S-Nitrosylation: an emerging redox-based post-translational modification in plants

Journal of Experimental Botany, May 2006

S-nitrosylation, the covalent attachment of a nitric oxide moiety to a cysteine thiol, is now established as a key post-translational modification in animals. This process has been shown to regulate the function of a wide variety of regulatory, structural, and metabolic proteins. The emerging evidence now suggests that S-nitrosylation may also have a central function in plant biology.

A PDF file should load here. If you do not see its contents the file may be temporarily unavailable at the journal website or you do not have a PDF plug-in installed and enabled in your browser.

Alternatively, you can download the file locally and open with any standalone PDF reader:

https://jxb.oxfordjournals.org/content/57/8/1777.full.pdf

S-Nitrosylation: an emerging redox-based post-translational modification in plants

Yiqin Wang 0 Byung-Wook Yun 0 EunJung Kwon 0 Jeum Kyu Hong 0 Joonseon Yoon 0 Gary J. Loake 0 0 Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh , King's Buildings, Edinburgh EH9 3JH , UK S-nitrosylation, the covalent attachment of a nitric oxide moiety to a cysteine thiol, is now established as a key post-translational modification in animals. This process has been shown to regulate the function of a wide variety of regulatory, structural, and metabolic proteins. The emerging evidence now suggests that S-nitrosylation may also have a central function in plant biology. Introduction The discovery of the biological functions of nitric oxide (NO) in the late 1980s came as an unexpected surprise. Subsequently, NO was named Molecule of the Year in 1992 by the journal Science. Furthermore, in 1998, Murad, Furchgott, and Ignarro shared the Nobel Prize for Physiology and Medicine for their work demonstrating that NO generated by endothelial cells relaxes smooth muscle through activation of guanylate cyclase (Murad, 1986). Gradually, the diverse cellular activities of NO, one of only a handful of gaseous signalling molecules, began to be appreciated. Early findings suggested that NO was a freely diffusible second messenger, with a promiscuous sphere of influence, functioning predominantly through the regulation of guanylate cyclase (Lancaster, 1994). More recent evidence, however, has resulted in a critical reappraisal of this initial paradigm, as NO signalling was increasingly found to occur independently of this key regulatory enzyme. The rich redox and additive chemistry of NO facilitates its interactions with centres of ironsulphur clusters and haem, present in a wide variety of proteins, impacting their activities (Stamler, 1994). In 1992, an additional mechanism underpinning NO signalling was established: in this scenario, NO could be coupled to a reactive cysteine thiol, forming an S-nitrosothiol (SNO) (Stamler et al., 1992). The presence of this group could subsequently modulate protein function, analogous to the addition of a phosphate group during phosphorylation. Over the last decade, S-nitrosylation has been demonstrated to regulate an increasing number of signalling systems, structural proteins, and metabolic processes in animals (Hess et al., 2005). There is also a developing appreciation of the precise spatial and temporal regulation of SNO formation, which confers an exquisite specificity to NO signalling (Stamler et al., 1997). S-Nitrosylation has now become established as the prototypic, redox-based, post-translational modification within the animal sciences. However, the functions of SNO synthesis and turnover in plant biology are only just beginning to emerge. Thus, the early sections of this review will cover the role of S-nitrosylation in animal systems, with the final sections addressing the nascent field of SNO biology in plants. S-Nitrosylation/de-nitrosylation/ transnitrosylation The NO moiety required for S-nitrosylation can be derived from a diversity of sources in addition to NO, including other NOx species, metalNO complexes, peroxynitrite, nitrite, or SNOs (Fig. 1). To date, specific enzymatic mechanisms responsible for S-nitrosylation have not been identified; however, several enzymes are known to promote Fig. 1. S-Nitrosylation of a target cysteine by NO. The formation of an SNO can be mediated directly by NO or indirectly via NOx, transition metal adducts (M-NO), SNOs or peroxynitrite (ONOO ). Reaction mechanisms and stoichiometries are not detailed in this rubric. The S-nitrosylated cysteine is shown embedded within a proposed linear SNO motif. S-nitrosylation or de-nitrosylation reactions. For example, ceruloplasmin catalyses the S-nitrosylation of the proteoglycan, glypican, and it can also promote the formation of S-nitrosoglutathione (GSNO) from NO (Inoue et al., 1999). Thiol-to-thiol SNO formation, termed transnitrosylation, has also been reported. In this case, NO from S-nitrosohaemoglobin has been shown to be directly transferred to a neighbouring thiol on Band3, a haemoglobin-interacting protein (Pawloski et al., 2001). SNO turnover or de-nitrosylation can be mediated by thioredoxin, exemplified by a reversal of the NO-mediated inhibition of protein kinase C (Kahlos et al., 2003). GSNO is formed rapidly in cells and body fluids following the interaction of NO with GSH, a major cellular antioxidant (Gaston et al., 1993). GSNO is a stable and mobile molecule and can therefore serve as a reservoir of NO bioactivity. Recently, an enzyme has been reported that turns over GSNO. This so-called GSNO reductase (GSNOR), first purified from Escherichia coli, is also thought to be important for the control of GSNO homeostasis in yeast and mice (Liu et al., 2001). The absence of GSNOR function increased GSNO and protein-SNO levels, even though GSNOR does not directly de-nitrosylate the latter. This observation suggests there is a dynami (...truncated)


This is a preview of a remote PDF: https://jxb.oxfordjournals.org/content/57/8/1777.full.pdf

Yiqin Wang, Byung-Wook Yun, EunJung Kwon, Jeum Kyu Hong, Joonseon Yoon, Gary J Loake. S-Nitrosylation: an emerging redox-based post-translational modification in plants, Journal of Experimental Botany, 2006, pp. 1777-1784, 57/8, DOI: 10.1093/jxb/erj211