Cancer as a disease of old age: changing mutational and microenvironmental landscapes
Open accessAbstract
Why do we get cancer mostly when we are old? According to current paradigms, the answer is simple: mutations accumulate in our tissues throughout life, and some of these mutations contribute to cancers. Although mutations are necessary for cancer development, a number of studies shed light on roles for ageing and exposure-dependent changes in tissue landscapes that determine the impact of oncogenic mutations on cellular fitness, placing carcinogenesis into an evolutionary framework. Natural selection has invested in somatic maintenance to maximise reproductive success. Tissue maintenance not only ensures functional robustness but also prevents the occurrence of cancer through periods of likely reproduction by limiting selection for oncogenic events in our cells. Indeed, studies in organisms ranging from flies to humans are revealing conserved mechanisms to eliminate damaged or oncogenically initiated cells from tissues. Reports of the existence of striking numbers of oncogenically initiated clones in normal tissues and of how this clonal architecture changes with age or external exposure to noxious substances provide critical insight into the early stages of cancer development. A major challenge for cancer biology will be the integration of these studies with epidemiology data into an evolutionary theory of carcinogenesis, which could have a large impact on addressing cancer risk and treatment.
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
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 theory of adaptive oncogenesis stipulates that environmental factors associated with tissue decline, such as inflammation, are crucial drivers of oncogenesis by selecting for emergent phenotypes, such as increased proliferation, self-renewal, or survival, that are linked to cancer-associated mutations.
“the theory of adaptive oncogenesis, which stipulates that environmental factors associated with tissue decline, such as inflammation, are crucial drivers of oncogenesis by selecting for emergent phenotypes, such as increased proliferation, self-renewal, or survival, that are linked cancer-associated mutations (Henry et al., 2015; Laconi et al., 2020).”
From PU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress (2021) · cites this paper as Laconi et al., 2020
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
The Evolution and Ecology of Resistance in Cancer TherapyPreprint
Gatenby, R. A., & Brown, J. S. (2017) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a033415 · Cited by 130 · see citing works
RetractedSiegel, R. L., Miller, K. D., & Jemal, A. (2018) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21442 · Cited by 16,632 · see citing works
Age-related clonal hematopoiesis associated with adverse outcomes
Jaiswal, S., Fontanillas, P., Flannick, J., Manning, A., Grauman, P. V., Mar, B. G., Lindsley, R. C., Mermel, C. H., Burtt, N., Chavez, A., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1408617 · Cited by 4,841 · see citing works
Pleiotropy, natural selection, and the evolution of senescence.
Williams, G. C. (1957) · Evolution · doi:10.1111/j.1558-5646.1957.tb02911.x · Cited by 4,279 · see citing works
Rapamycin fed late in life extends lifespan in genetically heterogeneous mice
Harrison, D. E., Strong, R., Sharp, Z. D., Nelson, J. F., Astle, C. M., Flurkey, K., Nadon, N. L., Wilkinson, J. E., Frenkel, K., Carter, C. S., et al. (2009) · Nature · doi:10.1038/nature08221 · Cited by 3,766 · see citing works
Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence
Genovese, G., Kähler, A. K., Handsaker, R. E., Lindberg, J., Rose, S. A., Bakhoum, S. F., Chambert, K., Mick, E., Neale, B. M., Fromer, M., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1409405 · Cited by 3,531 · see citing works
Naturally occurring p16Ink4a-positive cells shorten healthy lifespan
Baker, D. J., Childs, B. G., Durik, M., Wijers, M. E., Sieben, C. J., Zhong, J., A. Saltness, R., Jeganathan, K. B., Verzosa, G. C., Pezeshki, A., et al. (2016) · Nature · doi:10.1038/nature16932 · Cited by 2,891 · see citing works
The moulding of senescence by natural selection
Hamilton, W. D. O. (1966) · Journal of Theoretical Biology · doi:10.1016/0022-5193(66)90184-6 · Cited by 2,273 · see citing works
Understanding the odd science of aging
Kirkwood, T. B. L. (2005) · Cell · doi:10.1016/j.cell.2005.01.027 · Cited by 1,984 · see citing works
Variation in cancer risk among tissues can be explained by the number of stem cell divisions
Tomasetti, C., & Vogelstein, B. (2015) · Science · doi:10.1126/science.1260825 · Cited by 1,927 · see citing works
Age-related mutations associated with clonal hematopoietic expansion and malignancies
Xie, M., Lu, C., Wang, J., McLellan, M. D., Johnson, K. J., Wendl, M. C., McMichael, J. F., Schmidt, H. K., Yellapantula, V., Miller, C. A., et al. (2014) · Nature Medicine · doi:10.1038/nm.3733 · Cited by 1,874 · see citing works
AN UNSOLVED PROBLEM OF BIOLOGY
(1953) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.1953.tb84985.x · Cited by 1,805 · see citing works
High burden and pervasive positive selection of somatic mutations in normal human skin
Martincorena, I., Roshan, A., Gerstung, M., Ellis, P., Van Loo, P., McLaren, S., Wedge, D. C., Fullam, A., Alexandrov, L. B., Tubio, J. M., et al. (2015) · Science · doi:10.1126/science.aaa6806 · Cited by 1,770 · see citing works
Senescence surveillance of pre-malignant hepatocytes limits liver cancer development
Kang, T.-W., Yevsa, T., Woller, N., Hoenicke, L., Wuestefeld, T., Dauch, D., Hohmeyer, A., Gereke, M., Rudalska, R., Potapova, A., et al. (2011) · Nature · doi:10.1038/nature10599 · Cited by 1,621 · see citing works
Mittal, D., Gubin, M. M., Schreiber, R. D., & Smyth, M. J. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.01.004 · Cited by 1,471 · see citing works
Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention
Tomasetti, C., Li, L., & Vogelstein, B. (2017) · Science · doi:10.1126/science.aaf9011 · Cited by 1,113 · see citing works
Somatic mutant clones colonize the human esophagus with age
Martincorena, I., Fowler, J. C., Wabik, A., Lawson, A. R. J., Abascal, F., Hall, M. W. J., Cagan, A., Murai, K., Mahbubani, K., Stratton, M. R., et al. (2018) · Science · doi:10.1126/science.aau3879 · Cited by 1,113 · see citing works
An estimation of the number of cells in the human body
Bianconi, E., Piovesan, A., Facchin, F., Beraudi, A., Casadei, R., Frabetti, F., Vitale, L., Pelleri, M. C., Tassani, S., Piva, F., et al. (2013) · Annals of Human Biology · doi:10.3109/03014460.2013.807878 · Cited by 1,012 · see citing works
Minutes: Mutants of Drosophila autonomously affecting cell division rate
Morata, G., & Ripoll, P. L. (1975) · Developmental Biology · doi:10.1016/0012-1606(75)90330-9 · Cited by 983 · see citing works
Senescence and apoptosis: dueling or complementary cell fates?
Childs, B. G., Baker, D. J., Kirkland, J. L., Campisi, J., & van Deursen, J. M. (2014) · The EMBO Reports · doi:10.15252/embr.201439245 · Cited by 915 · see citing works
Coombs, C. C., Zehir, A., Devlin, S. M., Kishtagari, A., Syed, A., Jonsson, P., Hyman, D. M., Solit, D. B., Robson, M. E., Baselga, J., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.07.010 · Cited by 866 · see citing works
Finegold, J. A., Asaria, P., & Francis, D. P. (2012) · International Journal of Cardiology · doi:10.1016/j.ijcard.2012.10.046 · Cited by 861 · see citing works
Prediction of acute myeloid leukaemia risk in healthy individuals
Abelson, S., Collord, G., Ng, S. W. K., Weissbrod, O., Mendelson Cohen, N., Niemeyer, E., Barda, N., Zuzarte, P. C., Heisler, L., Sundaravadanam, Y., et al. (2018) · Nature · doi:10.1038/s41586-018-0317-6 · Cited by 850 · see citing works
Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis
Sharpless, N. E., Bardeesy, N., Lee, K.-H., Carrasco, D., Castrillon, D. H., Aguirre, A. J., Wu, E. A., Horner, J. W., & DePinho, R. A. (2001) · Nature · doi:10.1038/35092592 · Cited by 848 · see citing works
Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis
Busque, L., Patel, J. P., Figueroa, M. E., Vasanthakumar, A., Provost, S., Hamilou, Z., Mollica, L., Li, J., Viale, A., Heguy, A., et al. (2012) · Nature Genetics · doi:10.1038/ng.2413 · Cited by 830 · see citing works
Overexpression of Atg5 in mice activates autophagy and extends lifespan
Pyo, J.-O., Yoo, S.-M., Ahn, H.-H., Nah, J., Hong, S.-H., Kam, T.-I., Jung, S., & Jung, Y.-K. (2013) · Nature Communications · doi:10.1038/ncomms3300 · Cited by 721 · see citing works
Clonal haematopoiesis harbouring AML-associated mutations is ubiquitous in healthy adults
Young, A. L., Challen, G. A., Birmann, B. M., & Druley, T. E. (2016) · Nature Communications · doi:10.1038/ncomms12484 · Cited by 692 · see citing works
Frequent clones of p53-mutated keratinocytes in normal human skin
Jonason, A. S., Kunala, S., Price, G. J., Restifo, R. J., Spinelli, H. M., Persing, J. A., Leffell, D. J., Tarone, R. E., & Brash, D. E. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.14025 · Cited by 685 · see citing works
Substantial contribution of extrinsic risk factors to cancer development
Wu, S., Powers, S., Zhu, W., & Hannun, Y. A. (2015) · Nature · doi:10.1038/nature16166 · Cited by 667 · see citing works
The senescence-associated secretory phenotype induces cellular plasticity and tissue regeneration.
Ritschka, B., Storer, M., Mas, A., Heinzmann, F., Ortells, M. C., Morton, J. P., Sansom, O. J., Zender, L., & Keyes, W. M. (2017) · Genes & Development · doi:10.1101/gad.290635.116 · Cited by 650 · see citing works
An atlas of the aging lung mapped by single cell transcriptomics and deep tissue proteomics
Angelidis, I., Simon, L. M., Fernandez, I. E., Strunz, M., Mayr, C. H., Greiffo, F. R., Tsitsiridis, G., Ansari, M., Graf, E., Strom, T.-M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08831-9 · Cited by 637 · see citing works
Disruption of the beclin 1–BCL2 autophagy regulatory complex promotes longevity in mice
Fernández, Á. F., Sebti, S., Wei, Y., Zou, Z., Shi, M., McMillan, K. L., He, C., Ting, T., Liu, Y., Chiang, W.-C., et al. (2018) · Nature · doi:10.1038/s41586-018-0162-7 · Cited by 630 · see citing works
Age-related remodelling of oesophageal epithelia by mutated cancer drivers
Yokoyama, A., Kakiuchi, N., Yoshizato, T., Nannya, Y., Suzuki, H., Takeuchi, Y., Shiozawa, Y., Sato, Y., Aoki, K., Kim, S. K., et al. (2019) · Nature · doi:10.1038/s41586-018-0811-x · Cited by 628 · cited 3× · see citing works
“The nature of the selective environment is crucial to the genotype/phenotype of the clone that emerges, as one would expect.(85) In the haematopoietic system, age-related clonal expansions involving TP53 and spliceosome genes are predictive of the later development of acute myeloid leukaemia,(103) and clones with TP53…”
BackgroundLung Cancer in Never Smokers: Clinical Epidemiology and Environmental Risk Factors
Samet, J. M., Ávila-Tang, É., Boffetta, P., Hannan, L. M., Olivo‐Marston, S., Thun, M. J., & Rudin, C. M. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0376 · Cited by 568 · see citing works
Integrating evolutionary dynamics into treatment of metastatic castrate-resistant prostate cancer
Zhang, J., Cunningham, J. J., Brown, J. S., & Gatenby, R. A. (2017) · Nature Communications · doi:10.1038/s41467-017-01968-5 · Cited by 557 · see citing works
Leukemia-associated somatic mutations drive distinct patterns of age-related clonal hemopoiesis
McKerrell, T., Park, N., Moreno, T., Grove, C. S., Ponstingl, H., Stephens, J., Crawley, C., Craig, J., Scott, M. A., Hodkinson, C., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.005 · Cited by 534 · see citing works
Essential role for autophagy in life span extension
Madeo, F., Zimmermann, A., Maiuri, M. C., & Kroemer, G. (2015) · Journal of Clinical Investigation · doi:10.1172/jci73946 · Cited by 464 · see citing works
Bolton, H., Graham, S. J. L., der Aa, N. V., Kumar, P., Theunis, K., Gallardo, E. F., Voet, T., & Zernicka‐Goetz, M. (2016) · Nature Communications · doi:10.1038/ncomms11165 · Cited by 451 · see citing works
Clonal Hematopoiesis and Evolution to Hematopoietic Malignancies
Bowman, R. L., Busque, L., & Levine, R. L. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.011 · Cited by 448 · see citing works
Age as a determinant of renal sodium conservation in normal man.
Kirkendall, A. M., Connor, W. E., Abboud, F. M., Rastogi, S., Anderson, T. A., & Fry, M. M. (1976) · PubMed · Cited by 429 · see citing works
PPM1D Mutations Drive Clonal Hematopoiesis in Response to Cytotoxic Chemotherapy
Hsu, J. I., Dayaram, T., Tovy, A., De Braekeleer, E., Jeong, M., Wang, F., Zhang, J., Heffernan, T. P., Gera, S., Kovacs, J. J., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.10.004 · Cited by 425 · see citing works
Stem cell competition orchestrates skin homeostasis and ageing
Liu, N., Matsumura, H., Kato, T., Ichinose, S., Takada, A., Namiki, T., Asakawa, K., Morinaga, H., Mohri, Y., De Arcangelis, A., et al. (2019) · Nature · doi:10.1038/s41586-019-1085-7 · Cited by 422 · see citing works
Preleukaemic clonal haemopoiesis and risk of therapy-related myeloid neoplasms: a case-control study
Takahashi, K., Wang, F., Kantarjian, H., Doss, D., Khanna, K., Thompson, E., Zhao, L., Patel, K., Neelapu, S., Gumbs, C., et al. (2017) · The Lancet Oncology · doi:10.1016/s1470-2045(16)30626-x · Cited by 399 · see citing works
Targeting Inflammation in Cancer Prevention and Therapy
Todoric, J., Antonucci, L., & Karin, M. (2016) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-16-0209 · Cited by 367 · see citing works
NKG2D ligands mediate immunosurveillance of senescent cells
Sagiv, A., Burton, D. G. A., Moshayev, Z., Vadai, E., Wensveen, F., Ben-Dor, S., Golani, O., Polic, B., & Krizhanovsky, V. (2016) · Aging · doi:10.18632/aging.100897 · Cited by 345 · see citing works
(1999) · PubMed · Cited by 338 · see citing works
Age-related physiological changes and their clinical significance.
Boss, G. R., & Seegmiller, J. E. (1981) · PubMed · Cited by 325 · see citing works
Risk of Colorectal Cancer in the Families of Patients with Adenomatous Polyps
Winawer, S. J., Zauber, A. G., Gerdes, H., O’Brien, M. J., Gottlieb, L. S., Sternberg, S. S., Bond, J. H., Waye, J. D., Schapiro, M., Panish, J. F., et al. (1996) · New England Journal of Medicine · doi:10.1056/nejm199601113340204 · Cited by 324 · see citing works
Of mice and men: the benefits of caloric restriction, exercise, and mimetics
Mercken, E. M., Carboneau, B. A., Krzysik-Walker, S. M., & de Cabo, R. (2012) · Ageing Research Reviews · doi:10.1016/j.arr.2011.11.005 · Cited by 318 · see citing works
Gillis, N. K., Ball, M., Zhang, Q., Ma, Z., Zhao, Y., Yoder, S. J., Balasis, M. E., Mesa, T. E., Sallman, D. A., Lancet, J. E., et al. (2017) · The Lancet Oncology · doi:10.1016/s1470-2045(16)30627-1 · Cited by 317 · see citing works
Phillip, J. M., Aifuwa, I., Walston, J. D., & Wirtz, D. (2015) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071114-040829 · Cited by 293 · see citing works
Layde, P. M., Webster, L. A., Baughman, A. L., Wingo, P. A., Gl, R., & Ory, H. W. (1989) · Journal of Clinical Epidemiology · doi:10.1016/0895-4356(89)90161-3 · Cited by 287 · see citing works
Older age becomes common late in human evolution
Caspari, R., & Lee, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402857101 · Cited by 273 · see citing works
Somatic Mutations Increase Hepatic Clonal Fitness and Regeneration in Chronic Liver Disease
Zhu, M., Lu, T., Jia, Y., Luo, X., Gopal, P., Li, L., Odewole, M., Renteria, V., Singal, A. G., Jang, Y., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.026 · Cited by 250 · see citing works
Autophagy and aging: Maintaining the proteome through exercise and caloric restriction
Escobar, K. A., Cole, N. H., Mermier, C. M., & VanDusseldorp, T. A. (2018) · Aging Cell · doi:10.1111/acel.12876 · Cited by 226 · see citing works
Kahn, J. D., Miller, P. G., Silver, A. J., Sellar, R. S., Bhatt, S., Gibson, C., McConkey, M., Adams, D., Mar, B., Mertins, P., et al. (2018) · Blood · doi:10.1182/blood-2018-05-850339 · Cited by 225 · see citing works
Aging and the rise of somatic cancer-associated mutations in normal tissues
Risques, R. A., & Kennedy, S. R. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007108 · Cited by 212 · see citing works
New Insights into the Troubles of Aneuploidy
Siegel, J. J., & Amon, A. (2012) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155807 · Cited by 204 · see citing works
Senolytics and senostatics as adjuvant tumour therapy
Short, S. C., Fielder, E., Miwa, S., & von Zglinicki, T. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.01.056 · Cited by 201 · see citing works
Cell competition: how to eliminate your neighbours
Amoyel, M., & Bach, E. A. (2014) · Development · doi:10.1242/dev.079129 · Cited by 199 · see citing works
Ogrodnik, M., Salmonowicz, H., & Gladyshev, V. N. (2019) · Aging Cell · doi:10.1111/acel.12841 · Cited by 184 · see citing works
Rapamycin and Alzheimer’s disease: Time for a clinical trial?
Kaeberlein, M. R., & Galván, V. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aar4289 · Cited by 171 · see citing works
Elimination of Unfit Cells Maintains Tissue Health and Prolongs Lifespan
Merino, M. M., Rhiner, C., López-Gay, J. M., Buechel, D., Hauert, B., & Moreno, E. (2015) · Cell · doi:10.1016/j.cell.2014.12.017 · Cited by 170 · see citing works
Somatic mutation and clonal expansions in human tissues
Martincorena, I. (2019) · Genome Medicine · doi:10.1186/s13073-019-0648-4 · Cited by 166 · see citing works
Correction of aberrant growth preserves tissue homeostasis
Brown, S., Pineda, C. M., Xin, T., Boucher, J. D., Suozzi, K. C., Park, S., Matte-Martone, C. C., Gonzalez, D. G., Rytlewski, J. A., Beronja, S., et al. (2017) · Nature · doi:10.1038/nature23304 · Cited by 151 · see citing works
Cell competition: the winners and losers of fitness selection
Bowling, S., Lawlor, K., & Rodríguez, T. A. (2019) · Development · doi:10.1242/dev.167486 · Cited by 149 · see citing works
Glossmann, H. H., & Lutz, O. M. D. (2019) · Gerontology · doi:10.1159/000502257 · Cited by 149 · see citing works
Aging-associated inflammation promotes selection for adaptive oncogenic events in B cell progenitors
Henry, C. J., Casás-Selves, M., Kim, J., Zaberezhnyy, V., Aghili, L., Daniel, A. E., Jimenez, L., Azam, T., McNamee, E. N., Clambey, E. T., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci83024 · Cited by 148 · see citing works
Self-citationDistinct modes of cell competition shape mammalian tissue morphogenesis
Ellis, S. J., Gomez, N. C., Levorse, J. M., Mertz, A. F., Ge, Y., & Fuchs, E. V. (2019) · Nature · doi:10.1038/s41586-019-1199-y · Cited by 147 · see citing works
Somatic mutations, genome mosaicism, cancer and aging
Vijg, J. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2014.04.002 · Cited by 134 · see citing works
Evolved Tumor Suppression: Why Are We So Good at Not Getting Cancer?
DeGregori, J. V. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0342 · Cited by 127 · see citing works
Self-citationSasaki, A., Nagatake, T., Egami, R., Gu, G., Takigawa, I., Ikeda, W., Nakatani, T., Kunisawa, J., & Fujita, Y. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.104 · Cited by 125 · see citing works
Matai, L., Sarkar, G. C., Chamoli, M., Malik, Y., Kumar, R., Rautela, U., Jana, N. R., Chakraborty, K., & Mukhopadhyay, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1900055116 · Cited by 120 · see citing works
Rozhok, A. I., & DeGregori, J. V. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501713112 · Cited by 115 · see citing works
Self-citationKajita, M., & Fujita, Y. (2015) · The Journal of Biochemistry · doi:10.1093/jb/mvv050 · Cited by 111 · see citing works
Eldredge, N. (1998) · Cited by 109 · see citing works
The discontinuity theory of immunity
Pradeu, T., & Vivier, É. (2016) · Science Immunology · doi:10.1126/sciimmunol.aag0479 · Cited by 108 · see citing works
Outcompeting p53-Mutant Cells in the Normal Esophagus by Redox Manipulation
Fernández‐Antorán, D., Piedrafita, G., Murai, K., Ong, S. H., Herms, A., Frezza, C., & Jones, P. H. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.06.011 · Cited by 108 · see citing works
Pfau, S. J., Silberman, R. E., Knouse, K. A., & Amon, A. (2016) · Genes & Development · doi:10.1101/gad.278820.116 · Cited by 107 · see citing works
Menstrual Cycling and Breast Cancer: An Evolutionary Perspective
Strassmann, B. I. (1999) · Journal of Women s Health · doi:10.1089/jwh.1999.8.193 · Cited by 104 · see citing works
The evolving concept of tumor microenvironments
Laconi, E. (2007) · BioEssays · doi:10.1002/bies.20606 · Cited by 98 · see citing works
Self-citationSalk, J. J., Loubet-Senear, K. J., Maritschnegg, E., Valentine, C. C., Williams, L. N., Higgins, J. E., Horvat, R., Vanderstichele, A., Nachmanson, D., Baker, K. T., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.109 · Cited by 98 · see citing works
UVB-induced apoptosis drives clonal expansion during skin tumor development
Zhang, W. (2004) · Carcinogenesis · doi:10.1093/carcin/bgh300 · Cited by 85 · see citing works
DeGregori, J. V. (2012) · Oncogene · doi:10.1038/onc.2012.281 · Cited by 84 · see citing works
Self-citationDeclining lymphoid progenitor fitness promotes aging-associated leukemogenesis
Henry, C. J., Marusyk, A., Zaberezhnyy, V., Adane, B., & DeGregori, J. V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005486107 · Cited by 83 · see citing works
Self-citationEldredge, N., & Gould, S. J. (1997) · Science · doi:10.1126/science.276.5311.337c · Cited by 82 · see citing works
A framework for how environment contributes to cancer risk
Hochberg, M., & Noble, R. (2017) · Ecology Letters · doi:10.1111/ele.12726 · Cited by 80 · see citing works
Plasticity of the neoplastic phenotype in vivo is regulated by epigenetic factors
McCullough, K. D., Coleman, W. B., Ricketts, S. L., Wilson, J. W., Smith, G. J., & Grisham, J. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15333 · Cited by 79 · see citing works
A generalized theory of age-dependent carcinogenesis
Rozhok, A. I., & DeGregori, J. V. (2019) · eLife · doi:10.7554/elife.39950 · Cited by 73 · see citing works
Self-citationMarusyk, A., & DeGregori, J. V. (2007) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2007.09.001 · Cited by 67 · see citing works
Self-citationCell competition in development: information from flies and vertebrates
Madan, E., Gogna, R., & Moreno, E. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.08.002 · Cited by 65 · see citing works
Acute DNA damage activates the tumour suppressor p53 to promote radiation-induced lymphoma
Lee, C., Castle, K. D., Moding, E. J., Blum, J. M., Williams, N. T., Luo, L., Ma, Y., Borst, L. B., Kim, Y., & Kirsch, D. G. (2015) · Nature Communications · doi:10.1038/ncomms9477 · Cited by 58 · see citing works
Contribution of an Aged Microenvironment to Aging-Associated Myeloproliferative Disease
Vas, V., Wandhoff, C., Dörr, K., Niebel, A., & Geiger, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031523 · Cited by 55 · see citing works
Deep sequencing as a probe of normal stem cell fate and preneoplasia in human epidermis
Simons, B. D. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516123113 · Cited by 53 · see citing works
Connecting Cancer to Its Causes Requires Incorporation of Effects on Tissue Microenvironments
DeGregori, J. V. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-1207 · Cited by 47 · see citing works
Self-citationCell competition and tumorigenesis in the imaginal discs of Drosophila
Morata, G., & Calleja, M. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.06.010 · Cited by 47 · see citing works
To adapt or not to adapt: Consequences of declining Adaptive Homeostasis and Proteostasis with age
Pomatto, L. C. D., Sun, P. Y., & Davies, K. J. A. (2018) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2018.05.006 · Cited by 42 · see citing works
A new history of life: the radical new discoveries about the origins and evolution of life on Earth
(2015) · Choice Reviews Online · doi:10.5860/choice.191055 · Cited by 42 · see citing works
Aging is associated with increased clonogenic potential in rat liver in vivo
Pasciu, D., Montisci, S., Greco, M., Doratiotto, S., Pitzalis, S., Pani, P., Laconi, S., & Laconi, E. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00230.x · Cited by 38 · see citing works
Self-citationParikh, N., Shuck, R. L., Gagea, M., Shen, L., & Donehower, L. A. (2017) · Aging Cell · doi:10.1111/acel.12691 · Cited by 35 · see citing works
Aging promotes neoplastic disease through effects on the tissue microenvironment
Marongiu, F., Serra, M. P., Doratiotto, S., Sini, M., Fanti, M., Cadoni, E., Serra, M., & Laconi, E. (2016) · Aging · doi:10.18632/aging.101128 · Cited by 30 · see citing works
Self-citationSerra, M., Marongiu, F., Pisu, M. G., Serra, M., & Laconi, E. (2019) · Aging · doi:10.18632/aging.102021 · Cited by 30 · see citing works
Self-citationCell-autonomous decrease in proliferative competitiveness of the aged hepatocyte
Serra, M. P., Marongiu, F., Marongiu, M. E., Contini, A., & Laconi, E. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.01.015 · Cited by 29 · see citing works
Self-citationApoptosis or senescence? Which exit route do epithelial cells and fibroblasts preferentially follow?
Georgakopoulou, E. A., Evangelou, K., Havaki, S., Townsend, P. A., Kanavaros, P., & Gorgoulis, V. G. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.03.010 · Cited by 28 · see citing works
Koopman, J. J. E., van Heemst, D., van Bodegom, D., Bonkowski, M. S., Sun, L. Y., & Bartke, A. (2016) · Aging · doi:10.18632/aging.100919 · Cited by 27 · see citing works
Reconceiving autoimmunity: An overview
Tauber, A. I. (2014) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2014.05.029 · Cited by 26 · see citing works
Gompertz’ survivorship law as an intrinsic principle of aging
Sas, A. A., Snieder, H., & Korf, J. (2012) · Medical Hypotheses · doi:10.1016/j.mehy.2012.02.004 · Cited by 24 · see citing works
Caloric restriction delays early phases of carcinogenesis via effects on the tissue microenvironment
Cadoni, E., Marongiu, F., Fanti, M., Serra, M., & Laconi, E. (2017) · Oncotarget · doi:10.18632/oncotarget.16421 · Cited by 21 · see citing works
Self-citationMarongiu, F., Serra, M. P., Sini, M., Angius, F., & Laconi, E. (2014) · Aging · doi:10.18632/aging.100631 · Cited by 20 · see citing works
Self-citationDecoy fitness peaks, tumor suppression, and aging
Higa, K. C., & DeGregori, J. V. (2019) · Aging Cell · doi:10.1111/acel.12938 · Cited by 19 · see citing works
Self-citationFleenor, C. J., Rozhok, A. I., Zaberezhnyy, V., Mathew, D., Kim, J., Tan, A. C., Bernstein, I. D., & DeGregori, J. V. (2014) · Stem Cells · doi:10.1002/stem.1936 · Cited by 16 · see citing works
Self-citation(1976) · PubMed · Cited by 1 · see citing works
Kaplan (2000) · doi:10.1002/1520-6505(2000)9:4
Flagged first, then by citations
2 of the 115 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- [84]Martincorena, I., Fowler, J. C., Wabik, A., Lawson, A. R. J., Abascal, F., Hall, M. W. J. et al. Somatic mutant clones colonize the human esophagus with age. Science362, 911–917 (2018). PMC6298579 30337457
Cited by
Sorted by citations
Tumor initiation and early tumorigenesis: molecular mechanisms and interventional targets
Zhang, S., Xiao, X., Yi, Y., Wang, X., Zhu, L., Shen, Y., Lin, D., & Wu, C. H. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01848-7 · Cited by 440 · see citing works
Argentieri, M. A., Xiao, S., Bennett, D., Winchester, L. M., Nevado‐Holgado, A. J., Ghose, U., Albukhari, A., Yao, P., Mazidi, M., Lv, J., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-03164-7 · Cited by 378 · see citing works
Caiado, F., Pietras, E. M., & Manz, M. G. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20201541 · Cited by 289 · see citing works
Cancer evolution: Darwin and beyond
Vendramin, R., Litchfield, K., & Swanton, C. (2021) · The EMBO Journal · doi:10.15252/embj.2021108389 · Cited by 253 · see citing works
Immunosenescence, Inflammaging, and Frailty: Role of Myeloid Cells in Age-Related Diseases
Bleve, A., Motta, F., Durante, B., Pandolfo, C., Selmi, C., & Sica, A. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-021-08909-7 · Cited by 179 · see citing works
Aging drives <i>Tet2</i> <i>+/−</i> clonal hematopoiesis via IL-1 signaling
Caiado, F., Kovtonyuk, L. V., Gonullu, N. G., Fullin, J., Boettcher, S., & Manz, M. G. (2023) · Blood · doi:10.1182/blood.2022016835 · Cited by 161 · see citing works
Role of Reactive Oxygen Species in Aging and Age-Related Diseases: A Review
Anik, M. I., Mahmud, N., Masud, A. A., Khan, M. I., Islam, M. N., Uddin, S., & Hossain, M. K. (2022) · ACS Applied Bio Materials · doi:10.1021/acsabm.2c00411 · Cited by 156 · see citing works
Metabolic programs tailor T cell immunity in viral infection, cancer, and aging
Møller, S. H., Hsueh, P., Yu, Y.-R., Zhang, L., & Ho, P. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.02.003 · Cited by 148 · see citing works
Semmler, G., Meyer, E. L., Kozbial, K., Schwabl, P., Hametner‐Schreil, S., Zanetto, A., Bauer, D. J. M., Chromy, D., Simbrunner, B., Scheiner, B., et al. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.11.025 · Cited by 135 · see citing works
Clonal hematopoiesis: Mutation-specific adaptation to environmental change
Florez, M. A., Tran, B. T., Wathan, T. K., DeGregori, J., Pietras, E. M., & King, K. Y. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2022.05.006 · Cited by 129 · see citing works
Self-citationAn integrative analysis of the age-associated multi-omic landscape across cancers
Chatsirisupachai, K., Lesluyes, T., Paraoan, L., Loo, P. V., & de Magalhães, J. P. (2021) · Nature Communications · doi:10.1038/s41467-021-22560-y · Cited by 124 · see citing works
Roles of mitochondria in the hallmarks of metastasis
Scheid, A. D., Beadnell, T. C., & Welch, D. R. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-01125-8 · Cited by 124 · see citing works
Clonal hematopoiesis, somatic mosaicism, and age-associated disease
Evans, M. A., & Walsh, K. (2022) · Physiological Reviews · doi:10.1152/physrev.00004.2022 · Cited by 105 · see citing works
Identifying key questions in the ecology and evolution of cancer
Dujon, A. M., Aktipis, A., Alix‐Panabières, C., Amend, S. R., Boddy, A. M., Brown, J. S., Capp, J., DeGregori, J. V., Ewald, P. W., Gatenby, R. A., et al. (2020) · Evolutionary Applications · doi:10.1111/eva.13190 · Cited by 92 · see citing works
Self-citationPU.1 enforces quiescence and limits hematopoietic stem cell expansion during inflammatory stress
Chavez, J. S., Rabe, J. L., Loeffler, D., Higa, K. C., Hernandez, G., Mills, T. S., Ahmed, N., Gessner, R. L., Ke, Z., Idler, B. M., et al. (2021) · Journal of Experimental Medicine · doi:10.1084/jem.20201169 · Cited by 91 · see citing works
“These findings are consistent with the theory of adaptive oncogenesis, which stipulates that environmental factors associated with tissue decline, such as inflammation, are crucial drivers of oncogenesis by selecting for emergent phenotypes, such as increased proliferation, self-renewal, or survival, that are linked c…”
ResultSelf-citationCellular senescence in cancer: clinical detection and prognostic implications
Domen, A., Deben, C., Verswyvel, J., Flieswasser, T., Prenen, H., Peeters, M., Lardon, F., & Wouters, A. (2022) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-022-02555-3 · Cited by 94 · see citing works
Deterministic evolution and stringent selection during preneoplasia
Karlsson, K., Przybilla, M. J., Kotler, E., Khan, A., Xu, H., Karagyozova, K., Sockell, A., Wong, W. H., Liu, K., Mah, A., et al. (2023) · Nature · doi:10.1038/s41586-023-06102-8 · Cited by 83 · see citing works
How health systems can adapt to a population ageing with HIV and comorbid disease
Kiplagat, J., Tran, D. N., Barber, T., Njuguna, B., Vedanthan, R., Triant, V. A., & Pastakia, S. D. (2022) · The Lancet HIV · doi:10.1016/s2352-3018(22)00009-1 · Cited by 84 · see citing works
Untangling the web of intratumour heterogeneity
Li, Z., Seehawer, M., & Polyák, K. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00969-x · Cited by 81 · see citing works
Molecular principles underlying aggressive cancers
Nussinov, R., Yavuz, B. R., & Jang, H. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02129-7 · Cited by 86 · see citing works
The evolution and ecology of benign tumors
Boutry, J., Tissot, S., Újvári, B., Capp, J., Giraudeau, M., Nedelcu, A. M., & Frédéric Thomas, A. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188643 · Cited by 79 · see citing works
Age-associated differences in the cancer molecular landscape
Chatsirisupachai, K., Lagger, C., & de Magalhães, J. P. (2022) · Trends in cancer · doi:10.1016/j.trecan.2022.06.007 · Cited by 78 · see citing works
Lima, E., & Reis, L. V. D. (2023) · Molecules · doi:10.3390/molecules28135092 · Cited by 75 · see citing works
A generalized theory of age-dependent carcinogenesis
Rozhok, A. I., & DeGregori, J. V. (2019) · eLife · doi:10.7554/elife.39950 · Cited by 73 · see citing works
Self-citationMagnesium and the Hallmarks of Aging
Dominguez, L. J., Veronese, N., & Barbagallo, M. (2024) · Nutrients · doi:10.3390/nu16040496 · Cited by 75 · see citing works
Sarver, A. L., Makielski, K. M., DePauw, T. A., Schulte, A. J., & Modiano, J. F. (2022) · Aging and Cancer · doi:10.1002/aac2.12046 · Cited by 69 · see citing works
Role of E2F transcription factor in oral cancer: Recent insight and advancements
Kassab, A., Gupta, I., & Moustafa, A. A. (2023) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2023.03.004 · Cited by 68 · see citing works
Calorie Restriction for Cancer Prevention and Therapy: Mechanisms, Expectations, and Efficacy
Vidoni, C., Ferraresi, A., Esposito, A., Maheshwari, C., Dhanasekaran, D. N., Mollace, V., & Isidoro, C. (2021) · Journal of Cancer Prevention · doi:10.15430/jcp.2021.26.4.224 · Cited by 67 · see citing works
Understanding NK cell biology for harnessing NK cell therapies: targeting cancer and beyond
Shin, E., Bak, S. H., Park, T., Kim, J.-W., Yoon, S. R., Jung, H., & Noh, J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1192907 · Cited by 64 · see citing works
The importance of aging in cancer research
(2022) · Nature Aging · doi:10.1038/s43587-022-00231-x · Cited by 60 · see citing works
Somatic mutation and selection at population scale
Lawson, A. R. J., Abascal, F., Nicola, P. A., Lensing, S. V., Roberts, A. L., Kalantzis, G., Baez‐Ortega, A., Brzozowska, N., Moustafa, J. S. E.-S., Vaitkute, D., et al. (2025) · Nature · doi:10.1038/s41586-025-09584-w · Cited by 72 · see citing works
Ng, C. X., Affendi, M. M., Chong, P. P., & Lee, S. H. (2022) · Nutrition and Cancer · doi:10.1080/01635581.2022.2069274 · Cited by 58 · see citing works
Clonal hematopoiesis in sickle cell disease
Liggett, L. A., Cato, L. D., Weinstock, J. S., Zhang, Y., Nouraie, M. S., Gladwin, M. T., Garrett, M. E., Ashley‐Koch, A. E., Telen, M. J., Custer, B., et al. (2022) · Journal of Clinical Investigation · doi:10.1172/jci156060 · Cited by 59 · see citing works
Balancing DNA repair to prevent ageing and cancer
Stead, E. R., & Bjedov, I. (2021) · Experimental Cell Research · doi:10.1016/j.yexcr.2021.112679 · Cited by 56 · see citing works
Peroxiredoxin, Senescence, and Cancer
Wu, M., Deng, C., Lo, T.-H., Chan, K.-Y., Li, X., & Wong, C. (2022) · Cells · doi:10.3390/cells11111772 · Cited by 56 · see citing works
A Tale of Two Cancers: A Current Concise Overview of Breast and Prostate Cancer
Silva, F. D., & Alcorn, J. (2022) · Cancers · doi:10.3390/cancers14122954 · Cited by 55 · see citing works
Nasim, M. J., Zuraik, M. M., Abdin, A. Y., Ney, Y., & Jacob, C. (2021) · Antioxidants · doi:10.3390/antiox10060882 · Cited by 52 · see citing works
The complex interplay between aging and cancer
Trastus, L. A., & di Fagagna, F. D. (2025) · Nature Aging · doi:10.1038/s43587-025-00827-z · Cited by 52 · see citing works
Hagiwara, K., Natarajan, S., Wang, Z., Zubair, H., Mulder, H. L., Dong, L., Plyler, E. M., Thimmaiah, P., Ma, X., Ness, K. K., et al. (2023) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-0956 · Cited by 49 · see citing works
Age-associated disparity in phagocytic clearance affects the efficacy of cancer nanotherapeutics
Wang, Y., Deng, W., Lee, D., Long, Y., Lü, Y., Dong, S., Huntoon, K. M., Antony, A., Li, X., Ye, R., et al. (2023) · Nature Nanotechnology · doi:10.1038/s41565-023-01502-3 · Cited by 49 · see citing works
Attribution of Cancer Origins to Endogenous, Exogenous, and Preventable Mutational Processes
Cannataro, V. L., Mandell, J. D., & Townsend, J. P. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac084 · Cited by 48 · see citing works
Senescence-induced immune remodeling facilitates metastatic adrenal cancer in a sex-dimorphic manner
Warde, K. M., Smith, L., Liu, L., Stubben, C., Lohman, B. K., Willett, P. W., Ammer, J. L., Castaneda-Hernandez, G., Imodoye, S. O., Zhang, C., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00420-2 · Cited by 47 · see citing works
Midkine as a driver of age-related changes and increase in mammary tumorigenesis
Yan, P., Rojas-Jiménez, E. A., Li, Z., Bui, T. M., Seehawer, M., Nishida, J., Foidart, P., Stevens, L. E., Xie, Y., Gomez, M. M., et al. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.09.002 · Cited by 47 · see citing works
The use of immunotherapy in older patients with advanced non-small cell lung cancer
Tagliamento, M., Frélaut, M., Baldini, C., Naigeon, M., Nencioni, A., Chaput, N., & Besse, B. (2022) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2022.102394 · Cited by 47 · see citing works
Age Is Just a Number: Considerations for Older Adults in Cancer Clinical Trials
Habr, D., McRoy, L., & Papadimitrakopoulou, V. A. (2021) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djab070 · Cited by 46 · see citing works
Koklesová, L., Líšková, A., Samec, M., Zhai, K., AL-Ishaq, R. K., Bugos, O., Šudomová, M., Biringer, K., Péč, M. J., Adamkov, M., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22168649 · Cited by 46 · see citing works
The Aging–Cancer Cycle: Mechanisms and Opportunities for Intervention
Sedrak, M. S., & Cohen, H. J. (2022) · The Journals of Gerontology Series A · doi:10.1093/gerona/glac247 · Cited by 42 · see citing works
Somatic variation in normal tissues: friend or foe of cancer early detection?
Acha‐Sagredo, A., Ganguli, P., & Ciccarelli, F. D. (2022) · Annals of Oncology · doi:10.1016/j.annonc.2022.09.156 · Cited by 39 · see citing works
Skeletal muscle dysfunction with advancing age
Pabla, P., Jones, E. J., Piasecki, M., & Phillips, B. E. (2024) · Clinical Science · doi:10.1042/cs20231197 · Cited by 47 · see citing works
Torrens‐Mas, M., Perelló-Reus, C. M., Navas-Enamorado, C., Ibargüen-González, L., Sánchez-Polo, A., Segura‐Sampedro, J. J., Masmiquel, L., Barceló, C., & González‐Freire, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910547 · Cited by 36 · see citing works
The Role of Exercise in Cancer-Related Sarcopenia and Sarcopenic Obesity
Papadopetraki, A., Giannopoulos, A., Maridaki, M., Zagouri, F., Droufakou, S., Koutsilieris, M., & Philippou, A. (2023) · Cancers · doi:10.3390/cancers15245856 · Cited by 34 · see citing works
Mallongi, A., Astuti, R. D. P., Amiruddin, R., Hatta, M., & Rauf, A. U. (2021) · Environmental Nanotechnology Monitoring & Management · doi:10.1016/j.enmm.2021.100634 · Cited by 34 · see citing works
Marongiu, F., & DeGregori, J. V. (2022) · Molecular Oncology · doi:10.1002/1878-0261.13275 · Cited by 35 · see citing works
Self-citationTumor acidic environment directs nanoparticle impacts on cancer cells
Ghaemi, B., & Hajipour, M. J. (2022) · Journal of Colloid and Interface Science · doi:10.1016/j.jcis.2022.12.019 · Cited by 32 · see citing works
Group phenotypic composition in cancer
Capp, J., DeGregori, J. V., Nedelcu, A. M., Dujon, A. M., Boutry, J., Pujol, P., Alix‐Panabières, C., Hamede, R., Roche, B., Újvári, B., et al. (2021) · eLife · doi:10.7554/elife.63518 · Cited by 32 · see citing works
Self-citationCells with cancer‐associated mutations overtake our tissues as we age
Evans, E. J., & DeGregori, J. V. (2021) · Aging and Cancer · doi:10.1002/aac2.12037 · Cited by 34 · see citing works
Self-citationThe level of free-circulating mtDNA in patients with radon-induced lung cancer
Bulgakova, O., Kussainova, A., Kakabayev, A. A., Aripova, A., Baikenova, G., Izzotti, A., & Bersimbaev, R. I. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112215 · Cited by 31 · see citing works
Bischoff-Ferrari, H. A., Willett, W. C., Manson, J. E., Dawson‐Hughes, B., Manz, M. G., Theiler, R., Braendle, K., Vellas, B. J., Rizzoli, R., Kressig, R. W., et al. (2022) · Frontiers in Aging · doi:10.3389/fragi.2022.852643 · Cited by 31 · see citing works
CAR-NK cells: harnessing the power of natural killers for advanced cancer therapy
dos Reis, F. D., Saidani, Y., Martín-Rubio, P., Pamplona, R. S., Stojanovic, A., & Correia, M. P. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1603757 · Cited by 30 · see citing works
The role of host environment in cancer evolution
Solary, É., & Laplane, L. (2020) · Evolutionary Applications · doi:10.1111/eva.13039 · Cited by 31 · see citing works
Cardiovascular health: an important component of cancer survivorship
Cleary, S., Rosen, S. D., Gilbert, D. C., & Langley, R. E. (2023) · BMJ Oncology · doi:10.1136/bmjonc-2023-000090 · Cited by 29 · see citing works
Somatic mutations in aging and disease
Ren, P., Zhang, J., & Vijg, J. (2024) · GeroScience · doi:10.1007/s11357-024-01113-3 · Cited by 29 · see citing works
Bian, L., Ma, Z., Fu, X., Ji, C., Wang, T., Yan, C., Dai, J., Ma, H., Hu, Z., Shen, H., et al. (2024) · eLife · doi:10.7554/elife.91101.3 · Cited by 29 · see citing works
Plasticity and Functional Heterogeneity of Cancer-Associated Fibroblasts
Flynn, J. M., Thadani, N., Gallagher, E. E., Azzaro, I., Bodnar, C. M., McCarty, C. P., Romano, G., Webster, M. R., & Capparelli, C. (2025) · Cancer Research · doi:10.1158/0008-5472.can-24-3037 · Cited by 26 · see citing works
Nachtsheim, L., Mayer, M., Meyer, M. F., Oesterling, F., Kajueter, H., Arolt, C., Quaas, A., Klußmann, J. P., & Wolber, P. (2022) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-022-04278-6 · Cited by 26 · see citing works
Tuo, Z., Zhang, Y., Li, D., Wang, Y., Wu, R., Wang, J., Yu, Q., Ye, L., Shao, F., Wusiman, D., et al. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107302 · Cited by 27 · see citing works
Incidence and Mortality of Colorectal Cancer in Asia in 2022 and Projections for 2050
Fu, M., Li, Y., & Wang, J. (2025) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.16910 · Cited by 25 · see citing works
Chen, Y., Yang, C., Li, N., Wang, Z., Wu, P. S., Du, J., & Jiang, J. (2022) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2021.0538 · Cited by 25 · see citing works
Targeting immunosenescence for improved tumor immunotherapy
Liu, Z., Zuo, L., Zhou, Z., Liu, S., Ba, Y., Zuo, A., Ren, Y., Zhang, C., Chen, Y., Ma, H., et al. (2024) · MedComm · doi:10.1002/mco2.777 · Cited by 24 · see citing works
Astuti, R. D. P., Mallongi, A., Amiruddin, R., Hatta, M., & Rauf, A. U. (2022) · Sustainable Water Resources Management · doi:10.1007/s40899-022-00806-x · Cited by 24 · see citing works
Johnson, M. O., Bell, A., Lauing, K. L., Ladomersky, E., Zhai, L., Penco-Campillo, M., Shah, Y., Mauer, E. A., Xiu, J., Nicolaides, T. P., et al. (2023) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-23-0834 · Cited by 24 · see citing works
Pairwise and higher-order epistatic effects among somatic cancer mutations across oncogenesis
Alfaro-Murillo, J. A., & Townsend, J. P. (2023) · Mathematical Biosciences · doi:10.1016/j.mbs.2023.109091 · Cited by 24 · see citing works
PRDX1 stimulates non-small-cell lung carcinoma to proliferate via the Wnt/β-Catenin signaling
Song, C., Xiong, G., Yang, S., Xiaoqun, W. E. I., Ye, X., Huang, W., & ZHANG, R. (2021) · Panminerva Medica · doi:10.23736/s0031-0808.20.03978-6 · Cited by 23 · see citing works
Halophyte Plants as Potential Sources of Anticancer Agents: A Comprehensive Review
Custódio, L. M. B., García‐Caparrós, P., Pereira, C. G., & Castelo‐Branco, P. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14112406 · Cited by 23 · see citing works
Shrinking the battlefield in cancer therapy: Nanotechnology against cancer stem cells
Fernandes, Q., Therachiyil, L., Khan, A. Q., Bedhiafi, T., Korashy, H. M., Bhat, A. A., & Shahab Uddin, M. S. (2023) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2023.106586 · Cited by 24 · see citing works
Growth Hormone Action as a Target in Cancer: Significance, Mechanisms, and Possible Therapies
Basu, R., Boguszewski, C. L., & Kopchick, J. J. (2024) · Endocrine Reviews · doi:10.1210/endrev/bnae030 · Cited by 25 · see citing works
The Hallmarks of Cancer as Eco-Evolutionary Processes
Bhattacharya, R., Avdieiev, S. S., Bukkuri, A., Whelan, C. J., Gatenby, R. A., Tsai, K. Y., & Brown, J. S. (2025) · Cancer Discovery · doi:10.1158/2159-8290.cd-24-0861 · Cited by 23 · see citing works
Abdullahi, A., Wong, T. W. L., & Ng, S. S. M. (2023) · Cancer Medicine · doi:10.1002/cam4.6466 · Cited by 22 · see citing works
Preoperative glucose-to-lymphocyte ratio predicts survival in cancer
Liu, L., Zhang, B.-B., Li, Y.-Z., Huang, W., Niu, Y., Jia, Q.-C., Wang, W. J., Yuan, J., Miao, S., Wang, R., et al. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1284152 · Cited by 21 · see citing works
Cancer Screening, Surrogates of Survival, and the Soma
DeGregori, J. V., Pharoah, P. D. P., Sasieni, P. D., & Swanton, C. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.09.003 · Cited by 21 · see citing works
Self-citationLeukoplakia and Immunology: New Chemoprevention Landscapes?
Grigolato, R., Bizzoca, M. E., Calabrese, L. S., Leuci, S., Mignogna, M. D., & Muzio, L. L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186874 · Cited by 21 · see citing works
Distinct Genomic Landscapes in Early-Onset and Late-Onset Endometrial Cancer
Choi, J. Y., Holowatyj, A. N., Du, M., Chen, Z., Wen, W., Schultz, N., Lipworth, L., & Guo, X. (2022) · JCO Precision Oncology · doi:10.1200/po.21.00401 · Cited by 21 · see citing works
Age-Related Adaptive Immune Changes in Parkinson’s Disease
Kouli, A., & Williams-Gray, C. H. (2022) · Journal of Parkinson's Disease · doi:10.3233/jpd-223228 · Cited by 20 · see citing works
Aldriwesh, M. G., Alotibi, R. S., Alqurainy, N., Alrabiah, S., Arafah, A. M., Alghoribi, M. F., & Ajina, R. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2607076 · Cited by 20 · see citing works
Cleere, E. F., Davey, M. G., & O'Neill, J. P. (2022) · Head & Neck · doi:10.1002/hed.27110 · Cited by 20 · see citing works
Zhou, W.-L., & Yue, Y.-Y. (2022) · International Journal of Public Health · doi:10.3389/ijph.2022.1605021 · Cited by 20 · see citing works
Ruffieux, Y., Muchengeti, M. M., Olago, V., Dhokotera, T., Bohlius, J., Egger, M., & Rohner, E. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac925 · Cited by 21 · see citing works
Cui, J., Ding, R., Liu, H., Ma, M., Zuo, R., & Liu, X. (2024) · BMC Public Health · doi:10.1186/s12889-023-17571-x · Cited by 21 · see citing works
Capp, J., & Frédéric Thomas, A. (2020) · BioEssays · doi:10.1002/bies.202000140 · Cited by 20 · see citing works
Haugg, F., Lee, G. C., He, J., Johnson, J., Zapaishchykova, A., Bitterman, D. S., Kann, B. H., Aerts, H. J. W. L., & Mak, R. H. (2025) · The Lancet Healthy Longevity · doi:10.1016/j.lanhl.2025.100728 · Cited by 24 · see citing works
Cellular Senescence and Aging in Myotonic Dystrophy
Hasuike, Y., Mochizuki, H., & Nakamori, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042339 · Cited by 19 · see citing works
Zhu, S., Wang, J., Zellmer, L., Xu, N., Liu, M., Hu, Y., Ma, H., Deng, F., Yang, W., & Liao, D. J. (2022) · Journal of Cancer · doi:10.7150/jca.72628 · Cited by 21 · see citing works
Efficacy of Nano-Based Strategies on the Safe Delivery and Bioavailability of Vitamin D: Review
Hussain, M., Xu, J., Ahmad, I., Hussain, K., Qayum, A., Lu, X., Zhong, H., & Guan, R. (2023) · Food Reviews International · doi:10.1080/87559129.2023.2225591 · Cited by 19 · see citing works
Phosphatidylserine: paving the way for a new era in cancer therapies
Preetam, S., Pandey, A., Mishra, R., Mohapatra, G., Rath, P., Malik, S., Rustagi, S., Dash, A., & Samal, S. K. (2024) · Materials Advances · doi:10.1039/d4ma00511b · Cited by 18 · see citing works
Endoplasmic Reticulum Stress and Its Role in Metabolic Reprogramming of Cancer
Zarrella, S., Miranda, M. R., Covelli, V., Restivo, I., Novi, S., Pepe, G., Tesoriere, L., Rodriquez, M., Bertamino, A., Campiglia, P., et al. (2025) · Metabolites · doi:10.3390/metabo15040221 · Cited by 18 · see citing works
A bond between rheumatic diseases and cancer in the elderly: The interleukin‐6 pathway
Iorio, G. C., Ammendolia, A., Marotta, N., Ricardi, U., & Alessandro de, S. I. R. E. (2021) · International Journal of Rheumatic Diseases · doi:10.1111/1756-185x.14194 · Cited by 18 · see citing works
Kim, J. H., Hwang, S., Son, H., Kim, D., Kim, I. B., Kim, M.-H., Sim, N. S., Kim, D. S., Ha, Y.-J. J., Lee, J., et al. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010404 · Cited by 18 · see citing works
Lobo, N., Duan, Z., Sood, A., Tan, W. S., Grajales, V., Contieri, R., Lindskrog, S. V., Dyrskjøt, L., Zhao, H., Giordano, S. H., et al. (2024) · European Urology Oncology · doi:10.1016/j.euo.2024.01.011 · Cited by 18 · see citing works
Emerging and Biological Concepts in Pediatric High-Grade Gliomas
Yoel, A., Adjumain, S., Liang, Y., Daniel, P. M., Firestein, R., & Tsui, V. (2024) · Cells · doi:10.3390/cells13171492 · Cited by 18 · see citing works
Salama, R. M., Eissa, N., Doghish, A., Abulsoud, A., Abdelmaksoud, N. M., Mohammed, O. A., Mageed, S. S. A., & Darwish, S. (2024) · Frontiers in Aging · doi:10.3389/fragi.2024.1373741 · Cited by 15 · see citing works
- Authors
- Laconi, E., Marongiu, F., & DeGregori, J.
- Affiliations
- University of Cagliari (IT)
- University of Colorado Anschutz (US)
- Corresponding author
- Laconi, Ezio
- DeGregori, James
- Venue
- British Journal of Cancer
- Published
- 2020-02-11
- Volume
- 122
- Issue
- 7
- Pages
- 943-952
- ISSN
- 0007-0920 (ISSN-L)
- 1532-1827
- PMC
- PMC7109142
- OpenAlex
- W3005392003
- Cited by
- 348
- References
- 115
- Citations by year
- 2026: 41 · 2025: 68 · 2024: 80 · 2023: 59 · 2022: 57 · 2021: 29 · 2020: 13 · 2019: 1
- FWCI
- 4.03
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- British Journal of Cancer (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UNICA IRIS Institutional Research Information System (University of Cagliari) (submittedVersion, other-oa)
- Funders
- Associazione Italiana per la Ricerca sul Cancro (10604)
- U.S. Department of Health & Human Services | National Institutes of Health (U01AG066099)
- American Association for Cancer Research (18-90-52-DEGR)
- J.D. is also supported by the Courtenay C. and Lucy Patten Davis Endowed Chair in Lung Cancer Research.
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- somatic mutations, tumor microenvironment, clonal architecture, tissue maintenance, natural selection, oncogenic mutations, cell fitness, carcinogenesis, cancer risk
- MeSH terms
- Aged, Aged, 80 and over, Aging, Biological Evolution, Female, Humans, Male, Middle Aged, Mutation, Neoplasms, 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
