. 2013 Dec;19(23).
doi: 10.1158/1078-0432.CCR-13-0838.

Metastasis dormancy in estrogen receptor-positive breast cancer

Xiang H-F Zhang 1 Mario Giuliano  Meghana V Trivedi  Rachel Schiff  C Kent Osborne  
  • PMID: 24298069
  •     61 References
  •     87 citations


About 20% to 40% of patients with breast cancer eventually develop recurrences in distant organs, which are often not detected until years to decades after the primary tumor diagnosis. This phenomenon is especially pronounced in estrogen receptor-positive (ER(+)) breast cancer, suggesting that ER(+) cancer cells may stay dormant for a protracted period of time, despite adjuvant therapies. Multiple mechanisms have been proposed to explain how cancer cells survive and remain in dormancy, and how they become reactivated and exit dormancy. These mechanisms include angiogenic switch, immunosurveillance, and interaction with extracellular matrix and stromal cells. How to eradicate or suppress these dormant cancer cells remains a major clinical issue because of the lack of knowledge about the biologic and clinical nature of these cells. Herein, we review the clinical manifestation of metastasis dormancy in ER(+) tumors, the current biologic insights regarding tumor dormancy obtained from various experimental models, and the clinical challenges to predict, detect, and treat dormant metastases. We also discuss future research directions toward a better understanding of the biologic mechanisms and clinical management of ER(+) dormant metastasis.

Gene expression profiling predicts clinical outcome of breast cancer.
Laura J van 't Veer, Hongyue Dai, +13 authors, Stephen H Friend.
Nature, 2002 Feb 02; 415(6871). PMID: 11823860
Highly Cited.
Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis.
Susan E Moody, Christopher J Sarkisian, +7 authors, Lewis A Chodosh.
Cancer Cell, 2002 Dec 25; 2(6). PMID: 12498714
Highly Cited.
Tumour cells in the tumour draining vein of patients with non-small cell lung cancer: detection rate and clinical significance.
Wulf Sienel, Rita Seen-Hibler, +2 authors, Bernward Passlick.
Eur J Cardiothorac Surg, 2003 Apr 16; 23(4). PMID: 12694758
Isolated tumor cells in bone marrow three years after diagnosis in disease-free breast cancer patients predict unfavorable clinical outcome.
Gro Wiedswang, Elin Borgen, +5 authors, Bjørn Naume.
Clin Cancer Res, 2004 Aug 26; 10(16). PMID: 15328170
Differential expression of proliferation-associated molecules in individual micrometastatic carcinoma cells.
K Pantel, G Schlimok, +6 authors, G Riethmüller.
J Natl Cancer Inst, 1993 Sep 01; 85(17). PMID: 7688814
Highly Cited.
Prediction of late disease recurrence and extended adjuvant letrozole benefit by the HOXB13/IL17BR biomarker.
Dennis C Sgroi, Erin Carney, +16 authors, Paul E Goss.
J Natl Cancer Inst, 2013 Jul 03; 105(14). PMID: 23812955    Free PMC article.
Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape.
Bradley N Bidwell, Clare Y Slaney, +15 authors, Belinda S Parker.
Nat Med, 2012 Jul 24; 18(8). PMID: 22820642
Highly Cited.
A renewable tissue resource of phenotypically stable, biologically and ethnically diverse, patient-derived human breast cancer xenograft models.
Xiaomei Zhang, Sofie Claerhout, +26 authors, Michael T Lewis.
Cancer Res, 2013 Jun 06; 73(15). PMID: 23737486    Free PMC article.
Highly Cited.
Can immunity to breast cancer eliminate residual micrometastases?
Mary L Disis, Sasha E Stanton.
Clin Cancer Res, 2013 Dec 04; 19(23). PMID: 24298070    Free PMC article.
Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy.
R Demicheli, A Abbattista, +2 authors, G Bonadonna.
Breast Cancer Res Treat, 1996 Jan 01; 41(2). PMID: 8944336
Dormancy of mammary carcinoma after mastectomy.
T G Karrison, D J Ferguson, P Meier.
J Natl Cancer Inst, 1999 Jan 16; 91(1). PMID: 9890174
Highly Cited.
Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials.
Early Breast Cancer Trialists' Collaborative Group (EBCTCG).
Lancet, 2005 May 17; 365(9472). PMID: 15894097
Highly Cited.
Randomized trial of letrozole following tamoxifen as extended adjuvant therapy in receptor-positive breast cancer: updated findings from NCIC CTG MA.17.
Paul E Goss, James N Ingle, +15 authors, Joseph L Pater.
J Natl Cancer Inst, 2005 Sep 08; 97(17). PMID: 16145047
Highly Cited.
The transcriptional repressor Snail promotes mammary tumor recurrence.
Susan E Moody, Denise Perez, +6 authors, Lewis A Chodosh.
Cancer Cell, 2005 Sep 20; 8(3). PMID: 16169465
Highly Cited.
VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.
Rosandra N Kaplan, Rebecca D Riba, +18 authors, David Lyden.
Nature, 2005 Dec 13; 438(7069). PMID: 16341007    Free PMC article.
Highly Cited.
Real-time RT-PCR detection of disseminated tumour cells in bone marrow has superior prognostic significance in comparison with circulating tumour cells in patients with breast cancer.
I H Benoy, H Elst, +6 authors, L Y Dirix.
Br J Cancer, 2006 Feb 24; 94(5). PMID: 16495933    Free PMC article.
Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer.
Soonmyung Paik, Gong Tang, +11 authors, Norman Wolmark.
J Clin Oncol, 2006 May 25; 24(23). PMID: 16720680
Highly Cited.
The HOXB13:IL17BR expression index is a prognostic factor in early-stage breast cancer.
Xiao-Jun Ma, Susan G Hilsenbeck, +6 authors, Mark G Erlander.
J Clin Oncol, 2006 Sep 30; 24(28). PMID: 17008703
A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes.
Richard M Neve, Koei Chin, +24 authors, Joe W Gray.
Cancer Cell, 2006 Dec 13; 10(6). PMID: 17157791    Free PMC article.
Highly Cited.
Models, mechanisms and clinical evidence for cancer dormancy.
Julio A Aguirre-Ghiso.
Nat Rev Cancer, 2007 Oct 25; 7(11). PMID: 17957189    Free PMC article.
Highly Cited. Review.
Adaptive immunity maintains occult cancer in an equilibrium state.
Catherine M Koebel, William Vermi, +5 authors, Robert D Schreiber.
Nature, 2007 Nov 21; 450(7171). PMID: 18026089
Highly Cited.
Extended adjuvant therapy with anastrozole among postmenopausal breast cancer patients: results from the randomized Austrian Breast and Colorectal Cancer Study Group Trial 6a.
Raimund Jakesz, Richard Greil, +12 authors, Austrian Breast and Colorectal Cancer Study Group.
J Natl Cancer Inst, 2007 Dec 13; 99(24). PMID: 18073378
Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis.
Dingcheng Gao, Daniel J Nolan, +3 authors, Vivek Mittal.
Science, 2008 Jan 12; 319(5860). PMID: 18187653
Highly Cited.
Benefit from exemestane as extended adjuvant therapy after 5 years of adjuvant tamoxifen: intention-to-treat analysis of the National Surgical Adjuvant Breast And Bowel Project B-33 trial.
Eleftherios P Mamounas, Jong-Hyeon Jeong, +17 authors, Norman Wolmark.
J Clin Oncol, 2008 Mar 12; 26(12). PMID: 18332472
Detection, clinical relevance and specific biological properties of disseminating tumour cells.
Klaus Pantel, Ruud H Brakenhoff, Burkhard Brandt.
Nat Rev Cancer, 2008 Apr 12; 8(5). PMID: 18404148
Highly Cited. Review.
The epithelial-mesenchymal transition generates cells with properties of stem cells.
Sendurai A Mani, Wenjun Guo, +12 authors, Robert A Weinberg.
Cell, 2008 May 20; 133(4). PMID: 18485877    Free PMC article.
Highly Cited.
Cellular interactions in the vascular niche: implications in the regulation of tumor dormancy.
Elena Favaro, Alberto Amadori, Stefano Indraccolo.
APMIS, 2008 Oct 07; 116(7-8). PMID: 18834409
Tumor dormancy and immunoescape.
Bruno Quesnel.
APMIS, 2008 Oct 07; 116(7-8). PMID: 18834412
Dormancy and surgery-driven escape from dormancy help explain some clinical features of breast cancer.
M W Retsky, R Demicheli, +2 authors, I D Gukas.
APMIS, 2008 Oct 07; 116(7-8). PMID: 18834415
Cancer micrometastasis and tumour dormancy.
Harriet Wikman, Robert Vessella, Klaus Pantel.
APMIS, 2008 Oct 07; 116(7-8). PMID: 18834417
Latent bone metastasis in breast cancer tied to Src-dependent survival signals.
Xiang H-F Zhang, Qiongqing Wang, +5 authors, Joan Massagué.
Cancer Cell, 2009 Jul 04; 16(1). PMID: 19573813    Free PMC article.
Highly Cited.
Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution.
Sohrab P Shah, Ryan D Morin, +27 authors, Samuel Aparicio.
Nature, 2009 Oct 09; 461(7265). PMID: 19812674
Highly Cited.
Molecular MRI for sensitive and specific detection of lung metastases.
Rosa T Branca, Zackary I Cleveland, +5 authors, Bastiaan Driehuys.
Proc Natl Acad Sci U S A, 2010 Feb 10; 107(8). PMID: 20142483    Free PMC article.
Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10,159 cases from 12 studies.
Fiona M Blows, Kristy E Driver, +40 authors, David Huntsman.
PLoS Med, 2010 Jun 04; 7(5). PMID: 20520800    Free PMC article.
Highly Cited.
A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer.
Torsten O Nielsen, Joel S Parker, +12 authors, Matthew J Ellis.
Clin Cancer Res, 2010 Sep 15; 16(21). PMID: 20837693    Free PMC article.
Highly Cited.
Genomic Grade Index: An important tool for assessing breast cancer tumor grade and prognosis.
Otto Metzger Filho, Michail Ignatiadis, Christos Sotiriou.
Crit Rev Oncol Hematol, 2010 Feb 09; 77(1). PMID: 20138540
Inactivation of p53 in breast cancers correlates with stem cell transcriptional signatures.
Hideaki Mizuno, Benjamin T Spike, Geoffrey M Wahl, Arnold J Levine.
Proc Natl Acad Sci U S A, 2010 Dec 15; 107(52). PMID: 21149740    Free PMC article.
Mechanisms of endocrine resistance in breast cancer.
C Kent Osborne, Rachel Schiff.
Annu Rev Med, 2010 Oct 05; 62. PMID: 20887199    Free PMC article.
Highly Cited. Review.
Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow.
Yusuke Shiozawa, Elisabeth A Pedersen, +14 authors, Russell S Taichman.
J Clin Invest, 2011 Mar 26; 121(4). PMID: 21436587    Free PMC article.
Highly Cited.
Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast.
Christina Scheel, Elinor Ng Eaton, +8 authors, Robert A Weinberg.
Cell, 2011 Jun 15; 145(6). PMID: 21663795    Free PMC article.
Highly Cited.
Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs.
Thordur Oskarsson, Swarnali Acharyya, +7 authors, Joan Massagué.
Nat Med, 2011 Jun 28; 17(7). PMID: 21706029    Free PMC article.
Highly Cited.
Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes.
Yoko S DeRose, Guoying Wang, +12 authors, Alana L Welm.
Nat Med, 2011 Oct 25; 17(11). PMID: 22019887    Free PMC article.
Highly Cited.
The prognostic significance of tumour cell detection in the peripheral blood versus the bone marrow in 733 early-stage breast cancer patients.
Timothy J Molloy, Astrid J Bosma, +6 authors, Bjørn Naume.
Breast Cancer Res, 2011 Jun 16; 13(3). PMID: 21672237    Free PMC article.
VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging α4β1-positive osteoclast progenitors.
Xin Lu, Euphemia Mu, +11 authors, Yibin Kang.
Cancer Cell, 2011 Dec 06; 20(6). PMID: 22137794    Free PMC article.
Highly Cited.
Interactions between cancer stem cells and their niche govern metastatic colonization.
Ilaria Malanchi, Albert Santamaria-Martínez, +4 authors, Joerg Huelsken.
Nature, 2011 Dec 14; 481(7379). PMID: 22158103
Highly Cited.
Deep time: the long and the short of adjuvant endocrine therapy for breast cancer.
Harold J Burstein, Jennifer J Griggs.
J Clin Oncol, 2012 Jan 25; 30(7). PMID: 22271478
Accessories to the crime: functions of cells recruited to the tumor microenvironment.
Douglas Hanahan, Lisa M Coussens.
Cancer Cell, 2012 Mar 24; 21(3). PMID: 22439926
Highly Cited. Review.
Dormancy signatures and metastasis in estrogen receptor positive and negative breast cancer.
Ryung S Kim, Alvaro Avivar-Valderas, +4 authors, Jeffrey E Segall.
PLoS One, 2012 Apr 25; 7(4). PMID: 22530051    Free PMC article.
Single cell profiling of circulating tumor cells: transcriptional heterogeneity and diversity from breast cancer cell lines.
Ashley A Powell, Amirali H Talasaz, +18 authors, Stefanie S Jeffrey.
PLoS One, 2012 May 16; 7(5). PMID: 22586443    Free PMC article.
Highly Cited.
Modeling of response to endocrine therapy in a panel of human luminal breast cancer xenografts.
P Cottu, E Marangoni, +14 authors, D Decaudin.
Breast Cancer Res Treat, 2011 Oct 18; 133(2). PMID: 22002565
The outgrowth of micrometastases is enabled by the formation of filopodium-like protrusions.
Tsukasa Shibue, Mary W Brooks, +2 authors, Robert A Weinberg.
Cancer Discov, 2012 May 23; 2(8). PMID: 22609699    Free PMC article.
Highly Cited.
The BMP inhibitor Coco reactivates breast cancer cells at lung metastatic sites.
Hua Gao, Goutam Chakraborty, +7 authors, Filippo G Giancotti.
Cell, 2012 Aug 21; 150(4). PMID: 22901808    Free PMC article.
Highly Cited.
The natural history of hormone receptor-positive breast cancer.
Elgene Lim, Otto Metzger-Filho, Eric P Winer.
Oncology (Williston Park), 2012 Sep 11; 26(8). PMID: 22957400
Biomarkers characterization of circulating tumour cells in breast cancer patients.
Rosa Nadal, Ana Fernandez, +12 authors, María José Serrano.
Breast Cancer Res, 2012 May 05; 14(3). PMID: 22554015    Free PMC article.
Mouse models of breast cancer metastasis to bone.
Kelsi L Kretschmann, Alana L Welm.
Cancer Metastasis Rev, 2012 Jun 19; 31(3-4). PMID: 22706780
Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition.
Min Yu, Aditya Bardia, +17 authors, Shyamala Maheswaran.
Science, 2013 Feb 02; 339(6119). PMID: 23372014    Free PMC article.
Highly Cited.
Analysis of circulating tumor DNA to monitor metastatic breast cancer.
Sarah-Jane Dawson, Dana W Y Tsui, +15 authors, Nitzan Rosenfeld.
N Engl J Med, 2013 Mar 15; 368(13). PMID: 23484797
Highly Cited.
Long-term effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial.
Christina Davies, Hongchao Pan, +36 authors, Adjuvant Tamoxifen: Longer Against Shorter (ATLAS) Collaborative Group.
Lancet, 2012 Dec 12; 381(9869). PMID: 23219286    Free PMC article.
Highly Cited.
The perivascular niche regulates breast tumour dormancy.
Cyrus M Ghajar, Héctor Peinado, +10 authors, Mina J Bissell.
Nat Cell Biol, 2013 Jun 04; 15(7). PMID: 23728425    Free PMC article.
Highly Cited.
Inhibition of ron kinase blocks conversion of micrometastases to overt metastases by boosting antitumor immunity.
Henok Eyob, Huseyin Atakan Ekiz, +3 authors, Alana L Welm.
Cancer Discov, 2013 Apr 25; 3(7). PMID: 23612011    Free PMC article.
Circulating tumour cells: insights into tumour heterogeneity.
D F Hayes, C Paoletti.
J Intern Med, 2013 Jul 13; 274(2). PMID: 23844916
miR-639 promotes the proliferation and invasion of breast cancer cell in vitro.
Lin Li, Xin-Guang Qiu, Peng-Wei Lv, Fang Wang.
Cancer Cell Int, 2014 Jun 12; 14. PMID: 24917697    Free PMC article.
Upregulation of miR-301a correlates with poor prognosis in triple-negative breast cancer.
Hong Yu, Hui Li, +5 authors, Junxing Huang.
Med Oncol, 2014 Oct 15; 31(11). PMID: 25311065
FOSL2 positively regulates TGF-β1 signalling in non-small cell lung cancer.
Junfeng Wang, Dawei Sun, +4 authors, Shidong Xu.
PLoS One, 2014 Nov 07; 9(11). PMID: 25375657    Free PMC article.
Luminal breast cancer metastases and tumor arousal from dormancy are promoted by direct actions of estradiol and progesterone on the malignant cells.
Ndiya Ogba, Nicole G Manning, +7 authors, Kathryn B Horwitz.
Breast Cancer Res, 2014 Dec 06; 16(6). PMID: 25475897    Free PMC article.
Markers for the identification of late breast cancer recurrence.
Ivana Sestak, Jack Cuzick.
Breast Cancer Res, 2015 Apr 08; 17. PMID: 25848913    Free PMC article.
Potential clinical relevance of uPA and PAI-1 levels in node-negative, postmenopausal breast cancer patients bearing histological grade II tumors with ER/PR expression, during an early follow-up.
Marko Buta, Radan Džodić, +4 authors, Dragica Nikolić-Vukosavljević.
Tumour Biol, 2015 May 23; 36(10). PMID: 25994573
The GALNT9, BNC1 and CCDC8 genes are frequently epigenetically dysregulated in breast tumours that metastasise to the brain.
Rajendra P Pangeni, Prasanna Channathodiyil, +22 authors, Mark R Morris.
Clin Epigenetics, 2015 Jun 09; 7. PMID: 26052355    Free PMC article.
New Insights on COX-2 in Chronic Inflammation Driving Breast Cancer Growth and Metastasis.
Honor J Hugo, C Saunders, R G Ramsay, E W Thompson.
J Mammary Gland Biol Neoplasia, 2015 Jul 22; 20(3-4). PMID: 26193871
Role of the short isoform of the progesterone receptor in breast cancer cell invasiveness at estrogen and progesterone levels in the pre- and post-menopausal ranges.
Thomas McFall, Mugdha Patki, Rayna Rosati, Manohar Ratnam.
Oncotarget, 2015 Sep 12; 6(32). PMID: 26356672    Free PMC article.
Targeting Breast Cancer Metastasis.
Xin Jin, Ping Mu.
Breast Cancer (Auckl), 2015 Sep 19; 9(Suppl 1). PMID: 26380552    Free PMC article.
Modeling selective elimination of quiescent cancer cells from bone marrow.
Stephen P Cavnar, Andrew D Rickelmann, +8 authors, Gary D Luker.
Neoplasia, 2015 Sep 27; 17(8). PMID: 26408255    Free PMC article.
Oestrogen receptor positive breast cancer metastasis to bone: inhibition by targeting the bone microenvironment in vivo.
I Holen, M Walker, +4 authors, P D Ottewell.
Clin Exp Metastasis, 2015 Nov 21; 33(3). PMID: 26585891
ΔNp63α induces quiescence and downregulates the BRCA1 pathway in estrogen receptor-positive luminal breast cancer cell line MCF7 but not in other breast cancer cell lines.
Ruhul Amin, Yuiko Morita-Fujimura, +4 authors, Shuntaro Ikawa.
Mol Oncol, 2015 Dec 26; 10(4). PMID: 26704768    Free PMC article.
Annual Hazard Rates of Recurrence for Breast Cancer During 24 Years of Follow-Up: Results From the International Breast Cancer Study Group Trials I to V.
Marco Colleoni, Zhuoxin Sun, +8 authors, Aron Goldhirsch.
J Clin Oncol, 2016 Jan 21; 34(9). PMID: 26786933    Free PMC article.
Highly Cited.
Estrogen Enhances the Cell Viability and Motility of Breast Cancer Cells through the ERα-ΔNp63-Integrin β4 Signaling Pathway.
Jar-Yi Ho, Fung-Wei Chang, +7 authors, Ren-Jun Hsu.
PLoS One, 2016 Feb 06; 11(2). PMID: 26845172    Free PMC article.
Estrogen Receptor Status Predicts Late-Onset Skeletal Recurrence in Breast Cancer Patients.
Hyun Ho Han, Sung Hwan Lee, +3 authors, Nam Hoon Cho.
Medicine (Baltimore), 2016 Mar 05; 95(8). PMID: 26937933    Free PMC article.
Dynamic interplay between adhesion surfaces in carcinomas: Cell-cell and cell-matrix crosstalk.
Yvonne E Smith, Sri HariKrishna Vellanki, Ann M Hopkins.
World J Biol Chem, 2016 Mar 17; 7(1). PMID: 26981196    Free PMC article.
Causal Therapy of Breast Cancer Irrelevant of Age, Tumor Stage and ER-Status: Stimulation of Estrogen Signaling Coupled With Breast Conserving Surgery.
Zsuzsanna Suba.
Recent Pat Anticancer Drug Discov, 2016 Apr 19; 11(3). PMID: 27087654    Free PMC article.
Personalized in vitro cancer models to predict therapeutic response: Challenges and a framework for improvement.
Molly M Morgan, Brian P Johnson, +4 authors, David J Beebe.
Pharmacol Ther, 2016 May 25; 165. PMID: 27218886    Free PMC article.
Late recurrence of breast carcinoma metastasis to the hypopharynx: a case report.
Chisako Izumi, Kiyoshi Misawa, +7 authors, Hiroyuki Mineta.
Springerplus, 2016 Jun 02; 5. PMID: 27247895    Free PMC article.
Angiopoietin-2 promotes ER+ breast cancer cell survival in bone marrow niche.
Hyun Ho Han, Baek Gil Kim, +3 authors, Nam Hoon Cho.
Endocr Relat Cancer, 2016 Jun 30; 23(8). PMID: 27353038    Free PMC article.
Novel ERα positive breast cancer model with estrogen independent growth in the bone microenvironment.
Aude-Hélène Capietto, Szeman Ruby Chan, +5 authors, Roberta Faccio.
Oncotarget, 2016 Jul 09; 7(31). PMID: 27391074    Free PMC article.
Breast cancer epidemic in the early twenty-first century: evaluation of risk factors, cumulative questionnaires and recommendations for preventive measures.
Olga Golubnitschaja, Manuel Debald, +4 authors, Godfrey Grech.
Tumour Biol, 2016 Jul 23; 37(10). PMID: 27448308
Highly Cited. Review.
Similar lymphocytic infiltration pattern in primary breast cancer and their corresponding distant metastases.
Bettina Sobottka, Bernhard Pestalozzi, +2 authors, Zsuzsanna Varga.
Oncoimmunology, 2016 Jul 30; 5(6). PMID: 27471624    Free PMC article.
Nuclear respiratory factor-1 and bioenergetics in tamoxifen-resistant breast cancer cells.
Brandie N Radde, Margarita M Ivanova, +9 authors, Carolyn M Klinge.
Exp Cell Res, 2016 Aug 16; 347(1). PMID: 27515002    Free PMC article.
Liver metastatic disease: new concepts and biomarker panels to improve individual outcomes.
Olga Golubnitschaja, Krishna Chander Sridhar.
Clin Exp Metastasis, 2016 Aug 20; 33(8). PMID: 27541751
Tumor cell dormancy.
Roger R Gomis, Sylwia Gawrzak.
Mol Oncol, 2016 Dec 27; 11(1). PMID: 28017284    Free PMC article.
Estrogen receptors in breast and bone: from virtue of remodeling to vileness of metastasis.
I Bado, Z Gugala, S A W Fuqua, X H-F Zhang.
Oncogene, 2017 Apr 04; 36(32). PMID: 28368409    Free PMC article.
In vivo models in breast cancer research: progress, challenges and future directions.
Ingunn Holen, Valerie Speirs, Bethny Morrissey, Karen Blyth.
Dis Model Mech, 2017 Apr 07; 10(4). PMID: 28381598    Free PMC article.
Bone morphogenetic proteins, breast cancer, and bone metastases: striking the right balance.
Catherine Zabkiewicz, Jeyna Resaul, +2 authors, Lin Ye.
Endocr Relat Cancer, 2017 Jul 25; 24(10). PMID: 28733469    Free PMC article.
Exome-capture RNA sequencing of decade-old breast cancers and matched decalcified bone metastases.
Nolan Priedigkeit, Rebecca J Watters, +10 authors, Adrian V Lee.
JCI Insight, 2017 Sep 08; 2(17). PMID: 28878133    Free PMC article.
Extended Adjuvant Endocrine Therapy for Postmenopausal Women: Treating Many to Benefit a Few.
Paula R Pohlmann, Claudine Isaacs.
J Natl Cancer Inst, 2017 Sep 20; 110(1). PMID: 28922782    Free PMC article.
Long non-coding RNA00544 serves as a potential novel predictive and prognostic marker for HR+ HER2- subtype breast cancer.
Lei Liu, Yayun Chi, +5 authors, Jiong Wu.
Sci Rep, 2017 Sep 30; 7(1). PMID: 28959047    Free PMC article.
A Facile, In Vitro 384-Well Plate System to Model Disseminated Tumor Cells in the Bone Marrow Microenvironment.
Johanna M Buschhaus, Kathryn E Luker, Gary D Luker.
Methods Mol Biol, 2017 Oct 17; 1686. PMID: 29030823    Free PMC article.
Hallmarks of Bone Metastasis.
Rachelle W Johnson, Larry J Suva.
Calcif Tissue Int, 2017 Nov 16; 102(2). PMID: 29138883    Free PMC article.
Progesterone receptor A promotes invasiveness and metastasis of luminal breast cancer by suppressing regulation of critical microRNAs by estrogen.
Thomas McFall, Brooke McKnight, +4 authors, Manohar Ratnam.
J Biol Chem, 2017 Nov 23; 293(4). PMID: 29162724    Free PMC article.
Coactivation of Estrogen Receptor and IKKβ Induces a Dormant Metastatic Phenotype in ER-Positive Breast Cancer.
Lamiaa El-Shennawy, Oleksii Dubrovskyi, +5 authors, Jonna Frasor.
Cancer Res, 2017 Dec 13; 78(4). PMID: 29229606    Free PMC article.
Extracting microtentacle dynamics of tumor cells in a non-adherent environment.
Eleanor C Ory, Desu Chen, +5 authors, Stuart S Martin.
Oncotarget, 2018 Jan 18; 8(67). PMID: 29340075    Free PMC article.
Intratumor Heterogeneity of the Estrogen Receptor and the Long-term Risk of Fatal Breast Cancer.
Linda S Lindström, Christina Yau, +19 authors, STO Trialists Group.
J Natl Cancer Inst, 2018 Jan 24; 110(7). PMID: 29361175    Free PMC article.
Bone metastasis pattern in initial metastatic breast cancer: a population-based study.
Zhenchong Xiong, Guangzheng Deng, +5 authors, Xi Wang.
Cancer Manag Res, 2018 Feb 23; 10. PMID: 29467583    Free PMC article.
Modeling treatment-dependent glioma growth including a dormant tumor cell subpopulation.
Marvin A Böttcher, Janka Held-Feindt, +3 authors, Kirsten Hattermann.
BMC Cancer, 2018 Apr 05; 18(1). PMID: 29614985    Free PMC article.
Optimal management of luminal breast cancer: how much endocrine therapy is long enough?
Elisabetta Munzone, Marco Colleoni.
Ther Adv Med Oncol, 2018 Jul 07; 10. PMID: 29977350    Free PMC article.
The actin cytoskeletal architecture of estrogen receptor positive breast cancer cells suppresses invasion.
Marco Padilla-Rodriguez, Sara S Parker, +11 authors, Ghassan Mouneimne.
Nat Commun, 2018 Aug 01; 9(1). PMID: 30061623    Free PMC article.
Disrupting a negative feedback loop drives endocrine therapy-resistant breast cancer.
Charles E Foulds.
Proc Natl Acad Sci U S A, 2018 Aug 08; 115(33). PMID: 30082387    Free PMC article.
Reawakening of dormant estrogen-dependent human breast cancer cells by bone marrow stroma secretory senescence.
Samir Tivari, Haiyan Lu, +2 authors, Robert Wieder.
Cell Commun Signal, 2018 Aug 19; 16(1). PMID: 30119678    Free PMC article.
Ribociclib for the first-line treatment of advanced hormone receptor-positive breast cancer: a review of subgroup analyses from the MONALEESA-2 trial.
Gabriel N Hortobagyi.
Breast Cancer Res, 2018 Oct 21; 20(1). PMID: 30340505    Free PMC article.
The Osteogenic Niche Is a Calcium Reservoir of Bone Micrometastases and Confers Unexpected Therapeutic Vulnerability.
Hai Wang, Lin Tian, +12 authors, Xiang H-F Zhang.
Cancer Cell, 2018 Nov 14; 34(5). PMID: 30423299    Free PMC article.
Extended duration of adjuvant aromatase inhibitor in breast cancer: a meta-analysis of randomized controlled trials.
Zackariah Clement, James Kollias, +2 authors, Melissa Bochner.
Gland Surg, 2018 Dec 07; 7(5). PMID: 30505766    Free PMC article.
Late recurrence of breast cancer is associated with pro-cancerous immune microenvironment in the primary tumor.
Takashi Takeshita, Li Yan, +2 authors, Kazuaki Takabe.
Sci Rep, 2019 Nov 16; 9(1). PMID: 31729458    Free PMC article.
RNA-seq from archival FFPE breast cancer samples: molecular pathway fidelity and novel discovery.
Nathan D Pennock, Sonali Jindal, +10 authors, Zheng Xia.
BMC Med Genomics, 2019 Dec 21; 12(1). PMID: 31856832    Free PMC article.
Interleukin-23 receptor signaling mediates cancer dormancy and radioresistance in human esophageal squamous carcinoma cells via the Wnt/Notch pathway.
Yuepeng Zhou, Yuting Su, +7 authors, Deyu Chen.
J Mol Med (Berl), 2018 Nov 30; 97(2). PMID: 30483821    Free PMC article.
Molecular changes during extended neoadjuvant letrozole treatment of breast cancer: distinguishing acquired resistance from dormant tumours.
Cigdem Selli, Arran K Turnbull, +7 authors, Andrew H Sims.
Breast Cancer Res, 2019 Jan 09; 21(1). PMID: 30616553    Free PMC article.
Identification of Genes Regulating Breast Cancer Dormancy in 3D Bone Endosteal Niche Cultures.
Julie McGrath, Louis Panzica, +2 authors, Irwin H Gelman.
Mol Cancer Res, 2019 Jan 18; 17(4). PMID: 30651373    Free PMC article.
Osteoblasts are "educated" by crosstalk with metastatic breast cancer cells in the bone tumor microenvironment.
Alexus D Kolb, Alison B Shupp, +2 authors, Karen M Bussard.
Breast Cancer Res, 2019 Mar 01; 21(1). PMID: 30813947    Free PMC article.
Mesenchymal stem cell-derived extracellular vesicles may promote breast cancer cell dormancy.
Jake Casson, Owen G Davies, +2 authors, Catherine C Berry.
J Tissue Eng, 2019 Jan 11; 9. PMID: 30627418    Free PMC article.
Implication of environmental estrogens on breast cancer treatment and progression.
Thomas L Gonzalez, James M Rae, Justin A Colacino.
Toxicology, 2019 Apr 04; 421. PMID: 30940549    Free PMC article.
A framework for the development of effective anti-metastatic agents.
Robin L Anderson, Theo Balasas, +16 authors, Cancer Research UK and Cancer Therapeutics CRC Australia Metastasis Working Group.
Nat Rev Clin Oncol, 2018 Dec 06; 16(3). PMID: 30514977    Free PMC article.
Highly Cited.
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Ariella B Hanker, Dhivya R Sudhan, Carlos L Arteaga.
Cancer Cell, 2020 Apr 15; 37(4). PMID: 32289273    Free PMC article.
CPNE1 predicts poor prognosis and promotes tumorigenesis and radioresistance via the AKT singling pathway in triple-negative breast cancer.
Zhihong Shao, Xiaolong Ma, +6 authors, Xiaolong Gao.
Mol Carcinog, 2020 Mar 18; 59(5). PMID: 32181526    Free PMC article.
Factors associated with prolonged overall survival in patients with postmenopausal estrogen receptor-positive advanced breast cancer using real-world data: a follow-up analysis of the JBCRG-C06 Safari study.
Hidetoshi Kawaguchi, Norikazu Masuda, +20 authors, Shinji Ohno.
Breast Cancer, 2019 Dec 08; 27(3). PMID: 31811519    Free PMC article.
TIE2 Induces Breast Cancer Cell Dormancy and Inhibits the Development of Osteolytic Bone Metastases.
Florian Drescher, Patricia Juárez, +5 authors, Pierrick Gj Fournier.
Cancers (Basel), 2020 Apr 09; 12(4). PMID: 32260072    Free PMC article.
ERα-36 regulates progesterone receptor activity in breast cancer.
Henri-Philippe Konan, Loay Kassem, +8 authors, Muriel Le Romancer.
Breast Cancer Res, 2020 May 21; 22(1). PMID: 32429997    Free PMC article.
Clinical association of progesterone receptor isoform A with breast cancer metastasis consistent with its unique mechanistic role in preclinical models.
Rayna Rosati, Kailey Oppat, +2 authors, Manohar Ratnam.
BMC Cancer, 2020 Jun 05; 20(1). PMID: 32493230    Free PMC article.
High Expression of miR-34a Associated with Less Aggressive Cancer Biology but Not with Survival in Breast Cancer.
Yoshihisa Tokumaru, Eriko Katsuta, +8 authors, Kazuaki Takabe.
Int J Mol Sci, 2020 May 03; 21(9). PMID: 32357442    Free PMC article.
Targeting disseminated estrogen-receptor-positive breast cancer cells in bone marrow.
Johanna M Buschhaus, Brock A Humphries, +7 authors, Gary D Luker.
Oncogene, 2020 Jul 18; 39(34). PMID: 32678295    Free PMC article.
Transcription Factors in Cancer Development and Therapy.
Kanchan Vishnoi, Navin Viswakarma, Ajay Rana, Basabi Rana.
Cancers (Basel), 2020 Aug 23; 12(8). PMID: 32824207    Free PMC article.
Long non-coding NR2F1-AS1 is associated with tumor recurrence in estrogen receptor-positive breast cancers.
Anna Sanchez Calle, Tomofumi Yamamoto, +8 authors, Yusuke Yamamoto.
Mol Oncol, 2020 May 12; 14(9). PMID: 32392629    Free PMC article.
Transcriptomic and functional pathway features were associated with survival after pathological complete response to neoadjuvant chemotherapy in breast cancer.
Takashi Takeshita, Li Yan, +5 authors, Kazuaki Takabe.
Am J Cancer Res, 2020 Sep 10; 10(8). PMID: 32905537    Free PMC article.
Engineered In Vitro Models of Tumor Dormancy and Reactivation.
Shantanu Pradhan, John L Sperduto, Cindy J Farino, John H Slater.
J Biol Eng, 2019 Jan 04; 12. PMID: 30603045    Free PMC article.
Neoadjuvant Therapy for Breast Cancer as a Model for Translational Research.
Cigdem Selli, Andrew H Sims.
Breast Cancer (Auckl), 2019 Mar 01; 13. PMID: 30814840    Free PMC article.
Cytoplasmic HAX1 Is an Independent Risk Factor for Breast Cancer Metastasis.
Alicja Trebinska-Stryjewska, Lukasz Szafron, +7 authors, Ewa A Grzybowska.
J Oncol, 2019 May 17; 2019. PMID: 31093284    Free PMC article.
Dural and Leptomeningeal Spine Metastases of Breast Cancer.
Fernando Matos, Luís Cerqueira.
Case Rep Radiol, 2019 Jul 06; 2019. PMID: 31275688    Free PMC article.
The Central Contributions of Breast Cancer Stem Cells in Developing Resistance to Endocrine Therapy in Estrogen Receptor (ER)-Positive Breast Cancer.
David Rodriguez, Marc Ramkairsingh, +3 authors, Damu Tang.
Cancers (Basel), 2019 Jul 25; 11(7). PMID: 31336602    Free PMC article.
Early Prediction of Tumor Response to Neoadjuvant Chemotherapy and Clinical Outcome in Breast Cancer Using a Novel FDG-PET Parameter for Cancer Stem Cell Metabolism.
Chanwoo Kim, Sang-Ah Han, +2 authors, Deog Yoon Kim.
J Pers Med, 2020 Sep 23; 10(3). PMID: 32957507    Free PMC article.
MYC Targets Scores Are Associated with Cancer Aggressiveness and Poor Survival in ER-Positive Primary and Metastatic Breast Cancer.
Amy Schulze, Masanori Oshi, Itaru Endo, Kazuaki Takabe.
Int J Mol Sci, 2020 Nov 05; 21(21). PMID: 33143224    Free PMC article.
How to Predict Metastasis in Luminal Breast Cancer? Current Solutions and Future Prospects.
Sylwia Tabor, Małgorzata Szostakowska-Rodzos, Anna Fabisiewicz, Ewa A Grzybowska.
Int J Mol Sci, 2020 Nov 14; 21(21). PMID: 33182512    Free PMC article.
Technical Advancements for Studying Immune Regulation of Disseminated Dormant Cancer Cells.
Luigi Ombrato, Marco Montagner.
Front Oncol, 2020 Dec 01; 10. PMID: 33251149    Free PMC article.
Small molecule tyrosine kinase inhibitors of ErbB2/HER2/Neu in the treatment of aggressive breast cancer.
Richard L Schroeder, Cheryl L Stevens, Jayalakshmi Sridhar.
Molecules, 2014 Sep 25; 19(9). PMID: 25251190    Free PMC article.
The role of PIP5K1α/pAKT and targeted inhibition of growth of subtypes of breast cancer using PIP5K1α inhibitor.
Martuza Sarwar, Azharuddin Sajid Syed Khaja, +10 authors, Jenny L Persson.
Oncogene, 2018 Aug 15; 38(3). PMID: 30104711    Free PMC article.
Resistance to endocrine therapy in breast cancer: molecular mechanisms and future goals.
Małgorzata Szostakowska, Alicja Trębińska-Stryjewska, Ewa Anna Grzybowska, Anna Fabisiewicz.
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Response to First-line Recurrence Treatment Influences Survival in Hormone Receptor-positive, HER2-negative Breast Cancer: A Multicenter Study.
Jun Yamamura, Shunji Kamigaki, +9 authors, Yoshifumi Komoike.
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Oestrogen Non-Genomic Signalling is Activated in Tamoxifen-Resistant Breast Cancer.
Coralie Poulard, Julien Jacquemetton, +6 authors, Muriel Le Romancer.
Int J Mol Sci, 2019 Jun 15; 20(11). PMID: 31195751    Free PMC article.
Understanding ER+ Breast Cancer Dormancy Using Bioinspired Synthetic Matrices for Long-Term 3D Culture and Insights into Late Recurrence.
Elisa M Ovadia, Lina Pradhan, +8 authors, April M Kloxin.
Adv Biosyst, 2020 Jul 01; 4(9). PMID: 32603024    Free PMC article.
A Case of Pulmonary Metastasis of Breast Cancer 23 Years after Surgery Accompanied with Non-Tuberculous Mycobacterium Infection.
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'Educated' Osteoblasts Reduce Osteoclastogenesis in a Bone-Tumor Mimetic Microenvironment.
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Aromatase and CDK4/6 Inhibitor-Induced Musculoskeletal Symptoms: A Systematic Review.
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Crosstalk with lung epithelial cells regulates Sfrp2-mediated latency in breast cancer dissemination.
Marco Montagner, Rahul Bhome, +9 authors, Erik Sahai.
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