Organellar mechanosensitive channels in fission yeast regulate the hypo-osmotic shock response

Abstract

A key molecule of sensing machineries essential for survival upon hypo-osmotic shock is the mechanosensitive channel. The bacterial mechanosensitive channel mscs functions directly for this purpose by releasing cytoplasmic solutes out of the cell, whereas plant mscs homologues are found to function in chloroplast organization. Here we show that the fission yeast mscs homologues, designated msy1 and msy2, participate in the hypo-osmotic shock response by a mechanism different from that operated by the bacterial mscs. upon hypoosmotic shock, msy2 -and msy1 -msy2 -cells display greater cell swelling than wild-type cells and undergo cell death. Cell swelling precedes an intracellular Ca 2 + increase, which was greater in msy1 -and msy1 -msy2 -cells than in wild-type cells. Fluorescent microscopy showed that msy1 and msy2 localize mainly to the endoplasmic reticulum. These observations suggest that organellar msy1 and msy2 regulate intracellular Ca 2 + and cell volume for survival upon hypo-osmotic shock.

Arabidopsis MSL10 Has a Regulated Cell Death Signaling Activity That Is Separable from Its Mechanosensitive Ion Channel Activity

“…E. coli MscS is among the smallest members of its eponymous family of proteins, and deletion studies indicate that it contains little nonessential protein sequence (Miller et al, 2003b;Schumann et al, 2004). However, other MscS family members show substantial variation in size and topology, containing anywhere from 3 to 12 TM helices ) and a variety of domains not found in MscS, such as large cytoplasmic loops, N-or C-terminal extensions, extracellular domains, and ion or cyclic nucleotide binding motifs (Li et al, 2002(Li et al, , 2007Haswell et al, 2011;Malcolm and Maurer, 2012;Nakayama et al, 2012;Wilson et al, 2013).…”

“…Homologs of MscS are found in nearly all bacterial species (Pivetti et al, 2003;Lai et al, 2013;Martinac et al, 2013), protozoa (Prole and Taylor, 2013), archaea (Palmieri et al, 2009), some fungi (Nakayama et al, 2012), and all plant genomes so far analyzed (Wilson et al, 2013) but have not been identified in animals. The region of sequence similarity between MscS and other members of the MscS superfamily is restricted to a relatively small portion of the protein that includes the pore-lining helix of MscS and ;100 amino acids of the upper cytoplasmic domain (Kloda and Martinac, 2002;Pivetti et al, 2003;Balleza and Gómez-Lagunas, 2009;Haswell et al, 2011).…”

“…A particularly well-studied molecular mechanism for the perception and transduction of mechanical signals is provided by mechanosensitive (MS) ion channels, channels that open directly or indirectly in response to membrane tension (Arnadóttir and Chalfie, 2010;Kung et al, 2010;Sukharev and Sachs, 2012). Genes that are predicted to encode MS channels are found in all three domains of life, in a number of evolutionarily unrelated families Nakayama et al, 2012;Sukharev and Sachs, 2012;Prole and Taylor, 2013).…”

“…Much is unknown about the perception of stimuli that are mechanical in nature, such as touch, gravity, and membrane stretch (i.e., mechanotransduction), though it is clear that these types of signals are important regulators of growth and development in bacteria, plants, and animals (Nakayama et al, 2012;Steffens et al, 2012;Lai et al, 2013;Mousavi et al, 2013;Yan et al, 2013). A particularly well-studied molecular mechanism for the perception and transduction of mechanical signals is provided by mechanosensitive (MS) ion channels, channels that open directly or indirectly in response to membrane tension (Arnadóttir and Chalfie, 2010;Kung et al, 2010;Sukharev and Sachs, 2012).…”

“…MscS-Like 2 (MSL2) and MSL3 from Arabidopsis thaliana and MSC1 from the alga Chlamydomonas reinhardtii are localized to the plastid or chloroplast envelope, where they may provide a conduit for ions in response to osmotic imbalance between the stroma and the cytoplasm (Haswell and Meyerowitz, 2006;Nakayama et al, 2007;Veley et al, 2012). Msy1 and Msy2 from the fission yeast Schizosaccharomyces pombe are localized to the endoplasmic reticulum (ER), where they regulate cytosolic Ca 2+ accumulation, also in response to osmotic shock (Nakayama et al, 2012). The function of plasma membrane (PM)-localized MSLs remains under investigation.…”