Transmembrane protein sorting driven by membrane curvature

Abstract

The intricate structure of prokaryotic and eukaryotic cells depends on the ability to target proteins to specific cellular locations. In most cases, we have a poor understanding of the underlying mechanisms. A typical example is the assembly of bacterial chemoreceptors at cell poles. Here we show that the classical chemoreceptor TlpA of Bacillus subtilis does not localize according to the consensus stochastic nucleation mechanism but accumulates at strongly curved membrane areas generated during cell division. This preference was confirmed by accumulation at non-septal curved membranes. Localization appears to be an intrinsic property of the protein complex and does not rely on chemoreceptor clustering, as was previously shown for Escherichia coli. By constructing specific amino-acid substitutions, we demonstrate that the preference for strongly curved membranes arises from the curved shape of chemoreceptor trimer of dimers. These findings demonstrate that the intrinsic shape of transmembrane proteins can determine their cellular localization.

Origins of chemoreceptor curvature sorting in Escherichia coli

“…Recent work in B. subtilis with the chemoreceptor TlpA, which also forms ToDs, suggested that curvature sensitivity arises from rigidity within the ToD cone shape holding the transmembrane domains apart and at an angle in the membrane23. The researchers reported that curvature sensitivity was eliminated by the introduction of two glycine residues within the receptor HAMP domain, increasing receptor flexibility.…”

“…This ToD geometry led Endres22 to propose a curvature-based mechanism for polar localization of the array. Recent work in Bacillus subtilis supported this notion, concluding that TlpA, which is homologous to E. coli chemoreceptors, is sorted by membrane curvature23.…”

Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

“…Furthermore, although the AtKEA2 protein without the N-terminal domain constitutes an active antiporter (Aranda-Sicilia et al, 2012), it fails to complement the growth defects of the double mutant plant, suggesting that the specific localization of the protein is crucial for its function. The association of oligomers of AtKEA2 could depend on membrane tension or curvature, which is highest at the poles but more relaxed at the midcell, as in bacteria (Laloux and Jacobs-Wagner, 2014;Strahl et al, 2015).…”

Dash-and-Recruit Mechanism Drives Membrane Curvature Recognition by the Small Bacterial Protein SpoVM

“…During cell division, the region at which the division septum meets the lateral edge can display high two-dimensional concave curvature. Several reports have identified concave membrane curvature as a beacon that recruits certain shape-sensing proteins to reside preferentially at the poles, division septum, or along the lateral surface (Govindarajan et al, 2013; Lenarcic et al, 2009; Ramamurthi and Losick, 2009; Renner et al, 2013; Strahl et al, 2015; Ursell et al, 2014). …”