Spatial localisation of actin filaments across developmental stages of the malaria parasite.
Actin dynamics have been implicated in a variety of developmental processes during the malaria parasite lifecycle. Parasite motility, in particular, is thought to critically depend on an actomyosin motor located in the outer pellicle of the parasite cell. Efforts to understand the diverse roles acti...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Journal article |
| Language: | English |
| Published: |
Public Library of Science
2012
|
| _version_ | 1797082467695329280 |
|---|---|
| author | Angrisano, F Riglar, D Sturm, A Volz, J Delves, M Zuccala, E Turnbull, L Dekiwadia, C Olshina, M Marapana, D Wong, W Mollard, V Bradin, C Tonkin, C Gunning, P Ralph, SA Whitchurch, C Sinden, R Cowman, A McFadden, G Baum, J |
| author_facet | Angrisano, F Riglar, D Sturm, A Volz, J Delves, M Zuccala, E Turnbull, L Dekiwadia, C Olshina, M Marapana, D Wong, W Mollard, V Bradin, C Tonkin, C Gunning, P Ralph, SA Whitchurch, C Sinden, R Cowman, A McFadden, G Baum, J |
| author_sort | Angrisano, F |
| collection | OXFORD |
| description | Actin dynamics have been implicated in a variety of developmental processes during the malaria parasite lifecycle. Parasite motility, in particular, is thought to critically depend on an actomyosin motor located in the outer pellicle of the parasite cell. Efforts to understand the diverse roles actin plays have, however, been hampered by an inability to detect microfilaments under native conditions. To visualise the spatial dynamics of actin we generated a parasite-specific actin antibody that shows preferential recognition of filamentous actin and applied this tool to different lifecycle stages (merozoites, sporozoites and ookinetes) of the human and mouse malaria parasite species Plasmodium falciparum and P. berghei along with tachyzoites from the related apicomplexan parasite Toxoplasma gondii. Actin filament distribution was found associated with three core compartments: the nuclear periphery, pellicular membranes of motile or invasive parasite forms and in a ring-like distribution at the tight junction during merozoite invasion of erythrocytes in both human and mouse malaria parasites. Localisation at the nuclear periphery is consistent with an emerging role of actin in facilitating parasite gene regulation. During invasion, we show that the actin ring at the parasite-host cell tight junction is dependent on dynamic filament turnover. Super-resolution imaging places this ring posterior to, and not concentric with, the junction marker rhoptry neck protein 4. This implies motor force relies on the engagement of dynamic microfilaments at zones of traction, though not necessarily directly through receptor-ligand interactions at sites of adhesion during invasion. Combined, these observations extend current understanding of the diverse roles actin plays in malaria parasite development and apicomplexan cell motility, in particular refining understanding on the linkage of the internal parasite gliding motor with the extra-cellular milieu. |
| first_indexed | 2024-03-07T01:28:29Z |
| format | Journal article |
| id | oxford-uuid:92c77549-1c2d-45e2-9594-8ced672a9e2a |
| institution | University of Oxford |
| language | English |
| last_indexed | 2024-03-07T01:28:29Z |
| publishDate | 2012 |
| publisher | Public Library of Science |
| record_format | dspace |
| spelling | oxford-uuid:92c77549-1c2d-45e2-9594-8ced672a9e2a2022-03-26T23:28:09ZSpatial localisation of actin filaments across developmental stages of the malaria parasite.Journal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:92c77549-1c2d-45e2-9594-8ced672a9e2aEnglishSymplectic Elements at OxfordPublic Library of Science2012Angrisano, FRiglar, DSturm, AVolz, JDelves, MZuccala, ETurnbull, LDekiwadia, COlshina, MMarapana, DWong, WMollard, VBradin, CTonkin, CGunning, PRalph, SAWhitchurch, CSinden, RCowman, AMcFadden, GBaum, JActin dynamics have been implicated in a variety of developmental processes during the malaria parasite lifecycle. Parasite motility, in particular, is thought to critically depend on an actomyosin motor located in the outer pellicle of the parasite cell. Efforts to understand the diverse roles actin plays have, however, been hampered by an inability to detect microfilaments under native conditions. To visualise the spatial dynamics of actin we generated a parasite-specific actin antibody that shows preferential recognition of filamentous actin and applied this tool to different lifecycle stages (merozoites, sporozoites and ookinetes) of the human and mouse malaria parasite species Plasmodium falciparum and P. berghei along with tachyzoites from the related apicomplexan parasite Toxoplasma gondii. Actin filament distribution was found associated with three core compartments: the nuclear periphery, pellicular membranes of motile or invasive parasite forms and in a ring-like distribution at the tight junction during merozoite invasion of erythrocytes in both human and mouse malaria parasites. Localisation at the nuclear periphery is consistent with an emerging role of actin in facilitating parasite gene regulation. During invasion, we show that the actin ring at the parasite-host cell tight junction is dependent on dynamic filament turnover. Super-resolution imaging places this ring posterior to, and not concentric with, the junction marker rhoptry neck protein 4. This implies motor force relies on the engagement of dynamic microfilaments at zones of traction, though not necessarily directly through receptor-ligand interactions at sites of adhesion during invasion. Combined, these observations extend current understanding of the diverse roles actin plays in malaria parasite development and apicomplexan cell motility, in particular refining understanding on the linkage of the internal parasite gliding motor with the extra-cellular milieu. |
| spellingShingle | Angrisano, F Riglar, D Sturm, A Volz, J Delves, M Zuccala, E Turnbull, L Dekiwadia, C Olshina, M Marapana, D Wong, W Mollard, V Bradin, C Tonkin, C Gunning, P Ralph, SA Whitchurch, C Sinden, R Cowman, A McFadden, G Baum, J Spatial localisation of actin filaments across developmental stages of the malaria parasite. |
| title | Spatial localisation of actin filaments across developmental stages of the malaria parasite. |
| title_full | Spatial localisation of actin filaments across developmental stages of the malaria parasite. |
| title_fullStr | Spatial localisation of actin filaments across developmental stages of the malaria parasite. |
| title_full_unstemmed | Spatial localisation of actin filaments across developmental stages of the malaria parasite. |
| title_short | Spatial localisation of actin filaments across developmental stages of the malaria parasite. |
| title_sort | spatial localisation of actin filaments across developmental stages of the malaria parasite |
| work_keys_str_mv | AT angrisanof spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT riglard spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT sturma spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT volzj spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT delvesm spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT zuccalae spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT turnbulll spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT dekiwadiac spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT olshinam spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT marapanad spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT wongw spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT mollardv spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT bradinc spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT tonkinc spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT gunningp spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT ralphsa spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT whitchurchc spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT sindenr spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT cowmana spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT mcfaddeng spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite AT baumj spatiallocalisationofactinfilamentsacrossdevelopmentalstagesofthemalariaparasite |