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The issues with tissues : the wide range of cell fate separation enables the evolution of multicellularity and cancer

Hammarlund, Emma U. LU ; Amend, Sarah R. and Pienta, Kenneth J. (2020) In Medical Oncology 37(7).
Abstract

Our understanding of the rises of animal and cancer multicellularity face the same conceptual hurdles: what makes the clade originate and what makes it diversify. Between the events of origination and diversification lies complex tissue organization that gave rise to novel functionality for organisms and, unfortunately, for malignant transformation in cells. Tissue specialization with distinctly separated cell fates allowed novel functionality at organism level, such as for vertebrate animals, but also involved trade-offs at the cellular level that are potentially disruptive. These trade-offs are under-appreciated and here we discuss how the wide separation of cell phenotypes may contribute to cancer evolution by (a) how factors can... (More)

Our understanding of the rises of animal and cancer multicellularity face the same conceptual hurdles: what makes the clade originate and what makes it diversify. Between the events of origination and diversification lies complex tissue organization that gave rise to novel functionality for organisms and, unfortunately, for malignant transformation in cells. Tissue specialization with distinctly separated cell fates allowed novel functionality at organism level, such as for vertebrate animals, but also involved trade-offs at the cellular level that are potentially disruptive. These trade-offs are under-appreciated and here we discuss how the wide separation of cell phenotypes may contribute to cancer evolution by (a) how factors can reverse differentiated cells into a window of phenotypic plasticity, (b) the reversal to phenotypic plasticity coupled with asexual reproduction occurs in a way that the host cannot adapt, and (c) the power of the transformation factor correlates to the power needed to reverse tissue specialization. The role of reversed cell fate separation for cancer evolution is strengthened by how some tissues and organisms maintain high cell proliferation and plasticity without developing tumours at a corresponding rate. This demonstrates a potential proliferation paradox that requires further explanation. These insights from the cancer field, which observes tissue evolution in real time and closer than any other field, allow inferences to be made on evolutionary events in animal history. If a sweet spot of phenotypic and reproductive versatility is key to transformation, factors stimulating cell fate separation may have promoted also animal diversification on Earth.

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author
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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Animals, Cambrian explosion, Cancer, Evolution, Multicellularity, Phenotypic separation
in
Medical Oncology
volume
37
issue
7
article number
62
publisher
Humana Press
external identifiers
  • pmid:32535731
  • scopus:85086336105
ISSN
1357-0560
DOI
10.1007/s12032-020-01387-5
language
English
LU publication?
yes
id
340670d2-003a-4088-a368-d066fdfb58f1
date added to LUP
2020-07-02 11:30:34
date last changed
2021-01-12 03:24:25
@article{340670d2-003a-4088-a368-d066fdfb58f1,
  abstract     = {<p>Our understanding of the rises of animal and cancer multicellularity face the same conceptual hurdles: what makes the clade originate and what makes it diversify. Between the events of origination and diversification lies complex tissue organization that gave rise to novel functionality for organisms and, unfortunately, for malignant transformation in cells. Tissue specialization with distinctly separated cell fates allowed novel functionality at organism level, such as for vertebrate animals, but also involved trade-offs at the cellular level that are potentially disruptive. These trade-offs are under-appreciated and here we discuss how the wide separation of cell phenotypes may contribute to cancer evolution by (a) how factors can reverse differentiated cells into a window of phenotypic plasticity, (b) the reversal to phenotypic plasticity coupled with asexual reproduction occurs in a way that the host cannot adapt, and (c) the power of the transformation factor correlates to the power needed to reverse tissue specialization. The role of reversed cell fate separation for cancer evolution is strengthened by how some tissues and organisms maintain high cell proliferation and plasticity without developing tumours at a corresponding rate. This demonstrates a potential proliferation paradox that requires further explanation. These insights from the cancer field, which observes tissue evolution in real time and closer than any other field, allow inferences to be made on evolutionary events in animal history. If a sweet spot of phenotypic and reproductive versatility is key to transformation, factors stimulating cell fate separation may have promoted also animal diversification on Earth.</p>},
  author       = {Hammarlund, Emma U. and Amend, Sarah R. and Pienta, Kenneth J.},
  issn         = {1357-0560},
  language     = {eng},
  number       = {7},
  publisher    = {Humana Press},
  series       = {Medical Oncology},
  title        = {The issues with tissues : the wide range of cell fate separation enables the evolution of multicellularity and cancer},
  url          = {http://dx.doi.org/10.1007/s12032-020-01387-5},
  doi          = {10.1007/s12032-020-01387-5},
  volume       = {37},
  year         = {2020},
}