Light-sensing via hydrogen peroxide and a peroxiredoxin.
Yeast lacks dedicated photoreceptors; however, blue light still causes pronounced oscillations of the transcription factor Msn2 into and out of the nucleus. Here we show that this poorly understood phenomenon is initiated by a peroxisomal oxidase, which converts light into a hydrogen peroxide (H2O2) signal that is sensed by the peroxiredoxin Tsa1 and transduced to thioredoxin, to counteract PKA-dependent Msn2 phosphorylation. Upon H2O2, the nuclear retention of PKA catalytic subunits, which contributes to delayed Msn2 nuclear concentration, is antagonized in a Tsa1-dependent manner. Conversely, peroxiredoxin hyperoxidation interrupts the H2O2signal and drives Msn2 oscillations by superimposing on PKA feedback regulation. Our data identify a mechanism by which light could be sensed in all cells lacking dedicated photoreceptors. In particular, the use of H2O2as a second messenger in signalling is common to Msn2 oscillations and to light-induced entrainment of circadian rhythms and suggests conserved roles for peroxiredoxins in endogenous rhythms.
Department of Chemistry and Molecular Biology, University of Gothenburg, Box 462, S-413 90 Göteborg, Sweden.|Department of Physics, Chalmers University of Technology, S-412 96 Göteborg, Sweden.
Kristofer
K
Bodvard
Department of Chemistry and Molecular Biology, University of Gothenburg, Box 462, S-413 90 Göteborg, Sweden.
Ken
K
Peeters
Department of Chemistry and Molecular Biology, University of Gothenburg, Box 462, S-413 90 Göteborg, Sweden.
Friederike
F
Roger
Mass Spectrometry Facility, Max F. Perutz Laboratories, University of Vienna, Dr Bohrgasse 9, A-1030 Vienna, Austria.
Natalie
N
Romanov
Oxidative Stress and Cancer, SBIGEM, iBiTec-S, FRE3377 CEA-CNRS-Université Paris-Sud, CEA-Saclay, bat 142 F-91191 Gif Sur Yvette, France.
Aeid
A
Igbaria
Department of Chemistry and Molecular Biology, University of Gothenburg, Box 462, S-413 90 Göteborg, Sweden.|Hohmann Lab, Department of Biology and Biological Engineering, Chalmers University of Technology, S-412 96 Göteborg, Sweden.
Niek
N
Welkenhuysen
Oxidative Stress and Cancer, SBIGEM, iBiTec-S, FRE3377 CEA-CNRS-Université Paris-Sud, CEA-Saclay, bat 142 F-91191 Gif Sur Yvette, France.
Gaël
G
Palais
Department of Biochemistry, Max F. Perutz Laboratories, University of Vienna, Dr Bohrgasse 9, A-1030 Vienna, Austria.
Wolfgang
W
Reiter
Oxidative Stress and Cancer, SBIGEM, iBiTec-S, FRE3377 CEA-CNRS-Université Paris-Sud, CEA-Saclay, bat 142 F-91191 Gif Sur Yvette, France.
Michel B
MB
Toledano
Department of Physics, Chalmers University of Technology, S-412 96 Göteborg, Sweden.
Mikael
M
Käll
Department of Chemistry and Molecular Biology, University of Gothenburg, Box 462, S-413 90 Göteborg, Sweden.
Mikael
0000-0002-3903-8503
M
Molin
D055162:Biocatalysis / Q000528:radiation effects; D002467:Cell Nucleus / Q000378:metabolism / Q000528:radiation effects; D017868:Cyclic AMP-Dependent Protein Kinases / Q000378:metabolism; D006861:Hydrogen Peroxide / Q000378:metabolism*; D008027:Light; D055537:Light Signal Transduction / Q000528:radiation effects; D008954:Models, Biological; D010544:Peroxidases / Q000378:metabolism*; D054464:Peroxiredoxins / Q000378:metabolism*; D010766:Phosphorylation / Q000528:radiation effects; D021122:Protein Subunits / Q000378:metabolism; D021381:Protein Transport / Q000528:radiation effects; D012441:Saccharomyces cerevisiae / Q000378:metabolism* / Q000528:radiation effects; D029701:Saccharomyces cerevisiae Proteins / Q000378:metabolism*
D021122:Protein Subunits; D029701:Saccharomyces cerevisiae Proteins; D006861:Hydrogen Peroxide; D010544:Peroxidases; C496253:Tsa1 protein, S cerevisiae; D054464:Peroxiredoxins; D017868:Cyclic AMP-Dependent Protein Kinases