Reactive oxygen and oxidative stress: N-formyl kynurenine in photosystem II and non-photosynthetic proteins

Abstract

While light is the essential driving force for photosynthetic carbon fixation, high light intensities are toxic to photosynthetic organisms. Prolonged exposure to high light results in damage to the photosynthetic membrane proteins and suboptimal activity, a phenomenon called photoinhibition. The primary target for inactivation is the photosystem II (PSII) reaction center. PSII catalyzes the light-induced oxidation of water at the oxygen-evolving complex. Reactive oxygen species (ROS) are generated under photoinhibitory conditions and induce oxidative post translational modifications of amino acid side chains. Specific modification of tryptophan residues to N-formylkynurenine (NFK) occurs in the CP43 and D1 core polypeptides of PSII. The NFK modification has also been detected in other proteins, such as mitochondrial respiratory enzymes, and is formed by a non-random, ROS-targeted mechanism. NFK has been shown to accumulate in PSII during conditions of high light stress in vitro. This review provides a summary of what is known about the generation and function of NFK in PSII and other proteins. Currently, the role of ROS in photoinhibition is under debate. Furthermore, the triggers for the degradation and accelerated turnover of PSII subunits, which occur under high light, are not yet identified. Owing to its unique optical and Raman signal, NFK provides a new marker to use in the identification of ROS generation sites in PSII and other proteins. Also, the speculative hypothesis that NFK, and other oxidative modifications of tryptophan, play a role in the PSII damage and repair cycle is discussed. NFK may have a similar function during oxidative stress in other biologic systems.

Tripping up Trp: Modification of protein tryptophan residues by reactive oxygen species, modes of detection, and biological consequences

“…The photosystems also contain chlorophylls as well as ancillary light-harvesting pigments that enable the plant to convert light into chemical energy [91]. Intensive research over many years has focused on the goal of increasing photosynthetic efficiency.…”

“…One aspect of the sensing and repair mechanism seems to rely on the oxidation of Trp residues to NFK in core proteins of PSII, a reaction occurring readily in the presence of 1 O 2 . In PSII, increasing oxidation of Trp365 to NFK in the CP43 subunit correlates with increasing light stress and increasing photoinhibition in thylakoid membranes [91, 93]. While a small increase in ionic strength results in a decrease in NFK365 and leads instead to a Trp to NFK conversion in a different intrinsic polypeptide (D1), both the CP43 and the D1 Trp oxidations to NFK appear to be linked to D1 degradation and subsequent replacement of the damaged D1 proteins.…”

“…While a small increase in ionic strength results in a decrease in NFK365 and leads instead to a Trp to NFK conversion in a different intrinsic polypeptide (D1), both the CP43 and the D1 Trp oxidations to NFK appear to be linked to D1 degradation and subsequent replacement of the damaged D1 proteins. [91]. Because D1 protein degradation and replacement is a key step in photosynthetic recovery from high light stress Kasson et al [91] have proposed that Trp to NFK oxidation is a key signal for photosynthetic damage repair through protein turnover.…”

Unique Photobleaching Phenomena of the Twin-Arginine Translocase Respiratory Enzyme Chaperone DmsD

“…Residues W42 and W80 appeared to have an added mass corresponding to one oxygen molecule whereas W109 appeared to have two. It has been reported that addition of up to four oxygen molecules can occur on Trp upon UV irradiation [35]. With only a single oxygen molecule added to W42 and W80, these likely correspond to the formation of oxindolylalanine or hydroxytryptophan [36].…”

Stability of monoclonal antibodies (mAbs)

“…A suggested mechanistic route is the interaction of singlet oxygen with the Trp indole group resulting in a dioxetane intermediate, which can thermally decompose to kynurenine and N-formyl kynurenine (Adam, Ahrweiler, Sauter, & Schmiedeskamp, 1993). The detection of some of these oxidation products in proteins is aided by the changes in the UV absorption spectrum (Kasson & Barry, 2012). In addition, generation of kynurenine and N-formyl kynurenine can result in yellow-colored solutions due to red shifts in the absorption spectrum ( Figure 3.7(b)).…”