CXCL13 promotes broad immune responses induced by circular RNA vaccines

Proc Natl Acad Sci U S A. 2024 Oct 29;121(44):e2406434121. doi: 10.1073/pnas.2406434121. Epub 2024 Oct 22.

Abstract

Antibody responses induced by current vaccines for influenza and SARS-CoV-2 often lack robust cross-reactivity. As hubs where diverse immune cells converge and interact, the alterations in the immune microenvironment within lymph nodes (LNs) are intricately linked to immune responses. Herein, we designed a lipid nanoparticle (LNP) loaded with circular RNA (circRNA) and targeted to LNs, in which CXCL13 was directly integrated into antigen-encoding circRNA strands. We demonstrated that CXCL13 alters the transcriptomic profiles of LNs, especially the upregulation of IL-21 and IL-4. Meanwhile, CXCL13 promotes the formation of germinal center and elicits robust antigen-specific T cell responses. With the codelivery of CXCL13 and the antigen, CXCL13 enhances cross-reactive antibodies against influenza virus and SARS-CoV-2, achieving protection against both homologous and heterologous influenza virus challenges in a mouse model. Notably, the targeted modification of LNP surfaces with antibodies helps address some of the challenges associated with lyophilized LNP vaccines, which is crucial for the long-term storage of LNP-circRNA vaccines. Overall, the circRNA-based antigen-CXCL13 coexpression system developed herein provides a simple and robust platform that enhances the magnitude and breadth of antibody responses against multiple viral glycoproteins, highlighting the potential utility of CXCL13 in inducing broad immune responses.

Keywords: CXCL13; SARS-CoV-2; broadly cross-reactive antibodies; circRNA vaccine; influenza virus.

MeSH terms

  • Animals
  • Antibodies, Viral / immunology
  • COVID-19 Vaccines / administration & dosage
  • COVID-19 Vaccines / immunology
  • COVID-19* / immunology
  • COVID-19* / prevention & control
  • Chemokine CXCL13* / immunology
  • Cross Reactions / immunology
  • Female
  • Humans
  • Influenza Vaccines / immunology
  • Interleukin-4 / immunology
  • Interleukin-4 / metabolism
  • Interleukins
  • Lymph Nodes / immunology
  • Mice
  • Nanoparticles / chemistry
  • Orthomyxoviridae Infections / immunology
  • Orthomyxoviridae Infections / prevention & control
  • RNA, Circular* / genetics
  • RNA, Circular* / immunology
  • SARS-CoV-2* / genetics
  • SARS-CoV-2* / immunology

Substances

  • Chemokine CXCL13
  • RNA, Circular
  • COVID-19 Vaccines
  • Influenza Vaccines
  • Cxcl13 protein, mouse
  • Antibodies, Viral
  • interleukin-21
  • Interleukin-4
  • Interleukins