S-Nitrosylation: an emerging redox-based post-translational modification in plants
Yiqin Wang
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Byung-Wook Yun
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EunJung Kwon
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Jeum Kyu Hong
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Joonseon Yoon
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Gary J. Loake
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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)