Critically assessing atavism, an evolution-centered and deterministic hypothesis on cancer.


Journal

BioEssays : news and reviews in molecular, cellular and developmental biology
ISSN: 1521-1878
Titre abrégé: Bioessays
Pays: United States
ID NLM: 8510851

Informations de publication

Date de publication:
21 Apr 2024
Historique:
revised: 19 03 2024
received: 23 11 2023
accepted: 25 03 2024
medline: 22 4 2024
pubmed: 22 4 2024
entrez: 22 4 2024
Statut: aheadofprint

Résumé

Cancer is most commonly viewed as resulting from somatic mutations enhancing proliferation and invasion. Some hypotheses further propose that these new capacities reveal a breakdown of multicellularity allowing cancer cells to escape proliferation and cooperation control mechanisms that were implemented during evolution of multicellularity. Here we critically review one such hypothesis, named "atavism," which puts forward the idea that cancer results from the re-expression of normally repressed genes forming a program, or toolbox, inherited from unicellular or simple multicellular ancestors. This hypothesis places cancer in an interesting evolutionary perspective that has not been widely explored and deserves attention. Thinking about cancer within an evolutionary framework, especially the major transitions to multicellularity, offers particularly promising perspectives. It is therefore of the utmost important to analyze why one approach that tries to achieve this aim, the atavism hypothesis, has not so far emerged as a major theory on cancer. We outline the features of the atavism hypothesis that, would benefit from clarification and, if possible, unification.

Identifiants

pubmed: 38644621
doi: 10.1002/bies.202300221
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2300221

Subventions

Organisme : NewMoon research program of the University of Bordeaux
Organisme : Gordon and Betty Moore Foundation
ID : GBMF9021

Informations de copyright

© 2024 Wiley Periodicals LLC.

Références

Brown, J. S., Amend, S. R., Austin, R. H., Gatenby, R. A., Hammarlund, E. U., & Pienta, K. J. (2023). Updating the definition of cancer. Molecular Cancer Research, 21(11), 1142–1147. https://doi.org/10.1158/1541‐7786.MCR‐23‐0411
Pradeu, T., Daignan‐Fornier, B., Ewald, A., Germain, P., Okasha, S., Plutynski, A., Benzekry, S., Bertolaso, M., Bissell, M., Brown, J. S., Chin‐Yee, B., Chin‐Yee, I., Clevers, H., Cognet, L., Darrason, M., Farge, E., Feunteun, J., Galon, J., Giroux, E., … Laplane, L. (2023). Reuniting philosophy and science to advance cancer research. Biological Reviews, 98(5), 1668–1686. https://doi.org/10.1111/brv.12971
Egeblad, M., Nakasone, E. S., & Werb, Z. (2010). Tumors as organs: Complex tissues that interface with the entire organism. Developmental Cell, 18(6), 884–901. https://doi.org/10.1016/j.devcel.2010.05.012
Moore, P. S., & Chang, Y. (2010). Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nature Reviews Cancer, 10(12), Article 12. https://doi.org/10.1038/nrc2961
Soto, A. M., & Sonnenschein, C. (2011). The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory. BioEssays, 33(5), 332–340. https://doi.org/10.1002/bies.201100025
Bedessem, B., & Ruphy, S. (2015). SMT or TOFT? How the two main theories of carcinogenesis are made (artificially) incompatible. Acta Biotheoretica, 63(3), 257–267. https://doi.org/10.1007/s10441‐015‐9252‐1
Smithers, D. W. (1962). An attack on cytologism. Lancet (London, England), 1(7228), 493–499.
Willis, R. A. (1948). Pathology of Tumours. in. Pp. 1044 + xxiii Butterworth & Co. (Publishers) Ltd, London.
Rosenfeld, S. (2013). Are the somatic mutation and tissue organization field theories of carcinogenesis incompatible? Cancer Informatics, 12, CIN.S13013. https://doi.org/10.4137/CIN.S13013
Nedelcu, A. M. (2020). The evolution of multicellularity and cancer: Views and paradigms. Biochemical Society Transactions, 48(4), 1505–1518. https://doi.org/10.1042/BST20190992
Khozouz, R. (2021). Atavistic cancer model: A new theory of cancer? BioEssays, 43(12), 2100206. https://doi.org/10.1002/bies.202100206
Kasperski, A. (2022). Life entrapped in a network of atavistic attractors: How to find a rescue. International Journal of Molecular Sciences, 23(7), 4017. https://doi.org/10.3390/ijms23074017
Israel, L. (1996). Tumour progression: Random mutations or an integrated survival response to cellular stress conserved from unicellular organisms? Journal of Theoretical Biology, 178(4), 375–380. https://doi.org/10.1006/jtbi.1996.0033
Greaves, M. (2015). Evolutionary determinants of cancer. Cancer Discovery, 5(8), 806–820. https://doi.org/10.1158/2159‐8290.CD‐15‐0439
Russo, M., Sogari, A., & Bardelli, A. (2021). Adaptive evolution: How bacteria and cancer cells survive stressful conditions and drug treatment. Cancer Discovery, 11(8), 1886–1895. https://doi.org/10.1158/2159‐8290.CD‐20‐1588
Clairambault, J. (2019). An evolutionary perspective on cancer, with applications to anticancer drug resistance modelling and perspectives in therapeutic control. Journal of Mathematical Study, 52(4), 470–496.
Davies, P. C., & Agus, D. B. (2016). Stochasticity and determinism in cancer creation and progression. Convergent Science Physical Oncology, 1(2), 026003. https://doi.org/10.1088/2057‐1739/1/2/026003
Vincent, M. (2012). Cancer: A de‐repression of a default survival program common to all cells?: A life‐history perspective on the nature of cancer. BioEssays, 34(1), 72–82. https://doi.org/10.1002/bies.201100049
Vincent, M. D. (2011). Cancer: beyond speciation. Advances in cancer research. Elsevier. https://doi.org/10.1016/B978‐0‐12‐387688‐1.00010‐7
Davies, P. C. W., & Lineweaver, C. H. (2011). Cancer tumors as Metazoa 1.0: Tapping genes of ancient ancestors. Physical Biology, 8(1), 015001. https://doi.org/10.1088/1478‐3975/8/1/015001
Aktipis, C. A., Boddy, A. M., Jansen, G., Hibner, U., Hochberg, M. E., Maley, C. C., & Wilkinson, G. S. (2015). Cancer across the tree of life: Cooperation and cheating in multicellularity. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1673), 20140219. https://doi.org/10.1098/rstb.2014.0219
Okasha, S. (2021). Cancer and the Levels of Selection. The British Journal for the Philosophy of Science, 716178. https://doi.org/10.1086/716178
Vincent, M. (2017). Atavism theory – An introductory discourse. Ecology and evolution of cancer (pp. 211–218). Elsevier. https://doi.org/10.1016/B978‐0‐12‐804310‐3.00016‐8
Thomas, F., Ujvari, B., Renaud, F., & Vincent, M. (2017). Cancer adaptations: Atavism, de novo selection, or something in between? BioEssays, 39(8), 1700039. https://doi.org/10.1002/bies.201700039
Monod, J. (1971). Chance and necessity: An essay on the natural philosophy of modern biology (First american edition). ivx, 204pp Knopf, New York.
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., Marr, M., Pincus, D., Putnam, N., Rokas, A., Wright, K. J., Zuzow, R., Dirks, W., Good, M., Goodstein, D., … Rokhsar, D. (2008). The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature, 451(7180), 783–788. https://doi.org/10.1038/nature06617
Hanschen, E. R., Marriage, T. N., Ferris, P. J., Hamaji, T., Toyoda, A., Fujiyama, A., Neme, R., Noguchi, H., Minakuchi, Y., Suzuki, M., Kawai‐Toyooka, H., Smith, D. R., Sparks, H., Anderson, J., Bakarić, R., Luria, V., Karger, A., Kirschner, M. W., Durand, P. M., … Olson, B. J. S. C. (2016). The Gonium pectorale genome demonstrates co‐option of cell cycle regulation during the evolution of multicellularity. Nature Communications, 7(1), 11370. https://doi.org/10.1038/ncomms11370
Velicer, G. J., Lenski, R. E., & Kroos, L. (2002). Rescue of social motility lost during evolution of Myxococcus xanthus in an asocial environment. Journal of Bacteriology, 184(10), 2719–2727. https://doi.org/10.1128/JB.184.10.2719‐2727.2002
Velicer, G. J., Kroos, L., & Lenski, R. E. (1998). Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proceedings of the National Academy of Sciences, 95(21), 12376–12380. https://doi.org/10.1073/pnas.95.21.12376
Jeffery, W. R. (2009). Regressive evolution in Astyanax cavefish. Annual Review of Genetics, 43(1), 25–47. https://doi.org/10.1146/annurev‐genet‐102108‐134216
Lineweaver, C. H., & Davies, P. C. W. (2020). Comparison of the atavistic model of cancer to somatic mutation theory: Phylostratigraphic analyses support the atavistic model. In B. S. Gerstman (Ed.), The physics of cancer (pp. 243–261). WORLD SCIENTIFIC. https://doi.org/10.1142/9789811223495_0012
Lineweaver, C. H., Bussey, K. J., Blackburn, A. C., & Davies, P. C. W. (2021). Cancer progression as a sequence of atavistic reversions. BioEssays, 43(7), 2000305. https://doi.org/10.1002/bies.202000305
Lewontin, R. C. (2000). The triple helix: Gene, organism, and environment. Harvard University Press.
Oyama, S. (2000). The ontogeny of information: Developmental systems and evolution (2nd ed., rev.enl). Duke University Press.
Snow, H. (1893). A Treatise, practical and theoretic on cancers and the cancer‐process 384pp J. & A. Churchill(Ed), London.
Vincent, M. D. (2009). The animal within: Carcinogenesis and the clonal evolution of cancer cells are speciation events sensu stricto: Cancer as speciation. Evolution; International Journal of Organic Evolution, 64(4), 1173–1183. https://doi.org/10.1111/j.1558‐5646.2009.00942.x
Trigos, A. S., Pearson, R. B., Papenfuss, A. T., & Goode, D. L. (2017). Altered interactions between unicellular and multicellular genes drive hallmarks of transformation in a diverse range of solid tumors. Proceedings of the National Academy of Sciences, 114(24), 6406–6411. https://doi.org/10.1073/pnas.1617743114
Domazet‐Lošo, T., & Tautz, D. (2010). Phylostratigraphic tracking of cancer genes suggests a link to the emergence of multicellularity in metazoa. BMC Biology, 8(1), 66. https://doi.org/10.1186/1741‐7007‐8‐66
Bussey, K. J., & Davies, P. C. W. (2021). Reverting to single‐cell biology: The predictions of the atavism theory of cancer. Progress in Biophysics and Molecular Biology, 165, 49–55. https://doi.org/10.1016/j.pbiomolbio.2021.08.002
Lineweaver, C. H., Davies, P. C. W., & Vincent, M. D. (2014). Targeting cancer's weaknesses (not its strengths): Therapeutic strategies suggested by the atavistic model. BioEssays, 36(9), 827–835. https://doi.org/10.1002/bies.201400070

Auteurs

Bertrand Daignan-Fornier (B)

University of Bordeaux, CNRS, IBGC, Bordeaux, France.

Thomas Pradeu (T)

University of Bordeaux, CNRS, ImmunoConcEpT, Bordeaux, France.
Presidential Fellow, Chapman University, Orange, California, USA.

Classifications MeSH