Disassembly activity of actin-depolymerizing factor (ADF) is associated with distinct cellular processes in apicomplexan parasites

Proteins of the actin-depolymerizing factor (ADF)/cofilin family have been shown to be crucial for the motility and survival of apicomplexan parasites. However, the mechanisms by which ADF proteins fulfill their function remain poorly understood. In this study, we investigate the comparative activit...

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Published inMolecular biology of the cell Vol. 26; no. 17; pp. 3001 - 3012
Main Authors Haase, Silvia, Zimmermann, Dennis, Olshina, Maya A, Wilkinson, Mark, Fisher, Fabio, Tan, Yan Hong, Stewart, Rebecca J, Tonkin, Christopher J, Wong, Wilson, Kovar, David R, Baum, Jake
Format Journal Article
LanguageEnglish
Published United States The American Society for Cell Biology 01.09.2015
Subjects
Actin Cytoskeleton - metabolism
Actins - metabolism
Animals
Cell Movement - physiology
Cytoskeleton - metabolism
Destrin - genetics
Destrin - metabolism
Gene Knockout Techniques
Genetic Association Studies
Lysine - metabolism
Plasmodium falciparum - metabolism
Toxoplasma - metabolism
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Abstract Proteins of the actin-depolymerizing factor (ADF)/cofilin family have been shown to be crucial for the motility and survival of apicomplexan parasites. However, the mechanisms by which ADF proteins fulfill their function remain poorly understood. In this study, we investigate the comparative activities of ADF proteins from Toxoplasma gondii and Plasmodium falciparum, the human malaria parasite, using a conditional T. gondii ADF-knockout line complemented with ADF variants from either species. We show that P. falciparum ADF1 can fully restore native TgADF activity, demonstrating functional conservation between parasites. Strikingly, mutation of a key basic residue (Lys-72), previously implicated in disassembly in PfADF1, had no detectable phenotypic effect on parasite growth, motility, or development. In contrast, organelle segregation was severely impaired when complementing with a TgADF mutant lacking the corresponding residue (Lys-68). Biochemical analyses of each ADF protein confirmed the reduced ability of lysine mutants to mediate actin depolymerization via filament disassembly although not severing, in contrast to previous reports. These data suggest that actin filament disassembly is essential for apicomplexan parasite development but not for motility, as well as pointing to genus-specific coevolution between ADF proteins and their native actin.
AbstractList Proteins of the actin-depolymerizing factor (ADF)/cofilin family have been shown to be crucial for the motility and survival of apicomplexan parasites. However, the mechanisms by which ADF proteins fulfill their function remain poorly understood. In this study, we investigate the comparative activities of ADF proteins from Toxoplasma gondii and Plasmodium falciparum, the human malaria parasite, using a conditional T. gondii ADF-knockout line complemented with ADF variants from either species. We show that P. falciparum ADF1 can fully restore native TgADF activity, demonstrating functional conservation between parasites. Strikingly, mutation of a key basic residue (Lys-72), previously implicated in disassembly in PfADF1, had no detectable phenotypic effect on parasite growth, motility, or development. In contrast, organelle segregation was severely impaired when complementing with a TgADF mutant lacking the corresponding residue (Lys-68). Biochemical analyses of each ADF protein confirmed the reduced ability of lysine mutants to mediate actin depolymerization via filament disassembly although not severing, in contrast to previous reports. These data suggest that actin filament disassembly is essential for apicomplexan parasite development but not for motility, as well as pointing to genus-specific coevolution between ADF proteins and their native actin.
Complementation of a conditional KO of actin-depolymerizing factor (ADF) in Toxoplasma gondii demonstrates that ADF-dependent actin filament disassembly is essential for parasite development but not for cell motility. Furthermore, trans-genera complementation highlights genus-specific coevolution between ADF proteins and their native actins. Proteins of the actin-depolymerizing factor (ADF)/cofilin family have been shown to be crucial for the motility and survival of apicomplexan parasites. However, the mechanisms by which ADF proteins fulfill their function remain poorly understood. In this study, we investigate the comparative activities of ADF proteins from Toxoplasma gondii and Plasmodium falciparum , the human malaria parasite, using a conditional T. gondii ADF-knockout line complemented with ADF variants from either species. We show that P. falciparum ADF1 can fully restore native TgADF activity, demonstrating functional conservation between parasites. Strikingly, mutation of a key basic residue (Lys-72), previously implicated in disassembly in PfADF1, had no detectable phenotypic effect on parasite growth, motility, or development. In contrast, organelle segregation was severely impaired when complementing with a TgADF mutant lacking the corresponding residue (Lys-68). Biochemical analyses of each ADF protein confirmed the reduced ability of lysine mutants to mediate actin depolymerization via filament disassembly although not severing, in contrast to previous reports. These data suggest that actin filament disassembly is essential for apicomplexan parasite development but not for motility, as well as pointing to genus-specific coevolution between ADF proteins and their native actin.
Author Haase, Silvia
Zimmermann, Dennis
Tan, Yan Hong
Kovar, David R
Tonkin, Christopher J
Baum, Jake
Wong, Wilson
Fisher, Fabio
Wilkinson, Mark
Olshina, Maya A
Stewart, Rebecca J
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Snippet Proteins of the actin-depolymerizing factor (ADF)/cofilin family have been shown to be crucial for the motility and survival of apicomplexan parasites....
Complementation of a conditional KO of actin-depolymerizing factor (ADF) in Toxoplasma gondii demonstrates that ADF-dependent actin filament disassembly is...
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SubjectTerms Actin Cytoskeleton - metabolism
Actins - metabolism
Animals
Cell Movement - physiology
Cytoskeleton - metabolism
Destrin - genetics
Destrin - metabolism
Gene Knockout Techniques
Genetic Association Studies
Lysine - metabolism
Plasmodium falciparum - metabolism
Toxoplasma - metabolism
Title Disassembly activity of actin-depolymerizing factor (ADF) is associated with distinct cellular processes in apicomplexan parasites
URI https://www.ncbi.nlm.nih.gov/pubmed/26157165
https://search.proquest.com/docview/1708162372
https://pubmed.ncbi.nlm.nih.gov/PMC4551315
Volume 26
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