Complement activation promoted by the lectin pathway mediates C3aR-dependent sarcoma progression and immunosuppression

Nat Cancer. 2021 Feb;2(2):218-232. doi: 10.1038/s43018-021-00173-0. Epub 2021 Feb 18.

Abstract

Complement has emerged as a component of tumor promoting inflammation. We conducted a systematic assessment of the role of complement activation and effector pathways in sarcomas. C3-/-, MBL1/2-/- and C4-/- mice showed reduced susceptibility to 3-methylcholanthrene sarcomagenesis and transplanted sarcomas, whereas C1q and factor B deficiency had marginal effects. Complement 3a receptor (C3aR), but not C5aR1 and C5aR2, deficiency mirrored the phenotype of C3-/- mice. C3 and C3aR deficiency were associated with reduced accumulation and functional skewing of tumor-associated macrophages, increased T cell activation and response to anti-PD-1 therapy. Transcriptional profiling of sarcoma infiltrating macrophages and monocytes revealed the enrichment of MHC II-dependent antigen presentation pathway in C3-deficient cells. In patients, C3aR expression correlated with a macrophage population signature and C3 deficiency-associated signatures predicted better clinical outcome. These results suggest that the lectin pathway and C3a/C3aR axis are key components of complement and macrophage-mediated sarcoma promotion and immunosuppression.

Keywords: C3; C3a receptor (C3aR); Complement; cancer; cancer-related inflammation; immunotherapy; lectin pathway; macrophages; mannose binding lectin (MBL); sarcoma.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Complement Activation / physiology
  • Humans
  • Immunosuppression Therapy
  • Lectins* / metabolism
  • Mice
  • Monocytes / metabolism
  • Receptor, Anaphylatoxin C5a / metabolism
  • Receptors, Complement / metabolism*
  • Sarcoma* / drug therapy

Substances

  • C5ar2 protein, mouse
  • Lectins
  • Receptor, Anaphylatoxin C5a
  • Receptors, Complement
  • complement C3a receptor