Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts
Abstract Herpes simplex virus type 1 (HSV-1) is the leading pathogen in the maxillo-facial region, affecting millions of individuals worldwide. Its periodic reactivation aligns with the most common course pattern of periodontal disease. The present study used RNA sequencing to investigate the transc...
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BMC
2024-12-01
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| Online Access: | https://doi.org/10.1186/s12985-024-02595-5 |
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| author | Yu Zhang Kalam Lo Chunmei Wang Guoliang Zhou Xiping Feng Jing Ni Xi Chen |
| author_facet | Yu Zhang Kalam Lo Chunmei Wang Guoliang Zhou Xiping Feng Jing Ni Xi Chen |
| author_sort | Yu Zhang |
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| description | Abstract Herpes simplex virus type 1 (HSV-1) is the leading pathogen in the maxillo-facial region, affecting millions of individuals worldwide. Its periodic reactivation aligns with the most common course pattern of periodontal disease. The present study used RNA sequencing to investigate the transcriptomes of human gingival fibroblasts (HGFs) following HSV-1 infection from the early to late stages (12–72 h). At the early stage of infection (12 h post-infection), the most upregulated genes were interferon (IFN) regulatory factor family members, toll-like receptor (TLR) family members, IFN-β1, interleukin (IL)-1, C-C motif ligands, chemokine (C-X-C motif) ligands (CXCLs), and tumor necrosis factor (TNF). The strongest differential expression was observed in TNF, nucleotide-binding oligomerization domain-like receptor (NLR), and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) signaling pathways. At the late stage of infection, the most upregulated genes were CXCLs and ILs. The differentially expressed genes were divided into nine clusters, according to the time series expression trend. Next, the prominent activation of TLRs, retinoic acid-inducible gene I-like receptor signaling, NLRs, and downstream IFNAR-JAK-STAT signaling pathways were observed via a modified HSV-1 infection map. The HSV-1-induced upregulation of inflammatory cytokines in HGFs may drive inflammatory processes in periodontitis. The dynamic variations in mRNAs in HGFs from the early to late stages after HSV-1 infection can provide an analytical framework for determining the host anti-viral defense response to antagonize HSV-1 infection in periodontal tissues. |
| format | Article |
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| publishDate | 2024-12-01 |
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| series | Virology Journal |
| spelling | doaj-art-f31a2ef1a2a843d89db093a1ca5b89db2025-08-20T02:32:25ZengBMCVirology Journal1743-422X2024-12-0121111210.1186/s12985-024-02595-5Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblastsYu Zhang0Kalam Lo1Chunmei Wang2Guoliang Zhou3Xiping Feng4Jing Ni5Xi Chen6Department of Preventive Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of StomatologyDepartment of Preventive Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of StomatologyShanghai Veterinary Research Institute, Chinese Academy of Agricultural SciencesDancheng County Central HospitalDepartment of Preventive Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of StomatologyDepartment of Periodontology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of StomatologyDepartment of Preventive Dentistry, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine; College of Stomatology, Shanghai Jiao Tong University; National Center for Stomatology; National Clinical Research Center for Oral Diseases; Shanghai Key Laboratory of Stomatology; Shanghai Research Institute of StomatologyAbstract Herpes simplex virus type 1 (HSV-1) is the leading pathogen in the maxillo-facial region, affecting millions of individuals worldwide. Its periodic reactivation aligns with the most common course pattern of periodontal disease. The present study used RNA sequencing to investigate the transcriptomes of human gingival fibroblasts (HGFs) following HSV-1 infection from the early to late stages (12–72 h). At the early stage of infection (12 h post-infection), the most upregulated genes were interferon (IFN) regulatory factor family members, toll-like receptor (TLR) family members, IFN-β1, interleukin (IL)-1, C-C motif ligands, chemokine (C-X-C motif) ligands (CXCLs), and tumor necrosis factor (TNF). The strongest differential expression was observed in TNF, nucleotide-binding oligomerization domain-like receptor (NLR), and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) signaling pathways. At the late stage of infection, the most upregulated genes were CXCLs and ILs. The differentially expressed genes were divided into nine clusters, according to the time series expression trend. Next, the prominent activation of TLRs, retinoic acid-inducible gene I-like receptor signaling, NLRs, and downstream IFNAR-JAK-STAT signaling pathways were observed via a modified HSV-1 infection map. The HSV-1-induced upregulation of inflammatory cytokines in HGFs may drive inflammatory processes in periodontitis. The dynamic variations in mRNAs in HGFs from the early to late stages after HSV-1 infection can provide an analytical framework for determining the host anti-viral defense response to antagonize HSV-1 infection in periodontal tissues.https://doi.org/10.1186/s12985-024-02595-5Herpes simplex virusHuman gingival fibroblastsTranscriptomePeriodontitis |
| spellingShingle | Yu Zhang Kalam Lo Chunmei Wang Guoliang Zhou Xiping Feng Jing Ni Xi Chen Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts Virology Journal Herpes simplex virus Human gingival fibroblasts Transcriptome Periodontitis |
| title | Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts |
| title_full | Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts |
| title_fullStr | Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts |
| title_full_unstemmed | Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts |
| title_short | Herpes simplex virus-induced upregulation of inflammatory cytokines in human gingival fibroblasts |
| title_sort | herpes simplex virus induced upregulation of inflammatory cytokines in human gingival fibroblasts |
| topic | Herpes simplex virus Human gingival fibroblasts Transcriptome Periodontitis |
| url | https://doi.org/10.1186/s12985-024-02595-5 |
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