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Reducing lipid peroxidation attenuates stress-induced susceptibility to herpes simplex virus type 1

Jing-yu Weng1,2,3, Xin-xing Chen1,2,3, Xiao-hua Wang1,2,3, Hui-er Ye1,2,3, Yan-ping Wu1,2,3, Wan-yang Sun1,2,3, Lei Liang1,2,3, Wen-jun Duan1,2,3, Hiroshi Kurihara1,2,3, Feng Huang4, Xin-xin Sun5, Shu-hua Ou-Yang1,2,3, Rong-rong He1,2,3,4, Yi-fang Li1,2,3
1 Guangdong Engineering Research Center of Chinese Medicine & Disease Susceptibility
2 International Cooperative Laboratory of Traditional Chinese Medicine Modernization and Innovative Drug Development of Chinese Ministry of Education (MOE), College of Pharmacy, Jinan University, Guangzhou 510632, China
3 Guangdong Province Key Laboratory of Pharmacodynamic Constituents of TCM and New Drugs Research, College of Pharmacy, Jinan University, Guangzhou 510632, China
4 School of Chinese Materia Medica and Yunnan Key Laboratory of Southern Medicinal Utilization, Yunnan University of Chinese Medicine, Kunming 650500, China
5 Jiujiang Maternal and Child Health Hospital, Jiujiang 332000, China
Correspondence to: Shu-hua Ou-Yang: shouyang@jnu.edu.cn, Rong-rong He: rongronghe@jnu.edu.cn, Yi-fang Li: liyifang706@jnu.edu.cn,
DOI: 10.1038/s41401-023-01095-6
Received: 11 January 2023
Accepted: 19 April 2023
Advance online: 16 May 2023

Abstract

Psychological stress increases the susceptibility to herpes simplex virus type 1 (HSV-1) infection. There is no effective intervention due to the unknown pathogenesis mechanisms. In this study we explored the molecular mechanisms underlying stress-induced HSV-1 susceptibility and the antiviral effect of a natural compound rosmarinic acid (RA) in vivo and in vitro. Mice were administered RA (11.7, 23.4 mg·kg−1·d−1, i.g.) or acyclovir (ACV, 206 mg·kg−1·d−1, i.g.) for 23 days. The mice were subjected to restraint stress for 7 days followed by intranasal infection with HSV-1 on D7. At the end of RA or ACV treatment, mouse plasma samples and brain tissues were collected for analysis. We showed that both RA and ACV treatment significantly decreased stress-augmented mortality and alleviated eye swelling and neurological symptoms in HSV-1-infected mice. In SH-SY5Y cells and PC12 cells exposed to the stress hormone corticosterone (CORT) plus HSV-1, RA (100 μM) significantly increased the cell viability, and inhibited CORT-induced elevation in the expression of viral proteins and genes. We demonstrated that CORT (50 μM) triggered lipoxygenase 15 (ALOX15)-mediated redox imbalance in the neuronal cells, increasing the level of 4-HNE-conjugated STING, which impaired STING translocation from the endoplasmic reticulum to Golgi; the abnormality of STING-mediated innate immunity led to HSV-1 susceptibility. We revealed that RA was an inhibitor of lipid peroxidation by directly targeting ALOX15, thus RA could rescue stress-weakened neuronal innate immune response, thereby reducing HSV-1 susceptibility in vivo and in vitro. This study illustrates the critical role of lipid peroxidation in stress-induced HSV-1 susceptibility and reveals the potential for developing RA as an effective intervention in anti-HSV-1 therapy.

Keywords: Herpes simplex virus type 1; stress; corticosterone; arachidonate lipoxygenase 15; phospholipid peroxidation; STING; viral infection; rosmarinic acid; neuronal cells

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