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Classifying the evolutionary and ecological features of neoplasms
Carlo C. Maley, Athena Aktipis, Trevor A. Graham and 19 more
Nature Reviews Cancer · 2017 · Review
Abstract
Neoplasms change over time through a process of cell-level evolution, driven by genetic and epigenetic alterations. However, the ecology of the microenvironment of a neoplastic cell determines which changes provide adaptive benefits. There is widespread recognition of the importance of these evolutionary and ecological processes in cancer, but to date, no system has been proposed for drawing clinically relevant distinctions between how different tumours are evolving. On the basis of a consensus conference of experts in the fields of cancer evolution and cancer ecology, we propose a framework for classifying tumours that is based on four relevant components. These are the diversity of neoplastic cells (intratumoural heterogeneity) and changes over time in that diversity, which make up an evolutionary index (Evo-index), as well as the hazards to neoplastic cell survival and the resources available to neoplastic cells, which make up an ecological index (Eco-index). We review evidence demonstrating the importance of each of these factors and describe multiple methods that can be used to measure them. Development of this classification system holds promise for enabling clinicians to personalize optimal interventions based on the evolvability of the patient's tumour. The Evo- and Eco-indices provide a common lexicon for communicating about how neoplasms change in response to interventions, with potential implications for clinical trials, personalized medicine and basic cancer research.
References 188
- 1.
Greaves M, Maley CC. Clonal evolution in cancer. Nature. 2012;481:306-313.
Not in our library10.1038/nature10762
- 2.
Vogelstein B, et al. Cancer genome landscapes. Science. 2013;339:1546-1558.
Not in our library10.1126/science.1235122
- 3.
Greaves M. Evolutionary determinants of cancer. Cancer Discov. 2015;5:806-820.
Not in our library10.1158/2159-8290.cd-15-0439
- 4.
Nowell PC. The clonal evolution of tumor cell populations. Science. 1976;194:23-28.
Not in our library10.1126/science.959840
- 5.
Mroz EA, et al. High intratumor genetic heterogeneity is related to worse outcome in patients with head and neck squamous cell carcinoma. Cancer. 2013.
Not in our library10.1002/cncr.28150
- 6.
Andor N, et al. Pan-cancer analysis of the extent and consequences of intratumor heterogeneity. Nat Med. 2016;22:105-113.
Not in our library10.1038/nm.3984
- 7.
Wangsa D, et al. Phylogenetic analysis of multiple FISH markers in oral tongue squamous cell carcinoma suggests that a diverse distribution of copy number changes is associated with poor prognosis. Int J Cancer. 2016;138:98-109.
Not in our library10.1002/ijc.29691
- 8.
- 9.
Urbschat S, et al. Clonal cytogenetic progression within intratumorally heterogeneous meningiomas predicts tumor recurrence. Int J Oncol. 2011;39:1601-1608.
Not in our library10.3892/ijo.2011.1199
- 10.
Birkbak NJ, et al. Paradoxical relationship between chromosomal instability and survival outcome in cancer. Cancer Res. 2011;71:3447-3452.
Not in our library10.1158/0008-5472.can-10-3667
- 11.
Roylance R, et al. Relationship of extreme chromosomal instability with long-term survival in a retrospective analysis of primary breast cancer. Cancer Epidemiol Biomarkers Prev. 2011;20:2183-2194.
Not in our library10.1158/1055-9965.epi-11-0343
- 12.
Maley CC, et al. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat Genet. 2006;38:468-473.
Not in our library10.1038/ng1768
- 13.
Merlo LM, et al. A comprehensive survey of clonal diversity measures in barrett’s esophagus as biomarkers of progression to esophageal adenocarcinoma. Cancer Prev Res (Phila ). 2010;3:1388-1397.
Not in our library10.1158/1940-6207.capr-10-0108
- 14.
Martinez P, et al. Dynamic clonal equilibrium and predetermined cancer risk in Barrett’s oesophagus. Nat Commun. 2016;7:12158.
Not in our library10.1038/ncomms12158
- 15.
- 16.
- 17.
Williams MJ, Werner B, Barnes CP, Graham TA, Sottoriva A. Identification of neutral tumor evolution across cancer types. Nat Genet. 2016;48:238-244.
Not in our library10.1038/ng.3489
- 18.
Hong WS, Shpak M, Townsend JP. Inferring the origin of metastases from cancer phylogenies. Cancer Res. 2015;75:4021-4025.
Not in our library10.1158/0008-5472.can-15-1889
- 19.
Dawson SJ, et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med. 2013;368:1199-1209.
Not in our library10.1056/nejmoa1213261
- 20.
- 21.
McFarland CD, Korolev KS, Kryukov GV, Sunyaev SR, Mirny LA. Impact of deleterious passenger mutations on cancer progression. Proc Natl Acad Sci USA. 2013;110:2910-2915.
Not in our library10.1073/pnas.1213968110
- 22.
McFarland CD, Mirny LA, Korolev KS. Tug-of-war between driver and passenger mutations in cancer and other adaptive processes. Proc Natl Acad Sci USA. 2014;111:15138-15143.
Not in our library10.1073/pnas.1404341111
- 23.
Axelrod R, Axelrod DE, Pienta KJ. Evolution of cooperation among tumor cells. Proc Natl Acad Sci USA. 2006;103:13474-13479.
Not in our library10.1073/pnas.0606053103
- 24.
Marusyk A, et al. Non-cell-autonomous driving of tumour growth supports sub-clonal heterogeneity. Nature. 2014;514:54-58.
Not in our library10.1038/nature13556
- 25.
Marusyk A, Almendro V, Polyak K. Intra-tumour heterogeneity: a looking glass for cancer? Nat Rev Cancer. 2012;12:323-334.
Not in our library10.1038/nrc3261
- 26.
- 27.
Cleary AS, Leonard TL, Gestl SA, Gunther EJ. Tumour cell heterogeneity maintained by cooperating subclones in Wnt-driven mammary cancers. Nature. 2014;508:113-117.
Not in our library10.1038/nature13187
- 28.
Driscoll WW, Pepper JW. Theory for the evolution of diffusible external goods. Evol Int J Org Evol. 2010;64:2682-2687.
Not in our library10.1111/j.1558-5646.2010.01002.x
- 29.
Alizadeh AA, et al. Toward understanding and exploiting tumor heterogeneity. Nat Med. 2015;21:846-853.
Not in our library10.1038/nm.3915
- 30.
Magurran AE. Measuring Biological Diversity. 2004.
Not in our library10.1016/j.cub.2021.07.049
- 31.
Whittaker RH. Evolution and measurement of species diversity. Taxon. 1972;21:213-251.
Not in our library
- 32.
Park SY, Gonen M, Kim HJ, Michor F, Polyak K. Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. J Clin Invest. 2010;120:636-644.
Not in our library10.1172/jci40724
- 33.
- 34.
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011;5:169-172.
Not in our library10.1038/ismej.2010.133
- 35.
Fay JC, Wu CI. Sequence divergence, functional constraint, and selection in protein evolution. Annu Rev Genom Hum Genet. 2003;4:213-235.
Not in our library10.1146/annurev.genom.4.020303.162528
- 36.
Epstein JI, Amin MB, Reuter VE, Humphrey PA. Contemporary gleason grading of prostatic carcinoma: an update with discussion on practical issues to implement the 2014 international society of urological pathology (ISUP) consensus conference on gleason grading of prostatic carcinoma. Am J Surg Pathol. 2017;41:e1-e7.
Not in our library10.1097/pas.0000000000000820
- 37.
Babjuk M, et al. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013. Eur Urol. 2013;64:639-653.
Not in our library10.1016/j.eururo.2013.06.003
- 38.
Shaheen NJ, Falk GW, Iyer PG, Gerson LB. ACG Clinical Guideline: Diagnosis and management of Barrett’s esophagus. Am J Gastroenterol. 2016;111:30-50.
Not in our library10.1038/ajg.2015.322
- 39.
Abbosh C, et al. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature. 2017;545:446-451.
Not in our library10.1038/nature22364
- 40.
Wang J, et al. Clonal evolution of glioblastoma under therapy. Nat Genet. 2016;48:768-776.
Not in our library10.1038/ng.3590
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