Luteolin inhibits herpes simplex virus 1 infection by activating cyclic guanosine monophosphate-adenosine monophosphate synthase-mediated antiviral innate immunity.


Journal

Phytomedicine : international journal of phytotherapy and phytopharmacology
ISSN: 1618-095X
Titre abrégé: Phytomedicine
Pays: Germany
ID NLM: 9438794

Informations de publication

Date de publication:
Nov 2023
Historique:
received: 15 02 2023
revised: 30 07 2023
accepted: 09 08 2023
medline: 25 9 2023
pubmed: 27 8 2023
entrez: 26 8 2023
Statut: ppublish

Résumé

The successive outbreaks of large-scale infectious diseases due to virus infection have been a major threat to human health in recent decades. Herpes simplex virus I (HSV-1) is a widely-disseminated DNA virus that infects the central nervous system to cause herpes labialis, keratitis and herpes simplex virus encephalitis (HSE), resulting in recurrent lifelong clinical or subclinical episodes. Luteolin is a plant flavone that has been extensively used in the treatment of various human diseases, including carcinogenesis, inflammation and chronic degenerative diseases. The aim of this study was to investigate the antiviral molecular mechanism of luteolin against HSV-1 infection in vitro and in vivo. The antiviral effect of luteolin in cell lines was examined by viral plaque assay, RT-qPCR, Western blot and time-of-addition assay. The interaction between luteolin and cyclic guanosine monophosphate-adenosine monophosphate synthase (cGAS) was evaluated by molecular modeling and semi-denaturing detergent agarose gel electrophoresis. The efficacy of luteolin on HSE was evaluated in the HSE mouse model by analyzing weight loss, neurodegenerative symptoms and histopathological scores. Cytokine expression and protein levels were examined by RT-qPCR, Western blot and ELISA. Luteolin inhibited the early process of HSV-1 infection, without affecting the infection of acyclovir-resistant HSV-1 strains. In addition, luteolin enhanced antiviral type I interferon production and activated the cytoplasmic DNA-sensing cGAS-stimulator of interferon gene (STING) pathway. Luteolin directly bound the active substrate binding site and promoted the oligomerization of cGAS. Luteolin also inhibited HSE-related weight loss, neurodegeneration and neuroinflammation in mice caused by HSV-1 infection. Furthermore, luteolin enhanced type I interferon expression and stimulated the cGAS-STING signaling pathway in vivo. Luteolin inhibited the post-entry process of HSV-1 by activating the cGAS-STING pathway to promote antiviral interferon production. These results provided the rationale for luteolin as a potent cGAS activator and antiviral agent.

Sections du résumé

BACKGROUND BACKGROUND
The successive outbreaks of large-scale infectious diseases due to virus infection have been a major threat to human health in recent decades. Herpes simplex virus I (HSV-1) is a widely-disseminated DNA virus that infects the central nervous system to cause herpes labialis, keratitis and herpes simplex virus encephalitis (HSE), resulting in recurrent lifelong clinical or subclinical episodes. Luteolin is a plant flavone that has been extensively used in the treatment of various human diseases, including carcinogenesis, inflammation and chronic degenerative diseases.
PURPOSE OBJECTIVE
The aim of this study was to investigate the antiviral molecular mechanism of luteolin against HSV-1 infection in vitro and in vivo.
METHODS METHODS
The antiviral effect of luteolin in cell lines was examined by viral plaque assay, RT-qPCR, Western blot and time-of-addition assay. The interaction between luteolin and cyclic guanosine monophosphate-adenosine monophosphate synthase (cGAS) was evaluated by molecular modeling and semi-denaturing detergent agarose gel electrophoresis. The efficacy of luteolin on HSE was evaluated in the HSE mouse model by analyzing weight loss, neurodegenerative symptoms and histopathological scores. Cytokine expression and protein levels were examined by RT-qPCR, Western blot and ELISA.
RESULTS RESULTS
Luteolin inhibited the early process of HSV-1 infection, without affecting the infection of acyclovir-resistant HSV-1 strains. In addition, luteolin enhanced antiviral type I interferon production and activated the cytoplasmic DNA-sensing cGAS-stimulator of interferon gene (STING) pathway. Luteolin directly bound the active substrate binding site and promoted the oligomerization of cGAS. Luteolin also inhibited HSE-related weight loss, neurodegeneration and neuroinflammation in mice caused by HSV-1 infection. Furthermore, luteolin enhanced type I interferon expression and stimulated the cGAS-STING signaling pathway in vivo.
CONCLUSION CONCLUSIONS
Luteolin inhibited the post-entry process of HSV-1 by activating the cGAS-STING pathway to promote antiviral interferon production. These results provided the rationale for luteolin as a potent cGAS activator and antiviral agent.

Identifiants

pubmed: 37632997
pii: S0944-7113(23)00381-1
doi: 10.1016/j.phymed.2023.155020
pii:
doi:

Substances chimiques

Antiviral Agents 0
Luteolin KUX1ZNC9J2
cyclic guanosine monophosphate-adenosine monophosphate 0
Nucleotidyltransferases EC 2.7.7.-
Interferon Type I 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

155020

Informations de copyright

Copyright © 2023 Elsevier GmbH. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no conflicts of interest

Auteurs

Yuan Wang (Y)

Institute of Biomedicine, College of Life Science and Technology, Guangdong Province Key Laboratory of Bioengineering Medicine, Key Laboratory of innovative technology research on natural products and cosmetics raw materials, Jinan University, Guangzhou 510632, China.

Feng Li (F)

Institute of Biomedicine, College of Life Science and Technology, Guangdong Province Key Laboratory of Bioengineering Medicine, Key Laboratory of innovative technology research on natural products and cosmetics raw materials, Jinan University, Guangzhou 510632, China; Infectious Diseases Institute, Guangzhou Eighth People's Hospital, Guangzhou 510440, China.

Zexu Wang (Z)

Institute of Biomedicine, College of Life Science and Technology, Guangdong Province Key Laboratory of Bioengineering Medicine, Key Laboratory of innovative technology research on natural products and cosmetics raw materials, Jinan University, Guangzhou 510632, China.

Xiaowei Song (X)

Institute of Biomedicine, College of Life Science and Technology, Guangdong Province Key Laboratory of Bioengineering Medicine, Key Laboratory of innovative technology research on natural products and cosmetics raw materials, Jinan University, Guangzhou 510632, China.

Zhe Ren (Z)

Institute of Biomedicine, College of Life Science and Technology, Guangdong Province Key Laboratory of Bioengineering Medicine, Key Laboratory of innovative technology research on natural products and cosmetics raw materials, Jinan University, Guangzhou 510632, China; Guangdong Provincial biotechnology drug & Engineering Technology Research Center, National Engineering Research Center of Genetic Medicine, National Engineering Research Centre for Modernization of Chinese Medicine, Guangzhou 510632, China.

Xiao Wang (X)

Department of Pharmacy, Shenzhen People's Hospital, The Second Clinical Medical College, Jinan University; The First Affiliated Hospital, Southern University of Science and Technology, Shenzhen 518020, China. Electronic address: wangxiao0719@163.com.

Yifei Wang (Y)

Institute of Biomedicine, College of Life Science and Technology, Guangdong Province Key Laboratory of Bioengineering Medicine, Key Laboratory of innovative technology research on natural products and cosmetics raw materials, Jinan University, Guangzhou 510632, China; Guangdong Provincial biotechnology drug & Engineering Technology Research Center, National Engineering Research Center of Genetic Medicine, National Engineering Research Centre for Modernization of Chinese Medicine, Guangzhou 510632, China. Electronic address: twang-yf@163.com.

Kai Zheng (K)

School of Pharmacy, Shenzhen University Medical School, Shenzhen University, Shenzhen 518055, China. Electronic address: zhengk@szu.edu.cn.

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Classifications MeSH