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Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii.

Hu K - PLoS Pathog. (2008)

Bottom Line: This study focuses on key events during the biogenesis of the basal complex using high resolution light microscopy, and reveals that daughter basal complexes are established around the duplicated centrioles independently of the structural integrity of the daughter cortical cytoskeleton, and that they are dynamic "caps" at the growing ends of the daughters.This correlates with the constriction of the basal complex, a process that can be artificially induced by increasing cellular calcium concentration.The basal complex is therefore likely to be a new kind of centrin-based contractile apparatus.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Indiana University, Bloomington, Indiana, United States of America. kehu@indiana.edu

ABSTRACT
The apicomplexans are a large group of parasitic protozoa, many of which are important human and animal pathogens, including Plasmodium falciparum and Toxoplasma gondii. These parasites cause disease only when they replicate, and their replication is critically dependent on the proper assembly of the parasite cytoskeletons during cell division. In addition to their importance in pathogenesis, the apicomplexan parasite cytoskeletons are spectacular structures. Therefore, understanding the cytoskeletal biogenesis of these parasites is important not only for parasitology but also of general interest to broader cell biology. Previously, we found that the basal end of T. gondii contains a novel cytoskeletal assembly, the basal complex, a cytoskeletal compartment constructed in concert with the daughter cortical cytoskeleton during cell division. This study focuses on key events during the biogenesis of the basal complex using high resolution light microscopy, and reveals that daughter basal complexes are established around the duplicated centrioles independently of the structural integrity of the daughter cortical cytoskeleton, and that they are dynamic "caps" at the growing ends of the daughters. Compartmentation and polarization of the basal complex is first revealed at a late stage of cell division upon the recruitment of an EF-hand containing calcium binding protein, TgCentrin2. This correlates with the constriction of the basal complex, a process that can be artificially induced by increasing cellular calcium concentration. The basal complex is therefore likely to be a new kind of centrin-based contractile apparatus.

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Related in: MedlinePlus

Centriole Duplication Precedes the Construction of the Basal Complex and the Separation of the Spindle PolesImages show a parasitophorous vacuole containing parasites whose centrioles have duplicated, but the spindle pole still appears as one single spot. No TgMORN1 labeling is seen around the centrosomal area other than in the spindle pole itself. In the three parasites at the bottom of the figure, the duplicated centrioles are still near the basal end of the nucleus, whereas in the other five, the centrioles have started or completed their return migration to the apical end of the nucleus.Green, EGFP-TgMORN1; red, mCherryFP-TgCentrin1; blue, anti-IMC1 antibody detected by Alexa350-anti-mouse IgG.Inset: 2× magnification of the region indicated by the dotted frame. The inset does not include the anti-IMC1 labeling in order to emphasize the difference in localization between TgMORN1 and TgCentrin1 in the centriole/spindle pole assembly.All images are maximum intensity projections of deconvolved 3D stacks.
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ppat-0040010-g002: Centriole Duplication Precedes the Construction of the Basal Complex and the Separation of the Spindle PolesImages show a parasitophorous vacuole containing parasites whose centrioles have duplicated, but the spindle pole still appears as one single spot. No TgMORN1 labeling is seen around the centrosomal area other than in the spindle pole itself. In the three parasites at the bottom of the figure, the duplicated centrioles are still near the basal end of the nucleus, whereas in the other five, the centrioles have started or completed their return migration to the apical end of the nucleus.Green, EGFP-TgMORN1; red, mCherryFP-TgCentrin1; blue, anti-IMC1 antibody detected by Alexa350-anti-mouse IgG.Inset: 2× magnification of the region indicated by the dotted frame. The inset does not include the anti-IMC1 labeling in order to emphasize the difference in localization between TgMORN1 and TgCentrin1 in the centriole/spindle pole assembly.All images are maximum intensity projections of deconvolved 3D stacks.

Mentions: The first sign of cell division is the migration of the centriole to the basal pole of the nucleus, where it replicates (Nishi M, Hu K, Murray J, Roos D, manuscript submitted). The replicated centrioles sandwich the spindle pole (Figure 2), which at this point still appears as one spot. Surprisingly, ring structures containing TgMORN1 are observed forming around the duplicated centrioles even before the separation of the future apical and basal regions of the daughter parasites (Figure 3). These rings are at the outer edges of the initially planar aggregations of daughter cytoskeletal elements that will later become the daughter cortical cytoskeletons (Figure 4). The TgMORN1 rings are therefore likely to be the precursor of the future daughter basal ring complex. Two other components of the mature basal complex in adult parasites, TgCentrin2 (Figure 3B) and TgDLC (data not shown), however, are not found in these early ring structures.


Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii.

Hu K - PLoS Pathog. (2008)

Centriole Duplication Precedes the Construction of the Basal Complex and the Separation of the Spindle PolesImages show a parasitophorous vacuole containing parasites whose centrioles have duplicated, but the spindle pole still appears as one single spot. No TgMORN1 labeling is seen around the centrosomal area other than in the spindle pole itself. In the three parasites at the bottom of the figure, the duplicated centrioles are still near the basal end of the nucleus, whereas in the other five, the centrioles have started or completed their return migration to the apical end of the nucleus.Green, EGFP-TgMORN1; red, mCherryFP-TgCentrin1; blue, anti-IMC1 antibody detected by Alexa350-anti-mouse IgG.Inset: 2× magnification of the region indicated by the dotted frame. The inset does not include the anti-IMC1 labeling in order to emphasize the difference in localization between TgMORN1 and TgCentrin1 in the centriole/spindle pole assembly.All images are maximum intensity projections of deconvolved 3D stacks.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2211554&req=5

ppat-0040010-g002: Centriole Duplication Precedes the Construction of the Basal Complex and the Separation of the Spindle PolesImages show a parasitophorous vacuole containing parasites whose centrioles have duplicated, but the spindle pole still appears as one single spot. No TgMORN1 labeling is seen around the centrosomal area other than in the spindle pole itself. In the three parasites at the bottom of the figure, the duplicated centrioles are still near the basal end of the nucleus, whereas in the other five, the centrioles have started or completed their return migration to the apical end of the nucleus.Green, EGFP-TgMORN1; red, mCherryFP-TgCentrin1; blue, anti-IMC1 antibody detected by Alexa350-anti-mouse IgG.Inset: 2× magnification of the region indicated by the dotted frame. The inset does not include the anti-IMC1 labeling in order to emphasize the difference in localization between TgMORN1 and TgCentrin1 in the centriole/spindle pole assembly.All images are maximum intensity projections of deconvolved 3D stacks.
Mentions: The first sign of cell division is the migration of the centriole to the basal pole of the nucleus, where it replicates (Nishi M, Hu K, Murray J, Roos D, manuscript submitted). The replicated centrioles sandwich the spindle pole (Figure 2), which at this point still appears as one spot. Surprisingly, ring structures containing TgMORN1 are observed forming around the duplicated centrioles even before the separation of the future apical and basal regions of the daughter parasites (Figure 3). These rings are at the outer edges of the initially planar aggregations of daughter cytoskeletal elements that will later become the daughter cortical cytoskeletons (Figure 4). The TgMORN1 rings are therefore likely to be the precursor of the future daughter basal ring complex. Two other components of the mature basal complex in adult parasites, TgCentrin2 (Figure 3B) and TgDLC (data not shown), however, are not found in these early ring structures.

Bottom Line: This study focuses on key events during the biogenesis of the basal complex using high resolution light microscopy, and reveals that daughter basal complexes are established around the duplicated centrioles independently of the structural integrity of the daughter cortical cytoskeleton, and that they are dynamic "caps" at the growing ends of the daughters.This correlates with the constriction of the basal complex, a process that can be artificially induced by increasing cellular calcium concentration.The basal complex is therefore likely to be a new kind of centrin-based contractile apparatus.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Indiana University, Bloomington, Indiana, United States of America. kehu@indiana.edu

ABSTRACT
The apicomplexans are a large group of parasitic protozoa, many of which are important human and animal pathogens, including Plasmodium falciparum and Toxoplasma gondii. These parasites cause disease only when they replicate, and their replication is critically dependent on the proper assembly of the parasite cytoskeletons during cell division. In addition to their importance in pathogenesis, the apicomplexan parasite cytoskeletons are spectacular structures. Therefore, understanding the cytoskeletal biogenesis of these parasites is important not only for parasitology but also of general interest to broader cell biology. Previously, we found that the basal end of T. gondii contains a novel cytoskeletal assembly, the basal complex, a cytoskeletal compartment constructed in concert with the daughter cortical cytoskeleton during cell division. This study focuses on key events during the biogenesis of the basal complex using high resolution light microscopy, and reveals that daughter basal complexes are established around the duplicated centrioles independently of the structural integrity of the daughter cortical cytoskeleton, and that they are dynamic "caps" at the growing ends of the daughters. Compartmentation and polarization of the basal complex is first revealed at a late stage of cell division upon the recruitment of an EF-hand containing calcium binding protein, TgCentrin2. This correlates with the constriction of the basal complex, a process that can be artificially induced by increasing cellular calcium concentration. The basal complex is therefore likely to be a new kind of centrin-based contractile apparatus.

Show MeSH
Related in: MedlinePlus