The tubulin cofactor C family member TBCCD1 orchestrates cytoskeletal filament formation

Jane André, Stephanie Harrison, Katie Towers, Xin Qi, Sue Vaughan, Paul G McKean, Michael L Ginger

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

TBCCD1 is an enigmatic member of the tubulin-binding cofactor C (TBCC) family of proteins required for mother-daughter centriole linkage in the green alga Chlamydomonas reinhardtii and nucleus-centrosome-Golgi linkage in mammalian cells. Loss of these linkages has severe morphogenetic consequences, but the mechanism(s) through which TBCCD1 contributes to cell organisation is unknown. In the African sleeping sickness parasite Trypanosoma brucei a microtubule-dominant cytoskeleton dictates cell shape, influencing strongly the positioning and inheritance patterns of key intracellular organelles. Here, we show the trypanosome orthologue of TBCCD1 is found at multiple locations: centrioles, the centriole-associated Golgi 'bi-lobe', and the anterior end of the cell body. Loss of Trypanosoma brucei TBCCD1 results in disorganisation of the structurally complex bi-lobe architecture and loss of centriole linkage to the single unit-copy mitochondrial genome (or kinetoplast) of the parasite. We therefore identify TBCCD1 as an essential protein associated with at least two filament-based structures in the trypanosome cytoskeleton. The last common ancestor of trypanosomes, animals and green algae was arguably the last common ancestor of all eukaryotes. On the basis of our observations, and interpretation of published data, we argue for an unexpected co-option of the TBCC domain for an essential non-tubulin-related function at an early point during evolution of the eukaryotic cytoskeleton.

Original languageEnglish
Pages (from-to)5350-5356
Number of pages7
JournalJournal of Cell Science
Volume126
Issue numberPt 23
DOIs
Publication statusPublished - 1 Dec 2013
Externally publishedYes

Fingerprint

Centrioles
Tubulin
Cytoskeleton
Trypanosomiasis
Trypanosoma brucei brucei
Chlorophyta
Parasites
African Trypanosomiasis
Chlamydomonas reinhardtii
Inheritance Patterns
Centrosome
Mitochondrial Genome
Cell Shape
Eukaryota
Microtubules
Organelles
Proteins
Mothers
tubulin-specific chaperone C

Cite this

André, Jane ; Harrison, Stephanie ; Towers, Katie ; Qi, Xin ; Vaughan, Sue ; McKean, Paul G ; Ginger, Michael L. / The tubulin cofactor C family member TBCCD1 orchestrates cytoskeletal filament formation. In: Journal of Cell Science. 2013 ; Vol. 126, No. Pt 23. pp. 5350-5356.
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abstract = "TBCCD1 is an enigmatic member of the tubulin-binding cofactor C (TBCC) family of proteins required for mother-daughter centriole linkage in the green alga Chlamydomonas reinhardtii and nucleus-centrosome-Golgi linkage in mammalian cells. Loss of these linkages has severe morphogenetic consequences, but the mechanism(s) through which TBCCD1 contributes to cell organisation is unknown. In the African sleeping sickness parasite Trypanosoma brucei a microtubule-dominant cytoskeleton dictates cell shape, influencing strongly the positioning and inheritance patterns of key intracellular organelles. Here, we show the trypanosome orthologue of TBCCD1 is found at multiple locations: centrioles, the centriole-associated Golgi 'bi-lobe', and the anterior end of the cell body. Loss of Trypanosoma brucei TBCCD1 results in disorganisation of the structurally complex bi-lobe architecture and loss of centriole linkage to the single unit-copy mitochondrial genome (or kinetoplast) of the parasite. We therefore identify TBCCD1 as an essential protein associated with at least two filament-based structures in the trypanosome cytoskeleton. The last common ancestor of trypanosomes, animals and green algae was arguably the last common ancestor of all eukaryotes. On the basis of our observations, and interpretation of published data, we argue for an unexpected co-option of the TBCC domain for an essential non-tubulin-related function at an early point during evolution of the eukaryotic cytoskeleton.",
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The tubulin cofactor C family member TBCCD1 orchestrates cytoskeletal filament formation. / André, Jane; Harrison, Stephanie; Towers, Katie; Qi, Xin; Vaughan, Sue; McKean, Paul G; Ginger, Michael L.

In: Journal of Cell Science, Vol. 126, No. Pt 23, 01.12.2013, p. 5350-5356.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The tubulin cofactor C family member TBCCD1 orchestrates cytoskeletal filament formation

AU - André, Jane

AU - Harrison, Stephanie

AU - Towers, Katie

AU - Qi, Xin

AU - Vaughan, Sue

AU - McKean, Paul G

AU - Ginger, Michael L

PY - 2013/12/1

Y1 - 2013/12/1

N2 - TBCCD1 is an enigmatic member of the tubulin-binding cofactor C (TBCC) family of proteins required for mother-daughter centriole linkage in the green alga Chlamydomonas reinhardtii and nucleus-centrosome-Golgi linkage in mammalian cells. Loss of these linkages has severe morphogenetic consequences, but the mechanism(s) through which TBCCD1 contributes to cell organisation is unknown. In the African sleeping sickness parasite Trypanosoma brucei a microtubule-dominant cytoskeleton dictates cell shape, influencing strongly the positioning and inheritance patterns of key intracellular organelles. Here, we show the trypanosome orthologue of TBCCD1 is found at multiple locations: centrioles, the centriole-associated Golgi 'bi-lobe', and the anterior end of the cell body. Loss of Trypanosoma brucei TBCCD1 results in disorganisation of the structurally complex bi-lobe architecture and loss of centriole linkage to the single unit-copy mitochondrial genome (or kinetoplast) of the parasite. We therefore identify TBCCD1 as an essential protein associated with at least two filament-based structures in the trypanosome cytoskeleton. The last common ancestor of trypanosomes, animals and green algae was arguably the last common ancestor of all eukaryotes. On the basis of our observations, and interpretation of published data, we argue for an unexpected co-option of the TBCC domain for an essential non-tubulin-related function at an early point during evolution of the eukaryotic cytoskeleton.

AB - TBCCD1 is an enigmatic member of the tubulin-binding cofactor C (TBCC) family of proteins required for mother-daughter centriole linkage in the green alga Chlamydomonas reinhardtii and nucleus-centrosome-Golgi linkage in mammalian cells. Loss of these linkages has severe morphogenetic consequences, but the mechanism(s) through which TBCCD1 contributes to cell organisation is unknown. In the African sleeping sickness parasite Trypanosoma brucei a microtubule-dominant cytoskeleton dictates cell shape, influencing strongly the positioning and inheritance patterns of key intracellular organelles. Here, we show the trypanosome orthologue of TBCCD1 is found at multiple locations: centrioles, the centriole-associated Golgi 'bi-lobe', and the anterior end of the cell body. Loss of Trypanosoma brucei TBCCD1 results in disorganisation of the structurally complex bi-lobe architecture and loss of centriole linkage to the single unit-copy mitochondrial genome (or kinetoplast) of the parasite. We therefore identify TBCCD1 as an essential protein associated with at least two filament-based structures in the trypanosome cytoskeleton. The last common ancestor of trypanosomes, animals and green algae was arguably the last common ancestor of all eukaryotes. On the basis of our observations, and interpretation of published data, we argue for an unexpected co-option of the TBCC domain for an essential non-tubulin-related function at an early point during evolution of the eukaryotic cytoskeleton.

KW - Animals

KW - Centrioles/metabolism

KW - Chlamydomonas reinhardtii/genetics

KW - Cytoskeleton/metabolism

KW - Evolution, Molecular

KW - Golgi Apparatus/metabolism

KW - Humans

KW - Mitochondria/metabolism

KW - Molecular Chaperones/genetics

KW - Protozoan Proteins/genetics

KW - Trypanosoma brucei brucei/genetics

U2 - 10.1242/jcs.136515

DO - 10.1242/jcs.136515

M3 - Article

VL - 126

SP - 5350

EP - 5356

JO - Journal of Cell Science

JF - Journal of Cell Science

SN - 0021-9533

IS - Pt 23

ER -