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Preserving cell shape under environmental stress

Abstract

Maintaining cell shape and tone is crucial for the function and survival of cells and tissues. Mechanotransduction relies on the transformation of minuscule mechanical forces into high-fidelity electrical responses1,2,3. When mechanoreceptors are stimulated, mechanically sensitive cation channels open and produce an inward transduction current that depolarizes the cell. For this process to operate effectively, the transduction machinery has to retain integrity and remain unfailingly independent of environmental changes. This is particularly challenging for poikilothermic organisms, where changes in temperature in the environment may impact the function of mechanoreceptor neurons. Thus, we wondered how insects whose habitat might quickly vary over several tens of degrees of temperature manage to maintain highly effective mechanical senses. We screened for Drosophila mutants with defective mechanical responses at elevated ambient temperatures, and identified a gene, spam, whose role is to protect the mechanosensory organ from massive cellular deformation caused by heat-induced osmotic imbalance. Here we show that Spam protein forms an extracellular shield that guards mechanosensory neurons from environmental insult. Remarkably, heterologously expressed Spam protein also endowed other cells with superb defence against physically and chemically induced deformation. We studied the mechanical impact of Spam coating and show that spam-coated cells are up to ten times stiffer than uncoated controls. Together, these results help explain how poikilothermic organisms preserve the architecture of critical cells during environmental stress, and illustrate an elegant and simple solution to such challenge.

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Figure 1: Effect of heat exposure on the function of mechanoreceptor cells.
Figure 2: Mechanoreceptors of spam mutants undergo dramatic cellular deformation.
Figure 3: Spam coating prevents cell deformation induced by osmotic or chemical manipulation.
Figure 4: Mechanical impact of Spam coating.

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Acknowledgements

We particularly thank E. L. Elson for his help and hospitality in the cell poking studies. We are also indebted to A. Zelhof for advice, materials and reagents, and T. Avidor-Reiss for his help with the immunolocalization of Spam. We thank T. Meerloo for help with immunogold labelling, and A. Becker for help with tissue culture and transfections. We thank N. Ryba, A. Kiger and members of the Zuker laboratory for comments. C.S.Z. is an investigator of the Howard Hughes Medical Institute.

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Correspondence to Charles S. Zuker.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-6 with Legends and Supplementary Methods. (PDF 822 kb)

Supplementary Video 1

The file contains Supplementary Video 1 showing control cn bw flies at 21°C. (MOV 4600 kb)

Supplementary Video 2

The file contains Supplementary Video 2 showing control cn bw flies after 30 min. at 37°C. (MOV 4450 kb)

Supplementary Video 3

The file contains Supplementary Video 3 showing spam flies at 21°C. (MOV 4808 kb)

Supplementary Video 4

The file contains Supplementary Video 4 showing spam flies after 30 min. at 37°C. (MOV 4499 kb)

Supplementary Video 5

The file contains Supplementary Video 5 showing spam homozygous mutant flies expressing a transgenic Spam rescue construct (see methods), after 30 min. at 37°C. (MOV 4758 kb)

Supplementary Video 6

The file contains Supplementary Video 6 showing spam flies in a dish exposed to >90% RH, after 30 min. at 37°C. (MOV 3858 kb)

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Cook, B., Hardy, R., McConnaughey, W. et al. Preserving cell shape under environmental stress. Nature 452, 361–364 (2008). https://doi.org/10.1038/nature06603

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