Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane
Abstract Lipid rafts, sterol-rich and sphingolipid-rich microdomains on the plasma membrane are important in processes like cell signaling, adhesion, and protein and lipid transport. The virulence of many eukaryotic parasites is related to raft microdomains on the cell membrane. In the malaria paras...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2021-07-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-94037-3 |
| _version_ | 1818992865736392704 |
|---|---|
| author | Shiomi Koudatsu Tatsunori Masatani Rikako Konishi Masahito Asada Hassan Hakimi Yuna Kurokawa Kanna Tomioku Osamu Kaneko Akikazu Fujita |
| author_facet | Shiomi Koudatsu Tatsunori Masatani Rikako Konishi Masahito Asada Hassan Hakimi Yuna Kurokawa Kanna Tomioku Osamu Kaneko Akikazu Fujita |
| author_sort | Shiomi Koudatsu |
| collection | DOAJ |
| description | Abstract Lipid rafts, sterol-rich and sphingolipid-rich microdomains on the plasma membrane are important in processes like cell signaling, adhesion, and protein and lipid transport. The virulence of many eukaryotic parasites is related to raft microdomains on the cell membrane. In the malaria parasite Plasmodium falciparum, glycosylphosphatidylinositol-anchored proteins, which are important for invasion and are possible targets for vaccine development, are localized in the raft. However, rafts are poorly understood. We used quick-freezing and freeze-fracture immuno-electron microscopy to examine the localization of monosialotetrahexosylganglioside (GM1) and monosialodihexosylganglioside (GM3), putative raft microdomain components in P. falciparum and infected erythrocytes. This method immobilizes molecules in situ, minimizing artifacts. GM3 was localized in the exoplasmic (EF) and cytoplasmic leaflets (PF) of the parasite and the parasitophorous vacuole (PV) membranes, but solely in the EF of the infected erythrocyte membrane, as in the case for uninfected erythrocytes. Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) was localized solely in the PF of erythrocyte, parasite, and PV membranes. This is the first time that GM3, the major component of raft microdomains, was found in the PF of a biological membrane. The unique localization of raft microdomains may be due to P. falciparum lipid metabolism and its unique biological processes, like protein transport from the parasite to infected erythrocytes. |
| first_indexed | 2024-12-20T20:32:57Z |
| format | Article |
| id | doaj.art-df6f382aadb840d8af7110ce358534d8 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-20T20:32:57Z |
| publishDate | 2021-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-df6f382aadb840d8af7110ce358534d82022-12-21T19:27:18ZengNature PortfolioScientific Reports2045-23222021-07-0111111410.1038/s41598-021-94037-3Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membraneShiomi Koudatsu0Tatsunori Masatani1Rikako Konishi2Masahito Asada3Hassan Hakimi4Yuna Kurokawa5Kanna Tomioku6Osamu Kaneko7Akikazu Fujita8Department of Molecular and Cell Biology and Biochemistry, Basic Veterinary Science, Faculty of Veterinary Medicine, Kagoshima UniversityTransboundary Animal Diseases Research Center, Joint Faculty of Veterinary Medicine, Kagoshima UniversityDepartment of Molecular and Cell Biology and Biochemistry, Basic Veterinary Science, Faculty of Veterinary Medicine, Kagoshima UniversityDepartment of Protozoology, Institute of Tropical Medicine (NEKKEN), Nagasaki UniversityDepartment of Protozoology, Institute of Tropical Medicine (NEKKEN), Nagasaki UniversityDepartment of Molecular and Cell Biology and Biochemistry, Basic Veterinary Science, Faculty of Veterinary Medicine, Kagoshima UniversityDepartment of Molecular and Cell Biology and Biochemistry, Basic Veterinary Science, Faculty of Veterinary Medicine, Kagoshima UniversityDepartment of Protozoology, Institute of Tropical Medicine (NEKKEN), Nagasaki UniversityDepartment of Molecular and Cell Biology and Biochemistry, Basic Veterinary Science, Faculty of Veterinary Medicine, Kagoshima UniversityAbstract Lipid rafts, sterol-rich and sphingolipid-rich microdomains on the plasma membrane are important in processes like cell signaling, adhesion, and protein and lipid transport. The virulence of many eukaryotic parasites is related to raft microdomains on the cell membrane. In the malaria parasite Plasmodium falciparum, glycosylphosphatidylinositol-anchored proteins, which are important for invasion and are possible targets for vaccine development, are localized in the raft. However, rafts are poorly understood. We used quick-freezing and freeze-fracture immuno-electron microscopy to examine the localization of monosialotetrahexosylganglioside (GM1) and monosialodihexosylganglioside (GM3), putative raft microdomain components in P. falciparum and infected erythrocytes. This method immobilizes molecules in situ, minimizing artifacts. GM3 was localized in the exoplasmic (EF) and cytoplasmic leaflets (PF) of the parasite and the parasitophorous vacuole (PV) membranes, but solely in the EF of the infected erythrocyte membrane, as in the case for uninfected erythrocytes. Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) was localized solely in the PF of erythrocyte, parasite, and PV membranes. This is the first time that GM3, the major component of raft microdomains, was found in the PF of a biological membrane. The unique localization of raft microdomains may be due to P. falciparum lipid metabolism and its unique biological processes, like protein transport from the parasite to infected erythrocytes.https://doi.org/10.1038/s41598-021-94037-3 |
| spellingShingle | Shiomi Koudatsu Tatsunori Masatani Rikako Konishi Masahito Asada Hassan Hakimi Yuna Kurokawa Kanna Tomioku Osamu Kaneko Akikazu Fujita Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane Scientific Reports |
| title | Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane |
| title_full | Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane |
| title_fullStr | Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane |
| title_full_unstemmed | Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane |
| title_short | Glycosphingolipid GM3 is localized in both exoplasmic and cytoplasmic leaflets of Plasmodium falciparum malaria parasite plasma membrane |
| title_sort | glycosphingolipid gm3 is localized in both exoplasmic and cytoplasmic leaflets of plasmodium falciparum malaria parasite plasma membrane |
| url | https://doi.org/10.1038/s41598-021-94037-3 |
| work_keys_str_mv | AT shiomikoudatsu glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT tatsunorimasatani glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT rikakokonishi glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT masahitoasada glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT hassanhakimi glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT yunakurokawa glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT kannatomioku glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT osamukaneko glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane AT akikazufujita glycosphingolipidgm3islocalizedinbothexoplasmicandcytoplasmicleafletsofplasmodiumfalciparummalariaparasiteplasmamembrane |