The impact of food availability on tumorigenesis is evolutionarily conserved.

Sophie Tissot, Lena Guimard, Jordan Meliani, Justine Boutry, Antoine M Dujon, Jean-Pascal Capp, Jácint Tökölyi, Peter A Biro, Christa Beckmann, Laura Fontenille, Nam Do Khoa, Rodrigo Hamede, Benjamin Roche, Beata Ujvari, Aurora M Nedelcu, Frédéric Thomas
Author Information
  1. Sophie Tissot: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France. sophie.tissot@ird.fr.
  2. Lena Guimard: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  3. Jordan Meliani: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  4. Justine Boutry: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  5. Antoine M Dujon: School of Life and Environmental Sciences, Deakin University, Waurn Ponds, VIC, Australia.
  6. Jean-Pascal Capp: Toulouse Biotechnology Institute, University of Toulouse, INSA, CNRS, INRAE, Toulouse, France.
  7. Jácint Tökölyi: MTA-DE "Momentum" Ecology, Evolution and Developmental Biology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, 4032, Hungary.
  8. Peter A Biro: School of Life and Environmental Sciences, Deakin University, Waurn Ponds, VIC, Australia.
  9. Christa Beckmann: School of Life and Environmental Sciences, Deakin University, Waurn Ponds, VIC, Australia.
  10. Laura Fontenille: AZELEAD, 377 Rue du Professeur Blayac, 34080, Montpellier, France.
  11. Nam Do Khoa: AZELEAD, 377 Rue du Professeur Blayac, 34080, Montpellier, France.
  12. Rodrigo Hamede: School of Natural Sciences, University of Tasmania, Hobart, TAS, Australia.
  13. Benjamin Roche: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.
  14. Beata Ujvari: School of Life and Environmental Sciences, Deakin University, Waurn Ponds, VIC, Australia.
  15. Aurora M Nedelcu: Department of Biology, University of New Brunswick, Fredericton, NB, Canada.
  16. Frédéric Thomas: CREEC/MIVEGEC, Université de Montpellier, CNRS, IRD, Montpellier, France.

Abstract

The inability to control cell proliferation results in the formation of tumors in many multicellular lineages. Nonetheless, little is known about the extent of conservation of the biological traits and ecological factors that promote or inhibit tumorigenesis across the metazoan tree. Particularly, changes in food availability have been linked to increased cancer incidence in humans, as an outcome of evolutionary mismatch. Here, we apply evolutionary oncology principles to test whether food availability, regardless of the multicellular lineage considered, has an impact on tumorigenesis. We used two phylogenetically unrelated model systems, the cnidarian Hydra oligactis and the fish Danio rerio, to investigate the impact of resource availability on tumor occurrence and progression. Individuals from healthy and tumor-prone lines were placed on four diets that differed in feeding frequency and quantity. For both models, frequent overfeeding favored tumor emergence, while lean diets appeared more protective. In terms of tumor progression, high food availability promoted it, whereas low resources controlled it, but without having a curative effect. We discuss our results in light of current ideas about the possible conservation of basic processes governing cancer in metazoans (including ancestral life history trade-offs at the cell level) and in the framework of evolutionary medicine.

References

  1. Semin Cancer Biol. 2021 Aug;73:30-44 [PMID: 32977005]
  2. Nat Rev Cancer. 2018 Oct;18(10):646-661 [PMID: 30116020]
  3. Prev Med. 1978 Jun;7(2):205-17 [PMID: 674107]
  4. Sci Rep. 2023 May 8;13(1):7449 [PMID: 37156860]
  5. Biol Open. 2018 Jan 23;7(1): [PMID: 29362277]
  6. Nat Commun. 2015 Mar 09;6:6367 [PMID: 25751731]
  7. Nat Commun. 2021 Jul 28;12(1):4579 [PMID: 34321471]
  8. iScience. 2022 Aug 31;25(10):105034 [PMID: 36147948]
  9. Proc Biol Sci. 2022 Jan 26;289(1967):20212669 [PMID: 35078364]
  10. J Cancer Prev. 2021 Dec 30;26(4):224-236 [PMID: 35047448]
  11. Trends Endocrinol Metab. 2010 Mar;21(3):134-41 [PMID: 20004110]
  12. Mol Biol Evol. 2006 Aug;23(8):1460-4 [PMID: 16720695]
  13. Nat Ecol Evol. 2018 Jul;2(7):1065-1070 [PMID: 29784981]
  14. Biol Lett. 2022 Jun;18(6):20220059 [PMID: 35728616]
  15. Evol Appl. 2013 Jan;6(1):144-59 [PMID: 23396885]
  16. Physiol Behav. 2015 May 15;144:129-36 [PMID: 25802021]
  17. Nature. 2004 Oct 7;431(7009):693-6 [PMID: 15470429]
  18. J Cell Sci. 1977 Dec;28:117-32 [PMID: 599169]
  19. PLoS One. 2014 Dec 11;9(12):e115147 [PMID: 25502434]
  20. EMBO J. 1996 May 1;15(9):2150-9 [PMID: 8641280]
  21. J Cell Biol. 2005 Jun 6;169(5):711-7 [PMID: 15939758]
  22. Br J Cancer. 2018 Apr;118(8):1130-1141 [PMID: 29567982]
  23. Am J Clin Nutr. 2005 Jul;82(1 Suppl):265S-273S [PMID: 16002835]
  24. Nat Commun. 2014 Jun 24;5:4222 [PMID: 24957317]
  25. Nutr Rev. 2017 Jun 1;75(6):405-419 [PMID: 28969358]
  26. Plant Physiol. 2005 May;138(1):319-29 [PMID: 15849300]
  27. Evol Med Public Health. 2022 Apr 13;10(1):170-176 [PMID: 35498120]
  28. Nutrients. 2022 Jan 14;14(2): [PMID: 35057525]
  29. Appetite. 2018 Jan 1;120:589-595 [PMID: 29038018]
  30. Future Oncol. 2013 Jul;9(7):959-76 [PMID: 23837760]
  31. Prostate. 2010 Jul 1;70(10):1037-43 [PMID: 20166128]
  32. Proc Natl Acad Sci U S A. 2008 Jun 17;105(24):8215-20 [PMID: 18378900]
  33. Eukaryot Cell. 2006 Jan;5(1):26-44 [PMID: 16400166]
  34. Biol Lett. 2017 Sep;13(9): [PMID: 28931728]
  35. Nat Cell Biol. 2015 Apr;17(4):351-9 [PMID: 25774832]
  36. Nat Rev Cancer. 2013 Dec;13(12):883-92 [PMID: 24213474]
  37. PLoS One. 2010 Dec 10;5(12):e15170 [PMID: 21170325]
  38. Nat Commun. 2021 Oct 27;12(1):6201 [PMID: 34707136]
  39. Sci Transl Med. 2012 Mar 7;4(124):124ra27 [PMID: 22323820]
  40. Mol Cell Biol. 1988 Jan;8(1):505-10 [PMID: 2827010]
  41. PLoS Pathog. 2020 Mar 19;16(3):e1008375 [PMID: 32191776]
  42. Trends Endocrinol Metab. 2018 Apr;29(4):271-280 [PMID: 29463451]
  43. Nutrition. 1999 Jun;15(6):523-6 [PMID: 10378216]
  44. Circulation. 2008 Jul 15;118(3):230-7 [PMID: 18574045]
  45. Nat Commun. 2019 Jul 22;10(1):3257 [PMID: 31332174]
  46. Nat Rev Clin Oncol. 2016 Aug;13(8):504-15 [PMID: 26951041]
  47. Nat Rev Microbiol. 2006 Feb;4(2):113-20 [PMID: 16415927]
  48. Cancer Metab. 2013 Mar 07;1(1):10 [PMID: 24280167]
  49. Trends Cancer. 2020 Oct;6(10):829-837 [PMID: 32601046]
  50. Physiol Behav. 2018 Sep 1;193(Pt B):261-267 [PMID: 29471074]
  51. JAMA Netw Open. 2021 Feb 1;4(2):e2037341 [PMID: 33591366]
  52. Sci Total Environ. 2022 Jan 10;803:149923 [PMID: 34487898]
  53. Proc Natl Acad Sci U S A. 2011 Jun 28;108 Suppl 2:10855-62 [PMID: 21690338]
  54. BMJ Open. 2020 Jun 7;10(6):e034730 [PMID: 32513879]
  55. Br J Cancer. 2011 Dec 6;105 Suppl 2:S77-81 [PMID: 22158327]
  56. Metabolites. 2020 Mar 25;10(4): [PMID: 32218376]

MeSH Term

Animals
Humans
Cnidaria
Biological Evolution
Hydra
Carcinogenesis
Neoplasms

Word Cloud

Created with Highcharts 10.0.0availabilityfoodtumorigenesisevolutionaryimpacttumorcellresultsmulticellularconservationcancerprogressiondietsinabilitycontrolproliferationformationtumorsmanylineagesNonethelesslittleknownextentbiologicaltraitsecologicalfactorspromoteinhibitacrossmetazoantreeParticularlychangeslinkedincreasedincidencehumansoutcomemismatchapplyoncologyprinciplestestwhetherregardlesslineageconsideredusedtwophylogeneticallyunrelatedmodelsystemscnidarianHydraoligactisfishDaniorerioinvestigateresourceoccurrenceIndividualshealthytumor-pronelinesplacedfourdifferedfeedingfrequencyquantitymodelsfrequentoverfeedingfavoredemergenceleanappearedprotectivetermshighpromotedwhereaslowresourcescontrolledwithoutcurativeeffectdiscusslightcurrentideaspossiblebasicprocessesgoverningmetazoansincludingancestrallifehistorytrade-offslevelframeworkmedicineevolutionarilyconserved

Similar Articles

Cited By