Flagellar membrane fusion and protein exchange in trypanosomes; a new form of cell-cell communication?

Imhof, Simon; Fragoso, Cristina; Hemphill, Andrew; Von Schubert, Conrad; Li, Dong; Legant, Wesley; Betzig, Erik; Roditi, Isabel (2016). Flagellar membrane fusion and protein exchange in trypanosomes; a new form of cell-cell communication? F1000Research, 5(682), p. 682. F1000 Research Ltd 10.12688/f1000research.8249.1

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Diverse structures facilitate direct exchange of proteins between cells, including plasmadesmata in plants and tunnelling nanotubes in bacteria and higher eukaryotes. Here we describe a new mechanism of protein transfer, flagellar membrane fusion, in the unicellular parasite Trypanosoma brucei. When fluorescently tagged trypanosomes were co-cultured, a small proportion of double-positive cells were observed. The formation of double-positive cells was dependent on the presence of extracellular calcium and was enhanced by placing cells in medium supplemented with fresh bovine serum. Time-lapse microscopy revealed that double-positive cells arose by bidirectional protein exchange in the absence of nuclear transfer. Furthermore, super-resolution microscopy showed that this process occurred in ≤1 minute, the limit of temporal resolution in these experiments. Both cytoplasmic and membrane proteins could be transferred provided they gained access to the flagellum. Intriguingly, a component of the RNAi machinery (Argonaute) was able to move between cells, raising the possibility that small interfering RNAs are transported as cargo. Transmission electron microscopy showed that shared flagella contained two axonemes and two paraflagellar rods bounded by a single membrane. In some cases flagellar fusion was partial and interactions between cells were transient. In other cases fusion occurred along the entire length of the flagellum, was stable for several hours and might be irreversible. Fusion did not appear to be deleterious for cell function: paired cells were motile and could give rise to progeny while fused. The motile flagella of unicellular organisms are related to the sensory cilia of higher eukaryotes, raising the possibility that protein transfer between cells via cilia or flagella occurs more widely in nature.

Item Type:

Journal Article (Original Article)

Division/Institute:

08 Faculty of Science > Department of Biology > Institute of Cell Biology

Graduate School:

Graduate School for Cellular and Biomedical Sciences (GCB)

UniBE Contributor:

Imhof, Simon; Hemphill, Andrew; Von Schubert, Conrad and Roditi, Isabel

Subjects:

500 Science > 570 Life sciences; biology

ISSN:

2046-1402

Publisher:

F1000 Research Ltd

Funders:

[UNSPECIFIED] HHMI Senior International Scholars Program
[UNSPECIFIED] Swiss National Science Foundation
[UNSPECIFIED] Howard Hughes Medical Institute
[UNSPECIFIED] Janelia Research Campus Visitors' Program

Language:

English

Submitter:

Isabel Roditi

Date Deposited:

21 Sep 2016 08:03

Last Modified:

02 Oct 2016 02:12

Publisher DOI:

10.12688/f1000research.8249.1

PubMed ID:

27239276

BORIS DOI:

10.7892/boris.88000

URI:

https://boris.unibe.ch/id/eprint/88000

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