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A cell-body groove housing the new flagellum tip suggests an adaptation of cellular morphogenesis for parasitism in the bloodstream form of Trypanosoma brucei.

Hughes L, Towers K, Starborg T, Gull K, Vaughan S - J. Cell. Sci. (2013)

Bottom Line: We suggest that the groove has a similar function to the flagella connector.The groove is a mobile junction located alongside the microtubule quartet (MtQ) and occurred within a gap in the subpellicular microtubule corset, causing significant modification of microtubules during elongation of the new flagellum.It appears likely that this novel form of morphogenetic structure has evolved to withstand the hostile immune response in the mammalian blood.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological and Medical Sciences, Faculty of Health and Life Science, Oxford Brookes University, Oxford OX3 0BP, UK.

ABSTRACT
Flagella are highly conserved organelles present in a wide variety of species. In Trypanosoma brucei the single flagellum is necessary for morphogenesis, cell motility and pathogenesis, and is attached along the cell body. A new flagellum is formed alongside the old during the cell division cycle. In the (insect) procyclic form, the flagella connector (FC) attaches the tip of the new flagellum to the side of the old flagellum, ensuring faithful replication of cell architecture. The FC is not present in the bloodstream form of the parasite. We show here, using new imaging techniques including serial block-face scanning electron microscopy (SBF-SEM), that the distal tip of the new flagellum in the bloodstream form is embedded within an invagination in the cell body plasma membrane, named the groove. We suggest that the groove has a similar function to the flagella connector. The groove is a mobile junction located alongside the microtubule quartet (MtQ) and occurred within a gap in the subpellicular microtubule corset, causing significant modification of microtubules during elongation of the new flagellum. It appears likely that this novel form of morphogenetic structure has evolved to withstand the hostile immune response in the mammalian blood.

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Related in: MedlinePlus

A diagrammatic representation summarizing our interpretation of groove ultrastructure and subpellicular microtubule remodeling. (A) Longitudinal view showing the distal tip of the new flagellum embedded in a groove. Orientation is as indicated (a, anterior and p, posterior). Microtubules terminate with their plus ends anterior to the groove (+). The plasma membrane (PM), axoneme (Ax) and paraflagellar rod (PFR) are shown. (B) Diagram representing a hypothetical remodeling of microtubules around the groove through disassembly (deploymerization or severing) of the plus ends of microtubules located anterior to the tip of the new flagellum (1). The new flagellum is elongating in the direction of the red arrow. Assembly and growth of microtubules posterior to the groove might occur at the minus end immediately posterior to the groove or at the plus end, which is at the posterior end of the cell (2).
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f06: A diagrammatic representation summarizing our interpretation of groove ultrastructure and subpellicular microtubule remodeling. (A) Longitudinal view showing the distal tip of the new flagellum embedded in a groove. Orientation is as indicated (a, anterior and p, posterior). Microtubules terminate with their plus ends anterior to the groove (+). The plasma membrane (PM), axoneme (Ax) and paraflagellar rod (PFR) are shown. (B) Diagram representing a hypothetical remodeling of microtubules around the groove through disassembly (deploymerization or severing) of the plus ends of microtubules located anterior to the tip of the new flagellum (1). The new flagellum is elongating in the direction of the red arrow. Assembly and growth of microtubules posterior to the groove might occur at the minus end immediately posterior to the groove or at the plus end, which is at the posterior end of the cell (2).

Mentions: Unlike the spectrin-based cytoskeleton that covers the entire cytoplasmic face of the erythrocyte cell, the groove is a mobile invagination with an entirely different ultrastructure to the subpellicular cytoskeleton that surrounds it. The subpellicular microtubules are cross-linked to one another and to the plasma membrane (Gull, 1999; Hemphill et al., 1991; Vickerman, 1985). Progression of the groove along the cell body as the new flagellum tip progresses clearly requires significant re-modeling of this microtubule array, and Fig. 6 outlines a model for this. Subpellicular microtubules were found to terminate anterior to the groove. The arrangement of microtubule polarity within the planar array of the subpellicular microtubules would predict these to be plus ends (Fig. 6A,B, labeled 1 in B) (Robinson et al., 1995); thus there must be a coordinated disassembly of individual microtubules and associated cross-linking proteins to accommodate the advancing groove. Microtubules were also observed to terminate immediately posterior to the groove (Fig. 6A,B), demonstrating a second area of significant remodeling. It is unlikely that these microtubules have an opposite polarity to the rest of the microtubules in the subpellicular array. There are at least two alternative hypotheses for remodeling of microtubules behind the path of the groove. It is possible that polymerization occurs at the minus ends of these microtubules at the same rate as growth of the new flagellum in order to ‘fill in’ behind the advancing groove (Fig. 6B, labeled 2). Alternatively, microtubule growth could occur at the plus ends, located at or close to the posterior end of the cell (Fig. 6B, labeled 2) and the microtubules could then slide forward within the array.


A cell-body groove housing the new flagellum tip suggests an adaptation of cellular morphogenesis for parasitism in the bloodstream form of Trypanosoma brucei.

Hughes L, Towers K, Starborg T, Gull K, Vaughan S - J. Cell. Sci. (2013)

A diagrammatic representation summarizing our interpretation of groove ultrastructure and subpellicular microtubule remodeling. (A) Longitudinal view showing the distal tip of the new flagellum embedded in a groove. Orientation is as indicated (a, anterior and p, posterior). Microtubules terminate with their plus ends anterior to the groove (+). The plasma membrane (PM), axoneme (Ax) and paraflagellar rod (PFR) are shown. (B) Diagram representing a hypothetical remodeling of microtubules around the groove through disassembly (deploymerization or severing) of the plus ends of microtubules located anterior to the tip of the new flagellum (1). The new flagellum is elongating in the direction of the red arrow. Assembly and growth of microtubules posterior to the groove might occur at the minus end immediately posterior to the groove or at the plus end, which is at the posterior end of the cell (2).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3860315&req=5

f06: A diagrammatic representation summarizing our interpretation of groove ultrastructure and subpellicular microtubule remodeling. (A) Longitudinal view showing the distal tip of the new flagellum embedded in a groove. Orientation is as indicated (a, anterior and p, posterior). Microtubules terminate with their plus ends anterior to the groove (+). The plasma membrane (PM), axoneme (Ax) and paraflagellar rod (PFR) are shown. (B) Diagram representing a hypothetical remodeling of microtubules around the groove through disassembly (deploymerization or severing) of the plus ends of microtubules located anterior to the tip of the new flagellum (1). The new flagellum is elongating in the direction of the red arrow. Assembly and growth of microtubules posterior to the groove might occur at the minus end immediately posterior to the groove or at the plus end, which is at the posterior end of the cell (2).
Mentions: Unlike the spectrin-based cytoskeleton that covers the entire cytoplasmic face of the erythrocyte cell, the groove is a mobile invagination with an entirely different ultrastructure to the subpellicular cytoskeleton that surrounds it. The subpellicular microtubules are cross-linked to one another and to the plasma membrane (Gull, 1999; Hemphill et al., 1991; Vickerman, 1985). Progression of the groove along the cell body as the new flagellum tip progresses clearly requires significant re-modeling of this microtubule array, and Fig. 6 outlines a model for this. Subpellicular microtubules were found to terminate anterior to the groove. The arrangement of microtubule polarity within the planar array of the subpellicular microtubules would predict these to be plus ends (Fig. 6A,B, labeled 1 in B) (Robinson et al., 1995); thus there must be a coordinated disassembly of individual microtubules and associated cross-linking proteins to accommodate the advancing groove. Microtubules were also observed to terminate immediately posterior to the groove (Fig. 6A,B), demonstrating a second area of significant remodeling. It is unlikely that these microtubules have an opposite polarity to the rest of the microtubules in the subpellicular array. There are at least two alternative hypotheses for remodeling of microtubules behind the path of the groove. It is possible that polymerization occurs at the minus ends of these microtubules at the same rate as growth of the new flagellum in order to ‘fill in’ behind the advancing groove (Fig. 6B, labeled 2). Alternatively, microtubule growth could occur at the plus ends, located at or close to the posterior end of the cell (Fig. 6B, labeled 2) and the microtubules could then slide forward within the array.

Bottom Line: We suggest that the groove has a similar function to the flagella connector.The groove is a mobile junction located alongside the microtubule quartet (MtQ) and occurred within a gap in the subpellicular microtubule corset, causing significant modification of microtubules during elongation of the new flagellum.It appears likely that this novel form of morphogenetic structure has evolved to withstand the hostile immune response in the mammalian blood.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological and Medical Sciences, Faculty of Health and Life Science, Oxford Brookes University, Oxford OX3 0BP, UK.

ABSTRACT
Flagella are highly conserved organelles present in a wide variety of species. In Trypanosoma brucei the single flagellum is necessary for morphogenesis, cell motility and pathogenesis, and is attached along the cell body. A new flagellum is formed alongside the old during the cell division cycle. In the (insect) procyclic form, the flagella connector (FC) attaches the tip of the new flagellum to the side of the old flagellum, ensuring faithful replication of cell architecture. The FC is not present in the bloodstream form of the parasite. We show here, using new imaging techniques including serial block-face scanning electron microscopy (SBF-SEM), that the distal tip of the new flagellum in the bloodstream form is embedded within an invagination in the cell body plasma membrane, named the groove. We suggest that the groove has a similar function to the flagella connector. The groove is a mobile junction located alongside the microtubule quartet (MtQ) and occurred within a gap in the subpellicular microtubule corset, causing significant modification of microtubules during elongation of the new flagellum. It appears likely that this novel form of morphogenetic structure has evolved to withstand the hostile immune response in the mammalian blood.

Show MeSH
Related in: MedlinePlus