Tensegrity model of pattern formation during cytokinesis of a ciliate, Paramecium: Effects of an inhibitor of phosphorylation, 6‐dimethylaminopurine, and of adenine

Abstract

During cytokinesis of the ciliate Paramecium, the two oral apparatuses ( O h ) , localized close to the fission line, are displaced to a mid-region of daughter cells by a tearing off of the OAs and adjacent cortices from the fission line and their subsequent movement toward the poles of the dividing cell. Two possible mechanisms for this displacement were examined: 1) a mechanism whereby the contraction of the fission line in the vicinity of OAs brings about the change of configuration of the adjacent cortices and subsequent displacement of OAs and 2) a mechanism whereby programmed transient depolymerization of the inner cytoskeletal contractile infraciliary lattice in the vicinity of OAs acts as a motive force for displacement of the OAs, together with the most superficial outer lattice of the cytoskeleton which does not disassemble. Our working hypotheses were based on observations on the behavior of the outer lattice, where the infraciliary lattice disintegrates and the fission line assembles.To study the mechanics of pattern formation during cytokinesis of Paramecium, morphogenesis was followed in the presence of an inhibitor of phosphorylation, 6-dimethylaminopurine (6-DMAP), and of adenine, which prevented disassembly of the inner lattice and arrested cytokinesis and dislocation of OAs. Nearly all defects in morphogenesis were correlated with failure of the infraciliary lattice to disassemble and failure of the fission line to assemble. It appears that the superficial cortical structures and the contractile infraciliary lattice represent a tensegrity model of morphogenesis during cytokinesis in Paramecium.

Polarity in Ciliate Models: From Cilia to Cell Architecture

“…Another antibody, the XXXIX-12G9, obtained against the Tetrahymena cortex recognizes filaments that are visible before the proliferation of new BBs in the oral primordium and in the fission line suggesting that the recognized protein is involved in these events (Jerka-Dziadosz and Czupryn, 1997). Data coming from a few mutants support the view that the epiplasm may contain information for pattern organization (Kaczanowska et al, 1995). In Tetrahymena NPl mutant cells, the BBs of the anarchic field are unable to orient and attain a correct positioning during OA assembly.…”

Genetic and Epigenetic Factors Affecting Meiosis Induction in Eukaryotes Revealed in Paramecium Research

“…Hence, all the alterations in the balance of cellular mechanical forces will drive a structural remodeling cascade at the molecular level. In accordance to the tensegrity model, KACZANOWSKA et al (1995) demonstrated that during Paramecium cell division, the mechanical consequences of phosphorylation-dependent assembly or disassembly of certain proteins are involved in the mechanics of pattern formation that govern the equatorial positioning of the oral apparatus. Tensegrity is a plausible model explaining the mechanism of the cellular response to mechanical stress exerted on Paramecium doublets if initial mechanical cortical symmetry is broken at the moment of fusion of two macronuclei into one large structure, which is considered as a first step of the regulation process.…”

Nuclear and Cortical Regulation in Doublets of Paramecium: II. When and How do Two Cortical Domains Reorganize to One?

“…The central idea of this model is that cell integrity is maintained globally by a balance of tensional forces exerted by a continuous network (postulated to be actin filaments in tissue cells) and of discontinuous compression‐resistant struts (proposed to be microtubules) that resist this tension. This general model has been applied to cell division in Paramecium by Kaczanowska et al (1995). If it were also to be applied to regulation of unbalanced doublets to singlets, one would need to identify the relevant continuous tensional and discontinuous compressional elements in this microtubule‐rich but actin‐poor (Cohen, Garreau de Loubresse, and Beisson 1984) organism.…”

“…Furthermore, these two species differ in size, number of ciliary rows, and shapes of polar regions. Cultures of doublet cells were grown according to the standard method (Kaczanowska et al 1995) in a wheat grass powder buffered medium enriched with β‐sitosterol (0.5 μg/ml), inoculated with Enterobacter aerogenes.…”