Structure of the Human cGAS-DNA Complex Reveals Enhanced Control of Immune Surveillance

  • Cell. 2018 Jul 12;174(2):300-311.e11. doi: 10.1016/j.cell.2018.06.026.
Wen Zhou  1 Aaron T Whiteley  1 Carina C de Oliveira Mann  1 Benjamin R Morehouse  1 Radosław P Nowak  2 Eric S Fischer  2 Nathanael S Gray  2 John J Mekalanos  3 Philip J Kranzusch  4
Affiliations
  • 1. Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115, USA; Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA 02115, USA.
  • 2. Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02115, USA.
  • 3. Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115, USA.
  • 4. Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115, USA; Department of Cancer Immunology and Virology, Dana-Farber Cancer Institute, Boston, MA 02115, USA. Electronic address: [email protected].
Abstract

Cyclic GMP-AMP Synthase (cGAS) recognition of cytosolic DNA is critical for immune responses to pathogen replication, cellular stress, and Cancer. Existing structures of the mouse cGAS-DNA complex provide a model for enzyme activation but do not explain why human cGAS exhibits severely reduced levels of cyclic GMP-AMP (cGAMP) synthesis compared to Other mammals. Here, we discover that enhanced DNA-length specificity restrains human cGAS activation. Using reconstitution of cGAMP signaling in bacteria, we mapped the determinant of human cGAS regulation to two amino acid substitutions in the DNA-binding surface. Human-specific substitutions are necessary and sufficient to direct preferential detection of long DNA. Crystal structures reveal why removal of human substitutions relaxes DNA-length specificity and explain how human-specific DNA interactions favor cGAS oligomerization. These results define how DNA-sensing in humans adapted for enhanced specificity and provide a model of the active human cGAS-DNA complex to enable structure-guided design of cGAS therapeutics.

Keywords
STING; cGAS; innate immunity; structural biology.