Inseparable tandem : evolution chooses ATP and Ca2+ to control life, death and cellular signalling

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2016
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Verkhratsky, Alexei
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urn:nbn:de:bsz:352-0-347264
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10.1098/rstb.2015.0419
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Philosophical Transactions of the Royal Society B : Biological Sciences ; 371 (2016), 1700. - 20150419. - ISSN 0962-8436. - eISSN 1471-2970
Abstract
From the very dawn of biological evolution, ATP was selected as a multipurpose energy-storing molecule. Metabolism of ATP required intracellular free Ca2+ to be set at exceedingly low concentrations, which in turn provided the background for the role of Ca2+ as a universal signalling molecule. The early-eukaryote life forms also evolved functional compartmentalization and vesicle trafficking, which used Ca2+ as a universal signalling ion; similarly, Ca2+ is needed for regulation of ciliary and flagellar beat, amoeboid movement, intracellular transport, as well as of numerous metabolic processes. Thus, during evolution, exploitation of atmospheric oxygen and increasingly efficient ATP production via oxidative phosphorylation by bacterial endosymbionts were a first step for the emergence of complex eukaryotic cells. Simultaneously, Ca2+ started to be exploited for short-range signalling, despite restrictions by the preset phosphate-based energy metabolism, when both phosphates and Ca2+ interfere with each other because of the low solubility of calcium phosphates. The need to keep cytosolic Ca2+ low forced cells to restrict Ca2+ signals in space and time and to develop energetically favourable Ca2+ signalling and Ca2+ microdomains. These steps in tandem dominated further evolution. The ATP molecule (often released by Ca2+-regulated exocytosis) rapidly grew to be the universal chemical messenger for intercellular communication; ATP effects are mediated by an extended family of purinoceptors often linked to Ca2+ signalling. Similar to atmospheric oxygen, Ca2+ must have been reverted from a deleterious agent to a most useful (intra- and extracellular) signalling molecule. Invention of intracellular trafficking further increased the role for Ca2+ homeostasis that became critical for regulation of cell survival and cell death. Several mutually interdependent effects of Ca2+ and ATP have been exploited in evolution, thus turning an originally unholy alliance into a fascinating success story.
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ISO 690PLATTNER, Helmut, Alexei VERKHRATSKY, 2016. Inseparable tandem : evolution chooses ATP and Ca2+ to control life, death and cellular signalling. In: Philosophical Transactions of the Royal Society B : Biological Sciences. 371(1700), 20150419. ISSN 0962-8436. eISSN 1471-2970. Available under: doi: 10.1098/rstb.2015.0419
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@article{Plattner2016-08-05Insep-34662,
  year={2016},
  doi={10.1098/rstb.2015.0419},
  title={Inseparable tandem : evolution chooses ATP and Ca<sup>2+</sup> to control life, death and cellular signalling},
  number={1700},
  volume={371},
  issn={0962-8436},
  journal={Philosophical Transactions of the Royal Society B : Biological Sciences},
  author={Plattner, Helmut and Verkhratsky, Alexei},
  note={Article Number: 20150419}
}
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    <dcterms:abstract xml:lang="eng">From the very dawn of biological evolution, ATP was selected as a multipurpose energy-storing molecule. Metabolism of ATP required intracellular free Ca&lt;sup&gt;2+&lt;/sup&gt; to be set at exceedingly low concentrations, which in turn provided the background for the role of Ca&lt;sup&gt;2+&lt;/sup&gt; as a universal signalling molecule. The early-eukaryote life forms also evolved functional compartmentalization and vesicle trafficking, which used Ca&lt;sup&gt;2+&lt;/sup&gt; as a universal signalling ion; similarly, Ca&lt;sup&gt;2+&lt;/sup&gt; is needed for regulation of ciliary and flagellar beat, amoeboid movement, intracellular transport, as well as of numerous metabolic processes. Thus, during evolution, exploitation of atmospheric oxygen and increasingly efficient ATP production via oxidative phosphorylation by bacterial endosymbionts were a first step for the emergence of complex eukaryotic cells. Simultaneously, Ca&lt;sup&gt;2+&lt;/sup&gt; started to be exploited for short-range signalling, despite restrictions by the preset phosphate-based energy metabolism, when both phosphates and Ca&lt;sup&gt;2+&lt;/sup&gt; interfere with each other because of the low solubility of calcium phosphates. The need to keep cytosolic Ca&lt;sup&gt;2+&lt;/sup&gt; low forced cells to restrict Ca&lt;sup&gt;2+&lt;/sup&gt; signals in space and time and to develop energetically favourable Ca&lt;sup&gt;2+&lt;/sup&gt; signalling and Ca&lt;sup&gt;2+&lt;/sup&gt; microdomains. These steps in tandem dominated further evolution. The ATP molecule (often released by Ca&lt;sup&gt;2+&lt;/sup&gt;-regulated exocytosis) rapidly grew to be the universal chemical messenger for intercellular communication; ATP effects are mediated by an extended family of purinoceptors often linked to Ca&lt;sup&gt;2+&lt;/sup&gt; signalling. Similar to atmospheric oxygen, Ca&lt;sup&gt;2+&lt;/sup&gt; must have been reverted from a deleterious agent to a most useful (intra- and extracellular) signalling molecule. Invention of intracellular trafficking further increased the role for Ca&lt;sup&gt;2+&lt;/sup&gt; homeostasis that became critical for regulation of cell survival and cell death. Several mutually interdependent effects of Ca&lt;sup&gt;2+&lt;/sup&gt; and ATP have been exploited in evolution, thus turning an originally unholy alliance into a fascinating success story.</dcterms:abstract>
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