Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait
The redox state of the host-parasite unit has been hypothesized to play a central role for the fitness of the intraerythrocytic blood stages of the human malaria parasite Plasmodium falciparum. In particular, hemoglobinopathies have been suggested to cause a more oxidizing environment, thereby prote...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-12-01
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| Series: | Redox Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231722003081 |
| _version_ | 1811185448021655552 |
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| author | Marvin Haag Jessica Kehrer Cecilia P. Sanchez Marcel Deponte Michael Lanzer |
| author_facet | Marvin Haag Jessica Kehrer Cecilia P. Sanchez Marcel Deponte Michael Lanzer |
| author_sort | Marvin Haag |
| collection | DOAJ |
| description | The redox state of the host-parasite unit has been hypothesized to play a central role for the fitness of the intraerythrocytic blood stages of the human malaria parasite Plasmodium falciparum. In particular, hemoglobinopathies have been suggested to cause a more oxidizing environment, thereby protecting from severe malaria. Here we determined the redox potential of infected wild-type (hemoglobin AA) or sickle trait (hemoglobin AS) erythrocytes using parasite-encoded variants of the redox-sensitive green-fluorescent protein 2 (roGFP2). Our non-invasive roGFP2 single-cell measurements revealed a reducing steady-state redox potential of −304 ± 11 mV for the erythrocyte cytosol during ring-stage development and a rather sudden oxidation to −278 ± 12 mV during trophozoite-stage development around 28 h post invasion. There was no significant difference between wild-type or sickle trait erythrocytes regarding the stage dependence and the detected increase of the redox potential during the intraerythrocytic life cycle. The steady-state redox potential of the parasite cytosol, between −304 and −313 mV, was highly reducing throughout the life cycle. The redox potential in the parasitophorous vacuole at the interface between the secretory pathway and the erythrocyte was −284 ± 10 mV and remained stable during trophozoite-stage development with implications for the export of disulfide-containing proteins. In summary, P. falciparum blood stage development from the late ring to the early trophozoite stage causes a physiological jump in erythrocyte redox potential irrespective of the presence or absence of hemoglobin S. |
| first_indexed | 2024-04-11T13:29:41Z |
| format | Article |
| id | doaj.art-26d64065d5064f7e9bf306ade1537762 |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-04-11T13:29:41Z |
| publishDate | 2022-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Redox Biology |
| spelling | doaj.art-26d64065d5064f7e9bf306ade15377622022-12-22T04:21:52ZengElsevierRedox Biology2213-23172022-12-0158102536Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell traitMarvin Haag0Jessica Kehrer1Cecilia P. Sanchez2Marcel Deponte3Michael Lanzer4Center of Infectious Diseases, Heidelberg University Medical School, Im Neuenheimer Feld 324, 69120, Heidelberg, GermanyCenter of Infectious Diseases, Heidelberg University Medical School, Im Neuenheimer Feld 324, 69120, Heidelberg, Germany; Infectious Diseases Imaging Platform, Center for Integrative Infectious Diseases, Heidelberg University Medical School, Im Neuenheimer Feld 344, 69120, Heidelberg, GermanyCenter of Infectious Diseases, Heidelberg University Medical School, Im Neuenheimer Feld 324, 69120, Heidelberg, GermanyFaculty of Chemistry, TU Kaiserslautern, Kaiserslautern, Germany; Corresponding author.Center of Infectious Diseases, Heidelberg University Medical School, Im Neuenheimer Feld 324, 69120, Heidelberg, Germany; Corresponding author.The redox state of the host-parasite unit has been hypothesized to play a central role for the fitness of the intraerythrocytic blood stages of the human malaria parasite Plasmodium falciparum. In particular, hemoglobinopathies have been suggested to cause a more oxidizing environment, thereby protecting from severe malaria. Here we determined the redox potential of infected wild-type (hemoglobin AA) or sickle trait (hemoglobin AS) erythrocytes using parasite-encoded variants of the redox-sensitive green-fluorescent protein 2 (roGFP2). Our non-invasive roGFP2 single-cell measurements revealed a reducing steady-state redox potential of −304 ± 11 mV for the erythrocyte cytosol during ring-stage development and a rather sudden oxidation to −278 ± 12 mV during trophozoite-stage development around 28 h post invasion. There was no significant difference between wild-type or sickle trait erythrocytes regarding the stage dependence and the detected increase of the redox potential during the intraerythrocytic life cycle. The steady-state redox potential of the parasite cytosol, between −304 and −313 mV, was highly reducing throughout the life cycle. The redox potential in the parasitophorous vacuole at the interface between the secretory pathway and the erythrocyte was −284 ± 10 mV and remained stable during trophozoite-stage development with implications for the export of disulfide-containing proteins. In summary, P. falciparum blood stage development from the late ring to the early trophozoite stage causes a physiological jump in erythrocyte redox potential irrespective of the presence or absence of hemoglobin S.http://www.sciencedirect.com/science/article/pii/S2213231722003081ReductionOxidationGenetically encoded redox sensorsroGFP2Plasmodium falciparum infected red blood cellsErythrocyte redox potential |
| spellingShingle | Marvin Haag Jessica Kehrer Cecilia P. Sanchez Marcel Deponte Michael Lanzer Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait Redox Biology Reduction Oxidation Genetically encoded redox sensors roGFP2 Plasmodium falciparum infected red blood cells Erythrocyte redox potential |
| title | Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait |
| title_full | Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait |
| title_fullStr | Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait |
| title_full_unstemmed | Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait |
| title_short | Physiological jump in erythrocyte redox potential during Plasmodium falciparum development occurs independent of the sickle cell trait |
| title_sort | physiological jump in erythrocyte redox potential during plasmodium falciparum development occurs independent of the sickle cell trait |
| topic | Reduction Oxidation Genetically encoded redox sensors roGFP2 Plasmodium falciparum infected red blood cells Erythrocyte redox potential |
| url | http://www.sciencedirect.com/science/article/pii/S2213231722003081 |
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