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Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting
The complexity of intracellular compartments in eukaryotic cells evolved to provide distinct environments to regulate processes necessary for cell proliferation and survival. A large family of predicted cation/proton exchangers (CHX), represented by 28 genes in Arabidopsis thaliana, are associated w...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Biochemistry and Molecular Biology
2011
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3190763/ https://www.ncbi.nlm.nih.gov/pubmed/21795714 http://dx.doi.org/10.1074/jbc.M111.252650 |
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author | Chanroj, Salil Lu(路, Yongxian, 永憲) Padmanaban, Senthilkumar Nanatani(七, Kei, 谷圭) Uozumi(魚, Nobuyuki, 住信之) Rao, Rajini Sze(斯, Heven, 海文) |
author_facet | Chanroj, Salil Lu(路, Yongxian, 永憲) Padmanaban, Senthilkumar Nanatani(七, Kei, 谷圭) Uozumi(魚, Nobuyuki, 住信之) Rao, Rajini Sze(斯, Heven, 海文) |
author_sort | Chanroj, Salil |
collection | PubMed |
description | The complexity of intracellular compartments in eukaryotic cells evolved to provide distinct environments to regulate processes necessary for cell proliferation and survival. A large family of predicted cation/proton exchangers (CHX), represented by 28 genes in Arabidopsis thaliana, are associated with diverse endomembrane compartments and tissues in plants, although their roles are poorly understood. We expressed a phylogenetically related cluster of CHX genes, encoded by CHX15–CHX20, in yeast and bacterial cells engineered to lack multiple cation-handling mechanisms. Of these, CHX16–CHX20 were implicated in pH homeostasis because their expression rescued the alkaline pH-sensitive growth phenotype of the host yeast strain. A smaller subset, CHX17–CHX19, also conferred tolerance to hygromycin B. Further differences were observed in K(+)- and low pH-dependent growth phenotypes. Although CHX17 did not alter cytoplasmic or vacuolar pH in yeast, CHX20 elicited acidification and alkalization of the cytosol and vacuole, respectively. Using heterologous expression in Escherichia coli strains lacking K(+) uptake systems, we provide evidence for K(+) ((86)Rb) transport mediated by CHX17 and CHX20. Finally, we show that CHX17 and CHX20 affected protein sorting as measured by carboxypeptidase Y secretion in yeast mutants grown at alkaline pH. In plant cells, CHX20-RFP co-localized with an endoplasmic reticulum marker, whereas RFP-tagged CHX17–CHX19 co-localized with prevacuolar compartment and endosome markers. Together, these results suggest that in response to environmental cues, multiple CHX transporters differentially modulate K(+) and pH homeostasis of distinct intracellular compartments, which alter membrane trafficking events likely to be critical for adaptation and survival. |
format | Online Article Text |
id | pubmed-3190763 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2011 |
publisher | American Society for Biochemistry and Molecular Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-31907632011-10-20 Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting Chanroj, Salil Lu(路, Yongxian, 永憲) Padmanaban, Senthilkumar Nanatani(七, Kei, 谷圭) Uozumi(魚, Nobuyuki, 住信之) Rao, Rajini Sze(斯, Heven, 海文) J Biol Chem Membrane Biology The complexity of intracellular compartments in eukaryotic cells evolved to provide distinct environments to regulate processes necessary for cell proliferation and survival. A large family of predicted cation/proton exchangers (CHX), represented by 28 genes in Arabidopsis thaliana, are associated with diverse endomembrane compartments and tissues in plants, although their roles are poorly understood. We expressed a phylogenetically related cluster of CHX genes, encoded by CHX15–CHX20, in yeast and bacterial cells engineered to lack multiple cation-handling mechanisms. Of these, CHX16–CHX20 were implicated in pH homeostasis because their expression rescued the alkaline pH-sensitive growth phenotype of the host yeast strain. A smaller subset, CHX17–CHX19, also conferred tolerance to hygromycin B. Further differences were observed in K(+)- and low pH-dependent growth phenotypes. Although CHX17 did not alter cytoplasmic or vacuolar pH in yeast, CHX20 elicited acidification and alkalization of the cytosol and vacuole, respectively. Using heterologous expression in Escherichia coli strains lacking K(+) uptake systems, we provide evidence for K(+) ((86)Rb) transport mediated by CHX17 and CHX20. Finally, we show that CHX17 and CHX20 affected protein sorting as measured by carboxypeptidase Y secretion in yeast mutants grown at alkaline pH. In plant cells, CHX20-RFP co-localized with an endoplasmic reticulum marker, whereas RFP-tagged CHX17–CHX19 co-localized with prevacuolar compartment and endosome markers. Together, these results suggest that in response to environmental cues, multiple CHX transporters differentially modulate K(+) and pH homeostasis of distinct intracellular compartments, which alter membrane trafficking events likely to be critical for adaptation and survival. American Society for Biochemistry and Molecular Biology 2011-09-30 2011-07-27 /pmc/articles/PMC3190763/ /pubmed/21795714 http://dx.doi.org/10.1074/jbc.M111.252650 Text en © 2011 by The American Society for Biochemistry and Molecular Biology, Inc. Author's Choice—Final version full access. Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) applies to Author Choice Articles |
spellingShingle | Membrane Biology Chanroj, Salil Lu(路, Yongxian, 永憲) Padmanaban, Senthilkumar Nanatani(七, Kei, 谷圭) Uozumi(魚, Nobuyuki, 住信之) Rao, Rajini Sze(斯, Heven, 海文) Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting |
title | Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting |
title_full | Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting |
title_fullStr | Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting |
title_full_unstemmed | Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting |
title_short | Plant-Specific Cation/H(+) Exchanger 17 and Its Homologs Are Endomembrane K(+) Transporters with Roles in Protein Sorting |
title_sort | plant-specific cation/h(+) exchanger 17 and its homologs are endomembrane k(+) transporters with roles in protein sorting |
topic | Membrane Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3190763/ https://www.ncbi.nlm.nih.gov/pubmed/21795714 http://dx.doi.org/10.1074/jbc.M111.252650 |
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