Intracellular P2X receptors as novel calcium release channels and modulators of osmoregulation in<i>Dictyostelium</i>

Sivaramakrishnan, Venketesh; Fountain, Samuel J.

doi:10.4161/chan.22737

Cited by 16 publications

(16 citation statements)

References 17 publications

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“…This result is in accord with the basic function of P2X receptors as ligand-gated ion channels which open to allow ions such as Na+, Ca2+ to pass through the membrane [14]. However, 28 out of 180 predicted proteins are predicted to populate the membranes of intracellular organelles (cytoplasmic, chloroplast, mitochondrial, nuclear), supporting recent study which has showed that the P2X receptors populating the contractile vacuole mediate calcium release and osmoregulation in Dictyostelium discoideum [7,50,51]. We also found that 149 predicted P2X proteins have 2 TM domains, while 25 have only one TM domain, which mostly exist in invertebrates.…”

Section: Resultssupporting

confidence: 83%

Comparative study of the P2X gene family in animals and plants

Hou

Cao

2016

Purinergic Signalling

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P2X receptors are ligand-gated ion channels that can bind with the adenosine triphosphate (ATP) and have diverse functional roles in neuropathic pain, inflammation, special sense, and so on. In this study, 180 putative P2X genes, including 176 members in 32 animal species and 4 members in 3 species of lower plants, were identified. These genes were divided into 13 groups, including 7 groups in vertebrates and 6 groups in invertebrates and lower plants, through phylogenetic analysis. Their gene organization and motif composition are conserved in most predicted P2X members, while groupspecific features were also found. Moreover, synteny relationships of the putative P2X genes in vertebrates are conserved while simultaneously experiencing a series of gene insertion, inversion, and transposition. Recombination signals were detected in almost all of the vertebrates and invertebrates, suggesting that intragenic recombination may play a significant role in the evolution of P2X genes. Selection analysis also identified some positively selected sites that acted on the evolution of most of the predicted P2X proteins. The phenomenon of alternative splicing occurred commonly in the putative P2X genes of vertebrates. This article explored in depth the evolutional relationship among different subtypes of P2X genes in animal and plants and might serve as a solid foundation for deciphering their functions in further studies.

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Section: Resultssupporting

confidence: 83%

Comparative study of the P2X gene family in animals and plants

Hou

Cao

2016

Purinergic Signalling

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“…Activation of ionotropic purinergic receptors triggers Ca 2þ signals in many types of cells [228 -232]. Incidentally, P2X receptors may also serve as intracellular Ca 2þ -release channels, as has been shown in D. discoideum [233], further corroborating an intimate relation between ATP and Ca 2þ from the very early evolution of cellular signalling. The P2X receptors seem to operate in the membranes of other organelles, including mitochondria, lysosomes and nuclei [234], although whether activation of these intracellular receptors is linked to Ca 2þ movements remains to be found.…”

Section: Ca 2þ As a Regulator Of Programmed Cell Deathmentioning

confidence: 90%

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

Plattner

Verkhratsky

2016

Phil. Trans. R. Soc. B

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From the very dawn of biological evolution, ATP was selected as a multipurpose energy-storing molecule. Metabolism of ATP required intracellular free Ca 2þ to be set at exceedingly low concentrations, which in turn provided the background for the role of Ca 2þ as a universal signalling molecule. The early-eukaryote life forms also evolved functional compartmentalization and vesicle trafficking, which used Ca 2þ as a universal signalling ion; similarly, Ca 2þ 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 2þ started to be exploited for shortrange signalling, despite restrictions by the preset phosphate-based energy metabolism, when both phosphates and Ca 2þ interfere with each other because of the low solubility of calcium phosphates. The need to keep cytosolic Ca 2þ low forced cells to restrict Ca 2þ signals in space and time and to develop energetically favourable Ca 2þ signalling and Ca 2þ microdomains. These steps in tandem dominated further evolution. The ATP molecule (often released by Ca 2þ -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 2þ signalling. Similar to atmospheric oxygen, Ca 2þ 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 2þ homeostasis that became critical for regulation of cell survival and cell death. Several mutually interdependent effects of Ca 2þ and ATP have been exploited in evolution, thus turning an originally unholy alliance into a fascinating success story.This article is part of the themed issue 'Evolution brings Ca 2þ and ATP together to control life and death'.

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“…The PKD2 serves for the perception of fluid flow [108]. In Dictyostelium, Ca 2+ permeable purinoceptors of P2X type, serve as CRCs localised to the contractile vacuole complex [71,109] where they modulate osmoregulation [110]. In plants, InsP 3 Rs and TRPs seem to have disappeared ( [53], this special issue).…”

Section: Other Crcs and Additional Ca 2+ Storesmentioning

confidence: 98%

The ancient roots of calcium signalling evolutionary tree

Plattner¹,

Verkhratsky²

2015

Cell Calcium

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Molecular cascades of calcium homeostasis and signalling (Ca(2+) pumps, channels, cation exchangers, and Ca(2+)-binding proteins) emerged in prokaryotes and further developed at the unicellular stage of eukaryote evolution. With progressive evolution, mechanisms of signalling became diversified reflecting multiplication and specialisation of Ca(2+)-regulated cellular activities. Recent genomic analysis of organisms from different systematic positions, combined with proteomic and functional probing invigorated expansion in our understanding of the evolution of Ca(2+) signalling. Particularly impressive is the consistent role of Ca(2+)-ATPases/pumps, calmodulin and calcineurin from very early stages of eukaryotic evolution, although with interspecies differences. Deviations in Ca(2+) handling and signalling are observed between vertebrates and flowering plants as well as between protists at the basis of the two systematic categories, Unikonta (for example choanoflagellates) and Bikonta (for example ciliates). Only the B-subunit of calcineurin, for instance, is maintained to regulate highly diversified protein kinases for stress defence in flowering plants, whereas the complete dimeric protein, in vertebrates up to humans, regulates gene transcription, immune-defence and plasticity of the brain. Calmodulin is similarly maintained throughout evolution, but in plants a calmoldulin-like domain is integrated into protein kinase molecules. The eukaryotic cell has inherited and invented many mechanisms to exploit the advantages of signalling by Ca(2+), and there is considerable overall similarity in basic processes of Ca(2+) regulation and signalling during evolution, although some details may vary.

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Intracellular P2X receptors as novel calcium release channels and modulators of osmoregulation inDictyostelium

Cited by 16 publications

References 17 publications

Comparative study of the P2X gene family in animals and plants

Comparative study of the P2X gene family in animals and plants

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

The ancient roots of calcium signalling evolutionary tree

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Intracellular P2X receptors as novel calcium release channels and modulators of osmoregulation inDictyostelium

Cited by 16 publications

References 17 publications

Comparative study of the P2X gene family in animals and plants

Comparative study of the P2X gene family in animals and plants

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

The ancient roots of calcium signalling evolutionary tree

Contact Info

Product

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