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      Molecular principles of metastasis: a hallmark of cancer revisited

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          Abstract

          Metastasis is the hallmark of cancer that is responsible for the greatest number of cancer-related deaths. Yet, it remains poorly understood. The continuous evolution of cancer biology research and the emergence of new paradigms in the study of metastasis have revealed some of the molecular underpinnings of this dissemination process. The invading tumor cell, on its way to the target site, interacts with other proteins and cells. Recognition of these interactions improved the understanding of some of the biological principles of the metastatic cell that govern its mobility and plasticity. Communication with the tumor microenvironment allows invading cancer cells to overcome stromal challenges, settle, and colonize. These characteristics of cancer cells are driven by genetic and epigenetic modifications within the tumor cell itself and its microenvironment. Establishing the biological mechanisms of the metastatic process is crucial in finding open therapeutic windows for successful interventions. In this review, the authors explore the recent advancements in the field of metastasis and highlight the latest insights that contribute to shaping this hallmark of cancer.

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          Tumor metastasis: molecular insights and evolving paradigms.

          Scott Valastyan, Robert A Weinberg (2011)
          Metastases represent the end products of a multistep cell-biological process termed the invasion-metastasis cascade, which involves dissemination of cancer cells to anatomically distant organ sites and their subsequent adaptation to foreign tissue microenvironments. Each of these events is driven by the acquisition of genetic and/or epigenetic alterations within tumor cells and the co-option of nonneoplastic stromal cells, which together endow incipient metastatic cells with traits needed to generate macroscopic metastases. Recent advances provide provocative insights into these cell-biological and molecular changes, which have implications regarding the steps of the invasion-metastasis cascade that appear amenable to therapeutic targeting. Copyright © 2011 Elsevier Inc. All rights reserved.
          Article 0 comments Cited 1430 times – based on 0 reviews     Review now
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            Microenvironmental regulation of metastasis.

            Johanna A. Joyce, Jeffrey W Pollard (2009)
            Metastasis is a multistage process that requires cancer cells to escape from the primary tumour, survive in the circulation, seed at distant sites and grow. Each of these processes involves rate-limiting steps that are influenced by non-malignant cells of the tumour microenvironment. Many of these cells are derived from the bone marrow, particularly the myeloid lineage, and are recruited by cancer cells to enhance their survival, growth, invasion and dissemination. This Review describes experimental data demonstrating the role of the microenvironment in metastasis, identifies areas for future research and suggests possible new therapeutic avenues.
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              Every step of the way: integrins in cancer progression and metastasis

              Johanna Ivaska, Hellyeh Hamidi (2018)
              Cell adhesion to the extracellular matrix is fundamental to tissue integrity and human health. Integrins are the main cellular adhesion receptors that through multifaceted roles as signalling molecules, mechanotransducers and key components of the cell migration machinery are implicated in nearly every step of cancer progression from primary tumour development to metastasis. Altered integrin expression is frequently detected in tumours, where integrins have roles in supporting oncogenic growth factor receptor (GFR) signalling and GFR-dependent cancer cell migration and invasion. In addition, integrins determine colonization of metastatic sites and facilitate anchorage-independent survival of circulating tumour cells. Investigations describing integrin engagement with a growing number of versatile cell surface molecules, including channels, receptors and secreted proteins, continue to lead to the identification of novel tumour-promoting pathways. Integrin-mediated sensing, stiffening and remodelling of the tumour stroma are key steps in cancer progression supporting invasion, acquisition of cancer stem cell characteristics and drug resistance. Given the complexity of integrins and their adaptable and sometimes antagonistic roles in cancer cells and the tumour microenvironment, therapeutic targeting of these receptors has been a challenge. However, novel approaches to target integrins and antagonism of specific integrin subunits in stringently stratified patient cohorts are emerging as potential ways forward.
              Article 0 comments Cited 551 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Jawad Fares:
                ORCID: http://orcid.org/0000-0002-5368-8764
                jawad.fares@northwestern.edu
                Journal
                Journal ID (nlm-ta): Signal Transduct Target Ther
                Journal ID (iso-abbrev): Signal Transduct Target Ther
                Title: Signal Transduction and Targeted Therapy
                Publisher: Nature Publishing Group UK (London )
                ISSN (Print): 2095-9907
                ISSN (Electronic): 2059-3635
                Publication date (Electronic): 12 March 2020
                Publication date PMC-release: 12 March 2020
                Publication date Collection: 2020
                Volume: 5
                Electronic Location Identifier: 28
                Affiliations
                [1 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Neurological Surgery, Feinberg School of Medicine, , Northwestern University, ; Chicago, IL 60611 USA
                [2 ]ISNI 000000041936754X, GRID grid.38142.3c, High-Impact Cancer Research Program, , Harvard Medical School, ; Boston, MA 02115 USA
                [3 ]ISNI 0000 0004 1936 9801, GRID grid.22903.3a, Faculty of Medicine, , American University of Beirut, ; Beirut, Lebanon
                [4 ]ISNI 0000 0001 2324 3572, GRID grid.411324.1, Neuroscience Research Center, Faculty of Medical Sciences, , Lebanese University, ; Beirut, Lebanon
                Author information
                http://orcid.org/0000-0002-5368-8764
                Article
                Publisher ID: 134
                DOI: 10.1038/s41392-020-0134-x
                PMC ID: 7067809
                PubMed ID: 32296047
                SO-VID: 9c1dfc28-0b97-4c6c-a55b-b74e15c96bc0
                Copyright © © The Author(s) 2020
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                Date received : 30 October 2019
                Date revision received : 5 February 2020
                Date accepted : 11 February 2020
                Categories
                Subject: Review Article
                Custom metadata
                issue-copyright-statement © The Author(s) 2020

                Keywords: metastasis
                Data availability:
                Keywords: metastasis

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