Long-term multilineage engraftment of autologous genome-edited hematopoietic stem cells in nonhuman primates

Blood. 2016 May 19;127(20):2416-26. doi: 10.1182/blood-2015-09-672337. Epub 2016 Mar 15.

Abstract

Genome editing in hematopoietic stem and progenitor cells (HSPCs) is a promising novel technology for the treatment of many human diseases. Here, we evaluated whether the disruption of the C-C chemokine receptor 5 (CCR5) locus in pigtailed macaque HSPCs by zinc finger nucleases (ZFNs) was feasible. We show that macaque-specific CCR5 ZFNs efficiently induce CCR5 disruption at levels of up to 64% ex vivo, 40% in vivo early posttransplant, and 3% to 5% in long-term repopulating cells over 6 months following HSPC transplant. These genome-edited HSPCs support multilineage engraftment and generate progeny capable of trafficking to secondary tissues including the gut. Using deep sequencing technology, we show that these ZFNs are highly specific for the CCR5 locus in primary cells. Further, we have adapted our clonal tracking methodology to follow individual CCR5 mutant cells over time in vivo, reinforcing that CCR5 gene-edited HSPCs are capable of long-term engraftment. Together, these data demonstrate that genome-edited HSPCs engraft, and contribute to multilineage repopulation after autologous transplantation in a clinically relevant large animal model, an important step toward the development of stem cell-based genome-editing therapies for HIV and potentially other diseases as well.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Bone Marrow Transplantation*
  • Cell Line
  • Cell Lineage*
  • Electroporation
  • Feasibility Studies
  • Gene Editing*
  • Gene Knockdown Techniques
  • Graft Survival
  • Hematopoietic Stem Cell Transplantation*
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / metabolism
  • Macaca nemestrina / genetics*
  • Molecular Sequence Data
  • Mutation
  • Polymerase Chain Reaction / methods
  • RNA, Messenger / genetics
  • Receptors, CCR5 / deficiency
  • Receptors, CCR5 / genetics*
  • Sequence Analysis, DNA
  • Transplantation Conditioning
  • Transplantation, Autologous
  • Whole-Body Irradiation
  • Zinc Fingers

Substances

  • RNA, Messenger
  • Receptors, CCR5