A Multi-Functional Nanoadjuvant Coupling Manganese with Toll-Like 9 Agonist Stimulates Potent Innate and Adaptive Anti-Tumor Immunity

Adv Sci (Weinh). 2024 Nov;11(41):e2402678. doi: 10.1002/advs.202402678. Epub 2024 Sep 11.

Abstract

The effectiveness of Toll-like 9 agonists (CpG) as an adjuvant for tumor immunotherapy is restricted due to their insufficient ability to activate anti-tumor immunity. To address that, the common nutrient metal ions are explored (Mn2+, Cu2+, Ca2+, Mg2+, Zn2+, Fe3+, and Al3+), identifying Mn2+ as a key enhancer of CpG to mediate immune activation by augmenting the STING-NF-κB pathway. Mn2+ and CpG are then self-assembled with epigallocatechin gallate (EGCG) into a nanoadjuvant MPN/CpG. Local delivery of MPN/CpG effectively inhibits tumor growth in a B16 melanoma-bearing mouse model, reshaping the tumor microenvironment (TME) by repolarizing M2-type tumor-associated macrophages (TAMs) to an M1-type and boosting intra-tumoral infiltration of CD8+/CD4+ T lymphocytes and DCs. Furthermore, compared to free CpG, MPN/CpG exhibits heightened accumulation in lymph nodes, enhancing CpG uptake and DC activation, consequently inducing significant antigen-specific cytotoxic CD8+ T cell immune response and humoral immunity. In a prophylactic tumor-bearing mouse model, MPN/CpG vaccination with OVA antigen significantly delays B16-OVA melanoma growth and extends mouse survival. These findings underscore the potential of MPN/CpG as a multifunctional adjuvant platform to drive powerful innate and adaptive immunity and regulate TME against tumors.

Keywords: TLR9 agonist; manganese; nanoadjuvant; tumor immunotherapy; vaccine.

MeSH terms

  • Adaptive Immunity* / drug effects
  • Adaptive Immunity* / immunology
  • Adjuvants, Immunologic* / pharmacology
  • Animals
  • Disease Models, Animal*
  • Female
  • Immunity, Innate* / drug effects
  • Immunity, Innate* / immunology
  • Immunotherapy / methods
  • Manganese* / pharmacology
  • Melanoma, Experimental* / drug therapy
  • Melanoma, Experimental* / immunology
  • Mice
  • Mice, Inbred C57BL*
  • Toll-Like Receptor 9* / agonists
  • Toll-Like Receptor 9* / immunology
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology

Substances

  • Manganese
  • Adjuvants, Immunologic
  • Toll-Like Receptor 9