Membrane dynamics at the nuclear exchange junction during early mating (one to four hours) in the ciliate Tetrahymena thermophila

Eric S. Cole, Thomas H. Giddings, Courtney Ozzello, Mark Winey, Eileen O’toole, Judy Orias, Eileen Hamilton, Sabrice Guerrier, Anna Ballard, Tyler Aronsteina

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Using serial-section transmission electron microscopy and three-dimensional (3D) electron tomography, we characterized membrane dynamics that accompany the construction of a nuclear exchange junction between mating cells in the ciliate Tetrahymena thermophila. Our methods revealed a number of previously unknown features. (i) Membrane fusion is initiated by the extension of hundreds of 50-nm-diameter protrusions from the plasma membrane. These protrusions extend from both mating cells across the intercellular space to fuse with membrane of the mating partner. (ii) During this process, small membranebound vesicles or tubules are shed from the plasma membrane and into the extracellular space within the junction. The resultant vesicle-filled pockets within the extracellular space are referred to as junction lumens. (iii) As junction lumens fill with extracellular microvesicles and swell, the plasma membrane limiting these swellings undergoes another deformation, pinching off vesicle- filled vacuoles into the cytoplasm (reclamation). (iv) These structures (resembling multivesicular bodies) seem to associate with autophagosomes abundant near the exchange junction. We propose a model characterizing the membrane-remodeling events that establish cytoplasmic continuity between mating Tetrahymena cells. We also discuss the possible role of nonvesicular lipid transport in conditioning the exchange junction lipid environment. Finally, we raise the possibility of an intercellular signaling mechanism involving microvesicle shedding and uptake.

Original languageEnglish (US)
Pages (from-to)116-127
Number of pages12
JournalEukaryotic Cell
Volume14
Issue number2
DOIs
StatePublished - Jan 1 2015
Externally publishedYes

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Tetrahymena thermophila
Extracellular Space
Cell Membrane
Membranes
Cell-Derived Microparticles
Electron Microscope Tomography
Multivesicular Bodies
Lipids
Tetrahymena
Membrane Fusion
Vacuoles
Transmission Electron Microscopy
Cytoplasm

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

Membrane dynamics at the nuclear exchange junction during early mating (one to four hours) in the ciliate Tetrahymena thermophila. / Cole, Eric S.; Giddings, Thomas H.; Ozzello, Courtney; Winey, Mark; O’toole, Eileen; Orias, Judy; Hamilton, Eileen; Guerrier, Sabrice; Ballard, Anna; Aronsteina, Tyler.

In: Eukaryotic Cell, Vol. 14, No. 2, 01.01.2015, p. 116-127.

Research output: Contribution to journalArticle

Cole, ES, Giddings, TH, Ozzello, C, Winey, M, O’toole, E, Orias, J, Hamilton, E, Guerrier, S, Ballard, A & Aronsteina, T 2015, 'Membrane dynamics at the nuclear exchange junction during early mating (one to four hours) in the ciliate Tetrahymena thermophila', Eukaryotic Cell, vol. 14, no. 2, pp. 116-127. https://doi.org/10.1128/EC.00164-14
Cole, Eric S. ; Giddings, Thomas H. ; Ozzello, Courtney ; Winey, Mark ; O’toole, Eileen ; Orias, Judy ; Hamilton, Eileen ; Guerrier, Sabrice ; Ballard, Anna ; Aronsteina, Tyler. / Membrane dynamics at the nuclear exchange junction during early mating (one to four hours) in the ciliate Tetrahymena thermophila. In: Eukaryotic Cell. 2015 ; Vol. 14, No. 2. pp. 116-127.
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