogenesis, regeneration and cancerNat Rev Mol Cell Biol, 10
WJ Leeuw, G Berx, CB Vos, JL Peterse, MJ Vijver, S Litvinov, F Roy, CJ Cornelisse, AM Cleton-Jansen (1997)
Simultaneous loss of E-cadherin and catenins in invasive lobular breast cancer and lobular carcinoma in situJ Pathol, 183
A Haeger (2014)
2386Biochim Biophys Acta, 1840
KJ Cheung (2016)
E854Proc Natl Acad Sci USA, 113
Y Klymenko, J Johnson, B Bos, R Lombard, L Campbell, E Loughran, MS Stack (2017)
Heterogeneous cadherin expression and multicellular aggregate dynamics in ovarian cancer disseminationNeoplasia, 19
AA Khalil (2010)
568Integr Biol, 2
O Wever, M Mareel (2003)
Role of tissue stroma in cancer cell invasionJ Pathol, 200
S Valastyan, RA Weinberg (2011)
Tumor metastasis: molecular insights and evolving paradigmsCell, 147
A Haeger, M Krause, K Wolf, P Friedl (2014)
Cell jamming: collective invasion of mesenchymal tumor cells imposed by tissue confinementBiochim Biophys Acta, 1840
N Kirschner (2011)
932J Invest Dermatol, 131
S Valastyan (2011)
275Cell, 147
N Aceto (2014)
1110Cell, 158
JP Thiery, JP Sleeman (2006)
Complex networks orchestrate epithelial–mesenchymal transitionsNat Rev Mol Cell Biol, 7
HS Berner (2001)
7Breast Cancer Res Treat, 65
HS Berner, JM Nesland (2001)
Expression of CD44 isoforms in infiltrating lobular carcinoma of the breastBreast Cancer Res Treat, 65
PN Span (2015)
91Int J Cancer, 136
PW Derksen (2006)
437Cancer Cell, 10
TE Anwar, CG Kleer (2013)
Tissue-based identification of stem cells and epithelial-to-mesenchymal transition in breast cancerHum Pathol, 44
JP Thiery (2006)
131Nat Rev Mol Cell Biol, 7
I Kimijima, T Ohtake, H Sagara, T Watanabe, S Takenoshita (2000)
Scattered fat invasion: an indicator for poor prognosis in premenopausal, and for positive estrogen receptor in postmenopausal breast cancer patientsInt Soc Cell, 59
P Bronsert, K Enderle-Ammour, M Bader, S Timme, M Kuehs, A Csanadi, G Kayser, I Kohler, D Bausch, J Hoeppner (2014)
Cancer cell invasion and EMT marker expression: a three-dimensional study of the human cancer-host interfaceJ Pathol, 234
P Friedl, J Locker, E Sahai, JE Segall (2012)
Classifying collective cancer cell invasionNat Cell Biol, 14
T Schlange, Y Matsuda, S Lienhard, A Huber, NE Hynes (2007)
Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonical WNT pathway and EGFR transactivationBreast Cancer Res, 9
TE Anwar (2013)
1457Hum Pathol, 44
KJ Cheung (2013)
1639Cell, 155
Y Klymenko (2017)
549Neoplasia, 19
A Nagelkerke (2011)
39Radiother Oncol, 101
P Friedl (2009)
445Nat Rev Mol Cell Biol, 10
KJ Cheung, V Padmanaban, V Silvestri, K Schipper, JD Cohen, AN Fairchild, MA Gorin, JE Verdone, KJ Pienta, JS Bader (2016)
Polyclonal breast cancer metastases arise from collective dissemination of keratin 14-expressing tumor cell clustersProc Natl Acad Sci USA, 113
P Auvinen (2000)
529Am J Pathol, 156
LM Milstone (1994)
3183J Cell Sci, 107
PW Derksen, X Liu, F Saridin, H Gulden, J Zevenhoven, B Evers, JR Beijnum, AW Griffioen, J Vink, P Krimpenfort (2006)
Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesisCancer Cell, 10
A Nagelkerke, SJ Kuijk, FC Sweep, ID Nagtegaal, N Hoogerbrugge, JW Martens, MA Timmermans, HW Laarhoven, J Bussink, PN Span (2011)
Constitutive expression of gamma-H2AX has prognostic relevance in triple negative breast cancerRadiother Oncol, 101
M Reffay, MC Parrini, O Cochet-Escartin, B Ladoux, A Buguin, S Coscoy, F Amblard, J Camonis, P Silberzan (2014)
Interplay of RhoA and mechanical forces in collective cell migration driven by leader cellsNat Cell Biol, 16
J Yamaguchi, H Ohtani, K Nakamura, I Shimokawa, T Kanematsu (2008)
Prognostic impact of marginal adipose tissue invasion in ductal carcinoma of the breastAm J Clin Pathol, 130
Breast cancer undergoes collective tissue invasion and, in experimental models, can collectively metastasize. The prevalence of collective invasion and its contribution to distant metastasis in clinical disease, however, remains poorly defined. We here scored the adipose tissue invasion of primary invasive ductal carcinoma (IDC), expressing E-cadherin, and E-cadherin negative invasive lobular carcinoma (ILC) and identified predominantly collective invasion patterns (86/86 samples) in both carcinoma types. Whereas collective invasion in IDC lesions retained adherens junctions, multicellular clusters and “Indian files” in ILC, despite the absence of adherens junctions (AJ) proteins E-cadherin and β-catenin, retained CD44 at cell–cell contacts. By histomorphological scoring and semi-automated image analysis, we show that the extent of collective invasion into the adipose tissue correlated with decreased distant metastasis-free survival (5-year follow-up; hazard ratio: 2.32 and 2.29, respectively). Thus, collective invasion represents the predominant invasion mode in breast cancer, develops distinct junctional subtypes in IDC and ILC, and associates with distant metastasis, suggesting a critical role in systemic dissemination.
Clinical & Experimental Metastasis – Springer Journals
Published: Sep 11, 2017
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