The DOI matches its Crossref record; 228 of the 228 references it cites were found in a registry or an index.
How the ageing microenvironment influences tumour progression
Open accessAbstract
Most cancers arise in individuals over the age of 60. As the world population is living longer and reaching older ages, cancer is becoming a substantial public health problem. It is estimated that, by 2050, more than 20% of the world's population will be over the age of 60 - the economic, healthcare and financial burdens this may place on society are far from trivial. In this Review, we address the role of the ageing microenvironment in the promotion of tumour progression. Specifically, we discuss the cellular and molecular changes in non-cancerous cells during ageing, and how these may contribute towards a tumour permissive microenvironment; these changes encompass biophysical alterations in the extracellular matrix, changes in secreted factors and changes in the immune system. We also discuss the contribution of these changes to responses to cancer therapy as ageing predicts outcomes of therapy, including survival. Yet, in preclinical studies, the contribution of the aged microenvironment to therapy response is largely ignored, with most studies designed in 8-week-old mice rather than older mice that reflect an age appropriate to the disease being modelled. This may explain, in part, the failure of many successful preclinical therapies upon their translation to the clinic. Overall, the intention of this Review is to provide an overview of the interplay that occurs between ageing cell types in the microenvironment and cancer cells and how this is likely to impact tumour metastasis and therapy response.
Overview
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
Cites
Statistics
Verification
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?
The cited source says what the claim attributes to it.
In the citing paper
“In addition to the accumulation of genomic mutations over time, age-related cellular senescence also contributes to cancer development and progression (2).”
From Chromatin conformational changes at human satellite II contribute to the senescence phenotype in the tumor microenvironment (2023) · cites this paper as [2]
The cited source says what the claim attributes to it.
In the citing paper
“SASP has been linked to the aggressiveness of certain cancers (2, 10).”
From Chromatin conformational changes at human satellite II contribute to the senescence phenotype in the tumor microenvironment (2023) · cites this paper as [2]
In the citing paper
“However, the main obstacle to achieving efficacious immunotherapy is the tumor microenvironment (TME), which may accelerate senescence of the immune system [18, 19]: potential targets for rejuvenating the immune system are still a hypothesis.”
From Immunosenescence: a key player in cancer development (2020) · cites this paper as [18]
In the citing paper
“Furthermore, in aging TME, changes in immune cell function and secretion of SASP molecules dramatically affect tumor progression [18].”
From Immunosenescence: a key player in cancer development (2020) · cites this paper as [18]
In the citing paper
“Finally, emerging evidence suggests that the aging microenvironment largely contributes to age-related decline in immune function and may also provide potential targets for rejuvenating the immune system [18].”
From Immunosenescence: a key player in cancer development (2020) · cites this paper as [18]
In the citing paper
“as well as due to biophysical alterations of the extracellular matrix that affect the mobility and placement of immune effectors.261”
From Meta-hallmarks of aging and cancer (2023) · cites this paper as [261]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
1 retracted
Items 201–228 of 228
Changes with Advancing Age in the Cell Population of Human Dermis
Andrew, W., Behnke, R. H., & Sato, T. (2009) · Gerontology · doi:10.1159/000211369 · Cited by 47
Targeted therapy and elderly people: A review
Daste, A., Chakiba, C., Domblides, C., Gross‐Goupil, M., Quivy, A., Ravaud, A., & Soubeyran, P. (2016) · European Journal of Cancer · doi:10.1016/j.ejca.2016.10.005 · Cited by 47
Friedman, C. F., Horvat, T. Z., Minehart, J. C., Panageas, K. S., Callahan, M. K., Chapman, P. B., Momtaz, P., Postow, M. A., Shoushtari, A. N., Wolchok, J. D., et al. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.34.15_suppl.10009 · Cited by 47
Bad company: Microenvironmentally mediated resistance to targeted therapy in melanoma
Almeida, F. V., Douglass, S. M., Fane, M. E., & Weeraratna, A. T. (2018) · Pigment Cell & Melanoma Research · doi:10.1111/pcmr.12736 · Cited by 47
Self-citationConsiderations for successful cancer immunotherapy in aged hosts
Hurez, V. J., Padron, A. S., Svatek, R. S., & Curiel, T. J. (2017) · Experimental Gerontology · doi:10.1016/j.exger.2017.10.002 · Cited by 46
Hodi, F. S., Postow, M. A., Chesney, J. A., Pavlick, A. C., Robert, C., Grossmann, K. F., McDermott, D. F., Linette, G. P., Meyer, N., Giguere, J. K., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2015.33.15_suppl.9004 · Cited by 44
Freedman, R. A., Dockter, T., Lafky, J. M., Hurria, A., Muss, H. J., Cohen, H. J., Jatoi, A., Kemeny, M. M., & Ruddy, K. J. (2018) · The Oncologist · doi:10.1634/theoncologist.2018-0033 · Cited by 41
An early age‐related increase in the frequency of CD4+ Foxp3+ cells in BDC2·5NOD mice
Thomas, D., Mellanby, R. J., Phillips, J. M., & Cooke, A. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02604.x · Cited by 40
Onyema, O. O., Decoster, L., Njemini, R., Forti, L. N., Bautmans, I., Waele, M. D., & Mets, T. F. (2015) · BMC Cancer · doi:10.1186/s12885-015-2013-3 · Cited by 38
Senescence in the aging process
Faragher, R., McArdle, A., Willows, A. O. D., & Ostler, E. L. (2017) · F1000Research · doi:10.12688/f1000research.10903.1 · Cited by 38
Age‐related changes in the occurrence and characteristics of thymic CD4+ CD25+ T cells in mice
Kozłowska, E., Biernacka, M., Ciechomska, M., & Drela, N. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02667.x · Cited by 37
Age changes in the number and proliferation of fibroblasts in the human skin
Gunin, G., Корнилова, Н. К., Petrov, V. V., & Vasilyeva, O. V. (2011) · Advances in Gerontology · doi:10.1134/s2079057011040059 · Cited by 33
Young Age and Aggressive Treatment in Colon Cancer
Berian, J. R., Benson, A. B., & Nelson, H. (2015) · JAMA · doi:10.1001/jama.2015.9379 · Cited by 32
Taş, F., & Ertürk, K. (2017) · Molecular and Clinical Oncology · doi:10.3892/mco.2017.1439 · Cited by 32
Jackaman, C., & Nelson, D. J. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1120-5 · Cited by 29
Influence of Immune Myeloid Cells on the Extracellular Matrix During Cancer Metastasis
Jiang, D. G., & Lim, S. Y. (2016) · Cancer Microenvironment · doi:10.1007/s12307-016-0181-6 · Cited by 29
Dysregulation of IL-33/ST2 signaling and myocardial periarteriolar fibrosis
Garbern, J. C., Williams, J., Kristl, A. C., Malick, A., Rachmin, I., Gaeta, B., Ahmed, N., Vujić, A., Libby, P., & Lee, R. T. (2019) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2019.01.018 · Cited by 26
Page, A. J., Li, A., Hestley, A. C., Murray, D., Carlson, G. W., & Delman, K. A. (2012) · International Journal of Surgical Oncology · doi:10.1155/2012/456987 · Cited by 23
Regional differences in renewal rates of fibroblasts in young adult female mice
Ruchti, C., Haller, D., Nuber, M., & Cottier, H. (1983) · Cell and Tissue Research · doi:10.1007/bf00216434 · Cited by 20
Crosslinked CNBr-activated hyaluronan-collagen matrices: Effects on fibroblast contraction
Huang, L. L. H., & Nimni, M. E. (1994) · Matrix Biology · doi:10.1016/0945-053x(94)90004-3 · Cited by 17
An N‐terminal peptide from link protein is rapidly degraded by chondrocytes, monocytes and B cells
Martin, H., & Dean, M. C. (1993) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1993.tb17636.x · Cited by 13
Evaluation of age effects on doxorubicin-induced toxicity in mesenchymal stem cells
Dezfouli, A. B., Pourfathollah, A. A., Amoli, J. S., Khosravi, M., Nikogoftar-Zarif, M., Yazdi, M., & Ali-Esfahani, T. (2017) · Medical Journal of the Islamic Republic of Iran · doi:10.14196/mjiri.31.98 · Cited by 11
Grigorescu, A. C. (2015) · Journal of Translational Internal Medicine · doi:10.4103/2224-4018.154291 · Cited by 10
Gettinger, S. N., Horn, L., Ramalingam, S. S., Spigel, D. R., Paz-Ares, L. G., Paik, P. K., Reck, M., Reckamp, K. L., Mazières, J., Stinchcombe, T. E., et al. (2015) · European Journal of Cancer · doi:10.1016/s0959-8049(16)31735-x · Cited by 10
de Figueiredo, Á. S. P., Hurez, V. J., Liu, A., & Curiel, T. J. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.196.supp.213.4 · Cited by 9
Age-Related Increase Of IL-33 In Non-Eosinophilic Nasal Polyps
Kim, D. W., Kim, D., Kong, I. G., Eun, K. M., Casale, T. B., & Cho, S. (2018) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.12.213 · Cited by 2
Immunosenescence in testicular cancer survivors treated with chemotherapy.
Bourlon, M. T., Velazquez, H. E., Hinojosa, J., Lima, G., Rios-Corzo, R., Jimenez-Martinez, K., Zarco-Letzel, G., Llorente, L., & Atisha‐Fregoso, Y. (2017) · Journal of Clinical Oncology · doi:10.1200/jco.2017.35.15_suppl.e16037 · Cited by 1
Cited by
Sorted by citations
The evolving tumor microenvironment: From cancer initiation to metastatic outgrowth
de Visser, K. E., & Joyce, J. A. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.02.016 · Cited by 4,059
Hypoxic microenvironment in cancer: molecular mechanisms and therapeutic interventions
Chen, Z., Han, F., Du, Y., Shi, H., & Zhou, W. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01332-8 · Cited by 1,612
Crosby, D., Bhatia, S., Brindle, K. M., Coussens, L. M., Dive, C., Emberton, M., Esener, S., Fitzgerald, R. C., Gambhir, S. S., Kuhn, P., et al. (2022) · Science · doi:10.1126/science.aay9040 · Cited by 1,379
Diversity and biology of cancer-associated fibroblasts
Biffi, G., & Tuveson, D. A. (2021) · Physiological Reviews · doi:10.1152/physrev.00048.2019 · Cited by 1,265
Intratumor Heterogeneity: The Rosetta Stone of Therapy Resistance
Marusyk, A., Janiszewska, M., & Polyak, K. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.03.007 · Cited by 1,009
Metadata
- Authors
- Fane, M., & Weeraratna, A. T.
- Affiliations
- The Wistar Institute (US)
- Corresponding author
- Fane, Mitchell
- Weeraratna, Ashani T.
- Venue
- Nature Reviews Cancer
- Published
- 2019-12-13
- Volume
- 20
- Issue
- 2
- Pages
- 89-106
- ISSN
- 1474-175X (ISSN-L)
- 1474-1768
- PMC
- PMC7377404
- OpenAlex
- W2995607278
- Cited by
- 849
- References
- 228
- Citations by year
- 2026: 109 · 2025: 176 · 2024: 166 · 2023: 130 · 2022: 122 · 2021: 92 · 2020: 54
- FWCI
- 6.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature reviews. Cancer (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA207935, P01CA114046, R01CA174746, R01CA232256, P30CA010815, P30CA006973)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- tumor microenvironment, aging, tumor progression, extracellular matrix, secreted factors, cancer therapy response, tumour metastasis, preclinical mouse models
- MeSH terms
- Aging, Animals, Cell Transformation, Neoplastic, Combined Modality Therapy, Extracellular Matrix, Humans, Neoplasms, Treatment Outcome, Stromal Cells, Disease Progression, Tumor Microenvironment
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