Review
. 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  
Affiliations
  • PMID: 24298069
  •     61 References
  •     87 citations

Abstract

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.

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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.
Review.
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.
Overcoming Endocrine Resistance in Breast Cancer.
Ariella B Hanker, Dhivya R Sudhan, Carlos L Arteaga.
Cancer Cell, 2020 Apr 15; 37(4). PMID: 32289273    Free PMC article.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Review.
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.
Breast Cancer Res Treat, 2018 Nov 02; 173(3). PMID: 30382472    Free PMC article.
Review.
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.
In Vivo, 2018 Dec 28; 33(1). PMID: 30587637    Free PMC article.
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.
Yuki Yabuuchi, Takayuki Nakagawa, +17 authors, Yuko Minami.
Case Rep Oncol, 2021 Jan 15; 13(3). PMID: 33442355    Free PMC article.
'Educated' Osteoblasts Reduce Osteoclastogenesis in a Bone-Tumor Mimetic Microenvironment.
Alexus D Kolb, Jinlu Dai, Evan T Keller, Karen M Bussard.
Cancers (Basel), 2021 Jan 16; 13(2). PMID: 33445695    Free PMC article.
Aromatase and CDK4/6 Inhibitor-Induced Musculoskeletal Symptoms: A Systematic Review.
Angeliki Andrikopoulou, Oraianthi Fiste, +2 authors, Flora Zagouri.
Cancers (Basel), 2021 Feb 04; 13(3). PMID: 33530456    Free PMC article.
Review.
Crosstalk with lung epithelial cells regulates Sfrp2-mediated latency in breast cancer dissemination.
Marco Montagner, Rahul Bhome, +9 authors, Erik Sahai.
Nat Cell Biol, 2020 Feb 26; 22(3). PMID: 32094692