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Cancer and Metastasis Reviews
Published in: Cancer and Metastasis Reviews 1/2023

21-02-2023 | Metastasis

Regulation of dormancy during tumor dissemination: the role of the ECM

Authors: Ananya Mukherjee, Jose Javier Bravo-Cordero

Published in: Cancer and Metastasis Reviews | Issue 1/2023

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Abstract

The study of the metastatic cascade has revealed the complexity of the process and the multiple cellular states that disseminated cancer cells must go through. The tumor microenvironment and in particular the extracellular matrix (ECM) plays an important role in regulating the transition from invasion, dormancy to ultimately proliferation during the metastatic cascade. The time delay from primary tumor detection to metastatic growth is regulated by a molecular program that maintains disseminated tumor cells in a non-proliferative, quiescence state known as tumor cell dormancy. Identifying dormant cells and their niches in vivo and how they transition to the proliferative state is an active area of investigation, and novel approaches have been developed to track dormant cells during dissemination. In this review, we highlight the latest research on the invasive nature of disseminated tumor cells and their link to dormancy programs. We also discuss the role of the ECM in sustaining dormant niches at distant sites.
Literature
1.
2.
3.
Bravo-Cordero, J. J., Hodgson, L., & Condeelis, J. (2012). Directed cell invasion and migration during metastasis. Current Opinion in Cell Biology, 24, 277–283.PubMedCrossRef
4.
5.
Mondal, C., Di Martino, J. S., & Bravo-Cordero, J. J. (2021). Actin dynamics during tumor cell dissemination. International Review of Cell and Molecular Biology, 360, 65–98.PubMedCrossRef
6.
7.
Werner-Klein, M., et al. (2018). Genetic alterations driving metastatic colony formation are acquired outside of the primary tumour in melanoma. Nature Communications, 9, 595.PubMedPubMedCentralCrossRef
8.
Ray, A., et al. (2022). Stromal architecture directs early dissemination in pancreatic ductal adenocarcinoma. JCI Insight, 7.
9.
10.
Wang, J., & Kim, S. K. (2003). Global analysis of dauer gene expression in Caenorhabditis elegans. Development, 130, 1621–1634.PubMedCrossRef
11.
Koornneef, M., Bentsink, L., & Hilhorst, H. (2002). Seed dormancy and germination. Current Opinion in Plant Biology, 5, 33–36.PubMedCrossRef
12.
Willis, R. A. (1934). The spread of tumours in the human body. J. A. Churchill.
13.
14.
15.
Bryant, T. (1902). An analysis of forty-six cases of cancer of the breast which have been operated upon and survived the operation from 5 to 32 years, with remarks upon the treatment of recurrent growths, including the disease of the second breast, operative and otherwise. British Medical Journal, 1, 1200–1203.PubMedPubMedCentralCrossRef
16.
Ashley, D. J. (1965). On the incidence of carcinoma of the prostate. The Journal of Pathology and Bacteriology, 90, 217–224.PubMedCrossRef
17.
Mortensen, J. D., Woolner, L. B., & Bennett, W. A. (1955). Gross and microscopic findings in clinically normal thyroid glands. The Journal of Clinical Endocrinology and Metabolism, 15, 1270–1280.PubMedCrossRef
18.
Beckwith, J. B., & Perrin, E. V. (1963). In situ neuroblastomas: A contribution to the natural history of neural crest tumors. The American Journal of Pathology, 43, 1089–1104.PubMedPubMedCentral
19.
Holmgren, L., O’Reilly, M. S., & Folkman, J. (1995). Dormancy of micrometastases: Balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nature Medicine, 1, 149–153.PubMedCrossRef
20.
Townson, J. L., & Chambers, A. F. (2006). Dormancy of solitary metastatic cells. Cell Cycle, 5, 1744–1750.PubMedCrossRef
21.
22.
Phan, T. G., & Croucher, P. I. (2020). The dormant cancer cell life cycle. Nature Reviews. Cancer, 20, 398–411.PubMedCrossRef
23.
Naumov, G. N., Folkman, J., & Straume, O. (2009). Tumor dormancy due to failure of angiogenesis: Role of the microenvironment. Clinical & Experimental Metastasis, 26, 51–60.CrossRef
24.
Naumov, G. N., Akslen, L. A., & Folkman, J. (2006). Role of angiogenesis in human tumor dormancy: Animal models of the angiogenic switch. Cell Cycle, 5, 1779–1787.PubMedCrossRef
25.
Almog, N., et al. (2006). Prolonged dormancy of human liposarcoma is associated with impaired tumor angiogenesis. FASEB Journal, 20, 947–949.PubMedCrossRef
26.
Senft, D., & Ronai, Z. A. (2016). Immunogenic, cellular, and angiogenic drivers of tumor dormancy--A melanoma view. Pigment Cell & Melanoma Research, 29, 27–42.CrossRef
27.
Shchors, K., et al. (2006). The Myc-dependent angiogenic switch in tumors is mediated by interleukin 1beta. Genes & Development, 20, 2527–2538.CrossRef
28.
Stockmann, C., Schadendorf, D., Klose, R., & Helfrich, I. (2014). The impact of the immune system on tumor: Angiogenesis and vascular remodeling. Frontiers in Oncology, 4, 69.PubMedPubMedCentralCrossRef
29.
Koebel, C. M., et al. (2007). Adaptive immunity maintains occult cancer in an equilibrium state. Nature, 450, 903–907.PubMedCrossRef
30.
Schaller, J., & Agudo, J. (2020). Metastatic colonization: Escaping immune surveillance. Cancers (Basel), 12.
31.
32.
Mohme, M., Riethdorf, S., & Pantel, K. (2017). Circulating and disseminated tumour cells - Mechanisms of immune surveillance and escape. Nature Reviews Clinical Oncology, 14, 155–167.PubMedCrossRef
33.
Salmon, H., et al. (2016). Expansion and activation of CD103+dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity, 44, 924–938.PubMedPubMedCentralCrossRef
34.
Mahnke, Y. D., Schwendemann, J., Beckhove, P., & Schirrmacher, V. (2005). Maintenance of long-term tumour-specific T-cell memory by residual dormant tumour cells. Immunology, 115, 325–336.PubMedPubMedCentralCrossRef
35.
Müller-Hermelink, N., et al. (2008). TNFR1 signaling and IFN-gamma signaling determine whether T cells induce tumor dormancy or promote multistage carcinogenesis. Cancer Cell, 13, 507–518.PubMedCrossRef
36.
37.
Linde, N., Fluegen, G., & Aguirre-Ghiso, J. A. (2016). The relationship between dormant cancer cells and their microenvironment. Advances in Cancer Research, 132.
38.
Risson, E., Nobre, A. R., Maguer-Satta, V., & Aguirre-Ghiso, J. A. (2020). The current paradigm and challenges ahead for the dormancy of disseminated tumor cells. Nature Cancer, 1, 672–680.PubMedPubMedCentralCrossRef
39.
Raviraj, V., et al. (2012). Dormant but migratory tumour cells in desmoplastic stroma of invasive ductal carcinomas. Clinical & Experimental Metastasis, 29, 273–292.CrossRef
40.
Bayarmagnai, B., et al. (2019). Invadopodia-mediated ECM degradation is enhanced in the G1 phase of the cell cycle. Journal of Cell Science, 132.
41.
42.
43.
44.
45.
Borriello, L., et al. (2022). Primary tumor associated macrophages activate programs of invasion and dormancy in disseminating tumor cells. Nature Communications, 13, 626.PubMedPubMedCentralCrossRef
46.
Harney, A. S., et al. (2015). Real-time imaging reveals local, transient vascular permeability, and tumor cell intravasation stimulated by TIE2hi macrophage-derived VEGFA. Cancer Discovery, 5, 932–943.PubMedPubMedCentralCrossRef
47.
Pignatelli, J., et al. (2014). Invasive breast carcinoma cells from patients exhibit MenaINV- and macrophage-dependent transendothelial migration. Science Signaling, 7, ra112.PubMedPubMedCentralCrossRef
48.
Rohan, T. E., et al. (2014). Tumor microenvironment of metastasis and risk of distant metastasis of breast cancer. Journal of the National Cancer Institute, 106.
49.
Mondal, C., et al. (2022). A proliferative to invasive switch is mediated by srGAP1 downregulation through the activation of TGF-β2 signaling. Cell Reports, 40, 111358.PubMedCrossRef
50.
Kienast, Y., et al. (2010). Real-time imaging reveals the single steps of brain metastasis formation. Nature Medicine, 16, 116–122.PubMedCrossRef
51.
52.
53.
Hong, M. K. H., et al. (2015). Tracking the origins and drivers of subclonal metastatic expansion in prostate cancer. Nature Communications, 6, 6605.PubMedCrossRef
54.
Krøigård, A. B., et al. (2017). Genomic analyses of breast cancer progression reveal distinct routes of metastasis emergence. Scientific Reports, 7, 43813.PubMedPubMedCentralCrossRef
55.
Schwarz, R. F., et al. (2015). Spatial and temporal heterogeneity in high-grade serous ovarian cancer: A phylogenetic analysis. PLoS Medicine, 12, e1001789.PubMedPubMedCentralCrossRef
56.
Hoover, H. C. J., & Ketcham, A. S. (1975). Metastasis of metastases. American Journal of Surgery, 130, 405–411.PubMedCrossRef
57.
Hart, I. R., & Fidler, I. J. (1980). Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Research, 40, 2281–2287.PubMed
58.
Strauss, D. C., & Thomas, J. M. (2010). Transmission of donor melanoma by organ transplantation. The Lancet Oncology, 11, 790–796.PubMedCrossRef
59.
Stephens, J. K., et al. (2000). Fatal transfer of malignant melanoma from multiorgan donor to four allograft recipients. Transplantation, 70, 232–236.PubMed
60.
Borriello, L., Condeelis, J., Entenberg, D., & Oktay, M. H. (2021). Breast cancer cell re-dissemination from lung metastases-A mechanism for enhancing metastatic burden. Journal of Clinical Medicine, 10.
61.
Condeelis, J. S., & Entenberg, D. (2020). Hematogenous dissemination of breast cancer cells from lymph nodes is mediated by tumor microenvironment of metastasis doorways. Frontiers in Oncology, 10, 1–9.
62.
Pereira, E. R., et al. (2018). Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science, 359, 1403–1407.PubMedPubMedCentralCrossRef
63.
Brown, M., et al. (2018). Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science, 359, 1408–1411.PubMedCrossRef
64.
65.
66.
67.
Baccelli, I., et al. (2013). Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nature Biotechnology, 31, 539–544.PubMedCrossRef
68.
Nemec, S., & Kilian, K. A. (2021). Materials control of the epigenetics underlying cell plasticity. Nature Reviews Materials, 6, 69–83.CrossRef
69.
Dai, J., et al. (2022). Astrocytic laminin-211 drives disseminated breast tumor cell dormancy in brain. Nature Cancer, 3, 25–42.PubMedCrossRef
70.
Nallanthighal, S., Heiserman, J. P., & Cheon, D.-J. (2019). The role of the extracellular matrix in cancer stemness. Frontiers in Cell and Development Biology, 7, 86.CrossRef
71.
72.
Karamanos, N. K., et al. (2021). A guide to the composition and functions of the extracellular matrix. The FEBS Journal, 288, 6850–6912.PubMedCrossRef
73.
74.
Wolfenson, H., Yang, B., & Sheetz, M. P. (2019). Steps in mechanotransduction pathways that control cell morphology. Annual Review of Physiology, 81, 585–605.PubMedCrossRef
75.
Kechagia, J. Z., Ivaska, J., & Roca-Cusachs, P. (2019). Integrins as biomechanical sensors of the microenvironment. Nature Reviews. Molecular Cell Biology, 20, 457–473.PubMedCrossRef
76.
Burridge, K., Monaghan-Benson, E., & Graham, D. M. (2019). Mechanotransduction: From the cell surface to the nucleus via RhoA. Philosophical Transactions of the Royal Society B, 374, 20180229.CrossRef
77.
Ohashi, K., Fujiwara, S., & Mizuno, K. (2017). Roles of the cytoskeleton, cell adhesion and rho signalling in mechanosensing and mechanotransduction. Journal of Biochemistry, 161, 245–254.PubMed
78.
79.
Wang, Y., & Xiao, B. (2018). The mechanosensitive Piezo1 channel: Structural features and molecular bases underlying its ion permeation and mechanotransduction. The Journal of Physiology, 596, 969–978.PubMedCrossRef
80.
Geng, J., et al. (2020). A plug-and-latch mechanism for gating the mechanosensitive Piezo Channel. Neuron, 106, 438–451.e6.PubMedCrossRef
81.
82.
Pathak, M. M., et al. (2014). Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proceedings of the National Academy of Sciences of the United States of America, 111, 16148–16153.PubMedPubMedCentralCrossRef
83.
Sun, X., et al. (2021). Bone piezoelectricity-mimicking nanocomposite membranes enhance osteogenic differentiation of bone marrow mesenchymal stem cells by amplifying cell adhesion and actin cytoskeleton. Journal of Biomedical Nanotechnology, 17, 1058–1067.PubMedCrossRef
84.
Wang, F., et al. (2017). Mechanosensitive ion channel Piezo2 is important for enterochromaffin cell response to mechanical forces. The Journal of Physiology, 595, 79–91.PubMedCrossRef
85.
Lai, A., et al. (2022). Mechanosensing by Piezo1 and its implications for physiology and various pathologies. Biological Reviews of the Cambridge Philosophical Society, 97, 604–614.PubMedCrossRef
86.
Wu, J., Lewis, A. H., & Grandl, J. (2017). Touch, tension, and transduction - The function and regulation of Piezo ion channels. Trends in Biochemical Sciences, 42, 57–71.PubMedCrossRef
87.
Kenmochi, M., et al. (2022). Involvement of mechano-sensitive Piezo1 channel in the differentiation of brown adipocytes. The Journal of Physiological Sciences, 72, 13.PubMedCrossRef
88.
Wang, N., Tytell, J. D., & Ingber, D. E. (2009). Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nature Reviews. Molecular Cell Biology, 10, 75–82.PubMedCrossRef
89.
Bouzid, T., et al. (2019). The LINC complex, mechanotransduction, and mesenchymal stem cell function and fate. Journal of Biological Engineering, 13, 68.PubMedPubMedCentralCrossRef
90.
Kalukula, Y., Stephens, A. D., Lammerding, J., & Gabriele, S. (2022). Mechanics and functional consequences of nuclear deformations. Nature Reviews. Molecular Cell Biology, 23, 583–602.PubMedPubMedCentralCrossRef
91.
Hamouda, M. S., Labouesse, C., & Chalut, K. J. (2020). Nuclear mechanotransduction in stem cells. Current Opinion in Cell Biology, 64, 97–104.PubMedCrossRef
92.
93.
Chang, W., Worman, H. J., & Gundersen, G. G. (2015). Accessorizing and anchoring the LINC complex for multifunctionality. The Journal of Cell Biology, 208, 11–22.PubMedPubMedCentralCrossRef
94.
Sharili, A. S., & Connelly, J. T. (2014). Nucleocytoplasmic shuttling: A common theme in mechanotransduction. Biochemical Society Transactions, 42, 645–649.PubMedCrossRef
95.
Kofler, M., & Kapus, A. (2021). Nucleocytoplasmic shuttling of the mechanosensitive transcription factors MRTF and YAP /TAZ. Methods in Molecular Biology, 2299, 197–216.PubMedCrossRef
96.
Jang, J.-W., Kim, M.-K., & Bae, S.-C. (2020). Reciprocal regulation of YAP/TAZ by the Hippo pathway and the Small GTPase pathway. Small GTPases, 11, 280–288.PubMedCrossRef
97.
Miranda, M. Z., Lichner, Z., Szászi, K., & Kapus, A. (2021). MRTF: Basic biology and role in kidney disease. International Journal of Molecular Sciences, 22.
98.
Shreberk-Shaked, M., & Oren, M. (2019). New insights into YAP/TAZ nucleo-cytoplasmic shuttling: New cancer therapeutic opportunities? Molecular Oncology, 13, 1335–1341.PubMedPubMedCentralCrossRef
99.
Speight, P., Kofler, M., Szászi, K., & Kapus, A. (2016). Context-dependent switch in chemo/mechanotransduction via multilevel crosstalk among cytoskeleton-regulated MRTF and TAZ and TGFβ-regulated Smad3. Nature Communications, 7, 11642.PubMedPubMedCentralCrossRef
100.
Er, E. E., et al. (2018). Pericyte-like spreading by disseminated cancer cells activates YAP and MRTF for metastatic colonization. Nature Cell Biology, 20, 966–978.PubMedPubMedCentralCrossRef
101.
102.
Zabransky, D. J., Jaffee, E. M., & Weeraratna, A. T. (2022). Shared genetic and epigenetic changes link aging and cancer. Trends in Cell Biology, 32, 338–350.PubMedCrossRef
103.
104.
105.
Dawson, M. A., & Kouzarides, T. (2012). Cancer epigenetics: From mechanism to therapy. Cell, 150, 12–27.PubMedCrossRef
106.
Stowers, R., & Chaudhuri, O. (2021). Epigenetic regulation of mechanotransduction. Nature Biomedical Engineering, 5, 8–10.PubMedCrossRef
107.
Stowers, R. S., et al. (2019). Matrix stiffness induces a tumorigenic phenotype in mammary epithelium through changes in chromatin accessibility. Nature Biomedical Engineering, 3, 1009–1019.PubMedPubMedCentralCrossRef
108.
Jang, M., et al. (2021). Matrix stiffness epigenetically regulates the oncogenic activation of the Yes-associated protein in gastric cancer. Nature Biomedical Engineering, 5, 114–123.PubMedCrossRef
109.
Gupta, V. K., & Chaudhuri, O. (2022). Mechanical regulation of cell-cycle progression and division. Trends in Cell Biology, 32, 773–785.PubMedCrossRef
110.
Sosa, M. S., et al. (2015). NR2F1 controls tumour cell dormancy via SOX9- and RARβ-driven quiescence programmes. Nature Communications, 6, 6170.PubMedCrossRef
111.
Singh, D. K., et al. (2021). Epigenetic reprogramming of DCCs into dormancy suppresses metastasis <em>via</em> restored TGFβ–SMAD4 signaling. https://​arxiv.​org/​abs/​2021.​08.​01.​454684.​ https://​doi.​org/​10.​1101/​2021.​08.​01.​454684
112.
113.
Schofield, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 4, 7–25.PubMed
114.
115.
Naba, A., et al. (2012). The matrisome: In silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Molecular & Cellular Proteomics, 11, M111.014647-M111.014647.CrossRef
116.
Hynes, R. O., & Naba, A. (2012). Overview of the matrisome--An inventory of extracellular matrix constituents and functions. Cold Spring Harbor Perspectives in Biology, 4, a004903.PubMedPubMedCentralCrossRef
117.
118.
Aguirre Ghiso, J. A., Kovalski, K., & Ossowski, L. (1999). Tumor dormancy induced by downregulation of urokinase receptor in human carcinoma involves integrin and MAPK signaling. The Journal of Cell Biology, 147, 89–103.PubMedCrossRef
119.
Di Martino, J. S., et al. (2022). A tumor-derived type III collagen-rich ECM niche regulates tumor cell dormancy. Nature Cancer, 3, 90–107.PubMedCrossRef
120.
Montagner, M., et al. (2020). Crosstalk with lung epithelial cells regulates Sfrp2-mediated latency in breast cancer dissemination. Nature Cell Biology, 22, 289–296.PubMedPubMedCentralCrossRef
121.
122.
Aouad, P., et al. (2022). Epithelial-mesenchymal plasticity determines estrogen receptor positive breast cancer dormancy and epithelial reconversion drives recurrence. Nature Communications, 13, 4975.PubMedPubMedCentralCrossRef
123.
Coppock, D. L., Kopman, C., Scandalis, S., & Gilleran, S. (1993). Preferential gene expression in quiescent human lung fibroblasts. Cell Growth and Differentiation, 4, 483–493.PubMed
124.
125.
Ohta, Y., et al. (2022). Cell-matrix interface regulates dormancy in human colon cancer stem cells. Nature, 608, 784–794.PubMedCrossRef
126.
Albrengues, J., et al. (2018). Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science, 361(6409), eaao4227.PubMedPubMedCentralCrossRef
127.
128.
129.
Elkholi, I. E., Lalonde, A., Park, M., & Côté, J.-F. (2022). Breast cancer metastatic dormancy and relapse: An enigma of microenvironment(s). Cancer Research, 82, 4497–4510.PubMedPubMedCentralCrossRef
130.
Sosa, M. S., Bragado, P., & Aguirre-Ghiso, J. A. (2014). Mechanisms of disseminated cancer cell dormancy: An awakening field. Nature Reviews Cancer, 14, 611–622.PubMedPubMedCentralCrossRef
131.
Russo, S., Scotto di Carlo, F., & Gianfrancesco, F. (2022). The osteoclast traces the route to bone tumors and metastases. Frontiers in Cell and Development Biology, 10, 886305.CrossRef
132.
Heyn, C., et al. (2006). In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magnetic Resonance in Medicine, 56, 1001–1010.PubMedCrossRef
133.
Heyn, C., et al. (2006). In vivo magnetic resonance imaging of single cells in mouse brain with optical validation. Magnetic Resonance in Medicine, 55, 23–29.PubMedCrossRef
134.
Shapiro, E. M., Sharer, K., Skrtic, S., & Koretsky, A. P. (2006). In vivo detection of single cells by MRI. Magnetic Resonance in Medicine, 55, 242–249.PubMedCrossRef
135.
136.
Fukumura, D., Duda, D. G., Munn, L. L., & Jain, R. K. (2010). Tumor microvasculature and microenvironment: Novel insights through intravital imaging in pre-clinical models. Microcirculation, 17, 206–225.PubMedPubMedCentralCrossRef
137.
138.
Moore, N., & Lyle, S. (2011). Quiescent, slow-cycling stem cell populations in cancer: A review of the evidence and discussion of significance. Journal of Oncology, 2011.
139.
Cotsarelis, G., Sun, T. T., & Lavker, R. M. (1990). Label-retaining cells reside in the bulge area of pilosebaceous unit: Implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell, 61, 1329–1337.PubMedCrossRef
140.
Potten, C. S., Kellett, M., Roberts, S. A., Rew, D. A., & Wilson, G. D. (1992). Measurement of in vivo proliferation in human colorectal mucosa using bromodeoxyuridine. Gut, 33, 71–78.PubMedPubMedCentralCrossRef
141.
Schillert, A., Trumpp, A., & Sprick, M. R. (2013). Label retaining cells in cancer--The dormant root of evil? Cancer Letters, 341, 73–79.PubMedCrossRef
142.
Aguirre-Ghiso, J. A., Ossowski, L., & Rosenbaum, S. K. (2004). Green fluorescent protein tagging of extracellular signal-regulated kinase and p38 pathways reveals novel dynamics of pathway activation during primary and metastatic growth. Cancer Research, 64, 7336–7345.PubMedCrossRef
143.
Regot, S., Hughey, J. J., Bajar, B. T., Carrasco, S., & Covert, M. W. (2014). High-sensitivity measurements of multiple kinase activities in live single cells. Cell, 157, 1724–1734.PubMedPubMedCentralCrossRef
144.
Yano, S., Tazawa, H., Kagawa, S., Fujiwara, T., & Hoffman, R. M. (2020). FUCCI Real-time cell-cycle imaging as a guide for designing improved cancer therapy: A review of innovative strategies to target quiescent chemo-resistant cancer cells. Cancers (Basel), 12.
145.
Sakaue-Sawano, A., & Miyawaki, A. (2014). Visualizing spatiotemporal dynamics of multicellular cell-cycle progressions with fucci technology. Cold Spring Harbor Protocols, 2014.
146.
Sakaue-Sawano, A., et al. (2008). Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell, 132, 487–498.PubMedCrossRef
147.
Oki, T., et al. (2014). A novel cell-cycle-indicator, mVenus-p27K-, identifies quiescent cells and visualizes G0-G1 transition. Scientific Reports, 4, 4012.PubMedPubMedCentralCrossRef
148.
Spencer, S. L., et al. (2013). XThe proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell, 155, 369–383.PubMedPubMedCentralCrossRef
149.
Freter, R., et al. (2021). Establishment of a fluorescent reporter of RNA-polymerase II activity to identify dormant cells. Nature Communications, 12, 3318.PubMedPubMedCentralCrossRef
150.
Owen, K. L., et al. (2020). Prostate cancer cell-intrinsic interferon signaling regulates dormancy and metastatic outgrowth in bone. EMBO Reports, 21, e50162.PubMedPubMedCentralCrossRef
151.
Khoo, W. H., et al. (2019). A niche-dependent myeloid transcriptome signature defines dormant myeloma cells. Blood, 134, 30–43.PubMedCrossRef
152.
153.
154.
Pranzini, E., Raugei, G., & Taddei, M. L. (2022). Metabolic features of tumor dormancy: Possible therapeutic strategies. Cancers (Basel), 14.
155.
156.
157.
Ma, R.-Y., Black, A., & Qian, B.-Z. (2022). Macrophage diversity in cancer revisited in the era of single-cell omics. Trends in Immunology, 43, 546–563.PubMedCrossRef
Metadata
Title
Regulation of dormancy during tumor dissemination: the role of the ECM
Authors
Ananya Mukherjee
Jose Javier Bravo-Cordero
Publication date
21-02-2023
Publisher
Springer US
Keyword
Metastasis
Published in
Cancer and Metastasis Reviews / Issue 1/2023
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-023-10094-2

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