Varicella-zoster virus recapitulates its immune evasive behaviour in matured hiPSC-derived neurospheroids

Front Immunol. 2024 Sep 16:15:1458967. doi: 10.3389/fimmu.2024.1458967. eCollection 2024.

Abstract

Varicella-zoster virus (VZV) encephalitis and meningitis are potential central nervous system (CNS) complications following primary VZV infection or reactivation. With Type-I interferon (IFN) signalling being an important first line cellular defence mechanism against VZV infection by the peripheral tissues, we here investigated the triggering of innate immune responses in a human neural-like environment. For this, we established and characterised 5-month matured hiPSC-derived neurospheroids (NSPHs) containing neurons and astrocytes. Subsequently, NSPHs were infected with reporter strains of VZV (VZVeGFP-ORF23) or Sendai virus (SeVeGFP), with the latter serving as an immune-activating positive control. Live cell and immunocytochemical analyses demonstrated VZVeGFP-ORF23 infection throughout the NSPHs, while SeVeGFP infection was limited to the outer NSPH border. Next, NanoString digital transcriptomics revealed that SeVeGFP-infected NSPHs activated a clear Type-I IFN response, while this was not the case in VZVeGFP-ORF23-infected NSPHs. Moreover, the latter displayed a strong suppression of genes related to IFN signalling and antigen presentation, as further demonstrated by suppression of IL-6 and CXCL10 production, failure to upregulate Type-I IFN activated anti-viral proteins (Mx1, IFIT2 and ISG15), as well as reduced expression of CD74, a key-protein in the MHC class II antigen presentation pathway. Finally, even though VZVeGFP-ORF23-infection seems to be immunologically ignored in NSPHs, its presence does result in the formation of stress granules upon long-term infection, as well as disruption of cellular integrity within the infected NSPHs. Concluding, in this study we demonstrate that 5-month matured hiPSC-derived NSPHs display functional innate immune reactivity towards SeV infection, and have the capacity to recapitulate the strong immune evasive behaviour towards VZV.

Keywords: antigen presentation; human iPSc; neurospheroids; stress granules; structural integrity; type-I interferon signalling; varicella-zoster virus.

MeSH terms

  • Astrocytes / immunology
  • Astrocytes / metabolism
  • Astrocytes / virology
  • Cells, Cultured
  • Cytokines / immunology
  • Cytokines / metabolism
  • Herpesvirus 3, Human* / immunology
  • Humans
  • Immune Evasion
  • Immunity, Innate
  • Induced Pluripotent Stem Cells* / immunology
  • Induced Pluripotent Stem Cells* / virology
  • Interferon Type I / immunology
  • Interferon Type I / metabolism
  • Neurons / immunology
  • Neurons / virology
  • Signal Transduction / immunology
  • Varicella Zoster Virus Infection / immunology
  • Varicella Zoster Virus Infection / virology

Substances

  • Interferon Type I
  • Cytokines

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research and the PhD fellowship of JG was funded by the Fund for Scientific Research Flanders (FWO-Vlaanderen) of the Flemish Government (FWO senior research project G034721N; granted to PP, PD, BO, ML, CS-D, and SP), as well as FWO research projects I000123N and I003420N, granted to WDV. BO was holder of a ‘Fundamenteel Klinisch Mandaat (FKM)’ from the FWO-Vlaanderen (1861219N; granted to BO). Additional support by FWO-Vlaanderen includes: the FWO sabbatical bench fee K800224N (granted to PP) and the Short Research Stay in Flanders V511123N (granted to HM). The postdoctoral fellowship of EV is funded by M-ERA-NET program under grant agreement M-ERA-NET3/0007/2021 (granted to PP). We also acknowledge support from the Slovenia Research and Innovation Agency (P4-0127, J3-4503 and J3-3065; granted to BR) and the ‘Bijzonder Onderzoeksfonds’ (BOF) of the University of Antwerp under the agreements: UA BOF-GOA 2020 (granted to PP and WDV), UA BOF-SEP 2022 (granted to PP), BOF Research Sabbatical 2023 (granted to PP) and BOF IOF FFI210239 (granted to WDV). The PhD fellowship of JD was funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 813263 (PMSMatTrain, granted to PP).