Home LiteratureArticle Details
PMID: 15734904 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Proteomic identification of S-nitrosylated proteins in Arabidopsis.

Plant physiology ·Vol. 137 ·No. 3 ·2005-03-00 ·Pages 921-30

Lindermayr C, Saalbach G, Durner J

Abstract

Although nitric oxide (NO) has grown into a key signaling molecule in plants during the last few years, less is known about how NO regulates different events in plants. Analyses of NO-dependent processes in animal systems have demonstrated protein S-nitrosylation of cysteine (Cys) residues to be one of the dominant regulation mechanisms for many animal proteins. For plants, the principle of S-nitrosylation remained to be elucidated. We generated S-nitrosothiols by treating extracts from Arabidopsis (Arabidopsis thaliana) cell suspension cultures with the NO-donor S-nitrosoglutathione. Furthermore, Arabidopsis plants were treated with gaseous NO to analyze whether S-nitrosylation can occur in the specific redox environment of a plant cell in vivo. S-Nitrosylated proteins were detected by a biotin switch method, converting S-nitrosylated Cys to biotinylated Cys. Biotin-labeled proteins were purified and analyzed using nano liquid chromatography in combination with mass spectrometry. We identified 63 proteins from cell cultures and 52 proteins from leaves that represent candidates for S-nitrosylation, including stress-related, redox-related, signaling/regulating, cytoskeleton, and metabolic proteins. Strikingly, many of these proteins have been identified previously as targets of S-nitrosylation in animals. At the enzymatic level, a case study demonstrated NO-dependent reversible inhibition of plant glyceraldehyde-3-phosphate dehydrogenase, suggesting that this enzyme could be affected by S-nitrosylation. The results of this work are the starting point for further investigation to get insight into signaling pathways and other cellular processes regulated by protein S-nitrosylation in plants.

MeSH Terms
Amino Acid Sequence Arabidopsis/enzymology,metabolism Arabidopsis Proteins/chemistry,metabolism Cells, Cultured Glyceraldehyde-3-Phosphate Dehydrogenases/antagonists & inhibitors,metabolism Molecular Sequence Data Nitric Oxide/physiology Plant Leaves Proteomics S-Nitrosothiols/chemistry,metabolism Signal Transduction
Chemicals
Arabidopsis Proteins S-Nitrosothiols Nitric Oxide Glyceraldehyde-3-Phosphate Dehydrogenases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lindermayr Christian
Institute of Biochemical Plant Pathology, GSF-National Research Center for Environment and Health, D-85764 Munich/Neuherberg, Germany.
Saalbach Gerhard
Durner Jörg
References (69)
69 references, click to expand
  1. Numerous posttranslational modifications provide opportunities for the intricate regulation of metabolic enzymes at multiple levels.
    Curr Opin Plant Biol. 2004 Jun;7(3):318-22 PMID: 15134753
  2. Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana.
    Plant Cell Physiol. 2004 Jan;45(1):18-27 PMID: 14749482
  3. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide.
    Nat Cell Biol. 2001 Feb;3(2):193-7 PMID: 11175752
  4. Maize glutathione-dependent formaldehyde dehydrogenase: protein sequence and catalytic properties.
    Planta. 1999 Mar;208(1):12-8 PMID: 10213000
  5. Hydrogen peroxide and nitric oxide as signalling molecules in plants.
    J Exp Bot. 2002 May;53(372):1237-47 PMID: 11997372
  6. Nitrosylation. the prototypic redox-based signaling mechanism.
    Cell. 2001 Sep 21;106(6):675-83 PMID: 11572774
  7. Apoplastic synthesis of nitric oxide by plant tissues.
    Plant Cell. 2004 Feb;16(2):332-41 PMID: 14742874
  8. Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase.
    J Biol Chem. 1999 Apr 2;274(14):9427-30 PMID: 10092623
  9. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  10. The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide.
    J Biol Chem. 2002 Nov 22;277(47):44946-52 PMID: 12270927
  11. The biotin switch method for the detection of S-nitrosylated proteins.
    Sci STKE. 2001 Jun 12;2001(86):pl1 PMID: 11752655
  12. Proteomic analysis of S-nitrosylated proteins in mesangial cells.
    Mol Cell Proteomics. 2003 Mar;2(3):156-63 PMID: 12671063
  13. Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3330-4 PMID: 11854454
  14. S-nitrosoglutathione reversibly inhibits GAPDH by S-nitrosylation.
    Am J Physiol. 1995 Sep;269(3 Pt 1):C739-49 PMID: 7573405
  15. Regulation of chloroplast enzyme activities by thioredoxins: activation or relief from inhibition?
    Trends Plant Sci. 1999 Apr;4(4):136-141 PMID: 10322547
  16. Reversible inhibition of photophosphorylation in chloroplasts by nitric oxide.
    FEBS Lett. 2002 Feb 13;512(1-3):145-8 PMID: 11852069
  17. Maize glutathione-dependent formaldehyde dehydrogenase cDNA: a novel plant gene of detoxification.
    Plant Mol Biol. 1997 Aug;34(6):843-54 PMID: 9290637
  18. S-NO-actin: S-nitrosylation kinetics and the effect on isolated vascular smooth muscle.
    J Muscle Res Cell Motil. 2000 Feb;21(2):171-81 PMID: 10961840
  19. Novel application of S-nitrosoglutathione-Sepharose to identify proteins that are potential targets for S-nitrosoglutathione-induced mixed-disulphide formation.
    Biochem J. 2000 Jul 15;349(Pt 2):567-78 PMID: 10880356
  20. Identification of proteins undergoing glutathionylation in oxidatively stressed hepatocytes and hepatoma cells.
    Proteomics. 2003 Jul;3(7):1154-61 PMID: 12872216
  21. Nitric oxide: a new player in plant signalling and defence responses.
    Curr Opin Plant Biol. 2004 Aug;7(4):449-55 PMID: 15231269
  22. The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione.
    Plant Cell Physiol. 2003 Jul;44(7):655-60 PMID: 12881492
  23. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.
    Anal Chem. 1996 Mar 1;68(5):850-8 PMID: 8779443
  24. Specificity of antioxidant enzyme inhibition in skeletal muscle to reactive nitrogen species donors.
    Biochem Biophys Res Commun. 2002 Jun 28;294(5):1093-100 PMID: 12074589
  25. Isolation and characterization of a new peroxiredoxin from poplar sieve tubes that uses either glutaredoxin or thioredoxin as a proton donor.
    Plant Physiol. 2001 Nov;127(3):1299-309 PMID: 11706208
  26. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control.
    Nature. 1996 Mar 21;380(6571):221-6 PMID: 8637569
  27. Thylakoid protein phosphorylation and the thiol redox state.
    Biochemistry. 1999 Mar 9;38(10):3197-204 PMID: 10074375
  28. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3505-10 PMID: 11904414
  29. Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis.
    Arch Biochem Biophys. 2002 Oct 15;406(2):229-40 PMID: 12361711
  30. Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9438-43 PMID: 10430961
  31. Reversible cysteine-targeted oxidation of proteins during renal oxidative stress.
    J Am Soc Nephrol. 2003 Aug;14(8 Suppl 3):S290-6 PMID: 12874448
  32. Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol.
    J Biol Chem. 1999 Jun 11;274(24):17075-9 PMID: 10358060
  33. Inactivation of annexin II tetramer by S-nitrosoglutathione.
    Eur J Biochem. 2002 Sep;269(17):4277-86 PMID: 12199706
  34. Nitric oxide functions as a signal in plant disease resistance.
    Nature. 1998 Aug 6;394(6693):585-8 PMID: 9707120
  35. Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes.
    Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15811-6 PMID: 15498873
  36. Ancient origins of nitric oxide signaling in biological systems.
    Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14206-7 PMID: 10588683
  37. Purification and characterization of glutaredoxin (thioltransferase) from rice (Oryza sativa L.).
    J Biochem. 1997 May;121(5):842-8 PMID: 9192723
  38. The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid.
    FEBS Lett. 2003 May 22;543(1-3):136-9 PMID: 12753920
  39. Nitric oxide modulates the activity of tobacco aconitase.
    Plant Physiol. 2000 Feb;122(2):573-82 PMID: 10677450
  40. Nitric oxide and the regulation of gene expression.
    Trends Cell Biol. 2001 Feb;11(2):66-75 PMID: 11166214
  41. Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells.
    Planta. 2002 Oct;215(6):914-23 PMID: 12355151
  42. Protein S-thiolation and redox regulation of membrane-bound glutathione transferase.
    Chem Biol Interact. 1998 Apr 24;111-112:177-85 PMID: 9679553
  43. (S)NO signals: translocation, regulation, and a consensus motif.
    Neuron. 1997 May;18(5):691-6 PMID: 9182795
  44. Comprehensive survey of proteins targeted by chloroplast thioredoxin.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11224-9 PMID: 11553771
  45. Differential role of glutaredoxin and thioredoxin in metabolic oxidative stress-induced activation of apoptosis signal-regulating kinase 1.
    Biochem J. 2003 Aug 1;373(Pt 3):845-53 PMID: 12723971
  46. Detection and proteomic identification of S-nitrosylated proteins in endothelial cells.
    Arch Biochem Biophys. 2004 Mar 1;423(1):192-9 PMID: 14871481
  47. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7674-7 PMID: 1502182
  48. Nitric oxide inactivates rat hepatic methionine adenosyltransferase In vivo by S-nitrosylation.
    Hepatology. 1998 Oct;28(4):1051-7 PMID: 9755242
  49. Reversible S-glutathionylation of Cys 374 regulates actin filament formation by inducing structural changes in the actin molecule.
    Free Radic Biol Med. 2003 Jan 1;34(1):23-32 PMID: 12498976
  50. New insights into protein S-nitrosylation. Mitochondria as a model system.
    J Biol Chem. 2004 Jun 11;279(24):25891-7 PMID: 15069080
  51. Activation of rat liver microsomal glutathione S-transferase by reduced oxygen species.
    J Biol Chem. 1989 Feb 5;264(4):1998-2002 PMID: 2492517
  52. Biochemistry of nitric oxide and its redox-activated forms.
    Science. 1992 Dec 18;258(5090):1898-902 PMID: 1281928
  53. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae.
    Biochem J. 2003 Sep 1;374(Pt 2):513-9 PMID: 12755685
  54. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10328-33 PMID: 9707647
  55. Redox signaling: nitrosylation and related target interactions of nitric oxide.
    Cell. 1994 Sep 23;78(6):931-6 PMID: 7923362
  56. Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment.
    J Biol Chem. 1996 Feb 23;271(8):4209-14 PMID: 8626764
  57. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  58. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana.
    Planta. 2004 Apr;218(6):938-46 PMID: 14716563
  59. Abscisic acid, nitric oxide and stomatal closure - is nitrate reductase one of the missing links?
    Trends Plant Sci. 2003 Jan;8(1):20-6 PMID: 12523996
  60. Inactivation of glutathione peroxidase by NO leads to the accumulation of H2O2 and the induction of HB-EGF via c-Jun NH2-terminal kinase in rat aortic smooth muscle cells.
    FASEB J. 2001 Jun;15(8):1472-4 PMID: 11387261
  61. Regulation of microsomal and cytosolic glutathione S-transferase activities by S-nitrosylation.
    Biochem Pharmacol. 2002 Apr 15;63(8):1397-404 PMID: 11996880
  62. Identification of a plant nitric oxide synthase gene involved in hormonal signaling.
    Science. 2003 Oct 3;302(5642):100-3 PMID: 14526079
  63. Natural resistance and nitric oxide.
    Cell. 1995 Sep 22;82(6):873-6 PMID: 7553846
  64. Dual role of cysteine 172 in redox regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity and degradation.
    J Bacteriol. 2003 Mar;185(5):1509-17 PMID: 12591867
  65. Oxidative Stress Induces Partial Degradation of the Large Subunit of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase in Isolated Chloroplasts of Barley.
    Plant Physiol. 1996 Jul;111(3):789-796 PMID: 12226330
  66. S-nitrosoglutathione in rat cerebellum: identification and quantification by liquid chromatography-mass spectrometry.
    J Neurochem. 1997 Dec;69(6):2599-607 PMID: 9375694
  67. Determination of S-nitrosoglutathione in human and rat plasma by high-performance liquid chromatography with fluorescence and ultraviolet absorbance detection after precolumn derivatization with o-phthalaldehyde.
    Anal Biochem. 1999 Aug 15;273(1):32-40 PMID: 10452796
  68. SNARE-protein-mediated disease resistance at the plant cell wall.
    Nature. 2003 Oct 30;425(6961):973-7 PMID: 14586469
  69. Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase.
    J Biol Chem. 1992 Feb 5;267(4):2810-6 PMID: 1733975
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2005-03-00
Epub
2005-00-25
Pages
921-30
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC1065393
Subset
IM
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]