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

Emerging Biological Principles of Metastasis
Lambert, A. W., Pattabiraman, D. R., & Weinberg, R. A. (2017) · Cell · doi:10.1016/j.cell.2016.11.037 · Cited by 3,191
Molecular principles of metastasis: a hallmark of cancer revisited
Fares, J., Fares, M. Y., Khachfe, H. H., Salhab, H. A., & Fares, Y. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-0134-x · Cited by 2,536
Targeting cancer stem cell pathways for cancer therapy
Yang, L., Shi, P., Zhao, G., Xu, J., Peng, W., Zhang, J., Zhang, G., Wang, X., Dong, Z., Chen, F., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-0110-5 · Cited by 1,957
Mechanisms of disseminated cancer cell dormancy: an awakening field
Sosa, M. S., Bragado, P., & Aguirre‐Ghiso, J. A. (2014) · Nature reviews. Cancer · doi:10.1038/nrc3793 · Cited by 1,184
Integrin Signaling in Cancer: Mechanotransduction, Stemness, Epithelial Plasticity, and Therapeutic Resistance
Cooper, J. M., & Giancotti, F. G. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.01.007 · Cited by 967
Self-citation
Cancer stem cells as key drivers of tumour progression
Ayob, A. Z., & Ramasamy, T. S. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0426-4 · Cited by 910
Revisiting the hallmarks of cancer.
Fouad, Y. A., & Aanei, C. M. (2017) · Europe PMC (PubMed Central) · Cited by 875
Tracking Cancer Evolution Reveals Constrained Routes to Metastases: TRACERx Renal
Turajlic, S., Xu, H., Litchfield, K., Rowan, A., Chambers, T., Lopez, J. I., Nicol, D. L., O’Brien, T., Larkin, J., Horswell, S. D., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.057 · Cited by 830
Metastatic colorectal cancer: mechanisms and emerging therapeutics
Shin, A. E., Giancotti, F. G., & Rustgi, A. K. (2023) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2023.01.003 · Cited by 717
Self-citation
The dynamic nature of senescence in cancer
Lee, S., & Schmitt, C. A. (2019) · Nature Cell Biology · doi:10.1038/s41556-018-0249-2 · Cited by 588
Targeting the CCL2-CCR2 signaling axis in cancer metastasis
Lim, S. Y., Yuzhalin, A. E., Gordon-Weeks, A. N., & Muschel, R. J. (2016) · Oncotarget · doi:10.18632/oncotarget.7376 · Cited by 515
Bone metastasis: the importance of the neighbourhood
Croucher, P. I., McDonald, M. M., & Martin, T. J. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.44 · Cited by 489
Autophagy in cancer metastasis
Mowers, E. E., Sharifi, M. N., & Macleod, K. F. (2016) · Oncogene · doi:10.1038/onc.2016.333 · Cited by 487
Inside and out: the activities of senescence in cancer
Pérez-Mancera, P. A., Young, A. R. J., & Narita, M. (2014) · Nature Reviews Cancer · doi:10.1038/nrc3773 · Cited by 462
The systemic response to surgery triggers the outgrowth of distant immune-controlled tumors in mouse models of dormancy
Krall, J. A., Reinhardt, F., Mercury, O. A., Pattabiraman, D. R., Brooks, M. W., Dougan, M. L., Lambert, A. W., Bierie, B., Ploegh, H. L., Dougan, S. K., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aan3464 · Cited by 452
Proline metabolism supports metastasis formation and could be inhibited to selectively target metastasizing cancer cells
Elia, I., Broekaert, D., Christen, S., Boon, R., Radaelli, E., Orth, M. F., Verfaillie, C. M., Grünewald, T. G. P., & Fendt, S. (2017) · Nature Communications · doi:10.1038/ncomms15267 · Cited by 436
Triple-Negative Breast Cancer: A Brief Review About Epidemiology, Risk Factors, Signaling Pathways, Treatment and Role of Artificial Intelligence
Almansour, N. M. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.836417 · Cited by 435
Cancer progression and the invisible phase of metastatic colonization
Klein, C. A. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-020-00300-6 · Cited by 387
From Fly Wings to Targeted Cancer Therapies: A Centennial for Notch Signaling
Ntziachristos, P., Lim, J. S., Sage, J., & Aifantis, I. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.02.018 · Cited by 376
Autophagy, cancer stem cells and drug resistance
Smith, A. G., & Macleod, K. F. (2018) · The Journal of Pathology · doi:10.1002/path.5222 · Cited by 369
Targeting Cancer Cell Dormancy
Recasens, A., & Munoz, L. (2019) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.12.004 · Cited by 356
Cancer cell plasticity during tumor progression, metastasis and response to therapy
Pérez-González, A., Bévant, K., & Blanpain, C. (2023) · Nature Cancer · doi:10.1038/s43018-023-00595-y · Cited by 370
Distinctive properties of metastasis-initiating cellsPreprint
Celià-Terrassa, T., & Kang, Y. (2016) · Genes & Development · doi:10.1101/gad.277681.116 · Cited by 342
Metabolic reprogramming and epithelial‐to‐mesenchymal transition in cancer
Sciacovelli, M., & Frezza, C. (2017) · FEBS Journal · doi:10.1111/febs.14090 · Cited by 334
A tumor-derived type III collagen-rich ECM niche regulates tumor cell dormancy
Martino, J. S. D., Nobre, A. R., Mondal, C., Taha, I. N., Farias, E., Fertig, E. J., Naba, A., Aguirre‐Ghiso, J. A., & Bravo‐Cordero, J. J. (2021) · Nature Cancer · doi:10.1038/s43018-021-00291-9 · Cited by 341
Melanoma plasticity and phenotypic diversity: therapeutic barriers and opportunitiesPreprint
Rambow, F., Marine, J., & Goding, C. R. (2019) · Genes & Development · doi:10.1101/gad.329771.119 · Cited by 348
Metastasis prevention by targeting the dormant niche
Ghajar, C. M. (2015) · Nature reviews. Cancer · doi:10.1038/nrc3910 · Cited by 325
Curcumin effectively inhibits oncogenic NF-κB signaling and restrains stemness features in liver cancer
Marquardt, J. U., Gómez-Quiroz, L. E., Camacho, L. O. A., Pinna, F., Lee, Y., Kitade, M., Domínguez, M. P., Castven, D., Breuhahn, K., Conner, E. A., et al. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.04.018 · Cited by 313
Exploiting replicative stress to treat cancer
Dobbelstein, M., & Sørensen, C. S. (2015) · Nature Reviews Drug Discovery · doi:10.1038/nrd4553 · Cited by 310
Wnt signaling pathways in biology and disease: mechanisms and therapeutic advances
Chen, X., Chu, Q., Shi, Q., Zeng, Y., Lu, J., & Li, J. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02142-w · Cited by 347
Macrophages as Key Drivers of Cancer Progression and Metastasis
Nielsen, S. R., & Schmid, M. C. (2017) · Mediators of Inflammation · doi:10.1155/2017/9624760 · Cited by 308
Palbociclib with adjuvant endocrine therapy in early breast cancer (PALLAS): interim analysis of a multicentre, open-label, randomised, phase 3 study
Mayer, E. L., Dueck, A. C., Martín, M., Rubovszky, G., Burstein, H. J., Bellet, M., Miller, K. D., Zdenkowski, N., Winer, E. P., Pfeiler, G., et al. (2021) · The Lancet Oncology · doi:10.1016/s1470-2045(20)30642-2 · Cited by 260
Determinants of metastatic competency in colorectal cancer
Tauriello, D. V. F., Calon, A., Lonardo, E., & Batlle, E. (2017) · Molecular Oncology · doi:10.1002/1878-0261.12018 · Cited by 262
Invasion and metastasis in cancer: molecular insights and therapeutic targets
Li, Y., Liu, F., Cai, Q., Deng, L., Ouyang, Q., Zhang, X. H.-F., & Zheng, J. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02148-4 · Cited by 314
Multi-organ Site Metastatic Reactivation Mediated by Non-canonical Discoidin Domain Receptor 1 Signaling
Gao, H., Chakraborty, G., Zhang, Z., Akalay, I., Gadiya, M. M., Gao, Y., Sinha, S., Hu, J. M., Jiang, C., Akram, M. M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.06.009 · Cited by 247
Self-citation
The Polycomb Repressor Complex 1 Drives Double-Negative Prostate Cancer Metastasis by Coordinating Stemness and Immune Suppression
Su, W., Han, H. H., Wang, Y., Zhang, B., Zhou, B., Cheng, Y., Rumandla, A., Gurrapu, S., Chakraborty, G., Su, J., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.06.009 · Cited by 248
Self-citation
Targeting Breast Cancer Metastasis
Jin, X., & Mu, P. (2015) · Breast Cancer Basic and Clinical Research · doi:10.4137/bcbcr.s25460 · Cited by 250
The current paradigm and challenges ahead for the dormancy of disseminated tumor cells
Risson, E., Nobre, A. R., Maguer‐Satta, V., & Aguirre‐Ghiso, J. A. (2020) · Nature Cancer · doi:10.1038/s43018-020-0088-5 · Cited by 248
Fighting bacterial persistence: Current and emerging anti-persister strategies and therapeutics
Defraine, V., Fauvart, M., & Michiels, J. (2018) · Drug Resistance Updates · doi:10.1016/j.drup.2018.03.002 · Cited by 222
Mechanisms of Cancer Cell Dormancy—Another Hallmark of Cancer?
Yeh, A. C., & Ramaswamy, S. (2015) · Cancer Research · doi:10.1158/0008-5472.can-15-1370 · Cited by 232
Tracking and Functional Characterization of Epithelial–Mesenchymal Transition and Mesenchymal Tumor Cells during Prostate Cancer Metastasis
Ruscetti, M. A., Quach, B., Dadashian, E. L., Mulholland, D. J., & Wu, H. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3476 · Cited by 230
Functions of autophagy in the tumor microenvironment and cancer metastasis
Mowers, E. E., Sharifi, M. N., & Macleod, K. F. (2018) · FEBS Journal · doi:10.1111/febs.14388 · Cited by 224
Linking the future of anticancer metal-complexes to the therapy of tumour metastases
Bergamo, A., & Sava, G. (2015) · Chemical Society Reviews · doi:10.1039/c5cs00134j · Cited by 225
KRAS Oncogenic Signaling Extends beyond Cancer Cells to Orchestrate the Microenvironment
Dias Carvalho, P., Guimarães, C. F., Cardoso, A. P., Mendonça, S., Costa, Â. M., Oliveira, M. J., & Velho, S. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-2084 · Cited by 202
Cell–matrix interface regulates dormancy in human colon cancer stem cells
Ohta, Y., Fujii, M., Takahashi, S., Takano, A., Nanki, K., Matano, M., Hanyu, H., Saito, M. K., Shimokawa, M., Nishikori, S., et al. (2022) · Nature · doi:10.1038/s41586-022-05043-y · Cited by 219
Exosomal microRNA miR-1246 induces cell motility and invasion through the regulation of DENND2D in oral squamous cell carcinoma
Sakha, S., Muramatsu, T., Ueda, K., & Inazawa, J. (2016) · Scientific Reports · doi:10.1038/srep38750 · Cited by 201
Precision medicine for human cancers with Notch signaling dysregulation (Review)
Katoh, M., & Katoh, M. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4418 · Cited by 201
Tumor cell dormancy
Gomis, R. R., & Gawrzak, S. (2016) · Molecular Oncology · doi:10.1016/j.molonc.2016.09.009 · Cited by 202
Cancer stem cell metabolism: target for cancer therapy
Chae, Y. C., & Kim, J. H. (2018) · BMB Reports · doi:10.5483/bmbrep.2018.51.7.112 · Cited by 185
The Metabolic Mechanisms of Breast Cancer Metastasis
Wang, L., Zhang, S., & Wang, X. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2020.602416 · Cited by 200
Exploring the promising potential of induced pluripotent stem cells in cancer research and therapy
Chehelgerdi, M., Dehkordi, F. B., Chehelgerdi, M., Kabiri, H., Salehian-Dehkordi, H., Abdolvand, M. A., Salmanizadeh, S., Rashidi, M., Niazmand, A., Ahmadi, S., et al. (2023) · Molecular Cancer · doi:10.1186/s12943-023-01873-0 · Cited by 189
Are Integrins Still Practicable Targets for Anti-Cancer Therapy?
Alday-Parejo, B., Stupp, R., & Rüegg, C. (2019) · Cancers · doi:10.3390/cancers11070978 · Cited by 181
Adaptation to Stressors by Systemic Protein Amyloidogenesis
Audas, T. E., Audas, D. E., Jacob, M. D., Ho, J. J. D., Khacho, M., Wang, M., Perera, J. K., Gardiner, C., Bennett, C. A., Head, T., et al. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.09.002 · Cited by 172
Molecular Mechanisms and Emerging Therapeutic Targets of Triple-Negative Breast Cancer Metastasis
Neophytou, C. M., Boutsikos, P., & Papageorgis, P. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00031 · Cited by 175
Mechanisms of the Epithelial–Mesenchymal Transition and Tumor Microenvironment in Helicobacter pylori-Induced Gastric Cancer
Baj, J., Korona‐Głowniak, I., Forma, A., Maani, A., Sitarz, R., Rahnama, M., Radzikowska, E., & Portincasa, P. (2020) · Cells · doi:10.3390/cells9041055 · Cited by 180
Metastatic niche functions and therapeutic opportunities
Celià-Terrassa, T., & Kang, Y. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0145-9 · Cited by 174
Tumor Burden and Immunotherapy: Impact on Immune Infiltration and Therapeutic Outcomes
Kim, S. I., Cassella, C. R., & Byrne, K. T. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.629722 · Cited by 178
Cancer cells enter dormancy after cannibalizing mesenchymal stem/stromal cells (MSCs)
Bartosh, T. J., Ullah, M., Zeitouni, S., Beaver, J., & Prockop, D. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1612290113 · Cited by 169
Dormancy and cancer stem cells: An enigma for cancer therapeutic targeting
Talukdar, S., Bhoopathi, P., Emdad, L., Das, S. K., Sarkar, D., & Fisher, P. B. (2019) · Advances in cancer research · doi:10.1016/bs.acr.2018.12.002 · Cited by 167
YAP1 Regulates OCT4 Activity and SOX2 Expression to Facilitate Self-Renewal and Vascular Mimicry of Stem-Like Cells
Bora-Singhal, N., Nguyen, J. V., Schaal, C. M., Perumal, D., Singh, S., Coppola, D., & Chellappan, S. (2015) · Stem Cells · doi:10.1002/stem.1993 · Cited by 162
Cancer stem cells (CSCs), cervical CSCs and targeted therapies
Huang, R., & Rofstad, E. K. (2016) · Oncotarget · doi:10.18632/oncotarget.10169 · Cited by 162
Inflammation triggers Zeb1-dependent escape from tumor latency
Cock, J. D., Shibue, T., Dongre, A., Keckesova, Z., Reinhardt, F., & Weinberg, R. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-0608 · Cited by 143
Tumor cell–organized fibronectin maintenance of a dormant breast cancer population
Barney, L. E., Hall, C. L., Schwartz, A. D., Parks, A. N., Sparages, C., Galarza, S., Platt, M. O., Mercurio, A. M., & Peyton, S. R. (2020) · Science Advances · doi:10.1126/sciadv.aaz4157 · Cited by 161
Stem cell quiescence: the challenging path to activation
Urbán, N., & Cheung, T. H. (2021) · Development · doi:10.1242/dev.165084 · Cited by 168
Translational models of prostate cancer bone metastasis
Berish, R. B., Ali, A. N., Telmer, P. G., Ronald, J. A., & Leong, H. S. (2018) · Nature Reviews Urology · doi:10.1038/s41585-018-0020-2 · Cited by 149
Starvation and Pseudo-Starvation as Drivers of Cancer Metastasis through Translation Reprogramming
García‐Jiménez, C., & Goding, C. R. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.11.018 · Cited by 157
The CXCL5/CXCR2 axis is sufficient to promote breast cancer colonization during bone metastasis
Romero-Moreno, R., Curtis, K. J., Coughlin, T. R., Miranda-Vergara, M. C., Dutta, S., Natarajan, A., Facchine, B. A., Jackson, K. M., Nystrom, L. M., Li, J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12108-6 · Cited by 150
Meeting the Challenge of Targeting Cancer Stem Cells
Turdo, A., Veschi, V., Gaggianesi, M., Chinnici, A., Bianca, P., Todaro, M., & Stassi, G. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00016 · Cited by 155
Regulation of Epithelial Plasticity Determines Metastatic Organotropism in Pancreatic Cancer
Reichert, M., Bakir, B. S., Moreira, L., Pitarresi, J. R., Feldmann, K., Simon, L. A., Suzuki, K., Maddipati, R., Rhim, A. D., Schlitter, A. M., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.05.025 · Cited by 143
Hypoxia in solid tumors: a key promoter of cancer stem cell (CSC) resistance
Najafi, M., Farhood, B., Mortezaee, K., Kharazinejad, E., Majidpoor, J., & Ahadi, R. (2019) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-019-03080-1 · Cited by 151
Cancer-associated Fibroblasts Promote Irradiated Cancer Cell Recovery Through Autophagy
Wang, Y., Gan, G., Wang, B., Wu, J., Cao, Y., Zhu, D., Xu, Y., Wang, X., Han, H., Li, X., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.02.019 · Cited by 149
Metabolic reprogramming and dysregulated metabolism: cause, consequence and/or enabler of environmental carcinogenesis?
Robey, R. B., Weisz, J., Kuemmerle, N. B., Salzberg, A. C., Berg, A. S., Brown, D. G., Maurer, L. L., Palorini, R., Al‐Mulla, F., Al-Temaimi, R. A., et al. (2015) · Carcinogenesis · doi:10.1093/carcin/bgv037 · Cited by 143
Cancer cell cycle heterogeneity as a critical determinant of therapeutic resistance
Maleki, E. H., Bahrami, A. R., & Matin, M. M. (2023) · Genes & Diseases · doi:10.1016/j.gendis.2022.11.025 · Cited by 138
Tumor PD-L1 engages myeloid PD-1 to suppress type I interferon to impair cytotoxic T lymphocyte recruitment
Klement, J. D., Redd, P. S., Lu, C., Merting, A. D., Poschel, D. B., Yang, D., Savage, N. M., Zhou, G., Munn, D. H., Fallon, P. G., et al. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.02.005 · Cited by 137
Prrx1 isoform switching regulates pancreatic cancer invasion and metastatic colonizationPreprint
Takano, S., Reichert, M., Bakir, B. S., Das, K. K., Nishida, T., Miyazaki, M., Heeg, S., Collins, M. A., Marchand, B., Hicks, P. D., et al. (2016) · Genes & Development · doi:10.1101/gad.263327.115 · Cited by 130
EMT and Stemness in Tumor Dormancy and Outgrowth: Are They Intertwined Processes?
Weidenfeld, K., & Barkan, D. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00381 · Cited by 131
Advances in Therapeutic Targeting of Cancer Stem Cells within the Tumor Microenvironment: An Updated Review
Dzobo, K., Senthebane, D. A., Ganz, C., Thomford, N. E., Wonkam, A., & Dandara, C. (2020) · Cells · doi:10.3390/cells9081896 · Cited by 132
The current knowledge concerning solid cancer and therapy
Najafi, M., Majidpoor, J., Toolee, H., & Mortezaee, K. (2021) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22900 · Cited by 137
Microengineered cancer-on-a-chip platforms to study the metastatic microenvironment
Lara, R. P., & Annabi, N. (2016) · Lab on a Chip · doi:10.1039/c6lc00718j · Cited by 130
Liver metastases: Microenvironments and ex-vivo models
Clark, A. M., Ma, B., Taylor, D. L., Griffith, L. G., & Wells, A. H. (2016) · Experimental Biology and Medicine · doi:10.1177/1535370216658144 · Cited by 134
Engineering the pre-metastatic niche
Aguado, B. A., Bushnell, G. G., Rao, S. S., Jeruss, J. S., & Shea, L. D. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0077 · Cited by 131
Deregulation of cell signaling in cancer
Giancotti, F. G. (2014) · FEBS Letters · doi:10.1016/j.febslet.2014.02.005 · Cited by 133
Self-citation
Cancer metastasis: Molecular mechanisms and clinical perspectives
Khan, S. U., Fatima, K., Malik, F. A., Kalkavan, H., & Wani, A. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108522 · Cited by 127
Evolution of metastasis revealed by mutational landscapes of chemically induced skin cancers
McCreery, M. Q., Halliwill, K. D., Chin, D., Delrosario, R., Hirst, G. L., Vuong, P. T., Jen, K., Hewinson, J., Adams, D. J., & Balmain, A. (2015) · Nature Medicine · doi:10.1038/nm.3979 · Cited by 119
Cancer Metastasis: A Reappraisal of Its Underlying Mechanisms and Their Relevance to Treatment
Riggi, N., Aguet, M., & Stamenkovic, I. (2017) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-020117-044127 · Cited by 121
The Rho GTPase Rnd1 suppresses mammary tumorigenesis and EMT by restraining Ras-MAPK signalling
Okada, T., Sinha, S., Esposito, I., Schiavon, G., López-Lago, M. A., Su, W., Pratilas, C. A., Abele, C., Hernandez, J. M., Ohara, M., et al. (2014) · Nature Cell Biology · doi:10.1038/ncb3082 · Cited by 117
Self-citation
Adaptive Stress Responses During Tumor Metastasis and Dormancy
Senft, D., & Ronai, Z. A. (2016) · Trends in cancer · doi:10.1016/j.trecan.2016.06.004 · Cited by 118
Tumor Dormancy and Interplay with Hypoxic Tumor Microenvironment
Butturini, E., de Prati, A. C., Boriero, D., & Mariotto, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174305 · Cited by 121
Recent insight into the role of FBXW7 as a tumor suppressor
Yumimoto, K., & Nakayama, K. I. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.02.017 · Cited by 106
An epigenetic gateway to brain tumor cell identity
Mack, S. C., Hubert, C. G., Miller, T. E., Taylor, M. D., & Rich, J. N. (2015) · Nature Neuroscience · doi:10.1038/nn.4190 · Cited by 106
HIGD1A Regulates Oxygen Consumption, ROS Production, and AMPK Activity during Glucose Deprivation to Modulate Cell Survival and Tumor Growth
Ameri, K., Jahangiri, A., Rajah, A. M., Tormos, K. V., Nagarajan, R., Pekmezci, M., Nguyen, V., Wheeler, M. L., Murphy, M. P., Sanders, T. A., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.020 · Cited by 107
Lung-Seeking Metastases
Stella, G. M., Kolling, S., Benvenuti, S., & Bortolotto, C. (2019) · Cancers · doi:10.3390/cancers11071010 · Cited by 103
Dormant disseminated tumor cells and cancer stem/progenitor-like cells: Similarities and opportunities
Hen, O., & Barkan, D. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.09.002 · Cited by 100
Fatty acid synthase regulates invasion and metastasis of colorectal cancer via Wnt signaling pathway
Wang, H., Xi, Q., & Wu, G. (2016) · Cancer Medicine · doi:10.1002/cam4.711 · Cited by 96
Tuning Cancer Fate: Tumor Microenvironment's Role in Cancer Stem Cell Quiescence and Reawakening
Sistigu, A., Musella, M., Galassi, C., Vitale, I., & Maria, R. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02166 · Cited by 102
Mechanisms of Metastatic Tumor Dormancy and Implications for Cancer Therapy
Neophytou, C. M., Kyriakou, T.-C., & Papageorgis, P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20246158 · Cited by 96
Beyond Tumor Suppression: Senescence in Cancer Stemness and Tumor Dormancy
Triana-Martínez, F., Loza, M. I., & Domínguez, E. (2020) · Cells · doi:10.3390/cells9020346 · Cited by 102
Long non-coding RNA NR2F1-AS1 induces breast cancer lung metastatic dormancy by regulating NR2F1 and ΔNp63
Liu, Y., Zhang, P., Wu, Q., Fang, H., Wang, Y., Xiao, Y., Cong, M., Wang, T., He, Y., Ma, C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25552-0 · Cited by 97
Engineering 3D approaches to model the dynamic microenvironments of cancer bone metastasis
Qiao, H., & Tang, T. (2018) · Bone Research · doi:10.1038/s41413-018-0008-9 · Cited by 94
Roles of Wnt Target Genes in the Journey of Cancer Stem Cells
Kim, J., Park, S.-Y., Jun, Y., Kim, J., & Nam, J. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18081604 · Cited by 93

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