Genetic and cellular characterization of MscS-like putative channels in the filamentous fungus Aspergillus nidulans

References

• Naismith JH, Booth IR. bacterial mechanosensitive channels—MSCs: evolution’s solution to creating sensitivity in function. Annu Rev Biophys. 2012;41:157–177.
   PubMed Web of Science ®Google Scholar
• Kung C, Martinac B, Sukharev S. Mechanosensitive Channels in Microbes. Annu Rev Microbiol. 2010;64:313–329.
   PubMed Web of Science ®Google Scholar
• Kefauver JM, Ward AB, Patapoutian A. Discoveries in structure and physiology of mechanically activated ion channels. Nature. 2020;587:567–576.
   PubMed Web of Science ®Google Scholar
• Haswell ES, Phillips R, Rees DC. Mechanosensitive channels: what can they do and how do they do it? Structure. 2011;19:1356–1369.
   PubMed Web of Science ®Google Scholar
• Martinac B, Buechner M, Delcour AH, et al. Pressure-sensitive ion channel in Escherichia coli. Proceedings of the National Academy of Sciences. 1987;84:2297–2301.
   Google Scholar
• Wang Q, Chang A. Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1. Proceedings of the National Academy of Sciences [Internet]. 2002;99:12853–12858. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.202115499.
   Google Scholar
• Kapsalis C, Wang B, El Mkami H, et al. Allosteric activation of an ion channel triggered by modification of mechanosensitive nano-pockets. Nat Commun. 2019;10:4619.
   PubMed Web of Science ®Google Scholar
• Chang G, Spencer RH, Lee AT, et al. Structure of the MscL homolog from mycobacterium tuberculosis : a gated mechanosensitive ion channel. Science. 1998;282:2220–2226.
   PubMed Web of Science ®Google Scholar
• Pliotas C, Dahl ACE, Rasmussen T, et al. The role of lipids in mechanosensation. Nat Struct Mol Biol. 2015;22:991–998.
   PubMed Web of Science ®Google Scholar
• Ward R, Pliotas C, Branigan E, et al. Probing the structure of the mechanosensitive channel of small conductance in lipid bilayers with pulsed electron-electron double resonance. Biophys J. 2014;106:834–842.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Daday C, R-x G, et al. Visualization of the mechanosensitive ion channel MscS under membrane tension. Nature. 2021;590:509–514.
   PubMed Web of Science ®Google Scholar
• Pliotas C, Ward R, Branigan E, et al. Conformational state of the MscS mechanosensitive channel in solution revealed by pulsed electron–electron double resonance (PELDOR) spectroscopy. Proceedings of the National Academy of Sciences. 2012;109.
   Google Scholar
• Bass RB, Strop P, Barclay M, et al. Crystal Structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science. 2002;298:1582–1587.
   PubMed Web of Science ®Google Scholar
• Wang W, Black SS, Edwards MD, et al. The Structure of an Open Form of an E. coli Mechanosensitive Channel at 3.45 Å Resolution. Science. 2008;321:1179–1183.
   PubMed Web of Science ®Google Scholar
• Rasmussen T, Flegler VJ, Rasmussen A, et al. Structure of the mechanosensitive channel MSCs embedded in the membrane bilayer. J Mol Biol. 2019;431:3081–3090.
   PubMed Web of Science ®Google Scholar
• Edwards MD, Black S, Rasmussen T, et al. Characterization of three novel mechanosensitive channel activities in Escherichia coli. Channels. 2012;6:272–281.
   PubMed Web of Science ®Google Scholar
• Levina N. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J. 1999;18:1730–1737.
   PubMed Web of Science ®Google Scholar
• Sukharev SI, Blount P, Martinac B, et al. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 1994;368:265–268.
   PubMed Web of Science ®Google Scholar
• Li Y. Ionic regulation of MscK, a mechanosensitive channel from Escherichia coli. EMBO J. 2002;21:5323–5330.
   PubMed Web of Science ®Google Scholar
• Schumann U, Edwards MD, Rasmussen T, et al. YbdG in Escherichia coli is a threshold-setting mechanosensitive channel with MscM activity. Proceedings of the National Academy of Sciences. 2010;107:12664–12669.
   Google Scholar
• Flegler VJ, Rasmussen A, Rao S, et al. The MscS-like channel YnaI has a gating mechanism based on flexible pore helices. Proceedings of the National Academy of Sciences. 2020;117:28754–28762.
   Google Scholar
• Prole DL, Taylor CW. Identification and Analysis of putative homologues of mechanosensitive channels in pathogenic protozoa. PLoS ONE. 2013;8:e66068.
   PubMed Web of Science ®Google Scholar
• Johnson SC, Veres J, Malcolm HR. Exploring the diversity of mechanosensitive channels in bacterial genomes. Eur Biophys J. 2021;50:25–36.
   PubMed Web of Science ®Google Scholar
• Basu D, Codjoe JM, Veley KM, et al. The mechanosensitive ion channel msl10 modulates susceptibility to pseudomonas syringae in Arabidopsis thaliana. Molecular Plant-Microbe Interactions®. 2022. DOI:10.1094/MPMI-08-21-0207-FI
   PubMed Web of Science ®Google Scholar
• Tan M-W, Rahme LG, Sternberg JA, et al. Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proceedings of the National Academy of Sciences. 1999;96:2408–2413.
   Google Scholar
• Deng Z, Maksaev G, Schlegel AM, et al. Structural mechanism for gating of a eukaryotic mechanosensitive channel of small conductance. Nat Commun. 2020;11:3690.
   PubMed Web of Science ®Google Scholar
• Peyronnet R, Haswell ES, Barbier-Brygoo H, et al. AtMSL9 and AtMSL10: sensors of plasma membrane tension in Arabidopsis roots. Plant Signal Behav. 2008;3:726–729.
   PubMedGoogle Scholar
• Jojoa-Cruz S, Saotome K, Tsui CCA, et al. Structural insights into the Venus flytrap mechanosensitive ion channel Flycatcher1. Nat Commun. 2022;13:850.
   PubMed Web of Science ®Google Scholar
• Procko C, Murthy S, Keenan WT, et al. Stretch-activated ion channels identified in the touch-sensitive structures of carnivorous Droseraceae plants. Elife. 2021;10. DOI:10.7554/eLife.64250
   PubMed Web of Science ®Google Scholar
• Takahashi K, Takahashi H, Furuichi T, et al. Gravity sensing in plant and animal cells. Npj Microgravity. 2021;7:2.
   PubMed Web of Science ®Google Scholar
• Pliotas C, Naismith JH. Spectator no more, the role of the membrane in regulating ion channel function. Curr Opin Struct Biol. 2017;45:59–66.
   PubMed Web of Science ®Google Scholar
• Flegler VJ, Rasmussen A, Borbil K, et al. Mechanosensitive channel gating by delipidation. Proceedings of the National Academy of Sciences. 2021;118.
   Google Scholar
• Wang B, Lane BJ, Kapsalis C, et al. Pocket delipidation induced by membrane tension or modification leads to a structurally analogous mechanosensitive channel state. Structure. 2022;30:608–622.e5.
   PubMed Web of Science ®Google Scholar
• Kapsalis C, Ma Y, Bode BE, et al. In-lipid structure of pressure-sensitive domains hints mechanosensitive channel functional diversity. Biophys J. 2020;119:448–459.
   PubMed Web of Science ®Google Scholar
• Michou M, Kapsalis C, Pliotas C, et al. Optimization of recombinant membrane protein production in the engineered Escherichia coli strains suptoxd and suptoxR. ACS Synth Biol. 2019;8:1631–1641.
   PubMed Web of Science ®Google Scholar
• Pliotas C. Ion channel conformation and oligomerization assessment by site-directed spin labeling and pulsed-EPR. 2017. p. 203–242.
   Google Scholar
• Reddy B, Bavi N, Lu A, et al. Molecular basis of force-from-lipids gating in the mechanosensitive channel MscS. Elife. 2019;8:e50486.
   PubMed Web of Science ®Google Scholar
• Teng J, Loukin S, Anishkin A, et al. The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements. Pflügers Archiv - European Journal of Physiology. 2015;467:27–37.
   PubMed Web of Science ®Google Scholar
• Wray R, Iscla I, Kovacs Z, et al. Novel compounds that specifically bind and modulate MscL: insights into channel gating mechanisms. FASEB J. 2019;33:3180–3189.
   PubMed Web of Science ®Google Scholar
• Nakayama Y, Yoshimura K, Iida H. Organellar mechanosensitive channels in fission yeast regulate the hypo-osmotic shock response. Nat Commun. 2012;3:1020.
   PubMed Web of Science ®Google Scholar
• Nakayama Y, Iida H. Organellar mechanosensitive channels involved in hypo-osmoregulation in fission yeast. Cell Calcium. 2014;56:467–471.
   PubMed Web of Science ®Google Scholar
• Varadi M, Anyango S, Deshpande M, et al. AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50:D439–D444.
   PubMed Web of Science ®Google Scholar
• Jumper J, Evans R, Pritzel A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–589.
   PubMed Web of Science ®Google Scholar
• Punt PJ, Dingemanse MA, Kuyvenhoven A, et al. Functional elements in the promoter region of the Aspergillus nidulans gpdA gene encoding glyceraldehyde-3-phosphate dehydrogenase. Gene [Internet]. 1990;93:101–109. Available from.;.
   PubMed Web of Science ®Google Scholar
• Nayak T, Szewczyk E, Oakley CE, et al. A Versatile and Efficient Gene-Targeting System for Aspergillus nidulans. Genetics [Internet]. 2006;172:1557–1566. Available from.
   PubMed Web of Science ®Google Scholar
• Krypotou E, Evangelidis T, Bobonis J, et al. Origin, diversification and substrate specificity in the family of NCS1/FUR transporters. Mol Microbiol. 2015;96:927–950. https://onlinelibrary.wiley.com/doi/10.1111/mmi.12982
   PubMed Web of Science ®Google Scholar
• Martzoukou O, Diallinas G, Amillis S. Secretory vesicle polar sorting, endosome recycling and cytoskeleton organization require the AP-1 Complex in Aspergillus nidulans. Genetics. 2018;209:209.
   PubMed Web of Science ®Google Scholar
• Dereeper A, Guignon V, Blanc G, et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008;36:W465–W469.
   PubMed Web of Science ®Google Scholar
• Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988;16:10881–10890.
   PubMed Web of Science ®Google Scholar
• Pettersen EF, Goddard TD, Huang CC, et al. UCSF Chimera?A visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–1612.
   PubMed Web of Science ®Google Scholar
• Lee CP, Maksaev G, Jensen GS, et al. MSL1 is a mechanosensitive ion channel that dissipates mitochondrial membrane potential and maintains redox homeostasis in mitochondria during abiotic stress. Plant J. 2016;88:809–825.
   PubMed Web of Science ®Google Scholar