Hydrogen Sulfide Regulates the Cytosolic/Nuclear Partitioning of Glyceraldehyde-3-Phosphate Dehydrogenase by Enhancing its Nuclear Localization

Aroca, Ángeles; Schneider, Markus; Scheibe, Renate; Gotor, Cecilia; Romero, Luís C.

doi:10.1093/pcp/pcx056

Cited by 80 publications

(71 citation statements)

References 49 publications

(48 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…(Krishnan et al, 2011) and S-nitrosylation activates CYCLIN-DEPENDENT PROTEIN KINASE5 (Qu et al, 2011). Recent evidence indicates that S-sulfhydration by endogenous H 2 S regulates the functions of certain proteins, such as ASCORBATE PEROXIDASE1 and GLYCERALDEHYDE 3-PHOSPHATE DEHYDRO-GENASE (Aroca et al, 2015(Aroca et al, , 2017b.…”

Section: CMmentioning

confidence: 99%

Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth

Chen

Wang

et al. 2018

Plant Physiol.

View full text Add to dashboard Cite

Hydrogen sulfide (HS) is an important signaling molecule in plants. Our previous report suggested that HS signaling affects the actin cytoskeleton and root hair growth. However, the underlying mechanisms of its effects are not understood. -Sulfhydration of proteins is regulated directly by HS, which converts the thiol groups of cysteine (Cys) residues to persulfides and alters protein function. In this work, we studied the effects of -sulfhydration on actin dynamics in Arabidopsis (). We generated transgenic plants overexpressing the HS biosynthesis-related genes () and in the () mutant and Columbia-0 backgrounds. The HS content increased significantly in overexpressing / plants. The density of filamentous actin (F-actin) bundles and the F-actin/globular actin ratio decreased in overexpressing / plants. -Sulfhydration also was enhanced in overexpressing/ plants. An analysis of actin dynamics suggested that -sulfhydration inhibited actin polymerization. We also found that ACTIN2 (ACT2) was-sulfhydrated at Cys-287. Cys-287 is adjacent to the D-loop, which acts as a central region for hydrophobic and electrostatic interactions and stabilizes F-actin filaments. Overaccumulation of HS caused the depolymerization of F-actin bundles and inhibited root hair growth. Introduction of carrying a Cys-287-to-Ser mutation into an mutant partially suppressed HS-dependent inhibition of root hair growth. We conclude that HS regulates actin dynamics and affects root hair growth.

show abstract

Section: CMmentioning

confidence: 99%

Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth

Chen

Wang

et al. 2018

Plant Physiol.

View full text Add to dashboard Cite

show abstract

“…Several of the enzymes of the glycolytic pathway are redox regulated and are more active in their reduced form, such as glyceraldehyde 3-phosphate dehydrogenase (Holtgrefe et al, 2008). However, posttranslational modification of the cytosolic GAPDH GapC isoform by S-persulfidation of Cys-160 slightly regulates its activity but is critical to determine the cytosolic/ nuclear partitioning of the enzyme (Aroca et al, 2015(Aroca et al, , 2017b. In addition to its enolase activity, the LOS2/ENO2 locus can be alternatively translated from a second AUG translation initiation codon at position +93 to form the protein MBP1, which was found to bind c-myc-like elements in the promoter of the STZ/ZAT10 gene acting as a transcriptional repressor (Lee et al, 2002).…”

Section: Role Of S-cyanylation In Cellular Processesmentioning

confidence: 99%

“…The reaction of cyanide with cystine-containing proteins results in the formation of an S-cyanylated Cys motif that cycles and is subsequently cleaved to release an amino terminal peptide at one end and a 2-imino-thiazolidine-4-carboxylyl COOH-terminal peptide at the other (Catsimpoolas and Wood, 1966;Fasco et al, 2007). The reaction of cyanide ions with disulfide bridges within polypeptides has been considered to be similar to that of other small molecules, such as nitric oxide (NO) or H 2 S, that react with Cys residues to produce Cys modifications (Yamasaki et al, 2016;Aroca et al, 2017bAroca et al, , 2018.…”

mentioning

confidence: 99%

HCN Regulates Cellular Processes through Posttranslational Modification of Proteins by S-cyanylation

et al. 2018

Self Cite

View full text Add to dashboard Cite

Hydrogen cyanide (HCN) is coproduced with ethylene in plant cells and is primarily enzymatically detoxified by the mitochondrial b-CYANOALANINE SYNTHASE (CAS-C1). Permanent or transient depletion of CAS-C1 activity in Arabidopsis (Arabidopsis thaliana) results in physiological alterations in the plant that suggest that HCN acts as a gasotransmitter molecule. Label-free quantitative proteomic analysis of mitochondrially enriched samples isolated from the wild type and cas-c1 mutant revealed significant changes in protein content, identifying 451 proteins that are absent or less abundant in cas-c1 and 353 proteins that are only present or more abundant in cas-c1. Gene ontology classification of these proteins identified proteomic changes that explain the root hairless phenotype and the altered immune response observed in the cas-c1 mutant. The mechanism of action of cyanide as a signaling molecule was addressed using two proteomic approaches aimed at identifying the S-cyanylation of Cys as a posttranslational modification of proteins. Both the 2-imino-thiazolidine chemical method and the direct untargeted analysis of proteins using liquid chromatography-tandem mass spectrometry identified a set of 163 proteins susceptible to S-cyanylation that included SEDOHEPTULOSE 1,7-BISPHOSPHATASE (SBPase), the PEPTIDYL-PROLYL CIS-TRANS ISOMERASE 20-3 (CYP20-3), and ENOLASE2 (ENO2). In vitro analysis of these enzymes showed that S-cyanylation of SBPase Cys 74 , CYP20-3 Cys 259 , and ENO2 Cys 346 residues affected their enzymatic activity. Gene Ontology classification and protein-protein interaction cluster analysis showed that S-cyanylation is involved in the regulation of primary metabolic pathways, such as glycolysis, and the Calvin and S-adenosyl-Met cycles.

show abstract

“…Moreover, a fraction of GapC was shown to be localized to the nucleus of Arabidopsis mesophyll protoplasts [ 7 , 9 – 11 ], and associated with the outer mitochondrial membrane (OMM) and the cytoskeleton [ 9 ]. S-sulfhydrylation of GapC has been observed to also result in nuclear localization of the modified protein [ 12 ].…”

Section: Introductionmentioning

confidence: 99%

Cytosolic GAPDH as a redox-dependent regulator of energy metabolism

et al. 2018

Self Cite

View full text Add to dashboard Cite

BackgroundPlant cytosolic NAD-dependent glyceraldehyde-3-phosphate dehydrogenase (GapC) displays redox-dependent changes in its subcellular localizations and activity. Apart from its fundamental role in glycolysis, it also exhibits moonlighting properties. Since the exceptional redox-sensitivity of GapC has been suggested to play a crucial role in its various functions, we here studied its redox-dependent subcellular localization and the influence of the redox-state on GapC protein interactions.ResultsIn mesophyll protoplasts from Arabidopsis thaliana, colocalization of GapC with mitochondria was more pronounced under reducing conditions than upon oxidative stress. In accordance, reduced GapC showed an increased affinity to the mitochondrial voltage-dependent anion-selective channel (VDAC) compared to the oxidized one. On the other hand, nuclear localization of GapC was increased under oxidizing conditions. The essential role of the catalytic cysteine for nuclear translocation was shown by using the corresponding cysteine mutants. Furthermore, interaction of GapC with the thioredoxin Trx-h3 as a candidate to revert the redox-modifications, occurred in the nucleus of oxidized protoplasts. In a yeast complementation assay, we could demonstrate that the plant-specific non-phosphorylating glyceraldehyde 3-P dehydrogenase (GapN) can substitute for glucose 6-P dehydrogenase to generate NADPH for re-reduction of the Trx system and ROS defense.ConclusionsThe preferred association of reduced, glycolytically active GapC with VDAC suggests a substrate-channeling metabolon at the mitochondrial surface for efficient energy generation. Increased occurrence of oxidized GapC in the nucleus points to a function in signal transduction and gene expression. Furthermore, the interaction of GapC with Trx-h3 in the nucleus indicates reversal of the oxidative cysteine modification after re-establishment of cellular homeostasis. Both, energy metabolism and signal transfer for long-term adjustment and protection from redox-imbalances are mediated by the various functions of GapC. The molecular properties of GapC as a redox-switch are key to its multiple roles in orchestrating energy metabolism.Electronic supplementary materialThe online version of this article (10.1186/s12870-018-1390-6) contains supplementary material, which is available to authorized users.

show abstract

Hydrogen Sulfide Regulates the Cytosolic/Nuclear Partitioning of Glyceraldehyde-3-Phosphate Dehydrogenase by Enhancing its Nuclear Localization

Cited by 80 publications

References 49 publications

Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth

Hydrogen Sulfide Disturbs Actin Polymerization via S-Sulfhydration Resulting in Stunted Root Hair Growth

HCN Regulates Cellular Processes through Posttranslational Modification of Proteins by S-cyanylation

Cytosolic GAPDH as a redox-dependent regulator of energy metabolism

Contact Info

Product

Resources

About