Review
. 2016 Apr;129(9).
doi: 10.1242/jcs.183129.

Signatures of breast cancer metastasis at a glance

George S Karagiannis 1 Sumanta Goswami 1 Joan G Jones 2 Maja H Oktay 3 John S Condeelis 4 
Affiliations
  • PMID: 27084578
  •     114 References
  •     30 citations

Abstract

Gene expression profiling has yielded expression signatures from which prognostic tests can be derived to facilitate clinical decision making in breast cancer patients. Some of these signatures are based on profiling of whole tumor tissue (tissue signatures), which includes all tumor and stromal cells. Prognostic markers have also been derived from the profiling of metastasizing tumor cells, including circulating tumor cells (CTCs) and migratory-disseminating tumor cells within the primary tumor. The metastasis signatures based on CTCs and migratory-disseminating tumor cells have greater potential for unraveling cell biology insights and mechanistic underpinnings of tumor cell dissemination and metastasis. Of clinical interest is the promise that stratification of patients into high or low metastatic risk, as well as assessing the need for cytotoxic therapy, might be improved if prognostics derived from these two types of signatures are used in a combined way. The aim of this Cell Science at a Glance article and accompanying poster is to navigate through both types of signatures and their derived prognostics, as well as to highlight biological insights and clinical applications that could be derived from them, especially when they are used in combination.

Keywords: CTC; Chemotaxis; Circulating tumor cell; HIS; Human invasion signature; Intravasation; Invadopodia; Mena; TMEM; Tumor microenvironment of metastasis.

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Irène Baccelli, Andreas Schneeweiss, +16 authors, Andreas Trumpp.
Nat Biotechnol, 2013 Apr 24; 31(6). PMID: 23609047
Highly Cited.
Single-cell analysis reveals a stem-cell program in human metastatic breast cancer cells.
Devon A Lawson, Nirav R Bhakta, +10 authors, Zena Werb.
Nature, 2015 Sep 30; 526(7571). PMID: 26416748    Free PMC article.
Highly Cited.
Ki67 measured in metastatic tissue and prognosis in patients with advanced breast cancer.
Claudette Falato, Julie Lorent, +4 authors, Theodoros Foukakis.
Breast Cancer Res Treat, 2014 Aug 19; 147(2). PMID: 25129344
Prospective Validation of a 21-Gene Expression Assay in Breast Cancer.
Joseph A Sparano, Robert J Gray, +28 authors, George W Sledge.
N Engl J Med, 2015 Sep 29; 373(21). PMID: 26412349    Free PMC article.
Highly Cited.
IMP1, an mRNA binding protein that reduces the metastatic potential of breast cancer in a mouse model.
Chiso U Nwokafor, Rani S Sellers, Robert H Singer.
Oncotarget, 2016 Sep 23; 7(45). PMID: 27655671    Free PMC article.
MenaINV dysregulates cortactin phosphorylation to promote invadopodium maturation.
Maxwell D Weidmann, Chinmay R Surve, +4 authors, John S Condeelis.
Sci Rep, 2016 Nov 09; 6. PMID: 27824079    Free PMC article.
Macrophage-dependent tumor cell transendothelial migration is mediated by Notch1/MenaINV-initiated invadopodium formation.
Jeanine Pignatelli, Jose Javier Bravo-Cordero, +9 authors, John S Condeelis.
Sci Rep, 2016 Dec 03; 6. PMID: 27901093    Free PMC article.
Apoptosis-linked gene 2 promotes breast cancer growth and metastasis by regulating the cytoskeleton.
Juan Qin, Dengwen Li, +7 authors, Jun Zhou.
Oncotarget, 2016 Dec 08; 8(2). PMID: 27926525    Free PMC article.
Tumor Cell Invadopodia: Invasive Protrusions that Orchestrate Metastasis.
Robert J Eddy, Maxwell D Weidmann, Ved P Sharma, John S Condeelis.
Trends Cell Biol, 2017 Apr 17; 27(8). PMID: 28412099    Free PMC article.
Highly Cited. Review.
Neoadjuvant chemotherapy induces breast cancer metastasis through a TMEM-mediated mechanism.
George S Karagiannis, Jessica M Pastoriza, +13 authors, Maja H Oktay.
Sci Transl Med, 2017 Jul 07; 9(397). PMID: 28679654    Free PMC article.
Highly Cited.
The Selective Tie2 Inhibitor Rebastinib Blocks Recruitment and Function of Tie2Hi Macrophages in Breast Cancer and Pancreatic Neuroendocrine Tumors.
Allison S Harney, George S Karagiannis, +17 authors, John S Condeelis.
Mol Cancer Ther, 2017 Aug 26; 16(11). PMID: 28838996    Free PMC article.
Effects of FSTL1 on the proliferation and motility of breast cancer cells and vascular endothelial cells.
Yang Yang, Tianhao Mu, +4 authors, Dengwen Li.
Thorac Cancer, 2017 Sep 01; 8(6). PMID: 28857515    Free PMC article.
A metastasis biomarker (MetaSite Breast™ Score) is associated with distant recurrence in hormone receptor-positive, HER2-negative early-stage breast cancer.
Joseph A Sparano, Robert Gray, +13 authors, Joan Jones.
NPJ Breast Cancer, 2017 Nov 16; 3. PMID: 29138761    Free PMC article.
Chemotherapy-induced metastasis: mechanisms and translational opportunities.
George S Karagiannis, John S Condeelis, Maja H Oktay.
Clin Exp Metastasis, 2018 Jan 08; 35(4). PMID: 29307118    Free PMC article.
Review.
Chemotherapy-induced metastasis in breast cancer.
George S Karagiannis, John S Condeelis, Maja H Oktay.
Oncotarget, 2018 Jan 18; 8(67). PMID: 29340008    Free PMC article.
The Different Routes to Metastasis via Hypoxia-Regulated Programs.
Ana Rita Nobre, David Entenberg, +2 authors, Julio A Aguirre-Ghiso.
Trends Cell Biol, 2018 Jul 26; 28(11). PMID: 30041830    Free PMC article.
Review.
Development of a Novel Proteomic Risk-Classifier for Prognostication of Patients With Early-Stage Hormone Receptor-Positive Breast Cancer.
Charusheila Ramkumar, Ljubomir Buturovic, +7 authors, Manjiri M Bakre.
Biomark Insights, 2018 Aug 08; 13. PMID: 30083053    Free PMC article.
The emerging roles of macrophages in cancer metastasis and response to chemotherapy.
Luis Rivera Sanchez, Lucia Borriello, +3 authors, George S Karagiannis.
J Leukoc Biol, 2019 Feb 06; 106(2). PMID: 30720887    Free PMC article.
Review.
Assessing Tumor Microenvironment of Metastasis Doorway-Mediated Vascular Permeability Associated with Cancer Cell Dissemination using Intravital Imaging and Fixed Tissue Analysis.
George S Karagiannis, Jessica M Pastoriza, +5 authors, David Entenberg.
J Vis Exp, 2019 Jul 16; (148). PMID: 31305525    Free PMC article.
Identification of Alternatively-Activated Pathways between Primary Breast Cancer and Liver Metastatic Cancer Using Microarray Data.
Limei Wang, Jin Li, +9 authors, Lang Li.
Genes (Basel), 2019 Sep 29; 10(10). PMID: 31557971    Free PMC article.
The Regulatory Role of MicroRNAs in Breast Cancer.
Hui-Yi Loh, Brendan P Norman, +3 authors, Mohd Azuraidi Osman.
Int J Mol Sci, 2019 Oct 09; 20(19). PMID: 31590453    Free PMC article.
Review.
Tumor Microenvironment of Metastasis (TMEM) Doorways Are Restricted to the Blood Vessel Endothelium in Both Primary Breast Cancers and Their Lymph Node Metastases.
Paula S Ginter, George S Karagiannis, +4 authors, Maja H Oktay.
Cancers (Basel), 2019 Oct 11; 11(10). PMID: 31597373    Free PMC article.
Establishment and Characterization of a CTC Cell Line from Peripheral Blood of Breast Cancer Patient.
Pan Zhao, Wenbin Zhou, +12 authors, Chang Zou.
J Cancer, 2019 Nov 26; 10(24). PMID: 31762819    Free PMC article.
Chemotherapy-Induced Metastasis: Molecular Mechanisms, Clinical Manifestations, Therapeutic Interventions.
George S Karagiannis, John S Condeelis, Maja H Oktay.
Cancer Res, 2019 Aug 23; 79(18). PMID: 31431464    Free PMC article.
Review.
Gauging the Impact of Cancer Treatment Modalities on Circulating Tumor Cells (CTCs).
Trevor J Mathias, Katarina T Chang, Stuart S Martin, Michele I Vitolo.
Cancers (Basel), 2020 Apr 05; 12(3). PMID: 32245166    Free PMC article.
Review.
The stressful tumour environment drives plasticity of cell migration programmes, contributing to metastasis.
Savvas Nikolaou, Laura M Machesky.
J Pathol, 2020 Feb 15; 250(5). PMID: 32057095    Free PMC article.
Review.
Validation of an Automated Quantitative Digital Pathology Approach for Scoring TMEM, a Prognostic Biomarker for Metastasis.
David Entenberg, Maja H Oktay, +7 authors, John S Condeelis.
Cancers (Basel), 2020 Apr 05; 12(4). PMID: 32244564    Free PMC article.
Influence of Fibroblasts on Mammary Gland Development, Breast Cancer Microenvironment Remodeling, and Cancer Cell Dissemination.
Angelica Avagliano, Giuseppe Fiume, +8 authors, Alessandro Arcucci.
Cancers (Basel), 2020 Jul 02; 12(6). PMID: 32604738    Free PMC article.
Review.
The Contribution of Race to Breast Tumor Microenvironment Composition and Disease Progression.
Gina Kim, Jessica M Pastoriza, +4 authors, Maja H Oktay.
Front Oncol, 2020 Jul 28; 10. PMID: 32714862    Free PMC article.
Review.
The role of the tumor microenvironment in tumor cell intravasation and dissemination.
Lucia Borriello, George S Karagiannis, +4 authors, John S Condeelis.
Eur J Cell Biol, 2020 Aug 18; 99(6). PMID: 32800278    Free PMC article.
Profiling of Invasive Breast Carcinoma Circulating Tumour Cells-Are We Ready for the 'Liquid' Revolution?
Marcin Braun, Aleksandra Markiewicz, +2 authors, Hanna Romańska.
Cancers (Basel), 2019 Jan 30; 11(2). PMID: 30691008    Free PMC article.
Review.
Suppression of Tumor Growth, Metastasis, and Signaling Pathways by Reducing FOXM1 Activity in Triple Negative Breast Cancer.
Parama Dey, Alexander Wang, +4 authors, Benita S Katzenellenbogen.
Cancers (Basel), 2020 Sep 24; 12(9). PMID: 32961773    Free PMC article.
Comparison of breast cancer prognostic tests CanAssist Breast and Oncotype DX.
Aditya K Sengupta, Aparna Gunda, +4 authors, Manjiri M Bakre.
Cancer Med, 2020 Oct 08; 9(21). PMID: 33027559    Free PMC article.
Hematogenous Dissemination of Breast Cancer Cells From Lymph Nodes Is Mediated by Tumor MicroEnvironment of Metastasis Doorways.
Anouchka Coste, George S Karagiannis, +7 authors, David Entenberg.
Front Oncol, 2020 Nov 17; 10. PMID: 33194666    Free PMC article.