On the Origin of Superoxide Dismutase: An Evolutionary Perspective of Superoxide-Mediated Redox Signaling

Case, Adam J.

doi:10.3390/antiox6040082

Cited by 118 publications

(125 citation statements)

References 171 publications

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“…SOD1 aggregates have been shown to bind amyloid-sensitive dyes, such as congo red or thioflavin T and S, but yield less fluorescence than is observed for amyloid-β or α-synuclein (DiDonato et al, 2003;Chattopadhyay et al, 2008;Furukawa et al, 2008;Oztug Durer et al, 2009). Thioflavin S stains inclusions formed by the artificial SOD1 double mutant His46Arg/His48Gln and ALS mutants Gly37Arg, Gly85Arg and Gly93Ala in transgenic mouse spinal cord tissue (Wang et al, 2002).…”

Section: Amyloid or Not?mentioning

confidence: 99%

The biophysics of superoxide dismutase-1 and amyotrophic lateral sclerosis

Wright

Antonyuk

Hasnain

2019

Quart. Rev. Biophys.

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Few proteins have come under such intense scrutiny as superoxide dismutase-1 (SOD1). For almost a century, scientists have dissected its form, function and then later its malfunction in the neurodegenerative disease amyotrophic lateral sclerosis (ALS). We now know SOD1 is a zinc and copper metalloenzyme that clears superoxide as part of our antioxidant defence and respiratory regulation systems. The possibility of reduced structural integrity was suggested by the first crystal structures of human SOD1 even before deleterious mutations in thesod1gene were linked to the ALS. This concept evolved in the intervening years as an impressive array of biophysical studies examined the characteristics of mutant SOD1 in great detail. We now recognise how ALS-related mutations perturb the SOD1 maturation processes, reduce its ability to fold and reduce its thermal stability and half-life. Mutant SOD1 is therefore predisposed to monomerisation, non-canonical self-interactions, the formation of small misfolded oligomers and ultimately accumulation in the tell-tale insoluble inclusions found within the neurons of ALS patients. We have also seen that several post-translational modifications could push wild-type SOD1 down this toxic pathway. Recently we have come to view ALS as a prion-like disease where both the symptoms, and indeed SOD1 misfolding itself, are transmitted to neighbouring cells. This raises the possibility of intervention after the initial disease presentation. Several small-molecule and biologic-based strategies have been devised which directly target the SOD1 molecule to change the behaviour thought to be responsible for ALS. Here we provide a comprehensive review of the many biophysical advances that sculpted our view of SOD1 biology and the recent work that aims to apply this knowledge for therapeutic outcomes in ALS.

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Section: Amyloid or Not?mentioning

confidence: 99%

The biophysics of superoxide dismutase-1 and amyotrophic lateral sclerosis

Wright

Antonyuk

Hasnain

2019

Quart. Rev. Biophys.

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“…This also increases the availability of oxygen for oxygen‐dependent metabolic pathways like pigment synthesis (Fujita, Tsujimoto, & Aoki, ). In fact, maximum oxygen levels measured in pseudomats in freshwater medium under eCO 2 rO 2 atmosphere came close to ( G. violaceus ; Supporting Information Figure S3b) or exceeded ( C. thermalis ; Supporting Information Figure S2b) the oxygen saturation point of freshwater cultures exposed to present‐day levels of oxygen, stressing the importance of reactive oxygen species (ROS)‐detoxifying mechanisms having to have evolved prior to the GOE (Case, ; Cardona, ).…”

Section: Discussionmentioning

confidence: 94%

“…Chlorophyll-based photosynthesis is generally accepted to have originated in bacteria in an anoxic environment (Hohmann-Marriott & Blankenship, 2011). The evolution of a heterodimeric photosystem I reaction centre, found in all oxygenic phototrophs today, is thought to have evolved as a protection mechanism against the formation of reactive oxygen species more than 3.4 Ga (Cardona, 2018), necessitating the evolution of protective antioxidant systems (Sheng et al, 2014;Case, 2017). The energy released from the decomposition of water by photosystem I is higher than any other redox couple potentially used during anoxic photosynthesis and could be used to form organic molecules for growth and storage (Hohmann-Marriott & Blankenship, 2011).…”

Section: Introductionmentioning

confidence: 99%

An investigation into the effects of increasing salinity on photosynthesis in freshwater unicellular cyanobacteria during the late Archaean

Herrmann

Gehringer

2019

Geobiology

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The oldest species of bacteria capable of oxygenic photosynthesis today are the freshwater Cyanobacteria Gloeobacter spp., belonging to the class Oxyphotobacteria. Several modern molecular evolutionary studies support the freshwater origin of cyanobacteria during the Archaean and their subsequent acquisition of salt tolerance mechanisms necessary for their expansion into the marine environment. This study investigated the effect of a sudden washout event from a freshwater location into either a brackish or marine environment on the photosynthetic efficiency of two unicellular freshwater cyanobacteria: the salt‐tolerant Chroococcidiopsis thermalis PCC7203 and the cyanobacterial phylogenetic root species, Gloeobacter violaceus PCC7421. Strains were cultured under present atmospheric levels (PAL) of CO2 or an atmosphere containing elevated levels of CO2 and reduced O2 (eCO2rO2) in simulated shallow water or terrestrial environmental conditions. Both strains exhibited a reduction in growth rates and gross photosynthesis, accompanied by significant reductions in chlorophyll a content, in brackish water, with only C. thermalis able to grow at marine salinity levels. While the experimental atmosphere caused a significant increase in gross photosynthesis rates in both strains, it did not increase their growth rates, nor the amount of O2 released. The differences in growth responses to increasing salinities could be attributed to genetic differences, with C. thermalis carrying additional genes for trehalose synthesis. This study demonstrates that, if cyanobacteria did evolve in a freshwater environment, they would have been capable of withstanding a sudden washout into increasingly saline environments. Both C. thermalis and G. violaceus continued to grow and photosynthesise, albeit at diminished rates, in brackish water, thereby providing a route for the evolution of open ocean‐dwelling strains, necessary for the oxygenation of the Earth's atmosphere.

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“…photolysis of water by ultraviolet light) or cohabitation with an oxidative photosynthesising organism (Case, ). Three primary antioxidant enzymes arose prior to the Great Oxidation Event (GOE): superoxide dismutase, catalase and peroxiredoxins (Case, ). Pre‐Є, Pre‐Cambrian; Є, Cambrian; O, Ordovician; S, Silurian; D, Devonian; C, Carboniferous; P, Permian; Tr, Triassic; J, Jurassic; K, Cretaceous; T, Tertiary (Berner et al .…”

Section: Coupled Evolution Of Life and O2mentioning

confidence: 97%

“…Earth's oxidation was probably paralleled by selective pressure favouring survival of organisms that could tolerate O 2 toxicity and control oxidative processes to harness energy, including cellular protection through evolution of antioxidant defence, though sequence analyses suggest that even LUCA was capable of detoxifying reactive oxygen species (ROS) long before O 2 became abundant in the atmosphere or ocean, probably as a result of localised O 2 formation via abiotic sources (e.g. photolysis of water by ultraviolet light) or cohabitation with an oxidative photosynthesising organism (Case, ). Three primary antioxidant enzymes arose prior to the Great Oxidation Event (GOE): superoxide dismutase, catalase and peroxiredoxins (Case, ).…”

Section: Coupled Evolution Of Life and O2mentioning

confidence: 99%

Oxygen, evolution and redox signalling in the human brain; quantum in the quotidian

Bailey

2018

The Journal of Physiology

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Rising atmospheric oxygen (O2) levels provided a selective pressure for the evolution of O2‐dependent micro‐organisms that began with the autotrophic eukaryotes. Since these primordial times, the respiring mammalian cell has become entirely dependent on the constancy of electron flow, with molecular O2 serving as the terminal electron acceptor in mitochondrial oxidative phosphorylation. Indeed, the ability to ‘sense’ O2 and maintain homeostasis is considered one of the most important roles of the central nervous system (CNS) and probably represented a major driving force in the evolution of the human brain. Today, modern humans have evolved with an oversized brain committed to a continually active state and, as a consequence, paradoxically vulnerable to failure if the O2 supply is interrupted. However, our pre‐occupation with O2, the elixir of life, obscures the fact that it is a gas with a Janus face, capable of sustaining life in physiologically controlled amounts yet paradoxically deadly to the CNS when in excess. A closer look at its quantum structure reveals precisely why; the triplet ground state diatomic O2 molecule is paramagnetic and exists in air as a free radical, constrained from reacting aggressively with the brain's organic molecules due to its ‘spin restriction’, a thermodynamic quirk of evolutionary fate. By further exploring O2’s free radical ‘quantum quirkiness’, including emergent (quantum) physiological phenomena, our understanding of precisely how the human brain senses O2 deprivation (hypoxia) and the elaborate redox‐signalling defence mechanisms that defend O2 homeostasis has the potential to offer unique insights into the pathophysiology and treatment of human brain disease.

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On the Origin of Superoxide Dismutase: An Evolutionary Perspective of Superoxide-Mediated Redox Signaling

Cited by 118 publications

References 171 publications

The biophysics of superoxide dismutase-1 and amyotrophic lateral sclerosis

The biophysics of superoxide dismutase-1 and amyotrophic lateral sclerosis

An investigation into the effects of increasing salinity on photosynthesis in freshwater unicellular cyanobacteria during the late Archaean

Oxygen, evolution and redox signalling in the human brain; quantum in the quotidian

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