A Centriolar FGR1 Oncogene Partner-Like Protein Required for Paraflagellar Rod Assembly, But Not Axoneme Assembly in African Trypanosomes

Jane Harmer, Katie Towers, Max Addison, Sue Vaughan, Michael L. Ginger, Paul G. McKean

Research output: Contribution to journalArticle

Abstract

Proteins of the FGR1 oncogene partner (or FOP)family are found at microtubule organizing centres (MTOCs)including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing (in contrast with mammalian cells, where FOP is essential for flagellum assembly)depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising because PFR nucleation commences approximately 2 mm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localization of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.

LanguageEnglish
Article number170218
Number of pages13
JournalRoyal Society Open Science
Volume8
Issue number7
DOIs
Publication statusPublished - 25 Jul 2018

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Microtubule-Organizing Center
Axoneme
Trypanosomiasis
Flagella
Oncogenes
Basal Bodies
Spindle Poles
Centrioles
Trypanosoma brucei brucei
Spindle Apparatus
Proteins
Oncogene Proteins
Eukaryota
Mitosis
Cell Biology
Epitopes
Parasites

Cite this

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title = "A Centriolar FGR1 Oncogene Partner-Like Protein Required for Paraflagellar Rod Assembly, But Not Axoneme Assembly in African Trypanosomes",
abstract = "Proteins of the FGR1 oncogene partner (or FOP)family are found at microtubule organizing centres (MTOCs)including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing (in contrast with mammalian cells, where FOP is essential for flagellum assembly)depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising because PFR nucleation commences approximately 2 mm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localization of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.",
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A Centriolar FGR1 Oncogene Partner-Like Protein Required for Paraflagellar Rod Assembly, But Not Axoneme Assembly in African Trypanosomes. / Harmer, Jane; Towers, Katie; Addison, Max; Vaughan, Sue; Ginger, Michael L.; McKean, Paul G.

In: Royal Society Open Science, Vol. 8, No. 7, 170218, 25.07.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A Centriolar FGR1 Oncogene Partner-Like Protein Required for Paraflagellar Rod Assembly, But Not Axoneme Assembly in African Trypanosomes

AU - Harmer,Jane

AU - Towers,Katie

AU - Addison,Max

AU - Vaughan,Sue

AU - Ginger,Michael L.

AU - McKean,Paul G.

PY - 2018/7/25

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AB - Proteins of the FGR1 oncogene partner (or FOP)family are found at microtubule organizing centres (MTOCs)including, in flagellate eukaryotes, the centriole or flagellar basal body from which the axoneme extends. We report conservation of FOP family proteins, TbFOPL and TbOFD1, in the evolutionarily divergent sleeping sickness parasite Trypanosoma brucei, showing (in contrast with mammalian cells, where FOP is essential for flagellum assembly)depletion of a trypanosome FOP homologue, TbFOPL, affects neither axoneme nor flagellum elongation. Instead, TbFOPL depletion causes catastrophic failure in assembly of a lineage-specific, extra-axonemal structure, the paraflagellar rod (PFR). That depletion of centriolar TbFOPL causes failure in PFR assembly is surprising because PFR nucleation commences approximately 2 mm distal from the basal body. When over-expressed with a C-terminal myc-epitope, TbFOPL was also observed at mitotic spindle poles. Little is known about bi-polar spindle assembly during closed trypanosome mitosis, but indication of a possible additional MTOC function for TbFOPL parallels MTOC localization of FOP-like protein TONNEAU1 in acentriolar plants. More generally, our functional analysis of TbFOPL emphasizes significant differences in evolutionary cell biology trajectories of FOP-family proteins. We discuss how at the molecular level FOP homologues may contribute to flagellum assembly and function in diverse flagellates.

KW - Basal body

KW - Cell morphogenesis

KW - Ciliogenesis

KW - FGR1 oncogene partner

KW - Paraflagellar rod

KW - Trypanosoma brucei

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DO - 10.1098/rsob.170218

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T2 - Royal Society Open Science

JF - Royal Society Open Science

SN - 2054-5703

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