Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy
Apicomplexan parasites exhibit tremendous diversity in much of their fundamental cell biology, but study of these organisms using light microscopy is often hindered by their small size. Ultrastructural expansion microscopy (U-ExM) is a microscopy preparation method that physically expands the sample...
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| Format: | Article |
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eLife Sciences Publications Ltd
2023-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/88088 |
| _version_ | 1797387058281447424 |
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| author | Benjamin Liffner Ana Karla Cepeda Diaz James Blauwkamp David Anaguano Sonja Frolich Vasant Muralidharan Danny W Wilson Jeffrey D Dvorin Sabrina Absalon |
| author_facet | Benjamin Liffner Ana Karla Cepeda Diaz James Blauwkamp David Anaguano Sonja Frolich Vasant Muralidharan Danny W Wilson Jeffrey D Dvorin Sabrina Absalon |
| author_sort | Benjamin Liffner |
| collection | DOAJ |
| description | Apicomplexan parasites exhibit tremendous diversity in much of their fundamental cell biology, but study of these organisms using light microscopy is often hindered by their small size. Ultrastructural expansion microscopy (U-ExM) is a microscopy preparation method that physically expands the sample by ~4.5×. Here, we apply U-ExM to the human malaria parasite Plasmodium falciparum during the asexual blood stage of its lifecycle to understand how this parasite is organized in three dimensions. Using a combination of dye-conjugated reagents and immunostaining, we have cataloged 13 different P. falciparum structures or organelles across the intraerythrocytic development of this parasite and made multiple observations about fundamental parasite cell biology. We describe that the outer centriolar plaque and its associated proteins anchor the nucleus to the parasite plasma membrane during mitosis. Furthermore, the rhoptries, Golgi, basal complex, and inner membrane complex, which form around this anchoring site while nuclei are still dividing, are concurrently segregated and maintain an association to the outer centriolar plaque until the start of segmentation. We also show that the mitochondrion and apicoplast undergo sequential fission events while maintaining an association with the outer centriolar plaque during cytokinesis. Collectively, this study represents the most detailed ultrastructural analysis of P. falciparum during its intraerythrocytic development to date and sheds light on multiple poorly understood aspects of its organelle biogenesis and fundamental cell biology. |
| first_indexed | 2024-03-08T22:19:17Z |
| format | Article |
| id | doaj.art-63dcb9b405fd4cbf8adabdec1f6400ba |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-08T22:19:17Z |
| publishDate | 2023-12-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj.art-63dcb9b405fd4cbf8adabdec1f6400ba2023-12-18T15:41:44ZengeLife Sciences Publications LtdeLife2050-084X2023-12-011210.7554/eLife.88088Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopyBenjamin Liffner0https://orcid.org/0000-0002-1573-6139Ana Karla Cepeda Diaz1https://orcid.org/0000-0002-2033-461XJames Blauwkamp2https://orcid.org/0000-0002-7639-2800David Anaguano3Sonja Frolich4https://orcid.org/0000-0002-8673-3437Vasant Muralidharan5https://orcid.org/0000-0001-6367-6284Danny W Wilson6https://orcid.org/0000-0002-5073-1405Jeffrey D Dvorin7https://orcid.org/0000-0002-5883-7271Sabrina Absalon8https://orcid.org/0000-0003-2468-8156Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, United StatesBiological and Biomedical Sciences, Harvard Medical School, Boston, United States; Division of Infectious Diseases, Boston Children’s Hospital, Boston, United StatesDepartment of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, United StatesCenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, United States; Department of Cellular Biology, Franklin College of Arts and Sciences, University of Georgia, Athens, United StatesResearch Centre for Infectious Diseases, School of Biological Sciences, University of Adelaide, Adelaide, Australia; Institute for Photonics and Advanced Sensing, University of Adelaide, Adelaide, AustraliaCenter for Tropical and Emerging Global Diseases, University of Georgia, Athens, United States; Department of Cellular Biology, Franklin College of Arts and Sciences, University of Georgia, Athens, United StatesResearch Centre for Infectious Diseases, School of Biological Sciences, University of Adelaide, Adelaide, Australia; Institute for Photonics and Advanced Sensing, University of Adelaide, Adelaide, Australia; Burnet Institute, 85 Commercial Road, Melbourne, AustraliaDivision of Infectious Diseases, Boston Children’s Hospital, Boston, United States; Department of Pediatrics, Harvard Medical School, Boston, United StatesDepartment of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, United StatesApicomplexan parasites exhibit tremendous diversity in much of their fundamental cell biology, but study of these organisms using light microscopy is often hindered by their small size. Ultrastructural expansion microscopy (U-ExM) is a microscopy preparation method that physically expands the sample by ~4.5×. Here, we apply U-ExM to the human malaria parasite Plasmodium falciparum during the asexual blood stage of its lifecycle to understand how this parasite is organized in three dimensions. Using a combination of dye-conjugated reagents and immunostaining, we have cataloged 13 different P. falciparum structures or organelles across the intraerythrocytic development of this parasite and made multiple observations about fundamental parasite cell biology. We describe that the outer centriolar plaque and its associated proteins anchor the nucleus to the parasite plasma membrane during mitosis. Furthermore, the rhoptries, Golgi, basal complex, and inner membrane complex, which form around this anchoring site while nuclei are still dividing, are concurrently segregated and maintain an association to the outer centriolar plaque until the start of segmentation. We also show that the mitochondrion and apicoplast undergo sequential fission events while maintaining an association with the outer centriolar plaque during cytokinesis. Collectively, this study represents the most detailed ultrastructural analysis of P. falciparum during its intraerythrocytic development to date and sheds light on multiple poorly understood aspects of its organelle biogenesis and fundamental cell biology.https://elifesciences.org/articles/88088Plasmodiumexpansion microscopyMTOCcytokinesismalaria |
| spellingShingle | Benjamin Liffner Ana Karla Cepeda Diaz James Blauwkamp David Anaguano Sonja Frolich Vasant Muralidharan Danny W Wilson Jeffrey D Dvorin Sabrina Absalon Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy eLife Plasmodium expansion microscopy MTOC cytokinesis malaria |
| title | Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy |
| title_full | Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy |
| title_fullStr | Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy |
| title_full_unstemmed | Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy |
| title_short | Atlas of Plasmodium falciparum intraerythrocytic development using expansion microscopy |
| title_sort | atlas of plasmodium falciparum intraerythrocytic development using expansion microscopy |
| topic | Plasmodium expansion microscopy MTOC cytokinesis malaria |
| url | https://elifesciences.org/articles/88088 |
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