Abstract
Mechanosensitive (MS) ion channels likely underlie myriad force-sensing processes, from basic osmotic regulation to specified sensations of animal hearing and touch. Albeit important, the molecular identities of many eukaryotic MS channels remain elusive, let alone their working mechanisms. This is in stark contrast to our advanced knowledge on voltage- or ligand-sensitive channels. Several members of transient receptor potential (TRP) ion channel family have been implicated to function in mechanosensation and are recognized as promising candidate MS channels. The yeast TRP homolog, TRPY1, is clearly a first-line force transducer. It can be activated by hypertonic shock in vivo and by membrane stretch force in excised patches under patch clamp, making it a useful model for understanding TRP channel mechanosensitivity in general. TRPY1 offers two additional research advantages: (1) It has a large (∼300 pS) unitary conductance and therefore a favorable S/N ratio. (2) Budding yeast allows convenient and efficient genetic and molecular manipulations. In this review, we focus on the current research of TRPY1 and discuss its prospect. We also describe the use of yeast as a system to express and characterize animal TRP channels.
Similar content being viewed by others
References
Bandell M, Dubin AE, Petrus MJ, Orth A, Mathur J, Hwang SW, Patapoutian A (2006) High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat Neurosci 9:493–500
Batiza AF, Schulz T, Masson PH (1996) Yeast respond to hypotonic shock with a calcium pulse. J Biol Chem 271:23357–23362
Bertl A, Slayman CL (1990) Cation-selective channels in the vacuolar membrane of Saccharomyces: dependence on calcium, redox state, and voltage. Proc Natl Acad Sci USA 87:7824–7828
Booth IR, Edwards MD, Black S, Schumann U, Miller S (2007) Mechanosensitive channels in bacteria: signs of closure? Nat Rev Microbiol 5:431–440
Carlile M, Watkinson S, Gooday G (2001) The fungi. Academic, San Diego
Christensen AP, Corey DP (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev 8:510–521
Chung MK, Lee H, Mizuno A, Suzuki M, Caterina MJ (2004) TRPV3 and TRPV4 mediate warmth-evoked currents in primary mouse keratinocytes. J Biol Chem 279:21569–21575
Colbert HA, Smith TL, Bargmann CI (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259–8269
Corry B, Martinac B (2008) Bacterial mechanosensitive channels: experiment and theory. Biochim Biophys Acta 1778:1859–1870
Denis V, Cyert MS (2002) Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156:29–34
Di Palma F, Belyantseva IA, Kim HJ, Vogt TF, Kachar B, Noben-Trauth K (2002) Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice. Proc Natl Acad Sci USA 99:14994–14999
Domene C, Vemparala S, Klein ML, Venien-Bryan C, Doyle DA (2006) Role of aromatic localization in the gating process of a potassium channel. Biophys J 90:L01–L03
Driscoll M, Chalfie M (1991) The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349:588–593
Ernstrom GG, Chalfie M (2002) Genetics of sensory mechanotransduction. Annu Rev Genet 36:411–453
Gao X, Wu L, O'Neil RG (2003) Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278:27129–27137
Gottlieb P, Folgering J, Maroto R, Raso A, Wood TG, Kurosky A, Bowman C, Bichet D, Patel A, Sachs F, Martinac B, Hamill OP, Honore E (2008) Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflugers Arch 455:1097–1103
Grandl J, Hu H, Bandell M, Bursulaya B, Schmidt M, Petrus M, Patapoutian A (2008) Pore region of TRPV3 ion channel is specifically required for heat activation. Nat Neurosci 11:1007–1013
Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22:6408–6414
Gustin MC, Zhou XL, Martinac B, Kung C (1988) A mechanosensitive ion channel in the yeast plasma membrane. Science (New York, NY) 242:762–765
Guthrie C, Fink G (1990) Guide to yeast genetics and molecular and cell biology (Part A). Methods in enzymology 194. Academic, San Diego
Guthrie C, Fink G (2002) Guide to Yeast Genetics and Molecular and Cell Biology (Part B). Methods in Enzymology 350. Academic, San Diego
Hamill OP (2006) Twenty odd years of stretch-sensitive channels. Pflugers Arch 453:333–351
John Haynes W, Zhou XL, Su ZW, Loukin SH, Saimi Y, Kung C (2008) Indole and other aromatic compounds activate the yeast TRPY1 channel. FEBS lett 582:1514–1518
Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, Chakravarti A, Buchwald M, Tsui LC (1989) Identification of the cystic fibrosis gene: genetic analysis. Science (New York, NY) 245:1073–1080
Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84
Kung C (2005) A possible unifying principle for mechanosensation. Nature 436:647–654
Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525–535
Liedtke W, Tobin DM, Bargmann CI, Friedman JM (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc Natl Acad Sci USA 100(Suppl 2):14531–14536
Liu L, Li Y, Wang R, Yin C, Dong Q, Hing H, Kim C, Welsh MJ (2007) Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450:294–298
Loukin SH, Su Z, Kung C (2009) Hypotonic shocks activate rat TRPV4 in yeast in the absence of polyunsaturated fatty acids. FEBS lett 583:754–758
Lumpkin EA, Caterina MJ (2007) Mechanisms of sensory transduction in the skin. Nature 445:858–865
Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP (2005) TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7:179–185
Martinac B (2004) Mechanosensitive ion channels: molecules of mechanotransduction. J Cell Sci 117:2449–2460
Mayer ML (2006) Glutamate receptors at atomic resolution. Nature 440:456–462
Moiseenkova-Bell VY, Stanciu LA, Serysheva II, Tobe BJ, Wensel TG (2008) Structure of TRPV1 channel revealed by electron cryomicroscopy. Proc Natl Acad Sci USA 105:7451–7455
Myers BR, Bohlen CJ, Julius D (2008) A yeast genetic screen reveals a critical role for the pore helix domain in TRP channel gating. Neuron 58:362–373
Myers BR, Saimi Y, Julius D, Kung C (2008) Multiple unbiased prospective screens identify TRP channels and their conserved gating elements. J Gen Physiol 132:481–486
Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129–137
Palmer CP, Zhou XL, Lin J, Loukin SH, Kung C, Saimi Y (2001) A TRP homolog in Saccharomyces cerevisiae forms an intracellular Ca(2+)-permeable channel in the yeast vacuolar membrane. Proc Natl Acad Sci USA 98:7801–7805
Papazian DM, Schwarz TL, Tempel BL, Jan YN, Jan LY (1987) Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science (New York, NY) 237:749–753
Pedersen SF, Nilius B (2007) Transient receptor potential channels in mechanosensing and cell volume regulation. Methods Enzymol 428:183–207
Perozo E (2006) Gating prokaryotic mechanosensitive channels. Nat Rev Mol Cell Biol 7:109–119
Perozo E, Kloda A, Cortes DM, Martinac B (2002) Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat Struct Biol 9:696–703
Saimi Y, Zhou X, Loukin SH, Haynes W, Kung C (2007) Current topics in membranes. Elsevier, New York
Sine SM, Engel AG (2006) Recent advances in Cys-loop receptor structure and function. Nature 440:448–455
Spassova MA, Hewavitharana T, Xu W, Soboloff J, Gill DL (2006) A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci USA 103:16586–16591
Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695–702
Su Z, Zhou X, Haynes WJ, Loukin SH, Anishkin A, Saimi Y, Kung C (2007) Yeast gain-of-function mutations reveal structure-function relationships conserved among different subfamilies of transient receptor potential channels. Proc Natl Acad Sci USA 104:19607–19612
Su Z, Zhou X, Loukin SH, Saimi Y, Kung C (2009) Mechanical force and cytoplasmic Ca(2+) activate yeast TRPY1 in parallel. J Membr Biol 227:141–150
Sukharev S, Anishkin A (2004) Mechanosensitive channels: what can we learn from ‘simple’ model systems? Trends Neurosci 27:345–351
Swartz KJ (2008) Sensing voltage across lipid membranes. Nature 456:891–897
Ulmschneider MB, Sansom MS, Di Nola A (2005) Properties of integral membrane protein structures: derivation of an implicit membrane potential. Proteins 59:252–265
Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, Bodding M, Droogmans G, Nilius B (2002) Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277:33704–33710
Vriens J, Owsianik G, Voets T, Droogmans G, Nilius B (2004) Invertebrate TRP proteins as functional models for mammalian channels. Pflugers Arch 449:213–226
Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci USA 101:396–401
Wada Y, Ohsumi Y, Tanifuji M, Kasai M, Anraku Y (1987) Vacuolar ion channel of the yeast, Saccharomyces cerevisiae. J Biol Chem 262:17260–17263
Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424:434–438
Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B (2002) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277:47044–47051
Zhou X, Su Z, Anishkin A, Haynes WJ, Friske EM, Loukin SH, Kung C, Saimi Y (2007) Yeast screens show aromatic residues at the end of the sixth helix anchor transient receptor potential channel gate. Proc Natl Acad Sci USA 104:15555–15559
Zhou XL, Batiza AF, Loukin SH, Palmer CP, Kung C, Saimi Y (2003) The transient receptor potential channel on the yeast vacuole is mechanosensitive. Proc Natl Acad Sci USA 100:7105–7110
Zhou XL, Vaillant B, Loukin SH, Kung C, Saimi Y (1995) YKC1 encodes the depolarization-activated K+ channel in the plasma membrane of yeast. FEBS lett 373:170–176
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Su, Z., Zhou, X., Loukin, S.H. et al. The use of yeast to understand TRP-channel mechanosensitivity. Pflugers Arch - Eur J Physiol 458, 861–867 (2009). https://doi.org/10.1007/s00424-009-0680-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00424-009-0680-0