Cited by 587Cancer Cells and MetastasisMechanisms of cancer metastasisDevelopmental Biology and Gene Regulation

The DOI matches its Crossref record; 142 of the 143 references it cites were found in a registry or an index.

Mechanisms Governing Metastatic Dormancy and Reactivation

Open access

Giancotti, Filippo G.·2013·Cell

DOI 10.1016/j.cell.2013.10.029PMC PMC4354734

Open this paper in CoChat — free account Open PDF

Abstract

Many cancer patients suffer from metastatic relapse several years after they have undergone radical surgery. Early cancer cell dissemination followed by a protracted period of dormancy potentially explains this prevalent clinical behavior. Increasing evidence suggests that the metastasis-initiating cells are cancer stem cells or revert to this functional state upon infiltrating a target organ. Their entry into dormancy and subsequent reactivation are governed by intrinsic programs and by contextual cues, which resemble those regulating the self-renewal capability of adult stem cells. In addition, metastatic cells undergoing reactivation are nursed by specialized extracellular matrix niches, which support positive signals, such as Wnt and Notch, and attenuate negative signals, such as BMP. In spite of significant remaining uncertainties, these findings provide a framework to understand the logic of metastatic dormancy and reactivation and open new avenues for therapeutic intervention.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.cell.2013.10.029

Cites

142 of 142 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Epithelial-Mesenchymal Transitions in Development and Disease
Thiery, J. P., Acloque, H., Huang, R. Y. J., & Nieto, M. A. (2009) · Cell · doi:10.1016/j.cell.2009.11.007 · Cited by 9,931
Stem cells, cancer, and cancer stem cells
Reya, T., Morrison, S. J., Clarke, M. F., & Weissman, I. L. (2001) · Nature · doi:10.1038/35102167 · Cited by 9,738
The Epithelial-Mesenchymal Transition Generates Cells with Properties of Stem Cells
Mani, S. A., Guo, W., Liao, M.-J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M. W., Reinhard, F., Zhang, C. C., Shipitsin, M. V., et al. (2008) · Cell · doi:10.1016/j.cell.2008.03.027 · Cited by 8,839
Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing
Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1113205 · Cited by 7,774
Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis
Hanahan, D., & Folkman, J. (1996) · Cell · doi:10.1016/s0092-8674(00)80108-7 · Cited by 6,885
The Clonal Evolution of Tumor Cell Populations: Acquired genetic lability permits stepwise selection of variant sublines and underlies tumor progression.
Nowell, P. C. (1976) · Science · doi:10.1126/science.959840 · Cited by 6,471
Wnt/β-catenin signaling and disease
Clevers, H., & Nusse, R. (2012) · Cell · doi:10.1016/j.cell.2012.05.012 · Cited by 5,554
A Perspective on Cancer Cell Metastasis
Chaffer, C. L., & Weinberg, R. A. (2011) · Science · doi:10.1126/science.1203543 · Cited by 4,905
The pathogenesis of cancer metastasis: the ‘seed and soil’ hypothesis revisited
Fidler, I. J. (2003) · Nature Reviews Cancer · doi:10.1038/nrc1098 · Cited by 4,686
Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling
Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F. T., Csiszar, K., Giaccia, A., Weninger, W., et al. (2009) · Cell · doi:10.1016/j.cell.2009.10.027 · Cited by 4,101

Show all 143 references

Sorted by citations

Items 201–300 of 587

Adaptive Fibrogenic Reprogramming of Osteosarcoma Stem Cells Promotes Metastatic Growth
Zhang, W., Zhao, J.-M., Lin, J., Hu, C.-Z., Zhang, J., YANG, W.-L., Zhang, J., Zhang, J., & Zhu, J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.103 · Cited by 40
Immunogenic, cellular, and angiogenic drivers of tumor dormancy‐a melanoma view
Senft, D., & Ronai, Z. A. (2015) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.12432 · Cited by 44
3D functional and perfusable microvascular networks for organotypic microfluidic models
Bersini, S., & Moretti, M. (2015) · Journal of Materials Science Materials in Medicine · doi:10.1007/s10856-015-5520-5 · Cited by 39
Reductive Stress, Bioactive Compounds, Redox-Active Metals, and Dormant Tumor Cell Biology to Develop Redox-Based Tools for the Treatment of Cancer
Quiles, J. L., Sánchez‐González, C., Ramírez, L. V., Giampieri, F., Navarro‐Hortal, M. D., Xiao, J., Llopis, J., Battino, M. A., & Varela‐López, A. (2020) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8051 · Cited by 39
Molecular pathology underlying the robustness of cancer stem cells
Yoshida, G. J., & Saya, H. (2021) · Regenerative Therapy · doi:10.1016/j.reth.2021.02.002 · Cited by 38
Emerging Role of NRF2 Signaling in Cancer Stem Cell Phenotype
Hallis, S. P., Kim, J. M., & Kwak, M. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.2196 · Cited by 39
Premetastatic Niche Mimicking Bone‐On‐A‐Chip: A Microfluidic Platform to Study Bone Metastasis in Cancer Patients
Ji, X., Bei, H., Zhong, G., Shao, H., He, X., Qian, X., Zhang, Y., & Zhao, X. (2023) · Small · doi:10.1002/smll.202207606 · Cited by 39
Protein disulfide isomerases in the endoplasmic reticulum promote anchorage-independent growth of breast cancer cells
Wise, R., Duhachek-Muggy, S., Qi, Y., Žółkiewski, M., & Żółkiewska, A. (2016) · Breast Cancer Research and Treatment · doi:10.1007/s10549-016-3820-1 · Cited by 38
Spontaneous Fusion of MSC with Breast Cancer Cells Can Generate Tumor Dormancy
Melzer, C., von der Ohe, J., Luo, T., & Hass, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115930 · Cited by 37
Activation of anaphase-promoting complex by p53 induces a state of dormancy in cancer cells against chemotherapeutic stress
Dai, Y., Wang, L., Tang, J., Cao, P., Luo, Z., Sun, J., Kiflu, A. B., Sai, B., Zhang, M., Wang, F., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.8172 · Cited by 36
Research Progress of Plant-Derived Natural Products against Drug-Resistant Cancer
Liu, W., Wang, Y., Xia, L., & Li, J. (2024) · Nutrients · doi:10.3390/nu16060797 · Cited by 38
The Role of Complement in Angiogenesis
Markiewski, M. M., Daugherity, E. A., Reese, B., & Karbowniczek, M. (2020) · Antibodies · doi:10.3390/antib9040067 · Cited by 40
The use of molecular imaging combined with genomic techniques to understand the heterogeneity in cancer metastasis
Chowdhury, R., Ganeshan, B., Irshad, S., Lawler, K., Eisenblätter, M., Milewicz, H., Rodriguez‐Justo, M., Miles, K. A., Ellis, P., Groves, A. M., et al. (2014) · BJR|case reports · doi:10.1259/bjr.20140065 · Cited by 34
Cancer stem cells: Signaling pathways and therapeutic targeting
Talukdar, J., Srivastava, T. P., Sahoo, O. S., Karmakar, A., Rai, A. K., Sarma, A., Gogoi, G., Alqahtani, M. S., Abbas, M. A. E., Dhar, R., et al. (2023) · MedComm – Oncology · doi:10.1002/mog2.62 · Cited by 35
Surgical cytoreduction of the primary tumor reduces metastatic progression in a mouse model of prostate cancer
Cifuentes, F., VALENZUELA, R. H., Contreras, H. R., & Castellón, E. A. (2015) · Oncology Reports · doi:10.3892/or.2015.4319 · Cited by 34
New approaches to targeting the bone marrow microenvironment in multiple myeloma
Gooding, S., & Edwards, C. M. (2016) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2016.02.013 · Cited by 35
Wnt Signaling in the Development of Bone Metastasis
Ben-Ghedalia-Peled, N., & Vago, R. (2022) · Cells · doi:10.3390/cells11233934 · Cited by 33
The Influence of Ligand Density and Degradability on Hydrogel Induced Breast Cancer Dormancy and Reactivation
Farino, C. J., Pradhan, S., & Slater, J. H. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202002227 · Cited by 34
Cancer progression as a learning process
Shomar, A., Barak, O., & Brenner, N. (2022) · iScience · doi:10.1016/j.isci.2022.103924 · Cited by 33
Mitochondria in Cancer
Dong, L., & Neužil, J. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394625-6.00008-8 · Cited by 34
Melanoma dormancy in a mouse model is linked to GILZ/FOXO3A-dependent quiescence of disseminated stem-like cells
Touil, Y. S., Ségard, P., Ostyn, P., Bégard, S., Aspord, C., Machhour, R. E., Masselot, B., Vandomme, J., Flamenco, P., Idziorek, T., et al. (2016) · Scientific Reports · doi:10.1038/srep30405 · Cited by 32
A c-Myc-regulated stem cell-like signature in high-risk neuroblastoma: A systematic discovery (Target neuroblastoma ESC-like signature)
Yang, X. H., Tang, F., Shin, J., & Cunningham, J. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-00122-x · Cited by 32
Cell-intrinsic survival signals. The role of autophagy in metastatic dissemination and tumor cell dormancy
Ramírez, L. V. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.07.027 · Cited by 35
The Cell Biology of Metastatic Invasion in Pancreatic Cancer: Updates and Mechanistic Insights
Joshi, V. B., Gutierrez Ruiz, O. L., & Razidlo, G. L. (2023) · Cancers · doi:10.3390/cancers15072169 · Cited by 32
Protracted dormancy of pre-leukemic stem cells
Ford, A. M., Mansur, M. B., Furness, C. L., van Delft, F. W., Okamura, J., Suzuki, T., Kobayashi, H., Kaneko, Y., & Greaves, M. F. (2015) · Leukemia · doi:10.1038/leu.2015.132 · Cited by 32
Chemoquiescence for Ideal Cancer Treatment and Prevention: Where Are We Now?
Kangwan, N., Park, J., Kim, E., & Hahm, K. B. (2014) · Journal of Cancer Prevention · doi:10.15430/jcp.2014.19.2.89 · Cited by 31
The role of hematopoietic stem cell niche in prostate cancer bone metastasis
Decker, A. M., Jung, Y., Cackowski, F. C., & Taichman, R. S. (2016) · Journal of bone oncology · doi:10.1016/j.jbo.2016.02.005 · Cited by 31
Hydroxyethyl starch stabilized copper-diethyldithiocarbamate nanocrystals for cancer therapy
Xiao, C., Li, J., Wang, X., Li, S., Xu, C., Zhang, Z., Hua, A., Ding, Z., Zhang, B., Yang, X., et al. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.02.043 · Cited by 33
Intrinsic TGF-β2-triggered SDF-1-CXCR4 signaling axis is crucial for drug resistance and a slow-cycling state in bone marrow-disseminated tumor cells
Nakamura, T., Shinriki, S., Jono, H., Guo, J., Ueda, M., Hayashi, M., Yamashita, S., Zijlstra, A., Nakayama, H., Hiraki, A., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.2826 · Cited by 31
DNA polymerase iota (Pol ι) promotes invasion and metastasis of esophageal squamous cell carcinoma
Zou, S., Shang, Z., Liu, B., Zhang, S., Wu, J., Huang, M., Ding, W., & Zhou, J. (2016) · Oncotarget · doi:10.18632/oncotarget.8580 · Cited by 31
Ras and Wnt Interaction Contribute in Prostate Cancer Bone Metastasis
Lin, S., Mokgautsi, N., & Liu, Y. (2020) · Molecules · doi:10.3390/molecules25102380 · Cited by 31
The role of host environment in cancer evolution
Solary, É., & Laplane, L. (2020) · Evolutionary Applications · doi:10.1111/eva.13039 · Cited by 33
Epithelial-mesenchymal transition: a hallmark in pancreatic cancer stem cell migration, metastasis formation, and drug resistance
Safa, A. R. (2020) · Journal of Cancer Metastasis and Treatment · doi:10.20517/2394-4722.2020.55 · Cited by 32
The biology and clinical implications of prostate cancer dormancy and metastasis
Morrissey, C. M., Vessella, R. L., Lange, P. H., & Lam, H. (2015) · Journal of Molecular Medicine · doi:10.1007/s00109-015-1353-4 · Cited by 29
Epigenetic plasticity in metastatic dormancy: mechanisms and therapeutic implications
Robinson, N. J., Parker, K. A., & Schiemann, W. P. (2020) · Annals of Translational Medicine · doi:10.21037/atm.2020.02.177 · Cited by 31
Trends in Bone Metastasis Modeling
Laranga, R., Duchi, S., Ibrahim, T., Guerrieri, A. N., Donati, D. M., & Lucarelli, E. (2020) · Cancers · doi:10.3390/cancers12082315 · Cited by 31
Long non‐coding NR2F1‐AS1 is associated with tumor recurrence in estrogen receptor‐positive breast cancers
Calle, A. S., Yamamoto, T., Kawamura, Y., Hironaka‐Mitsuhashi, A., Ono, M., Tsuda, H., Shimomura, A., Tamura, K., Takeshita, F., Ochiya, T., et al. (2020) · Molecular Oncology · doi:10.1002/1878-0261.12704 · Cited by 28
Serum Amyloid A Proteins and Their Impact on Metastasis and Immune Biology in Cancer
Lee, J., & Beatty, G. L. (2021) · Cancers · doi:10.3390/cancers13133179 · Cited by 28
Extracellular vesicles released by non-small cell lung cancer cells drive invasion and permeability in non-tumorigenic lung epithelial cells
Hasan, H., Sohal, I., Soto-Vargas, Z., Byappanahalli, A. M., Humphrey, S. E., Kubo, H., Kitdumrongthum, S., Copeland, S. E., Tian, F., Chairoungdua, A., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-04940-6 · Cited by 29
Role of myeloid-derived suppressor cells in tumor recurrence
Cole, K., Al-Kadhimi, Z. S., & Talmadge, J. E. (2023) · Cancer and Metastasis Reviews · doi:10.1007/s10555-023-10079-1 · Cited by 30
Means to the ends: The role of telomeres and telomere processing machinery in metastasis
Robinson, N. J., & Schiemann, W. P. (2016) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2016.10.005 · Cited by 28
The Adhesion G-Protein-Coupled Receptor, GPR56/ADGRG1, Inhibits Cell–Extracellular Matrix Signaling to Prevent Metastatic Melanoma Growth
Millar, M. W., Corson, N., & Xu, L. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00008 · Cited by 28
Autophagy defects and related genetic variations in renal cell carcinoma with eosinophilic cytoplasmic inclusions
Yu, Z., Ma, J., Li, X., Liu, Y., Li, M., Wang, L., Zhao, M., He, H., Zhang, Y., Rao, Q., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-28369-y · Cited by 27
Molecular principles of tissue invasion and metastasis
Dhanisha, S. S., & Guruvayoorappan, C. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00348.2022 · Cited by 29
FRIZZLED7 Is Required for Tumor Inititation and Metastatic Growth of Melanoma Cells
Tiwary, S., & Xu, L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147638 · Cited by 26
Minimal residual disease in advanced or metastatic solid cancers: The G0-G1 state and immunotherapy are key to unwinding cancer complexity
Nicolini, A., Rossi, G., Ferrari, P., & Carpi, A. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.03.009 · Cited by 26
Lipid-Based Nano-Sized Cargos as a Promising Strategy in Bone Complications: A Review
Hallan, S. S., Amirian, J., Brangule, A., & Bandere, D. (2022) · Nanomaterials · doi:10.3390/nano12071146 · Cited by 27
Immune surveillance of brain metastatic cancer cells is mediated by IFITM1
She, X., Shen, S., Chen, G., Gao, Y., Ma, J., Gao, Y., Liu, Y., Gao, G., Zhao, Y. F., Wang, C., et al. (2023) · The EMBO Journal · doi:10.15252/embj.2022111112 · Cited by 24
Iron metabolism: backfire of cancer cell stemness and therapeutic modalities
Yu, R., Hang, Y., Tsai, H., Wang, D., & Zhu, H. (2024) · Cancer Cell International · doi:10.1186/s12935-024-03329-x · Cited by 29
Characterization and functional analysis of a slow-cycling subpopulation in colorectal cancer enriched by cell cycle inducer combined chemotherapy
Wu, F., Mu, L., Li, X.-L., Hu, Y., Liu, H., Han, L., & Gong, J. (2017) · Oncotarget · doi:10.18632/oncotarget.19638 · Cited by 25
Development of an arteriolar niche and self-renewal of breast cancer stem cells by lysophosphatidic acid/protein kinase D signaling
Jiang, Y., Guo, Y., Hao, J., Guenter, R. E., Lathia, J. D., Beck, A. W., Hattaway, R., Hurst, D. R., Wang, Q. J., Liu, Y., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-02308-6 · Cited by 25
Chromatin accessibility regulates chemotherapy-induced dormancy and reactivation
Wang, L., Qiu, P., Yin, N., Xie, Y., Xu, J., Chen, A., Yi, J., Tang, J., & Xiang, J. (2021) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2021.07.019 · Cited by 25
Effects of Cancer Stem Cells in Triple-Negative Breast Cancer and Brain Metastasis: Challenges and Solutions
Lee, K., Chen, G., Chen, T., Kuo, Y., & Su, Y.-K. (2020) · Cancers · doi:10.3390/cancers12082122 · Cited by 25
Awakening of Dormant Breast Cancer Cells in the Bone Marrow
Wieder, R. (2023) · Cancers · doi:10.3390/cancers15113021 · Cited by 26
An engineered model of metastatic colonization of human bone marrow reveals breast cancer cell remodeling of the hematopoietic niche
Baldassarri, I., Tavakol, D. N., Graney, P. L., Chramiec, A. G., Hibshoosh, H. H., & Vunjak‐Novakovic, G. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2405257121 · Cited by 25
Inhibition of DEC2 is necessary for exiting cell dormancy in salivary adenoid cystic carcinoma
Yang, X. Y., Wu, J., Li, M., Zhang, W., Gao, X., Wang, H., Yu, X., Pang, X., Zhang, M., Liang, X., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01956-0 · Cited by 23
The Next-Generation of Combination Cancer Immunotherapy: Epigenetic Immunomodulators Transmogrify Immune Training to Enhance Immunotherapy
Mokhtari, R. B., Sambi, M., Qorri, B., Baluch, N., Ashayeri, N., Kumar, S., Cheng, H. M., Yeger, H., Das, B., & Szewczuk, M. R. (2021) · Cancers · doi:10.3390/cancers13143596 · Cited by 25
Angiopoietin-2 promotes ER+ breast cancer cell survival in bone marrow niche
Han, H. H., Kim, B. G., Lee, J. H., Kang, S., Kim, J. E., & Cho, N. H. (2016) · Endocrine Related Cancer · doi:10.1530/erc-16-0086 · Cited by 24
Development and Characterization of a Spontaneously Metastatic Patient-Derived Xenograft Model of Human Prostate Cancer
Lange, T., Oh‐Hohenhorst, S. J., Joosse, S. A., Pantel, K., Hahn, O., Gosau, T., Dyshlovoy, S. A., Wellbrock, J., Feldhaus, S., Maar, H., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-35695-8 · Cited by 25
The concepts of rechallenge and retreatment in melanoma: A proposal for consensus definitions
Gebhardt, C., Ascierto, P. A., Atkinson, V. G., Corrie, P. G., Dummer, R., & Schadendorf, D. (2020) · European Journal of Cancer · doi:10.1016/j.ejca.2020.07.016 · Cited by 25
Clinical applications of circulating tumor cells in metastasis and therapy
Yang, C., Liu, C., Xia, C., & Fu, L. (2025) · Journal of Hematology & Oncology · doi:10.1186/s13045-025-01733-y · Cited by 27
Rescue of Targeted Nonstem-Like Cells from Bystander Stem-Like Cells in Human Fibrosarcoma HT1080
Liu, Y., Kobayashi, A., Fu, Q., Yang, G., Konishi, T., Uchihori, Y., Hei, T. K., & Wang, Y. (2015) · Radiation Research · doi:10.1667/rr14050.1 · Cited by 23
Prostate Cancer Dormancy and Reactivation in Bone Marrow
Singh, D. K., Patel, V. G., Oh, W. K., & Aguirre‐Ghiso, J. A. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10122648 · Cited by 27
ABCG2, CD44 and SOX9 are increased with the acquisition of drug resistance and involved in cancer stem cell activities in head and neck squamous cell carcinoma cells
Murakami, K., Umemura, N., Adachi, M., Motoki, M., & Ohkoshi, E. (2022) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2022.11658 · Cited by 23
Gamma tocotrienol targets tyrosine phosphatase SHP2 in mammospheres resulting in cell death through RAS/ERK pathway
Gu, W., Prasadam, I., Yu, M., Zhang, F., Ling, P., Xiao, Y., & Yu, C. (2015) · BMC Cancer · doi:10.1186/s12885-015-1614-1 · Cited by 23
Cytokeratin 19 expression in primary thoracic tumors and lymph node metastases
Masai, K., Nakagawa, K., Yoshida, A., Sakurai, H., WATANABE, S.-I. J., Asamura, H., & Tsuta, K. (2014) · Lung Cancer · doi:10.1016/j.lungcan.2014.09.018 · Cited by 23
Suppression of Breast Cancer Metastasis Using Stapled Peptides Targeting the WASF Regulatory Complex
Cowell, J. K., Teng, Y., Bendzunas, N. G., Ara, R., Arbab, A. S., & Kennedy, E. J. (2017) · Cancer Growth and Metastasis · doi:10.1177/1179064417713197 · Cited by 24
Subversion of NK-cell and TNFα Immune Surveillance Drives Tumor Recurrence
Kottke, T., Evgin, L., Shim, K. G., Rommelfanger, D. M., Boisgerault, N., Zaidi, S., Díaz, R. M., Thompson, J., Ilett, E. J., Coffey, M. C., et al. (2017) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0175 · Cited by 24
ING5 inhibits cell proliferation and invasion in esophageal squamous cell carcinoma through regulation of the Akt/NF-κB/MMP-9 signaling pathway
Zhang, G.-J., Zhao, J., Jiang, M.-L., & Zhang, L.-C. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.01.045 · Cited by 23
Circulating Tumour Cells (CTCs) in NSCLC: From Prognosis to Therapy Design
Kejík, Z., Kaplánek, R., Dytrych, P., Masařík, M., Veselá, K., Abramenko, N., Hoskovec, D., Vašáková, M., Králová, J., Pavel Martasek, E., et al. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13111879 · Cited by 23
Matricellular proteins: multifaceted extracellular regulators in tumor dormancy
Wu, T., & Ouyang, G. (2014) · Protein & Cell · doi:10.1007/s13238-014-0023-6 · Cited by 23
Fuling Granule, a Traditional Chinese Medicine Compound, Suppresses Cell Proliferation and TGFβ-Induced EMT in Ovarian Cancer
Tao, F., Ruan, S., Liu, W., Wang, L., Xiong, Y., & Shen, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0168892 · Cited by 23
A Perspective on Therapeutic Pan-Resistance in Metastatic Cancer
Korentzelos, D. K., Clark, A. M., & Wells, A. H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197304 · Cited by 21
Premalignant pancreatic cells seed stealth metastasis in distant organs in mice
Yamaguchi, J., Kokuryo, T., Yokoyama, Y., Ebata, T., Ochiai, Y., & Nagino, M. (2021) · Oncogene · doi:10.1038/s41388-021-01706-8 · Cited by 22
Anti-GD2 CAR MSCs against metastatic Ewing's sarcoma
Golinelli, G., Grisendi, G., Dall’Ora, M., Casari, G., Spano, C., Talami, R., Banchelli, F., Prapa, M., Chiavelli, C., Rossignoli, F., et al. (2021) · Translational Oncology · doi:10.1016/j.tranon.2021.101240 · Cited by 22
Cross Talk Between Macrophages and Cancer Cells in the Bone Metastatic Environment
Batoon, L., & McCauley, L. K. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.763846 · Cited by 22
1H-NMR metabolomics analysis identifies hypoxanthine as a novel metastasis-associated metabolite in breast cancer
Shakartalla, S. B., Ashmawy, N. S., Semreen, M. H., Fayed, B. E., Shareef, Z. A., Jayakumar, M. N., Ibrahim, S. M., Rahmani, M., Hamdy, R., & Soliman, S. S. M. (2024) · Scientific Reports · doi:10.1038/s41598-023-50866-y · Cited by 22
High MMP-21 expression in metastatic lymph nodes predicts unfavorable overall survival for oral squamous cell carcinoma patients with lymphatic metastasis
Pu, Y., Wang, L., Wu, H., Feng, Z., Wang, Y., & Guo, C. (2014) · Oncology Reports · doi:10.3892/or.2014.3124 · Cited by 22
Development of an orthotopic model of human metastatic prostate cancer in the NOD-SCIDγ mouse (Mus musculus) anterior prostate
Cifuentes, F., VALENZUELA, R. H., Contreras, H. R., & Castellón, E. A. (2015) · Oncology Letters · doi:10.3892/ol.2015.3522 · Cited by 22
Estrogen Receptor Status Predicts Late-Onset Skeletal Recurrence in Breast Cancer Patients
Han, H. H., Lee, S. H., Kim, B. G., Lee, J. H., Kang, S., & Cho, N. H. (2016) · Medicine · doi:10.1097/md.0000000000002909 · Cited by 22
Rapid identification of antimicrometastases drugs using integrated model systems with two dimensional monolayer, three dimensional spheroids, and zebrafish xenotransplantation tumors
Fu, A., Peh, Y. M., Ngan, W., Wei, N., & Luo, K. Q. (2018) · Biotechnology and Bioengineering · doi:10.1002/bit.26816 · Cited by 22
Sonic hedgehog pathway mediates genistein inhibition of renal cancer stem cells
Li, E., Zhang, T., Sun, X., Li, Y., Geng, H., Yu, D., & Zhong, C. (2019) · Oncology Letters · doi:10.3892/ol.2019.10657 · Cited by 22
Aurora Kinase A Is an Independent Predictor of Invasive Recurrence in Breast Ductal Carcinoma in situ
Miligy, I. M., Toss, M. S., Gorringe, K. L., Ellis, I. O., Green, A. R., & Rakha, E. A. (2022) · Pathobiology · doi:10.1159/000522244 · Cited by 21
From molecular mechanisms of prostate cancer to translational applications: based on multi-omics fusion analysis and intelligent medicine
Ren, S., Li, J., Dorado, J., Sierra, A., González‐Díaz, H., Duardo-Sánchez, A., & Shen, B. (2023) · Health Information Science and Systems · doi:10.1007/s13755-023-00264-5 · Cited by 22
Lung metastases
Zullo, L., Filippiadis, D. K., Hendriks, L. E. L., Portik, D., Spicer, J. D., Wistuba, I. I., & Besse, B. (2025) · Nature Reviews Disease Primers · doi:10.1038/s41572-025-00642-1 · Cited by 23
Potential of Protein-based Anti-metastatic Therapy with Serpins and Inter α-Trypsin Inhibitors
Weidle, U. H., Birzele, F., & Tiefenthaler, G. (2018) · Cancer Genomics & Proteomics · doi:10.21873/cgp.20081 · Cited by 21
Lung fibrosis is a novel therapeutic target to suppress lung metastasis of osteosarcoma
Yui, Y., Kumai, J., Watanabe, K., Wakamatsu, T., & Sasagawa, S. (2022) · International Journal of Cancer · doi:10.1002/ijc.34008 · Cited by 23
Tumor removal limits prostate cancer cell dissemination in bone and osteoblasts induce cancer cell dormancy through focal adhesion kinase
Liu, R., Su, S., Xing, J., Liu, K., Zhao, Y., Stangis, M. M., Jacho, D., Yildirim-Ayan, E. D., Gatto-Weis, C. M., Chen, B., et al. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02849-0 · Cited by 25
Microfluidics and Nanomaterial-based Technologies for Circulating Tumor Cell Isolation and Detection
Cheng, S.-J., Hsieh, K. Y., Chen, S.-L., Chen, C., Huang, C., Tsou, H.-I., Kumar, P. V., Hsieh, C., & Chen, G. (2020) · Sensors · doi:10.3390/s20071875 · Cited by 19
Cell-cell contact-driven EphB1 cis- and trans- signalings regulate cancer stem cells enrichment after chemotherapy
Wang, L., Qiu, P., Xie, Y., Yin, N., Xu, J., Chen, A., Yi, J., Shi, W., Tang, J., & Xiang, J. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05385-5 · Cited by 20
Oncofetal reprogramming in tumor development and progression: novel insights into cancer therapy
Cao, J., Zhang, Z., Zhou, L., Luo, M., Li, L., Li, B., Nice, E. C., He, W., Zheng, S., & Huang, C. (2023) · MedComm · doi:10.1002/mco2.427 · Cited by 19
Brd7 loss reawakens dormant metastasis initiating cells in lung by forging an immunosuppressive niche
Mondal, J., Zhang, J., Qing, F., Li, S., Kumar, D., Huse, J. T., & Giancotti, F. G. (2025) · Nature Communications · doi:10.1038/s41467-025-56347-2 · Cited by 20
Self-citation
LINC01798/miR-17-5p axis regulates ITGA8 and causes changes in tumor microenvironment and stemness in lung adenocarcinoma
Li, X., Zhu, G., Li, Y., Huang, H., Wu, D., 曹佩军, Shi, R., Chen, C., Su, L., Zhang, R., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1096818 · Cited by 18
The updates on metastatic mechanism and treatment of colorectal cancer
Ni, Y., Liang, Y., Li, M., Lin, Y., Zou, X., 韩芳毅, Cao, J., & Li, L. (2023) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.154837 · Cited by 20
β-hydroxybutyrate inhibits malignant phenotypes of prostate cancer cells through β-hydroxybutyrylation of indoleacetamide-N-methyltransferase
Zhang, Y., & Li, Y. (2024) · Cancer Cell International · doi:10.1186/s12935-024-03277-6 · Cited by 19
Considering the biology of late recurrences in selecting patients for extended endocrine therapy in breast cancer
Bense, R. D., Qiu, S.-Q., de Vries, E. G. E., Schröder, C. P., & Fehrmann, R. S. N. (2018) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2018.07.015 · Cited by 19
Inflammation awakens dormant cancer cells by modulating the epithelial–mesenchymal phenotypic state
Zhang, J., Zhang, J., Han, L., Wu, S., Li, J., Eaton, E. N., Yuan, B., Reinhardt, F., Li, H., Strasser, P. C., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2515009122 · Cited by 18
Reprogramming the tumor metastasis cascade by targeting galectin-driven networks
Perrotta, R. M., Bach, C. A., Salatino, M., & Rabinovich, G. A. (2021) · Biochemical Journal · doi:10.1042/bcj20200167 · Cited by 18
Melanoma-Derived BRAFV600E Mutation in Peritumoral Stromal Cells: Implications for in Vivo Cell Fusion
Kurgyis, Z., Kemény, L., Buknicz, T., Groma, G., Oláh, J., Jakab, Á., Polyánka, H., Zänker, K. S., Dittmar, T., Kemény, L., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060980 · Cited by 18
A circulating tumor cell cluster-based model for tumor metastasis (Hypothesis)
Hong, Y., Li, Z., & Zhang, Q. (2016) · Oncology Letters · doi:10.3892/ol.2016.5358 · Cited by 18

Authors: Giancotti, F. G.
Affiliations: Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Giancotti, Filippo G.
ORCID: Giancotti, Filippo G.
Venue: Cell
Publisher: Elsevier BV
Published: 2013-11
Volume: 155
Issue: 4
Pages: 750-764
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2013.10.029
PMC: PMC4354734
OpenAlex: W2088035579
Cited by: 586
References: 143
Citations by year: 2026: 20 · 2025: 35 · 2024: 45 · 2023: 68 · 2022: 47 · 2021: 50 · 2020: 53 · 2019: 47 · 2018: 53 · 2017: 39 · 2016: 57 · 2015: 44 · 2014: 28
FWCI: 4.54
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 371 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (R01CA175712)
Topics: Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords: metastatic dormancy, cancer stem cells, metastasis-initiating cells, Wnt signaling, Notch signaling, BMP signaling, metastatic relapse, therapeutic interventions
MeSH terms: Animals, Extracellular Matrix, Humans, Neoplasm Metastasis, Neoplasms, Neoplastic Stem Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Mechanisms Governing Metastatic Dormancy and Reactivation

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks