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Additive Effect of Resveratrol on Astrocyte Swelling Post-exposure to Ammonia, Ischemia and Trauma In Vitro

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Abstract

Swelling of astrocytes represents a major component of the brain edema associated with many neurological conditions, including acute hepatic encephalopathy (AHE), traumatic brain injury (TBI) and ischemia. It has previously been reported that exposure of cultured astrocytes to ammonia (a factor strongly implicated in the pathogenesis of AHE), oxygen/glucose deprivation, or to direct mechanical trauma results in an increase in cell swelling. Since dietary polyphenols have been shown to exert a protective effect against cell injury, we examined whether resveratrol (RSV, 3,5,4′-trihydroxy-trans-stilbene, a stilbenoid phenol), has a protective effect on astrocyte swelling following its exposure to ammonia, oxygen–glucose deprivation (OGD), or trauma in vitro. Ammonia increased astrocyte swelling, and pre- or post-treatment of astrocytes with 10 and 25 µM RSV displayed an additive effect, while 5 µM did not prevent the effect of ammonia. However, pre-treatment of astrocytes with 25 µM RSV slightly, but significantly, reduced the trauma-induced astrocyte swelling at earlier time points (3 h), while post-treatment had no significant effect on the trauma-induced cell swelling at the 3 h time point. Instead, pre- or post-treatment of astrocytes with 25 µM RSV had an additive effect on trauma-induced astrocyte swelling. Further, pre- or post-treatment of astrocytes with 5 or 10 µM RSV had no significant effect on trauma-induced astrocyte swelling. When 5 or 10 µM RSV were added prior to, or during the process of OGD, as well as post-OGD, it caused a slight, but not statistically significant decline in cell swelling. However, when 25 µM RSV was added during the process of OGD, as well as after the cells were returned to normal condition (90 min period), such treatment showed an additive effect on the OGD-induced astrocyte swelling. Noteworthy, a higher concentration of RSV (25 µM) exhibited an additive effect on levels of phosphorylated forms of ERK1/2, and p38MAPK, as well as an increased activity of the Na+–K+–Cl− co-transporter-1 (NKCC1), factors known to induce astrocytes swelling, when the cells were treated with ammonia or after trauma or ischemia. Further, inhibition of ERK1/2, and p38MAPK diminished the RSV-induced exacerbation of cell swelling post-ammonia, trauma and OGD treatment. These findings strongly suggest that treatment of cultured astrocytes with RSV enhanced the ammonia, ischemia and trauma-induced cell swelling, likely through the exacerbation of intercellular signaling kinases and ion transporters. Accordingly, caution should be exercised when using RSV for the treatment of these neurological conditions, especially when brain edema is also suspected.

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Acknowledgements

This work was supported by Stanley J. Glaser Research Grant and AASLD/American Liver Foundation grants (ARJ), and by a Merit Review from the US Department of Veterans Affairs (MDN). The authors thank Alina Fernandez-Revuelta for the preparation of cell cultures and Dr. Xiaoying Tong, Bobby Price and Margaret Rodriguez for technical assistance.

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Authors and Affiliations

  1. General Medical Research, Neuropathology Section, R&D Service, Veterans Affairs Medical Center, Miami, FL, 33125, USA

    Mehran Taherian, Kiran S. Panickar, Purbasha Rahman & Arumugam R. Jayakumar

  2. Department of Pathology, University of Miami School of Medicine, Miami, FL, USA

    Michael D. Norenberg

  3. Department of Biochemistry & Molecular Biology, University of Miami School of Medicine, Miami, FL, USA

    Michael D. Norenberg

  4. Department of Neurology and Neurological Surgery, University of Miami School of Medicine, Miami, FL, USA

    Michael D. Norenberg

  5. GeneChem Diagnostic Laboratories, Miami, FL, USA

    Nagarajarao Shamaladevi

  6. Department of Radiation Oncology, Sylvester Cancer Center, University of Miami School of Medicine, Miami, FL, USA

    Anis Ahmad

  7. Department of Microbiology and Immunology, University of Miami, Coral Cables, Miami, FL, USA

    Purbasha Rahman

  8. South Florida VA Foundation for Research and Education Inc, Veterans Affairs Medical Center, Miami, FL, 33125, USA

    Arumugam R. Jayakumar

  9. General Medical Research, Neuropathology Section, R&D Service, Veterans Affairs Medical Center, 1201 NW 16th St, Res-151, Room 314, Miami, FL, USA

    Arumugam R. Jayakumar

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  1. Mehran Taherian
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Contributions

ARJ, MDN, and NS conceived the study; ARJ, MT, AA and PR carried out the experiments; ARJ, NS, AA, KP and MT conducted the analyses; ARJ, NS, MT and KP wrote the paper.

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Correspondence to Arumugam R. Jayakumar.

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MT, MDN, NS, KSP, AA, PR and ARJ declare no conflicts of interest. NS is currently Director/CEO, GeneChem Diagnostic Laboratories, Miami, FL.

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Taherian, M., Norenberg, M.D., Panickar, K.S. et al. Additive Effect of Resveratrol on Astrocyte Swelling Post-exposure to Ammonia, Ischemia and Trauma In Vitro. Neurochem Res 45, 1156–1167 (2020). https://doi.org/10.1007/s11064-020-02997-1

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