Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles
ABSTRACT Inorganic pyrophosphate (PPi) is a by-product of biosynthetic reactions and has bioenergetic and regulatory roles in a variety of cells. Here we show that PPi and other pyrophosphate-containing compounds, including polyphosphate (polyP), can stimulate sodium-dependent depolarization of the...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2019-04-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00045-19 |
| _version_ | 1828953586899353600 |
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| author | Evgeniy Potapenko Ciro D. Cordeiro Guozhong Huang Roberto Docampo |
| author_facet | Evgeniy Potapenko Ciro D. Cordeiro Guozhong Huang Roberto Docampo |
| author_sort | Evgeniy Potapenko |
| collection | DOAJ |
| description | ABSTRACT Inorganic pyrophosphate (PPi) is a by-product of biosynthetic reactions and has bioenergetic and regulatory roles in a variety of cells. Here we show that PPi and other pyrophosphate-containing compounds, including polyphosphate (polyP), can stimulate sodium-dependent depolarization of the membrane potential and Pi conductance in Xenopus oocytes expressing a Saccharomyces cerevisiae or Trypanosoma brucei Na+/Pi symporter. PPi is not taken up by Xenopus oocytes, and deletion of the TbPho91 SPX domain abolished its depolarizing effect. PPi generated outward currents in Na+/Pi-loaded giant vacuoles prepared from wild-type or pho91Δ yeast strains expressing TbPHO91 but not from the pho91Δ strains. Our results suggest that PPi, at physiological concentrations, can function as a signaling molecule releasing Pi from S. cerevisiae vacuoles and T. brucei acidocalcisomes. IMPORTANCE Acidocalcisomes, first described in trypanosomes and known to be present in a variety of cells, have similarities with S. cerevisiae vacuoles in their structure and composition. Both organelles share a Na+/Pi symporter involved in Pi release to the cytosol, where it is needed for biosynthetic reactions. Here we show that PPi, at physiological cytosolic concentrations, stimulates the symporter expressed in either Xenopus oocytes or yeast vacuoles via its SPX domain, revealing a signaling role of this molecule. |
| first_indexed | 2024-12-14T07:13:34Z |
| format | Article |
| id | doaj.art-8406d6ebc9084f0c9049b7819072ecab |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-14T07:13:34Z |
| publishDate | 2019-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-8406d6ebc9084f0c9049b7819072ecab2022-12-21T23:11:45ZengAmerican Society for MicrobiologymSphere2379-50422019-04-014210.1128/mSphere.00045-19Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> VacuolesEvgeniy Potapenko0Ciro D. Cordeiro1Guozhong Huang2Roberto Docampo3Center for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USACenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USACenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USACenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, Georgia, USAABSTRACT Inorganic pyrophosphate (PPi) is a by-product of biosynthetic reactions and has bioenergetic and regulatory roles in a variety of cells. Here we show that PPi and other pyrophosphate-containing compounds, including polyphosphate (polyP), can stimulate sodium-dependent depolarization of the membrane potential and Pi conductance in Xenopus oocytes expressing a Saccharomyces cerevisiae or Trypanosoma brucei Na+/Pi symporter. PPi is not taken up by Xenopus oocytes, and deletion of the TbPho91 SPX domain abolished its depolarizing effect. PPi generated outward currents in Na+/Pi-loaded giant vacuoles prepared from wild-type or pho91Δ yeast strains expressing TbPHO91 but not from the pho91Δ strains. Our results suggest that PPi, at physiological concentrations, can function as a signaling molecule releasing Pi from S. cerevisiae vacuoles and T. brucei acidocalcisomes. IMPORTANCE Acidocalcisomes, first described in trypanosomes and known to be present in a variety of cells, have similarities with S. cerevisiae vacuoles in their structure and composition. Both organelles share a Na+/Pi symporter involved in Pi release to the cytosol, where it is needed for biosynthetic reactions. Here we show that PPi, at physiological cytosolic concentrations, stimulates the symporter expressed in either Xenopus oocytes or yeast vacuoles via its SPX domain, revealing a signaling role of this molecule.https://journals.asm.org/doi/10.1128/mSphere.00045-19SPX domainSaccharomyces cerevisiaeTrypanosoma bruceiXenopus laevisacidocalcisomephosphate-sodium symporter |
| spellingShingle | Evgeniy Potapenko Ciro D. Cordeiro Guozhong Huang Roberto Docampo Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles mSphere SPX domain Saccharomyces cerevisiae Trypanosoma brucei Xenopus laevis acidocalcisome phosphate-sodium symporter |
| title | Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles |
| title_full | Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles |
| title_fullStr | Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles |
| title_full_unstemmed | Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles |
| title_short | Pyrophosphate Stimulates the Phosphate-Sodium Symporter of <italic toggle="yes">Trypanosoma brucei</italic> Acidocalcisomes and <italic toggle="yes">Saccharomyces cerevisiae</italic> Vacuoles |
| title_sort | pyrophosphate stimulates the phosphate sodium symporter of italic toggle yes trypanosoma brucei italic acidocalcisomes and italic toggle yes saccharomyces cerevisiae italic vacuoles |
| topic | SPX domain Saccharomyces cerevisiae Trypanosoma brucei Xenopus laevis acidocalcisome phosphate-sodium symporter |
| url | https://journals.asm.org/doi/10.1128/mSphere.00045-19 |
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