Cancer across the tree of life: Cooperation and cheating in multicellularity

C Athena Aktipis, Amy M. Boddy, Gunther Jansen, Urszula Hibner, Michael E. Hochberg, Carlo Maley, Gerald S. Wilkinson

Research output: Contribution to journalArticle

115 Scopus citations

Abstract

Multicellularity is characterized by cooperation among cells for the development, maintenance and reproduction of the multicellular organism. Cancer can be viewed as cheating within this cooperative multicellular system. Complex multicellularity, and the cooperation underlying it, has evolved independently multiple times. We review the existing literature on cancer and cancer-like phenomena across life, not only focusing on complex multicellularity but also reviewing cancer-like phenomena across the tree of life more broadly. We find that cancer is characterized by a breakdown of the central features of cooperation that characterize multicellularity, including cheating in proliferation inhibition, cell death, division of labour, resource allocation and extracellular environment maintenance (which we term the five foundations of multicellularity). Cheating on division of labour, exhibited by a lack of differentiation and disorganized cell masses, has been observed in all forms of multicellularity. This suggests that deregulation of differentiation is a fundamental and universal aspect of carcinogenesis that may be underappreciated in cancer biology. Understanding cancer as a breakdown of multicellular cooperation provides novel insights into cancer hallmarks and suggests a set of assays and biomarkers that can be applied across species and characterize the fundamental requirements for generating a cancer.

Original languageEnglish (US)
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume370
Issue number1673
DOIs
StatePublished - Jul 19 2015

Keywords

  • Cancer hallmarks
  • Complex multicellularity
  • Division of labour
  • Major transitions
  • Microenvironment
  • Resource allocation

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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