Alphaherpesvirus infection of mice primes PNS neurons to an inflammatory state regulated by TLR2 and type I IFN signaling.
Open accessAbstract
Pseudorabies virus (PRV), an alphaherpesvirus closely related to Varicella-Zoster virus (VZV) and Herpes simplex type 1 (HSV1) infects mucosa epithelia and the peripheral nervous system (PNS) of its host.We previously demonstrated that PRV infection induces a specific and lethal inflammatory response, contributing to severe neuropathy in mice.So far, the mechanisms that initiate this neuroinflammation remain unknown.Using a mouse footpad inoculation model, we found that PRV infection rapidly and simultaneously induces high G-CSF and IL-6 levels in several mouse tissues, including the footpad, PNS and central nervous system (CNS) tissues.Interestingly, this global increase occurred before PRV had replicated in dorsal root ganglia (DRGs) neurons and also was independent of systemic inflammation.These high G-CSF and IL-6 levels were not caused by neutrophil infiltration in PRV infected tissues, as we did not detect any neutrophils.Efficient PRV replication and spread in the footpad was sufficient to activate DRGs to produce cytokines.Finally, by using knockout mice, we demonstrated that TLR2 and IFN type I play crucial roles in modulating the early neuroinflammatory response and clinical outcome of PRV infection in mice.Overall, these results give new insights into the initiation of virus-induced neuroinflammation during herpesvirus infections. Author summaryHerpesviruses are major pathogens worldwide.Pseudorabies virus (PRV) is an alphaherpesvirus related to varicella-zoster virus (VZV) and herpes simplex virus type 1 (HSV1).The natural host is the pig, but PRV can infect most mammals.In these non-natural hosts, the virus causes a severe pruritus called the 'mad itch'.Interestingly, PRV infects the peripheral nervous system (PNS) and induces a specific and lethal inflammatory response in mice, yet little is know about how this neuroinflammatory response is initiated.In this study, we demonstrated for the first time how PNS neurons tightly regulate the inflammatory response during PRV infection and contribute to severe clinical outcome in mice.Our work provides new insights into the process of alphaherpesvirus-induced neuropathies, leading to the development of innovative therapeutic strategies.
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The imbalance between antiviral and pro-inflammatory immune responses plays an important role in the clinical outcome of alphaherpesvirus infection in vivo.
“The imbalance between antiviral and pro-inflammatory immune responses has been shown to play an important role in the clinical outcome of alphaherpesviruses infection in vivo (Laval et al., 2019).”
From The Pathogenesis and Immune Evasive Mechanisms of Equine Herpesvirus Type 1 (2021) · cites this paper as Laval et al., 2019
The Discussion (page not provided) says the imbalance is likely to contribute to the distinct clinical outcomes of PRV-Becker and PRV-Bartha infections in mice. The citing sentence presents that tentative, strain-specific interpretation as an established finding about alphaherpesvirus infections generally. (LLM, conf=0.88)
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Yang, X., Xu, S., Chen, D., Jiang, R., Kang, H., Ge, X., Zhou, L., Han, J., Zhang, Y., Guo, X., et al. (2022) · Viruses · doi:10.3390/v14040755 · Cited by 2 · see citing works
Cronin, S. J. F., Tejada, M. A., Song, R., Laval, K., Cikes, D., Ji, M., Brai, A., Stadlmann, J., Novatchikova, M., Perlot, T., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.09.539956 · Cited by 2 · see citing works
Invasion of the Nervous System
Koyuncu, O. Ö., Enquist, L. W., & Engel, E. A. (2020) · Caister Academic Press eBooks · doi:10.21775/9781913652555.05 · Cited by 1 · see citing works
Biographical Feature: The Long and Winding Road: My Career Path and How I Ended Up Where I Am Now
Enquist, L. W. (2020) · Journal of Virology · doi:10.1128/jvi.01625-20
Pan, Q., Yan, F., Liu, S., Wang, X., Zhu, B., Ye, J., Cao, S., Zhang, A., & 司有辉 (2026) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2026.154682
- Authors
- Laval, K., Van Cleemput, J., Vernejoul, J. B., & Enquist, L. W.
- Affiliations
- Princeton University (US)
- Corresponding author
- Laval, Kathlyn
- Venue
- PLoS Pathogens
- Publisher
- Public Library of Science (PLoS)
- Published
- 2019-11-01
- Volume
- 15
- Issue
- 11
- Pages
- e1008087
- ISSN
- 1553-7366 (ISSN-L)
- 1553-7374
- PMC
- PMC6824567
- OpenAlex
- W2986568404
- Cited by
- 36
- References
- 59
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 8 · 2021: 6 · 2020: 10
- FWCI
- 4.57
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Pathogens (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Ghent University Academic Bibliography (Ghent University) (publishedVersion, other-oa)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Neurological Disorders and Stroke (RO1 NS033506, RO1 NS060699)
- Topics
- Health Sciences › Medicine › Epidemiology › Herpesvirus Infections and Treatments
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Keywords
- pseudorabies virus, alphaherpesvirus, neuroinflammation, peripheral nervous system neurons, dorsal root ganglia, TLR2, type I interferon signaling, granulocyte colony-stimulating factor, interleukin-6, neuropathy, footpad inoculation
- MeSH terms
- Animals, Antiviral Agents, Herpesviridae Infections, Inflammation, Interferon Type I, Male, Mice, Inbred C57BL, Neurons, Virus Replication, Peripheral Nervous System, Alphaherpesvirinae, Toll-Like Receptor 2, Mice
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