mRNA Delivery of a Bispecific Single-Domain Antibody to Polarize Tumor-Associated Macrophages and Synergize Immunotherapy against Liver Malignancies

Adv Mater. 2021 Jun;33(23):e2007603. doi: 10.1002/adma.202007603. Epub 2021 May 4.

Abstract

Liver malignancies are among the tumor types that are resistant to immune checkpoint inhibition therapy. Tumor-associated macrophages (TAMs) are highly enriched and play a major role in inducing immunosuppression in liver malignancies. Herein, CCL2 and CCL5 are screened as two major chemokines responsible for attracting TAM infiltration and inducing their polarization toward cancer-promoting M2-phenotype. To reverse this immunosuppressive process, an innovative single-domain antibody that bispecifically binds and neutralizes CCL2 and CCL5 (BisCCL2/5i) with high potency and specificity is directly evolved. mRNA encoding BisCCL2/5i is encapsulated in a clinically approved lipid nanoparticle platform, resulting in a liver-homing biomaterial that allows transient yet efficient expression of BisCCL2/5i in the diseased organ in a multiple dosage manner. This BisCCL2/5i mRNA nanoplatform significantly induces the polarization of TAMs toward the antitumoral M1 phenotype and reduces immunosuppression in the tumor microenvironment. The combination of BisCCL2/5i with PD-1 ligand inhibitor (PD-Li) achieves long-term survival in mouse models of primary liver cancer and liver metastasis of colorectal and pancreatic cancers. The work provides an effective bispecific targeting strategy that could broaden the PD-Li therapy to multiple types of malignancies in the human liver.

Keywords: bispecific single-domain antibody; immunotherapy; liver malignancies; mRNA-lipid nanoparticles; tumor-associated macrophages.

MeSH terms

  • Animals
  • Antibodies, Bispecific* / chemistry
  • Antibodies, Bispecific* / pharmacology
  • Cell Line, Tumor
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Chemokine CCL5 / metabolism
  • Humans
  • Immunotherapy*
  • Liver Neoplasms* / therapy
  • Mice
  • Nanoparticles / chemistry
  • RNA, Messenger* / genetics
  • RNA, Messenger* / metabolism
  • Single-Domain Antibodies / chemistry
  • Single-Domain Antibodies / pharmacology
  • Tumor Microenvironment / drug effects
  • Tumor-Associated Macrophages* / drug effects
  • Tumor-Associated Macrophages* / metabolism

Substances

  • RNA, Messenger
  • Antibodies, Bispecific
  • Single-Domain Antibodies
  • Chemokine CCL5
  • Chemokine CCL2