Targeting antioxidant enzyme expression as a therapeutic strategy for ischemic stroke

https://doi.org/10.1016/j.neuint.2016.12.007Get rights and content

Highlights

  • Overview of antioxidants as treatment for stroke.

  • Explanation of failed attempts to develop exogenous antioxidant treatment.

  • Overview of endogenous antioxidant systems.

  • Use of agents that activate these endogenous antioxidant systems to develop stroke therapeutic.

Abstract

During ischemic stroke, neurons and glia are subjected to damage during the acute and neuroinflammatory phases of injury. Production of reactive oxygen species (ROS) from calcium dysregulation in neural cells and the invasion of activated immune cells are responsible for stroke-induced neurodegeneration. Scientists have failed thus far to identify antioxidant-based drugs that can enhance neural cell survival and improve recovery after stroke. However, several groups have demonstrated success in protecting against stroke by increasing expression of antioxidant enzymes in neural cells. These enzymes, which include but are not limited to enzymes in the glutathione peroxidase, catalase, and superoxide dismutase families, degrade ROS that otherwise damage cellular components such as DNA, proteins, and lipids. Several groups have identified cellular therapies including neural stem cells and human umbilical cord blood cells, which exert neuroprotective and oligoprotective effects through the release of pro-survival factors that activate PI3K/Akt signaling to upregulation of antioxidant enzymes. Other studies demonstrate that treatment with soluble factors released by these cells yield similar changes in enzyme expression after stroke. Treatment with the cytokine leukemia inhibitory factor increases the expression of peroxiredoxin IV and metallothionein III in glia and boosts expression of superoxide dismutase 3 in neurons. Through cell-specific upregulation of these enzymes, LIF and other Akt-inducing factors have the potential to protect multiple cell types against damage from ROS during the early and late phases of ischemic damage.

Section snippets

Production of reactive oxygen species

Oxidative stress is characterized by the excess production of reactive oxygen species (ROS), which may cause irreversible damage to cellular components. Although neural cell damage during stroke is partially triggered by hypoxia, oxidative stress plays an instrumental role during the initial and later phases of ischemic stroke pathophysiology. During the initial phase of injury, energy failure interferes with the activity of ATP-dependent ion channels and the maintenance of the electrochemical

Glutathione metabolism

Under physiological and pathophysiological conditions, several enzymes are responsible for regulating redox balance in neurons. Some of these enzymes protect neurons from oxidative stress by maintaining adequate expression levels of the antioxidant glutathione. Glutathione, an oligopeptide containing a cysteine residue, acts as a nucleophile by donating electrons to break the disulfide bonds of oxidized proteins. Once reduced, these proteins are unable to react with other cellular components

Sex-specific antioxidant expression

Preclinical and clinical studies indicate that high levels of estrogen protect younger females against the risk of ischemic stroke. In addition to decreasing inflammation, estrogen increases the expression and activity of several antioxidant enzymes in the brain. In a study by Borras et al., female rats were less prone to mitochondrial damage compared to male rats due to higher basal expression of GSH-PX and SOD2 (Borrás et al., 2003). Strehlow et al. showed that 17β-estradiol administration

Human umbilical cord blood cells

Although these therapies contain mesenchymal stem cells, cells isolated from autologous peripheral and umbilical cord blood also contain a large fraction of mononuclear cells, which consist of monocytes/macrophages, lymphocytes, and neutrophils. Similar to NSCs, these cell populations have been shown to exert protective effects via released factors that activate survival signaling. HUCB treatment 48 h after stroke increases PI3K/Akt signaling and induces the expression of antioxidant enzymes.

Antioxidant enzymes upregulated by LIF

Since LIF is among the factors produced by HUCB cell (Seo et al., 2011), LIF does promote antioxidant expression and reduce white matter damage after permanent FCI in a manner similar to HUCB therapy. Rats were administered either LIF or PBS at 6, 24, and 48 h after undergoing permanent MCAO and euthanized at 72 h. According to the results of this study, LIF treatment increased motor skill recovery and reduced stroke volume at 72 h post-MCAO. White matter showed considerably lower levels of

Antioxidant effects of other IL-6 family cytokines

Despite the failures of exogenous agents, focusing research efforts on drugs that confer long-lasting changes in antioxidant expression have shown great potential in treating animal models of stroke. Anti-inflammatory cytokines provide a unique benefit to stroke patients: they exert their signaling quickly before being cleared from the body, thus lessening the potential for adverse side effects. However, the downstream effects of these signaling pathways confer long-lasting protection by

Conclusion

One of the current shortcomings of clinical stroke treatments stems from the inability to address both phases of stroke pathophysiology. Increased expression of enzymes such as Prdx4, Mt3, and SOD3 would not only protect neural cells against ROS that are generated during the acute cytotoxic phase of damage, but also against ROS produced by activated microglia and peripheral leukocytes. Moreover, these antioxidant enzymes can be modified (polyethylene glycol) to increase their stability thus

Funding

This study was funded by project #7R01NS091146-02 from the National Institute of Neurological Disorders and Stroke.

Conflict of interest

Stephanie M. Davis declares that she has no conflict of interest. Keith R. Pennypacker declares that he has no conflict of interest.

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