Electrochemical Regulation of Budding Yeast Polarity

PLoS Biology

Volumn 12, Issue 12, 2014, Pages

  Haupt, Armin ^a   Campetelli, Alexis ^a   Bonazzi, Daria ^a   Piel, Matthieu ^b   Chang, Fred ^c   Minc, Nicolas ^a  

^a CNRS   (France)

^b INSTITUT CURIE   (France)

^c Department of Microbiology and Immunology Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; PHOSPHATIDYLSERINE; PROTEIN CDC42; PROTEIN TRK1P; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; LIPID; SACCHAROMYCES CEREVISIAE PROTEIN; TRK1 PROTEIN, S CEREVISIAE;

ARTICLE; CELL BUDDING; CELL POLARITY; CONTROLLED STUDY; ELECTROCHEMISTRY; FUNGAL CELL; GENE IDENTIFICATION; MEMBRANE POTENTIAL; NONHUMAN; OPTOGENETICS; SACCHAROMYCES CEREVISIAE; BIOLOGICAL MODEL; BUDDING YEAST; CYTOLOGY; ELECTRICITY; METABOLISM;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

CATION TRANSPORT PROTEINS; CDC42 GTP-BINDING PROTEIN, SACCHAROMYCES CEREVISIAE; CELL POLARITY; ELECTRICITY; ELECTROCHEMISTRY; LIPIDS; MEMBRANE POTENTIALS; MODELS, BIOLOGICAL; OPTOGENETICS; PHOSPHATIDYLSERINES; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES;

EID: 84924027299     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002029     Document Type: Article

References (76)

1. Drubin DG, Nelson WJ, (1996) Origins of cell polarity. Cell 84: 335–344.
2. Campetelli A, Bonazzi D, Minc N, (2012) Electrochemical regulation of cell polarity and the cytoskeleton. Cytoskeleton (Hoboken) 69: 601–612.
3. Schonichen A, Webb BA, Jacobson MP, Barber DL, (2013) Considering protonation as a posttranslational modification regulating protein structure and function. Annu Rev Biophys 42: 289–314.
4. Simons M, Gault WJ, Gotthardt D, Rohatgi R, Klein TJ, et al. (2009) Electrochemical cues regulate assembly of the Frizzled/Dishevelled complex at the plasma membrane during planar epithelial polarization. Nat Cell Biol 11: 286–294.
5. Magalhaes MA, Larson DR, Mader CC, Bravo-Cordero JJ, Gil-Henn H, et al. (2011) Cortactin phosphorylation regulates cell invasion through a pH-dependent pathway. J Cell Biol 195: 903–920.
6. Levin M, (2009) Bioelectric mechanisms in regeneration: unique aspects and future perspectives. Semin Cell Dev Biol 20: 543–556.
7. Inaba M, Yamanaka H, Kondo S, (2012) Pigment pattern formation by contact-dependent depolarization. Science 335: 677.
8. Chang F, Minc N, (2014) Electrochemical control of cell and tissue polarity. Annu Rev Cell Dev Biol 30: 317–336.
9. Sun Y, Do H, Gao J, Zhao R, Zhao M, et al. (2013) Keratocyte fragments and cells utilize competing pathways to move in opposite directions in an electric field. Curr Biol 23: 569–574.
10. Zhao M, Song B, Pu J, Wada T, Reid B, et al. (2006) Electrical signals control wound healing through phosphatidylinositol-3-OH kinase-gamma and PTEN. Nature 442: 457–460.
11. Song B, Zhao M, Forrester JV, McCaig CD, (2002) Electrical cues regulate the orientation and frequency of cell division and the rate of wound healing in vivo. Proc Natl Acad Sci U S A 99: 13577–13582.
12. Sato MJ, Kuwayama H, van Egmond WN, Takayama AL, Takagi H, et al. (2009) Switching direction in electric-signal-induced cell migration by cyclic guanosine monophosphate and phosphatidylinositol signaling. Proc Natl Acad Sci U S A 106: 6667–6672.
13. Minc N, Chang F, (2010) Electrical control of cell polarization in the fission yeast Schizosaccharomyces pombe. Curr Biol 20: 710–716.
14. Bonazzi D, Minc N, (2014) Dissecting the molecular mechanisms of electrotactic effects. Adv Wound Care (New Rochelle) 3: 139–148.
15. Jaffe LF, Stern CD, (1979) Strong electrical currents leave the primitive streak of chick embryos. Science 206: 569–571.
16. Kropf DL, Caldwell JH, Gow NA, Harold FM, (1984) Transcellular ion currents in the water mold Achlya. Amino acid proton symport as a mechanism of current entry. J Cell Biol 99: 486–496.
17. van West P, Morris BM, Reid B, Appiah AA, Osborne MC, et al. (2002) Oomycete plant pathogens use electric fields to target roots. Mol Plant Microbe Interact 15: 790–798.
18. Lin F, Baldessari F, Gyenge CC, Sato T, Chambers RD, et al. (2008) Lymphocyte electrotaxis in vitro and in vivo. J Immunol 181: 2465–2471.
19. Hotary KB, Robinson KR, (1992) Evidence of a role for endogenous electrical fields in chick embryo development. Development 114: 985–996.
20. Zhao M, (2009) Electrical fields in wound healing—an overriding signal that directs cell migration. Semin Cell Dev Biol 20: 674–682.
21. Drubin DG, (1991) Development of cell polarity in budding yeast. Cell 65: 1093–1096.
22. Chang F, Peter M, (2003) Yeasts make their mark. Nat Cell Biol 5: 294–299.
23. Chant J, Herskowitz I, (1991) Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65: 1203–1212.
24. Martin SG, Arkowitz RA, (2014) Cell polarization in budding and fission yeasts. FEMS Microbiol Rev 38: 228–253.
25. Nern A, Arkowitz RA, (1998) A GTP-exchange factor required for cell orientation. Nature 391: 195–198.
26. Butty AC, Pryciak PM, Huang LS, Herskowitz I, Peter M, (1998) The role of Far1p in linking the heterotrimeric G protein to polarity establishment proteins during yeast mating. Science 282: 1511–1516.
27. Nern A, Arkowitz RA, (1999) A Cdc24p-Far1p-Gbetagamma protein complex required for yeast orientation during mating. J Cell Biol 144: 1187–1202.
28. Evangelista M, Blundell K, Longtine MS, Chow CJ, Adames N, et al. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276: 118–122.
29. Chenevert J, Corrado K, Bender A, Pringle J, Herskowitz I, (1992) A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature 356: 77–79.
30. Brand A, Shanks S, Duncan VM, Yang M, Mackenzie K, et al. (2007) Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 17: 347–352.
31. Brand AC, Morrison E, Milne S, Gonia S, Gale CA, et al. (2014) Cdc42 GTPase dynamics control directional growth responses. Proc Natl Acad Sci U S A 111: 811–816.
32. Ferrigno P, Posas F, Koepp D, Saito H, Silver PA, (1998) Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin beta homologs NMD5 and XPO1. EMBO J 17: 5606–5614.
33. Whiteway M, Hougan L, Thomas DY, (1990) Overexpression of the STE4 gene leads to mating response in haploid Saccharomyces cerevisiae. Mol Cell Biol 10: 217–222.
34. Kozminski KG, Chen AJ, Rodal AA, Drubin DG, (2000) Functions and functional domains of the GTPase Cdc42p. Mol Biol Cell 11: 339–354.
35. Wedlich-Soldner R, Altschuler S, Wu L, Li R, (2003) Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299: 1231–1235.
36. Nern A, Arkowitz RA, (2000) Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J Cell Biol 148: 1115–1122.
37. Butty AC, Perrinjaquet N, Petit A, Jaquenoud M, Segall JE, et al. (2002) A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J 21: 1565–1576.
38. Gross D, Loew LM, Webb WW, (1986) Optical imaging of cell membrane potential changes induced by applied electric fields. Biophys J 50: 339–348.
39. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE, (2011) Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333: 345–348.
40. Allen GM, Mogilner A, Theriot JA, (2013) Electrophoresis of cellular membrane components creates the directional cue guiding keratocyte galvanotaxis. Curr Biol 23: 560–568.
41. Jaffe LF, (1977) Electrophoresis along cell membranes. Nature 265: 600–602.
42. Madrid R, Gomez MJ, Ramos J, Rodriguez-Navarro A, (1998) Ectopic potassium uptake in trk1 trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential. J Biol Chem 273: 14838–14844.
43. Gaber RF, Styles CA, Fink GR, (1988) TRK1 encodes a plasma membrane protein required for high-affinity potassium transport in Saccharomyces cerevisiae. Mol Cell Biol 8: 2848–2859.
44. Calero F, Gomez N, Arino J, Ramos J, (2000) Trk1 and Trk2 define the major K(+) transport system in fission yeast. J Bacteriol 182: 394–399.
45. Perez-Valle J, Jenkins H, Merchan S, Montiel V, Ramos J, et al. (2007) Key role for intracellular K+ and protein kinases Sat4/Hal4 and Hal5 in the plasma membrane stabilization of yeast nutrient transporters. Mol Cell Biol 27: 5725–5736.
46. Eldakak A, Rancati G, Rubinstein B, Paul P, Conaway V, et al. (2010) Asymmetrically inherited multidrug resistance transporters are recessive determinants in cellular replicative ageing. Nat Cell Biol 12: 799–805.
47. Adams DS, Tseng AS, Levin M, (2013) Light-activation of the Archaerhodopsin H(+)-pump reverses age-dependent loss of vertebrate regeneration: sparking system-level controls in vivo. Biol Open 2: 306–313.
48. Zhang F, Vierock J, Yizhar O, Fenno LE, Tsunoda S, et al. (2011) The microbial opsin family of optogenetic tools. Cell 147: 1446–1457.
49. Hildebrandt V, Fendler K, Heberle J, Hoffmann A, Bamberg E, et al. (1993) Bacteriorhodopsin expressed in Schizosaccharomyces pombe pumps protons through the plasma membrane. Proc Natl Acad Sci U S A 90: 3578–3582.
50. Lang-Hinrichs C, Queck I, Buldt G, Stahl U, Hildebrandt V, (1994) The archaebacterial membrane protein bacterio-opsin is expressed and N-terminally processed in the yeast Saccharomyces cerevisiae. Mol Gen Genet 244: 183–188.
51. Arrenberg AB, Del Bene F, Baier H, (2009) Optical control of zebrafish behavior with halorhodopsin. Proc Natl Acad Sci U S A 106: 17968–17973.
52. Strickland D, Lin Y, Wagner E, Hope CM, Zayner J, et al. (2012) TULIPs: tunable, light-controlled interacting protein tags for cell biology. Nat Methods 9: 379–384.
53. Ko CH, Liang H, Gaber RF, (1993) Roles of multiple glucose transporters in Saccharomyces cerevisiae. Mol Cell Biol 13: 638–648.
54. Kono K, Saeki Y, Yoshida S, Tanaka K, Pellman D, (2012) Proteasomal degradation resolves competition between cell polarization and cellular wound healing. Cell 150: 151–164.
55. McNamee MG, McConnell HM, (1973) Transmembrane potentials and phospholipid flip-flop in excitable membrane vesicles. Biochemistry 12: 2951–2958.
56. McLaughlin S, Harary H, (1974) Phospholipid flip-flop and the distribution of surface charges in excitable membranes. Biophys J 14: 200–208.
57. Hall JE, (1981) Voltage-dependent lipid flip-flop induced by alamethicin. Biophys J 33: 373–381.
58. Fairn GD, Hermansson M, Somerharju P, Grinstein S, (2011) Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat Cell Biol 13: 1424–1430.
59. Das A, Slaughter BD, Unruh JR, Bradford WD, Alexander R, et al. (2012) Flippase-mediated phospholipid asymmetry promotes fast Cdc42 recycling in dynamic maintenance of cell polarity. Nat Cell Biol 14: 304–310.
60. Yeung T, Gilbert GE, Shi J, Silvius J, Kapus A, et al. (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319: 210–213.
61. Nuccitelli R, Jaffe LF, (1976) The ionic components of the current pulses generated by developing fucoid eggs. Dev Biol 49: 518–531.
62. Robinson KR, Jaffe LF, (1975) Polarizing fucoid eggs drive a calcium current through themselves. Science 187: 70–72.
63. Peng HB, Jaffe LF, (1976) Polarization of fucoid eggs by steady electrical fields. Dev Biol 53: 277–284.
64. Weisenseel MH, Nuccitelli R, Jaffe LF, (1975) Large electrical currents traverse growing pollen tubes. J Cell Biol 66: 556–567.
65. Nuccitelli R, Poo MM, Jaffe LF, (1977) Relations between ameboid movement and membrane-controlled electrical currents. J Gen Physiol 69: 743–763.
66. Gao RC, Zhang XD, Sun YH, Kamimura Y, Mogilner A, et al. (2011) Different roles of membrane potentials in electrotaxis and chemotaxis of dictyostelium cells. Eukaryot Cell 10: 1251–1256.
67. Choi CH, Webb BA, Chimenti MS, Jacobson MP, Barber DL, (2013) pH sensing by FAK-His58 regulates focal adhesion remodeling. J Cell Biol 202: 849–859.
68. Frantz C, Barreiro G, Dominguez L, Chen X, Eddy R, et al. (2008) Cofilin is a pH sensor for actin free barbed end formation: role of phosphoinositide binding. J Cell Biol 183: 865–879.
69. Frantz C, Karydis A, Nalbant P, Hahn KM, Barber DL, (2007) Positive feedback between Cdc42 activity and H+ efflux by the Na-H exchanger NHE1 for polarity of migrating cells. J Cell Biol 179: 403–410.
70. Stewart MP, Helenius J, Toyoda Y, Ramanathan SP, Muller DJ, et al. (2011) Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469: 226–230.
71. Hughes AL, Gottschling DE, (2012) An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492: 261–265.
72. Pai VP, Aw S, Shomrat T, Lemire JM, Levin M, (2012) Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development 139: 313–323.
73. Denker SP, Barber DL, (2002) Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. J Cell Biol 159: 1087–1096.
74. Follette PJ, Arkowitz RA, (2009) Chemotropism during yeast mating. Methods Mol Biol 571: 99–110.
75. Charvin G, Cross FR, Siggia ED, (2008) A microfluidic device for temporally controlled gene expression and long-term fluorescent imaging in unperturbed dividing yeast cells. PLoS ONE 3: e1468.
76. Cole KS (1969) Membranes, ions and impulses. Berkeley: University of California Press.