Killer cell immunoglobulin–like receptor 3DL1 variation modifies HLA-B*57 protection against HIV-1

  • Maureen P. Martin ,
  • Vivek Naranbhai ,
  • Patrick R. Shea ,
  • Ying Qi ,
  • Veron Ramsuran ,
  • Nicolas Vince ,
  • Xiaojiang Gao ,
  • Rasmi Thomas ,
  • Zabrina L. Brumme ,
  • ,
  • Steven M. Wolinsky ,
  • James J. Goedert ,
  • Bruce D. Walker ,
  • Florencia P. Segal ,
  • Steven G. Deeks ,
  • David W. Haas ,
  • Stephen A. Migueles ,
  • Mark Connors ,
  • Nelson Michael ,
  • Jacques Fellay ,
  • Emma Gostick ,
  • Sian Llewellyn-Lacey ,
  • David A. Price ,
  • Bernard A. Lafont ,
  • Phillip Pymm ,
  • Philippa M. Saunders ,
  • Jacqueline Widjaja ,
  • Shu Cheng Wong ,
  • Julian P. Vivian ,
  • Jamie Rossjohn ,
  • Andrew G. Brooks, ,
  • Mary Carrington

Journal of Clinical Investigation | , Vol 128(5): pp. 1903-1912

Publication

HLA-B*57 control of HIV involves enhanced CD8+ T cell responses against infected cells, but extensive heterogeneity exists in the level of HIV control among B*57+ individuals. Using whole-genome sequencing of untreated B*57+ HIV-1–infected controllers and noncontrollers, we identified a single variant (rs643347A/G) encoding an isoleucine-tovaline substitution at position 47 (I47V) of the inhibitory killer cell immunoglobulin-like receptor KIR3DL1 as the only significant modifier of B*57 protection. The association was replicated in an independent cohort and across multiple outcomes. The modifying effect of I47V was confined to B*57:01 and was not observed for the closely related B*57:03. Positions 2, 47, and 54 tracked one another nearly perfectly, and 2 KIR3DL1 allotypes differing only at these 3 positions showed significant differences in binding B*57:01 tetramers, whereas the protective allotype showed lower binding. Thus, variation in an immune NK cell receptor that binds B*57:01 modifies its protection. These data highlight the exquisite specificity of KIR-HLA interactions in human health and disease.