Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development

ABSTRACT The inner membrane complex (IMC) of apicomplexan parasites contains a network of intermediate filament-like proteins. The 14 alveolin domain-containing IMC proteins in Toxoplasma gondii fall into different groups defined by their distinct spatiotemporal dynamics during the internal budding...

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Autores principales:	Rashmi Dubey, Brooke Harrison, Sriveny Dangoudoubiyam, Giulia Bandini, Katherine Cheng, Aziz Kosber, Carolina Agop-Nersesian, Daniel K. Howe, John Samuelson, David J. P. Ferguson, Marc-Jan Gubbels
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	IMC Sarcocystis Toxoplasma endodyogeny endopolygeny gametocyte Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/42927399fafb4a71bb9dae7a12a49fc4
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spelling	oai:doaj.org-article:42927399fafb4a71bb9dae7a12a49fc42021-11-15T15:22:05ZDifferential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development10.1128/mSphere.00409-172379-5042https://doaj.org/article/42927399fafb4a71bb9dae7a12a49fc42017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00409-17https://doaj.org/toc/2379-5042ABSTRACT The inner membrane complex (IMC) of apicomplexan parasites contains a network of intermediate filament-like proteins. The 14 alveolin domain-containing IMC proteins in Toxoplasma gondii fall into different groups defined by their distinct spatiotemporal dynamics during the internal budding process of tachyzoites. Here, we analyzed representatives of different IMC protein groups across all stages of the Toxoplasma life cycle and during Sarcocystis neurona asexual development. We found that across asexually dividing Toxoplasma stages, IMC7 is present exclusively in the mother’s cytoskeleton, whereas IMC1 and IMC3 are both present in mother and daughter cytoskeletons (IMC3 is strongly enriched in daughter buds). In developing macro- and microgametocytes, IMC1 and -3 are absent, whereas IMC7 is lost in early microgametocytes but retained in macrogametocytes until late in their development. We found no roles for IMC proteins during meiosis and sporoblast formation. However, we observed that IMC1 and IMC3, but not IMC7, are present in sporozoites. Although the spatiotemporal pattern of IMC15 and IMC3 suggests orthologous functions in Sarcocystis, IMC7 may have functionally diverged in Sarcocystis merozoites. To functionally characterize IMC proteins, we knocked out IMC7, -12, -14, and -15 in Toxoplasma. IMC14 and -15 appear to be involved in switching between endodyogeny and endopolygeny. In addition, IMC7, -12, and -14, which are all recruited to the cytoskeleton outside cytokinesis, are critical for the structural integrity of extracellular tachyzoites. Altogether, stage- and development-specific roles for IMC proteins can be discerned, suggesting different niches for each IMC protein across the entire life cycle. IMPORTANCE The inner membrane complex (IMC) is a defining feature of apicomplexan parasites key to both their motility and unique cell division. To provide further insights into the IMC, we analyzed the dynamics and functions of representative alveolin domain-containing IMC proteins across developmental stages. Our work shows universal but distinct roles for IMC1, -3, and -7 during Toxoplasma asexual division but more specialized functions for these proteins during gametogenesis. In addition, we find that IMC15 is involved in daughter formation in both Toxoplasma and Sarcocystis. IMC14 and IMC15 function in limiting the number of Toxoplasma offspring per division. Furthermore, IMC7, -12, and -14, which are recruited in the G1 cell cycle stage, are required for stress resistance of extracellular tachyzoites. Thus, although the roles of the different IMC proteins appear to overlap, stage- and development-specific behaviors indicate that their functions are uniquely tailored to each life stage requirement.Rashmi DubeyBrooke HarrisonSriveny DangoudoubiyamGiulia BandiniKatherine ChengAziz KosberCarolina Agop-NersesianDaniel K. HoweJohn SamuelsonDavid J. P. FergusonMarc-Jan GubbelsAmerican Society for MicrobiologyarticleIMCSarcocystisToxoplasmaendodyogenyendopolygenygametocyteMicrobiologyQR1-502ENmSphere, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	IMC Sarcocystis Toxoplasma endodyogeny endopolygeny gametocyte Microbiology QR1-502
spellingShingle	IMC Sarcocystis Toxoplasma endodyogeny endopolygeny gametocyte Microbiology QR1-502 Rashmi Dubey Brooke Harrison Sriveny Dangoudoubiyam Giulia Bandini Katherine Cheng Aziz Kosber Carolina Agop-Nersesian Daniel K. Howe John Samuelson David J. P. Ferguson Marc-Jan Gubbels Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development
description	ABSTRACT The inner membrane complex (IMC) of apicomplexan parasites contains a network of intermediate filament-like proteins. The 14 alveolin domain-containing IMC proteins in Toxoplasma gondii fall into different groups defined by their distinct spatiotemporal dynamics during the internal budding process of tachyzoites. Here, we analyzed representatives of different IMC protein groups across all stages of the Toxoplasma life cycle and during Sarcocystis neurona asexual development. We found that across asexually dividing Toxoplasma stages, IMC7 is present exclusively in the mother’s cytoskeleton, whereas IMC1 and IMC3 are both present in mother and daughter cytoskeletons (IMC3 is strongly enriched in daughter buds). In developing macro- and microgametocytes, IMC1 and -3 are absent, whereas IMC7 is lost in early microgametocytes but retained in macrogametocytes until late in their development. We found no roles for IMC proteins during meiosis and sporoblast formation. However, we observed that IMC1 and IMC3, but not IMC7, are present in sporozoites. Although the spatiotemporal pattern of IMC15 and IMC3 suggests orthologous functions in Sarcocystis, IMC7 may have functionally diverged in Sarcocystis merozoites. To functionally characterize IMC proteins, we knocked out IMC7, -12, -14, and -15 in Toxoplasma. IMC14 and -15 appear to be involved in switching between endodyogeny and endopolygeny. In addition, IMC7, -12, and -14, which are all recruited to the cytoskeleton outside cytokinesis, are critical for the structural integrity of extracellular tachyzoites. Altogether, stage- and development-specific roles for IMC proteins can be discerned, suggesting different niches for each IMC protein across the entire life cycle. IMPORTANCE The inner membrane complex (IMC) is a defining feature of apicomplexan parasites key to both their motility and unique cell division. To provide further insights into the IMC, we analyzed the dynamics and functions of representative alveolin domain-containing IMC proteins across developmental stages. Our work shows universal but distinct roles for IMC1, -3, and -7 during Toxoplasma asexual division but more specialized functions for these proteins during gametogenesis. In addition, we find that IMC15 is involved in daughter formation in both Toxoplasma and Sarcocystis. IMC14 and IMC15 function in limiting the number of Toxoplasma offspring per division. Furthermore, IMC7, -12, and -14, which are recruited in the G1 cell cycle stage, are required for stress resistance of extracellular tachyzoites. Thus, although the roles of the different IMC proteins appear to overlap, stage- and development-specific behaviors indicate that their functions are uniquely tailored to each life stage requirement.
format	article
author	Rashmi Dubey Brooke Harrison Sriveny Dangoudoubiyam Giulia Bandini Katherine Cheng Aziz Kosber Carolina Agop-Nersesian Daniel K. Howe John Samuelson David J. P. Ferguson Marc-Jan Gubbels
author_facet	Rashmi Dubey Brooke Harrison Sriveny Dangoudoubiyam Giulia Bandini Katherine Cheng Aziz Kosber Carolina Agop-Nersesian Daniel K. Howe John Samuelson David J. P. Ferguson Marc-Jan Gubbels
author_sort	Rashmi Dubey
title	Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development
title_short	Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development
title_full	Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development
title_fullStr	Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development
title_full_unstemmed	Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development
title_sort	differential roles for inner membrane complex proteins across <named-content content-type="genus-species">toxoplasma gondii</named-content> and <italic toggle="yes">sarcocystis neurona</italic> development
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/42927399fafb4a71bb9dae7a12a49fc4
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Differential Roles for Inner Membrane Complex Proteins across <named-content content-type="genus-species">Toxoplasma gondii</named-content> and <italic toggle="yes">Sarcocystis neurona</italic> Development

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